The hepatocyte growth factor system as a regulator of female and male gonadal function

Journal of Endocrinology

Volumn 195, Issue 3, 2007, Pages 359-371

  Zachow, Rob ^a   Uzumcu, Mehmet ^b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; PROTEIN TYROSINE KINASE; SCATTER FACTOR; SCATTER FACTOR ACTIVATOR; SCATTER FACTOR ACTIVATOR INHIBITOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; SEX HORMONE;

APOPTOSIS; AUTOCRINE EFFECT; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL STRUCTURE; ENZYME ACTIVATION; FEEDBACK SYSTEM; FEMALE GENITAL SYSTEM; GONAD DEVELOPMENT; GONAD FUNCTION; GRANULOSA CELL; HORMONAL REGULATION; HUMAN; LEYDIG CELL; MORPHOGENESIS; NONHUMAN; ONTOGENY; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; SERTOLI CELL; SIGNAL TRANSDUCTION; SOMATIC CELL; STEROIDOGENESIS; TARGET CELL; TESTIS DEVELOPMENT; TESTIS FUNCTION; THECA CELL; ANIMAL; BIOSYNTHESIS; CELL DIVISION; CYTOLOGY; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; OVARY; OVARY FOLLICLE; PHYSIOLOGY; TESTIS;

ANIMALS; APOPTOSIS; CELL DIVISION; FEMALE; GONADAL STEROID HORMONES; GRANULOSA CELLS; HEPATOCYTE GROWTH FACTOR; HUMANS; LEYDIG CELLS; MALE; OVARIAN FOLLICLE; OVARY; TESTIS; THECA CELLS;

EID: 38349038175     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-07-0466     Document Type: Review

References (95)

1. Baffy G, Yang L, Michalopoulos GK & Williamson JR 1992 Hepatocyte growth factor induces calcium mobilization and inositol phosphate production in rat hepatocytes. Journal of Cell Physiology 153 332-339.
2. Barnett KR, Schilling C, Greenfeld CR, Tornic D & Flaws JA 2006 Ovarian follicle development and transgenic mouse models. Human Reproduction Update 12 537-555.
3. Bornstein SR, Rutowski H & Vrezas I 2004 Cytokines and steroidogenesis. Molecular and Cellular Endocrinology 215 135-141.
4. Bott RC, McFee RM, Clopton DT, Toombs C & Cupp AS 2006 Vascular endothelial growth factor and kinase domain region receptor are involved in both seminiferous cord formation and vascular development during testis morphogenesis in the rat. Biology of Reproduction 75 56-67.
5. Bottaro DP, Rubin JS & Faletto DL 1991 Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251 802-804.
6. Brennan J & Capel B 2004 One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nature Review Genetics 5 509-521.
7. Brennan J, Tilmann C & Capel B 2003 Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes and Development 17 800-810.
8. Burns KH & Matzuk MM 2002 Genetic models for the study of gonadotropin actions. Endocrinology 143 2823-2835.
9. Bussolino F, DiRenzo M, Ziche M, Bocchietto E, Olivero, M, Naldini L, Gaudino G, Tomagnone L, Coffer A & Comoglio P 1992 Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. Journal of Cell Biology 119 629-641.
10. Carreau S, Dalande C, Silandre D, Bourguiba S & Lambard S 2006 Aromatase and estrogen receptors in male reproduction. Molecular and Cellular Endocrinology 246 65-68.
11. Catizone A, Ricci G, Arista V, Innocenzi A & Galcheri M 1999 Hepatocyte growth factor and c-Met are expressed in the rat prepubertal testis. Endocrinology 140 3106-3113.
12. Carizone A, Ricci G & Galdieri M 2001 Expression and a functional role of hepatocyte growth factor receptor (c-Met) during postnatal rat testis development. Endocrinology 142 1828-1834.
13. Catizone A, Ricci G & Galdieri M 2002 Functional role of hepatocyte growth factor receptor during sperm maturation. Journal of Andrology 23 911-918.
14. Catizone A, Ricci G & Galdieri M 2005 HGF and post-natal testis development. Molecular and Cellular Endocrinology 241 32-40.
15. Catizone A, Ricci G, Del Bravo J & Galdieri M 2006 Hepatocyte growth factor modulates in vitro cell survival and proliferation of germ cells during postnatal testis development. Journal of Endocrinology 189 137-146.
16. Colvin JS, Green RP, Schmal J, Capel B & Ornitz DM 2001 Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104 875-889.
17. Conti M, Hsieh M, Park YJ & Su YQ 2006 Role of the epidermal growth factor network in ovarian follicles. Molecular Endocrinolgy 20 715-723.
18. Cupp AS, Kim G & Skinner MK 1999 Expression and action of transforming growth factor β (TGFβ1, TGFβ2 and TGFβ3) during embryonic rat testis development. Biology of Reproduction 60 1304-1313.
19. Cupp AS, Kim GH & Skinner MK 2000 Expression and action of neurotropin-3 and nerve growth factor in embryonic and early postnatal rat testis development. Biology of Reproduction 63 1617-1628.
20. Del Bravo J, Catizone A, Ricci G & Galdieri M 2007 Hepatocyte growth factor modulates rat Leydig cell functions. Journal of Andrology In Press.
21. Depuydt CE, Zalata A, de Potter CR, van Emmelo J & Comhaire FH 1996 The receptor encoded by human c-met oncogene is expressed in testicular tissue and on human spermatozoa. Molecular Human Reproduction 2 2-8.
22. Ehrmann DA 2005 Polycystic ovary syndrome. New England Journal of Medicine 325 1223-1236.
23. Erickson GF 1983 Primary cultures of ovarian cells in serum-free medium as models of hormone-dependent differentiation. Molecular and Cellular Endocrinology 29 21-49.
24. Erickson GF 1994 Polycystic ovary syndrome: normal and abnormal steroidogenesis. In Ovarian Endocrinopathies: Proceedings of the 8th Reinier deGraaf Symposium, pp 103-115. Eds R Schats & J Schoemaker. New York: Parthenon Publishing.
25. Fortune JE 2003 The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Animal Reproduction Science 78 135-163.
26. Gheradi E & Stoker M 1991 Hepatocyte growth factor-scatter factor: mitogen, motogen, and Met. Cancer Cell 3 227-232.
27. Giordano S, Ponzetto C & DiRenzo MF 1989 Tyrosine kinase receptor indistinguishable from the c-mer protein. Nature 339 155-156.
28. Goda K, Fujisawa M, Shirakawa T, Dobashi M, Shiota G, Zhang ZJ, Gotoh A & Kamidono S 2004 Adenoviral-mediated HGF expression inhibits germ cell apoptosis in rats with cryptorchidism. Journal of Gene Medicine 6 869-876.
29. Gonzatti-Haces M, Seth A, Park M, Copeland T, Oroszlan S & Vande Woude GF 1988 Characterization of the tpr-met oncogene p65 and the met protooncogene p140 protein tyrosine kinases. PNAS 85 21-25.
30. Griswold MD 1998 The central role of Sertoli cells in spermatogenesis. Seminars in Cell and Developmental Biology 9 411-416.
31. Haider SG 2004 Cell biology of Leydig cells in the testis. International Review of Cytology 233 181-241.
32. Hilber SG 2001 Gonadotropic control of ovarian follicular growth and development. Molecular and Cellular Endocrinology 179 39-46.
33. Hsueh AJ, Eisenhauer K, Chun SY, Hsu SY & Billig H 1996 Gonadal cell apoptosis. Recent Progress in Hormone Research 51 433-455.
34. Huleihel M & Lunenfeld E 2004 Regulation of spermatogenesis by paracrine/autocrine testicular factors. Asian Journal of Andrology 6 259-268.
35. Hussein MR 2005 Apoptosis in the ovary: molecular mechanisms. Human Reproduction Update 11 162-177.
36. Itman C, Mendis S, Barakat B & Loveland KL 2006 All in the family: TGF-beta family action in testis development. Reproduction 132 233-246.
37. Ito M, Harada T, Tanikawa M, Fuji A, Shiota G & Terakawa N 2001 Hepatocyte growth factor and stem cell factor involvement in paracrine interplays of theca and granulosa cells in the human ovary. Fertility and Sterility 75 973-979.
38. Kaipia A & Hsueh AJ 1997 Regulation of ovarian follicle atresia. Annual Review of Physiology 59 349-363.
39. Knight PG & Glister C 2006 TGF-beta superfamily members and ovarian follicle development. Reproduction 132 177-178.
40. Lail-Trecker M, Gulati R & Peluso JJ 1998 A role for hepatocyte growth factor/scatter factor in regulating normal and neoplastic cells of reproductive tissues. Journal of the Society for Gynecologic Investigations 5 114-121.
41. LaPolt PS & Hong LS 1995 Inhibitory effects of superoxide dismutase and cyclic guanosine 3′, 5′-monophosphate on estrogen production in cultured rat granulosa cells. Endocrinology 136 5533-5539.
42. Levine E, Cupp AS & Skinner MK 2000 Role of neurotropins in rat embryonic testis morphogenesis (cord formation). Biology of Reproduction 62 132-142.
43. Liu Y 1999 Hepatocyte growth factor promotes renal epithelial cell survival by dual mechanisms. American Journal of Physiology 277 F624-F633.
44. Liu Y, Lin L & Zarnegar R 1994 Modulation of hepatocyte growth factor gene expression by estrogen in mouse ovary. Molecular and Cellular Endocrinology 104 173-181.
45. Mackay S & Smith RA 2007 Effects of growth factors on testicular morphogenesis. International Review of Cytology 260 113-173.
46. Magoffin DA 1991 Regulation of differentiated functions in ovarian theca cells. Seminars in Reproductive Endocrinology 9 321-331.
47. Makondo K, Kimura K, Kitamura N, Kitamma T, Yamaji D, Jung BD & Saito M 2004 Hepatocyte growth factor activates endothelial nitric oxide synthase by Ca(2 +)- and phosphoinositide 3-kinase/Akt-dependent phosphorylation in aortic endothelial cells. Biochemistry Journal 374 63-69.
48. Le Margueresse B & Jegou B 1988 In vitro effects of germ cells on the secretory activity of Sertoli cells recovered from rats of different ages. Endocrinology 122 1672-1680.
49. Matzuk MM, Burns KH, Viveiros MM & Eppig JJ 2002 Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296 2178-2180.
50. Maulik G, Shrikhande A, Kijima T, Ma PC, Morrison PT & Salgia R 2002 Role ofhepatocyte growth factor receptor, c-Met, in oncogenesis and potential for therapeutic inhibition. Cytokine and Growth Factor Reviews 13 41-59.
51. McNatty KP, juengel JL, Reader KL, Lim S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP et al. 2005 Bone morphogenetic protein 15 and growth differentiation factor 9 cooperate to regulate granulosa cell function in ruminants. Reproduction 129 481-487.
52. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de, Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M et al. 2000 Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287 1489-1493.
53. Miyazawa K, Tsubouchi H, Naka D, Takahashi K, Okigaki M, Arakaki N, Nakayama H, Hirono S, Sakiyama O, Takahashi K et al. 1989 Molecular cloning and sequence analysis of cDNA for human hepatocyte growth factor. Biochemical and Biophysical Research Communications 163 967-973.
54. Miyazawa K, Shimomura T, Kitamura A, Kondo J, Morimoto Y & Kitamura N 1993 Molecular cloning and sequence analysis of the cDNA for a human serine protease responsible for activation of hepatocyte growth factor, structural similarity of the protease precursor to blood coagulation factor-xii. Journal of Biological Chemistry 269 10024-10028.
55. Nakamura T, Nishizawa T, Hagiya M, Seki T, Shimonishi M, Sugimura A, Tashiro K & Shimizu S 1989 Molecular cloning and expression of human hepatocyte growth factor. Nature 342 440-443.
56. Naz RK, Joseph A, Lee Y, Ahmad K & Bhargava MM 1994 Expression of scatter factor/hepatocyte growth factor is regionally correlated with the initiation of sperm motility in murine male genital tract: is scatter factor/hepatocyte growth factor involved in the initiation of sperm motility. Molecular Reproduction and Development 38 431-439.
57. Osuga Y, Tsutsumi O, Momoeda M, Okagaki R, Matsumi H, Hiroi H, Suenaga A, Yano T & Taketani Y 1999 Evidence for the presence of hepatocyte growth factor expression in human ovarian follicles. Molecular Human Reproduction 5 703-707.
58. Parrott JA & Skinner MK 1998a Developmental and hormonal regulation of hepatocyte growth factor expression and action in the bovine ovarian follicle. Biology of Reproduction 59 553-560.
59. Parrott JA & Skinner MK 1998b Theca cell-granulosa cell interactions involve a positive feedback loop among keratinocyte growth factor, hepatocyte growth factor, and kit hgand during ovarian follicular development. Endocrinology 139 2240-2245.
60. Parrott JA & Skinner MK 2000 Kit ligand actions an ovarian stromal cells: effects on theca cell recruitment and steroid production. Molecular Reproduction and Development 55 55-64.
61. Parrott JA, Vigne JL, Chu BZ & Skinner MK 1994 Mesenchymal epithelial interactions within the ovarian follicle involve keratinocyte and hepatocyte growth factor production by theca cells and their action on granulosa cells. Endocrinology 135 569-575.
62. Peluso JJ & Pappalardo A 2004 Progesterone regulates granulosa cell viability through a protein kinase G-dependent mechanism that may involve 14-3-3-s. Biology of Reproduction 71 1870-1878.
63. Peruzzi B & Bortaro DP 2006 Targeting the c-Met signaling pathway in cancer. Clinical Cancer Research 12 3657-3660.
64. Rao AJ 2005 Hormonal regulation of Leydig cell proliferation and differentiation in rodent testis: a dynamic interplay between gonadotropins and testicular factors. Reproductive Biomedicine Online 11 507-518.
65. Ricci G, Catizone A, Innocenzi A & Galdieri M 1999 Hepatocyte growth factor (HGF) receptor expression and role of HGF during embryonic mouse testis development. Developmental Biology 216 340-347.
66. Ricci G, Catizone A & Galdieri M 2002 Pleiotropic activity of hepatocyte growth factor during embryonic mouse testis development. Mechanism of Development 118 19-28.
67. Ricci G, Catizone A & Galcheri M 2006 Expression and functional role of hepatocyte growth factor and its receptor (c-met) during fetal mouse tesis development. Journal of Endocrinology 191 559-570.
68. Roy A & Matzuk MM 2006 Deconstructing mammalian reproduction: using knockouts to define fertility pathways. Reproduction 131 207-219.
69. Schmahl J, Kim Y, Colvin JS, Ornitz DM & Capel B 2004 Fgf-9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 131 3627-3636.
70. Shimizu T, Iijima K, Sasada H & Sato E 2003 Messenger ribonucleic acid expressions of hepatocyte growth factor, angiopoietins and their receptors during follicular development in gilts. Journal of Reproduction and Development 49 203-211.
71. Shimomura T, Denda K, Kitamura A, Kawaguchi T, Kito M, Kondo J, Kagaya S, Qin L, Takata H, Miyazawa K et al. 1997 Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. Journal of Biological Chemistry 272 6370-6376.
72. Sierens JE, Sneddon SF, Collins F, Millar MR & Saunders PTK 2005 Estrogens in testis biology. Annals of New York Academy of Sciences 1061 65-76.
73. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R & Goodfellow PN 1990 A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346 240-244.
74. Skinner MK 1991 Cell-cell interactions in the testis. Endocrine Reviews 12 45-77.
75. Skinner MK 2005 Regulation of primordial follicle assembly and development. Human Reproduction Update 11 461-471.
76. Skinner MK, Tung PS & Fritz IB 1985 Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. Journal of Cell Biology 100 1941-1947.
77. Terranova PF 1991 Regulation of the granulosa cell: growth factor interactions. Seminars in Reproductive Endocrinology 9 313-320.
78. Tilmann C & Capel B 1999 Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126 2883-2890.
79. Uehara Y, Minowa O, Mori C, Shiota K, Kuno J, Noda T & Kitamura N 1995 Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373 702-705.
80. Uzumcu M, Dirks KA & Skinner MK 2002a Inhibition of platelet-derived growth factor actions in the embryonic testis influences normal cord development and morphology. Biology of Reproduction 66 745-753.
81. Uzumcu M, Westfall SD, Dirks KA & Skinner MK 2002b Embryonic testis cord formation and mesonephric cell migration requires the phosphotidylinositol 3-kinase signaling pathway. Biology of Reproduction 67 1927-1935.
82. Uzumcu M, Pan Z, Chu Y, Kuhn PE & Zachow RJ 2006 Immunolocalization of the hepatocyte growth factor (HGF) system in the rat ovary and the antiapoptotic effect of HGF in rat ovarian granulosa cells in vitro. Reproduction 132 291-299.
83. Vincent S, Segretain D, Nishikawa S, Nishikawa SI, Sage J, Cuzin F & Rassoulzadegan M 1998 Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: a Kit-KL interaction critical for meiosis. Development 125 4585-4593.
84. Vitt UA, Hayashi M, Klein C & Hsueh AJW 2000 Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biology of Reproduction 62 370-377.
85. Walker WH & Cheng J 2005 FSH and testosterone signaling in Sertoli cells. Reproduction 130 15-28.
86. Webb R, Garnsworthy PC, Gong JG & Armstrong DG 2004 Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science 82 E63-1374.
87. Van der Wee K & Hoffman MC 1999 An in vitro tubule assay identifies HGF as a morphogen for the formation of seminiferous tubules in the postnatal mouse testis. Experimental Cell Research 252 175-185.
88. Westfall SD, Hendry IR, Obholz KL & Davis JS 2001 Putative role of phosphatidylinositol 3-kinase-Akt signaling pathway in the survival of granulosa cells. Endocrine 12 315-321.
89. Yamauchi M, Itoh H, Naganuma S, Koono M, Hasui Y, Osada Y & Kataoka H 2002 Expression of hepatocyte growth factor activator inhibitor type 2 (HAI-2) in human testis: identification of a distinct transcription start site for the HAI-2 gene in the testis. Biological Chemistry 383 1953-1957.
90. Yang XM & Park M 1995 Expression ofthe hepatocyte growth factor/ scatter factor receptor tyrosine kinase is localized to epithelia in the adult mouse. Laboratory Investigation 73 483-491.
91. Yao HH, Tilmann C, Zhao GQ & Capel B 2002 The battle of the sexes: opposing pathways in sex determination. Novartis Foundation Symposium 187-198.
92. Zachow RJ & Woolery JK 2002 The effect of hepatocyte growth factor on cyclic nucleotide-dependent signaling and steroidogenesis in rat granulosa cells in vitro. Biology of Reproduction 67 454-459.
93. Zachow RJ, Weitsman SR & Magoffin DA 1997 Hepatocyte growth factor regulates ovarian theca-interstitial cell differentiation and androgen production. Endocrinology 138 691-697.
94. Zachow RJ, Ramski BE & Lee H 2000 Modulation of estrogen production and 17β-hydroxysteroid dehydrogenase-type 1, cytochrome P450 aromatase, c-Met, and protein kinase Bα messenger ribonucleic content in rat ovarian granulosa cells by hepatocyte growth factor and follicle-stimulating hormone. Biology of Reproduction 62 1851-1857.
95. Zhang C, Yeh S, Chen YT, Wu CC, Chuang KH, Lin HY, Wang RS, Chang YJ, Mendis-Handagama C, Hu L et al. 2006 Oligozoospermia with normal fertility in male mice lacking the androgen receptor in testis peritubular myoid cells. PNAS 103 17718-17723.