Essential role of mitogen-activated protein kinase pathways in protease activated receptor 2-mediated nitric-oxide production from rat primary astrocytes

Nitric Oxide - Biology and Chemistry

Volumn 21, Issue 2, 2009, Pages 110-119

  Park, Gyu Hwan ^a   Jeon, Se Jin ^a   Ryu, Jae Ryun ^a   Choi, Min Sik ^a   Han, Seol Heui ^d   Yang, Sung Il ^d   Ryu, Jong Hoon ^b   Cheong, Jae Hoon ^c   Shin, Chan Young ^d   Ko, Kwang Ho ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

^c Sahmyook University   (South Korea)

^d Department of Pharmacology   (South Korea)

Author keywords

Astrocytes; MAPKs; NF B; NO; PAR 2; Trypsin

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; NITRITE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEINASE ACTIVATED RECEPTOR 2; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRYPSIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DNA BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; TRANSCRIPTION INITIATION;

ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; CELL SURVIVAL; I-KAPPA B PROTEINS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PAR-2; TRYPSIN;

RATTUS;

EID: 68249151075     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2009.05.007     Document Type: Article

References (65)

1. Cervos-Navarro J., and Lafuente J.V. Traumatic brain injuries: structural changes. J. Neurol. Sci. 103 Suppl. (1991) S3-S14
2. Eng L.F., Yu A.C., and Lee Y.L. Astrocytic response to injury. Prog. Brain Res. 94 (1992) 353-365
3. Moumdjian R.A., Antel J.P., and Yong V.W. Origin of contralateral reactive gliosis in surgically injured rat cerebral cortex. Brain Res. 547 (1991) 223-228
4. Bernaudin M., Nouvelot A., MacKenzie E.T., and Petit E. Selective neuronal vulnerability and specific glial reactions in hippocampal and neocortical organotypic cultures submitted to ischemia. Exp. Neurol. 150 (1998) 30-39
5. Beach T.G., Walker R., and McGeer E.G. Patterns of gliosis in Alzheimer's disease and aging cerebrum. Glia 2 (1989) 420-436
6. Stoltzner S.E., Grenfell T.J., Mori C., Wisniewski K.E., Wisniewski T.M., Selkoe D.J., and Lemere C.A. Temporal accrual of complement proteins in amyloid plaques in Down's syndrome with Alzheimer's disease. Am. J. Pathol. 156 (2000) 489-499
7. Akiyama H., Arai T., Kondo H., Tanno E., Haga C., and Ikeda K. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis. Assoc. Disord. 14 Suppl. 1 (2000) S47-S53
8. Griffin W.S., Sheng J.G., Royston M.C., Gentleman S.M., McKenzie J.E., Graham D.I., Roberts G.W., and Mrak R.E. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol. 8 (1998) 65-72
9. Koprowski H., Zheng Y.M., Heber-Katz E., Fraser N., Rorke L., Fu Z.F., Hanlon C., and Dietzschold B. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc. Natl. Acad. Sci. USA 90 (1993) 3024-3027
10. Nomura Y. NF-kappaB activation and IkappaB alpha dynamism involved in iNOS and chemokine induction in astroglial cells. Life Sci. 68 (2001) 1695-1701
11. Hua L.L., Zhao M.L., Cosenza M., Kim M.O., Huang H., Tanowitz H.B., Brosnan C.F., and Lee S.C. Role of mitogen-activated protein kinases in inducible nitric oxide synthase and TNFalpha expression in human fetal astrocytes. J. Neuroimmunol. 126 (2002) 180-189
12. Bhat N.R., Zhang P., Lee J.C., and Hogan E.L. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J. Neurosci. 18 (1998) 1633-1641
13. Katsuki H., Okawara M., Shibata H., Kume T., and Akaike A. Nitric oxide-producing microglia mediate thrombin-induced degeneration of dopaminergic neurons in rat midbrain slice culture. J. Neurochem. 97 (2006) 1232-1242
14. Pyo H., Joe E., Jung S., Lee S.H., and Jou I. Gangliosides activate cultured rat brain microglia. J. Biol. Chem. 274 (1999) 34584-34589
15. Doi M., Shichiri M., Katsuyama K., Marumo F., and Hirata Y. Cytokine-activated p42/p44 MAP kinase is involved in inducible nitric oxide synthase gene expression independent from NF-kappaB activation in vascular smooth muscle cells. Hypertens. Res. 23 (2000) 659-667
16. Choi S.H., Lee D.Y., Kim S.U., and Jin B.K. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J. Neurosci. 25 (2005) 4082-4090
17. Park G.H., Ryu J.R., Shin C.Y., Choi M.S., Han B.H., Kim W.K., Kim H.C., and Ko K.H. Evidence that protease-activated receptor-2 mediates trypsin-induced reversal of stellation in cultured rat astrocytes. Neurosci. Res. 54 (2006) 15-23
18. Sheehan J.J., and Tsirka S.E. Fibrin-modifying serine proteases thrombin, tPA, and plasmin in ischemic stroke: a review. Glia 50 (2005) 340-350
19. Rohatgi T., Sedehizade F., Reymann K.G., and Reiser G. Protease-activated receptors in neuronal development, neurodegeneration, and neuroprotection: thrombin as signaling molecule in the brain. Euroscientist 10 (2004) 501-512
20. Macfarlane S.R., Seatter M.J., Kanke T., Hunter G.D., and Plevin R. Proteinase-activated receptors. Pharmacol. Rev. 53 (2001) 245-282
21. Wang H., Ubl J.J., and Reiser G. Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 37 (2002) 53-63
22. Vergnolle N., Ferazzini M., D'Andrea M.R., Buddenkotte J., and Steinhoff M. Proteinase-activated receptors: novel signals for peripheral nerves. Trends Neurosci. 26 (2003) 496-500
23. Suo Z., Wu M., Ameenuddin S., Anderson H.E., Zoloty J.E., Citron B.A., Andrade-Gordon P., and Festoff B.W. Participation of protease-activated receptor-1 in thrombin-induced microglial activation. J. Neurochem. 80 (2000) 655-666
24. Nicole O., Goldshmidt A., Hamill C.E., Sorensen S.D., Sastre A., Lyuboslavsky P., Hepler J.R., McKeon R.J., and Traynelis S.F. Activation of protease-activated receptor-1 triggers astrogliosis after brain injury. J. Neurosci. 25 (2005) 4319-4329
25. Nagai T., Ito M., Nakamichi N., Mizoguchi H., Kamei H., Fukakusa A., Nabeshima T., Takuma K., and Yamada K. The rewards of nicotine: regulation by tissue plasminogen activator-plasmin system through protease activated receptor-1. J. Neurosci. 26 (2006) 12374-12383
26. Smith-Swintosky V.L., Cheo-Isaacs C.T., D'Andrea M.R., Santulli R.J., Darrow A.L., and Andrade-Gordon P. Protease-activated receptor-2 (PAR-2) is present in the rat hippocampus and is associated with neurodegeneration. J. Neurochem. 69 (1997) 1890-1896
27. Steinhoff M., Vergnolle N., Young S.H., Tognetto M., Amadesi S., Ennes H.S., Trevisani M., Hollenberg M.D., Wallace J.L., Caughey G.H., Mitchell S.E., Williams L.M., Geppetti P., Mayer E.A., and Bunnett N.W. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6 (2000) 151-158
28. Wang Y., Luo W., and Reiser G. Trypsin and trypsin-like proteases in the bra proteolysis and cellular functions. Cell. Mol. Life Sci. 65 (2008) 237-252
29. Vergnolle N. Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo. J. Immunol. 163 (1999) 5064-5069
30. Sobey C.G., Moffatt J.D., and Cocks T.M. Evidence for selective effects of chronic hypertension on cerebral artery vasodilatation to protease-activated receptor-2 activation. Stroke 30 (1999) 1933-1940
31. Hou M., Carneskog J., Mellqvis U.H., Stockelberg D., Hedberg M., Wadenvik H., and Kutti J. Impact of endogenous thrombopoietin levels on the differential diagnosis of essential thrombocythaemia and reactive thrombocytosis. Eur. J. Haematol. 61 (1998) 119-122
32. Kim M.S., Jo H., Um J.Y., Yi J.M., Kim D.K., Choi S.C., Kim T.H., Nah Y.H., Kim H.M., and Lee Y.M. Agonists of proteinase-activated receptor 2 induce TNF-alpha secretion from astrocytoma cells. Cell Biochem. Funct. 20 (2002) 339-345
33. Pyo H., Jou I., Jung S., Hong S., and Joe E.H. Mitogen-activated protein kinases activated by lipopolysaccharide and beta-amyloid in cultured rat microglia. Neuroreport 9 (1998) 871-874
34. Xie Q.W., Kashiwabara Y., and Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269 (1994) 4705-4758
35. Lee H., Kim Y.O., Kim H., Kim S.Y., Noh H.S., Kang S.S., Cho G.J., Choi W.S., and Suk K. Flavonoid wogonin from medicinal herb is neuroprotective by inhibiting inflammatory activation of microglia. FASEB J. 17 (2003) 1943-1944
36. Murphy S. Production of nitric oxide by glial cells: regulation and potential roles in the CNS. Glia 29 (2000) 1-13
37. Shin C.Y., Choi J.W., Ryu J.R., Ryu J.H., Kim W., Kim H., and Ko K.H. Immunostimulation of rat primary astrocytes decreases intracellular ATP level. Brain Res. 902 (2001) 198-204
38. Bolanos J.P., Heales S.J., Land J.M., and Clark J.B. Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary culture. J. Neurochem. 64 (1995) 1965-1972
39. Stewart V.C., Sharpe M.A., Clark J.B., and Heales S.J. Astrocyte-derived nitric oxide causes both reversible and irreversible damage to the neuronal mitochondrial respiratory chain. J. Neurochem. 75 (2000) 694-700
40. Heales S.J., Bolanos J.P., Stewart V.C., Brookes P.S., Land J.M., and Clark J.B. Nitric oxide, mitochondria and neurological disease. Biochim. Biophys. Acta 1410 (1999) 215-228
41. Murphy M.P. Nitric oxide and cell death. Biochim. Biophys. Acta 1411 (1999) 401-414
42. Bolanos J.P., Peuchen S., Heales S.J., Land J.M., and Clark J.B. Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J. Neurochem. 63 (1994) 910-916
43. Bolanos J.P., Heales S.J., Peuchen S., Barker J.E., Land J.M., and Clark J.B. Nitric oxide-mediated mitochondrial damage: a potential neuroprotective role for glutathione. Free Radic. Biol. Med. 21 (1996) 995-1001
44. Stewart V.C., Land J.M., Clark J.B., and Heales S.J. Pretreatment of astrocytes with interferon-alpha/beta prevents neuronal mitochondrial respiratory chain damage. J. Neurochem. 70 (1998) 432-434
45. Brown G.C. Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta 1411 (1999) 351-369
46. Viner R.I., Williams T.D., and Schoneich C. Peroxynitrite modification of protein thiols: oxidation, nitrosylation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38 (1999) 12408-12415
47. Brown G.C., and Borutaite V. Nitric oxide, mitochondria, and cell death. IUBMB Life 52 (2001) 189-195
48. Bosca L., and Hortelano S. Mechanisms of nitric oxide-dependent apoptosis: involvement of mitochondrial mediators. Cell. Signal. 11 (1999) 239-244
49. Ju Z., Fan L., and Lu L. Study on normal pregnancy and recurrent spontaneous abortions from helper T cell 1/helper T cell 2 cytokines balance. Zhonghua Fu Chan Ke Za Zhi 35 (2000) 473-475
50. Trotti D., Rossi D., Gjesdal O., Levy L.M., Racagni G., Danbolt N.C., and Volterra A. Peroxynitrite inhibits glutamate transporter subtypes. J. Biol. Chem. 271 (1996) 5976-5979
51. Choi B.H., Kim R.C., Vaughan P.J., Lau A., Van-Nostrand W.A., Cotman C.W., and Cunningham D.D. Decreases in protease nexins in Alzheimer's disease brain. Neurobiol. Aging 16 (1995) 557-562
52. Boven L.A., Vergnolle N., Henry S.D., Silva C., Imai Y., Holden J., Warren K., Hollenberg M.D., and Power C. Up-regulation of proteinase-activated receptor 1 expression in astrocytes during HIV encephalitis. J. Immunol. 170 (2003) 2638-2646
53. Noorbakhsh F., Vergnolle N., McArthur J.C., Silva C., Vodjgani M., Andrade-Gordon P., Hollenberg M.D., and Power C. Proteinase-activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J. Immunol. 174 (2005) 7320-7329
54. Jin G., Hayashi T., Kawagoe J., Takizawa T., Nagata T., Nagano I., Syoji M., and Abe K. Deficiency of PAR-2 gene increases acute focal ischemic brain injury. J. Cereb. Blood Flow Metab. 25 (2005) 302-313
55. Hoogerwerf W.A., Shenoy M., Winston J.H., Xiao S.Y., He Z., and Pasricha P.J. Trypsin mediates nociception via the proteinase-activated receptor 2: a potentially novel role in pancreatic pain. Gastroenterology 127 (2004) 883-891
56. 2+]i-inducing protease-activated receptors (PAR-1 and PAR-2) in rat astrocytes and C6 glioma cells. Neuroscience 86 (1998) 597-609
57. Vergnolle N., Bunnett N.W., Sharkey K.A., Brussee V., Compton S.J., Grady E.F., Cirino G., Gerard N., Basbaum A.I., Andrade-Gordon P., Hollenberg M.D., and Wallace J.L. Proteinase-activated receptor 2 and hyperalgesia a novel pain pathway. Nat. Med. 7 (2001) 821-826
58. Vergnolle N., Wallace J.L., Bunnett N.W., and Hollenberg M.D. Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol. Sci. 22 (2001) 146-152
59. Meli R., Raso G.M., Cicala C., Esposito E., Fiorino F., and Cirino G. Thrombin and PAR-1 activating peptide increase iNOS expression in cytokine-stimulated C6 glioma cells. J. Neurochem. 79 (2001) 556-563
60. Kang K.W., Choi S.Y., Cho M.K., Lee C.H., and Kim S.G. Thrombin induces nitric-oxide synthase via Galpha12/13-coupled protein kinase C-dependent I-kappaBalpha phosphorylation and JNK-mediated I-kappaBalpha degradation. J. Biol. Chem. 278 (2003) 17368-17378
61. Lee W.J., Shin C.Y., Yoo B.K., Ryu J.R., Choi E.Y., Cheong J.H., Ryu J.H., and Ko K.H. Induction of matrix metalloproteinase-9 (MMP-9) in lipopolysaccharide-stimulated primary astrocytes is mediated by extracellular signal-regulated protein kinase 1/2 (Erk1/2). Glia 41 (2003) 15-24
62. Bonaiuto C., McDonald P.P., Rossi F., and Cassatella M.A. Activation of nuclear factor-kappa B by beta-amyloid peptides and interferon-gamma in murine microglia. J. Neuroimmunol. 77 (1997) 51-56
63. Bushell T.J., Plevin R., Cobb S., and Irving A.J. Characterization of proteinase-activated receptor 2 signalling and expression in rat hippocampal neurons and astrocytes. Neuropharmacology 50 (2006) 714-725
64. Lochner J.E., Honigman L.S., Grant W.F., Gessford S.K., Hansen A.B., Silverman M.A., and Scalettar B.A. Activity-dependent release of tissue plasminogen activator from the dendritic spines of hippocampal neurons revealed by live-cell imaging. J. Neurobiol. 66 (2006) 564-577
65. Kunz A., Park L., Abe T., Gallo E.F., Anrather J., Zhou P., and Iadecola C. Neurovascular protection by ischemic tolerance: role of nitric oxide and reactive oxygen species. J. Neurosci. 27 (2007) 7083-7093