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Journal of Molecular Histology

, Volume 41, Issue 4–5, pp 215–224 | Cite as

Distribution of laminin β2, collagen type IV, fibronectin and MMP-9 in ovaries of the teleost fish

  • Ralph Thomé
  • Hélio Batista dos Santos
  • Yoshimi Sato
  • Elizete Rizzo
  • Nilo Bazzoli
Original Paper

Abstract

Extracellular matrix in the ovarian follicle has been characterised for several mammalian species but there are no reports that describe the immunolocalisation of the extracellular matrix elements, matrix metalloproteinases, and its relation to plasma 17β estradiol levels and follicular apoptosis during the teleost’s reproductive cycle. The present study used immunohistochemistry to characterise the distribution of laminin β2, collagen type IV, fibronectin and matrix metalloproteinases-9 (MMP-9). The TUNEL in situ technique was used to quantify apoptosis and indirect immunofluorimetric to determine plasma 17β estradiol levels. The TUNEL-positive reaction associated with morphological features exhibited follicular apoptosis. During postovulatory follicle involution, the drop in plasma 17β estradiol levels after spawning contributed to the intense apoptosis observed. By immunohistochemical analysis, laminin β2 and collagen type IV were identified as the major constituents of the basement membrane. The loss of integrity of the basement membrane occurred due to lyses of the major constituents, and coincides with increased follicular apoptosis. The integrity of the basement membrane is important for the survival of follicular cells. Furthermore, the MMP-9 results suggest that this enzyme is involved in final oocyte maturation and regression of postovulatory follicles. Fibronectin was observed on the surface of follicular cells of the postovulatory follicle in P. argenteus, this being important for maintaining normal cell adhesion to extracellular matrix. In conclusion, our results suggest that the structure and composition of the extracellular matrix, and plasma 17β estradiol levels related to apoptosis, play an important role during the follicular development and post-spawning involution in teleost fishes.

Keywords

Apoptosis 17β estradiol Extracellular matrix Matrix metalloproteinases Ovarian follicle 

Notes

Acknowledgment

This work was supported by CNPq, FAPEMIG, CAPES and CODEVASF.

References

  1. Berkholtz CB, Lai BE, Woodruff TK, Shea LD (2006a) Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochem Cell Biol 126:583–592CrossRefPubMedGoogle Scholar
  2. Berkholtz CB, Shea LD, Woodruff TK (2006b) Extracellular matrix functions in follicle maturation. Semin Reprod Med 24:262–269CrossRefPubMedGoogle Scholar
  3. Boudreau N, Werb Z, Bissel MJ (1996) Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci 93:3509–3513CrossRefPubMedGoogle Scholar
  4. Câmara-Pereira ES, Campos LM, Vanier-Santos MA, Mermelstein CS, Costa ML (2009) Distribution of cytoskeletal and adhesion proteins in adult zebrafish skeletal muscle. Hist Histopathol 24:187–196Google Scholar
  5. Carnegie JA (1990) Secretion of fibronectin by rat granulosa cells occurs primarily during early follicular development. J Reprod Fertil 89:579–589CrossRefPubMedGoogle Scholar
  6. Chun SY, Eisenhauer KM, Minami S, Billig H, Perlas E, Hsueh AJW (1996) Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinol 137:1447–1456CrossRefGoogle Scholar
  7. Curry TE, Osteen KG (2001) Cyclic changes in the matrix metalloproteinase system in the ovary and uterus. Biol Reprod 64:1285–1296CrossRefPubMedGoogle Scholar
  8. Curry TE, Osteen KG (2003) The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24:428–465CrossRefPubMedGoogle Scholar
  9. Drevinick PE, Sandheinrich MB, Oris JT (2006) Increased ovarian follicular apoptosis in fathead minnows (Pimephales promelas) exposed to dietary methylmercury. Aquat Toxicol 79:49–54CrossRefGoogle Scholar
  10. Drummond CD, Bazzoli N, Rizzo E, Sato Y (2000) Postovulatory follicle: a model for experimental studies of programmed cell death or apoptosis in teleost. J Exp Zool 287:176–182CrossRefPubMedGoogle Scholar
  11. Frisch SM, Francis H (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124:619–626CrossRefPubMedGoogle Scholar
  12. Grier HJ, Uribe MC, Parenti LR (2007) Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout, Oncorhynchus mykiss (Walbaum, 1972) (Teleostei, Protacanthopterygii, Salmoniformes). J Morphol 268:293–310CrossRefPubMedGoogle Scholar
  13. Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA (1995) Atresia in follicles grown after ovulation in the pig: measurement of increased apoptosis in granulosa cells and reduced follicular fluid 17β estradiol. Biol Reprod 52:920–927CrossRefPubMedGoogle Scholar
  14. Hensey C, Gauter J (1998) Programmed cell death during Xenopus development: a spatial-temporal analysis. Develop Biol 203:36–48CrossRefPubMedGoogle Scholar
  15. Hulboy DL, Rudolph LA, Matrisian LM (1997) Matrix metalloproteinases as mediators of reproductive function. Mol Hum Reprod 3:27–45CrossRefPubMedGoogle Scholar
  16. Irving-Rodgers HF, Rodgers RJ (2005) Extracellular matrix in ovarian follicular development and disease. Cell Tissue Res 322:89–98CrossRefPubMedGoogle Scholar
  17. Ito T, Kobayashi Y, Morita T, Horimoto T, Kawaoka Y (2002) Virulent influenza A viruses induce apoptosis in chickens. Virus Res 84:27–35CrossRefPubMedGoogle Scholar
  18. Iwahashi M, Muragaki Y, Ooshima A, Nakano R (2000) Type VI collagen expression during growth of human ovarian follicles. Fert Steril 74:343–347CrossRefGoogle Scholar
  19. Jalabert B (2005) Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reprod Nutr Dev 45:261–279CrossRefPubMedGoogle Scholar
  20. Janz DM, Van Der Kraak G (1997) Supression of apoptosis by gonadotropin 17β estradiol and epidermal growth factor in rainbow trout preovulatory ovarian follicles. Gen Comp Endocrinol 105:186–193CrossRefPubMedGoogle Scholar
  21. Kaptaner B, Ural G (2006) Apoptosis in postovulatory follicles of Chalcalburnus tarichi Pallas, 1811. J Fish Aquat Sci 23:263–267Google Scholar
  22. Kerr JFR, Willie AH, Currie AR (1972) Apoptosis: basis biological phenomenon with wide ranging implicatons in tissue kinetics. Br J Cancer 26:239–257PubMedGoogle Scholar
  23. Kook S, Kim DH, Shim SR, Kim H, Chun J-S, Song WK (2003) Caspase-dependent cleavage of tensin induces disruption of actin cytoskeleton during apoptosis. Biochem Biophys Res Commun 303:37–45CrossRefPubMedGoogle Scholar
  24. Korpos E, Wu C, Song J, Hallmann R, Sorokin L (2009) Role of the extracellular matrix lymphocite migration. Cell Tissue Res. doi:  10.1007/s0441-009-0853-3
  25. Korsnes MS, Hetland DL, Espenes A, Aune T (2007) Cleavage of tensin during cytoskeleton disruption in YTX-induced apoptosis. Toxicol In Vitro 21:9–15CrossRefPubMedGoogle Scholar
  26. Kulms D, DuBmann H, Poppelmann B, Stander S, Schwarz A, Schwarz T (2002) Apoptosis induced by disruption of the actin cytoskeleton is mediated via activation of CD95 (Fas/APO-1). Cell Death Differ 9:598–608CrossRefPubMedGoogle Scholar
  27. Lang DM, Romero-Aleman MM, Arbelo-Galvan J, Sturmer AO, Monzon-Mayor M (2002) Regeneration of retinal axon in the lizard Gallotia galloti is not linked to regeneration of new retinal ganglions cells. J Neurobiol 52:322–335CrossRefPubMedGoogle Scholar
  28. Le Bellego F, Pisselet C, Huet C, Monget P, Monniaux D (2002) Laminin-alpha6beta1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells. J Endocrinol 172:45–59CrossRefPubMedGoogle Scholar
  29. Matsui H, Ogiwara K, Ohkura R, Yamashita M, Takahashi T (2000) Expression of gelatinases A and B in the ovary of the medaka fish Oryzias latipes. Eur J Biochem 267:4658–4667CrossRefPubMedGoogle Scholar
  30. Narkar M, Kholkute S, Nandedkar T (2006) Hormonal regulation of apoptosis in the endometrium of common marmosets (Callithrix jacchus). Theriogenology 66:1194–1209CrossRefPubMedGoogle Scholar
  31. Ndozangue-Touriguine O, Hamelin J, Breàrd J (2008) Cytoskeleton and apoptosis. Biochem Pharmacol 76:11–18CrossRefPubMedGoogle Scholar
  32. Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T (2005) Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci 102:8442–8447CrossRefPubMedGoogle Scholar
  33. Ortiz-Delgado JB, Sarasquete C (2004) Toxicity, histopathological alterations and immunohistochemical CYP1A induction in the early life stages of the seabream, Sparus aurata, following waterborne exposure to B(a)P and TCDD. J Mol Hist 35:29–45CrossRefGoogle Scholar
  34. Quagio-Grassiotto I, Guimarães ACD (2006) Follicular ephitellium, theca and egg envelope formation in Serrasalmus spilopleura (Teleostei, Characiformes, Characidae). Acta Zool 84:121–129CrossRefGoogle Scholar
  35. Rodgers RJ, Irving-Rodgers HF, Russell DL (2003) Extracellular matrix of the developing ovarian follicle. Reproduction 126:415–424CrossRefPubMedGoogle Scholar
  36. Romagosa E, Godinho HM, Nahara MY (1985) Tipo de desova do curimbatá Prochilodus scrofa do Rio Mogi-Guaçu, Pirassununga, SP. Rev Bras Reprod Ani 8:113–120Google Scholar
  37. Santos HB, Rizzo E, Bazzoli N, Sato Y, Moro L (2005) Ovarian regression and apoptosis in the South American teleost Leporinus taeniatus Lütken (Characiformes, Anostomidae) from the São Francisco Basin. J Fish Biol 67:1446–1459CrossRefGoogle Scholar
  38. Santos JE, Padilha GEV, Bomcompagni-Júnior O, Santos GB, Rizzo E, Bazzoli N (2006) Ovarian follicle growth in the catfish Iheringichthys labrosus (Siluriformes: Pimelodidae). Tissue Cell 38:303–310CrossRefPubMedGoogle Scholar
  39. Santos HB, Sato Y, Moro L, Bazzoli N, Rizzo E (2009) Relationship among follicular apoptosis, integrin β1 and collagen type IV during early ovarian regression in the teleost Prochilodus argenteus after induced spawning. Cell Tissue Res 332:159–170CrossRefGoogle Scholar
  40. Sato Y, Cardoso EL, Godinho AL, Godinho HP (1996) Hypofysation parameters of the fish Prochilodus marggravii obtained in routine hatchery station conditions. Rev Bras Biol 56:59–64Google Scholar
  41. Senthilkumaran B, Yoshikuni M, Nagahama Y (2004) A shift in steroidogenesis occuring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215:11–18CrossRefPubMedGoogle Scholar
  42. Sharma D, Kinsey WH (2006) Fertilization triggers localized activation of Src-family protein kinases in the zebrafish egg. Develop Biol 295:604–614CrossRefPubMedGoogle Scholar
  43. Smith MF, Ricke WA, Bakke LJ, Dow MPD, Smith GW (2002) Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors. Mol Cell Endocrinol 191:45–56CrossRefPubMedGoogle Scholar
  44. Sternilicht MD, Werb Z (2001) How matrix metalloproteinase regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516CrossRefGoogle Scholar
  45. Suzukawa M, Komiya A, Iikura M, Nagase H, Yoshimura-Uchiyama C, Yamada H, Kawasaki H, Ohta K, Matsushima K, Hirai K, Yamamoto K, Yamaguchi M (2006) Trans-basement membrane migration of human basophils: role of matrix metalloproteinase-9. Int Immunol 18:1575–1583CrossRefPubMedGoogle Scholar
  46. Svoltys M, Tabarowski Z, Pawlik A (2000) Apoptosis of postovulatory cumulus granulosa cells of the rat. Anat Embryol 202:523–529CrossRefGoogle Scholar
  47. Takle H, Andersen O (2007) Caspases and apoptosis in fish. J Fish Biol 71:326–349CrossRefGoogle Scholar
  48. Thomé RG, Santos HB, Arantes FP, Prado PS, Domingos FFT, Sato Y, Bazzoli N, Rizzo E (2006) Regression of post-ovulatory follicles in Prochilodus costatus Valenciennes, 1850 (Characiformes, Prochilodontidae). Braz J Morphol Sci 23:495–500Google Scholar
  49. Thomé RG, Santos HB, Arantes FP, Domingos FFT, Bazzoli N, Rizzo E (2009) Dual roles for autophagy during follicular atresia in fish ovary. Autophagy 5:1–3CrossRefGoogle Scholar
  50. Van Wezel IL, Rodgers HF, Rodgers RJ (1998) Differencial localization of laminin chains in the bovine follicle. J Reprod Fertil 112:1334–1341Google Scholar
  51. Zhao Y, Luck MR (1995) Gene expression and protein distribution of collagen, fibronectin and laminin in bovine follicles and corpora lutea. J Reprod Fertil 104:115–123CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Ralph Thomé
    • 1
  • Hélio Batista dos Santos
    • 1
  • Yoshimi Sato
    • 2
  • Elizete Rizzo
    • 1
  • Nilo Bazzoli
    • 3
  1. 1.Universidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Estação de Hidrobiologia e Piscicultura de Três Marias (CODEVASF)Três MariasBrazil
  3. 3.Programa de Pós graduação em Zoologia de Vertebrados (PUC-minas)Belo HorizonteBrazil

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