Analysis of activin/TGFB-signaling modulators within the normal and dysfunctional adult human testis reveals evidence of altered signaling capacity in a subset of seminomas

Reproduction

Volumn 138, Issue 5, 2009, Pages 801-811

  Dias, Vinali L ^a   Rajpert De Meyts, Ewa ^c   McLachlan, Robert ^d   Loveland, Kate Lakoski ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b Australian Government Australian Research Council   (Australia)

^c Rigshospitalet   (Denmark)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; GONADOTROPIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME REGULATION; ENZYME REPRESSION; ENZYME SYNTHESIS; GAMETE; GERM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PUBERTY; SEMINOMA; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS DEVELOPMENT; TESTIS FUNCTION;

ACTIVINS; ADULT; HEALTH; HUMANS; MALE; MODELS, BIOLOGICAL; SEMINOMA; SIGNAL TRANSDUCTION; TESTICULAR DISEASES; TESTICULAR NEOPLASMS; TESTIS; TESTOSTERONE; TRANSFORMING GROWTH FACTOR BETA;

RODENTIA;

EID: 70449475325     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-09-0206     Document Type: Article

References (62)

1. Anderson RA, Cambray N, Hartley PS & McNeilly AS 2002 Expression and localization of inhibin alpha, inhibin/activin betaA and betaB and the activin type II and inhibin beta-glycan receptors in the developing human testis. Reproduction 123 779-788. (Pubitemid 34662054)
2. Andersson AM, Muller J & Skakkebaek NE 1998 Different roles of prepubertal and postpubertal germ cells and Sertoli cells in the regulation of serum inhibin B levels. Journal of Clinical Endocrinology and Metabolism 83 4451-4458. (Pubitemid 29100151)
3. Arora DS, Cooke IE, Ganesan TS, Ramsdale J, Manek S, Charnock FM, Groome NP & Wells M 1997 Immunohistochemical expression of inhibin/activin subunits in epithelial and granulosa cell tumours of the ovary. Journal of Pathology 181 413-418. (Pubitemid 27223527)
4. Bai S & Cao X 2002 A nuclear antagonistic mechanism of inhibitory Smads in transforming growth factor-beta signaling. Journal of Biological Chemistry 277 4176-4182. (Pubitemid 34968679)
5. Barakat B, O'Connor A, Gold E, de Kretser D & Loveland K 2008 Inhibin, activin, follistatin and follicle stimulating hormone serum levels and testicular production are highly modulated during the first spermatogenic wave in mice. Reproduction 136 345-359.
6. Bergstrom R, Adami HO, Mohner M, Zatonski W, Storm H, Ekbom A, Tretli S, Teppo L, Akre O & Hakulinen T 1996 Increase in testicular cancer incidence in six European countries: a birth cohort phenomenon. Journal of National Cancer Institute 88 727-733. (Pubitemid 26195020)
7. Boitani C, Stefanini M, Fragale A & Morena AR 1995 Activin stimulates Sertoli cell proliferation in a defined period of rat testis development. Endocrinology 136 5438-5444.
8. Brown CW, Houston-Hawkins DE, Woodruff TK & Matzuk MM 2000 Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions. Nature Genetics 25 453-457.
9. Caputo S, Couprie J, Duband-Goulet I, Konde E, Lin F, Braud S, Gondry M, Gilquin B, Worman HJ & Zinn-Justin S 2006 The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. Journal of Biological Chemistry 281 18208-18215. (Pubitemid 44035621)
10. Chang H, Brown CW & Matzuk MM 2002 Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocrine Reviews 23 787-823. (Pubitemid 35454589)
11. Cobellis L, Cataldi P, Reis FM, De Palo G, Raspagliesi F, Pilotti S, Arcuri F & Petraglia F 2001 Gonadal malignant germ cell tumors express immunoreactive inhibin/activin subunits. European Journal of Endocrinology 145 779-784. (Pubitemid 33133686)
12. Denissova NG, Pouponnot C, Long J, He D & Liu F 2000 Transforming growth factor beta-inducible independent binding of SMAD to the Smad7 promoter. PNAS 97 6397-6402. (Pubitemid 30412725)
13. Dias V, Meachem S, Rajpert-De Meyts E, McLachlan R, Manuelpillai U & Loveland KL 2008 Activin receptor subunits in normal and dysfunctional adult human testis. Human Reproduction 23 412-420. (Pubitemid 351651241)
14. Dong M, How T, Kirkbride KC, Gordon KJ, Lee JD, Hempel N, Kelly P, Moeller BJ, Marks JR & Blobe GC 2007 The type III TGF-beta receptor suppresses breast cancer progression. Journal of Clinical Investigation 117 206-217. (Pubitemid 46048467)
15. Esparza-Lopez J, Montiel JL, Vilchis-Landeros MM, Okadome T, Miyazono K & Lopez-Casillas F 2001 Ligand binding and functional properties of betaglycan, a co-receptor of the transforming growth factor-beta superfamily. Specialized binding regions for transforming growth factor-beta and inhibin A. Journal of Biological Chemistry 276 14588-14596. (Pubitemid 37373328)
16. Finger EC, Turley RS, Dong M, How T, Fields TA & Blobe GC 2008 TbetaRIII suppresses non-small cell lung cancer invasiveness and tumorigenicity. Carcinogenesis 29 528-535.
17. Fragale A, Puglisi R, Morena AR, Stefanini M & Boitani C 2001 Age-dependent activin receptor expression pinpoints activin A as a physiological regulator of rat Sertoli cell proliferation. Molecular Human Reproduction 7 1107-1114. (Pubitemid 33150205)
18. Gordon KJ, Dong M, Chislock EM, Fields TA & Blobe GC 2008 Loss of type III transforming growth factor beta receptor expression increases motility and invasiveness associated with epithelial to mesenchymal transition during pancreatic cancer progression. Carcinogenesis 29 252-262. (Pubitemid 351359663)
19. Goto K, Kamiya Y, Imamura T, Miyazono K & Miyazawa K 2007 Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors. Journal of Biological Chemistry 282 20603-20611. (Pubitemid 47100044)
20. Groome N & O'Brien M 1993 Immunoassays for inhibin and its subunits. Further applications of the synthetic peptide approach. Journal of Immunological Methods 165 167-176. (Pubitemid 23316403)
21. Hanyu A, Ishidou Y, Ebisawa T, Shimanuki T, Imamura T & Miyazono K 2001 The N domain of Smad7 is essential for specific inhibition of transforming growth factor-beta signaling. Journal of Cell Biology 155 1017-1027. (Pubitemid 34286252)
22. Harrison CA, Wiater E, Gray PC, Greenwald J, Choe S & Vale W 2004 Modulation of activin and BMP signaling. Molecular and Cellular Endocrinology 225 19-24.
23. Harrison CA, Gray PC, Vale WW & Robertson DM 2005 Antagonists of activin signaling: mechanisms and potential biological applications. Trends in Endocrinology and Metabolism 16 73-78.
24. Hellemans J, Preobrazhenska O, Willaert A, Debeer P, Verdonk PC, Costa T, Janssens K, Menten B, Van Roy N, Vermeulen SJ et al. 2004 Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis. Nature Genetics 36 1213-1218.
25. Hempel N, How T, Dong M, Murphy SK, Fields TA & Blobe GC 2007 Loss of betaglycan expression in ovarian cancer: role in motility and invasion. Cancer Research 67 5231-5238. (Pubitemid 46997261)
26. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M & Miyazono K 1997 Smad6 inhibits signaling by the TGF-beta superfamily. Nature 389 622-626. (Pubitemid 27446182)
27. Ishida W, Hamamoto T, Kusanagi K, Yagi K, Kawabata M, Takehara K, Sampath TK, Kato M & Miyazono K 2000 Smad6 is a Smad1/5-induced smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. Journal of Biological Chemistry 275 6075-6079. (Pubitemid 30129890)
28. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H & Nishihara T 1999 Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. Journal of Biological Chemistry 274 13637-13642.
29. Itman C & Loveland KL 2008 SMAD expression in the testis: an insight into BMP regulation of spermatogenesis. Developmental Dynamics 237 97-111.
30. Itman C, Mendis S, Barakat B & Loveland KL 2006 All in the family: TGF-beta family action in testis development. Reproduction 132 233-246. (Pubitemid 44269705)
31. Itman C, Whiley PA, Zhou W, Meistrich M, Sahin Z & Loveland KL 2009 Regulated production of SnoN2 is a feature of testicular differentiation. Microscopy Research and Technique [in press]. DOI: 10.1002/jemt.20739.
32. Itoh S, Landstrom M, Hermansson A, Itoh F, Heldin CH, Heldin NE & ten Dijke P 1998 Transforming growth factor beta1 induces nuclear export of inhibitory Smad7. Journal of Biological Chemistry 273 29195-29201.
33. Kirkbride KC, Townsend TA, Bruinsma MW, Barnett JV & Blobe GC 2008 Bone morphogenetic proteins signal through the transforming growth factor-{beta} type III receptor. Journal of Biological Chemistry 283 7628-7637.
34. Konrad L, Keilani MM, Laible L, Nottelmann U & Hofmann R 2006 Effects of TGF-betas and a specific antagonist on apoptosis of immature rat male germ cells in vitro. Apoptosis 11 739-748. (Pubitemid 43876843)
35. Lewis KA, Gray PC, Blount AL, MacConell LA, Wiater E, Bilezikjian LM & Vale W 2000 Betaglycan binds inhibin and can mediate functional antagonism of activin signaling. Nature 404 411-414. (Pubitemid 30164345)
36. Lin F, Morrison JM, Wu W & Worman HJ 2005 MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling. Human Molecular Genetics 14 437-445. (Pubitemid 40220661)
37. Lin SJ, Lerch TF, Cook RW, Jardetzky TS &Woodruff TK 2006 The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding. Reproduction 132 179-190.
38. Lopez-Casillas F, Wrana JL & Massague J 1993 Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73 1435-1444. (Pubitemid 23201155)
39. Loveland KL & Robertson DM 2005 The TGFβ Superfamily in Sertoli Cell Biology. San Diego, CA, USA: Elsevier Science.
40. Loveland KL, Herszfeld D, Chu B, Rames E, Christy E, Briggs LJ, Shakri R, de Kretser DM & Jans DA 1999 Novel low molecular weight microtubule associated protein-2 isoforms contain a functional nuclear localization sequence. Journal of Biological Chemistry 274 19261-19268. (Pubitemid 129519353)
41. Loveland KL, Bakker M, Meehan T, Christy E, von Schonfeldt V, Drummond A & de Kretser D 2003 Expression of Bambi is widespread in juvenile and adult rat tissues and is regulated in male germ cells. Endocrinology 144 4180-4186. (Pubitemid 37088774)
42. Majdic G, McNeilly AS, Sharpe RM, Evans LR, Groome NP & Saunders PT 1997 Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology 138 2136-2147. (Pubitemid 27180834)
43. Marchetti C, Hamdane M, Mitchell V, Mayo K, Devisme L, Rigot JM, Beauvillain JC, Hermand E & Defossez A 2003 Immunolocalization of inhibin and activin alpha and betaB subunits and expression of corresponding messenger RNAs in the human adult testis. Biology of Reproduction 68 230-235. (Pubitemid 36076341)
44. Mather JP, Attie KM, Woodruff TK, Rice GC & Phillips DM 1990 Activin stimulates spermatogonial proliferation in germ-Sertoli cell cocultures from immature rat testis. Endocrinology 127 3206-3214.
45. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ & Bradley A 1992 Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360 313-319. (Pubitemid 23000668)
46. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R & Bradley A 1995 Functional analysis of activins during mammalian development. Nature 374 354-356.
47. Mazerbourg S, Sangkuhl K, Luo CW, Sudo S, Klein C & Hsueh AJ 2005 Identification of receptors and signaling pathways for orphan bone morphogenetic protein/growth differentiation factor ligands based on genomic analyses. Journal of Biological Chemistry 280 32122-32132. (Pubitemid 41361818)
48. McLachlan RI, O'Donnell L, Stanton PG, Balourdos G, Frydenberg M, de Kretser DM & Robertson DM 2002 Effects of testosterone plus medroxyprogesterone acetate on semen quality, reproductive hormones, and germ cell populations in normal young men. Journal of Clinical Endocrinology and Metabolism 87 546-556. (Pubitemid 34158217)
49. Meehan T, Schlatt S, O'Bryan MK, de Kretser DM & Loveland KL 2000 Regulation of germ cell and Sertoli cell development by activin, follistatin, and FSH. Developmental Biology 220 225-237. (Pubitemid 30228149)
50. Nagarajan RP, Zhang J, Li W & Chen Y 1999 Regulation of Smad7 promoter by direct association with Smad3 and Smad4. Journal of Biological Chemistry 274 33412-33418. (Pubitemid 129511646)
51. Olaso R, Pairault C, Boulogne B, Durand P & Habert R 1998 Transforming growth factor beta1 and beta2 reduce the number of gonocytes by increasing apoptosis. Endocrinology 139 733-740. (Pubitemid 28513225)
52. Pan D, Estevez-Salmeron LD, Stroschein SL, Zhu X, He J, Zhou S & Luo K 2005 The integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-{beta} superfamily of cytokines. Journal of Biological Chemistry 280 15992-16001. (Pubitemid 40616723)
53. Rajpert-de Meyts E & Hoei-Hansen CE 2007 From gonocytes to testicular cancer: the role of impaired gonadal development. Annals of the New York Academy of Sciences 1120 168-180.
54. Rajpert-De Meyts E & Skakkebaek NE 1993 The possible role of sex hormones in the development of testicular cancer. European Urology 23 54-59 discussion 60-151 (Pubitemid 23103460)
55. Roberts VJ 1997 Tissue-specific expression of inhibin/activin subunit and follistatin mRNAs in mid- to late-gestational age human fetal testis and epididymis. Endocrine 6 85-90.
56. Sarraj MA, Chua HK, Umbers A, Loveland KL, Findlay JK & Stenvers KL 2007 Differential expression of TGFBR3 (betaglycan) in mouse ovary and testis during gonadogenesis. Growth Factors 25 334-345. (Pubitemid 351194032)
57. van Schaik RH, Wierikx CD, Looijenga LH, Oosterhuis JW & de Jong FH 1997 Human testicular germ cell tumours express inhibin subunits, activin receptors and follistatin mRNAs. British Journal of Cancer 76 1191-1198.
58. Shi Y & Massague J 2003 Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 685-700. (Pubitemid 36724933)
59. Skakkebaek NE 1972 Possible carcinoma-in-situ of the testis. Lancet 2 516-517.
60. Sonne SB, Hoei-Hansen CE, Nielsen JE, Herlihy AS, Andersson AM, Almstrup K, Daugaard G, Skakkebaek NE, Leffers H & Rajpert-De Meyts E 2006 CDH1 (E-cadherin) in testicular germ cell neoplasia: suppressed translation of mRNA in pre-invasive carcinoma in situ but increased protein levels in advanced tumours. Acta Pathologica, Microbiologica, et Immunologica Scandinavica 114 549-558. (Pubitemid 44252509)
61. Turley RS, Finger EC, Hempel N, How T, Fields TA & Blobe GC 2007 The type III transforming growth factor-beta receptor as a novel tumor suppressor gene in prostate cancer. Cancer Research 67 1090-1098. (Pubitemid 46270765)
62. Vliegen MK, Schlatt S, Weinbauer GF, Bergmann M, Groome NP & Nieschlag E 1993 Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men. Cell Tissue Research 273 261-268. (Pubitemid 23249408)