Extracellular matrix functions in follicle maturation

Seminars in Reproductive Medicine

Volumn 24, Issue 4, 2006, Pages 262-269

  Berkholtz, Courtney B ^a   Shea, Lonnie D ^a,b   Woodruff, Teresa K ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Northwestern University   (United States)

Author keywords

Extracellular matrix; Granulosa cells; Morphology; Proliferation; Survival

Indexed keywords

COLLAGEN; FIBRONECTIN; LAMININ; MATRIGEL;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; EXTRACELLULAR MATRIX; GRANULOSA CELL; HUMAN; NONHUMAN; OOCYTE MATURATION; OVARY CELL; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; REVIEW; STEROIDOGENESIS;

ANIMALS; EXTRACELLULAR MATRIX; FEMALE; FORECASTING; GRANULOSA CELLS; HUMANS; OVARIAN FOLLICLE;

EID: 33748643187     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2006-948555     Document Type: Review

References (68)

1. Hirshfield AN. Theca cells may be present at the outset of follicular growth. Biol Reprod 1991;44:1157-1162
2. Gospodarowicz D, Lepine J, Massoglia S, Wood I. Comparison of the ability of basement membranes produced by corneal endothelial and mouse-derived endodermal PF-HR-9 cells to support the proliferation and differentiation of bovine kidney tubule epithelial cells in vitro. J Cell Biol 1984;99:947-961
3. Spira O, Vlodavsky I, Ulmansky R, et al. Thyrotrophin and growth hormone secretion and cell morphology in hypothyroid pituitary cells cultured on a natural extracellular matrix. Acta Endocrinol (Copenh) 1983;104:279-286
4. Gospodarowicz D, Delgado D, Vlodavsky I. Permissive effect of the extracellular matrix on cell proliferation in vitro. Proc Natl Acad Sci USA 1980;77:4094-4098
5. Vlodavsky I, Korner G, Ishai-Michaeli R, et al. Extracellular matrix-resident growth factors and enzymes: possible involvement in tumor metastasis and angiogenesis. Cancer Metastasis Rev 1990;9:203-226
6. Rodgers RJ, van Wezel IL, Irving-Rodgers HF, et al. Roles of extracellular matrix in follicular development. J Reprod Fertil Suppl 1999;54:343-352
7. Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 2005;15:378-386
8. Huet C, Monget P, Pisselet C, Monniaux D. Changes in extracellular matrix components and steroidogenic enzymes during growth and atresia of antral ovarian follicles in the sheep. Biol Reprod 1997;56:1025-1034
9. Bortolussi M, Zanchetta R, Doliana R, et al. Changes in the organization of the extracellular matrix in ovarian follicles during the preovulatory phase and atresia. An immunofluorescence study. Basic Appl Histochem 1989;33:31-38
10. Luck MR. The gonadal extracellular matrix. Oxf Rev Reprod Biol 1994;16:33-85
11. van Wezel IL, Rodgers HF, Rodgers RJ. Differential localization of laminin chains in bovine follicles. J Reprod Fertil 1998;112:267-278
12. Amsterdam A, Koch Y, Lieberman ME, Lindner HR. Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J Cell Biol 1975;67:894-900
13. Hirshfield AN. Patterns of [3H] thymidine incorporation differ in immature rats and mature, cycling rats. Biol Reprod 1986;34:229-235
14. Rowley JA, Madlambayan G, Mooney DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 1999;20:45-53
15. Geller HM, Fawcett JW. Building a bridge: engineering spinal cord repair. Exp Neurol 2002;174:125-136
16. Kreeger PK, Woodruff TK, Shea LD. Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix. Mol Cell Endocrinol 2003;205:1-10
17. Kreeger PK, Deck JW, Woodruff TK, Shea LD. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials 2006;27:714-723
18. van der Flier A, Sonnenberg A. Function and interactions of integrins. Cell Tissue Res 2001;305:285-298
19. De Arcangelis A, Georges-Labouesse E. Integrin and ECM functions: roles in vertebrate development. Trends Genet 2000;16:389-395
20. Sheppard D. In vivo functions of integrins: lessons from null mutations in mice. Matrix Biol 2000;19:203-209
21. Ben-Ze'ev A, Amsterdam A. Regulation of cytoskeletal proteins involved in cell contact formation during differentiation of granulosa cells on extracellular matrix. Proc Natl Acad Sci USA 1986;83:2894-2898
22. Hay E. The Role of Extracellular Matrix in Development. New York: Liss; 1984
23. Folkman J, Moscona A. Role of cell shape in growth control. Nature 1978;273:345-349
24. Spiegelman BM, Ginty CA. Fibronectin modulation of cell shape and lipogenic gene expression in 3T3-adipocytes. Cell 1983;35:657-666
25. Benya PD, Shaffer JD. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 1982;30:215-224
26. Amsterdam A, Rotmensch S. Structure-function relationships during granulosa cell differentiation. Endocr Rev 1987;8:309-337
27. Sites CK, Kessel B, LaBarbera AR. Adhesion proteins increase cellular attachment, follicle-stimulating hormone receptors, and progesterone production in cultured porcine granulosa cells. Proc Soc Exp Biol Med 1996;212:78-83
28. Furman A, Rotmensch S, Kohen F, Mashiach S, Amsterdam A. Regulation of rat granulosa cell differentiation by extracellular matrix produced by bovine corneal endothelial cells. Endocrinology 1986;118:1878-1885
29. Ben-Rafael Z, Benadiva CA, Mastroianni L Jr, et al. Collagen matrix influences the morphologic features and steroid secretion of human granulosa cells. Am J Obstet Gynecol 1988;159:1570-1574
30. Furman A, Rotmensch S, Dor J, et al. Culture of human granulosa cells from an in vitro fertilization program: effects of extracellular matrix on morphology and cyclic adenosine 3′,5′ monophosphate production. Fertil Steril 1986;46:514-517
31. Le Bellego F, Pisselet C, Huet C, Monget P, Monniaux D. Laminin-alpha6beta1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells. J Endocrinol 2002;172:45-59
32. Asem EK, Feng S, Stingley-Salazar SR, et al. Basal lamina of avian ovarian follicle: influence on morphology of granulosa cells in-vitro. Comp Biochem Physiol Part C 2000;125:189-201
33. Bussenot I, Ferre G, Azoulay-Barjonet C, et al. Culture of human preovulatory granulosa cells: effect of extracellular matrix on steroidogenesis. Biol Cell 1993;77:181-186
34. Carnegie JA, Byard R, Dardick I, Tsang BK. Culture of granulosa cells in collagen gels: the influence of cell shape on steroidogenesis. Biol Reprod 1988;38:881-890
35. Gomes JE, Correia SC, Gouveia-Oliveira A, Cidadao AJ, Plancha CE. Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth. Mol Reprod Dev 1999;54:163-172
36. Hwang DH, Kee SH, Kim K, et al. Role of reconstituted basement membrane in human granulosa cell culture. Endocr J 2000;47:177-183
37. Huet C, Pisselet C, Mandon-Pepin B, Monget P, Monniaux D. Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. J Endocrinol 2001;169:347-360
38. Maresh GA, Timmons TM, Dunbar BS. Effects of extracellular matrix on the expression of specific ovarian proteins. Biol Reprod 1990;43:965-976
39. Amsterdam A, Rotmensch S, Furman A, Venter EA, Vlodavsky I. Synergistic effect of human chorionic gonadotropin and extracellular matrix on in vitro differentiation of human granulosa cells: progesterone production and gap junction formation. Endocrinology 1989;124:1956-1964
40. Figueiredo J, Hulshof SCJ, Thiry M, et al. Extracellular matrix proteins and basement membrane: their identification in bovine ovaries and significance for the attachment of cultured preantral follicles. Theriogenology 1995;43:845-858
41. Aharoni D, Meiri I, Atzmon R, Vlodavsky I, Amsterdam A. Differential effect of components of the extracellular matrix on differentiation and apoptosis. Curr Biol 1997;7:43-51
42. Albertini DF, Kravit NG. Isolation and biochemical characterization of ten-nanometer filaments from cultured ovarian granulosa cells. J Biol Chem 1981;256:2484-2492
43. Albertini DF, Anderson E. The appearance and structure of intercellular connections during the ontogeny of the rabbit ovarian follicle with particular reference to gap junctions. J Cell Biol 1974;63:234-250
44. Anderson E, Albertini DF. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 1976;71:680-686
45. Kidder GM, Mhawi AA. Gap junctions and ovarian folliculogenesis. Reproduction 2002;123:613-620
46. Aten RF, Kolodecik TR, Behrman HR. A cell adhesion receptor antiserum abolishes, whereas laminin and fibronectin glycoprotein components of extracellular matrix promote, luteinization of cultured rat granulosa cells. Endocrinology 1995;136:1753-1758
47. Richardson MC, Slack C, Stewart IJ. Rearrangement of extracellular matrix during cluster formation by human luteinising granulosa cells in culture. J Anat 2000;196 (pt 2):243-248
48. Ruoslahti E, Reed JC. Anchorage dependence, integrins, and apoptosis. Cell 1994;77:477-478
49. Adams JC, Watt FM. Regulation of development and differentiation by the extracellular matrix. Development 1993;117:1183-1198
50. Irving-Rodgers HF, Mussard ML, Kinder JE, Rodgers RJ. Composition and morphology of the follicular basal lamina during atresia of bovine antral follicles. Reproduction 2002;123:97-106
51. Yasuda K, Hagiwara E, Takeuchi A, et al. Changes in the distribution of tenascin and fibronectin in the mouse ovary during folliculogenesis, atresia, corpus luteum formation and luteolysis. Zoolog Sci 2005;22:237-245
52. Hovatta O, Silye R, Abir R, Krausz T, Winston RM. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod 1997;12:1032-1036
53. Colman-Lerner A, Fischman ML, Lanuza GM, et al. Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development. Endocrinology 1999;140:2541-2548
54. Oktay K, Karlikaya G, Akman O, Ojakian GK, Oktay M. Interaction of extracellular matrix and activin-A in the initiation of follicle growth in the mouse ovary. Biol Reprod 2000;63:457-461
55. Mulac-Jericevic B, Conneely OM. Reproductive tissue selective actions of progesterone receptors. Reproduction 2004;128:139-146
56. Fujiwara H, Honda T, Ueda M, et al. Laminin suppresses progesterone production by human luteinizing granulosa cells via interaction with integrin alpha 6 beta 1. J Clin Endocrinol Metab 1997;82:2122-2128
57. Asem EK, Stingley-Salazar SR, Robinson JP, Turek JJ. Effect of basal lamina on progesterone production by chicken granulosa cells in vitro-influence of follicular development. Comp Biochem Physiol Part C 2000;125:233-244
58. Wang X, Otsu K, Saito H, Hiroi M, Ishikawa K. Sandwich configuration of type I collagen suppresses progesterone production in primary cultured porcine granulosa cells by reducing gene expression of cytochrome P450 cholesterol side-chain cleavage enzyme. Arch Biochem Biophys 2000;376:117-123
59. Emmen JM, Couse JF, Elmore SA, et al. In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology 2005;146:2817-2826
60. Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 1998;95:6965-6970
61. Krege JH, Hodgin JB, Couse JF, et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 1998;95:15677-15682
62. Lubahn DB, Moyer JS, Golding TS, et al. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 1993;90:11162-11166
63. Rodgers RJ, Vella CA, Rodgers HF, Scott K, Lavranos TC. Production of extracellular matrix, fibronectin and steroidogenic enzymes, and growth of bovine granulosa cells in anchorage-independent culture. Reprod Fertil Dev 1996;8:249-257
64. O'Shea JD. Heterogeneous cell types in the corpus luteum of sheep, goats and cattle. J Reprod Fertil Suppl 1987;34:71-85
65. Rodgers HF, Lavranos TC, Vella CA, Rodgers RJ. Basal lamina and other extracellular matrix produced by bovine granulosa cells in anchorage-independent culture. Cell Tissue Res 1995;282:463-471
66. Qin W, Rane SG, Asem EK. Basal lamina of ovarian follicle regulates an inward Cl(-) current in differentiated granulosa cells. Am J Physiol Cell Physiol 2002;282:C34-C48
67. Kreeger PK, Fernandes NN, Woodruff TK, Shea LD. Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol Reprod 2005;73:942-950
68. Pangas SA. A novel in vitro culture system for the analysis of follicle development. Tissue Eng 2003;9:1013-1021