Broad-spectrum antiviral activity of chebulagic acid and punicalagin against viruses that use glycosaminoglycans for entry

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Lin, Liang Tzung ^a,b   Chen, Ting Ying ^c   Lin, Song Chow ^a   Chung, Chueh Yao ^c   Lin, Ta Chen ^d   Wang, Guey Horng ^e   Anderson, Robert ^b,f   Lin, Chun Ching ^c   Richardson, Christopher D ^b,f  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b IWK HEALTH CENTRE   (Canada)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d CENTRAL TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^e CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^f DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Broad spectrum antivirals; Chebulagic acid; Glycosaminoglycans; Punicalagin; Tannin; Viral entry

Indexed keywords

ANTIVIRUS AGENT; CHEBULAGIC ACID; GLYCOSAMINOGLYCAN; PUNICALAGIN; TANNIN DERIVATIVE; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENGUE VIRUS; DRUG EFFICACY; DRUG SCREENING; HEPATITIS C VIRUS; HUMAN CYTOMEGALOVIRUS; INFECTION; MEASLES VIRUS; NONHUMAN; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INHIBITION;

ANIMALS; ANTIVIRAL AGENTS; BENZOPYRANS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSIDES; GLYCOSAMINOGLYCANS; HUMANS; HYDROLYZABLE TANNINS; RECEPTORS, VIRUS; VIRUS DISEASES; VIRUS INTERNALIZATION; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

DENGUE VIRUS; HEPATITIS C VIRUS; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 5; MEASLES VIRUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 84881035529     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-187     Document Type: Article

References (72)

1. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Rothman AL, Nat Rev Immunol 2011 11 8 532 543 10.1038/nri3014 21760609
2. Progress in the development of preventive and therapeutic vaccines for hepatitis C virus. Torresi J, Johnson D, Wedemeyer H, J Hepatol 2011 54 6 1273 1285 10.1016/j.jhep.2010.09.040 21236312
3. Update on the current status of cytomegalovirus vaccines. Sung H, Schleiss MR, Expert Rev Vaccines 2010 9 11 1303 1314 10.1586/erv.10.125 21087108
4. Respiratory syncytial virus prevention and therapy: past, present, and future. Wright M, Piedimonte G, Pediatr Pulmonol 2011 46 4 324 347 10.1002/ppul.21377 21438168
5. HIV vaccines: progress to date. Munier CM, Andersen CR, Kelleher AD, Drugs 2011 71 4 387 414 21395355
6. Zoonotic viral diseases and the frontier of early diagnosis, control and prevention. Heeney JL, J Intern Med 2006 260 5 399 408 10.1111/j.1365-2796.2006. 01711.x 17040245 (Pubitemid 44571127)
7. The global burden of bacterial and viral zoonotic infections. Christou L, Clin Microbiol Infect 2011 17 3 326 330 10.1111/j.1469-0691.2010.03441.x 21129102
8. The socio-ecology of zoonotic infections. Cascio A, Bosilkovski M, Rodriguez-Morales AJ, Pappas G, Clin Microbiol Infect 2011 17 3 336 342 10.1111/j.1469-0691.2010.03451.x 21175957
9. Measles vaccination in humanitarian emergencies: a review of recent practice. Grais RF, Strebel P, Mala P, Watson J, Nandy R, Gayer M, Confl Health 2011 5 1 21 10.1186/1752-1505-5-21 21942984
10. Oral and perioral herpes simplex virus type 1 (HSV-1) infection: review of its management. Arduino PG, Porter SR, Oral diseases 2006 12 3 254 270 10.1111/j.1601-0825.2006.01202.x 16700734 (Pubitemid 43736414)
11. Directly acting antivirals against hepatitis C virus. Soriano V, Vispo E, Poveda E, Labarga P, Martin-Carbonero L, Fernandez-Montero JV, Barreiro P, J Antimicrob Chemother 2011 66 8 1673 1686 10.1093/jac/dkr215 21652618
12. Advances in the structure-based design of the influenza A neuraminidase inhibitors. Mitrasinovic PM, Curr Drug Targets 2010 11 3 315 326 10.2174/138945010790711932 20210756
13. Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Pawlotsky JM, Hepatology 2011 53 5 1742 1751 10.1002/hep.24262 21374691
14. Recent advances in antiretroviral drugs. Ghosh RK, Ghosh SM, Chawla S, Expert Opin Pharmacother 2011 12 1 31 46 10.1517/14656566.2010.509345 20698725
15. Interferons as therapeutic agents for infectious diseases. Bergman SJ, Ferguson MC, Santanello C, Infect Dis Clin North Am 2011 25 4 819 834 10.1016/j.idc.2011.07.008 22054758
16. Human interferons alpha, beta and omega. Bekisz J, Schmeisser H, Hernandez J, Goldman ND, Zoon KC, Growth Factors 2004 22 4 243 251 10.1080/08977190400000833 15621727 (Pubitemid 40123402)
17. Management of adverse effects of Peg-IFN and ribavirin therapy for hepatitis C. Sulkowski MS, Cooper C, Hunyady B, Jia J, Ogurtsov P, Peck-Radosavljevic M, Shiffman ML, Yurdaydin C, Dalgard O, Nat Rev Gastroenterol Hepatol 2011 8 4 212 223 10.1038/nrgastro.2011.21 21386812
18. The structure of glycosaminoglycans and their interactions with proteins. Gandhi NS, Mancera RL, Chem Biol Drug Des 2008 72 6 455 482 10.1111/j.1747-0285.2008.00741.x 19090915
19. Heparan sulphate proteoglycans fine-tune mammalian physiology. Bishop JR, Schuksz M, Esko JD, Nature 2007 446 7139 1030 1037 10.1038/nature05817 17460664 (Pubitemid 46676065)
20. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW, Zarski JP, Drouet E, J Med Virol 2002 68 2 206 215 10.1002/jmv.10196 12210409
21. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, Kinoshita-Toyoda A, Toida T, Van Kuppevelt TH, Depla E, et al. J Biol Chem 2003 278 42 41003 41012 10.1074/jbc.M302267200 12867431 (Pubitemid 37280923)
22. Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. Banfield BW, Leduc Y, Esford L, Schubert K, Tufaro F, J Virol 1995 69 6 3290 3298 7745676
23. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. Shieh MT, WuDunn D, Montgomery RI, Esko JD, Spear PG, J Cell Biol 1992 116 5 1273 1281 10.1083/jcb.116.5.1273 1310996
24. The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. Feldman SA, Audet S, Beeler JA, J Virol 2000 74 14 6442 6447 10.1128/JVI.74.14.6442-6447.2000 10864656 (Pubitemid 30429811)
25. Heparin-like glycosaminoglycans prevent the infection of measles virus in SLAM-negative cell lines. Terao-Muto Y, Yoneda M, Seki T, Watanabe A, Tsukiyama-Kohara K, Fujita K, Kai C, Antiviral Res 2008 80 3 370 376 10.1016/j.antiviral.2008.08.006 18812191
26. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Compton T, Nowlin DM, Cooper NR, Virology 1993 193 2 834 841 10.1006/viro.1993.1192 8384757
27. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hilgard P, Stockert R, Hepatology 2000 32 5 1069 1077 10.1053/jhep.2000.18713 11050058
28. Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. Barth H, Schnober EK, Zhang F, Linhardt RJ, Depla E, Boson B, Cosset FL, Patel AH, Blum HE, Baumert TF, J Virol 2006 80 21 10579 10590 10.1128/JVI.00941-06 16928753 (Pubitemid 44628904)
29. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, Pietschmann T, Bartenschlager R, J Virol 2006 80 11 5308 5320 10.1128/JVI.02460-05 16699011
30. Envelope-dependent, cyclophilin-independent effects of glycosaminoglycans on human immunodeficiency virus type 1 attachment and infection. Zhang YJ, Hatziioannou T, Zang T, Braaten D, Luban J, Goff SP, Bieniasz PD, J Virol 2002 76 12 6332 6343 10.1128/JVI.76.12.6332-6343.2002 12021366 (Pubitemid 34556328)
31. Contribution of the respiratory syncytial virus G glycoprotein and its secreted and membrane-bound forms to virus replication in vitro and in vivo. Teng MN, Whitehead SS, Collins PL, Virology 2001 289 2 283 296 10.1006/viro.2001.1138 11689051 (Pubitemid 33141008)
32. Identification of linear heparin-binding peptides derived from human respiratory syncytial virus fusion glycoprotein that inhibit infectivity. Crim RL, Audet SA, Feldman SA, Mostowski HS, Beeler JA, J Virol 2007 81 1 261 271 10.1128/JVI.01226-06 17050595 (Pubitemid 44975166)
33. Hydrolyzable tannins (chebulagic acid and punicalagin) target viral glycoprotein-glycosaminoglycan interactions to inhibit herpes simplex virus 1 entry and cell-to-cell spread. Lin LT, Chen TY, Chung CY, Noyce RS, Grindley TB, McCormick C, Lin TC, Wang GH, Lin CC, Richardson CD, J Virol 2011 85 9 4386 4398 10.1128/JVI.01492-10 21307190
34. Important advances in the field of anti-dengue virus research. Julander JG, Perry ST, Shresta S, Antivir Chem Chemother 2011 21 3 105 116 21233532
35. The search for new therapies for human cytomegalovirus infections. Prichard MN, Kern ER, Virus Res 2011 157 2 212 221 10.1016/j.virusres.2010.11. 004 21095209
36. Measles control-can measles virus inhibitors make a difference? Plemper RK, Snyder JP, Curr Opin Investig Drugs 2009 10 8 811 820 19649926
37. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. Ono N, Tatsuo H, Hidaka Y, Aoki T, Minagawa H, Yanagi Y, J Virol 2001 75 9 4399 4401 10.1128/JVI.75.9.4399-4401.2001 11287589 (Pubitemid 32410152)
38. Welstead GG, 'The interaction between measles virus and its receptor SLAM'. Dissertation: University of Toronto 2006
39. Human cytomegalovirus glycoprotein B is required for virus entry and cell-to-cell spread but not for virion attachment, assembly, or egress. Isaacson MK, Compton T, J Virol 2009 83 8 3891 3903 10.1128/JVI.01251-08 19193805
40. Modified apoptotic molecule (BID) reduces hepatitis C virus infection in mice with chimeric human livers. Hsu EC, Hsi B, Hirota-Tsuchihara M, Ruland J, Iorio C, Sarangi F, Diao J, Migliaccio G, Tyrrell DL, Kneteman N, et al. Nat Biotechnol 2003 21 5 519 525 10.1038/nbt817 12704395 (Pubitemid 36532016)
41. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Marukian S, Jones CT, Andrus L, Evans MJ, Ritola KD, Charles ED, Rice CM, Dustin LB, Hepatology 2008 48 6 1843 1850 10.1002/hep.22550 19003912
42. Dramatic caspase-dependent apoptosis in antibody-enhanced dengue virus infection of human mast cells. Brown MG, Huang YY, Marshall JS, King CA, Hoskin DW, Anderson R, J Leukoc Biol 2009 85 1 71 80 18809735
43. Murine host responses to respiratory syncytial virus (RSV) following intranasal administration of a Protollin-adjuvanted, epitope-enhanced recombinant G protein vaccine. Huang Y, Cyr SL, Burt DS, Anderson R, J Clin Virol 2009 44 4 287 291 10.1016/j.jcv.2009.01.009 19233722
44. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, Braun W, McCray PB Jr, McChesney MB, Cattaneo R, J Clin Invest 2008 118 7 2448 2458 18568079 (Pubitemid 351949773)
45. Sulfated derivatives of Escherichia coli K5 capsular polysaccharide are potent inhibitors of human cytomegalovirus. Mercorelli B, Oreste P, Sinigalia E, Muratore G, Lembo D, Palu G, Loregian A, Antimicrob Agents Chemother 2010 54 11 4561 4567 10.1128/AAC.00721-10 20713657
46. Specific inhibition of paramyxovirus and myxovirus replication by oligopeptides with amino acid sequences similar to those at the N-termini of the F1 or HA2 viral polypeptides. Richardson CD, Scheid A, Choppin PW, Virology 1980 105 1 205 222 10.1016/0042-6822(80)90168-3 7414950 (Pubitemid 10049375)
47. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Sainz B Jr, Barretto N, Martin DN, Hiraga N, Imamura M, Hussain S, Marsh KA, Yu X, Chayama K, Alrefai WA, et al. Nat Med 2012 18 2 281 285 10.1038/nm.2581 22231557
48. Complete replication of hepatitis C virus in cell culture. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, et al. Science 2005 309 5734 623 626 10.1126/science.1114016 15947137 (Pubitemid 41033648)
49. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Russell RS, Meunier JC, Takikawa S, Faulk K, Engle RE, Bukh J, Purcell RH, Emerson SU, Proc Natl Acad Sci USA 2008 105 11 4370 4375 10.1073/pnas.0800422105 18334634 (Pubitemid 351754387)
50. Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus. Baba M, Snoeck R, Pauwels R, de Clercq E, Antimicrob Agents Chemother 1988 32 11 1742 1745 10.1128/AAC.32.11.1742 2472775 (Pubitemid 18267628)
51. Role of the putative heparan sulfate glycosaminoglycan-binding site of the adenovirus type 5 fiber shaft on liver detargeting and knob-mediated retargeting. Bayo-Puxan N, Cascallo M, Gros A, Huch M, Fillat C, Alemany R, J Gen Virol 2006 87 Pt 9 2487 2495 16894186
52. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Dechecchi MC, Tamanini A, Bonizzato A, Cabrini G, Virology 2000 268 2 382 390 10.1006/viro.1999.0171 10704346 (Pubitemid 30159987)
53. Molecular umbrellas: a novel class of candidate topical microbicides to prevent human immunodeficiency virus and herpes simplex virus infections. Madan RP, Mesquita PM, Cheshenko N, Jing B, Shende V, Guzman E, Heald T, Keller MJ, Regen SL, Shattock RJ, et al. J Virol 2007 81 14 7636 7646 10.1128/JVI.02851-06 17494078 (Pubitemid 47047849)
54. Vaccines: correlates of vaccine-induced immunity. Plotkin SA, Clin Infect Dis 2008 47 3 401 409 10.1086/589862 18558875 (Pubitemid 352009364)
55. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, Fafi-Kremer S, Soulier E, Royer C, Thumann C, Mee CJ, et al. Gastroenterology 2010 139 3 953 964 964 e951-954 10.1053/j.gastro.2010.05.073 20685314
56. Drugs in development for influenza. Boltz DA, Aldridge JR Jr, Webster RG, Govorkova EA, Drugs 2010 70 11 1349 1362 10.2165/11537960-000000000-00000 20614944
57. A broad-spectrum antiviral targeting entry of enveloped viruses. Wolf MC, Freiberg AN, Zhang T, Akyol-Ataman Z, Grock A, Hong PW, Li J, Watson NF, Fang AQ, Aguilar HC, et al. Proc Natl Acad Sci USA 2010 107 7 3157 3162 10.1073/pnas.0909587107 20133606
58. Rigid amphipathic fusion inhibitors, small molecule antiviral compounds against enveloped viruses. St Vincent MR, Colpitts CC, Ustinov AV, Muqadas M, Joyce MA, Barsby NL, Epand RF, Epand RM, Khramyshev SA, Valueva OA, et al. Proc Natl Acad Sci USA 2010 107 40 17339 17344 10.1073/pnas.1010026107 20823220
59. Squalamine as a broad-spectrum systemic antiviral agent with therapeutic potential. Zasloff M, Adams AP, Beckerman B, Campbell A, Han Z, Luijten E, Meza I, Julander J, Mishra A, Qu W, et al. Proc Natl Acad Sci USA 2011 108 38 15978 15983 10.1073/pnas.1108558108 21930925
60. Viral entry mechanisms: the increasing diversity of paramyxovirus entry. Smith EC, Popa A, Chang A, Masante C, Dutch RE, Febs J 2009 276 24 7217 7227 10.1111/j.1742-4658.2009.07401.x 19878307
61. Structural basis of viral invasion: lessons from paramyxovirus F. Lamb RA, Jardetzky TS, Curr Opin Struct Biol 2007 17 4 427 436 10.1016/j.sbi.2007.08. 016 17870467 (Pubitemid 47451774)
62. Molecular mechanisms involved in the early steps of flavivirus cell entry. Kaufmann B, Rossmann MG, Microbes Infect 2011 13 1 1 9 10.1016/j.micinf.2010.09.005 20869460
63. Virus entry and innate immune activation. Isaacson MK, Juckem LK, Compton T, Curr Top Microbiol Immunol 2008 325 85 100 10.1007/978-3-540-77349-8-5 18637501
64. Hepatitis C virus entry into hepatocytes: molecular mechanisms and targets for antiviral therapies. Zeisel MB, Fofana I, Fafi-Kremer S, Baumert TF, J Hepatol 2011 54 3 566 576 10.1016/j.jhep.2010.10.014 21146244
65. Vaccines: past, present and future. Plotkin SA, Nat Med 2005 11 4 Suppl 5 11 15812490
66. Heparin induced thrombocytopenia: diagnosis and management. Alaraj A, Wallace A, Tesoro E, Ruland S, Amin-Hanjani S, Charbel FT, Aletich V, J Neurointerv Surg 2010 2 4 371 378 10.1136/jnis.2010.002840 21990651
67. Repeated oral administration of high doses of the pomegranate ellagitannin punicalagin to rats for 37 days is not toxic. Cerda B, Ceron JJ, Tomas-Barberan FA, Espin JC, J Agric Food Chem 2003 51 11 3493 3501 10.1021/jf020842c 12744688
68. Anti-hyperglycemic effect of chebulagic acid from the fruits of terminalia chebula retz. Huang YN, Zhao DD, Gao B, Zhong K, Zhu RX, Zhang Y, Xie WJ, Jia LR, Gao H, Int J Mol Sci 2012 13 5 6320 6333 22754367
69. Structural features and biological properties of ellagitannins in some plant families of the order myrtales. Yoshida T, Amakura Y, Yoshimura M, Int J Mol Sci 2010 11 1 79 106 10.3390/ijms11010079 20162003
70. Tannins and related compounds from combretaceae plants. Lin TC, Chien SC, Chen HF, Hsu FL, Chin Pharm J 2000 52 1 1 26 10.1211/0022357001773616
71. Tannins and related compounds. CII. Structures of terchebulin, an ellagitannin having a novel tetraphenylcarboxylic acid (terchebulic acid) moiety, and biogenetically related tannins from Terminalia chebula Retz. Lin TC, Nonaka G, Nishioka I, Ho FC, Chem Pharm Bull 1990 38 3004 3008 10.1248/cpb.38.3004
72. Synthesis of ellagitannin natural products. Pouysegu L, Deffieux D, Malik G, Natangelo A, Quideau S, Nat Prod Rep 2011 28 5 853 874 10.1039/c0np00058b 21321753