Vaccination with dendritic cells pulsed with peptides of myelin basic protein promotes functional recovery from spinal cord injury

Journal of Neuroscience

Volumn 23, Issue 25, 2003, Pages 8808-8819

  Hauben, Ehud ^a   Gothilf, Amalia ^a   Cohen, Avi ^b   Butovsky, Oleg ^a   Nevo, Uri ^a,c   Smirnov, Igor ^b   Yoles, Eti ^b   Akselrod, Solange ^c   Schwartz, Michal ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Proneuron Biotechnologies   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Autoimmunity; CNS trauma; Dendritic cells; Inflammation; Neuroprotection; Neuroregeneration; Spinal cord injury (SCI)

Indexed keywords

MYELIN BASIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MACROPHAGE; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCAR FORMATION; SPINAL CORD INJURY; T LYMPHOCYTE; VACCINATION;

EID: 0141535147     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-25-08808.2003     Document Type: Article

References (58)

1. Basso DM, Beattie MS, Bresnahan JC (1996) Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256.
2. Bavetta S, Hamlyn PJ, Burnstock G, Lieberman AR, Anderson PN (1999) The effects of FK506 on dorsal column axons following spinal cord injury in adult rats: neuroprotection and local regeneration. Exp Neurol 158:382-393.
3. Bazan NG, Rodriguez de Turco EB, Allan G (1995) Mediators of injury in neurotrauma: intracellular signal transduction and gene expression. J Neurotrauma 12:791-814.
4. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463.
5. Behrmann DL, Bresnahan JC, Beattie MS (1994) Modeling of acute spinal cord injury in the rat: neuroprotection and enhanced recovery with methylprednisolone, U-74006F and YM-14673. Exp Neurol 126:61-75.
6. Bethea JR, Nagashima H, Acosta MC, Briceno C, Gomez F, Marcillo AE, Loor K, Green J, Dietrich WD (1999) Systemically administered interleukin-10 reduces tumor necrosis factor-α production and significantly improves functional recovery following traumatic spinal cord injury in rats. J Neurotrauma 16:851-863.
7. Blesch A, Tuszynski MH (1997) Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF-secreting cells. Exp Neurol 148:444-452.
8. Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, Fulga V, Yoles E (2003) Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J Neuroimmunol, in press.
9. Bregman BS (1998) Regeneration in the spinal cord. Curr Opin Neurobiol 8:800-807.
10. Brewer KL, Bethea JR, Yezierski RP (1999) Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp Neurol 159:484-493.
11. Butovsky O, Hauben E, Schwartz M (2001) Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7-2 (CD86) and prevention of cyst formation. FASEB J 15:1065-1067.
12. Constantini S, Young W (1994) The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. J Neurosurg 80:97-111.
13. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
14. Dittel BN, Visintin I, Merchant RM, Janeway Jr CA (1999) Presentation of the self-antigen myelin basic protein by dendritic cells leads to experimental autoimmune encephalomyelitis. J Immunol 163:32-39.
15. Faden AI (1993) Experimental neurobiology of central nervous system trauma. Crit Rev Neurobiol 7:175-186.
16. Fisher J, Levkovitch-Verbin H, Schori H, Yoles E, Butovsky O, Kaye JF, Ben-Nun A, Schwartz M (2001) Vaccination for neuroprotection in the mouse optic nerve: implications for optic neuropathies. J Neurosci 21:136-142.
17. Fong L, Brockstedt D, Benike C, Wu L, Engleman EG (2001) Dendritic cells injected via different routes induce immunity in cancer patients. J Immunol 166:4254-4259.
18. Franzen R, Schoenen J, Leprince P, Joosten E, Moonen G, Martin D (1998) Effects of macrophage transplantation in the injured adult rat spinal cord: a combined immunocytochemical and biochemical study. J Neurosci Res 51:316-327.
19. Galanos C, Freudenberg MA (1993) Mechanisms of endotoxin shock and endotoxin hypersensitivity. Immunobiology 187:346-356.
20. Gaur A, Boehme SA, Chalmers D, Crowe PD, Pahuja A, Ling N, Brocke S, Steinman L, Conlon PJ (1997) Amelioration of relapsing experimental autoimmune encephalomyelitis with altered myelin basic protein peptides involves different cellular mechanisms. J Neuroimmunol 74:149-158.
21. Hauben E, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Akselrod S, Neeman M, Cohen IR, Schwartz M (2000a) Autoimmune T cells as potential neuroprotective therapy for spinal cord injury. Lancet 355:286-287.
22. Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M (2000b) Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 20:6421-6430.
23. Hauben E, Agranov E, Gothilf A, Nevo U, Cohen A, Smirnov I, Steinman L, Schwartz M (2001a) Posttraumatic therapeutic vaccination with modified myelin self-antigen prevents complete paralysis while avoiding autoimmune disease. J Clin Invest 108:591-599.
24. Hauben E, Ibarra A, Mizrahi T, Barouch R,Agranov E, Schwartz M (2001b) Vaccination with a Nogo-A-derived peptide after incomplete spinal cord injury promotes recovery via T-cell-mediated neuroprotective response: comparison with other myelin antigens. Proc Natl Acad Sci USA 98:15173-15178.
25. Hauben E, Mizrahi T, Agranov E, Schwartz M (2002) Sexual dimorphism in the spontaneous recovery from spinal cord injury: a gender gap in beneficial autoimmunity? Eur J Neurosci 16:1731-1740.
26. Jakeman LB, Guan Z, Wei P, Ponnappan R, Dzwonczyk R, Popovich PG, Stokes BT (2000) Traumatic spinal cord injury produced by controlled contusion in mouse. J Neurotrauma 17:299-319.
27. Kipnis J, Yoles E, Schori H, Hauben E, Shaked I, Schwartz M (2001) Neuronal survival after CNS insult is determined by a genetically encoded autoimmune response. J Neurosci 21:4564-4571.
28. + regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci USA 99:15620-15625.
29. Knight SC, Burke F, Bedford PA (2002) Dendritic cells, antigen distribution, and the initiation of primary immune responses to self and non-self antigens. Semin Cancer Biol 12:301-308.
30. Kostulas N, Li HL, Xiao BG, Huang YM, Kostulas V, Link H (2002) Dendritic cells are present in ischemic brain after permanent middle cerebral artery occlusion in the rat. Stroke 33:1129-1134.
31. Lau R, Wang F, Jeffery G, Marty V, Kuniyoshi J, Bade E, Ryback ME, Weber J (2001) Phase I trial of intravenous peptide-pulsed dendritic cells in patients with metastatic melanoma. J Immunother 24:66-78.
32. Lazarov-Spiegler O, Solomon AS, Zeev-Brann AB, Hirschberg DL, Lavie V, Schwartz M (1996) Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J 10:1296-1302.
33. Link H, Huang YM, Masterman T, Xiao BG (2001) Vaccination with autologous dendritic cells: from experimental autoimmune encephalomyelitis to multiple sclerosis. J Neuroimmunol 114:1-7.
34. Liu D, Yang R, Yan X, McAdoo DJ (1994) Hydroxyl radicals generated in vivo kill neurons in the rat spinal cord: electrophysiological, histological, and neurochemical results. J Neurochem 62:37-44.
35. Liu YJ (2001) Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106:259-262.
36. Lutz M, Schuler G (2002) Immature, semi-mature, and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23:445.
37. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223:77-92.
38. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB (2001) Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp Neurol 169:239-254.
39. McMenamin PG (1999) Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 405:553-562.
40. McTigue DM, Tani M, Krivacic K, Chernosky A, Kelner GS, Maciejewski D, Maki R, Ransohoff RM, Stokes BT (1998) Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J Neurosci Res 53:368-376.
41. Mellman I, Steinman RM (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255-258.
42. Menges M, Rossner S, Voigtlander C, Schindler H, Kukutsch NA, Bogdan C, Erb K, Schuler G, Lutz MB (2002) Repetitive injections of dendritic cells matured with tumor necrosis factor a induce antigen-specific protection of mice from autoimmunity. J Exp Med 195:15-21.
43. Mizrahi T, Hauben E, Schwartz M (2002) The tissue-specific self-pathogen is the protective self-antigen: the case of uveitis. J Immunol 169:5971-5977.
44. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M (1999) Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 5:49-55.
45. Nevo U, Hauben E, Yoles E, Agranov E, Akselrod S, Schwartz M, Neeman M (2001) Diffusion anisotropy MRI for quantitative assessment of recovery in injured rat spinal cord. Magn Reson Med 45:1-9.
46. Nevo U, Kipnis J, Golding I, Shaked I, Neumann A, Akselrod S, Schwartz M (2003) Autoimmunity as a special case of immunity: removing threats from within. Trends Mol Med 9:88-93.
47. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M (1998) Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821.
48. Sai T, Milling SW, Mintz B (2002) Freezing and thawing of bone marrow-derived murine dendritic cells with subsequent retention of immunophenotype and of antigen processing and presentation characteristics. J Immunol Methods 264:153-162.
49. + T cells as part of the evolutionary compromise between a "need" and a "risk." Trends Immunol 23:530-534.
50. Schwartz M, Moalem G, Leibowitz-Amit R, Cohen IR (1999) Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22:295-299.
51. Stein DG (2001) Brain damage, sex hormones, and recovery: a new role for progesterone and estrogen? Trends Neurosci 24:386-391.
52. Talmor M, Mirza A, Turley S, Mellman I, Hoffman LA, Steinman RM (1998) Generation or large numbers of immature and mature dendritic cells from rat bone marrow cultures. Eur J Immunol 28:811-817.
53. Turley SJ (2002) Dendritic cells: inciting and inhibiting autoimmunity. Curr Opin Immunol 14:765-770.
54. Ulevitch RJ, Tobias PS (1994) Recognition of endotoxin by cells leading to transmembrane signaling. Curr Opin Immunol 6:125-130.
55. Wildbaum G, Netzer N, Karin N (2002) Tr1 cell-dependent active tolerance blunts the pathogenic effects of determinant spreading. J Clin Invest 110:701-710.
56. Xiao BG, Huang YM, Yang JS, Xu LY, Link H (2001) Bone marrow-derived dendritic cells from experimental allergic encephalomyelitis induce immune tolerance to EAE in Lewis rats. Clin Exp Immunol 125:300-309.
57. Yoles E, Hauben E, Palgi O, Agranov E, Gothilf A, Cohen A, Kuchroo V, Cohen IR, Weiner H, Schwartz M (2001) Protective autoimmunity is a physiological response to CNS trauma. J Neurosci 21:3740-3748.
58. Young W (1996) Spinal cord regeneration [comment]. Science 273:451.