The Wilms Tumor Gene, Wt1, Is Critical for Mouse Spermatogenesis via Regulation of Sertoli Cell Polarity and Is Associated with Non-Obstructive Azoospermia in Humans

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Wang, Xiao Na ^a,b   Li, Ze Song ^c,d   Ren, Yu ^a,b   Jiang, Tao ^e   Wang, Ya Qing ^f   Chen, Min ^a   Zhang, Jun ^a,b   Hao, Jian Xiu ^a,b   Wang, Yan Bo ^a,b   Sha, Ri Na ^a,b   Huang, Yi ^c,d   Liu, Xiao ^e   Hu, Jing Chu ^e   Sun, Guang Qing ^e   Li, Hong Gang ^g   Xiong, Cheng Liang ^g   Xie, Jun ^c   Jiang, Zhi Mao ^c   Cai, Zhi Ming ^c,d   Wang, Jun ^e   Wang, Jian ^e   Huff, Vicki ^h   Gui, Yao Ting ^c   Gao, Fei ^a   more..

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c PEKING UNIVERSITY SHENZHEN HOSPITAL   (China)

^d THE FIRST AFFILIATED HOSPITAL OF SHENZHEN UNIVERSITY   (China)

^e BGI SHENZHEN   (China)

^f INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^g HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^h UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UVOMORULIN; WT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AZOOSPERMIA; BLOOD TESTIS BARRIER; CELL DEATH; CELL LOSS; CELL POLARITY; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; E CADHERIN GENE; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INACTIVATION; HUMAN; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PAR6B GENE; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; UPREGULATION; WESTERN BLOTTING; WNT 11 GENE; WNT 4 GENE; WNT SIGNALING PATHWAY; WT1 GENE;

ANIMALS; AZOOSPERMIA; CELL POLARITY; HUMANS; INFERTILITY, MALE; MALE; MICE; SERTOLI CELLS; SPERMATOGENESIS; WNT PROTEINS; WNT4 PROTEIN; WT1 PROTEINS;

EID: 84884639133     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003645     Document Type: Article

References (60)

1. Ferlin A, Arredi B, Foresta C, (2006) Genetic causes of male infertility. Reprod Toxicol 22: 133-141.
2. Oliva R, (2006) Protamines and male infertility. Hum Reprod Update 12: 417-435.
3. Dam AH, Koscinski I, Kremer JA, Moutou C, Jaeger AS, et al. (2007) Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. Am J Hum Genet 81: 813-820.
4. Dieterich K, Soto Rifo R, Faure AK, Hennebicq S, Ben Amar B, et al. (2007) Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet 39: 661-665.
5. Yatsenko AN, Roy A, Chen R, Ma L, Murthy LJ, et al. (2006) Non-invasive genetic diagnosis of male infertility using spermatozoal RNA: KLHL10 mutations in oligozoospermic patients impair homodimerization. Hum Mol Genet 15: 3411-3419.
6. Mackay S, (2000) Gonadal development in mammals at the cellular and molecular levels. Int Rev Cytol 200: 47-99.
7. Josso N, di Clemente N, Gouedard L, (2001) Anti-Mullerian hormone and its receptors. Mol Cell Endocrinol 179: 25-32.
8. Dym M, Raj HG, (1977) Response of adult rat Sertoli cells and Leydig cells to depletion of luteinizing hormone and testosterone. Biol Reprod 17: 676-696.
9. Feig LA, Bellve AR, Erickson NH, Klagsbrun M, (1980) Sertoli cells contain a mitogenic polypeptide. Proc Natl Acad Sci U S A 77: 4774-4778.
10. Johnson L, Varner DD, Thompson DL Jr, (1991) Effect of age and season on the establishment of spermatogenesis in the horse. J Reprod Fertil Suppl 44: 87-97.
11. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, et al. (2006) The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc Natl Acad Sci U S A 103: 11987-11992.
12. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, et al. (1993) WT-1 is required for early kidney development. Cell 74: 679-691.
13. Gao F, Maiti S, Sun G, Ordonez NG, Udtha M, et al. (2004) The Wt1+/R394W mouse displays glomerulosclerosis and early-onset renal failure characteristic of human Denys-Drash syndrome. Mol Cell Biol 24: 9899-9910.
14. Rao MK, Pham J, Imam JS, MacLean JA, Murali D, et al. (2006) Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 20: 147-152.
15. Chau YY, Brownstein D, Mjoseng H, Lee WC, Buza-Vidas N, et al. (2011) Acute multiple organ failure in adult mice deleted for the developmental regulator Wt1. PLoS Genet 7: e1002404.
16. Stoll R, Lee BM, Debler EW, Laity JH, Wilson IA, et al. (2007) Structure of the Wilms tumor suppressor protein zinc finger domain bound to DNA. J Mol Biol 372: 1227-1245.
17. Lyon GJ, Jiang T, Van Wijk R, Wang W, Bodily PM, et al. (2011) Exome sequencing and unrelated findings in the context of complex disease research: ethical and clinical implications. Discov Med 12: 41-55.
18. Ng PC, Henikoff S, (2003) SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 31: 3812-3814.
19. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
20. Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AF, et al. (2004) Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 14: 708-715.
21. Cooper GM, Goode DL, Ng SB, Sidow A, Bamshad MJ, et al. (2010) Single-nucleotide evolutionary constraint scores highlight disease-causing mutations. Nat Methods 7: 250-251.
22. Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE, (2005) Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci U S A 102: 16696-16700.
23. Wong CH, Cheng CY, (2005) The blood-testis barrier: its biology, regulation, and physiological role in spermatogenesis. Curr Top Dev Biol 71: 263-296.
24. Essafi A, Webb A, Berry RL, Slight J, Burn SF, et al. (2011) A wt1-controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev Cell 21: 559-574.
25. Martinez-Estrada OM, Lettice LA, Essafi A, Guadix JA, Slight J, et al. (2010) Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42: 89-93.
26. Mruk DD, Cheng CY, (2004) Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25: 747-806.
27. Jegou B, (1993) The Sertoli-germ cell communication network in mammals. Int Rev Cytol 147: 25-96.
28. Russell LD, Peterson RN, (1985) Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94: 177-211.
29. Gow A, Southwood CM, Li JS, Pariali M, Riordan GP, et al. (1999) CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99: 649-659.
30. Wang RS, Yeh S, Tzeng CR, Chang C, (2009) Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev 30: 119-132.
31. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, et al. (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476: 101-104.
32. Kyronlahti A, Euler R, Bielinska M, Schoeller EL, Moley KH, et al. (2011) GATA4 regulates Sertoli cell function and fertility in adult male mice. Mol Cell Endocrinol 333: 85-95.
33. Brehm R, Zeiler M, Ruttinger C, Herde K, Kibschull M, et al. (2007) A sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am J Pathol 171: 19-31.
34. Mazaud-Guittot S, Meugnier E, Pesenti S, Wu X, Vidal H, et al. Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod 82: 202-213.
35. Joberty G, Petersen C, Gao L, Macara IG, (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2: 531-539.
36. Gao L, Joberty G, Macara IG, (2002) Assembly of epithelial tight junctions is negatively regulated by Par6. Curr Biol 12: 221-225.
37. Wong EW, Mruk DD, Lee WM, Cheng CY, (2008) Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci U S A 105: 9657-9662.
38. Chen WS, Antic D, Matis M, Logan CY, Povelones M, et al. (2008) Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133: 1093-1105.
39. Rauch GJ, Hammerschmidt M, Blader P, Schauerte HE, Strahle U, et al. (1997) Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb Symp Quant Biol 62: 227-234.
40. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, et al. (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
41. Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, et al. (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306: 121-133.
42. Kispert A, Vainio S, McMahon AP, (1998) Wnt-4 is a mesenchymal signal for epithelial transformation of metanephric mesenchyme in the developing kidney. Development 125: 4225-4234.
43. Stark K, Vainio S, Vassileva G, McMahon AP, (1994) Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372: 679-683.
44. Hosono S, Gross I, English MA, Hajra KM, Fearon ER, et al. (2000) E-cadherin is a WT1 target gene. J Biol Chem 275: 10943-10953.
45. Bruening W, Bardeesy N, Silverman BL, Cohn RA, Machin GA, et al. (1992) Germline intronic and exonic mutations in the Wilms' tumour gene (WT1) affecting urogenital development. Nat Genet 1: 144-148.
46. Gessler M, Poustka A, Cavenee W, Neve RL, Orkin SH, et al. (1990) Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 343: 774-778.
47. Pelletier J, Bruening W, Li FP, Haber DA, Glaser T, et al. (1991) WT1 mutations contribute to abnormal genital system development and hereditary Wilms' tumour. Nature 353: 431-434.
48. Pfeiffer DC, Vogl AW, (1991) Evidence that vinculin is co-distributed with actin bundles in ectoplasmic ("junctional") specializations of mammalian Sertoli cells. Anat Rec 231: 89-100.
49. Call KM, Glaser T, Ito CY, Buckler AJ, Pelletier J, et al. (1990) Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 60: 509-520.
50. Huff V, Miwa H, Haber DA, Call KM, Housman D, et al. (1991) Evidence for WT1 as a Wilms tumor (WT) gene: intragenic germinal deletion in bilateral WT. Am J Hum Genet 48: 997-1003.
51. Royer-Pokora B, Beier M, Henzler M, Alam R, Schumacher V, et al. (2004) Twenty-four new cases of WT1 germline mutations and review of the literature: genotype/phenotype correlations for Wilms tumor development. Am J Med Genet A 127A: 249-257.
52. Gui Y, Guo G, Huang Y, Hu X, Tang A, et al. (2011) Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet 43: 875-878.
53. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
54. Li R, Li Y, Fang X, Yang H, Wang J, et al. (2009) SNP detection for massively parallel whole-genome resequencing. Genome Res 19: 1124-1132.
55. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
56. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, et al. (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18: 5931-5942.
57. Zhang X, Hao L, Meng L, Liu M, Zhao L, et al. (2013) Digital gene expression tag profiling analysis of the gene expression patterns regulating the early stage of mouse spermatogenesis. PLoS One 8: e58680.
58. Audic S, Claverie JM, (1997) The significance of digital gene expression profiles. Genome Res 7: 986-995.
59. van der Wee KS, Johnson EW, Dirami G, Dym TM, Hofmann MC, (2001) Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J Androl 22: 696-704.
60. Meng F, Chen S, Miao Q, Zhou K, Lao Q, et al. (2012) Induction of fibroblasts to neurons through adenoviral gene delivery. Cell Res 22: 436-440.