Rapid insulin-like growth factor-1-induced changes in granulosa cell thrombospondin-1 expression in vitro

Journal of Reproduction and Development

Volumn 57, Issue 1, 2011, Pages 76-83

  Robert McGray, A J ^a   Gingerich, Timothy ^a   Petrik, James J ^a   Lamarre, Jonathan ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Extracellular matrix; Gene expression; mRNA stability; Ovary; Post transcriptional

Indexed keywords

MESSENGER RNA; NUCLEIC ACID SYNTHESIS INHIBITOR; SOMATOMEDIN C; THROMBOSPONDIN 1;

3' UNTRANSLATED REGION; ANIMAL; ARTICLE; CELL LINE; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GRANULOSA CELL; HALF LIFE TIME; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; RAT; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; SITE DIRECTED MUTAGENESIS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL LINE, TRANSFORMED; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; GRANULOSA CELLS; HALF-LIFE; INSULIN-LIKE GROWTH FACTOR I; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEIC ACID SYNTHESIS INHIBITORS; OOGENESIS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, MESSENGER; THROMBOSPONDIN 1; TRANSCRIPTION, GENETIC;

MAMMALIA; RATTUS;

EID: 79952975482     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.10-045H     Document Type: Article

References (35)

1. Richards J. Hormonal control of gene expression in the ovary. Endocr Rev 1994; 15: 725-751.
2. Craig J. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Frontiers in Bioscience 2007; 12: 3628-3639.
3. Quirk SM, Cowan RG, Harman RM, Hu C-, Porter DA. Ovarian follicular growth and atresia: The relationship between cell proliferation and survival. J Anim Sci 2004; 82: E40-52.
4. Baker J, Hardy M, Zhou J, Bondy C, Lupu F, Bellve A, Efstratiadis A. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996; 10: 903-918.
5. Monniaux D, Pisselet C. Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro. Biol Reprod 1992; 46: 109-119.
6. Demeestere I, Gervy C, Centner J, Devreker F, Englert Y, Delbaere A. Effect of insulin-like growth factor-I during preantral follicular culture on steroidogenesis, in vitro oocyte maturation, and embryo development in mice. Biol Reprod 2004; 70: 1664-1669.
7. Zhou J, Kumar TR, Matzuk MM, Bondy C. Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol Endocrinol 1997; 11: 1924-1933.
8. Grado-Ahuir JA, Aad PY, Ranzenigo G, Caloni F, Cremonesi F, Spicer LJ. Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: possible role of insulin-like growth factor-I in angiogenesis. J Anim Sci. 2009; 87: 1921-1933.
9. Bornstein P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 1995; 130: 503-506.
10. Adams J. Thrombospondin-1. Internatl J Biochem & Cell Biol 1997; 29: 861-865.
11. Esemuede N, Lee T, Pierre-Paul D, Sumpio B, Gahtan V. The role of thrombospondin-1 in human disease. J Surg Res 2004; 122: 135-142.
12. Petrik JJ, Gentry PA, Feige J, LaMarre J. Expression and localization of thrombospondin-1 and -2 and their cell-surface receptor, CD36, during rat follicular development and formation of the corpus luteum. Biol Reprod 2002; 67: 1522-1531.
13. Greenaway J, Gentry PA, Feige J, LaMarre J, Petrik JJ. Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development. Biol Reprod 2005, 72: 1071-1078.
14. Gingerich TJ, Feige JJ, LaMarre J. AU-rich elements and the control of gene expression through regulated mRNA stability. Anim Health Res Rev 2004; 5: 49-63.
15. Shaw G, Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 1986; 46: 659-667.
16. Wilusz J. The cap-to-tail guide to mRNA turnover. Nature Rev. Molecular Cell Biol 2001; 2: 237-242.
17. Mazan-Mamczarz K, Hagner PR, Corl S, Srikantan S, Wood WH, Becker KG, Gorospe M, Keene JD, Levenson AS, Gartenhaus RB. Post-transcriptional gene regula- tion by HuR promotes a more tumorigenic phenotype. Oncogene 2008; 27: 6151-6163.
18. Janz A, Sevignani C, Kenyon K, Ngo CV, Thomas-Tikhonenko A. Activation of the myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucleic Acids Res 2000; 28: 2268-2275
19. Stein LS, Stoica G, Tilley R, Burghardt RC. Rat ovarian granulosa cell culture: a model system for the study of cell-cell communication during multistep transformation. Cancer Res 1991; 51: 696-706.
20. Greenaway J, Lawler J, Moorehead R, Bornstein P, LaMarre J, Petrik J. Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). J Cell Physiol 2007; 210: 807-818.
21. Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK, Sharma SC. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 2002; 57: 195-220.
22. San Roman G, Magoffin D. Insulin-like growth factor binding proteins in ovarian follicles from women with polycystic ovarian disease: cellular source and levels in follicular fluid. J Clin Endocrinol Metab 1992; 75: 1010-1016.
23. Martinez-Chequer JC, Stouffer RL, Hazzard TM, Patton PE, Molskness TA. Insulin-like growth factors-1 and -2, but not hypoxia, synergize with gonadotropin hormone to promote vascular endothelial growth factor-A secretion by monkey granulosa cells from preovulatory follicles. Biol Reprod 2003; 68: 1112-1118.
24. Armstrong LC, Bornstein P. Thrombospondins 1 and 2 function as inhibitors of angiogenesis. Matrix Biology 2003; 22: 63-71.
25. Sid B, Sartelet H, Bellon G, El Btaouri H, Rath G, Delorme N, Haye B, Martiny L. Thrombospondin 1: a multifunctional protein implicated in the regulation of tumor growth. Critical Rev Oncol/Hematol 2004; 49: 245-258.
26. Godyna S, Liau G, Popa I, Stefansson S, Argraves WS. Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J Cell Biol 1995; 129: 1403-1410.
27. Mikhailenko I, Kounnas MZ, Strickland DK. Low density lipoprotein receptor-related protein/alpha-2-macroglobulin receptor mediates the cellular internalization and degradation of thrombospondin. J Biol Chem 1995; 270: 9543-9549.
28. Wagner BJ, DeMaria CT, Sun Y, Wilson GM, Brewer G. Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics 1998; 48: 195-202.
29. Alvarez AA, Axelrod JR, Whitaker RS, Isner PD, Bentley RC, Dodge RK, Rodriguez GC. Thrombospondin-1 expression in epithelial ovarian carcinoma: association with p53 status, tumor angiogenesis, and survival in platinum-treated patients. Gynecol Oncol 2001; 82: 273-278.
30. Mettouchi A, Cabon F, Montreau N, Vernier P, Mercier G, Blangy D, Tricoire H, Vigier P, Binétruy B. SPARC and thrombospondin genes are repressed by the c-jun oncogene in rat embryo fibroblasts. EMBO J 1994; 13: 5668-5678.
31. Wang PH, Schaaf GJ, Chen WH, Feng J, Prins BA, Levin ER, Bahl JJ. IGF I induction of p53 requires activation of MAP kinase in cardiac muscle cells. Biochem Biophys Res Commun 1998; 245: 912-917.
32. Mamay CL, Mingo-Sion AM, Wolf DM, Molina MD, Van Den Berg CL. An inhibitory function for JNK in the regulation of IGF-I signaling in breast cancer. Oncogene 2003; 22: 602-614.
33. Thomas FH, Wilson H, Silvestri A, Fraser H. Thrombospondin-1 expression is increased during follicular atresia in the primate ovary. Endocrinology 2008; 149: 185-192.
34. Stanek MB, Borman SM, Molskness TA, Larson JM, Stouffer RL, Patton PE. Insulin and insulin-like growth factor stimulation of vascular endothelial growth factor production by luteinized granulosa cells: comparison between polycystic ovarian syndrome (PCOS) and non-PCOS women. J Clin Endocrinol Metab 2007; 92: 2726-2733.
35. Poulaki V, Mitsiades CS, McMullan C, Sykoutri D, Fanourakis G, Kotoula V, Tseleni-Balafouta S, Koutras DA, Mitsiades N. Regulation of vascular endothelial growth factor expression by insulin-like growth factor I in thyroid carcinomas. J Clin Endocrinol Metab 2003: 88: 5392-5398.