Inhibition of rotavirus infection in cultured cells by N-acetyl-cysteine, PPARγ agonists and NSAIDs

Antiviral Research

Volumn 96, Issue 1, 2012, Pages 1-12

  Guererero, Carlos A ^a   Murillo, Andrea ^a   Acosta, Orlando ^a  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

N Acetylcysteine; NSAIDs; Redox reactions; Rotavirus infection; Thiazolidinediones

Indexed keywords

ACETYLCYSTEINE; ASCORBIC ACID; DISULFIDE; IBUPROFEN; INDOMETACIN; KETOPROFEN; MEFENAMIC ACID; NONSTEROID ANTIINFLAMMATORY AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PIOGLITAZONE; ROSIGLITAZONE; ROTAVIRUS VACCINE; THIOL;

ANTIVIRAL ACTIVITY; ARTICLE; CELL CULTURE; CELL STRAIN CACO 2; CELL STRAIN MA104; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SCREENING; HUMAN; HUMAN CELL; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; ROTAVIRUS INFECTION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS SHEDDING; VIRUS STRAIN;

ACETYLCYSTEINE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE; DRUG EVALUATION, PRECLINICAL; HAPLORHINI; MICROBIAL SENSITIVITY TESTS; PPAR GAMMA; ROTAVIRUS; VIRUS REPLICATION;

ROTAVIRUS;

EID: 84864916737     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.06.011     Document Type: Article

References (86)

1. Ahola T., Fellman V., Laaksonen R., Laitila J., Lapatto R., Neuvonen P.J., Raivio K.O. Pharmacokinetics of intravenous N-acetylcysteine in pre-term new-born infants. Eur. J. Clin. Pharmacol. 1999, 55:645-650.
2. Anderson E. Rotavirus vaccines: viral shedding and risk of transmission. Lancet Infect. Dis. 2008, 8:642-649.
3. Arias C.F., Lizano M., López S. Synthesis in Escherichia coli and immunological characterisation of a polypeptide containing the cleavage sites associated with trypsin enhancement of rotavirus SA11 infectivity. J. Gen. Virol. 1987, 68:633-642.
4. Arranz L., Fernández C., Rodríguez A., Ribera J.M., De la Fuente M. The glutathione precursor N-acetylcysteine improves immune function in post-menopausal women. Free Radic. Biol. Med. 2008, 45:1252-1262.
5. Atkuri K.R., Mantovani J.J., Herzenberg L.A., Herzenberg L.A. N-Acetylcysteine - a safe antidote for cysteine/glutathione deficiency. Curr. Opin. Pharmacol. 2007, 7:355-359.
6. Auroma O.I., Halliwell B., Hoey B.M., Butler J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic. Biol. Med. 1989, 6:593-597.
7. Bagchi P., Dutta D., Chattopadhyay S., Mukherjee A., Halder U.C., Sarkar S., Kobayashi N., Komoto S., Taniguchi K., Chawla-Sarkar M. Rotavirus nonstructural protein 1 suppresses virus-Induced cellular apoptosis to facilitate viral growth by activating the cell survival pathways during early stages of infection. J. Virol. 2010, 84:6834-6845.
8. Bailey J.M., Erramouspe J. Nitazoxanide treatment for giardiasis and cryptosporidiosis in children. Ann. Pharmacother. 2004, 38:634-640.
9. Baker W.L., Anglade M.W., Baker E.L., White C.M., Kluger J., Coleman C.I. Use of N-acetylcysteine to reduce post-cardiothoracic surgery complications: a meta-analysis. Eur. J. Cardiothorac. Surg. 2009, 35:521-527.
10. Bartlett S.R., Sawdy R., Mann G. Induction of cyclooxygenase-2 expression in human myometrial smooth muscle cells by interleukin-1-beta: involvement of p38 mitogen-activated protein kinase. J. Physiol. 1999, 520:399-406.
11. Bassaganya-Riera J., Song R., Roberts P.C., Hontecillas R. PPAR-gamma activation as an anti-inflammatory therapy for respiratory virus infections. Viral Immunol. 2010, 23:343-352.
12. Benureau Y., Huet J.C., Charpilienne A., Poncet D., Cohen J. Trypsin is associated with the rotavirus capsid and is activated by solubilisation of outer capsid proteins. J. Gen. Virol. 2005, 86:3143-3151.
13. Brigelius-Flohe R., Banning A., Kny M., Bol G.F. Redox events in interleukin-1 signaling. Arch. Biochem. Biophys. 2004, 423:66-73.
14. Buffinton G.D., Christen S., Peterhans E., Stocker R. Oxidative stress in lungs of mice infected with influenza A virus. Free Radic. Res. Commun. 1992, 16:99-110.
15. Cai J., Chen Y., Seth S., Furukawa S., Compans R.W., Jones D.P. Inhibition of influenza infection by glutathione. Free Radic. Biol. Med. 2003, 34:928-936.
16. Calderon M.N., Guerrero C.A., Acosta O., Lopez S., Arias C.F. Inhibiting rotavirus infection by membrane-impermeant thiol/disulfide exchange blockers and antibodies against protein disulfide isomerase. Intervirology 2012, 10.1159/000335262.
17. Casola A., Garofalo R.P., Crawford S.E., Estes M.K., Mercurio F., Crowe S.E., Brasier A.R. Interleukin-8 gene regulation in intestinal epithelial cells infected with rotavirus: role of viral-induced IkB kinase activation. Virology 2002, 298:8-19.
18. Clark A., Sanderson C. Timing of children's vaccinations in 45 low-income and middle-income countries: an analysis of survey data. Lancet 2009, 373:1543-1549.
19. Clément S., Pascarella S., Negro F. Hepatitis C virus infection: molecular pathways to steatosis, insulin resistance and oxidative stress. Viruses 2009, 1:126-143.
20. Cotgreave I.A. N-Acetylcysteine: pharmacological considerations and experimental and clinical applications. Adv. Pharmacol. 1997, 38:205-227.
21. Danchin M.H., Bines J.E. Defeating rotavirus? The global recommendation for rotavirus vaccination. N. Engl. J. Med. 2009, 361:1919-1921.
22. De Flora S., Grassi C., Carati L. Attenuation of influenza-like symptomatology and improvement of cell-mediated immunity with long-term N-acetylcysteine treatment. Eur. Respir. J. 1997, 10:1535-1541.
23. Estes M., Kapikian A. Rotaviruses: Fields Virology 2007, 1917-1974. Kluwer Health/Lippincott, Williams and Wilkins, Philadelphia. fifth ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
24. Fujisawa K., Nishikawa T., Kukidome D., Imoto K., Yamashiro T., Motoshima H., Matsumura T., Araki E. TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis. Biochem. Biophys. Res. Commun. 2009, 379:43-48.
25. Gac M., Bigda J., Vahlenkamp T.W. Increased mitochondrial superoxide dismutase expression and lowered production of reactive oxygen species during rotavirus infection. Virology 2010, 404:293-303.
26. Garcia M.A., Gallego P., Campagna M., González-Santamaría J., Martínez G., et al. Activation of NF-kB pathway by virus infection requires Rb expression. PLoS One 2009, 4(7):e6422. 10.1371/journal.pone.0006422.
27. Garozzo A., Tempera G., Ungheri D., Timpanaro R., Castro A. N-Acetylcysteine synergises with oseltamivir in protecting mice from lethal influenza infection. Int. J. Immunopathol. Pharmacol. 2007, 20:349-354.
28. Ghezzi P., Ungheri D. Synergistic combination of N-acetylcysteine and ribavirin to protect from lethal influenza viral infection in a mouse model. Int. J. Immunopathol. Pharmacol. 2004, 17:99-102.
29. Graham K.L., Halasz P., Tan Y., Hewish M.J., Takada Y., Mackow E.R., Robinson M.K., Coulson B.S. Integrin-using rotaviruses bind alpha2beta1 integrin alpha2 I domain via VP4 DGE sequence and recognise alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. J. Virol. 2003, 77:9969-9978.
30. Gualtero D.F., Guzman F., Acosta O., Guerrero C.A. Amino acid domains 280-297 of VP6 and 531-554 of VP4 are implicated in heat shock cognate protein Hsc70-mediated rotavirus infection. Arch. Virol. 2007, 152:2183-2196.
31. Guerrero C.A., Bouyssounade D., Zarate S., Isa P., Lopez T., Espinosa R., Romero P., Méndez E., Lopez S., Arias C.F. Heat shock cognate protein 70 is involved in rotavirus cell entry. J. Virol. 2002, 76:4096-4102.
32. Guerrero C.A., Santana A.Y., Acosta O. Mouse intestinal villi as a model system for studies of rotavirus infection. J. Virol. Methods 2010, 168:22-30.
33. Guerrero, C.A., Acosta, O., 2012. N-acetyl-cysteine treatment of children with acute rotavirus infection. Case reports. In preparation.
34. Gupta S.C., Sundaram C., Reuter S., Aggarwal B.B. Inhibiting NF-κB activation by small molecules as a therapeutic strategy. Biochim. Biophys. Acta 2010, 1799:775-787.
35. Hamid R., Rotshteyn Y., Rabadi L., Parikh R., Bullock P. Comparison of alamar blue and MTT assays for high through-put screening. Toxicol. In Vitro 2004, 18:703-710.
36. Haselhorst T., Fleming F.E., Dyason J.C., Hartnell R.D., Yu X., Holloway G., Santegoets K., Kiefel M.J., Blanchard H., Coulson B.S., von Itzstein M. Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol. 2009, 5:91-93.
37. Hirasawa K., Kim A., Han H.-S., Han J., Jun H.-S., Yoon J.-W. Effect of p38 mitogen-activated protein kinase on the replication of encephalomyocarditis virus. J. Virol. 2003, 77:5649-5656.
38. Ho W.Z., Dougla S.D. Glutathione and N-acetylcysteine suppression of human immunodeficiency virus replication in human monocyte/macrophages in vitro. AIDS Res. Hum. Retroviruses 1992, 8:1249-1253.
39. Holloway G., Truong T.T., Barbara S., Coulson B.S. Rotavirus antagonises cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kB. J. Virol. 2009, 83:4942-4951.
40. Isa P., Gutiérrez M., Arias C.F., López S. Rotavirus cell entry. Future Virol. 2008, 3:135-146.
41. Israël N., Gougerot-Pocidalo M.A. Oxidative stress in human immunodeficiency virus infection. Cell. Mol. Life Sci. 1997, 53:864-870.
42. Jackson A.C., Kammouni W., Zherebitskaya E., Fernyhough P. Role of oxidative stress in rabies virus infection of adult mouse dorsal root ganglion neurons. J. Virol. 2010, 84:4697-4705.
43. Jiang C., Ting A.T., Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998, 391:82-86.
44. Jones P.L., Ping D., Boss J.M. Tumor necrosis factor alpha and interleukin-1 beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB. Mol. Cell. Biol. 1997, 17:6970-6981.
45. Josset L., Textoris J., Loriod B., Ferraris O., Moules V., Lina B., N'guyen C., Diaz J.J., Rosa-Calatrava M. Gene expression signature-based screening identifies new broadly effective influenza A antivirals. PLoS One 2010, 5(10):e13169. 10.1371/journal.pone.0013169.
46. Kavouras J.H., Prandovszky E., Valyi-Nagy K., Kovacs S.K., Tiwari V., Kovacs M., Shukla D., Valyi-Nagy T. Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures. J. Neurovirol. 2007, 13:416-425.
47. Lai K.Y., Ng W.Y., Osburga Chan P.K., Wong K.F., Cheng F. High-dose N-acetylcysteine therapy for novel H1N1 influenza pneumonia. Ann. Intern. Med. 2010, 152:687-688.
48. Lamb J. The connectivity map: a new tool for biomedical research. Nat. Rev. Cancer 2007, 7:54-60.
49. Lamb J., Crawford E.D., Peck D., Modell J.W., Blat I.C., Wrobel M.J., Lerner J., Brunet J.P., Subramanian A., Ross K.N., Reich M., Hieronymus H., Wei G., Armstrong S.A., Haggarty S.J., Clemons P.A., Wei R., Carr S.A., Lander E.S., Golub T.R. The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease. Science 2006, 313:1929-1935.
50. Lappas M., Permezel M., Rice G.E. N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-κB deoxyribonucleic acid-binding activity in human foetal membranes in vitro. J. Clin. Endocrinol. Metab. 2003, 88:1723-1729.
51. Lopez S., Arias C.F. Early steps in rotavirus cell entry. Curr. Top. Microbiol. Immunol. 2006, 309:39-66.
52. Marnett L.J., Kalgutkar A.S. Cyclooxygenase 2 inhibitors: discovery, selectivity and the future. Trends Pharmacol. Sci. 1999, 20:465-469.
53. Maruri-Avidal L., Lopez S., Arias C.F. Endoplasmic reticulum chaperones are involved in the morphogenesis of rotavirus infectious particles. J. Virol. 2008, 82:5368-5380.
54. Mirazimi A., Svensson L. Carbohydrates facilitate correct disulphide bond formation and folding of rotavirus VP7. J. Virol. 1998, 75:3887-3892.
55. Mosman T. Rapid colorimetric assay for cellular growth and survival: application of proliferation and cytotoxicity assay. J. Immunol. Methods 1983, 65:55-63.
56. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 1987, 326:711-713.
57. Nelson E.A., Glass R.I. Rotavirus: realising the potential of a promising vaccine. Lancet 2010, 376:568-570.
58. Nencioni L., Iuvara A., Aquilano K., Ciriolo M.R., Cozzolino F., Rotilio G., Garaci E., Palamara A.T. Influenza A virus replication is dependent on an antioxidant pathway that involves GSH and Bcl-2. FASEB J. 2003, 17:758-760.
59. Newton R., Kuitert L.M., Bergmann M., Adcock I.M., Barnes P.J. Evidence for involvement of NF-kappaB in the transcriptional control of COX-2 gene expression by IL-1beta. Biochem. Biophys. Res. Commun. 1997, 237:28-32.
60. Oberley-Deegan R.E., Rebits B.W., Weaver M.R., Tollefson A.K., Xiyuan B.A.I., McGibney M., Ovrutsky A.R., Chan E.D., Crapo J. An oxidative environment promotes growth of Mycobacterium abscessus. Free Radic. Biol. Med. 2010, 49:1666-1673.
61. Parashar U.D., Christopher J., Gibson C.J., Bresee J.S., Glass R.I. Rotavirus and severe childhood diarrhoea. Emerg. Infect. Dis. 2006, 12:304-306.
62. Parez N. Rotavirus gastroenteritis: why to back up the development of new vaccines?. Comp. Immunol. Microbiol. Infect. Dis. 2008, 31:253-269.
63. Peiris J., Hui K.P., Yen H.L. Host response to influenza virus: protection versus immunopathology. Curr. Opin. Immunol. 2010, 22:475-481.
64. Pleschka S., Wolff T., Ehrhardt C., Hobom G., Planz O., Rapp U.R., Ludwig S. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell. Biol. 2001, 3:301-305.
65. Raju P.A., Herzenberg L.A., Herzenberg L.A., Roederer M. Glutathione precursor and antioxidant activities of N-acetylcysteine and oxothiazolidine carboxylate compared in in vitro studies of HIV replication. AIDS Res. Hum. Retroviruses 1994, 10:961-967.
66. Ricote M., Glass C.K. PPARs and molecular mechanisms of transrepression. Biochim. Biophys. Acta 2007, 1771:926-935.
67. Rollo E.E., Kumar K.P., Reich N.C., Cohen J., Angel J., Greenberg H.B., Sheth R., Anderson J., Oh B., Hempson S.J., Mackow E.R., Shaw R.D. The epithelial cell response to rotavirus infection. J. Immunol. 1999, 163:4442-4452.
68. Rossen J.W., Bouma J., Raatgeep R.H., Buller H.A., Einerhand A.W. Inhibition of cyclooxygenase activity reduces rotavirus infection at a post-binding step. J. Virol. 2004, 78:9721-9730.
69. Rossignol J.F., Abu-Zekry M., Hussein A., Santoro M.G. Effect of nitazoxanide for treatment of severe rotavirus diarrhoea: randomised double-blind placebo-controlled trial. The Lancet 2006, 368:124-129.
70. Roulston A., Marcellus R.C., Branton P.E. Viruses and apoptosis. Annu. Rev. Microbiol. 1999, 53:577-628.
71. Santosham M. Rotavirus vaccine - a powerful tool to combat deaths from diarrhoea. N. Engl. J. Med. 2010, 362:358-360.
72. Schubert S.Y., Neeman I., Resnick N. A novel mechanism for the inhibition of NF-κB activation in vascular endothelial cells by natural antioxidants. FASEB J. 2002, 16:1931-1933.
73. Schwarz K.B. Oxidative stress during viral infection: a review. Free Radic. Biol. Med. 1996, 21:641-649.
74. Severi T., Ying C., Vermeesch J.R., Cassiman D., Cnops L., Verslype C., Fevery J., Arckens L., Neyts J., van Pelt J.F. Hepatitis B virus replication causes oxidative stress in HepAD38 liver cells. Mol. Cell. Biochem. 2006, 290:79-85.
75. Schafera F.Q., Buettner Garry R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30(11):1191-1212.
76. Sheth R., Anderson J., Sato T., Oh B., Hempson S.J., Rollo E., Mackow E.R., Shaw R.D. Rotavirus stimulates IL-8 secretion from cultured epithelial cells. Virology 1996, 221:251-259.
77. Smith W.L., DeWitt D.L., Garavito R.M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 2000, 69:145-182.
78. Stephensen C.B., Marquis G.S., Douglas S.D., Kruzich L.A., Wilson C.M. Glutathione, glutathione peroxidase, and selenium status in HIV-positive and HIV-negative adolescents and young adults. Am. J. Clin. Nutr. 2007, 85:173-181.
79. Straus D.S., Pascual G., Li M., Welch J.S., Ricote M., Hsiang C.-H., Sengchanthalangsy L.L., Ghosh G., Glass C.K. 15-Deoxy-D12,14-prostaglandin J2 inhibits multiple steps in the NF-kB signalling pathway. Proc. Natl. Acad. Sci. USA 2000, 97:4844-4849.
80. Subbaramaiah K., Hart J.C., Norton L., Dannenberg A.J. Microtubule-interfering agents stimulate the transcription of cyclooxygenase-2. Evidence for the involvement of ERK1/2 and p38 mitogen-activated protein kinase pathways. J. Biol. Chem. 2000, 275:14838-14845.
81. Subbaramaiah K., Lin D.T., Hart J.C., Dannenberg A.J. Peroxisome proliferator-activated receptor gamma ligands suppress the transcriptional activation of cyclooxygenase-2. Evidence for involvement of activator protein-1 and CREB-binding protein/p300. J. Biol. Chem. 2001, 276:12440-12448.
82. Svensson L., Dormitzer P.R., von Bonsdorff C.H., Maunula L., Greenberg H.B. Intracellular manipulation of disulphide bond formation in rotavirus proteins during assembly. J. Virol. 1994, 68:5204-5215.
83. Technau-Ihling K., Ihling C., Kromeier J., Brandner G. Influenza A virus infection of mice induces nuclear accumulation of the tumour suppressor protein p53 in the lung. Arch. Virol. 2001, 146:1655-1666.
84. Vandoros G.P., Konstantinopoulos P.A., Sotiropoulou-Bonikou G., Kominea A., Papachristou G.I., Karamouzis M.V., Gkermpesi M., Varakis I., Papavassiliou A.G. PPAR-gamma is expressed and NF-kB pathway is activated and correlates positively with COX-2 expression in stromal myofibroblasts surrounding colon adenocarcinomas. J. Cancer Res. Clin. Oncol. 2006, 132:76-84.
85. Zarate S., Cuadras M.A., Espinosa R., Romero P., Juarez K.O., Camacho-Nuez M., Arias C.F., Lopez S. Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J. Virol. 2003, 77:7254-7260.
86. Zarate S., Romero P., Espinosa R., Arias C.F., Lopez S. VP7 mediates the interaction of rotaviruses with integrin alphavbeta3 through a novel integrin-binding site. J. Virol. 2004, 78:10839-10847.