Cerebrospinal fluid levels of high-mobility group box 1 and cytochrome C predict outcome after pediatric traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 11, 2012, Pages 2013-2021

  Au, Alicia K ^a   Aneja, Rajesh K ^a   Bell, Michael J ^a   Bayir, Hülya ^a,b   Feldman, Keri ^a   Adelson, P David ^c   Fink, Ericka L ^a   Kochanek, Patrick M ^a   Clark, Robert S B ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b Center for Free Radical and Antioxidant Health   (United States)

^c PHOENIX CHILDREN'S HOSPITAL   (United States)

Author keywords

abusive head trauma; child abuse; cytochrome c; high mobility group box 1

Indexed keywords

CYTOCHROME C; HIGH MOBILITY GROUP B1 PROTEIN;

ADOLESCENT; APOPTOSIS; ARTICLE; CELL DEATH; CEREBROSPINAL FLUID LEVEL; CHILD; CHILDHOOD INJURY; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLASGOW OUTCOME SCALE; HEAD INJURY; HUMAN; INFANT; INTENSIVE CARE; MALE; PRESCHOOL CHILD; SCHOOL CHILD; TRAUMATIC BRAIN INJURY;

BIOLOGICAL MARKERS; BRAIN INJURIES; CHILD; CHILD, PRESCHOOL; CYTOCHROMES C; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLASGOW OUTCOME SCALE; HMGB1 PROTEIN; HUMANS; INFANT; MALE; TREATMENT OUTCOME;

EID: 84864621433     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.2171     Document Type: Article

References (50)

1. Adachi, N., Hirota, M., Hamaguchi, M., Okamoto, K., Watanabe, K. Endo, F. (2004). Serum cytochrome c level as a prognostic indicator in patients with systemic inflammatory response syndrome. Clin. Chim. Acta. 342, 127-136.
2. Adamsbaum, C., Grabar, S., Mejean, N. Rey-Salmon, C. (2010). Abusive head trauma: judicial admissions highlight violent and repetitive shaking. Pediatrics 126, 546-555.
3. Adelson, P.D., Bratton, S.L., Carney, N.A., Chesnut, R.M., du Coudray, H.E., Goldstein, B., Kochanek, P.M., Miller, H.C., Partington, M.D., Selden, N.R., Warden, C.R. Wright, D.W. (2003). Guidelines for the acute medical management of severe traumatic brain injury in infants, children. adolescents. Pediatr. Crit. Care Med. 4, S2-S75.
4. Adelson, P.D., Ragheb, J., Kanev, P., Brockmeyer, D., Beers, S.R., Brown, S.D., Cassidy, L.D., Chang, Y. Levin, H. (2005). Phase II clinical trial of moderate hypothermia after severe traumatic brain injury in children. Neurosurgery 56, 740-754; discussion 740-754.
5. Agrawal, A. Schatz, D.G. (1997). RAG1 and RAG2 form a stable postcleavage synaptic complex with DNA containing signal ends in V(D)J recombination. Cell 89, 43-53.
6. Ahlemeyer, B., Klumpp, S.Krieglstein, J. (2002). Release of cytochrome c into the extracellular space contributes to neuronal apoptosis induced by staurosporine. Brain Res. 934, 107-116.
7. Andersson, U., Wang, H., Palmblad, K., Aveberger, A.C., Bloom, O., Erlandsson-Harris, H., Janson, A., Kokkola, R., Zhang, M., Yang, H.Tracey, K.J. (2000). High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192, 565-570.
8. Barczyk, K., Kreuter, M., Pryjma, J., Booy, E.P., Maddika, S., Ghavami, S., Berdel, W.E., Roth, J. Los, M. (2005). Serum cytochrome c indicates in vivo apoptosis and can serve as a prognostic marker during cancer therapy. Int. J. Cancer 116, 167-173.
9. Ben-Ari, Z., Schmilovotz-Weiss, H., Belinki, A., Pappo, O., Sulkes, J., Neuman, M.G., Kaganovsky, E., Kfir, B., Tur- Kaspa, R. Klein, T. (2003). Circulating soluble cytochrome c in liver disease as a marker of apoptosis. J. Intern. Med. 254, 168-175.
10. Berger, R.P., Adelson, P.D., Richichi, R. Kochanek, P.M. (2006). Serum biomarkers after traumatic and hypoxemic brain injuries: insight into the biochemical response of the pediatric brain to inflicted brain injury. Dev. Neurosci. 28, 327-335.
11. Bianchi, M.E. Manfredi, A.A. (2007). High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev. 220, 35-46.
12. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A. Bianchi, M.E. (2003). Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551-5560.
13. Brophy, G.M., Pineda, J.A., Papa, L., Lewis, S.B., Valadka, A.B., Hannay, H.J., Heaton, S.C., Demery, J.A., Liu, M.C., Tepas, J.J., 3rd, Gabrielli, A., Robicsek, S., Wang, K.K., Robertson, C.S. Hayes, R.L. (2009). alphaII-Spectrin breakdown product cerebrospinal fluid exposure metrics suggest differences in cellular injury mechanisms after severe raumatic brain injury. J. Neurotrauma 26, 471-479.
14. Bustin, M. Reeves, R. (1996). High-mobility-group chromosomal proteins: Architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol. 54, 35-100.
15. Cohen, M.J., Brohi, K., Calfee, C.S., Rahn, P., Chesebro, B.B., Christiaans, S.C., Carles, M., Howard, M. Pittet, J.F. (2009). Early release of high mobility group box nuclear protein 1 after severe trauma in humans: Role of injury severity and tissue hypoperfusion. Crit. Care 13, R174.
16. Darwish, R.S. Amiridze, N.S. (2010). Detectable levels of cytochrome C and activated caspase-9 in cerebrospinal fluid after human traumatic brain injury. Neurocrit. Care 12, 337-341.
17. Ewing-Cobbs, L., Prasad, M., Kramer, L. Landry, S. (1999). Inflicted traumatic brain injury: Relationship of developmental outcome to severity of injury. Pediatr. Neurosurg. 31, 251-258.
18. Exo, J., Kochanek, P.M., Adelson, P.D., Greene, S., Clark, R.S., Bayir, H., Wisniewski, S.R. Bell, M.J. (2011). Intracranial pressure-monitoring systems in children with traumatic brain injury: Combining therapeutic and diagnostic tools. Pediatr. Crit. Care Med. 12, 560-565.
19. Fan, J., Li, Y., Levy, R.M., Fan, J.J., Hackam, D.J., Vodovotz, Y., Yang, H., Tracey, K.J., Billiar, T.R. Wilson, M.A. (2007). Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: Role of HMGB1-TLR4 signaling. J. Immunol. 178, 6573-6580.
20. Faul, M., Xu, L., Wald, M.M. Coronado, V.G. (2010). Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006.
21. Atlanta: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control. Fink, M.P. (2007). Bench-to-bedside review: High-mobility group box 1 and critical illness. Crit. Care 11, 229.
22. Gao, H.M., Zhou, H., Zhang, F., Wilson, B.C., Kam, W. Hong, J.S. (2011). HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J. Neurosci. 31, 1081-1092.
23. Gardella, S., Andrei, C., Ferrera, D., Lotti, L.V., Torrisi, M.R., Bianchi, M.E. Rubartelli, A. (2002). The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesiclemediated secretory pathway. EMBO Rep. 3, 995-1001.
24. Goodwin, G.H., Sanders, C. Johns, E.W. (1973). A new group of chromatin-associated proteins with a high content of acidic and basic amino acids. Eur. J. Biochem. 38, 14-19.
25. Guenther, E., Powers, A., Srivastava, R. Bonkowsky, J.L. (2010). Abusive head trauma in children presenting with an apparent life-threatening event. J. Pediatr. 157, 821-825.
26. Jenny, C., Hymel, K.P., Ritzen, A., Reinert, S.E. Hay, T.C. (1999). Analysis of missed cases of abusive head trauma. JAMA 281, 621-626.
27. Keenan, H.T., Runyan, D.K., Marshall, S.W., Nocera, M.A. Merten, D.F. (2004). A population-based comparison of clinical and outcome characteristics of young hildren with serious inflicted and noninflicted traumatic brain injury. Pediatrics 114, 633-639.
28. Kim, J.B., Sig Choi, J., Yu, Y.M., Nam, K., Piao, C.S., Kim, S.W., Lee, M.H., Han, P.L., Park, J.S. Lee, J.K. (2006). HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J. Neurosci. 26, 6413-6421.
29. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. Newmeyer, D.D. (1997). The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
30. Klune, J.R., Dhupar, R., Cardinal, J., Billiar, T.R. Tsung, A. (2008). HMGB1: Endogenous danger signaling. Mol. Med. 14, 476-484.
31. Kochanek, P.M., Berger, R.P., Bayir, H., Wagner, A.K., Jenkins, L.W.Clark, R.S. (2008). Biomarkers of primary and evolving damage in traumatic and ischemic brain injury: Diagnosis, prognosis, probing mechanisms. therapeutic decision making. Curr. Opin. Crit. Care 14, 135-141.
32. Liu, X., Kim, C.N., Yang, J., Jemmerson, R. Wang, X. (1996). Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86, 147-157.
33. Matzinger, P. (2002). The danger model: A renewed sense of self. Science 296, 301-305.
34. Matzinger, P. (1994). Tolerance, danger the extended family. Annu. Rev. Immunol. 12, 991-1045.
35. Messmer, D., Yang, H., Telusma, G., Knoll, F., Li. J., Messmer, B., Tracey, K.J. Chiorazzi, N. (2004). High mobility group box protein 1: An endogenous signal for dendritic cell maturation and Th1 polarization. J. Immunol. 173, 07-313.
36. Mondello, S., Robicsek, S.A., Gabrielli, A., Brophy, G.M., Papa, L., Tepas, J., Robertson, C., Buki, A., Scharf, D., Jixiang, M., Akinyi, L., Muller, U., Wang, K.K. Hayes, R.L. (2010). AlphaII-spectrin breakdown products (SBDPs): Diagnosis and outcome in severe traumatic brain injury patients. J. Neurotrauma 27, 1203-1213.
37. Nakahara, T., Tsuruta, R., Kaneko, T., Yamashita, S., Fujita, M., Kasaoka, S., Hashiguchi, T., Suzuki, M., Maruyama, I. Maekawa, T. (2009). High-mobility group box 1 protein in CSF of patients with subarachnoid hemorrhage. Neurocrit. Care 11, 362-368.
38. Palumbo, R. Bianchi, M.E. (2004). High mobility group box 1 protein, a cue for stem cell recruitment. Biochem. Pharmacol. 68, 1165-1170.
39. Peltz, E.D., Moore, E.E., Eckels, P.C., Damle, S.S., Tsuruta, Y., Johnson, J.L., Sauaia, A., Silliman, C.C., Banerjee, A. Abraham, E. (2009). HMGB1 is markedly elevated within 6 hours of mechanical trauma in humans. Shock 32, 17-22.
40. Pineda, J.A., Lewis, S.B., Valadka, A.B., Papa, L., Hannay, H.J., Heaton, S.C., Demery, J.A., Liu, M.C., Aikman, J.M., Akle, V., Brophy, G.M., Tepas, J.J., Wang, K.K., Robertson, C.S. Hayes, R.L. (2007). Clinical significance of alphaII-spectrin breakdown products in cerebrospinal fluid after severe traumatic brain injury. J. Neurotrauma 24, 354-366.
41. Raucci, A., Palumbo, R. Bianchi, M.E. (2007). HMGB1: A signal of necrosis. Autoimmunity 40, 285-289.
42. Renz, A., Berdel, W.E., Kreuter, M., Belka, C., Schulze-Osthoff, K. Los, M. (2001). Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo. Blood 98, 1542-1548.
43. Rock, K.L., Hearn, A., Chen, C.J. Shi, Y. (2005). Natural endogenous adjuvants. Springer Semin. Immunopathol. 26, 231-246.
44. Rouhiainen, A., Kuja-Panula, J., Wilkman, E., Pakkanen, J., Stenfors, J., Tuominen, R.K., Lepantalo, M., Carpen, O., Parkkinen, J. Rauvala, H. (2004). Regulation of monocyte migration by amphotericin (HMGB1). Blood 104, 1174-1182.
45. Satchell, M.A., Lai, Y., Kochanek, P.M., Wisniewski, S.R., Fink, E.L., Siedberg, N.A., Berger, R.P., DeKosky, S.T., Adelson, P.D. Clark, R.S. (2005). Cytochrome c, a biomarker of apoptosis, is increased in cerebrospinal fluid from infants with inflicted brain injury from child abuse. J. Cereb. Blood Flow Metab. 25, 919-927.
46. Scaffidi, P., Misteli, T. Bianchi, M.E. (2002). Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191-195.
47. Shore, P.M., Berger, R.P., Varma, S., Janesko, K.L., Wisniewski, S.R., Clark, R.S., Adelson, P.D., Thomas, N.J., Lai, Y.C., Bayir, H. Kochanek, P.M. (2007). Cerebrospinal fluid biomarkers versus Glasgow Coma Scale and Glasgow Outcome Scale in pediatric traumatic brain injury: The role of oung age and inflicted injury. J. Neurotrauma 24, 75-86.
48. Sutrias-Grau, M., Bianchi, M.E. Bernues, J. (1999). High mobility group protein 1 interacts specifically with the core domain of human TATA box-binding protein and interferes with transcription factor IIB within the pre-initiation complex. J. Biol. Chem. 274, 1628-1634.
49. Tang, D., Kang, R., Cao, L., Zhang, G., Yu, Y., Xiao, W., Wang, H. Xiao, X. (2008). A pilot study to detect high mobility group box 1 and heat shock protein 72 in cerebrospinal fluid of pediatric patients with meningitis. Crit. Care Med. 36, 291-295.
50. Yakovlev, A.G., Ota, K., Wang, G., Movsesyan, V., Bao, W.L., Yoshihara, K. Faden, A.I. (2001). Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury. J. Neurosci. 21, 7439-7446.