Null mutation of the transcription factor inhibitor of DNA binding 3 (Id3) in male mice adversely impacts on fertility and reproductive outcome

Journal of Andrology

Volumn 33, Issue 4, 2012, Pages 667-674

  Carroll, Michelle ^a   Robaire, Bernard ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Infertility; Reproductive genetics; Spermatogenesis

Indexed keywords

INHIBITOR OF DIFFERENTIATION 3;

ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; CONGENITAL MALFORMATION; CONTROLLED STUDY; FEMALE; FETUS; FETUS DEATH; GENE EXPRESSION; GENE MUTATION; GENOTYPE; MALE; MALE FERTILITY; MOUSE; NONHUMAN; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; PROGENY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEMALE; FERTILITY; FETAL DEVELOPMENT; INHIBITOR OF DIFFERENTIATION PROTEINS; MALE; MICE; MICE, INBRED C57BL; MUTATION; PREGNANCY; PREGNANCY OUTCOME; REPRODUCTION;

EID: 84866381174     PISSN: 01963635     EISSN: 19394640     Source Type: Journal    
DOI: 10.2164/jandrol.111.014522     Document Type: Article

References (41)

1. Alani RM, Young AZ, Shifflett CB. Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc Natl Acad Sci U S A. 2001;98:7812-7816.
2. Aldinger KA, Sokoloff G, Rosenberg DM, Palmer AA, Millen KJ. Genetic variation and population substructure in outbred CD-1 mice: implications for genome-wide association studies. PLoS One. 2009;4:e4729.
3. Bai G, Sheng N, Xie Z, Bian W, Yokota Y, Benezra R, Kageyama R, Guillemot F, Jing N. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev Cell. 2007;13:283-297.
4. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990;61:49-59.
5. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD. Genetically haploid spermatids are phenotypically diploid. Nature. 1989;337:373-376.
6. Burgos MH, Fawcett DW. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol. 1955;1(4):287-300.
7. Carroll M, Hamzeh M, Robaire B. Expression, localization, and regulation of inhibitor of DNA binding (Id) proteins in the rat epididymis. J Androl. 2006;27:212-224.
8. Carroll M, Luu T, Robaire B. Null mutation of the transcription factor inhibitor of DNA binding 3 (Id3) affects spermatozoal motility parameters and epididymal gene expression in mice. Biol Reprod. 2011;84:765-774.
9. Chambers I. The molecular basis of pluripotency in mouse embryonic stem cells. Cloning Stem Cells. 2004;6:386-391.
10. Chaudhary J, Johnson J, Kim G, Skinner MK. Hormonal regulation and differential actions of the helix-loop-helix transcriptional inhibitors of differentiation (Id1, Id2, Id3, and Id4) in Sertoli cells. Endocrinology. 2001;142:1727-1736.
11. Chen H, Weng YC, Schatteman GC, Sanders L, Christy RJ, Christy BA. Expression of the dominant-negative regulator Id4 is induced during adipocyte differentiation. Biochem Biophys Res Commun. 1999;256:614-619.
12. Cooper CL, Newburger PE. Differential expression of Id genes in multipotent myeloid progenitor cells: Id-1 is induced by early- and late-acting cytokines while Id-2 is selectively induced by cytokines that drive terminal granulocytic differentiation. J Cell Biochem. 1998;71:277-285.
13. Duncan M, DiCicco-Bloom EM, Xiang X, Benezra R, Chada K. The gene for the helix-loop-helix protein, Id, is specifically expressed in neural precursors. Dev Biol. 1992;154:1-10.
14. Ellmeier W, Weith A. Expression of the helix-loop-helix gene Id3 during murine embryonic development. Dev Dyn. 1995;203:163-173.
15. Fawcett DW. Ultrastructure and function of the Sertoli cell. In: Hamilton DW, Greep RO, eds. Handbook of Physiology. Washington, DC: American Physiological Society; 1975:21-25.
16. Fraidenraich D, Stillwell E, Romero E, Wilkes D, Manova K, Basson CT, Benezra R. Rescue of cardiac defects in id knockout embryos by injection of embryonic stem cells. Science. 2004;306:247-252.
17. Hogg RN. Modified Giemsa stain technique for sections. In: Gurr E, ed. Biological Staining Methods. 8th ed. Buckinghamshire, United Kingdom: Searle Diagnostic Gurr Products; 1973:34.
18. Jankovic V, Ciarrocchi A, Boccuni P, DeBlasio T, Benezra R, Nimer SD. Id1 restrains myeloid commitment, maintaining the selfrenewal capacity of hematopoietic stem cells. Proc Natl Acad Sci U S A. 2007;104:1260-1265.
19. Jen Y, Manova K, Benezra R. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn. 1996;207:235-252.
20. Jen Y, Weintraub H, Benezra R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev. 1992;6:1466-1479.
21. Johnston DS, Wright WW, Dicandeloro P, Wilson E, Kopf GS, Jelinsky SA. Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells. Proc Natl Acad Sci U S A. 2008;105:8315-8320.
22. Kadesch T. Consequences of heteromeric interactions among helixloop-helix proteins. Cell Growth Differ. 1993;4:49-55.
23. Kreider BL, Benezra R, Rovera G, Kadesch T. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science. 1992;255:1700-1702.
24. Lee JE. Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol. 1997;7:13-20.
25. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature. 1999;401:670-677.
26. Massari ME, Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol. 2000;20: 429-440.
27. Norton JD, Deed RW, Craggs G, Sablitzky F. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 1998;8:58-65.
28. Oatley MJ, Kaucher AV, Racicot KE, Oatley JM. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod. 2011;85:347-356.
29. Olson EN, Klein WH. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 1994;8:1-8.
30. Pan L, Sato S, Frederick JP, Sun XH, Zhuang Y. Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol Cell Biol. 1999;19:5969-5980.
31. Paul C, Nagano M, Robaire B. Aging results in differential regulation of DNA repair pathways in pachytene spermatocytes in the brown Norway rat. Biol Reprod. 2011;85:1269-1278.
32. Rivera RR, Johns CP, Quan J, Johnson RS, Murre C. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity. 2000;12:17-26.
33. Ruzinova MB, Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 2003;13:410-418.
34. Sablitzky F, Moore A, Bromley M, Deed RW, Newton JS, Norton JD. Stage- and subcellular-specific expression of Id proteins in male germ and Sertoli cells implicates distinctive regulatory roles for Id proteins during meiosis, spermatogenesis, and Sertoli cell function. Cell Growth Differ. 1998;9:1015-1024.
35. Segretain D. Endocytosis in spermatids during spermiogenesis of the mouse. Biol Cell. 1989;67:289-298.
36. Segretain D. Endocytic activity of male germ cells during puberty. Biol Cell. 1993;78:199-205.
37. Segretain D, Egloff M, Gesṕrard N, Pineau C, Jesṕgou B. Receptormediated and absorptive endocytosis by male germ cells of different mammalian species. Cell Tissue Res. 1992;268:471-478.
38. Sun XH, Copeland NG, Jenkins NA, Baltimore D. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol. 1991;11:5603-5611.
39. Whitaker J, Dix KM. Double staining technique for rat foetus skeletons in teratological studies. Lab Anim. 1979;13:309-310.
40. Ying QL, Nichols J, Chambers I, Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell. 2003;115:281-292.
41. Yokota Y. Id and development. Oncogene. 2001;20:8290-8298.