Tissue kallikrein protects against ischemic stroke by suppressing TLR4/NF-κB and activating Nrf2 signaling pathway in rats

Experimental and Therapeutic Medicine

Volumn 14, Issue 2, 2017, Pages 1163-1170

  Yang, Jiawei ^a,b   Su, Jianhua ^c   Wan, Fen ^a   Yang, Nan ^a   Jiang, Haibo ^a   Fang, Mingming ^d   Xiao, Hang ^e   Wang, Jun ^e   Tang, Jinrong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c China   (China)

^d Jiangsu Hospital of Traditional Chinese Medicine   (China)

^e NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Cerebral infarction; Inflammation; Neuroprotection; Oxidative stress; Tissue kallikrein

Indexed keywords

GELATINASE B; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TISSUE KALLIKREIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BEHAVIOR ASSESSMENT; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DENSITOMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOREACTIVITY; INFLAMMATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; THERAPY DELAY; WESTERN BLOTTING;

EID: 85023757869     PISSN: 17920981     EISSN: 17921015     Source Type: Journal    
DOI: 10.3892/etm.2017.4614     Document Type: Article

References (48)

1. Liu L, Wang D, Wong KS and Wang Y: Stroke and stroke care in China: Huge burden, significant workload, and a national priority. Stroke 42: 3651-3654, 2011.
2. Song D and Cho AH: Previous and recent evidence of endovascular therapy in acute ischemic stroke. Neurointervention 10: 51-59, 2015.
3. Amar AP, Griffin JH and Zlokovic BV: Combined neurothrombectomy or thrombolysis with adjunctive delivery of 3K3A-activated protein C in acute ischemic stroke. Front Cell Neurosci 9: 344, 2015.
4. Reuter B, Grudzenski S, Chatzikonstantinou E, Meairs S, Ebert A, Heiler P, Schad LR, Staufenbiel M, Hennerici MG and Fatar M: Thrombolysis in experimental cerebral amyloid angiopathy and the risk of secondary intracerebral hemorrhage. Stroke 45: 2411-2416, 2014.
5. Chechneva OV, Mayrhofer F, Daugherty DJ, Krishnamurty RG, Bannerman P, Pleasure DE and Deng W: A Smoothened receptor agonist is neuroprotective and promotes regeneration after ischemic brain injury. Cell Death Dis 5: e1481, 2014.
6. Chen X, Zhang X, Wang Y, Lei H, Su H, Zeng J, Pei Z and Huang R: Inhibition of immunoproteasome reduces infarction volume and attenuates inflammatory reaction in a rat model of ischemic stroke. Cell Death Dis 6: e1626, 2015.
7. Ahmad M and Graham SH: Inflammation after stroke: Mechanisms and therapeutic approaches. Transl Stroke Res 1: 74-84, 2010.
8. Nakajima H, Kubo T, Ihara H, Hikida T, Danjo T, Nakatsuji M, Shahani N, Itakura M, Ono Y, Azuma YT, et al: Nuclear-translocated Glyceraldehyde-3-phosphate dehydrogenase promotes poly (ADP-ribose) polymerase-1 activation during oxidative/nitrosative stress in stroke. J Biol Chem 290: 14493-14503, 2015.
9. Yainoy S, Houbloyfa P, Eiamphungporn W, Isarankura-Na-Ayudhya C and Prachayasittikul V: Engineering of chimeric catalase-Angiopep-2 for intracellular protection of brain endothelial cells against oxidative stress. Int J Biol Macromol 68: 60-66, 2014.
10. Wang L, Li Z, Zhang X, Wang S, Zhu C, Miao J, Chen L, Cui L and Qiao H: Protective effect of shikonin in experimental ischemic stroke: Attenuated TLR4, p-p38MAPK, NF-κB, TNF-α and MMP-9 expression, up-regulated claudin-5 expression, ameliorated BBB permeability. Neurochem Res 39: 97-106, 2014.
11. Candelario-Jalil E, Yang Y and Rosenberg GA: Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158: 983-994, 2009.
12. Vahedi K, Hofmeijer J, Juettler E, Vicaut E, George B, Algra A, Amelink GJ, Schmiedeck P, Schwab S, Rothwell PM, et al: Early decompressive surgery in malignant infarction of the middle cerebral artery: A pooled analysis of three randomised controlled trials. Lancet Neurol 6: 215-222, 2007.
13. Medzhitov R, Preston-Hurlburt P and Janeway CA Jr: A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397, 1997.
14. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A and Antel JP: TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175: 4320-4330, 2005.
15. Wang Y, Ge P and Zhu Y: TLR2 and TLR4 in the brain injury caused by cerebral ischemia and reperfusion. Mediators Inflamm 2013: 124614, 2013.
16. Zou N, Ao L, Cleveland JC Jr, Yang X, Su X, Cai GY, Banerjee A, Fullerton DA and Meng X: Critical role of extracellular heat shock cognate protein 70 in the myocardial inflammatory response and cardiac dysfunction after global ischemia-reperfusion. Am J Physiol Heart Circ Physiol 294: H2805-H2813, 2008.
17. Hyakkoku K, Hamanaka J, Tsuruma K, Shimazawa M, Tanaka H, Uematsu S, Akira S, Inagaki N, Nagai H and Hara H: Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia. Neuroscience 171: 258-267, 2010.
18. Caso JR, Pradillo JM, Hurtado O, Lorenzo P, Moro MA and Lizasoain I: Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115: 1599-1608, 2007.
19. Cao CX, Yang QW, Lv FL, Cui J, Fu HB and Wang JZ: Reduced cerebral ischemia-reperfusion injury in Toll-like receptor 4 deficient mice. Biochem Biophys Res Commun 353: 509-514, 2007.
20. Rao J, Qian X, Li G, Pan X, Zhang C, Zhang F, Zhai Y, Wang X and Lu L: ATF3-mediated NRF2/HO-1 signaling regulates TLR4 innate immune responses in mouse liver ischemia/reperfusion injury. Am J Transplant 15: 76-87, 2015.
21. Surh YJ and Na HK: NF-kappaB and Nrf2 as prime molecular targets for chemoprevention and cytoprotection with anti-inflammatory and antioxidant phytochemicals. Genes Nutr 2: 313-317, 2008.
22. Shah ZA, Li RC, Ahmad AS, Kensler TW, Yamamoto M, Biswal S and Doré S: The flavanol (-)-epicatechin prevents stroke damage through the Nrf2/HO1 pathway. J Cereb Blood Flow Metab 30: 1951-1961, 2010.
23. Albert-Weißenberger C, Sirén AL and Kleinschnitz C: Ischemic stroke and traumatic brain injury: The role of the kallikrein-kinin system. Prog Neurobiol 101-102: 65-82, 2013.
24. Xia CF, Yin H, Yao YY, Borlongan CV, Chao L and Chao J: Kallikrein protects against ischemic stroke by inhibiting apoptosis and inflammation and promoting angiogenesis and neurogenesis. Hum Gene Ther 17: 206-219, 2006.
25. Xia CF, Yin H, Borlongan CV, Chao L and Chao J: Kallikrein gene transfer protects against ischemic stroke by promoting glial cell migration and inhibiting apoptosis. Hypertension 43: 452-459, 2004.
26. Longa EZ, Weinstein PR, Carlson S and Cummins R: Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91, 1989.
27. Tatlisumak T, Carano RA, Takano K, Opgenorth TJ, Sotak CH and Fisher M: A novel endothelin antagonist, A-127722, attenuates ischemic lesion size in rats with temporary middle cerebral artery occlusion: A diffusion and perfusion MRI study. Stroke 29: 850-858, 1998.
28. Arumugam TV, Tang SC, Lathia JD, Cheng A, Mughal MR, Chigurupati S, Magnus T, Chan SL, Jo DG, Ouyang X, et al: Intravenous immunoglobulin (IVIG) protects the brain against experimental stroke by preventing complement-mediated neuronal cell death. Proc Natl Acad Sci USA 104: 14104-14109, 2007.
29. Hua F, Ma J, Ha T, Xia Y, Kelley J, Williams DL, Kao RL, Browder IW, Schweitzer JB, Kalbfleisch JH and Li C: Activation of Toll-like receptor 4 signaling contributes to hippocampal neuronal death following global cerebral ischemia/reperfusion. J Neuroimmunol 190: 101-111, 2007.
30. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, et al: Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 104: 13798-13803, 2007.
31. Ridder DA and Schwaninger M: NF-kappaB signaling in cerebral ischemia. Neuroscience 158: 995-1006, 2009.
32. Hayden MS, West AP and Ghosh S: NF-kappaB and the immune response. Oncogene 25: 6758-6780, 2006.
33. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T and Schwaninger M: NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 5: 554-559, 1999.
34. Morita-Fujimura Y, Fujimura M, Yoshimoto T and Chan PH: Superoxide during reperfusion contributes to caspase-8 expression and apoptosis after transient focal stroke. Stroke 32: 2356-2361, 2001.
35. Shih AY, Li P and Murphy TH: A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 25: 10321-10335, 2005.
36. Poss KD and Tonegawa S: Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 94: 10925-10930, 1997.
37. Satoh T, Izumi M, Inukai Y, Tsutsumi Y, Nakayama N, Kosaka K, Shimojo Y, Kitajima C, Itoh K, Yokoi T and Shirasawa T: Carnosic acid protects neuronal HT22 cells through activation of the antioxidant-responsive element in free carboxylic acid-and catechol hydroxyl moieties-dependent manners. Neurosci Lett 434: 260-265, 2008.
38. Shi H, Jing X, Wei X, Perez RG, Ren M, Zhang X and Lou H: S-allyl cysteine activates the Nrf2-dependent antioxidant response and protects neurons against ischemic injury in vitro and in vivo. J Neurochem 133: 298-308, 2015.
39. Li L, Zhang X, Cui L, Wang L, Liu H, Ji H and Du Y: Ursolic acid promotes the neuroprotection by activating Nrf2 pathway after cerebral ischemia in mice. Brain Res 1497: 32-39, 2013.
40. Kunze R, Urrutia A, Hoffmann A, Liu H, Helluy X, Pham M, Reischl S, Korff T and Marti HH: Dimethyl fumarate attenuates cerebral edema formation by protecting the blood-brain barrier integrity. Exp Neurol 266: 99-111, 2015.
41. Sapojnikova N, Kartvelishvili T, Asatiani N, Zinkevich V, Kalandadze I, Gugutsidze D, Shakarishvili R and Tsiskaridze A: Correlation between MMP-9 and extracellular cytokine HMGB1 in prediction of human ischemic stroke outcome. Biochim Biophys Acta 1842: 1379-1384, 2014.
42. Clark AW, Krekoski CA, Bou SS, Chapman KR and Edwards DR: Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett 238: 53-56, 1997.
43. Cai Y, Liu X, Chen W, Wang Z, Xu G, Zeng Y and Ma Y: TGF-β1 prevents blood-brain barrier damage and hemorrhagic transformation after thrombolysis in rats. Exp Neurol 266: 120-126, 2015.
44. Kamiya T, Katayama Y, Kashiwagi F and Terashi A: The role of bradykinin in mediating ischemic brain edema in rats. Stroke 24: 571-576, 1993.
45. Zausinger S, Lumenta DB, Pruneau D, Schmid-Elsaesser R, Plesnila N and Baethmann A: Effects of LF 16-0687 Ms, a bradykinin B(2) receptor antagonist, on brain edema formation and tissue damage in a rat model of temporary focal cerebral ischemia. Brain Res 950: 268-278, 2002.
46. Lu RY, Luo DF, Xiao SH, Yang LH, Zhao J, Ji EN, Tao EX, Xing YG, Zhu FY, Luan P and Liu J: Kallikrein gene transfer induces angiogenesis and further improves regional cerebral blood flow in the early period after cerebral ischemia/reperfusion in rats. CNS Neurosci Ther 18: 395-399, 2012.
47. Chen ZB, Huang DQ, Niu FN, Zhang X, Li EG and Xu Y: Human urinary kallidinogenase suppresses cerebral inflammation in experimental stroke and downregulates nuclear factor-kappaB. J Cereb Blood Flow Metab 30: 1356-1365, 2010.
48. Chao J, Shen B, Gao L, Xia CF, Bledsoe G and Chao L: Tissue kallikrein in cardiovascular, cerebrovascular and renal diseases and skin wound healing. Biol Chem 391: 345-355, 2010.