Paradoxical effect of chloroquine treatment in enhancing chikungunya virus infection

Viruses

Volumn 10, Issue 5, 2018, Pages

  Roques, Pierre ^a   Thiberville, Simon Djamel ^b,e   Dupuis Maguiraga, Laurence ^a   Lum, Fok Moon ^c   Labadie, Karine ^a,f   Martinon, Frédéric ^a   Gras, Gabriel ^a   Lebon, Pierre ^d   Ng, Lisa F P ^c   de Lamballerie, Xavier ^b   Le Grand, Roger ^a  

^a CEA Fontenay aux Roses Bâtiment 61   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c AGENCY FOR SCIENCE   (Singapore)

^d Paris Descartes University ^*  (France)

^e Infectious Disease and Internal Medicine   (France)

^f CENTRE NATIONAL DE SÉQUENÇAGE   (France)

Author keywords

Alphavirus; Chikungunya; Chloroquine; Macaque; Monocyte macrophage

Indexed keywords

CHLOROQUINE; IMMUNOGLOBULIN M;

ARTICLE; CHIKUNGUNYA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; GENERAL PRACTITIONER; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LYMPHOCYTOPENIA; MACACA FASCICULARIS; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIREMIA; VIRUS REPLICATION; ANIMAL; CELL CULTURE; CHIKUNGUNYA VIRUS; COHORT ANALYSIS; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; EPIDEMIC; FIBROBLAST; IMMUNITY; IMMUNOLOGY; MACROPHAGE; MALE; REUNION; VIROLOGY; VIRUS LOAD;

ANIMALS; CELLS, CULTURED; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; CHLOROQUINE; COHORT STUDIES; DISEASE MODELS, ANIMAL; DISEASE OUTBREAKS; FIBROBLASTS; HUMANS; IMMUNITY; MACACA FASCICULARIS; MACROPHAGES; MALE; REUNION; VIRAL LOAD; VIRUS REPLICATION;

EID: 85047499799     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v10050268     Document Type: Article

References (48)

1. Mason, P.J.; Haddow, A.J. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952–53: An additional note on Chikungunya virus isolations and serum antibodies. Trans. R. Soc. Trop. Med. Hyg. 1957, 51, 238–240. [CrossRef]
2. Dupuis-Maguiraga, L.; Noret, M.; Brun, S.; Le Grand, R.; Gras, G.; Roques, P. Chikungunya disease: Infection-associated markers from the acute to the chronic phase of arbovirus-induced arthralgia. PLoS Negl. Trop. Dis. 2012, 6. [CrossRef] [PubMed]
3. Ahola, T.; Courderc, T.; Ng, L.F.; Hallengärd, D.; Powers, A.; Lecuit, M.; Esteban, M.; Merits, A.; Roques, P.; Liljeström, P. Therapeutics and vaccines against chikungunya virus. Vector Borne Zoonotic Dis. 2015, 15, 250–257. [CrossRef] [PubMed]
4. Bettadapura, J.; Herrero, L.J.; Taylor, A.; Mahalingam, S. Approaches to the treatment of disease induced by chikungunya virus. Indian J. Med. Res. 2013, 138, 762–765. [PubMed]
5. Weaver, S.C.; Lecuit, M. Chikungunya virus and the global spread of a mosquito-borne disease. N. Engl. J. Med. 2015, 372, 1231–1239. [CrossRef] [PubMed]
6. Cassell, S.; Edwards, J.; Brown, D.T. Effects of lysosomotropic weak bases on infection of BHK-21 cells by Sindbis virus. J. Virol. 1984, 52, 857–864. [PubMed]
7. Coombs, K.; Mann, E.; Edwards, J.; Brown, D.T. Effects of chloroquine and cytochalasin B on the infection of cells by Sindbis virus and vesicular stomatitis virus. J. Virol. 1981, 37, 1060–1065. [PubMed]
8. Helenius, A.; Marsh, M.; White, J. Inhibition of Semliki forest virus penetration by lysosomotropic weak bases. J. Gen. Virol. 1982, 58, 47–61. [CrossRef] [PubMed]
9. Inglot, A.D. Comparison of the antiviral activity in vitro of some non-steroidal anti-inflammatory drugs. J. Gen. Virol. 1969, 4, 203–214. [CrossRef] [PubMed]
10. Savarino, A.; Di Trani, L.; Donatelli, I.; Cauda, R.; Cassone, A. New insights into the antiviral effects of chloroquine. Lancet Infect. Dis. 2006, 6, 67–69. [CrossRef]
11. Shimizu, Y.; Yamamoto, S.; Homma, M.; Ishida, N. Effect of chloroquine on the growth of animal viruses. Arch. Die Gesamte Virusforsch. 1972, 36, 93–104. [CrossRef]
12. De Lamballerie, X.; Boisson, V.; Reynier, J.C.; Enault, S.; Charrel, R.N.; Flahault, A.; Roques, P.; Le Grand, R. On chikungunya acute infection and chloroquine treatment. Vector Borne Zoonotic Dis. 2008, 8, 837–839. [CrossRef] [PubMed]
13. Khan, M.; Santhosh, S.R.; Tiwari, M.; Lakshmana Rao, P.V.; Parida, M. Assessment of in vitro prophylactic and therapeutic efficacy of chloroquine against Chikungunya virus in vero cells. J. Med. Virol. 2010, 82, 817–824. [CrossRef] [PubMed]
14. De Lamballerie, X.; Ninove, L.; Charrel, R.N. Antiviral treatment of chikungunya virus infection. Infect. Disord. Drug Targets 2009, 9, 101–104. [CrossRef] [PubMed]
15. Thiberville, S.D.; Boisson, V.; Gaudart, J.; Simon, F.; Flahault, A.; de Lamballerie, X. Chikungunya Fever: A clinical and virological investigation of outpatients on reunion island, South-west Indian ocean. PLoS Negl. Trop. Dis. 2013, 7. [CrossRef] [PubMed]
16. Labadie, K.; Larcher, T.; Joubert, C.; Mannioui, A.; Delache, B.; Brochard, P.; Guigand, L.; Dubreil, L.; Lebon, P.; Verrier, B.; et al. Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J. Clin. Investig. 2010, 120, 894–906. [CrossRef] [PubMed]
17. Spouge, J.L. Statistical analysis of sparse infection data and its implications for retroviral treatment trials in primates. Proc. Natl. Acad. Sci. USA 1992, 89, 7581–7585. [CrossRef] [PubMed]
18. Rolain, J.M.; Mallet, M.N.; Raoult, D. Correlation between serum doxycycline concentrations and serologic evolution in patients with Coxiella burnetii endocarditis. J. Infect. Dis. 2003, 188, 1322–1325. [CrossRef] [PubMed]
19. Malleret, B.; Maneglier, B.; Karlsson, I.; Lebon, P.; Nascimbeni, M.; Perié, L.; Brochard, P.; Delache, B.; Calvo, J.; Andrieu, T.; et al. Primary infection with simian immunodeficiency virus: Plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood 2008, 112, 4598–4608. [CrossRef] [PubMed]
20. Martinon, F.; Kaldma, K.; Sikut, R.; Culina, S.; Romain, G.; Tuomela, M.; Adojaan, M.; Männik, A.; Toots, U.; Kivisild, T.; et al. Persistent immune responses induced by a human immunodeficiency virus DNA vaccine delivered in association with electroporation in the skin of nonhuman primates. Hum. Gene Ther. 2009, 20, 1291–1307. [CrossRef] [PubMed]
21. Zeger, S.L.; Liang, K.Y.; Albert, P.S. Models for longitudinal data: A generalized estimating equation approach. Biometrics 1988, 44, 1049–1060. [CrossRef] [PubMed]
22. Hoarau, J.J.; Jaffar Bandjee, M.C.; Trotot, P.K.; Das, T.; Li-Pat-Yuen, G.; Dassa, B.; Denizot, M.; Guichard, E.; Ribera, A.; Henni, T.; et al. Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. J. Immunol. 2010, 184, 5914–5927. [CrossRef] [PubMed]
23. Mzayek, F.; Deng, H.; Mather, F.J.; Wasilevich, E.C.; Liu, H.; Hadi, C.M.; Chansolme, D.H.; Murphy, H.A.; Melek, B.H.; Tenaglia, A.N.; et al. Randomized dose-ranging controlled trial of AQ-13, a candidate antimalarial, and chloroquine in healthy volunteers. PLoS Clin. Trials 2007, 2. [CrossRef] [PubMed]
24. Solomon, V.R.; Lee, H. Chloroquine and its analogs: A new promise of an old drug for effective and safe cancer therapies. Eur. J. Pharmacol. 2009, 625, 220–233. [CrossRef] [PubMed]
25. Couderc, T.; Khandoudi, N.; Grandadam, M.; Visse, C.; Gangneux, N.; Bagot, S.; Prost, J.F.; Lecuit, M. Prophylaxis and therapy for Chikungunya virus infection. J. Infect. Dis. 2009, 200, 516–523. [CrossRef] [PubMed]
26. Jaffar-Bandjee, M.C.; Das, T.; Hoarau, J.J.; Krejbich Trotot, P.; Denizot, M.; Ribera, A.; Roques, P.; Gasque, P. Chikungunya virus takes centre stage in virally induced arthritis: Possible cellular and molecular mechanisms to pathogenesis. Microbes Infect. 2009, 11, 1206–1218. [CrossRef] [PubMed]
27. Kam, Y.-W.; Simarmata, D.; Chow, A.; Her, Z.; Teng, T.-S.; Ong, E.K.S.; Renia, L.; Leo, Y.-S.; Ng, L.F.P. Early appearance of neutralizing IgG3-antibodies is associated with Chikungunya Virus clearance and long-term clinical protection. J. Infect. Dis. 2012, in press.
28. Teng, T.S.; Kam, Y.W.; Lee, B.; Hapuarachchi, H.C.; Wimal, A.; Ng, L.C.; Ng, L.F. A systematic meta-analysis of immune signatures in patients with acute chikungunya virus infection. J. Infect. Dis. 2015, 211, 1925–1935. [CrossRef] [PubMed]
29. Rainsford, K.D.; Parke, A.L.; Clifford-Rashotte, M.; Kean, W.F. Therapy and pharmacological properties of hydroxychloroquine and chloroquine in treatment of systemic lupus erythematosus, rheumatoid arthritis and related diseases. Inflammopharmacology 2015, 23, 231–269. [CrossRef] [PubMed]
30. Soumahoro, M.-K.; Boëlle, P.-Y.; Gauzere, B.A.; Atsou, K.; Pelat, C.; Lambert, B.; La Ruche, G.; Gastellu-Etchegorry, M.; Renault, P.; Sarazin, M.; et al. The chikungunya epidemic on la réunion Island in 2005–2006: A cost-of-illness study. PLoS Negl. Trop. Dis. 2011, 5. [CrossRef] [PubMed]
31. Brighton, S.W. Chloroquine phosphate treatment of chronic Chikungunya arthritis. An open pilot study. S. Afr. Med. J. 1984, 66, 217–218. [PubMed]
32. Savarino, A.; Cauda, R.; Cassone, A. On the use of chloroquine for chikungunya. Lancet Infect. Dis. 2007, 7. [CrossRef]
33. Schilte, C.; Couderc, T.; Chretien, F.; Sourisseau, M.; Gangneux, N.; Guivel-Benhassine, F.; Kraxner, A.; Tschopp, J.; Higgs, S.; Michault, A.; et al. Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. J. Exp. Med. 2010, 207, 429–442. [CrossRef] [PubMed]
34. Silva, M.C.; Guerrero-Plata, A.; Gilfoy, F.D.; Garofalo, R.P.; Mason, P.W. Differential activation of human monocyte-derived and plasmacytoid dendritic cells by West Nile virus generated in different host cells. J. Virol. 2007, 81, 13640–13648. [CrossRef] [PubMed]
35. Desmyter, J.; Melnick, J.L.; Rawls, W.E. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J. Virol. 1968, 2, 955–961. [PubMed]
36. Her, Z.; Malleret, B.; Chan, M.; Ong, E.K.; Wong, S.C.; Kwek, D.J.; Tolou, H.; Lin, R.T.; Tambyah, P.A.; Rénia, L.; et al. Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. J. Immunol. 2010, 184, 5903–5913. [CrossRef] [PubMed]
37. Roques, P.; Gras, G.; Labadie, K.; Larcher, T.; Cherel, Y.; Suhrbier, A.; Grand, R.L. Chikungunya virus infection involved monocytes and during chronic phase of the disease persisted in tissue macrophages. In Proceedings of the 45th Annual Scientific Meeting of the European Society for Clinical Investigation, Crete, Greece, 13–16 April 2011.
38. Maheshwari, R.K.; Srikantan, V.; Bhartiya, D. Chloroquine enhances replication of Semliki Forest virus and encephalomyocarditis virus in mice. J. Virol. 1991, 65, 992–995. [PubMed]
39. Seth, P.; Mani, H.; Singh, A.K.; Banaudha, K.K.; Madhavan, S.; Sidhu, G.S.; Gaddipati, J.P.; Vogel, S.N.; Maheshwari, R.K. Acceleration of viral replication and up-regulation of cytokine levels by antimalarials: implications in malaria-endemic areas. Am. J. Trop. Med. Hyg. 1999, 61, 180–186. [CrossRef] [PubMed]
40. Connolly, K.M.; Stecher, V.J.; Danis, E.; Pruden, D.J.; LaBrie, T. Alteration of interleukin-1 activity and the acute phase response in adjuvant arthritic rats treated with disease modifying antirheumatic drugs. Agents Actions 1988, 25, 94–105. [CrossRef] [PubMed]
41. Katz, S.J.; Russell, A.S. Re-evaluation of antimalarials in treating rheumatic diseases: Re-appreciation and insights into new mechanisms of action. Curr. Opin. Rheumatol. 2011, 23, 278–281. [CrossRef] [PubMed]
42. Savarino, A.; Boelaert, J.R.; 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. [CrossRef]
43. Werneke, S.W.; Schilte, C.; Rohatgi, A.; Monte, K.J.; Michault, A.; Arenzana-Seisdedos, F.; Vanlandingham, D.L.; Higgs, S.; Fontanet, A.; Albert, M.L.; et al. ISG15 is critical in the control of Chikungunya Virus infection independent of UbE1L mediated conjugation. PLoS Pathog. 2011, 7. [CrossRef] [PubMed]
44. Ziegler, H.K.; Unanue, E.R. 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. [CrossRef] [PubMed]
45. Schulz, O.; Diebold, S.S.; Chen, M.; Näslund, T.I.; Nolte, M.A.; Alexopoulou, L.; Azuma, Y.T.; Flavell, R.A.; Liljeström, P.; Reis e Sousa, C. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433, 887–892. [CrossRef] [PubMed]
46. Belizaire, R.; Unanue, E.R. Targeting proteins to distinct subcellular compartments reveals unique requirements for MHC class I and II presentation. Proc. Natl. Acad. Sci. USA 2009, 106, 17463–17468. [CrossRef] [PubMed]
47. Fox, R.I.; Kang, H.I. Mechanism of action of antimalarial drugs: Inhibition of antigen processing and presentation. Lupus 1993, 2 (Suppl. 1), S9–S12. [PubMed]
48. Accapezzato, D.; Visco, V.; Francavilla, V.; Molette, C.; Donato, T.; Paroli, M.; Mondelli, M.U.; Doria, M.; Torrisi, M.R.; Barnaba, V. Chloroquine enhances human CD8+ T cell responses against soluble antigens in vivo. J. Exp. Med. 2005, 202, 817–828. [CrossRef] [PubMed]