Astrocytes induce hemeoxygenase-1 expression in microglia: A feasible mechanism for preventing excessive brain inflammation

Journal of Neuroscience

Volumn 26, Issue 6, 2006, Pages 1880-1887

  Min, Kyoung Jin ^a   Yang, Myung Soon ^a   Kim, Seung Up ^a,b   Jou, Ilo ^a   Joe, Eun Hye ^a,c  

^a Ajou University School of Medicine   (South Korea)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c NONE   (South Korea)

Author keywords

Astrocyte; Brain inflammation; Cell cell interaction; Hemeoxygenase 1; Microglia; Reactive oxygen species

Indexed keywords

BILIRUBIN; CARBON MONOXIDE; FERROUS ION; GAMMA INTERFERON; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NUCLEAR FACTOR E2 RELATED FACTOR 2 TRANSCRIPTION FACTOR; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTROCYTE; BINDING AFFINITY; BRAIN; BRAIN PROTECTION; CONTROLLED STUDY; CULTURE MEDIUM; ENCEPHALITIS; ENZYME ACTIVITY; ENZYME INDUCTION; FEASIBILITY STUDY; MACROPHAGE ACTIVATION; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT;

ACTINS; ANIMALS; ASTROCYTES; CELL CULTURE TECHNIQUES; CEREBRAL CORTEX; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; ENCEPHALITIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; MICROGLIA; MODELS, NEUROLOGICAL; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 32544455798     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3696-05.2006     Document Type: Article

References (61)

1. Aktan F (2004) iNOS-mediated nitric oxide production and its regulation. Life Sci 75:639-653.
2. Alam J (1994) Multiple elements within the 5′ distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals. J Biol Chem 269:25049-25056.
3. Alam J, Cook JL (2003) Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9:2499-2511.
4. Alam J, Camhi S, Choi AM (1995) Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcription enhancer. J Biol Chem 270:11977-11984.
5. Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AM, Burow ME, Tou J (2000) Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J Biol Chem 275:27694-27702.
6. Alam J, Killeen E, Gong P, Naquin R, Hu B, Stewart D, Ingelfinger JR, Nath KA (2003) Heme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2. Am J Physiol Renal Physiol 284:F743-F752.
7. Aloisi F, Penna G, Cerase J, Menendez IB, Adorini L (1997) IL-12 production by central nervous system microglia is inhibited by astrocytes. J Immunol 159:1604-1612.
8. Beschorner R, Adjodah D, Schwab JM, Mittelbronn M, Pedal I, Mattern R, Schluesener HJ, Meyermann R (2000) Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol (Berl) 100:377-384.
9. Canolle B, Masmejean F, Melon C, Nieoullon A, Pisano P, Lortet S (2004) Glial soluble factors regulate the activity and expression of the neuronal glutamate transporter EAAC1: implication of cholesterol. J Neurochem 88:1521-1532.
10. Chapman JT, Otterbein LE, Elias JA, Choi AM (2001) Carbon monoxide attenuates aeroallergen-induced inflammation in mice. Am J Physiol Lung Cell Mol Physiol 281:L209-L216.
11. Daley JM, Reichner JS, Mahoney EJ, Manfield L, Henry Jr WL, Mastrofrancesco B, Albina JE (2005) Modulation of macrophage phenotype by soluble product(s) released from neutrophils. J Immunol 174:2265-2272.
12. Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429-440.
13. Daniels M, Brown DR (2001) Astrocytes regulate N-methyl-D-aspartate receptor subunit composition increasing neuronal sensitivity to excitotoxicity. J Biol Chem 276:22446 -22452.
14. Dennery PA, Sridhar KJ, Lee CS, Wong HE, Shokoohi V, Rodgers PA, Spitz DR (1997) Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem 272:14937-14942.
15. Dhandapani KM, Hadman M, De SL, Wade MF, Mahesh VB, Brann DW (2003) Astrocyte protection of neurons: role of transforming growth factor-beta signaling via a c-Jun-AP-1 protective pathway. J Biol Chem 278:43329-43339.
16. Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141:2407-2412.
17. Eriksen JL, Druse MJ (2001) Astrocyte-mediated trophic support of developing serotonin neurons: effects of ethanol, buspirone, and S100B. Brain Res Dev Brain Res 131:9-15.
18. Giulian D, Baker TJ (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163-2178.
19. Gonzalez-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219-240.
20. Hill-Kapturczak N, Truong L, Thamilselvan V, Visner GA, Nick HS, Agarwal A (2000) Smad7-dependent regulation of heme oxygenase-1 by transforming growth factor-beta in human renal epithelial cells. J Biol Chem 275:40904-40909.
21. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313-322.
22. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13:76-86.
23. Jyonouchi H, Sun S, Le H (2001) Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression. J Neuroimmunol 120:170-179.
24. Kang J, Yang M, Jou I, Joe E (2001) Identification of protein kinase C isoforms involved in interferon-gamma-induced expression of inducible nitric oxide synthase in murine BV2 microglia. Neurosci Lett 299:205-208.
25. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A (2004) Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165:1045-1053.
26. Kesslak JP, Nieto-Sampedro M, Globus J, Cotman CW (1986) Transplants of purified astrocytes promote behavioral recovery after frontal cortex ablation. Exp Neurol 92:377-390.
27. Kimura M, Soeda S, Oda M, Ochiai T, Kihara T, Ono N, Shimeno H (2000) Release of plasminogen activator inhibitor-1 from human astrocytes is regulated by intracellular ceramide. J Neurosci Res 62:781-788.
28. Koistinaho J, Miettinen S, Keinanen R, Vartiainen N, Roivainen R, Laitinen JT (1996) Long-term induction of haem oxygenase-1 (HSP-32) in astrocytes and microglia following transient focal brain ischaemia in the rat. Eur J Neurosci 8:2265-2272.
29. Kutty RK, Maines MD (1982) Oxidation of heme c derivatives by purified heme oxygenase. Evidence for the presence of one molecular species of heme oxygenase in the rat liver. J Biol Chem 257:9944-9952.
30. Langeveld CH, Jongenelen CA, Schepens E, Stoof JC, Bast A, Drukarch B (1995) Cultured rat striatal and cortical astrocytes protect mesencephalic dopaminergic neurons against hydrogen peroxide toxicity independent of their effect on neuronal development. Neurosci Lett 192:13-16.
31. Lee PJ, Alam J, Wiegand GW, Choi AM (1996) Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA 93:10393-10398.
32. Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA 96:7526-7531.
33. Liu Y, Zhu B, Wang X, Luo L, Li P, Paty DW, Cynader MS (2003) Bilirubin as a potent antioxidant suppresses experimental autoimmune encephalomyelitis: implications for the role of oxidative stress in the development of multiple sclerosis. J Neuroimmunol 139:27-35.
34. Maes M (1995) Evidence for an immune response in major depression: a review and hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 19:11-38.
35. Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2:2557-2568.
36. Meda L, Cassatella MA, Szendrei GI, Otvos Jr L, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
37. Min KJ, Jou I, Joe E (2003) Plasminogen-induced IL-1beta and TNF-alpha production in microglia is regulated by reactive oxygen species. Biochem Biophys Res Commun 312:969-974.
38. Min KJ, Pyo HK, Yang MS, Ji KA, Jou I, Joe EH (2004) Gangliosides activate microglia via protein kinase C and NADPH oxidase. Glia 48:197-206.
39. Minghetti L, Polazzi E, Nicolini A, Levi G (1998) Opposite regulation of prostaglandin E2 synthesis by transforming growth factor-beta1 and interleukin 10 in activated microglial cultures. J Neuroimmunol 82:31-39.
40. Nath KA, Vercellotti GM, Grande JP, Miyoshi H, Paya CV, Manivel JC, Haggard JJ, Croatt AJ, Payne WD, Alam J (2001) Heme protein-induced chronic renal inflammation: suppressive effect of induced heme oxygenase-1. Kidney Int 59:106-117.
41. Ott MC, Scott JR, Bihari A, Badhwar A, Otterbein LE, Gray DK, Harris KA, Potter RF (2005) Inhalation of carbon monoxide prevents liver injury and inflammation following hind limb ischemia/reperfusion. FASEB J 19:106-108.
42. Panahian N, Yoshiura M, Maines MD (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72:1187-1203.
43. Pier GB, Markham RB, Eardley D (1981) Correlation of the biologic responses of C3H/HEJ mice to endotoxin with the chemical and structural properties of the lipopolysaccharides from Pseudomonas aeruginosa and Escherichia coli. J Immunol 127:184-191.
44. Pyo H, Jou I, Jung S, Hong S, Joe EH (1998) Mitogen-activated protein kinases activated by lipopolysaccharide and beta-amyloid in cultured rat microglia. NeuroReport 9:871-874.
45. Pyo H, Yang MS, Jou I, Joe EH (2003) Wortmannin enhances lipopolysaccharide-induced inducible nitric oxide synthase expression in microglia in the presence of astrocytes in rats. Neurosci Lett 346:141-144.
46. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS (2004) NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279:1415-1421.
47. Reuss B, Unsicker K (2000) Survival and differentiation of dopaminergic mesencephalic neurons are promoted by dopamine-mediated induction of FGF-2 in striatal astroglial cells. Mol Cell Neurosci 16:781-792.
48. Ryu J, Pyo H, Jou I, Joe E (2000) Thrombin induces NO release from cultured rat microglia via protein kinase C, mitogen-activated protein kinase, and NF-kappa B. J Biol Chem 275:29955-29959.
49. Sawle P, Foresti R, Mann BE, Johnson TR, Green CJ, Motterlini R (2005) Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages. Br J Pharmacol 145:800-810.
50. Suh JH, Shenvi SV, Dixon BM, Liu H, Jaiswal AK, Liu RM, Hagen TM (2004) Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci USA 101:3381-3386.
51. Tanaka J, Toku K, Zhang B, Ishihara K, Sakanaka M, Maeda N (1999) Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia 28:85-96.
52. Tran ND, Correale J, Schreiber SS, Fisher M (1999) Transforming growth factor-beta mediates astrocyte-specific regulation of brain endothelial anticoagulant factors. Stroke 30:1671-1678.
53. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57:67-81.
54. Vesce S, Bezzi P, Volterra A (1999) The active role of astrocytes in synaptic transmission. Cell Mol Life Sci 56:991-1000.
55. Vila M, Jackson-Lewis V, Guegan C, Wu DC, Teismann P, Choi DK, Tieu K, Przedborski S (2001) The role of glial cells in Parkinson's disease. Curr Opin Neurol 14:483-489.
56. Vincent VA, Van Dam AM, Persoons JH, Schotanus K, Steinbusch HW, Schoffelmeer AN, Berkenbosch F (1996) Gradual inhibition of inducible nitric oxide synthase but not of interleukin-1 beta production in rat microglial cells of endotoxin-treated mixed glial cell cultures. Glia 17:94-102.
57. Vincent VA, Tilders FJ, Van Dam AM (1997) Inhibition of endotoxin-induced nitric oxide synthase production in microglial cells by the presence of astroglial cells: a role for transforming growth factor beta. Glia 19:190-198.
58. Wang WW, Smith DL, Zucker SD (2004) Bilirubin inhibits iNOS expression and NO production in response to endotoxin in rats. Hepatology 40:424-433.
59. Ward RJ, Kuhn LC, Kaldy P, Florence A, Peters TJ, Crichton RR (1994) Control of cellular iron homeostasis by iron-responsive elements in vivo. Eur J Biochem 220:927-931.
60. Willis D, Moore AR, Frederick R, Willoughby DA (1996) Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 2:87-90.
61. Yamauchi T, Lin Y, Sharp FR, Noble-Haeusslein LJ (2004) Hemin induces heme oxygenase-1 in spinal cord vasculature and attenuates barrier disruption and neutrophil infiltration in the injured murine spinal cord. J Neurotrauma 21:1017-1030.