Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica

EvoDevo

Volumn 2, Issue 1, 2011, Pages

  Jager, Muriel ^a   Quéinnec, Eric ^a   Le Guyader, Hervé ^a   Manuel, Michaël ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BILATERIA; CLYTIA; CLYTIA HEMISPHAERICA; CNIDARIA; CTENOPHORA (COELENTERATES); HYDROZOA;

EID: 84879155321     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-2-12     Document Type: Article

References (57)

1. Kiefer JC. Back to basics: Sox genes. Dev Dyn 2007, 236:2356-2366. 10.1002/dvdy.21218, 17584862.
2. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentitation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell B 2007, 39:2195-2214.
3. Chew LJ, Gallo V. The Yin and Yang of Sox proteins: activation and repression in development and disease. J Neurosci Res 2009, 87:3277-3287. 10.1002/jnr.22128, 2767240, 19437544.
4. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, DeBiasi S, Nicolis SK. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 2004, 131:3805-3819. 10.1242/dev.01204, 15240551.
5. 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. 10.1016/S0959-437X(02)00323-4, 12100890.
6. 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. 10.1016/j.biocel.2009.09.003, 19747562.
7. 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. 10.1006/dbio.2000.9883, 11071752.
8. 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. 10.1007/s00427-005-0022-y, 16193320.
9. Jager M, Queinnec E, Houliston E, Manuel M. Expansion of the SOX gene family predated the emergence of the Bilateria. Mol Phylogenet Evol 2006, 39:468-477. 10.1016/j.ympev.2005.12.005, 16439161.
10. Jager M, Queinnec 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 B Mol Dev Evol 2008, 310:650-667.
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. 10.1111/j.1525-142X.2006.00086.x, 16509894.
12. Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM. Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 2008, 25:980-996. 10.1093/molbev/msn047, 18296413.
13. Pevny L, Placzek M. Sox genes and neural progenitor identity. Curr Opin Neurobiol 2005, 15:7-13. 10.1016/j.conb.2005.01.016, 15721738.
14. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci 2005, 28:583-588. 10.1016/j.tins.2005.08.008, 16139372.
15. Graham V, Khudyakov J, Ellis P, Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39:749-765. 10.1016/S0896-6273(03)00497-5, 12948443.
16. Guth SI, Wegner M. Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 2008, 65:3000-3018. 10.1007/s00018-008-8138-7, 18516494.
17. Pevny LH, Nicolis SK. Sox2 roles in neural stem cells. Int J Biochem Cell Biol 2010, 42:421-424. 10.1016/j.biocel.2009.08.018, 19733254.
18. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676. 10.1016/j.cell.2006.07.024, 16904174.
19. Kerner P, Simionato E, Le Gouar M, Vervoort M. Orthologs of key vertebrate neural genes are expressed during neurogenesis in the annelid Platynereis dumerilii. Evol Dev 2009, 11:513-524. 10.1111/j.1525-142X.2009.00359.x, 19754708.
20. Phochanukul N, Russell S. No backbone but lots of SOX: the invertebrate SOX family. Int J Biochem Cell Biol 2009, 42:453-464.
21. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, 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. 10.1038/nature06614, 18322464.
22. 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. 10.1016/j.cub.2009.02.052, 19345102.
23. Schierwater B, Eitel M, Jakob W, Osigus H, Hadrys H, Dellaporta SL, Kolokotronis S, Desalle. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis. PLoS Biol 2009, 7:e1000020.
24. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alié A, Morgenstern B, Manuel M, Wörheide G. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 2010, 27:1983-1987. 10.1093/molbev/msq089, 2922619, 20378579.
25. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 2011, 9:e1000602. 10.1371/journal.pbio.1000602, 3057953, 21423652.
26. 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. 10.1186/1471-2148-8-311, 2613919, 19014479.
27. 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. 10.1016/j.ydbio.2010.10.019, 21036163.
28. Houliston E, Momose T, Manuel M. Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet 2010, 26:159-167. 10.1016/j.tig.2010.01.008, 20227783.
29. Bodo F, Bouillon J. Etude histologique du développement embryonnaire de quelques Hydroméduses de Roscoff. Cah Biol Mar 1968, 9:69-79.
30. Bode HR, David CN. Regulation of a multipotent stem cell, the interstitial cell of Hydra. Prog Biophys Mol Biol 1978, 33:189-206.
31. Bode HR, Heimfeld S, Chow MA, Huang LW. Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 1987, 122:577-585. 10.1016/0012-1606(87)90321-6, 3596022.
32. Bode HR, Gee LW, Chow MA. Neuron differentiation in hydra involves dividing intermediates. Dev Biol 1990, 139:231-243. 10.1016/0012-1606(90)90292-Q, 2338167.
33. Bode HR. The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. J Cell Sci 1996, 109:1155-1164.
34. Bouillon J. Classe des Hydrozoaires. Traité de Zoologie, Cnidaires, Ctenaires, 3(3) 1994, 29-416. Masson, Paris, Grassé P-P.
35. Denker E, Manuel M, Leclère L, Le Guyader H, Rabet N. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev Biol 2008, 315:99-113. 10.1016/j.ydbio.2007.12.023, 18234172.
36. Galliot B, Quiquand M, Ghila L, de Rosa R, Miljkovic-Licina M, Chera S. Origins of neurogenesis, a cnidarian view. Dev Biol 2009, 332:2-24. 10.1016/j.ydbio.2009.05.563, 19465018.
37. Thurm U, Brinkmann M, Golz R, Holtmann M, Oliver D, Sieger T. Mechanoreception and synaptic transmission of hydrozoan nematocytes. Hydrobiologia 2004, (530-531):97-105.
38. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL. Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 2003, 23:8084-8091. 10.1128/MCB.23.22.8084-8091.2003, 262333, 14585968.
39. Osaki E, Nishina Y, Inazawa J, Copeland NG, Gilbert DJ, Jenkins NA, Ohsugi M, Tezuka T, Yoshida M, Semba K. Identification of a novel Sry-related gene and its germ cell-specific expression. Nucleic Acids Res 1999, 27:2503-2510. 10.1093/nar/27.12.2503, 148454, 10359848.
40. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus-oocyte complex gene-expression profile. Human Reprod 2006, 21:1705-1719.
41. Mukherjee A, Melnattur KV, Zhang M, Nambu JR. Maternal expression and function of the Drosophila sox gene Dichaete during oogenesis. Dev Dyn 2006, 235:2828-2835. 10.1002/dvdy.20904, 16894603.
42. Wilson MJ, Dearden PK. Evolution of the insect Sox genes. BMC Evol Biol 2008, 8:120. 10.1186/1471-2148-8-120, 2386450, 18439299.
43. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, Kurohmaru M, Sanai Y, Yonekawa H, Yazaki K, Tam PP, Hayashi Y. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 2002, 129:2367-2379.
44. Leclère L. Evolution de la reproduction sexuée des hydrozoaires: aspects historiques, analyse phylogénétique et développementale. 2008, Thèse de l'Université Pierre Marie Curie, Paris.
45. Extavour CG, Akam M. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 2003, 130:5869-5884. 10.1242/dev.00804, 14597570.
46. Extavour CGM. Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol 2007, 47:770-785.
47. Travis JA. Close look at urbisexuality. Science 2007, 316:391-391.
48. Francois M, Koopman P, Beltrame M. SoxF genes: key players in the development of the cardio-vascular system. Int J Biochem Cell Biol 2010, 42:445-448. 10.1016/j.biocel.2009.08.017, 19733255.
49. Chapman J, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, et al. The dynamic genome of Hydra. Nature 2010, 464:592-596. 10.1038/nature08830, 20228792.
50. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 2004, 5:113.
51. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95.
52. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Syst Biol 2003, (52):696-704.
53. Swofford DL. PAUP 4.0: Phylogenetic Analysis Using Parsimony (And Other Methods) 1999, Sunderland, MA, Sinauer Associates, Inc..
54. Ronquist F, Huelsenbeck JP, van der Mark P. MrBayes 3.1. 2005, , http://mrbayes.csit.fsu.edu/index.php
55. Chevalier S, Martin A, Leclère L, Amiel A, Houliston E. Polarised expression of FoxB and FoxQ2 genes during development of the hydrozoan Clytia hemisphaerica. Dev Genes Evol 2006, 216:709-720. 10.1007/s00427-006-0103-6, 17021866.
56. Chiori R, Jager M, Denker E, Wincker P, Da Silva C, Le Guyader H, Manuel M, Queinnec E. Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS One 2009, 4:e4231. 10.1371/journal.pone.0004231, 2626245, 19156208.
57. Ohba H, Chiyoda T, Endo E, Yano M, Hayakawa Y, Sakaguchi M, Darnell RB, Okano HJ, Okano H. Sox21 is a repressor of neuronal differentiation and is antagonized by YB-1. Neurosci Lett 2004, 358:157-160. 10.1016/j.neulet.2004.01.026, 15039105.