Developmental endothelial locus-1 is a homeostatic factor in the central nervous system limiting neuroinflammation and demyelination

Molecular Psychiatry

Volumn 20, Issue 7, 2015, Pages 880-888

  Choi, E Y ^a,b,c   Lim, J H ^c   Neuwirth, A ^c   Economopoulou, M ^c   Chatzigeorgiou, A ^c   Chung, K J ^c   Bittner, S ^d   Lee, S H ^a   Langer, H ^b,e   Samus, M ^c   Kim, H ^a   Cho, G S ^a   Ziemssen, T ^c   Bdeir, K ^f   Chavakis, E ^g   Koh, J Y ^a   Boon, L ^h   Hosur, K ⁱ   Bornstein, S R ^c   Meuth, S G ^d   Hajishengallis, G ⁱ   Chavakis, T ^b,c,j   more..

^a University of Ulsan College of Medicine   (South Korea)

^b NATIONAL CANCER INSTITUTE   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g GOETHE UNIVERSITY   (Germany)

^h BIOCEROS   (Netherlands)

ⁱ UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

^j CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; DEVELOPMENTAL ENDOTHELIAL LOCUS 1; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CARRIER PROTEIN; EDIL3 PROTEIN, MOUSE; IL17R PROTEIN, MOUSE; INTERLEUKIN 17 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FLOW CYTOMETRY; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; MACROPHAGE; MONOCYTE; MOUSE; MULTIPLE SCLEROSIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; ANIMAL; AXON; C57BL MOUSE; CAPILLARY PERMEABILITY; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETICS; GRANULOCYTE; HOMEOSTASIS; IMMUNOMODULATION; KNOCKOUT MOUSE; METABOLISM; MYELIN SHEATH; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX;

ANIMALS; AXONS; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CARRIER PROTEINS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GRANULOCYTES; HOMEOSTASIS; INTERLEUKIN-17; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN SHEATH; NEUROIMMUNOMODULATION; NEUTROPHILS; RECEPTORS, INTERLEUKIN-17; SEVERITY OF ILLNESS INDEX; SPINAL CORD;

EID: 84932199529     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2014.146     Document Type: Article

References (50)

1. Rebenko-Moll NM, Liu L, Cardona A, Ransohoff RM. Chemokines mononuclear cells and the nervous system: heaven (or hell) is in the details. Curr Opin Immunol 2006; 18: 683-689
2. Korn T. Pathophysiology of multiple sclerosis. J Neurol 2008; 255 (Suppl 6): 2-6
3. Ransohoff RM. Natalizumab for multiple sclerosis. N Engl J Med 2007; 356: 2622-2629
4. Xie C, Alcaide P, Geisbrecht BV, Schneider D, Herrmann M, Preissner KT, et al. Suppression of experimental autoimmune encephalomyelitis by extracellular adherence protein of Staphylococcus aureus. J Exp Med 2006; 203: 985-994
5. Rothhammer V, Heink S, Petermann F, Srivastava R, Claussen MC, Hemmer B, et al. Th17 lymphocytes traffic to the central nervous system independently of alpha4 integrin expression during EAE. J Exp Med 2011; 208: 2465-2476
6. Rudick R, Polman C, Clifford D, Miller D, Steinman L. Natalizumab: bench to bedside and beyond. JAMA Neurol 2013; 70: 172-182
7. Steinman L A molecular trio in relapse and remission in multiple sclerosis. Nat Rev Immunol 2009; 9: 440-447
8. Bullard DC, Hu X, Schoeb TR, Collins RG, Beaudet AL, Barnum SR. Intercellular adhesion molecule-1 expression is required on multiple cell types for the development of experimental autoimmune encephalomyelitis. J Immunol 2007; 178: 851-857
9. Dugger KJ, Zinn KR, Weaver C, Bullard DC, Barnum SR. Effector and suppressor roles for LFA-1 during the development of experimental autoimmune encephalomyelitis. J Neuroimmunol 2009; 206: 22-27
10. Chavakis E, Choi EY, Chavakis T. Novel aspects in the regulation of the leukocyte adhesion cascade. Thromb Haemost 2009; 102: 191-197
11. Hajishengallis G, Chavakis T. Endogenous modulators of inflammatory cell recruitment. Trends Immunol 2013; 34: 1-6
12. Choi EY, Chavakis E, Czabanka MA, Langer HF, Fraemohs L, Economopoulou M, et al. Del-1, an endogenous leukocyte-endothelial adhesion inhibitor, limits inflammatory cell recruitment. Science 2008; 322: 1101-1104
13. Chavakis T. Leucocyte recruitment in inflammation and novel endogenous negative regulators thereof. Eur J Clin Invest 2012; 42: 686-691
14. Mitroulis I, Kang YY, Gahmberg CG, Siegert G, Hajishengallis G, Chavakis T, et al. Developmental endothelial locus-1 attenuates complement-dependent phagocytosis through inhibition of Mac-1-integrin. Thromb Haemost 2014; 111: 1004-1006
15. Eskan MA, Jotwani R, Abe T, Chmelar J, Lim JH, Liang S, et al. The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat Immunol 2012; 13: 465-473
16. Goris A, Sawcer S, Vandenbroeck K, Carton H, Billiau A, Setakis E, et al. New candidate loci for multiple sclerosis susceptibility revealed by a whole genome association screen in a Belgian population. J Neuroimmunol 2003; 143: 65-69
17. Shin J, Hosur KB, Pyaram K, Jotwani R, Liang S, Chavakis T, et al. Expression and function of the homeostatic molecule Del-1 in endothelial cells and the periodontal tissue. Clin Dev Immunol 2013; 2013: 617-809
18. Langer HF, Choi EY, Zhou H, Schleicher R, Chung KJ, Tang Z, et al. Platelets contribute to the pathogenesis of experimental autoimmune encephalomyelitis. Circ Res 2012; 110: 1202-1210
19. Dasgupta SK, Le A, Chavakis T, Rumbaut RE, Thiagarajan P. Developmental endothelial locus-1 (Del-1) mediates clearance of platelet microparticles by the endothelium. Circulation 2012; 125: 1664-1672
20. Kanczkowski W, Chatzigeorgiou A, Grossklaus S, Sprott D, Bornstein SR, Chavakis T. Role of the endothelial-derived endogenous anti-inflammatory factor Del-1 in inflammation-mediated adrenal gland dysfunction. Endocrinology 2013; 154: 1181-1189
21. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 2010; 140: 918-934
22. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 2011; 14: 1142-1149
23. McCandless EE, Budde M, Lees JR, Dorsey D, Lyng E, Klein RS. IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J Immunol 2009; 183: 613-620
24. Chang RA, Miller SD, Longnecker R. Epstein-Barr virus latent membrane protein 2A exacerbates experimental autoimmune encephalomyelitis and enhances antigen presentation function. Sci Rep 2012; 2: 353
25. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 1995; 154: 4309-4321
26. Becher B, Durell BG, Noelle RJ. IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis. J Clin Invest 2003; 112: 1186-1191
27. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 187: 490-500
28. Carlson T, Kroenke M, Rao P, Lane TE, Segal B. The Th17-ELR+ CXC chemokine pathway is essential for the development of central nervous system autoimmune disease. J Exp Med 2008; 205: 811-823
29. Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S, et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol 2006; 177: 566-573
30. Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, Cua DJ, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 2011; 12: 255-263
31. Huber M, Heink S, Pagenstecher A, Reinhard K, Ritter J, Visekruna A, et al. IL-17A secretion by CD8+ T cells supports Th17-mediated autoimmune encephalomyelitis. J Clin Invest 2013; 123: 247-260
32. Hart BA, Gran B, Weissert R. EAE: imperfect but useful models of multiple sclerosis. Trends Mol Med 2011; 17: 119-125
33. Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010; 10: 479-489
34. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M, et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007; 13: 1173-1175
35. Berard JL, Wolak K, Fournier S, David S. Characterization of relapsing-remitting and chronic forms of experimental autoimmune encephalomyelitis in C57BL/6 mice. Glia 2010; 58: 434-445
36. Kroenke MA, Carlson TJ, Andjelkovic AV, Segal BM. IL-12-And IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J Exp Med 2008; 205: 1535-1541
37. Stromnes IM, Cerretti LM, Liggitt D, Harris RA, Goverman JM. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat Med 2008; 14: 337-342
38. Domingues HS, Mues M, Lassmann H, Wekerle H, Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One 2010; 5: e15531
39. Berghmans N, Nuyts A, Uyttenhove C, Van Snick J, Opdenakker G, Heremans H. Interferon-gamma orchestrates the number and function of Th17 cells in experimental autoimmune encephalomyelitis. J Interferon Cytokine Res 2011; 31: 575-587
40. Xiao BG, Ma CG, Xu LY, Link H, Lu CZ. IL-12/IFN-gamma/NO axis plays critical role in development of Th1-mediated experimental autoimmune encephalomyelitis. Mol Immunol 2008; 45: 1191-1196
41. Ferber IA, Brocke S, Taylor-Edwards C, Ridgway W, Dinisco C, Steinman L, et al. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J Immunol 1996; 156: 5-7
42. Huppert J, Closhen D, Croxford A, White R, Kulig P, Pietrowski E, et al. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J 24: 1023-1034
43. Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007; 8: 345-350
44. Haak S, Croxford AL, Kreymborg K, Heppner FL, Pouly S, Becher B, et al. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest 2009; 119: 61-69
45. Steinman L A rush to judgment on Th17. J Exp Med 2008; 205: 1517-1522
46. Hu Y, Ota N, Peng I, Refino CJ, Danilenko DM, Caplazi P, et al. IL-17RC is required for IL-17A-And IL-17F-dependent signaling and the pathogenesis of experimental autoimmune encephalomyelitis. J Immunol 184: 4307-4316
47. Gonzalez-Garcia I, Zhao Y, Ju S, Gu Q, Liu L, Kolls JK, et al. IL-17 signaling-independent central nervous system autoimmunity is negatively regulated by TGF-beta. J Immunol 2009; 182: 2665-2671
48. Das Sarma J, Ciric B, Marek R, Sadhukhan S, Caruso ML, Shafagh J, et al. Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. J Neuroinflamm 2009; 6: 14
49. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, Esiri MM, et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008; 172: 146-155
50. Ramanan VK, Risacher SL, Nho K, Kim S, Swaminathan S, Shen L, et al. APOE and BCHE as modulators of cerebral amyloid deposition: a florbetapir PET genomewide association study. Mol Psychiatry 2013; 19: 351-357