S-nitrosylated SHP-2 contributes to NMDA receptormediated excitotoxicity in acute ischemic stroke

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 8, 2013, Pages 3137-3142

  Shi, Zhong Qing ^a   Sunico, Carmen R ^a   McKercher, Scott R ^a   Cui, Jiankun ^a   Feng, Gen Sheng ^b   Nakamura, Tomohiro ^a   Lipton, Stuart A ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Nitrosative stress; Reactive nitrogen species; Reactive oxygen species

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXCITOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; MICE; NEURONS; NITRIC OXIDE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RECEPTORS, N-METHYL-D-ASPARTATE; STROKE;

EID: 84874276438     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215501110     Document Type: Article

References (48)

1. Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347 (6295):768-770.
2. Huang Z, et al. (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265 (5180):1883-1885.
3. Nakamura T, Lipton SA (2007) S-Nitrosylation and uncompetitive/fast off-rate (UFO) drug therapy in neurodegenerative disorders of protein misfolding. Cell Death Differ 14 (7):1305-1314.
4. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: Purview and parameters. Nat Rev Mol Cell Biol 6 (2):150-166.
5. Lipton SA, et al. (1993) A redox-based mechanism for the neuroprotective and neu-rodestructive effects of nitric oxide and related nitroso-compounds. Nature 364 (6438):626-632.
6. Cho DH, et al. (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mito-chondrial fission and neuronal injury. Science 324 (5923):102-105.
7. Chung KK, et al. (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304 (5675):1328-1331.
8. Hara MR, et al. (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7 (7):665-674.
9. Qu J, et al. (2011) S-Nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by β-amyloid peptide. Proc Natl Acad Sci USA 108 (34):14330-14335.
10. Uehara T, et al. (2006) S-nitrosylated protein-disulphide isomerase links protein mis-folding to neurodegeneration. Nature 441 (7092):513-517.
11. Yao D, et al. (2004) Nitrosative stress linked to sporadic Parkinson's disease: S-nitro-sylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 101 (29):10810-10814.
12. Zhang ZY (2002) Protein tyrosine phosphatases: Structure and function, substrate specificity, and inhibitor development. Annu Rev Pharmacol Toxicol 42:209-234.
13. Qu CK (2002) Role of the SHP-2 tyrosine phosphatase in cytokine-induced signaling and cellular response. Biochim Biophys Acta 1592 (3):297-301.
14. Ke Y, et al. (2007) Deletion of Shp2 in the brain leads to defective proliferation and differentiation in neural stem cells and early postnatal lethality. Mol Cell Biol 27 (19):6706-6717.
15. Shi ZQ, Yu DH, Park M, Marshall M, Feng GS (2000) Molecular mechanism for the Shp-2 tyrosine phosphatase function in promoting growth factor stimulation of Erk activity. Mol Cell Biol 20 (5):1526-1536.
16. Zhang SQ, et al. (2004) Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 13 (3):341-355.
17. Chan RJ, Feng GS (2007) PTPN11 is the first identified proto-oncogene that encodes a tyrosine phosphatase. Blood 109 (3):862-867.
18. Zhang SS, et al. (2009) Coordinated regulation by Shp2 tyrosine phosphatase of signaling events controlling insulin biosynthesis in pancreatic beta-cells. Proc Natl Acad Sci USA 106 (18):7531-7536.
19. Jarvis LA, Toering SJ, Simon MA, Krasnow MA, Smith-Bolton RK (2006) Sprouty proteins are in vivo targets of Corkscrew/SHP-2 tyrosine phosphatases. Development 133 (6):1133-1142.
20. Agazie YM, Hayman MJ (2003) Molecular mechanism for a role of SHP2 in epidermal growth factor receptor signaling. Mol Cell Biol 23 (21):7875-7886.
21. Mehta SL, Manhas N, Raghubir R (2007) Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res Brain Res Rev 54 (1):34-66.
22. Nozaki K, Nishimura M, Hashimoto N (2001) Mitogen-activated protein kinases and cerebral ischemia. Mol Neurobiol 23 (1):1-19.
23. Szatmari E, Kalita KB, Kharebava G, Hetman M (2007) Role of kinase suppressor of Ras-1 in neuronal survival signaling by extracellular signal-regulated kinase 1/2. J Neurosci 27 (42):11389-11400.
24. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270 (5240):1326-1331.
25. Frödin M, Gammeltoft S (1999) Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol 151 (1-2):65-77.
26. Wang Y, Liu L, Xia Z (2007) Brain-derived neurotrophic factor stimulates the tran-scriptional and neuroprotective activity of myocyte-enhancer factor 2C through an ERK1/2-RSK2 signaling cascade. J Neurochem 102 (3):957-966.
27. Yan L, et al. (2007) Type 5 adenylyl cyclase disruption increases longevity and protects against stress. Cell 130 (2):247-258.
28. Tonks NK (2006) Protein tyrosine phosphatases: From genes, to function, to disease. Nat Rev Mol Cell Biol 7 (11):833-846.
29. Barrett DM, et al. (2005) Inhibition of protein-tyrosine phosphatases by mild oxidative stresses is dependent on S-nitrosylation. J Biol Chem 280 (15):14453-14461.
30. Mikkelsen RB, Wardman P (2003) Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22 (37):5734-5754.
31. Hsu MF, Meng TC (2010) Enhancement of insulin responsiveness by nitric oxide-mediated inactivation of protein-tyrosine phosphatases. J Biol Chem 285 (11):7919-7928.
32. Lu W, Gong D, Bar-Sagi D, Cole PA (2001) Site-specific incorporation of a phospho-tyrosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol Cell 8 (4):759-769.
33. Aoki Y, et al. (2000) Increased susceptibility to ischemia-induced brain damage in transgenic mice overexpressing a dominant negative form of SHP2. FASEB J 14 (13):1965-1973.
34. Jakob S, et al. (2008) Nuclear protein tyrosine phosphatase Shp-2 is one important negative regulator of nuclear export of telomerase reverse transcriptase. J Biol Chem 283 (48):33155-33161.
35. Schaeffer HJ, Weber MJ (1999) Mitogen-activated protein kinases: Specific messages from ubiquitous messengers. Mol Cell Biol 19 (4):2435-2444.
36. Forrester MT, Foster MW, Stamler JS (2007) Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J Biol Chem 282 (19):13977-13983.
37. Gu Z, et al. (2002) S-nitrosylation of matrix metalloproteinases: Signaling pathway to neuronal cell death. Science 297 (5584):1186-1190.
38. Chu CT, Levinthal DJ, Kulich SM, Chalovich EM, DeFranco DB (2004) Oxidative neu-ronal injury. The dark side of ERK1/2. Eur J Biochem 271 (11):2060-2066.
39. Hetman M, Gozdz A (2004) Role of extracellular signal regulated kinases 1 and 2 in neuronal survival. Eur J Biochem 271 (11):2050-2055.
40. Luo Y, DeFranco DB (2006) Opposing roles for ERK1/2 in neuronal oxidative toxicity: Distinct mechanisms of ERK1/2 action at early versus late phases of oxidative stress. J Biol Chem 281 (24):16436-16442.
41. Rusanescu G, Yang W, Bai A, Neel BG, Feig LA (2005) Tyrosine phosphatase SHP-2 is a mediator of activity-dependent neuronal excitotoxicity. EMBO J 24 (2):305-314.
42. Stanciu M, et al. (2000) Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J Biol Chem 275 (16):12200-12206.
43. Basso M, et al. (2012) Transglutaminase inhibition protects against oxidative stress-induced neuronal death downstream of pathological ERK activation. J Neurosci 32 (19):6561-6569.
44. Yun HY, Gonzalez-Zulueta M, Dawson VL, Dawson TM (1998) Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras. Proc Natl Acad Sci USA 95 (10):5773-5778.
45. Wink DA, et al. (1999) Detection of S-nitrosothiols by fluorometric and colorimetric methods. Methods Enzymol 301:201-211.
46. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-ni-trosylation: A physiological signal for neuronal nitric oxide. Nat Cell Biol 3 (2):193-197.
47. Kermer P, et al. (2003) BAG1 over-expression in brain protects against stroke. Brain Pathol 13 (4):495-506.
48. Qu CK, et al. (1997) A deletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development. Mol Cell Biol 17 (9):5499-5507.