Increased gene copy number of VAMP7 disrupts human male urogenital development through altered estrogen action

Nature Medicine

Volumn 20, Issue 7, 2014, Pages 715-724

  Tannour Louet, Mounia ^a,b   Han, Shuo ^a   Louet, Jean Francois ^a,c   Zhang, Bin ^a   Romero, Karina ^a   Addai, Josephine ^a   Sahin, Aysegul ^a   Cheung, Sau Wai ^a   Lamb, Dolores J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CNRS   (France)

^c CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIRTH DEFECT; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CRYPTORCHISM; DEVELOPMENT; ESTROGEN ACTIVITY; FEMALE; GENE; GENE DOSAGE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOSPADIAS; MALE; MALE GENITAL TRACT MALFORMATION; MALE UROGENITAL DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON MOTILITY; SUBFERTILITY; TRANSGENIC MOUSE; UPREGULATION; URETHRA DISEASE; URETHRAL DEFECT; VAMP7 GENE; VIRILIZATION;

BACTERIA (MICROORGANISMS); MUS MUSCULUS;

ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FERTILITY; GENE DOSAGE; HUMANS; MALE; MICE; MICE, TRANSGENIC; R-SNARE PROTEINS; RECEPTORS, ANDROGEN; UROGENITAL SYSTEM;

EID: 84904054043     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3580     Document Type: Article

References (60)

1. Sharpe, R.M. & Skakkebaek, N.E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 341, 1392-1395 (1993).
2. Wilhelm, D. & Koopman, P. The makings of maleness: towards an integrated view of male sexual development. Nat. Rev. Genet. 7, 620-631 (2006).
3. Vidaeff, A.C. & Sever, L.E. In utero exposure to environmental estrogens and male reproductive health: a systematic review of biological and epidemiologic evidence. Reprod. Toxicol. 20, 5-20 (2005).
4. Storgaard, L., Bonde, J.P. & Olsen, J. Male reproductive disorders in humans and prenatal indicators of estrogen exposure. A review of published epidemiological studies. Reprod. Toxicol. 21, 4-15 (2006).
5. Mc Lachlan, J.A., Newbold, R.R. & Bullock, B. Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol. Science 190, 991-992 (1975).
6. Goyal, H.O. et al. Estrogen receptor α mediates estrogen-inducible abnormalities in the developing penis. Reproduction 133, 1057-1067 (2007).
7. Goyal, H.O., Braden, T.D., Williams, C.S. & Williams, J.W. Estrogen-induced developmental disorders of the rat penis involve both estrogen receptor (ESR)- and androgen receptor (AR)-mediated pathways. Biol. Reprod. 81, 507-516 (2009).
8. Simon, L. et al. Exposure of neonatal rats to anti-androgens induces penile mal-developments and infertility comparable to those induced by oestrogens. Int. J. Androl. 35, 364-376 (2012).
9. Li, X. et al. Altered structure and function of reproductive organs in transgenic male mice overexpressing human aromatase. Endocrinology 142, 2435-2442 (2001).
10. Kloepper, T.H., Kienle, C.N. & Fasshauer, D. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18, 3463-3471 (2007).
11. Pryor, P.R. et al. Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the Arf GAP Hrb. Cell 134, 817-827 (2008).
12. Pryor, P.R. et al. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 5, 590-595 (2004).
13. Advani, R.J. et al. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146, 765-776 (1999).
14. Rao, S.K., Huynh, C., Proux-Gillardeaux, V., Galli, T. & Andrews, N.W. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J. Biol. Chem. 279, 20471-20479 (2004).
15. Fader, C.M., Sanchez, D.G., Mestre, M.B. & Colombo, M.I. TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta 1793, 1901-1916 (2009).
16. Moreau, K., Ravikumar, B., Renna, M., Puri, C. & Rubinsztein, D.C. Autophagosome precursor maturation requires homotypic fusion. Cell 146, 303-317 (2011).
17. Tannour-Louet, M. et al. Identification of de novo copy number variants associated with human disorders of sexual development. PLo S ONE 5, e15392 (2010).
18. Shono, T. et al. Scanning electron microscopy shows inhibited gubernacular development in relation to undescended testes in oestrogen-treated mice. Int. J. Androl. 19, 263-270 (1996).
19. Nef, S., Shipman, T. & Parada, L.F. A molecular basis for estrogen-induced cryptorchidism. Dev. Biol. 224, 354-361 (2000).
20. Jiang, X.W., Li, J.H., Huang, T.H. & Deng, W.D. Effect of prenatal exposure to diethylstilbestrol on gubernacular development in fetal male mice. Asian J. Androl. 6, 325-329 (2004).
21. Cederroth, C.R. et al. Estrogen receptor α is a major contributor to estrogen-mediated fetal testis dysgenesis and cryptorchidism. Endocrinology 148, 5507-5519 (2007).
22. Kent, H.M. et al. Structural basis of the intracellular sorting of the SNARE VAMP7 by the AP3 adaptor complex. Dev. Cell 22, 979-988 (2012).
23. Magee, J.A., Chang, L.W., Stormo, G.D. & Milbrandt, J. Direct, androgen receptor-mediated regulation of the FKBP5 gene via a distal enhancer element. Endocrinology 147, 590-598 (2006).
24. Makkonen, H., Kauhanen, M., Paakinaho, V., Jaaskelainen, T. & Palvimo, J.J. Long-range activation of FKBP51 transcription by the androgen receptor via distal intronic enhancers. Nucleic Acids Res. 37, 4135-4148 (2009).
25. Chen, H. et al. Fkbp52 regulates androgen receptor transactivation activity and male urethra morphogenesis. J. Biol. Chem. 285, 27776-27784 (2010).
26. Nishida, H. et al. Gene expression analyses on embryonic external genitalia: identification of regulatory genes possibly involved in masculinization processes. Congenit. Anom. (Kyoto) 48, 63-67 (2008).
27. Miyagawa, S. et al. The role of sonic hedgehog-Gli2 pathway in the masculinization of external genitalia. Endocrinology 152, 2894-2903 (2011).
28. Rivas, A., Fisher, J.S., Mc Kinnell, C., Atanassova, N. & Sharpe, R.M. Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 143, 4797-4808 (2002).
29. Wang, Z. et al. Up-regulation of estrogen responsive genes in hypospadias: microarray analysis. J. Urol. 177, 1939-1946 (2007).
30. Liu, B. et al. Estradiol upregulates activating transcription factor 3, a candidate gene in the etiology of hypospadias. Pediatr. Dev. Pathol. 10, 446-454 (2007).
31. Liu, B. et al. Activating transcription factor 3 is up-regulated in patients with hypospadias. Pediatr. Res. 58, 1280-1283 (2005).
32. Liu, B., Agras, K., Willingham, E., Vilela, M.L. & Baskin, L.S. Activating transcription factor 3 is estrogen-responsive in utero and upregulated during sexual differentiation. Horm. Res. 65, 217-222 (2006).
33. Gurbuz, C. et al. Is activating transcription factor 3 up-regulated in patients with hypospadias? Korean J. Urol. 51, 561-564 (2010).
34. Kalfa, N. et al. Genomic variants of ATF3 in patients with hypospadias. J. Urol. 180, 2183-2188, discussion 2188 (2008).
35. Beleza-Meireles, A. et al. Activating transcription factor 3: a hormone responsive gene in the etiology of hypospadias. Eur. J. Endocrinol. 158, 729-739 (2008).
36. Thenot, S., Charpin, M., Bonnet, S. & Cavailles, V. Estrogen receptor cofactors expression in breast and endometrial human cancer cells. Mol. Cell. Endocrinol. 156, 85-93 (1999).
37. Lambard, S. et al. Aromatase in testis: expression and role in male reproduction. J. Steroid Biochem. Mol. Biol. 95, 63-69 (2005).
38. Song, W.C., Qian, Y., Sun, X. & Negishi, M. Cellular localization and regulation of expression of testicular estrogen sulfotransferase. Endocrinology 138, 5006-5012 (1997).
39. Hazary, S. & Gardner, W.U. Influence of sex hormones on abdominal musculature and the formation of inguinal and scrotal hernias in mice. Anat. Rec. 136, 437-443 (1960).
40. Reinert, R.B. et al. Tamoxifen-induced Cre-loxP recombination is prolonged in pancreatic islets of adult mice. PLo S ONE 7, e33529 (2012).
41. Li, X. & Rahman, N. Impact of androgen/estrogen ratio: lessons learned from the aromatase over-expression mice. Gen. Comp. Endocrinol. 159, 1-9 (2008).
42. Wang, H. et al. The stress response mediator ATF3 represses androgen signaling by binding the androgen receptor. Mol. Cell. Biol. 32, 3190-3202 (2012).
43. Girirajan, S., Campbell, C.D. & Eichler, E.E. Human copy number variation and complex genetic disease. Annu. Rev. Genet. 45, 203-226 (2011).
44. Ferlin, A. et al. Genetic alterations associated with cryptorchidism. J. Am. Med. Assoc. 300, 2271-2276 (2008).
45. Hadziselimovic, F. et al. EGR4 is a master gene responsible for fertility in cryptorchidism. Sex Dev. 3, 253-263 (2009).
46. Hadziselimovic, F., Hadziselimovic, N.O., Demougin, P. & Oakeley, E.J. Testicular gene expression in cryptorchid boys at risk of azoospermia. Sex Dev. 5, 49-59 (2011).
47. Mills, I.G. et al. Huntingtin interacting protein 1 modulates the transcriptional activity of nuclear hormone receptors. J. Cell Biol. 170, 191-200 (2005).
48. Ray, M.R. et al. Cyclin G-associated kinase: a novel androgen receptor-interacting transcriptional coactivator that is overexpressed in hormone refractory prostate cancer. Int. J. Cancer 118, 1108-1119 (2006).
49. Jasavala, R. et al. Identification of putative androgen receptor interaction protein modules: cytoskeleton and endosomes modulate androgen receptor signaling in prostate cancer cells. Mol. Cell. Proteomics 6, 252-271 (2007).
50. Kang, J. et al. A nuclear function of β-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 123, 833-847 (2005).
51. Yang, L. et al. APPL suppresses androgen receptor transactivation via potentiating Akt activity. J. Biol. Chem. 278, 16820-16827 (2003).
52. Enari, M., Ohmori, K., Kitabayashi, I. & Taya, Y. Requirement of clathrin heavy chain for p53-mediated transcription. Genes Dev. 20, 1087-1099 (2006).
53. Wei, X., Xu, H. & Kufe, D. MUC1 oncoprotein stabilizes and activates estrogen receptor α. Mol. Cell 21, 295-305 (2006).
54. Reid, G. et al. Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11, 695-707 (2003).
55. Lonard, D.M., Nawaz, Z., Smith, C.L. & O'Malley, B.W. The 26S proteasome is required for estrogen receptor-α and coactivator turnover and for efficient estrogen receptor-α transactivation. Mol. Cell 5, 939-948 (2000).
56. Nawaz, Z., Lonard, D.M., Dennis, A.P., Smith, C.L. & O'Malley, B.W. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. USA 96, 1858-1862 (1999).
57. Korolchuk, V.I., Menzies, F.M. & Rubinsztein, D.C. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 584, 1393-1398 (2010).
58. Korolchuk, V.I., Mansilla, A., Menzies, F.M. & Rubinsztein, D.C. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol. Cell 33, 517-527 (2009).
59. Ou, Z. et al. Branchiootorenal syndrome and oculoauriculovertebral spectrum features associated with duplication of SIX1, SIX6, and OTX2 resulting from a complex chromosomal rearrangement. Am. J. Med. Genet. A 146A, 2480-2489 (2008).
60. Ou, Z. et al. Bacterial artificial chromosome-emulation oligonucleotide arrays for targeted clinical array-comparative genomic hybridization analyses. Genet. Med. 10, 278-289 (2008). Diseases