Table of Contents Author Guidelines Submit a Manuscript
International Journal of Cell Biology
Volume 2014, Article ID 495817, 10 pages
http://dx.doi.org/10.1155/2014/495817
Research Article

Necrostatin-1 Reduces Neurovascular Injury after Intracerebral Hemorrhage

Department of Neurosurgery, Medical College of Georgia, Georgia Regents University, 1120 15th Street, Augusta, GA 30912, USA

Received 11 November 2013; Revised 24 January 2014; Accepted 27 January 2014; Published 6 March 2014

Academic Editor: Claudia Giampietri

Copyright © 2014 Melanie D. King et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. S. Dennis, J. P. S. Burn, P. A. G. Sandercock, J. M. Bamford, D. T. Wade, and C. P. Warlow, “Long-term survival after first-ever stroke: the Oxfordshire Community Stroke Project,” Stroke, vol. 24, no. 6, pp. 796–800, 1993. View at Google Scholar · View at Scopus
  2. J. M. Gebel Jr., E. C. Jauch, T. G. Brott et al., “Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage,” Stroke, vol. 33, no. 11, pp. 2636–2641, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Rincon and S. A. Mayer, “Novel therapies for intracerebral hemorrhage,” Current Opinion in Critical Care, vol. 10, no. 2, pp. 94–100, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Weimar, C. Weber, M. Wagner et al., “Management patterns and health care use after intracerebral hemorrhage: a cost-of-illness study from a societal perspective in Germany,” Cerebrovascular Diseases, vol. 15, no. 1-2, pp. 29–36, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. M. S. Dennis, “Outcome after brain haemorrhage,” Cerebrovascular Diseases, vol. 16, supplement 1, pp. 9–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. A. I. Qureshi, S. Tuhrim, J. P. Broderick, H. H. Batjer, H. Hondo, and D. F. Hanley, “Spontaneous intracerebral hemorrhage,” The New England Journal of Medicine, vol. 344, no. 19, pp. 1450–1460, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. G. A. Christoforidis, A. Slivka, Y. Mohammad, C. Karakasis, B. Avutu, and M. Yang, “Size matters: hemorrhage volume as an objective measure to define significant intracranial hemorrhage associated with thrombolysis,” Stroke, vol. 38, no. 6, pp. 1799–1804, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. M. E. Fewel, B. G. Thompson Jr., and J. T. Hoff, “Spontaneous intracerebral hemorrhage: a review,” Neurosurgical Focus, vol. 15, no. 4, p. E1, 2003. View at Google Scholar · View at Scopus
  9. P. D. Lyden, A. Shuaib, K. R. Lees et al., “Safety and tolerability of NXY-059 for acute intracerebral hemorrhage: the CHANT trial,” Stroke, vol. 38, no. 8, pp. 2262–2269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. A. D. Mendelow, B. A. Gregson, H. M. Fernandes et al., “Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial,” The Lancet, vol. 365, no. 9457, pp. 387–397, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Silva, R. Leira, J. Tejada, J. M. Lainez, J. Castillo, and A. Dávalos, “Molecular signatures of vascular injury are associated with early growth of intracerebral hemorrhage,” Stroke, vol. 36, no. 1, pp. 86–91, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Leira, A. Dávalos, Y. Silva et al., “Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors,” Neurology, vol. 63, no. 3, pp. 461–467, 2004. View at Google Scholar · View at Scopus
  13. T. Doczi, “The pathogenetic and prognostic significance of blood-brain barrier damage at the acute stage of aneurysmal subarachnoid haemorrhage. Clinical and experimental studies,” Acta Neurochirurgica, vol. 77, no. 3-4, pp. 110–132, 1985. View at Google Scholar · View at Scopus
  14. S. Park, M. Yamaguchi, C. Zhou, J. W. Calvert, J. Tang, and J. H. Zhang, “Neurovascular protection reduces early brain injury after subarachnoid hemorrhage,” Stroke, vol. 35, no. 10, pp. 2412–2417, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. S. L. Hickenbottom, J. C. Grotta, R. Strong, L. A. Denner, and J. Aronowski, “Nuclear factor-κB and cell death after experimental intracerebral hemorrhage in rats,” Stroke, vol. 30, no. 11, pp. 2472–2478, 1999. View at Google Scholar · View at Scopus
  16. N. Platt, R. P. da Silva, and S. Gordon, “Recognizing death: the phagocytosis of apoptotic cells,” Trends in Cell Biology, vol. 8, no. 9, pp. 365–372, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Zhao, Y. Zhang, R. Strong, J. Zhang, J. C. Grotta, and J. Aronowski, “Distinct patterns of intracerebral hemorrhage-induced alterations in NF-κB subunit, iNOS, and COX-2 expression,” Journal of Neurochemistry, vol. 101, no. 3, pp. 652–663, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. J. S. Kim, S. S. Yoon, Y. H. Kim, and J. S. Ryu, “Serial measurement of interleukin-6, transforming growth factor-β, and S-100 protein in patients with acute stroke,” Stroke, vol. 27, no. 9, pp. 1553–1557, 1996. View at Google Scholar · View at Scopus
  19. J. Castillo, A. Dávalos, J. Álvarez-Sabín et al., “Molecular signatures of brain injury after intracerebral hemorrhage,” Neurology, vol. 58, no. 4, pp. 624–629, 2002. View at Google Scholar · View at Scopus
  20. T. Dziedzic, S. Bartus, A. Klimkowicz, M. Motyl, A. Slowik, and A. Szczudlik, “Intracerebral hemorrhage triggers interleukin-6 and interleukin-10 release in blood,” Stroke, vol. 33, no. 9, pp. 2334–2335, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Woiciechowsky, B. Schöning, J. Cobanov, W. R. Lanksch, H.-D. Volk, and W.-D. Döcke, “Early IL6 plasma concentrations correlate with severity of brain injury and pneumonia in brain-injured patients,” Journal of Trauma, vol. 52, no. 2, pp. 339–345, 2002. View at Google Scholar · View at Scopus
  22. H.-Y. Fang, W.-J. Ko, and C.-Y. Lin, “Inducible heat shock protein 70, interleukin-18, and tumor necrosis factor alpha correlate with outcomes in spontaneous intracerebral hemorrhage,” Journal of Clinical Neuroscience, vol. 14, no. 5, pp. 435–441, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Aronowski and C. E. Hall, “New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies,” Neurological Research, vol. 27, no. 3, pp. 268–279, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Mayne, W. Ni, H. J. Yan et al., “Antisense oligodeoxynucleotide inhibition of tumor necrosis factor-α expression is neuroprotective after intracerebral hemorrhage,” Stroke, vol. 32, no. 1, pp. 240–248, 2001. View at Google Scholar · View at Scopus
  25. G. Xi, Y. Hua, R. F. Keep, J. G. Younger, and J. T. Hoff, “Systemic complement depletion diminishes perihematomal brain edema in rats,” Stroke, vol. 32, no. 1, pp. 162–167, 2001. View at Google Scholar · View at Scopus
  26. A. Lu, Y. Tang, R. Ran, T. L. Ardizzone, K. R. Wagner, and F. R. Sharp, “Brain genomics of intracerebral hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 2, pp. 230–252, 2006. View at Google Scholar
  27. K. R. Wagner, S. Beiler, C. Beiler et al., “Delayed profound local brain hypothermia markedly reduces interleukin-1β gene expression and vasogenic edema development in a porcine model of intracerebral hemorrhage,” Acta Neurochirurgica. Supplement, vol. 96, pp. 177–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. J. K. Wasserman, X. Zhu, and L. C. Schlichter, “Evolution of the inflammatory response in the brain following intracerebral hemorrhage and effects of delayed minocycline treatment,” Brain Research, vol. 1180, no. 1, pp. 140–154, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Kroemer, L. Galluzzi, P. Vandenabeele et al., “Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009,” Cell Death and Differentiation, vol. 16, no. 1, pp. 3–11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Galluzzi and G. Kroemer, “Necroptosis: a specialized pathway of programmed necrosis,” Cell, vol. 135, no. 7, pp. 1161–1163, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Hitomi, D. E. Christofferson, A. Ng et al., “Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway,” Cell, vol. 135, no. 7, pp. 1311–1323, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Kitanaka and Y. Kuchino, “Caspase-independent programmed cell death with necrotic morphology,” Cell Death and Differentiation, vol. 6, no. 6, pp. 508–515, 1999. View at Google Scholar · View at Scopus
  33. P. B. Letarte, K. Lieberman, K. Nagatani, R. A. Haworth, G. B. Odell, and T. A. Duff, “Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells,” Journal of Neurosurgery, vol. 79, no. 2, pp. 252–255, 1993. View at Google Scholar · View at Scopus
  34. M. D. Laird, C. Wakade, C. H. Alleyne Jr., and K. M. Dhandapani, “Hemin-induced necroptosis involves glutathione depletion in mouse astrocytes,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1103–1114, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. A. Kelliher, S. Grimm, Y. Ishida, F. Kuo, B. Z. Stanger, and P. Leder, “The death domain kinase RIP mediates the TNF-induced NF-κB signal,” Immunity, vol. 8, no. 3, pp. 297–303, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Degterev, J. Hitomi, M. Germscheid et al., “Identification of RIP1 kinase as a specific cellular target of necrostatins,” Nature Chemical Biology, vol. 4, no. 5, pp. 313–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Degterev, Z. Huang, M. Boyce et al., “Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury,” Nature Chemical Biology, vol. 1, no. 2, pp. 112–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. Z. You, S. I. Savitz, J. Yang et al., “Necrostatin-1 reduces histopathology and improves functional outcome after controlled cortical impact in mice,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 9, pp. 1564–1573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. M. D. King, D. J. McCracken, F. M. Wade, S. E. Meiler, C. H. Alleyne Jr., and K. M. Dhandapani, “Attenuation of hematoma size and neurological injury with curcumin following intracerebral hemorrhage in mice: laboratory investigation,” Journal of Neurosurgery, vol. 115, no. 1, pp. 116–123, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. M. D. King, C. H. Alleyne Jr., and K. M. Dhandapani, “TNF-alpha receptor antagonist, R-7050, improves neurological outcomes following intracerebral hemorrhage in mice,” Neuroscience Letters, vol. 542, pp. 92–96, 2013. View at Google Scholar
  41. D. E. Kimbler, J. Shields, N. Yanasak, J. R. Vender, and K. M. Dhandapani, “Activation of P2X7 promotes cerebral edema and neurological injury after traumatic brain injury in mice,” PLoS ONE, vol. 7, no. 7, Article ID e41229, 2012. View at Google Scholar
  42. M. D. Laird, S. Sukumari-Ramesh, A. E. B. Swift, S. E. Meiler, J. R. Vender, and K. M. Dhandapani, “Curcumin attenuates cerebral edema following traumatic brain injury in mice: a possible role for aquaporin-4?” Journal of Neurochemistry, vol. 113, no. 3, pp. 637–648, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Wakade, M. D. King, M. D. Laird, C. H. Alleyne Jr., and K. M. Dhandapani, “Curcumin attenuates vascular inflammation and cerebral vasospasm after subarachnoid hemorrhage in mice,” Antioxidants and Redox Signaling, vol. 11, no. 1, pp. 35–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Sukumari-Ramesh, C. H. Alleyne Jr., and K. M. Dhandapani, “Astrocyte-specific expression of survivin after intracerebral hemorrhage in mice: a possible role in reactive gliosis?” Journal of Neurotrauma, vol. 29, no. 18, pp. 2798–2804, 2012. View at Publisher · View at Google Scholar
  45. G. A. Rosenberg, S. Mun-Bryce, M. Wesley, and M. Kornfeld, “Collagenase-induced intracerebral hemorrhage in rats,” Stroke, vol. 21, no. 5, pp. 801–807, 1990. View at Google Scholar · View at Scopus
  46. W. Clark, L. Gunion-Rinker, N. Lessov, and K. Hazel, “Citicoline treatment for experimental intracerebral hemorrhage in mice,” Stroke, vol. 29, no. 10, pp. 2136–2140, 1998. View at Google Scholar · View at Scopus
  47. L. F. Eng and R. S. Ghirnikar, “GFAP and astrogliosis,” Brain Pathology, vol. 4, no. 3, pp. 229–237, 1994. View at Google Scholar · View at Scopus
  48. M. V. Sofroniew, “Reactive astrocytes in neural repair and protection,” Neuroscientist, vol. 11, no. 5, pp. 400–407, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Broderick, S. Connolly, E. Feldmann et al., “Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group,” Stroke, vol. 38, no. 6, pp. 2001–2023, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. D. L. Labovitz and R. L. Sacco, “Intracerebral hemorrhage: update,” Current Opinion in Neurology, vol. 14, no. 1, pp. 103–108, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Wu, Y. Hua, R. F. Keep, T. Nakamura, J. T. Hoff, and G. Xi, “Iron and iron-handling proteins in the brain after intracerebral hemorrhage,” Stroke, vol. 34, no. 12, pp. 2964–2969, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Davalos, J. Grutzendler, G. Yang et al., “ATP mediates rapid microglial response to local brain injury in vivo,” Nature Neuroscience, vol. 8, no. 6, pp. 752–758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. L. P. Wang, F. Li, X. Shen, and J. Z. Tsien, “Conditional knockout of NMDA receptors in dopamine neurons prevents nicotine-conditioned place preference,” PLoS ONE, vol. 5, no. 1, Article ID e8616, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. S. M. Davis, J. Broderick, M. Hennerici et al., “Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage,” Neurology, vol. 66, no. 8, pp. 1175–1181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. M. R. McLaughlin and D. W. Marion, “Cerebral blood flow and vasoresponsivity within and around cerebral contusions,” Journal of Neurosurgery, vol. 85, no. 5, pp. 871–876, 1996. View at Google Scholar · View at Scopus
  56. D. G. Nehls, A. D. Mendelow, D. I. Graham, E. J. Sinar, G. M. Teasdale, and R. R. Smith, “Experimental intracerebral hemorrhage: progression of hemodynamic changes after production of a spontaneous mass lesion,” Neurosurgery, vol. 23, no. 4, pp. 439–444, 1988. View at Google Scholar · View at Scopus
  57. P. Delgado, E. Cuadrado, A. Rosell et al., “Fas system activation in perihematomal areas after spontaneous intracerebral hemorrhage,” Stroke, vol. 39, no. 6, pp. 1730–1734, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Hua, J. Wu, R. F. Keep, T. Nakamura, J. T. Hoff, and G. Xi, “Tumor necrosis factor-alpha increases in the brain after intracerebral hemorrhage and thrombin stimulation,” Neurosurgery, vol. 58, no. 3, pp. 542–550, 2006. View at Google Scholar · View at Scopus
  59. A. P. Nguyen, H. D. Huynh, S. B. Sjovold, and F. Colbourne, “Progressive brain damage and alterations in dendritic arborization after collagenase-induced intracerebral hemorrhage in rats,” Current Neurovascular Research, vol. 5, no. 3, pp. 171–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Matsushita, W. Meng, X. Wang et al., “Evidence for apoptosis after intracerebral hemorrhage in rat striatum,” Journal of Cerebral Blood Flow and Metabolism, vol. 20, no. 2, pp. 396–404, 2000. View at Google Scholar · View at Scopus
  61. A. I. Qureshi, M. F. Suri, P. T. Ostrow et al., “Apoptosis as a form of cell death in intracerebral hemorrhage,” Neurosurgery, vol. 52, no. 5, pp. 1041–1047, 2003. View at Google Scholar
  62. C. Gong, N. Boulis, J. Qian, D. E. Turner, J. T. Hoff, and R. F. Keep, “Intracerebral hemorrhage-induced neuronal death,” Neurosurgery, vol. 48, no. 4, pp. 875–883, 2001. View at Google Scholar · View at Scopus
  63. X. Zhu, L. Tao, E. Tejima-Mandeville et al., “Plasmalemma permeability and necrotic cell death phenotypes after intracerebral hemorrhage in mice,” Stroke, vol. 43, no. 2, pp. 524–531, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. D. E. Christofferson and J. Yuan, “Necroptosis as an alternative form of programmed cell death,” Current Opinion in Cell Biology, vol. 22, no. 2, pp. 263–268, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Chang, W. Dong, M. Zhang et al., “Anti-necroptosis chemical necrostatin-1 can also suppress apoptotic and autophagic pathway to exert neuroprotective effect in mice intracerebral hemorrhage model,” Journal of Molecular Neuroscience, vol. 52, no. 2, pp. 242–249, 2014. View at Google Scholar
  66. N. Takahashi, L. Duprez, S. Grootjans et al., “Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models,” Cell Death & Disease, vol. 3, article e437, 2012. View at Publisher · View at Google Scholar
  67. W. Declercq, T. Vanden Berghe, and P. Vandenabeele, “RIP kinases at the crossroads of cell death and survival,” Cell, vol. 138, no. 2, pp. 229–232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Chamnanvanakij, L. R. Margraf, D. Burns, and J. M. Perlman, “Apoptosis and white matter injury in preterm infants,” Pediatric and Developmental Pathology, vol. 5, no. 2, pp. 184–189, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. C. L. Willis, C. C. Nolan, S. N. Reith et al., “Focal astrocyte loss is followed by microvascular damage, with subsequent repair of the blood-brain barrier in the apparent absence of direct astrocytic contact,” Glia, vol. 45, no. 4, pp. 325–337, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Lee, T. Cho, N. Jantaratnotai, Y. T. Wang, E. McGeer, and P. L. McGeer, “Depletion of GSH in glial cells induces neurotoxicity: relevance to aging and degenerative neurological diseases,” The FASEB Journal, vol. 24, no. 7, pp. 2533–2545, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. X. Xu, C. C. Chua, J. Kong et al., “Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells,” Journal of Neurochemistry, vol. 103, no. 5, pp. 2004–2014, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Sukumari-Ramesh, M. D. Laird, N. Singh, J. R. Vender, C. H. Alleyne, and K. M. Dhandapani, “Astrocyte-derived glutathione attenuates hemin-induced apoptosis in cerebral microvascular cells,” Glia, vol. 58, no. 15, pp. 1858–1870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Degterev, J. L. Maki, and J. Yuan, “Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase,” Cell Death and Differentiation, vol. 20, no. 2, article 366, 2013. View at Publisher · View at Google Scholar