Theaflavin-3,3′-digallate and lactic acid combinations reduce herpes simplex virus infectivity

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 8, 2013, Pages 3806-3814

  Isaacs, Charles E ^a   Xu, Weimin ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; LACTIC ACID; THEAFLAVIN 3,3' DIGALLATE;

ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; NONHUMAN; PH; PRIORITY JOURNAL; SPERM; STORAGE TEMPERATURE; VAGINA DISCHARGE; VIRUS INACTIVATION; VIRUS LOAD;

ANIMALS; ANTIVIRAL AGENTS; BIFLAVONOIDS; CATECHIN; CERCOPITHECUS AETHIOPS; DRUG COMBINATIONS; DRUG EVALUATION, PRECLINICAL; FEMALE; HERPESVIRUS 1, HUMAN; HERPESVIRUS 2, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; LACTIC ACID; SEMEN ANALYSIS; VAGINA; VERO CELLS; VIRAL LOAD; VIRUS INACTIVATION;

EID: 84880305024     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00659-13     Document Type: Article

References (51)

1. Xu F, Sternberg MR, Kottiri BJ, McQuillan GM, Lee FK, Nahmias AJ, Berman SM, Markowitz LE. 2006. Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 296:964-973.
2. Ryder N, Jin F, McNulty AM, Grulich AE, Donovan B. 2009. Increasing role of herpes simplex virus type 1 in first-episode anogenital herpes in heterosexual women and younger men who have sex with men, 1992-2006. Sex. Transm. Infect. 85:416-419.
3. Mindel A. 1998. Genital herpes: how much of a public-health problem? Lancet 351:16-18.
4. Belshe RB, Leone PA, Bernstein DI, Wald A, Levin MJ, Stapleton JT, Gorfinkel I, Morrow RLA, Ewell MG, Stokes-Riner A, Dubin G, Heineman TC, Schulte JM, Deal CD. 2012. Efficacy results of a trial of a herpes simplex vaccine. N. Engl. J. Med. 366:34-43.
5. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ. 2006. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 20:73-83.
6. Celum C, Wald A, Lingappa JR, Magaret AS, Wang RS, Mugo N, Mujugira A, Baeten JM, Mullins JI, Hughes JP, Bukusi EA, Cohen CR, Katabira E, Ronald A, Kiarie J, Farquhar C, Stewart GJ, Makhema J, Essex M, Were E, Fife KH, de Bruyn G, Gray GE, McIntyre JA, Manongi R, Kapiga S, Coetzee D, Allen S, Inambao M, Kayitenkore K, Karita E, Kanweka W, Delany S, Rees H, Vwalika B, Stevens W, Campbell MS, Thomas KK, Coombs RW, Morrow R, Whittington WLH, McElrath MJ, Barnes L, Ridzon R, Corey L, for the partners in the Prevention HSV/HIV Transmission Study Team. 2010. Acyclovir and transmission of HIV-1 from persons infected with HIV-1 and HSV-2. N. Engl. J. Med. 362:427-439.
7. Naranbhai V, Karim SSA, Altfeld M, Samsunder N, Durgiah R, Sibeko S, Karim QA, Carr WH, and the CAPRISA004 TRAPS team. 2012. Innate immune activation enhances HIV acquisition in women, diminishing the effectiveness of tenofovir microbicide gel. J. Infect. Dis. 206: 993-1001.
8. Zhu J, Hladik F, Woodward A, Klock A, Peng T, Johnston C, Remington M, Magaret A, Koelle DM, Wald A, Corey L. 2009. Persistence of HIV-1 receptor-positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition. Nat. Med. 15:886-893.
9. Schiffer JT, Abu-Raddad L, Mark KE, Zhu J, Selke S, Magaret A, Wald A, Corey L. 2009. Frequent release of low amounts of herpes simplex virus from neurons: results of a mathematical model. Sci. Transl. Med. 1:7ral6.
10. Tata S, Johnston C, Huang ML, Selke S, Magaret A, Corey L, Wald A. 2010. Overlapping reactivations of herpes simplex virus type 2 in the genital and perianal mucosa. J. Infect. Dis. 201:499-504.
11. Phipps W, Saracino M, Magaret A, Selke S, Remington M, Huang ML, Warren T, Casper C, Corey L, Wald A. 2011. Persistent genital herpes simplex virus-2 shedding years following the first clinical episode. J. Infect. Dis. 203:180-187.
12. Johnston C, Saracino M, Kuntz S, Magaret A, Selke S, Huang ML, Schiffer JT, Koelle DM, Corey L, Wald A. 2012. Standard-dose and high-dose daily antiviral therapy for short episodes of genital HSV-2 reactivation: three randomized, open-label, crossover trials. Lancet 379: 641-647.
13. Isaacs CE, Xu W, Merz G, Hillier S, Rohan L, Wen GY. 2011. Digallate dimers of-epigallocatechin gallate inactivate herpes simplex virus. Antimicrob. Agents Chemother. 55:5646-5653.
14. De Clercq E. 2012. Where rilpivirine meets with tenofovir, the start of a new anti-HIV drug combination era. Biochem. Pharmacol. 84:241-248.
15. Swiss Association for the Study of the Liver. 2012. Review Article. Treatment of chronic hepatitis C genotype 1 with triple therapy comprising telaprevir or boceprevir. Swiss Med. Wkly. 142:1w13516.
16. Valore EV, Park CH, Igreti SL, Ganz T. 2002. Antimicrobial components of vaginal fluid. Am. J. Obstet. Gynecol. 187:561-568.
17. Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R, Hope TJ, Hanes J. 2009. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J. Virol. 83:11196-11200.
18. Witkin SS, Ledger WJ. 2012. Complexities of the uniquely human vagina. Sci. Transl. Med. 4:132fs11.
19. Isaacs CE, Wen GY, Xu W, Jia JH, Rohan L, Corbo C, Di Maggio V, Jenkins EC, Jr, Hillier S. 2008. Epigallocatechin gallate inactivates clinical isolates of herpes simplex virus. Antimicrob. Agents Chemother. 52:962-970.
20. Thormar H, Isaacs CE, Brown HR, Barshatzky MR, Pessolano T. 1987. Inactivation of enveloped viruses and killing of cells by fatty acids and monoglycerides. Antimicrob. Agents Chemother. 31:27-31.
21. Reed LJ, Muench M. 1938. A simple method of estimating 50 per cent end points. Am. J. Hyg. (Lond.) 27:493-497.
22. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ. 2011. Vaginal microbiome of reproductiveage women. Proc. Natl. Acad. Sci. U. S. A. 108:4680-4687.
23. Neurath AR, Strick N, Li YY. 2006. Role of seminal plasma in the anti-HIV-1 activity of candidate microbicides. BMC Infect. Dis. 6:1471-2334/6/1501-10.
24. Patel S, Hazrati E, Cheshenko N, Galen B, Yang H, Guzman E, Wang R, Herold BC, Keller MJ. 2007. Seminal plasma reduces the effectiveness of topical polyanionic microbicides. J. Infect. Dis. 196:1394-1402.
25. Herold BC, Mesquita PM, Madan RP, Keller MJ. 2011. Female genital tract secretions and semen impact the development of microbicides for the prevention of HIV and other sexually transmitted infections. Am. J. Reprod. Immunol. 65:325-333.
26. Alakomi H-L, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM. 2000. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 66:2001-2005.
27. Mossop H, Linhares IM, Bongiovanni AM, Ledger WJ, Witkin SS. 2011. Influence of lactic acid on endogenous and viral RNA-induced immune mediator production by vaginal epithelial cells. Obstet. Gynecol. 118:840-846.
28. Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UME, Zhong X, Koenig SSK, Fu L, Ma Z, Zhou X, Abdo Z, Forney LJ, Ravel J. 2012. Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med. 4:132ra52.
29. Lieleg O, Lieleg C, Bloom J, Buck CB, Ribbeck K. 2012. Mucin biopolymers as broad-spectrum antiviral agents. Biomacromolecules 13:1724-1732.
30. Liu S, Lu H, Zhao Q, He Y, Niu J, Debnath AK, Wu S, Jiang S. 2005. Theaflavin derivatives in black tea and catechin derivatives in green tea inhibit HIV-1 entry by targeting gp41. Biochim. Biophys. Acta 1723:270-281.
31. Ciesek S, von Hahn T, Colpitts CC, Schang LM, Friesland M, Steinmann J, Manns MP, Ott M, Wedemeyer H, Meuleman P, Pietschmann T, Steinmann E. 2011. The green tea polyphenol, epigallocatechin-3-gallate, inhibits hepatitis C virus entry. Hepatology 504:1947-1955.
32. Calland N, Albecka A, Belouzard S, Wychowski C, Duverlie G, Descamps V, Hober D, Dubuisson J, Rouillé Y, Séron K. 2012.-Epigallocatechin- 3-gallate is a new inhibitor of hepatitis C virus entry. Hepatology 55:720-729.
33. Kajiya K, Kumazawa S, Naito A, Nakayama T. 2008. Solid-state NMR analysis of the orientation and dynamics of epigallocatechin gallate, a green tea polyphenol, incorporated into lipid bilayers. Magn. Reson. Chem. 26:174-177.
34. Sirk TW, Friedman M, Brown EF. 2011. Molecular binding of black tea theaflavins to biological membranes: relationship to bioactivities. J. Agric. Food Chem. 59:3780-3787.
35. Eisenberg RJ, Atanasiu D, Cairns TM, Gallagher JR, Krummenacher C, Cohen GH. 2012. Herpesvirus fusion and entry: a story with many characters. Viruses 4:800-832.
36. Friedman M, Henika PR, Levin CE, Mandrell RE, Kozukue N. 2006. Antimicrobial activities of tea catechins and theaflavins and tea extracts against Bacillus cereus. J. Food Prot. 69:354-361.
37. Yang J, Li L, Jin H, Tan S, Qiu J, Yang L, Ding Y, Jiang ZH, Jiang S, Liu S. 2012. Vaginal gel formulation based on theaflavin derivatives as a microbicide to prevent HIV sexual transmission. Aids Res. Hum. Retrovir. 11:1498-1508.
38. Mulder TPJ, van Platerink CJ, Schuyl PJW, van Amelsvoort JMM. 2001. Analysis of theaflavins in biological fluids using liquid chromatographyelectrospray mass spectrometry. J. Chromatogr. 760:271-279.
39. Yang CS, Wang X, Lu G, Picinich SC. 2009. Cancer prevention by tea: animal studies molecular mechanisms and human relevance. Cancer 9:429-439.
40. Ullmann U, Haller J, Decourt JP, Girault N, Girault J, Richard-Caudron AS, Pineau B, Weber P. 2003. A single ascending dose study of epigallocatechin gallate in healthy volunteers. J. Int. Med. Res. 31:88-101.
41. Stratton SP, Bangert JL, Alberts DS, Dorr RT. 2000. Dermal toxicity of topical epigallocatechin-3-gallate in BALB/c and SKH1 mice. Cancer Lett. 158:47-52.
42. Herold BC, Gerber SI, Belval BJ, Siston AM, Shulman N. 1996. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J. Virol. 70:3461-3469.
43. Trybala E, Liljeqvist JA Svennerholm B, Bergström T. 2000. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J. Virol. 74:9106-9114.
44. Langeland N, Holmsen H, Lillehaug JR, Haarr L. 1987. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J. Virol. 61:3388-3393.
45. Patton DL, Sweeney YC, Cummings PK, Meyn L, Rabe LK, Hillier SL. 2004. Safety and efficacy evaluations for vaginal and rectal use of buffer gel in the macaque model. Sex. Transm. Dis. 31:290-296.
46. Strand M, Islam K, Edlund K, öberg CT, Allard A, Bergström T, Mei Elofsson Y-FM, Wadell G. 2012. 2-[4,5-difluoro-2-(2-fluorobenzoylamino)- benzoylamino] benzoic acid, an antiviral compound with activity against acyclovir-resistant isolates of herpes simplex virus types 1 and Antimicrob. Agents Chemother. 56:5735-5743.
47. Prichard MN, Kaiwar R, Jackman WT, Quenelle DC, Collins DJ, Kern ER, Kemble GM, Spaete RR. 2005. Evaluation of AD472, a live attenuated recombinant herpes simplex virus type 2 vaccine in guinea pigs. Vaccine 24:5424-5431.
48. Whitley RJ. 1994. Herpes simplex virus infections of women and their offspring: implications for a developed society. Proc. Natl. Acad. 91:2441-2447.
49. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, Meehan MO, Lutalo T, Gray RH. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 11 N. Engl. J. Med. 342:921-929.
50. Barouch DH, Klasse PJ, Dufour J, Veazey RS, Moore JP. 2012. Macaque studies of vaccine and microbicide combinations for preventing HIV-1 sexual transmission. Proc. Natl. Acad. Sci. U. S. A. 109:8694-8698.
51. Yang J, Li L, Tan S, Jin H, Qiu J, Mao Q, Li R, Xia C, Jiang Jiang Z-HS, Liu S. 2012. A natural theaflavins preparation inhibits HIV-1 infection by targeting the entry step: potential applications for preventing HIV-1 infection. Fioterapia 83:348-355.