WISP1 neuroprotection requires FoxO3a post-translational modulation with autoregulatory control of SIRT1

Current Neurovascular Research

Volumn 10, Issue 1, 2013, Pages 54-69

  Wang, Shaohui ^a,c   Chong, Zhao Zhong ^a,c   Shang, Yan Chen ^a,c   Maiese, Kenneth ^a,b,c  

^a New Jersey Medical School University Hospital Cancer Center   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^c New Jersey Health Sciences University   (United States)

Author keywords

14 3 3 protein; Akt1; Apoptosis; Caspase; CCN4; Forkhead transcription factor; FoxO3a; Histone deacetylase; Neurons; Oxidative stress; PI 3 K; SIRT1; Sirtuin; WISP1

Indexed keywords

CASPASE 3; INTERLEUKIN 1BETA CONVERTING ENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN 14 3 3; PROTEIN KINASE B; REGULATOR PROTEIN; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; WNT1 INDUCIBLE SIGNALING PATHWAY PROTEIN 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOREGULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENZYME INACTIVATION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT;

EID: 84873045065     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/156720213804805945     Document Type: Article

References (84)

1. Maiese K, Chong ZZ, Shang YC, Wang S. Targeting disease through novel pathways of apoptosis and autophagy. Expert opinion on therapeutic targets. 2012 Aug 27;(in press).
2. Su F, Overholtzer M, Besser D, Levine AJ. WISP-1 attenuates p53- mediated apoptosis in response to DNA damage through activation of the Akt kinase. Genes Dev. 2002 Jan 1;16(1):46-57.
3. Colston JT, de la Rosa SD, Koehler M, Gonzales K, Mestril R, Freeman GL, et al. Wnt-induced secreted protein-1 is a prohypertrophic and profibrotic growth factor. Am J Physiol Heart Circ Physiol. 2007 Sep;293(3):H1839-46.
4. Heise RL, Stober V, Cheluvaraju C, Hollingsworth JW, Garantziotis S. Mechanical stretch induces epithelial-mesenchymal transition in alveolar epithelia via hyaluronan activation of innate immunity. J Biol Chem. 2011 May 20;286(20):17435-44.
5. Shanmugam P, Valente AJ, Prabhu SD, Venkatesan B, Yoshida T, Delafontaine P, et al. Angiotensin-II type 1 receptor and NOX2 mediate TCF/LEF and CREB dependent WISP1 induction and cardiomyocyte hypertrophy. J Mol Cell Cardiol. 2011 Jun;50(6):928-38.
6. Reddy VS, Valente AJ, Delafontaine P, Chandrasekar B. Interleukin-18/WNT1-inducible signaling pathway protein-1 signaling mediates human saphenous vein smooth muscle cell proliferation. J Cell Physiol. 2011 Dec;226(12):3303-15.
7. French DM, Kaul RJ, D'Souza AL, Crowley CW, Bao M, Frantz GD, et al. WISP-1 is an osteoblastic regulator expressed during skeletal development and fracture repair. Am J Pathol. 2004 Sep;165(3):855-67.
8. Macsai CE, Georgiou KR, Foster BK, Zannettino AC, Xian CJ. Microarray expression analysis of genes and pathways involved in growth plate cartilage injury responses and bony repair. Bone. 2012 May;50(5):1081-91.
9. Venkatesan B, Prabhu SD, Venkatachalam K, Mummidi S, Valente AJ, Clark RA, et al. WNT1-inducible signaling pathway protein-1 activates diverse cell survival pathways and blocks doxorubicininduced cardiomyocyte death. Cell Signal. 2010 May;22(5):809-20.
10. Shang YC, Chong ZZ, Wang S, Maiese K. WNT1 Inducible Signaling Pathway Protein 1 (WISP1) Targets PRAS40 to Govern beta-Amyloid Apoptotic Injury of Microglia. Curr Neurovasc Res. 2012 Aug 6;9(4):239-49.
11. Wang S, Chong ZZ, Shang YC, Maiese K. Wnt1 inducible signaling pathway protein 1 (WISP1) blocks neurodegeneration through phosphoinositide 3 kinase/Akt1 and apoptotic mitochondrial signaling involving Bad, Bax, Bim, and Bcl-xL. Curr Neurovasc Res. 2012 Feb;9(1):20-31.
12. Wang S, Chong ZZ, Shang YC, Maiese K. WISP1 (CCN4) autoregulates its expression and nuclear trafficking of beta-catenin during oxidant stress with limited effects upon neuronal autophagy. Curr Neurovasc Res. 2012 Apr 4;9(2):89-99.
13. Case N, Ma M, Sen B, Xie Z, Gross TS, Rubin J. Beta-catenin levels influence rapid mechanical responses in osteoblasts. J Biol Chem. 2008 Oct 24;283(43):29196-205.
14. Marchand A, Atassi F, Gaaya A, Leprince P, Le Feuvre C, Soubrier F, et al. The Wnt/beta-catenin pathway is activated during advanced arterial aging in humans. Aging Cell. 2011 Apr;10(2):220-32.
15. Bahia PK, Pugh V, Hoyland K, Hensley V, Rattray M, Williams RJ. Neuroprotective effects of phenolic antioxidant tBHQ associate with inhibition of FoxO3a nuclear translocation and activity. J Neurochem. 2012 Oct;123(1):182-91.
16. Chong ZZ, Hou J, Shang YC, Wang S, Maiese K. EPO Relies upon Novel Signaling of Wnt1 that Requires Akt1, FoxO3a, GSK-3beta, and beta-Catenin to Foster Vascular Integrity During Experimental Diabetes. Curr Neurovasc Res. 2011 May 1;8(2):103-20.
17. Chong ZZ, Maiese K. Erythropoietin involves the phosphatidylinositol 3-kinase pathway, 14-3-3 protein and FOXO3a nuclear trafficking to preserve endothelial cell integrity. Br J Pharmacol. 2007 Apr;150(7):839-50.
18. Lai CS, Tsai ML, Badmaev V, Jimenez M, Ho CT, Pan MH. Xanthigen suppresses preadipocyte differentiation and adipogenesis through down-regulation of PPARgamma and C/EBPs and modulation of SIRT-1, AMPK, and FoxO pathways. Journal of agricultural and food chemistry. 2012 Feb 1;60(4):1094-101.
19. Maiese K, Chong ZZ, Shang YC. OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med. 2008 May;14(5):219-27.
20. Maiese K, Chong ZZ, Shang YC, Hou J. A "FOXO" in sight: targeting Foxo proteins from conception to cancer. Med Res Rev. 2009 May;29(3):395-418.
21. Maiese K, Chong ZZ, Shang YC, Wang S. Erythropoietin: New Directions for the Nervous System. Int J Mol Sci. 2012;13:11102-29.
22. Wang X, Chen WR, Xing D. A pathway from JNK through decreased ERK and Akt activities for FOXO3a nuclear translocation in response to UV irradiation. J Cell Physiol. 2011 May 20.
23. Chong ZZ, Shang YC, Wang S, Maiese K. SIRT1: New avenues of discovery for disorders of oxidative stress. Expert opinion on therapeutic targets. 2012 Feb;16(2):167-78.
24. Maiese K, Chong ZZ, Shang YC, Wang S. Translating cell survival and cell longevity into treatment strategies with SIRT1. Rom J Morphol Embryol. 2011;52(4):1173-85.
25. Wang Y, Liang Y, Vanhoutte PM. SIRT1 and AMPK in regulating mammalian senescence: a critical review and a working model. FEBS Lett. 2011 Apr 6;585(7):986-94.
26. Frojdo S, Durand C, Molin L, Carey AL, El-Osta A, Kingwell BA, et al. Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1. Mol Cell Endocrinol. 2011 Mar 30;335(2):166-76.
27. Hou J, Chong ZZ, Shang YC, Maiese K. Early apoptotic vascular signaling is determined by Sirt1 through nuclear shuttling, forkhead trafficking, bad, and mitochondrial caspase activation. Curr Neurovasc Res. 2010 May;7(2):95-112.
28. Hou J, Wang S, Shang YC, Chong ZZ, Maiese K. Erythropoietin Employs Cell Longevity Pathways of SIRT1 to Foster Endothelial Vascular Integrity During Oxidant Stress. Curr Neurovasc Res. 2011 Aug 1;8(3):220-35.
29. Maiese K, Chong ZZ, Shang YC, Hou J. FoxO proteins: cunning concepts and considerations for the cardiovascular system. Clin Sci (Lond). 2009 Feb;116(3):191-203.
30. Maiese K, Hou J, Chong ZZ, Shang YC. A fork in the path: Developing therapeutic inroads with FoxO proteins. Oxid Med Cell Longev. 2009 Jul;2(3):119-29.
31. Storz P. Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal. 2011 Feb 15;14(4):593-605.
32. Hou J, Chong ZZ, Shang YC, Maiese K. FoxO3a governs early and late apoptotic endothelial programs during elevated glucose through mitochondrial and caspase signaling. Mol Cell Endocrinol. 2010 Mar 4;321(2):194-206.
33. Obexer P, Geiger K, Ambros PF, Meister B, Ausserlechner MJ. FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ. 2007 Mar;14(3):534-47.
34. Chong ZZ, Kang JQ, Maiese K. Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation ofmicroglia, Akt1, Bad, and caspase-mediated pathways. Br J Pharmacol. 2003 Mar;138(6):1107-18.
35. Chong ZZ, Shang YC, Hou J, Maiese K. Wnt1 neuroprotection translates into improved neurological function during oxidant stress and cerebral ischemia through AKT1 and mitochondrial apoptotic pathways. Oxid Med Cell Longev. 2010 Mar-Apr;3(2):153-65.
36. Shang YC, Chong ZZ, Hou J, Maiese K. FoxO3a governs early microglial proliferation and employs mitochondrial depolarization with caspase 3, 8, and 9 cleavage during oxidant induced apoptosis. Curr Neurovasc Res. 2009 Nov;6(4):223-38.
37. Chong ZZ, Kang JQ, Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation. 2002 Dec 3;106(23):2973-9.
38. Chong ZZ, Lin SH, Kang JQ, Maiese K. Erythropoietin prevents early and late neuronal demise through modulation of Akt1 and induction of caspase 1, 3, and 8. J Neurosci Res. 2003 Mar 1;71(5):659-69.
39. Kang JQ, Chong ZZ, Maiese K. Critical role for Akt1 in the modulation of apoptotic phosphatidylserine exposure and microglial activation. Mol Pharmacol. 2003 Sep;64(3):557-69.
40. Chong ZZ, Kang JQ, Maiese K. AKT1 drives endothelial cell membrane asymmetry and microglial activation through Bcl-xL and caspase 1, 3, and 9. Exp Cell Res. 2004 Jun 10;296(2):196-207.
41. Shang YC, Chong ZZ, Wang S, Maiese K. Erythropoietin and Wnt1 Govern Pathways of mTOR, Apaf-1, and XIAP in Inflammatory Microglia. Curr Neurovasc Res. 2011 Oct 19;8(4):270-85.
42. Shang YC, Chong ZZ, Wang S, Maiese K. Prevention of betaamyloid degeneration of microglia by erythropoietin depends on Wnt1, the PI 3-K/mTOR pathway, Bad, and Bcl-xL. Aging (Albany NY). 2012 Mar 3;4(3):187-201.
43. Wymann MP, Bulgarelli-Leva G, Zvelebil MJ, Pirola L, Vanhaesebroeck B, Waterfield MD, et al. Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol Cell Biol. 1996 Apr;16(4):1722-33.
44. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1- benzopyran-4-one (LY294002). J Biol Chem. 1994 Feb 18;269(7):5241-8.
45. Zhu W, Bijur GN, Styles NA, Li X. Regulation of FOXO3a by brain-derived neurotrophic factor in differentiated human SHSY5Y neuroblastoma cells. Brain Res Mol Brain Res. 2004 Jul 5;126(1):45-56.
46. Solomon JM, Pasupuleti R, Xu L, McDonagh T, Curtis R, DiStefano PS, et al. Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Mol Cell Biol. 2006 Jan;26(1):28-38.
47. Hennemeier I, Humpf HU, Gekle M, Schwerdt G. The food contaminant and nephrotoxin ochratoxin A enhances Wnt1 inducible signaling protein 1 and tumor necrosis factor-alpha expression in human primary proximal tubule cells. Molecular nutrition & food research. 2012 Sep;56(9):1375-84.
48. Venkatachalam K, Venkatesan B, Valente AJ, Melby PC, Nandish S, Reusch JE, et al. WISP1, a pro-mitogenic, pro-survival factor, mediates tumor necrosis factor-alpha (TNF-alpha)-stimulated cardiac fibroblast proliferation but inhibits TNF-alpha-induced cardiomyocyte death. J Biol Chem. 2009 May 22;284(21):14414- 27.
49. Price RM, Tulsyan N, Dermody JJ, Schwalb M, Soteropoulos P, Castronuovo JJ Jr. Gene expression after crush injury of human saphenous vein: using microarrays to define the transcriptional profile. J Am Coll Surg. 2004 Sep;199(3):411-8.
50. Konigshoff M, Kramer M, Balsara N, Wilhelm J, Amarie OV, Jahn A, et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest. 2009 Apr;119(4):772-87.
51. Kapasa M, Serafimidis I, Gavalas A, Kossida S. Identification of phylogenetically conserved enhancer elements implicated in pancreas development in the WISP1 and CTGF orthologs. Genomics. 2008 Nov;92(5):301-8.
52. Kohara H, Tabata Y. Enhancement of ectopic osteoid formation following the dual release of bone morphogenetic protein 2 and Wnt1 inducible signaling pathway protein 1 from gelatin sponges. Biomaterials. 2011 Aug;32(24):5726-32.
53. Davies SR, Davies ML, Sanders A, Parr C, Torkington J, Jiang WG. Differential expression of the CCN family member WISP-1, WISP-2 and WISP-3 in human colorectal cancer and the prognostic implications. Int J Oncol. 2010 May;36(5):1129-36.
54. Nagai Y, Watanabe M, Ishikawa S, Karashima R, Kurashige J, Iwagami S, et al. Clinical significance of Wnt-induced secreted protein-1 (WISP-1/CCN4) in esophageal squamous cell carcinoma. Anticancer Res. 2011 Mar;31(3):991-7.
55. Wang Q, Liu H, Liu T, Shu S, Jiang H, Cheng S, et al. BRCA2 Dysfunction Promotes Malignant Transformation of Pancreatic Intraepithelial Neoplasia. Anticancer Agents Med Chem. 2012 Aug 24.
56. Maiese K, Chong ZZ, Wang S, Shang YC. Oxidant Stress and Signal Transduction in the Nervous System with the PI 3-K, Akt, and mTOR Cascade. Int J Mol Sci. 2012;13(11):13830-66.
57. Mannell HK, Pircher J, Chaudhry DI, Alig SK, Koch EG, Mettler R, et al. ARNO regulates VEGF-dependent tissue responses by stabilizing endothelial VEGFR-2 surface expression. Cardiovasc Res. 2012 Jan 1;93(1):111-9.
58. Su KH, Shyue SK, Kou YR, Ching LC, Chiang AN, Yu YB, et al. beta Common receptor integrates the erythropoietin signaling in activation of endothelial nitric oxide synthase. J Cell Physiol. 2011 Dec;226(12):3330-9.
59. Pineda D, Ampurdanes C, Medina MG, Serratosa J, Tusell JM, Saura J, et al. Tissue plasminogen activator induces microglial inflammation via a noncatalytic molecular mechanism involving activation of mitogen-activated protein kinases and Akt signaling pathways and AnnexinA2 and Galectin-1 receptors. Glia. 2012 Apr;60(4):526-40.
60. Shang YC, Chong ZZ, Hou J, Maiese K. The forkhead transcription factor FoxO3a controls microglial inflammatory activation and eventual apoptotic injury through caspase 3. Curr Neurovasc Res. 2009 Feb;6(1):20-31.
61. Zhou X, Wang L, Wang M, Xu L, Yu L, Fang T, et al. Emodininduced microglial apoptosis is associated with TRB3 induction. Immunopharmacol Immunotoxicol. 2011 Dec;33(4):594-602.
62. Chong ZZ, Shang YC, Wang S, Maiese K. PRAS40 Is an Integral Regulatory Component of Erythropoietin mTOR Signaling and Cytoprotection. PLoS ONE. 2012;7(9):e45456.
63. Malagelada C, Jin ZH, Jackson-Lewis V, Przedborski S, Greene LA. Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci. 2010 Jan 20;30(3):1166-75.
64. Shen J, Wu Y, Xu JY, Zhang J, Sinclair SH, Yanoff M, et al. ERKand Akt-dependent neuroprotection by erythropoietin (EPO) against glyoxal-AGEs via modulation of Bcl-xL, Bax, and BAD. Invest Ophthalmol Vis Sci. 2010 Jan;51(1):35-46.
65. Zeng KW, Wang XM, Ko H, Kwon HC, Cha JW, Yang HO. Hyperoside protects primary rat cortical neurons from neurotoxicity induced by amyloid beta-protein via the PI3K/Akt/Bad/Bcl(XL)-regulated mitochondrial apoptotic pathway. Eur J Pharmacol. 2011 Dec 15;672(1-3):45-55.
66. Chong ZZ, Shang YC, Wang S, Maiese K. Shedding new light on neurodegenerative diseases through the mammalian target of rapamycin. Prog Neurobiol. 2012 Aug 15;99:128-48.
67. Simao F, Matte A, Matte C, Soares FM, Wyse AT, Netto CA, et al. Resveratrol prevents oxidative stress and inhibition of Na(+)K(+)- ATPase activity induced by transient global cerebral ischemia in rats. The Journal of nutritional biochemistry. 2011 Jan 3.
68. Balan V, Miller GS, Kaplun L, Balan K, Chong ZZ, Li F, et al. Life span extension and neuronal cell protection by Drosophila nicotinamidase. J Biol Chem. 2008 Oct 10;283(41):27810-9.
69. Chong ZZ, Maiese K. Enhanced Tolerance against Early and Late Apoptotic Oxidative Stress in Mammalian Neurons through Nicotinamidase and Sirtuin Mediated Pathways. Curr Neurovasc Res. 2008 Aug;5(3):159-70.
70. Maiese K, Chong ZZ, Shang YC, Wang S. Novel directions for diabetes mellitus drug discovery. Expert opinion on drug discovery. 2012 Oct 24;(in press).
71. Michan S, Li Y, Chou MM, Parrella E, Ge H, Long JM, et al. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci. 2010 Jul 21;30(29):9695-707.
72. Donmez G, Wang D, Cohen DE, Guarente L. SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell. 2010 Jul 23;142(2):320-32.
73. Sundaresan NR, Pillai VB, Wolfgeher D, Samant S, Vasudevan P, Parekh V, et al. The deacetylase SIRT1 promotes membrane localization and activation of Akt and PDK1 during tumorigenesis and cardiac hypertrophy. Science signaling. 2011;4(182):ra46.
74. Wang RH, Kim HS, Xiao C, Xu X, Gavrilova O, Deng CX. Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance. J Clin Invest. 2011 Nov;121(11):4477-90.
75. Wang F, Chan CH, Chen K, Guan X, Lin HK, Tong Q. Deacetylation of FOXO3 by SIRT1 or SIRT2 leads to Skp2- mediated FOXO3 ubiquitination and degradation. Oncogene. 2012 Mar 22;31(12):1546-57.
76. Oppenheimer H, Gabay O, Meir H, Haze A, Kandel L, Liebergall M, et al. 75-kd sirtuin 1 blocks tumor necrosis factor alphamediated apoptosis in human osteoarthritic chondrocytes. Arthritis Rheum. 2012 Mar;64(3):718-28.
77. Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, Shimohama S, et al. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci U S 2008 Oct 7;105(40):15599-604.
78. Tanno M, Kuno A, Yano T, Miura T, Hisahara S, Ishikawa S, et al. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem. 2010 Mar 12;285(11):8375-82.
79. Balaiya S, Ferguson LR, Chalam KV. Evaluation of sirtuin role in neuroprotection of retinal ganglion cells in hypoxia. Invest Ophthalmol Vis Sci. 2012;53(7):4315-22.
80. Kozako T, Aikawa A, Shoji T, Fujimoto T, Yoshimitsu M, Shirasawa S, et al. High expression of the longevity gene product SIRT1 and apoptosis induction by sirtinol in adult T-cell leukemia cells. Int J Cancer. 2012 Nov 1;131(9):2044-55.
81. Hong EH, Lee SJ, Kim JS, Lee KH, Um HD, Kim JH, et al. Ionizing radiation induces cellular senescence of articular chondrocytes via negative regulation of SIRT1 by p38 kinase. J Biol Chem. 2010 Jan 8;285(2):1283-95.
82. Gao Z, Zhang J, Kheterpal I, Kennedy N, Davis RJ, Ye J. Sirtuin 1 (SIRT1) protein degradation in response to persistent c-Jun Nterminal kinase 1 (JNK1) activation contributes to hepatic steatosis in obesity. J Biol Chem. 2011 Jun 24;286(25):22227-34.
83. Nemoto S, Fergusson MM, Finkel T. Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science. 2004 Dec 17;306(5704):2105-8.
84. Kelly KR, Nawrocki ST, Espitia CM, Zhang M, Yang JJ, Padmanabhan S, et al. Targeting Aurora A kinase activity with the investigational agent alisertib increases the efficacy of cytarabine through a FOXO-dependent mechanism. Int J Cancer. 2012 Dec 1;131(11):2693-703.