ERK5/KLF4 signaling as a common mediator of the neuroprotective effects of both nerve growth factor and hydrogen peroxide preconditioning

Age

Volumn 36, Issue 4, 2014, Pages

  Su, Chang ^a   Sun, Fen ^a   Cunningham, Rebecca L ^a   Rybalchenko, Nataliya ^a   Singh, Meharvan ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

ERK5; KLF4; Neuroprotection; NGF; Oxidative stress; Preconditioning

Indexed keywords

HYDROGEN PEROXIDE; KRUPPEL LIKE FACTOR 4; MITOGEN ACTIVATED PROTEIN KINASE 7; NERVE GROWTH FACTOR; NEURONAL APOPTOSIS INHIBITORY PROTEIN; PROTEIN BAX; PROTEIN BCL 2; KRUPPEL LIKE FACTOR; NEUROPROTECTIVE AGENT; RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL TYPE; CELLULAR STRESS RESPONSE; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HIPPOCAMPAL NEURONAL CULTURE; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; PRECONDITIONING; PRIMARY CULTURE; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; METABOLISM; NEURODEGENERATIVE DISEASES; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HYDROGEN PEROXIDE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 7; NERVE GROWTH FACTOR; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION;

EID: 84903863414     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-014-9685-5     Document Type: Article

References (68)

1. Akaogi K, Nakajima Y et al (2009) KLF4 suppresses estrogen-dependent breast cancer growth by inhibiting the transcriptional activity of ERalpha. Oncogene 28(32):2894-2902
2. Aliaghaei A, Khodagholi F, et al (2014) Conditioned media of choroid plexus epithelial cells induces Nrf2-activated phase II antioxidant response proteins and suppresses oxidative stress-induced apoptosis in PC12 Cells. J Mol Neurosci
3. 2 preconditioning modulates phase II enzymes through p38 MAPK and PI3K/Akt activation. Am J Physiol Heart Circ Physiol 300(6):H2196-H2205
4. Briones AM, Touyz RM (2010) Oxidative stress and hypertension: current concepts. Curr Hypertens Rep 12(2):135-142
5. 2. Pharmacol Rep 59(5):573-579
6. Cavanaugh JE, Jaumotte JD et al (2006) Neuroprotective role of ERK1/2 and ERK5 in a dopaminergic cell line under basal conditions and in response to oxidative stress. J Neurosci Res 84(6):1367-1375 (Pubitemid 44654460)
7. Chang S, Jiang X et al (2008) Exogenous low dose hydrogen peroxide increases hypoxia-inducible factor-1alpha protein expression and induces preconditioning protection against ischemia in primary cortical neurons. Neurosci Lett 441(1):134-138
8. Cho YG, Song JH et al (2007) Genetic and epigenetic analysis of the KLF4 gene in gastric cancer. APMIS 115(7):802-808 (Pubitemid 47030107)
9. Clark PR, Jensen TJ et al (2011) MEK5 is activated by shear stress, activates ERK5 and induces KLF4 to modulate TNF responses in human dermal microvascular endothelial cells. Microcirculation 18(2):102-117
10. Clark VE, Erson-Omay EZ et al (2013) Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339(6123):1077-1080
11. Cundiff P, Liu L et al (2009) ERK5 MAP kinase regulates neurogenin1 during cortical neurogenesis. PLoS One 4(4):e5204
12. Davies SP, Reddy H et al (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351(Pt 1):95-105
13. Dijkmans TF, van Hooijdonk LW et al (2009) Identification of new Nerve Growth Factor-responsive immediate-early genes. Brain Res 1249:19-33
14. Dirnagl U, Becker K et al (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8(4):398-412
15. Dong HM, Huang L (2009) Role of the transcription factor Kruppel-like factor 4 (KLF4) in the pathogenesis of atherosclerosis. Zhonghua Xin Xue Guan Bing Za Zhi 37(10):950-952
16. Fuenzalida K, Quintanilla R et al (2007) Peroxisome proliferator- activated receptor gamma up-regulates the Bcl-2 antiapoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J Biol Chem 282(51):37006-37015
17. Fukuhara S, Marinissen MJ et al (2000) Signaling from G protein-coupled receptors to ERK5/Big MAPK 1 involves Galpha q and Galpha 12/13 families of heterotrimeric G proteins. Evidence for the existence of a novel Ras AND Rho-independent pathway. J Biol Chem 275(28):21730-21736 (Pubitemid 30481882)
18. Furuichi T, Liu W et al (2005) Generation of hydrogen peroxide during brief oxygen-glucose deprivation induces preconditioning neuronal protection in primary cultured neurons. J Neurosci Res 79(6):816-824 (Pubitemid 40476506)
19. Godmann M, Kosan C et al (2010) Kruppel-like factor 4 is widely expressed in the mouse male and female reproductive tract and responds as an immediate early gene to activation of the protein kinase A in TM4 Sertoli cells. Reproduction 139(4):771-782
20. Greene LA (1978) Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-freemedium. J Cell Biol 78(3):747-755
21. 2. Role in cell survival following oxidant injury. J Biol Chem 271(8):4138-4142
22. Hota KB, Hota SK et al (2012) Acetyl-L-carnitine-mediated neuroprotection during hypoxia is attributed to ERK1/2-Nrf2-regulated mitochondrial biosynthesis. Hippocampus 22(4):723-736
23. Jou MJ (2008) Pathophysiological and pharmacological implications of mitochondria-targeted reactive oxygen species generation in astrocytes. Adv Drug Deliv Rev 60(13-14):1512-1526
24. Kim DK, Cho ES et al (2001) Adaptive concentrations of hydrogen peroxide suppress cell death by blocking the activation of SAPK/JNK pathway. J Cell Sci 114(Pt 23):4329-4334 (Pubitemid 33138669)
25. Ky N, Lim CB et al (2009) KLF4 suppresses HDACi induced caspase activation and the SAPK pathway by targeting p57(Kip2). Apoptosis 14(9):1095-1107
26. Lebesgue D, Chevaleyre V et al (2009) Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids 74(7):555-561
27. Lee BR, Um HD (1999) Hydrogen peroxide suppresses U937 cell death by two different mechanisms depending on its concentration. Exp Cell Res 248(2):430-438 (Pubitemid 29394803)
28. Li RC, Morris MW et al (2008) Neuroglobin protects PC12 cells against oxidative stress. Brain Res 1190:159-166
29. Li Z, Zhao J et al (2010) KLF4 promotes hydrogen-peroxide-induced apoptosis of chronic myeloid leukemia cells involving the bcl-2/bax pathway. Cell Stress Chaperones 15(6):905-912
30. Liu L, Cavanaugh JE et al (2003) ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc Natl Acad Sci U S A 100(14):8532-8537 (Pubitemid 36842579)
31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408 (Pubitemid 34164012)
32. Miller AA, Budzyn K et al (2010) Vascular dysfunction in cerebrovascular disease: mechanisms and therapeutic intervention. Clin Sci (Lond) 119(1):1-17
33. Mo L, Yang C et al (2012) PI3K/Akt signaling pathway-induced heme oxygenase-1 upregulation mediates the adaptive cytoprotection of hydrogen peroxide preconditioning against oxidative injury in PC12 cells. Int JMol Med 30(2):314-320
34. Moore DL, Blackmore MG et al (2009) KLF family members regulate intrinsic axon regeneration ability. Science 326(5950):298-301
35. Murphy LO, Blenis J (2006) MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31(5):268-275 (Pubitemid 43674354)
36. Nair VD, Olanow CW (2008) Differential modulation of Akt/glycogen synthase kinase-3beta pathway regulates apoptotic and cytoprotective signaling responses. J Biol Chem 283(22):15469-15478
37. Nakahara Y, Northcott PA et al (2010) Genetic and epigenetic inactivation of Kruppel-like factor 4 in medulloblastoma. Neoplasia 12(1):20-27
38. Nigro P, Abe J et al (2011) Flow shear stress and atherosclerosis: a matter of site specificity. Antioxid Redox Signal 15(5):1405-1414
39. Obara Y, Yamauchi A et al (2009) ERK5 activity is required for nerve growth factor-induced neurite outgrowth and stabilization of tyrosine hydroxylase in PC12 cells. J Biol Chem 284(35):23564-23573
40. Obata K, Katsura H et al (2007) Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain. J Neurochem 102(5):1569-1584 (Pubitemid 47256198)
41. Ohnesorge N, Viemann D et al (2010) Erk5 activation elicits a vasoprotective endothelial phenotype via induction of Kruppel-like factor 4 (KLF4). J Biol Chem 285(34):26199-26210
42. Ohtsuka M, Fukumitsu H et al (2009) Neurotrophin-3 stimulates neurogenetic proliferation via the extracellular signal-regulated kinase pathway. J Neurosci Res 87(2):301-306
43. Pan YW, Storm DR et al. (2013) Role of adult neurogenesis in hippocampus-dependent memory, contextual fear extinction and remote contextual memory: new insights from ERK5 MAP kinase. Neurobiol Learn Mem
44. Park CS, Lee PH et al (2012) Kruppel-like factor 4 (KLF4) promotes the survival of natural killer cells and maintains the number of conventional dendritic cells in the spleen. J Leukoc Biol 91(5):739-750
45. Pazyra-Murphy MF, Hans A et al (2009) A retrograde neuronal survival response: target-derived neurotrophins regulate MEF2D and bcl-w. J Neurosci 29(20):6700-6709
46. Pi X, Yan C et al (2004) Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis. Circ Res 94(3):362-369 (Pubitemid 38240728)
47. Roux PP, Blenis J (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68(2):320-344 (Pubitemid 38756868)
48. Sanchez A, Tripathy D et al (2012) Pigment epithelium-derived factor (PEDF) protects cortical neurons in vitro from oxidant injury by activation of extracellular signal-regulated kinase (ERK) 1/2 and induction of Bcl-2. Neurosci Res 72(1):1-8
49. 2+ channels. Proc Natl Acad Sci U S A 105(39):15148-15153
50. Scapoli L, Ramos-Nino ME et al (2004) Src-dependent ERK5 and Src/EGFR-dependent ERK1/2 activation is required for cell proliferation by asbestos. Oncogene 23(3):805-813 (Pubitemid 38241281)
51. Seidman R, Gitelman I et al (2001) The role of ERK 1/2 and p38 MAP-kinase pathways in taxol-induced apoptosis in human ovarian carcinoma cells. Exp Cell Res 268(1):84-92 (Pubitemid 32678863)
52. Shalizi A, Lehtinen M et al (2003) Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23(19):7326-7336 (Pubitemid 36999522)
53. Singh M, Setalo G Jr et al (1999) Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19(4):1179-1188 (Pubitemid 29088901)
54. Su C, Underwood W et al (2011) ERK1/2 and ERK5 have distinct roles in the regulation of brain-derived neurotrophic factor expression. J Neurosci Res 89(10):1542-1550
55. Sunadome K, Yamamoto T et al (2011) ERK5 regulates muscle cell fusion through Klf transcription factors. Dev Cell 20(2):192-205
56. Suzaki Y, Yoshizumi M et al (2002) Hydrogen peroxide stimulates c-Src-mediated big mitogen-activated protein kinase 1 (BMK1) and the MEF2C signaling pathway in PC12 cells: potential role in cell survival following oxidative insults. J Biol Chem 277(11):9614-9621 (Pubitemid 34953051)
57. Suzaki Y, Yoshizumi M et al (2004) BMK1 is activated in glomeruli of diabetic rats and in mesangial cells by high glucose conditions. Kidney Int 65(5):1749-1760 (Pubitemid 38591023)
58. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676 (Pubitemid 44233629)
59. Tatake RJ, O'Neill MM et al (2008) Identification of pharmacological inhibitors of the MEK5/ERK5 pathway. Biochem Biophys Res Commun 377(1):120-125
60. 2+ influx via NMDA receptors and contributes to ischemic tolerance in the hippocampal CA1 region of rats. Life Sci 79(19):1839-1846
61. Wang Y, Su B et al (2006b) Brain-derived neurotrophic factor activates ERK5 in cortical neurons via a Rap1-MEKK2 signaling cascade. J Biol Chem 281(47):35965-35974 (Pubitemid 46041328)
62. Wang W, Pan YW et al (2013) Extracellular signal-regulated kinase 5 (ERK5) mediates prolactin-stimulated adult neurogenesis in the subventricular zone and olfactory bulb. J Biol Chem 288(4):2623-2631
63. Watson FL, Heerssen HM et al (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 4(10):981-988 (Pubitemid 32924137)
64. Wiese AG, Pacifici RE et al (1995) Transient adaptation of oxidative stress in mammalian cells. Arch Biochem Biophys 318(1):231-240
65. Wruck CJ, Claussen M et al (2007) Luteolin protects rat PC12 and C6 cells against MPP+induced toxicity via an ERK dependent Keap1-Nrf2-ARE pathway. J Neural Transm Suppl(72):57-67
66. Xiao H, Lv F et al (2011) Deprenyl prevents MPP(+)-induced oxidative damage in PC12 cells by the upregulation of Nrf2-mediated NQO1 expression through the activation of PI3K/Akt and Erk. Toxicology 290(2-3):286-294
67. Yu SJ, Grider JR et al (2012) Up-regulation of brain-derived neurotrophic factor is regulated by extracellular signal-regulated protein kinase 5 and by nerve growth factor retrograde signaling in colonic afferent neurons in colitis. Exp Neurol 238(2):209-217
68. Zhu S, Tai C et al (2009) Glutamatergic stimulation triggers rapid Krupple-like factor 4 expression in neurons and the overexpression of KLF4 sensitizes neurons to NMDA-induced caspase-3 activity. Brain Res 1250:49-62