Microparticles impair hypotensive cerebrovasodilation and cause hippocampal neuronal cell injury after traumatic brain injury

Journal of Neurotrauma

Volumn 33, Issue 2, 2016, Pages 168-174

  Bohman, Leif Erik ^a   Riley, John ^a   Milovanova, Tatyana N ^a,b   Sanborn, Matthew R ^a   Thom, Stephen R ^a,b   Armstead, William M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

endothelin; fluid percussion injury; hypotensive cerebrovasodilation; microparticles; tissue plasminogen activator; traumatic brain injury

Indexed keywords

ENDOTHELIN 1; MACROGOL; MITOGEN ACTIVATED PROTEIN KINASE; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN OXYGEN TENSION; CARBON DIOXIDE TENSION; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; HEMODYNAMICS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HYPOTENSION; MALE; NERVE CELL LESION; NEWBORN; NONHUMAN; PARTICLE SIZE; PIA ARTERY; PIGLET; PROTEIN PHOSPHORYLATION; TRAUMATIC BRAIN INJURY; VASODILATATION; ANIMAL; BLOOD; BRAIN INJURY; CEREBROSPINAL FLUID; DISEASE MODEL; MEMBRANE MICROPARTICLE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PIG;

ANIMALS; ANIMALS, NEWBORN; BRAIN INJURIES; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CELL-DERIVED MICROPARTICLES; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HYPOTENSION; MALE; SWINE; TISSUE PLASMINOGEN ACTIVATOR; VASODILATION;

EID: 84954325464     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.3885     Document Type: Article

References (42)

1. Langlois, J.A., Rutland-Brown, W., and Thomas, K.E. (2005). The incidence of traumatic brain injury among children in the United States: differences by race. J. Head Trauma Rehabil. 20, 229-238.
2. Adelson, P.D., Clyde, B., Kochanek, P.M., Wisniewski, S.R., Marion, D.W., and Yonas, H. (1997). Cerebrovascular response in infants and young children following severe traumatic brain injury: a preliminary report. Pediatr. Neurosurg. 26, 200-207.
3. Adelson, P.D., Srinivas, R., Chang, Y., Bell, M., and Kochanek, P.M. (2011). Cerebrovascular response in children following severe traumatic brain injury. Childs. Nerv. Syst. 27, 1465-1476.
4. Coates, B.M., Vavilala, M.S., Mack, C.D., Muangman, S., Suz, P., Sharar, S.R., Bulger, E., and Lam, A.M. (2005). Influence of definition and location of hypotension on outcome following severe pediatric traumatic brain injury. Crit. Care Med. 33, 2645-2650.
5. Freeman, S.S., Udomphorn, Y., Armstead, W.M., Fisk, D.M., and Vavilala, M.S. (2008). Young age as a risk factor for impaired cerebral autoregulation after moderate to severe pediatric traumatic brain injury. Anesthesiology. 108, 588-595.
6. Chaiwat, O., Sharma, D., Udomphorn, Y., Armstead, W.M., and Vavilala, M.S. (2009). Cerebral hemodynamic predictors of poor 6- month Glasgow Outcome Score in severe pediatric traumatic brain injury. J. Neurotrauma. 26, 657-663.
7. Vavilala, M.S., Bowen, A., Lam, A.M., Uffman, J.C., Powell, J., Winn, H.R., and Rivara, F.P. (2003). Blood pressure and outcome after severe pediatric traumatic brain injury. J. Trauma. 55, 1039-1044.
8. Armstead, W.M. (2000). Age-dependent cerebral hemodynamic effects of traumatic brain injury in newborn and juvenile pigs. Microcirculation. 7, 225-2035.
9. Blann, A., Shantsila, E., and Shantsila, A. (2009). Microparticles and arterial disease. Semin. Thromb. Hemost. 35, 488-496.
10. Thom, S.R., Yang, M., Bhopale, V.M., Huang, S., and Milovanova, T.N. (2011). Microparticles initiate decompression-induced neutrophil activation and subsequent vascular injuries. J. Appl. Physiol. 110, 340-351.
11. Mackman, N. (2009). On the trail of microparticles. Circ. Res. 104, 925-927.
12. Meziani, F., Delabranche, X., Asfar, P., and Toti, F. (2010). Bench-Tobedside review: circulating microparticles-A new player in sepsis?. Crit. Care. 14, 236.
13. Bidot, L., Jy, W., Bidot, C., Jimenez, J.J., Fontana, V., Horstman, L.L., and Ahn, Y.S. (2008). Microparticle-mediated thrombin generation assay: increased activity in patients with recurrent thrombosis. J. Thromb. Haemost. 6, 913-919.
14. Amabile, N., Guérin, A.P., Leroyer, A., Mallat, Z., Nguyen, C., Boddaert, J., London, G.M., Tedgui, A., and Boulanger, C.M. (2005). Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J. Am. Soc. Nephrol. 16, 3381-3388.
15. Agouni, A., Lagrue-Lak-Hal, A.H., Ducluzeau, P.H., Mostefai, H.A., Draunet-Busson, C., Leftheriotis, G., Heymes, C., Martinez, M.C., and Andriantsitohaina, R. (2008). Endothelial dysfunction caused by circulating microparticles from patients with metabolic syndrome. Am. J. Pathol. 173, 1210-1219.
16. Morel, N., Morel, O., Petit, L., Hugel, B., Cochard, J.F., Freyssinet, J.M., Sztark, F., and Dabadie, P. (2008). Generation of procoagulant microparticles in cerebrospinal fluid and peripheral blood after traumatic brain injury. J. Trauma. 64, 698-704.
17. Nekludov, M., Mobarrez, F., Gryth, D., Bellander, B.M., and Wallen, H. (2014). Formation of microparticles in the injured brain of patiens with severe isolated traumatic brain injury. J. Neurotrauma. 31, 1927-1933.
18. Simak, J., Gelderman, M.P., Yu, H., Wright, V., and Baird, A.E. (2006). Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J. Thromb. Haemost. 4, 1296-1302.
19. Sanborn, M.R., Thom, S.R., Bohman, L.-E., Stein, S.C., Levine, J.M., Milovanova, T., Maloney-Wilensky, E., Frangos, S., and Kumar, M.A. (2012). Temporal dynamics of microparticle elevation following subarachnoid hemorrhage. J. Neurosurg. 117, 579-586.
20. Lackner, P., Dietmann, A., Beer, R., Fischer, M., Broessner, G., Helbok, R., Marxgut, J., Pfausler, B., and Schmutzhard, E. (2010). Cellular microparticles as a marker for cerebral vasospasm in spontaneous subarachnoid hemorrhage. Stroke. 41, 2353-2357.
21. Faraci, F.M., and Heistad, D.D. (1998). Regulation of the cerebral circulation: role of endothelium and potassium channels. Physiol. Rev. 78, 53-97.
22. Armstead, W.M. (1999). Hypotension dilates pial arteries by KATP and kca channel activation. Brain Res. 816, 158-164.
23. Armstead,W.M. (2001). Endothelin-Induced cyclooxygenase-dependent superoxide generation contributes to K+ channel functional impairment after brain injury. J. Neurotrauma. 18, 1039-1048.
24. Armstead, W.M. (1999). Age-dependent impairment of K(ATP) channel function following brain injury. J. Neurotrauma. 16, 391-402.
25. Leffler, C.W., Busija, D.W., Beasley, D.G., and Fletcher, A.M. (1986). Maintenance of cerebral circulation during hemorrhagic hypotension in newborn pigs: role of prostanoids. Circ. Res. 59, 562-567.
26. Leffler, C.W. and Busija, D.W. (1987). Prostanoids and pial arteriolar diameter in hypotensive newborn pigs. Am. J. Physiol. 252, H687-H691.
27. Armstead, W.M. and Kurth, C.D. (1994). Different cerebral hemodynamic responses following fluid percussion brain injury in the newborn and juvenile pig. J. Neurotrauma. 11, 487-497.
28. Armstead, W.M., Riley, J., and Vavilala, M.S. (2012). TBI sex dependently upregulates ET-1 to impair autoregulation, which is aggravated by phenylephrine in males but is abrogated in females. J. Neurotrauma. 29, 1483-1490.
29. Armstead, W.M., Riley, J., Cines, D.B., and Higazi, A.A. (2011). tPA contributes to impairment of ATP and Ca sensitive K channel mediated cerebrovasodilation after hypoxia/ischemia through upregulation of ERK MAPK. Brain Res. 1376, 88-93.
30. Armstead, W.M., Bohman, L.-E., Riley, J., Yarovoi, S., Higazi, A.A., and Cines, D.B. (2013). tPA-S(481)A prevents impairment of cerebrovascular autoregulation by endogenous tPA after traumatic brain injury by upregulating p38 MAPK and inhibiting ET-1. J. Neurotrauma 30:1898-1907.
31. Armstead, W.M., Cines, D.B., and Higazie, A.A. (2005). Plasminogen activators contribute to age-dependent impairment of NMDA cerebrovasodilation after brain injury. Brain Res. Dev. Brain Res. 156, 139-146.
32. Armstead, W.M., Kiessling, J.W., Cines, D.B., and Higazi, A.A. (2011). Glucagon protects against impaired NMDA-mediated cerebrovasodilation and cerebral autoregulation during hypotension after brain injury by activating cAMP protein kinase A and inhibiting upregulation of tPA. J. Neurotrauma. 28, 451-457.
33. Nantakomol, D., Chimma, P., Day, N.P., Dondorp, A.M., Combes, V., Krudsood, S., Looareesuwan, S., White, N.J., Pattanapanyasat, K., and Chotivanich, K. (2008). Quantitation of cell-derived microparticles in plasma using flow rate based calibration. Southeast Asian J. Trop. Med. Public Health. 39, 146-153.
34. Zubkov, A.Y., Rollins, K.S., Parent, A.D., Zhang, J., and Bryan, R.M. (2000). Mechanism of endothelin-1-induced contraction in rabbit basilar artery. Stroke. 31, 526-533.
35. Armstead, W.M., Riley, J., and Vavilala, M.S. (2013). Dopamine prevents impairment of autoregulation after traumatic brain injury in the newborn pig through inhibition of up-regulation of endothelin-1 and extracellular signal-regulated kinase mitogen-Activated protein kinase. Pediatr. Crit. Care Med. 14, e103-e111.
36. Armstead WM, Raghupathi R. (2011). Endothelin and the neurovascular unit in pediatricntraumatic brain injury. Neurol. Res. 33, 127-132.
37. Armstead, W.M., Riley, J., Yarovoi, S., Cines, D.B., Smith, D.H., and Higazi, A.A. (2012). tPA-S481A prevents neurotoxicity of endogenous tPA in traumatic brain injury. J. Neurotrauma. 29, 1794-1802.
38. Ayers, L., Kohler, M., Harrison, P., Sargent, I., Dragovic, R., Schaap, M., Nieuwland, R., Brooks, S.A., and Ferry, B. (2011). Measurement of circulating cell-derived microparticles by flow cytometry: sources of variability within the assay. Thromb. Res. 127, 370-377.
39. Grayburn, P.A., Weiss, J.L., Hack, T.C., Klodas, E., Raichlen, J.S., Vannan, M.A., Klein, A.L., Kitzman, D.W., Chrysant, S.G., Cohen, J.L., Abrahamson, D., Foster, E., Perez, J.E., Aurigemma, G.P., Panza, J.A., Picard, M.H., Byrd, B.F., Segar, D.S., Jacobson, S.A., Sahn, D.J., and DeMaria, A.N. (1998). Phase III multicenter trial comparing the efficacy of 2% dodecafluoropentane emulsion (EchoGen) and sonicated 5% human albumin (Albunex) as ultrasound contrast agents in patients with suboptimal echocardiograms. J. Am. Coll. Cardiol. 32, 230-236.
40. Beppu, S., Matsuda, H., Shishido, T., Matsumura, M., and Miyatake, K. (1997). Prolonged myocardial contrast echocardiography via peripheral venous administration of QW3600 Injection (EchoGen): its efficacy and side effects. J. Am. Soc. Echocardiogr. 10, 11-24.
41. Young, B., Runge, J.W., Waxman, K.S., Harrington, T., Wilberger, J., Muizelaar, J.P., Boddy, A., and Kupiec, J.W. (1996). Effects of pegorgotein on neurologic outcome of patients with severe head injury A multicenter, randomized controlled trial. JAMA. 276, 538-543.
42. Armstead, W.M. (2002). Age dependent NMDA contribution to impaired hypotensive cerebral hemodynamics following brain injury. Brain Res. Dev. Brain Res. 139, 19-28.