Atresia and Apoptosis in preovulatory follicles in the ovary of Danio rerio (zebrafish)

Although apoptosis, the programmed cell death, is the main mechanism in follicular atresia and especially postovulatory regression in mammals, its role in fish ovary is still controversial. In order to discuss the possible functions of atresia as a context of apoptosis, the preovulatory follicles of the freshwater teleost, Danio rerio (zebrafish) were investigated by light microscopy. The main characteristics of atresia of vitellogenic oocytes of zebrafish were determined as a significant hypertrophy and hyperplasia of the granulosa cells. The theca cells also became slightly hyperplasic while the zona radiata was degenerated and the basal membrane located between granulosa and theca was also disintegrated. The aggregation of compacted chromatin in a crescent pattern, and cell fragmentation that indicates to formation of apoptotic bodies were evaluated as the morphological evidences for apoptosis in granulosa cells of the oocytes of zebrafish. Towards the end of atresia, the vitellus is fully degenerated and absorbed, some apoptotic bodies were also observed between the translucent clusters of theca cells. Apoptotic process was still continued when an atrium had been formed.

___

Andreu-Vieyra, C.V. and Habibi, H.R. 2000. Factors controlling ovarian apoptosis. Can. J. Physiol. Pharmacol., 78(12): 1003-1012.

Besseau, L. and Faliex, E. 1994. Resorption of unemitted gametes in Lithognathus mormyrus (Sparidae, Teleostei): a possible synergic action of somatic and immune cells. Cell Tissue Res., 276: 123-132.

Bromley, P.J., Ravier, C. and Witthames, P.R. 2000. The influence of feeding regime on sexual maturation, fecundity and atresia in first-time spawning turbot. J. Fish Biol., 56: 264-278.

Carnevali, O., Cionna, C., Tosti, L., Lubzens, E. and Maradonna, F. 2006. Role of cathepsins in ovarian follicle growth and maturation. Gen. Comp. Endocrinol., 146(3): 195-203.

Chevalier, C., De Conto, C. and Exbrayat, J.M. 2008. Apoptosis in Zingel asper (Percidae) ovarian and testicular development. Cybium, 32(2) suppl.: 228- 229.

Choi, C.Y., Takemur, A. and Takashima, F. 2000. Cellular apoptosis susceptibility gene messenger ribonucleic acid in the ovary of red sea bream: molecular cloning and correlation with acquisition of oocyte maturational competence. Fish Physiol. Biochem., 23: 119-125.

Counis, M.F. and Torriglia, A. 2000. DNAses and apoptosis. Biochem. Cell Biol.; 78: 405-414.

Çakıcı, Ö. and İşisağ Üçüncü, S. 2007. Oocyte development in the zebrafısh, Danio rerio (Teleostei: Cyprinidae). E.U. J. Fisheries Aquatic Sci., 24: 137-141.

Drummond, C.D., Bazzoli, N., Rizzo, E. and Sato, Y. 2000. Postovulatory follicle: a model for experimental studies of programmed cell death or apoptosis in teleosts. J. Exper. Zool., 287: 176-182.

Eimon, P.M., Kratz, E., Varfolomeev, E., Hymowitz, S.G., Stern, H., Zha, J. and Ashkenazi, A. 2006. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Different. 13: 1619-1630. doi:10.1038/sj.cdd.4402015.

Gonçalves, T.L., Bazzoli, N. and Brito, M.F.G. 2006. Gametogênese e reprodução do matrinxã Brycon orthotaenia (Günther, 1864) (Pisces: Characidae) do rio São Francisco, Minas Gerais. Braz. J. Biol., 66(2a). doi: 10.1590/S1519-69842006000300018.

Hacker, G. 2000. The morphology of apoptosis. Cell Tissue Res., 301: 5-17.

Hall, P.A. 1999. Assessing apoptosis: a critical survey. Endoc. Related Cancer 6: 3-8.

Hsueh, A.J.W., Billig, H. and Tsafriri, A. 1994. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endoc. Rev., 15: 707-724.

Hussein, M. 2005. Apoptosis in the ovary: molecular mechanisms. Human Reproduct. Update 11(2):162- 178; doi:10.1093/humupd/dmi001

Imsland, A.K., Folkvord, A., Grung, G.L., Stefanson, S.O. and Taranger, G.L. 1997. Sexual dimorphism in growth and maturation of turbot, Scopthalmus maximus. Aqua. Res., 28: 101-115.

Janz, D.M. and Van Der Kraak, G. 1997. Suppression of apoptosis by gonadotropin, 17b-estradiol and epidermal growth factor in trout preovulatory ovarian follicles. Gen. Comp. Endocrinol. 105: 186-193.

Johnson, A.L., Bridgham, J.T., Witty, J.P. and Till, J.L. 1996. Susceptibility of avian ovarian granulosa cells to apoptosis is dependent upon stage of follicle development and is related to endogenous levels of bcl-xlong gene expression. Endocrinology, 137: 2059- 2066.

Kagawa, H. 1991. Ultrastructural observations in the ovarian follicles of the yellowtail (Seriola quinquerdiata) during oocyte maturation and ovulation. Bull. Natl. Res. Aqua., 19: 1-10.

Kasuya, K. 1997. Elimination of apoptotic granulosa cells by ıntact granulosa cells and macrophages in atretic mature follicles of the guinea pig ovary. Archives of Histol. Cytol., 60(2): 175-184

Kennedy, A.M. 2002. Reproduction of striped bass Morone saxatilis; a structural, biochemical and functional characterization of atresia. http://www.lib.ncsu.edu/ theses/available/etd-06162002-210408/

Kerr, J.F., Wyllie, A.H. and Currie, A.R. 1972. Apoptosis: basis biological phenomenon with wide ranging implications in tissue kinetics, Brit. J. Cancer, 26: 239-257

Khoo, K.H. 1975. The corpus luteum of goldfish (Carassius auratus L.) and its functions. Can. J. Zool., 53: 1306- 1323.

MacKenzie, S., Montserrat, N., Mas, M., Acerete, L., Tort, L., Krasnov, A., Goetz, F.W. and Planas, J.V. 2006. Bacterial lipopolysaccharide induces apoptosis in the trout ovary. Reprod. Biol. Endocrinol., 4: 46. doi:10.1186/1477-7827-4-46

Markström, E., Svensson, E. Ch., Shao, R., Svanberg, B. and Billig, H. 2002. Survival factors regulating ovarian apoptosis-dependence on follicle differentiation. Reproduction, 123: 23-30.

Matsubara, T., Ohkubo, N., Andoh, T., Sullivan, C.V. and Hara, A. 1999. Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Dev. Biol., 213: 18-32.

Matsuda-Minehata, F., Inoue, N., Goto, Y. and Manabe, N. 2006. The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules. J. Reprod. Dev., 52(6): 695-705.

Miranda, A.C.L., Bazzoli, N., Rizzo, E. and Sato, Y. 1999. Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tiss. Cell., 31: 480-488.

Mylonas, C.C., Woods, II L.C, Thomas, P. and Zohar, Y. 1998. Endocrine profiles of female striped bass (Morone saxatilis) in captivity, during postvitellogenesis and induction of final oocyte maturation via controlled-release GnRHa delivery systems. Gen. Comp. Endocrinol., 110: 276-289.

Rizzo, E. and Bazzoli, N. 1995. Follicular atrezya in curimata´-pioa Prochilodus affinis Reinhardt, 1874 (Pisces, Characiformes). Rev. Bras. de Biol., 55: 697- 703.

Saidapur, S.K. 1978. Follicular atresia in the ovaries of nonmammalian vertebrates. Int. Rev. Cytol., 54: 225- 244.

Santos, H.B., Rizzo, E., Bazzoli, N., Sato, Y. and 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: 1446-1459.

Santos, H.B., Sato, Moro, L.Y. Bazzoli, N. and Rizzo, E. 2008. Relationship among follicular apoptosis, integrin beta1 and collagen type IV during early ovarian regression in the teleost Prochilodus argenteus after induced spawning. Cell Tissue Res., 332(1): 159-170.

Sundaresan, N.R., Saxena, V.K., Sastry, K.V.H., Anish, D., Saxena, M.K. and Nagarajan, K. 2007. Nitric oxide: a possible mediator of ovulation and postovulatory follicle regression in chicken, Anim. Reprod. Sci., 101: 351-357

Thomé, R.G., dos Santos, H.B., Arantes, F.P., Prado, P.S., Domingos, F.T.F., Sato, Y., Bazzoli, N. and Rizzo, E. 2006. Regression of post-ovulatory follicles in Prochilodus costatus Valenciennes, 1850 (Characiformes, Prochilodontidae). Braz. J. Morphol. Sci., 23(3-4): 495-500.

Tyler, C.R., Pottinger, T.G., Santos, E., Sumpter, J.P., Price, S-A., Brooks, S. and Nagler, J.J. 1996. Mechanisms controlling egg size and number in the rainbow trout, Oncorhynchus mykiss. Biol. Reprod., 54: 8-15.

Uchida, D., Yamashita, M., Kitano, T. and Iguchi, T. 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exper. Biol., 205: 711-718.

Wallace, R.A and Selman, K. 1985. Major protein change during vitellogenesis and maturation of Fundulus oocytes. Dev. Biol., 110: 492-498.

Webb, S.J., Harrison, D.J. and Wyllie, A.H. 1997. Apoptosis: an overview of the process and its relevance in disease. Adv. Pharmacol., 41: 1-34.

Witthames, P.R., Andersson, E., Greenwood, L.N., Lyons, B., Fonn, M. and Kjesbu, O.S. 2003. Apoptosis in regressing follicles from Solea solea and Gadus morhua. Fish Physiol. Biochem., 28: 377-378.

Wood, A.W. and van Der Kraak, G. 2001. Apoptosis and ovarian function: novel perspectives from the teleosts. Biol. Reprod., 64: 264-271.

Wood, A.W. and van Der Kraak, G. 2002. Inhibition of apoptosis in vitellogenic ovarian follicles of rainbow trout (Oncorhynchus mykiss) by salmon gonadotrophin, epidermal growth factor and 17bestradiol. Mol. Reprod. Develop., 61: 511-518.

Wood, A.W. and van Der Kraak, G. 2003. Yolk proteolysis in rainbow trout oocytes after serum-free culture: Evidence for a novel biochemical mechanism of atresia in oviparous vertebrates. Mol. Reprod. Develop., 65: 219-227.

Zelennikov, O.V. 1997. The effect of acidification on oogenesis of rainbow trout during sex differentiation. J. Fish Biol., 50: 18-21.

Zwain, I.H. and Amato, P. 2001. cAMP-induced apoptosis in granulosa cells is associated with upregulation of p53 and bax and down-regulation of clusterin. Endocrine Res.; 27(1-2):233-249.
Turkish Journal of Fisheries and Aquatic Sciences-Cover
  • ISSN: 1303-2712
  • Başlangıç: 2015
  • Yayıncı: Su Ürünleri Merkez Araştırma Enstitüsü - Trabzon
Sayıdaki Diğer Makaleler

Morphological plasticity of dominant Species in response to nutrients dynamics in Bidighinzu reservoir of Sardinia, Italy

Yelda AKTAN, Antonella LUGLIE, Nicola SECHI

Cellular architecture and functional aspects of the olfactory rosette of Wallago attu (Bleeker)

Saroj Kumar GHOSH, Padmanabha CHAKRABARTI

The effect of pingers on harbour porpoise, Phocoena phocoena bycatch and fishing effort in the turbot gill Net fishery in the Turkish Black Sea coast

Sedat GÖNENER, SABRİ BİLGİN

Development of fingerling production techniques in nursery ponds for the critically endangered reba carp, Cirrhinus ariza (Hamilton, 1807)

M. Aminur RAHMAN, M. ZAHER, K.M. AZİMUDDİN

Behavioural responses of the freshwater Fish, cyprinus carpio (Linnaeus) following sublethal exposure to chlorpyrifos

Ramesh HALAPPA, Muniswamy DAVID

Sensitivity of bacteria isolated from fish to some medicinal plants

HAKAN TÜRKER, Arzu Birinci YILDIRIM, FATMA PEHLİVAN KARAKAŞ

Morphometric, meristic characteristics and conservation of the threatened fish, Puntius sarana (Hamilton, 1822) (Cyprinidae) in the Ganges River, northwestern Bangladesh

Md. Yeamin HOSSAIN, Jun OHTOMI, Zoarder Faruque AHMED

New record for the east Mediterranean, Dardanelles (Turkey) and its distribution: Polysiphonia morrowii Harvey (Ceramiales, Rhodophyta)

HÜSEYİN ERDUĞAN, CÜNEYT AKI, Okan ACAR, Berrin DURAL, Veysel AYSEL

Estimation of stream temperature in Degirmendere river (Trabzon- Turkey) using Artificial Neural Network model

Nüket SİVRİ, H. Kurtuluş ÖZCAN, O. Nuri UÇAN, Orkun AKİNCİLAR

Assessing the habitat structure for common snook (Centropomus undecimalis bloch, 1792) and Tarpon (Megalops atlanticus valenciennes, 1847) in Santa Teresa lagoons, Puerto Rico

Orlando JOSE, Ferrer MONTANO