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Basic Science

Chronic cerebrovascular abnormalities in a mouse model of repetitive mild traumatic brain injury

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Pages 1414-1427 | Received 01 Mar 2016, Accepted 26 Jul 2016, Published online: 11 Nov 2016

References

  • Goldstein LE, Fisher AM, Tagge CA, Zhang XL, Velisek L, Sullivan JA, Upreti C, Kracht JM, Ericsson M, Wojnarowicz MW, et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Science Translational Medicine 2012;4: 134ra60.
  • McKee AC, Daneshvar DH, Alvarez VE, Stein TD. The neuropathology of sport. Acta Neuropathologica 2014;127:29–51.
  • Millspaugh JA. Dementia pugilistica. US Naval Medicine Bulletin 1937;35:261–297.
  • Omalu BI, DeKosky ST, Hamilton RL, Minster RL, Kamboh MI, Shakir AM, Wecht CH. Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery 2006;59:1086–1092; discussion 1092–1093.
  • Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL, Wecht CH. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005;57:128–134; discussion 128–134.
  • McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, Lee HS, Wojtowicz SM, Hall G, Baugh CM, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013;136:43–64.
  • Gardner A, Iverson GL, McCrory P. Chronic traumatic encephalopathy in sport: a systematic review. British Journal of Sports Medicine 2014;48:84–90.
  • Hazrati LN, Tartaglia MC, Diamandis P, Davis KD, Green RE, Wennberg R, Wong JC, Ezerins L, Tator CH. Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Frontiers in Human Neuroscience 2013;7:222.
  • Ojo JO, Mouzon BC, Crawford F. Repetitive head trauma, chronic traumatic encephalopathy and tau: Challenges in translating from mice to men. Experimental Neurology 2016;275:389–404.
  • Kenney K, Amyot F, Haber M, Pronger A, Bogoslovsky T, Moore C, Diaz-Arrastia R. Cerebral vascular injury in traumatic brain injury. Experimental Neurology 2015;87:95–110.
  • Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron 2015;87:95–110.
  • Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, Zlokovic BV. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nature Communication 2013;4:2932.
  • Castejon OJ. Ultrastructural pathology of cortical capillary pericytes in human traumatic brain oedema. Folia Neuropathologica 2011;49:162–173.
  • Castejon OJ. Ultrastructural alterations of human cortical capillary basement membrane in human brain oedema. Folia Neuropathologica 2014;52:10–21.
  • Ostergaard L, Engedal TS, Aamand R, Mikkelsen R, Iversen NK, Anzabi M, Naess-Schmidt ET, Drasbek KR, Bay V, Blicher JU, et al.: All authors needed Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury. Journal of Cerebral Blood Flow Metabolism 2014;34:1585–1598.
  • Berger RP, Adelson PD, Pierce MC, Dulani T, Cassidy LD, Kochanek PM. Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. Journal of Neurosurgery 2005;10312 Suppl):61–68.
  • Gardner RC, Burke JF, Nettiksimmons J, Goldman S, Tanner CM, Yaffe K. Traumatic brain injury in later life increases risk for Parkinson disease. Annals of Neurology 2015;77:987–995.
  • Gardner RC, Yaffe K. Epidemiology of mild traumatic brain injury and neurodegenerative disease. Molecular and Cellular Neuroscience 2015;66B:75–80.
  • Plassman BL, Havlik RJ, Steffens DC, Helms MJ, Newman TN, Drosdick D, Phillips C, Gau BA, Welsh-Bohmer KA, Burke JR, et al. Documented head injury in early adulthood and risk of Alzheimer’s disease and other dementias. Neurology 2000;55:1158–1166.
  • Schofield PW, Logroscino G, Andrews HF, Albert S, Stern Y. An association between head circumference and Alzheimer’s disease in a population-based study of aging and dementia. Neurology 1997;49:30–37.
  • Ruitenberg A, den Heijer T, Bakker SL, van Swieten JC, Koudstaal PJ, Hofman A, Breteler MM. Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Annals of Neurology 2005;57:789–794.
  • Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 1997;277:813–817.
  • Hirao K, Ohnishi T, Hirata Y, Yamashita F, Mori T, Moriguchi Y, Matsuda H, Nemoto K, Imabayashi E, Yamada M, et al. The prediction of rapid conversion to Alzheimer’s disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 2005;28:1014–1021.
  • Ahn MJ, Sherwood ER, Prough DS, Lin CY, DeWitt DS. The effects of traumatic brain injury on cerebral blood flow and brain tissue nitric oxide levels and cytokine expression. Journal of Neurotrauma 2004;21:1431–1442.
  • Mouzon B, Chaytow H, Crynen G, Bachmeier C, Stewart J, Mullan M, Stewart W, Crawford F. Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. Journal of Neurotrauma 2012;29:2761–2773.
  • Mouzon BC, Bachmeier C, Ferro A, Ojo JO, Crynen G, Acker CM, Davies P, Mullan M, Stewart W, Crawford F. Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Annals of Neurology 2014;75:241–254.
  • Paris D, Quadros A, Humphrey J, Patel N, Crescentini R, Crawford F, Mullan M. Nilvadipine antagonizes both Abeta vasoactivity in isolated arteries, and the reduced cerebral blood flow in APPsw transgenic mice. Brain Research 2004;999:53–61.
  • Halfter W, Dong S, Schurer B, Osanger A, Schneider W, Ruegg M, Cole GJ. Composition, synthesis, and assembly of the embryonic chick retinal basal lamina. Developmental Biology 2000;220:111–128.
  • Len TK, Neary JP, Asmundson GJ, Goodman DG, Bjornson B, Bhambhani YN. Cerebrovascular reactivity impairment after sport-induced concussion. Medical Science and Sports Exercise 2011;43:2241–2248.
  • Yezhuvath US, Lewis-Amezcua K, Varghese R, Xiao G, Lu H. On the assessment of cerebrovascular reactivity using hypercapnia BOLD MRI. NMR Biomedicine 2009;22:779–786.
  • Ponto LL, Brashers-Krug TM, Pierson RK, Menda Y, Acion L, Watkins GL, Sunderland JJ, Koeppel JA, Jorge RE. Preliminary investigation of cerebral blood flow and amyloid burden in Veterans with and without combat-related traumatic brain injury. Journal of Neuropsychiatry and Clinical Neurosciences 2016;28:89–96.
  • Amen DG, Willeumier K, Omalu B, Newberg A, Raghavendra C, Raji CA. Perfusion neuroimaging abnormalities alone distinguish national football league players from a healthy population. Journal of Alzheimers Disease 2016;53:237–241.
  • Searcy JL, Le Bihan T, Salvadores N, McCulloch J, Horsburgh K. Impact of age on the cerebrovascular proteomes of wild-type and Tg-SwDI mice. PLoS One 2014;9:e89970.
  • Xiong Y, Mahmood A, Chopp M. Angiogenesis, neurogenesis and brain recovery of function following injury. Current Opinion in Investigative Drugs 2010;11:298–308.
  • Prakash R, Carmichael ST. Blood-brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury. Current Opinions in Neurology 2015;28:556–564.
  • Hayward NM, Tuunanen PI, Immonen R, Ndode-Ekane XE, Pitkanen A, Grohn O. Magnetic resonance imaging of regional hemodynamic and cerebrovascular recovery after lateral fluid-percussion brain injury in rats. Journal of Cerebral Blood Flow Metabolism 2011;31:166–177.
  • Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010;68:409–427.
  • Dore-Duffy P, Wang S, Mehedi A, Katyshev V, Cleary K, Tapper A, Reynolds C, Ding Y, Zhan P, Rafols J, et al. Pericyte-mediated vasoconstriction underlies TBI-induced hypoperfusion. Neurological Research 2011;33:176–186.
  • Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 2010;107:22290–22295.
  • Hall CN, Reynell C, Gesslein B, Hamilton NB, Mishra A, Sutherland BA, O’Farrell FM, Buchan AM, Lauritzen M, Attwell D. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014;508:55–60.
  • Kornfield TE, Newman EA. Regulation of blood flow in the retinal trilaminar vascular network. Journal of Neuroscience 2014;34:11504–11513.
  • O’Farrell FM, Attwell D. A role for pericytes in coronary no-reflow. Nature Reviews: Cardiology 2014;11:427–432.
  • Peppiatt CM, Howarth C, Mobbs P, Attwell D. Bidirectional control of CNS capillary diameter by pericytes. Nature 2006;443:700–704.
  • Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nature Medicine 2009;15:1031–1037.
  • Yamin R, Morgan KG. Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell. Journa of Physiology 2012;590:4145–4154.
  • Chow N, Bell RD, Deane R, Streb JW, Chen J, Brooks A, Van Nostrand W, Miano JM, Zlokovic BV. Serum response factor and myocardin mediate arterial hypercontractility and cerebral blood flow dysregulation in Alzheimer’s phenotype. Proceedings of the National Academy of Sciences (USA) 2007;104:823–828.
  • Merlini M, Wanner D, Nitsch RM. Tau pathology-dependent remodelling of cerebral arteries precedes Alzheimer’s disease-related microvascular cerebral amyloid angiopathy. Acta Neuropathologica 2016;131:737–752.
  • Chaigneau E, Oheim M, Audinat E, Charpak S. Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proceedings of the National Academy of Sciences (USA) 2003;100:13081–13086.
  • Armstead WM, Bohman LE, Riley J, Yarovoi S, Higazi AA, Cines DB. tPA-S(481)A prevents impairment of cerebrovascular autoregulation by endogenous tPA after traumatic brain injury by upregulating p38 MAPK and inhibiting ET-1. Journal of Neurotrauma 2013;30:1898–1907.
  • Petrov T. Amelioration of hypoperfusion after traumatic brain injury by in vivo endothelin-1 knockout. Canadian Journal of Physiology and Pharmacology 2009;87:379–386.
  • Salonia R, Empey PE, Poloyac SM, Wisniewski SR, Klamerus M, Ozawa H, Wagner AK, Ruppel R, Bell MJ, Feldman K, et al.. Endothelin-1 is increased in cerebrospinal fluid and associated with unfavorable outcomes in children after severe traumatic brain injury. Journal of Neurotrauma 2010;27:1819–1825.
  • DeGracia DJ, Kreipke CW, Kayali FM, Rafols JA. Brain endothelial HSP-70 stress response coincides with endothelial and pericyte death after brain trauma. Neurological Research 2007;29:356–361.
  • Torres-Platas SG, Comeau S, Rachalski A, Bo GD, Cruceanu C, Turecki G, Giros B, Mechawar N. Morphometric characterization of microglial phenotypes in human cerebral cortex. Journal of Neuroinflammation 2014;11:12.
  • Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiology of Disease 2010;37:13–25.
  • Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood–brain barrier. Nature Medicine 2013;19:1584–1596.
  • Abdul-Muneer PM, Schuetz H, Wang F, Skotak M, Jones J, Gorantla S, Zimmerman MC, Chandra N, Haorah J. Induction of oxidative and nitrosative damage leads to cerebrovascular inflammation in an animal model of mild traumatic brain injury induced by primary blast. Free Radical Biology and Medicine 2013;60:282–291.

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