Tgf/j signaling promotes juvenile granulosa cell tumorigenesis by suppressing apoptosis

Molecular Endocrinology

Volumn 28, Issue 11, 2014, Pages 1887-1898

  Mansouri Attia, NadéRa ^a   Tripurani, Swamy K ^a   Gokul, Nisha ^a   Piard, Hermann ^a   Anderson, Matthew L ^a   Eldin, Karen ^a   Pangas, Stephanie A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; CASPASE 3; CASPASE 7; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; PROTEIN SERINE THREONINE KINASE; SMAD PROTEIN; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER SURVIVAL; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE DELETION; GENE REPRESSION; GRANULOSA CELL TUMOR; HUMAN; HUMAN CELL; IN VIVO STUDY; JUVENILE FORM OF GRANULOSA CELL TUMOR; KNOCKOUT MOUSE; MOUSE; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR VOLUME; ANIMAL; C57BL MOUSE; CELL SURVIVAL; CELL TRANSFORMATION; GENETICS; GRANULOSA CELL; MALE; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; CARCINOGENESIS; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GRANULOSA CELL TUMOR; GRANULOSA CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84908340431     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1217     Document Type: Article

References (62)

1. Schumer ST, Cannistra SA. Granulosa cell tumor of the ovary. J Clin Oncol. 2003;21:1180–1189.
2. Young RH, Dickersin GR, Scully RE. Juvenile granulosa cell tumor of the ovary. A clinicopathological analysis of 125 cases. Am J Surg Pathol. 1984;8:575-596.
3. Jamieson S, Butzow R, Andersson N, et al. The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Mod Pathol. 2010;23:1477-1485.
4. Greenacre CB. Spontaneous tumors of small mammals. Vet Clin North Am Exot Anim Pract. 2004;7:627-651, vi.
5. Liebelt AG, Sass B, Lombard LS. Mouse ovarian tumors—a review including classification and induction of neoplastic lesions and description of several previously unreported types. J Exp Pathol. 1987;3:115-145.
6. Shah SP, Köbel M, Senz J, et al. Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med. 2009;360:2719-2729.
7. Pangas SA, Li X, Umans L, et al. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol. 2008;28:248-257.
8. Middlebrook BS, Eldin K, Li X, Shivasankaran S, Pangas SA. Smad1-Smad5 ovarian conditional knockout mice develop a disease profile similar to the juvenile form of human granulosa cell tumors. Endocrinology. 2009;150:5208-5217.
9. Coerver KA, Woodruff TK, Finegold MJ, Mather J, Bradley A, Matzuk MM. Activin signaling through activin receptor type II causes the cachexia-like symptoms in inhibin-deficient mice. Mol Endocrinol. 1996;10:534-543.
10. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. A-Inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature. 1992;360:313-319.
11. Shi Y, Massagué J. Mechanisms of TGF-/3 signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
12. Massagué J. TGF/3 signalling in context. Nat Rev Mol Cell Biol. 2012;13:616-630.
13. Li Q, Graff JM, O’Connor AE, Loveland KL, Matzuk MM. SMAD3 regulates gonadal tumorigenesis. Mol Endocrinol. 2007; 21:2472-2486.
14. Hill CS. Nucleocytoplasmic shuttling of Smad proteins. Cell Res. 2009;19:36-46.
15. Pangas SA, Li X, Robertson EJ, Matzuk MM. Premature luteiniza-tion and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol Endocrinol. 2006;20:1406-1422.
16. Nagaraja AK, Middlebrook BS, Rajanahally S, et al. Defective go-nadotropin-dependent ovarian folliculogenesis and granulosa cell gene expression in inhibin-deficient mice. Endocrinology. 2010; 151:4994-5006.
17. Cheng G, Weihua Z, Mäkinen S, et al. A role for the androgen receptor in follicular atresia of estrogen receptor /3 knockout mouse ovary. Biol Reprod. 2002;66:77-84.
18. Hu YC, Wang PH, Yeh S, et al. Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci USA. 2004;101:11209-11214.
19. Tripurani SK, Cook RW, Eldin KW, Pangas SA. BMP-specific SMADs function as novel repressors of PDGFA and modulate its expression in ovarian granulosa cells and tumors. Oncogene. 2013; 32:3877-3885.
20. DaCosta Byfield S, Major C, Laping NJ, Roberts AB. SB-505124 is a selective inhibitor of transforming growth factor-/3 type I receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 2004;65:744-752.
21. Vogt J, Traynor R, Sapkota GP. The specificities of small molecule inhibitors of the TGF/3 and BMP pathways. Cell Signal. 2011;23: 1831-1842.
22. Wu TH, Chou YW, Chiu PH, Tang MJ, Hu CW, Yeh ML. Validation of the effects of TGF-/31 on tumor recurrence and prognosis through tumor retrieval and cell mechanical properties. Cancer Cell Int. 2014;14:20.
23. Remst DF, Blaney Davidson EN, Vitters EL, et al. TGF-/3 induces lysyl hydroxylase 2b in human synovial osteoarthritic fibroblasts through ALK5 signaling. Cell Tissue Res. 2014;355:163-171.
24. Von Zee CL, Langert KA, Stubbs EB Jr. Transforming growth factor-/32 induces synthesis and secretion of endothelin-1 in human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2012;53: 5279-5286.
25. Buckley S, Shi W, Barsky L, Warburton D. TGF-/3 signaling promotes survival and repair in rat alveolar epithelial type 2 cells during recovery after hyperoxic injury. Am J Physiol Lung Cell Mol Physiol. 2008;294:L739-L748.
26. Noma K, Smalley KS, Lioni M, et al. The essential role of fibroblasts in esophageal squamous cell carcinoma-induced angiogenesis. Gastroenterology. 2008;134:1981-1993.
27. Jamin SP, Arango NA, Mishina Y, et al. Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat Genet. 2002;32:408-410.
28. Cheifetz S, Hernandez H, Laiho M, ten Dijke P, Iwata KK, Mas-sagué J. Distinct transforming growth factor-/3 (TGF-/3) receptor subsets as determinants of cellular responsiveness to three TGF-/3 isoforms. J Biol Chem. 1990;265:20533-20538.
29. Bilandzic M, Chu S, Farnworth PG, et al. Loss of betaglycan contributes to the malignant properties of human granulosa tumor cells. Mol Endocrinol. 2009;23:539-548.
30. Li Q, Kumar R, Underwood K, et al. Prevention of cachexia-like syndrome development and reduction of tumor progression in in-hibin-deficient mice following administration of a chimeric activin receptor type II-murine Fc protein. Mol Hum Reprod. 2007;13: 675-683.
31. Bilandzic M, Chu S, Wang Y, et al. Betaglycan alters NFkB-TGF/32 cross talk to reduce survival of human granulosa tumor cells. Mol Endocrinol. 2013;27:466-479.
32. Cohen GM. Caspases: the executioners of apoptosis. Biochem J. 1997;326(Pt 1):1-16.
33. Findlay JK, Drummond AE, Dyson ML, Baillie AJ, Robertson DM, Ethier JF. Recruitment and development of the follicle; the roles of the transforming growth factor-/3 superfamily. Mol Cell Endocrinol. 2002;191:35-43.
34. Pangas SA. Bone morphogenetic protein signaling transcription factor (SMAD) function in granulosa cells. Mol Cell Endocrinol. 2012; 356:40-47.
35. Myers M, Pangas SA. Regulatory roles of transforming growth factor /3 family members in folliculogenesis. Wiley Interdiscip Rev Syst Biol Med. 2010;2:117-125.
36. Thompson TB, Lerch TF, Cook RW, Woodruff TK, Jardetzky TS. The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev Cell. 2005;9:535-543.
37. Knight PG, Glister C. TGF-/3 superfamily members and ovarian follicle development. Reproduction. 2006;132:191-206.
38. Glister C, Kemp CF, Knight PG. Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction. 2004;127: 239-254.
39. De Crescenzo G, Hinck CS, Shu Z, et al. Three key residues underlie the differential affinity of the TGF/3 isoforms for the TGF/3 type II receptor. J Mol Biol. 2006;355:47-62.
40. Olsson M, Zhivotovsky B. Caspases and cancer. Cell Death Differ. 2011;18:1441-1449.
41. Boulares AH, Zoltoski AJ, Contreras FJ, Yakovlev AG, Yoshihara K, Smulson ME. Regulation of DNAS1L3 endonuclease activity by poly(ADP-ribosyl)ation during etoposide-induced apoptosis. Role of poly(ADP-ribose) polymerase-1 cleavage in endonuclease activation. J Biol Chem. 2002;277:372-378.
42. Pangas SA, Woodruff TK. Production and purification of recombinant human inhibin and activin. J Endocrinol. 2002;172:199-210.
43. Martens JW, de Winter JP, Timmerman MA, et al. Inhibin interferes with activin signaling at the level of the activin receptor complex in Chinese hamster ovary cells. Endocrinology 1997;138: 2928-2936.
44. Lebrun JJ, Vale WW. Activin and inhibin have antagonistic effects on ligand-dependent heteromerization of the type I and type II activin receptors and human erythroid differentiation. Mol Cell Biol. 1997;17:1682-1691.
45. Iemura S, Yamamoto TS, Takagi C, et al. Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc Natl Acad Sci USA. 1998;95:9337-9342.
46. Wolfraim LA, Fernandez TM, Mamura M, et al. Loss of Smad3 in acute T-cell lymphoblastic leukemia. NEnglJMed. 2004;351:552-559.
47. Maliekal TT, Antony ML, Nair A, Paulmurugan R, Karunagaran D. Loss of expression, and mutations of Smad 2 and Smad 4 in human cervical cancer. Oncogene. 2003;22:4889-4897.
48. Hahn SA, Schutte M, Hoque AT, et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science. 1996; 271:350-353.
49. Xu X, Brodie SG, Yang X, et al. Haploid loss of the tumor suppressor Smad4/Dpc4 initiates gastric polyposis and cancer in mice. Oncogene. 2000;19:1868-1874.
50. Schutte M. DPC4/SMAD4 gene alterations in human cancer, and their functional implications. Ann Oncol. 1999;10(suppl 4):56-59.
51. Takei K, Kohno T, Hamada K, et al. A novel tumor suppressor locus on chromosome 18q involved in the development of human lung cancer. Cancer Res. 1998;58:3700-3705.
52. Yu C, Zhang YL, Fan HY. Selective Smad4 knockout in ovarian preovulatory follicles results in multiple defects in ovulation. Mol Endocrinol. 2013;27:966-978.
53. Koinuma D, Tsutsumi S, Kamimura N, Imamura T, Aburatani H, Miyazono K. Promoter-wide analysis of Smad4 binding sites in human epithelial cells. Cancer Sci. 2009;100:2133-2142.
54. Kennedy BA, Deatherage DE, Gu F, et al. ChIP-seq defined genome-wide map of TGF/3/SMAD4 targets: implications with clinical outcome of ovarian cancer. PLoS One. 2011;6:e22606.
55. Wang W, Chen X, Li X, et al. Interference RNA-based silencing of endogenous SMAD4 in porcine granulosa cells resulted in decreased FSH-mediated granulosa cells proliferation and steroidogenesis. Reproduction. 2011;141:643-651.
56. Wang W, Wang L, Li XX, et al. Effect of interrupted endogenous BMP/Smad signaling on growth and steroidogenesis of porcine granulosa cells. J Zhejiang Univ Sci B. 2010;11:719-727.
57. Park SM, Jung JS, Jang MS, Kang KS, Kang SK. Transforming growth factor-/31 regulates the fate of cultured spinal cord-derived neural progenitor cells. Cell Prolif. 2008;41:248-264.
58. Teramoto T, Kiss A, Thorgeirsson SS. Induction of p53 and Bax during TGF-/31 initiated apoptosis in rat liver epithelial cells. Biochem Biophys Res Commun. 1998;251:56-60.
59. /ow cells that express Bcl-2 at a low level. Exp Hematol. 2001;29:1098-1108.
60. Wicik Z, Sadkowski T, Jank M, Motyl T. Transcriptional pattern of TGF-/31 inhibitory effect on mouse C2C12 myoblasts differentiation. Pol J Vet Sci. 2010;13:629-638.
61. Yao G, Yin M, Lian J, et al. MicroRNA-224 is involved in transforming growth factor-β-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol Endocrinol. 2010;24:540-551.
62. Zhang Y, Takahashi S, Tasaka A, Yoshima T, Ochi H, Chayama K. Involvement of microRNA-224 in cell proliferation, migration, invasion, and anti-apoptosis in hepatocellular carcinoma. J Gastroenterol Hepatol. 2013;28:565-575.