Impaired leptomeningeal collateral flow contributes to the poor outcome following experimental stroke in the type 2 diabetic mice

Journal of Neuroscience

Volumn 35, Issue 9, 2015, Pages 3851-3864

  Akamatsu, Yosuke ^a,b,c   Nishijima, Yasuo ^a,b,c   Lee, Chih Cheng ^a,b   Yang, Shih Yen ^a,b   Shi, Lei ^d   An, Lin ^d   Wang, Ruikang K ^d   Tominaga, Teiji ^c   Liu, Jialing ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anastomosis; Arteriogenesis; Doppler OCT; MCAO; Metabolic syndrome; Vascular remodeling

Indexed keywords

HUMAN ALBUMIN;

ANASTOMOSIS; ANGIOGENESIS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CEREBRAL ARTERY; ARTICLE; BLOOD FLOW VELOCITY; BRAIN BLOOD FLOW; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PERFUSION; COLLATERAL CIRCULATION; CONTROLLED STUDY; CORNER TEST; GLUCOSE BLOOD LEVEL; HORIZONTAL LADDER TEST; HYPERGLYCEMIA; LEPTOMENINGEAL COLLATERAL FLOW; MALE; MICROANGIOGRAPHY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROLOGIC EXAMINATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SPATIOTEMPORAL ANALYSIS; VASCULAR REMODELING; ANIMAL; BRAIN CIRCULATION; C57BL MOUSE; COMPLICATION; GENETICS; KNOCKOUT MOUSE; MENINX; MIDDLE CEREBRAL ARTERY; PATHOPHYSIOLOGY; PHYSIOLOGY; STROKE; VASCULARIZATION;

ANIMALS; BEHAVIOR, ANIMAL; CEREBROVASCULAR CIRCULATION; COLLATERAL CIRCULATION; DIABETES MELLITUS, TYPE 2; MALE; MENINGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE CEREBRAL ARTERY; STROKE; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84924777566     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3838-14.2015     Document Type: Article

References (55)

1. Alessi MC, Juhan-Vague I (2006) PAI-1 and the metabolic syndrome: links, causes, and consequences. Arterioscler Thromb Vasc Biol 26:2200–2207.
2. Armitage GA, Todd KG, Shuaib A, Winship IR (2010) Laser speckle contrast imaging of collateral blood flow during acute ischemic stroke. J Cereb Blood Flow Metab 30:1432–1436.
3. Belayev L, Zhao W, Pattany PM, Weaver RG, Huh PW, Lin B, Busto R, Ginsberg MD (1998) Diffusion-weighted magnetic resonance imaging confirms marked neuroprotective efficacy of albumin therapy in focal cerebral ischemia. Stroke 29:2587–2599.
4. Belayev L, Liu Y, Zhao W, Busto R, Ginsberg MD (2001) Human albumin therapy of acute ischemic stroke: marked neuroprotective efficacy at moderate doses and withabroad therapeutic window. Stroke 32:553–560.
5. Belayev L, Pinard E, Nallet H, Seylaz J, Liu Y, Riyamongkol P, Zhao W, Busto R, Ginsberg MD (2002) Albumin therapy of transient focal cerebral ischemia: in vivo analysis of dynamic microvascular responses. Stroke 33:1077–1084.
6. Braaten JV, Handt S, Jerome WG, Kirkpatrick J, Lewis JC, Hantgan RR (1993) Regulation of fibrinolysis by platelet-released plasminogen activator inhibitor 1: light scattering and ultrastructural examination of lysis of a model platelet-fibrin thrombus. Blood 81:1290–1299.
7. Bruno A, Biller J, Adams HP Jr, Clarke WR, Woolson RF, Williams LS, Han-sen MD (1999) Acute blood glucose level and outcome from ischemic stroke: Trial of ORG 10172 in Acute Stroke Treatment (TOAST) Investigators. Neurology 52:280–284.
8. Caplan LR, Hennerici M (1998) Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol 55:1475–1482.
9. Chen J, Cui X, Zacharek A, Cui Y, Roberts C, Chopp M (2011) White matter damage and the effectofmatrix metalloproteinasesin type 2diabetic mice after stroke. Stroke 42:445–452.
10. Defazio RA, Zhao W, Deng X, Obenaus A, Ginsberg MD (2012) Albumin therapy enhances collateral perfusion after laser-induced middle cerebral artery branch occlusion: a laser speckle contrast flow study. J Cereb Blood Flow Metab 32:2012–2022.
11. Dobrin PB, Schwarcz TH, Baker WH (1988) Mechanisms of arterial and aneurysmal tortuosity. Surgery 104:568–571.
12. Emerging Risk Factors Collaboration, Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, DiAngelantonio E, Ingelsson E, Lawlor DA, Selvin E, Stampfer M, Stehouwer CD, Lewington S, Pennells L, Thompson A, Sattar N, White IR, Ray KK, Danesh J (2010) Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 375:2215–2222.
13. Faber JE, Zhang H, Lassance-Soares RM, Prabhakar P, Najafi AH, Burnett MS, Epstein SE (2011) Aging causes collateral rarefaction and increased severity of ischemic injury in multiple tissues. Arterioscler Thromb Vasc Biol 31:1748–1756.
14. Faber JE, Chilian WM, Deindl E, van Royen N, Simons M (2014) A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol 34:1854–1859.
15. Fuentes B, Castillo J, San José B, Leira R, Serena J, Vivancos J, Dávalos A, Nuñez AG, Egido J, Díez-Tejedor E, Díez-Tejedor E (2009) The prognostic value of capillary glucose levels in acute stroke: the GLycemia in Acute Stroke (GLIAS) study. Stroke 40:562–568.
16. Goto Y, Kakizaki M, Masaki N (1976) Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med 119:85–90.
17. Granger DN, Rodrigues SF, Yildirim A, Senchenkova EY (2010) Microvas-cular responses to cardiovascular risk factors. Microcirculation 17:192–205.
18. Grant PJ (2007) Diabetes mellitus as a prothrombotic condition. J Intern Med 262:157–172.
19. Gresele P, Deckmyn H, Huybrechts E, Vermylen J (1984) Serum albumin enhances the impairment of platelet aggregation with thromboxane synthase inhibition by increasing the formation of prostaglandin D2. Biochem Pharmacol 33:2083–2088.
20. Hecht N, He J, Kremenetskaia I, Nieminen M, Vajkoczy P, Woitzik J (2012) Cerebral hemodynamic reserve and vascular remodeling in C57BL/6 mice are influenced by age. Stroke 43:3052–3062.
21. Hill MD, Martin RH, Palesch YY, Tamariz D, Waldman BD, Ryckborst KJ, Moy CS, Barsan WG, Ginsberg MD (2011) The Albumin in Acute Stroke Part 1 Trial: an exploratory efficacy analysis. Stroke 42:1621–1625.
22. Hoi Y, Gao L, Tremmel M, Paluch RA, Siddiqui AH, Meng H, Mocco J (2008) In vivo assessment of rapid cerebrovascular morphological adaptation following acute blood flow increase. J Neurosurg 109:1141–1147.
23. Keaney JF Jr, Simon DI, Stamler JS, Jaraki O, Scharfstein J, Vita JA, Loscalzo J (1993) NO forms an adduct with serum albumin that has endothelium-derived relaxing factor-like properties. J Clin Invest 91:1582–1589.
24. Kumari R, Willing LB, Patel SD, Baskerville KA, Simpson IA (2011) Increased cerebral matrix metalloprotease-9 activity isassociated with compromised recovery in the diabetic db/db mouse following a stroke. J Neurochem 119:1029–1040.
25. Li Q, Atochin D, Kashiwagi S, Earle J, Wang A, Mandeville E, Hayakawa K, d’Uscio LV, Lo EH, Katusic Z, Sessa W, Huang PL (2013) Deficient eNOS phosphorylation is a mechanism for diabetic vascular dysfunction contributing to increased stroke size. Stroke 44:3183–3188.
26. Li W, Prakash R, Kelly-Cobbs AI, Ogbi S, Kozak A, El-Remessy AB, Schreihofer DA, Fagan SC, Ergul A (2010) Adaptive cerebral neovascu-larization in a model of type 2 diabetes: relevance to focal cerebral ischemia. Diabetes 59:228–235.
27. Li Y, Song Y, Zhao L, Gaidosh G, Laties AM, Wen R (2008) Direct labeling and visualization of blood vessels with lipophilic carbocyanine dye DiI. Nat Protoc 3:1703–1708.
28. Liebeskind DS (2003) Collateral circulation. Stroke 34:2279–2284.
29. Liebeskind DS (2013) Trials of endovascular therapies or collaterals? Int J Stroke 8:258–259.
30. Liu J, Wang Y, Akamatsu Y, Lee CC, Stetler RA, Lawton MT, Yang GY (2013) Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog Neurobiol 115:138–156.
31. MacDougall NJ, Muir KW (2011) Hyperglycaemia and infarct size in animal models of middle cerebral artery occlusion: systematic review and meta-analysis. J Cereb Blood Flow Metab 31:807–818.
32. Majid A, He YY, Gidday JM, Kaplan SS, Gonzales ER, Park TS, Fenstermacher JD, Wei L, Choi DW, Hsu CY (2000) Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke 31:2707–2714.
33. Martini SR, Kent TA (2007) Hyperglycemia in acute ischemic stroke: a vascular perspective. J Cereb Blood Flow Metab 27:435–451.
34. Megherbi SE, Milan C, Minier D, Couvreur G, Osseby GV, Tilling K, Di Carlo A, Inzitari D, Wolfe CD, Moreau T, Giroud M (2003) Association between diabetes and stroke subtype on survival and functional outcome 3 months after stroke: data from the European BIOMED Stroke Project. Stroke 34:688–694.
35. Menon BK, Smith EE, Coutts SB, Welsh DG, Faber JE, Goyal M, Hill MD, Demchuk AM, Damani Z, Cho KH, Chang HW, Hong JH, Sohn SI (2013) Leptomeningeal collaterals are associated with modifiable metabolic risk factors. Ann Neurol 74:241–248.
36. Nimmagadda A, Park HP, Prado R, Ginsberg MD (2008) Albumin therapy improves local vascular dynamicsin arat modelofprimary microvascular thrombosis: a two-photon laser-scanning microscopy study. Stroke 39: 198–204.
37. Obrenovitch TP, Hallenbeck JM (1985) Platelet accumulation in regions of low blood flow during the postischemic period. Stroke 16:224–234.
38. Parsons MW, Barber PA, Desmond PM, Baird TA, Darby DG, Byrnes G, Tress BM, Davis SM (2002) Acute hyperglycemia adversely affects stroke out-come:a magnetic resonance imaging and spectroscopy study. Ann Neurol 52:20–28.
39. Porcellati S, Gresele P, Stasi M, Buratta S, Horrocks LA, De Franceschi S, Nenci GG, Goracci G (1995) Albumin prevents TxB, formation from thrombin-stimulated human platelets by sequestering the liberated ara-chidonic acid in the extracellular space. Platelets 6:381–387.
40. Raber J, Fan Y, Matsumori Y, Liu Z, Weinstein PR, Fike JR, Liu J (2004) Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann Neurol 55:381–389.
41. Sangle GV, Zhao R, Mizuno TM, Shen GX (2010) Involvement of RAGE, NADPH oxidase, and Ras/Raf-1 pathway in glycated LDL-induced expression of heat shock factor-1 and plasminogen activator inhibitor-1 in vascular endothelial cells. Endocrinology 151:4455–4466.
42. Santisakultarm TP, Schaffer CB (2011) Optically quantified cerebral blood flow. J Cereb Blood Flow Metab 31:1337–1338.
43. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, Kleinfeld D (2006) Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol 4:e22.
44. Shih AY, Friedman B, Drew PJ, Tsai PS, Lyden PD, Kleinfeld D (2009) Active dilation of penetrating arterioles restores red blood cell flux to penumbral neocortex after focal stroke. J Cereb Blood Flow Metab 29:738–751.
45. Shuaib A, Butcher K, Mohammad AA, Saqqur M, Liebeskind DS (2011) Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurol 10:909–921.
46. Srinivasan VJ, Atochin DN, Radha Krishnan H, Jiang JY, Ruvinskaya S, Wu W, Barry S, Cable AE, Ayata C, Huang PL, Boas DA (2011) Optical coherence tomography for the quantitative study of cerebrovascular physiology. J Cereb Blood Flow Metab 31:1339–1345.
47. Sun C, Sun H, Wu S, Lee CC, Akamatsu Y, Wang RK, Kernie SG, Liu J (2013) Conditional ablation of neuroprogenitor cells in adult mice impedes re-coveryofpoststroke cognitive function and reduces synaptic connectivity in the perforant pathway. J Neurosci 33:17314–17325.
48. Tennant KA, Brown CE (2013) Diabetes augments in vivo microvascular blood flow dynamics after stroke. J Neurosci 33:19194–19204.
49. Thompson SG, Kienast J, Pyke SD, Haverkate F, van de Loo JC (1995) He-mostatic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris: European Concerted Action on Thrombosis and Disabilities Angina Pectoris Study Group. N Engl J Med 332:635–641.
50. Trost S, Pratley R, Sobel B (2006) Impaired fibrinolysis and risk for cardiovascular diseaseinthe metabolic syndrome and type2 diabetes. Curr Diab Rep 6:47–54.
51. Uyttenboogaart M, Koch MW, Stewart RE, Vroomen PC, Luijckx GJ, De Keyser J (2007) Moderate hyperglycaemia is associated with favourable outcomeinacute lacunar stroke. Brain 130:1626–1630.
52. Wahlgren N, Ahmed N, Dávalos A, Hacke W, Millán M, Muir K, Roine RO, Toni D, Lees KR (2008) Thrombolysis with alteplase 3–4.5 h after acute ischaemic stroke (SITS-ISTR): an observational study. Lancet 372:1303–1309.
53. Wang RK, An L (2009) Doppler optical micro-angiography for volumetric imaging of vascular perfusion in vivo. Opt Express 17:8926–8940.
54. Won SJ, Tang XN, Suh SW, Yenari MA, Swanson RA (2011) Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by increasing superoxide production. Ann Neurol 70:583–590.
55. Zhang L, Schallert T, Zhang ZG, Jiang Q, Arniego P, Li Q, Lu M, Chopp M (2002) A test for detecting long-term sensorimotor dysfunction in the mouse after focal cerebral ischemia. J Neurosci Methods 117:207–214.