A Wt1-Dmrt1 Transgene Restores DMRT1 to Sertoli Cells of Dmrt1-/- Testes: A Novel Model of DMRT1-Deficient Germ Cells

Biology of Reproduction

Volumn 88, Issue 2, 2013, Pages

  Agbor, Valentine A ^a   Tao, Shixin ^b   Lei, Ning ^a,c   Heckert, Leslie L ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

DMRT1; Male infertility; Sertoli cells; Spermatogenesis; Testis

Indexed keywords

DOUBLESEX AND MAB 3 RELATED TRANSCRIPTION FACTOR 1; NECTIN 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BLOOD TESTIS BARRIER; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; ELECTRON MICROSCOPY; GENE LOCUS; GENOTYPE; GERM CELL; GONAD; GRANULOSA CELL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; MALE; MALE FERTILITY; MALE INFERTILITY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON MOTILITY; TESTIS; TESTIS DEVELOPMENT; TESTIS SIZE; TESTIS WEIGHT; TIGHT JUNCTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; CELL ADHESION MOLECULES; INFERTILITY, MALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, ANIMAL; SERTOLI CELLS; SPERM MOTILITY; TESTIS; TRANSCRIPTION FACTORS; TRANSGENES;

MUS; MUS MUSCULUS; RATTUS;

EID: 84877032008     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.103135     Document Type: Article

References (88)

1. Ferguson-Smith M. The evolution of sex chromosomes and sex determination in vertebrates and the key role of DMRT1. Sex Dev 2007; 1:2-11.
2. Kim S, Bardwell VJ, Zarkower D. Cell type-autonomous and nonautonomous requirements for Dmrt1 in postnatal testis differentiation. Dev Biol 2007; 307:314-327.
3. Krentz AD, Murphy MW, Kim S, Cook MS, Capel B, Zhu R, Matin A, Sarver AL, Parker KL, Griswold MD, Looijenga LH, Bardwell VJ, et al. The DM domain protein DMRT1 is a dose-sensitive regulator of fetal germ cell proliferation and pluripotency. Proc Natl Acad Sci U S A 2009; 106:22323-22328.
4. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre J, Bernot A, Laudet V, Guiguen Y. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 2000; 1493:180-187.
5. Matson CK, Murphy MW, Griswold MD, Yoshida S, Bardwell VJ, Zarkower D. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev Cell 2010; 19:612-624.
6. Erdman SE, Burtis KC. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 1993; 12:527-535.
7. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature 1998; 391:691-695.
8. Zhu L, Wilken J, Phillips NB, Narendra U, Chan G, Stratton SM, Kent SB, Weiss MA. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev 2000; 14:1750-1764.
9. Volff JN, Zarkower D, Bardwell VJ, Schartl M. Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol 2003; 57(suppl 1): S241-S249.
10. Bratus A, Slota E. DMRT1/Dmrt1, the sex determining or sex differentiating gene in Vertebrata. Folia Biol (Krakow) 2006; 54:81-86.
11. Nagahama Y. Molecular mechanisms of sex determination and gonadal sex differentiation in fish. Fish Physiol Biochem 2005; 31:105-109.
12. Smith CA, Sinclair AH. Sex determination: insights from the chicken. Bioessays 2004; 26:120-132.
13. Sinclair A, Smith C, Western P, McClive P. A comparative analysis of vertebrate sex determination. Novartis Found Symp 2002; 244:102-111; discussion 111-104, 203-106, 253-107.
14. Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH. Conservation of a sex-determining gene. Nature 1999; 402:601-602.
15. Boyer A, Dornan S, Daneau I, Lussier J, Silversides DW. Conservation of the function of DMRT1 regulatory sequences in mammalian sex differentiation. Genesis 2002; 34:236-243.
16. Hong CS, Park BY, Saint-Jeannet JP. The function of Dmrt genes in vertebrate development: it is not just about sex. Dev Biol 2007; 310:1-9.
17. Lints R, Emmons SW. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev 2002; 16:2390-2402.
18. Zhang W, Li B, Singh R, Narendra U, Zhu L, Weiss MA. Regulation of sexual dimorphism: mutational and chemogenetic analysis of the doublesex DM domain. Mol Cell Biol 2006; 26:535-547.
19. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 1999; 215:208-220.
20. Fahrioglu U, Murphy MW, Zarkower D, Bardwell VJ. mRNA expression analysis and the molecular basis of neonatal testis defects in Dmrt1 mutant mice. Sex Dev 2007; 1:42-58.
21. Herpin A, Schartl M. Molecular mechanisms of sex determination and evolution of the Y-chromosome: insights from the medakafish (Oryzias latipes). Mol Cell Endocrinol 2009; 306:51-58.
22. Koopman P. The delicate balance between male and female sex determining pathways: potential for disruption of early steps in sexual development. Int J Androl 2010; 33:252-258.
23. Moniot B, Berta P, Scherer G, Sudbeck P, Poulat F. Male specific expression suggests role of DMRT1 in human sex determination. Mech Dev 2000; 91:323-325.
24. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000; 14:2587-2595.
25. Rhen T, Schroeder A. Molecular mechanisms of sex determination in reptiles. Sex Dev 2010; 4:16-28.
26. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009; 461:267-271.
27. Lei N, Hornbaker KI, Rice DA, Karpova T, Agbor VA, Heckert LL. Sexspecific differences in mouse DMRT1 expression are both cell type-and stage-dependent during gonad development. Biol Reprod 2007; 77:466-475.
28. Kettlewell JR, Raymond CS, Zarkower D. Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 2000; 26:174-178.
29. Repetto GM, Wagstaff J, Korf BR, Knoll JH. Complex familial rearrangement of chromosome 9p24.3 detected by FISH. Am J Med Genet 1998; 76:306-309.
30. Christ LA, Crowe CA, Micale MA, Conroy JM, Schwartz S. Chromosome breakage hotspots and delineation of the critical region for the 9p-deletion syndrome. Am J Hum Genet 1999; 65:1387-1395.
31. Swinkels ME, Simons A, Smeets DF, Vissers LE, Veltman JA, Pfundt R, de Vries BB, Faas BH, Schrander-Stumpel CT, McCann E, Sweeney E, May P, et al. Clinical and cytogenetic characterization of 13 Dutch patients with deletion 9p syndrome: delineation of the critical region for a consensus phenotype. Am J Med Genet A 2008; 146A:1430-1438.
32. Barbaro M, Balsamo A, Anderlid BM, Myhre AG, Gennari M, Nicoletti A, Pittalis MC, Oscarson M, Wedell A. Characterization of deletions at 9p affecting the candidate regions for sex reversal and deletion 9p syndrome by MLPA. Eur J Hum Genet 2009; 17:1439-1447.
33. Vinci G, Chantot-Bastaraud S, El Houate B, Lortat-Jacob S, Brauner R, McElreavey K. Association of deletion 9p, 46, XY gonadal dysgenesis and autistic spectrum disorder. Mol Hum Reprod 2007; 13:685-689.
34. Vasquez-Velasquez AI, Arnaud-Lopez L, Figuera LE, Padilla-Gutierrez JR, Rivas F, Rivera H. Ambiguous genitalia by 9p deletion inherent to a dic(Y;9)(q12;p24). J Appl Genet 2005; 46:415-418.
35. Ounap K, Uibo O, Zordania R, Kiho L, Ilus T, Oiglane-Shlik E, Bartsch O. Three patients with 9p deletions including DMRT1 and DMRT2: a girl with XY complement, bilateral ovotestes, and extreme growth retardation, and two XX females with normal pubertal development. Am J Med Genet A 2004; 130A:415-423.
36. Vialard F, Ottolenghi C, Gonzales M, Choiset A, Girard S, Siffroi JP, McElreavey K, Vibert-Guigue C, Sebaoun M, Joye N, Portnoi MF, Jaubert F, et al. Deletion of 9p associated with gonadal dysfunction in 46, XY but not in 46, XX human fetuses. J Med Genet 2002; 39:514-518.
37. Shetty S, Kirby P, Zarkower D, Graves JA. DMRT1 in a ratite bird: evidence for a role in sex determination and discovery of a putative regulatory element. Cytogenet Genome Res 2002; 99:245-251.
38. Yi W, Zarkower D. Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 1999; 126:873-881.
39. Herpin A, Schartl M. Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 2011; 278:1010-1019.
40. Koopman P. Sex determination: the power of DMRT1. Trends Genet 2009; 25:479-481.
41. Krentz AD, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 promotes oogenesis by transcriptional activation of Stra8 in the mammalian fetal ovary. Dev Biol 2011; 356:63-70.
42. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011; 476:101-104.
43. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006; 133:1495-1505.
44. 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; 269:447-458.
45. Karpova T, Presley J, Manimaran RR, Scherrer SP, Tejada L, Peterson KR, Heckert LL. A FTZ-F1-containing yeast artificial chromosome recapitulates expression of steroidogenic factor 1 in vivo. Mol Endocrinol 2005; 19:2549-2563.
46. Godwin AR, Capecchi MR. Hoxc13 mutant mice lack external hair. Genes Dev 1998; 12:11-20.
47. Poorkaj P, Peterson KR, Schellenberg GD. Single-step conversion of P1 and P1 artificial chromosome clones into yeast artificial chromosomes. Genomics 2000; 68:106-110.
48. Burgers PM, Percival KJ. Transformation of yeast spheroplasts without cell fusion. Anal Biochem 1987; 163:391-397.
49. Hermann BP, Hornbaker KI, Maran RR, Heckert LL. Distal regulatory elements are required for Fshr expression, in vivo. Mol Cell Endocrinol 2007; 260-262:49-58.
50. Karpova T, Maran RR, Presley J, Scherrer SP, Tejada L, Heckert LL. Transgenic rescue of SF-1-null mice. Ann N Y Acad Sci 2005; 1061:55-64.
51. Peterson KR, Clegg CH, Li Q, Stamatoyannopoulos G. Production of transgenic mice with yeast artificial chromosomes. Trends Genet 1997; 13:61-66.
52. Peterson KR. Production and analysis of transgenic mice containing yeast artificial chromosomes. Genet Eng (N Y) 1997; 19:235-255.
53. 2+, and pH to maintain motility in rat spermatozoa. Reproduction 2010; 139:835-845.
54. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-675.
55. Heckert LL, Sawadogo M, Daggett MA, Chen JK. The USF proteins regulate transcription of the follicle-stimulating hormone receptor but are insufficient for cell-specific expression. Mol Endocrinol 2000; 14:1836-1848.
56. Gifford CA, Racicot K, Clark DS, Austin KJ, Hansen TR, Lucy MC, Davies CJ, Ott TL. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. J Dairy Sci 2007; 90:274-280.
57. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
58. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet 2001; 28:216-217.
59. Moore AW, Schedl A, McInnes L, Doyle M, Hecksher-Sorensen J, Hastie ND. YAC transgenic analysis reveals Wilms' tumour 1 gene activity in the proliferating coelomic epithelium, developing diaphragm and limb. Mech Dev 1998; 79:169-184.
60. Tarulli GA, Stanton PG, Lerchl A, Meachem SJ. Adult Sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH on proliferation and junction protein organization. Biol Reprod 2006; 74:798-806.
61. Yomogida K, Ohtani H, Harigae H, Ito E, Nishimune Y, Engel JD, Yamamoto M. Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 1994; 120:1759-1766.
62. Imai T, Kawai Y, Tadokoro Y, Yamamoto M, Nishimune Y, Yomogida K. In vivo and in vitro constant expression of GATA-4 in mouse postnatal Sertoli cells. Mol Cell Endocrinol 2004; 214:107-115.
63. Russell LD, Bartke A, Goh JC. Postnatal development of the Sertoli cell barrier, tubular lumen, and cytoskeleton of Sertoli and myoid cells in the rat, and their relationship to tubular fluid secretion and flow. Am J Anat 1989; 184:179-189.
64. Cheng CY, Mruk DD. Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem J 2011; 435:553-562.
65. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825-874.
66. Mruk DD, Cheng CY. Tight junctions in the testis: new perspectives. Philos Trans R Soc Lond B Biol Sci 2010; 365:1621-1635.
67. Ramos AS Jr, Dym M. Ultrastructural differentiation of rat Sertoli cells. Biol Reprod 1979; 21:909-922.
68. Russell LD, Ren HP, Sinha Hikim I, Schulze W, Sinha Hikim AP. A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the Sertoli cell. Am J Anat 1990; 188:21-30.
69. Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y. Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 2000; 258:210-220.
70. Montoliu L. Gene transfer strategies in animal transgenesis. Cloning Stem Cells 2002; 4:39-46.
71. 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.
72. Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 1993; 119:1329-1341.
73. Buckler AJ, Pelletier J, Haber DA, Glaser T, Housman DE. Isolation, characterization, and expression of the murine Wilms' tumor gene (WT1) during kidney development. Mol Cell Biol 1991; 11:1707-1712.
74. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003; 125:769-784.
75. 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.
76. Ketola I, Anttonen M, Vaskivuo T, Tapanainen JS, Toppari J, Heikinheimo M. Developmental expression and spermatogenic stage specificity of transcription factors GATA-1 and GATA-4 and their cofactors FOG-1 and FOG-2 in the mouse testis. Eur J Endocrinol 2002; 147:397-406.
77. LaVoie HA. The role of GATA in mammalian reproduction. Exp Biol Med (Maywood) 2003; 228:1282-1290.
78. Maga G, Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 2003; 116:3051-3060.
79. Bar-Shira Maymon B, Paz G, Elliott DJ, Hammel I, Kleiman SE, Yogev L, Hauser R, Botchan A, Yavetz H. Maturation phenotype of Sertoli cells in testicular biopsies of azoospermic men. Hum Reprod 2000; 15:1537-1542.
80. Jung A, Schuppe HC, Schill WB. Comparison of semen quality in older and younger men attending an andrology clinic. Andrologia 2002; 34:116-122.
81. Eskenazi B, Wyrobek AJ, Sloter E, Kidd SA, Moore L, Young S, Moore D. The association of age and semen quality in healthy men. Hum Reprod 2003; 18:447-454.
82. Levitas E, Lunenfeld E, Weisz N, Friger M, Potashnik G. Relationship between age and semen parameters in men with normal sperm concentration: analysis of 6022 semen samples. Andrologia 2007; 39:45-50.
83. Vogl AW, Pfeiffer DC, Redenbach DM. Ectoplasmic ("junctional") specializations in mammalian Sertoli cells: influence on spermatogenic cells. Ann N Y Acad Sci 1991; 637:175-202. AGBOR ET AL.
84. Bartles JR, Wierda A, Zheng L. Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci 1996; 109(pt 6):1229-1239.
85. Mueller S, Rosenquist TA, Takai Y, Bronson RA, Wimmer E. Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration. Biol Reprod 2003; 69:1330-1340.
86. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, Mueller S, Irie K, Ikeda W, Sakai T, Wimmer E, Nishimune Y, Takai Y. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 2002; 12:1145-1150.
87. Byers S, Graham R, Dai HN, Hoxter B. Development of Sertoli cell junctional specializations and the distribution of the tight-junctionassociated protein ZO-1 in the mouse testis. Am J Anat 1991; 191:35-47.
88. Myers M, Ebling FJ, Nwagwu M, Boulton R, Wadhwa K, Stewart J, Kerr JB. Atypical development of Sertoli cells and impairment of spermatogenesis in the hypogonadal (hpg) mouse. J Anat 2005; 207:797-811.