Bilirubin and its oxidation products damage brain white matter

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 11, 2014, Pages 1837-1847

  Lakovic, Katarina ^a,b   Ai, Jinglu ^a   D'Abbondanza, Josephine ^a,b   Tariq, Asma ^a   Sabri, Mohammed ^a,b   Alarfaj, Abdullah K ^a   Vasdev, Punarjot ^a   MacDonald, Robert Loch ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

bilirubin toxicity; intracerebral hemorrhage; mice; white matter

Indexed keywords

BILIRUBIN; BILIRUBIN OXIDATION PRODUCT; CALCIUM CHANNEL L TYPE; DIMETHYL SULFOXIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXIDIZING AGENT; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILIRUBIN METABOLISM; BRAIN PROTECTION; BRAIN SLICE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORPUS CALLOSUM; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MASS SPECTROMETRY; MOUSE; MYELINATED NERVE; NEUROTOXICITY; NONHUMAN; NONMYELINATED NERVE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROPHOTOMETRY; WHITE MATTER INJURY; ANIMAL; BRAIN CORTEX; BRAIN HEMORRHAGE; BRAIN INJURY; CEREBROVASCULAR ACCIDENT; METABOLISM; NERVE FIBER; OXIDATION REDUCTION REACTION; PATHOLOGY;

ANIMALS; AXONS; BILIRUBIN; BRAIN INJURIES; CEREBRAL CORTEX; CEREBRAL HEMORRHAGE; MALE; MICE; OXIDATION-REDUCTION; STROKE;

EID: 84922235681     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.154     Document Type: Article

References (43)

1. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 2006; 5: 53-63.
2. Sacco S, Marini C, Toni D, Olivieri L, Carolei A. Incidence and 10-year survival of intracerebral hemorrhage in a population-based registry. Stroke 2009; 40: 394-399.
3. Narayan RK, Maas AI, Servadei F, Skolnick BE, Tillinger MN, Marshall LF. Progression of traumatic intracerebral hemorrhage: a prospective observational study. J Neurotrauma 2008; 25: 629-639.
4. Parker D, Jr, Rhoney DH, Liu-DeRyke X. Management of spontaneous nontraumatic intracranial hemorrhage. J Pharm Pract 2010; 23: 398-407.
5. Kellner CP, Connolly ES, Jr. Neuroprotective strategies for intracerebral hemorrhage: trials and translation. Stroke 2010; 41: S99-102.
6. Loftspring MC, Wurster WL, Pyne-Geithman GJ, Clark JF. An in vitro model of aneurysmal subarachnoid hemorrhage: oxidation of unconjugated bilirubin by cytochrome oxidase. J Neurochem 2007; 102: 1990-1995.
7. Loftspring MC, Hansen C, Clark JF. A novel brain injury mechanism after intracerebral hemorrhage: the interaction between heme products and the immune system. Med Hypotheses 2010; 74: 63-66.
8. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF. Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab 2003; 23: 629-652.
9. Huang FP, Xi G, Keep RF, Hua Y, Nemoianu A, Hoff JT. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J Neurosurg 2002; 96: 287-293.
10. Hua Y, Keep RF, Hoff JT, Xi G. Brain injury after intracerebral hemorrhage: the role of thrombin and iron. Stroke 2007; 38: 759-762.
11. Roy-Chowdhury N, Lu Y, Roy-Chowdhury J. Bilirubin metabolism. Textbook of Hepatology: from basic science to clinical practice, 3rd edn. Blackwell Publishing Ltd: Singapore, 2008, pp 165-172.
12. Clark JF, Sharp FR. Bilirubin oxidation products (BOXes) and their role in cerebral vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2006; 26: 1223-1233.
13. Rost NS, Rahman RM, Biffi A, Smith EE, Kanakis A, Fitzpatrick K et al. White matter hyperintensity volume is increased in small vessel stroke subtypes. Neurology 2010; 75: 1670-1677.
14. Lee HB, Blaufox MD. Blood volume in the rat. J Nucl Med 1985; 26: 72-76.
15. Lee SH, Kim BJ, Ryu WS, Kim CK, Kim N, Park BJ et al. White matter lesions and poor outcome after intracerebral hemorrhage: a nationwide cohort study. Neurology 2010; 74: 1502-1510.
16. Lou M, Al-Hazzani A, Goddeau RP, Jr, Novak V, Selim M. Relationship between white-matter hyperintensities and hematoma volume and growth in patients with intracerebral hemorrhage. Stroke 2010; 41: 34-40.
17. Belayev L, Saul I, Curbelo K, Busto R, Belayev A, Zhang Y et al. Experimental intracerebral hemorrhage in the mouse: histological, behavioral, and hemodynamic characterization of a double-injection model. Stroke 2003; 34: 2221-2227.
18. Ai J, Liu E, Wang J, Chen Y, Yu J, Baker AJ. Calpain inhibitor MDL-28170 reduces the functional and structural deterioration of corpus callosum following fluid percussion injury. J Neurotrauma 2007; 24: 960-978.
19. Chomiak T, Hu B. What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS ONE 2009; 4: e7754.
20. Reeves TM, Phillips LL, Povlishock JT. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp Neurol 2005; 196: 126-137.
21. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6: 258-268.
22. Wurster WL, Pyne-Geithman GJ, Peat IR, Clark JF. Bilirubin oxidation products (BOXes): synthesis, stability and chemical characteristics. Acta Neurochir Suppl 2008; 104: 43-50.
23. Kranc KR, Pyne GJ, Tao L, Claridge TD, Harris DA, Cadoux-Hudson TA et al. Oxidative degradation of bilirubin produces vasoactive compounds. Eur J Biochem 2000; 267: 7094-7101.
24. Wasserman JK, Schlichter LC. White matter injury in young and aged rats after intracerebral hemorrhage. Exp Neurol 2008; 214: 266-275.
25. Grojean S, Koziel V, Vert P, Daval JL. Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 2000; 166: 334-341.
26. Genc S, Genc K, Kumral A, Baskin H, Ozkan H. Bilirubin is cytotoxic to rat oligodendrocytes in vitro. Brain Res 2003; 985: 135-141.
27. Kumral A, Genc S, Genc K, Duman N, Tatli M, Sakizli M et al. Hyperbilirubinemic serum is cytotoxic and induces apoptosis in murine astrocytes. Biol Neonate 2005; 87: 99-104.
28. Zhang L, Liu W, Tanswell AK, Luo X. The effects of bilirubin on evoked potentials and long-term potentiation in rat hippocampus in vivo. Pediatr Res 2003; 53: 939-944.
29. Chang FY, Lee CC, Huang CC, Hsu KS. Unconjugated bilirubin exposure impairs hippocampal long-term synaptic plasticity. PLoS ONE 2009; 4: e5876.
30. Wang J, Dore S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 2007; 130: 1643-1652.
31. Fernandes A, Vaz AR, Falcao AS, Silva RF, Brito MA, Brites D. Glycoursodeoxycholic acid and interleukin-10 modulate the reactivity of rat cortical astrocytes to unconjugated bilirubin. J Neuropathol Exp Neurol 2007; 66: 789-798.
32. Clark JF, Loftspring M, Wurster WL, Beiler S, Beiler C, Wagner KR et al. Bilirubin oxidation products, oxidative stress, and intracerebral hemorrhage. Acta Neurochir Suppl 2008; 105: 7-12.
33. Loftspring MC, Johnson HL, Feng R, Johnson AJ, Clark JF. Unconjugated bilirubin contributes to early inflammation and edema after intracerebral hemorrhage. J Cereb Blood Flow Metab 2011; 31: 1133-1142.
34. Dore S, Snyder SH. Neuroprotective action of bilirubin against oxidative stress in primary hippocampal cultures. Ann NY Acad Sci 1999; 890: 167-172.
35. Neuzil J, Stocker R. Bilirubin attenuates radical-mediated damage to serum albumin. FEBS Lett 1993; 331: 281-284.
36. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235: 1043-1046.
37. Sedlak TW, Snyder SH. Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics 2004; 113: 1776-1782.
38. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 2006; 439: 988-992.
39. Notman R, Noro M, O'Malley B, Anwar J. Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J Am Chem Soc 2006; 128: 13982-13983.
40. Bardutzky J, Meng X, Bouley J, Duong TQ, Ratan R, Fisher M. Effects of intravenous dimethyl sulfoxide on ischemia evolution in a rat permanent occlusion model. J Cereb Blood Flow Metab 2005; 25: 968-977.
41. Di Giorgio AM, Hou Y, Zhao X, Zhang B, Lyeth BG, Russell MJ. Dimethyl sulfoxide provides neuroprotection in a traumatic brain injury model. Restor Neurol Neurosci 2008; 26: 501-507.
42. Howard MJ, David G, Barrett JN. Resealing of transected myelinated mammalian axons in vivo: evidence for involvement of calpain. Neuroscience 1999; 93: 807-815.
43. Lu C, Mattson MP. Dimethyl sulfoxide suppresses NMDA-and AMPA-induced ion currents and calcium influx and protects against excitotoxic death in hippocampal neurons. Exp Neurol 2001; 170: 180-185.