Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T20:25:50.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Sphingosine-1-phosphate and ceramide are associated with health and atresia of bovine ovarian antral follicles

Published online by Cambridge University Press:  23 September 2014

C. G. Hernández-Coronado ,
A. Guzmán ,
R. Espinosa-Cervantes ,
M. C. Romano ,
J. R. Verde-Calvo  and
A. M. Rosales-Torres
C. G. Hernández-Coronado
Affiliation:
Departamento Producción Agrícola y Animal, Universidad Autónoma Metropolitana-Xochimilco, Calzada del Hueso 1100, CP 04960, México D.F., México
A. Guzmán
Affiliation:
Departamento Producción Agrícola y Animal, Universidad Autónoma Metropolitana-Xochimilco, Calzada del Hueso 1100, CP 04960, México D.F., México
R. Espinosa-Cervantes
Affiliation:
Departamento Producción Agrícola y Animal, Universidad Autónoma Metropolitana-Xochimilco, Calzada del Hueso 1100, CP 04960, México D.F., México
M. C. Romano
Affiliation:
CINVESTAV, I.P.N. Departamento de Fisiología, Biofísica y Neurociencias, Av. Instituto Politécnico Nacional 2508, Código Postal 07360, México D.F., México
J. R. Verde-Calvo
Affiliation:
Universidad Autónoma Metropolitana-Iztapalapa, Departamento de Biotecnología, San Rafael Atlixco 186, CP 09340, México D.F., México
A. M. Rosales-Torres*
Affiliation:
Departamento Producción Agrícola y Animal, Universidad Autónoma Metropolitana-Xochimilco, Calzada del Hueso 1100, CP 04960, México D.F., México
*
†E-mail: [email protected]
Get access

Abstract

The follicle destiny towards ovulation or atresia is multi-factorial in nature and involves outcries, paracrine and endocrine factors that promote cell proliferation and survival (development) or unchain apoptosis as part of the atresia process. In several types of cells, sphingosine-1-phospate (S1P) promotes cellular proliferation and survival, whereas ceramide (CER) triggers cell death, and the S1P/CER ratio may determine the fate of the cell. The aim of present study was to quantify S1P and CER concentrations and their ratio in bovine antral follicles of 8 to 17 mm classified as healthy and atretic antral follicles. Follicles were dissected from cow ovaries collected from a local abattoir. The theca cell layer, the granulosa cells and follicular fluid were separated, and 17β-estradiol (E2) and progesterone (P4) concentrations were measured in the follicular fluid by radioimmunoassay. Based on the E2/P4 ratio, the follicles were classified as healthy (2.2±0.3) or atretic (0.2±0.3). In both follicular compartments (granulosa and theca cell layer), sphingolipids were extracted and S1P and CER concentrations were quantified by HPLC (XTerra RP18; 5 µm, 3.0×150 mm column). Results showed that in both follicular compartments, S1P concentrations were higher in healthy antral follicles than in atretic antral follicles (P<0.05). The concentration of CER in the granulosa cells was higher in atretic antral follicles than in healthy antral follicles, but no differences were observed in the theca cell layer. The S1P/CER ratio in both follicular compartments was also higher in healthy antral follicles. Interestingly, in these follicles, there was a 45-fold greater concentration of S1P than CER in the granulosa cells (P<0.05), whereas in the theca cell layer, S1P had only a 14-fold greater concentration than CER when compared with atretic antral follicles. These results suggest that S1P plays a role in follicle health, increasing cellular proliferation and survival. In contrast, reduction of S1P and the S1P/CER in the antral follicle could trigger cellular death and atresia.

Keywords

bovineantral follicleatresiaceramidesphingosine-1-phospohate
Type
Research Article
Information
animal , Volume 9 , Issue 2 , February 2015 , pp. 308 - 312
Copyright
© The Animal Consortium 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aerts, JM and Bols, PE 2010. Ovarian folicular dynamics. A review with emphasis of the bovine species. Part II: antral development, exogenous influence and future prospects. Reproduction in Domestic Animals 45, 180–187.CrossRefGoogle Scholar
Argraves, KM, Wilkerson, BA and Argraves, WS 2010. Sphingosine-1-phosphate signaling in vasculogenesis and angiogénesis. World Journal of Biological Chemistry 1, 291–297.CrossRefGoogle ScholarPubMed
Baran, Y, Salas, A, Senkal, CE, Gunduz, U, Bielawski, J, Obeid, LM and Ogretmen, B 2007. Alterations of ceramide/sphingosine 1-phosphate rheostat involved in the regulation of resistance to imatinib-induced apoptosis in K562 human chronic myeloid leukemia cells. The Journal of Biological Chemistry 282, 10922–10934.CrossRefGoogle ScholarPubMed
Bielawski, J, Szulc, ZM, Hannun, YA and Bielawska, A 2006. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39, 82–91.CrossRefGoogle ScholarPubMed
Breslow, DK and Weissman, JS 2010. Membranes in balance: mechanisms of sphingolipid homeostasis. Molecular Cell 40, 267–279.CrossRefGoogle ScholarPubMed
Burke, CR, Cárdenas, H, Mussard, ML and Day, ML 2005. Histological and steroidogenic changes in dominant ovarian follicles during oestradiol-induced atresia in heifers. Reproduction 129, 611–620.CrossRefGoogle ScholarPubMed
Chmura, SJ, Nodzenski, E, Crane, MA, Virudachalam, S, Hallahan, DE, Weichselbaum, RR and Quintans, J 1996. Cross-talk between ceramide and PKC activity in the control of apoptosis in WEHI-231. Advances in Experimental Medicine and Biology 406, 39–55.CrossRefGoogle ScholarPubMed
Chowdhury, I, Branch, A, Olatinwo, M, Thomas, K, Matthews, R and Thompson, WE 2011. Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells. Life Sciences 89, 295–303.CrossRefGoogle ScholarPubMed
Clark, LJ, Irving-Rodgers, HF, Dharmarajan, AM and Rodgers, JL 2004. Theca interna: the other side of bovine follicular atresia. Biology of Reproduction 7, 1071–1078.CrossRefGoogle Scholar
Diab, KJ, Adamowicz, JJ, Kamocki, K, Rush, NI, Garrison, J, Gu, Y, Schweitzer, KS, Skobeleva, A, Rajashekhar, G, Hubbard, WC, Berdyshev, EV and Petrache, I 2010. Stimulation of sphingosine 1-phosphate signaling as an alveolar cell survival strategy in emphysema. American Journal of Respiratory and Critical Care Medicine 181, 344–352.CrossRefGoogle ScholarPubMed
Donati, C, Cencetti, F, Nincheri, P, Bernacchioni, C, Brunelli, S, Clementi, E, Cossu, G and Bruni, P 2007. Sphingosine 1-phosphate mediates proliferation and survival of mesoangioblasts. Stem Cells 25, 1713–1719.CrossRefGoogle ScholarPubMed
Evans, AC, Ireland, JL, Winn, ME, Lonergan, P, Smith, GW, Coussens, PM and Ireland, JJ 2004. Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle. Biology of Reproduction 70, 1475–1484.CrossRefGoogle ScholarPubMed
Fortune, JE, Rivera, GM, Evans, ACO and Turzillo, AM 2001. Differentiation of dominant versus subordinate follicles in cattle. Biology of Reproduction 65, 648–654.CrossRefGoogle ScholarPubMed
Fraser, HM 2006. Regulation of the ovarian follicular vasculature. Reproductive Biology and Endocrinology 4, 1477–7827.CrossRefGoogle ScholarPubMed
Gupta, C, Chapekar, T, Chhabra, Y, Singh, P, Sinha, S and Luthra, K 2012. Differential response to sustained stimulation by hCG & LH on goat ovarian granulosa cells. The Indian Journal of Medical Reseach 135, 331–340.Google ScholarPubMed
Husari, AW, Dbaibo, GS, Bitar, H, Khayat, A, Panjarian, S, Nasser, M, Bitar, FF, El-Sabban, M, Zaatari, G and Mroueh, SM 2006. Apoptosis and the activity of ceramide, Bax and Bcl-2 in the lungs of neonatal rats exposed to limited and prolonged hyperoxia. Respiratory Research 7, 100. doi:10.1186/1465-9921-7-100, Published only by Division of Pulmonary and Critical Care Medicine Press 26 July 2006.CrossRefGoogle ScholarPubMed
Igarashi, J and Michel, T 2008. The enigma of sphingosine 1-phosphate synthesis: a novel role for endothelial sphingosine kinases. Circulation Research 102, 630–632.CrossRefGoogle ScholarPubMed
Kotelevets, N, Fabbro, D, Huwiler, A and Zangemeister-Wittke, U 2012. Targeting sphingosine kinase 1 in carcinoma cells decreases proliferation and survival by compromising PKC activity and cytokinesis. PLoS One 7, e39209.CrossRefGoogle ScholarPubMed
Martelli, A, Bernabó, N, Berardinelli, P, Russo, V, Rinaldi, C, Di Giacinto, O, Mauro, A and Barboni, B 2009. Vascular supply as a discriminating factor for pig preantral follicle selection. Reproduction 37, 45–58.CrossRefGoogle Scholar
Merrill, AH, Wang, E, Mullins, RE, Jamison, WCL, Nimkar, S and Liotta, DC 1988. Quantitation of free sphingosine in liver by high-performance liquid chromatograph. Analytical Biochemistry 171, 373–381.CrossRefGoogle Scholar
Mihm, M, Baker, P, Ireland, J, Smith, G, Coussens, P, Evans, A and Ireland, J 2006. Molecular evidence that growth of dominant follicles involves a reduction in follicle-stimulating hormone dependence and an increase in luteinizing hormone dependence in cattle. Biology of Reproduction 74, 1051–1059.CrossRefGoogle Scholar
Morales, A, Lee, H, Goñi, FM, Kolesnick, F and Fernández-Checa, JC 2007. Sphingolipids and cell death. Apoptosis 12, 923–939.CrossRefGoogle ScholarPubMed
Mulders, ACM, Peters, SLM and Michel, MC 2007. Sphingomyelin metabolism and endothelial cell function. European Heart Journal 28, 777–779.CrossRefGoogle ScholarPubMed
Pettus, BJ, Chalfant, CE and Hannun, YA 2002. Ceramide in apoptosis: an overview and current perspectives. Biochimica et Biophysica Acta – Molecular and Cell Biology of Lipids 1585, 114–125.CrossRefGoogle ScholarPubMed
Quirk, SM, Cowan, RG, Harman, RM, Hu, CL and Porter, DA 2004. Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. Journal of Animal Science 82, 40–52.CrossRefGoogle ScholarPubMed
Rodgers, RJ and Irving-Rodgers, HF 2010. Morphological classification of bovine ovarian follicles. Reproduction 139, 309–318.CrossRefGoogle ScholarPubMed
Rosales-Torres, AM and Guzmán, SA 2008. Apoptosis in follicular atresia and luteal regression. Review. Técnica Pecuaria México 46, 159–182.Google Scholar
Rosales-Torres, AM, Guzmán, SA and Gutiérrez, AC 2012. Follicular development in domestic ruminants. Tropical and Subtropical Agroecosystems 1, 147–160.Google Scholar
Rosales-Torres, AM, Ávalos-Rodríguez, A, Vergara-Onofre, M, Hernández-Pérez, O, Ballesteros, LM, García-Macedo, R, Ortíz-Navarrete, V and Rosado, A 2000. Multiparametric study of atresia in ewe antral follicles: histology, flow citometry, internucleosomal DNA fragmentation, and lysosomal enzyme activities in granulosa cells and folicular fluid. Molecular Reproduction and Development 55, 270–281.3.0.CO;2-H>CrossRefGoogle Scholar
Rosales-Torres, AM, Alonso, I, Vergara, M, Romano, MC, Castillo-Juárez, H, Avalos, A, Rosado, A and Gutiérrez, CG 2010. Vascular endothelial growth factor isoforms 120, 164 and 205 are reduced with atresia in ovarian follicles of sheep. Animal Reproduction Science 122, 111–117.CrossRefGoogle Scholar
Schiffmann, S, Sandner, J, Birod, K, Wobst, I, Angioni, C, Ruckhäberle, E, Kaufmann, M, Ackermann, H, Lötsch, J, Schmidt, H, Geisslinger, G and Grösch, S 2009. Ceramide synthases and ceramide levels are increased in breast cancer tissue. Carcinogenesis 30, 745–752.CrossRefGoogle ScholarPubMed
Spiegel, S and Milstien, S 2002. Sphingosine-1-phosphate: a key cell signaling molecule. The Journal of Biological Chemistry 277, 25851–25854.CrossRefGoogle ScholarPubMed
Spiegel, S and Milstien, S 2003. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nature Reviews Molecular Cell Biology 4, 397–407.CrossRefGoogle ScholarPubMed
Sterin, SN and Leocata, NF 2007. Los esfingolipidos en la muerte y proliferación celular. Química Viva 3, 112–138.Google Scholar
Tao, R, Zhang, J, Vessey, DA, Honbo, N and Karliner, JS 2007. Deletion of the sphingosine kinase-1 gene influences cell fate during hypoxia and glucose deprivation in adult mouse cardiomyocytes. Cardiovascular Research 74, 56–63.CrossRefGoogle ScholarPubMed
Villa, NY, Kupchak, BR, Garitaonandia, I, Smith, JL, Alonso, E, Alford, C, Cowart, LA, Hannun, YA and Lyons, TJ 2009. Sphingolipids function as downstream effectors of a fungal PAQR. Molecular Pharmacology 75, 866–875.CrossRefGoogle ScholarPubMed
Webb, R, Garnsworthy, P, Gong, JG and Armstrong, D 2004. Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science 82, 63–74.Google ScholarPubMed
Wulff, C, Wilson, H, Wiegand, SJ, Rudge, JS and Fraser, HM 2002. Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor Trap R1R2. Endocrinology 143, 2797–2807.CrossRefGoogle ScholarPubMed