Identification and characterization of U83A viral chemokine, a broad and potent β-chemokine agonist for human CCRs with unique selectivity and inhibition by spliced isoform

Journal of Immunology

Volumn 176, Issue 1, 2006, Pages 544-556

  Dewin, David R ^a   Catusse, Julie ^a   Gompels, Ursula A ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR8; CHEMOKINE U83A; UNCLASSIFIED DRUG; VIRUS DNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ARTICLE; AUTOIMMUNE DISEASE; CALCIUM MOBILIZATION; CENTRAL NERVOUS SYSTEM DISEASE; CHEMOTAXIS; CHO CELL; CONTROLLED STUDY; DENDRITIC CELL; DNA REPLICATION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOTHERAPY; LATENT VIRUS INFECTION; LEUKEMIA CELL LINE; LEUKOCYTE; MACROPHAGE; MONOCYTE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECEPTOR AFFINITY; T LYMPHOCYTE; TH2 CELL; VIRUS INFECTION; WESTERN BLOTTING;

EID: 29644445595     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.1.544     Document Type: Article

References (90)

1. Compels, U. A. 2004. Roseoloviruses: human herpesviruses 6 and 7. In Principles and Practice of Clinical Virology, 5th Ed. A. J. Zuckerman, J. E. Banatvala, J. R. Pattison, P. D. Griffiths, and B. D. Schoub, eds. John Wiley & Sons, Chichester, pp. 147-168.
2. Compels, U. A., J. Nicholas, G. Lawrence, M. Jones, B. J. Thomson, M. E. Martin, S. Efstathiou, M. Craxton, and H. A. Macaulay. 1995. the DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 209: 29-51.
3. Isegawa, Y., T. Mukai, K. Nakano, M. Kagawa, J. Chen, Y. Mori, T. Sunagawa, K. Kawanishi, J. Sashihara, A. Hata, et al. 1999. Comparison of the complete DNA sequences of human herpesvirus 6 variants A and B. J. Virol. 73: 8053-8063.
4. Dominguez, G., T. R. Dambaugh, F. R. Stamey, S. Dewhurst, N. Inoue, and P. E. Pellett. 1999. Human herpesvirus 6B genome sequence: coding content and comparison with human herpesvirus 6A. J. Virol. 73: 8040-8052.
5. Billstrom, M. A., G. L. Johnson, N. J. Avdi, and G. S. Worthen. 1998. Intracellular signaling by the chemokine receptor US28 during human cytomegalovirus infection. J. Virol. 72: 5535-5544.
6. Kasolo, F. C., E. Mpabalwani, and U. A. Compels. 1997. Infection with AIDS-related herpesviruses in human immunodeficiency virus-negative infants and endemic childhood Kaposi's sarcoma in Africa. J. Gen. Virol. 78: 847-855.
7. Akhyani, N., R. Berti, M. B. Brennan, S. S. Soldan, J. M. Eaton, H. F. McFarland, and S. Jacobson. 2000. Tissue distribution and variant characterization of human herpesvirus (HHV)-6: increased prevalence of HHV-6A in patients with multiple sclerosis. 7. Infect. Dis. 182: 1321-1325.
8. Soldan, S. S., T. P. Leist, K. N. Juhng, H. F. McFarland, and S. Jacobson. 2000. Increased lymphoproliferative response to human herpesvirus type 6A variant in multiple sclerosis patients. Ann. Neurol. 47: 306-313.
9. Kim, J. S., K. S. Lee, J. H. Park, M. Y. Kim, and W. S. Shin. 2000. Detection of human herpesvirus 6 variant A in peripheral blood mononuclear cells from multiple sclerosis patients. Eur. Neurol. 43: 170-173.
10. Alvarez-Lafuente, R., V. De las Heras, M. Bartolome, J. J. Picazo, and R. Arroyo. 2004. Relapsing-remitting multiple sclerosis and human herpesvirus 6 active infection. Arch. Neurol. 61: 1523-1527.
11. Rotola, A., I. Merlotti, L. Caniatti, E. Caselli, E. Granieri, M. R. Tola, D. Di Luca, and E. Cassai. 2004. Human herpesvirus 6 infects the central nervous system of multiple sclerosis patients in the early stages of the disease. Mult. Scler. 10: 348-354.
12. Hall, C. B., M. T. Caserta, K. C. Schnabel, C. Long, L. G. Epstein, R. A. Insel, and S. Dewhurst. 1998. Persistence of human herpesvirus 6 according to site and variant: possible greater neurotropism of variant A. Clin. Infect. Dis. 26: 132-137.
13. Byington, C. L., D. M. Zerr, E. W. Taggart, L. Nguy, D. R. Hillyard, K. C. Carroll, and L. Corey. 2002. Human herpesvirus 6 infection in febrile infants ninety days of age and younger. Pediatr. Infect. Dis. J. 21: 996-999.
14. De Bolle, L., J. Van Loon, E. De Clercq, and L. Naesens. 2005. Quantitative analysis of human herpesvirus 6 cell tropism. J. Med. Virol. 75: 76-85.
15. Murphy, P. M., M. Baggiolini, I. F. Charo, C. A. Hebert, R. Horuk, K. Matsushima, L. H. Miller, J. J. Oppenheim, and C. A. Power. 2000. International Union of Pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev. 52: 145-176.
16. Penfold, M. E., D. J. Dairaghi, G. M. Duke, N. Saederup, E. S. Mocarski, G. W. Kemble, and T. J. Schall. 1999. Cytomegalovirus encodes a potent a-chemokine. Proc. Natl. Acad. Sci. USA 96: 9839-9844.
17. Akter, P., C. Cunningham, B. P. McSharry, A. Dolan, C. Addison, D. J. Dargan, A. F. Hassan-Walker, V. C. Emery, P. D. Griffiths, G. W. Wilkinson, and A. J. Davison. 2003. Two novel spliced genes in human cytomegalovirus. J. Gen. Virol. 84: 1117-1122.
18. + T cells. J. Gen. Virol. 86: 275-284.
19. Hahn, G., M. G. Revello, M. Patrone, E. Percivalle, G. Campanini, A. Sarasini, M. Wagner, A. Gallina, G. Milanesi, U. Koszinowski, et al. 2004. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J. Virol. 78: 10023-10033.
20. Saederup, N., S. A. Aguirre, T. E. Sparer, D. M. Bouley, and E. S.-Mocarski. 2001. Murine cytomegalovirus CC chemokine homolog MCK-2 (m131-129) is a determinant of dissemination that increases inflammation at initial sites of infection. J. Virol. 75: 9966-9976.
21. Saederup, N., Y. C. Lin, D. J. Dairaghi, T. J. Schall, and E. S. Mocarski. 1999. Cytomegalovirus-encoded β-chemokine promotes monocyte-associated viremia in the host. Proc. Natl. Acad. Sci. USA 96: 10881-10886.
22. Fleming, P., N. Davis-Poynter, M. Degli-Esposti, E. Densley, J. Papadimitriou, G. Shellam, and H. Farrell. 1999. The murine cylomegalovirus chemokine homolog, m131/129, is a determinant of viral pathogenicity. J. Virol. 73: 6800-6809.
23. French, C., P. Menegazzi, L. Nicholson, H. Macaulay, D. DiLuca, and U. A. Compels. 1999. Novel, nonconsensus cellular splicing regulates expression of a gene encoding a chemokine-like protein that shows high variation and is specific for human herpesvirus 6. Virology 262: 139-151.
24. Zou, P., Y. Isegawa, K. Nakano, M. Haque, Y. Horiguchi, and K. Yamanishi. 1999. Human herpesvirus 6 open reading frame U83 encodes a functional chemokine. J. Virol. 73: 5926-5933.
25. Luttichau, H. R., I. dark-Lewis, P. O. Jensen, C. Moser, J. Gerstoft, and T. W. Schwartz. 2003. A highly selective CCR2 chemokine agonist encoded by human herpesvirus 6. J. Biol. Chem. 278: 10928-10933.
26. Smith, D., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutatione S-transferase. Gene 67: 31-40.
27. Rial, D. V., and E. A. Ceccarelli. 2002. Removal of DnaK contamination during fusion protein purifications. Protein Expr. Purif. 25: 503-507.
28. Sherrnan, M., and A. L. Goldberg. 1992. Involvement of the chaperonin dnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO J. 11: 71-77.
29. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
30. Proudfoot, A. E., and F. Borlat. 2000. Analysis, quantitation, and storage of chemokines. Methods Mol. Biol. 138: 85-87.
31. Tsuchiya, S., M. Yamabe, Y. Yamaguchi, Y. Kobayashi, T. Kono, and K. Tada. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26: 171-176.
32. Klein, E. 1976. Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. Int. J. Cancer 18: 421-431.
33. Gazdar, A. F., D. N. Carney, P. A. Bunn, E. K. Russell, E. S. Jaffe, G. P. Schechter, and J. G. Guccion. 1980. Mitogen requirements for the in vitro propagation of cutaneous T-cell lymphomas. Blood 55: 409-417.
34. Milne, R. S., C. Mattick, L. Nicholson, P. Devaraj, A. Alcami, and U. A. Compels. 2000. RANTES binding and down-regulation by a novel human herpesvirus-6 β-chemokine receptor. J. Immunol. 164: 2396-2404.
35. Di Luca, D., P. Mirandola, T. Ravaioli, B. Bigoni, and E. Cassai. 1996. Distribution of HHV-6 variants in human tissues. Infect. Agents Dis. 5: 203-214.
36. Cone, R. W., M. L. Huang, R. C. Hackman, and L. Corey. 1996. Coinfection with human herpesvirus 6 variants A and B in lung tissue. J. Clin. Microhiol. 34: 877-881.
37. Takahashi, K., S. Sonoda, K. Higashi, T. Hondo, H. Takahashi, M. Takahashi, and K. Yamanishi. 1989. Predominant CD4 T-lymphocyte tropism of human herpesvirus 6-related virus. J. Virol. 63: 3161-3163.
38. Kondo, K., T. Kondo, T. Okuno, M. Takahashi, and K. Yamanishi. 1991. Latent human herpesvirus 6 infection of human monocytes/macrophages. J. Cen. Virol. 72: 1401-1408.
39. Kondo, K., T. Kondo, K. Shimada, K. Amo, H. Miyagawa, and K. Yamanishi. 2002. Strong interaction between human herpesvirus 6 and peripheral blood monocytes/macrophages during acute infection. J. Med. Virol. 67: 364-369.
40. Trebst, C., S. M. Staugaitis, P. Kivisakk, D. Mahad, M. K. Cathcart, B. Tucky, T. Wei, M. R. Rani, R. Horuk, K. D. Aldape, et al. 2003. CC chemokine receptor 8 in the central nervous system is associated with phagocytic macrophages. Am. J. Pathol. 162: 427-438.
41. Kaufmann, A., R. Salentin, D. Gemsa, and H. Sprenger. 2001. Increase of CCR1 and CCR5 expression and enhanced functional response to MIP-1α during differentiation of human monocytes to macrophages. J. Leukocyte Biol. 69: 248-252.
42. Asojo, O. A., C. Boulegue, D. M. Hoover, W. Lu, and J. Lubkowski. 2003. Structures of thymus and activation-regulated chemokine (TARC). Acta Crystallogr. D 59: 1165-1173.
43. Saederup, N., and E. S. Mocarski, Jr. 2002. Fatal attraction: cytomegalovirus-encoded chemokine homologs. Curr. Top. Microbiol. Immunol. 269: 235-256.
44. Luttichau, H. R., J. Gerstoft, and T. W. Schwartz. 2001. MC148 encoded by human molluscum contagiosum poxvirus is an antagonist for human but not murine CCR8. J. Leukocyte Biol. 70: 277-282.
45. Endres, M. J., C. G. Garlisi, H. Xiao, L. Shan, and J. A. Hedrick. 1999. The Kaposi's sarcoma-related herpesvirus (KSHV)-encoded chemokine vMIP-1 is a specific agonist for the CC chemokine receptor (CCR8). J. Exp. Med. 189: 1993-1998.
46. Boshoff, C., Y. Endo, P. D. Collins, Y. Takeuchi, J. D. Reeves, V. L. Schweickart, M. A. Siani, T. Sasaki, T. J. Williams, P. W. Gray, et al. 1997. Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 278: 290-294.
47. Dairaghi, D. J., R. A. Fan, B. E. McMaster, M. R. Hanley, and T. J. Schall. 1999. HHV8-encoded vMIP-1 selectively engages chemokine receptor CCR8: agonist and antagonist profiles of viral chemokines. J. Biol. Chem. 274: 21569-21574.
48. Damon, I., P. M. Murphy, and B. Moss. 1998. Broad-spectrum chemokine antagonistic activity of a human poxvirus chemokine homolog. Frac. Natl. Acad. Sci. USA 95: 6403-6407.
49. Luttichau, H. R., I. C. Lewis, J. Gerstoft, and T. W. Schwartz. 2001. The herpesvirus 8-encoded chemokine vMIP-2, but not the poxvirus-encoded chemokine MC148, inhibits the CCR10 receptor. Eur. J. Immunol. 31: 1217-1220.
50. Luttichau, H. R., J. Stine, T. P. Boesen, A. H. Johnsen, D. Chantry, J. Gerstoft. and T. W. Schwartz. 2000. A highly selective CC chemokine receptor (CCR)8 antagonist encoded by the poxvirus molluscum contagiosum. J. Exp. Med. 191: 171-180.
51. Kledal, T. N., M. M. Rosenkilde, F. Coulin, G. Simmons, A. H. Johnsen, S. Alouani, C. A. Power, H. R. Luttichau, J. Gerstoft, P. R. Clapham, et al. 1997. A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science 277: 1656-1659.
52. Sozzani, S., W. Luini, G. Bianchi, P. Allavena, T. N. Wells, M. Napolitano, G. Bernardini, A. Vecchi, D. D'Ambrosio, D. Mazzeo, et al. 1998. The viral chemokine macrophage inflammatory protein-11 is a selective Th2 chemoattractant. Blood 92: 4036-4039.
53. Stine, J. T., C. Wood, M. Hill, A. Epp, C. J. Raport, V. L. Schweickart, Y. Endo, T. Sasaki, G. Simmons, C. Boshoff, et al. 2000. KSHV-encoded CC chemokine vMIP-111 is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts Th2 cells. Blood 95: 1151-1157.
54. Zhang, Y., H. Yoneyama, Y. Wang, S. Ishikawa, S. Hashimoto, J. L. Gao, P. Murphy, and K. Matsushima. 2004. Mobilization of dendritic cell precursors into the circulation by administration of MIP-1αa in mice. J. Natl. Cancer Inst. 96: 201-209.
55. Zibert, A., S. Balzer, M. Souquet, T. H. Quang, C. Paris-Scholz, M. Roskrow, and D. Dilloo. 2004. CCL3/MIP-1α is a potent immunostimulator when coexpressed with interleukin-2 or granulocyte-macrophage colony-stimulating factor in a leukemia/lymphoma vaccine. Hum. Gene Ther. 15: 21-34.
56. Furumoto, K., L. Scares, E. G. Engleman, and M. Merad. 2004. Induction of potent antitumor immunity by in situ targeting of intratumoral DCs. J. Clin. Invest. 113: 774-783.
57. Crittenden, M., M. Cough, K. Harrington, K. Olivier, J. Thompson, and R. G. Vile. 2003. Expression of inflammatory chemokines combined with local tumor destruction enhances tumor regression and long-term immunity. Cancer Res. 63: 5505-5512.
58. Broxmeyer, H. E., C. H. Kim, S. H. Cooper, G. Hangoc, R. Hromas, and L. M. Pelus. 1999. Effects of CC, CXC, C. and CX3C chemokines on proliferation of myeloid progenitor cells, and insights into SDF-1-induced chemotaxis of progenitors. Ann. NY Acad. Sci. 872:142-163.
59. Isomura, H., M. Yamada, M. Yoshida, H. Tanaka, T. Kitamura, M. Oda, S. Nu, and Y. Seino. 1997. Suppressive effects of human herpesvirus 6 on in vitro colony formation of hematopoietic progenitor cells. J. Med. Virol. 52: 406-412.
60. Knox, K. K., and D. R. Carrigan. 1992. In vitro suppression of bone marrow progenitor cell differentiation by human herpesvirus 6 infection. J. Infect. Dis. 165: 925-929.
61. Carrigan, D. R., and K. K. Knox. 1995. Bone marrow suppression by human herpesvirus-6: comparison of the A and B variants of the virus. Blood 86: 835-836.
62. Nitsche, A., J. Fleischmann, K. M. Klima, A. Radonic, S. Thulke, and W. Siegert. 2004. Inhibition of cord blood cell expansion by human herpesvirus 6 in vitro. Stem Cells Dev. 13: 197-203.
63. Hromas, R., L. Cripe, G. Hangoc, S. Cooper, and H. E. Broxmeyer. 2000. The exodus subfamily of CC chemokines inhibits the proliferation of chronic myelogenous leukemia progenitors. Blood 95: 1506-1508.
64. Yang, D., Q. Chen, D. M. Hoover, P. Staley, K. D. Tucker, J. Lubkowski, and J. J. Oppenheim. 2003. Many chemokines, including CCL20/MIP-3α, display antimicrobial activity. J. Leukocyte Biol. 74: 448-455.
65. Biragyn, A., M. Surenhu, D. Yang, P. A. Ruffini, B. A. Haines, E. Klyushnenkova, J. J. Oppenheim, and L. W. Kwak. 2001. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J. Immunol. 167: 6644-6653.
66. Simmons, G., J. D. Reeves, S. Hibbitts, J. T. Stine, P. W. Gray, A. E. Proudfoot, and P. R. Clapham. 2000. Coreceptor use by HIV and inhibition of HIV infection by chemokine receptor ligands. Immunol. Rev. 177: 112-126.
67. Proudfoot, A. E. 2002. Chemokine receptors: multifaceted therapeutic targets. Nat. Rev. Immunol. 2: 106-115.
68. Utaipat, U., A. Duerr, D. L. Rudolph, C. Yang, S. T. Butera, D. Lupo, T. Pisell, A. Tangmunkongvorakul, N. Kamtorn, N. Nantachit, et al. 2002. Coreceptor utilization of HIV type 1 subtype E viral isolates from Thai men with HIV type 1-infected and uninfected wives. AIDS Res. Hum. Retroviruses 18: 1-11.
69. Agrawal, L., Z. Vanhorn-Ali, and G. Alkhatib. 2002. Multiple determinants.are involved in HIV coreceptor use as demonstrated by CCR4/CCL22 interaction in peripheral blood mononuclear cells (PBMCs). J. Leukocyte Biol. 72: 1063-1074.
70. Clapham, P. R., and A. McKnight. 2001. HIV-1 receptors and cell tropism. Br. Med. Bull. 58; 43-59.
71. Clapham, P. R., and A. McKnight. 2002. Cell surface receptors, virus entry, and tropism of primate lentiviruses. J. Gen. Virol. 83: 1809-1829.
72. Fairfax, M. R., T. Schacker, R. W. Cone, A. C. Collier, and L. Corey. 1994. Human herpesvirus 6 DNA in blood cells of human immunodeficiency virus-infected men: correlation of high levels with high CD4 cell counts. J. Infect. Dis. 169: 1342-1345.
73. Knox, K. K., and D. R. Carrigan. 1994. Disseminated active HHV-6 infections in patients with AIDS. Lancet 343: 577-578.
74. Corbellino, M., P. Lusso, R. C. Gallo, C. Parravicini, M. Galli, and M. Moroni. 1993. Disseminated human herpesvirus 6 infection in AIDS. Lancet 342: 1242.
75. Robinson, S. C., K. A. Scott, J. L. Wilson, R. G. Thompson, A. E. Proudfoot, and F. R. Balkwill. 2003. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res. 63: 8360-8365.
76. Gladue, R. P., L. A. Tylaska, W. H. Brissette, P. D. Lira, J. C. Kath, C. S. Poss, M. F. Brown, T. J. Paradis, M. J. Conklyn, K. T. Ogborne, et al. 2003. CP-481,715, a potent and selective CCR1 antagonist with potential therapeutic implications for inflammatory diseases. J. Biol. Chem. 278: 40473-40480.
77. Haringman, J. J., M. C. Kraan, T. J. Smeets, K. H. Zwinderman, and P. P. Tak. 2003. Chemokine blockade and chronic inflammatory disease: proof of concept in patients with rheumatoid arthritis. Ann. Rheum. Dis. 62: 715-721.
78. DeBruyne, L. A., K. Li, D. K. Bishop, and J. S. Bromberg. 2000. Gene transfer of virally encoded chemokine antagonists vMIP-11 and MC148 prolongs cardiac allograft survival and inhibits donor-specific immunity. Gene Ther. 7: 575-582.
79. Lezcano-Meza, D., M. C. Negrete-Garcia, M. Dante-Escobedo, and L. M. Teran. 2003. The monocyte-derived chemokine is released in the bronchoalveolar lavage fluid of steady-state asthmatics. Allergy 58: 1125-1130.
80. Panina-Bordignon, P., A. Papi, M. Mariani, P. Di Lucia, G. Casoni, C. Bellettato, C. Buonsanti, D. Miotto, C. Mapp, A. Villa, et al. 2001. The C-C chemokine receptors CCR4 and CCR8 identify airway T cells of allergen-challenged atopic asthmatics. J. clin. Invest. 107: 1357-1364.
81. Bishop, B., and C. M. Lloyd. 2003. CC chemokine ligand 1 promotes recruitment of eosinophils, but not Th2 cells, during the development of allergic airways disease. J. Immunol. 170: 4810-4817.
82. Eltayeb, S., D. Sunnemark, A. L. Berg, G. Nordvall, A. Malmberg, H. Lassmann, E. Wallstrom, T. Olsson, and A. Ericsson-Dahlstrand. 2003. Effector stage CC chemokine receptor-1 selective antagonism reduces multiple sclerosis-like rat disease. J. Neuroimmunol. 142: 75-85.
83. Liang, M., C. Mallari, M. Rosser, H. P. Ng, K. May, S. Monahan, J. G. Bauman, I. Islam, A. Ghannam, B. Buckman, et al. 2000. Identification and characterization of a potent, selective, and orally active antagonist of the CC chemokine receptor-1. J. Biol. Chem. 275: 19000-19008.
84. Sunnemark, D., S. Eltayeb, E. Wallstrom, L. Appelsved, A. Malmberg, H. Lassmann, A. Ericsson-Dahlstrand, F. Piehl, and T. Olsson. 2003. Differential expression of the chemokine receptors CX3CR1 and CCR1 by microglia and macrophages in myelin-oligodendrocyte-glycoprotein-induced experimental autoimmune encephalomyelitis. Brain Pathol. 13:617-629.
85. Rottman, J. B., A. J. Slavin, R. Suva, H. L. Weiner, C. G. Gerard, and W. W. Hancock. 2000. Leukocyte recruitment during onset of experimental allergic encephalomyelitis is CCR1 dependent. Eur. J. Immunol. 30: 2372-2377.
86. Trebst, C., S. M. Staugaitis, B. Tucky, T. Wei, K. Suzuki, K. D. Aldape, C. A. Pardo, J. Troncoso, H. Lassmann, and R. M. Ransohoff. 2003. Chemokine receptors on infiltrating leucocytes in inflammatory pathologies of the central nervous system (CNS). Neuropathol. Appl. Neurobiol. 29: 584-595.
87. + mononuclear phagocytes accumulate in the central nervous system of patients with multiple sclerosis. Am. J. Pathol, 159: 1701-1710.
88. Tuke, P. W., S. Hawke, P. D. Griffiths, and D. A. Clark. 2004. Distribution and quantification of human herpesvirus 6 in multiple sclerosis and control brains. Mult. Scler. 10: 355-359.
89. Tomsone, V., I. Logina, A. Millers, S. Chapenko, S. Kozireva, and M. Murovska. 2001. Association of human herpesvirus 6 and human herpesvirus 7 with demyelinating diseases of the nervous system. J. Neurovirol. 1: 564-569.
90. Nicholas, J. 1996. Determination and analysis of the complete nucleotide sequence of human herpesvirus. J. Virol. 70: 5975-5989.