Swift entry of myelin-specific T lymphocytes into the central nervous system in spontaneous autoimmune encephalomyelitis

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 4648-4655

  Furtado, Gláucia C ^a,b   Marcondes, Maria Cecilia G ^a,c   Latkowski, Jo Ann ^a   Tsai, Julia ^a   Wensky, Allen ^a,d   Lafaille, Juan J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d University of California Berkeley   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD69 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 1BETA; MYELIN BASIC PROTEIN; BIOLOGICAL MARKER; EPITOPE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL TRANSPORT; CENTRAL NERVOUS SYSTEM; CERVICAL LYMPH NODE; CONTROLLED STUDY; DISEASE SEVERITY; IMMUNIZATION; IMMUNOPATHOGENESIS; LYMPHADENECTOMY; LYMPHATIC DRAINAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; UPREGULATION; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CEREBROSPINAL FLUID; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; TIME; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL MARKERS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPITOPES, T-LYMPHOCYTE; LYMPH NODE EXCISION; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELIN BASIC PROTEINS; TIME FACTORS; UP-REGULATION;

EID: 58149294030     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.4648     Document Type: Article

References (52)

1. Ransohoff, R. M., P. Kivisakk, and G. Kidd. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3: 569-581. (Pubitemid 37328676)
2. Lowenstein, P. R. 2002. Immunology of viral-vector-mediated gene transfer into the brain: an evolutionary and developmental perspective. Trends Immunol. 23: 23-30.
3. Aloisi, F., F. Ria, and L. Adorini. 2000. Regulation of T-cell responses by CNS antigen-presenting cells: different roles for microglia and astrocytes. Immunol. Today 21: 141-147. (Pubitemid 30122704)
4. Hickey, W. F. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124. (Pubitemid 33055900)
5. Hickey, W. F., B. L. Hsu, and H. Kimura. 1991. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 28: 254-260.
6. Cross, A. H., B. Cannella, C. F. Brosnan, and C. S. Raine. 1990. Homing to central nervous system vasculature by antigen-specific lymphocytes: I. Localization of 14C-labeled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab. Invest. 63: 162-170. (Pubitemid 20262131)
7. Wekerle, H., B. Engelhardt, W. Risau, and R. Meyermann. 1991. Interaction of T lymphocytes with cerebral endothelial cells in vitro. Brain Pathol. 1: 107-114.
8. Hemmer, B., S. Cepok, S. Nessler, and N. Sommer. 2002. Pathogenesis of multiple sclerosis: an update on immunology. Curr. Opin. Neurol. 15: 227-231. (Pubitemid 34596882)
9. Pedotti, R., J. J. DeVoss, S. Youssef, D. Mitchell, J. Wedemeyer, R. Madanat, H. Garren, P. Fontoura, M. Tsai, S. J. Galli, et al. 2003. Multiple elements of the allergic arm of the immune response modulate autoimmune demyelination. Proc. Natl. Acad. Sci. USA 100: 1867-1872. (Pubitemid 36254540)
10. Zamvil, S. S., and L. Steinman. 1990. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol 8: 579-621.
11. Karpus, W. J., and R. M. Ransohoff. 1998. Chemokine regulation of experimental autoimmune encephalomyelitis: temporal and spatial expression patterns govern disease pathogenesis. J. Immunol. 161: 2667-2671.
12. Lafaille, J. J., K. Nagashima, M. Katsuki, and S. Tonegawa. 1994. High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 78: 399-408.
13. + T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J. Exp. Med. 188: 1883-1894.
14. Baron, J. L., J. A. Madri, N. H. Ruddle, G. Hashim, and C. A. Janeway, Jr. 1993. Surface expression of α 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J. Exp. Med. 177: 57-68.
15. Furtado, G. C., D. Olivares-Villagomez, M. A. Curotto de Lafaille, A. K. Wensky, J. A. Latkowski, and J. J. Lafaille. 2001. Regulatory T cells in spontaneous autoimmune encephalomyelitis. Immunol. Rev. 182: 122-134.
16. Cserr, H. F., and P. M. Knopf. 1992. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol. Today 13: 507-512.
17. Kida, S., A. Pantazis, and R. O. Weller. 1993. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat: anatomy, histology and immunological significance. Neuropathol. Appl. Neurobiol. 19: 480-488. (Pubitemid 24010674)
18. Zhang, E. T., H. K. Richards, S. Kida, and R. O. Weller. 1992. Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol. 83: 233-239.
19. Boulton, M., M. Flessner, D. Armstrong, R. Mohamed, J. Hay, and M. Johnston. 1999. Contribution of extracranial lymphatics and arachnoid villi to the clearance of a CSF tracer in the rat. Am. J. Physiol. 276: R818-R823. (Pubitemid 29157512)
20. Sonti, G., S. E. Ilyin, and C. R. Plata-Salaman. 1996. Anorexia induced by cytokine interactions at pathophysiological concentrations. Am. J. Physiol. 270: R1394-R1402. (Pubitemid 26298639)
21. Bluthe, R. M., S. Laye, B. Michaud, C. Combe, R. Dantzer, and P. Parnet. 2000. Role of interleukin-1β and tumour necrosis factor-α in lipopolysaccharide-induced sickness behaviour: a study with interleukin-1 type I receptor-deficient mice. Eur. J. Neurosci. 12: 4447-4456.
22. Yao, J. H., S. M. Ye, W. Burgess, J. F. Zachary, K. W. Kelley, and R. W. Johnson. 1999. Mice deficient in interleukin-1β converting enzyme resist anorexia induced by central lipopolysaccharide. Am. J. Physiol. 277: R1435-R1443.
23. Laye, S., G. Gheusi, S. Cremona, C. Combe, K. Kelley, R. Dantzer, and P. Parnet. 2000. Endogenous brain IL-1 mediates LPS-induced anorexia and hypothalamic cytokine expression. Am. J. Physiol. 279: R93-R98. (Pubitemid 30625421)
24. Oliveira-dos-Santos, A. J., A. Ho, Y. Tada, J. J. Lafaille, S. Tonegawa, T. W. Mak, and J. M. Penninger. 1999. CD28 costimulation is crucial for the development of spontaneous autoimmune encephalomyelitis. J. Immunol. 162: 4490-4495.
25. McMahon, E. J., S. L. Bailey, C. V. Castenada, H. Waldner, and S. D. Miller. 2005. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat. Med. 11: 335-339.
26. Greter, M., F. L. Heppner, M. P. Lemos, B. M. Odermatt, N. Goebels, T. Laufer, R. J. Noelle, and B. Becher. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11: 328-334. (Pubitemid 40460562)
27. Miller, S. D., E. J. McMahon, B. Schreiner, and S. L. Bailey. 2007. Antigen presentation in the CNS by myeloid dendritic cells drives progression of relapsing experimental autoimmune encephalomyelitis. Ann. NY Acad. Sci. 1103: 179-191.
28. + TH-17 cells in relapsing EAE. Nat. Immunol. 8: 172-180.
29. Hoglund, P., J. Mintern, C. Waltzinger, W. Heath, C. Benoist, and D. Mathis. 1999. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 189: 331-339. (Pubitemid 29063254)
30. Gagnerault, M. C., J. J. Luan, C. Lotton, and F. Lepault. 2002. Pancreatic lymph nodes are required for priming of β cell reactive T cells in NOD mice. J. Exp. Med. 196: 369-377.
31. + T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195: 135-141.
32. Mora, J. R., M. R. Bono, N. Manjunath, W. Weninger, L. L. Cavanagh, M. Rosemblatt, and U. H. Von Andrian. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424: 88-93. (Pubitemid 36834847)
33. Davenport, M. P., M. C. Grimm, and A. R. Lloyd. 2000. A homing selection hypothesis for T-cell trafficking. Immunol. Today 21: 315-317.
34. Lehmann, P. V. 1998. The fate of T cells in the brain: veni, vidi, vici and veni, mori. Am. J. Pathol. 153: 677-680.
35. Brabb, T., P. von Dassow, N. Ordonez, B. Schnabel, B. Duke, and J. Goverman. 2000. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J. Exp. Med. 192: 871-880. (Pubitemid 30737593)
36. Juedes, A. E., and N. H. Ruddle. 2001. Resident and infiltrating central nervous system APCs regulate the emergence and resolution of experimental autoimmune encephalomyelitis. J. Immunol. 166: 5168-5175.
37. Flugel, A., T. Berkowicz, T. Ritter, M. Labeur, D. E. Jenne, Z. Li, J. W. Ellwart, M. Willem, H. Lassmann, and H. Wekerle. 2001. Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 14: 547-560. (Pubitemid 32520866)
38. Miller, S. D., C. L. Vanderlugt, W. S. Begolka, W. Pao, R. L. Yauch, K. L. Neville, Y. Katz-Levy, A. Carrizosa, and B. S. Kim. 1997. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 3: 1133-1136.
39. Itano, A. A., S. J. McSorley, R. L. Reinhardt, B. D. Ehst, E. Ingulli, A. Y. Rudensky, and M. K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19: 47-57.
40. Fairchild, P. J., R. Wildgoose, E. Atherton, S. Webb, and D. C. Wraith. 1993. An autoantigenic T cell epitope forms unstable complexes with class II MHC: a novel route for escape from tolerance induction. Int. Immunol. 5: 1151-1158.
41. Mason, K., D. W. Denney, Jr., and H. M. McConnell. 1995. Kinetics of the reaction of a myelin basic protein peptide with soluble IAu. Biochemistry 34: 14874-14878.
42. Mason, K., D. W. Denney, Jr., and H. M. McConnell. 1995. Myelin basic protein peptide complexes with the class II MHC molecules I-Au and I-Ak form and dissociate rapidly at neutral pH. J. Immunol. 154: 5216-5227.
43. Harrington, C. J., A. Paez, T. Hunkapiller, V. Mannikko, T. Brabb, M. Ahearn, C. Beeson, and J. Goverman. 1998. Differential tolerance is induced in T cells recognizing distinct epitopes of myelin basic protein. Immunity 8: 571-580.
44. Kawakami, N., S. Lassmann, Z. Li, F. Odoardi, T. Ritter, T. Ziemssen, W. E. Klinkert, J. W. Ellwart, M. Bradl, K. Krivacic, et al. 2004. The activation status of neuroantigen-specific T cells in the target organ determines the clinical outcome of autoimmune encephalomyelitis. J. Exp. Med. 199: 185-197. (Pubitemid 38129699)
45. Phillips, M. J., M. Needham, and R. O. Weller. 1997. Role of cervical lymph nodes in autoimmune encephalomyelitis in the Lewis rat. J. Pathol. 182: 457-464.
46. Cserr, H. F., C. J. Harling-Berg, and P. M. Knopf. 1992. Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol. 2: 269-276.
47. Weller, R. O., B. Engelhardt, and M. J. Phillips. 1996. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol. 6: 275-288.
48. + T cells into the central nervous system by professional antigen-presenting cells. Am. J. Pathol. 154: 481-494.
49. Karman, J., C. Ling, M. Sandor, and Z. Fabry. 2004. Initiation of immune responses in brain is promoted by local dendritic cells. J. Immunol. 173: 2353-2361. (Pubitemid 39063091)
50. de Vos, A. F., M. van Meurs, H. P. Brok, L. A. Boven, R. Q. Hintzen, P. van der Valk, R. Ravid, S. Rensing, L. Boon, B. A. 't Hart, and J. D. Laman. 2002. Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J. Immunol. 169: 5415-5423.
51. Caversaccio, M., O. Peschel, and W. Arnold. 1996. The drainage of cerebrospinal fluid into the lymphatic system of the neck in humans. ORL J. Otorhinolaryngol. Relat. Spec. 58: 164-166. (Pubitemid 26187693)
52. Zhang, H., J. R. Podojil, X. Luo, and S. D. Miller. 2008. Intrinsic and induced regulation of the age-associated onset of spontaneous experimental autoimmune encephalomyelitis. J. Immunol. 181: 4638-4647.