C-terminal mechano-growth factor induces heme oxygenase-1-mediated neuroprotection of SH-SY5Y cells via the protein kinase Cε/Nrf2 pathway

Journal of Neuroscience Research

Volumn 89, Issue 3, 2011, Pages 394-405

  Quesada, Arnulfo ^a,b   Ogi, Julie ^b   Schultz, James ^b   Handforth, Adrian ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

Apoptosis; HO 1; Nrf2; Oxidative stress; Parkinson's disease; PKC

Indexed keywords

GROWTH FACTOR; HEME OXYGENASE 1; PROTEIN KINASE C EPSILON; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN; CELL STRAIN SH SY5Y; ENZYME ACTIVITY; GENE SILENCING; GENE TRANSLOCATION; NEUROPROTECTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

ANALYSIS OF VARIANCE; CELL LINE, TUMOR; CELL SURVIVAL; HEME OXYGENASE-1; HUMANS; INSULIN-LIKE GROWTH FACTOR I; NEUROBLASTOMA; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDOPAMINE; PEPTIDE FRAGMENTS; PROTEIN KINASES; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYMPATHOLYTICS; TRANSFECTION; UP-REGULATION;

EID: 78751695298     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22543     Document Type: Article

References (56)

1. Adams RN, Murrill E, McCreery R, Blank L, Karolczak M. 1972. 6-Hydroxydopamine, a new oxidation mechanism. Eur J Pharmacol 17: 287-292.
2. Aperghis M, Johnson IP, Cannon J, Yang SY, Goldspink G. 2004. Different levels of neuroprotection by two insulin-like growth factor-I splice variants. Brain Res 1009: 213-218.
3. Bar-Am O, Amit T, Youdim MB. 2007. Aminoindan and hydroxyaminoindan, metabolites of rasagiline and ladostigil, respectively, exert neuroprotective properties in vitro. J Neurochem 103: 500-508.
4. Baranano DE, Snyder SH. 2001. Neural roles for heme oxygenase: contrasts to nitric oxide synthase. Proc Natl Acad Sci U S A 98: 10996-11002.
5. Behrens MM, Strasser U, Koh JY, Gwag BJ, Choi DW. 1999. Prevention of neuronal apoptosis by phorbol ester-induced activation of protein kinase C: blockade of p38 mitogen-activated protein kinase. Neuroscience 94: 917-927.
6. Burton NC, Kensler TW, Guilarte TR. 2006. In vivo modulation of the Parkinsonian phenotype by Nrf2. Neurotoxicology 27: 1094-1100.
7. Calabrese V, Lodi R, Tonon C, D'Agata V, Sapienza M, Scapagnini G, Mangiameli A, Pennisi G, Stella AM, Butterfield DA. 2005. Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J Neurol Sci 233: 145-162.
8. Calkins JM, Johnson DA, Townsend JA, Vargas MR, Dowell JA, Williamson TP, Kraft AD, Lee JM, Li J, Johnson JA. 2009. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal 3: 497-508 review.
9. Cao TT, Ma L, Kandpal G, Warren L, Hess JF, Seabrook GR. 2005. Increased nuclear factor-erythroid 2 p45-related factor 2 activity protects SH-SY5Y cells against oxidative damage. J Neurochem 95: 406-417.
10. Carpenter V, Matthews K, Devlin G, Stuart S, Jensen J, Conaglen J, Jeanplong F, Goldspink P, Yang SY, Goldspink G, Bass J, McMahon C. 2008. Mechano-growth factor reduces loss of cardiac function in acute myocardial infarction. Heart Lung Circ 17: 33-39.
11. Carter CA, Kane CJ. 2004. Therapeutic potential of natural compounds that regulate the activity of protein kinase C. Curr Med Chem 11: 2883-2902.
12. Chen K, Gunter K, Maines MD. 2000. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 75: 304-313.
13. Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, Kan YW, Johnson JA. 2009. Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte. Proc Natl Acad Sci U S A 106: 2933-2938.
14. Cohen G, Heikkila RE. 1974. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 249: 2447-2452.
15. Cuadrado A, Rojo AI. 2008. Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections. Curr Pharm Des 14: 429-442.
16. Dave KR, DeFazio RA, Raval AP, Torraco A, Saul I, Barrientos A, Perez-Pinzon MA. 2008. Ischemic preconditioning targets the respiration of synaptic mitochondria via protein kinase C epsilon. J Neurosci 28: 4172-4182.
17. Dennery PA. 2000. Regulation and role of heme oxygenase in oxidative injury. Curr Top Cell Regul 36: 181-199.
18. Dennery PA, Sridhar KJ, Lee CS, Wong HE, Shokoohi V, Rodgers PA, Spitz DR. 1997. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem 272: 14937-14942.
19. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P. 2002. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci U S A 99: 11908-11913.
20. Dluzniewska J, Sarnowska A, Beresewicz M, Johnson I, Srai SK, Ramesh B, Goldspink G, Gorecki DC, Zablocka B. 2005. A strong neuroprotective effect of the autonomous C-terminal peptide of IGF-1 Ec (MGF) in brain ischemia. FASEB J 19: 1896-1898.
21. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH. 1999. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A 96: 2445-2450.
22. Fernandez-Gonzalez A, Perez-Otano I, Morgan JI. 2000. MPTP selectively induces haem oxygenase-1 expression in striatal astrocytes. Eur J Neurosci 12: 1573-1583.
23. Huang E, Ong WY, Go ML, Garey LJ. 2005. Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment. J Neurosci Res 80: 268-278.
24. Huang HC, Nguyen T, Pickett CB. 2002. Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 277: 42769-42774.
25. Hung SY, Liou HC, Kang KH, Wu RM, Wen CC, Fu WM. 2008. Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4-phenylpyridinium-induced neurotoxicity. Mol Pharmacol 74: 1564-1575.
26. Hwang YP, Jeong HG. 2008. The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett 582: 2655-2662.
27. Hwang YP, Kim HG, Han EH, Jeong HG. 2008. Metallothionein-III protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a PI3K and ERK/Nrf2-dependent manner. Toxicol Appl Pharmacol 231: 318-327.
28. Itoh K, Tong KI, Yamamoto M. 2004. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med 36: 1208-1213.
29. Jakel RJ, Townsend JA, Kraft AD, Johnson JA. 2007. Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144: 192-201.
30. Kong AN, Owuor E, Yu R, Hebbar V, Chen C, Hu R, Mandlekar S. 2001. Induction of xenobiotic enzymes by the MAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab Rev 33: 255-271.
31. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA. 2003. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278: 12029-12038.
32. Li MH, Cha YN, Surh YJ. 2006. Carbon monoxide protects PC12 cells from peroxynitrite-induced apoptotic death by preventing the depolarization of mitochondrial transmembrane potential. Biochem Biophys Res Commun 342: 984-990.
33. Morse D, Choi AM. 2002. Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27: 8-16.
34. Nakaso K, Yano H, Fukuhara Y, Takeshima T, Wada-Isoe K, Nakashima K. 2003. PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Lett 546: 181-184.
35. Numazawa S, Ishikawa M, Yoshida A, Tanaka S, Yoshida T. 2003. Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am J Physiol Cell Physiol 285: C334-C342.
36. Otterbein LE, Soares MP, Yamashita K, Bach FH. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24: 449-455.
37. Owuor ED, Kong AN. 2002. Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol 64: 765-770.
38. Panahian N, Yoshiura M, Maines MD. 1999. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72: 1187-1203.
39. Prawan A, Kukongviriyapan V, Tassaneeyakul W, Pairojkul C, Bhudhisawasdi V. 2005. Association between genetic polymorphisms of CYP1A2, arylamine N-acetyltransferase 1 and 2 and susceptibility to cholangiocarcinoma. Eur J Cancer Prev 14: 245-250.
40. Quesada A, Micevych P, Handforth A. 2009. C-terminal mechano growth factor protects dopamine neurons: a novel peptide that induces heme oxygenase-1. Exp Neurol 220: 255-266.
41. Ramsey CP, Glass CA, Montgomery MB, Lindl KA, Ritson GP, Chia LA, Hamilton RL, Chu CT, Jordan-Sciutto KL. 2007. Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66: 75-85.
42. Raval AP, Dave KR, Mochly-Rosen D, Sick TJ, Perez-Pinzon MA. 2003. Epsilon PKC is required for the induction of tolerance by ischemic and NMDA-mediated preconditioning in the organotypic hippocampal slice. J Neurosci 23: 384-391.
43. Riddoch-Contreras J, Yang SY, Dick JR, Goldspink G, Orrell RW, Greensmith L. 2009. Mechano-growth factor, an IGF-I splice variant, rescues motoneurons and improves muscle function in SOD1(G93A) mice. Exp Neurol 215: 281-289.
44. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. 2005. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 175: 4408-4415.
45. Scapagnini G, D'Agata V, Calabrese V, Pascale A, Colombrita C, Alkon D, Cavallaro S. 2002. Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res 954: 51-59.
46. Schipper HM, Cisse S, Stopa EG. 1995. Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann Neurol 37: 758-768.
47. Siebert A, Desai V, Chandrasekaran K, Fiskum G, Jafri MS. 2009. Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J Neurosci Res 87: 1659-1669.
48. Soto-Otero R, Mendez-Alvarez E, Hermida-Ameijeiras A, Munoz-Patino AM, Labandeira-Garcia JL. 2000. Autoxidation and neurotoxicity of 6-hydroxydopamine in the presence of some antioxidants: potential implication in relation to the pathogenesis of Parkinson's disease. J Neurochem 74: 1605-1612.
49. Suzuki S, Hayashi H, Takagi K, Kondo T, Ueyama J, Wakusawa S. 2006. Protein kinase Cbeta isoform down-regulates the expression of MDR3 P-glycoprotein in human Chang liver cells. Biochim Biophys Acta 1760: 1552-1557.
50. Weinreb O, Amit T, Bar-Am O, Chillag-Talmor O, Youdim MB. 2005. Novel neuroprotective mechanism of action of rasagiline is associated with its propargyl moiety: interaction of Bcl-2 family members with PKC pathway. Ann N Y Acad Sci 1053: 348-355.
51. Yang L, Calingasan NY, Thomas B, Chaturvedi RK, Kiaei M, Wille EJ, Liby KT, Williams C, Royce D, Risingsong R, Musiek ES, Morrow JD, Sporn M, Beal MF. 2009. Neuroprotective effects of the triterpenoid, CDDO methyl amide, a potent inducer of Nrf2-mediated transcription. PLoS One 4: e5757.
52. Yang S, Alnaqeeb M, Simpson H, Goldspink G. 1996. Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J Muscle Res Cell Motil 17: 487-495.
53. Yoo MS, Chun HS, Son JJ, DeGiorgio LA, Kim DJ, Peng C, Son JH. 2003. Oxidative stress regulated genes in nigral dopaminergic neuronal cells: correlation with the known pathology in Parkinson's disease. Brain Res Mol Brain Res 110: 76-84.
54. Zhang H, Forman HJ. 2008. Acrolein induces heme oxygenase-1 through PKC-delta and PI3K in human bronchial epithelial cells. Am J Respir Cell Mol Biol 38: 483-490.
55. Zhao X, Song S, Sun G, Strong R, Zhang J, Grotta JC, Aronowski J. 2009. Neuroprotective role of haptoglobin after intracerebral hemorrhage. J Neurosci 29: 15819-15827.
56. Zhou Y, Wang D, Li F, Shi J, Song J. 2006. Different roles of protein kinase C-betaI and -delta in the regulation of adipocyte differentiation. Int J Biochem Cell Biol 38: 2151-2163.