Gene expression study in the juvenile mouse testis: Identification of stage-specific molecular pathways during spermatogenesis

Mammalian Genome

Volumn 17, Issue 9, 2006, Pages 956-975

  Clemente, Emily J ^a   Furlong, Robert A ^a   Loveland, Kate L ^b   Affara, Nabeel A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL LINEAGE; CELL PROLIFERATION; CELL TYPE; CORRELATION ANALYSIS; DNA MICROARRAY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GERM CELL; IN SITU HYBRIDIZATION; JUVENILE; MALE; MOUSE; MOUSE MUTANT; NEWBORN; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATIC CELL; SPERMATOGENESIS; TESTIS; TESTIS CELL;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; MALE; MICE; MICE, INBRED C57BL; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

EID: 33748956663     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-006-0029-3     Document Type: Article

References (64)

1. Braun RE (1998) Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9, 483-489
2. Breckenridge DG, Nguyen M, Kuppig S, Reth M, Shore GC (2002) The procaspase-8 isoform, procaspase-8L, recruited to the BAP31 complex at the endoplasmic reticulum. Proc Natl Acad Sci USA 99, 4331-4336
3. Chau BN, Cheng EH, Kerr DA, Hardwick JM (2000) Aven, an novel inhibitor of capsase activation, binds Bcl-xL and Apaf-1. Mol Cell 6, 31-40
4. Chen G, Goeddel DV (2002) TNF-R1 signaling: a beautiful pathway. Science 296, 1634-1635
5. Chubb C (1989) Genetically defined mouse models of male infertility. J Androl 10, 77-88
6. Cohen PE, Pollard JW (2001) Regulation of meiotic recombination and prophase I progression in mammals. BioEssays 23, 996-1009
7. Colussi PA, Kumar S (1999) Targeted disruption of caspase genes in mice: What they tell us about the functions of individual caspases in apoptosis. Immunol Cell Biol 77, 58-63
8. Cooke HJ, Saunders PT (2002) Mouse models of male infertility. Nat Rev Genet 3, 790-801
9. Crepieux P, Marion S, Martinat N, Fafeur V, Vern Y, et al. (2001) The ERK-dependent signalling is stagespecifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 20, 4696-4709
10. D'Alessio A, Riccioli A, Lauretti P, Padula F, Muciaccia B, et al. (2001) Testicular FasL is expressed by sperm cells. Proc Natl Acad Sci USA 98, 3316-3321
11. De SK, Chen HL, Pace JL, Hunt JS, Terranova PF, et al. (1993) Expression of tumor necrosis factor-alpha in mouse spermatogenic cells. Endocrinology 133, 389-396
12. Duan H, Wang Y, Aviram M, Swaroop M, Loo JA, et al. (1999) SAG, a novel zinc RING finger protein that protects cells from apoptosis induced by redox agents. Mol Cell Biol 19, 3145-3155
13. Eddy EM (2002) Male Germ Cell Gene Expression. Recent Prog Horm Res 57, 103-128
14. Ellis PJI, Furlong RA, Wilson A, Morris S, Carter D, et al. (2004) Modulation of the mouse testis transcriptome during postnatal development and in selected models of male infertility. Mol Hum Reprod 10, 271-281
15. Ellis PJ, Clemente EJ, Ball P, Toure A, Ferguson L, et al. (2005) Deletions on mouse Yq lead to upregulation of multiple X- and Y-linked transcripts in spermatids. Hum Mol Genet 14, 2705-2715
16. Grana X, Garriga J, Mayol X (1998) Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth. Oncogene 17, 3365-3383
17. Griswold MD (1995) Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52, 211-216
18. Guo B, Godzik A, Reed JC (2001) Bcl-G, a Novel Proapoptotic member of the Bcl-2 family. J Biol Chem 276, 2780-2785
19. Handel M (1987) Genetic control of spermatogenesis in mice. Results Probl Cell Differ 15, 1-62
20. Hecht NB (1998) Molecular mechanisms of male germ cell differentiation. BioEssays 20, 555-561
21. Herrada G, Wolgemuth DJ (1997) The mouse transcription factor Stat4 is expressed in haploid male germ cells and is present in the perinuclear theca of spermatozoa. J Cell Sci 110, 1543-1553
22. Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9, 811-818
23. Holdcraft RW, Braun RE (2004) Hormonal regulation of spermatogenesis. Int J Androl 27, 335-342
24. Inohara N, Gourley TS, Carrio R, Muniz M, Merino J, et al. (1998) Diva, a Bcl-2 homologue that binds directly to Apaf-1 and induces BH3- independent cell death. J Biol Chem 273, 32479-32486
25. Jahnukainen K, Chrysis D, Hou M, Parvinen M, Eksborg S, et al. (2004) Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol Reprod 70, 290-296
26. Jain AK, Dubes RC (1988) Algorithms for Clustering Data (Englewood Cliffs, NJ: Prentice-Hall)
27. Khatri P, Draghici S, Ostermeier G, Krawetz S (2002) Profiling gene expression using onto-express. Genomics 79, 266-270
28. Klappacher G, Lunyak V, Sykes D, Sawka-Verhelle D, Sage J, et al. (2002) An induced Ets repressor complex regulates growth arrest during terminal macrophage differentiation. Cell 109, 169-180
29. Kleene KC (2003) Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet Genome Res 103, 217-224
30. Kleene KC (2005) Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. Dev Biol 277, 16-26
31. Knudson C, Tung K, Tourtellotte W, Brown G Korsmeyer S (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 6, 96-99
32. Krajewski S, Krajewska M, Shabaik A, Miyashita T, Wang HG, et al. (1994) Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am J Pathol 145, 1323-1336
33. Krajewski S, Krajewska M, Shabaik A, Wang HG, Irie S, et al. (1994) Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res 54, 5501-5507
34. Leo CP, Hsu SY, McGee EA, Salanova M, Hsueh AJ (1998) DEFT, a novel death effector domain-containing molecule predominantly expressed in testicular germ cells. Endocrinology 139, 4839-4848
35. Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412, 95-99
36. Los M, Van de Craen M, Penning LC, Schenk H, Westendorp M, et al. (1995) Requirement of an ICE/ CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 375, 81-83
37. Maratou K, Forster T, Costa Y, Taggart M, Speed RM, et al. (2004) Expression profiling of the developing testis in wild-type and Dazl knockout mice. Mol Reprod Dev 67, 26-54
38. Mauduit C, Besset V, Caussanel V, Benahmed M (1996) Tumor necrosis factor alpha receptor p55 is under hormonal (follicle-stimulating hormone) control in testicular Sertoli cells. Biochem Biophys Res Commun 224, 631-637
39. Mazeyrat S, Saut N, Grigoriev V, Mahadevaiah SK, Ojarikre OA, et al. (2001) A Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis. Nat Genet 29, 49-53
40. McCarrey JR, O'Brien DA, Skinner MK (1999) Construction and preliminary characterization of a series of mouse and rat testis cDNA library. J Androl 20, 635-639
41. McLaren A, Monk M (1981) X-chromosome activity in the germ cells of sex-reversed mouse embryos. J Reprod Fertil 63, 533-537
42. Meehan T, Schlatt S, O'Bryan MK, de Kretser DM, Loveland KL (2000) Regulation of germ cell and Sertoli cell development by activin, follistatin, and FSH. Dev Biol 220, 225-237
43. Nair R, Shaha C (2003) Diethylstilbestrol induces rat spermatogenic cell apoptosis in vivo through increased expression of spermatogenic cell Fas/FasL system. J Biol Chem 278, 6470-6481
44. Orth JM (1984) The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology 115, 1248-1255
45. Pawlowski WP, Cande WZ (2005) Coordinating the events of the meiotic prophase. Trends Cell Biol 15, 674-681
46. Poccia D (1986) Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. Int Rev Cytol 105, 1-65
47. Riccioli A, Starace D, D'Alessio A, Starace G, Padula F, et al. (2000) TNF-alpha and IFN-gamma regulate expression and function of the Fas system in the seminiferous epithelium. J Immunol 165, 743-749
48. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P (1997) An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16, 2262-2270
49. Russell LD, Chiarini-Garcia H, Korsmeyer SJ, Knudson CM (2002) Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 66, 950-958
50. Saunders PT (2003) Germ cell-somatic cell interactions during spermatogenesis. Reprod Suppl 61, 91-101
51. Schultz N, Hamra FK, Garbers DL (2003) A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 100, 12201-12206
52. Sha J, Zhou Z, Li J, Yin L, Yang H, et al. (2002) Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays. Mol Hum Reprod 8, 511-517
53. Shima JE, McLean DJ, McCarrey JR, Griswold MD (2004) The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 71, 319-330
54. Starace D, Riccioli A, D'Alessio A, Giampietri C, Petrungaro S, et al. (2004) Characterization of signaling pathways leading to Fas expression induced by TNF-alpha: pivotal role of NF-kappaB. FASEB J 19, 473-475
55. Sykacek P, Furlong RA, Micklem G (2005) A friendly statistics package for microarray analysis. Bioinformatics 21, 4069-4070
56. Taylor CA, Senchyna M, Flanagan J, Joyce EM, Cliche DO, et al. (2004) Role of eIF5A in TNF-α-mediated apoptosis of lamina cribrosa cells. Invest Ophthalmol Vis Sci 45, 3568-3576
57. Toure A, Clemente EJ, Ellis P, Mahadevaiah SK, Ojarikre OA, et al. (2005) Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol 6, R102
58. Varnum D (1983) Blind-sterile: a new mutation on chromosome 2 of the house mouse. J Hered 74, 206-207
59. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, et al. (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102, 43-53
60. Waldner H, Sobel RA, Howard E, Kuchroo VK (1997) Fas- and FasL-deficient mice are resistant to induction of autoimmune encephalomyelitis. J Immunol 159, 3100-3103
61. Ward-Bailey P, Johnson K, Handel M, Harris B, Davisson M (1996) A new mouse mutation causing male sterility and histoincompatibility. Mamm Genome 7, 793-797
62. Wrobel G, Primig M (2005) Mammalian male germ cells are fertile ground for expression profiling of sexual reproduction. Reproduction 129, 1-7
63. Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D (1997) Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89, 357-364
64. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, et al. (1999) Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13, 1924-1935