The power of mouse genetics to study spermatogenesis

Journal of Andrology

Volumn 31, Issue 1, 2010, Pages 34-44

  Yatsenko, A N ^a   Iwamori, N ^a   Iwamori, T ^a   Matzuk, M M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Human male infertility; Mouse model; Reproduction

Indexed keywords

ACTIVIN RECEPTOR 2; ADENOSINE TRIPHOSPHATE; BONE MORPHOGENETIC PROTEIN 15; COLONY STIMULATING FACTOR 1; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN A1; DNA BINDING PROTEIN; FOLLISTATIN; FOLLITROPIN BETA SUBUNIT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH DIFFERENTIATION FACTOR 9; HORMONE RECEPTOR; INHIBIN A; KELCH LIKE 10; MESSENGER RNA; NUCLEOPLASMIN 2; OXYTOCIN; OXYTOCIN RECEPTOR; PROTEIN; PROTEIN GASZ; PROTEIN NOBOX; RNA BINDING PROTEIN; SMAD5 PROTEIN; TEKTIN 3; TEKTIN 4; UNCLASSIFIED DRUG; UNINDEXED DRUG; Y BOX PROTEIN; ZONA PELLUCIDA BINDING PROTEIN 1; ZONA PELLUCIDA BINDING PROTEIN 2; ZYGOTE ARREST PROTEIN;

ASTHENOSPERMIA; CONFERENCE PAPER; CONTRACEPTION; FERTILIZATION; FLAGELLUM; GENE DELETION; GENE FUNCTION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MALE; MALE FERTILITY; MALE INFERTILITY; MEIOSIS; MITOSIS; MOLECULAR EVOLUTION; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON MOTILITY; STEM CELL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; ZONA PELLUCIDA;

ANIMALS; HUMANS; INFERTILITY, MALE; MALE; MICE; SPERMATOGENESIS; SPERMATOZOA; TRANSCRIPTION FACTORS;

EID: 77749246487     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.109.008227     Document Type: Conference Paper

References (84)

1. Ballow D, Meistrich ML, Matzuk M, Rajkovic A. Sohlh1 is essential for spermatogonial differentiation. Dev Biol. 2006a;294(1):161-167.
2. Ballow DJ, Xin Y, Choi Y, Pangas SA, Rajkovic A. Sohlh2 is a germ cell-specific bHLH transcription factor. Gene Expr Patterns. 2006b;6(8):1014-1018.
3. Barna M, Merghoub T, Costoya JA, Ruggero D, Branford M, Bergia A, Samori B, Pandolfi PP. Plzf mediates transcriptional repression of HoxD gene expression through chromatin remodeling. Dev Cell. 2002;3(4):499-510.
4. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD. Genetically haploid spermatids arc phenotypically diploid. Nature. 1989;337(6205):373-376.
5. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet. 2004;36(6):647-652.
6. Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, Frail DE, Eppig JJ, Matzuk MM. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science. 2003;300(5619):633-636.
7. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113(5):643-655.
8. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. Nanog safeguards pluripotency and mediates germline development. Nature. 2007;450(7173):1230-1234.
9. Chang H, Matzuk MM. Smad5 is required for mouse primordial germ cell development. Mech Dev. 2001;104(1-2):61-67.
10. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, Aicher W, Bühring HJ, Mattheus U, Mack A, Wagner HJ, Minger S, Matzkies M, Reppel M, Hescheler J, Sievert KD, Stenzl A, Skutella T. Generation of pluripotent stem cells from adult human testis. Nature. 2008;456(7220):344-349.
11. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet. 2004;36(6):653-659.
12. Dam AH, Koscinski I, Kremer JA, Moutou C, Jaeger AS, Oudakker AR, Tournaye H, Charlet N, Lagier-Tourenne C, van Bokhoven H, Viville S. Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. Am J Hum Genet. 2007;81:813-820.
13. Dann CT, Alvarado AL, Molyneux LA, Denard BS, Garbers DL, Porteus MH. Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem Cells. 2008;26(11):2928-2937.
14. Dieterich K, Soto Rifo R, Faure AK, Hennebicq S, Ben Amar B, Zahi M, Perrin J, Martinez D, Sele B, Jouk PS, others. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet. 2007;39(5):661-665.
15. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383:531-535.
16. Dym M, Fawcett DW. Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol Reprod. 1971;4(2):195-215.
17. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. Molecular characterization of the follicle defects in the growth differentiation factor-9-deficient ovary. Mol Endocrinol. 1999;13:1018-1034.
18. Falender AE, Freiman RN, Geles KG, Lo KC, Hwang K, Lamb DJ, Morris PL, Tjian R, Richards JS. Maintenance of spermatogenesis requires TAF4b, a gonad-specific subunit of TFIID. Genes Dev. 2005;19(7):794-803.
19. Fawcett DW, Ito S, Slautterback D. The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. J Biophys Biochem Cytol. 1959;5(3):453-460.
20. Freiman RN, Albright SR, Zheng S, Sha WC, Hammer RE, Tjian R. Requirement of tissue-selective TBP-associated factor TAFII105 in ovarian development. Science. 2001;293(5537):2084-2087.
21. Greenbaum MP, Ma L, Matzuk MM. Conversion of midbodies into germ cell intercellular bridges. Dev Biol. 2007;305:389-396.
22. Greenbaum MP, Yan W, Wu MH, Lin YN, Agno JE, Sharma M, Braun RE, Rajkovic A, Matzuk MM. TEX14 is essential for intercellular bridges and fertility in male mice. Proc Natl Acad Sci U S A. 2006;103(13):4982-4987.
23. Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W, Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature. 2006;440(7088):1199-1203.
24. Hao J, Yamamoto M, Richardson TE, Chapman KM, Denard BS, Hammer RE, Zhao GQ, Hamra FK. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells. 2008;26(6):1587-1597.
25. Ho YS, Gargano M, Cao J, Bronson RT, Heimler I, Hutz RJ. Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J Biol Chem. 1998;273(13):7765-7769.
26. Huckins C. Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am J Anat. 1978;153(1):97-121.
27. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, Louis JC, Hu S, Altrock BW, Fox GM. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell. 1996;85(7):1113-1124.
28. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S, Toyoshima M, Niwa O, Oshimura M, Heike T, Nakahata T, Ishino F, Ogura A, Shinohara T. Generation of pluripotent stem cells from neonatal mouse testis. Cell. 2004;119(7):1001-1012.
29. Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A, Shinohara T. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod. 2005;72(4):985-991.
30. Krawetz SA. Paternal contribution: new insights and future challenges. Nat Rev Genet. 2005;6(8):633-642.
31. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 2004;101(47):16489-16494.
32. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet. 1997;15:201-204.
33. Lin YN, Roy A, Yan W, Burns KH, Matzuk MM. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol. 2007;27(19):6794-6805.
34. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ. Cyclin A1 is required for meiosis in the male mouse. Nat Genet. 1998;20(4):377-388.
35. Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, Zhu H, Han DY, Harris RA, Coarfa C, Gunaratne PH, Yan W, Matzuk MM. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet. 2009;5(9):e1000635.
36. Ma X, Dong Y, Matzuk MM, Kumar TR. Targeted disruption of luteinizing hormone b subunit leads to hypogonadism, defects in gonadal steroidogenesis and infertility. Proc Natl Acad Sci U S A. 2004;101(49):17294-17299.
37. Ma X, Reyna A, Mani SK, Matzuk MM, Kumar TR. Impaired male sexual behavior in activin receptor type II knockout mice. Biol Reprod. 2005;73(6):1182-1190.
38. Matuliene J, Kuriyama R. Role of the midbody matrix in cytokinesis: RNAi and genetic rescue analysis of the mammalian motor protein CHO1. Mol Biol Cell. 2004;15(7):3083-3094.
39. Matzuk MM, Dionne L, Guo Q, Kumar TR, Lebovitz RM. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology. 1998;139:4008-4011.
40. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. a-Inhibin is a tumor-suppressor gene with gonadal specificity in mice. Nature. 1992;360:313-319.
41. Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature. 1995;374:356-360.
42. Matzuk MM, Lamb DJ. Genetic dissection of mammalian fertility pathways. Nat Med. 2002;8(suppl 1):S41-S49.
43. Matzuk MM, Lamb DJ. The biology of infertility: research advances and clinical challenges. Nat Med. 2008;14(11):1197-1213.
44. Meng X, Lindahl M, Hyvonen ME, Parvinen M, Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science. 2000;287(5457):1489-1493.
45. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RR. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev. 1996;10:2577-2587.
46. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113(5):631-642.
47. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod. 2006;74(2):314-321.
48. Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, Matzuk MM. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A. 1996;93:11699-11704.
49. Oatley JM, Avarbock MR, Brinster RL. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem. 2007;282(35):25842-25851.
50. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci U S A. 2006;103(25):9524-9529.
51. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development. 2009;136(7):1191-1199.
52. Ohta H, Yomogida K, Dohmae K, Nishimune Y. Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Development. 2000;127(10):2125-2131.
53. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, Matzuk MM, Rajkovic A. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci U S A. 2006;103(21):8090-8095.
54. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ. Disease-specific induced pluripotent stem cells. Cell. 2008a;134(5):877-886.
55. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008b;451(7175):141-146.
56. Pesce M, Wang X, Wolgemuth DJ, Schöler H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev. 1998;71(1-2):89-98.
57. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004;305:1157-1159.
58. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM. Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. FASEB J. 2007;21(4):1013-1025.
59. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM. Tektin 3 is required for progressive sperm motility in mice. Mol Reprod Dev. 2009;76(5):453-459.
60. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci U S A. 2000;97(15):8346-8351.
61. Soyal SM, Amleh A, Dean J. FIGa, a germ cell-specific transcription factor required for ovarian follicle formation. Development. 2000;127(21)4645-4654.
62. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861-872.
63. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663-676.
64. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LJ, Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A. 2005;102(44):16096-16101.
65. Tang CJ, Lin CY, Tang TK. Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol. 2006;290(2):398-410.
66. Toyoda S, Miyazaki T, Miyazaki S, Yoshimura T, Yamamoto M, Tashiro F, Yamato E, Miyazaki J. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Dev Biol. 2009;325(1):238-248.
67. Treanor JJ, Goodman L, de Sauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, Phillips HS, Goddard A, Moore MW, Buj-Bello A, Davies AM, Asai N, Takahashi M, Vandlen R, Henderson CE, Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature. 1996;382(6586):80-83.
68. Van de Putte T, Zwijsen A, Lonnoy O, Rybin V, Cozijnsen M, Francis A, Baekelandt V, Kozak CA, Zerial M, Huylebroeck D. Mice with a homozygous gene trap vector insertion in mgcRacGAP die during pre-implantation development. Mech Dev. 2001;102(1-2):33-44.
69. Vassalli A, Matzuk MM, Gardner HA, Lee KF, Jaenisch R. Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 1994;8(4):414-427.
70. Ventela S, Toppari J, Parvinen M. Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: mechanisms of haploid gene product sharing. Mol Biol Cell. 2003;14(7):2768-2780.
71. Wang PJ, McCarrey JR, Yang F, Page DC. An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 2001;27(4):422-426.
72. Wang S, Zheng H, Esaki Y, Kelly F, Yan W. Cullin3 is a KLHL10-interacting protein preferentially expressed during late spermiogenesis. Biol Reprod. 2006;74(1):102-108.
73. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007;448(7151):318-324.
74. Wu MH, Rajkovic A, Burns KH, Yan W, Lin YN, Matzuk MM. Sequence and expression of testis-expressed gene 14 (Tex14): a gene encoding a protein kinase preferentially expressed during spermatogenesis. Gene Expr Patterns. 2003a;3(2):231-236.
75. Wu X, Viveiros M, Eppig J, Bai Y, Fitzpatrick S, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet. 2003b;33(2):187-191.
76. Yan C, Wang P, DeMayo J, DeMayo F, Elvin J, Carino C, Prasad S, Skinner S, Dunbar B, Dube JL, Celeste AJ, Matzuk MM. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15(6):854-866.
77. Yan W, Assadi AH, Wynshaw-Boris A, Eichele G, Matzuk MM, Clark GD. Previously uncharacterized roles of platelet-activating factor acetylhydrolase 1b complex in mouse spermatogenesis. Proc Natl Acad Sci U S A. 2003;100(12):7189-7194.
78. Yan W, Ma L, Burns KH, Matzuk MM. Haploinsufficiency of kelch-like protein homolog 10 causes infertility in male mice. Proc Natl Acad Sci U S A. 2004;101(20):7793-7798.
79. Yan W, Ma L, Pangas SA, Burns KH, Bai Y, Schultz RM, Matzuk MM. Mice deficient in oocyte-specific oligoadenylate synthase-like protein, OAS1D display reduced fertility. Mol Cell Biol. 2005;25(11):4615-4624.
80. Yang J, Medvedev S, Yu J, Tang LC, Agno JE, Matzuk MM, Schultz RM, Hecht NB. Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc Natl Acad Sci U S A. 2005;102(16):5755-5760.
81. Yao HHC, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn. 2004;230:210-215.
82. Yatsenko AN, Roy A, Chen R, Ma L, Murthy LJ, Yan W, Lamb DJ, Matzuk MM. Non-invasive genetic diagnosis of male infertility using spermatozoal RNA: KLHL10 mutations in oligozoospermic patients impair homodimerization. Hum Mol Genet. 2006;15(23):3411-3419.
83. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol. 2004;269(2):447-458.
84. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917-1920.