Microglia regulate blood clearance in subarachnoid hemorrhage by heme oxygenase-1

Journal of Clinical Investigation

Volumn 125, Issue 7, 2015, Pages 2609-2625

  Schallner, Nils ^a,b   Pandit, Rambhau ^a   LeBlanc, Robert ^a   Thomas, Ajith J ^a   Ogilvy, Christopher S ^a   Zuckerbraun, Brian S ^c   Gallo, David ^a   Otterbein, Leo E ^a,d   Hanafy, Khalid A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d ASTON UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE 1; ENZYME INHIBITOR; HMOX1 PROTEIN, HUMAN; HMOX1 PROTEIN, MOUSE; MEMBRANE PROTEIN; METALLOPORPHYRIN; PROTOPORPHYRIN; PROTOPORPHYRIN TIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN ARTERY ANEURYSM; BRAIN HEMATOMA; CELL DEATH; CEREBROSPINAL FLUID; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; ERYTHROPHAGOCYTOSIS; FEMALE; MICROGLIA; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PLASMA CLEARANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBARACHNOID HEMORRHAGE; VASOSPASM; ACUTE PHASE RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; ERYTHROCYTE; HUMAN; INTRACRANIAL ANEURYSM; KNOCKOUT MOUSE; MALE; MAZE TEST; METABOLISM; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY;

ACUTE-PHASE REACTION; ANIMALS; APOPTOSIS; CARBON MONOXIDE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; ERYTHROCYTES; FEMALE; HEME OXYGENASE-1; HUMANS; INTRACRANIAL ANEURYSM; MALE; MAZE LEARNING; MEMBRANE PROTEINS; METALLOPORPHYRINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; PHAGOCYTOSIS; PROTOPORPHYRINS; SUBARACHNOID HEMORRHAGE;

EID: 84936817005     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI78443     Document Type: Article

References (75)

1. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest. 1999;103(7):1047-1054.
2. Zuckerbraun BS, et al. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med. 2003;198(11):1707-1716.
3. Tayem Y, Green CJ, Motterlini R, Foresti R. Isothiocyanate-cysteine conjugates protect renal tissue against cisplatin-induced apoptosis via induction of heme oxygenase-1. Pharmacol Res. 2014;81:1-9.
4. Clark JE, Foresti R, Sarathchandra P, Kaur H, Green CJ, Motterlini R. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol. 2000;278(2):H643-H651.
5. Wegiel B, Nemeth Z, Correa-Costa M, Bulmer AC, Otterbein LE. Heme oxygenase-1: A metabolic nike. Antioxid Redox Signal. 2014;20(11):1709-1722.
6. Sun MH, et al. Retinal protection from acute glaucoma-induced ischemia-reperfusion injury through pharmacologic induction of heme oxygenase-1. Invest Ophthalmol Vis Sci. 2010;51(9):4798-4808.
7. Shimada Y, Tsunoda H, Zang L, Hirano M, Oka T, Tanaka T. Synergistic induction of heme oxygenase-1 by nicaraven after subarachnoid hemorrhage to prevent delayed cerebral vasospasm. Eur J Pharmacol. 2009;620(1-3):16-20.
8. Zhang F, et al. Pharmacological induction of heme oxygenase-1 by a triterpenoid protects neurons against ischemic injury. Stroke. 2012;43(5):1390-1397.
9. Saleem S, Zhuang H, Biswal S, Christen Y, Dore S. Ginkgo biloba extract neuroprotective action is dependent on heme oxygenase 1 in ischemic reperfusion brain injury. Stroke. 2008;39(12):3389-3396.
10. Wang HQ, Xu YX, Zhu CQ. Upregulation of heme oxygenase-1 by acteoside through ERK PI3 K/ Akt pathway confer neuroprotection against beta-amyloid-induced neurotoxicity. Neurotox Res. 2012;21(4):368-378.
11. Chen G, Fang Q, Zhang J, Zhou D, Wang Z. Role of the Nrf2-ARE pathway in early brain injury after experimental subarachnoid hemorrhage. J Neurosci Res. 2011;89(4):515-523.
12. Foresti R, et al. Small molecule activators of the Nrf2-HO-1 antioxidant axis modulate heme metabolism inflammation in BV2 microglia cells. Pharmacol Res. 2013;76:132-148.
13. Sutherland BA, Rahman RM, Clarkson AN, Shaw OM, Nair SM, Appleton I. Cerebral heme oxygenase 1 and 2 spatial distribution is modulated following injury from hypoxia-ischemia middle cerebral artery occlusion in rats. Neurosci Res. 2009;65(4):326-334.
14. Matz P, Turner C, Weinstein PR, Massa SM, Panter SS, Sharp FR. Heme-oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. Brain Res. 1996;713(1-2):211-222.
15. Takeda A, Kimpara T, Onodera H, Itoyama Y, Shibahara S, Kogure K. Regional difference in induction of heme oxygenase-1 protein following rat transient forebrain ischemia. Neurosci Lett. 1996;205(3):169-172.
16. Turner CP, Panter SS, Sharp FR. Anti-oxidants prevent focal rat brain injury as assessed by induction of heat shock proteins (HSP70, HO-1/ HSP32, HSP47) following subarachnoid injections of lysed blood. Brain Res Mol Brain Res. 1999;65(1):87-102.
17. Matz PG, Weinstein PR, Sharp FR. Heme oxygenase-1 and heat shock protein 70 induction in glia neurons throughout rat brain after experimental intracerebral hemorrhage. Neurosurgery. 1997;40(1):152-160.
18. Fukuda K, Panter SS, Sharp FR, Noble LJ. Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci Lett. 1995;199(2):127-130.
19. Kuroki M, Kanamaru K, Suzuki H, Waga S, Semba R. Effect of vasospasm on heme oxygenases in a rat model of subarachnoid hemorrhage. Stroke. 1998;29(3):683-688.
20. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol. 1999;276(4 pt 1):L688-L694.
21. Otterbein LE, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000;6(4):422-428.
22. Song R, et al. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am J Pathol. 2003;163(1):231-242.
23. Zhang X, Shan P, Alam J, Davis RJ, Flavell RA, Lee PJ. Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen-activated protein kinase pathway during ischemia-reperfusion lung injury. J Biol Chem. 2003;278(24):22061-22070.
24. Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev. 2005;57(4):585-630.
25. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/ carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86(2):583-650.
26. Goebel U, et al. Carbon monoxide inhalation reduces pulmonary inflammatory response during cardiopulmonary bypass in pigs. Anesthesiology. 2008;108(6):1025-1036.
27. Yabluchanskiy A, Sawle P, Homer-Vanniasinkam S, Green CJ, Foresti R, Motterlini R. CORM-3, a carbon monoxide-releasing molecule, alters the inflammatory response reduces brain damage in a rat model of hemorrhagic stroke. Crit Care Med. 2012;40(2):544-552.
28. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 2010;9(9):728-743.
29. Vieira HL, Queiroga CS, Alves PM. Pre-conditioning induced by carbon monoxide provides neuronal protection against apoptosis. J Neurochem. 2008;107(2):375-384.
30. Almeida AS, Queiroga CS, Sousa MF, Alves PM, Vieira HL. Carbon monoxide modulates apoptosis by reinforcing oxidative metabolism in astrocytes: role of Bcl-2. J Biol Chem. 2012;287(14):10761-10770.
31. Zeynalov E, Dore S. Low doses of carbon monoxide protect against experimental focal brain ischemia. Neurotox Res. 2009;15(2):133-137.
32. Biermann J, Lagreze WA, Dimitriu C, Stoykow C, Goebel U. Preconditioning with inhalative carbon monoxide protects rat retinal ganglion cells from ischemia/reperfusion injury. Invest Ophthalmol Vis Sci. 2010;51(7):3784-3791.
33. Mildner A, et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci. 2007;10(12):1544-1553.
34. Roof RL, Hall ED. Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J Neurotrauma. 2000;17(5):367-388.
35. Brouard S, et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 2000;192(7):1015-1026.
36. Dallas ML, et al. Carbon monoxide protects against oxidant-induced apoptosis via inhibition of Kv2.1. FASEB J. 2011;25(5):1519-1530.
37. Ogawa T, et al. Protein therapy using hemeoxygenase-1 fused to a polyarginine transduction domain attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2011;31(11):2231-2242.
38. Liu Y, Zhang Z, Luo B, Schluesener HJ, Zhang Z. Lesional accumulation of heme oxygenase-1+ microglia/macrophages in rat traumatic brain injury. Neuroreport. 2013;24(6):281-286.
39. Parada E, et al. The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal. 2013;19(11):1135-1148.
40. Nakaso K, et al. Co-induction of heme oxygenase-1 and peroxiredoxin I in astrocytes microglia around hemorrhagic region in the rat brain. Neurosci Lett. 2000;293(1):49-52.
41. Beck K, et al. Interplay between heme oxygenase-1 and the multifunctional transcription factor yin yang 1 in the inhibition of intimal hyperplasia. Circ Res. 2010;107(12):1490-1497.
42. Collinson EJ, et al. The yeast homolog of heme oxygenase-1 affords cellular antioxidant protection via the transcriptional regulation of known antioxidant genes. J Biol Chem. 2011;286(3):2205-2214.
43. Lin Q, et al. Heme oxygenase-1 protein localizes to the nucleus activates transcription factors important in oxidative stress. J Biol Chem. 2007;282(28):20621-20633.
44. Lin QS, Weis S, Yang G, Zhuang T, Abate A, Dennery PA. Catalytic inactive heme oxygenase-1 protein regulates its own expression in oxidative stress. Free Radic Biol Med. 2008;44(5):847-855.
45. Basuroy S, et al. HO-2 provides endogenous protection against oxidative stress apoptosis caused by TNF-alpha in cerebral vascular endothelial cells. Am J Physiol Cell Physiol. 2006;291(5):C897-C908.
46. Chang EF, et al. Heme oxygenase-2 protects against lipid peroxidation-mediated cell loss impaired motor recovery after traumatic brain injury. J Neurosci. 2003;23(9):3689-3696.
47. Zakhary R, Poss KD, Jaffrey SR, Ferris CD, Tonegawa S, Snyder SH. Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide. Proc Natl Acad Sci U S A. 1997;94(26):14848-14853.
48. King JT Jr. Epidemiology of aneurysmal subarachnoid hemorrhage. Neuroimaging Clin N Am. 1997;7(4):659-668.
49. Rincon F, Rossenwasser RH, Dumont A. The epidemiology of admissions of nontraumatic subarachnoid hemorrhage in the United States. Neurosurgery. 2013;73(2):217-222.
50. Hijdra A, Van Gijn J, Stefanko S, Van Dongen KJ, Vermeulen M, Van Crevel H. Delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: clinicoanatomic correlations. Neurology. 1986;36(3):329-333.
51. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg. 1990;73(1):18-36.
52. Rosengart AJ, et al. Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg. 2007;107(2):253-260.
53. Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658-667.
54. Macdonald RL, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebocontrolled phase 2 dose-finding trial. Stroke. 2008;39(11):3015-3021.
55. Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and-independent effects. Stroke. 2011;42(4):924-929.
56. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med. 2011;17(7):796-808.
57. Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44-58.
58. Hanafy KA. The role of microglia and the TLR4 pathway in neuronal apoptosis vasospasm after subarachnoid hemorrhage. J Neuroinflammation. 2013;10:83.
59. Vinet J, et al. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation. 2012;9:27.
60. Montero M, Gonzalez B, Zimmer J. Immunotoxic depletion of microglia in mouse hippocampal slice cultures enhances ischemia-like neurodegeneration. Brain Res. 2009;1291:140-152.
61. Boscia F, Esposito CL, Di Crisci A, de Franciscis V, Annunziato L, Cerchia L. GDNF selectively induces microglial activation and neuronal survival in CA1/CA3 hippocampal regions exposed to NMDA insult through Ret/ERK signalling. PLoS One. 2009;4(8):e6486.
62. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci. 2007;10(12):1538-1543.
63. Soulet D, Rivest S. Bone-marrow-derived microglia: myth or reality? Curr Opin Pharmacol. 2008;8(4):508-518.
64. Kristiansen M, et al. Identification of the haemoglobin scavenger receptor. Nature. 2001;409(6817):198-201.
65. Zhao X, et al. Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann Neurol. 2007;61(4):352-362.
66. Figueiredo RT, et al. Characterization of heme as activator of Toll-like receptor 4. J Biol Chem. 2007;282(28):20221-20229.
67. D'Amico G, Lam F, Hagen T, Moncada S. Inhibition of cellular respiration by endogenously produced carbon monoxide. J Cell Sci. 2006;119(pt 11):2291-2298.
68. Wegiel B, et al. Heme oxygenase-1 derived carbon monoxide permits maturation of myeloid cells. Cell Death Dis. 2014;5:e1139.
69. Smith A, Wu AH, Lynch KL, Ko N, Grenache DG. Multi-wavelength spectrophotometric analysis for detection of xanthochromia in cerebrospinal fluid and accuracy for the diagnosis of subarachnoid hemorrhage. Clin Chim Acta. 2013;424:231-236.
70. Jung S, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20(11):4106-4114.
71. Imai T, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration adhesion. Cell. 1997;91(4):521-530.
72. Fong AM, et al. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, activation under physiologic flow. J Exp Med. 1998;188(8):1413-1419.
73. Foussat A, et al. Fractalkine receptor expression by T lymphocyte subpopulations and in vivo production of fractalkine in human. Eur J Immunol. 2000;30(1):87-97.
74. Tong N, et al. Neuronal fractalkine expression in HIV-1 encephalitis: roles for macrophage recruitment neuroprotection in the central nervous system. J Immunol. 2000;164(3):1333-1339.
75. Harrison JK, et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A. 1998;95(18):10896-10901.