Full Access
Insulin-like growth factor I rescues SH-SY5Y human neuroblastoma cells from hyperosmotic induced programmed cell death
Christopher C. Matthews,
Eva L. Feldman,
Christopher C. Matthews
Department of Neurology and Neurosciences Program, University of Michigan, Ann Arbor, Michigan 48109
Search for more papers by this authorCorresponding Author
Eva L. Feldman
Department of Neurology and Neurosciences Program, University of Michigan, Ann Arbor, Michigan 48109
University of Michigan, Department of Neurology, 200 Zina Pitcher Place, 4414 Kresge III, Ann Arbor, MI 48109-0588Search for more papers by this authorChristopher C. Matthews,
Eva L. Feldman,
Christopher C. Matthews
Department of Neurology and Neurosciences Program, University of Michigan, Ann Arbor, Michigan 48109
Search for more papers by this authorCorresponding Author
Eva L. Feldman
Department of Neurology and Neurosciences Program, University of Michigan, Ann Arbor, Michigan 48109
University of Michigan, Department of Neurology, 200 Zina Pitcher Place, 4414 Kresge III, Ann Arbor, MI 48109-0588Search for more papers by this authorFirst published: February 1996
Citations: 136
Abstract
Insulin-like growth factor I (IGF-I) and the type I IGF receptor are widely distributed in developing and adult mammalian nervous systems. In vitro, IGF-I is a mitogen for primary neurons and also for cells from the SH-SY5Y human neuroblastoma cell line, a well-characterized model system of neuronal growth. In the current study, we examined the effects of osmotic stress on SH-SY5Y cell viability and the mechanism by which IGF-I serves as a neuronal osmoprotectant. Within 24 hr, exposure of SH-SY5Y cells to hyperosmotic serum-free media decreased (1) the number of viable cells, (2) the rate of 3H-thymidine incorporation, and (3) cell cycle progression. The inclusion of 10 nM IGF-I with hyperosmotic media prevented the loss of cell viability. The osmoprotective effects of IGF-I were inhibited by α-IRJ, a blocking antibody of the type I IGF receptor. The observed loss of SH-SY5Y cell viability following hyperosmotic shock was due to an induction of programmed cell death as determined by flow cytometry and gel electrophoresis. Our results suggest that IGF-I can protect SH-SY5Y cells from hyperosmotic induced programmed cell death. © 1996 Wiley-Liss, Inc.
Literature Cited
- Allsopp, T. E., Wyatt, S., Patterson, H. F., and Davies, A. M. (1994) The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell, 73: 295–307.
- Barry, M. A., and Eastman, A. (1995) Endonuclease activation during apoptosis: The role of cytosolic Ca2+ and pH. Biochem. Biophys. Res. Commun., 186: 782–789.
- Beck, F., Samani, N. J., Byrne, S., Morgan, K., Gebhard, R., and Brammar, W. J. (1988) Histochemical localization of IGF-I and IGF-II mRNA in the rat between birth and adulthood. Development, 104: 29–39.
- Boise, L. H., Gonzalez-Garcia, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nunez, G., and Thompson, C. B. (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell, 74: 597–608.
- Bothwell, M. (1982) Insulin and somatomedin MSA promote nerve growth factor-independent neurite formation by cultured chick dorsal root ganglionic sensory neurons. J. Neurosci. Res., 8: 225–231.
- Caceres-Cortes, J., Rajotte, D., Dumouchel, J., Haddad, P., and Hoang, T. (1994) Product of the steel locus suppresses apoptosis in hemopoietic cells. J. Biol. Chem., 269: 12084–12091.
- Cadena, D. L., and Gill, G. N. (1992) Receptor tyrosine kinases. FASEB J., 6: 2332–2337.
- Cala, P. M. (1985) Volume regulation by Amphiuma red blood cells: Strategies for identifying alkali metal/H+ transport. FASEB J., 44: 2500–2507.
- Cuende, E., Ales-Martinez, J. E., Ding, L., Gonzalez-Garcia, M., Martinez-, A. C., and Nunez, G. (1993) Programmed cell death by bcl-2-dependent and independent mechanisms in B lymphoma cells. EMBO J., 12: 1555–1560.
- Darzynkiewicz, Z., Bruno, S., DelBino, G., Gorczyca, W., Hotz, M. A., Lassota, P., and Traganos, F. (1992) Features of apoptotic cells measured by flow cytometry. Cytometry, 13: 795–808.
- DiCicco-Bloom, E., and Black, I. B. (1988) Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proc. Natl. Acad. Sci. U.S.A., 85: 4066–4070.
- D'Mello, S. R., Galli, C., Ciotti, T., and Calissano, P. (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: Inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. U.S.A., 90: 10989–10993.
- Dole, M., Nunez, G., Merchant, A. K., Maybaum, J., Rode, C. K., Bloch, C. A., and Castle, V. P. (1994) Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res. 54: 3253–3259.
- Eastman, A., Grant, S., Lock, R., Tritton, T., Van Houten, N., and Yuan, J. (1994) Cell death in cancer and development: AACR special conference in cancer research. Cancer Res., 54: 2812–2818.
- Enokido, Y., Akaneya, Y., Niinobe, M., Mikoshiba, K., and Hatanaka, H. (1992) Basic fibroblast growth factor rescues CNS neurons from cell death caused by high oxygen atmosphere in culture. Brain Res., 599: 261–271.
- Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M., Waters, C. M., Penn, L. Z., and Hancock, D. C. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell, 69: 119–128.
- Fearnhead, H. O., Chwalinshi, M., Snowden, R. T., Ormerod, M. G., and Cohen, G. M. (1994) Dexamethasone and etoposide induce apoptosis in rat thymocytes from different phases of the cell cycle. Biochem. Pharmacol., 48: 1073–1079.
- Feldman, E. L., Randolph, A., and Yee, D. (1993) Insulin-like growth factor binding protein expression in SH-SY5Y neuroblastoma cells. In: The Role of Insulin-Like Growth Factors in the Nervous System. M. K. Raizada and D. LeRoith, eds. Annals of New York Academy of Sciences, New York, pp. 262–264.
- Gorczyca, W., Gong, J., Ardelt, B., Traganos, F., and Darzynkiewicz, Z. (1993) The cell cycle related differences in susceptibility of HL-60 cells to apoptosis induced by various antitumor agents. Cancer Res., 53: 3186–3192.
- Gratiot-Deans, J., Merino, R., Nunez, G., and Turka, L. A. (1994) Bcl-2 expression during T-cell development: Early loss and late return occur at specific stages of commitment to differentiation and survival. Proc. Natl. Acad. Sci. U.S.A., 91: 10685–10689.
- Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R. D., and Korsmeyer, S. J. (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 348: 334–336.
- Hoffmann, E. K., and Simonsen, L. O. (1989) Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol. Rev., 69: 315–382.
- Hotz, M. A., Gong, J., Traganos, F., and Darzynkiewicz, Z. (1994) Flow cytometric detection of apoptosis: Comparison of the assays on in situ DNA degradation and chromatin changes. Cytometry, 15: 237–244.
- Kokileva, L. (1994) Multi-step chromatin degradation in apoptosis. Int. Arch. Allergy Immunol. 105: 339–343.
- Kull, F. C., Jacobs, S., Su, Y. F., Svobuda, M. E., Van Wyk, J. J., and Cuatrecasas, P. (1983) Monoclonal antibodies to receptor for insulin and somatomedin C. J. Biol. Chem., 258: 6561–6566.
- Lam, M., Dubyak, G., Chen, L., Nunez, G., Miesfeld, R. L., and Distelhorst, C. W. (1994) Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc. Natl. Acad. Sci. U.S.A., 91: 6569–6573.
- LeBrun, D. P., Warnke, R. A., and Cleary, M. L. (1993) Expression of bcl-2 in fetal tissues suggests a role in morphogenesis. Am. J. Pathol., 142: 743–753.
- Lee, J. E., Pintar, J., and Efstratiadis, A. (1990) Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. Development, 110: 151–159.
- Mah, S. P., Zhong, L. T., Liu, Y., Roghani, A., Edwards, R. H., and Bredesen, D. E. (1993) The protooncogene bcl-2 inhibits apoptosis in PC12 cells. J. Neurochem., 60: 1183–1186.
- Martin, D. M., and Feldman, E. L. (1993a) Regulation of insulin-like growth factor-II expression and its role in autocrine growth of human neuroblastoma cells. J. Cell. Physiol., 155: 290–300.
- Martin, D. M., and Feldman, E. L. (1993b) Reversibility of serum removal effects on IGF-II mRNA in human neuroblastoma cells. In: The Role of Insulin-Like Growth Factors in the Nervous System. M. K. Raizada and D. LeRoith, eds. The New York Academy of Sciences, New York, pp. 259–261.
- Martin, D. M., Yee, D., Carlson, R. O., and Feldman, E. L. (1992) Gene expression of the insulin-like growth factors and their receptors in human neuroblastoma cells. Mol. Brain Res., 15: 241–246.
- Martin, D. M., Carlson, R. O., and Feldman, E. L. (1993a) Interferon-γ inhibits DNA synthesis and insulin-like growth factor-II expression in human neuroblastoma cells. J. Neurosci. Res., 34: 489–501.
- Martin, D. M., Singleton, J. R., Meghani, M. A., and Feldman, E. L. (1993b) IGF receptor function and regulation in autocrine human neuroblastoma cell growth. Regul. Pept., 48: 225–232.
- Martinou, J.-C., Dubois-Dauphin, M., Staple, J. K., Rodriguez, I., Frankowshi, H., Missotten, M., Albertini, P., Talabot, D., Catsicass, S., Pietra, C., and Huarte, J. (1994) Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron, 13: 1017–1030.
- Matsubara, K., Kubota, M., Kuwakado, K., Hirota, H., Wakazono, Y., Okuda, A., Bessho, R., Lin, Y. W., Adachi, S., and Akiyama, Y. (1994) Variable susceptibility to apoptosis induced by calcium ionophore in hybridomas between HL-60 promyelocytic and CEM T-lymphoblastic leukemia cell lines: Relationship to constitutive Mg(2+)-dependent endonuclease. Exp. Cell Res., 213: 412–417.
- Matthews, C. C., Bryant, J., and Feldman, E. L. (1994) IGF-I rescues neurons from hyperosmotic shock. Soc. Neurosci. Abstr., 20: 231.
- McCall, C., and Cohen, J. J. (1991) Programmed cell death in terminally differentiating keratinocytes: Role of endogenous endonuclease. J. Invest. Dermatol., 97: 111–114.
- Meghani, M. A., Martin, D. M., Singleton, J. R., and Feldman, E. L. (1993) Effects of serum and insulin-like growth factors on human neuroblastoma cell growth. Regul. Pept., 48: 217–224.
- Merino, R., Ding, L., Veis, D. J., Korsmeyer, S. J., and Nunez, G. (1994) Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J., 13: 683–691.
- Merry, D. E., Veis, D. J., Hickey, W. F., and Korsmeyer, S. J. (1994) bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development, 120: 301–311.
- Morgan, D. O., Jarnagin, K., and Roth, R. A. (1986) Purification and characterization of the receptor for insulin-like growth factor I. Biochemistry, 25: 5560–5564.
- Nunez, G., London, L., Hockenbery, D., Alexander, M., McKearn, J. P., and Korsmeyer, S. J. (1990) Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. J. Immunol., 144: 3602–3610.
- Ormerod, M. G., Sun, X.-M., Brown, D., Snowden, R. T., and Cohen, G. M. (1993) Quantification of apoptosis and necrosis by flow cytometry. Acta Oncol., 32: 417–424.
- Pittman, R. N., Wang, S., DiBenedetto, A. J., and Mills, J. C. (1993) A system for characterizing cellular and molecular events in programmed neuronal cell death. J. Neurosci., 13: 3669–3680.
- Rodriguez-Tarduchy, G., Collins, M. K. L., García, I., and López-Rivas, A. (1992) Insulin-like growth factor-I inhibits apoptosis in IL-3-dependent hemopoietic cells. J. Immunol., 149: 535–540.
- Roth, R. A. (1988) Structure of the receptor for insulin-like growth factor II: The puzzle amplified. Science, 239: 1269–1271.
- Rotwein, P. (1991) Structure, evolution, expression and regulation of insulin-like growth factors I and II. Growth Factors, 5: 3–18.
- Rukenstein, A., Rydel, R. E., and Greene, L. A. (1991) Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J. Neurosci., 11: 2552–2563.
- Sara, V. R., Carlsson-Skwirut, C., Andersson, C., Hall, E., Sjogren, B., Holmgren, A., and Jornval, H. (1986) Characterization of somatomedins from human fetal brain: Identification of a variant form of insulin-like growth factor I. Proc. Natl. Acad. Sci., U.S.A., 83: 4904–4907.
- Sardet, C., Franchi, A., and Pouyssegur, J. (1989) Molecular cloning, primary structure, and expression of the human growth factor-activatable Na+/H+ antiporter. Cell, 56: 271–280.
- Sgonc, R., and Wick, G. (1994) Methods for the detection of apoptosis. Int. Arch. Allergy Immunol., 105: 327–332.
- Shindo, H., Thomas, T., Kato, K., and Greene, D. (1994a) myo-inositol depletion inhibits phosphatidylinositol synthesis and turnover and muscarinic-induced cytosolic Ca++ flux in human neuroblastoma cells. Diabetes, 43(Suppl.): 207A.
- Shindo, H., Thomas, T., Stevens, M., and Greene, D. (1994b) Hyperglycemia decreases nitric oxide synthase activity in human SY5Y neuroblastoma cells via impaired protein kinase C activation. 15th Int. Diabetes Fed. Congr., 135.
- Stylianopoulou, F., Herbert, J., Soares, M. B., and Efstratiadis, A. (1988) Expression of the insulin-like growth factor II gene in the choroid plexus and the leptomeninges of the adult rat central nervous system. Proc. Natl. Acad. Sci. U.S.A., 85: 141–145.
- Sumantran, V. N., and Feldman, E. L. (1993) Insulin-like growth factor I regulates c-myc and GAP-43 messenger ribonucleic acid expression in SH-SY5Y human neuroblastoma cells. Endocrinology, 132: 2017–2023.
- Takasu, N., Komiya, I., Nagasawa, Y., Asawa, T., Shimizu, Y., and Yamada, T. (1995) Cytoplasmic pH in the action of insulin-like growth factor-I in cultured porcine thyroid cells. J. Endocrinol. 127: 305–309.
- Thompson, C. B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science, 267: 1456–1462.
- Woods, D. J., Soden, J., Tomlinson, S., and Bidey, S. P. (1990) Transmembrane Na+/H+ exchange in the rat thyroid cell strain FRTL-5: A possible role in insulin-like growth factor-I-mediated proliferation. J. Mol. Endocrinol. 4: 177–185.
Citing Literature
