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.
KEYWORDS
Ovary - follicle - extracellular matrix - basal lamina - focimatrix - laminin - collagen type IV - nidogen - collagen type XVIII - usherin
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