Effective combination of human bone marrow mesenchymal stem cells and minocycline in experimental autoimmune encephalomyelitis mice

Stem Cell Research and Therapy

Volumn 4, Issue 4, 2013, Pages

  Hou, Yun ^a   Ryu, Chung Heon ^b   Park, Kwang Ywel ^b   Kim, Seong Muk ^b   Jeong, Chang Hyun ^a   Jeun, Sin Soo ^a,b  

^a The Catholic University of Korea   (South Korea)

^b The Catholic University of Korea   (South Korea)

Author keywords

Demyelination; EAE; hBM MSCs; Minocycline; MS; Neuroprotection

Indexed keywords

CELL MARKER; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MINOCYCLINE; TUMOR NECROSIS FACTOR ALPHA; ANTIINFECTIVE AGENT;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL COUNT; CELL DIFFERENTIATION; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; DEMYELINATION; DOSE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VIVO STUDY; INFLAMMATORY CELL; LOW DRUG DOSE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; MYELITIS; NERVE CELL NECROSIS; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPINAL CORD ATROPHY; TH1 CELL; TH2 CELL; THERAPY EFFECT; TREATMENT OUTCOME; ANIMAL; APOPTOSIS; BONE MARROW CELL; C57BL MOUSE; DISEASE MODEL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES;

MUS;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; BONE MARROW CELLS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MINOCYCLINE;

EID: 84879819444     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt228     Document Type: Article

References (40)

1. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW, Brain 2002 125 1297 1308 10.1093/brain/awf133 12023318 (Pubitemid 34587139)
2. Inhibition of autoimmune encephalomyelitis by a tetracycline. Popovic N, Schubart A, Goetz BD, Zhang SC, Linington C, Duncan ID, Ann Neurol 2002 51 215 223 10.1002/ana.10092 11835378 (Pubitemid 34111444)
3. Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Metz LM, Zhang Y, Yeung M, Patry DG, Bell RB, Stoian CA, Yong VW, Patten SB, Duquette P, Antel JP, Mitchell JR, Ann Neurol 2004 55 756 10.1002/ana.20111 15122721 (Pubitemid 38544341)
4. Multiple neuroprotective mechanisms of minocycline in autoimmune CNS inflammation. Maier K, Merkler D, Gerber J, Taheri N, Kuhnert AV, Williams SK, Neusch C, Bähr M, Diem R, Neurobiol Dis 2007 25 514 525 10.1016/j.nbd.2006.10.022 17239606
5. Minocycline down-regulates MHC II expression in microglia and macrophages through inhibition of IRF-1 and protein kinase C (PKC)alpha/betaII. Nikodemova M, Watters JJ, Jackson SJ, Yang SK, Duncan ID, J Biol Chem 2007 282 15208 15216 10.1074/jbc.M611907200 17395590 (Pubitemid 47093379)
6. Effective combination of minocycline and interferon-beta in a model of multiple sclerosis. Giuliani F, Fu SA, Metz LM, Yong VW, J Neuroimmunol 2005 165 83 91 10.1016/j.jneuroim.2005.04.020 15958276 (Pubitemid 40984625)
7. Combination of methylprednisolone and minocycline synergistically improves experimental autoimmune encephalomyelitis in C57 BL/6 mice. Chen X, Pi R, Liu M, Ma X, Jiang Y, Liu Y, Mao X, Hu X, J Neuroimmunol 2010 226 104 109 10.1016/j.jneuroim.2010.05.039 20538348
8. Combined treatment with atorvastatin and minocycline suppresses severity of EAE. Luccarini I, Ballerini C, Biagioli T, Biamonte F, Bellucci A, Rosi MC, Grossi C, Massacesi L, Casamenti F, Exp Neurol 2008 211 214 226 10.1016/j.expneurol.2008.01.022 18346732
9. Minocycline and lupuslike syndrome in acne patients. Sturkenboom MC, Meier CR, Jick H, Stricker BH, Arch Intern Med 1999 159 493 497 10.1001/archinte.159.5.493 10074958 (Pubitemid 29108915)
10. Minocycline-induced autoimmune syndromes: an overview. Elkayam O, Yaron M, Caspi D, Semin Arthritis Rheum 1999 28 392 397 10.1016/S0049-0172(99)80004-3 10406406 (Pubitemid 29289376)
11. Chemotactic and cytotoxic effects of minocycline on human retinal pigment epithelial cells. Hollborn M, Wiedemann P, Bringmann A, Kohen L, Invest Ophthalmol Vis Sci 2010 51 2721 2729 10.1167/iovs.09-4661 20019360
12. Effects of minocycline and doxycycline on cell survival and gene expression in human gingival and periodontal ligament cells. Suzuki A, Yagisawa J, Kumakura S, Tsutsui T, J Periodont Res 2006 41 124 131 10.1111/j.1600-0765. 2005.00843.x 16499715 (Pubitemid 43341285)
13. Mesenchymal stem cells: biology and potential clinical uses. Deans RJ, Moseley AB, Exp Hematol 2000 28 875 884 10.1016/S0301-472X(00)00482-3 10989188
14. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM, Blood 2002 99 3838 3843 10.1182/blood.V99.10.3838 11986244 (Pubitemid 34534559)
15. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A, Blood 2005 106 1755 1761 10.1182/blood-2005-04-1496 15905186 (Pubitemid 41208591)
16. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, Miller SD, Miller RH, Glia 2009 57 1192 1203 10.1002/glia.20841 19191336
17. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R, Exp Hematol 2002 30 42 48 10.1016/S0301-472X(01)00769-X 11823036 (Pubitemid 34059216)
18. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M, Exp Neurol 2005 195 16 26 10.1016/j.expneurol.2005.03.018 15904921 (Pubitemid 41116810)
19. Bone marrow stromal cells reduce axonal loss in experimental autoimmune encephalomyelitis mice. Zhang J, Li Y, Lu M, Cui Y, Chen J, Noffsinger L, Elias SB, Chopp M, J Neurosci Res 2006 84 587 595 10.1002/jnr.20962 16773650 (Pubitemid 44196699)
20. Remyelination of the spinal cord following intravenous delivery of bone marrow cells. Akiyama Y, Radtke C, Honmou O, Kocsis JD, Glia 2002 39 229 236 10.1002/glia.10102 12203389
21. Multilineage potential of adult human mesenchymal stem cells. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR, Science 1999 284 143 147 10.1126/science.284.5411.143 10102814 (Pubitemid 29282067)
22. Combination therapy of lovastatin and rolipram provides neuroprotection and promotes neurorepair in inflammatory demyelination model of multiple sclerosis. Paintlia AS, Paintlia MK, Singh I, Skoff RB, Singh AK, Glia 2009 57 182 193 10.1002/glia.20745 18720408
23. The promise of minocycline in neurology. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM, Lancet Neurol 2004 3 7447 7451
24. The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Chabas D, Baranzini SE, Mitchell D, Bernard CC, Rittling SR, Denhardt DT, Sobel RA, Lock C, Karpuj M, Pedotti R, Heller R, Oksenberg JR, Steinman L, Science 2001 294 1731 1735 10.1126/science.1062960 11721059 (Pubitemid 33104847)
25. Th1/Th2 cytokine balance and nitric oxide in cerebrospinal fluid and serum from patients with multiple sclerosis. Rodríguez-Sáinz Mdel C, Sánchez-Ramón S, de Andrés C, Rodríguez-Mahou M, Muñoz-Fernández MA, Eur Cytokine Netw 2002 13 110 114 11956029
26. Cytokine shifts and tolerance in experimental autoimmune encephalomyelitis. Chitnis T, Khoury SJ, Immunol Res 2003 28 223 239 10.1385/IR:28:3:223 14713716 (Pubitemid 38091061)
27. Beta-interferon unbalances the peripheral T cell proinflammatory response in experimental autoimmune encephalomyelitis. Martín-Saavedra FM, Flores N, Dorado B, Eguiluz C, Bravo B, García-Merino A, Ballester S, Mol Immunol 2007 44 3597 3607 10.1016/j.molimm.2007.03.002 17420051 (Pubitemid 46754436)
28. Two types of murine helper T cell clone: I. Definition according to profiles of lymphokine activities and secreted proteins. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL, J Immunol 1986 136 2348 2357 2419430 (Pubitemid 16136806)
29. Combined medication of lovastatin with rolipram suppresses severity of experimental autoimmune encephalomyelitis. Paintlia AS, Paintlia MK, Singh I, Singh AK, Exp Neurol 2008 214 168 180 10.1016/j.expneurol.2008.07.024 18775426
30. + T-cell subsets in autoimmunity. O'Garra A, Steinman L, Gijbels K, Curr Opin Immunol 1997 9 872 883 10.1016/S0952-7915(97)80192-6 9492992 (Pubitemid 28062274)
31. Minocycline attenuates experimental autoimmune encephalomyelitis in rats by reducing T cell infiltration into the spinal cord. Nikodemova M, Lee J, Fabry Z, Duncan ID, J Neuroimmunol 2010 219 33 37 10.1016/j.jneuroim.2009.11.009 20089316
32. Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. Bjartmar C, Wujek JR, Trapp BD, J Neurol Sci 2003 206 165 171 10.1016/S0022-510X(02)00069-2 12559505 (Pubitemid 36143722)
33. Inhibition of glial cell activation ameliorates the severity of experimental autoimmune encephalomyelitis. Guo X, Nakamura K, Kohyama K, Harada C, Behanna HA, Watterson DM, Matsumoto Y, Harada T, Neurosci Res 2007 59 457 466 10.1016/j.neures.2007.08.014 17920148 (Pubitemid 350007814)
34. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J, J Neurosci 2001 21 2580 2588 11306611 (Pubitemid 32298200)
35. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. Tikka TM, Koistinaho JE, J Immunol 2001 166 7527 7533 11390507 (Pubitemid 32525632)
36. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, Slavin S, Abramsky O, Karussis D, Arch Neurol 2008 65 753 761 10.1001/archneur.65.6.753 18541795 (Pubitemid 351831453)
37. Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1. Block GJ, Ohkouchi S, Fung F, Frenkel J, Gregory C, Pochampally R, DiMattia G, Sullivan DE, Prockop DJ, Stem Cells 2009 27 670 681 19267325
38. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. Akiyama Y, Radtke C, Kocsis JD, J Neurosci 2002 22 6623 6630 12151541 (Pubitemid 35386418)
39. Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. Chopp M, Zhang XH, Li Y, Wang L, Chen J, Lu D, Lu M, Rosenblum M, Neuroreport 2000 11 3001 3005 10.1097/00001756-200009110-00035 11006983
40. Mesenchymal stem cells for the treatment of neurodegenerative disease. Joyce N, Annett G, Wirthlin L, Olson S, Bauer G, Nolta JA, Regen Med 2010 5 933 946 10.2217/rme.10.72 21082892