Activation of survival and apoptotic signaling pathways in lymphocytes exposed to palmitic acid

Journal of Cellular Physiology

Volumn 227, Issue 1, 2012, Pages 339-350

  Takahashi, Hilton Kenji ^a   Cambiaghi, Tavane David ^a   Luchessi, Augusto Ducati ^a   Hirabara, Sandro Massao ^a   Vinolo, Marco Aurelio Ramirez ^a   Newsholme, Philip ^b   Curi, Rui ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL ESTER; CYTOCHROME C; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE P38; PALMITIC ACID; PHOSPHOLIPID; STRESS ACTIVATED PROTEIN KINASE; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA CHAIN; BIOACCUMULATION; CELL MEMBRANE; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DEPOLARIZATION; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA FRAGMENTATION; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INSULIN TREATMENT; LETHAL DOSE; MALE; MESENTERY LYMPH NODE; MITOCHONDRIAL MEMBRANE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME INHIBITORS; GLUCOSE; HUMANS; IMMUNOPRECIPITATION; INSULIN; JURKAT CELLS; MALE; PALMITIC ACID; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

RATTUS;

EID: 80054951241     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22740     Document Type: Article

References (75)

1. Abaraviciene SM, Lundquist I, Salehi A. 2008. Rosiglitazone counteracts palmitate-induced beta-cell dysfunction by suppression of MAP kinase, inducible nitric oxide synthase and caspase 3 activities. Cell Mol Life Sci 65:2256-2265.
2. Anel JN, Gonzalez B, Torres JM, Mishal Z, Uriel J, Pineiro A. 1990. Fatty acid metabolism in human lymphocytes. I. Time-course changes in fatty acid composition and membrane fluidity during blastic transformation of peripheral blood lymphocytes. Biochim Biophys Acta 1044:323-331.
3. Bosca L, Zeini M, Traves PG, Hortelano S. 2005. Nitric oxide and cell viability in inflammatory cells: A role for NO in macrophage function and fate. Toxicology 208:249-258.
4. Brown TJ, Ercolani L, Ginsberg BH. 1983. Properties and regulation of the T lymphocyte insulin receptor. J Recept Res 3:481-494.
5. Brown TJ, Ercolani L, Ginsberg BH. 1985. Demonstration of receptors for insulin-like growth factor-II on human T-lymphocytes. J Recept Res 5:297-309.
6. Buffington CK, el-Shiekh T, Kitabchi AE, Matteri R. 1986. Phytohemagglutinin (PHA) activated human T-lymphocytes: Concomitant appearance of insulin binding, degradation and insulin-mediated activation of pyruvate dehydrogenase (PDH). Biochem Biophys Res Commun 134:412-419.
7. Cacicedo JM, Benjachareowong S, Chou E, Ruderman NB, Ido Y. 2005. Palmitate-induced apoptosis in cultured bovine retinal pericytes: Roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes 54:1838-1845.
8. Calder PC, Dimitriadis G, Newsholme P. 2007. Glucose metabolism in lymphoid and inflammatory cells and tissues. Curr Opin Clin Nutr Metab Care 10:531-540.
9. Chai W, Liu Z. 2007. p38 Mitogen-activated protein kinase mediates palmitate-induced apoptosis but not inhibitor of nuclear factor-kappaB degradation in human coronary artery endothelial cells. Endocrinology 148:1622-1628.
10. Chakrabarti R, Jung CY, Lee TP, Liu H, Mookerjee BK. 1994. Changes in glucose transport and transporter isoforms during the activation of human peripheral blood lymphocytes by phytohemagglutinin. J Immunol 152:2660-2668.
11. Chang WK, Yang KD, Shaio MF. 1999. Effect of glutamine on Th1 and Th2 cytokine responses of human peripheral blood mononuclear cells. Clin Immunol 93:294-301.
12. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. 2001. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 50:1771-1777.
13. Collins JM, Scott RB, Grogan WM. 1990. Plasma membrane fluidity gradients of human peripheral blood leukocytes. J Cell Physiol 144:42-51.
14. Curi R, Newsholme P, Pithon-Curi TC, Pires-de-Melo M, Garcia C, Homem-de-Bittencourt PI, Jr, Guimarães ARP. 1999. Metabolic fate of glutamine in lymphocytes, macrophages and neutrophils. Braz J Med Biol Res 32:15-21.
15. Curi R, Newsholme P, Newsholme EA. 1988. Metabolism of pyruvate by isolated rat mesenteric lymphocyte, lymphocyte mitochondria and isolated mouse macrophages. Biochem J 250:383-388.
16. Curi R, Lagranha CJ, Doi SQ, Sellitti DF, Procopio J, Pithon-Curi TC, Corless M, Newsholme P. 2005. Molecular mechanisms of glutamine action. J Cell Physiol 204:392-401.
17. Cury-Boaventura MF, Gorjao R, de Lima TM, Newsholme P, Curi R. 2006. Comparative toxicity of oleic and linoleic acid on human lymphocytes. Life Sci 78:1448-1456.
18. Cury-Boaventura MF, Pompeia C, Curi R. 2004. Comparative toxicity of oleic acid and linoleic acid on Jurkat cells. Clin Nutr 23:721-732.
19. DeLeve LD, Kaplowitz N. 1991. Glutathione metabolism and its role in hepatotoxicity. Pharmacol Ther 52:287-305.
20. Franco R, Cidlowski JA. 2006. SLCO/OATP-like transport of glutathione in FasL-induced apoptosis: Glutathione efflux is coupled to an organic anion exchange and is necessary for the progression of the execution phase of apoptosis. J Biol Chem 281:29542-29557.
21. Goodman DW, Isakson PC. 1993. Mitogen activation of resting lymphocytes exposes cryptic insulin receptors. J Biol Chem 268:4207-4215.
22. Gorjao R, Cury-Boaventura MF, de Lima TM, Curi R. 2007. Regulation of human lymphocyte proliferation by fatty acids. Cell Biochem Funct 25:305-315.
23. Gould GW, Holman GD. 1993. The glucose transporter family: Structure, function and tissue-specific expression. Biochem J 295:329-341.
24. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281:1309-1312.
25. Guo W, Wong S, Xie W, Lei T, Luo Z. 2007. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 293:E576-E586.
26. Hammond CL, Madejczyk MS, Ballatori N. 2004. Activation of plasma membrane reduced glutathione transport in death receptor apoptosis of HepG2 cells. Toxicol Appl Pharmacol 195:12-22.
27. Iida KT, Suzuki H, Sone H, Shimano H, Toyoshima H, Yatoh S, Asano T, Okuda Y, Yamada N. 2002. Insulin inhibits apoptosis of macrophage cell line, THP-1 cells, via phosphatidylinositol-3-kinase-dependent pathway. Arterioscler Thromb Vasc Biol 22:380-386.
28. Jacobson MD, Raff MC. 1995. Programmed cell death and Bcl-2 protection in very low oxygen. Nature 374:814-816.
29. Karsten S, Schafer G, Schauder P. 1994. Cytokine production and DNA synthesis by human peripheral lymphocytes in response to palmitic, stearic, oleic, and linoleic acid. J Cell Physiol 161:15-22.
30. Kroemer G, Dallaporta B, Resche-Rigon M. 1998. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60:619-642.
31. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
32. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC. 2008. Palmitate increases superoxide production through mitochondrial electron transport chain and NADPH oxidase activity in skeletal muscle cells. J Cell Physiol 216:796-804.
33. Lee SH, Park SW, Pyo CW, Yoo NK, Kim J, Choi SY. 2009. Requirement of the JNK-associated Bcl-2 pathway for human lactoferrin-induced apoptosis in the Jurkat leukemia T cell line. Biochimie 91:102-108.
34. Lima TM, Kanunfre CC, Pompeia C, Verlengia R, Curi R. 2002. Ranking the toxicity of fatty acids on Jurkat and Raji cells by flow cytometric analysis. Toxicol In Vitro 16:741-747.
35. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Jr, Ory DS, Schaffer JE. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100:3077-3082.
36. Listenberger LL, Ory DS, Schaffer JE. 2001. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem 276:14890-14895.
37. Maratou E, Dimitriadis G, Kollias A, Boutati E, Lambadiari V, Mitrou P, Raptis SA. 2007. Glucose transporter expression on the plasma membrane of resting and activated white blood cells. Eur J Clin Invest 37:282-290.
38. Marsden VS, Strasser A. 2003. Control of apoptosis in the immune system: Bcl-2, BH3-only proteins and more. Annu Rev Immunol 21:71-105.
39. Martins EF, Miyasaka CK, Newsholme P, Curi R, Carpinelli AR. 2004. Changes of fatty acid composition in incubated rat pancreatic islets. Diabetes Metab 30:21-27.
40. Merrill AH, Jr. 2002. De novo sphingolipid biosynthesis: A necessary, but dangerous, pathway. J Biol Chem 277:25843-25846.
41. Miyasaka CK, Mendonca JR, Nishiyama A, de Souza JA, Pires de Melo M, Pithon-Curi TC, Curi R. 2001. Comparative effects of fish oil given by gavage and fish oil-enriched diet on leukocytes. Life Sci 69:1739-1751.
42. Muller D, Jones PM, Persaud SJ. 2006. Autocrine anti-apoptotic and proliferative effects of insulin in pancreatic beta-cells. FEBS Lett 580:6977-6980.
43. Newsholme EA. 1996. The possible role of glutamine in some cells of the immune system and the possible consequence for the whole animal. Experientia 52:455-459.
44. Newsholme EA, Newsholme P, Curi R. 1987. The role of the citric acid cycle in cells of the immune system and its importance in sepsis, trauma and burns. Biochem Soc Symp 54:145-162.
45. Newsholme P, Curi R, Pithon Curi TC, Murphy CJ, Garcia C, Pires de Melo M. 1999. Glutamine metabolism by lymphocytes, macrophages, and neutrophils: Its importance in health and disease. J Nutr Biochem 10:316-324.
46. Newton K, Kurts C, Harris AW, Strasser A. 2001. Effects of a dominant interfering mutant of FADD on signal transduction in activated T cells. Curr Biol 11:273-276.
47. Nieves D, Moreno JJ. 2006. Effect of arachidonic and eicosapentaenoic acid metabolism on RAW 264.7 macrophage proliferation. J Cell Physiol 208:428-434.
48. Nogueira AC, Kawabata V, Biselli P, Lins MH, Valeri C, Seckler M, Hoshino W, Júnior LG, Bernik MM, de Andrade Machado JB, Martinez MB, Lotufo PA, Caldini EG, Martins E, Curi R, Soriano FG. 2008. Changes in plasma free fatty acid levels in septic patients are associated with cardiac damage and reduction in heart rate variability. Shock 29:342-348.
49. Ogino T, Ozaki M, Hosako M, Omori M, Okada S, Matsukawa A. 2009. Activation of c-Jun N-terminal kinase is essential for oxidative stress-induced Jurkat cell apoptosis by monochloramine. Leuk Res 33:151-158.
50. Opferman JT. 2008. Apoptosis in the development of the immune system. Cell Death Differ 15:234-242.
51. Otton R, Curi R. 2005. Toxicity of a mixture of fatty acids on human blood lymphocytes and leukemia cell lines. Toxicol In Vitro 19:749-755.
52. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. 2001. Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev 22:153-183.
53. Pires J, Curi R, Otton R. 2007. Induction of apoptosis in rat lymphocytes by starvation. Clin Sci (Lond) 112:59-67.
54. Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini AF. 2003. The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol 66:1499-1503.
55. Poitout V, Robertson RP. 2008. Glucolipotoxicity: Fuel excess and β-cell dysfunction. Endocr Rev 29:351-366.
56. Purasiri P, McKechnie A, Heys SD, Eremin O. 1997. Modulation in vitro of human natural cytotoxicity, lymphocyte proliferative response to mitogens and cytokine production by essential fatty acids. Immunology 92:166-172.
57. Rahman I, Kode A, Biswas SK. 2006. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159-3165.
58. Rathmell JC, Thompson CB. 2002. Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell 109:S97-S107.
59. Ricchi M, Odoardi MR, Carulli L, Anzivino C, Ballestri S, Pinetti A, Fantoni LI, Marra F, Bertolotti M, Banni S, Lonardo A, Carulli N, Loria P. 2009. Differential effect of oleic and palmitic acid on lipid accumulation and apoptosis in cultured hepatocytes. J Gastroenterol Hepatol.
60. Russell RR III, Bergeron R, Shulman GI, Young LH. 1999. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 277:H643-H649.
61. Shaikh SR, Mitchell D, Carroll E, Li M, Schneck J, Edidin M. 2008. Differential effects of a saturated and a monounsaturated fatty acid on MHC class I antigen presentation. Scand J Immunol 68:30-42.
62. Salvesen GS, Duckett CS. 2002. IAP proteins: Blocking the road to death's door. Nat Rev Mol Cell Biol 3:401-410.
63. Simon MN, Azevedo-Martins AK, Amanso AM, Carvalho CR, Curi R. 2008. Persistent activation of Akt or ERK prevents the toxicity induced by saturated and polyunsaturated fatty acids in RINm5F beta-cells. Toxicol In Vitro 22:1018-1024.
64. Stentz FB, Kitabchi AE. 2006. Palmitic acid-induced activation of human T-lymphocytes and aortic endothelial cells with production of insulin receptors, reactive oxygen species, cytokines, and lipid peroxidation. Biochem Biophys Res Commun 346:721-726.
65. Sumitomo M, Ohba M, Asakuma J, Asano T, Kuroki T, Hayakawa M. 2002. Protein kinase Cdelta amplifies ceramide formation via mitochondrial signaling in prostate cancer cells. J Clin Invest 109:827-836.
66. Sweeney G, Garg RR, Ceddia RB, Li D, Ishiki M, Somwar R, Foster LJ, Neilsen PO, Prestwich GD, Rudich A, Klip A. 2004. Intracellular delivery of phosphatidylinositol (3, 4, 5)-trisphosphate causes incorporation of glucose transporter 4 into the plasma membrane of muscle and fat cells without increasing glucose uptake. J Biol Chem 279:32233-32242.
67. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
68. Ulloth JE, Casiano CA, De Leon M. 2003. Palmitic and stearic fatty acids induce caspase-dependent and -independent cell death in nerve growth factor differentiated PC12 cells. J Neurochem 84:655-668.
69. Wood TE, Dalili S, Simpson CD, Hurren R, Mao X, Saiz FS, Gronda M, Eberhard Y, Minden MD, Bilan PJ, Klip A, Batey RA, Schimmer AD. 2008. A novel inhibitor of glucose uptake sensitizes cells to FAS-induced cell death. Mol Cancer Ther 7:3546-3555.
70. Wu H, Ichikawa S, Tani C, Zhu B, Tada M, Shimoishi Y, Murata Y, Nakamura Y. 2009. Docosahexaenoic acid induces ERK1/2 activation and neuritogenesis via intracellular reactive oxygen species production in human neuroblastoma SH-SY5Y cells. Biochim Biophys Acta 1791:8-16.
71. Xu W, Liu L, Charles IG, Moncada S. 2004. Nitric oxide induces coupling of mitochondrial signalling with the endoplasmic reticulum stress response. Nat Cell Biol 6:1129-1134.
72. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B, Roth KA, Korsmeyer SJ. 1999. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400:886-891.
73. Yoon S, Seger R. 2006. The extracellular signal-regulated kinase: Multiple substrates regulate diverse cellular functions. Growth Factors 24:21-44.
74. Zhao Y, Coloff JL, Ferguson EC, Jacobs SR, Cui K, Rathmell JC. 2008. Glucose metabolism attenuates p53 and Puma-dependent cell death upon growth factor deprivation. J Biol Chem 283:36344-36353.
75. Zou H, Li Y, Liu X, Wang X. 1999. An APAF-1. cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274:11549-11556.