Effect of DAB389IL-2 immunotoxin on the course of experimental autoimmune encephalomyelitis in Lewis rats

Journal of the Neurological Sciences

Volumn 263, Issue 1-2, 2007, Pages 59-69

  Phillips, S Michael ^b,e   Bhopale, Mahendra K ^c,e   Constantinescu, Cris S ^d,e   Ciric, Bogoljub ^a,e   Hilliard, Brendan ^b,e   Ventura, Elvira ^a,e   Lavi, Ehud ^b,e   Rostami, Abdolmohamad ^b,e  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

DAB389IL 2; EAE; IL 2; Immunotherapy; Immunotoxin

Indexed keywords

ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; DIPHTHERIA TOXIN; HYBRID PROTEIN; IMMUNOTOXIN DAB 389 INTERLEUKIN 2 FUSION PROTEIN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; MITOGENIC AGENT; MYELIN BASIC PROTEIN; RECOMBINANT PROTEIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CHRONOPHARMACOLOGY; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE SEVERITY; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG EXPOSURE; DRUG FATALITY; FEMALE; GENETIC ENGINEERING; GUINEA PIG; IMMUNIZATION; IMMUNOMODULATION; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; LEWIS RAT; LYMPHOCYTE PROLIFERATION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; TISSUE HOMOGENATE;

ANIMALS; ANTIGENS, CD; CELL PROLIFERATION; CELLS, CULTURED; DIPHTHERIA TOXIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GUINEA PIGS; IMMUNOTOXINS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MUTATION; MYELIN BASIC PROTEINS; RATS; RATS, INBRED LEW; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT FUSION PROTEINS; SEVERITY OF ILLNESS INDEX; SPINAL CORD; T-LYMPHOCYTES, HELPER-INDUCER; TIME FACTORS;

EID: 35649019809     PISSN: 0022510X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jns.2007.05.032     Document Type: Article

References (67)

1. Noseworthy J.H., Lucchinetti C., Rodriguez M., and Weinshenker B.G. Multiple sclerosis. N Engl J Med 343 (2000) 938-952 [Review]
2. Barnett M.H., and Sutton I. The pathology of multiple sclerosis: a paradigm shift. Curr Opin Neurol 19 (2006) 242-247
3. Hauser S.L., and Oksenberg J.R. The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 52 (2006) 61-76 [Review]
4. Martin Mdel P., and Monson N.L. Potential role of humoral immunity in the pathogenesis of multiple sclerosis (MS) and experimental autoimmune encephalomyelitis (EAE). Front Biosci 12 (2007) 2735-2749
5. Barnett M.H., Henderson A.P., and Prineas J.W. The macrophage in MS: just a scavenger after all? Pathology and pathogenesis of the acute MS lesion. Mult Scler 12 (2006) 121-132 [Review]
6. Merkler D., Schmelting B., Czeh B., Fuchs E., Stadelmann C., and Bruck W. Myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis in the common marmoset reflects the immunopathology of pattern II multiple sclerosis lesions. Mult Scler 12 (2006) 369-374
7. Bruck W. Inflammatory demyelination is not central to the pathogenesis of multiple sclerosis. J Neurol 252 Suppl 5 (2005) v10-v15 [Review]
8. Okuda Y., Okuda M., Apatoff B.R., and Posnet D.N. The activation of memory CD4+ cells and CD8+ T cells in patients with multiple sclerosis. J Neurol Sci 235 (2005) 11-17
9. Venken K., Hellings N., Hensen K., Rummens J.L., Medaer R., D'Hooghe M.B., et al. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+CD25+ regulatory T-cell function and FOXP3 expression. J Neurosci Res 83 (2006) 1432-1446
10. Gran B., and Rostami A. T cells, cytokines, and autoantigens in multiple sclerosis. Curr Neurol Neurosci Rep 1 (2001) 263-270 [Review]
11. Hofstetter H.H., Toyka K.V., and Gold R. Permanent effector phenotype of neuroantigen-specific T cells acquired in the central nervous system during experimental allergic encephalomyelitis. Neurosci Lett 39 (2006) 127-130
12. Tang X., Maricic I., Purohit N., Bakamjian B., Reed-Loisel L.M., Beeston T., et al. Regulation of Immunity by a Novel Population of Qa-1-Restricted CD8{alpha}{alpha}+ TCR {alpha}beta+ T Cells. J Immunol 177 (2006) 7645-7655
13. Pastor S., Vaccaro C.G., Minguela A., Ober R.J., and Ward E.S. Analyses of TCR clustering at the T cell-antigen-presenting cell interface and its impact on the activation of naive CD4+ T cells. Int Immunol 18 (2006) 1615-1625
14. Paust S., and Cantor H. Regulatory. T cells and autoimmune disease. Immunol Rev 204 (2005) 195-207 [Review]
15. Espinoza-Delgado I., Ortaldo J.R., Winkler-Pickett R., Sugamura K., Varesio L., and Longo D.L. Expression and role of p75 interleukin 2 receptor on human monocytes. J Exp Med 171 (1990) 1821-1826
16. Sanchez A.J., Puerta C., Ballester S., Gonzalez P., Arriaga A., and Garcia-Merino A. Rolipram impairs NF-kappaB activity and MMP-9 expression in experimental autoimmune encephalomyelitis. J Neuroimmunol 168 (2005) 13-20
17. Fujii M., Sugamura K., Sano K., Nakai M., Sugita K., and Hinuma Y. High-affinity receptor-mediated internalization and degradation of interleukin 2 in human T cells. J Exp Med 163 (1986) 550-562
18. Kohm A.P., Carpentier P.A., and Miller S.D. Regulation of experimental autoimmune encephalomyelitis (EAE) by CD4+CD25+ regulatory T cells. Novartis Found Symp 252 (2003) 45-52 [Review]
19. Chen X., Oppenheim J.J., Winkler-Pickett R.T., Ortaldo J.R., and Howard O.M. Glucocorticoid amplifies IL-2-dependent expansion of functional FoxP3(+)CD4(+)CD25(+) T regulatory cells in vivo and enhances their capacity to suppress EAE. Eur J Immunol 36 (2006) 2139-2149
20. Williams D.P., Parker K., Bacha P., Bishai W., Borowski M., Genbauffe F., et al. Diphtheria toxin receptor binding domain substitution with interleukin-2: genetic construction and properties of a diphtheria toxin-related interleukin-2 fusion protein. Protein Eng 1 (1987) 493-498
21. Bacha P., Williams D.P., Waters C., Williams J.M., Murphy J.R., and Strom T.B. Interleukin-2 receptor targeted cytotoxicity: interleukin-2 receptor mediated action of a diphtheria toxin-related interleukin-2 fusion protein. J Exp Med 167 (1988) 612-622
22. Walz G., Zanker B., Brand K., Waters C., Genbauffe F., Zeldis J.B., et al. Sequential effects of interleukin 2-diphtheria toxin fusion protein on T-cell activation. Proc Natl Acad Sci U S A 86 (1989) 9485-9488
23. Williams D.P., Wen Z., Watson R.S., Boyd J., Strom T.B., and Murphy J.R. Cellular processing of the interleukin-2 fusion toxin DAB486-IL-2 and efficient delivery of diphtheria fragment A to the cytosol of target cells requires Arg194. J Biol Chem 265 (1990) 20673-20677
24. Kelley V.E., Bacha P., Pankewycz O., Nichols J.C., Murphy J.R., and Strom T.B. Interleukin-2 diphtheria toxin fusion protein can abolish cell-mediated immunity in vivo. Proc Natl Acad Sci U S A 85 (1988) 3980-3984
25. Pacheco-Solva A., Bastos M.G., Pankewycz O., Muggia R.A., Murphy J.R., Strom T.B., et al. IL-2 toxin treatment blocks diabetogenic autoimmunity in NOD mice. Eur J Immunol 22 (1992) 697-702
26. Woodworth T.G. Early clinical studies of IL-2 fusion toxin in patients with severe rheumatoid arthritis and recently onset insulin-dependent diabetes mellitus. Clin Exp Rheumatol Suppl 8 (1993) S177-S180
27. Bacha P., Forte S.E., Perper S.J., Trentham D.E., and Nichols J.C. Anti-arthritic effects demonstrated by an interleukin-2 receptor-targeted cytotoxin (DAB486IL-2) in rat adjuvant arthritis. Eur J Immunol 22 (1992) 1673-1679
28. McIntosh K.K., Linsley P.S., Bacha P.A., and Drachman D.B. Immunotherapy of experimental autoimmune myasthenia gravis: selective effects of CTLA4Ig and synergistic combination with an IL2-diphtheria toxin fusion protein. J Neuroimmunol 87 (1998) 136-146
29. Kjeldsen K., Simonsen O., and Heron I. Immunity against diphtheria 25-30 years after primary vaccination in childhood. Lancet 1 (1985) 900-902
30. Kiyokawa T., Williams D.P., Snider C.E., Strom T.B., and Murphy J.R. Protein engineering of diphtheria-toxin-interleukin-2 fusion products to increase cytotoxic potency for high-affinity IL-2-receptor-bearing target cells. Protein Eng 4 (1991) 463-468
31. Dannull J., Su Z., Rizzieri D., Yang B.K., Coleman D., Yancey D., et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 115 (2005) 3623-3633
32. Deibler G.E., Martenson R.E., and Kies M.W. Large scale preparation of myelin basic protein from central nervous tissue of several mammalian species. Prep Biochem 2 (1972) 139-165
33. Chalk J.B., McCombe P.A., Smith R., and Pender M.P. Clinical and histological findings in proteolipid protein-induced experimental autoimmune encephalomyelitis (EAE) in the Lewis rat. Distribution of demyelination differs from that in EAE induced by other antigens. J Neurol Sci 123 (1994) 154-161
34. Fujioka T., Purev E., Kremlev S.G., Ventura E.S., and Rostami A.M. Flow cytometric analysis of infiltrating cells in the peripheral nerves in experimental allergic neuritis. J Neuroimmunol 108 (2000) 181-191
35. Fritzsching B., Korporal M., Haas J., Krammer P.H., Suri-Payer E., and Wildemann B. Similar sensitivity of regulatory T cells towards CD95L-mediated apoptosis in patients with multiple sclerosis and healthy individuals. J Neurol Sci 251 (2006) 91-97
36. Hellings N., Baree M., Verhoeven C., D'hooghe M.B., Medaer R., Bernard C.C., et al. T-cell reactivity to multiple myelin antigens in multiple sclerosis patients and healthy controls. J Neurosci Res 163 (2001) 290-302
37. Suri-Payer E., and Fritzsching B. Regulatory T cells in experimental autoimmune disease. Springer Semin Immunopathol 28 (2006) 3-16
38. Gartner D., Hoff H., Gimsa U., Burmester G.R., and Brunner-Weinzierl M.C. CD25 regulatory T cells determine secondary but not primary remission in EAE: impact on long-term disease progression. J Neuroimmunol 172 (2006) 73-84
39. Cohen A.C., Nadeau K.C., Tu W., Hwa V., Dionis K., Bezrodnik L., et al. Cutting edge: decreased accumulation and regulatory function of CD4+ CD25(high) T cells in human STAT5b deficiency. J Immunol 177 (2006) 2770-2774
40. Zajicek J. Diagnosis and disease modifying treatments in multiple sclerosis. Postgrad Med J 81 (2005) 556-561 [Review]
41. Farrell R., Heaney D., and Giovannoni G. Emerging therapies in multiple sclerosis. Expert Opin Emerg Drugs 10 (2005) 797-816 [Review]
42. Pede P.D., Visintini D., Telera A., Cucurachi L., Campanini C., Immovilli P., et al. Immunomodulatory effects of IFN-beta1a treatment alone or associated with pentoxifylline in patients with relapsing-remitting multiple sclerosis (RRMS). J Interferon Cytokine Res 25 (2005) 485-489
43. + regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol 169 (2002) 4712-4716
44. Furtado G.C., Curotto de Lafaille M.A., Kutchukhidze N., and Lafaille J.J. Interleukin 2 signaling is required for CD4 (+) regulatory T cell function. J Exp Med 196 (2002) 851-857
45. Takahashi T., Kuniyasu Y., Toda M., Sakaguchi N., Itoh M., Iwata M., et al. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 10 (1998) 1969-1980
46. Thornton A.M., and Shevach E.M. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188 (1998) 287-296
47. Sharfe N., Dadi H.K., Shahar M., and Roifman C.M. Human immune disorder arising from mutation of the alpha chain of the interleukin-2 receptor. Proc Natl Acad Sci U S A 94 (1997) 3168-3171
48. Sakaguchi S. Fox3+CD25+CD4+ regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212 (2006) 8-27
49. Grunebaum E., Sharfe N., and Roifman C.M. Human T cell immunodeficiency: when signal transduction goes wrong. Immunol Res 35 (2006) 117-126 [Review]
50. Norris M.S., McConnell T.J., and Mannie M.D. Interleukin-2 promotes antigenic reactivity of rested T cells but prolongs the postactivational refractory phase of activated T cells. Cell Immunol 211 (2001) 51-60
51. Malek T.R., Yu A., Vincek V., Scibelli P., and Kong L. CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rbeta-deficient mice. Implications for the nonredundant function of IL-2. Immunity 17 (2002) 167-178
52. Williams D.P., Snider C.E., Strom T.B., and Murphy J.R. Structure/function analysis of interleukin-2-toxin (DAB486-IL-2). Fragment B sequences required for the delivery of fragment A to the cytosol of target cells. J Biol Chem 265 (1990) 11885-11889
53. Almeida A.R., Legrand N., Papiernik M., and Freitas A.A. Homeostasis of peripheral CD4+ T cells: IL-2R alpha and IL-2 shape a population of regulatory cells that controls CD4+ T cell numbers. Immunology 169 (2002) 4850-4860
54. Steinman L. Myelin-specific CD8 T cells in the pathogenesis of experimental allergic encephalitis and multiple sclerosis. J Exp Med 194 (2001) F27-F30
55. 389IL-2. I. Studies of in vitro and in vivo efficacy. Cell Immunol 166 (1995) 217-226
56. Beraud E., Lorberboum-Galski H., Chan C.C., FitzGerald D., Pastan I., and Nussenblatt R.B. Immunospecific suppression of encephalitogenic-activated T lymphocytes by chimeric cytotoxin IL-2-PE40. Cell Immunol 133 (1991) 379-389
57. Rose J.W., Lorberboum-Galski H., Fitzgerald D., McCarron R., Hill K.E., Townsend J.J., et al. Chimeric cytotoxin IL2-PE40 inhibits relapsing experimental allergic encephalomyelitis. J Neuroimmunol 32 (1991) 209-217
58. Rook G.A., Ristori G., Salvetti M., Giovannoni G., Thompson E.J., and Stanford J.L. Bacterial vaccines for the treatment of multiple sclerosis and other autoimmune disorders. Immunol Today 21 (2000) 503-508
59. Sewell D.L., Reinke E.K., Co D.O., Hogan L.H., Fritz R.B., Sandor M., et al. Infection with Mycobacterium bovis BCG diverts traffic of myelin oligodendroglial glycoprotein autoantigen-specific T cells away from the central nervous system and ameliorates experimental autoimmune encephalomyelitis. Clin Diagn Lab Immunol 10 (2003) 564-572
60. Hu H., Stavrou S., Cairns Baker B., Tomatore C., Scharff J., Okunieff P., et al. Depletion of T lymphocytes with immunotoxin retards the progress of experimental allergic encephalomyelitis in rhesus monkeys. Cell Immunol 177 (1997) 26-34
61. Hong J., Li N., Zhang X., Zheng B., and Zhang J.Z. Induction of CD4+CD25+ regulatory T cells by copolymer-I through activation of transcription factor Foxp3. Proc Natl Acad Sci U S A 102 (2005) 6449-6454
62. Kumar M., Putzki N., Limmroth V., Remus R., Lindemann M., Knop D., et al. CD4(+)CD25(+)FoxP3(+) T lymphocytes fail to suppress myelin basic protein-induced proliferation in patients with multiple sclerosis. J Neuroimmunol 180 (2006) 178-184
63. Venken K., Hellings N., Hensen K., Rummens J.L., Medaer R., D'hooghe M.B., et al. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+CD25+ regulatory T-cell function and FOXP3 expression. J Neurosci Res 83 (2006) 1432-1446
64. Kuzel T.M. DAB(389)IL-2 (denileukin diftitox, ONTAK): review of clinical trials to date. Clin Lymphoma 1 (2000) S33-S36 [Suppl]
65. Polder K., Wang C., Duvic M., Diwan A.H., Parks D., Jankov A., et al. Toxic epidermal necrolysis associated with denileukin diftitox (DAB389IL-2) administration in a patient with follicular large cell lymphoma. Leuk Lymphoma 46 (2005) 1807-1811
66. Attia P., Maker A.V., Haworth L.R., Rogers-Freezer L., and Rosenberg S.A. Inability of a fusion protein of IL-2 and diphtheria toxin (Denileukin Diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma. J Immunother 28 (2005) 582-592
67. Kawakami K., Nakajima O., Morishita R., and Nagai R. Targeted anticancer immunotoxins and cytotoxic agents with direct killing moieties. Sci World J 6 (2006) 781-790 [Review]