Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis

Genes and Development

Volumn 20, Issue 2, 2006, Pages 147-152

  Rao, Manjeet K ^a   Pham, John ^a   Imam, J Saadi ^a   MacLean, James A ^a   Murali, Deepa ^a   Furuta, Yasuhide ^a   Sinha Hikim, Amiya P ^b   Wilkinson, Miles F ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Germ cell; miRNA; RNAi; Sertoli cell; Spermatogenesis; WT1

Indexed keywords

MICRORNA; TRANSCRIPTION FACTOR; WT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; GENE TARGETING; GERM CELL; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SERTOLI CELL; SPERMATOGENESIS; TRANSGENIC MOUSE;

ADHERENS JUNCTIONS; ANIMALS; APOPTOSIS; CELL SURVIVAL; DNA POLYMERASE II; GENE EXPRESSION; GERM CELLS; GONADS; MALE; MICE; MICE, TRANSGENIC; MUTATION; ORGAN SPECIFICITY; REPRODUCIBILITY OF RESULTS; RIBONUCLEASE III; RNA INTERFERENCE; RNA PRECURSORS; SERTOLI CELLS; SPERMATOGENESIS; TRANSCRIPTION FACTORS; TRANSFECTION; WT1 PROTEINS;

ANIMALIA; MUS MUSCULUS;

EID: 30944469656     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad1367806     Document Type: Article

References (37)

1. Armstrong, J.F., Pritchard-Jones, K., Bickmore, W.A., Hastie, N.D., and Bard, J.B. 1993. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech. Dev. 40: 85-97.
2. Blume-Jensen, P., Jiang, G., Hyman, R., Lee, K.F., O'Gorman, S., and Hunter, T. 2000. Kit/stem cell factor receptor-induced activation of phosphatidylinositol 3′-kinase is essential for male fertility. Nat. Genet. 24: 157-162.
3. Bouvard, D., Vignoud, L., Dupe-Manet, S., Abed, N., Fournier, H.N., Vincent-Monegat, C., Retta, S.F., Fassler, R., and Block, M.R. 2003. Disruption of focal adhesions by integrin cytoplasmic domain-associated protein-1 α. J. Biol. Chem. 278: 6567-6574.
4. Calderwood, D.A., Fujioka, Y., de Pereda, J.M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C.J., Liddington, R.C., and Ginsberg, M.H. 2003. Integrin β cytoplasmic domain interactions with phosphotyrosine- binding domains: A structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. 100: 2272-2277.
5. Chang, D.D., Hoang, B.Q., Liu, J., and Springer, T.A. 2002. Molecular basis for interaction between Icap1 α PTB domain and β 1 integrin. J. Biol. Chem. 277: 8140-8145.
6. Chapin, R.E., Wine, R.N., Harris, M.W., Borchers, C.H., and Haseman, J.K. 2001. Structure and control of a cell-cell adhesion complex associated with spermiation in rat seminiferous epithelium. J. Androl. 22: 1030-1052.
7. Davies, J.A., Ladomery, M., Hohenstein, P., Michael, L., Shafe, A., Spraggon, L., and Hastie, N. 2004. Development of an siRNA-based method for repressing specific genes in renal organ culture and its use to show that the Wt1 tumour suppressor is required for nephron differentiation. Hum. Mol. Genet. 13: 235-246.
8. Degani, S., Balzac, F., Brancaccio, M., Guazzone, S., Retta, S.F., Silengo, L., Eva, A., and Tarone, G. 2002. The integrin cytoplasmic domain-associated protein ICAP-1 binds and regulates Rho family GTPases during cell spreading. J. Cell Biol. 156: 377-387.
9. Disanza, A., Carlier, M.F., Stradal, T.E., Didry, D., Frittoli, E., Confalonieri, S., Croce, A., Wehland, J., Di Fiore, P.P., and Scita, G. 2004. Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat. Cell Biol. 6: 1180-1188.
10. Faisst, A.M. and Gruss, P. 1998. Bodenin: A novel murine gene expressed in restricted areas of the brain. Dev. Dyn. 212: 293-303.
11. Fedoriw, A.M., Stein, P., Svoboda, P., Schultz, R.M., and Bartolomei, M.S. 2004. Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303: 238-240.
12. Gudikote, J.P. and Wilkinson, M.F. 2002. T-cell receptor sequences that elicit strong down-regulation of premature termination codon-bearing transcripts. EMBO J. 21: 125-134.
13. Hogarth, C., Itman, C., Jans, D.A., and Loveland, K.L. 2005. Regulated nucleocytoplasmic transport in spermatogenesis: A driver of cellular differentiation? Bioessays 27: 1011-1025.
14. Innocenti, M., Frittoli, E., Ponzanelli, I., Falck, J.R., Brachmann, S.M., Di Fiore, P.P., and Scita, G. 2003. Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. J. Cell Biol. 160: 17-23.
15. Ketola, I., Rahman, N., Toppari, J., Bielinska, M., Porter-Tinge, S.B., Tapanainen, J.S., Huhtaniemi, I.T., Wilson, D.B., and Heikinheimo, M. 1999. Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 140: 1470-1480.
16. Kumar, T.R., Varani, S., Wreford, N.G., Telfer, N.M., de Kretser, D.M., and Matzuk, M.M. 2001. Male reproductive phenotypes in double mutant mice lacking both FSHβ and activin receptor IIA. Endocrinology 142: 3512-3518.
17. Lindsey, J.S. and Wilkinson, M.F. 1996. Pem: A testosterone- and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymis. Dev. Biol. 179: 471-484.
18. Little, M., Holmes, G., and Walsh, P. 1999. WT1: What has the last decade told us? Bioessays 21: 191-202.
19. MacLean II, J.A., Chen, M.A., Wayne, C.M., Bruce, S.R., Rao, M., Meistrich, M.L., Macleod, C., and Wilkinson, M.F. 2005. Rhox: A new homeobox gene cluster. Cell 120: 369-382.
20. Mruk, D.D. and Cheng, C.Y. 2004. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol. Metab. 15: 439-447.
21. Park, S.Y. and Jameson, J.L. 2005. Minireview: Transcriptional regulation of gonadal development and differentiation. Endocrinology 146: 1035-1042.
22. Pelletier, J., Schalling, M., Buckler, A.J., Rogers, A., Haber, D.A., and Housman, D. 1991. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes & Dev. 5: 1345-1356.
23. Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. 2005. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309: 1573-1576.
24. Rao, M.K., Wayne, C.M., and Wilkinson, M.F. 2002. Pem homeobox gene regulatory sequences that direct androgen-dependent developmentally regulated gene expression in different subregions of the epididymis. J. Biol. Chem. 277: 48771-48778.
25. Rao, M.K., Wayne, C.M., Meistrich, M.L., and Wilkinson, M.F. 2003. Pem homeobox gene promoter sequences that direct transcription in a Sertoli cell-specific, stage-specific, and androgen-dependent manner in the testis in vivo. Mol. Endocrinol. 17: 223-233.
26. Raymond, K., Bergeret, E., Avet-Rochex, A., Griffin-Shea, R., and Fauvarque, M.O. 2004. A screen for modifiers of RacGAP(84C) gain-offunction in the Drosophila eye revealed the LIM kinase Cdi/TESK1 as a downstream effector of Rac1 during spermatogenesis. J. Cell Sci. 117: 2777-2789.
27. Reddy, J.C., Morris, J.C., Wang, J., English, M.A., Haber, D.A., Shi, Y., and Licht, J.D. 1995. WT1-mediated transcriptional activation is inhibited by dominant negative mutant proteins. J. Biol. Chem. 270: 10878-10884.
28. Scharnhorst, V., Dekker, P., van der Eb, A.J., and Jochemsen, A.G. 1999. Internal translation initiation generates novel WT1 protein isoforms with distinct biological properties. J. Biol. Chem. 274: 23456-23462.
29. Scita, G., Nordstrom, J., Carbone, R., Tenca, P., Giardina, G., Gutkind, S., Bjarnegard, M., Betsholtz, C., and Di Fiore, P.P. 1999. EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401: 290-293.
30. Shen, J.H. and Ingraham, H.A. 2002. Regulation of the orphan nuclear receptor steroidogenic factor 1 by Sox proteins. Mol. Endocrinol. 16: 529-540.
31. Siu, M.K.Y., Wong, C.H., Lee, W.M., and Cheng, C.Y. 2005. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J. Biol. Chem. 280: 25029-25047.
32. Sutton, K.A., Maiti, S., Tribley, W.A., Lindsey, J.S., Meistrich, M.L., Bucana, C.D., Sanborn, B.M., Joseph, D.R., Griswold, M.D., Cornwall, G.A., et al. 1998. Androgen regulation of the Pem homeodomain gene in mice and rat Sertoli and epididymal cells. J. Androl. 19: 21-30.
33. Tamai, K.T., Monaco, L., Alastalo, T.P., Lalli, E., Parvinen, M., and Sassone-Corsi, P. 1996. Hormonal and developmental regulation of DAX-1 expression in Sertoli cells. Mol. Endocrinol. 10: 1561-1569.
34. Tang, G. 2005. siRNA and miRNA: An insight into RISCs. Trends Biochem. Sci. 30: 106-114.
35. Ventura, A., Meissner, A., Dillon, C.P., McManus, M., Sharp, P.A., Van Parijs, L., Jaenisch, R., and Jacks, T. 2004. Cre-lox-regulated conditional RNA interference from transgenes. Proc. Natl. Acad. Sci. 101: 10380-10385.
36. Wayne, C.M., Sutton, K., and Wilkinson, M.F. 2002. Expression of the Pem homeobox gene in Sertoli cells increases the frequency of adjacent germ cells with deoxyribonucleic acid strand breaks. Endocrinology 143: 4875-4885.
37. Zeng, Y. and Cullen, B.R. 2004. Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 32: 4776-4785.