Amyloid beta enhances cytosolic phospholipase A2 level and arachidonic acid release via nitric oxide in APP-transfected PC12 cells

• Autorzy: Chalimoniuk M. , Stolecka A. , Cakala M. , Hauptmann S. , Schulz K. , Lipka U. , Leuner K. , Eckert A. , Muller W.E. , Strosznajder J.B.
• Języki publikacji: EN

Abstrakty

EN

Cytosolic phospholipase A2 (cPLA2) preferentially liberates arachidonic acid (AA), which is known to be elevated in Alzheimer's disease (AD). The aim of this study was to investigate the possible relationship between enhanced nitric oxide (NO) generation observed in AD and cPLA2 protein level, phosphorylation, and AA release in rat pheochromocytoma cell lines (PC12) differing in amyloid beta secretion. PC12 control cells, PC12 cells bearing the Swedish double mutation in amyloid beta precursor protein (APPsw), and PC12 cells transfected with human APP (APPwt) were used. The transfected APPwt and APPsw PC12 cells showed an about 2.8- and 4.8-fold increase of amyloid β (Aβ) secretion comparing to control PC12 cells. An increase of NO synthase activity, cGMP and free radical levels in APPsw and APPwt PC12 cells was observed. cPLA2 protein level was higher in APPsw and APPwt PC12 cells comparing to PC12 cells. Moreover, phosphorylated cPLA2 protein level and [3H]AA release were also higher in APP-transfected PC12 cells than in the control PC12 cells. An NO donor, sodium nitroprusside, stimulated [3H]AA release from prelabeled cells. The highest NO-induced AA release was observed in control PC12 cells, the effect in the other cell lines being statistically insignificant. Inhibition of cPLA2 by AACOCF3 significantly decreased the AA release. Inhibitors of nNOS and γ-secretase reduced AA release in APPsw and APPwt PC12 cells. The basal cytosolic [Ca2+]i and mitochondrial Ca2+ concentration was not changed in all investigated cell lines. Stimulation with thapsigargin increased the cytosolic and mitochondrial Ca2+ level, activated NOS and stimulated AA release in APP-transfected PC12 cells. These results indicate that Aβ peptides enhance the protein level and phosphorylation of cPLA2 and AA release by the NO signaling pathway.

Słowa kluczowe

EN

arachidonic acid; calcium; nitric oxide synthase; mitochondrion; amyloid beta; cytosolic phospholipase A2; reactive oxygen species; antioxidative enzyme

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2007
• Tom: 54
• Numer: 3
• Opis fizyczny: p.611-623,fig.,ref.

Twórcy

autor

Chalimoniuk M.

• Polish Academy of Sciences, A.Pawinskiego 5a, 01-106 Warsaw, Poland

autor

Stolecka A.

autor

Cakala M.

autor

Hauptmann S.

autor

Schulz K.

autor

Lipka U.

autor

Leuner K.

autor

Eckert A.

autor

Muller W.E.

autor

Strosznajder J.B.

Bibliografia

• Adamczyk A, Kazimierczak A, Strosznajder JB (2006) Alpha- synuclein and its neurotoxic fragment inhibit dopamine uptake into rat striatal synaptosomes. Relationship to nitric oxide. Neurochem Int 49: 407–412.
• Bazan NG, Colangelo V, Lukiw WJ (2002) Prostaglandins and other lipid mediators in Alzheimer’s disease. Prostaglandins Other Lipid Mediat 68–69: 197–210.
• Birbes H, Gothie E, Pageaux JF, Lagarde M, Laugier C (2000) Hydrogen peroxide activation of Ca2+-independent phospholipase A2 in uterine stromal cells. Biochem Biophys Res Commun 276: 613–618.
• Buchet R, Pikuła S (2000) Alzheimer’s disease: its origin at the membrane, evidence and questions. Acta Biochim Polon 47: 725–733.
• Butterfield DA (2002) Amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer’s disease brain. A review. Free Radic Res 36: 1307–1313.
• Butterfield DA, Boyd-Kimball D (2004) Amyloid betapeptide (1–42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol 14: 426–432.
• Cai XD, Golde TE, Younkin SG (1993) Release of excess amyloid beta protein from a mutant amyloid beta protein precursor. Science 259: 514–516.
• Chalimoniuk M, Strosznajder JB (1998) Aging modulates nitric oxide synthesis and cGMP levels in hippocampus and cerebellum. Effects of amyloid beta peptide. Mol Chem Neuropathol 35: 77–95.
• Chalimoniuk M, Głowacka J, Zabielna A, Eckert A, Strosznajder JB (2006a) Nitric oxide alters arachidonic acid turnover in brain cortex synaptoneurosomes. Neurochem Int 48: 1–8.
• Chalimoniuk M, King-Pospisil K, Metz CN, Toborek M (2006b) Macrophage migration inhibitor factor induces cell death and decreases neuronal nitric oxide expression in spinal cord neurons. Neuroscience 139: 1117–1128.
• Citron M, Westaway D, Xia W, Carlson G, Diehl T, Levesque G, Johnsin-Wood R, Lee M, Seubert P, Davis A, Kholodenko D, Motter R, Sherrington R, Perry B, Ya H, Stome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St George-Hyslop P, Selkoe DJ (1997) Mutant presenilins of Alzheimer’s disease increase production of 42-residue amyloid beta transfected cells and transgenic mice. Nat Med 3: 1021–1023.
• Dobashi K, Asayama K, Nakane T, Kodera K, Hayashibe H, Nakazawa S (2001) Induction of glutathione peroxidase in response to inactivation by nitric oxide. Free Radic Res 35: 319–327.
• Eckert A, Steiner B, Marques C, Leutz S, Romig H, Haass C, Muller WE (2001) Elevated vulnerability to oxidative stress-induced cell death and activation of caspase-3 by the Swedish amyloid precursor protein mutation. J Neurosci Res 64: 183–193.
• Evans JH, Fergus DJ, Leslie ChC (2002) Inhibition of the MEK1/Erk pathway reduces arachidonic acid release independently of cPLA2 phosphorylation and translocation. BMC Biochem 3: 30–42.
• Farooqui AA, Yang H-Ch, Rosenberger TA, Horrocks LA (1997) Phospholipase A2 and its role in brain tissue. J Neurochem 69: 889–901.
• Gijon MA, Spencer DM, Siddiqi AR, Bonventre JV, Leslie CC (2000) Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that do and do not mobilize calcium. Novel role of mitogenactivated protein kinase pathways in cytosolic phospholipase A2 regulation. J Biol Chem 275: 20146–20156.
• Haass C (2004) Take five-BACE and the gamma-secretase quartet conduct Alzheimer’s amyloid β-peptide generation. EMBO J 23: 483–488.
• Handlogten ME, Huang C, Shiraishi N, Awata H, Miller RT (2001) The Ca2+-sensing receptor activates cytosolic phospholipase A2 via a Gqα-dependent ERK-independent pathway. J Biol Chem 276: 13941–13948.
• Hauptmann S, Keil U, Scherping I, Bonert A, Eckert A, Muller WE (2006) Mitochondrial dysfunction in sporadic and genetic Alzheimer’s disease. Exp Gerontol 41: 668–673.
• Hempel SL, Buettner GR, O’Malley YQ, Wessels DA, Flaherty DM (1999) Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2’,7’-dichlorodihydrofluorescein diacetate, 5 (and 6)-carboxy-2’,7’-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radic Biol Med 27: 146–159.
• Holscher C (1998) Possible causes of Alzheimer’s disease: amyloid fragments, free radicals, and calcium homeostasis. Neurobiol Dis 5: 129–141.
• Keil U, Bonert A, Marques CA, Scherping I, Weyermann J, Strosznajder JB, Muller-Spahn F, Haass Ch, Czech Ch, Paradier L, Muller WE, Eckert A (2004) Amyloid betainduced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J Biol Chem 279: 50310–50320.
• Kukreja RC, Kontos HA, Hess ML, Ellis E (1986) PGH synthase and lipooxygenase generate superoxide in the presence of NADH or NADPH. Circul Res 59: 612–619, 1986.
• Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
• Lahiri DK, Chen D, Ge Y-W, Farlow M, Kotwal G, Kanthasamy A, Ingram DK, Greig NH (2003) Does nitric oxide synthase contribute to the pathogenesis of Alzheimer’s disease? Effects of β-amyloid deposition on NOS in transgenic mouse brain with AD pathology. Ann NY Acad Sci 1010: 639–642.
• Lukiw WJ, Bazan NG (2000) Neuroinflammatory signaling upregulation in Alzheimer’s disease. Neurochem Res 25: 1173–1184.
• Luth HJ, Arendt Th (1998) Nitric oxide and Alzheimer’s disease. J Brain Res 39: 245–251.
• Luth HJ, Holzer M, Gartner U, Staufenbiel M, Arendt T (2001) Expression of endothelial and inducible NOSisoforms is increased in Alzheimer’s disease, in APP23
• transgenic mice and after experimental brain lesion in rat: evidence for an induction by amyloid pathology. Brain Res 913: 57–67.
• Madesh M, Balasnbramamin KA (1997) Activation of liver mitochondrial phospholipase A2 by superoxide. Arch Biochem Biophys 346: 187–192.
• Marques CA, Keil U, Bonert A, Steiner B, Haass C, Muller WE, Eckert A (2003) Neurotoxic mechanisms caused by the Alzheimer’s disease-linked Swedish amyloid precursor protein mutation: oxidative stress, caspases, and the JNK pathway. J Biol Chem 278: 28294–28302.
• Miyamoto Y, Koh YH, Park YS, Fujiwara N, Sakiyama H, Misonou Y, Ookawara T, Suzuki K, Honke K, Taniguchi N (2003) Oxidative stress caused by inactivation of glutathione peroxidase and adaptive responses. J Biol Chem 384: 567–574.
• Molloy GY, Rattray M, Willams RJ (1998) Genes encoding multiple forms of phospholipase A2 are expressed in rat brain. Neurosci Lett 258: 139–142.
• Murakami M, Nakatani Y, Atsumi G, Inoue K, Kudo I (1997) Regulatory functions of phospholipase A2. Crit Rev Immunol 17: 225–283.
• Oh SO, Hong JH, Kim YR, Yoo HS, Lee SH, Lim K, Hwang BD, Exton JH, Park SK (2000) Regulation of phospholipase D2 by H2O2 in PC12 cells. J Neurochem 75: 2445–2454.
• Perry G, Cash AD, Smith MA (2002) Alzheimer’s disease and oxidative stress. J Biomed Biotechnol 2: 120–123.
• Pratico D, Sung S (2004) Lipid peroxidation and oxidative imbalance: early functional events in Alzheimer’s disease. J Alzheimers Dis 6: 171–175.
• Rosenberger TA, Villacreses NE, Hovda JT, Bosetti F, Weerasinghe G, Wine RN, Harry GJ, Rapoport SI (2004) Rat brain arachidonic acid metabolism is induced by a six-day intracerebral ventricular infusion of bacterial lipopolysaccharide. J Neurochem 88: 1168–1178.
• Ross BM, Moszczynska A, Erlich J, Kish SJ (1998) Phospholipid-metabolizing enzymes in Alzheimer’s disease: increased lysophospholipid acyltransferase activity and decreased phospholipase A2 activity. J Neurochem 70: 786–793.
• Rothe G, Valet G (1990) Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2’,7’-dichlorofluorescin. J Leukocyt Biol 47: 440–448.
• Royall JA, Ischiropoulos H (1993) Evaluation of 2’,7’-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 302: 348–355.
• Samanta S, Perkinton MS, Morgan M, Williams RJ (1998) Hydrogen peroxide enhances signal-responsive arachidonic acid release from neurons: role of mitogen-activated protein kinase. J Neurochem 70: 2082–2090.
• Sapirstein A, Spech RA, Witzgall R, Bonvetre JV (1996) Cytosolic phospholipase A2 (PLA2), but not secretery PLA2, potentiates hydrogen peroxide cytotoxicity in kidney epithelial cells. J Biol Chem 271: 21505–21513.
• Schuessel K, Frey C, Jourdan C, Keil U, Weber CC, Muller-Spahn F, Muller WE, Eckert A, (2006) Aging sensitizes toward ROS formation and lipid peroxidation in PS1M146L transgenic mice. Free Radic Biol Med 40: 850–862.
• Selkoe DJ (2001) Presenilin, Notch, and the genesis and treatment of Alzheimer’s disease. Proc Natl Acad Sci USA 98: 11039–11041.
• Selkoe DJ (2006) The ups and downs of Aβ. Nature Med 12: 758–759.
• Shasby DM, Winter M, Shasby SS (1988) Oxidants and conductance of cultured epithelial cell monolayers: inositol phospholipid hydrolysis. Am J Physiol 255: C781–C788.
• Shimizu M, Azuma C, Taniguchi T, Murayama T (2004) Expression of cytosolic phospholipase A2 alpha in murine PC12 cells, a variant of L929 cells, induces arachidonic acid release in response to phorbol myristate acetate and Ca2+ ionophores, but not to tumor necrosis factor-alpha. J Pharm Sci 96: 324–332.
• Six DA, Dennis EA (2000) The expading superfamily of phospholipase A2 enzymes: classification and characterization. Biochim Biophys Acta 1488: 1–19.
• Stephenson DT, Lemere CA, Selkoe DJ, Clemens JA (1996) Cytosolic phospholipase A2 (cPLA2) immunoreactivity is elevated in Alzheimer’s disease brain. Neurobiol Dis 3: 51–63.
• Strokin M, Sergeeva M, Reiser G (2003) Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and Ca2+. Br J Pharmacol 139: 1014–1022.
• Sun GY, Hu J, Jensen MD, Simonyi A (2004) Phospholipase A2 in the central nervous system: implications for neurodegenerative diseases. J Lipids Res 45: 205–213.
• Teismann P, Vila M, Choi DK, Tieu K, Wu DC, Jackson- Lewis V, Przedborski S (2003) COX-2 and neurodegeneration in Parkinson’s disease. Ann N Y Acad Sci 991: 272–277.
• Xu J, Weng YI, Simonyi A, Krugh BW, Liao Z, Weisman GA, Sun GY, Simonyi A (2002) Role of PKC and MAPK in cytosolic PLA2 phosphorylation and arachidonic acid release in primary murine astrocytes. J Neurochem 83: 259–270.
• Xu J, Yu S, Sun AY, Sun GY (2003) Oxidant-mediated AA release from astrocytes involves cPLA2 and iPLA2. Free Radic Biol Med 34: 1531–1543.
• Yatin SM, Varadarajan S, Link CD, Butterfield DA (1999) In vitro and in vivo oxidative stress associated with Alzheimer’s amyloid-beta peptide (1–42). Neurobiol Aging 20: 325–330; Discussion 339–342.