The biological functions, structure and sources of CXCL10 and its outstanding part in the pathophysiology of multiple sclerosis

NeuroImmunoModulation

Volumn 21, Issue 6, 2014, Pages 322-330

  Vazirinejad, Reza ^a   Ahmadi, Zahra ^b   Arababadi, Mohammad Kazemi ^b   Hassanshahi, Gholamhossein ^b   Kennedy, Derek ^c  

^a Social Determinants of Health Research Center   (Iran)

^b RAFSANJAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c GRIFFITH UNIVERSITY   (Australia)

Author keywords

Chemokine; CXCL10; Inflammation; Multiple sclerosis; Pathogenesis

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10;

BIOLOGICAL FUNCTIONS; CEREBROSPINAL FLUID; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; MULTIPLE SCLEROSIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; BIBLIOGRAPHIC DATABASE; FEMALE; IMMUNOLOGY; MALE; METABOLISM; STATISTICS AND NUMERICAL DATA; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN STRUCTURE;

CHEMOKINE CXCL10; DATABASES, BIBLIOGRAPHIC; FEMALE; HUMANS; MALE; MULTIPLE SCLEROSIS; SIGNAL TRANSDUCTION;

EID: 84906934600     PISSN: 10217401     EISSN: 14230216     Source Type: Journal    
DOI: 10.1159/000357780     Document Type: Review

References (83)

1. Bach JF, Chatenoud L: Tolerance to islet autoantigens in type 1 diabetes. Annu Rev Immunol 2001; 19: 131-161.
2. Rubin SM: Management of multiple sclerosis: an overview. Dis Mon 2013; 59: 253-260.
3. Ozakbas S, Kaya D, Idiman E: Early onset multiple sclerosis has worse prognosis than adult onset multiple sclerosis based on cognition and magnetic resonance imaging. Autoimmune Dis 2012; 2012: 563989.
4. Lin GY, Wang CW, Chiang TT, Peng GS, Yang FC: Multiple sclerosis presenting initially with a worsening of migraine symptoms. J Headache Pain 2013; 14: 70.
5. Rotondi M, Batocchi AP, Coperchini F, Caggiula M, Zerbini F, Sideri R, Leporati P, Nociti V, Frisullo G, Mirabella M: Severe disability in patients with relapsing-remitting multiple sclerosis is associated with profound changes in the regulation of leptin secretion. Neuroimmunomodulation 2013; 20: 341-347.
6. Gil Moreno MJ, Cerezo García M, Marasescu R, Pinel González A, López Álvarez L, Aladro Benito Y: Neuropsychological syndromes in multiple sclerosis. Psicothema 2013; 25: 452-460.
7. Agrawal SM, Yong VW: Immunopathogenesis of multiple sclerosis. Int Rev Neurobiol 2007; 79: 99-126.
8. Gandhi KS, McKay FC, Diefenbach E, Crossett B, Schibeci SD, Heard RN, Stewart GJ, Booth DR, Arthur JW: Novel approaches to detect serum biomarkers for clinical response to interferon-β treatment in multiple sclerosis. PLoS One 2010; 5:e10484.
9. LaSalle JM, Ota K, Hafler DA: Presentation of autoantigen by human T cells. J Immunol 1991; 147: 774-780.
10. H 17 and regulatory T cells. Nature 2006; 441: 235-238.
11. Iwakura Y, Ishigame H: The IL-23/IL-17 axis in inflammation. J Clin Invest 2006; 116: 1218-1222.
12. Martin R, McFarland HF, McFarlin DE: Immunological aspects of demyelinating diseases. Annu Rev Immunol 1992; 10: 153-187.
13. Pettinelli CB, McFarlin DE: Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1 + 2-T lymphocytes. J Immunol 1981; 127: 1420-1423.
14. Derakhshan R, Arababadi MK, Ahmadi Z, Karimabad MN, Salehabadi VA, Abedinzadeh M, Khorramdelazad H, Balaei P, Kennedy D, Hassanshahi G: Increased circulating levels of SDF-1 (CXCL12) in type 2 diabetic patients are correlated to disease state but are unrelated to polymorphism of the SDF-1β gene in the Iranian population. Inflammation 2012; 35: 900-904.
15. Ciesielski CJ, Andreakos E, Foxwell BM, Feldmann M: TNFα-induced macrophage chemokine secretion is more dependent on NF- κB expression than lipopolysaccharides-induced macrophage chemokine secretion. Eur J Immunol 2002; 32: 2037-2045.
16. Ohmori Y, Hamilton TA: The interferon-stimulated response element and a κB site mediate synergistic induction of murine IP-10 gene transcription by IFN-γ and TNF-α. J Immunol 1995; 154: 5235-5244.
17. Shields PL, Morland CM, Salmon M, Qin S, Hubscher SG, Adams DH: Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J Immunol 1999; 163: 6236-6243.
18. Dillman JF 3rd, McGary KL, Schlager JJ: An inhibitor of p38 MAP kinase downregulates cytokine release induced by sulfur mustard exposure in human epidermal keratinocytes. Toxicol In Vitro 2004; 18: 593-599.
19. Ohmori Y, Hamilton TA: Cell type and stimulus specific regulation of chemokine gene expression. Biochem Biophys Res Commun 1994; 198: 590-596.
20. Treacy O, Ryan AE, Heinzl T, O'Flynn L, Cregg M, Wilk M, Odoardi F, Lohan P, O'Brien T, Nosov M, Ritter T: Adenoviral transduction of mesenchymal stem cells: in vitro responses and in vivo immune responses after cell transplantation. PLoS One 2012; 7:e42662.
21. Ge MQ, Ho AW, Tang Y, Wong KH, Chua BY, Gasser S, Kemeny DM: NK cells regulate CD8+ T cell priming and dendritic cell migration during influenza A infection by IFN-γ and perforin-dependent mechanisms. J Immunol 2012; 189: 2099-2109.
22. Zeissig S, Murata K, Sweet L, Publicover J, Hu Z, Kaser A, Bosse E, Iqbal J, Hussain MM, Balschun K, Rocken C, Arlt A, Gunther R, Hampe J, Schreiber S, Baron JL, Moody DB, Liang TJ, Blumberg RS: Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat Med 2012; 18: 1060-1068.
23. Hassanshahi G, Patel SS, Jafarzadeh AA, Dickson AJ: Expression of CXC chemokine IP-10/Mob-1 by primary hepatocytes following heat shock. Saudi Med J 2007; 28: 514-518.
24. Rotondi M, Chiovato L, Romagnani S, Serio M, Romagnani P: Role of chemokines in endocrine autoimmune diseases. Endocr Rev 2007; 28: 492-520.
25. Hassanshahi G, Jafarzadeh A, Esmaeilzadeh B, Arababadi MK, Yousefi H, Dickson AJ: Assessment of NK cells response to hepatocyte derived chemotactic agents. Pak J Biol Sci 2008; 11: 1120-1125.
26. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, Borsatti A, Sozzani S, Allavena P, Gray PA, Mantovani A, Sinigaglia F: Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 1998; 187: 129-134.
27. Arababadi MK, Mosavi R, Khorramdelazad H, Yaghini N, Zarandi ER, Araste M, Pourali R, Nekhei Z, Kennedy D: Cytokine patterns after therapy with Avonex®, Rebif®, Betaferon® and CinnoVex™ in relapsing-remitting multiple sclerosis in Iranian patients. Biomark Med 2010; 4: 755-759.
28. Sørensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM: Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 1999; 103: 807-815.
29. + T cells are increased in multiple sclerosis and their ligands MIP-1α and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci USA 1999; 96: 6873-6878.
30. Ahmadi Z, Arababadi MK, Hassanshahi G: CXCL10 activities, biological structure, and source along with its significant role played in pathophysiology of type I diabetes mellitus. Inflammation 2013; 36: 364-371.
31. Liang P, Averboukh L, Zhu W, Pardee AB: Ras activation of genes: Mob-1 as a model. Proc Natl Acad Sci USA 1994; 91: 12515-12519.
32. Strieter RM, Polverini PJ, Kunkel SL, Arenberg DA, Burdick MD, Kasper J, Dzuiba J, van Damme J, Walz A, Marriott D, et al: The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J Biol Chem 1995; 270: 27348-27357.
33. Deng W, Ohmori Y, Hamilton TA: Mechanisms of IL-4-mediated suppression of IP-10 gene expression in murine macrophages. J Immunol 1994; 153: 2130-2136.
34. Ohmori Y, Hamilton TA: Cooperative interaction between interferon (IFN) stimulus response element and κB sequence motifs controls IFNγ- and lipopolysaccharide-stimulated transcription from the murine IP-10 promoter. J Biol Chem 1993; 268: 6677-6688.
35. Kelsen SG, Aksoy MO, Yang Y, Shahabuddin S, Litvin J, Safadi F, Rogers TJ: The chemokine receptor CXCR3 and its splice variant are expressed in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004; 287:L584-L591.
36. Lasagni L, Francalanci M, Annunziato F, Lazzeri E, Giannini S, Cosmi L, Sagrinati C, Mazzinghi B, Orlando C, Maggi E, Marra F, Romagnani S, Serio M, Romagnani P: An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med 2003; 197: 1537-1549.
37. Bodnar RJ, Yates CC, Wells A: IP-10 blocks vascular endothelial growth factor-induced endothelial cell motility and tube formation via inhibition of calpain. Circ Res 2006; 98: 617-625.
38. Bodnar RJ, Yates CC, Rodgers ME, Du X, Wells A: IP-10 induces dissociation of newly formed blood vessels. J Cell Sci 2009; 122: 2064-2077.
39. Taub DD, Lloyd AR, Conlon K, Wang JM, Ortaldo JR, Harada A, Matsushima K, Kelvin DJ, Oppenheim JJ: Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J Exp Med 1993; 177: 1809-1814.
40. Taub DD, Longo DL, Murphy WJ: Human interferon-inducible protein-10 induces mononuclear cell infiltration in mice and promotes the migration of human T lymphocytes into the peripheral tissues and human peripheral blood lymphocytes-SCID mice. Blood 1996; 87: 1423-1431.
41. Park JW, Gruys ME, McCormick K, Lee JK, Subleski J, Wigginton JM, Fenton RG, Wang JM, Wiltrout RH: Primary hepatocytes from mice treated with IL-2/IL-12 produce T cell chemoattractant activity that is dependent on monokine induced by IFN-γ (Mig) and chemokine responsive to γ-2 (Crg-2). J Immunol 2001; 166: 3763-3770.
42. Laing KJ, Secombes CJ: Chemokines. Dev Comp Immunol 2004; 28: 443-460.
43. Wang X, Yue TL, Ohlstein EH, Sung CP, Feuerstein GZ: Interferon-inducible protein- 10 involves vascular smooth muscle cell migration, proliferation, and inflammatory response. J Biol Chem 1996; 271: 24286-24293.
44. Neville LF, Abdullah F, McDonnell PM, Young PR, Feuerstein GZ, Rabinovici R: Mob-1 expression in IL-2-induced ARDS: regulation by TNF-α. Am J Physiol 1995; 269:L884-L890.
45. Lloyd AR, Oppenheim JJ, Kelvin DJ, Taub DD: Chemokines regulate T cell adherence to recombinant adhesion molecules and extracellular matrix proteins. J Immunol 1996; 156: 932-938.
46. Kanda N, Watanabe S: Histamine inhibits the production of interferon-induced protein of 10 kDa in human squamous cell carcinoma and melanoma. J Invest Dermatol 2002; 119: 1411-1419.
47. Majumder S, Zhou LZ, Chaturvedi P, Babcock G, Aras S, Ransohoff RM: Regulation of human IP-10 gene expression in astrocytoma cells by inflammatory cytokines. J Neurosci Res 1998; 54: 169-180.
48. Varley CL, Armitage S, Hassanshahiraviz G, Dickson AJ: Regulation of the C-X-C chemokine, mob-1, gene expression in primary rat hepatocytes. Cytokine 2003; 23: 64-75.
49. Han B, Logsdon CD: Cholecystokinin induction of mob-1 chemokine expression in pancreatic acinar cells requires NF-κB activation. Am J Physiol 1999; 277(pt 1):C74-C82.
50. 2+. Am J Physiol Cell Physiol 2000; 278:C344-C351.
51. Kaplan G, Luster AD, Hancock G, Cohn ZA: The expression of a gamma interferon-induced protein (IP-10) in delayed immune responses in human skin. J Exp Med 1987; 166: 1098-1108.
52. Romagnani P, Lazzeri E, Lasagni L, Mavilia C, Beltrame C, Francalanci M, Rotondi M, Annunziato F, Maurenzig L, Cosmi L, Galli G, Salvadori M, Maggi E, Serio M: IP-10 and Mig production by glomerular cells in human proliferative glomerulonephritis and regulation by nitric oxide. J Am Soc Nephrol 2002; 13: 53-64.
53. Majumder S, Zhou LZ, Chaturvedi P, Babcock G, Aras S, Ransohoff RM: p48/STAT- 1α-containing complexes play a predominant role in induction of IFN-γ-inducible protein, 10 kDa (IP-10) by IFN-γ alone or in synergy with TNF-α. J Immunol 1998; 161: 4736-4744.
54. Kopydlowski KM, Salkowski CA, Cody MJ, van Rooijen N, Major J, Hamilton TA, Vogel SN: Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J Immunol 1999; 163: 1537-1544.
55. Ubogu EE, Cossoy MB, Ransohoff RM: The expression and function of chemokines involved in CNS inflammation. Trends Pharmacol Sci 2006; 27: 48-55.
56. Muller DM, Pender MP, Greer JM: Chemokines and chemokine receptors: potential therapeutic targets in multiple sclerosis. Curr Drug Targets Inflamm Allergy 2004; 3: 279-290.
57. Buttmann M, Merzyn C, Rieckmann P: Interferon-β induces transient systemic IP- 10/CXCL10 chemokine release in patients with multiple sclerosis. J Neuroimmunol 2004; 156: 195-203.
58. Gutierrez-Ramos JC, Lloyd C, Gonzalo JA: Eotaxin: from an eosinophilic chemokine to a major regulator of allergic reactions. Immunol Today 1999; 20: 500-504.
59. Sørensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM: Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 1999; 103: 807-815.
60. Simpson JE, Newcombe J, Cuzner ML, Woodroofe MN: Expression of the interferon-γ- inducible chemokines IP-10 and Mig and their receptor, CXCR3, in multiple sclerosis lesions. Neuropathol Appl Neurobiol 2000; 26: 133-142.
61. Sørensen TL, Sellebjerg F, Jensen CV, Strieter RM, Ransohoff RM: Chemokines CXCL10 and CCL2: differential involvement in intrathecal inflammation in multiple sclerosis. Eur J Neurol 2001; 8: 665-672.
62. Karkamandi H, Hosseini-zijoud S, Hosseini J: Genetic variation at the CXC chemokine IP- 10 (CXCL10) in parallel with its increased serum level in south-eastern Iranian multiple sclerosis patients. AAM 2012; 1: 71-76.
63. Abousaidi H, Vazirinejad R, Arababadi MK, Rafatpanah H, Pourfathollah AA, Derakhshan R, Daneshmandi S, Hassanshahi G: Lack of association between chemokine receptor 5 (CCR5) δ32 mutation and pathogenesis of asthma in Iranian patients. South Med J 2011; 104: 422-425.
64. Asadikaram G, Asiabanha M, Sayadi A, Jafarzadeh A, Hassanshahi G: Impact of opium on the serum levels of TGF-β in diabetic, addicted and addicted-diabetic rats. Iran J Immunol 2010; 7: 186-192.
65. Scarpini E, Galimberti D, Baron P, Clerici R, Ronzoni M, Conti G, Scarlato G: IP-10 and MCP-1 levels in CSF and serum from multiple sclerosis patients with different clinical subtypes of the disease. J Neurol Sci 2002; 195: 41-46.
66. Sprenger H, Rösler A, Tonn P, Braune HJ, Huffmann G, Gemsa D: Chemokines in the cerebrospinal fluid of patients with meningitis. Clin Immunol Immunopathol 1996; 80: 155-161.
67. Franciotta D, Martino G, Zardini E, Furlan R, Bergamaschi R, Andreoni L, Cosi V: Serum and CSF levels of MCP-1 and IP-10 in multiple sclerosis patients with acute and stable disease and undergoing immunomodulatory therapies. J Neuroimmunol 2001; 115: 192-198.
68. Comini-Frota ER, Teixeira AL, Angelo JP, Andrade MV, Brum DG, Kaimen-Maciel DR, Foss NT, Donadi EA: Evaluation of serum levels of chemokines during interferon-β treatment in multiple sclerosis patients: a 1-year, observational cohort study. CNS Drugs 2011; 25: 971-981.
69. Sørensen TL, Trebst C, Kivisakk P, Klaege KL, Majmudar A, Ravid R, Lassmann H, Olsen DB, Strieter RM, Ransohoff RM, Sellebjerg F: Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system. J Neuroimmunol 2002; 127: 59-68.
70. Christophi GP, Christophi JA, Gruber RC, Mihai C, Mejico LJ, Massa PT, Jubelt B: Quantitative differences in the immunomodulatory effects of Rebif and Avonex in IFN-β 1a treated multiple sclerosis patients. J Neurol Sci 2011; 307: 41-45.
71. Satoh J, Nanri Y, Tabunoki H, Yamamura T: Microarray analysis identifies a set of CXCR3 and CCR2 ligand chemokines as early IFNβ- responsive genes in peripheral blood lymphocytes in vitro: an implication for IFNβ-related adverse effects in multiple sclerosis. BMC Neurol 2006; 6: 18.
72. Wandinger KP, Stürzebecher CS, Bielekova B, Detore G, Rosenwald A, Staudt LM, McFarland HF, Martin R: Complex immunomodulatory effects of interferon-β in multiple sclerosis include the upregulation of T helper 1-associated marker genes. Ann Neurol 2001; 50: 349-357.
73. Comabella M, Imitola J, Weiner HL, Khoury SJ: Interferon-β treatment alters peripheral blood monocytes chemokine production in MS patients. J Neuroimmunol 2002; 126: 205-212.
74. Sellebjerg F, Frederiksen JL, Nielsen PM, Olesen J: Double-blind, randomized, placebocontrolled study of oral, high-dose methylprednisolone in attacks of MS. Neurology 1998; 51: 529-534.
75. Sellebjerg F, Christiansen M, Jensen J, Frederiksen JL: Immunological effects of oral high-dose methylprednisolone in acute optic neuritis and multiple sclerosis. Eur J Neurol 2000; 7: 281-289.
76. Rudick RA, Cookfair DL, Simonian NA, Ransohoff RM, Richert JR, Jacobs LD, Herndon RM, Salazar AM, Fischer JS, Granger CV, Goodkin DE, Simon JH, Bartoszak DM, Bourdette DN, Braiman J, Brownscheidle CM, Coats ME, Cohan SL, Dougherty DS, Kinkel RP, Mass MK, Munchsauer FE, O'Reilly K, Priore RL, Whitham RH, et al: Cerebrospinal fluid abnormalities in a phase III trial of Avonex (IFNβ-1a) for relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group. J Neuroimmunol 1999; 93: 8-14.
77. Mellergård J, Edström M, Vrethem M, Ernerudh J, Dahle C: Natalizumab treatment in multiple sclerosis: marked decline of chemokines and cytokines in cerebrospinal fluid. Mult Scler 2010; 16: 208-217.
78. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, Estes ML, Thomas DM, Tuohy VK: Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 1993; 7: 592-600.
79. Azin H, Vazirinejad R, Ahmadabadi BN, Khorramdelazad H, Zarandi ER, Arababadi MK, Karimabad MN, Shamsizadeh A, Rafatpanah H, Hassanshahi G: The SDF-1 3 ′ A genetic variation of the chemokine SDF-1α (CXCL12) in parallel with its increased circulating levels is associated with susceptibility to MS: a study on Iranian multiple sclerosis patients. J Mol Neurosci 2012; 47: 431-436.
80. Salmaggi A, Gelati M, Dufour A, Corsini E, Pagano S, Baccalini R, Ferrero E, Scabini S, Silei V, Ciusani E, de Rossi M: Expression and modulation of IFN-γ-inducible chemokines (IP-10, Mig, and I-TAC) in human brain endothelium and astrocytes: possible relevance for the immune invasion of the central nervous system and the pathogenesis of multiple sclerosis. J Interferon Cytokine Res 2002; 22: 631-640.
81. Poggi A, Catellani S, Fenoglio D, Borsellino G, Battistini L, Zocchi MR: Adhesion molecules and kinases involved in γδ T cells migratory pathways: implications for viral and autoimmune diseases. Curr Med Chem 2007; 14: 3166-3170.
82. Buttmann M, Goebeler M, Toksoy A, Schmid S, Graf W, Berberich-Siebelt F, Rieckmann P: Subcutaneous interferon-β injections in patients with multiple sclerosis initiate inflammatory skin reactions by local chemokine induction. J Neuroimmunol 2005; 168: 175-182.
83. Revesz T, Kidd D, Thompson AJ, Barnard RO, McDonald WI: A comparison of the pathology of primary and secondary progressive multiple sclerosis. Brain 1994; 117(pt 4):759-765.