Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life

Biology Direct

Jan Brábek¹  Fatima Cvrčková⁴  Roberto Buccione²  Margaret Nikolič³  Daniel Rösel¹  Viktor Žárský⁴  Katarína Vaškovičová¹ 

[1]Department of Cell Biology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 43, Prague 2, Czech Republic

[2]Tumour Cell Invasion Laboratory, Consorzio Mario Negri Sud, S. Maria Imbaro, Chieti, 66030, Italy

[3]Department of Human and Environmental Sciences, School of Life and Medical Sciences, University of Hertfordshire, College Lane Campus, Hatfield, AL10 9AB, United Kingdom

[4]Department of Experimental Plant Biology, Faculty of Science, Charles University Prague, Vinicna 5, 128 43, Prague 2, Czech Republic

关键词: Actin, Secretory pathway;    GTPases;    Neurite;    Pollen tube;    Invadopodia;    Invasiveness;   

Others  :  799851
DOI  :  10.1186/1745-6150-8-8

 received in 2012-11-23, accepted in 2013-03-21,  发布年份 2013

【 摘 要 】

Invasive cell growth and migration is usually considered a specifically metazoan phenomenon. However, common features and mechanisms of cytoskeletal rearrangements, membrane trafficking and signalling processes contribute to cellular invasiveness in organisms as diverse as metazoans and plants – two eukaryotic realms genealogically connected only through the last common eukaryotic ancestor (LECA). By comparing current understanding of cell invasiveness in model cell types of both metazoan and plant origin (invadopodia of transformed metazoan cells, neurites, pollen tubes and root hairs), we document that invasive cell behavior in both lineages depends on similar mechanisms. While some superficially analogous processes may have arisen independently by convergent evolution (e.g. secretion of substrate- or tissue-macerating enzymes by both animal and plant cells), at the heart of cell invasion is an evolutionarily conserved machinery of cellular polarization and oriented cell mobilization, involving the actin cytoskeleton and the secretory pathway. Its central components - small GTPases (in particular RHO, but also ARF and Rab), their specialized effectors, actin and associated proteins, the exocyst complex essential for polarized secretion, or components of the phospholipid- and redox- based signalling circuits (inositol-phospholipid kinases/PIP2, NADPH oxidases) are aparently homologous among plants and metazoans, indicating that they were present already in LECA.

Reviewer This article was reviewed by Arcady Mushegian, Valerian Dolja and Purificacion Lopez-Garcia.

【 授权许可】

   
2013 Vaškovičová et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Simpson AG, Roger AJ: The real ‘kingdoms’ of eukaryotes. Curr Biol 2004, 14:R693-R696.
• [2]Arkowitz RA, Bassilana M: Polarized growth in fungi: symmetry breaking and hyphal formation. Semin Cell Dev Biol 2011, 22:806-815.
• [3]Dickinson JR: Filament formation in Saccharomyces cerevisiae–a review. Folia Microbiol (Praha) 2008, 53:3-14.
• [4]Howell AS, Lew DJ: Morphogenesis and the cell cycle. Genetics 2012, 190:51-77.
• [5]Kebdani N, Pieuchot L, Deleury E, Panabieres F, Le Berre JY, Gourgues M: Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytol 2010, 185:248-257.
• [6]Wang Y, Meng Y, Zhang M, Tong X, Wang Q, Sun Y, Quan J, Govers F, Shan W: Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol Plant Pathol 2011, 12:187-201.
• [7]Buccione R, Caldieri G, Ayala I: Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev 2009, 28:137-149.
• [8]Caldieri G, Buccione R: Aiming for invadopodia: organizing polarized delivery at sites of invasion. Trends Cell Biol 2010, 20:64-70.
• [9]Murphy DA, Courtneidge SA: The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 2011, 12:413-426.
• [10]Poincloux R, Lizarraga F, Chavrier P: Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 2009, 122:3015-3024.
• [11]Kelly T, Mueller SC, Yeh Y, Chen WT: Invadopodia promote proteolysis of a wide variety of extracellular matrix proteins. J Cell Physiol 1994, 158:299-308.
• [12]Chen WT: Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 1989, 251:167-185.
• [13]Mueller SC, Chen WT: Cellular invasion into matrix beads: localization of beta 1 integrins and fibronectin to the invadopodia. J Cell Sci 1991, 99(Pt 2):213-225.
• [14]Bowden ET, Barth M, Thomas D, Glazer RI, Mueller SC: An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 1999, 18:4440-4449.
• [15]Chen WT: Proteases associated with invadopodia, and their role in degradation of extracellular matrix. Enzyme Protein 1996, 49:59-71.
• [16]Monsky WL, Lin CY, Aoyama A, Kelly T, Akiyama SK, Mueller SC, Chen WT: A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res 1994, 54:5702-5710.
• [17]Mueller SC, Yeh Y, Chen WT: Tyrosine phosphorylation of membrane proteins mediates cellular invasion by transformed cells. J Cell Biol 1992, 119:1309-1325.
• [18]Nakahara H, Howard L, Thompson EW, Sato H, Seiki M, Yeh Y, Chen WT: Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A 1997, 94:7959-7964.
• [19]Baldassarre M, Ayala I, Beznoussenko G, Giacchetti G, Machesky LM, Luini A, Buccione R: Actin dynamics at sites of extracellular matrix degradation. Eur J Cell Biol 2006, 85:1217-1231.
• [20]Bowden ET, Onikoyi E, Slack R, Myoui A, Yoneda T, Yamada KM, Mueller SC: Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp Cell Res 2006, 312:1240-1253.
• [21]Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, Segall J, Eddy R, Miki H, Takenawa T: Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 2005, 168:441-452.
• [22]Linder S: The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 2007, 17:107-117.
• [23]Linder S, Aepfelbacher M: Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 2003, 13:376-385.
• [24]Janostiak R, Tolde O, Bruhova Z, Novotny M, Hanks SK, Rosel D, Brabek J: Tyrosine phosphorylation within the SH3 domain regulates CAS subcellular localization, cell migration, and invasiveness. Mol Biol Cell 2011, 22:4256-4267.
• [25]Li A, Dawson JC, Forero-Vargas M, Spence HJ, Yu X, Konig I, Anderson K, Machesky LM: The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol 2010, 20:339-345.
• [26]Schoumacher M, Goldman RD, Louvard D, Vignjevic DM: Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol 2010, 189:541-556.
• [27]Tolde O, Rosel D, Vesely P, Folk P, Brabek J: The structure of invadopodia in a complex 3D environment. Eur J Cell Biol 2010, 89:674-680.
• [28]Fishell G, Hanashima C: Pyramidal neurons grow up and change their mind. Neuron 2008, 57:333-338.
• [29]Megias M, Emri Z, Freund TF, Gulyas AI: Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 2001, 102:527-540.
• [30]Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR: Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 2002, 22:3161-3173.
• [31]Valiente M, Marin O: Neuronal migration mechanisms in development and disease. Curr Opin Neurobiol 2010, 20:68-78.
• [32]Zheng W, Yuan X: Guidance of cortical radial migration by gradient of diffusible factors. Cell Adh Migr 2008, 2:48-50.
• [33]Reiner O, Sapir T: Polarity regulation in migrating neurons in the cortex. Mol Neurobiol 2009, 40:1-14.
• [34]Kawauchi T, Chihama K, Nabeshima Y, Hoshino M: Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol 2006, 8:17-26.
• [35]Letinic K, Sebastian R, Toomre D, Rakic P: Exocyst is involved in polarized cell migration and cerebral cortical development. Proc Natl Acad Sci U S A 2009, 106:11342-11347.
• [36]Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH: Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 2004, 44:263-277.
• [37]Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG: Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 2004, 165:709-721.
• [38]Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH: Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003, 114:469-482.
• [39]Anton ES, Kreidberg JA, Rakic P: Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 1999, 22:277-289.
• [40]Elias LA, Wang DD, Kriegstein AR: Gap junction adhesion is necessary for radial migration in the neocortex. Nature 2007, 448:901-907.
• [41]Forster E, Bock HH, Herz J, Chai X, Frotscher M, Zhao S: Emerging topics in reelin function. Eur J Neurosci 2010, 31:1511-1518.
• [42]Gongidi V, Ring C, Moody M, Brekken R, Sage EH, Rakic P, Anton ES: SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron 2004, 41:57-69.
• [43]Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH: Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci 2003, 6:1284-1291.
• [44]Rakic S, Yanagawa Y, Obata K, Faux C, Parnavelas JG, Nikolic M: Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb Cortex 2009, 19:1857-1869.
• [45]Causeret F, Terao M, Jacobs T, Nishimura YV, Yanagawa Y, Obata K, Hoshino M, Nikolic M: The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb Cortex 2009, 19:861-875.
• [46]Banker GA, Cowan WM: Rat hippocampal neurons in dispersed cell culture. Brain Res 1977, 126:397-42.
• [47]Craig AM, Banker G: Neuronal polarity. Annu Rev Neurosci 1994, 17:267-310.
• [48]Dotti CG, Sullivan CA, Banker GA: The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988, 8:1454-1468.
• [49]Arimura N, Kaibuchi K: Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 2007, 8:194-205.
• [50]Bradke F, Dotti CG: Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol 2000, 10:574-581.
• [51]Barnes AP, Solecki D, Polleux F: New insights into the molecular mechanisms specifying neuronal polarity in vivo. Curr Opin Neurobiol 2008, 18:44-52.
• [52]de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG: Centrosome localization determines neuronal polarity. Nature 2005, 436:704-708.
• [53]Asada N, Sanada K, Fukada Y: LKB1 regulates neuronal migration and neuronal differentiation in the developing neocortex through centrosomal positioning. J Neurosci 2007, 27:11769-11775.
• [54]Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR: Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004, 7:136-144.
• [55]Sapir T, Shmueli A, Levy T, Timm T, Elbaum M, Mandelkow EM, Reiner O: Antagonistic effects of doublecortin and MARK2/Par-1 in the developing cerebral cortex. J Neurosci 2008, 28:13008-13013.
• [56]de Anda FC, Meletis K, Ge X, Rei D, Tsai LH: Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci 2010, 30:10391-10406.
• [57]Chae K, Lord EM: Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot 2011, 108:627-636.
• [58]Lord EM: Adhesion and guidance in compatible pollination. J Exp Bot 2003, 54:47-54.
• [59]Tabuchi A, Li LC, Cosgrove DJ: Matrix solubilization and cell wall weakening by beta-expansin (group-1 allergen) from maize pollen. Plant J 2011, 68:546-559.
• [60]Szymanski DB, Cosgrove DJ: Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol 2009, 19:R800-R811.
• [61]Winship LJ, Obermeyer G, Geitmann A, Hepler PK: Pollen tubes and the physical world. Trends Plant Sci 2011, 16:353-355.
• [62]Carol RJ, Dolan L: Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 2002, 357:815-821.
• [63]Schiefelbein J, Kwak SH, Wieckowski Y, Barron C, Bruex A: The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 2009, 60:1515-1521.
• [64]Fischer U, Ikeda Y, Grebe M: Planar polarity of root hair positioning in Arabidopsis. Biochem Soc Trans 2007, 35:149-151.
• [65]Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua NH, Barlow PW, Volkmann D: Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 2000, 227:618-632.
• [66]Vissenberg K, Fry SC, Verbelen JP: Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol 2001, 127:1125-1135.
• [67]Singh SK, Fischer U, Singh M, Grebe M, Marchant A: Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana. BMC Plant Biol 2008, 8:57. BioMed Central Full Text
• [68]Zarsky V, Fowler JE: ROP (Rho-related protein from plants) GTPases for spatial control of root hair morphogenesis. New York: Springer; 2009:191-210. [Root hairs]
• [69]Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S: Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci U S A 2007, 104:20996-21001.
• [70]Monshausen GB, Messerli MA, Gilroy S: Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol 2008, 147:1690-1698.
• [71]Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A: Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 2009, 150:1322-1334.
• [72]Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z: Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 2010, 143:99-110.
• [73]Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M: ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 2010, 143:111-121.
• [74]Bourne HR, Sanders DA, McCormick F: The GTPase superfamily: a conserved switch for diverse cell functions. Nature 1990, 348:125-132.
• [75]Bourne HR, Sanders DA, McCormick F: The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991, 349:117-127.
• [76]Hall A: Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol 1994, 10:31-54.
• [77]Hall A: Rho GTPases and the control of cell behaviour. Biochem Soc Trans 2005, 33:891-895.
• [78]Harris SD: Cdc42/Rho GTPases in fungi: variations on a common theme. Mol Microbiol 2011, 79:1123-1127.
• [79]Kwon MJ, Arentshorst M, Roos ED, van den Hondel CA, Meyer V, Ram AF: Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol Microbiol 2011, 79:1151-1167.
• [80]Etienne-Manneville S: Cdc42–the centre of polarity. J Cell Sci 2004, 117:1291-1300.
• [81]Heasman SJ, Ridley AJ: Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 2008, 9:690-701.
• [82]Nobes CD, Hall A: Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
• [83]Nakahara H, Otani T, Sasaki T, Miura Y, Takai Y, Kogo M: Involvement of Cdc42 and Rac small G proteins in invadopodia formation of RPMI7951 cells. Genes Cells 2003, 8:1019-1027.
• [84]Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, D’Souza-Schorey C, Chavrier P: The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 2008, 181:985-998.
• [85]Luo L, Liao YJ, Jan LY, Jan YN: Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 1994, 8:1787-1802.
• [86]Allen MJ, Shan X, Murphey RK: A role for Drosophila Drac1 in neurite outgrowth and synaptogenesis in the giant fiber system. Mol Cell Neurosci 2000, 16:754-765.
• [87]Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L: Rac GTPases control axon growth, guidance and branching. Nature 2002, 416:442-447.
• [88]Hakeda-Suzuki S, Ng J, Tzu J, Dietzl G, Sun Y, Harms M, Nardine T, Luo L, Dickson BJ: Rac function and regulation during Drosophila development. Nature 2002, 416:438-442.
• [89]Malartre M, Ayaz D, Amador FF, Martin-Bermudo MD: The guanine exchange factor vav controls axon growth and guidance during Drosophila development. J Neurosci 2010, 30:2257-2267.
• [90]Miyamoto Y, Yamauchi J: Cellular signaling of Dock family proteins in neural function. Cell Signal 2010, 22:175-182.
• [91]Song JK, Giniger E: Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev Dyn 2011, 240:324-332.
• [92]Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan CY: Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci 2007, 27:3884-3893.
• [93]Kassai H, Terashima T, Fukaya M, Nakao K, Sakahara M, Watanabe M, Aiba A: Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur J Neurosci 2008, 28:257-267.
• [94]Corbetta S, Gualdoni S, Ciceri G, Monari M, Zuccaro E, Tybulewicz VL, de Curtis I: Essential role of Rac1 and Rac3 GTPases in neuronal development. FASEB J 2009, 23:1347-1357.
• [95]Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, Flynn KC, Stradal TE, Chrostek-Grashoff A, Brakebusch C, Bradke F: Rac1 regulates neuronal polarization through the WAVE complex. J Neurosci 2010, 30:6930-6943.
• [96]Chen L, Liao G, Yang L, Campbell K, Nakafuku M, Kuan CY, Zheng Y: Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc Natl Acad Sci U S A 2006, 103:16520-16525.
• [97]Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Brauninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB: The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 2006, 9:1099-1107.
• [98]Yalovsky S, Bloch D, Sorek N, Kost B: Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol 2008, 147:1527-1543.
• [99]Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S: A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol 2010, 8:e1000282.
• [100]Nagawa S, Xu T, Yang Z: RHO GTPase in plants: Conservation and invention of regulators and effectors. Small GTPases 2010, 1:78-88.
• [101]Li H, Lin Y, Heath RM, Zhu MX, Yang Z: Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 1999, 11:1731-1742.
• [102]Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K: Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 2001, 20:2779-2788.
• [103]Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L: A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 2005, 438:1013-1016.
• [104]Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, Palme K, Scheres B, Grebe M: Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity. Curr Biol 2006, 16:2143-2149.
• [105]Berken A, Thomas C, Wittinghofer A: A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 2005, 436:1176-1180.
• [106]Locke S, Fricke I, Mucha E, Humpert ML, Berken A: Interactions in the pollen-specific receptor-like kinases-containing signaling network. Eur J Cell Biol 2010, 89:917-923.
• [107]Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH: Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16:1220-1234.
• [108]Duan Q, Kita D, Li C, Cheung AY, Wu HM: FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci U S A 2010, 107:17821-17826.
• [109]Zhou K, Wang Y, Gorski JL, Nomura N, Collard J, Bokoch GM: Guanine nucleotide exchange factors regulate specificity of downstream signaling from Rac and Cdc42. J Biol Chem 1998, 273:16782-16786.
• [110]Olson MF: Guanine nucleotide exchange factors for the Rho GTPases: a role in human disease? J Mol Med (Berl) 1996, 74:563-571.
• [111]Pasteris NG, Cadle A, Logie LJ, Porteous ME, Schwartz CE, Stevenson RE, Glover TW, Wilroy RS, Gorski JL: Isolation and characterization of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell 1994, 79:669-678.
• [112]Ayala I, Giacchetti G, Caldieri G, Attanasio F, Mariggio S, Tete S, Polishchuk R, Castronovo V, Buccione R: Faciogenital dysplasia protein Fgd1 regulates invadopodia biogenesis and extracellular matrix degradation and is up-regulated in prostate and breast cancer. Cancer Res 2009, 69:747-752.
• [113]Kost B: Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol 2008, 18:119-127.
• [114]Donaldson JG, Jackson CL: ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 2011, 12:362-375.
• [115]Nielsen ME, Feechan A, Bohlenius H, Ueda T, Thordal-Christensen H: Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci U S A 2012, 109:11443-11448.
• [116]Palacios F, Price L, Schweitzer J, Collard JG, D’Souza-Schorey C: An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 2001, 20:4973-4986.
• [117]Hashimoto S, Onodera Y, Hashimoto A, Tanaka M, Hamaguchi M, Yamada A, Sabe H: Requirement for Arf6 in breast cancer invasive activities. Proc Natl Acad Sci U S A 2004, 101:6647-6652.
• [118]Tague SE, Muralidharan V, D’Souza-Schorey C: ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc Natl Acad Sci U S A 2004, 101:9671-9676.
• [119]Muralidharan-Chari V, Hoover H, Clancy J, Schweitzer J, Suckow MA, Schroeder V, Castellino FJ, Schorey JS, D’Souza-Schorey C: ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res 2009, 69:2201-2209.
• [120]Hernandez-Deviez DJ, Casanova JE, Wilson JM: Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci 2002, 5:623-624.
• [121]Albertinazzi C, Za L, Paris S, de Curtis I: ADP-ribosylation factor 6 and a functional PIX/p95-APP1 complex are required for Rac1B-mediated neurite outgrowth. Mol Biol Cell 2003, 14:1295-1307.
• [122]Hernandez-Deviez DJ, Roth MG, Casanova JE, Wilson JM: ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol Biol Cell 2004, 15:111-120.
• [123]Moore CD, Thacker EE, Larimore J, Gaston D, Underwood A, Kearns B, Patterson SI, Jackson T, Chapleau C, Pozzo-Miller L: The neuronal Arf GAP centaurin alpha1 modulates dendritic differentiation. J Cell Sci 2007, 120:2683-2693.
• [124]Song XF, Yang CY, Liu J, Yang WC: RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol 2006, 141:966-976.
• [125]Yoo CM, Wen J, Motes CM, Sparks JA, Blancaflor EB: A class I ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis. Plant Physiol 2008, 147:1659-1674.
• [126]Yoo CM, Quan L, Cannon AE, Wen J, Blancaflor EB: AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J 2012, 69:1064-1076.
• [127]Hutagalung AH, Novick PJ: Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011, 91:119-149.
• [128]Stenmark H: Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009, 10:513-525.
• [129]Woollard AA, Moore I: The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol 2008, 11:610-619.
• [130]Bravo-Cordero JJ, Marrero-Diaz R, Megias D, Genis L, Garcia-Grande A, Garcia MA, Arroyo AG, Montoya MC: MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J 2007, 26:1499-1510.
• [131]Caswell PT, Spence HJ, Parsons M, White DP, Clark K, Cheng KW, Mills GB, Humphries MJ, Messent AJ, Anderson KI: Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev Cell 2007, 13:496-510.
• [132]Hendrix A, Maynard D, Pauwels P, Braems G, Denys H, Van den BR, Lambert J, Van Belle S, Cocquyt V, Gespach C: Effect of the secretory small GTPase Rab27B on breast cancer growth, invasion, and metastasis. J Natl Cancer Inst 2010, 102:866-880.
• [133]Peranen J: Rab8 GTPase as a regulator of cell shape. Cytoskeleton (Hoboken) 2011, 68:527-539.
• [134]Wang L, Liang Z, Li G: Rab22 controls NGF signaling and neurite outgrowth in PC12 cells. Mol Biol Cell 2011, 22:3853-3860.
• [135]Mori Y, Matsui T, Furutani Y, Yoshihara Y, Fukuda M: Small GTPase Rab17 regulates dendritic morphogenesis and postsynaptic development of hippocampal neurons. J Biol Chem 2012, 287:8963-8973.
• [136]Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M: van den BW, van Dongen W, Richter S, Geldner N, Takano J et al.: Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 2010, 22:1344-1357.
• [137]Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E: The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 2004, 16:1589-1603.
• [138]de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM: Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 2005, 17:2564-2579.
• [139]Szumlanski AL, Nielsen E: The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 2009, 21:526-544.
• [140]Vignjevic D, Montagnac G: Reorganisation of the dendritic actin network during cancer cell migration and invasion. Semin Cancer Biol 2008, 18:12-22.
• [141]Jacobs T, Causeret F, Nishimura YV, Terao M, Norman A, Hoshino M, Nikolic M: Localized activation of p21-activated kinase controls neuronal polarity and morphology. J Neurosci 2007, 27:8604-8615.
• [142]Geitmann A: How to shape a cylinder: pollen tube as a model system for the generation of complex cellular geometry. Sex Plant Reprod 2010, 23:63-71.
• [143]Gossot O, Geitmann A: Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton. Planta 2007, 226:405-416.
• [144]Cheung AY, Niroomand S, Zou Y, Wu HM: A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc Natl Acad Sci U S A 2010, 107:16390-16395.
• [145]Daher FB, Geitmann A: Actin depolymerizing factors ADF7 and ADF10 play distinct roles during pollen development and pollen tube growth. Plant Signal Behav 2012, 7:879-881.
• [146]Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK: Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 2005, 221:95-104.
• [147]Gibbon BC, Kovar DR, Staiger CJ: Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 1999, 11:2349-2363.
• [148]Ketelaar T, de Ruijter NC, Emons AM: Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 2003, 15:285-292.
• [149]Chen T, Teng N, Wu X, Wang Y, Tang W, Samaj J, Baluska F, Lin J: Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol 2007, 48:19-30.
• [150]Muallem S, Kwiatkowska K, Xu X, Yin HL: Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 1995, 128:589-598.
• [151]Bradke F, Dotti CG: The role of local actin instability in axon formation. Science 1999, 283:1931-1934.
• [152]Jog NR, Rane MJ, Lominadze G, Luerman GC, Ward RA, McLeish KR: The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am J Physiol Cell Physiol 2007, 292:C1690-C1700.
• [153]Valentijn KM, Gumkowski FD, Jamieson JD: The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells. J Cell Sci 1999, 112(Pt 1):81-96.
• [154]Goley ED, Welch MD: The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 2006, 7:713-726.
• [155]Stradal TE, Scita G: Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol 2006, 18:4-10.
• [156]Lorenz M, Yamaguchi H, Wang Y, Singer RH, Condeelis J: Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Curr Biol 2004, 14:697-703.
• [157]Cudmore S, Cossart P, Griffiths G, Way M: Actin-based motility of vaccinia virus. Nature 1995, 378:636-638.
• [158]Gouin E, Welch MD, Cossart P: Actin-based motility of intracellular pathogens. Curr Opin Microbiol 2005, 8:35-45.
• [159]Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM: Arp2/3 is a negative regulator of growth cone translocation. Neuron 2004, 43:81-94.
• [160]Mongiu AK, Weitzke EL, Chaga OY, Borisy GG: Kinetic-structural analysis of neuronal growth cone veil motility. J Cell Sci 2007, 120:1113-1125.
• [161]Korobova F, Svitkina T: Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 2010, 21:165-176.
• [162]Pommereit D, Wouters FS: An NGF-induced Exo70-TC10 complex locally antagonises Cdc42-mediated activation of N-WASP to modulate neurite outgrowth. J Cell Sci 2007, 120:2694-2705.
• [163]Szymanski DB: Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol 2005, 8:103-112.
• [164]Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB: A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci U S A 2008, 105:4044-4049.
• [165]Deeks MJ, Hussey PJ, Davies B: Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 2002, 7:492-498.
• [166]Cvrckova F, Novotny M, Pickova D, Zarsky V: Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics 2004, 5:44. BioMed Central Full Text
• [167]Grunt M, Zarsky V, Cvrckova F: Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing proteins. BMC Evol Biol 2008, 8:115. BioMed Central Full Text
• [168]Lizarraga F, Poincloux R, Romao M, Montagnac G, Le Dez G, Bonne I, Rigaill G, Raposo G, Chavrier P: Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res 2009, 69:2792-2800.
• [169]Ridley AJ: Life at the leading edge. Cell 2011, 145:1012-1022.
• [170]Matusek T, Gombos R, Szecsenyi A, Sanchez-Soriano N, Czibula A, Pataki C, Gedai A, Prokop A, Rasko I, Mihaly J: Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci 2008, 28:13310-13319.
• [171]Cheung AY, Wu HM: Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 2004, 16:257-269.
• [172]Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z: Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 2009, 21:3868-3884.
• [173]Yi K, Guo C, Chen D, Zhao B, Yang B, Ren H: Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiol 2005, 138:1071-1082.
• [174]Deeks MJ, Cvrckova F, Machesky LM, Mikitova V, Ketelaar T, Zarsky V, Davies B, Hussey PJ: Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol 2005, 168:529-540.
• [175]Goode BL, Eck MJ: Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 2007, 76:593-627.
• [176]Vidali L, van Gisbergen PA, Guerin C, Franco P, Li M, Burkart GM, Augustine RC, Blanchoin L, Bezanilla M: Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc Natl Acad Sci U S A 2009, 106:13341-13346.
• [177]Firat-Karalar EN, Welch MD: New mechanisms and functions of actin nucleation. Curr Opin Cell Biol 2011, 23:4-13.
• [178]Ahuja R, Pinyol R, Reichenbach N, Custer L, Klingensmith J, Kessels MM, Qualmann B: Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 2007, 131:337-350.
• [179]Vidali L, Burkart GM, Augustine RC, Kerdavid E, Tuzel E, Bezanilla M: Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell 2010, 22:1868-1882.
• [180]Peremyslov VV, Prokhnevsky AI, Dolja VV: Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell 2010, 22:1883-1897.
• [181]Prokhnevsky AI, Peremyslov VV, Dolja VV: Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 2008, 105:19744-19749.
• [182]Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV: Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 2008, 146:1109-1116.
• [183]Ojangu EL, Jarve K, Paves H, Truve E: Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma 2007, 230:193-202.
• [184]Peremyslov VV, Mockler TC, Filichkin SA, Fox SE, Jaiswal P, Makarova KS, Koonin EV, Dolja VV: Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 2011, 155:1191-1204.
• [185]Wagner W, Brenowitz SD, Hammer JA III: Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol 2011, 13:40-48.
• [186]McMichael BK, Cheney RE, Lee BS: Myosin X regulates sealing zone patterning in osteoclasts through linkage of podosomes and microtubules. J Biol Chem 2010, 285:9506-9515.
• [187]Peremyslov VV, Klocko AL, Fowler JE, Dolja VV: Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin. Front Plant Sci 2012, 3:184.
• [188]Schott DH, Collins RN, Bretscher A: Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J Cell Biol 2002, 156:35-39.
• [189]Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, Chen X, Desmarais V, van Rheenen J, Koleske AJ, Condeelis J: Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 2009, 186:571-587.
• [190]Kronenberg G, Gertz K, Baldinger T, Kirste I, Eckart S, Yildirim F, Ji S, Heuser I, Schrock H, Hortnagl H: Impact of actin filament stabilization on adult hippocampal and olfactory bulb neurogenesis. J Neurosci 2010, 30:3419-3431.
• [191]Ren H, Xiang Y: The function of actin-binding proteins in pollen tube growth. Protoplasma 2007, 230:171-182.
• [192]Strohmaier AR, Porwol T, Acker H, Spiess E: Three-dimensional organization of microtubules in tumor cells studied by confocal laser scanning microscopy and computer-assisted deconvolution and image reconstruction. Cells Tissues Organs 2000, 167:1-8.
• [193]Kikuchi K, Takahashi K: W. Cancer Sci 2008, 99:2252-2259.
• [194]Govek EE, Hatten ME, Van Aelst L: The role of Rho GTPase proteins in CNS neuronal migration. Dev Neurobiol 2011, 71:528-553.
• [195]Pak CW, Flynn KC, Bamburg JR: Actin-binding proteins take the reins in growth cones. Nat Rev Neurosci 2008, 9:136-147.
• [196]Stiess M, Bradke F: Neuronal polarization: the cytoskeleton leads the way. Dev Neurobiol 2011, 71:430-444.
• [197]Gallo G: The cytoskeletal and signaling mechanisms of axon collateral branching. Dev Neurobiol 2011, 71:201-220.
• [198]Goryunov D, He CZ, Lin CS, Leung CL, Liem RK: Nervous-tissue-specific elimination of microtubule-actin crosslinking factor 1a results in multiple developmental defects in the mouse brain. Mol Cell Neurosci 2010, 44:1-14.
• [199]Leung CL, Sun D, Zheng M, Knowles DR, Liem RK: Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 1999, 147:1275-1286.
• [200]Wu X, Kodama A, Fuchs E: ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008, 135:137-148.
• [201]Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E: ACF7: an essential integrator of microtubule dynamics. Cell 2003, 115:343-354.
• [202]Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L, He W, Chan WM, Andrews C, Demer JL, Robertson RL: Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 2010, 140:74-87.
• [203]Sieberer BJ, Ketelaar T, Esseling JJ, Emons AM: Microtubules guide root hair tip growth. New Phytol 2005, 167:711-719.
• [204]Bao Y, Kost B, Chua NH: Reduced expression of alpha-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J 2001, 28:145-157.
• [205]Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V: Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 2003, 217:122-130.
• [206]Bibikova TN, Blancaflor EB, Gilroy S: Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 1999, 17:657-665.
• [207]Cai G, Faleri C, Del Casino C, Emons AM, Cresti M: Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol 2011, 155:1169-1190.
• [208]Wu G, Gu Y, Li S, Yang Z: A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 2001, 13:2841-2856.
• [209]Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z: Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 2005, 120:687-700.
• [210]Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B: Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans 2006, 34:683-686.
• [211]Wu H, Rossi G, Brennwald P: The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol 2008, 18:397-404.
• [212]Koumandou VL, Dacks JB, Coulson RM, Field MC: Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol 2007, 7:29. BioMed Central Full Text
• [213]Synek L, Schlager N, Elias M, Quentin M, Hauser MT, Zarsky V: AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J 2006, 48:54-72.
• [214]Zarsky V, Cvrckova F, Potocky M, Hala M: Exocytosis and cell polarity in plants - exocyst and recycling domains. New Phytol 2009, 183:255-272.
• [215]Cvrckova F, Grunt M, Bezvoda R, Hala M, Kulich I, Rawat A, Zarsky V: Evolution of the land plant exocyst complexes. Front Plant Sci 2012, 3:159.
• [216]Liu J, Yue P, Artym VV, Mueller SC, Guo W: The role of the exocyst in matrix metalloproteinase secretion and actin dynamics during tumor cell invadopodia formation. Mol Biol Cell 2009, 20:3763-3771.
• [217]Lalli G: RalA and the exocyst complex influence neuronal polarity through PAR-3 and aPKC. J Cell Sci 2009, 122:1499-1506.
• [218]Lalli G, Hall A: Ral GTPases regulate neurite branching through GAP-43 and the exocyst complex. J Cell Biol 2005, 171:857-869.
• [219]Cole RA, Synek L, Zarsky V, Fowler JE: SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 2005, 138:2005-2018.
• [220]Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE: An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 2008, 20:1330-1345.
• [221]Geitmann A, Dumais J: Not-so-tip-growth. Plant Signal Behav 2009, 4:136-138.
• [222]Zuo X, Zhang J, Zhang Y, Hsu SC, Zhou D, Guo W: Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat Cell Biol 2006, 8:1383-1388.
• [223]Wang S, Liu Y, Adamson CL, Valdez G, Guo W, Hsu SC: The mammalian exocyst, a complex required for exocytosis, inhibits tubulin polymerization. J Biol Chem 2004, 279:35958-35966.
• [224]Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K: IQGAP1: a key regulator of adhesion and migration. J Cell Sci 2005, 118:2085-2092.
• [225]Jadeski L, Mataraza JM, Jeong HW, Li Z, Sacks DB: IQGAP1 stimulates proliferation and enhances tumorigenesis of human breast epithelial cells. J Biol Chem 2008, 283:1008-1017.
• [226]Dupraz S, Grassi D, Bernis ME, Sosa L, Bisbal M, Gastaldi L, Jausoro I, Caceres A, Pfenninger KH, Quiroga S: The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J Neurosci 2009, 29:13292-13301.
• [227]Sosa L, Dupraz S, Laurino L, Bollati F, Bisbal M, Caceres A, Pfenninger KH, Quiroga S: IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat Neurosci 2006, 9:993-995.
• [228]Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S: A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 2007, 17:947-952.
• [229]Li S, Gu Y, Yan A, Lord E, Yang ZB: RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant 2008, 1:1021-1035.
• [230]Das A, Guo W: Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol 2011, 21:383-386.
• [231]Caldieri G, Giacchetti G, Beznoussenko G, Attanasio F, Ayala I, Buccione R: Invadopodia biogenesis is regulated by caveolin-mediated modulation of membrane cholesterol levels. J Cell Mol Med 2009, 13:1728-1740.
• [232]Yamaguchi H, Takeo Y, Yoshida S, Kouchi Z, Nakamura Y, Fukami K: Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res 2009, 69:8594-8602.
• [233]Harel R, Futerman AH: Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J Biol Chem 1993, 268:14476-14481.
• [234]Schwarz A, Rapaport E, Hirschberg K, Futerman AH: A regulatory role for sphingolipids in neuronal growth. Inhibition of sphingolipid synthesis and degradation have opposite effects on axonal branching. J Biol Chem 1995, 270:10990-10998.
• [235]Pfrieger FW: Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? Bioessays 2003, 25:72-78.
• [236]Spor TC, Dezonne RS, Rehen SK, Gomes FC: Astrocytes treated by lysophosphatidic acid induce axonal outgrowth of cortical progenitors through extracellular matrix protein and epidermal growth factor signaling pathway. J Neurochem 2011, 119:113-123.
• [237]Ovecka M, Berson T, Beck M, Derksen J, Samaj J, Baluska F, Lichtscheidl IK: Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. Plant Cell 2010, 22:2999-3019.
• [238]Liu P, Li RL, Zhang L, Wang QL, Niehaus K, Baluska F, Samaj J, Lin JX: Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 2009, 60:303-313.
• [239]Boutte Y, Grebe M: Cellular processes relying on sterol function in plants. Curr Opin Plant Biol 2009, 12:705-713.
• [240]Balasubramanian N, Scott DW, Castle JD, Casanova JE, Schwartz MA: Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat Cell Biol 2007, 9:1381-1391.
• [241]Hanzal-Bayer MF, Hancock JF: Lipid rafts and membrane traffic. FEBS Lett 2007, 581:2098-2104.
• [242]Leitinger B, Hogg N: The involvement of lipid rafts in the regulation of integrin function. J Cell Sci 2002, 115:963-972.
• [243]Mazzone M, Baldassarre M, Beznoussenko G, Giacchetti G, Cao J, Zucker S, Luini A, Buccione R: Intracellular processing and activation of membrane type 1 matrix metalloprotease depends on its partitioning into lipid domains. J Cell Sci 2004, 117:6275-6287.
• [244]Otsuki M, Itoh T, Takenawa T: Neural Wiskott-Aldrich syndrome protein is recruited to rafts and associates with endophilin A in response to epidermal growth factor. J Biol Chem 2003, 278:6461-6469.
• [245]Lingwood D, Simons K: Lipid rafts as a membrane-organizing principle. Science 2010, 327:46-50.
• [246]Ko M, Zou K, Minagawa H, Yu W, Gong JS, Yanagisawa K, Michikawa M: Cholesterol-mediated neurite outgrowth is differently regulated between cortical and hippocampal neurons. J Biol Chem 2005, 280:42759-42765.
• [247]Meriane M, Tcherkezian J, Webber CA, Danek EI, Triki I, McFarlane S, Bloch-Gallego E, Lamarche-Vane N: Phosphorylation of DCC by Fyn mediates Netrin-1 signaling in growth cone guidance. J Cell Biol 2004, 167:687-698.
• [248]Pooler AM, Xi SC, Wurtman RJ: The 3-hydroxy-3-methylglutaryl co-enzyme A reductase inhibitor pravastatin enhances neurite outgrowth in hippocampal neurons. J Neurochem 2006, 97:716-723.
• [249]Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M: Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 2002, 157:521-532.
• [250]Shapiro L, Love J, Colman DR: Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci 2007, 30:451-474.
• [251]Gupta N, Wollscheid B, Watts JD, Scheer B, Aebersold R, DeFranco AL: Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol 2006, 7:625-633.
• [252]Xu X, Warrington AE, Wright BR, Bieber AJ, Van KV, Pease LR, Rodriguez M: A human IgM signals axon outgrowth: coupling lipid raft to microtubules. J Neurochem 2011, 119:100-112.
• [253]Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F: Proteomics of plant detergent-resistant membranes. Mol Cell Proteomics 2006, 5:1396-1411.
• [254]Simon-Plas F, Perraki A, Bayer E, Gerbeau-Pissot P, Mongrand S: An update on plant membrane rafts. Curr Opin Plant Biol 2011, 14:642-649.
• [255]Sorek N, Segev O, Gutman O, Bar E, Richter S, Poraty L, Hirsch JA, Henis YI, Lewinsohn E, Jurgens G: An S-acylation switch of conserved G domain cysteines is required for polarity signaling by ROP GTPases. Curr Biol 2010, 20:914-920.
• [256]del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA: Integrins regulate Rac targeting by internalization of membrane domains. Science 2004, 303:839-842.
• [257]Golub T, Caroni P: PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 2005, 169:151-165.
• [258]Yakir-Tamang L, Gerst JE: Phosphoinositides, exocytosis and polarity in yeast: all about actin? Trends Cell Biol 2009, 19:677-684.
• [259]Pike LJ, Miller JM: Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem 1998, 273:22298-22304.
• [260]Caroni P: New EMBO members’ review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts. EMBO J 2001, 20:4332-4336.
• [261]Yamaguchi H, Yoshida S, Muroi E, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K: Phosphatidylinositol 4,5-bisphosphate and PIP5-kinase Ialpha are required for invadopodia formation in human breast cancer cells. Cancer Sci 2010, 101:1632-1638.
• [262]Yamaguchi H, Yoshida S, Muroi E, Yoshida N, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K: Phosphoinositide 3-kinase signaling pathway mediated by p110alpha regulates invadopodia formation. J Cell Biol 2011, 193:1275-1288.
• [263]Thapa N, Sun Y, Schramp M, Choi S, Ling K, Anderson RA: Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells. Dev Cell 2012, 22:116-130.
• [264]Koh CG: Rho GTPases and their regulators in neuronal functions and development. Neurosignals 2006, 15:228-237.
• [265]Kouchi Z, Igarashi T, Shibayama N, Inanobe S, Sakurai K, Yamaguchi H, Fukuda T, Yanagi S, Nakamura Y, Fukami K: Phospholipase Cdelta3 regulates RhoA/Rho kinase signaling and neurite outgrowth. J Biol Chem 2011, 286:8459-8471.
• [266]Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH: Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 1999, 145:317-330.
• [267]Ischebeck T, Vu LH, Jin X, Stenzel I, Lofke C, Heilmann I: Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes. Mol Plant 2010, 3:870-881.
• [268]Ischebeck T, Stenzel I, Hempel F, Jin X, Mosblech A, Heilmann I: Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum. Plant J 2011, 65:453-468.
• [269]Xu N, Gao XQ, Zhao XY, Zhu DZ, Zhou LZ, Zhang XS: Arabidopsis AtVPS15 is essential for pollen development and germination through modulating phosphatidylinositol 3-phosphate formation. Plant Mol Biol 2011, 77:251-260.
• [270]Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E: A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 2006, 172:991-998.
• [271]Camacho L, Smertenko AP, Perez-Gomez J, Hussey PJ, Moore I: Arabidopsis Rab-E GTPases exhibit a novel interaction with a plasma-membrane phosphatidylinositol-4-phosphate 5-kinase. J Cell Sci 2009, 122:4383-4392.
• [272]Pleskot R, Pejchar P, Bezvoda R, Lichtscheidl IK, Wolters-Arts M, Marc J, Zarsky V, Potocky M: Turnover of Phosphatidic Acid through Distinct Signaling Pathways Affects Multiple Aspects of Pollen Tube Growth in Tobacco. Front Plant Sci 2012, 3:54.
• [273]Bedard K, Krause KH: The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007, 87:245-313.
• [274]Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, Courtneidge SA: Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2009, 2:ra53.
• [275]Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, Bokoch GM: Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal 2009, 2:ra54.
• [276]Tsatmali M, Walcott EC, Crossin KL: Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors. Brain Res 2005, 1040:137-150.
• [277]Tsatmali M, Walcott EC, Makarenkova H, Crossin KL: Reactive oxygen species modulate the differentiation of neurons in clonal cortical cultures. Mol Cell Neurosci 2006, 33:345-357.
• [278]Kennedy KA, Ostrakhovitch EA, Sandiford SD, Dayarathna T, Xie X, Waese EY, Chang WY, Feng Q, Skerjanc IS, Stanford WL: Mammalian numb-interacting protein 1/dual oxidase maturation factor 1 directs neuronal fate in stem cells. J Biol Chem 2010, 285:17974-17985.
• [279]Katoh S, Mitsui Y, Kitani K, Suzuki T: Hyperoxia induces the differentiated neuronal phenotype of PC12 cells by producing reactive oxygen species. Biochem Biophys Res Commun 1997, 241:347-351.
• [280]Katoh S, Mitsui Y, Kitani K, Suzuki T: Hyperoxia induces the neuronal differentiated phenotype of PC12 cells via a sustained activity of mitogen-activated protein kinase induced by Bcl-2. Biochem J 1999, 338(Pt 2):465-470.
• [281]Suzukawa K, Miura K, Mitsushita J, Resau J, Hirose K, Crystal R, Kamata T: Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J Biol Chem 2000, 275:13175-13178.
• [282]Kamata H, Oka S, Shibukawa Y, Kakuta J, Hirata H: Redox regulation of nerve growth factor-induced neuronal differentiation of PC12 cells through modulation of the nerve growth factor receptor, TrkA. Arch Biochem Biophys 2005, 434:16-25.
• [283]Camacho L, Malho R: Endo/exocytosis in the pollen tube apex is differentially regulated by Ca2+ and GTPases. J Exp Bot 2003, 54:83-92.
• [284]Coelho PC, Malho R: Correlative Analysis of [Ca](C) and Apical Secretion during Pollen Tube Growth and Reorientation. Plant Signal Behav 2006, 1:152-157.
• [285]Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu LH, Obermeyer G, Feijo JA: Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 2011, 332:434-437.
• [286]Bibikova TN, Zhigilei A, Gilroy S: Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 1997, 203:495-505.
• [287]Wymer CL, Bibikova TN, Gilroy S: Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 1997, 12:427-439.
• [288]Mucha E, Hoefle C, Huckelhoven R, Berken A: RIP3 and AtKinesin-. Eur J Cell Biol 2010, 89:906-916.
• [289]Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD: Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003, 422:442-446.
• [290]Potocky M, Jones MA, Bezvoda R, Smirnoff N, Zarsky V: Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 2007, 174:742-751.
• [291]Weaver AM: Regulation of cancer invasion by reactive oxygen species and Tks family scaffold proteins. Sci Signal 2009, 2:e56.
• [292]Giannoni E, Taddei ML, Chiarugi P: Src redox regulation: again in the front line. Free Radic Biol Med 2010, 49:516-527.
• [293]Gianni D, Bohl B, Courtneidge SA, Bokoch GM: The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol Biol Cell 2008, 19:2984-2994.
• [294]Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW: Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 1991, 353:668-670.
• [295]Woo CH, Lee ZW, Kim BC, Ha KS, Kim JH: Involvement of cytosolic phospholipase A2, and the subsequent release of arachidonic acid, in signalling by rac for the generation of intracellular reactive oxygen species in rat-2 fibroblasts. Biochem J 2000, 348(Pt 3):525-530.
• [296]Zhou L, Too HP: Mitochondrial localized STAT3 is involved in NGF induced neurite outgrowth. PLoS One 2011, 6:e21680.
• [297]Sagi M, Fluhr R: Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 2006, 141:336-340.
• [298]Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L: Local positive feedback regulation determines cell shape in root hair cells. Science 2008, 319:1241-1244.
• [299]Munnamalai V, Suter DM: Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J Neurochem 2009, 108:644-661.
• [300]Swanson S, Gilroy S: ROS in plant development. Physiol Plant 2010, 138:384-392.
• [301]Elias M, Klimes V: Rho GTPases: deciphering the evolutionary history of a complex protein family. Methods Mol Biol 2012, 827:13-34.
• [302]Cvrckova F, Rivero F, Bavlnka B: Evolutionarily conserved modules in actin nucleation: lessons from Dictyostelium discoideum and plants. Review article. Protoplasma 2004, 224:15-31.
• [303]Rivero F, Cvrckova F: Origins and evolution of the actin cytoskeleton. Adv Exp Med Biol 2007, 607:97-110.
• [304]Zhang Y, Franco M, Ducret A, Mignot T: A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 2010, 8:e1000430.