Nerve growth factor induces vascular endothelial growth factor expression in granulosa cells via a trkA receptor/mitogen-activated protein kinase-extracellularly regulated kinase 2-dependent pathway

Journal of Clinical Endocrinology and Metabolism

Volumn 94, Issue 8, 2009, Pages 3065-3071

  Julio Pieper, Marcela ^a   Lozada, Patricia ^a   Tapia, Veronica ^a   Vega, Margarita ^a   Miranda, Cristián ^a   Vantman, David ^a   Ojeda, Sergio R ^b   Romero, Carmen ^a  

^a HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE A; VASCULOTROPIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FERTILIZATION IN VITRO; GRANULOSA CELL; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

EID: 68549096011     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-0542     Document Type: Article

References (49)

1. Levi-Montalcini R 1987 The nerve growth factor 35 years later. Science 237:1154-1162
2. García-Suárez O, Germanà A, Hannestad J, Ciriaco E, Laurà R, Naves J, Esteban I, Silos-Santiago I, Vega JA 2000 TrkA is necessary for the normal development of the murine thymus. J Neuroimmunol 108:11-21
3. Polak M, Scharfmann R, Seilheimer B, Eisenbarth G, Dressler D, Verma IM, Potter H 1993 Nerve growth factor induces neuron-like differentiation of an insulin-secreting pancreatic β-cell line. Proc Natl Acad Sci USA 90:5781-5785
4. Scharfmann R, Tazi A, Polak M, Kanaka C, Czernichow P 1993 Expression of functional nerve growth factor receptors in pancreatic β-cell lines and fetal rat islets in primary culture. Diabetes 42:1829-1836
5. Dissen GA, Paredes A, Romero C, Dees WL, Ojeda SR 2004 Neural and neurotrophic control of ovarian development. In: Leung P, Adashi E, eds. The ovary. 2nd ed. San Diego: Academic Press; 3-23
6. Dissen GA, Hirshfield AN, Malamed S, Ojeda SR 1995 Expression of neurotrophins and their receptors in the mammalian ovary is developmentally regulated: changes at the time of folliculogenesis. Endocrinology 136:4681-4692
7. Dissen GA, Romero C, Hirshfield AN, Ojeda SR 2001 Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142:2078-2086
8. Lara HE, Hill DF, Katz KH, Ojeda SR 1990 The gene encoding nerve growth factor is expressed in the immature rat ovary: effect of denervation and hormonal treatment. Endocrinology 126:357-363
9. Dissen GA, Hill DF, Costa ME, Les Dees CW, Lara HE, Ojeda SR 1996 A role for trkA nerve growth factor receptors in mammalian ovulation. Endocrinology 137:198-209
10. Mayerhofer A, Dissen GA, Parrott JA, Hill DF, Mayerhofer D, Garfield RE, Costa ME, Skinner MK, Ojeda SR 1996 Involvement of nerve growth factor in the ovulatory cascade: trkA receptor activation inhibits gap junctional communication between thecal cells. Endocrinology 137:5662-5670
11. Romero C, Paredes A, Dissen GA, Ojeda SR 2002 Nerve growth factor induces the expression of functional FSH receptors in newly formed follicles of the rat ovary. Endocrinology 143:1485-1494
12. Salas C, Julio-Pieper M, Valladares M, Pommer R, Vega M, Mastronardi C, Kerr B, Ojeda SR, Lara HE, Romero C 2006 Nerve growth factor-dependent activation of trkA receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J Clin Endocrinol Metab 91:2396-2403
13. Chiaretti A, Piastra M, Caresta E, Nanni L, Aloe L 2002 Improving ischaemic skin revascularisation by nerve growth factor in a child with crush syndrome. Arch Dis Child 87:446-448
14. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P 2002 Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 106:2257-2262
15. Seo K, Choi J, Park M, Rhee C 2001 Angiogenesis effects of nerve growth factor (NGF) on rat corneas. J Vet Sci 2:125-130
16. Calza L, Giardino L, Giuliani A, Aloe L, Levi-Montalcini R 2001 Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc Natl Acad Sci USA 98:4160-4165
17. Landi F, Aloe L, Russo A, Cesari M, Onder G, Bonini S, Carbonin PU, Bernabei R 2003 Topical treatment of pressure ulcers with nerve growth factor: a randomized clinical trial. Ann Intern Med 139:635-641
18. Raychaudhuri SK, Raychaudhuri SP, Weltman H, Farber EM 2001 Effect of nerve growth factor on endothelial cell biology: proliferation and adherence molecule expression on human dermal microvascular endothelial cells. Arch Dermatol Res 293:291-295
19. Cantarella G, Lempereur L, Presta M, Ribatti D, Lombardo G, Lazarovici P, Zappalà G, Pafumi C, Bernardini R 2002 Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 16:1307-1309
20. Park MJ, Kwak HJ, Lee HC, Yoo DH, Park IC, Kim MS, Lee SH, Rhee CH, Hong SI 2007 Nerve growth factor induces endothelial cell invasion and cord formation by promoting matrix metalloproteinase-2 expression through the phosphatidylinositol-3 kinase/Akt signaling pathway and AP-2 transcription factor. J Biol Chem 282:30485-30496
21. Middeke M, Hoffmann S, Hassan I, Wunderlich A, Hofbauer LC, Zielke A 2002 In vitro and in vivo angiogenesis in PC12 pheochromocytoma cells is mediated by vascular endothelial growth factor. Exp Clin Endocrinol Diabetes 110:386-392
22. Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Nagura H 1998 Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum Reprod 13:953-959
23. Fraser HM, Wulff C 2001 Angiogenesis in the primate ovary. Reprod Fertil Dev 13:557-566
24. Shimizu T, Kawahara M, Abe Y, Yokoo M, Sasada H, Sato E 2003 Follicular microvasculature and angiogenic factors in the ovaries in domestic animals. J Reprod Dev 49:181-192
25. Kaczmarek MM, Schams D, Ziecik AJ 2005 Role of vascular endothelial growth factor in ovarian physiology - an overview. Reprod Biol 5:111-136
26. Ferrara N 2001 Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 280:C1358-C1366
27. Geva E, Jaffe RB 2000 Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril 74:429-438
28. Campos X, Muñoz Y, Selman A, Yazigi R, Moyano L, Weinstein-Oppenheimer C, Lara HE, Romero C 2007 Nerve growth factor and its high-affinity receptor trkA participate in the control of vascular endothelial growth factor expression in epithelial ovarian cancer. Gynecol Oncol 104:168-175
29. Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M 2001 Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J Clin Endocrinol Metab 86:768-772
30. Hazzard TM, Xu F, Stouffer RL 2002 Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol Reprod 67:1305-1312
31. Dissen GA, Lara HE, Fahrenbach WH, Costa ME, Ojeda SR 1994 Immature rat ovaries become revascularized rapidly after autotransplantation and show a gonadotropin-dependent increase in angiogenic factor gene expression. Endocrinology 134:1146-1154
32. Nakanishi Y, Kodama J, Yoshinouchi M, Tokumo K, Kamimura S, Okuda H, Kudo T 1997 The expression of vascular endothelial growth factor and transforming growth factor-β associates with angiogenesis in epithelial ovarian cancer. Int J Gynecol Pathol 16:256-262
33. Agrawal R, Sladkevicius P, Engmann L, Conway GS, Payne NN, Bekis J, Tan SL, Campbell S, Jacobs HS 1998 Serum vascular endothelial growth factor concentrations and ovarian stromal blood flow are increased in women with polycystic ovaries. Hum Reprod 13:651-655
34. Ludwig M, Jelkmann W, Bauer O, Diedrich K 1999 Prediction of severe ovarian hyperstimulation syndrome by free serum vascular endothelial growth factor concentration on the day of human chorionic gonadotrophin administration. Hum Reprod 14:2437-2441
35. Albert C, Garrido N, Mercader A, Rao CV, Remohí J, Simó n C, Pellicer A 2002 The role of endothelial cells in the pathogenesis of ovarian hyperstimulation syndrome. Mol Hum Reprod 8:409-418
36. Julio-Pieper M, Lara HE, Bravo JA, Romero C 2006 Effects of nerve growth factor (NGF) on blood vessels area and expression of the angiogenic factors VEGF and TGF-β 1 in the rat ovary. Reprod Biol Endocrinol 4:57-67
37. Ferrara N, Frantz G, LeCouter J, Dillard-Telm L, Pham T, Draksharapu A, Giordano T, Peale F 2003 Differential expression of the angiogenic factor genes vascular endothelial growth factor (VEGF) and endocrine gland-derived VEGF in normal and polycystic human ovaries. Am J Pathol 162:1881-1893
38. Zapf-Colby A, Eichhorn J, Webster NJ, Olefsky JM 1999 Inhibition of PLC-γ1 activity converts nerve growth factor from an anti-mitogenic to a mitogenic signal in CHO cells. Oncogene 18:4908-4919
39. Abir R, Fisch B, Jin S, Barnnet M, Ben-Haroush A, Felz C, Kessler-Icekson G, Feldberg D, Nitke S, Ao A 2005 Presence of NGF and its receptors in ovaries from human fetuses and adults. Mol Hum Reprod 11:229-236
40. Lawrence MC, McGlynn K, Shao C, Duan L, Naziruddin B, Levy MF, Cobb MH 2008 Chromatin-bound mitogen-activated protein kinases transmit dynamic signals in transcription complexes in β-cells. Proc Natl Acad Sci USA 105:13315-13320
41. Anderson RA, Robinson LL, Brooks J, Spears N 2002 Neurotropins and their receptors are expressed in the human fetal ovary. J Clin Endocrinol Metab 87:890-897
42. Spears N, Molinek MD, Robinson LL, Fulton N, Cameron H, Shimoda K, Telfer EE, Anderson RA, Price DJ 2003 The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development 130:5481-5491
43. Papetti M, Herman IM 2002 Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol 282:C947-C970
44. Stouffer RL, Martínez-Chequer JC, Molskness TA, Xu F, Hazzard TM 2001 Regulation and action of angiogenic factors in the primate ovary. Arch Med Res 32:567-575
45. Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D 2008 Nerve growth factor as an angiogenic factor. Microvasc Res 75:135-141
46. Shimizu T, Iijima K, Miyabayashi K, Ogawa Y, Miyazaki H, Sasada H, Sato E 2007 Effect of direct ovarian injection of vascular endothelial growth factor gene fragments on follicular development in immature female rats. Reproduction 134:677-682
47. Neulen J, Yan Z, Raczek S, Weindel K, Keck C, Weich HA, Marmé D, Breckwoldt M 1995 Human chorionic gonadotropin-dependent expression of vascular endothelial growth factor/vascular permeability factor in human granulosa cells: importance in ovarian hyperstimulation syndrome. J Clin Endocrinol Metab 80:1967-1971
48. Lee A, Christenson LK, Stouffer RL, Burry KA, Patton PE 1997 Vascular endothelial growth factor levels in serum and follicular fluid of patients undergoing in vitro fertilization. Fertil Steril 68:305-311
49. Dissen GA, Garcia-Rudaz C, Paredes A, Mayer C, Mayerhofer A, Ojeda SR 2009 Excessive ovarian production of nerve growth factor facilitates development of cystic ovarian morphology in mice and is a feature of polycystic ovarian syndrome in humans. Endocrinology 150:2906-2914