Palmitate induces apoptosis in Schwann cells via both ceramide-dependent and independent pathways

Neuroscience

Volumn 176, Issue , 2011, Pages 188-198

  Suzuki, J ^a   Akahane, K ^a   Nakamura, J ^a   Naruse, K ^b   Kamiya, H ^a   Himeno, T ^a   Nakamura, N ^a   Shibata, T ^a   Kondo, M ^a   Nagasaki, H ^a   Fujiya, A ^a   Oiso, Y ^a   Hamada, Y ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI GAKUIN UNIVERSITY   (Japan)

Author keywords

Apoptosis; Ceramide; Obesity; Palmitate; Peripheral neuropathy; Schwann cells

Indexed keywords

CASPASE 3; CERAMIDE; CYTOCHROME C; FUMONISIN B1; HOE 33342; PALMITIC ACID; PROTEIN BAX; PROTEIN BCL 2; THERMOZYMOCIDIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL IMMORTALIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; INCUBATION TIME; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCHWANN CELL;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; CERAMIDES; DIABETIC NEUROPATHIES; FLUORESCENT ANTIBODY TECHNIQUE; MICE; OBESITY; PALMITATES; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 79851508128     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.11.035     Document Type: Article

References (48)

1. Adams J.M., Pratipanawatr T., Berria R., Wang E., DeFronzo R.A., Sullards M.C., Mandarino L.J. Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 2004, 53:25-31.
2. Aerts J.M., Ottenhoff R., Powlson A.S., Grefhorst A., van Eijk M., Dubbelhuis P.F., Aten J., Kuipers F., Serlie M.J., Wennekes T., Sethi J.K., O'Rahilly S., Overkleeft H.S. Pharmacological inhibition of glucosylceramide synthase enhances insulin sensitivity. Diabetes 2007, 56:1341-1349.
3. Basu A., Basu R., Shah P., Vella A., Rizza R.A., Jensen M.D. Systemic and regional free fatty acid metabolism in type 2 diabetes. Am J Physiol Endocrinol Metab 2001, 280:E1000-E1006.
4. Bektas M., Jolly P.S., Milstien S., Spiegel S. A specific ceramide kinase assay to measure cellular levels of ceramide. Anal Biochem 2003, 320:259-265.
5. Bidère N., Senik A. Caspase-independent apoptotic pathways in T lymphocytes: a minireview. Apoptosis 2001, 6:371-375.
6. Cacicedo J.M., Benjachareowong S., Chou E., Ruderman N.B., Ido Y. Palmitate-induced apoptosis in cultured bovine retinal pericytes: roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes 2005, 54:1838-1845.
7. Diakogiannaki E., Welters H.J., Morgan N.G. Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J Endocrinol 2008, 197:553-563.
8. Drel V.R., Xu W., Zhang J., Kador P.F., Ali T.K., Shin J., Julius U., Slusher B., El-Remessy A.B., Obrosova I.G. Poly(ADP-ribose)polymerase inhibition counteracts cataract formation and early retinal changes in streptozotocin-diabetic rats. Invest Ophthalmol Vis Sci 2009, 50:1778-1790.
9. Dyntar D., Eppenberger-Eberhardt M., Maedler K., Pruschy M., Eppenberger H.M., Spinas G.A., Donath M.Y. Glucose and palmitic acid induce degeneration of myofibrils and modulate apoptosis in rat adult cardiomyocytes. Diabetes 2001, 50:2105-2113.
10. Smith G.A., Singleton J.R. Idiopathic neuropathy, prediabetes and the metabolic syndrome. J Neurol Sci 2006, 242:9-14.
11. Guenther G.G., Peralta E.R., Rosales K.R., Wong S.Y., Siskind L.J., Edinger A.L. Ceramide starves cells to death by downregulating nutrient transporter proteins. Proc Natl Acad Sci U S A 2008, 105:17402-17407.
12. Guo W., Wong S., Xie W., Lei T., Luo Z. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 2007, 293:E576-E586.
13. Hannun Y.A. Functions of ceramide in coordinating cellular responses to stress. Science 1996, 274:1855-1859.
14. Hardy S., El-Assaad W., Przybytkowski E., Joly E., Prentki M., Langelier Y. Saturated fatty acid-induced apoptosis in MDA-MB-231 breast cancer cells. A role for cardiolipin. J Biol Chem 2003, 278:31861-31870.
15. Hatzoglou A., Kampa M., Kogia C., Charalampopoulos I., Theodoropoulos P.A., Anezinis P., Dambaki C., Papakonstanti E.A., Stathopoulos E.N., Stournaras C., Gravanis A., Castanas E. Membrane androgen receptor activation induces apoptotic regression of human prostate cancer cells in vitro and in vivo. J Clin Endocrinol Metab 2005, 90:893-903.
16. Hirata H., Hibasami H., Yoshida T., Ogawa M., Matsumoto M., Morita A., Uchida A. Nerve growth factor signaling of p75 induces differentiation and ceramide-mediated apoptosis in Schwann cells cultured from degenerating nerves. Glia 2001, 36:245-258.
17. Holland W.L., Summers S.A. Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev 2008, 29:381-402.
18. Isley W.L., Harris W.S., Miles J.M. The effect of high-dose simvastatin on free fatty acid metabolism in patients with type 2 diabetes mellitus. Metabolism 2006, 55:758-762.
19. Karaskov E., Scott C., Zhang L., Teodoro T., Ravazzola M., Volchuk A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 2006, 147:3398-3407.
20. Kurita-Ochiai T., Amano S., Fukushima K., Ochiai K. Cellular events involved in butyric acid-induced T cell apoptosis. J Immunol 2003, 171:3576-3584.
21. Lee J.Y., Sohn K.H., Rhee S.H., Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 2001, 276:16683-16689.
22. Listenberger L.L., Ory D.S., Schaffer J.E. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem 2001, 276:14890-14895.
23. Lu Z.H., Mu Y.M., Wang B.A., Li X.L., Lu J.M., Li J.Y., Pan C.Y., Yanase T., Nawata H. Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cell. Biochem Biophys Res Commun 2003, 303:1002-1007.
24. Maedler K., Oberholzer J., Bucher P., Spinas G.A., Donath M.Y. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003, 52:726-733.
25. Minano A., Caballero-Benitez A., Lluch M., Moran J., Rodriguez-Alvarez J. C2-ceramide mediates cerebellar granule cells apoptosis by activation of caspases-2, -9, and -3. J Neurosci Res 2008, 86:1734-1747.
26. Miscio G., Guastamacchia G., Brunani A., Priano L., Baudo S., Mauro A. Obesity and peripheral neuropathy risk: a dangerous liaison. J Peripher Nerv Syst 2005, 10:354-358.
27. Mittendorfer B., Liem O., Patterson B.W., Miles J.M., Klein S. What does the measurement of whole-body fatty acid rate of appearance in plasma by using a fatty acid tracer really mean?. Diabetes 2003, 52:1641-1648.
28. Monti B., Zanghellini P., Contestabile A. Characterization of ceramide-induced apoptotic death in cerebellar granule cells in culture. Neurochem Int 2001, 39:11-18.
29. Movsesyan V.A., Yakovlev A.G., Dabaghyan E.A., Stoica B.A., Faden A.I. Ceramide induces neuronal apoptosis through the caspase-9/caspase-3 pathway. Biochem Biophys Res Commun 2002, 299:201-207.
30. Nagano S., Takeda M., Ma L., Soliven B. Cytokine-induced cell death in immortalized Schwann cells: roles of nitric oxide and cyclic AMP. J Neurochem 2001, 77:1486-1495.
31. Nakamura J., Kato K., Hamada Y., Nakayama M., Chaya S., Nakashima E., Naruse K., Kasuya Y., Mizubayashi R., Miwa K., Yasuda Y., Kamiya H., Ienaga K., Sakakibara F., Koh N., Hotta N. A protein kinase C-beta-selective inhibitor ameliorates neural dysfunction in streptozotocin-induced diabetic rats. Diabetes 1999, 48:2090-2095.
32. Obrosova I.G., Ilnytska O., Lyzogubov V.V., Pavlov I.A., Mashtalir N., Nadler J.L., Drel V.R. High-fat diet induced neuropathy of pre-diabetes and obesity: effects of "healthy" diet and aldose reductase inhibition. Diabetes 2007, 56:2598-2608.
33. Ota K., Nakamura J., Li W., Kozakae M., Watarai A., Nakamura N., Yasuda Y., Nakashima E., Naruse K., Watabe K., Kato K., Oiso Y., Hamada Y. Metformin prevents methylglyoxal-induced apoptosis of mouse Schwann cells. Biochem Biophys Res Commun 2007, 357:270-275.
34. Ow Y.P., Green D.R., Hao Z., Mak T.W. Cytochrome c: functions beyond respiration. Nat Rev Mol Cell Biol 2008, 9:532-542.
35. Rachek L.I., Musiyenko S.I., LeDoux S.P., Wilson G.L. Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 2007, 148:293-299.
36. Reaven G.M., Hollenbeck C., Jeng C.Y., Wu M.S., Chen Y.D. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 1988, 37:1020-1024.
37. Sango K., Suzuki T., Yanagisawa H., Takaku S., Hirooka H., Tamura M., Watabe K. High glucose-induced activation of the polyol pathway and changes of gene expression profiles in immortalized adult mouse Schwann cells IMS32. J Neurochem 2006, 98:446-458.
38. Shimabukuro M., Higa M., Zhou Y.T., Wang M.Y., Newgard C.B., Unger R.H. Lipoapoptosis in beta-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J Biol Chem 1998, 273:32487-32490.
39. Staiger K., Staiger H., Weigert C., Haas C., Haring H.U., Kellerer M. Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-kappaB activation. Diabetes 2006, 55:3121-3126.
40. Sumbayev V.V. LPS-induced Toll-like receptor 4 signalling triggers cross-talk of apoptosis signal-regulating kinase 1 (ASK1) and HIF-1alpha protein. FEBS Lett 2008, 582:319-326.
41. Tang S.C., Lathia J.D., Selvaraj P.K., Jo D.G., Mughal M.R., Cheng A., Siler D.A., Markesbery W.R., Arumugam T.V., Mattson M.P. Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp Neurol 2008, 213:114-121.
42. Tosaki T., Kamiya H., Yasuda Y., Naruse K., Kato K., Kozakae M., Nakamura N., Shibata T., Hamada Y., Nakashima E., Oiso Y., Nakamura J. Reduced NGF secretion by Schwann cells under the high glucose condition decreases neurite outgrowth of DRG neurons. Exp Neurol 2008, 213:381-387.
43. Turpin S.M., Lancaster G.I., Darby I., Febbraio M.A., Watt M.J. Apoptosis in skeletal muscle myotubes is induced by ceramides and is positively related to insulin resistance. Am J Physiol Endocrinol Metab 2006, 291:E1341-E1350.
44. Vaudry D., Falluel-Morel A., Basille M., Pamantung T.F., Fontaine M., Fournier A., Vaudry H., Gonzalez B.J. Pituitary adenylate cyclase-activating polypeptide prevents C2-ceramide-induced apoptosis of cerebellar granule cells. J Neurosci Res 2003, 72:303-316.
45. Wang Y., Schmeichel A.M., Iida H., Schmelzer J.D., Low P.A. Ischemia-reperfusion injury causes oxidative stress and apoptosis of Schwann cell in acute and chronic experimental diabetic neuropathy. Antioxid Redox Signal 2005, 7:1513-1520.
46. Wang Y., Schmeichel A.M., Iida H., Schmelzer J.D., Low P.A. Enhanced inflammatory response via activation of NF-kappaB in acute experimental diabetic neuropathy subjected to ischemia-reperfusion injury. J Neurol Sci 2006, 247:47-52.
47. Watabe K., Fukuda T., Tanaka J., Honda H., Toyohara K., Sakai O. Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities. J Neurosci Res 1995, 41:279-290.
48. Wei Y., Wang D., Topczewski F., Pagliassotti M.J. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006, 291:E275-E281.