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Semin Reprod Med 2006; 24(4): 262-269
DOI: 10.1055/s-2006-948555
Copyright © 2006 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Extracellular Matrix Functions in Follicle Maturation

Courtney B. Berkholtz1 , 2 , Lonnie D. Shea2 , 3 , Teresa K. Woodruff2 , 4 , 5
  • 1Interdepartmental Biological Sciences Program, Northwestern University, Evanston, Illinois
  • 2Center for Reproductive Research, Northwestern University, Evanston, Illinois
  • 3Department of Chemical and Biological Engineering, Northwestern University, Evanston, Illinois
  • 4Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois
  • 5Department of Medicine, Northwestern University, Evanston, Illinois
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Publication History

Publication Date:
30 August 2006 (online)

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ABSTRACT

The extracellular matrix (ECM) promotes and/or inhibits many cellular processes, including but not limited to proliferation, differentiation, and survival, which must occur for follicle growth and oocyte maturation. The ECM regulation of cellular processes in ovarian cells is being investigated in many animal models, including avian, rat, bovine, porcine, rabbit, sheep, human, and mouse. Granulosa cells are more frequently employed; however, the culture of intact follicles and ovaries has been developed and enables ECM functions in folliculogenesis to be studied. ECM components that have been examined are used individually (collagen, laminin, fibronectin) or collectively (Matrigel, isolated basal lamina, and ECM produced by cell lines) in both two- and three-dimensional model systems. In granulosa cell cultures, ECM affects morphology, aggregation and communication, survival, proliferation, and steroidogenesis; whereas follicle and ovary cultures demonstrate a regulation of folliculogenesis. This article describes the ECM functionality on ovarian cells throughout development, and highlights the potential of developing technologies to identify structure-function relationships in follicle maturation.

KEYWORDS

Extracellular matrix - granulosa cells - morphology - proliferation - survival

REFERENCES

  • 1 Hirshfield A N. Theca cells may be present at the outset of follicular growth.  Biol Reprod. 1991;  44 1157-1162
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 6 Rodgers R J, van Wezel I L, Irving-Rodgers H F et al.. Roles of extracellular matrix in follicular development.  J Reprod Fertil Suppl. 1999;  54 343-352
    PubMedGoogle Scholar
  • 7 Kleinman H K, Martin G R. Matrigel: basement membrane matrix with biological activity.  Semin Cancer Biol. 2005;  15 378-386
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 10 Luck M R. The gonadal extracellular matrix.  Oxf Rev Reprod Biol. 1994;  16 33-85
    PubMedGoogle Scholar
  • 11 van Wezel I L, Rodgers H F, Rodgers R J. Differential localization of laminin chains in bovine follicles.  J Reprod Fertil. 1998;  112 267-278
    PubMedGoogle Scholar
  • 12 Amsterdam A, Koch Y, Lieberman M E, Lindner H R. Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat.  J Cell Biol. 1975;  67 894-900
    CrossrefPubMedGoogle Scholar
  • 13 Hirshfield A N. Patterns of [3H] thymidine incorporation differ in immature rats and mature, cycling rats.  Biol Reprod. 1986;  34 229-235
    CrossrefPubMedGoogle Scholar
  • 14 Rowley J A, Madlambayan G, Mooney D J. Alginate hydrogels as synthetic extracellular matrix materials.  Biomaterials. 1999;  20 45-53
    CrossrefPubMedGoogle Scholar
  • 15 Geller H M, Fawcett J W. Building a bridge: engineering spinal cord repair.  Exp Neurol. 2002;  174 125-136
    CrossrefPubMedGoogle Scholar
  • 16 Kreeger P K, Woodruff T K, Shea L D. Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix.  Mol Cell Endocrinol. 2003;  205 1-10
    CrossrefPubMedGoogle Scholar
  • 17 Kreeger P K, Deck J W, Woodruff T K, Shea L D. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels.  Biomaterials. 2006;  27 714-723
    CrossrefPubMedGoogle Scholar
  • 18 van der Flier A, Sonnenberg A. Function and interactions of integrins.  Cell Tissue Res. 2001;  305 285-298
    PubMedGoogle Scholar
  • 19 De Arcangelis A, Georges-Labouesse E. Integrin and ECM functions: roles in vertebrate development.  Trends Genet. 2000;  16 389-395
    CrossrefPubMedGoogle Scholar
  • 20 Sheppard D. In vivo functions of integrins: lessons from null mutations in mice.  Matrix Biol. 2000;  19 203-209
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 22 Hay E. The Role of Extracellular Matrix in Development. New York; Liss 1984
    Google Scholar
  • 23 Folkman J, Moscona A. Role of cell shape in growth control.  Nature. 1978;  273 345-349
    PubMedGoogle Scholar
  • 24 Spiegelman B M, Ginty C A. Fibronectin modulation of cell shape and lipogenic gene expression in 3T3-adipocytes.  Cell. 1983;  35 657-666
    CrossrefPubMedGoogle Scholar
  • 25 Benya P D, Shaffer J D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels.  Cell. 1982;  30 215-224
    CrossrefPubMedGoogle Scholar
  • 26 Amsterdam A, Rotmensch S. Structure-function relationships during granulosa cell differentiation.  Endocr Rev. 1987;  8 309-337
    PubMedGoogle Scholar
  • 27 Sites C K, Kessel B, LaBarbera A R. 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 29 Ben-Rafael Z, Benadiva C A, Mastroianni Jr L et al.. Collagen matrix influences the morphologic features and steroid secretion of human granulosa cells.  Am J Obstet Gynecol. 1988;  159 1570-1574
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 32 Asem E K, Feng S, Stingley-Salazar S R 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 34 Carnegie J A, Byard R, Dardick I, Tsang B K. Culture of granulosa cells in collagen gels: the influence of cell shape on steroidogenesis.  Biol Reprod. 1988;  38 881-890
    CrossrefPubMedGoogle Scholar
  • 35 Gomes J E, Correia S C, Gouveia-Oliveira A, Cidadao A J, Plancha C E. Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth.  Mol Reprod Dev. 1999;  54 163-172
    CrossrefPubMedGoogle Scholar
  • 36 Hwang D H, Kee S H, Kim K et al.. Role of reconstituted basement membrane in human granulosa cell culture.  Endocr J. 2000;  47 177-183
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 38 Maresh G A, Timmons T M, Dunbar B S. Effects of extracellular matrix on the expression of specific ovarian proteins.  Biol Reprod. 1990;  43 965-976
    CrossrefPubMedGoogle Scholar
  • 39 Amsterdam A, Rotmensch S, Furman A, Venter E A, 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
    PubMedGoogle Scholar
  • 40 Figueiredo J, Hulshof S CJ, 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 42 Albertini D F, Kravit N G. Isolation and biochemical characterization of ten-nanometer filaments from cultured ovarian granulosa cells.  J Biol Chem. 1981;  256 2484-2492
    PubMedGoogle Scholar
  • 43 Albertini D F, 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
    CrossrefPubMedGoogle Scholar
  • 44 Anderson E, Albertini D F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary.  J Cell Biol. 1976;  71 680-686
    CrossrefPubMedGoogle Scholar
  • 45 Kidder G M, Mhawi A A. Gap junctions and ovarian folliculogenesis.  Reproduction. 2002;  123 613-620
    CrossrefPubMedGoogle Scholar
  • 46 Aten R F, Kolodecik T R, Behrman H R. 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
    CrossrefPubMedGoogle Scholar
  • 47 Richardson M C, Slack C, Stewart I J. Rearrangement of extracellular matrix during cluster formation by human luteinising granulosa cells in culture.  J Anat. 2000;  196(pt 2) 243-248
    CrossrefPubMedGoogle Scholar
  • 48 Ruoslahti E, Reed J C. Anchorage dependence, integrins, and apoptosis.  Cell. 1994;  77 477-478
    CrossrefPubMedGoogle Scholar
  • 49 Adams J C, Watt F M. Regulation of development and differentiation by the extracellular matrix.  Development. 1993;  117 1183-1198
    PubMedGoogle Scholar
  • 50 Irving-Rodgers H F, Mussard M L, Kinder J E, Rodgers R J. Composition and morphology of the follicular basal lamina during atresia of bovine antral follicles.  Reproduction. 2002;  123 97-106
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 52 Hovatta O, Silye R, Abir R, Krausz T, Winston R M. 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
    CrossrefPubMedGoogle Scholar
  • 53 Colman-Lerner A, Fischman M L, Lanuza G M et al.. Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development.  Endocrinology. 1999;  140 2541-2548
    CrossrefPubMedGoogle Scholar
  • 54 Oktay K, Karlikaya G, Akman O, Ojakian G K, 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
    CrossrefPubMedGoogle Scholar
  • 55 Mulac-Jericevic B, Conneely O M. Reproductive tissue selective actions of progesterone receptors.  Reproduction. 2004;  128 139-146
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 57 Asem E K, Stingley-Salazar S R, Robinson J P, Turek J J. 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 59 Emmen J M, Couse J F, Elmore S A 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
    CrossrefPubMedGoogle Scholar
  • 60 Fisher C R, Graves K H, Parlow A F, Simpson E R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene.  Proc Natl Acad Sci USA. 1998;  95 6965-6970
    CrossrefPubMedGoogle Scholar
  • 61 Krege J H, Hodgin J B, Couse J F et al.. Generation and reproductive phenotypes of mice lacking estrogen receptor beta.  Proc Natl Acad Sci USA. 1998;  95 15677-15682
    CrossrefPubMedGoogle Scholar
  • 62 Lubahn D B, Moyer J S, Golding T S 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
    CrossrefPubMedGoogle Scholar
  • 63 Rodgers R J, Vella C A, Rodgers H F, Scott K, Lavranos T C. 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
    CrossrefPubMedGoogle Scholar
  • 64 O'Shea J D. Heterogeneous cell types in the corpus luteum of sheep, goats and cattle.  J Reprod Fertil Suppl. 1987;  34 71-85
    PubMedGoogle Scholar
  • 65 Rodgers H F, Lavranos T C, Vella C A, Rodgers R J. Basal lamina and other extracellular matrix produced by bovine granulosa cells in anchorage-independent culture.  Cell Tissue Res. 1995;  282 463-471
    PubMedGoogle Scholar
  • 66 Qin W, Rane S G, Asem E K. Basal lamina of ovarian follicle regulates an inward Cl(-) current in differentiated granulosa cells.  Am J Physiol Cell Physiol. 2002;  282 C34-C48
    PubMedGoogle Scholar
  • 67 Kreeger P K, Fernandes N N, Woodruff T K, Shea L D. 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
    CrossrefPubMedGoogle Scholar
  • 68 Pangas S A. A novel in vitro culture system for the analysis of follicle development.  Tissue Eng. 2003;  9 1013-1021
    CrossrefPubMedGoogle Scholar

Teresa K Woodruff

Department of Neurobiology and Physiology, Northwestern University

2205 Tech Dr, Hogan 4-150, Evanston, IL 60208-3520

Email: tkw@northwestern.edu

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