Disruption of genital ridge development causes aberrant primordial germ cell proliferation but does not affect their directional migration

BMC Biology

Volumn 11, Issue , 2013, Pages

  Chen, Su Ren ^a,b   Zheng, Qiao Song ^a   Zhang, Yang ^a   Gao, Fei ^a   Liu, Yi Xun ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Genital ridge; Migration, Proliferation; Primordial germ cells

Indexed keywords

ANIMALIA;

BETA1 INTEGRIN; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; WT1 PROTEIN;

ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL COMMUNICATION; CELL COUNT; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; EPITHELIUM; FEMALE; GENETICS; GERM CELL; GONAD; MALE; METABOLISM; MITOSIS; MOUSE; MUTATION; PRENATAL DEVELOPMENT; SEX DETERMINATION PROCESS;

ANIMALS; ANTIGENS, CD29; CELL COMMUNICATION; CELL COUNT; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; EMBRYO, MAMMALIAN; EPITHELIUM; FEMALE; GERM CELLS; GONADS; MALE; MICE; MITOSIS; MUTATION; SEX DETERMINATION PROCESSES; STEM CELL FACTOR; WT1 PROTEINS;

EID: 84874505358     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-22     Document Type: Article

References (52)

1. Saga Y. Mouse germ cell development during embryogenesis. Curr Opin Genet Dev 2008, 18:337-341. 10.1016/j.gde.2008.06.003, 18625315.
2. Starz-Gaiano M, Lehmann R. Moving towards the next generation. Mech Dev 2001, 105:5-18. 10.1016/S0925-4773(01)00392-6, 11429277.
3. Santos AC, Lehmann R. Germ cell specification and migration in Drosophila and beyond. Curr Biol 2004, 14:R578-589. 10.1016/j.cub.2004.07.018, 15268881.
4. Anderson R, Copeland TK, Scholer H, Heasman J, Wylie C. The onset of germ cell migration in the mouse embryo. Mech Dev 2000, 91:61-68. 10.1016/S0925-4773(99)00271-3, 10704831.
5. Molyneaux KA, Stallock J, Schaible K, Wylie C. Time-lapse analysis of living mouse germ cell migration. Dev Biol 2001, 240:488-498. 10.1006/dbio.2001.0436, 11784078.
6. Molyneaux K, Wylie C. Primordial germ cell migration. Int J Dev Biol 2004, 48:537-544. 10.1387/ijdb.041833km, 15349828.
7. Raz E. Guidance of primordial germ cell migration. Curr Opin Cell Biol 2004, 16:169-173. 10.1016/j.ceb.2004.01.004, 15196560.
8. Richardson BE, Lehmann R. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 2010, 11:37-49. 10.1038/nrm2815, 20027186.
9. Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci USA 2003, 100:5319-5323. 10.1073/pnas.0730719100, 154343, 12684531.
10. Bacon K, Baggiolini M, Broxmeyer H, Horuk R, Lindley I, Mantovani A, Matsushima K, Murphy P, Nomiyama N, Oppenheim J, Rot A, Schall T, Tsang M, Thorpe R, Van Damme J, Wadhwa M, Yoshie O, Zlotnik A, Zoon K. Chemokine/chemokine receptor nomenclature. Cytokine 2003, 21:48-49.
11. Molyneaux KA, Zinszner H, Kunwar PS, Schaible K, Stebler J, Sunshine MJ, O'Brien W, Raz E, Littman D, Wylie C, Lehmann R. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 2003, 130:4279-4286. 10.1242/dev.00640, 12900445.
12. Matsui Y, Zsebo KM, Hogan BL. Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature 1990, 347:667-669. 10.1038/347667a0, 1699134.
13. Bendel-Stenzel MR, Gomperts M, Anderson R, Heasman J, Wylie C. The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 2000, 91:143-152. 10.1016/S0925-4773(99)00287-7, 10704839.
14. Di Carlo A, De Felici M. A role for E-cadherin in mouse primordial germ cell development. Dev Biol 2000, 226:209-219. 10.1006/dbio.2000.9861, 11023681.
15. Anderson R, Fassler R, Georges-Labouesse E, Hynes RO, Bader BL, Kreidberg JA, Schaible K, Heasman J, Wylie C. Mouse primordial germ cells lacking beta 1 integrins enter the germline but fail to migrate normally to the gonads. Development 1999, 126:1655-1664.
16. Donovan PJ, Stott D, Cairns LA, Heasman J, Wylie CC. Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 1986, 44:831-838. 10.1016/0092-8674(86)90005-X, 3955652.
17. Enders GC, May JJ. Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev Biol 1994, 163:331-340. 10.1006/dbio.1994.1152, 8200475.
18. Dudley B, Palumbo C, Nalepka J, Molyneaux K. BMP signaling controls formation of a primordial germ cell niche within the early genital ridges. Dev Biol 2010, 343:84-93. 10.1016/j.ydbio.2010.04.011, 2885459, 20417197.
19. Farini D, Scaldaferri ML, Iona S, La Sala G, De Felici M. Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev Biol 2005, 285:49-56. 10.1016/j.ydbio.2005.06.036, 16139834.
20. Menke DB, Koubova J, Page DC. Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol 2003, 262:303-312. 10.1016/S0012-1606(03)00391-9, 14550793.
21. Suzuki A, Saga Y. Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev 2008, 22:430-435. 10.1101/gad.1612708, 2238665, 18281459.
22. Agoulnik AI, Lu BS, Zhu QC, Truong C, Ty MT, Arango N, Chada KK, Bishop CE. A novel gene, Pog, is necessary for primordial germ cell proliferation in the mouse and underlies the germ cell deficient mutation, gcd. Hum Mol Genet 2002, 11:3047-3053. 10.1093/hmg/11.24.3047, 12417526.
23. Atchison FW, Capel B, Means AR. Pin1 regulates the timing of mammalian primordial germ cell proliferation. Development 2003, 130:3579-3586. 10.1242/dev.00584, 12810604.
24. Beck AR, Miller IJ, Anderson P, Streuli M. RNA-binding protein TIAR is essential for primordial germ cell development. Proc Natl Acad Sci USA 1998, 95:2331-2336. 10.1073/pnas.95.5.2331, 19335, 9482885.
25. Kim B, Kim Y, Sakuma R, Hui C-C, Ruether U, Jorgensen JS. Primordial germ cell proliferation is impaired in Fused Toes mutant embryos. Dev Biol 2011, 349:417-426. 10.1016/j.ydbio.2010.10.010, 20969841.
26. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 2000, 14:841-853. 316497, 10766740.
27. McLaren A. Germline and soma: Interactions during early mouse development. Sem Dev Biol 1994, 5:43-49.
28. Armstrong JF, Pritchard-Jones K, Bickmore WA, Hastie ND, Bard JB. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech Dev 1993, 40:85-97. 10.1016/0925-4773(93)90090-K, 8382938.
29. Pelletier J, Schalling M, Buckler AJ, Rogers A, Haber DA, Housman D. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev 1991, 5:1345-1356. 10.1101/gad.5.8.1345, 1651275.
30. Rackley RR, Flenniken AM, Kuriyan NP, Kessler PM, Stoler MH, Williams BR. Expression of the Wilms' tumor suppressor gene WT1 during mouse embryogenesis. Cell Growth Differ 1993, 4:1023-1031.
31. Englert C, Maheswaran S, Garvin AJ, Kreidberg J, Haber DA. Induction of p21 by the Wilms' tumor suppressor gene WT1. Cancer Res 1997, 57:1429-1434.
32. Loeb DM, Korz D, Katsnelson M, Burwell EA, Friedman AD, Sukumar S. Cyclin E is a target of WT1 transcriptional repression. J Biol Chem 2002, 277:19627-19632. 10.1074/jbc.M201336200, 11919196.
33. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. WT-1 is required for early kidney development. Cell 1993, 74:679-691. 10.1016/0092-8674(93)90515-R, 8395349.
34. Gao F, Maiti S, Sun G, Ordonez NG, Udtha M, Deng JM, Behringer RR, Huff V. The Wt1+/R394W mouse displays glomerulosclerosis and early-onset renal failure characteristic of human Denys-Drash syndrome. Mol Cell Biol 2004, 24:9899-9910. 10.1128/MCB.24.22.9899-9910.2004, 525476, 15509792.
35. Godin I, Wylie C, Heasman J. Genital ridges exert long-range effects on mouse primordial germ cell numbers and direction of migration in culture. Development 1990, 108:357-363.
36. Koff A, Giordano A, Desai D, Yamashita K, Harper JW, Elledge S, Nishimoto T, Morgan DO, Franza BR, Roberts JM. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 1992, 257:1689-1694. 10.1126/science.1388288, 1388288.
37. Hossain A, Saunders GF. Role of Wilms tumor 1 (WT1) in the transcriptional regulation of the Mullerian-inhibiting substance promoter. Biol Reprod 2003, 69:1808-1814. 10.1095/biolreprod.103.015826, 12855602.
38. Chen SR, Chen M, Wang XN, Zhang J, Wen Q, Ji SY, Zheng QS, Gao F, Liu YX. The Wilms tumor gene, Wt1, maintains testicular cord integrity by regulating the expression of Col4a1 and Col4a2. Biol Reprod 2013,
39. Runyan C, Schaible K, Molyneaux K, Wang Z, Levin L, Wylie C. Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development 2006, 133:4861-4869. 10.1242/dev.02688, 17107997.
40. Ross A, Munger S, Capel B. Bmp7 regulates germ cell proliferation in mouse fetal gonads. Sex Dev 2007, 1:127-137. 10.1159/000100034, 18391523.
41. Richards AJ, Enders GC, Resnick JL. Activin and TGFbeta limit murine primordial germ cell proliferation. Dev Biol 1999, 207:470-475. 10.1006/dbio.1998.9174, 10068477.
42. Chuva de Sousa LSM, van den Driesche S, Carvalho RL, Larsson J, Eggen B, Surani MA, Mummery CL. Altered primordial germ cell migration in the absence of transforming growth factor beta signaling via ALK5. Dev Biol 2005, 284:194-203. 10.1016/j.ydbio.2005.05.019, 15993878.
43. Hartwig S, Ho J, Pandey P, Macisaac K, Taglienti M, Xiang M, Alterovitz G, Ramoni M, Fraenkel E, Kreidberg JA. Genomic characterization of Wilms' tumor suppressor 1 targets in nephron progenitor cells during kidney development. Development 2010, 137:1189-1203. 10.1242/dev.045732, 2835332, 20215353.
44. Zamboni L, Upadhyay S. Germ-cell differentiation in mouse adrenal-glands. J Exp Zool 1983, 228:173-193. 10.1002/jez.1402280204, 6663256.
45. Pesce M, Farrace MG, Piacentini M, Dolci S, Defelici M. Stem-cell factor and leukemia inhibitory factor promote primordial germ-cell survival by suppressing programmed cell-death (apoptosis). Development 1993, 118:1089-1094.
46. Stallock J, Molyneaux K, Schaible K, Knudson CM, Wylie C. The pro-apoptotic gene Bax is required for the death of ectopic primordial germ cells during their migration in the mouse embryo. Development 2003, 130:6589-6597. 10.1242/dev.00898, 14660547.
47. De Felici M, Scaldaferri ML, Lobascio M, Iona S, Nazzicone V, Klinger FG, Farini D. Experimental approaches to the study of primordial germ cell lineage and proliferation. Hum Reprod Update 2004, 10:197-206. 10.1093/humupd/dmh020, 15140867.
48. Mintz B, Russell ES. Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool 1957, 134:207-237. 10.1002/jez.1401340202, 13428952.
49. Tam PP, Snow MH. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol 1981, 64:133-147.
50. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121. 10.1038/351117a0, 2030730.
51. Schmahl J, Eicher EM, Washburn LL, Capel B. Sry induces cell proliferation in the mouse gonad. Development 2000, 127:65-73.
52. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 2009, 327:301-312. 10.1016/j.ydbio.2008.12.011, 19124014.