Characterization of biaxial stretch as an in vitro model of traumatic brain injury to the blood-brain barrier

Molecular Neurobiology

Volumn 55, Issue 1, 2018, Pages 258-266

  Rosas Hernandez, Hector ^a   Cuevas, Elvis ^a   Escudero Lourdes, Claudia ^b   Lantz, Susan M ^a   Gomez Crisostomo, Nancy P ^c   Sturdivant, Nasya M ^d   Balachandran, Kartik ^d   Imam, Syed Z ^a   Slikker, William ^a   Paule, Merle G ^a   Ali, Syed F ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^c Universidad Juarez de Tabasco   (Mexico)

^d University of Arkansas   (United States)

Author keywords

Biaxial stretch; Blood brain barrier; In vitro models; Traumatic brain injury

Indexed keywords

CASPASE 3; CASPASE 7; LACTATE DEHYDROGENASE; PROTEIN S100B; TIGHT JUNCTION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BIAXIAL STRETCH; BIOMECHANICS; BLOOD BRAIN BARRIER; CAPILLARY ENDOTHELIAL CELL; CELL DEATH; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME RELEASE; EXTRAVASATION; HEAD INJURY; IN VITRO STUDY; IN VIVO STUDY; NECROSIS; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; TRAUMATIC BRAIN INJURY; ANIMAL; CAPILLARY PERMEABILITY; DISEASE MODEL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIGHT JUNCTION; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES, TRAUMATIC; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; RATS; RATS, SPRAGUE-DAWLEY; TIGHT JUNCTIONS;

EID: 85028296776     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0738-5     Document Type: Article

References (35)

1. Centers for Disease Control and Prevention (2015) Report to Congress on traumatic brain injury in the United States: Epidemiology and rehabilitatio. National Center for Injury Prevention and Control; Division of UnintentionalInjury Prevention, Atlanta
2. Young LA, Rule GT, Bocchieri RT, Burns JM (2015) Biophysical mechanisms of traumatic brain injuries. Semin Neurol 35(1): 5-11. doi: 10.1055/s-0035-1544242
3. Duckworth JL, Grimes J, Ling GS (2013) Pathophysiology of battlefield associated traumatic brain injury. Pathophysiology 20(1): 23-30. doi: 10.1016/j.pathophys.2012.03.001
4. Pearn ML, Niesman IR, Egawa J, Sawada A, Almenar-Queralt A, Shah SB, Duckworth JL, Head BP (2016) Pathophysiology associated with traumatic brain injury: current treatments and potential novel therapeutics. Cell Mol Neurobiol. doi: 10.1007/s10571-016-0400-1
5. Kabadi SV, Stoica BA, Zimmer DB, Afanador L, Duffy KB, Loane DJ, Faden AI (2015) S100B inhibition reduces behavioral and pathologic changes in experimental traumatic brain injury. J Cereb Blood Flow Metab 35(12): 2010-2020. doi: 10.1038/jcbfm.2015.165
6. Liu M, Zhang C, Liu W, Luo P, Zhang L, Wang Y, Wang Z, Fei Z (2015) A novel rat model of blast-induced traumatic brain injury simulating different damage degree: implications for morphological, neurological, and biomarker changes. Front Cell Neurosci 9: 168. doi: 10.3389/fncel.2015.00168
7. Chow BW, Gu C (2015) The molecular constituents of the bloodbrain barrier. Trends Neurosci 38(10): 598-608. doi: 10.1016/j.tins.2015.08.003
8. Blyth BJ, Farhavar A, Gee C, Hawthorn B, He H, Nayak A, Stocklein V, Bazarian JJ (2009) Validation of serum markers for blood-brain barrier disruption in traumatic brain injury. J Neurotrauma 26(9): 1497-1507. doi: 10.1089/neu.2008-0738
9. Kawoos U, Gu M, Lankasky J, McCarron RM, Chavko M (2016) Effects of exposure to blast overpressure on intracranial pressure and blood-brain barrier permeability in a rat model. PLoS One 11(12): e0167510. doi: 10.1371/journal.pone.0167510
10. LiW, Watts L, Long J, Zhou W, Shen Q, Jiang Z, Li Y, Duong TQ (2016) Spatiotemporal changes in blood-brain barrier permeability, cerebral blood flow, T2 and diffusion following mild traumatic brain injury. Brain Res 1646: 53-61. doi: 10.1016/j.brainres.2016.05.036
11. Mishra V, Skotak M, Schuetz H, Heller A, Haorah J, Chandra N (2016) Primary blast causes mild, moderate, severe and lethal TBI with increasing blast overpressures: experimental rat injury model. Sci Rep 6: 26992. doi: 10.1038/srep26992
12. Shetty AK,Mishra V, Kodali M, Hattiangady B (2014) Blood brain barrier dysfunction and delayed neurological deficits in mild traumatic brain injury induced by blast shock waves. Front Cell Neurosci 8: 232. doi: 10.3389/fncel.2014.00232
13. Wang ZG, Cheng Y, Yu XC, Ye LB, Xia QH, Johnson NR,Wei X, Chen DQ et al (2016) bFGF protects against blood-brain barrier damage through junction protein regulation via PI3K-Akt-Rac1 pathway following traumatic brain injury. Mol Neurobiol 53(10): 7298-7311. doi: 10.1007/s12035-015-9583-6
14. Xu ZM, Yuan F, Liu YL, Ding J, Tian HL (2016) Glibenclamide attenuates blood-brain barrier disruption in adult mice after traumatic brain injury. J Neurotrauma. doi: 10.1089/neu.2016.4491
15. Mychasiuk R, Farran A, Angoa-Perez M, Briggs D, Kuhn D, Esser MJ (2014)A novel model of mild traumatic brain injury for juvenile rats. J Vis Exp (94), e51820. doi: 10.3791/51820
16. Romine J, Gao X, Chen J (2014) Controlled cortical impact model for traumatic brain injury. J Vis Exp 90: e51781. doi: 10.3791/51781
17. Williams AJ, Hartings JA, Lu XC, Rolli ML, Dave JR, Tortella FC (2005) Characterization of a new rat model of penetrating ballistic brain injury. J Neurotrauma 22(2): 313-331. doi: 10.1089/neu.2005.22.313
18. Andrews AM, Lutton EM, Merkel SF, Razmpour R, Ramirez SH (2016) Mechanical injury induces brain endothelial-derived microvesicle release: implications for cerebral vascular injury during traumatic brain injury. Front Cell Neurosci 10: 43. doi: 10.3389/ fncel.2016.00043
19. Salvador E, Neuhaus W, Foerster C (2013) Stretch in brain microvascular endothelial cells (cEND) as an in vitro traumatic brain injury model of the blood brain barrier. J Vis Exp 80: e50928. doi: 10.3791/50928
20. Sturdivant NM, Smith SG, Ali SF, Wolchok JC, Balachandran K (2016) Acetazolamide mitigates astrocyte cellular edema following mild traumatic brain injury. Sci Rep 6: 33330. doi: 10.1038/ srep33330
21. Shear DA, Lu XC, Pedersen R, Wei G, Chen Z, Davis A, Yao C, Dave J et al (2011) Severity profile of penetrating ballistic-like brain injury on neurofunctional outcome, blood-brain barrier permeability, and brain edema formation. J Neurotrauma 28(10): 2185-2195. doi: 10.1089/neu.2011.1916
22. Hue CD, Cho FS, Cao S, Nicholls RE, Vogel Iii EW, Sibindi C, Arancio O, Dale Bass CR et al (2016) Time course and size of blood-brain barrier opening in a mouse model of blast-induced traumatic brain injury. J Neurotrauma 33(13): 1202-1211. doi: 10.1089/neu.2015.4067
23. Li H, Sun J,Wang F, Ding G, ChenW, Fang R, Yao Y, PangMet al (2016) Sodium butyrate exerts neuroprotective effects by restoring the blood-brain barrier in traumatic brain injury mice. Brain Res 1642: 70-78. doi: 10.1016/j.brainres.2016.03.031
24. Salvador E, Burek M, Forster CY (2015) Stretch and/or oxygen glucose deprivation (OGD) in an in vitro traumatic brain injury (TBI) model induces calcium alteration and inflammatory cascade. Front Cell Neurosci 9: 323. doi: 10.3389/fncel.2015.00323
25. Sherman SA, Phillips JK, Costa JT, Cho FS, Oungoulian SR, Finan JD (2016) Stretch injury of human induced pluripotent stem cell derived neurons in a 96 well format. Sci Rep 6: 34097. doi: 10.1038/ srep34097
26. KangWH, Morrison B 3rd (2015) Functional tolerance to mechanical deformation developed from organotypic hippocampal slice cultures. Biomech Model Mechanobiol 14(3): 561-575. doi: 10.1007/s10237-014-0622-4
27. Knutsen AK, Magrath E,McEntee JE, Xing F, Prince JL, Bayly PV, Butman JA, Pham DL (2014) Improved measurement of brain deformation during mild head acceleration using a novel tagged MRI sequence. J Biomech 47(14): 3475-3481. doi: 10.1016/j.jbiomech.2014.09.010
28. Bayly PV, Clayton EH, Genin GM (2012) Quantitative imaging methods for the development and validation of brain biomechanics models. Annu Rev Biomed Eng 14: 369-396. doi: 10.1146/annurevbioeng-071811-150032
29. Rosas-Hernandez H, Cuevas E, Lantz SM, Rice KC, Gannon BM, Fantegrossi WE, Gonzalez C, Paule MG et al (2016) Methamphetamine, 3,4-methylenedioxymethamphetamine (MDMA) and 3,4-methylenedioxypyrovalerone (MDPV) induce differential cytotoxic effects in bovine brain microvessel endothelial cells. Neurosci Lett 629: 125-130. doi: 10.1016/j.neulet.2016.06.029
30. Decker T, Lohmann-Matthes ML (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115(1): 61-69
31. Rayamajhi M, Zhang Y, Miao EA (2013) Detection of pyroptosis by measuring released lactate dehydrogenase activity. Methods Mol Biol 1040: 85-90. doi: 10.1007/978-1-62703-523-1_7
32. Collins NT, Cummins PM, Colgan OC, Ferguson G, Birney YA, Murphy RP, Meade G, Cahill PA (2006) Cyclic strain-mediated regulation of vascular endothelial occludin and ZO-1: influence on intercellular tight junction assembly and function. Arterioscler Thromb Vasc Biol 26(1): 62-68. doi: 10.1161/01.ATV.0000194097.92824.b3
33. Birukova AA, Moldobaeva N, Xing J, Birukov KG (2008) Magnitude-dependent effects of cyclic stretch on HGF- and VEGF-induced pulmonary endothelial remodeling and barrier regulation. AmJ Physiol Lung CellMol Phys 295(4): L612-L623. doi: 10.1152/ajplung.90236.2008
34. Liu XM, Peyton KJ, Durante W (2013) Physiological cyclic strain promotes endothelial cell survival via the induction of heme oxygenase-1. Am J Physiol Heart Circ Physiol 304(12): H1634-H1643. doi: 10.1152/ajpheart.00872.2012
35. SuzukiM, Naruse K, Asano Y, Okamoto T, Nishikimi N, Sakurai T, Nimura Y, Sokabe M (1997) Up-regulation of integrin beta 3 expression by cyclic stretch in human umbilical endothelial cells. Biochem Biophys Res Commun 239(2): 372-376. doi: 10.1006/ bbrc.1997.7364