Dendritic cells treated with chloroquine modulate experimental autoimmune encephalomyelitis

Immunology and Cell Biology

Volumn 92, Issue 2, 2014, Pages 124-132

  Thomé, Rodolfo ^a   Issayama, Luidy Kazuo ^a   Digangi, Rosaria ^a   Bombeiro, Andre Luis ^a   Da Costa, Thiago Alves ^a   Ferreira, Isadora Tassinari ^a   De Oliveira, Alexandre Leite Rodrigues ^a   Verinaud, Liana ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Chloroquine; Dendritic cells; Experimental autoimmune encephalomyelitis; Immunomodulation; Neuroinflammation

Indexed keywords

ANTIRHEUMATIC AGENT; CHLOROQUINE;

ADOPTIVE TRANSFER; ANIMAL; ANTIGEN PRESENTATION; CELL PROLIFERATION; DENDRITIC CELL; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOLOGY; MOUSE; PATHOLOGY; T LYMPHOCYTE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN PRESENTATION; ANTIRHEUMATIC AGENTS; CELL PROLIFERATION; CHLOROQUINE; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; MICE; T-LYMPHOCYTES;

EID: 84893824447     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2013.73     Document Type: Article

References (77)

1. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767-811. (Pubitemid 30365397)
2. Mahnke K, Johnson TS, Ring S, Enk AH. Tolerogenic dendritic cells and regulatory T cells: a two-way relationship. J Dermatol Sci 2007; 46: 159-167. (Pubitemid 46601842)
3. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252. (Pubitemid 28155090)
4. Lange C, Durr M, Doster H, Melms A, Bischof F. Dendritic cell-regulatory T-cell interactions control self-directed immunity. Immunol Cell Biol 2007; 85: 575-581. (Pubitemid 350224203)
5. Liu YJ, Kanzler H, Soumelis V, Gilliet M. Dendritic cell lineage, plasticity and crossregulation. Nat Immunol 2001; 2: 585-589. (Pubitemid 32677624)
6. Kim J, Smith-Garvin J, Koretzky G, Jordan M. The requirements for natural Th17 cell development are distinct from those of conventional Th17 cells. J Exp Med 2011; 208: 2201-2207.
7. Lu Y, Hong S, Li H, Park J, Hong B, Wang L et al. Th9 cells promote antitumor immune responses in vivo. J Clin Invest 2012; 122: 4160-4171.
8. Wu B, Huang C, Kato-Maeda M, Hopewell PC, Daley CL, Krensky AM et al. IL-9 is associated with an impaired Th1 immune response in patients with tuberculosis. Clin Immunol 2008; 126: 202-210.
9. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J ExpMed 2007; 204: 57-63. (Pubitemid 46148756)
10. Lim DS, Kang MS, Jeong JA, Bae YS, Semi-mature DC. are immunogenic and not tolerogenic when inoculated at a high dose in collagen-induced arthritis mice. Eur J Immunol 2009; 39: 1334-1343.
11. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 2002; 23: 445-449. (Pubitemid 35015188)
12. Terness P, Oelert T, Ehser S, Chuang JJ, Lahdou I, Kleist C et al. Mitomycin C-treated dendritic cells inactivate autoreactive T cells: toward the development of a tolerogenic vaccine in autoimmune diseases. Proc Natl Acad Sci USA 2008; 105: 18442-18447.
13. Zhou F, Ciric B, Zhang GX, Rostami A. Immune tolerance induced by intravenous transfer of immature dendritic cells via up-regulating numbers of suppressive IL- 10(+) IFN-gamma (+)-producing CD4 (+) T cells. Immunol Res 2013; 56: 1-8.
14. Min SY, Park KS, Cho ML, Kang JW, Cho YG, Hwang SY et al. Antigen-induced, tolerogenic CD11c+,CD11b+ dendritic cells are abundant in Peyer?s patches during the induction of oral tolerance to type II collagen and suppress experimental collageninduced arthritis. Arthritis Rheum 2006; 54: 887-898.
15. Giannoukakis N, Phillips B, Finegold D, Harnaha J, Trucco M. Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care 2011; 34: 2026-2032.
16. Farias AS, Spagnol GS, Bordeaux-Rego P, Oliveira CO, Fontana AG, de Paula RF et al. Vitamin D3 induces IDO(+) tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther 2013; 19: 269-277.
17. Alarcon GS. Effect of hydroxychloroquine on the survival of patients with systemic lupus erythematosus: data from LUMINA, a multiethnic US cohort (LUMINA L). Ann Rheum Dis 2007; 66: 1168-1172. (Pubitemid 47309732)
18. Scott DL, Dawes PT, Tunn E, Fowler PD, Shadforth MF, Fisher J et al. Combination therapy with gold and hydroxychloroquine in rheumatoid arthritis: a prospective, randomized, placebo-controlled study. Br J Rheumatol 1989; 28: 128-133. (Pubitemid 19117059)
19. Felson DT, Anderson JJ, Meenan RF. The comparative efficacy and toxicity of secondline drugs in rheumatoid arthritis. Results of two metaanalyses. Arthritis Rheum 1990; 33: 1449-1461. (Pubitemid 20362087)
20. Thome R, Lopes SCP, Costa FTM, Verinaud L. Chloroquine: modes of action of an undervalued drug. Immunol Lett 2013; 153: 50-57.
21. Lombard-Platlet S, Bertolino P, Deng H, Gerlier D, Rabourdin-Combe C. Inhibition by chloroquine of the class II major histocompatibility complex-restricted presentation of endogenous antigens varies according to the cellular origin of the antigen-presenting cells, the nature of the T-cell epitope, and the responding T cell. Immunology 1993; 80: 566-573. (Pubitemid 24010116)
22. Garulli B, Stillitano MG, Barnaba V, Castrucci MR. Primary CD8+ T-cell response to soluble ovalbumin is improved by chloroquine treatment in vivo. Clin Vaccine Immunol 2008; 15: 1497-1504.
23. Ziegler HK, Unanue ER. Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc Natl Acad Sci USA 1982; 79: 175-178. (Pubitemid 12181509)
24. Goldman FD, Gilman AL, Hollenback C, Kato RM, Premack BA, Rawlings DJ. Hydroxychloroquine inhibits calcium signals in T cells: a new mechanism to explain its immunomodulatory properties. Blood 2000; 95: 3460-3466. (Pubitemid 30428477)
25. Legssyer R, Josse C, Piette J, Ward RJ, Crichton RR. Changes in function of iron-loaded alveolar macrophages after in vivo administration of desferrioxamine and/or chloroquine. J Inorg Biochem 2003; 94: 36-42. (Pubitemid 36293412)
26. Savarino A. A historical sketch of the discovery and development of HIV-1 integrase inhibitors. Expert Opin Investig Drugs 2006; 15: 1507-1522. (Pubitemid 44848975)
27. Picot S, Peyron F, Donadille A, Vuillez JP, Barbe G, Ambroise-Thomas P. Chloroquineinduced inhibition of the production of TNF, but not of IL-6, is affected by disruption of iron metabolism. Immunology 1993; 80: 127-133. (Pubitemid 23284200)
28. Thome R, Moraes AS, Bombeiro AL, Farias AD, Francelin C, da Costa TA et al. Chloroquine treatment enhances regulatory T Cells and reduces the severity of experimental autoimmune encephalomyelitis. PLoS One 2013; 8: e65913.
29. Namer IJ, Steibel J, Poulet P, Armspach JP, Mohr M, Mauss Y et al. Blood-brain barrier breakdown in MBP-specific T cell induced experimental allergic encephalomyelitis. A quantitative in vivo MRI study. Brain 1993; 116 (Pt 1), 147-159. (Pubitemid 23087040)
30. Engelhardt B, Ransohoff RM. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 2005; 26: 485-495. (Pubitemid 41139258)
31. Mix E, Meyer-Rienecker H, Hartung HP, Zettl UK. Animal models of multiple sclerosis- potentials and limitations. Prog Neurobiol 2010; 92: 386-404.
32. Ghigo D, Aldieri E, Todde R, Costamagna C, Garbarino G, Pescarmona G et al. Chloroquine stimulates nitric oxide synthesis in murine, porcine, and human endothelial cells. J Clin Invest 1998; 102: 595-605. (Pubitemid 28376162)
33. Ahmed MH, Osman MM. Why does chloroquine impair renal function?: chloroquine may modulate the renal tubular response to vasopressin either directly by inhibiting cyclic AMP generation, or indirectly via nitric oxide. Med Hypotheses 2007; 68: 140-143. (Pubitemid 44767611)
34. Ahmed MH, Ashton N, Balment RJ. The effect of chloroquine on renal function and vasopressin secretion: a nitric oxide-dependent effect. J Pharmacol Exp Ther 2003; 304: 156-161. (Pubitemid 36008923)
35. Hrabak A, Sefrioui H, Vercruysse V, Temesi A, Bajor T, Vray B. Action of chloroquine on nitric oxide production and parasite killing by macrophages. Eur J Pharmacol 1998; 354: 83-90. (Pubitemid 28410234)
36. Park YC, Pae HO, Yoo JC, Choi BM, Jue DM, Chung HT. Chloroquine inhibits inducible nitric oxide synthase expression in murine peritoneal macrophages. Pharmacol Toxicol 1999; 85: 188-191. (Pubitemid 29484985)
37. Liao B, Zhao W, Beers DR, Henkel JS, Appel SH. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp Neurol 2012; 237: 147-152.
38. Huang H, Dawicki W, Zhang X, Town J, Gordon J. Tolerogenic dendritic cells induce CD4+CD25hiFoxp3+ regulatory T cell differentiation from CD4+CD25-/loFoxp3- effector T cells. J Immunol 2010; 185: 5003-5010.
39. Canadian Rheumatology Association. Canadian Consensus Conference on hydroxychloroquine. J Rheumatol 2000; 27: 2919-2921.
40. Gladman DD, Urowitz MB, Senecal JL, Fortin PJ, Petty RE, Esdaile JM et al. Aspects of use of antimalarials in systemic lupus erythematosus. J Rheumatol 1998; 25: 983-985. (Pubitemid 28210566)
41. Sundelin SP, Terman A. Different effects of chloroquine and hydroxychloroquine on lysosomal function in cultured retinal pigment epithelial cells. APMIS 2002; 110: 481-489. (Pubitemid 34856490)
42. Fox RI. Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum 1993; 23 (2 Suppl 1), 82-91.
43. McChesney EW, Banks WF Jr., Sullivan DJ. Metabolism of chloroquine and hydroxychloroquine in albino and pigmented rats. Toxicol Appl Pharmacol 1965; 7: 627-636.
44. Wibo M, Poole B. Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J Cell Biol 1974; 63 (2 Pt 1), 430-440.
45. Demachi-Okamura A, Torikai H, Akatsuka Y, Miyoshi H, Yoshimori T, Kuzushima K. Autophagy creates a CTL epitope that mimics tumor-associated antigens. PLoS One 2012; 7: e47126.
46. Savarino A, Boelaert JR, Cassone A, Majori G, Cauda R. Effects of chloroquine on viral infections: an old drug against today?s diseases? Lancet Infect Dis 2003; 3: 722-727. (Pubitemid 37345352)
47. Lutz MB. Therapeutic potential of semi-mature dendritic cells for tolerance induction. Front Immunol 2012; 3: 123.
48. Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol 2002; 20: 621-667. (Pubitemid 34293436)
49. Petkovic F, Blazevski J, Momcilovic M, Mostarica Stojkovic M, Miljkovic D. Nitric oxide inhibits CXCL12 expression in neuroinflammation. Immunol Cell Biol 2013; 91: 427-434.
50. Gregory SH, Wing EJ, Hoffman RA, Simmons RL. Reactive nitrogen intermediates suppress the primary immunologic response to Listeria. J Immunol 1993; 150: 2901-2909. (Pubitemid 23127539)
51. Pearl JE, Torrado E, Tighe M, Fountain JJ, Solache A, Strutt T et al. Nitric oxide inhibits the accumulation of CD4+CD44hiTbet+CD69lo T cells in mycobacterial infection. Eur J Immunol 2012; 42: 3267-3279.
52. Niedbala W, Alves-Filho JC, Fukada SY, Vieira SM, Mitani A, Sonego F et al. Regulation of type 17 helper T-cell function by nitric oxide during inflammation. Proc Natl Acad Sci USA 2011; 108: 9220-9225.
53. Niedbala W, Cai B, Liu H, Pitman N, Chang L, Liew FY. Nitric oxide induces CD4+ CD25+ Foxp3 regulatory T cells from CD4+CD25 T cells via p53, IL-2, and OX40. Proc Natl Acad Sci USA 2007; 104: 15478-15483.
54. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003; 19: 59-70. (Pubitemid 36859901)
55. Ji Q, Castelli L, Goverman JM. MHC class I-restricted myelin epitopes are crosspresented by Tip-DCs that promote determinant spreading to CD8(+) T cells. Nat Immunol 2013; 14: 254-261.
56. Kania G, Siegert S, Behnke S, Prados-Rosales R, Casadevall A, Luscher TF et al. Innate signaling promotes formation of regulatory nitric oxide-producing dendritic cells limiting T-cell expansion in experimental autoimmune myocarditis. Circulation 2013; 127: 2285-2294.
57. Thompson AG, Thomas R. Induction of immune tolerance by dendritic cells: implications for preventative and therapeutic immunotherapy of autoimmune disease. Immunol Cell Biol 2002; 80: 509-519. (Pubitemid 35335013)
58. Carranza F, Falcon CR, Nunez N, Knubel C, Correa SG, Bianco I et al. Helminth antigens enable CpG-activated dendritic cells to inhibit the symptoms of collageninduced arthritis through Foxp3+ regulatory T cells. PLoS One 2012; 7: e40356.
59. Nikolic T, Roep BO. Regulatory multitasking of tolerogenic dendritic cells-lessons taken from vitamin d3-treated tolerogenic dendritic cells. Front Immunol 2013; 4: 113.
60. Zhou F, Lauretti E, di Meco A, Ciric B, Gonnella P, Zhang GX et al. Intravenous transfer of apoptotic cell-treated dendritic cells leads to immune tolerance by blocking Th17 cell activity. Immunobiology 2013; 218: 1069-1076.
61. Clemente AM, Fadigati G, Caporale R, Marchese DG, Castronovo G, Sannella AR et al. Modulation of the immune and inflammatory responses by Plasmodium falciparum schizont extracts: role of myeloid dendritic cells in effector and regulatory functions of CD4+ lymphocytes. Infect Immun 2013; 81: 1842-1851.
62. Skorokhod OA, Alessio M, Mordmuller B, Arese P, Schwarzer E. Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J Immunol 2004; 173: 4066-4074. (Pubitemid 39280771)
63. Tian L, Ma L, Kaarela T, Li Z. Neuroimmune crosstalk in the central nervous system and its significance for neurological diseases. J Neuroinflammation 2012; 9: 155.
64. Pekny M, Wilhelmsson U, Bogestal YR, Pekna M. The role of astrocytes and complement system in neural plasticity. Int Rev Neurobiol 2007; 82: 95-111.
65. Kang W, Hebert JM. Signaling pathways in reactive astrocytes, a genetic perspective. Mol Neurobiol 2011; 43: 147-154.
66. Ridet JL, Malhotra SK, Privat A, Gage FH. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 1997; 20: 570-577. (Pubitemid 27508969)
67. Karimi-Abdolrezaee S, Billakanti R. Reactive astrogliosis after spinal cord injurybeneficial and detrimental effects. Mol Neurobiol 2012; 46: 251-264.
68. Prodinger C, Bunse J, Kruger M, Schiefenhovel F, Brandt C, Laman JD et al. CD11cexpressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system. Acta neuropathologica 2011; 121: 445-458.
69. Loehberg CR, Strissel PL, Dittrich R, Strick R, Dittmer J, Dittmer A et al. Akt and p53 are potential mediators of reduced mammary tumor growth by Chloroquine and the mTOR inhibitor RAD001. Biochem Pharmacol 2012; 83: 480-488.
70. Rosborough BR, Raich-Regue D, Matta BM, Lee K, Gan B, Depinho RA et al. Murine dendritic cell rapamycin-resistant and rictor-independent mTOR controls IL-10, B7-H1, and regulatory T-cell induction. Blood 2013; 121: 3619-3630.
71. Bernstein HN. Ophthalmologic considerations and testing in patients receiving longterm antimalarial therapy. Am J Med 1983; 75: 25-34. (Pubitemid 13025977)
72. Bernstein HN. Chloroquine ocular toxicity. Surv Ophthalmol 1967; 12: 415-447.
73. Raines MF, Bhargava SK, Rosen ES. The blood-retinal barrier in chloroquine retinopathy. Invest Ophthalmol Vis Sci 1989; 30: 1726-1731. (Pubitemid 19214992)
74. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999; 223: 77-92. (Pubitemid 29096240)
75. Ruberti M, Fernandes LG, Simioni PU, Gabriel DL, Yamada AT, Tamashiro WM. Phenotypical and functional analysis of intraepithelial lymphocytes from small intestine of mice in oral tolerance. Clin Dev Immunol 2012; 2012: 208054. http:// dx.doi.org/10.1155/2012/208054.
76. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982; 126: 131-138. (Pubitemid 13203451)
77. Delgado GT, Thome R, Gabriel DL, Tamashiro WM, Pastore GM. Yacon (Smallanthus sonchifolius)-derived fructooligosaccharides improves the immune parameters in the mouse. Nutr Res 2012; 32: 884-892.