CXCL1 can be regulated by IL-6 and promotes granulocyte adhesion to brain capillaries during bacterial toxin exposure and encephalomyelitis

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Roy, Monica ^a   Richard, Jean François ^a   Dumas, Aline ^a   Vallières, Luc ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Autoimmunity; Cerebral endothelium; Chemotaxis; Myeloid cells; Neuroimmunity; Neuroinflammation; Neutrophils; Polymorphonuclear cells

Indexed keywords

BACTERIAL TOXIN; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; PERTUSSIS TOXIN; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; ANTIBODY; CALCIUM BINDING PROTEIN; CXCL1 PROTEIN, RAT; CXCL2 CHEMOKINE; CXCL2 PROTEIN, RAT; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LEUKOCYTE ANTIGEN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CAPILLARY; CELL ADHESION; CELL COUNT; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GRANULOCYTE FUNCTION; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEREOLOGY; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; GRANULOCYTE; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTIBODIES; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD; BRAIN; CALCIUM-BINDING PROTEINS; CELL ADHESION; CELLS, CULTURED; CHEMOKINE CXCL1; CHEMOKINE CXCL2; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GRANULOCYTES; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; PERTUSSIS TOXIN; RECEPTORS, INTERLEUKIN-8B;

EID: 84856053756     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-18     Document Type: Article

References (48)

1. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009, 9:393-407. 10.1038/nri2550, 2813731, 19444307.
2. King IL, Dickendesher TL, Segal BM. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009, 113:3190-3197. 10.1182/blood-2008-07-168575, 2665891, 19196868.
3. Serafini B, Rosicarelli B, Magliozzi R, et al. Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells. J Neuropathol Exp Neurol 2006, 65:124-141. 10.1097/01.jnen.0000199572.96472.1c, 16462204.
4. Fischer HG, Reichmann G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J Immunol 2001, 166:2717-2726.
5. Serafini B, Columba-Cabezas S, Di Rosa F, Aloisi F. Intracerebral recruitment and maturation of dendritic cells in the onset and progression of experimental autoimmune encephalomyelitis. Am J Pathol 2000, 157:1991-2002. 10.1016/S0002-9440(10)64838-9, 1885753, 11106572.
6. Tran EH, Hoekstra K, van Rooijen N, Dijkstra CD, Owens T. Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J Immunol 1998, 161:3767-3775.
7. Heppner FL, Greter M, Marino D, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005, 11:146-152. 10.1038/nm1177, 15665833.
8. Maatta JA, Sjoholm UR, Nygardas PT, Salmi AA, Hinkkanen AE. Neutrophils secreting tumor necrosis factor alpha infiltrate the central nervous system of BALB/c mice with experimental autoimmune encephalomyelitis. J Neuroimmunol 1998, 90:162-175. 10.1016/S0165-5728(98)00135-0, 9817444.
9. Reiseter BS, Miller GT, Happ MP, Kasaian MT. Treatment of murine experimental autoimmune encephalomyelitis with a myelin basic protein peptide analog alters the cellular composition of leukocytes infiltrating the cerebrospinal fluid. J Neuroimmunol 1998, 91:156-170. 10.1016/S0165-5728(98)00171-4, 9846832.
10. Tran EH, Prince EN, Owens T. IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J Immunol 2000, 164:2759-2768.
11. Reddy J, Waldner H, Zhang X, et al. Cutting edge: CD4+CD25+ regulatory T cells contribute to gender differences in susceptibility to experimental autoimmune encephalomyelitis. J Immunol 2005, 175:5591-5595.
12. 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. 10.1084/jem.20072404, 2292221, 18347102.
13. 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. 10.1084/jem.20080159, 2442630, 18573909.
14. Soulika AM, Lee E, McCauley E, Miers L, Bannerman P, Pleasure D. Initiation and progression of axonopathy in experimental autoimmune encephalomyelitis. J Neurosci 2009, 29:14965-14979. 10.1523/JNEUROSCI.3794-09.2009, 2990681, 19940192.
15. Wu F, Cao W, Yang Y, Liu A. Extensive infiltration of neutrophils in the acute phase of experimental autoimmune encephalomyelitis in C57BL/6 mice. Histochem Cell Biol 2010, 133:313-322. 10.1007/s00418-009-0673-2, 20063008.
16. Kang Z, Altuntas CZ, Gulen MF, et al. Astrocyte-restricted ablation of interleukin-17-induced Act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity 2010, 32:414-425. 10.1016/j.immuni.2010.03.004, 3073618, 20303295.
17. Richard JF, Roy M, Audoy-Remus J, Tremblay P, Vallieres L. Crawling phagocytes recruited in the brain vasculature after pertussis toxin exposure through IL6, ICAM1, and ITGαM. Brain Pathol 2011, 21:661-671. 10.1111/j.1750-3639.2011.00490.x, 21418369.
18. McColl SR, Staykova MA, Wozniak A, Fordham S, Bruce J, Willenborg DO. Treatment with anti-granulocyte antibodies inhibits the effector phase of experimental autoimmune encephalomyelitis. J Immunol 1998, 161:6421-6426.
19. Kerstetter AE, Padovani-Claudio DA, Bai L, Miller RH. Inhibition of CXCR2 signaling promotes recovery in models of multiple sclerosis. Exp Neurol 2009, 220:44-56. 10.1016/j.expneurol.2009.07.010, 2761527, 19616545.
20. Liu L, Darnall L, Hu T, Choi K, Lane TE, Ransohoff RM. Myelin repair is accelerated by inactivating CXCR2 on nonhematopoietic cells. J Neurosci 2010, 30:9074-9083. 2917803, 20610741.
21. Audoy-Remus J, Richard JF, Soulet D, Zhou H, Kubes P, Vallieres L. Rod-Shaped monocytes patrol the brain vasculature and give rise to perivascular macrophages under the influence of proinflammatory cytokines and angiopoietin-2. J Neurosci 2008, 28:10187-10199. 10.1523/JNEUROSCI.3510-08.2008, 18842879.
22. Vallieres L, Sawchenko PE. Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity. J Neurosci 2003, 23:5197-5207.
23. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010, 33:657-670. 10.1016/j.immuni.2010.11.011, 21094463.
24. Zhou H, Andonegui G, Wong CH, Kubes P. Role of endothelial TLR4 for neutrophil recruitment into central nervous system microvessels in systemic inflammation. J Immunol 2009, 183:5244-5250. 10.4049/jimmunol.0901309, 19786543.
25. Kielian T, Barry B, Hickey WF. CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J Immunol 2001, 166:4634-4643.
26. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000, 18:217-242. 10.1146/annurev.immunol.18.1.217, 10837058.
27. Rossi DL, Hurst SD, Xu Y, et al. Lungkine, a novel CXC chemokine, specifically expressed by lung bronchoepithelial cells. J Immunol 1999, 162:5490-5497.
28. Godiska R, Chantry D, Dietsch GN, Gray PW. Chemokine expression in murine experimental allergic encephalomyelitis. J Neuroimmunol 1995, 58:167-176. 10.1016/0165-5728(95)00008-P, 7539012.
29. Glabinski AR, Tani M, Strieter RM, Tuohy VK, Ransohoff RM. Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis. Am J Pathol 1997, 150:617-630. 1858292, 9033275.
30. Glabinski AR, Tuohy VK, Ransohoff RM. Expression of chemokines RANTES, MIP-1alpha and GRO-alpha correlates with inflammation in acute experimental autoimmune encephalomyelitis. Neuroimmunomodulation 1998, 5:166-171. 10.1159/000026333, 9730682.
31. Stromnes IM, Goverman JM. Active induction of experimental allergic encephalomyelitis. Nat Protoc 2006, 1:1810-1819. 10.1038/nprot.2006.285, 17487163.
32. Gijbels K, Brocke S, Abrams JS, Steinman L. Administration of neutralizing antibodies to interleukin-6 (IL-6) reduces experimental autoimmune encephalomyelitis and is associated with elevated levels of IL-6 bioactivity in central nervous system and circulation. Mol Med 1995, 1:795-805. 2230023, 8612202.
33. Samoilova EB, Horton JL, Hilliard B, Liu TS, Chen Y. IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J Immunol 1998, 161:6480-6486.
34. Okuda Y, Sakoda S, Bernard CC, et al. IL-6-deficient mice are resistant to the induction of experimental autoimmune encephalomyelitis provoked by myelin oligodendrocyte glycoprotein. Int Immunol 1998, 10:703-708. 10.1093/intimm/10.5.703, 9645618.
35. Eugster HP, Frei K, Kopf M, Lassmann H, Fontana A. IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur J Immunol 1998, 28:2178-2187. 10.1002/(SICI)1521-4141(199807)28:07<2178::AID-IMMU2178>3.0.CO;2-D, 9692887.
36. Okuda Y, Sakoda S, Fujimura H, Saeki Y, Kishimoto T, Yanagihara T. IL-6 plays a crucial role in the induction phase of myelin oligodendrocyte glucoprotein 35-55 induced experimental autoimmune encephalomyelitis. J Neuroimmunol 1999, 101:188-196. 10.1016/S0165-5728(99)00139-3, 10580801.
37. Luu-The V, Paquet N, Calvo E, Cumps J. Improved real-time RT-PCR method for high-throughput measurements using second derivative calculation and double correction. Biotechniques 2005, 38:287-293. 10.2144/05382RR05, 15727135.
38. Villeneuve J, Tremblay P, Vallieres L. Tumor necrosis factor reduces brain tumor growth by enhancing macrophage recruitment and microcyst formation. Cancer Res 2005, 65:3928-3936. 10.1158/0008-5472.CAN-04-3612, 15867393.
39. Bouchard C, Page J, Bedard A, Tremblay P, Vallieres L. G protein-coupled receptor 84, a microglia-associated protein expressed in neuroinflammatory conditions. Glia 2007, 55:790-800. 10.1002/glia.20506, 17390309.
40. Starr R, Willson TA, Viney EM, et al. A family of cytokine-inducible inhibitors of signalling. Nature 1997, 387:917-921. 10.1038/43206, 9202125.
41. Stromnes IM, Goverman JM. Passive induction of experimental allergic encephalomyelitis. Nat Protoc 2006, 1:1952-1960. 10.1038/nprot.2006.284, 17487182.
42. Carbonetti NH. Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 2010, 5:455-469. 10.2217/fmb.09.133, 2851156, 20210554.
43. Omari KM, Lutz SE, Santambrogio L, Lira SA, Raine CS. Neuroprotection and remyelination after autoimmune demyelination in mice that inducibly overexpress CXCL1. Am J Pathol 2009, 174:164-176. 10.2353/ajpath.2009.080350, 2631329, 19095949.
44. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 2011, 11:519-531. 10.1038/nri3024, 21785456.
45. Robinson S, Tani M, Strieter RM, Ransohoff RM, Miller RH. The chemokine growth-regulated oncogene-alpha promotes spinal cord oligodendrocyte precursor proliferation. J Neurosci 1998, 18:10457-10463.
46. Tsai HH, Frost E, To V, et al. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 2002, 110:373-383. 10.1016/S0092-8674(02)00838-3, 12176324.
47. Filipovic R, Zecevic N. The effect of CXCL1 on human fetal oligodendrocyte progenitor cells. Glia 2008, 56:1-15. 10.1002/glia.20582, 17910053.
48. Hosking MP, Tirotta E, Ransohoff RM, Lane TE. CXCR2 signaling protects oligodendrocytes and restricts demyelination in a mouse model of viral-induced demyelination. PLoS One 2010, 5:e11340. 10.1371/journal.pone.0011340, 2893165, 20596532.