Chronic metformin treatment improves post-stroke angiogenesis and recovery after experimental stroke

European Journal of Neuroscience

Volumn 39, Issue 12, 2014, Pages 2129-2138

  Venna, Venugopal R ^a   Li, Jun ^a   Hammond, Matthew D ^a   Mancini, Nickolas S ^b   Mccullough, Louise D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

AMPK; Apomorphine; Cerebral ischemia; Metformin

Indexed keywords

APOMORPHINE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; VASCULOTROPIN; AMPK ALPHA2 SUBUNIT, MOUSE; DOPAMINE RECEPTOR STIMULATING AGENT; NEUROPROTECTIVE AGENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ADHESIVE REMOVAL TEST; ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR DISORDER; BODY WEIGHT; BRAIN BLOOD VESSEL; BRAIN INFARCTION; CEREBRAL REVASCULARIZATION; CIRCLING BEHAVIOR; CONTROLLED STUDY; CONVALESCENCE; DOPAMINERGIC ACTIVITY; EXPERIMENTAL STROKE; EXPERIMENTAL TEST; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; LONG TERM CARE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; C57BL MOUSE; CEREBROVASCULAR ACCIDENT; DISEASE MODEL; DRUG EFFECTS; GENETICS; GLIA; INFARCTION, MIDDLE CEREBRAL ARTERY; KNOCKOUT MOUSE; METABOLISM; MOTOR ACTIVITY; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; STIMULATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOMORPHINE; BRAIN; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; METFORMIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEOVASCULARIZATION, PATHOLOGIC; NEUROGLIA; NEUROPROTECTIVE AGENTS; PHYSICAL STIMULATION; RANDOM ALLOCATION; RECOVERY OF FUNCTION; STROKE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84902547561     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12556     Document Type: Article

References (52)

1. Bland, S.T., Schallert, T., Strong, R., Aronowski, J., Grotta, J.C. & Feeney, D.M. (2000) Early exclusive use of the affected forelimb after moderate transient focal ischemia in rats: functional and anatomic outcome. Stroke, 31, 1144-1152.
2. Bouet, V., Boulouard, M., Toutain, J., Divoux, D., Bernaudin, M., Schumann-Bard, P. & Freret, T. (2009) The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat. Protoc., 4, 1560-1564.
3. Burke, J.F., Lisabeth, L.D., Brown, D.L., Reeves, M.J. & Morgenstern, L.B. (2012) Determining stroke's rank as a cause of death using multicause mortality data. Stroke, 43, 2207-2211.
4. Chopp, M., Zhang, Z.G. & Jiang, Q. (2007) Neurogenesis, angiogenesis, and MRI indices of functional recovery from stroke. Stroke, 38, 827-831.
5. Dereski, M.O., Chopp, M., Knight, R.A., Rodolosi, L.C. & Garcia, J.H. (1993) The heterogeneous temporal evolution of focal ischemic neuronal damage in the rat. Acta Neuropathol., 85, 327-333.
6. Ergul, A., Alhusban, A. & Fagan, S.C. (2012) Angiogenesis: a harmonized target for recovery after stroke. Stroke, 43, 2270-2274.
7. Font, M.A., Arboix, A. & Krupinski, J. (2010) Angiogenesis, neurogenesis and neuroplasticity in ischemic stroke. Curr. Cardiol. Rev., 6, 238-244.
8. Fridriksson, J. (2010) Preservation and modulation of specific left hemisphere regions is vital for treated recovery from anomia in stroke. J. Neurosci., 30, 11558-11564.
9. Garcia, J.H., Yoshida, Y., Chen, H., Li, Y., Zhang, Z.G., Lian, J., Chen, S. & Chopp, M. (1993) Progression from ischemic injury to infarct following middle cerebral artery occlusion in the rat. Am. J. Pathol., 142, 623-635.
10. Hoehn, M., Nicolay, K., Franke, C. & van der Sanden, B. (2001) Application of magnetic resonance to animal models of cerebral ischemia. J. Magn. Reson. Imaging, 14, 491-509.
11. Johnston, D.G., Denizet, M., Mostany, R. & Portera-Cailliau, C. (2012) Chronic in vivo imaging shows no evidence of dendritic plasticity or functional remapping in the contralesional cortex after stroke. Cereb. Cortex, 23, 751-762.
12. Kim, S.A. & Choi, H.C. (2012) Metformin inhibits inflammatory response via AMPK-PTEN pathway in vascular smooth muscle cells. Biochem. Bioph. Res. Co., 425, 866-872.
13. Kronenberg, G., Balkaya, M., Prinz, V., Gertz, K., Ji, S., Kirste, I., Heuser, I., Kampmann, B., Hellmann-Regen, J., Gass, P., Sohr, R., Hellweg, R., Waeber, C., Juckel, G., Hortnagl, H., Stumm, R. & Endres, M. (2012) Exofocal dopaminergic degeneration as antidepressant target in mouse model of poststroke depression. Biol. Psychiat., 72, 273-281.
14. Labuzek, K., Liber, S., Gabryel, B., Adamczyk, J. & Okopien, B. (2010a) Metformin increases phagocytosis and acidifies lysosomal/endosomal compartments in AMPK-dependent manner in rat primary microglia. N.-S. Arch. Pharmacol., 381, 171-186.
15. Labuzek, K., Suchy, D., Gabryel, B., Bielecka, A., Liber, S. & Okopien, B. (2010b) Quantification of metformin by the HPLC method in brain regions, cerebrospinal fluid and plasma of rats treated with lipopolysaccharide. Pharmacol. Rep., 62, 956-965.
16. Lelekov-Boissard, T., Chapuisat, G., Boissel, J.P., Grenier, E. & Dronne, M.A. (2009) Exploration of beneficial and deleterious effects of inflammation in stroke: dynamics of inflammation cells. Philos. T. R. Soc. A., 367, 4699-4716.
17. Li, X., Blizzard, K.K., Zeng, Z., DeVries, A.C., Hurn, P.D. & McCullough, L.D. (2004) Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender. Exp. Neurol., 187, 94-104.
18. Li, J., Benashski, S.E., Venna, V.R. & McCullough, L.D. (2010) Effects of metformin in experimental stroke. Stroke, 41, 2645-2652.
19. Liu, F. & McCullough, L.D. (2011) Middle cerebral artery occlusion model in rodents: methods and potential pitfalls. J. Biomed. Biotechnol., 2011, 464701.
20. van Lookeren Campagne, M., Thomas, G.R., Thibodeaux, H., Palmer, J.T., Williams, S.P., Lowe, D.G. & van Bruggen, N. (1999) Secondary reduction in the apparent diffusion coefficient of water, increase in cerebral blood volume, and delayed neuronal death after middle cerebral artery occlusion and early reperfusion in the rat. J. Cerebr. Blood F. Met., 19, 1354-1364.
21. Manoonkitiwongsa, P.S., Jackson-Friedman, C., McMillan, P.J., Schultz, R.L. & Lyden, P.D. (2001) Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J. Cerebr. Blood F. Met., 21, 1223-1231.
22. Menendez, J.A. & Vazquez-Martin, A. (2012) Rejuvenating regeneration: metformin activates endogenous adult stem cells. Cell Cycle, 11, 3521-3522.
23. Meyers, P.M., Schumacher, H.C., Alexander, M.J., Derdeyn, C.P., Furlan, A.J., Higashida, R.T., Moran, C.J., Tarr, R.W., Heck, D.V., Hirsch, J.A., Jensen, M.E., Linfante, I., McDougall, C.G., Nesbit, G.M., Rasmussen, P.A., Tomsick, T.A., Wechsler, L.R., Wilson, J.R. & Zaidat, O.O. (2012) Performance and training standards for endovascular acute ischemic stroke treatment. Neurology, 79, S234-S238.
24. Muller, T., Benz, S., Bornke, C. & Przuntek, H. (2004) Differential response in choice reaction time following apomorphine based on prior dopaminergic treatment. Acta Neurol. Scand., 109, 348-354.
25. Murphy, T.H. & Corbett, D. (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci., 10, 861-872.
26. Nagata, D., Mogi, M. & Walsh, K. (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem., 278, 31000-31006.
27. Nathan, D.M., Buse, J.B., Davidson, M.B., Ferrannini, E., Holman, R.R., 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, 193-203.
28. Newton, J.M., Ward, N.S., Parker, G.J., Deichmann, R., Alexander, D.C., Friston, K.J. & Frackowiak, R.S. (2006) Non-invasive mapping of corticofugal fibres from multiple motor areas-relevance to stroke recovery. Brain, 129, 1844-1858.
29. Ortega-Gonzalez, C., Cardoza, L., Coutino, B., Hidalgo, R., Arteaga-Troncoso, G. & Parra, A. (2005) Insulin sensitizing drugs increase the endogenous dopaminergic tone in obese insulin-resistant women with polycystic ovary syndrome. J. Endocrinol., 184, 233-239.
30. Ouchi, N., Shibata, R. & Walsh, K. (2005) AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ. Res., 96, 838-846.
31. Potts, M.B. & Lim, D.A. (2012) An old drug for new ideas: metformin promotes adult neurogenesis and spatial memory formation. Cell Stem Cell, 11, 5-6.
32. Prakash, R., Li, W., Qu, Z., Johnson, M. A., Fagan, S. C. & Ergul, A. (2013) Vascularization pattern after ischemic stroke is different in control versus diabetic rats: relevance to stroke recovery. Stroke, 44, 2875-2882.
33. Rocamonde, B., Paradells, S., Barcia, J.M., Barcia, C., Garcia Verdugo, J.M., Miranda, M., Romero Gomez, F.J. & Soria, J.M. (2012) Neuroprotection of lipoic acid treatment promotes angiogenesis and reduces the glial scar formation after brain injury. Neuroscience, 224, 102-115.
34. Rossini, P.M., Calautti, C., Pauri, F. & Baron, J.C. (2003) Post-stroke plastic reorganisation in the adult brain. Lancet Neurol., 2, 493-502.
35. Roussel, R., Travert, F., Pasquet, B., Wilson, P.W., Smith, S.C. Jr, Goto, S., Ravaud, P., Marre, M., Porath, A., Bhatt, D.L. & Steg, P.G. (2010) Metformin use and mortality among patients with diabetes and atherothrombosis. Arch. Intern. Med., 170, 1892-1899.
36. Shibuya, M. & Claesson-Welsh, L. (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp. Cell Res., 312, 549-560.
37. Stahmann, N., Woods, A., Spengler, K., Heslegrave, A., Bauer, R., Krause, S., Viollet, B., Carling, D. & Heller, R. (2010) Activation of AMP-activated protein kinase by vascular endothelial growth factor mediates endothelial angiogenesis independently of nitric-oxide synthase. J. Biol. Chem., 285, 10638-10652.
38. Strong, K., Mathers, C. & Bonita, R. (2007) Preventing stroke: saving lives around the world. Lancet Neurol., 6, 182-187.
39. Sun, X., Zhang, Q.W., Xu, M., Guo, J.J., Shen, S.W., Wang, Y.Q. & Sun, F.Y. (2012) New striatal neurons form projections to substantia nigra in adult rat brain after stroke. Neurobiol. Dis., 45, 601-609.
40. Szpak, G.M., Lechowicz, W., Lewandowska, E., Bertrand, E., Wierzba-Bobrowicz, T. & Dymecki, J. (1999) Border zone neovascularization in cerebral ischemic infarct. Folia Neuropathol., 37, 264-268.
41. Thiyagarajan, M., Fernandez, J.A., Lane, S.M., Griffin, J.H. & Zlokovic, B.V. (2008) Activated protein C promotes neovascularization and neurogenesis in postischemic brain via protease-activated receptor 1. J. Neurosci., 28, 12788-12797.
42. Towfighi, A. & Saver, J.L. (2011) Stroke declines from third to fourth leading cause of death in the United States: historical perspective and challenges ahead. Stroke, 42, 2351-2355.
43. Truong, D.T., Venna, V.R., McCullough, L.D. & Fitch, R.H. (2012) Deficits in auditory, cognitive, and motor processing following reversible middle cerebral artery occlusion in mice. Exp. Neurol., 238, 114-121.
44. Uehara, M.H., Kohlmann, N.E., Zanella, M.T. & Ferreira, S.R. (2001) Metabolic and haemodynamic effects of metformin in patients with type 2 diabetes mellitus and hypertension. Diabetes Obes. Metab., 3, 319-325.
45. UK Prospective Diabetes Study (UKPDS) Group (1998) Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). Lancet, 352, 854-865.
46. Veizovic, T., Beech, J.S., Stroemer, R.P., Watson, W.P. & Hodges, H. (2001) Resolution of stroke deficits following contralateral grafts of conditionally immortal neuroepithelial stem cells. Stroke, 32, 1012-1019.
47. Venna, V.R., Li, J., Benashski, S.E., Tarabishy, S. & McCullough, L.D. (2012a) Preconditioning induces sustained neuroprotection by downregulation of adenosine 5′-monophosphate-activated protein kinase. Neuroscience, 201, 280-287.
48. Venna, V.R., Weston, G., Benashski, S.E., Tarabishy, S., Liu, F., Li, J., Conti, L.H. & McCullough, L.D. (2012b) NF-kappaB contributes to the detrimental effects of social isolation after experimental stroke. Acta Neuropathol., 124, 425-438.
49. Viollet, B., Guigas, B., Sanz Garcia, N., Leclerc, J., Foretz, M. & Andreelli, F. (2012) Cellular and molecular mechanisms of metformin: an overview. Clin. Sci., 122, 253-270.
50. Wang, J., Gallagher, D., DeVito, L.M., Cancino, G.I., Tsui, D., He, L., Keller, G.M., Frankland, P.W., Kaplan, D.R. & Miller, F.D. (2012) Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation. Cell Stem Cell, 11, 23-35.
51. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M.F., Goodyear, L.J. & Moller, D.E. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest., 108, 1167-1174.
52. Zimmet, P. & Collier, G. (1999) Clinical efficacy of metformin against insulin resistance parameters: sinking the iceberg. Drugs, 58(Suppl 1), 21-28; discussion 75-82.