Massive apoptosis in lymphoid organs in animal models for primary and secondary progressive multiple sclerosis

American Journal of Pathology

Volumn 167, Issue 6, 2005, Pages 1631-1646

  Tsunoda, Ikuo ^a   Libbey, Jane E ^a   Kuang, Li Qing ^a   Terry, Emily Jane ^a   Fujinami, Robert S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

AGAR GEL ELECTROPHORESIS; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY TITER; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEMYELINATION; DISEASE COURSE; DISEASE EXACERBATION; FEMALE; IMMUNOHISTOCHEMISTRY; LYMPHOID TISSUE; MOUSE; MULTIPLE SCLEROSIS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TH1 CELL; TH2 CELL; THYMOCYTE;

EID: 28244459495     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)61247-3     Document Type: Article

References (83)

1. Willenborg DO, Staykova MA: Cytokines in the pathogenesis and therapy of autoimmune encephalomyelitis and multiple sclerosis. Adv Exp Med Biol 2003, 520:96-119
2. Lublin FD, Reingold SC: Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 1996, 46:907-911
3. Pender MP, Csurhes PA, Wolfe NP, Hooper KD, Good MF, McCombe PA, Greer JM: Increased circulating T cell reactivity to GM3 and GQ1b gangliosides in primary progressive multiple sclerosis. J Clin Neurosci 2003, 10:63-66
4. Sadatipour BT, Greer JM, Pender MP: Increased circulating antiganglioside antibodies in primary and secondary progressive multiple sclerosis. Ann Neuroi 1998, 44:980-983
5. Stevenson VL, Leary SM, Losseff NA, Parker GJM, Barker GJ, Husmani Y, Miller DH, Thompson AJ: Spinal cord atrophy and disability in MS: a longitudinal study. Neurology 1998, 51:234-238
6. 1H MRSI comparison of white matter and lesions in primary progressive and relapsing-remitting MS. Mult Scler 2000, 6:148-155
7. Revesz T, Kidd D, Thompson AJ, Barnard RO, McDonald WI: A comparison of the pathology of primary and secondary progressive multiple sclerosis. Brain 1994, 117:759-765
8. Berger T, Reindl M: Immunopathogenic and clinical relevance of antibodies against myelin oligodendrocyte glycoprotein (MOG) in multiple sclerosis. J Neural Transm 2000, 60 (Suppl):351-360
9. S mouse strains. Brain Pathol 2000, 10:402-418
10. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RAB, Henson PM: A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000, 405:85-90
11. McDonald PP, Fadok VA, Bratton D, Henson PM: Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J Immunol 1999, 163:6164-6172
12. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I: Immunosuppressive effects of apoptotic cells. Nature 1997, 390:350-351
13. Mevorach D, Zhou JL, Song X, Elkon KB: Systemic exposure to irradiated apoptotic cells induces autoantibody production. J Exp Med 1998, 188:387-392
14. Hanayama R, Tanaka M, Miyasaka K, Aozasa K, Koike M, Uchiyama Y, Nagata S: Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 2004, 304:1147-1150
15. Amor S, Groome N, Linington C, Morris MM, Dornmair K, Gardinier MV, Matthieu JM, Baker D: Identification of epitopes of myelin oligodendrocyte glycoprotein for the induction of experimental allergic encephalomyelitis in SJL and Biozzi AB/H mice. J Immunol 1994, 153:4349-4356
16. Papenfuss TL, Rogers CJ, Gienapp I, Yurrita M, McClain M, Damico N, Valo J, Song F, Whitacre CC: Sex differences in experimental autoimmune encephalomyelitis in multiple murine strains. J Neuroimmunol 2004, 150:59-69
17. Tsunoda I, Kuang L-Q, Tolley ND, Whitton JL, Fujinami RS: Enhancement of experimental allergic encephalomyelitis (EAE) by DNA immunization with myelin proteolipid protein (PLP) plasmid DNA, J Neuropathol Exp Neurol 1998, 57:758-767
18. Greer JM, Sobel RA, Sette A, Southwood S, Lees MB, Kuchroo VK: Immunogenic and encephalitogenic epitope clusters of myelin proteolipid protein. J Immunol 1996, 156:371-379
19. Sellins KS, Cohen JJ: Gene induction by γ-irradiation leads to DNA fragmentation in lymphocytes. J Immunol 1987, 139:3199-3206
20. Dropp JJ: Mast cells in mammalian brain. I. Distribution. Acta Anat (Basel) 1976, 94:1-21
21. Mason DY, Cordell J, Brown M, Pallesen G, Ralfkiaer E, Rothbard J Crumpton M, Gatter KC: Detection of T cells in paraffin wax embedded tissue using antibodies against a peptide sequence from the CD3 antigen. J Clin Pathol 1989, 42:1194-1200
22. Tsunoda I, Kuang L-Q, Libbey JE, Fujinami RS: Axonal injury heralds virus-induced demyelination. Am J Pathol 2003, 162:1259-1269
23. Fukuda T, Yoshida T, Okada S, Hatano M, Miki T, Ishibashi K, Okabe S, Koseki H, Hirosawa S, Taniguchi M, Miyasaka N, Tokuhisa T: Disruption of the Bc16 gene results in an impaired germinal center formation, J Exp Med 1997, 186:439-448
24. Tsunoda I, Sette A, Fujinami RS, Oseroff C, Ruppert J, Dahlberg C, Southwood S, Arrhenius T, Kuang L-Q, Kubo RT, Chesnut RW, Ishioka GY: Lipopeptide particles as the immunologically active component of CTL inducing vaccines. Vaccine 1999, 17:675-685
25. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trelstad RL, Bernfield M: Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues, A light and electron microscopic study. J Histochem Cytochem 1987, 35:1079-1088
26. Sanderson RD, Lalor P, Bernfield M: B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul 1989 1:27-35
27. Portera-Cailliau C, Sung C-H, Nathans J. Adler R: Apoptotic photo-receptor cell death in mouse models of retinitis pigmentosa. Proc Natl Acad Sci USA 1994, 91:974-978
28. Tsunoda I, McCright IJ, Kuang L-Q, Zurbriggen A, Fujinami RS: Hydrocephalus in mice infected with a Theiler's murine encephalo-myelitis virus variant. J Neuropathol Exp Neurol 1997, 56:1302-1313
29. Tsunoda I, Tolley ND, Theil DJ, Whitton JL, Kobayashi H, Fujinami RS: Exacerbation of viral and autoimmune animal models for multiple sclerosis by bacterial DNA. Brain Pathol 1999, 9:481-493
30. Martin RM, Brady JL, Lew AM: The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J Immunol Methods 1998, 212:187-192
31. Martin RV, Lew AM: Is IgG2a a good Th1 marker in mice? Immunol Today 1998, 19:49
32. Matous-Malbohan I, Holub M, Krásenska ́ J, Mareš V, Lodin Z: Expermental allergic encephalomyelitis: changes in growth and proliferation within the draining lymph node following injection of basic encephalitogenic protein in Freund's complete adjuvant. Cell Immunol 1974, 12:350-362
33. Matouš-Malbohan I, Holub M, Mareš V, Lodin Z: Experimental allergic encephalomyelitis: the effect of dexamethasone on growth and proliferation in the draining lymph node, Exp Pathol (Jena) 1976, 12:295-300
34. Tsunoda I, Kuang L-Q, Igenge IZM, Fujinami RS: Converting relapsing remitting to secondary progressive experimental allergic encephalomyelitis (EAE) by ultraviolet B irradiation. J Neuroimmunol 2005, 160:122-134
35. Henry K, Farrer-Brown G: A Color Atlas of Thymus and Lymph Node Histopathology with Ultrastructure. Weert, Wolfe Medical Publications Ltd., 1981
36. Viklický V: High frequency of mast cells in spleens of A-strain mice. Experientia 1967, 23:194-195
37. Hockenbery DM, Zutter M, Hickey W, Nahm M, Korsmeyer SJ: BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci USA 1991, 88:6961-6965
38. Krajewski S, Krajewska M, Shabaik A, Miyashita T, Wang HG, Reed JC: Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am J Pathol 1994, 145:1323-1336
39. Pezzella F, Tse AGD, Cordell JL, Pulford KAF, Gatter KC, Mason DY: Expression of the bcl-2 oncogene protein is not specific for the 14; 18 chromosomal translocation. Am J Pathol 1990, 137:225-232
40. Sobel RA: Genetic and epigenetic influence on EAE phenotypes induced with different encephalitogenic peptides. J Neuroimmunol 2000, 108:45-52
41. Muller DM, Pender MP, Greer JM: A neuropathological analysis of experimental autoimmune encephalomyelitis with predominant brain stem and cerebellar involvement and differences between active and passive induction. Acta Neuropathol (Berl) 2000, 100:174-182
42. Abromson-Leeman S, Bronson R, Luo Y, Berman M, Leeman R, Leeman J, Dorf M: T-cell properties determine disease site, clinical presentation, and cellular pathology of experimental autoimmune encephalomyelitis. Am J Pathol 2004, 165:1519-1533
43. Muller DM, Pender MP, Greer JM: Blood-brain barrier disruption and lesion localisation in experimental autoimmune encephalomyelitis with predominant cerebellar and brainstem involvement. J Neuroimmunol 2005, 160:162-169
44. Wensky AK, Furtado GC, Garibaldi Marcondes MC, Chen S, Manfra D, Lira SA, Zagzag D, Lafaille JJ: IFN-γ determines distinct clinical outcomes in autoimmune encephalomyelitis. J Immunol 2005, 174:1416-1423
45. b H chain constant regions are derived from two distinct isotypic genes, Immunogenetics 1989, 29:92-97
46. Chelmicka-Schorr E, Wiegmann K, Wollmann R, Arnason BGW, Kim DH: Immunoaugmenting effect of FK 506 on experimental allergic encephalomyelitis in Lewis rats. J Autoimmun 1998, 11:329-334
47. Lafaille JJ, Van de Keere F, Hsu AL, Baron JL, Haas W, Raine CS, Tonegawa S: Myelin basic protein-specific T helper 2 (Th2) cells cause experimental autoimmune encephalomyelitis in immunodeficient hosts rather than protect them from the disease. J Exp Med 1997, 186:307-312
48. Myers LW, Ellison GW, Fahey JL, Tesler A, Gottlieb MS: Clinical drawbacks of total lymphoid irradiation: the cons. Neurology 1988, 38(Suppl 2):38-41
49. Zandman-Goddard G, Lorber M, Shoenfeld Y: Systemic lupus erythematosus and thymoma-a double-edged sword, Int Arch Allergy Immunol 1995, 108:99-102
50. Sakaguchi S, Sakaguchi N: Thymus, T cells and autoimmunity: various causes but a common mechanism of autoimmune disease. Autoimmunity: Physiology and Disease. Edited by Coutinho A, Kazatchkine MD. New York, Wiley-Liss, Inc., 1994, pp 203-227
51. Shevach EM: Regulatory/suppressor T cells. Fundamental Immunology. Edited by Paul WE. Philadelphia, Lippincott Williams & Wilkins, 2003, pp 935-963
52. + T cells is mediated by interferon-γ and is defective in chronic progressive multiple sclerosis. J Clin Invest 1995, 95:2711-2719
53. Seino K, Harada M, Taniguchi M: NKT cells are relatively resistant to apoptosis, Trends Immunol 2004, 25:219-221
54. Oberholzer C, Oberholzer A, Clare-Salzler M, Moldawer LL: Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J 2001, 15:879-892
55. Oleszak EL, Hoffman BE, Chang JR, Zaczynska E, Gaughan J, Katsetos CD, Platsoucas CD, Harvey N: Apoptosis of infiltrating T cells in the central nervous system of mice infected with Theiler's murine encephalomyelitis virus. Virology 2003, 315:110-123
56. Pedotti R, De Voss JJ, Steinman L, Galli SJ: Involvement of both 'allergic' and 'autoimmune' mechanisms in EAE, MS and other autoimmune diseases. Trends Immunol 2003, 24:479-484
57. Tanzola MB, Robbie-Ryan M, Gutekunst CA, Brown MA: Mast cells exert effects outside the central nervous system to influence experimental allergic encephalomyelitis disease course. J Immunol 2003, 171:4385-4391
58. Zappulla JP, Arock M, Mars LT, Liblau RS: Mast cells: new targets for multiple sclerosis therapy? J Neuroimmunol 2002, 131:5-20
59. Tunon de Lara JM, Okayama Y, McEuen AR, Heusser CH, Church MK, Walls AF: Release and inactivation of interleukin-4by mast cells. Ann NY Acad Sci 1994, 725:50-58
60. Billiau A, Heremans H, Vandekerckhove F, Dijkmans R, Sobis H, Meulepas E, Carton H: Enhancement of experimental allergic encephalomyelitis in mice by antibodies against IFN-γ. J Immunol 1988, 140:1506-1510
61. Lublin FD, Knobler RL, Kalman B, Goldhaber M, Marini J, Perrault M, D'Imperio C, Joseph J, Alkan SS, Korngold R: Monoclonal antigamma interferon antibodies enhance experimental allergic encephalomyelitis. Autoimmunity 1993, 16:267-274
62. Heremans H, Dillen C, Groenen M, Martens E, Billiau A: Chronic relapsing experimental autoimmune encephalomyelitis (CREAE) in mice: enhancement by monoclonal antibodies against interferon-γ. Eur J Immunol 1996, 26:2393-2398
63. Duong TT, St. Louis J, Gilbert JJ, Finkelman FD, Strejah GH: Effect of anti-interferon-γ and anti-interleukin-2 monoclonal antibody treatment on the development of actively and passively induced experimental allergic encephalomyelitis in the SJL/J mouse, J Neuroimmunol 1992, 36:105-115
64. Duong TT, Finkelman FD, Singh B, Strejan GH: Effect of anti-interferon-γ monoclonal antibody treatment on the development of experimental allergic encephalomyelitis in resistant mouse strains. J Neuroimmunol 1994, 53:101-107
65. Neiman RS, Orazi A: Hyposplenism. Disorders of the Spleen. Edited by LiVolsi VA. Philadelphia, W.B. Saunders Company, 1999, pp 47-64
66. Dillon AM, Stein HB, English RA: Splenic atrophy in systemic lupus erythematosus. Ann Intern Med 1982, 96:40-43
67. Piliero P, Furie R: Functional asplenia in systemic lupus erythematosus. Semin Arthritis Rheum 1990, 20:185-189
68. 1 mice. Immunology 1967, 12:179-196
69. Theofilopoulos AN, Dixon FJ: Murine models of systemic lupus erythematosus. Adv Immunol 1985, 37:269-390
70. De Vos AF, van Riel DAJ, van Meurs M, Brok HPM, Boon L, Hintzen RQ, Claassen E, 't Hart BA, Laman JD: Severe T-cell depletion from the PALS leads to altered spleen composition in common marmosets with experimental autoimmune encephalomyelitis (EAE). J Neuroimmunol 2005, 161:29-39
71. Rosenthale ME, Nagra CL: Comparative effects of some immunosuppressive and anti-inflammatory drugs on allergic encephalomyelitis and adjuvant arthritis. Proc Soc Exp Biol Med 1967, 125:149-153
72. Rosenthale ME, Datko LJ, Kassarich J, Schneider F: Chemotherapy of experimental allergic encephalomyelitis (EAE). Arch Int Pharmacodyn 1969, 179:251-275
73. Levine S, Sowinski R, Steinetz B: Effects of experimental allergic encephalomyelitis on thymus and adrenal: relation to remission and relapse. Proc Soc Exp Biol Med 1980, 165:218-224
74. Hara N, Yoshida S, Takai N, Saito T, Tanaka R: Morphological changes of the thymus and spleen with acute experimental allergic encephalomyelitis (EAE) in Lewis rats. No To Shinkei 1986, 38:81-85
75. Oger J, Szuchet S, Antel J, Arnason BGW: A monoclonal antibody against human T suppressor lymphocytes binds specifically to the surface of cultured oligodendrocytes. Nature 1982, 295:66-68
76. Henry J, Miller MM, Pontarotti P: Structure and evolution of the extended B7 family, Immunol Today 1999, 20:285-288
77. Linsley PS, Peach R, Gladstone P, Bajorath J: Extending the B7 (CD80) gene family. Protein Sci 1994, 3:1341-1343
78. Stefferl A, Schubert A, Storch M, Amini A, Mather I, Lassmann H, Linington C: Butyrophilin, a milk protein, modulates the encephalitogenic T cell response to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis. J Immunol 2000, 165:2859-2865
79. Winfield JB: Antilymphocyte autoantibodies. Dubois' Lupus Erythematosus. Edited by Wallace DJ, Hahn BH, Quismorio FP Jr, Klinenberg JR. Baltimore, Williams & Wilkins, 1997, pp 505-515
80. Hotchkiss RS, Swanson PE, Cobb JP, Jacobson A, Buchman TG, Karl IE: Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit Care Med 1997, 25:1298-1307
81. Hotchkiss RS, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, Matuschak GM, Buchman TG, Karl IE: Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999, 27:1230-1251
82. Keel M, Ungethüm U, Steckholzer U, Niederer E, Hartung T, Trentz O, Ertel W: Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis Blood 1997, 90:3356-3363
83. Wang S-D, Huang K-J, Lin Y-S, Lei H-Y: Sepsis-induced apoptosis of the thymocytes in mice. J Immunol 1994, 152:5014-5021