Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes
Dorit Kalo A and Zvi Roth A B
+ Author Affiliations
- Author Affiliations
A Department of Animal Sciences, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University, Rehovot 76100, Israel.
B Corresponding author. Email: roth@agri.huji.ac.il
Reproduction, Fertility and Development 23(7) 876-888 https://doi.org/10.1071/RD10330
Submitted: 4 December 2010 Accepted: 30 March 2011 Published: 19 August 2011
Abstract
Programmed cell death via the sphingomyelin pathway has been suggested to underlie heat-shock disturbance of oocyte developmental competence. A series of experiments were performed to characterise the role of the sphingolipid ceramide in heat-shock-induced apoptosis, and to determine whether ceramide formation can be regulated. Bovine cumulus–oocyte complexes (COCs) were aspirated from ovaries collected in the cold season (November–April), in vitro-matured, fertilised and cultured for 8 days. Exposure of COCs to heat shock (41°C) during maturation reduced cleavage rate and blastocyst formation relative to the control group (38.5°C). Annexin-V binding (V-FITC assay), which is associated with the early apoptotic event of membrane phosphatidylserine turnover, was higher in oocytes exposed to short-term versus long-term heat shock, suggesting that heat-shock-induced apoptosis involves membrane alterations. Similar to heat exposure, oocyte maturation with C2-ceramide had a dose-dependent deleterious effect on the first cleavages and subsequent embryonic development in association with increased annexin-V binding. Blocking endogenous ceramide generation with fumonisin B1, a specific inhibitor of dihydroceramide synthase (i.e. de novo formation), moderated, to some extent, the effects of heat shock on oocyte developmental competence, suggesting that ceramide plays an important role in heat-shock-induced apoptosis.
Additional keywords: Annexin, developmental competence, fumonisin B1, phosphatidylserine.
References
Allen, R. T., Hunter, W. J., and Agrawal, D. K. (1997). Morphological and biochemical characterization and analysis of apoptosis. J. Pharmacol. Toxicol. Methods 37, 215–228.| Morphological and biochemical characterization and analysis of apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls12lsLk%3D&md5=e2a5c29481a968c3f856914a97e85cbdCAS | 9279777PubMed |
Andrieu-Abadie, N., and Levade, T. (2002). Sphingomyelin hydrolysis during apoptosis. Biochim. Biophys. Acta 1585, 126–134.
| 1:CAS:528:DC%2BD3sXivVOqtw%3D%3D&md5=6e3e967df2bae5a01701556b045e26f2CAS | 12531545PubMed |
Anguita, B., Vandaele, L., Mateusen, B., Maes, D., and Van Soom, A. (2007). Developmental competence of bovine oocytes is not related to apoptosis incidence in oocytes, cumulus cells and blastocysts. Theriogenology 67, 537–549.
| Developmental competence of bovine oocytes is not related to apoptosis incidence in oocytes, cumulus cells and blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlyrsQ%3D%3D&md5=b4f4c1112e2c243c4a20b12cca8dd33eCAS | 17007918PubMed |
Arana, L., Gangoiti, P., Ouro, A., Trueba, M., and Gómez-Muñoz, A. (2010). Ceramide and ceramide 1-phosphate in health and disease. Lipids Health Dis. 9, 15.
| Ceramide and ceramide 1-phosphate in health and disease.Crossref | GoogleScholarGoogle Scholar | 20137073PubMed |
Arav, A. (2001). Transillumination increases oocyte recovery from ovaries collected at slaughter. A new technique report. Theriogenology 55, 1561–1565.
| Transillumination increases oocyte recovery from ovaries collected at slaughter. A new technique report.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3ls1SgsQ%3D%3D&md5=17726e6b888f5a4cb10e927548957365CAS | 11354714PubMed |
Balasubramanian, K., Mirnikjoo, B., and Schroit, A. J. (2007). Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J. Biol. Chem. 282, 18357–18364.
| Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsVOksrg%3D&md5=b25597937749dd051325073c79b404f4CAS | 17470427PubMed |
Bielawska, A., Crane, H. M., Liotta, D., Obeid, L. M., and Hannun, Y. A. (1993). Selectivity of ceramide-mediated biology. J. Biol. Chem. 268, 26226–26232.
| 1:CAS:528:DyaK3sXmsVKmu7k%3D&md5=8d73a07da5a0ab4680cb68e23a25ba79CAS | 8253743PubMed |
Birbes, H., Bawab, E. l., Obeid, L. M., and Hannun, Y. A. (2002). Mitochondria and ceramide: intertwined roles in regulation of apoptosis. Adv. Enzyme Regul. 42, 113–129.
| Mitochondria and ceramide: intertwined roles in regulation of apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslyjsw%3D%3D&md5=124d76a6f8c8b7c73182442bfa5e2cc1CAS | 12123710PubMed |
Chan, A., Reiter, R., Wiese, S., Fertig, G., and Gold, R. (1998). Plasma membrane phospholipid asymmetry precedes DNA fragmentation in different apoptotic cell models. Histochem. Cell Biol. 110, 553–558.
| Plasma membrane phospholipid asymmetry precedes DNA fragmentation in different apoptotic cell models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFKmsro%3D&md5=8038fa5c8f6ca2bc4e3d634bfd84c4e6CAS | 9860253PubMed |
Chung, H. S., Park, S. R., Choi, E. K., Park, H. J., Griffin, R. J., Song, C. W., and Park, H. (2003). Role of sphingomyelin-MAPKs pathway in heat-induced apoptosis. Exp. Mol. Med. 35, 181–188.
| 1:CAS:528:DC%2BD3sXlsVKqtbk%3D&md5=ddc323b04cb6d13b0d46d65cf37d23a9CAS | 12858017PubMed |
Coll, O., Morales, A., Fernández-Checa, J. C., and Garcia-Ruiz, C. (2007). Neutral sphingomyelinase-induced ceramide triggers germinal vesicle breakdown and oxidant-dependent apoptosis in Xenopus laevis oocytes. J. Lipid Res. 48, 1924–1935.
| Neutral sphingomyelinase-induced ceramide triggers germinal vesicle breakdown and oxidant-dependent apoptosis in Xenopus laevis oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslOjurY%3D&md5=dbbdab3b103dd1cd5a84b523f22182c9CAS | 17556754PubMed |
Contreras, F. X., Basañez, G., Alonso, A., Herrmann, A., and Goñi, F. M. (2005). Asymmetric addition of ceramides but not dihydroceramides promotes transbilayer (flip-flop) lipid motion in membranes. Biophys. J. 88, 348–359.
| Asymmetric addition of ceramides but not dihydroceramides promotes transbilayer (flip-flop) lipid motion in membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyntLo%3D&md5=0d285b1e3369d0168cba107e0baf0f88CAS | 15465865PubMed |
Cowart, L. A., and Hannun, Y. A. (2007). Selective substrate supply in the regulation of yeast de novo sphingolipid synthesis. J. Biol. Chem. 282, 12330–12340.
| Selective substrate supply in the regulation of yeast de novo sphingolipid synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFeksLo%3D&md5=f7f5e17091a8a19b4a319db701a10e79CAS | 17322298PubMed |
Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., and Coso, O. A. (1996). Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381, 800–803.
| Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvVKnsro%3D&md5=262c5b61ba66be44bfcd672ecdfd5f43CAS | 8657285PubMed |
Delgado, A., Casas, J., Llebaria, A., Abad, J. L., and Fabrias, G. (2006). Inhibitors of sphingolipid metabolism enzymes. Biochim. Biophys. Acta 1758, 1957–1977.
| Inhibitors of sphingolipid metabolism enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12kt7zO&md5=a41ee73876fd2c291b6d4d71ae4fdc88CAS | 17049336PubMed |
Di Nardo, A., Benassi, L., Magnoni, C., Cossarizza, A., Seidenari, S., and Giannetti, A. (2000). Ceramide 2 (N-acetyl sphingosine) is associated with reduction in Bcl-2 protein levels by Western blotting and with apoptosis in cultured human keratinocytes. Br. J. Dermatol. 143, 491–497.
| Ceramide 2 (N-acetyl sphingosine) is associated with reduction in Bcl-2 protein levels by Western blotting and with apoptosis in cultured human keratinocytes.Crossref | GoogleScholarGoogle Scholar | 10971319PubMed |
Ealy, A. D., Drost, M., and Hansen, P. J. (1993). Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J. Dairy Sci. 76, 2899–2905.
| Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FksVSmtQ%3D%3D&md5=23092f2b490a5fb9de3b55715799e6c6CAS | 8227617PubMed |
Edwards, J. L., and Hansen, P. J. (1996). Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol. Reprod. 55, 341–346.
| Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28vis1Gmuw%3D%3D&md5=510f2f8d19e1ccd2bc777156755d2373CAS | 8828838PubMed |
Edwards, J. L., and Hansen, P. J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–145.
| Differential responses of bovine oocytes and preimplantation embryos to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXoslWhtQ%3D%3D&md5=5dceffa5a96a2a75d219df7f1b477999CAS | 9021745PubMed |
Eliyahu, E., Park, J. H., Shtraizent, N., He, X., and Schuchman, E. H. (2007). Acid ceramidase is a novel factor required for early embryo survival. FASEB J. 21, 1403–1409.
| Acid ceramidase is a novel factor required for early embryo survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlamtrk%3D&md5=0bdb858af1c51acdc6ebbb2576a549c4CAS | 17264167PubMed |
Eliyahu, E., Shtraizent, N., Martinuzzi, K., Barritt, J., He, X., Wei, H., Chaubal, S., Copperman, A. B., and Schuchman, E. H. (2010). Acid ceramidase improves the quality of oocytes and embryos and the outcome of in vitro fertilization. FASEB J. 24, 1229–1238.
| Acid ceramidase improves the quality of oocytes and embryos and the outcome of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOqtr0%3D&md5=9c40bf1ef44094845d9299e68128fdbeCAS | 20007509PubMed |
Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493–501.
| Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVyhsbs%3D&md5=3e48f2351b15fbb4082d548bc469abe0CAS | 1400587PubMed |
Goldkorn, T., Balaban, N., Shannon, M., Chea, V., Matsukuma, K., Gilchrist, D., Wang, H., and Chan, C. (1998). H2O2 acts on cellular membranes to generate ceramide signaling and initiate apoptosis in tracheobronchial epithelial cells. J. Cell Sci. 111, 3209–3220.
| 1:CAS:528:DyaK1cXnvFOqt70%3D&md5=79cbace421fc61d6f10241db2df491f6CAS | 9763515PubMed |
Goodman, Y., and Mattson, M. P. (1996). Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid b-peptide toxicity. J. Neurochem. 66, 869–872.
| Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid b-peptide toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFGjtg%3D%3D&md5=0f29bd758dd141d9c52fffe9c2ef4faaCAS | 8592164PubMed |
Haimovitz-Friedman, A., Kan, C. C., Ehleiter, D., Persaud, R. S., and McLoughlin, M. (1994). Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med. 180, 525–535.
| Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVeit70%3D&md5=28881d2a4d809d24bc6aafda158b7620CAS | 8046331PubMed |
Hannun, Y. A. (1996). Functions of ceramide in coordinating cellular responses to stress. Science 274, 1855–1859.
| Functions of ceramide in coordinating cellular responses to stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFGisrc%3D&md5=e5f457b03394c04d0610410ab2350847CAS | 8943189PubMed |
Hannun, Y. A., and Luberto, C. (2000). Ceramide in the eukaryotic stress response. Trends Cell Biol. 10, 73–80.
| Ceramide in the eukaryotic stress response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXpsFKisw%3D%3D&md5=4dd819d402fdaabd7143204b2fd8dc2fCAS | 10652518PubMed |
Henkel, R., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Gips, H., Schill, W. B., and Kruger, T. F. (2004). Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil. Steril. 81, 965–972.
| Influence of deoxyribonucleic acid damage on fertilization and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFCrtrY%3D&md5=f1ea73675d8484d2d0e33bda8de2c10fCAS | 15066449PubMed |
Huppertz, B., Frank, H. G., and Kaufmann, P. (1999). The apoptosis cascade-morphological and immunohistochemical methods for its visualization. Anat. Embryol. (Berl.) 200, 1–18.
| The apoptosis cascade-morphological and immunohistochemical methods for its visualization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzitV2htg%3D%3D&md5=1c05bd27ded8650908a42e10b79e860fCAS |
Jayadev, S., Liu, B., Bielawska, A. E., Lee, J. Y., Nazaire, F., Pushkareva, M. Y., Obeid, L. M., and Hannun, Y. A. (1995). Role for ceramide in cell cycle arrest. J. Biol. Chem. 270, 2047–2052.
| Role for ceramide in cell cycle arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsV2ks7s%3D&md5=0b774e10ce68b5fc47ccad9bdd775d22CAS | 7836432PubMed |
Jenkins, G. M. (2003). The emerging role for sphingolipids in the eukaryotic heat shock response. Cell. Mol. Life Sci. 60, 701–710.
| The emerging role for sphingolipids in the eukaryotic heat shock response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlyjurg%3D&md5=67f032380f71fe899259293ac1553ddeCAS | 12785717PubMed |
Jenkins, G. M., Cowart, L. A., Signorelli, P., Pettus, B. J., Chalfant, C. E., and Hannun, Y. A. (2002). Acute activation of de novo sphingolipid biosynthesis upon heat shock causes an accumulation of ceramide and subsequent dephosphorylation of SR proteins. J. Biol. Chem. 277, 42572–42578.
| Acute activation of de novo sphingolipid biosynthesis upon heat shock causes an accumulation of ceramide and subsequent dephosphorylation of SR proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1ensb4%3D&md5=bd2f8960a7297318f64a668fd334549cCAS | 12200446PubMed |
Ju, J. C., Jiang, S., Tseng, J. K., Parks, J. E., and Yang, X. (2005). Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64, 1677–1689.
| Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15951010PubMed |
Kenis, H., Zandbergen, H. R., Hofstra, L., Petrov, A. D., Dumont, E. A., Blankenberg, F. D., Haider, N., Bitsch, N., Gijbels, M., Verjans, J. W., Narula, N., Narula, J., and Reutelingsperger, C. P. (2010). Annexin A5 uptake in ischemic myocardium: demonstration of reversible phosphatidylserine externalization and feasibility of radionuclide imaging. J. Nucl. Med. 51, 259–267.
| Annexin A5 uptake in ischemic myocardium: demonstration of reversible phosphatidylserine externalization and feasibility of radionuclide imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivFWmsb8%3D&md5=e8d3997c753df860068aeb54576a5303CAS | 20124049PubMed |
Kobrinsky, E., Spielman, A. I., Rosenzweig, S., and Marks, A. R. (1999). Ceramide triggers intracellular calcium release via the IP(3) receptor in Xenopus laevis oocytes. Am. J. Physiol. 277, 665–672.
Kondo, T., Matsuda, T., Kitano, T., Takahashi, A., Tashima, M., Ishikura, H., Umehara, H., Domae, N., Uchiyama, T., and Okazaki, T. (2000). Role of c-jun expression increased by heat shock- and ceramide-activated caspase-3 in HL-60 cell apoptosis. Possible involvement of ceramide in heat shock-induced apoptosis. J. Biol. Chem. 275, 7668–7676.
| Role of c-jun expression increased by heat shock- and ceramide-activated caspase-3 in HL-60 cell apoptosis. Possible involvement of ceramide in heat shock-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVyls7g%3D&md5=a340329b42c927f1f4560d02ba41075fCAS | 10713077PubMed |
Kregel, K. C. (2002). Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92, 2177–2186.
| 1:CAS:528:DC%2BD38XjvFersrk%3D&md5=afa1826c296d034b743b02e9d4ddf23cCAS | 11960972PubMed |
Lahorte, C. M. M., Vanderheyden, J. L., Steinmetz, N., Van de Wiele, C., Dierckx, R. A., and Slegers, G. (2004). Apoptosis-detecting radioligands: current state of the art and future perspectives. Eur. J. Nucl. Med. Mol. Imaging 31, 887–919.
| Apoptosis-detecting radioligands: current state of the art and future perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVensb4%3D&md5=658497ab5c464fd8e79f22ae15a05683CAS |
Lang, K. S., Myssina, S., Brand, V., Sandu, C., Lang, P. A., Berchtold, S., Huber, S. M., Lang, F., and Wieder, T. (2004). Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ. 11, 231–243.
| Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1KmtA%3D%3D&md5=21dbb0839d30745435bc6bc6dcf469d1CAS | 14615798PubMed |
Lin, L., Kragh, P. M., Purup, S., Kuwayama, M., Du, Y. T., Zhang, X. Q., Yang, H. M., Bolund, L., Callesen, H., and Vajta, G. (2009). Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes. Reprod. Fertil. Dev. 21, 338–344.
| Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVensb8%3D&md5=9a0b9c08dbc368544469eef9ce6d2794CAS | 19210925PubMed |
Luiz Augusto, d. C. e. P., and Hansen, P. J. (2008). Ceramide inhibits development and cytokinesis and induces apoptosis in preimplantation bovine embryos. Mol. Reprod. Dev. 75, 1063–1070.
| Ceramide inhibits development and cytokinesis and induces apoptosis in preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., and Green, D. R. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545–1556.
| Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFWqsL4%3D&md5=a69b46cffb1b57eb9278d3b0cd5baf5cCAS | 7595224PubMed |
Mathias, S., Pena, L. A., and Kolesnick, R. N. (1998). Signal transduction of stress via ceramide. Biochem. J. 335, 465–480.
| 1:CAS:528:DyaK1cXnsFekurw%3D&md5=1b55e27fb7d78bf4a39bf7ea72cf1662CAS | 9794783PubMed |
Merrill, A. H. J. r., Sullards, M. C., Wang, E., Voss, K. A., and Riley, R. T. (2001). Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ. Health Perspect. 109, 283–289.
| Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVOgt70%3D&md5=9112e6a00db06b5b5d5def3675eee9c7CAS |
Metchat, A., Akerfelt, M., Boerkamp, C., Delsinne, V., Sistonen, L., Alexandre, H., and Christians, E. S. (2009). Mammalian heat shock factor 1 is essential for oocyte meiosis and regulates Hsp90alpha expression. J. Biol. Chem. 284, 9521–9528.
| Mammalian heat shock factor 1 is essential for oocyte meiosis and regulates Hsp90alpha expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1ymsbg%3D&md5=70b85bcda9ce5f4d24e9d4cbf296069fCAS | 19158073PubMed |
Mitoma, J., Ito, M., Furuya, S., and Hirabayashi, Y. (1998). Bipotential roles of ceramide in the growth of hippocampal neurons: promotion of cell survival and dendritic outgrowth in dose- and developmental stage-dependent manners. J. Neurosci. Res. 51, 712–722.
| Bipotential roles of ceramide in the growth of hippocampal neurons: promotion of cell survival and dendritic outgrowth in dose- and developmental stage-dependent manners.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFGgurc%3D&md5=25c4a489614d3614792c67ca6e92cb6aCAS | 9545085PubMed |
Modrak, D. E., Leon, E., Goldenberg, D. M., and Gold, D. V. (2009). Ceramide regulates gemcitabine-induced senescence and apoptosis in human pancreatic cancer cell lines. Mol. Cancer Res. 7, 890–896.
| Ceramide regulates gemcitabine-induced senescence and apoptosis in human pancreatic cancer cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1Skt7o%3D&md5=e7b2b28a7bdddb7c96c8b01e0747213cCAS | 19531570PubMed |
Morimoto, R. I. (1998). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788–3796.
| Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGjsQ%3D%3D&md5=0731aa36d41dda93a57cfdc0322b61aeCAS | 9869631PubMed |
Morita, Y., Perez, G. I., Paris, F., Miranda, S. R., Ehleiter, D., Haimovitz-Friedman, A., Fuks, Z., Xie, Z., Reed, J. C., Schuchman, E. H., Kolesnick, R. N., and Tilly, J. L. (2000). Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat. Med. 6, 1109–1114.
| Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntlKntrg%3D&md5=06e01df72f860bdcda923ac474a3f30bCAS | 11017141PubMed |
O’Brien, I. E., Reutelingsperger, C. P., and Holdaway, K. M. (1997). The use of annexin-V and TUNEL to monitor the progression of apoptosis in plants. Cytometry 29, 28–33.
| The use of annexin-V and TUNEL to monitor the progression of apoptosis in plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svkt1amuw%3D%3D&md5=c2724c3be9629a78caa872f4c97c49e9CAS | 9298808PubMed |
Parrish, J. J., and Foote, R. H. (1986). Fertility of cooled and frozen rabbit sperm measured by competitive fertilization. Biol. Reprod. 35, 253–257.
| Fertility of cooled and frozen rabbit sperm measured by competitive fertilization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s%2Fis1yhuw%3D%3D&md5=b961ff735d9cebfe6cbb0c9b1e3814e6CAS | 3768452PubMed |
Pastorino, J. G., Tafani, M., Rothman, R. J., Marcinkeviciute, A., Hoek, J. B., and Farber, J. L. (1999). Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J. Biol. Chem. 274, 31734–31739.
| Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFOjsLo%3D&md5=dd916eaf4896ad784b954429831947d9CAS | 10531385PubMed |
Payton, R. R., Romar, R., Coy, P., Saxton, A. M., Lawrence, J. L., and Edwards, J. L. (2004). Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol. Reprod. 71, 1303–1308.
| Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtbk%3D&md5=bc4d86e308051fd179f91599da932525CAS | 15201201PubMed |
Peña, L. A., Fuks, Z., and Kolesnick, R. (1997). Stress-induced apoptosis and the sphingomyelin pathway. Biochem. Pharmacol. 53, 615–621.
| Stress-induced apoptosis and the sphingomyelin pathway.Crossref | GoogleScholarGoogle Scholar | 9113079PubMed |
Perez, G. I., Jurisicova, A., Matikainen, T., Moriyama, T., Kim, M. R., Takai, Y., Pru, J. K., Kolesnick, R. N., and Tilly, J. L. (2005). A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J. 19, 860–862.
| 1:CAS:528:DC%2BD2MXktVKmt7Y%3D&md5=818d179237751108d3986c3a96b8645fCAS | 15728664PubMed |
Perks, C. M., Newcomb, P. V., Grohmann, M., Wright, R. J., Mason, H. D., and Holly, J. M. P. (2003). Prolactin acts as a potent survival factor against C2-ceramide-induced apoptosis in human granulosa cells. Hum. Reprod. 18, 2672–2677.
| Prolactin acts as a potent survival factor against C2-ceramide-induced apoptosis in human granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVemu7s%3D&md5=2bc4d4d5f2efc8538e31c95b8203c44fCAS | 14645190PubMed |
Petcoff, D. W., Holland, W. L., and Stith, B. J. (2008). Lipid levels in sperm, eggs, and during fertilization in Xenopus laevis. J. Lipid Res. 49, 2365–2378.
| Lipid levels in sperm, eggs, and during fertilization in Xenopus laevis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12it7vN&md5=ffbb7f453a7386dcd1c9221eae11f0c9CAS | 18577769PubMed |
Posse de Chaves, E. I. (2006). Sphingolipids in apoptosis, survival and regeneration in the nervous system. Biochim. Biophys. Acta 1758, 1995–2015.
| Sphingolipids in apoptosis, survival and regeneration in the nervous system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12kt7zI&md5=7dc7048d91c59d0b53a6b6ba1aab63afCAS | 17084809PubMed |
Pribenszky, C., Du, Y., Molnar, A., Harnos, A., and Vajta, G. (2008). Increased stress tolerance of matured pig oocytes after high hydrostatic pressure treatment. Anim. Reprod. Sci. 106, 200–207.
| Increased stress tolerance of matured pig oocytes after high hydrostatic pressure treatment.Crossref | GoogleScholarGoogle Scholar | 18329829PubMed |
Pushkareva, M., Obeid, L. M., and Hannun, Y. A. (1995). Ceramide: an endogenous regulator of apoptosis and growth suppression. Immunol. Today 16, 294–297.
| Ceramide: an endogenous regulator of apoptosis and growth suppression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFeht70%3D&md5=cc89f86463160fcd5b7a6d78228c6b8cCAS | 7662099PubMed |
Putney, D. J., Drost, M., and Thatcher, W. W. (1989). Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology 31, 765–778.
| Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFemtA%3D%3D&md5=54304547986f8ad924cc96cf3f151bcdCAS | 16726592PubMed |
Pyne, S., and Pyne, N. J. (2000). Sphingosine 1-phosphate signaling in mammalian cells. Biochem. J. 349, 385–402.
| Sphingosine 1-phosphate signaling in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFOmu74%3D&md5=930e0832565f654cad158c99abfc0eccCAS | 10880336PubMed |
Roth, Z., and Hansen, P. J. (2004a). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–1906.
| Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsrzL&md5=5501ee91f5a07765b8eab9801c18e599CAS | 15306551PubMed |
Roth, Z., and Hansen, P. J. (2004b). Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol. Reprod. 71, 2072–2078.
| Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsrrF&md5=adfa869d6e606cc4868a39b0303e178fCAS | 15317688PubMed |
Roth, Z., and Hansen, P. J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–244.
| Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1yrsrg%3D&md5=ffa26d93b17697a02908ea028ea47696CAS | 15695618PubMed |
Scheid, M. P., Foltz, I. N., Young, P. R., Schrader, J. W., and Duronio, V. (1999). Ceramide and cyclic adenosine monophosphate (cAMP) induce cAMP response element binding protein phosphorylation via distinct signaling pathways while having opposite effects on myeloid cell survival. Blood 93, 217–225.
| 1:STN:280:DyaK1M%2FotFKhsg%3D%3D&md5=bd48d90d450165273f3ea7297be81af0CAS | 9864164PubMed |
Soto, P., and Smith, L. C. (2009). BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol. Reprod. Dev. 76, 637–646.
| BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVaisL8%3D&md5=08f96db66ece34ef28486a1b87cea18cCAS | 19062170PubMed |
Strum, J. C., Swenson, K. I., Turner, J. E., and Bell, R. M. (1995). Ceramide triggers meiotic cell cycle progression in Xenopus oocytes. J. Biol. Chem. 270, 13541–13547.
| Ceramide triggers meiotic cell cycle progression in Xenopus oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtV2hsLk%3D&md5=656ed6b26e360f706abe15e957d67002CAS | 7768956PubMed |
Tepper, A. D., Ruurs, P., Wiedmer, T., Sims, P. J., Borst, J., and van Blitterswijk, W. J. (2000). Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology. J. Cell Biol. 150, 155–164.
| Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltVGhtro%3D&md5=403bda50d8c1ce23de000d3b1d1e954dCAS | 10893264PubMed |
van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B., and Reutelingsperger, C. P. (1998). Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1–9.
| Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVGruw%3D%3D&md5=1bd98586099eeaf49ca2d99d831afad3CAS | 9450519PubMed |
Vandaele, L., Thys, M., Bijttebier, J., Van Langendonckt, A., Donnay, I., Maes, D., Meyer, E., and Van Soom, A. (2010). Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development. Reproduction 139, 505–511.
| Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtV2lsb8%3D&md5=97eb0414b47c697e32dee6ecf0194742CAS | 19939885PubMed |
Veldman, R. J., Klappe, K., Hoekstra, D., and Kok, J. W. (1998). Metabolism and apoptotic properties of elevated ceramide in HT29rev cells. Biochem. J. 331, 563–569.
| 1:CAS:528:DyaK1cXivV2itr4%3D&md5=96ac0a6f5a84ca209276b7ebcd1b4966CAS | 9531498PubMed |
Verheij, M., Bose, R., Lin, S. H., Yao, B., Jarvis, W. D., Grant, S., Birrer, M. J., Szabo, E., Zon, L. I., Kyriakis, J. M., Haimovitz-Friedman, A., Fuks, Z., and Kolesnick, R. (1996). Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380, 75–79.
| Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsFeisbw%3D&md5=2bbb322b6ee0e364bc830a71bd1b79e7CAS | 8598911PubMed |
Westwick, J. K., Bielawska, A. E., Dbaibo, G., Hannun, Y. A., and Brenner, D. A. (1995). Ceramide activates the stress-activated protein kinases. J. Biol. Chem. 270, 22689–22692.
| Ceramide activates the stress-activated protein kinases.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2Fjt1Krtw%3D%3D&md5=5299f75a87a673718c6c921f634806e3CAS | 7559390PubMed |
Witty, J. P., Bridgham, J. T., and Johnson, A. L. (1996). Induction of apoptotic cell death in hen granulosa cells by ceramide. Endocrinology 137, 5269–5277.
| Induction of apoptotic cell death in hen granulosa cells by ceramide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1Gns7k%3D&md5=40524b6f80272d45dc46fde2b3868979CAS | 8940345PubMed |
Wu, C. (1995). Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441–469.
| Heat shock transcription factors: structure and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXps1aqtrY%3D&md5=13bc14f21be27231be43485c6708d92bCAS | 8689565PubMed |
Zhang, J., Alter, N., Reed, J. C., Borner, C., Obeid, L. M., and Hannun, Y. A. (1996). Bcl-2 interrupts the ceramide mediated pathway of cell death. Proc. Natl. Acad. Sci. USA 93, 5325–5328.
| Bcl-2 interrupts the ceramide mediated pathway of cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjt1Kqu7k%3D&md5=4a37cc156fd10fe282bd50d50511fac5CAS | 8643573PubMed |
Zhou, Q., Zhao, J., Stout, J. G., Luhm, R. A., Wiedmer, T., and Sims, P. J. (1997). Molecular cloning of human plasma membrane phospholipid scramblase. J. Biol. Chem. 272, 18240–18244.
| Molecular cloning of human plasma membrane phospholipid scramblase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslKqtLc%3D&md5=2779a06f81d3672cf4b639f300e7fb1fCAS | 9218461PubMed |
