Chronic Metformin Preconditioning Provides Neuroprotection via Suppression of NF-κB-Mediated Inflammatory Pathway in Rats with Permanent Cerebral Ischemia

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 375-385

  Zhu, Xi Chen ^a   Jiang, Teng ^a   Zhang, Qiao Quan ^a   Cao, Lei ^a   Tan, Meng Shan ^b   Wang, Hui Fu ^a   Ding, Zheng Zheng ^a   Tan, Lan ^a,b,c   Yu, Jin Tai ^a,b,c,d  

^a NANJING MEDICAL UNIVERSITY   (China)

^b OCEAN UNIVERSITY OF CHINA   (China)

^c QINGDAO UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Inflammation; Metformin; NF B; Preconditioning; Stroke

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; METFORMIN; TUMOR NECROSIS FACTOR ALPHA; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; AUTACOID; CALCIUM BINDING PROTEIN; CYTOKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN ISCHEMIA; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; GLIOSIS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; RAT; ACUTE DISEASE; ANIMAL; ASTROCYTE; BRAIN; COMPLICATION; DRUG EFFECTS; GENETICS; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; METABOLISM; MICROGLIA; PATHOLOGY; SPRAGUE DAWLEY RAT; STROKE;

ACUTE DISEASE; ANIMALS; ASTROCYTES; BRAIN; BRAIN ISCHEMIA; CALCIUM-BINDING PROTEINS; CYTOKINES; GLIAL FIBRILLARY ACIDIC PROTEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; METFORMIN; MICROFILAMENT PROTEINS; MICROGLIA; NEUROPROTECTION; NF-KAPPA B; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STROKE;

EID: 84937963126     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8866-7     Document Type: Article

References (46)

1. Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, Sherwin R, Zinman B (2009) Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 32(1):193–203. doi:10.2337/dc08-9025
2. Cheng YY, Leu HB, Chen TJ, Chen CL, Kuo CH, Lee SD, Kao CL (2013) Metformin-inclusive therapy reduces the risk of stroke in patients with diabetes: a 4-year follow-up study. J Stroke Cerebrovasc Dis: Off J Nat Stroke Assoc. doi:10.1016/j.jstrokecerebrovasdis.2013.09.001
3. Nathan DM (1998) Some answers, more controversy, from UKPDS. United Kingdom Prospective Diabetes Study. Lancet 352(9131):832–833
4. Selvin E, Hirsch AT (2008) Contemporary risk factor control and walking dysfunction in individuals with peripheral arterial disease: NHANES 1999–2004. Atherosclerosis 201(2):425–433. doi:10.1016/j.atherosclerosis.2008.02.002
5. Li J, Benashski SE, Venna VR, McCullough LD (2010) Effects of metformin in experimental stroke. Stroke; J Cereb Circ 41(11):2645–2652. doi:10.1161/STROKEAHA.110.589697
6. Ashabi G, Khodagholi F, Khalaj L, Goudarzvand M, Nasiri M (2014) Activation of AMP-activated protein kinase by metformin protects against global cerebral ischemia in male rats: interference of AMPK/PGC-1alpha pathway. Metab Brain Dis 29(1):47–58. doi:10.1007/s11011-013-9475-2
7. del Zoppo GJ (2010) Acute anti-inflammatory approaches to ischemic stroke. Ann N Y Acad Sci 1207:143–148. doi:10.1111/j.1749-6632.2010.05761.x
8. Danton GH, Dietrich WD (2003) Inflammatory mechanisms after ischemia and stroke. J Neuropathol Exp Neurol 62(2):127–136
9. Ridder DA, Schwaninger M (2009) NF-kappaB signaling in cerebral ischemia. Neuroscience 158(3):995–1006. doi:10.1016/j.neuroscience.2008.07.007
10. Schmitz ML, Bacher S, Kracht M (2001) I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations. Trends Biochem Sci 26(3):186–190
11. Pizzi M, Goffi F, Boroni F, Benarese M, Perkins SE, Liou HC, Spano P (2002) Opposing roles for NF-kappa B/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1beta. J Biol Chem 277(23):20717–20723. doi:10.1074/jbc.M201014200
12. Nurmi A, Lindsberg PJ, Koistinaho M, Zhang W, Juettler E, Karjalainen-Lindsberg ML, Weih F, Frank N, Schwaninger M, Koistinaho J (2004) Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke J Cereb Circ 35(4):987–991. doi:10.1161/01.STR.0000120732.45951.26
13. Crack PJ, Taylor JM, Ali U, Mansell A, Hertzog PJ (2006) Potential contribution of NF-kappaB in neuronal cell death in the glutathione peroxidase-1 knockout mouse in response to ischemia-reperfusion injury. Stroke J Cereb Circ 37(6):1533–1538. doi:10.1161/01.STR.0000221708.17159.64
14. Zhang W, Potrovita I, Tarabin V, Herrmann O, Beer V, Weih F, Schneider A, Schwaninger M (2005) Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 25(1):30–40. doi:10.1038/sj.jcbfm.9600004
15. Kunz A, Abe T, Hochrainer K, Shimamura M, Anrather J, Racchumi G, Zhou P, Iadecola C (2008) Nuclear factor-kappaB activation and postischemic inflammation are suppressed in CD36-null mice after middle cerebral artery occlusion. J Neurosci: Off J Soc Neurosci 28(7):1649–1658. doi:10.1523/JNEUROSCI.5205-07.2008
16. Harari OA, Liao JK (2010) NF-kappaB and innate immunity in ischemic stroke. Ann N Y Acad Sci 1207:32–40. doi:10.1111/j.1749-6632.2010.05735.x
17. Jiang T, Gao L, Guo J, Lu J, Wang Y, Zhang Y (2012) Suppressing inflammation by inhibiting the NF-kappaB pathway contributes to the neuroprotective effect of angiotensin-(1-7) in rats with permanent cerebral ischaemia. Br J Pharmacol 167(7):1520–1532. doi:10.1111/j.1476-5381.2012.02105.x
18. Desai A, Singh N, Raghubir R (2010) Neuroprotective potential of the NF-kappaB inhibitor peptide IKK-NBD in cerebral ischemia-reperfusion injury. Neurochem Int 57(8):876–883. doi:10.1016/j.neuint.2010.09.006
19. Hwang SY, Shin JH, Hwang JS, Kim SY, Shin JA, Oh ES, Oh S, Kim JB, Lee JK, Han IO (2010) Glucosamine exerts a neuroprotective effect via suppression of inflammation in rat brain ischemia/reperfusion injury. Glia 58(15):1881–1892. doi:10.1002/glia.21058
20. Park CS, Bang BR, Kwon HS, Moon KA, Kim TB, Lee KY, Moon HB, Cho YS (2012) Metformin reduces airway inflammation and remodeling via activation of AMP-activated protein kinase. Biochem Pharmacol 84(12):1660–1670. doi:10.1016/j.bcp.2012.09.025
21. Woo SL, Xu H, Li H, Zhao Y, Hu X, Zhao J, Guo X, Guo T, Botchlett R, Qi T, Pei Y, Zheng J, Xu Y, An X, Chen L, Li Q, Xiao X, Huo Y, Wu C (2014) Metformin ameliorates hepatic steatosis and inflammation without altering adipose phenotype in diet-induced obesity. PLoS One 9(3):e91111. doi:10.1371/journal.pone.0091111
22. Martin-Montalvo A, Mercken EM, Mitchell SJ, Palacios HH, Mote PL, Scheibye-Knudsen M, Gomes AP, Ward TM, Minor RK, Blouin MJ, Schwab M, Pollak M, Zhang Y, Yu Y, Becker KG, Bohr VA, Ingram DK, Sinclair DA, Wolf NS, Spindler SR, Bernier M, de Cabo R (2013) Metformin improves healthspan and lifespan in mice. Nat Commun 4:2192. doi:10.1038/ncomms3192
23. Hattori Y, Suzuki K, Hattori S, Kasai K (2006) Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension 47(6):1183–1188. doi:10.1161/01.HYP.0000221429.94591.72
24. Isoda K, Young JL, Zirlik A, MacFarlane LA, Tsuboi N, Gerdes N, Schonbeck U, Libby P (2006) Metformin inhibits proinflammatory responses and nuclear factor-kappaB in human vascular wall cells. Arterioscler Thromb Vasc Biol 26(3):611–617. doi:10.1161/01.ATV.0000201938.78044.75
25. Ma TC, Buescher JL, Oatis B, Funk JA, Nash AJ, Carrier RL, Hoyt KR (2007) Metformin therapy in a transgenic mouse model of Huntington’s disease. Neurosci Lett 411(2):98–103. doi:10.1016/j.neulet.2006.10.039
26. Nath N, Khan M, Paintlia MK, Singh I, Hoda MN, Giri S (2009) Metformin attenuated the autoimmune disease of the central nervous system in animal models of multiple sclerosis. J Immunol 182(12):8005–8014. doi:10.4049/jimmunol.0803563
27. Paintlia AS, Paintlia MK, Mohan S, Singh AK, Singh I (2013) AMP-activated protein kinase signaling protects oligodendrocytes that restore central nervous system functions in an experimental autoimmune encephalomyelitis model. Am J Pathol 183(2):526–541. doi:10.1016/j.ajpath.2013.04.030
28. Jiang T, Yu JT, Zhu XC, Wang HF, Tan MS, Cao L, Zhang QQ, Gao L, Shi JQ, Zhang YD, Tan L (2014) Acute metformin preconditioning confers neuroprotection against focal cerebral ischemia by pre-activation of AMPK-dependent autophagy. Br J Pharmacol. doi:10.1111/bph.12655
29. Jiang T, Yu JT, Zhu XC, Zhang QQ, Tan MS, Cao L, Wang HF, Shi JQ, Gao L, Qin H, Zhang YD, Tan L (2014) Ischemic preconditioning provides neuroprotection by induction of AMP-activated protein kinase-dependent autophagy in a rat model of ischemic stroke. Mol Neurobiol. doi:10.1007/s12035-014-8725-6
30. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H (1986) Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke J Cereb Circ 17(3):472–476
31. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 10(2):290–293. doi:10.1038/jcbfm.1990.47
32. Jiang T, Yu JT, Zhu XC, Tan MS, Gu LZ, Zhang YD, Tan L (2014) Triggering receptor expressed on myeloid cells 2 knockdown exacerbates aging-related neuroinflammation and cognitive deficiency in senescence-accelerated mouse prone 8 mice. Neurobiol Aging 35(6):1243–1251. doi:10.1016/j.neurobiolaging.2013.11.026
33. Tan MS, Yu JT, Jiang T, Zhu XC, Guan HS, Tan L (2014) IL12/23 p40 inhibition ameliorates Alzheimer’s disease-associated neuropathology and spatial memory in SAMP8 mice. Journal of Alzheimer’s disease: JAD 38(3):633–646. doi:10.3233/JAD-131148
34. Jiang T, Tan L, Zhu XC, Zhang QQ, Cao L, Tan MS, Gu LZ, Wang HF, Ding ZZ, Zhang YD, Yu JT (2014) Up-regulation of TREM2 ameliorates neuropathology and rescues spatial cognitive impairment in a transgenic mouse model of Alzheimer’s disease. Neuropsychopharmacol: Off Publ Am College Neuropsychopharmacol. doi:10.1038/npp.2014.164
35. Sarnico I, Lanzillotta A, Boroni F, Benarese M, Alghisi M, Schwaninger M, Inta I, Battistin L, Spano P, Pizzi M (2009) NF-kappaB p50/RelA and c-Rel-containing dimers: opposite regulators of neuron vulnerability to ischaemia. J Neurochem 108(2):475–485. doi:10.1111/j.1471-4159.2008.05783.x
36. Schmitz ML, Mattioli I, Buss H, Kracht M (2004) NF-kappaB: a multifaceted transcription factor regulated at several levels. Chembiochem: Eur J Chem Biol 5(10):1348–1358. doi:10.1002/cbic.200400144
37. Viatour P, Merville MP, Bours V, Chariot A (2005) Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30(1):43–52. doi:10.1016/j.tibs.2004.11.009
38. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T, Schwaninger M (1999) NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 5(5):554–559. doi:10.1038/8432
39. Sironi L, Banfi C, Brioschi M, Gelosa P, Guerrini U, Nobili E, Gianella A, Paoletti R, Tremoli E, Cimino M (2006) Activation of NF-kB and ERK1/2 after permanent focal ischemia is abolished by simvastatin treatment. Neurobiol Dis 22(2):445–451. doi:10.1016/j.nbd.2005.12.004
40. Zhang HL, Gu ZL, Savitz SI, Han F, Fukunaga K, Qin ZH (2008) Neuroprotective effects of prostaglandin A(1) in rat models of permanent focal cerebral ischemia are associated with nuclear factor-kappaB inhibition and peroxisome proliferator-activated receptor-gamma up-regulation. J Neurosci Res 86(5):1132–1141. doi:10.1002/jnr.21569
41. Xu L, Zhan Y, Wang Y, Feuerstein GZ, Wang X (2002) Recombinant adenoviral expression of dominant negative IkappaB alpha protects brain from cerebral ischemic injury. Biochem Biophys Res Commun 299(1):14–17
42. Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184(1–2):53–68. doi:10.1016/j.jneuroim.2006.11.014
43. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35. doi:10.1007/s00401-009-0619-8
44. Dong Y, Benveniste EN (2001) Immune function of astrocytes. Glia 36(2):180–190
45. Wood PL (1995) Microglia as a unique cellular target in the treatment of stroke: potential neurotoxic mediators produced by activated microglia. Neurol Res 17(4):242–248
46. Jiang T, Yu JT, Zhu XC, Wang HF, Tan MS, Cao L, Zhang QQ, Gao L, Shi JQ, Zhang YD, Tan L (2014) Acute metformin preconditioning confers neuroprotection against focal cerebral ischaemia by pre-activation of AMPK-dependent autophagy. Br J Pharmacol 171(13):3146–3157. doi:10.1111/bph.12655