Tetramethylpyrazine reduces cellular inflammatory response following permanent focal cerebral ischemia in rats

Experimental Neurology

Volumn 247, Issue , 2013, Pages 188-201

  Kao, Tsung Kuei ^a,b   Chang, Cheng Yi ^c   Ou, Yen Chuan ^d   Chen, Wen Ying ^e   Kuan, Yu Hsiang ^f   Pan, Hung Chuan ^d   Liao, Su Lan ^d   Li, Guo Zhang ^a   Chen, Chun Jung ^d,e,g,h  

^a BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^b TAJEN INSTITUTE OF TECHNOLOGY   (Taiwan)

^c FENG YUAN HOSPITAL   (Taiwan)

^d TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^e NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^f CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^g TUNGHAI UNIVERSITY   (Taiwan)

^h HUNGKUANG UNIVERSITY   (Taiwan)

Author keywords

Leukocyte; Neuroinflammation; Stroke; Tetramethylpyrazine

Indexed keywords

CYTOKINE; HEME OXYGENASE 1; TETRAMETHYLPYRAZINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BEHAVIOR DISORDER; BIOCHEMICAL COMPOSITION; BRAIN EDEMA; BRAIN INFARCTION; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; IMMUNE DEFICIENCY; LYMPHOCYTE MIGRATION; MACROPHAGE; MACROPHAGE ACTIVATION; MICROGLIA; NERVE CELL LESION; NERVE CELL STIMULATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

LEUKOCYTE; NEUROINFLAMMATION; STROKE; TETRAMETHYLPYRAZINE;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD45; ANTIGENS, LY; BRAIN EDEMA; BRAIN ISCHEMIA; CEREBRAL INFARCTION; ENCEPHALITIS; FIBRINOLYTIC AGENTS; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; HEME OXYGENASE (DECYCLIZING); MALE; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; NF-E2-RELATED FACTOR 2; PYRAZINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84878857984     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.04.010     Document Type: Article

References (69)

1. Balogun E., Hoque M., Gong P., Killeen E., Green C.J., Foresti R., Alam J., Motterlini R. Curcumin activates the heme oxygenase-1 gene via regulation of Nrf2 and the antioxidant responsive element. Biochem. J. 2003, 371:887-895.
2. Chang Y., Hsiao G., Chen S., Chen Y., Lin J., Lin K., Chou D., Sheu J. Tetramethylpyrazine suppresses HIF-1α, TNF-α, and activated caspase-3 expression in middle cerebral artery occlusion-induced brain ischemia in rats. Acta Pharmacol. Sin. 2007, 28:327-333.
3. Chen S.Y., Hsiao G., Hwang H.R., Cheng P.Y., Lee Y.M. Tetramethylpyrazine induces heme oxygenase-1 expression and attenuates myocardial ischemia/reperfusion injury in rats. J. Biomed. Sci. 2006, 13:731-740.
4. Clausen B.H., Lambersten K.L., Babcock A.A., Holm T.H., Dagnaes-Hansen F., Finsen B. Interleukin-1beta and tumor necrosis factor-alpha are expressed by different subsets of microglia and macrophages after ischemic stroke in mice. J. Neuroinflammation 2008, 5:46.
5. Connolly E.S., Winfree C.J., Springer T.A., Naka Y., Liao Y., Yan S.D., Stern D.M., Solomon R.A., Gutierrez-Ramos J.C., Pinsky D.J. Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion: role of neutrophil adhesion in the pathogenesis of stroke. J. Clin. Invest. 1996, 97:209-216.
6. Dai X.Z., Bache R.J. Coronary and systemic haemodynamic effect of tetramethylpyrazine in the dog. J. Cardiovasc. Pharmacol. 1985, 7:841-849.
7. Fan L., Wang K., Cheng B., Wang C., Dang X. Anti-apoptotic and neuroprotective effects of tetramethylpyrazine following spinal cord ischemia in rabbits. BMC Neurosci. 2006, 7:48.
8. Fan L., Wang K., Shi Z., Die J., Wang C., Dang X. Tetramethylpyrazine protects spinal cord and reduces inflammation in a rat model of spinal cord ischemia-reperfusion injury. J. Vasc. Surg. 2011, 54:192-200.
9. Feng M.G., Feng G.H., Zhou Q.G. Effects of methylhesperidin on coronary, renal and cerebral circulation in dogs (original in Chinese). Acta Pharmacol. Sin. 1988, 9:548-550.
10. Feng L., Ke N., Cheng F., Guo Y., Li S., Li Q., Li Y. The protective mechanism of ligustrazine against renal ischemia/reperfusion injury. J. Surg. Res. 2011, 166:298-305.
11. Garcia J.H., Liu K.F., Yoshida Y., Lian J., Chen S., del Zoppo G.J. Influx of leukocytes and platelets in an evolving brain infarct (Wistar rat). Am. J. Pathol. 1994, 144:188-199.
12. Gelderblom M., Leypoldt F., Steinbach K., Behrens D., Choe C.U., Siler D.A., Arumugam T.V., Orthey E., Gerloff C., Tolosa E., Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009, 40:1849-1857.
13. Gelderblom M., Leypoldt F., Lewerenz J., Birkenmayer G., Orozco D., Ludewig P., Thundyil J., Arumugam T.V., Gerloff C., Tolosa E., Maher P., Magnus T. The flavonoid fisetin attenuates postischemic immune cell infiltration, activation and infarct size after transient cerebral middle cerebral artery occlusion in mice. J. Cereb. Blood Flow Metab. 2012, 32:835-843.
14. Ho W.K., Wen H.L., Lee C.M. Tetramethylpyrazine for treatment of experimentally induced stroke in Mongolian gerbils. Stroke 1989, 20:96-99.
15. Hurn P.D., Subramanian S., Parker S.M., Afentoulis M.E., Kaler L.J., Vandenbark A.A., Offner H. T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. J. Cereb. Blood Flow Metab. 2007, 27:1798-1805.
16. Ichihara S., Yamada Y., Liu F., Murohara T., Itoh K., Yamamoto M., Ichihara G. Ablation of the transcription factor Nrf2 promotes ischemia-induced neovascularization by enhancing the inflammatory response. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1553-1561.
17. Innamorato N.C., Rojo A.I., Garcia-Yague A.J., Yamamoto M., de Ceballos M.L., Cuadrado A. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol. 2008, 181:680-689.
18. Jeong G.S., Lee D.S., Kim D.C., Jahng Y., Son J.K., Lee S.H., Kim Y.C. Neuroprotective and anti-inflammatory effects of mollugin via up-regulation of heme oxygenase-1 in mouse hippocampal and microglial cells. Eur. J. Pharmacol. 2011, 654:226-234.
19. Jia J., Zhang X., Hu Y.S., Wu Y., Wang Q.Z., Li N.N., Wu C.Q., Yu H.X., Guo Q.C. Protective effect of tetramethylpyrazine against focal cerebral ischemia/reperfusion injury in rats: therapeutic time window and its mechanism. Thromb. Res. 2009, 123:727-730.
20. Jin R., Yang G., Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol. 2010, 87:779-789.
21. Johnson J., Johnson D., Kraft A., Calkins M., Jakel R., Vargas M., Chen P. The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 2008, 1147:61-69.
22. Kao T.K., Ou Y.C., Kuo J.S., Chen W.Y., Liao S.L., Wu C.W., Chen C.J., Ling N.N., Zhang Y.H., Peng W.H. Neuroprotection by tetramethylpyrazine against ischemic brain injury in rats. Neurochem. Int. 2006, 48:166-176.
23. Kao T.K., Ou Y.C., Raung S.L., Chen W.Y., Yen Y.J., Lai C.Y., Chou S.T., Chen C.J. Graptopetalum paraguayense E. Walther leaf extracts protect against brain injury in ischemic rats. Am. J. Chin. Med. 2010, 38:495-516.
24. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19:312-318.
25. Lee M.Y., Kuan Y.H., Chen H.Y., Chen T.Y., Chen S.T., Huang C.C., Yang I.P., Hsu Y.S., Wu T.S., Lee E.J. Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J. Pineal Res. 2007, 42:297-309.
26. Lee I.S., Lim J., Gal J., Kang J.C., Kim H.J., Kang B.Y., Choi H.J. Anti-inflammatory activity of xanthohumol involves heme oxygenase-1 induction via NRF2-ARE signaling in microglial BV2 cells. Neurochem. Int. 2011, 58:153-160.
27. Lee I.S., Ryu D.K., Lim J., Cho S., Kang B.Y., Choi H.J. Artesunate activates Nrf2 pathway-driven anti-inflammatory potential through ERK signaling in microglial BV2 cells. Neurosci. Lett. 2012, 509:17-21.
28. Leonard M.O., Kieran N.E., Howell K., Burne M.J., Varadarajan R., Dhakshinamoorthy S., Porter A.G., O'Farrelly C., Rabb H., Taylor C.T. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J. 2006, 20:E2166-E2176.
29. Li X.Y., He J.L., Liu H.T., Li W.M., Yu C. Tetramethylpyrazine suppresses interleukin-8 expression in LPS-stimulated human umbilical vein endothelial cells by blocking ERK, p38 and nuclear factor-κB signaling pathways. J. Ethnopharmacol. 2009, 125:83-89.
30. Li M., Zhang X., Cui L., Yang R., Wang L., Liu L., Du W. The neuroprotection of oxymatrine in cerebral ischemia/reperfusion is related to nuclear factor erythroid 2-related factor 2 (Nrf2)-mediated antioxidant response: role of Nrf2 and hemeoxygenase-1 expression. Biol. Pharm. Bull. 2011, 34:595-601.
31. Li M., Qu Y.Z., Zhao Z.W., Wu S.X., Liu Y.Y., Wei X.Y., Gao L., Gao G.D. Astragaloside IV protects against focal cerebral ischemia/reperfusion injury correlating to suppression of neutrophils adhesion-related molecules. Neurochem. Int. 2012, 60:458-465.
32. Li Y., He D., Zhang X., Liu Z., Zhang X., Dong L., Xing Y., Wang C., Qiao H., Zhu C., Chen Y. Protective effect of celastrol in a rat cerebral ischemia model: down-regulating p-JNK, p-c-Jun and NF-κB. Brain Res. 2012, 1464:8-13.
33. Liao S.L., Kao T.K., Chen W.Y., Lin Y.S., Chen S.Y., Raung S.L., Wu C.W., Lu H.C., Chen C.J. Tetramethylpyrazine reduces ischemic brain injury in rats. Neurosci. Lett. 2004, 372:40-45.
34. Liu H.T., Du Y.G., He J.L., Chen W.J., Li W.M., Yang Z., Wang Y.X., Yu C. Tetramethylpyrazine inhibits production of nitric oxide and inducible nitric oxide synthase in lipopolysaccharide-induced N9 microglial cells through blockade of MAPK and PI3K/Akt signaling pathways, and suppression of intracellular reactive oxygen species. J. Ethnopharmacol. 2010, 129:335-343.
35. Liu Y., Wang H., Zhu Y., Chen L., Qu Y., Zhu Y. The protective effect of nordihydroguaiaretic acid on cerebral ischemia/reperfusion injury is mediated by the JNK pathway. Brain Res. 2012, 1445:73-81.
36. Longa E.Z., Weinstein P.R., Carlson S., Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-89.
37. Lu C.S., Yin M.H., Huang Y.H., Pao C., Sung C.F. Radix salviae miltiorrhizae and Rhizoma ligustici wallichii in coronary heart disease. Chin. Med. J. 1978, 4:43-46.
38. Moreira T.J.T.P., Cebere A., Cebers G., Ostenson C.G., Efendic S., Liljequist S. Reduced HO-1 protein expression is associated with more severe neurodegeneration after transient ischemia induced by cortical compression in diabetic Goto-Kakizaki rats. J. Cereb. Blood Flow Metab. 2007, 27:1710-1723.
39. Moxon-Emre L., Schlichter L.C. Evolution of inflammation and white matter injury in a model of transient focal ischemia. J. Neuropathol. Exp. Neurol. 2010, 69:1-15.
40. Murata Y., Fujiwara N., Seo J.H., Yan F., Liu X., Terasaki Y., Luo Y., Arai K., Ji X., Lo E.H. Delayed inhibition of c-Jun N-terminal kinase worsens outcomes after focal cerebral ischemia. J. Neurosci. 2012, 32:8112-8115.
41. Nijboer C.H., van der Kooij M.A., van Bel F., Ohl F., Heijnen C.J., Kavelaars A. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic-ischemic brain injury. Brain Behav. Immunol. 2010, 24:812-821.
42. Pan H.C., Kao T.K., Ou Y.C., Yang D.Y., Yen Y.J., Wang C.C., Chuang Y.H., Liao S.L., Raung S.L., Wu C.W., Chiang A.N., Chen C.J. Protective effect of docosahexaenoic acid against brain injury in ischemic rats. J. Nutr. Biochem. 2009, 28:715-725.
43. Pan H.C., Yang D.Y., Ou Y.C., Ho S.P., Cheng F.C., Chen C.J. Neuroprotective effect of atorvastatin in an experimental model of nerve crush injury. Neurosurgery 2010, 67:376-389.
44. Panahian N., Yoshiura M., Maines M.D. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 1999, 72:1187-1203.
45. Ping Z., Liu W., Kang Z., Gai J., Wang Q., Cheng N., Wang S., Wang S., Zhang J.H., Sun X. Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res. 2010, 1343:178-185.
46. Poss K.D., Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:10925-10930.
47. Saleem S., Zhuang H., Biswal S., Christen Y., Doré S. Ginkgo biloba extract neuroprotective action is dependent on heme oxygenase 1 in ischemic reperfusion brain injury. Stroke 2008, 39:3389-3396.
48. Satoh S., Kobayashi T., Hitomi A., Ikegaki I., Suzuki Y., Shibuya M., Yoshida J., Asano T. Inhibition of neutrophil migration by a protein kinase inhibitor for the treatment of ischemic brain infarction. Jpn. J. Pharmacol. 1999, 80:41-48.
49. Schilling M., Besselmann M., Leonhard C., Mueller M., Ringelstein E.B., Kiefer R. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: a study in green fluorescent protein transgenic bone marrow chimeric mice. Exp. Neurol. 2003, 183:25-33.
50. Schuette-Nuetgen K., Strecker J.K., Minnerup J., Ringelstein E.B., Schilling M. MCP-1/CCR-2-double-deficiency severely impairs the migration of hematogenous inflammatory cells following transient cerebral ischemia in mice. Exp. Neurol. 2012, 233:849-858.
51. Schwarzkopf T.M., Horn T., Lang D., Klein J. Blood gases and energy metabolites in mouse blood before and after cerebral ischemia: the effects of anesthetics. Exp. Biol. Med. (Maywood) 2013, 238:84-89.
52. Shah Z.A., Li R., Ahmad A.S., Kensler T.W., Yamamoto M., Biswal S., Doré S. The flavanol (-)-epicatechin prevents stroke damage through the Nrf2/HO-1 pathway. J. Cereb. Blood Flow Metab. 2010, 30:1951-1961.
53. Son T.G., Camandola S., Arumugam T.V., Cutler R.G., Telljohann R.S., Mughal M.R., Moore T.A., Luo W., Yu Q.S., Johnson D.A., Johnson J.A., Greig N.H., Mattson M.P. Plumbagin, a novel Nrf2/ARE activator, protects against cerebral ischemia. J. Neurochem. 2010, 112:1316-1326.
54. Soriano S.G., Coxon A., Wang Y.F., Frosch M.P., Lipton S.A., Hickey P.R., Mayadas T.N. Mice deficient in Mac-1 (CD11b/CD18) are less susceptible to cerebral ischemia/reperfusion injury. Stroke 1999, 30:134-139.
55. Stoll G., Jander S., Schrocter M. Inflammation and glial responses in ischemic brain lesions. Prog. Neurobiol. 1998, 56:149-171.
56. Sue Y.M., Cheng C.F., Chang C.C., Chou Y., Chen C.H., Juan S.H. Anti-oxidation and anti-inflammation by haem oxygenase-1 contribute to protection by tetramethylpyrazine against gentamicin-induced apoptosis in murine renal tubular cells. Nephrol. Dial. Transplant. 2009, 24:769-777.
57. Tanaka N., Ikeda Y., Ohta Y., Deguchi K., Tian F., Shang J., Matsuura T., Abe K. Expression of Keap1-Nrf2 system and antioxidative proteins in mouse brain after transient middle cerebral artery occlusion. Brain Res. 2011, 1370:246-253.
58. Tanaka S., Masuda Y., Honma C., Hosaka K., Takahashi K., Kubohara Y. Manganese promotes phorbol ester-induced interleukin-2 production via AP-1 activation in Jurkat T-cells. Toxicol. Lett. 2012, 211:312-318.
59. Tuttle R.S., Marmelstein L., Trad T., Reddy S., Radley T. In vitro uterine response to tetramethylpyrazine, the active constituent of chung chong (a traditional Chinese medicine). Am. J. Obstet. Gynecol. 1989, 161:1319-1323.
60. Wang J., Fields J., Zhao C., Langer J., Thimmulappa R.K., Kensler T.W., Yamamoto M., Biswal S., Dore S. Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic. Biol. Med. 2007, 43:408-414.
61. Wang L.W., Tu Y.F., Huang C.C., Ho C.J. JNK signaling is the shared pathway linking neuroinflammation, blood-brain barrier disruption, and oligodendroglial apoptosis in white matter injury of the immature brain. J. Neuroinflammation 2012, 9:175.
62. Wu C.C., Liao M.H., Chen S.J., Yen M.H. Tetramethylpyrazine prevents inducible NO synthase expression and improves survival in rodent models of endotoxic shock. Naunyn Schmiedebergs Arch. Pharmacol. 1999, 360:435-444.
63. Xiao X., Liu Y., Qi C., Qiu F., Chen X., Zhang J., Yang P. Neuroprotection and enhanced neurogenesis by tetramethylpyrazine in adult rat brain after focal ischemia. Neurol. Res. 2010, 32:547-555.
64. Yalniz M., Demirel U., Orhan C., Bahcecioglu I.H., Ozercan I.H., Aygun C., Tuzcu M., Sahin K. Nadroparin sodium activates Nrf2/HO-1 pathway in acetic acid-induced colitis in rats. Inflammation 2012, 35:1213-1221.
65. Yang C., Zhang X., Fan H., Liu Y. Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res. 2009, 1282:133-141.
66. Yenari M.A., Kunis D., Sun G.H., Onley D., Watson L., Tuner S., Whitaker S., Steinberg G.K. Hu23f2g, an antibody recognizing the leukocyte cd11/cd18 integrin, reduces injury in a rabbit model of transient focal cerebral ischemia. Exp. Neurol. 1998, 153:223-233.
67. Zhang Z., Wei T., Hou J., Li G., Yu S., Xin W. Tetramethylpyrazine scavenges superoxide anion and decreases nitric oxide production in human polymorphonuclear leukocytes. Life Sci. 2003, 72:2465-2472.
68. Zhao H., Zhuang F., Stoltz J.F., Wang X. Comparative studies of LFA-1/ICAM-1 interaction by micropipette and flow chamber techniques. Biorheology 2003, 40:179-187.
69. Zhao X., Sun G., Zhang J., Strong R., Dash P.K., Kan Y.W., Crotta J.C., Aronowski J. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke 2007, 38:3280-3286.