Transplantation of autologous adipose stem cells lacks therapeutic efficacy in the experimental autoimmune encephalomyelitis model

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zhang, Xiujuan ^a,b   Bowles, Annie C ^b,c   Semon, Julie A ^b   Scruggs, Brittni A ^b   Zhang, Shijia ^b   Strong, Amy L ^b   Gimble, Jeffrey M ^d   Bunnell, Bruce A ^b,c,e  

^a School of Petroleum and Chemical Engineering Dalian University of Technology Panjin Campus   (China)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Tulane University   (United States)

^d PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^e TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KERATIN; MEMBRANE ANTIGEN; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOLOGOUS ADIPOSE STEM CELL TRANSPLANTATION; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL DIFFERENTIATION; CELL INFILTRATION; CELL ISOLATION; CELL STRUCTURE; COLONY FORMING UNIT; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; SPINAL CORD LESION; STEM CELL EXPANSION; THERAPY EFFECT; WILD TYPE;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; TRANSPLANTATION, AUTOLOGOUS; TREATMENT FAILURE;

EID: 84898647373     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085007     Document Type: Article

References (49)

1. Miller DH (2004) Biomarkers and surrogate outcomes in neurodegenerative disease: lessons from multiple sclerosis. NeuroRx 1: 284-294.
2. Hemmer B, Nessler S, Zhou D, Kieseier B, Hartung HP (2006) Immunopathogenesis and immunotherapy of multiple sclerosis. Nat Clin Pract Neurol 2: 201-211.
3. Kieseier BC, Wiendl H, Hemmer B, Hartung HP (2007) Treatment and treatment trials in multiple sclerosis. Curr Opin Neurol 20: 286-293. (Pubitemid 46743110)
4. Fisher-Shoval Y, Barhum Y, Sadan O, Yust-Katz S, Ben-Zur T, et al. (2012) Transplantation of Placenta-Derived Mesenchymal Stem Cells in the EAE Mouse Model of MS. J Mol Neurosci.
5. Baker D, Jackson SJ (2007) Models of Multiple Sclerosis. ACNR 6: 10-12.
6. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, et al. (2005) Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106: 1755-1761. (Pubitemid 41208591)
7. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, et al. (2008) Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 65: 753-761. (Pubitemid 351831453)
8. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, et al. (2009) Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 57: 1192-1203.
9. Rafei M, Birman E, Forner K, Galipeau J (2009) Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther 17: 1799-1803.
10. Rafei M, Campeau PM, Aguilar-Mahecha A, Buchanan M, Williams P, et al. (2009) Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. J Immunol 182: 5994-6002.
11. Gordon D, Pavlovska G, Uney JB, Wraith DC, Scolding NJ (2010) Human mesenchymal stem cells infiltrate the spinal cord, reduce demyelination, and localize to white matter lesions in experimental autoimmune encephalomyelitis. J Neuropathol Exp Neurol 69: 1087-1095.
12. Lanz TV, Opitz CA, Ho PP, Agrawal A, Lutz C, et al. (2010) Mouse mesenchymal stem cells suppress antigen-specific TH cell immunity independent of indoleamine 2,3-dioxygenase 1 (IDO1). Stem Cells Dev 19: 657-668.
13. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24: 150-154.
14. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, et al. (2009) Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27: 2624-2635.
15. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, et al. (2003) Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174: 101-109. (Pubitemid 36819010)
16. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T (2005) Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52: 2521-2529. (Pubitemid 41117441)
17. Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, et al. (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99: 1285-1297.
18. Kern S, Eichler H, Stoeve J, Klüter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24: 1294-1301. (Pubitemid 44464698)
19. Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, et al. (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212: 702-709. (Pubitemid 47271882)
20. Schäffler A, Büchler C (2007) Concise review: adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25: 818-827.
21. Payne N, Dantanarayana A, Sun G, Moussa L, Caine S, et al. (2012) Early intervention with gene-modified mesenchymal stem cells overexpressing interleukin-4 enhances anti-inflammatory responses and functional recovery in experimental autoimmune demyelination. Cell Adh Migr 6.
22. Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J (2005) Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106: 4057-4065. (Pubitemid 41775910)
23. Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100: 1249-1260. (Pubitemid 46742916)
24. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108. (Pubitemid 351818697)
25. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
26. Niimi N, Kohyama K, Matsumoto Y (2013) Minocycline suppresses experimental autoimmune encephalomyelitis by increasing tissue inhibitors of metalloproteinases. Neuropathology doi: 10.1111/neup.12039.
27. Gerdoni E, Gallo B, Casazza S, Musio S, Bonanni I, et al. (2007) Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 61: 219-227. (Pubitemid 46557346)
28. Semon JA, Zhang X, Pandey AC, Alandete SM, Maness C, et al. (2013) Administration of murine stromal vascular fraction ameliorates chronic experimental autoimmune encephalomyelitis. Stem Cells Transl Med 2: 789-796.
29. Sela J, Applebaum J, Uretzky G (1986) Osteogenesis induced by bone matrix is inhibited by inflammation. Biomater Med Devices Artif Organs 14: 227-237. (Pubitemid 17219839)
30. Liu Y, Liu W, Hu C, Xue Z, Wang G, et al. (2011) MiR-17 modulates osteogenic differentiation through a coherent feed-forward loop in mesenchymal stem cells isolated from periodontal ligaments of patients with periodontitis. Stem Cells 29: 1804-1816.
31. Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29: 313-326.
32. Dawson J, Miltz W, Mir AK, Wiessner C (2003) Targeting monocyte chemoattractant protein-1 signalling in disease. Expert Opin Ther Targets 7: 35-48. (Pubitemid 36204587)
33. Mahad DJ, Ransohoff RM (2003) The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 15: 23-32. (Pubitemid 36092176)
34. Ge S, Shrestha B, Paul D, Keating C, Cone R, et al. (2012) The CCL2 synthesis inhibitor bindarit targets cells of the neurovascular unit, and suppresses experimental autoimmune encephalomyelitis. J Neuroinflammation 9: 171.
35. Fuentes ME, Durham SK, Swerdel MR, Lewin AC, Barton DS, et al. (1995) Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J Immunol 155: 5769-5776.
36. Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV (2003) Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase. J Cell Sci 116: 4615-4628. (Pubitemid 37461616)
37. Song L, Pachter JS (2004) Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvasc Res 67: 78-89. (Pubitemid 38050226)
38. Toft-Hansen H, Buist R, Sun XJ, Schellenberg A, Peeling J, et al. (2006) Metalloproteinases control brain inflammation induced by pertussis toxin in mice overexpressing the chemokine CCL2 in the central nervous system. J Immunol 177: 7242-7249. (Pubitemid 44715093)
39. Yao Y, Tsirka SE (2011) Truncation of monocyte chemoattractant protein 1 by plasmin promotes blood-brain barrier disruption. J Cell Sci 124: 1486-1495.
40. Godiska R, Chantry D, Dietsch GN, Gray PW (1995) Chemokine expression in murine experimental allergic encephalomyelitis. J Neuroimmunol 58: 167-176.
41. Luo Y, Fischer FR, Hancock WW, Dorf ME (2000) Macrophage inflammatory protein-2 and KC induce chemokine production by mouse astrocytes. J Immunol 165: 4015-4023. (Pubitemid 32057313)
42. Liang J, Zhang H, Hua B, Wang H, Wang J, et al. (2009) Allogeneic mesenchymal stem cells transplantation in treatment of multiple sclerosis. Mult Scler 15: 2.
43. Freedman SM, Bar-Or A, Atkins LH, Karussis D, Frassoni F, et al. (2010) The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: consensus report of the International MSCT Study Group. Mult Scler 16: 7.
44. Mallam E, Kemp K, Wilkins A, Rice C, Scolding N (2010) Characterization of in vitro expanded bone marrow-derived mesenchymal stem cells from patients with multiple sclerosis. Multiple Sclerosis 16: 909-918.
45. Mohyeddin Bonab M, Yazdanbakhsh S, Lotfi J, Alimoghaddom K, Talebian F, et al. (2007) Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran J Immunol 4: 50-57. (Pubitemid 46799666)
46. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, et al. (2010) Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 67: 1187-1194.
47. Yamout B, Hourani R, Salti H, Barada W, El-Hajj T, et al. (2010) Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study. J Neuroimmunol 227: 185-189.
48. Connick P, Kolappan M, Crawley C, Webber DJ, Patani R, et al. (2012) Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Lancet Neurol 11: 150-156.
49. Uccelli A, Laroni A, Freedman MS (2012) Mesenchymal stem cells as treatment for MS - progress to date. Multiple Sclerosis Journal 0: 1-5.