期刊论文详细信息
EvoDevo
Expression of multiple Sox genes through embryonic development in the ctenophore Mnemiopsis leidyi is spatially restricted to zones of cell proliferation
Andreas D Baxevanis2  Mark Q Martindale3  Kevin Pang1  David K Simmons3  Christine E Schnitzler2 
[1] Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway;Genome Technology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA;Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL, USA
关键词: Stem cell;    Cell proliferation;    Mnemiopsis leidyi;    Lobate;    Ctenophore;    Sox;   
Others  :  801684
DOI  :  10.1186/2041-9139-5-15
 received in 2014-02-13, accepted in 2014-03-21,  发布年份 2014
PDF
【 摘 要 】

Background

The Sox genes, a family of transcription factors characterized by the presence of a high mobility group (HMG) box domain, are among the central groups of developmental regulators in the animal kingdom. They are indispensable in progenitor cell fate determination, and various Sox family members are involved in managing the critical balance between stem cells and differentiating cells. There are 20 mammalian Sox genes that are divided into five major groups (B, C, D, E, and F). True Sox genes have been identified in all animal lineages but not outside Metazoa, indicating that this gene family arose at the origin of the animals. Whole-genome sequencing of the lobate ctenophore Mnemiopsis leidyi allowed us to examine the full complement and expression of the Sox gene family in this early-branching animal lineage.

Results

Our phylogenetic analyses of the Sox gene family were generally in agreement with previous studies and placed five of the six Mnemiopsis Sox genes into one of the major Sox groups: SoxB (MleSox1), SoxC (MleSox2), SoxE (MleSox3, MleSox4), and SoxF (MleSox5), with one unclassified gene (MleSox6). We investigated the expression of five out of six Mnemiopsis Sox genes during early development. Expression patterns determined through in situ hybridization generally revealed spatially restricted Sox expression patterns in somatic cells within zones of cell proliferation, as determined by EdU staining. These zones were located in the apical sense organ, upper tentacle bulbs, and developing comb rows in Mnemiopsis, and coincide with similar zones identified in the cydippid ctenophore Pleurobrachia.

Conclusions

Our results are consistent with the established role of multiple Sox genes in the maintenance of stem cell pools. Both similarities and differences in juvenile cydippid stage expression patterns between Mnemiopsis Sox genes and their orthologs from Pleurobrachia highlight the importance of using multiple species to characterize the evolution of development within a given phylum. In light of recent phylogenetic evidence that Ctenophora is the earliest-branching animal lineage, our results are consistent with the hypothesis that the ancient primary function of Sox family genes was to regulate the maintenance of stem cells and function in cell fate determination.

【 授权许可】

   
2014 Schnitzler et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140708011946136.pdf 3555KB PDF download
Figure 7. 45KB Image download
Figure 6. 108KB Image download
Figure 5. 83KB Image download
Figure 4. 177KB Image download
Figure 3. 57KB Image download
Figure 2. 50KB Image download
Figure 1. 79KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】
  • [1]Chew L-J, Gallo V: The Yin and Yang of Sox proteins: activation and repression in development and disease. J Neurosci Res 2009, 87:3277-3287.
  • [2]Wegner M: All purpose Sox: the many roles of Sox proteins in gene expression. Int J Biochem Cell Biol 2010, 42:381-390.
  • [3]Bowles J, Schepers G, Koopman P: Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 2000, 227:239-255.
  • [4]Wegner M, Stolt CC: From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci 2005, 28:583-588.
  • [5]Dong C, Wilhelm D, Koopman P: Sox genes and cancer. Cytogenet Genome Res 2004, 105:442-447.
  • [6]Aaboe M: SOX4 Expression in bladder carcinoma: clinical aspects and in vitro functional characterization. Cancer Res 2006, 66:3434-3442.
  • [7]Wilson M, Koopman P: Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr Opin Genet Dev 2002, 12:441-446.
  • [8]Kamachi Y, Uchikawa M, Kondoh H: Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 2000, 16:182-187.
  • [9]Kondoh H, Kamachi Y: SOX–partner code for cell specification: regulatory target selection and underlying molecular mechanisms. Int J Biochem Cell Biol 2010, 42:391-399.
  • [10]Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I: Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 2011, 28:1241-1254.
  • [11]Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan BM: Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 2006, 8:150-173.
  • [12]Fortunato S, Adamski M, Bergum B, Guder C, Jordal S, Leininger S, Zwafink C, Rapp HT, Adamska M: Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns. Evol Dev 2012, 3:14.
  • [13]Jager M, Quéinnec E, Houliston E, Manuel M: Expansion of the SOX gene family predated the emergence of the Bilateria. Mol Phylogenet Evol 2006, 39:468-477.
  • [14]Jager M, Quéinnec E, Chiori R, Le Guyader H, Manuel M: Insights into the early evolution of SOX genes from expression analyses in a ctenophore. J Exp Zool 2008, 310B:650-667.
  • [15]Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Muller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW: Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond B Biol Sci 2009, 276:4261-4270.
  • [16]Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G: Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
  • [17]Ryan JF, Pang K, Schnitzler CE, Nguyen A-D, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD, NISC Comparative Sequencing Program: The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 2013, 342:1242592.
  • [18]Hernandez-Nicaise ML: Ctenophora. In Microscopic Anatomy of the Invertebrates Volume II: Placozoa, Porifera, Cnidaria and Ctenophora. Edited by Harrison W. New York: Wiley-Liss Inc; 1991:359-418.
  • [19]Tamm SL, Tamm S: Ciliary reversal without rotation of axonemal structures in ctenophore comb Plates. J Cell Biol 1981, 89:495-509.
  • [20]Horridge GA: Presumed photoreceptive cilia in a ctenophore. Q J Microsc Sci 1964, 105:311-317.
  • [21]Chun C: Die Ctenophoren des Golfo von Neapel und der angrenzenden Meeres-Abschnitte. In Flora und Fauna des Golfes von Neapel. Volume 1. Leipzig: Engelmann; 1880::1-311.
  • [22]Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan JF, Simmons D, Tada T, Park M, Gupta J, Brooks SY, Blakesley RW, Yokoyama S, Haddock SH, Martindale MQ, Baxevanis AD: Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol 2012, 10:107. BioMed Central Full Text
  • [23]Tamm SL: Ctenophora. In Electrical Conduction and Behaviour in Simple Invertebrates. Edited by Shelton G. Oxford: Clarendon Press; 1982.
  • [24]Jager M, Chiori R, Alié A, Dayraud C, Quéinnec E, Manuel M: New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Müller, 1776). J Exp Zool B Mol Dev Evol 2011, 316:171-187.
  • [25]Freeman G, Reynolds GT: The development of bioluminescence in the ctenophore Mnemiopsis leidyi. Dev Biol 1973, 31:61-100.
  • [26]Martindale M, Henry JQ: Ctenophorans, the Comb Jellies. In Embryology: Constructing the Organism. Edited by Gilbert SF, Raunio AM. Sunderland, MA: Sinauer; 1997:87-111.
  • [27]Martindale MQ, Henry JQ: Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages. Dev Biol 1999, 214:243-257.
  • [28]Reverberi G, Reverberi G: Ctenophores. In Experimental Embryology of Marine and Freshwater Invertebrates. Edited by Reverberi G. Amsterdam: North Holland Publishing Company; 1971:85-103.
  • [29]Pianka HD: Ctenophora. In Reproduction of Marine Invertebrates. Volume 1. Edited by Giese AC, Pearse JS. New York: Academic Press Inc; 1974::201-265.
  • [30]Martindale MQ: Larval reproduction in the ctenophore Mnemiopsis mccradyi (order Lobata). Mar Biol 1987, 94:409-414.
  • [31]Alié A, Leclère L, Jager M, Dayraud C, Chang P, Le Guyader H, Quéinnec E, Manuel M: Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev Biol 2011, 350:183-197.
  • [32]Hernandez-Nicaise ML, Franc JM: Embranchement des Cténaires. Morphologie, Biologie, Écologie. In Traité de Zoologie Anatomie, Systématique, Biologie Tome III, Fascicule 2 (Cnidaires, Cténaires). Edited by Grassé PP. Paris: Masson; 1993:943-1055.
  • [33]Magie CR, Pang K, Martindale MQ: Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 2005, 215:618-630.
  • [34]Shinzato C, Iguchi A, Hayward DC, Technau U, Ball EE, Miller DJ: Sox genes in the coral Acropora millepora: divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol Biol 2008, 8:311.
  • [35]Jager M, Quéinnec E, Le Guyader H, Manuel M: Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica. Evol Dev 2011, 2:12.
  • [36]King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing J, Bork P, Lim WA, Manning G, et al.: The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451:783-788.
  • [37]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
  • [38]Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
  • [39]Le SQ, Gascuel O: An improved general amino acid replacement matrix. Mol Biol Evol 2008, 25:1307-1320.
  • [40]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
  • [41]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
  • [42]Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL: AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 2008, 24:581-583.
  • [43]FigTree, a graphical viewer of phylogenetic trees http://tree.bio.ed.ac.uk/software/figtree/ webcite
  • [44]Pang K, Martindale MQ: Comb jellies (ctenophora): a model for basal metazoan evolution and development. Cold Spring Harb Protoc 2008, 2008:pdb.emo106.
  • [45]Smith SA, Dunn CW: Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 2008, 24:715-716.
  • [46]Pang K, Ryan JF, Baxevanis AD, Martindale MQ: Evolution of the TGF-β signaling pathway and its potential role in the Ctenophore. Mnemiopsis leidyi. PLoS One 2011, 6:e24152.
  • [47]Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Wörheide G, Manuel M: Phylogenomics revives traditional views on deep animal relationships. Curr Biol 2009, 19:706-712.
  • [48]Schierwater B, Eitel M, Jakob W, Osigus H-J, Hadrys H, Dellaporta SL, Kolokotronis S-O, Desalle R: Concatenated analysis sheds light on early metazoan evolution and fuels a modern “Urmetazoon” hypothesis. PLoS Biol 2009, 7:e20.
  • [49]Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Muller WEG, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G: Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 2013, 67:223-233.
  • [50]Martindale MQ: The ontogeny and maintenance of adult symmetry properties in the ctenophore, Mnemiopsis mccradyi. Dev Biol 1986, 118:556-576.
  • [51]Coonfield BR: Regeneration in Mnemiopsis leidyi, Agassiz. Biol Bull 1936, 71:421-428.
  • [52]Molofsky AV, Pardal R, Morrison SJ: Diverse mechanisms regulate stem cell self-renewal. Curr Opin Cell Biol 2004, 16:700-707.
  • [53]Sarkar A, Hochedlinger K: The Sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 2013, 12:15-30.
  • [54]Extavour CG, Akam M: Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 2003, 130:5869-5884.
  • [55]Baker LD, Reeve MR: Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Mar Biol 1974, 26:57-62.
  • [56]Pang K: Understanding early animal evolution: genomics and cell fate specification in the ctenophore, Mnemiopsis leidyi. Honolulu, HI: University of Hawai’i at Manoa; 2010.
  • [57]Phochanukul N, Russell S: No backbone but lots of Sox: invertebrate Sox genes. Int J Biochem Cell Biol 2010, 42:453-464.
  文献评价指标  
  下载次数:166次 浏览次数:62次