Semin Reprod Med 2006; 24(4): 195-203
DOI: 10.1055/s-2006-948549
Copyright © 2006 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Extracellular Matrix of the Developing Ovarian Follicle

Helen F. Irving-Rodgers1 , Raymond J. Rodgers1
  • 1Research Centre for Reproductive Health, Discipline of Obstetrics and Gynaecology, School of Paediatrics and Reproductive Health, University of Adelaide, Adelaide, South Australia, Australia
Further Information

Publication History

Publication Date:
30 August 2006 (online)

ABSTRACT

There are many different types of extracellular matrices in the different follicle compartments. These have different roles in follicle development and atresia, and they change in composition during these processes. This review focuses on basal lamina matrix in particular, and considers follicular fluid, the newly identified focimatrix, and thecal matrices. When follicles commence growing, the follicular basal lamina changes in its composition from containing all six α chains of type IV collagen to only α1 and α2. Perlecan and nidogen-1 and -2 subsequently become components of the follicular basal lamina, and there is an increase in the amount of laminin chains α1, β2, and γ1, in the bovine at least. Late in follicular development and on atresia some follicles contain laminin α2. On atresia the follicular basal lamina is not degraded, as occurs in ovulation, but can be breached by cells from the thecal layer when it is not aligned by granulosa cells. A novel type of basal lamina-like matrix, called focimatrix (abbreviated from focal intraepithelial matrix), develops between the cells of the membrana granulosa as aggregates of basal lamina material. It does not envelop cells and so cannot perform functions of basal lamina as currently understood. It is hypothesized that focimatrix assists or initiates depolarization of the membrana granulosa necessary for the transformation into luteal cells. The largest osmotically active molecules in follicular fluid are hyaluronan and chondroitin sulfate proteoglycans, including versican and inter-α trypsin inhibitor. It has been suggested that these might be responsible for the formation of follicular fluid by creating an osmotic gradient across the follicular wall. The formation, development, and then either ovulation or regression of follicles requires considerable tissue remodeling, cellular replication, and specialization. The expectation of researchers is that extracellular matrix will be intimately involved in many of these processes. Much research has focused in identifying the components of extracellular matrix and associated developmental changes. We review the components of extracellular matrix associated with follicular development, including the basal lamina, focimatrix, follicular fluid, and matrix of the thecal layers.

REFERENCES

  • 1 Timpl R, Brown J C. Supramolecular assembly of basement membranes.  Bioessays. 1996;  18(2) 123-132
  • 2 Paulsson M. Basement membrane proteins: structure, assembly, and cellular interactions.  Crit Rev Biochem Mol Biol. 1992;  27(1-2) 93-127
  • 3 Schymeinsky J, Nedbal S, Miosge N et al.. Gene structure and functional analysis of the mouse nidogen-2 gene: nidogen-2 is not essential for basement membrane formation in mice.  Mol Cell Biol. 2002;  22(19) 6820-6830
  • 4 Bhattacharya G, Kalluri R, Orten D J, Kimberling W J, Cosgrove D. A domain-specific usherin/collagen IV interaction may be required for stable integration into the basement membrane superstructure.  J Cell Sci. 2004;  117 233-242
  • 5 Bhattacharya G, Cosgrove D. Evidence for functional importance of usherin/fibronectin interactions in retinal basement membranes.  Biochemistry. 2005;  44(34) 11518-11524
  • 6 Pearsall N, Bhattacharya G, Wisecarver J, Adams J, Cosgrove D, Kimberling W. Usherin expression is highly conserved in mouse and human tissues.  Hear Res. 2002;  174(1-2) 55-63
  • 7 Hay E. Cell Biology of Extracellular Matrix. New York; Plenum Press 1991
  • 8 Sado Y, Kagawa M, Naito I et al.. Organization and expression of basement membrane collagen IV genes and their roles in human disorders.  J Biochem (Tokyo). 1998;  123(5) 767-776
  • 9 Aumailley M, Bruckner-Tuderman L, Carter W G et al.. A simplified laminin nomenclature.  Matrix Biol. 2005;  24(5) 326-332
  • 10 Luck M R. The gonadal extracellular matrix.  Oxf Rev Reprod Biol. 1994;  16 33-85
  • 11 Rodgers R J, Irving-Rodgers H F, van Wezel I L. Extracellular matrix in ovarian follicles.  Mol Cell Endocrinol. 2000;  163(1-2) 73-79
  • 12 Shalgi R, Kraicer P, Rimon A, Pinto M, Soferman N. Proteins of human follicular fluid: the blood-follicle barrier.  Fertil Steril. 1973;  24(6) 429-434
  • 13 Hess K A, Chen L, Larsen W J. The ovarian blood follicle barrier is both charge- and size-selective in mice.  Biol Reprod. 1998;  58(3) 705-711
  • 14 McArthur M E, Irving-Rodgers H F, Byers S, Rodgers R J. Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles.  Biol Reprod. 2000;  63(3) 913-924
  • 15 Rodgers H F, Irvine C M, van Wezel I L et al.. Distribution of the alpha1 to alpha6 chains of type IV collagen in bovine follicles.  Biol Reprod. 1998;  59(6) 1334-1341
  • 16 Rodgers R J, van Wezel I L, Irving-Rodgers H F, Lavranos T C, Irvine C M, Krupa M. Roles of extracellular matrix in follicular development.  J Reprod Fertil. 1999;  54(suppl) 343-352
  • 17 Frojdman K, Pelliniemi L J, Virtanen I. Differential distribution of type IV collagen chains in the developing rat testis and ovary.  Differentiation. 1998;  63(3) 125-130
  • 18 van Wezel I L, Rodgers H F, Rodgers R J. Differential localization of laminin chains in bovine follicles.  J Reprod Fertil. 1998;  112(2) 267-278
  • 19 Champliaud M F, Virtanen I, Tiger C F, Korhonen M, Burgeson R, Gullberg D. Posttranslational modifications and beta/gamma chain associations of human laminin alpha1 and laminin alpha5 chains: purification of laminin-3 from placenta.  Exp Cell Res. 2000;  259(2) 326-335
  • 20 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(1) 97-106
  • 21 Erickson A C, Couchman J R. Still more complexity in mammalian basement membranes.  J Histochem Cytochem. 2000;  48(10) 1291-1306
  • 22 Erickson A C, Couchman J R. Basement membrane and interstitial proteoglycans produced by MDCK cells correspond to those expressed in the kidney cortex.  Matrix Biol. 2001;  19(8) 769-778
  • 23 Irving-Rodgers H F, Catanzariti K D, Aspden W J, D'Occhio M J, Rodgers R J. Remodeling of extracellular matrix at ovulation of the bovine ovarian follicle.  Mol Reprod Dev. 2006;  , In press
  • 24 Irving-Rodgers H F, Rodgers R J. Granulosa cell expression of basal lamina matrices: Call-Exner bodies and focimatrix.  Ital J Anat Embryol. 2005;  110(suppl 1) 225-230
  • 25 Bader B L, Smyth N, Nedbal S et al.. Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice.  Mol Cell Biol. 2005;  25(15) 6846-6856
  • 26 Jiang X, Couchman J R. Perlecan and tumor angiogenesis.  J Histochem Cytochem. 2003;  51(11) 1393-1410
  • 27 Govindraj P, West L, Smith S, Hassell J R. Modulation of FGF-2 binding to chondrocytes from the developing growth plate by perlecan.  Matrix Biol. 2006;  25(4) 232-239
  • 28 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(3) 463-471
  • 29 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(2) 249-257
  • 30 Carnegie J A. Secretion of fibronectin by rat granulosa cells occurs primarily during early follicular development.  J Reprod Fertil. 1990;  89(2) 579-589
  • 31 Zhao Y, Luck M R. Gene expression and protein distribution of collagen, fibronectin and laminin in bovine follicles and corpora lutea.  J Reprod Fertil. 1995;  104(1) 115-123
  • 32 Irving-Rodgers H, Rodgers R. A novel basal lamina matrix of stratified epithelia.  Matrix Biol. 2004;  23 207-217
  • 33 Sorokin L M, Pausch F, Durbeej M, Ekblom P. Differential expression of five laminin alpha (1-5) chains in developing and adult mouse kidney.  Dev Dyn. 1997;  210(4) 446-462
  • 34 Lefebvre O, Sorokin L, Kedinger M, Simon-Assmann P. Developmental expression and cellular origin of the laminin alpha2, alpha4, and alpha5 chains in the intestine.  Dev Biol. 1999;  210(1) 135-150
  • 35 van Wezel I L, Irving-Rodgers H F, Sado Y, Ninomiya Y, Rodgers R J. Ultrastructure and composition of Call-Exner bodies in bovine follicles.  Cell Tissue Res. 1999;  296(2) 385-394
  • 36 Irving-Rodgers H F, Harland M L, Rodgers R J. A novel basal lamina matrix of the stratified epithelium of the ovarian follicle.  Matrix Biol. 2004;  23(4) 207-217
  • 37 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(4) 1025-1034
  • 38 Irving-Rodgers H F, van Wezel I L, Mussard M L, Kinder J E, Rodgers R J. Atresia revisited: two basic patterns of atresia of bovine antral follicles.  Reproduction. 2001;  122(5) 761-775
  • 39 Eriksen G V, Carlstedt I, Morgelin M, Uldbjerg N, Malmstrom A. Isolation and characterization of proteoglycans from human follicular fluid.  Biochem J. 1999;  340 613-620
  • 40 Nagyova E, Camaioni A, Prochazka R, Salustri A. Covalent transfer of heavy chains of inter-alpha-trypsin inhibitor family proteins to hyaluronan in in vivo and in vitro expanded porcine oocyte-cumulus complexes.  Biol Reprod. 2004;  71(6) 1838-1843
  • 41 Clarke H G, Hope S A, Byers S, Rodgers R J. Identification of osmotically-active proteoglycans for formation of mammalian ovarian follicular fluid.  Reproduction. 2006;  132(1) 119-131
  • 42 Chen L, Mao S J, Larsen W J. Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-alpha-trypsin inhibitor family.  J Biol Chem. 1992;  267(17) 12380-12386
  • 43 Rugg M S, Willis A C, Mukhopadhyay D et al.. Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan.  J Biol Chem. 2005;  280(27) 25674-25686
  • 44 Odum L, Jessen T E, Andersen C Y. Glycosaminoglycan-bound and free inter-alpha-trypsin inhibitor components of follicular fluid.  Zygote. 2001;  9(4) 283-288
  • 45 Kobayashi H, Sun G W, Terao T. Immunolocalization of hyaluronic acid and inter-alpha-trypsin inhibitor in mice.  Cell Tissue Res. 1999;  296(3) 587-597
  • 46 Irving-Rodgers H F, Rodgers R J. Extracellular matrix in ovarian follicular development and disease.  Cell Tissue Res. 2005;  322(1) 89-98
  • 47 Russell D L, Ochsner S A, Hsieh M, Mulders S, Richards J S. Hormone-regulated expression and localization of versican in the rodent ovary.  Endocrinology. 2003;  144(3) 1020-1031
  • 48 Saito H, Kaneko T, Takahashi T, Kawachiya S, Saito T, Hiroi M. Hyaluronan in follicular fluids and fertilization of oocytes.  Fertil Steril. 2000;  74(6) 1148-1152
  • 49 Salustri A, Yanagishita M, Underhill C B, Laurent T C, Hascall V C. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle.  Dev Biol. 1992;  151(2) 541-551
  • 50 Schoenfelder M, Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle.  Biol Reprod. 2003;  69(1) 269-277
  • 51 Alexopoulos E, Shahid J, Ongley H Z, Richardson M C. Luteinized human granulosa cells are associated with endogenous basement membrane-like components in culture.  Mol Hum Reprod. 2000;  6(4) 324-330
  • 52 Yamada S, Fujiwara H, Honda T et al.. Human granulosa cells express integrin alpha2 and collagen type IV: possible involvement of collagen type IV in granulosa cell luteinization.  Mol Hum Reprod. 1999;  5(7) 607-617
  • 53 Sutovsky P, Flechon J E, Pavlok A. F-actin is involved in control of bovine cumulus expansion.  Mol Reprod Dev. 1995;  41(4) 521-529
  • 54 Rodgers R J, Irving-Rodgers H F, van Wezel I L, Krupa M, Lavranos T C. Dynamics of the membrana granulosa during expansion of the ovarian follicular antrum.  Mol Cell Endocrinol. 2001;  171(1-2) 41-48
  • 55 Rodgers R J, Irving Rodgers H F. Extracellular matrix of the bovine ovarian membrana granulosa.  Mol Cell Endocrinol. 2002;  191(1) 57-64
  • 56 Crissman J D, Hart W R. Ovarian sex cord tumors with annular tubules. An ultrastructural study of three cases.  Am J Clin Pathol. 1981;  75(1) 11-17
  • 57 Chalvardjian A, Derzko C. Gynandroblastoma: its ultrastructure.  Cancer. 1982;  50(4) 710-721
  • 58 Motta P, Nesci E. The “Call and Exner bodies” of mammalian ovaries with reference to the problem of rosette formation.  Arch Anat Microsc Morphol Exp. 1969;  58(3) 283-290
  • 59 Motta P. On the ultrastructure of “Call-Exner bodies” in the rabbit ovary [in French].  Z Zellforsch Mikrosk Anat. 1965;  68(3) 308-319
  • 60 Motta P. Research on the formation of “follicular fluid” in the rabbit ovary.  Biol Lat. 1965;  18(4) 341-357
  • 61 Gosden R G, Brown N, Grant K. Ultrastructural and histochemical investigations of Call-Exner bodies in rabbit Graafian follicles.  J Reprod Fertil. 1989;  85(2) 519-526
  • 62 Luck M R, Zhao Y, Silvester L M. Identification and localization of collagen types I and IV in the ruminant follicle and corpus luteum.  J Reprod Fertil. 1995;  49(suppl) 517-521
  • 63 Iwahashi M, Muragaki Y, Ooshima A, Nakano R. Type VI collagen expression during growth of human ovarian follicles.  Fertil Steril. 2000;  74(2) 343-347
  • 64 De Candia L M, Rodgers R J. Characterization of the expression of the alternative splicing of the ED-A, ED-B and V regions of fibronectin mRNA in bovine ovarian follicles and corpora lutea.  Reprod Fertil Dev. 1999;  11(6) 367-377
  • 65 Colman-Lerner A, Fischman M L, Lanuza G M, Bissell D M, Kornblihtt A R, Baranao J L. Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development.  Endocrinology. 1999;  140(6) 2541-2548

 Dr.
R.J. Rodgers

Research Centre for Reproductive Health, Discipline of Obstetrics and Gynaecology

University of Adelaide, Adelaide, South Australia 5005, Australia

Email: ray.rodgers@adelaide.edu.au

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