Genetic ablation of steroid receptor coactivator-3 promotes PPAR-β-mediated alternative activation of microglia in experimental autoimmune encephalomyelitis

GLIA

Volumn 58, Issue 8, 2010, Pages 932-942

  Xiao, Yichuan ^a   Xu, Jingwei ^a   Wang, Shu ^b,c   Mao, Chaoming ^a   Jin, Min ^a   Ning, Guang ^b,c   Xu, Jianming ^d   Zhang, Yanyun ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI UNIVERSITY OF MEDICINE AND HEALTH SCIENCES   (China)

^c SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Alternative activation; EAE; Microglia; PPAR ; SRC 3

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1QA; COMPLEMENT COMPONENT C1QB; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELIN; OPSONIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; RANTES; STEROID RECEPTOR COACTIVATOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEMYELINATION; DISEASE COURSE; DISEASE SEVERITY; GENE EXPRESSION REGULATION; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY INFILTRATE; LIPID METABOLISM; METABOLIC REGULATION; MICROGLIA; MOUSE; NERVE REGENERATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; T LYMPHOCYTE; UPREGULATION; WHITE MATTER;

ANALYSIS OF VARIANCE; ANIMALS; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLYCOPROTEINS; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MYELIN SHEATH; NUCLEAR RECEPTOR COACTIVATOR 3; PEPTIDE FRAGMENTS; PPAR-BETA; RNA, MESSENGER;

EID: 77952571744     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20975     Document Type: Article

References (48)

1. Adibhatla RM, Hatcher JF. 2007. Role of lipids in brain injury diseases. Future Lipidol 2:403-422.
2. Aharoni R, Herschkovitz A, Eilam R, Blumberg-Hazan M, Sela M, Bruck W, Arnon R. 2008. Demyelination arrest and remyelination induced by glatiramer acetate treatment of experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 105:11358-11363.
3. Becher B, Prat A, Antel JP. 2000. Brain-immune connection: Immunoregulatory properties of CNS-resident cells. Glia 29:293-304.
4. Bensinger SJ, Tontonoz P. 2008. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454:470-477.
5. Bright JJ, Du C, Coon M, Sriram S, Klaus SJ. 1998. Prevention of experimental allergic encephalomyelitis via inhibition of IL-12 signaling and IL-12-mediated Th1 differentiation: An effect of the novel antiinflammatory drug lisofylline. J Immunol 161:7015-7022. (Pubitemid 28562251)
6. Butovsky O, Landa G, Kunis G, Ziv Y, Avidan H, Greenberg N, Schwartz A, Smirnov I, Pollack A, Jung S, Schwartz M. 2006. Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116:905-915.
7. Carson MJ. 2002. Microglia as liaisons between the immune and central nervous systems: Functional implications for multiple sclerosis. Glia 40:218-231.
8. Carter SL, Müller M, Manders PM, Campbell IL. 2007. Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-γ but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia 55:1728-1739.
9. Coste A, Louet JF, Lagouge M, Lerin C, Antal MC, Meziane H, Schoonjans K, Puigserver P, O'Malley BW, Auwerx J. 2008. The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1α. Proc Natl Acad Sci USA 105:17187-17192.
10. 12,14-prostaglandin J2 ameliorates experimental autoimmune encephalomyelitis. J Immunol 168:2508-2515.
11. Evans RM, Barish GD, Wang YX. 2004. PPARs and the complex journey to obesity. Nat Med 10:1-7.
12. Franklin RJ, Ffrench-Constant C. 2008. Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 9:839-855.
13. Gerard C, Rollins BJ. 2001. Chemokines and disease. Nat Immunol 2:108-115.
14. Girard C, Bemelmans AP, Dufour N, Mallet J, Bachelin C, Nait Oumesmar B, Baron Van Evercooren A, Lachapelle F. 2005. Grafts of brainderived neurotrophic factor and neurotrophin 3-transduced primate schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J Neurosci 25:7924-7933.
15. Gocke AR, Hussain RZ, Yang Y, Peng H, Weiner J, Ben LH, Drew PD, Stuve O, Lovett-Racke AE, Racke MK. 2009. Transcriptional modulation of the immune response by peroxisome proliferator-activated receptor- α agonists in autoimmune disease. J Immunol 182:4479-4487.
16. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3:23-35.
17. Hemmer B, Archelos JJ, Hartung HP. 2002. New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 3:291-301. (Pubitemid 135706608)
18. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hövelmeyer N, Waisman A, Rülicke T, Prinz M, Priller J, Becher B, Aguzzi A. 2005. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 11:146-152.
19. Jurevics H, Largent C, Hostettler J, Sammond DW, Matsushima GK, Kleindienst A, Toews AD, Morell P. 2002. Alterations in metabolism and gene expression in brain regions during cuprizone-induced demyelination and remyelination. J Neurochem 82:126-136.
20. Kang K, Reilly SM, Karabacak V, Gangl MR, Fitzgerald K, Hatano B, Lee CH. 2008. Adipocyte-derived Th2 cytokines and myeloid PPARd regulate macrophage polarization and insulin sensitivity. Cell Metab 7:485-495.
21. Kassiotis G, Kranidioti K, Kollias G. 2001. Defective CD4T cell priming and resistance to experimental autoimmune encephalomyelitis in TNF-deficient mice due to innate immune hypo-responsiveness. J Neuroimmunol 119:239-247.
22. Lee CH, Olson P, Hevener A, Mehl I, Chong LW, Olefsky JM, Gonzalez FJ, Ham J, Kang H, Peters JM, Evans RM. 2006. PPARd regulates glucose metabolism and insulin sensitivity. Proc Natl Acad Sci USA 103:3444-3449.
23. Lees JR, Golumbek PT, Sim J, Dorsey D, Russell JH. 2008. Regional CNS responses to IFN-γ determine lesion localization patterns during EAE pathogenesis. J Exp Med 205:2633-2642.
24. Lerin C, Rodgers JT, Kalume DE, Kim SH, Pandey A, Puigserver P. 2006. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha. Cell Metab 3:429-438.
25. Li B, Reynolds JM, Stout RD, Bernlohr DA, Suttles J. 2009. Regulation of Th17 differentiation by epidermal fatty acid-binding protein. J Immunol 182:7625-7633.
26. Lin W, Kemper A, Dupree JL, Harding HP, Ron D, Popko B. 2006. Interferon-g inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 129:1306-1318.
27. Ling EA, Wong WC. 1993. The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7:9-18.
28. Louet J, Coste A, Amazit L, Tannour-Louet M, Wu R, Tsai SY, Tsai M, Auwerx J, O'Malley BW. 2006. Oncogenic steroid receptor coactivator-3 is a key regulator of the white adipogenic program. Proc Natl Acad Sci USA 103:17868-17873.
29. Makowski L, Brittingham KC, Reynolds JM, Suttles J, Hotamisligil GS. 2005. The fatty acid-binding protein, aP2, coordinates macrophage cholesterol trafficking and inflammatory activity: Macrophage expression of aP2 impacts peroxisome proliferator-activated receptor γ and IκB kinase activities. J Biol Chem 280:12888-12895.
30. Michalik L, Wahli W. 2006. Involvement of PPAR nuclear receptors in tissue injury and wound repair. J Clin Invest 116:598-606.
31. Mukundan L, Odegaard JI, Morel CR, Heredia JE, Mwangi JW, Ricardo-Gonzalez RR, Goh YP, Eagle AR, Dunn SE, Awakuni JU, Nguyen KD, Steinman L, Michie SA, Chawla A. 2009. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat Med 15:1266-1272.
32. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, Vats D, Morel CR, Goforth MH, Subramanian V, Mukundan L, Ferrante AW, Chawla A. 2008. Alternative M2 activation of Kupffer cells by PPARd ameliorates obesity-induced insulin resistance. Cell Metab 7:496-507.
33. Omoúlu S, Yardimci S, Oku Z. 2004. Body fat distribution and plasma lipid profiles of patients with multiple sclerosis. Turk J Med Sci 34:43-48. (Pubitemid 38295498)
34. Pan D, Fujimoto M, Lopes A, Wang YX. 2009. Twist-1 is a PPARd-inducible, negative-feedback regulator of PGC-1a in brown fat metabolism. Cell 137:73-86.
35. Polak PE, Kalinin S, Dello Russo C, Gavrilyuk V, Sharp A, Peters JM, Richardson J, Willson TM, Weinberg G, Feinstein DL. 2005. Protective effects of a peroxisome proliferator-activated receptor-β/δ agonist in experimental autoimmune encephalomyelitis. J Neuroimmunol 168:65-75.
36. Ponomarev ED, Maresz K, Tan Y, Dittel BN. 2007. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci 27:10714-10721.
37. Ponomarev ED, Novikova M, Maresz K, Shriver L, Dittel BN. 2005. Development of a culture system that supports adult microglial cell proliferation and maintenance in the resting state. J Immunol Methods 300:32-46.
38. Popovich PG, Longbrake EE. 2008. Can the immune system be harnessed to repair the CNS? Nat Rev Neurosci 9:481-493.
39. Sobrado M, Pereira MP, Ballesteros I, Hurtado O, Fernández- López D, Pradillo JM, Caso JR, Vivancos J, Nombela F, Serena J, Lizasoain I, Moro MA. 2009. Synthesis of lipoxin A4 by 5-lipoxygenase mediates PPARg-dependent, neuroprotective effects of rosiglitazone in experimental stroke. J Neurosci 29:3875-3884.
40. Tan NS, Michalik L, Noy N, Yasmin R, Pacot C, Heim M, Flühmann B, Desvergne B, Wahli W. 2001. Critical roles of PPAR b/d in keratinocyte response to inflammation. Genes Dev 15:3263-3277.
41. Van't Veer A, Du Y, Fischer TZ, Boetig DR, Wood MR, Dreyfus CF. 2009. Brain-derived neurotrophic factor effects on oligodendrocyte progenitors of the basal forebrain are mediated through trkB and the MAP kinase pathway. J Neurosci Res 87:69-78.
42. Wang Z, Rose DW, Hermanson O, Liu F, Herman T, Wu W, Szeto D, Gleiberman A, Krones A, Pratt K, Rosenfeld R, Glass CK, Rosenfeld MG. 2000. Regulation of somatic growth by the p160 coactivator p/ CIP. Proc Natl Acad Sci USA 97:13549-13554.
43. Webb M, Luo L, Ma JY, Tham CS. 2008. Genetic deletion of fatty acid amide hydrolase results in improved long-term outcome in chronic autoimmune encephalitis. Neurosci Lett 439:106-110.
44. Wheeler D, Bandaru VV, Calabresi PA, Nath A, Haughey NJ. 2008. A defect of sphingolipid metabolism modifies the properties of normal appearing white matter in multiple sclerosis. Brain 131:3092-3102.
45. White AB, Givogri MI, Lopez-Rosas A, Cao H, van Breemen R, Thinakaran G, Bongarzone ER. 2009. Psychosine accumulates in membrane microdomains in the brain of krabbe patients, disrupting the raft architecture. J Neurosci 29:6068-6077.
46. Wu RC, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, O'Malley BW. 2004. Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways. Mol Cell 15:937-949.
47. Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O'Malley BW. 2000. The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/ TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc Natl Acad Sci USA 97:6379-6384.
48. Yu C, York B, Wang S, Feng Q, Xu J, O'Malley BW. 2007. An essential function of the SRC-3 coactivator in suppression of cytokine mRNA translation and inflammatory response. Mol Cell 25:765-778.