Suramin treatment reduces chikungunya pathogenesis in mice

Antiviral Research

Volumn 134, Issue , 2016, Pages 89-96

  Kuo, Szu Cheng ^a   Wang, Yu Ming ^a   Ho, Yi Jung ^a   Chang, Tein Yao ^a   Lai, Zheng Zong ^a   Tsui, Pei Yi ^a   Wu, Tzong Yuan ^b,c   Lin, Chang Chi ^a  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Animal model; Antiviral; Chikungunya; Suramin

Indexed keywords

GLYCOPROTEIN E2; SURAMIN; ANTIVIRUS AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTHRITIS; ARTICLE; BONE CELL; CARTILAGE CELL; CARTILAGE DEGENERATION; CHIKUNGUNYA; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FOOT EDEMA; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATORY INFILTRATE; MACROPHAGE; MOUSE; MUSCLE CELL; NONHUMAN; PATHOGENESIS; PERIOSTEUM; PERIOSTITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT OUTCOME; VIREMIA; VIRUS LOAD; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CHIKUNGUNYA VIRUS; DISEASE MODEL; DRUG EFFECTS; FOOT; MUSCULOSKELETAL DISEASE; PATHOGENICITY; PATHOLOGY; VIROLOGY; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; DISEASE MODELS, ANIMAL; FOOT; MICE; MICE, INBRED C57BL; MUSCULOSKELETAL DISEASES; SURAMIN; VIRAL LOAD; VIRUS REPLICATION;

EID: 84986269473     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.07.025     Document Type: Article

References (52)

1. Albulescu, I.C., van Hoolwerff, M., Wolters, L.A., Bottaro, E., Nastruzzi, C., Yang, S.C., Tsay, S.C., Hwu, J.R., Snijder, E.J., van Hemert, M.J., Suramin inhibits chikungunya virus replication through multiple mechanisms. Antivir. Res. 121 (2015), 39–46.
2. Amaro, C.A., Gonzalez-Cortazar, M., Herrera-Ruiz, M., Roman-Ramos, R., Aguilar-Santamaria, L., Tortoriello, J., Jimenez-Ferrer, E., Hypoglycemic and hypotensive activity of a root extract of Smilax aristolochiifolia, standardized on N-trans-feruloyl-tyramine. Molecules 19 (2014), 11366–11384.
3. Ashbrook, A.W., Burrack, K.S., Silva, L.A., Montgomery, S.A., Heise, M.T., Morrison, T.E., Dermody, T.S., Residue 82 of the chikungunya virus E2 attachment protein modulates viral dissemination and arthritis in mice. J. Virol. 88 (2014), 12180–12192.
4. Bouquillard, E., Combe, B., A report of 21 cases of rheumatoid arthritis following chikungunya fever. A mean follow-up of two years. Jt. Bone Spine Rev. Rhum. 76 (2009), 654–657.
5. Brighton, S.W., Prozesky, O.W., de la Harpe, A.L., Chikungunya virus infection. A retrospective study of 107 cases. South Afr. Med. J. Suid Afrik. tydskr. vir geneeskd. 63 (1983), 313–315.
6. Chaaithanya, I.K., Muruganandam, N., Raghuraj, U., Sugunan, A.P., Rajesh, R., Anwesh, M., Rai, S.K., Vijayachari, P., Chronic inflammatory arthritis with persisting bony erosions in patients following chikungunya infection. Indian J. Med. Res. 140 (2014), 142–145.
7. Chen, W., Foo, S.S., Taylor, A., Lulla, A., Merits, A., Hueston, L., Forwood, M.R., Walsh, N.C., Sims, N.A., Herrero, L.J., Mahalingam, S., Bindarit, an inhibitor of monocyte chemotactic protein synthesis, protects against bone loss induced by chikungunya virus infection. J. Virol. 89 (2015), 581–593.
8. Chopra, A., Anuradha, V., Lagoo-Joshi, V., Kunjir, V., Salvi, S., Saluja, M., Chikungunya virus aches and pains: an emerging challenge. Arthritis Rheum. 58 (2008), 2921–2922.
9. Couderc, T., Chretien, F., Schilte, C., Disson, O., Brigitte, M., Guivel-Benhassine, F., Touret, Y., Barau, G., Cayet, N., Schuffenecker, I., Despres, P., Arenzana-Seisdedos, F., Michault, A., Albert, M.L., Lecuit, M., A mouse model for chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog., 4, 2008, e29.
10. Delang, L., Segura Guerrero, N., Tas, A., Querat, G., Pastorino, B., Froeyen, M., Dallmeier, K., Jochmans, D., Herdewijn, P., Bello, F., Snijder, E.J., de Lamballerie, X., Martina, B., Neyts, J., van Hemert, M.J., Leyssen, P., Mutations in the chikungunya virus non-structural proteins cause resistance to favipiravir (T-705), a broad-spectrum antiviral. J. Antimicrob. Chemother. 69 (2014), 2770–2784.
11. Fox, J.M., Long, F., Edeling, M.A., Lin, H., van Duijl-Richter, M.K., Fong, R.H., Kahle, K.M., Smit, J.M., Jin, J., Simmons, G., Doranz, B.J., Crowe, J.E. Jr. Fremont, D.H., Rossmann, M.G., Diamond, M.S., Broadly neutralizing alphavirus antibodies bind an epitope on E2 and inhibit entry and egress. Cell 163 (2015), 1095–1107.
12. Garcia-Arriaza, J., Cepeda, V., Hallengard, D., Sorzano, C.O., Kummerer, B.M., Liljestrom, P., Esteban, M., A novel poxvirus-based vaccine, MVA-CHIKV, is highly immunogenic and protects mice against chikungunya infection. J. Virol. 88 (2014), 3527–3547.
13. Gardner, J., Anraku, I., Le, T.T., Larcher, T., Major, L., Roques, P., Schroder, W.A., Higgs, S., Suhrbier, A., Chikungunya virus arthritis in adult wild-type mice. J. Virol. 84 (2010), 8021–8032.
14. Hallengard, D., Kakoulidou, M., Lulla, A., Kummerer, B.M., Johansson, D.X., Mutso, M., Lulla, V., Fazakerley, J.K., Roques, P., Le Grand, R., Merits, A., Liljestrom, P., Novel attenuated chikungunya vaccine candidates elicit protective immunity in C57BL/6 mice. J. Virol. 88 (2014), 2858–2866.
15. Herrero, L.J., Foo, S.S., Sheng, K.C., Chen, W., Forwood, M.R., Bucala, R., Mahalingam, S., Pentosan polysulfate: a novel glycosaminoglycan-like molecule for effective treatment of alphavirus-induced cartilage destruction and inflammatory disease. J. Virol. 89 (2015), 8063–8076.
16. Ho, Y.J., Wang, Y.M., Lu, J.W., Wu, T.Y., Lin, L.I., Kuo, S.C., Lin, C.C., Suramin inhibits chikungunya virus entry and transmission. PloS One, 10, 2015, e0133511.
17. Jaffar-Bandjee, M.C., Ramful, D., Gauzere, B.A., Hoarau, J.J., Krejbich-Trotot, P., Robin, S., Ribera, A., Selambarom, J., Gasque, P., Emergence and clinical insights into the pathology of chikungunya virus infection. Expert Rev. Anti Infect. Ther. 8 (2010), 987–996.
18. Javelle, E., Ribera, A., Degasne, I., Gauzere, B.A., Marimoutou, C., Simon, F., Specific management of post-chikungunya rheumatic disorders: a retrospective study of 159 cases in Reunion Island from 2006-2012. PLoS Negl. Trop. Dis., 9, 2015, e0003603.
19. Jin, J., Liss, N.M., Chen, D.H., Liao, M., Fox, J.M., Shimak, R.M., Fong, R.H., Chafets, D., Bakkour, S., Keating, S., Fomin, M.E., Muench, M.O., Sherman, M.B., Doranz, B.J., Diamond, M.S., Simmons, G., Neutralizing monoclonal antibodies block chikungunya virus entry and release by targeting an epitope critical to viral pathogenesis. Cell Rep. 13 (2015), 2553–2564.
20. Kuo, S.C., Chen, Y.J., Wang, Y.M., Kuo, M.D., Jinn, T.R., Chen, W.S., Chang, Y.C., Tung, K.L., Wu, T.Y., Lo, S.J., Cell-based analysis of chikungunya virus membrane fusion using baculovirus-expression vectors. J. Virol. Methods 175 (2011), 206–215.
21. Lam, S., Chen, H., Chen, C.K., Min, N., Chu, J.J., Antiviral phosphorodiamidate morpholino oligomers are protective against chikungunya virus infection on cell-based and murine models. Sci. Rep., 5, 2015, 12727.
22. Liu, K., Vergani, A., Zhao, P., Ben Nasr, M., Wu, X., Iken, K., Jiang, D., Su, X., Fotino, C., Fiorina, P., Visner, G.A., Inhibition of the purinergic pathway prolongs mouse lung allograft survival. Am. J. Respir. Cell Mol. Biol. 51 (2014), 300–310.
23. Mancini, F., Toro, C.M., Mabilia, M., Giannangeli, M., Pinza, M., Milanese, C., Inhibition of tumor necrosis factor-alpha (TNF-alpha)/TNF-alpha receptor binding by structural analogues of suramin. Biochem. Pharmacol. 58 (1999), 851–859.
24. Manimunda, S.P., Vijayachari, P., Uppoor, R., Sugunan, A.P., Singh, S.S., Rai, S.K., Sudeep, A.B., Muruganandam, N., Chaitanya, I.K., Guruprasad, D.R., Clinical progression of chikungunya fever during acute and chronic arthritic stages and the changes in joint morphology as revealed by imaging. Trans. R. Soc. Trop. Med. Hyg. 104 (2010), 392–399.
25. Margolles-Clark, E., Jacques-Silva, M.C., Ganesan, L., Umland, O., Kenyon, N.S., Ricordi, C., Berggren, P.O., Buchwald, P., Suramin inhibits the CD40–CD154 costimulatory interaction: a possible mechanism for immunosuppressive effects. Biochem. Pharmacol 77 (2009), 1236–1245.
26. McGeary, R.P., Bennett, A.J., Tran, Q.B., Cosgrove, K.L., Ross, B.P., Suramin: clinical uses and structure-activity relationships. Mini Rev. Med. Chem. 8 (2008), 1384–1394.
27. Miner, J.J., Aw Yeang, H.X., Fox, J.M., Taffner, S., Malkova, O.N., Oh, S.T., Kim, A.H., Diamond, M.S., Lenschow, D.J., Yokoyama, W.M., Chikungunya viral arthritis in the United States: a mimic of seronegative rheumatoid arthritis. Arthritis Rheumatol. 67 (2015), 1214–1220.
28. Mishra, P., Kumar, A., Mamidi, P., Kumar, S., Basantray, I., Saswat, T., Das, I., Nayak, T.K., Chattopadhyay, S., Subudhi, B.B., Chattopadhyay, S., Inhibition of chikungunya virus replication by 1-[(2-methylbenzimidazol-1-yl) methyl]-2-oxo-indolin-3-ylidene] amino] thiourea(MBZM-N-IBT). Sci. Rep., 6, 2016, 20122.
29. Morrison, T.E., Oko, L., Montgomery, S.A., Whitmore, A.C., Lotstein, A.R., Gunn, B.M., Elmore, S.A., Heise, M.T., A mouse model of chikungunya virus-induced musculoskeletal inflammatory disease: evidence of arthritis, tenosynovitis, myositis, and persistence. Am. J. Pathol. 178 (2011), 32–40.
30. Mylonas, A.D., Brown, A.M., Carthew, T.L., McGrath, B., Purdie, D.M., Pandeya, N., Vecchio, P.C., Collins, L.G., Gardner, I.D., de Looze, F.J., Reymond, E.J., Suhrbier, A., Natural history of Ross River virus-induced epidemic polyarthritis. Med. J. Aust. 177 (2002), 356–360.
31. Ozden, S., Huerre, M., Riviere, J.P., Coffey, L.L., Afonso, P.V., Mouly, V., de Monredon, J., Roger, J.C., El Amrani, M., Yvin, J.L., Jaffar, M.C., Frenkiel, M.P., Sourisseau, M., Schwartz, O., Butler-Browne, G., Despres, P., Gessain, A., Ceccaldi, P.E., Human muscle satellite cells as targets of chikungunya virus infection. PloS One, 2, 2007, e527.
32. Pal, P., Dowd, K.A., Brien, J.D., Edeling, M.A., Gorlatov, S., Johnson, S., Lee, I., Akahata, W., Nabel, G.J., Richter, M.K., Smit, J.M., Fremont, D.H., Pierson, T.C., Heise, M.T., Diamond, M.S., Development of a highly protective combination monoclonal antibody therapy against chikungunya virus. PLoS Pathog., 9, 2013, e1003312.
33. Piper, A., Ribeiro, M., Smith, K.M., Briggs, C.M., Huitt, E., Nanda, K., Spears, C.J., Quiles, M., Cullen, J., Thomas, M.E., Brown, D.T., Hernandez, R., Chikungunya virus host range E2 transmembrane deletion mutants induce protective immunity against challenge in C57BL/6J mice. J. Virol. 87 (2013), 6748–6757.
34. Poo, Y.S., Nakaya, H., Gardner, J., Larcher, T., Schroder, W.A., Le, T.T., Major, L.D., Suhrbier, A., CCR2 deficiency promotes exacerbated chronic erosive neutrophil-dominated chikungunya virus arthritis. J. Virol. 88 (2014), 6862–6872.
35. Poo, Y.S., Rudd, P.A., Gardner, J., Wilson, J.A., Larcher, T., Colle, M.A., Le, T.T., Nakaya, H.I., Warrilow, D., Allcock, R., Bielefeldt-Ohmann, H., Schroder, W.A., Khromykh, A.A., Lopez, J.A., Suhrbier, A., Multiple immune factors are involved in controlling acute and chronic chikungunya virus infection. PLoS Negl. Trop. Dis., 8, 2014, e3354.
36. Ren, P., Zou, G., Bailly, B., Xu, S., Zeng, M., Chen, X., Shen, L., Zhang, Y., Guillon, P., Arenzana-Seisdedos, F., Buchy, P., Li, J., von Itzstein, M., Li, Q., Altmeyer, R., The approved pediatric drug suramin identified as a clinical candidate for the treatment of EV71 infection-suramin inhibits EV71 infection in vitro and in vivo. Emerg. Microbes Infect., 3, 2014, e62.
37. Rodriguez-Morales, A.J., Cardona-Ospina, J.A., Villamil-Gomez, W., Paniz-Mondolfi, A.E., How many patients with post-chikungunya chronic inflammatory rheumatism can we expect in the new endemic areas of Latin America?. Rheumatol. Int. 35 (2015), 2091–2094.
38. Romas, E., Sims, N.A., Hards, D.K., Lindsay, M., Quinn, J.W., Ryan, P.F., Dunstan, C.R., Martin, T.J., Gillespie, M.T., Osteoprotegerin reduces osteoclast numbers and prevents bone erosion in collagen-induced arthritis. Am. J. Pathol. 161 (2002), 1419–1427.
39. Rosario, V., Munoz-Louis, R., Valdez, T., Adames, S., Medrano, J., Paulino, I., Paula, J., Alba-Feriz, R., Chikungunya infection in the general population and in patients with rheumatoid arthritis on biological therapy. Clin. Rheumatol. 34 (2015), 1285–1287.
40. Rothan, H.A., Bahrani, H., Abdulrahman, A.Y., Mohamed, Z., Teoh, T.C., Othman, S., Rashid, N.N., Rahman, N.A., Yusof, R., Mefenamic acid in combination with ribavirin shows significant effects in reducing chikungunya virus infection in vitro and in vivo. Antivir. Res. 127 (2016), 50–56.
41. Rulli, N.E., Rolph, M.S., Srikiatkhachorn, A., Anantapreecha, S., Guglielmotti, A., Mahalingam, S., Protection from arthritis and myositis in a mouse model of acute chikungunya virus disease by bindarit, an inhibitor of monocyte chemotactic protein-1 synthesis. J. Infect. Dis. 204 (2011), 1026–1030.
42. Safadi, R.A., Musleh, A.S., Al-Khateeb, T.H., Hamasha, A.A., Analysis of immunohistochemical expression of k19 in oral epithelial dysplasia and oral squamous cell carcinoma using color deconvolution-image analysis method. Head Neck Pathol. 4 (2010), 282–289.
43. Sahu, D., Saroha, A., Roy, S., Das, S., Srivastava, P.S., Das, H.R., Suramin ameliorates collagen induced arthritis. Int. Immunopharmacol. 12 (2012), 288–293.
44. Schilte, C., Staikowsky, F., Couderc, T., Madec, Y., Carpentier, F., Kassab, S., Albert, M.L., Lecuit, M., Michault, A., Chikungunya virus-associated long-term arthralgia: a 36-month prospective longitudinal study. PLoS Negl. Trop. Dis., 7, 2013, e2137.
45. Schuffenecker, I., Iteman, I., Michault, A., Murri, S., Frangeul, L., Vaney, M.C., Lavenir, R., Pardigon, N., Reynes, J.M., Pettinelli, F., Biscornet, L., Diancourt, L., Michel, S., Duquerroy, S., Guigon, G., Frenkiel, M.P., Brehin, A.C., Cubito, N., Despres, P., Kunst, F., Rey, F.A., Zeller, H., Brisse, S., Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med., 3, 2006, e263.
46. Suhrbier, A., La Linn, M., Clinical and pathologic aspects of arthritis due to Ross River virus and other alphaviruses. Curr. Opin. Rheumatol. 16 (2004), 374–379.
47. Toivanen, A., Alphaviruses: an emerging cause of arthritis?. Curr. Opin. Rheumatol. 20 (2008), 486–490.
48. Tsetsarkin, K.A., Vanlandingham, D.L., McGee, C.E., Higgs, S., A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog., 3, 2007, e201.
49. Vazeille, M., Moutailler, S., Coudrier, D., Rousseaux, C., Khun, H., Huerre, M., Thiria, J., Dehecq, J.S., Fontenille, D., Schuffenecker, I., Despres, P., Failloux, A.B., Two chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PloS One, 2, 2007, e1168.
50. Wang, D., Suhrbier, A., Penn-Nicholson, A., Woraratanadharm, J., Gardner, J., Luo, M., Le, T.T., Anraku, I., Sakalian, M., Einfeld, D., Dong, J.Y., A complex adenovirus vaccine against chikungunya virus provides complete protection against viraemia and arthritis. Vaccine 29 (2011), 2803–2809.
51. Yoneda, T., Williams, P., Rhine, C., Boyce, B.F., Dunstan, C., Mundy, G.R., Suramin suppresses hypercalcemia and osteoclastic bone resorption in nude mice bearing a human squamous cancer. Cancer Res. 55 (1995), 1989–1993.
52. Zeana, C., Kelly, P., Heredia, W., Cifuentes, A., Franchin, G., Purswani, M., Tieng, A., Hagmann, S.H., Post-chikungunya rheumatic disorders in travelers after return from the Caribbean. Travel Med. Infect. Dis. 14 (2016), 21–25.