Mesenchymal stem cells do not prevent antibody responses against human α-L-iduronidase when used to treat mucopolysaccharidosis type i

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Matsumoto Martin, Priscila Keiko ^a   Stilhano, Roberta Sessa ^a   Samoto, Vivian Yochiko ^b   Takiya, Christina Maeda ^b   Peres, Giovani Bravin ^a   Correa Da Silva Michelacci, Yara Maria ^a   Da Silva, Flavia Helena ^a,c   Pereira, Vanessa Gonçalves ^a   D'Almeida, Vânia ^a   Marques, Fabio Luiz Navarro ^d   Otake, Andreia Hanada ^d,e   Chammas, Roger ^d,e   Han, Sang Won ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e Sao Paulo State Institute of Cancer   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

LEVO IDURONIDASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; BOWMAN CAPSULE; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; ENZYME SYNTHESIS; GLOMERULUS; HURLER SYNDROME; INFLAMMATION; INFLAMMATORY INFILTRATE; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY TUBULE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; TISSUE INJURY;

EID: 84898613417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092420     Document Type: Article

References (44)

1. McKusick VA, Kaplan D, Wise D, Hanley WB, Suddarth SB, et al. (1965) The genetic mucopolysaccharidoses. Medicine (Baltimore) 44: 445-483.
2. Clarke LA, Russell CS, Pownall S, Warrington CL, Borowski A, et al. (1997) Murine mucopolysaccharidosis type I (Pubitemid 27142098)
3. Scriver CR (1995) The metabolic and molecular bases of inherited disease. New York: McGraw-Hill, Health Professions Division.
4. Ponder KP (2008) Immune response hinders therapy for lysosomal storage diseases. J Clin Invest 118: 2686-2689.
5. Brooks DA, Kakavanos R, Hopwood JJ (2003) Significance of immune response to enzyme-replacement therapy for patients with a lysosomal storage disorder. Trends Mol Med 9: 450-453. (Pubitemid 37309647)
6. Wraith JE, Clarke LA, Beck M, Kolodny EH, Pastores GM, et al. (2004) Enzyme replacement therapy for mucopolysaccharidosis I: a randomized, double-blinded, placebo-controlled, multinational study of recombinant human alpha-L-iduronidase (laronidase). J Pediatr 144: 581-588. (Pubitemid 38594757)
7. Wraith JE, Beck M, Lane R, van der Ploeg A, Shapiro E, et al. (2007) Enzyme replacement therapy in patients who have mucopolysaccharidosis I and are younger than 5 years: results of a multinational study of recombinant human alpha-L-iduronidase (laronidase). Pediatrics 120: e37-46. (Pubitemid 47036214)
8. Kakavanos R, Turner CT, Hopwood JJ, Kakkis ED, Brooks DA (2003) Immune tolerance after long-term enzyme-replacement therapy among patients who have mucopolysaccharidosis I. Lancet 361: 1608-1613. (Pubitemid 36578998)
9. Meirelles Lda S, Nardi NB (2003) Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br J Haematol 123: 702-711. (Pubitemid 37468069)
10. da Silva Meirelles L, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119: 2204-2213. (Pubitemid 43960310)
11. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, et al. (2008) Mesenchymal stem cellmediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2: 141-150. (Pubitemid 351181031)
12. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, et al. (2007) Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109: 228-234. (Pubitemid 46053063)
13. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506. (Pubitemid 350159613)
14. Duffy MM, Ritter T, Ceredig R, Griffin MD (2011) Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther 2: 34.
15. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, et al. (2008) Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotox-icity, and cytokine production: role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood 111: 1327-1333. (Pubitemid 351213419)
16. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L (2009) MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood 113: 6576-6583.
17. Francois M, Romieu-Mourez R, Li M, Galipeau J (2012) Human MSC suppression correlates with cytokine induction of indoleamine 2, 3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther 20: 187-195.
18. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, et al. (2005) Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35: 1482-1490. (Pubitemid 40691430)
19. Rafei M, Hsieh J, Fortier S, Li M, Yuan S, et al. (2008) Mesenchymal stromal cell-derived CCL2 suppresses plasma cell immunoglobulin production via STAT3 inactivation and PAX5 induction. Blood 112: 4991-4998.
20. Comoli P, Ginevri F, Maccario R, Avanzini MA, Marconi M, et al. (2008) Human mesenchymal stem cells inhibit antibody production induced in vitro by allostimulation. Nephrol Dial Transplant 23: 1196-1202. (Pubitemid 351767482)
21. Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, et al. (2006) Human mesenchymal stem cells modulate B-cell functions. Blood 107: 367-372. (Pubitemid 43053565)
22. da Silva FH, Pereira VG, Yasumura EG, Tenorio LZ, de Carvalho LP, et al. (2012) Treatment of adult MPSI mouse brains with IDUA-expressing mesenchymal stem cells decreases GAG deposition and improves exploratory behavior. Genet Vaccines Ther 10: 2.
23. Sacramento CB, da Silva FH, Nardi NB, Yasumura EG, Baptista-Silva JC, et al. (2010) Synergistic effect of vascular endothelial growth factor and granulocyte colony-stimulating factor double gene therapy in mouse limb ischemia. J Gene Med 12: 310-319.
24. Aronovich EL, Bell JB, Belur LR, Gunther R, Koniar B, et al. (2007) Prolonged expression of a lysosomal enzyme in mouse liver after Sleeping Beauty transposon-mediated gene delivery: implications for non-viral gene therapy of mucopolysaccharidoses. J Gene Med 9: 403-415. (Pubitemid 46796586)
25. Di Domenico C, Di Napoli D, Gonzalez YRE, Lombardo A, Naldini L, et al. (2006) Limited transgene immune response and long-term expression of human alpha-L-iduronidase in young adult mice with mucopolysaccharidosis type I by liver-directed gene therapy. Hum Gene Ther 17: 1112-1121. (Pubitemid 44749712)
26. Behmer OA TE, Freitas Neto AG (1976) Manual de Técnicas para Histologia Normal e Patológica. Sã Paulo: Edarth.
27. Parise CB, Lisboa B, Takeshita D, Sacramento CB, de Moraes JZ, et al. (2008) Humoral immune response after genetic immunization is consistently improved by electroporation. Vaccine 26: 3812-3817.
28. Kakkis ED, Muenzer J, Tiller GE, Waber L, Belmont J, et al. (2001) Enzyme-replacement therapy in mucopolysaccharidosis I. N Engl J Med 344: 182-188. (Pubitemid 32064139)
29. Dickson P, Peinovich M, McEntee M, Lester T, Le S, et al. (2008) Immune tolerance improves the efficacy of enzyme replacement therapy in canine mucopolysaccharidosis I. J Clin Invest 118: 2868-2876.
30. Baldo G, Mayer FQ, Martinelli BZ, de Carvalho TG, Meyer FS, et al. (2013) Enzyme replacement therapy started at birth improves outcome in difficult-to-treat organs in mucopolysaccharidosis I mice. Mol Genet Metab 109: 33-40.
31. Kobayashi H, Carbonaro D, Pepper K, Petersen D, Ge S, et al. (2005) Neonatal gene therapy of MPS I mice by intravenous injection of a lentiviral vector. Mol Ther 11: 776-789. (Pubitemid 40567982)
32. Dierenfeld AD MM, Vogler CA, Vite CH, Chen AH, Passage M, et al. (2010) Replacing the enzyme alpha-L-iduronidase at birth ameliorates symptoms in the brain and periphery of dogs with mucopolysaccharidosis type I. Sci Transl Med 2: 60-89.
33. Belay E, Matrai J, Acosta-Sanchez A, Ma L, Quattrocelli M, et al. (2010) Novel hyperactive transposons for genetic modification of induced pluripotent and adult stem cells: a nonviral paradigm for coaxed differentiation. Stem Cells 28: 1760-1771.
34. Jin Z, Maiti S, Huls H, Singh H, Olivares S, et al. (2011) The hyperactive Sleeping Beauty transposase SB100X improves the genetic modification of T cells to express a chimeric antigen receptor. Gene Ther 18: 849-856.
35. Grassel S, Stockl S, Jenei-Lanzl Z (2012) Isolation, culture, and osteogenic/chondrogenic differentiation of bone marrow-derived mesenchymal stem cells. Methods Mol Biol 879: 203-267.
36. Bhaumik S, Mitra R, Varalakshmi C, Khar A (2001) Activated macrophages migrate to the subcutaneous tumor site via the peritoneum: a novel route of cell trafficking. Exp Cell Res 266: 44-52. (Pubitemid 32989041)
37. Hopper KE (1986) Kinetics of macrophage recruitment and turnover in peritoneal inflammatory exudates induced by Salmonella or thioglycollate broth. J Leukoc Biol 39: 435-446. (Pubitemid 16106318)
38. Roca M, de Vries EF, Jamar F, Israel O, Signore A (2010) Guidelines for the labelling of leucocytes with (111)In-oxine. Inflammation/Infection Taskgroup of the European Association of Nuclear Medicine. Eur J Nucl Med Mol Imaging 37: 835-841.
39. Becker W, Fischbach W, Jenett M, Reiners C, Borner W (1986) 111In-oxine-labelled white blood cells in the diagnosis and follow-up of Crohn's disease. Klin Wochenschr 64: 141-148. (Pubitemid 16169598)
40. Goedemans WT, de Jong MM (1987) Comparison of several indium-111 ligands in labeling blood cells: effect of diethylpyrocarbonate and CO2. J Nucl Med 28: 1020-1026.
41. Chung S, Ma X, Liu Y, Lee D, Tittiger M, et al. (2007) Effect of neonatal administration of a retroviral vector expressing alpha-L-iduronidase upon lysosomal storage in brain and other organs in mucopolysaccharidosis I mice. Mol Genet Metab 90: 181-192. (Pubitemid 46108606)
42. Zhang H, Zeng X, Sun L (2010) Allogenic bone-marrow-derived mesenchymal stem cells transplantation as a novel therapy for systemic lupus erythematosus. Expert Opin Biol Ther 10: 701-709.
43. Yoshida H, Satoh M, Behney KM, Lee CG, Richards HB, et al. (2002) Effect of an exogenous trigger on the pathogenesis of lupus in (NZB x NZW)F1 mice. Arthritis Rheum 46: 2235-2244.
44. Youd M, Blickarz C, Woodworth L, Touzjian T, Edling A, et al. (2010) Allogeneic mesenchymal stem cells do not protect NZBxNZW F1 mice from developing lupus disease. Clin Exp Immunol 161: 176-186.