Novel genes modulated by FSH in normal and immortalized FSH-responsive cells: New insights into the mechanism of FSH action

FASEB Journal

Volumn 17, Issue 10, 2003, Pages 1256-1266

  Sasson, Ravid ^a   Dantes, Ada ^a   Tajima, Kimihisa ^a   Amsterdam, Abraham ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Apoptosis; DNA microarray; Granzyme; Human granulosa cells; Ovary; Steroidogenesis

Indexed keywords

ACID PHOSPHATASE PROSTATE ISOENZYME; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANGIOGENIC FACTOR; CARBOXYPEPTIDASE H; DECAY ACCELERATING FACTOR; DNA; FOLLITROPIN; FOLLITROPIN RECEPTOR; GRANZYME A; GRANZYME LIKE PROTEIN 1; GRANZYME LIKE PROTEIN 3; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; NATURAL KILLER CELL PROTEASE 1; OXIDATIVE STRESS INDUCIBLE PROTEIN TYROSINE PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1B; PROTEIN RGS16; PROTEIN TYROSINE PHOSPHATASE; PROTEINASE; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMINO ACID SEQUENCE; ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL COMMUNICATION; CELL IMMORTALIZATION; CELL MATURATION; CELL STIMULATION; CELL TRANSFORMATION; CONTROLLED STUDY; DNA MICROARRAY; ENZYME REGULATION; FOLLITROPIN RELEASE; GENE EXPRESSION REGULATION; GENE ISOLATION; GRANULOSA CELL; HORMONE RESPONSE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; ION TRANSPORT; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROBABILITY; PROCESS DEVELOPMENT; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; STEROIDOGENESIS; UNINDEXED SEQUENCE;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL COMMUNICATION; CELL LINE, TRANSFORMED; CELLS, CULTURED; CYTOKINES; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GRANULOSA CELLS; GROWTH SUBSTANCES; HUMANS; NERVOUS SYSTEM PHYSIOLOGY; PEPTIDE HYDROLASES; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASES; RATS; SIGNAL TRANSDUCTION; STEROIDS;

MAMMALIA;

EID: 0038122824     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.02-0740com     Document Type: Article

References (80)

1. Amsterdam, A., Rotmensch, S., and Ben-Ze'ev, A. (1989) Coordinated regulation of morphological and biochemical differentiation in a steroidogenic cell: the granulosa cell model. Trends Biochem. Sci. 14, 377-382
2. Amsterdam, A., and Selvaraj, N. (1997) Control of differentiation, transformation, and apoptosis in granulosa cells by oncogenes, oncoviruses, and tumor suppressor genes. Endocr. Rev. 18, 435-461
3. Amsterdam, A., Gold, R. S., Hosokawa, K., Yoshida, Y., Sasson, R., Jung, Y., and Kotsuji, F. (1999) Crosstalk among multiple signaling pathways controlling ovarian cell death. Trends Endocrinol. Metab. 10, 255-262
4. Robker, R. L., Russell, D. L., Yoshioka, S., Sharma, S. C., Lydon, J. P., O'Malley, B. W., Espey, L. L., and Richards, J. S. (2000) Ovulation: a multi-gene, multi-step process. Steroids 65, 559-570
5. Gebauer, H., Lindner, H. R., and Amsterdam, A. (1978) Synthesis of heparin-like glycosaminoglycans in rat ovarian slices. Biol. Reprod. 18, 350-358
6. Albertini, D. F., and Anderson, E. (1974) The appearance and structure of intercellular connections during the ontogeny of the rabbit ovarian follicle with particular reference to gap junctions. J. Cell Biol. 63, 234-250
7. Amsterdam, A., Josephs, R., Lieberman, M. E., and Lindner, H. R. (1976) Organization of intramembrane particles in freeze-cleaved gapjunctions of rat graafian follicles: optical-diffraction analysis. J. Cell Sci. 21, 93-105
8. Richards, J. S. (2001) New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol. Endocrinol. 15, 209-218
9. Leo, C. P., Pisarska, M. D., and Hsueh, A. J. (2001) DNA array analysis of changes in preovulatory gene expression in the rat ovary. Biol. Reprod. 65, 269-276
10. Morohashi, K. I., and Omura, T. (1996) Ad4BP/SF-1, a transcription factor essential for the transcription of steroidogenic cytochrome P450 genes and for the establishment of the reproductive function. FASEB J. 10, 1569-1577
11. Omura, T., and Morohashi, K. (1995) Gene regulation of steroidogenesis. J. Steroid Biochem. Mol. Biol. 53, 19-25
12. Amsterdam, A., and Rotmensch, S. (1987) Structure-function relationships during granulosa cell differentiation. Endocr. Rev. 8, 309-337
13. Amsterdam, A., Hanoch, T., Dantes, A., Kimihisa, T., Strauss, I. J., and Seger, R. (2002) Mechanisms of gonadtropin desensitization. Mol. Cell. Endocrinol. 187, 69-74
14. Amsterdam, A., Koch, Y., Lieberman, M. E., and Lindner, H. R. (1975) Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J. Cell Biol. 67, 894-900
15. Amsterdam, A., Zauberman, A., Meir, G., Pinhasi-Kimhi, O., Suh, B. S., and Oren, M. (1988) Cotransfection of granulosa cells with simian virus 40 and Ha-RAS oncogene generates stable lines capable of induced steroidogenesis. Proc. Natl. Acad. Sci. USA 85, 7582-7586
16. Hanukoglu, I., Suh, B. S., Himmelhoch, S., and Amsterdam, A. (1990) Induction and mitochondrial localization of cytochrome P450scc system enzymes in normal and transformed ovarian granulosa cells. J. Cell Biol. 111, 1373-1381
17. Suh, B. S., Sprengel, R., Keren-Tal, I., Himmelhoch, S., and Amsterdam, A. (1992) Introduction of a gonadotropin receptor expression plasmid into immortalized granulosa cells leads to reconstitution of hormone-dependent steroidogenesis. J. Cell Biol. 119, 439-450
18. Keren-Tal, I., Dantes, A., Sprengel, R., and Amsterdam, A. (1993) Mol. Cell. Endocrinol. 95, R1-R10
19. Keren-Tal, I., Suh, B. S., Dantes, A., Lindner, S., Oren, M., and Amsterdam, A. (1995) Establishment of steroidogenic granulosa cell lines expressing follicle stimulating hormone receptors. Involvement of p53 expression in cAMP-mediated apoptosis in immortalized granulosa cells. Exp. Cell Res. 218, 283-295
20. Amsterdam, A., Keren-Tal, I., Dantes, A., Matityahou, A., and Plehn-Dujowich, D. (1993) In The Ovary, Chapt. 24 (Adashi, E. Y., and Leung, P. C. K., eds) pp. 487-500, Raven Press Ltd., New York
21. Hosokawa, K., Aharoni, D., Dantes, A., Shaulian, E., Schere-Levy, C., Atzmon, R., Kotsuji, F., Oren, M., Vlodavsky, I., and Amsterdam, A. (1998) Modulation of Mdm2 expression and p53-induced apoptosis in immortalized human ovarian granulosa cells. Endocrinology 139, 4688-4700
22. Hosokawa, K., Dantes, A., Schere-Levy, C., Barash, A., Yoshida, Y., Kotsuji, F., Vlodavsky, I., and Amsterdam, A. (1998) Induction of Ad4BP/SF-1, steroidogenic acute regulatory protein, and cytochrome P450scc enzyme system expression in newly established human granulosa cell lines. Endocrinology 139, 4679-4687
23. Tajima, K., Hosokawa, K., Yoshida, Y., Dantes, A., Sasson, R., Kotsuji, F., and Amsterdam, A. (2002) Establishment of FSH-responsive cell lines by transfection of pre-ovulatory human granulosa cells with mutated p53 (p53val135) and Ha-ras genes. Mol. Hum. Reprod. 8, 48-57
24. Keren-Tal, I., Dantes, A., Plehn-Dujowich, D., and Amsterdam, A. (1997) Association of Ad4BP/SF-1 transcription factor with steroidogenic activity in oncogene-transformed granulosa cells. Mol. Cell. Endocrinol. 127, 49-57
25. Sommersberg, B., Bulling, A., Salzer, U., Frohlich, U., Garfield, R. E., Amsterdam, A., and Mayerhofer, A. (2000) Gap junction communication and connexin 43 gene expression in a rat granulosa cell line: regulation by follicle-stimulating hormone. Biol. Reprod. 63, 1661-1668
26. Shukovski, L., Keren-Tal, I., Dantes, A., and Amsterdam, A. (1995) Regulation of follistatin messenger ribonucleic acid in steroidogenic rat granulosa cell lines. Endocrinology 136, 2889-2895
27. Grosse, J., Bulling, A., Brucker, C., Berg, U., Amsterdam, A., Mayerhofer, A., and Gratzl, M. (2000) Synaptosome-associated protein of 25 kilodaltons in oocytes and steroid-producing cells of rat and human ovary: molecular analysis and regulation by gonadotropins. Biol. Reprod. 63, 643-650
28. Fritz, S., Wessler, I., Breitling, R., Rossmanith, W., Ojeda, S. R., Dissen, G. A., Amsterdam, A., and Mayerhofer, A. (2001) Expression of muscarinic receptor types in the primate ovary and evidence for nonneuronal acetylcholine synthesis. J. Clin. Endocrinol. Metab. 86, 349-354
29. Breckwoldt, M., Selvaraj, N., Aharoni, D., Barash, A., Segal, I., Insler, V., and Amsterdam, A. (1996) Expression of Ad4-BP/cytochrome P450 side chain cleavage enzyme and induction of cell death in long-term cultures of human granulosa cells. Mol. Hum. Reprod. 2, 391-400
30. Sasson, R., and Amsterdam, A. (2002) Stimulation of apoptosis in human granulosa cells from in vitro fertilization patients and its prevention by dexamethasone: involvement of cell contact and bcl-2 expression. J. Clin. Endocrinol. Metab. 87, 3441-3451
31. Shastri, N., and Gonzalez, F. (1993) Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells. J. Immunol. 150, 2724-2736
32. Sasson, R., Tajima, K., and Amsterdam, A. (2001) Glucocorticoids protect against apoptosis induced by serum deprivation, cyclic adenosine 3′,5′-monophosphate and p53 activation in immortalized human granulosa cells: involvement of Bcl-2. Endocrinology 142, 802-811
33. Amsterdam, A., Plehn-Dujowich, D., and Suh, B. S. (1992) Structure-function relationships during differentiation of normal and oncogene-transformed granulosa cells. Biol. Reprod. 46, 513-522
34. Rennert, H., Amsterdam, A., Billheimer, J. T., and Strauss, J. F., III (1991) Regulated expression of sterol carrier protein 2 in the ovary: a key role for cyclic AMP. Biochemistry 30, 11280-11285
35. Suh, B. S., and Amsterdam, A. (1990)) Establishment of highly steroidogenic granulosa cell lines by cotransfection with SV40 and Ha-ras oncogene: induction of steroidogenesis by cyclic adenosine 3′-5′-monophosphate and its suppression by phorbol ester. Endocrinology 127, 2489-2500
36. Grigorenko, V. G., Yarovoi, S. V., Paulauskaite, R., and Amerik, A. (1994) Cloning of cDNA for granzyme-like protein III, a novel serine proteinase from rat duodenum. FEBS Lett. 342, 278-280
37. Zunino, S. J., Bleackley, R. C., Martinez, J., and Hudig, D. (1990) RNKP-1, a novel natural killer-associated serine protease gene cloned from RNK-16 cytotoxic lymphocytes. J. Immunol. 144, 2001-2009
38. Shi, L., Kraut, R. P., Aebersold, R., and Greenberg, A. H. (1992) A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175, 553-566
39. Wang, G. Q., Wieckowski, E., Goldstein, L. A., Gastman, B. R., Rabinovitz, A., Gambotto, A., Li, S., Fang, B., Yin, X. M., and Rabinowich, H. (2001) Resistance to granzyme B-mediated cytochrome c release in Bak-deficient cells. J. Exp. Med. 194, 1325-1337
40. Berke, G. (1995) The CTL's kiss of death. Cell 81, 9-12
41. Pham, C. T., and Ley, T. J. (1999) Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. USA 96, 8627-8632
42. Aharoni, D., Dantes, A., Oren, M., and Amsterdam, A. (1995) cAMP-mediated signals as determinants for apoptosis in primary granulosa cells. Exp. Cell Res. 218, 271-282
43. Sun, J., Ooms, L., Bird, C. H., Sutton, V. R., Trapani, J. A., and Bird, P. I. (1997) A new family of 10 murine ovalbumin serpins includes two homologs of proteinase inhibitor 8 and two homologs of the granzyme B inhibitor (proteinase inhibitor 9). J. Biol. Chem. 272, 15434-15441
44. Bladergroen, B. A., Strik, M. C., Bovenschen, N., van Berkum, O., Scheffer, G. L., Meijer, C.J., Hack, C. E., and Kummer, J. A. (2001) The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J. Immunol. 166, 3218-3225
45. Liu, H. C., He, Z., and Rosenwaks, Z. (2001) Application of complementary DNA microarray (DNA chip) technology in the study of gene expression profiles during folliculogenesis. Fertil. Steril. 75, 947-955
46. Cool, D. R., and Loh, Y. P. (1998) Carboxypeptidase E is a sorting receptor for prohormones: binding and kinetic studies. Mol. Cell. Endocrinol. 139, 7-13
47. Fricker, L. D., Adelman, J. P., Douglass, J., Thompson, R. C., von Strandmann, R. P., and Hutton, J. (1989) Isolation and sequence analysis of cDNA for rat carboxypeptidase E [EC 3.4.17.10], a neuropeptide processing enzyme. Mol. Endocrinol. 3, 666-673
48. Conn, G., Bayne, M. L., Soderman, D. D., Kwok, P. W., Sullivan, K. A., Palisi, T. M., Hope, D. A., and Thomas, K. A. (1990) Amino acid and cDNA sequences of a vascular endothelial cell mitogen that is homologous to platelet-derived growth factor. Proc. Natl. Acad. Sci. USA 87, 2628-2632
49. Neulen, J., Raczek, S., Pogorzelski, M., Grunwald, K., Yeo, T. K., Dvorak, H. F., Weich, H. A., and Breckwoldt, M. (1998) Secretion of vascular endothelial growth factor/vascular permeability factor from human luteinized granulosa cells is human chorionic gonadotrophin dependent. Mol. Hum. Reprod. 4, 203-206
50. Plate, K. H., Breier, G., Millauer, B., Ullrich, A., and Risau, W. (1993) Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res. 53, 5822-5827
51. Rizk, B., Aboulghar, M., Smitz, J., and Ron-El, R. (1997) The role of vascular endothelial growth factor and interleukins in the pathogenesis of severe ovarian hyperstimulation syndrome. Hum. Reprod. Update 3, 255-266
52. Schams, D., Kosmann, M., Berisha, B., Amselgruber, W. M., and Miyamoto, A. (2001) Stimulatory and synergistic effects of luteinising hormone and insulin like growth factor 1 on the secretion of vascular endothelial growth factor and progesterone of cultured bovine granulosa cells. Exp. Clin. Endocrinol. Diabetes 109, 155-162
53. Enskog, A., Nilsson, L., and Brannstrom, M. (2001) Plasma levels of free vascular endothelial growth factor(165) (VEGF(165)) are not elevated during gonadotropin stimulation in in vitro fertilization (IVF) patients developing ovarian hyperstimulation syndrome (OHSS): results of a prospective cohort study with matched controls. Eur. J. Obstet. Gynecol. Reprod. Biol. 96, 196-201
54. Barkan, D., Jia, H., Dantes, A., Vardimon, L., Amsterdam, A., and Rubinstein, M. (1999) Leptin modulates the glucocorticoid-induced ovarian steroidogenesis. Endocrinology 140, 1731-1738
55. Almog, B., Gold, R., Tajima, K., Dantes, A., Salim, K., Rubinstein, M., Barkan, D., Homburg, R., Lessing, J. B., Nevo, N., et al. (2001) Leptin attenuates follicular apoptosis and accelerates the onset of puberty in immature rats. Mol. Cell. Endocrinol. 183, 179-191
56. Terranova, P. F., and Rice, V. M. (1997) Review: cytokine involvement in ovarian processes. Am. J. Reprod. Immunol. 37, 50-63
57. Sasson, R., Winder, N., Kees, S., and Amsterdam, A. (2002) Induction of apoptosis in granulosa cells by TNFα and its attenuation by glucocorticoids involve modulation of Bcl-2. Biochem. Biophys. Res. Commun. 294, 51-59
58. Spicer, L. J., and Chamberlain, C. S. (1999) Insulin-like growth factor binding protein-3: its biological effect on bovine granulosa cells. Domest. Amin. Endocrinol. 16, 19-29
59. Amato, G., Izzo, A., Tucker, A. T., and Bellastella, A. (1999) Lack of insulin-like growth factor binding protein-3 variation after follicle-stimulating hormone stimulation in women with polycystic ovary syndrome undergoing in vitro fertilization. Fertil. Steril. 72, 454-457
60. Eva, C., Oberto, A., Sprengel, R., and Genazzani, E. (1992) The murine NPY-1 receptor gene. Structure and delineation of tissue-specific expression. FEBS Lett. 314, 285-288
61. Ghersi, G., Chen, W., Lee, E. W., and Zukowska, Z. (2001) Critical role of dipeptidyl peptidase IV in neuropeptide Y-mediated endothelial cell migration in response to wounding. Peptides 22, 453-458
62. Faigle, W., Colucci-Guyon, E., Louvard, D., Amigorena, S., and Galli, T. (2000) Vimentin filaments in fibroblasts are a reservoir for SNAP23, a component of the membrane fusion machinery. Mol. Biol. Cell 11, 3485-3494
63. Aharoni, D., Meiri, I., Atzmon, R., Vlodavsky, I., and Amsterdam, A. (1997) Differential effect of components of the extracellular matrix on differentiation and apoptosis. Curr. Biol. 7, 43-51
64. Lucas, A. D., Chadwick, N., Warren, B. F., Jewell, D. P., Gordon, S., Powrie, F., and Greaves, D. R. (2001) The transmembrane form of the CX3CL1 chemokine fractalkine is expressed predominantly by epithelial cells in vivo. Am. J. Pathol. 158, 855-866
65. Tripp, R. A., Jones, L. P., Haynes, L. M., Zheng, H., Murphy, P. M., and Anderson, L. J. (2001) CX3C chemokine mimicry by respiratory syncytial virus G glycoprotein. Nat. Immunol. 2, 732-738
66. Rajasekaran, S. A., Palmer, L. G., Quan, K., Harper, J. F., Ball, W. J., Jr., Bander, N. H., Peralta Soler, A., and Rajasekaran, A. K. (2001) Na,K-ATPase beta-subunit is required for epithelial polarization, suppression of invasion, and cell motility. Mol. Biol. Cell 12, 279-295
67. Cohen, P. T. (1988) Two isoforms of protein phosphatase 1 may be produced from the same gene. FEBS Lett. 232, 17-23
68. Keyse, S. M., and Emslie, E. A. (1992) Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase. Nature (London) 359, 644-647
69. Lopez, F., Esteve, J. P., Buscail, L., Delesque, N., Saint-Laurent, N., Theveniau, M., Nahmias, C., Vaysse, N., and Susini, C. (1997) J. Biol. Chem. 272, 24448-24454
70. Tao, J., Malbon, C. C., and Wang, H. Y. (2001) Insulin stimulates tyrosine phosphorylation and inactivation of protein-tyrosine phosphatase 1B in vivo. J. Biol. Chem. 276, 29520-29525
71. Sidhu, J., and Sanchez, R. L. (1993) Prostatic acid phosphatase in strumal carcinoids of the ovary. An immunohistochemical study. Cancer 72, 1673-1678
72. Lin, M. F., Lee, M. S., Zhou, X. W., Andressen, J. C., Meng, T. C., Johansson, S. L., West, W. W., Taylor, R. J., Anderson, J. R., and Lin, F. F. (2001) Decreased expression of cellular prostatic acid phosphatase increases tumorigenicity of human prostate cancer cells. J. Urol. 166, 1943-1950
73. Gonzalez-Robayna, I.J., Falender, A. E., Ochsner, S., Firestone, G. L., and Richards, J. S. (2000) Follicle-stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-induced kinase (Sgk): evidence for A kinase-independent signaling by FSH in granulosa cells. Mol. Endocrinol. 14, 1283-1300
74. Chen, C., Zheng, B., Han, J., and Lin, S. C. (1997) Characterization of a novel mammalian RGS protein that binds to Galpha proteins and inhibits pheromone signaling in yeast. J. Biol. Chem. 272, 8679-8685
75. Druey, K. M., Ugur, O., Caron, J. M., Chen, C. K., Backlund, P. S., and Jones, T. L. (1999) Amino-terminal cysteine residues of RGS16 are required for palmitoylation and modulation of Gi-and Gq-mediated signaling. J. Biol. Chem. 274, 18836-18842
76. Nagai, Y., Aoki, J., Sato, T., Amano, K., Matsuda, Y., Arai, H., and Inoue, K. (1999) An alternative splicing form of phosphatidylserine-specific phospholipase A1 that exhibits lysophosphatidylserine-specific lysophospholipase activity in humans. J. Biol. Chem. 274, 11053-11059
77. Wen, X. Y., Stewart, A. K., Skaug, J., Wei, E., and Tsui, L. C. (2001) Murine phosphatidylserine-specific phospholipase A1 (Ps-pla1) maps to chromosome 16 but is distinct from the 1pd (lipid defect) locus. Mamm. Genome 12, 129-132
78. Pierce, S. B., Costa, M., Wisotzkey, R., Devadhar, S., Homburger, S. A., Buchman, A. R., Ferguson, K. C., Heller, J., Platt, D. M., Pasquinelli, A. A., et al. (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 15, 672-686
79. Miwa, T., Okada, N., and Okada, H. (2000) Alternative exon usage in the 3′ region of a single gene generates glycosylphosphatidylinositol-anchored and transmembrane forms of rat decay-accelerating factor. Immunogenetics 51, 129-137
80. Del Razo, L. M., Quintanilla-Vega, B., Brambila-Colombres, E., Calderon-Aranda, E. S., Manno, M., and Albores, A. (2001) Stress proteins induced by arsenic. Toxicol. Appl. Pharmacol. 177, 132-148