期刊论文详细信息
EvoDevo
Transcriptional dynamics of a conserved gene expression network associated with craniofacial divergence in Arctic charr
Sigrídur Rut Franzdóttir1  Zophonías O Jónsson2  Sigurdur S Snorrason1  Jóhannes Gudbrandsson1  Valerie Helene Maier1  Arnar Pálsson2  Kalina Hristova Kapralova1  Ehsan Pashay Ahi1 
[1] Institute of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavik, Iceland;Biomedical Center, University of Iceland, Vatnsmýrarvegur 16, 101 Reykjavik, Iceland
关键词: Salvelinus alpinus;    Morphogenesis;    Gene network;    Divergent evolution;    Craniofacial development;    Coexpression;    Arctic charr;   
Others  :  1093218
DOI  :  10.1186/2041-9139-5-40
 received in 2014-07-11, accepted in 2014-09-17,  发布年份 2014
PDF
【 摘 要 】

Background

Understanding the molecular basis of craniofacial variation can provide insights into key developmental mechanisms of adaptive changes and their role in trophic divergence and speciation. Arctic charr (Salvelinus alpinus) is a polymorphic fish species, and, in Lake Thingvallavatn in Iceland, four sympatric morphs have evolved distinct craniofacial structures. We conducted a gene expression study on candidates from a conserved gene coexpression network, focusing on the development of craniofacial elements in embryos of two contrasting Arctic charr morphotypes (benthic and limnetic).

Results

Four Arctic charr morphs were studied: one limnetic and two benthic morphs from Lake Thingvallavatn and a limnetic reference aquaculture morph. The presence of morphological differences at developmental stages before the onset of feeding was verified by morphometric analysis. Following up on our previous findings that Mmp2 and Sparc were differentially expressed between morphotypes, we identified a network of genes with conserved coexpression across diverse vertebrate species. A comparative expression study of candidates from this network in developing heads of the four Arctic charr morphs verified the coexpression relationship of these genes and revealed distinct transcriptional dynamics strongly correlated with contrasting craniofacial morphologies (benthic versus limnetic). A literature review and Gene Ontology analysis indicated that a significant proportion of the network genes play a role in extracellular matrix organization and skeletogenesis, and motif enrichment analysis of conserved noncoding regions of network candidates predicted a handful of transcription factors, including Ap1 and Ets2, as potential regulators of the gene network. The expression of Ets2 itself was also found to associate with network gene expression. Genes linked to glucocorticoid signalling were also studied, as both Mmp2 and Sparc are responsive to this pathway. Among those, several transcriptional targets and upstream regulators showed differential expression between the contrasting morphotypes. Interestingly, although selected network genes showed overlapping expression patterns in situ and no morph differences, Timp2 expression patterns differed between morphs.

Conclusion

Our comparative study of transcriptional dynamics in divergent craniofacial morphologies of Arctic charr revealed a conserved network of coexpressed genes sharing functional roles in structural morphogenesis. We also implicate transcriptional regulators of the network as targets for future functional studies.

【 授权许可】

   
2014 Ahi et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150130161415399.pdf 1629KB PDF download
Figure 5. 179KB Image download
Figure 4. 107KB Image download
Figure 3. 134KB Image download
Figure 2. 107KB Image download
Figure 1. 113KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Albertson RC, Kocher TD: Genetic and developmental basis of cichlid trophic diversity. Heredity 2006, 97:211-221.
  • [2]Mabuchi K, Miya M, Azuma Y, Nishida M: Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evol Biol 2007, 7:10. BioMed Central Full Text
  • [3]Ward AJW, Webster MM, Hart PJB: Intraspecific food competition in fishes. Fish Fish 2006, 7:231-261.
  • [4]Whiteley AR: Trophic polymorphism in a riverine fish: morphological, dietary, and genetic analysis of mountain whitefish. Biol J Linn Soc 2007, 92:253-267.
  • [5]Jeffery WR: Chapter 8. Evolution and development in the cavefish Astyanax. Curr Top Dev Biol 2009, 86:191-221.
  • [6]Helms JA, Cordero D, Tapadia MD: New insights into craniofacial morphogenesis. Development 2005, 132:851-861.
  • [7]Yelick PC, Schilling TF: Molecular dissection of craniofacial development using zebrafish. Crit Rev Oral Biol Med 2002, 13:308-322.
  • [8]Parsons KJ, Trent Taylor A, Powder KE, Albertson RC: Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids. Nat Commun 2014, 5:3629.
  • [9]Ekblom R, Galindo J: Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 2011, 107:1-15.
  • [10]Hinaux H, Poulain J, Da Silva C, Noirot C, Jeffery WR, Casane D, Rétaux S: De novo sequencing of Astyanax mexicanus surface fish and Pachón cavefish transcriptomes reveals enrichment of mutations in cavefish putative eye genes. PLoS One 2013, 8:e53553.
  • [11]Snorrason SS, Skúlason S: Adaptive speciation in northern freshwater fishes. In Adaptive Speciation (Cambridge Studies in Adaptive Dynamics No. 3). Edited by Dieckmann U, Doebeli M, Metz JAJ, Tautz D. Cambridge, UK: Cambridge University Press; 2004:210-228.
  • [12]Skúlason S, Smith TB: Resource polymorphisms in vertebrates. Trends Ecol Evol 1995, 10:366-370.
  • [13]Jonsson B, Jonsson N: Polymorphism and speciation in Arctic charr. J Fish Biol 2001, 58:605-638.
  • [14]Brunner PC, Douglas MR, Osinov A, Wilson CC, Bernatchez L: Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evolution 2001, 55:573-586.
  • [15]Skúlason S, Snorrason SS, Noakes DLG, Ferguson MM, Malmquist HJ: Segregation in spawning and early life history among polymorphic Arctic charr, Salvelinus alpinus, in Thingvallavatn, Iceland. J Fish Biol 2006, 35(Suppl sA):225-232.
  • [16]Snorrason SS, Skúlason S, Jonsson B, Malquist HJ, Jonasson PM, Sandlund OT, Lindem T: Trophic specialization in Arctic charr Salvelinus alpinus (Pisces; Salmonidae): morphological divergence and ontogenetic niche shifts. Biol J Linn Soc 1994, 52:1-18.
  • [17]Malmquist H, Snorrason S, Skúlason S, Jonsson B, Sandlund O, Jonasson P: Diet differentiation in polymorphic Arctic charr in Thingvallavatn, Iceland. J Anim Ecol 1992, 61:21-35.
  • [18]Sandlund T, Gunnarsson K, Jónasson P, Jonsson B, Lindem T, Magnússon K, Malmquist H, Sigurjónsdóttir H, Skúlason S, Snorrason S: The Arctic charr Salvelinus alpinus in Thingvallavatn. Oikos 1992, 64:305-351.
  • [19]Jonsson B, Skúlason S, Snorrason SS, Sandlund OT, Malmquist HJ, Jónasson PM, Cydemo R, Lindem T: Life history variation of polymorphic Arctic charr (Salvelinus alpinus) in Thingvallavatn, Iceland. Can J Fish Aquat Sci 1988, 45:1537-1547.
  • [20]Kapralova KH, Morrissey MB, Kristjánsson BK, Olafsdóttir GÁ, Snorrason SS, Ferguson MM: Evolution of adaptive diversity and genetic connectivity in Arctic charr (Salvelinus alpinus) in Iceland. Heredity (Edinb) 2011, 472-487.
  • [21]Kapralova KH, Gudbrandsson J, Reynisdottir S, Santos CB, Baltanás VC, Maier VH, Snorrason SS, Palsson A: Differentiation at the MHCIIα and Cath2 loci in sympatric Salvelinus alpinus resource morphs in Lake Thingvallavatn. PLoS One 2013, 8:e69402.
  • [22]Skúlason S, Noakess D, Snorrason S: Ontogeny of trophic morphology in four sympatric morphs of Arctic charr Salvelinus alpinus in Thingvallavatn, Iceland. Biol J Linn Soc 1989, 38:281-301.
  • [23]Eiriksson GM, Skulason S, Snorrason SS: Heterochrony in skeletal development and body size in progeny of two morphs of Arctic charr from Thingvallavatn, Iceland. J Fish Biol 1999, 55:175-185.
  • [24]Parsons KJ, Skúlason S, Ferguson M: Morphological variation over ontogeny and environments in resource polymorphic Arctic charr (Salvelinus alpinus). Evol Dev 2010, 12:246-257.
  • [25]Boughton DA, Collette BB, McCune AR: Heterochrony in jaw morphology of needlefishes (Teleostei: Belonidae). Syst Biol 1991, 40:329-354.
  • [26]Albertson RC, Yan YL, Titus TA, Pisano E, Vacchi M, Yelick PC, Detrich HW 3rd, Postlethwait JH: Molecular pedomorphism underlies craniofacial skeletal evolution in Antarctic notothenioid fishes. BMC Evol Biol 2010, 10:4. BioMed Central Full Text
  • [27]Gunter HM, Koppermann C, Meyer A: Revisiting de Beer’s textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronic growth, and underlies morphological innovation in the jaws of belonoid fishes. EvoDevo 2014, 5:8. BioMed Central Full Text
  • [28]Sibthorpe D, Sturlaugsdóttir R, Kristjansson BK, Thorarensen H, Skúlason S, Johnston IA: Characterisation and expression of the paired box protein 7 (Pax7) gene in polymorphic Arctic charr (Salvelinus alpinus). Comp Biochem Physiol B Biochem Mol Biol 2006, 145:371-383.
  • [29]Stern DL: The genetic causes of convergent evolution. Nat Rev Genet 2013, 14:751-764.
  • [30]Filteau M, Pavey SA, St-Cyr J, Bernatchez L: Gene coexpression networks reveal key drivers of phenotypic divergence in lake whitefish. Mol Biol Evol 2013, 30:1384-1396.
  • [31]Macqueen DJ, Kristjánsson BK, Paxton CGM, Vieira VLA, Johnston IA: The parallel evolution of dwarfism in Arctic charr is accompanied by adaptive divergence in mTOR-pathway gene expression. Mol Ecol 2011, 20:3167-3184.
  • [32]Ahi EP, Guðbrandsson J, Kapralova KH, Franzdóttir SR, Snorrason SS, Maier VH, Jónsson ZO: Validation of reference genes for expression studies during craniofacial development in Arctic charr. PLoS One 2013, 8:e66389.
  • [33]Rotllant J, Liu D, Yan Y, Postlethwait JH, Westerfield M, Du S: Sparc (Osteonectin) functions in morphogenesis of the pharyngeal skeleton and inner ear. Matrix Biol 2008, 27:561-572.
  • [34]Renn J, Schaedel M, Volff JN, Goerlich R, Schartl M, Winkler C: Dynamic expression of sparc precedes formation of skeletal elements in the Medaka (Oryzias latipes). Gene 2006, 372:208-218.
  • [35]Hillegass JM, Villano CM, Cooper KR, White LA: Glucocorticoids alter craniofacial development and increase expression and activity of matrix metalloproteinases in developing zebrafish (Danio rerio). Toxicol Sci 2008, 102:413-424.
  • [36]Bonventre JA, White LA, Cooper KR: Craniofacial abnormalities and altered wnt and mmp mRNA expression in zebrafish embryos exposed to gasoline oxygenates ETBE and TAME. Aquat Toxicol 2012, 120–121:45-53.
  • [37]Mosig RA, Dowling O, DiFeo A, Ramirez MCM, Parker IC, Abe E, Diouri J, Al AA, Wylie JD, Oblander SA, Madri J, Bianco P, Apte SS, Zaidi M, Doty SB, Majeska RJ, Schaffler MB, Martignetti JA: Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum Mol Genet 2007, 16:1113-1123.
  • [38]Seet LF, Su R, Toh LZ, Wong TT: In vitro analyses of the anti-fibrotic effect of SPARC silencing in human Tenon’s fibroblasts: comparisons with mitomycin C. J Cell Mol Med 2012, 16:1245-1259.
  • [39]Li B, Li F, Chi L, Zhang L, Zhu S: The expression of SPARC in human intracranial aneurysms and its relationship with MMP-2/-9. PLoS One 2013, 8:e58490.
  • [40]Yamanaka M, Kanda K, Li NC, Fukumori T, Oka N, Kanayama HO, Kagawa S: Analysis of the gene expression of SPARC and its prognostic value for bladder cancer. J Urol 2001, 166:2495-2499.
  • [41]Gorodilov YN: Description of the early ontogeny of the Atlantic salmon, Salmo salar, with a novel system of interval (state) identification. Environ Biol Fishes 1996, 47:109-127.
  • [42]Walker MB, Kimmel CB: A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 2007, 82:23-28.
  • [43]Rohlf FJ: tps series software. http://life.bio.sunysb.edu/morph/soft-tps.html webcite (accessed 25 September 2014)
  • [44]Klingenberg CP: MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 2011, 11:353-357.
  • [45]Rohlf FJ, Slice D: Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 1990, 39:40-59.
  • [46]Klingenberg CP, Barluenga M, Meyer A: Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 2002, 56:1909-1920.
  • [47]R Core Team: R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2013. http://www.R-project.org/ webcite
  • [48]Obayashi T, Kinoshita K: COXPRESdb: a database to compare gene coexpression in seven model animals. Nucleic Acids Res 2011, 39(Database issue):D1016-D1022.
  • [49]Bradford Y, Conlin T, Dunn N, Fashena D, Frazer K, Howe DG, Knight J, Mani P, Martin R, Moxon SAT, Paddock H, Pich C, Ramachandran S, Ruef BJ, Ruzicka L, Bauer Schaper H, Schaper K, Shao X, Singer A, Sprague J, Sprunger B, Van Slyke C, Westerfield M: ZFIN: enhancements and updates to the Zebrafish Model Organism Database. Nucleic Acids Res 2011, 39(Database issue):D822-D829.
  • [50]Alexeyenko A, Sonnhammer ELL: Global networks of functional coupling in eukaryotes from comprehensive data integration. Genome Res 2009, 19:1107-1116.
  • [51]Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
  • [52]Wang J, Duncan D, Shi Z, Zhang B: WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 2013, 41(Web Server issue):W77-W83.
  • [53]Ramakers C, Ruijter JM, Deprez RHL, Moorman AF: Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 2003, 339:62-66.
  • [54]Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
  • [55]Bergkvist A, Rusnakova V, Sindelka R, Garda JMA, Sjögreen B, Lindh D, Forootan A, Kubista M: Gene expression profiling–clusters of possibilities. Methods 2010, 50:323-335.
  • [56]Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, Raney BJ, Pohl A, Malladi VS, Li CH, Lee BT, Learned K, Kirkup V, Hsu F, Heitner S, Harte RA, Haeussler M, Guruvadoo L, Goldman M, Giardine BM, Fujita PA, Dreszer TR, Diekhans M, Cline MS, Clawson H, Barber GP, et al.: The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 2013, 41(Database issue):D64-D69.
  • [57]Carlson JM, Chakravarty A, DeZiel CE, Gross RH: SCOPE: a web server for practical de novo motif discovery. Nucleic Acids Res 2007, 35(Web Server issue):W259-W264.
  • [58]Liu X, Brutlag DL, Liu JS: BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 2001, 6:127-138.
  • [59]Mahony S, Benos PV: STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 2007, 35(Web Server issue):W253-W258.
  • [60]Matys V, Fricke E, Geffers R, Gößling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Münch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E: TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 2003, 31:374-378.
  • [61]Macqueen DJ, Johnston IA: Evolution of follistatin in teleosts revealed through phylogenetic, genomic and expression analyses. Dev Genes Evol 2008, 218:1-14.
  • [62]Ng KW, Manji SS, Young MF, Findlay DM: Opposing influences of glucocorticoid and retinoic acid on transcriptional control in preosteoblasts. Mol Endocrinol 1989, 3:2079-2085.
  • [63]Yao W, Cheng Z, Busse C, Pham A, Nakamura MC, Lane NE: Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum 2008, 58:1674-1686.
  • [64]Kimoto S, Cheng SL, Zhang SF, Avioli LV: The effect of glucocorticoid on the synthesis of biglycan and decorin in human osteoblasts and bone marrow stromal cells. Endocrinology 1994, 135:2423-2431.
  • [65]Pereira RC, Blanquaert F, Canalis E: Cortisol enhances the expression of mac25/insulin-like growth factor-binding protein-related protein-1 in cultured osteoblasts. Endocrinology 1999, 140:228-232.
  • [66]Hamidouche Z, Fromigué O, Ringe J, Häupl T, Vaudin P, Pagès JC, Srouji S, Livne E, Marie PJ: Priming integrin α5 promotes human mesenchymal stromal cell osteoblast differentiation and osteogenesis. Proc Natl Acad Sci U S A 2009, 106:18587-18591.
  • [67]Zhang XN, Xue LQ, Jiang H, Yang SY, Song HD, Ma QY: The mechanism of mimecan transcription induced by glucocorticoid in pituitary corticotroph cells. Mol Cell Biochem 2012, 360:321-328.
  • [68]Désarnaud F, Bidichandani S, Patel PI, Baulieu EE, Schumacher M: Glucocorticosteroids stimulate the activity of the promoters of peripheral myelin protein-22 and protein zero genes in Schwann cells. Brain Res 2000, 865:12-16.
  • [69]Zhou H, Mak W, Kalak R, Street J, Fong-Yee C, Zheng Y, Dunstan CR, Seibel MJ: Glucocorticoid-dependent Wnt signaling by mature osteoblasts is a key regulator of cranial skeletal development in mice. Development 2009, 136:427-436.
  • [70]Hillegass JM, Villano CM, Cooper KR, White LA: Matrix metalloproteinase-13 is required for zebra fish (Danio rerio) development and is a target for glucocorticoids. Toxicol Sci 2007, 100:168-179.
  • [71]Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R: MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995, 377:68-71.
  • [72]Koliwad SK, Kuo T, Shipp LE, Gray NE, Backhed F, So AYL, Farese RV Jr, Wang JC: Angiopoietin-like 4 (ANGPTL4, fasting-induced adipose factor) is a direct glucocorticoid receptor target and participates in glucocorticoid-regulated triglyceride metabolism. J Biol Chem 2009, 284:25593–25601. A published erratum appears in. J Biol Chem 2012, 287:4394.
  • [73]Webster MK, Goya L, Ge Y, Maiyar AC, Firestone GL: Characterization of sgk, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol Cell Biol 1993, 13:2031-2040.
  • [74]Martin LJ, Tremblay JJ: Glucocorticoids antagonize cAMP-induced Star transcription in Leydig cells through the orphan nuclear receptor NR4A1. J Mol Endocrinol 2008, 41:165-175.
  • [75]Chasiotis H, Wood CM, Kelly SP: Cortisol reduces paracellular permeability and increases occludin abundance in cultured trout gill epithelia. Mol Cell Endocrinol 2010, 323:232-238.
  • [76]Perretti M, D’Acquisto F: Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 2009, 9:62-70.
  • [77]Wang FS, Lin CL, Chen YJ, Wang CJ, Yang KD, Huang YT, Sun YC, Huang HC: Secreted frizzled-related protein 1 modulates glucocorticoid attenuation of osteogenic activities and bone mass. Endocrinology 2005, 146:2415-2423.
  • [78]Beato M, Klug J: Steroid hormone receptors: an update. Hum Reprod Update 2000, 6:225-236.
  • [79]Baker ME: Evolutionary analysis of 11β-hydroxysteroid dehydrogenase-type 1, -type 2, -type 3 and 17β-hydroxysteroid dehydrogenase-type 2 in fish. FEBS Lett 2004, 574:167-170.
  • [80]Kino T, Nordeen SK, Chrousos GP: Conditional modulation of glucocorticoid receptor activities by CREB-binding protein (CBP) and p300. J Steroid Biochem Mol Biol 1999, 70:15-25.
  • [81]Rüdiger JJ, Roth M, Bihl MP, Cornelius BC, Johnson M, Ziesche R, Block L-H: Interaction of C/EBPα and the glucocorticoid receptor in vivo and in nontransformed human cells. FASEB J 2002, 16:177-184.
  • [82]Geng C, Vedeckis WV: c-Myb and members of the c-Ets family of transcription factors act as molecular switches to mediate opposite steroid regulation of the human glucocorticoid receptor 1A promoter. J Biol Chem 2005, 280:43264-43271.
  • [83]Mullick J, Anandatheerthavarada HK, Amuthan G, Bhagwat SV, Biswas G, Camasamudram V, Bhat NK, Reddy SE, Rao V, Avadhani NG: Physical interaction and functional synergy between glucocorticoid receptor and Ets2 proteins for transcription activation of the rat cytochrome P-450c27 promoter. J Biol Chem 2001, 276:18007-18017.
  • [84]Hasegawa T, Zhao L, Caron KM, Majdic G, Suzuki T, Shizawa S, Sasano H, Parker KL: Developmental roles of the steroidogenic acute regulatory protein (StAR) as revealed by StAR knockout mice. Mol Endocrinol 2000, 14:1462-1471.
  • [85]Shea-Eaton WK, Trinidad MJ, Lopez D, Nackley A, McLean MP: Sterol regulatory element binding protein-1a regulation of the steroidogenic acute regulatory protein gene. Endocrinology 2001, 142:1525-1533.
  • [86]Piasecka B, Lichocki P, Moretti S, Bergmann S, Robinson-Rechavi M: The hourglass and the early conservation models—co-existing patterns of developmental constraints in vertebrates. PLoS Genet 2013, 9:e1003476.
  • [87]Tanay A, Regev A, Shamir R: Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A 2005, 102:7203-7208.
  • [88]Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, Barkai N: Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 2005, 309:938-940.
  • [89]Raouf A, Ganss B, McMahon C, Vary C, Roughley PJ, Seth A: Lumican is a major proteoglycan component of the bone matrix. Matrix Biol 2002, 21:361-367.
  • [90]Pedersen ME, Ytteborg E, Kohler A, Baeverfjord G, Enersen G, Ruyter B, Takle H, Hannesson KO: Small leucine-rich proteoglycans in the vertebrae of Atlantic salmon Salmo salar. Dis Aquat Organ 2013, 106:57-68.
  • [91]Ying S, Shiraishi A, Candace W, Converse RL, James L, Swiergiel J, Mary R, Conrad GW, Winston W, Chem JB, Kao CWC, Funderburgh JL, Roth MR, Kao WWY: Characterization and expression of the mouse lumican gene. J Biol Chem 1997, 272:30306-30313.
  • [92]Yeh LK, Liu CY, Kao WWY, Huang CJ, Hu FR, Chien CL, Wang IJ: Knockdown of zebrafish lumican gene (zlum) causes scleral thinning and increased size of scleral coats. J Biol Chem 2010, 285:28141-28155.
  • [93]Brugmann SA, Goodnough LH, Gregorieff A, Leucht P, ten Berge D, Fuerer C, Clevers H, Nusse R, Helms JA: Wnt signaling mediates regional specification in the vertebrate face. Development 2007, 134:3283-3295.
  • [94]Zhou H, Mak W, Zheng Y, Dunstan CR, Seibel MJ: Osteoblasts directly control lineage commitment of mesenchymal progenitor cells through Wnt signaling. J Biol Chem 2008, 283:1936-1945.
  • [95]Zoeller JJ, Pimtong W, Corby H, Goldoni S, Iozzo AE, Owens RT, Ho S-Y, Iozzo RV: A central role for decorin during vertebrate convergent extension. J Biol Chem 2009, 284:11728-11737.
  • [96]Petrey AC, Flanagan-Steet H, Johnson S, Fan X, De la Rosa M, Haskins ME, Nairn AV, Moremen KW, Steet R: Excessive activity of cathepsin K is associated with cartilage defects in a zebrafish model of mucolipidosis II. Dis Model Mech 2012, 5:177-190.
  • [97]Damazo AS, Moradi-Bidhendi N, Oliani SM, Flower RJ: Role of annexin 1 gene expression in mouse craniofacial bone development. Birth Defects Res A Clin Mol Teratol 2007, 79:524-532.
  • [98]Kassel O, Herrlich P: Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 2007, 275:13-29.
  • [99]Draper N, Stewart PM: 11β-hydroxysteroid dehydrogenase and the pre-receptor regulation of corticosteroid hormone action. J Endocrinol 2005, 186:251-271.
  • [100]Lane T, Sage E: The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J 1994, 8:163-173.
  • [101]Mott JD, Werb Z: Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004, 16:558-564.
  • [102]Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz JD, Schu P, von Figura K: Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A 1998, 95:13453-13458.
  • [103]Filanti C, Dickson GR, Di Martino D, Ulivi V, Sanguineti C, Romano P, Palermo C, Manduca P: The expression of metalloproteinase-2, -9, and -14 and of tissue inhibitors-1 and -2 is developmentally modulated during osteogenesis in vitro, the mature osteoblastic phenotype expressing metalloproteinase-14. J Bone Miner Res 2000, 15:2154-2168.
  • [104]Hocking AM, Shinomura T, McQuillan DJ: Leucine-rich repeat glycoproteins of the extracellular matrix. Matrix Biol 1998, 17:1-19.
  • [105]Keen RW, Woodford-Richens KL, Grant SF, Ralston SH, Lanchbury JS, Spector TD: Association of polymorphism at the type I collagen (COL1A1) locus with reduced bone mineral density, increased fracture risk, and increased collagen turnover. Arthritis Rheum 1999, 42:285-290.
  • [106]Nakashima K, de Crombrugghe B: Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet 2003, 19:458-466.
  • [107]Hess J, Angel P, Schorpp-Kistner M: AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 2004, 117:5965-5973.
  • [108]Chai Y, Ito Y, Han J: TGF-β signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit Rev Oral Biol Med 2003, 14:78-88.
  • [109]Sumarsono SH, Wilson TJ, Tymms MJ, Venter DJ, Corrick CM, Kola R, Lahoud MH, Papas TS, Seth A, Kola I: Down’s syndrome-like skeletal abnormalities in Ets2 transgenic mice. Nature 1996, 379:534-537.
  • [110]Rockman MV: The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. Evolution 2012, 66:1-17.
  • [111]Kapralova KH, Franzdóttir SR, Jónsson H, Snorrason SS, Jónsson ZO: Patterns of miRNA expression in Arctic charr development. PLoS One 2014, 9:e106084.
  • [112]Attanasio C, Nord AS, Zhu Y, Blow MJ, Li Z, Liberton DK, Morrison H, Plajzer-Frick I, Holt A, Hosseini R, Phouanenavong S, Akiyama JA, Shoukry M, Afzal V, Rubin EM, FitzPatrick DR, Ren B, Hallgrímsson B, Pennacchio LA, Visel A: Fine tuning of craniofacial morphology by distant-acting enhancers. Science 2013, 342:1241006.
  • [113]Parsons KJ, Sheets HD, Skúlason S, Ferguson MM: Phenotypic plasticity, heterochrony and ontogenetic repatterning during juvenile development of divergent Arctic charr (Salvelinus alpinus). J Evol Biol 2011, 24:1640-1652.
  文献评价指标  
  下载次数:17次 浏览次数:18次