Top

Published in:

01-06-2014 | Original Article

Smooth Muscle Phenotype Switching in Blast Traumatic Brain Injury-Induced Cerebral Vasospasm

Authors: Eric S. Hald, Patrick W. Alford

Published in: Translational Stroke Research | Issue 3/2014

Abstract

Due to increased survival rates among soldiers exposed to explosive blasts, blast-induced traumatic brain injury (bTBI) has become much more prevalent in recent years. Cerebral vasospasm (CVS) is a common manifestation of brain injury whose incidence is significantly increased in bTBI. CVS is characterized by initial vascular smooth muscle cell (VSMC) hypercontractility, followed by prolonged vessel remodeling and lumen occlusion, and is traditionally associated with subarachnoid hemorrhage (SAH), but recent results suggest that mechanical injury during bTBI can cause mechanotransduced VSMC hypercontractility and phenotype switching necessary for CVS development, even in the absence of SAH. Here, we review the mechanisms by which mechanical stimulation and SAH can synergistically drive CVS progression, complicating treatment options in bTBI patients.

Faul MD, Wald MM, Xu L, Coronado VG. Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths, 2002–2006. Atlanta: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control 2010; 2010.

Armonda RA, Bell RS, Vo AH, Ling G, DeGraba TJ, Crandall B, et al. Wartime traumatic cerebral vasospasm: recent review of combat casualties. Neurosurgery. 2006;59(6):1215–25. doi:10.1227/01.neu.0000249190.46033.94. discussion 25.PubMed

Goldstein LE, Fisher AM, Tagge CA, Zhang XL, Velisek L, Sullivan JA, et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Transl Med. 2012;4(134):134ra60. doi:10.1126/scitranslmed.3003716.PubMedCentralPubMed

Bhattacharjee Y. Shell shock revisited: solving the puzzle of blast trauma. Science. 2008;319:406–8.PubMed

Ling G, Bandak F, Armonda R, Grant G, Ecklund J. Explosive blast neurotrauma. J Neurotrauma. 2009;26(6):815–25. doi:10.1089/neu.2007.0484.PubMed

Borel CO, McKee A, Parra A, Haglund MM, Solan A, Prabhakar V, et al. Possible role for vascular cell proliferation in cerebral vasospasm after subarachnoid hemorrhage. Stroke. 2003;34(2):427–33. doi:10.1161/01.str.0000053848.06436.ab. Editorial comment.

Zhang ZD, Macdonald RL. Contribution of the remodeling response to cerebral vasospasm. Neurol Res. 2006;28(7):713–20. doi:10.1179/016164106X151990.PubMed

Humphrey JD, Baek S, Niklason LE. Biochemomechanics of cerebral vasospasm and its resolution: I. A new hypothesis and theoretical framework. Ann Biomed Eng. 2007;35(9):1485–97. doi:10.1007/s10439-007-9321-y.

Alford PW, Dabiri BE, Goss JA, Hemphill MA, Brigham MD, Parker KK. Blast-induced phenotypic switching in cerebral vasospasm. Proc Natl Acad Sci U S A. 2011;108(31):12705–10. doi:10.1073/pnas.1105860108.

10.

Courtney AC, Courtney MW. A thoracic mechanism of mild traumatic brain injury due to blast pressure waves. Med Hypotheses. 2009;72(1):76–83. doi:10.1016/j.mehy.2008.08.015.PubMed

11.

Long JB, Bentley TL, Wessner KA, Cerone C, Sweeney S, Bauman RA. Blast overpressure in rats: recreating a battlefield injury in the laboratory. J Neurotrauma. 2009;26(6):827–40. doi:10.1089/neu.2008.0748.PubMed

12.

Bauman RA, Ling G, Tong L, Januszkiewicz A, Agoston D, Delanerolle N, et al. An introductory characterization of a combat-casualty-care relevant swine model of closed head injury resulting from exposure to explosive blast. J Neurotrauma. 2009;26(6):841–60. doi:10.1089/neu.2009-0898.PubMed

13.

Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci. 2011;12(12):723–38. doi:10.1038/nrn3114.PubMed

14.

Geddes DM, Cargill RS 2nd, LaPlaca MC. Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J Neurotrauma. 2003;20(10):1039–49. doi:10.1089/089771503770195885.

15.

Kilinc D, Gallo G, Barbee KA. Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage. Exp Neurol. 2008;212(2):422–30. doi:10.1016/j.expneurol.2008.04.025.PubMed

16.

Pettus EH, Christman CW, Giebel ML, Povlishock JT. Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J Neurotrauma. 1994;11(5):507–22.PubMed

17.

Hemphill MA, Dabiri BE, Gabriele S, Kerscher L, Franck C, Goss JA, et al. A possible role for integrin signaling in diffuse axonal injury. PLoS One. 2011;6(7):e22899. doi:10.1371/journal.pone.0022899.PubMedCentralPubMed

18.

Yeoh S, Bell ED, Monson KL. Distribution of blood–brain barrier disruption in primary blast injury. Ann Biomed Eng. 2013;41(10):2206–14. doi:10.1007/s10439-013-0805-7.PubMed

19.

Chen Y, Huang W, Constantini S. Blast shock wave mitigation using the hydraulic energy redirection and release technology. PLoS One. 2012;7(6):e39353. doi:10.1371/journal.pone.0039353.PubMedCentralPubMed

20.

Kuehn R, Simard PF, Driscoll I, Keledjian K, Ivanova S, Tosun C, et al. Rodent model of direct cranial blast injury. J Neurotrauma. 2011;28(10):2155–69. doi:10.1089/neu.2010.1532.PubMed

21.

Garman RH, Jenkins LW, Switzer RC 3rd, Bauman RA, Tong LC, Swauger PV, et al. Blast exposure in rats with body shielding is characterized primarily by diffuse axonal injury. J Neurotrauma. 2011;28(6):947–59. doi:10.1089/neu.2010.1540.

22.

Readnower RD, Chavko M, Adeeb S, Conroy MD, Pauly JR, McCarron RM, et al. Increase in blood–brain barrier permeability, oxidative stress, and activated microglia in a rat model of blast-induced traumatic brain injury. J Neurosci Res. 2010;88(16):3530–9. doi:10.1002/jnr.22510.PubMedCentralPubMed

23.

Hue CD, Cao S, Haider SF, Vo KV, Effgen GB, Vogel E 3rd, et al. Blood–brain barrier dysfunction after primary blast injury in vitro. J Neurotrauma. 2013;30(19):1652–63. doi:10.1089/neu.2012.2773.

24.

Murakami K, Koide M, Dumont TM, Russell SR, Tranmer BI, Wellman GC. Subarachnoid hemorrhage induces gliosis and increased expression of the pro-inflammatory cytokine high mobility group box 1 protein. Transl Stroke Res. 2011;2(1):72–9. doi:10.1007/s12975-010-0052-2.PubMedCentralPubMed

25.

Harrison P, Cramer EM. Platelet alpha-granules. Blood Rev. 1993;7(1):52–62.PubMed

26.

Keilin D, Hartree EF. Reaction of nitric oxide with haemoglobin and methaemoglobin. Nature. 1937;139:548.

27.

Gow J, Stamler J. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature. 1998;391:169–73.PubMed

28.

Gladwin MT, Lancaster JR Jr, Freeman BA, Schechter AN. Nitric oxide's reactions with hemoglobin: a view through the SNO-storm. Nat Med. 2003;9(5):496–500. doi:10.1038/nm0503-496.

29.

Shimokawa H, Ito A, Fukumoto Y, Kadokami T, Nakaike R, Sakata M, et al. Chronic treatment with interleukin-1 beta induces coronary intimal lesions and vasospastic responses in pigs in vivo. The role of platelet-derived growth factor. J Clin Investig. 1996;97(3):769–76. doi:10.1172/JCI118476.PubMedCentralPubMed

30.

Dietrich HH, Dacey RG Jr. Molecular keys to the problems of cerebral vasospasm. Neurosurgery. 2000;46(3):517–30.

31.

Dumont AS, Dumont RJ, Chow MM, Lin CL, Calisaneller T, Ley KF, et al. Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery. 2003;53(1):123–33. discussion 33–5.PubMed

32.

Grasso G. An overview of new pharmacological treatments for cerebrovascular dysfunction after experimental subarachnoid hemorrhage. Brain Res Brain Res Rev. 2004;44(1):49–63.PubMed

33.

Boron WF, Boulpaep EL. Medical physiology: a cellular and molecular approach. 1st ed. Philadelphia: W.B. Saunders; 2003.

34.

Balabanov R, Goldman H, Murphy S, Pellizon G, Owen C, Rafols J, et al. Endothelial cell activation following moderate traumatic brain injury. Neurol Res. 2001;23(2–3):175–82.PubMed

35.

Clower BR, Yamamoto Y, Cain L, Haines DE, Smith RR. Endothelial injury following experimental subarachnoid hemorrhage in rats: effects on brain blood flow. Anat Rec. 1994;240(1):104–14. doi:10.1002/ar.1092400110.PubMed

36.

Bohm F, Pernow J. The importance of endothelin-1 for vascular dysfunction in cardiovascular disease. Cardiovasc Res. 2007;76(1):8–18. doi:10.1016/j.cardiores.2007.06.004.PubMed

37.

Zimmermann M, Seifert V. Endothelin and subarachnoid hemorrhage: an overview. Neurosurgery. 1998;43(4):863–75. discussion 75–6.PubMed

38.

Vatter H, Konczalla J, Seifert V. Endothelin related pathophysiology in cerebral vasospasm: what happens to the cerebral vessels? Acta Neurochir Suppl. 2011;110(Pt 1):177–80. doi:10.1007/978-3-7091-0353-1_31.PubMed

39.

Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75(3):487–517.PubMed

40.

Iyemere VP, Proudfoot D, Weissberg PL, Shanahan CM. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J Intern Med. 2006;260(3):192–210. doi:10.1111/j.1365-2796.2006.01692.x.PubMed

41.

Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Plant Physiol Plant Mol Biol. 2012;74:13–40. doi:10.1146/annurev-physiol-012110-142315.

42.

Stegemann JP, Hong H, Nerem RM. Mechanical, biochemical, and extracellular matrix effects on vascular smooth muscle cell phenotype. J Appl Physiol. 2005;98(6):2321–7. doi:10.1152/japplphysiol.01114.2004.PubMed

43.

Chesler NC, Ku DN, Galis ZS. Transmural pressure induces matrix-degrading activity in porcine arteries ex vivo. Am J Physiol. 1999;277(5 Pt 2):H2002–9.PubMed

44.

Zabramski JM. Vasospasm after subarachnoid hemorrhage. In: Bederson JB, editor. Subarachnoid hemorrhage: pathophysiology and management. Park Ridge: The American Association of Neurological Surgeons; 1997. p. 127–56.

45.

Macdonald RL. Pathophysiology and molecular genetics of vasospasm. Acta Neurochir Supplement. 2001;77:7–11.

46.

Mayberg MR, Okada T, Bark DH. The significance of morphological changes in cerebral arteries after subarachnoid hemorrhage. J Neurosurg. 1990;72(4):626–33. doi:10.3171/jns.1990.72.4.0626.PubMed

47.

McGirt MJ, Lynch JR, Blessing R, Warner DS, Friedman AH, Laskowitz DT. Serum von Willebrand factor, matrix metalloproteinase-9, and vascular endothelial growth factor levels predict the onset of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2002;51(5):1128–34. discussion 34–5.PubMed

48.

Pluta RM. Delayed cerebral vasospasm and nitric oxide: review, new hypothesis, and proposed treatment. Pharmacol Ther. 2005;105(1):23–56. doi:10.1016/j.pharmthera.2004.10.002.PubMed

49.

Zhang B, Fugleholm K, Day LB, Ye S, Weller RO, Day IN. Molecular pathogenesis of subarachnoid haemorrhage. Intern J Biochem Cell Biol. 2003;35(9):1341–60.

50.

Liu SQ, Fung YC. Zero-stress states of arteries. J Biomech Eng. 1988;110(1):82–4.PubMed

51.

Armentano R, Simon A, Levenson J, Chau NP, Megnien JL, Pichel R. Mechanical pressure versus intrinsic effects of hypertension on large arteries in humans. Hypertension. 1991;18(5):657–64.PubMed

52.

Intengan HD, Schiffrin EL. Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension. 2001;38(3 Pt 2):581–7.PubMed

53.

Fung YC, Liu SQ. Changes of zero-stress state of rat pulmonary arteries in hypoxic hypertension. J Appl Physiol. 1991;70(6):2455–70.PubMed

54.

Fung YC, Liu SQ. Change of residual strains in arteries due to hypertrophy caused by aortic constriction. Circ Res. 1989;65(5):1340–9.PubMed

55.

Alford PW, Humphrey JD, Taber La. Growth and remodeling in a thick-walled artery model: effects of spatial variations in wall constituents. Biomech Model Mechanobiol. 2008;7(4):245–62. doi:10.1007/s10237-007-0101-2.

56.

Alford PW, Taber LA. Computational study of growth and remodelling in the aortic arch. Comput Method Biomech Biomed Engin. 2008;11(5):525–38. doi:10.1080/10255840801930710.

57.

Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84(3):767–801. doi:10.1152/physrev.00041.2003.PubMed

58.

Kawai-Kowase K, Owens GK. Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol. 2007;292(1):C59–69. doi:10.1152/ajpcell.00394.2006.PubMed

59.

Chow N, Bell RD, Deane R, Streb JW, Chen J, Brooks A, et al. Serum response factor and myocardin mediate arterial hypercontractility and cerebral blood flow dysregulation in Alzheimer's phenotype. Proc Natl Acad Sci U S A. 2007;104(3):823–8. doi:10.1073/pnas.0608251104.PubMedCentralPubMed

60.

Li S, Lao J, Chen BP, Li YS, Zhao Y, Chu J, et al. Genomic analysis of smooth muscle cells in 3-dimensional collagen matrix. FASEB J. 2003;17(1):97–9. doi:10.1096/fj.02-0256fje.PubMed

61.

Schulze PC, de Keulenaer GW, Kassik KA, Takahashi T, Chen Z, Simon DI, et al. Biomechanically induced gene iex-1 inhibits vascular smooth muscle cell proliferation and neointima formation. Circ Res. 2003;93(12):1210–7. doi:10.1161/01.RES.0000103635.38096.2F.PubMed

62.

Chapman GB, Durante W, Hellums JD, Schafer AI. Physiological cyclic stretch causes cell cycle arrest in cultured vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2000;278(3):H748–54.PubMed

63.

Kim BS, Nikolovski J, Bonadio J, Mooney DJ. Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat Biotechnol. 1999;17(10):979–83. doi:10.1038/13671.PubMed

64.

Williams B. Mechanical influences on vascular smooth muscle cell function. J Hypertens. 1998;16(12 Pt 2):1921–9.PubMed

65.

McDaniel DP, Shaw GA, Elliott JT, Bhadriraju K, Meuse C, Chung KH, et al. The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype. Biophys J. 2007;92(5):1759–69. doi:10.1529/biophysj.106.089003.PubMedCentralPubMed

66.

Sazonova OV, Lee KL, Isenberg BC, Rich CB, Nugent MA, Wong JY. Cell–cell interactions mediate the response of vascular smooth muscle cells to substrate stiffness. Biophys J. 2011;101(3):622–30. doi:10.1016/j.bpj.2011.06.051.PubMedCentralPubMed

67.

Alford PW, Nesmith AP, Seywerd JN, Grosberg A, Parker KK. Vascular smooth muscle contractility depends on cell shape. Integr Biol (Camb). 2011;3(11):1063–70. doi:10.1039/c1ib00061f.

68.

Peyton SR, Putnam AJ. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol. 2005;204(1):198–209. doi:10.1002/jcp.20274.PubMed

69.

Masel BE, Bell RS, Brossart S, Grill RJ, Hayes RL, Levin HS, et al. Galveston brain injury conference 2010: clinical and experimental aspects of blast injury. J Neurotrauma. 2012;29(12):2143–71. doi:10.1089/neu.2011.2258.PubMed

70.

DeWitt DS, Prough DS. Blast-induced brain injury and posttraumatic hypotension and hypoxemia. J Neurotrauma. 2009;26(6):877–87. doi:10.1089/neu.2007.0439.PubMed

71.

Liu G, Wang H, Ou D, Huang H, Liao D. Endothelin-1, an important mitogen of smooth muscle cells of spontaneously hypertensive rats. Chin Med J. 2002;115(5):750–2.PubMed

72.

Chambers RC, Leoni P, Kaminski N, Laurent GJ, Heller RA. Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am J Pathol. 2003;162(2):533–46.PubMedCentralPubMed

73.

Jain MK, Fujita KP, Hsieh CM, Endege WO, Sibinga NE, Yet SF, et al. Molecular cloning and characterization of SmLIM, a developmentally regulated LIM protein preferentially expressed in aortic smooth muscle cells. J Biol Chem. 1996;271(17):10194–9.PubMed

74.

Lin DW, Chang IC, Tseng A, Wu ML, Chen CH, Patenaude CA, et al. Transforming growth factor beta up-regulates cysteine-rich protein 2 in vascular smooth muscle cells via activating transcription factor 2. J Biol Chem. 2008;283(22):15003–14. doi:10.1074/jbc.M801621200.PubMedCentralPubMed

75.

Wu YC, Cui L, Li G, Yin S, Gao YJ, Cao YL. [PDGF-BB initiates vascular smooth muscle-like phenotype differentiation of human bone marrow mesenchymal stem cells in vitro]. Zhonghua zheng xing wai ke za zhi Zhonghua zhengxing waike zazhi (Chin J Plast Surg). 2007;23(4):335–9.

76.

Holycross BJ, Blank RS, Thompson MM, Peach MJ, Owens GK. Platelet-derived growth factor-BB-induced suppression of smooth muscle cell differentiation. Circ Res. 1992;71(6):1525–32.PubMed

77.

Li X, Van Putten V, Zarinetchi F, Nicks ME, Thaler S, Heasley LE, et al. Suppression of smooth-muscle alpha-actin expression by platelet-derived growth factor in vascular smooth-muscle cells involves Ras and cytosolic phospholipase A2. Biochem J. 1997;327(Pt 3):709–16.PubMedCentralPubMed

78.

Lehti K, Rose NF, Valavaara S, Weiss SJ, Keski-Oja J. MT1-MMP promotes vascular smooth muscle dedifferentiation through LRP1 processing. J Cell Sci. 2009;122(Pt 1):126–35. doi:10.1242/jcs.035279.PubMed

79.

Song JN, Yan WT, An JY, Hao GS, Guo XY, Zhang M, et al. Potential contribution of SOCC to cerebral vasospasm after experimental subarachnoid hemorrhage in rats. Brain Res. 2013;1517:93–103. doi:10.1016/j.brainres.2013.01.004.PubMed

80.

Berra-Romani R, Mazzocco-Spezzia A, Pulina MV, Golovina VA. Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol. 2008;295(3):C779–90. doi:10.1152/ajpcell.00173.2008.PubMedCentralPubMed

81.

House SJ, Potier M, Bisaillon J, Singer HA, Trebak M. The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflugers Archiv: Eur J Physiol. 2008;456(5):769–85. doi:10.1007/s00424-008-0491-8.

82.

Hubbell MC, Semotiuk AJ, Thorpe RB, Adeoye OO, Butler SM, Williams JM, et al. Chronic hypoxia and VEGF differentially modulate abundance and organization of myosin heavy chain isoforms in fetal and adult ovine arteries. Am J Physiol Cell Physiol. 2012;303(10):C1090–103. doi:10.1152/ajpcell.00408.2011.PubMedCentralPubMed

83.

Adeoye OO, Butler SM, Hubbell MC, Semotiuk A, Williams JM, Pearce WJ. Contribution of increased VEGF receptors to hypoxic changes in fetal ovine carotid artery contractile proteins. Am J Physiol Cell Physiol. 2013;304(7):C656–65. doi:10.1152/ajpcell.00110.2012.PubMedCentralPubMed

84.

MacDonald RL, Weir, B. Cerebral Vasospasm. Academic Press; 2001.

85.

Sugawara T, Ayer R, Jadhav V, Chen W, Tsubokawa T, Zhang JH. Mechanisms of statin treatment in cerebral vasospasm. Acta Neurochir Suppl. 2011;110(Pt 2):9–11. doi:10.1007/978-3-7091-0356-2_2.PubMed

86.

Satoh S, Takayasu M, Kawasaki K, Ikegaki I, Hitomi A, Yano K, et al. Antivasospastic effects of hydroxyfasudil, a Rho-kinase inhibitor, after subarachnoid hemorrhage. J Pharmacol Sci. 2012;118(1):92–8.PubMed

87.

Naraoka M, Munakata A, Matsuda N, Shimamura N, Ohkuma H. Suppression of the Rho/Rho-kinase pathway and prevention of cerebral vasospasm by combination treatment with statin and fasudil after subarachnoid hemorrhage in rabbit. Transl Stroke Res. 2013;4(3):368–74. doi:10.1007/s12975-012-0247-9.PubMedCentralPubMed

88.

Amenta F, Lanari A, Mignini F, Silvestrelli G, Traini E, Tomassoni D. Nicardipine use in cerebrovascular disease: a review of controlled clinical studies. J Neurol Sci. 2009;283(1–2):219–23. doi:10.1016/j.jns.2009.02.335.PubMed

89.

Inzitari D, Poggesi A. Calcium channel blockers and stroke. Aging Clin Exp Res. 2005;17(4 Suppl):16–30.PubMed

90.

Mesis RG, Wang H, Lombard FW, Yates R, Vitek MP, Borel CO, et al. Dissociation between vasospasm and functional improvement in a murine model of subarachnoid hemorrhage. Neurosurg Focus. 2006;21(3):E4.PubMed

91.

Zhang Z, Mondello S, Kobeissy F, Rubenstein R, Streeter J, Hayes RL, et al. Protein biomarkers for traumatic and ischemic brain injury: from bench to bedside. Transl Stroke Res. 2011;2:455–62.PubMed

92.

North SH, Shriver-Lake LC, Taitt CR, Ligler FS. Rapid analytical methods for on-site triage for traumatic brain injury. Annu Rev Anal Chem (Palo Alto, CA). 2012;5:35–56. doi:10.1146/annurev-anchem-062011-143105.

93.

Ogawa T, Hanggi D, Wu Y, Michiue H, Tomizawa K, Ono S, et al. Protein therapy using heme-oxygenase-1 fused to a polyarginine transduction domain attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2011;31(11):2231–42. doi:10.1038/jcbfm.2011.87.PubMedCentralPubMed

94.

Ram Z, Sadeh M, Shacked I, Sahar A, Hadani M. Magnesium sulfate reverses experimental delayed cerebral vasospasm after subarachnoid hemorrhage in rats. Stroke. 1991;22(7):922–7.PubMed

95.

Huang B, Khatibi NH, Tong L, Yan P, Xie P, Zhang JH. Magnesium sulfate treatment improves outcome in patients with subarachnoid hemorrhage: a meta-analysis study. Transl Stroke Res. 2010;1(2):108–12. doi:10.1007/s12975-010-0022-8.PubMedCentralPubMed

96.

MacDonald RL, Kakarieka A, Mayer SA, Pasqualin A, Ruefenacht D, Schmiedek P, et al. Prevention of cerebral vasospasm after aneurysmal subarachnoid hemorrhage with clazosentan, an endothelin receptor antagonist. Neurosurgery. 2006;59(2):453.

97.

Macdonald RL. Clazosentan: an endothelin receptor antagonist for treatment of vasospasm after subarachnoid hemorrhage. Expert Opin Investig Drug. 2008;17(11):1761–7. doi:10.1517/13543784.17.11.1761.

98.

Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol. 2011;10(7):618–25. doi:10.1016/S1474-4422(11)70108-9.PubMed

99.

Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Randomized trial of clazosentan in patients with aneurysmal subarachnoid hemorrhage undergoing endovascular coiling. Stroke. 2012;43(6):1463–9. doi:10.1161/STROKEAHA.111.648980.PubMed

100.

Yamaguchi-Okada M, Nishizawa S, Mizutani A, Namba H. Multifaceted effects of selective inhibitor of phosphodiesterase III, cilostazol, for cerebral vasospasm after subarachnoid hemorrhage in a dog model. Cerebrovasc Dis. 2009;28(2):135–42. doi:10.1159/000223439.PubMed

101.

Ostrowski RP, Zhang JH. Hyperbaric oxygen for cerebral vasospasm and brain injury following subarachnoid hemorrhage. Transl Stroke Res. 2011;2(3):316–27. doi:10.1007/s12975-011-0069-1.PubMedCentralPubMed

102.

Soejima Y, Hu Q, Krafft PR, Fujii M, Tang J, Zhang JH. Hyperbaric oxygen preconditioning attenuates hyperglycemia-enhanced hemorrhagic transformation by inhibiting matrix metalloproteinases in focal cerebral ischemia in rats. Exp Neurol. 2013;247:737–43. doi:10.1016/j.expneurol.2013.03.019.PubMed

103.

Monson KL, Matsumoto MM, Young WL, Manley GT, Hashimoto T. Abrupt increase in rat carotid blood flow induces rapid alteration of artery mechanical properties. J Mech Behav Biomed Mater. 2011;4(1):9–15. doi:10.1016/j.jmbbm.2010.08.003.PubMedCentralPubMed

104.

Jackson ZS, Gotlieb AI, Langille BL. Wall tissue remodeling regulates longitudinal tension in arteries. Circ Res. 2002;90(8):918–25.PubMed

105.

Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2011;31(6):1443–51. doi:10.1038/jcbfm.2011.7.PubMedCentralPubMed

106.

Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain: J Neurol. 2009;132(Pt 7):1866–81. doi:10.1093/brain/awp102.

107.

Vergouwen MD, Etminan N, Ilodigwe D, Macdonald RL. Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2011;31(7):1545–53. doi:10.1038/jcbfm.2011.56.PubMedCentralPubMed

108.

Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42(4):924–9. doi:10.1161/STROKEAHA.110.597914.PubMed

109.

Cernak I, Savic J, Malicevic Z, Zunic G, Djurdjevic D, Prokic V. The pathogenesis of pulmonary blast injury: our point of view. Chinese J Traumatol. 1996;12:28–31.

110.

Cernak I, Malicevik Z, Prokic V, Zunic G, Djurdjevic D, Ilic S, et al. Indirect neurotrauma caused by pulmonary blast injury: development and prognosis. Int Rev Armed Forces Med Serv. 1997;52:114–20.

111.

Cernak I, Wang Z, Jiang J, Bian X, Savic J. Ultrastructural and functional characteristics of blast injury-induced neurotrauma. J Trauma. 2001;50(4):695–706.PubMed

112.

Cernak I, Ignjatovic D, Andelic G, Savic J. Metabolic changes as part of the general response of the body to the effect of blast waves. Vojnosanitetski Pregled Mil (Med Pharm Rev). 1991;48(6):515–22.

Title: Smooth Muscle Phenotype Switching in Blast Traumatic Brain Injury-Induced Cerebral Vasospasm
Authors: Eric S. Hald
Patrick W. Alford
Publication date: 01-06-2014
Publisher: Springer US
Published in: Translational Stroke Research / Issue 3/2014
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI: https://doi.org/10.1007/s12975-013-0300-3

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Smooth Muscle Phenotype Switching in Blast Traumatic Brain Injury-Induced Cerebral Vasospasm

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2014

Brain Arteriovenous Malformation Modeling, Pathogenesis, and Novel Therapeutic Targets

Plasticity of Cerebrovascular Smooth Muscle Cells After Subarachnoid Hemorrhage

Catheter Placement for Lysis of Spontaneous Intracerebral Hematomas: Is a Navigated Stylet Better Than Pointer-Guided Frameless Stereotaxy for Intrahematomal Catheter Positioning?

Smooth Muscle Cells and the Formation, Degeneration, and Rupture of Saccular Intracranial Aneurysm Wall—a Review of Current Pathophysiological Knowledge

Smooth Muscle Cell Phenotypic Switching in Stroke

Vascular Neural Network Phenotypic Transformation After Traumatic Injury: Potential Role in Long-Term Sequelae