Combination of antiretroviral drugs as microbicides

Current HIV Research

Volumn 10, Issue 1, 2012, Pages 53-60

  Balzarini, Jan ^a   Schols, Dominique ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

AIDS; Antiretroviral drugs; CBAs; Drug combinations; Entry inhibitors; HIV; Microbicides; Reverse transcriptase; Synergy; Tenofovir

Indexed keywords

ACICLOVIR; AGGLUTININ; ANTIRETROVIRUS AGENT; APLAVIROC; BANANA LECTIN; CARBOHYDRATE BINDING AGENT; CYANOVIRIN N; DAPIVIRINE; EFAVIRENZ; EMTRICITABINE; ENFUVIRTIDE; GRIFFITHSIN; INDINAVIR; LAMIVUDINE; MARAVIROC; MICROBICIDE; MICROVIRIN; MONOCLONAL ANTIBODY 2G12; MYCOPHENOLIC ACID; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; NEVIRAPINE; PLERIXAFOR; RIBAVIRIN; T 1144; TE 14011; TENOFOVIR; TIFUVIRTIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; URTICA DIOICA EXTRACT; ZIDOVUDINE;

ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; DRUG BINDING; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; HERPES SIMPLEX VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL (TOPIC); SEXUAL TRANSMISSION; VIRUS ENVELOPE; VIRUS REPLICATION; VIRUS TRANSMISSION;

ADENINE; ANTI-INFECTIVE AGENTS, LOCAL; ANTI-RETROVIRAL AGENTS; DRUG THERAPY, COMBINATION; HIV INFECTIONS; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; PHOSPHONIC ACIDS; RECEPTORS, HIV;

EID: 84857132880     PISSN: 1570162X     EISSN: 18734251     Source Type: Journal    
DOI: 10.2174/157016212799304652     Document Type: Article

References (75)

1. Shattock RJ, Moore JP. Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol2003; 1: 25-34.
2. Balzarini J, Van Damme L. Microbicide drug candidates to prevent HIV infection. Lancet 2007; 369: 787-797.
3. Klasse PJ, Shattock R, Moore JP. Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu Rev Med 2008; 59: 455-471.
4. Doncel GF, Clark MR. Preclinical evaluation of anti-HIV microbicide products: New models and biomarkers. Antiviral Res 2010; 88, Suppl 1: S10-S18.
5. Van Damme L, Ramjee G, Alary M, et al. Effectiveness of COL- 1492, a nonoxynol-9 vaginal gel, on HIV-1 transmission in female sex workers: a randomised controlled trial. Lancet 2002; 360: 971-977.
6. Van Damme L, Govinden R, Mirembe FM, et al. Lack of effectiveness of cellulose sulfate gel for the prevention of vaginal HIV transmission. N Engl J Med 2008; 359: 463-472.
7. Skoler-Karpoff S, Ramjee G, Ahmed K, et al. Efficacy of Carraguard for prevention of HIV infection in women in South Africa: a randomised, double-blind, placebo-controlled trial. Lancet 2008; 372: 1977-1987.
8. van Damme L, Wright A, Depraetere K, et al. A phase I study of a novel potential intravaginal microbicide, PRO 2000, in healthy sexually inactive women. Sex. Transm. Infect 2000; 76: 126-130.
9. Keller MJ, Zerhouni-Layachi B, Cheshenko N, et al. PRO 2000 gel inhibits HIV and herpes simplex virus infection following vaginal application: A double-blind placebo-controlled trial. J Infect Dis 2006; 193: 27-35.
10. Scordi-Bello IA, Mosoian A, He C, et al. Candidate sulfonated and sulfated topical microbicides: Comparison of anti-human immunodeficiency virus activities and mechanisms of action. Antimicrob Agents Chemother 2005; 49: 3607-3615.
11. Karim SA, Coletti A, Richardson B, et al. Safety and effectiveness of vaginal microbicides BufferGel and 0.5% PRO 2000/5 gel for the prevention of HIV infection in women: results of the HPTN 035 trial. 16th Conference on Retroviruses and Opportnistic Infections Feb 9, 2009 Oral abstract 48LB 2009.
12. McCormack S, Ramjee G, Kamali A, et al. PRO2000 vaginal gel for prevention of HIV-1 infection (Microbicides Development Programme 301): a phase 3, randomised, double-blind, parallelgroup trial. Lancet 2010; 376: 1329-1337.
13. Balzarini J, Holý A, Jindrich J, et al. Differential antiherpesvirus and antiretrovirus effects of the (S) and (R) enantiomers of acyclic nucleoside phosphonates: potent and selective in vitro and in vivo antiretrovirus activities of (R)-9-(2-phosphonomethoxypropyl)-2,6- diaminopurine. Antimicrob Agents Chemother 1993; 37: 332-338.
14. Abdool KQ, Abdool Karim SS, Frohlich JA, et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 2010; 329: 1168-1174.
15. Tilton JC, Doms RW. Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res 2010; 85: 91-100.
16. Balzarini J. Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat Rev Microbiol 2007; 5: 583-597.
17. Férir G, Vermeire K, Huskens D, et al. Synergistic in vitro anti- HIV type 1 activity of tenofovir with carbohydrate-binding agents (CBAs). Antiviral Res 2011; 90: 200-204.
18. Férir G, Palmer KE, Schols D. Synergistic activity profile of griffithsin in combination with tenofovir, maraviroc and enfuvirtide against HIV-1 clade C. Virology 2011; 417: 253-258.
19. Scanlan CN, Pantophlet R, Wormald MR, et al. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha-1,2-mannose residues on the outer face of gp120. J Virol 2002; 76: 7306-7321.
20. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drug or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
21. Perrin L, Kaiser L, Yerly S. Travel and the spread of HIV-1 genetic variants. Lancet Infect Dis 2003; 3: 22-27.
22. Balzarini J, Hatse S, Vermeire K, et al. Mannose-specific plant lectins from the Amaryllidaceae family qualify as efficient microbicides for prevention of human immunodeficiency virus infection. Antimicrob Agents Chemother 2004; 48: 3858-3870.
23. Balzarini J, Van Laethem K, Hatse S, et al. Carbohydrate-binding agents cause deletions of highly conserved glycosylation sites in HIV gp120: a new therapeutic concept to hit the Achilles heel of HIV. J Biol Chem 2005; 280: 41005-41014.
24. Balzarini J, Francois KO, Van Laethem K, et al. Pradimicin S, a highly soluble nonpeptidic small-size carbohydrate-binding antibiotic, is an anti-HIV drug lead for both microbicidal and systemic use. Antimicrob Agents Chemother 2010; 54: 1425-1435.
25. Huskens D, Férir G, Vermeire K, et al. Microvirin, a novel alpha(1,2)-mannose-specific lectin isolated from Microcystis aeruginosa, has anti-HIV-1 activity comparable with that of cyanovirin-N but a much higher safety profile. J Biol Chem 2010; 285: 24845-24854.
26. Huskens D, Van Laethem K, Vermeire K, Balzarini J, Schols D. Resistance of HIV-1 to the broadly HIV-1-neutralizing, anticarbohydrate antibody 2G12. Virology 2007; 360: 294-304.
27. Huskens D, Vermeire K, Vandemeulebroucke E, Balzarini J, Schols D. Safety concerns for the potential use of cyanovirin-N as microbicidal anti-HIV agent. Int J Biochem Cell Biol 2008; 40: 2802-2814.
28. Lannoo N, Peumans WJ, Pamel EV, et al. Localization and in vitro binding studies suggest that the cytoplasmic/nuclear tobacco lectin can interact in situ with high-mannose and complex N-glycans. FEBS Lett 2006; 580: 6329-6337.
29. Lannoo N, Vervecken W, Proost P, Rouge P, Van Damme EJ. Expression of the nucleocytoplasmic tobacco lectin in the yeast Pichia pastoris. Protein Expr Purif 2007; 53: 275-282.
30. Swanson MD, Winter HC, Goldstein IJ, Markovitz DM. A lectin isolated from bananas is a potent inhibitor of HIV replication. J Biol Chem 2010; 285: 8646-8655.
31. Emau P, Tian B, O'Keefe BR, et al. Griffithsin, a potent HIV entry inhibitor, is an excellent candidate for anti-HIV microbicide. J Med Primatol 2007; 36: 244-253.
32. O'Keefe, B. R., Vojdani, F., et al. 2009. Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc Natl Acad Sci U S A 2009; 106: 6099-6104.
33. Vermeire K, Princen K, Hatse S, et al. CADA, a novel CD4- targeted HIV inhibitor, is synergistic with various anti-HIV drugs in vitro. AIDS 2004; 18: 2115-2125.
34. Schols D, Struyf S, Van Damme J, Este JA, Henson G, De Clercq E. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J Exp Med 1997; 186:1383-1388.
35. Dorr P, Westby M, Dobbs S, et al. Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob Agents Chemother 2005; 49: 4721-4732.
36. Schader SM, Colby-Germinario SP, Schachter JR, Xu H, Wainberg MA. Synergy against drug-resistant HIV-1 with the microbicide antiretrovirals, dapivirine and tenofovir, in combination. AIDS 2011; 25: 1585-1594.
37. Mulato AS, Charrington JM. Anti-HIV activity of adefovir (PMEA) and PMPA in combination with antiretroviral compounds: in vitro analyses. Antiviral Res 1997; 36: 91-97.
38. Feng JY, Ly JK, Myrick F, et al. The triple combination of tenofovir, emtricitabine and efavirenz shows synergistic anti-HIV-1 activity in vitro: a mechanism of action study. Retrovirology 2009; 6: 44.
39. Tremblay CL, Giguel F, Kollmann C, et al. Anti-human immunodeficiency virus interactions of SCH-C (SCH 351125), a CCR5 antagonist, with other antiretroviral agents in vitro. Antimicrob Agents Chemother 2002; 46: 1336-1339.
40. Murga JD, Franti M, Pevear DC, Maddon PJ, Olson WC. Potent antiviral synergy between monoclonal antibody and small-molecule CCR5 inhibitors of human immunodeficiency virus type 1. Antimicrob Agents Chemother 2006; 50: 3289-3296.
41. Latinovic O, Le N, Reitz M, et al. Synergistic inhibition of R5 HIV-1 by maraviroc and CCR5 antibody HGS004 in primary cells: implications for treatment and prevention. AIDS 2011; 25: 1232-1235.
42. Nakata H, Steinberg SM, Koh Y, et al. Potent synergistic antihuman immunodeficiency virus (HIV) effects using combinations of the CCR5 inhibitor aplaviroc with other anti-HIV drugs. Antimicrob Agents Chemother 2008; 52: 2111-2119.
43. Gouwy M., Struyf S, Berghmans N., Vanormelingen C., Schols D., Van Damme J. CXCR4 and CCR5 ligands cooperate in monocyte and lymphocyte migration and in inhibition of dual-tropic (R5/X4) HIV-1 infection. Eur J Immunol 2011; 41: 963-973.
44. Kilby JM, Hopkins S, Venetta TM, et al. Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41- mediated virus entry. Nat Med 1998; 4: 1302-1307.
45. Tremblay CL, Kollmann C, Giguel F, Chou TC, Hirsch MS. Strong in vitro synergy between the fusion inhibitor T-20 and the CXCR4 blocker AMD-3100. J Acquir Immune DeficSyndr 2000; 25: 99-102.
46. Pan C, Cai L, Lu H, Qi Z, Jiang S. Combinations of the first and next generations of human immunodeficiency virus (HIV) fusion inhibitors exhibit a highly potent synergistic effect against enfuvirtide-sensitive and -resistant HIV type 1 strains. J Virol 2009; 83: 7862-7872.
47. Shahzad-ul-Hussan S, Gustchina E, Ghirlando R, Clore GM, Bewley CA. Solution structure of the monovalent lectinmicrovirin in complex with Man(alpha)(1-2)Man provides a basis for anti-HIV activity with low toxicity. J BiolChem 2011; 286: 20788-20796.
48. Armbruster C, Stiegler GM, Vcelar BA, et al. Passive immunization with the anti-HIV-1 human monoclonal antibody (hMAb) 4E10 and the hMAb combination 4E10/2F5/2G12. J Antimicrob Chemother 2004; 54: 915-920.
49. Trkola A, Kuster H, Rusert P, et al. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 2005; 11: 615-622.
50. Baba M, Pauwels R, Balzarini J, et al. Ribavirin antagonizes inhibitory effects of pyrimidine 2',3'-dideoxynucleosides but enhances inhibitory effects of purine 2',3'-dideoxynucleosides on replication of human immunodeficiency virus in vitro. Antimicrob Agents Chemother 1987; 31: 1613-1617.
51. Balzarini J, Herdewijn P, De Clercq E. Potentiating effect of ribavirin on the anti-retrovirus activity of 3'-azido-2,6-diaminopurine-2',3'-dideoxyriboside in vitro and in vivo. Antiviral Res 1989; 11: 161-171.
52. Balzarini J, Naesens L, Robins MJ, De Clercq E. Potentiating effect of ribavirin on the in vitro and in vivo antiretrovirus activities of 2',3'-dideoxyinosine and 2',3'-dideoxy-2,6-diaminopurine riboside. J Acquir Immune Defic Syndr 1990; 3: 1140-1147.
53. Neyts J, De Clercq E. The anti-herpesvirus activity of (1'S,2'R)-9-[[1',2'-bis(hydroxymethyl)-cycloprop-1'-yl]methyl]guanine is markedly potentiated by the immunosuppressive agent mycophenolate mofetil. Antiviral Res. 2001; 49: 121-127.
54. Neyts J, Andrei G, De Clercq E. The antiherpesvirus activity of H2G [(R)-9-[4-hydroxy-2-(hydroxymethyl)butyl]guanine] is markedly enhanced by the novel immunosuppressive agent mycophenolate mofetil. Antimicrob Agents Chemother 1998; 42: 3285-3289.
55. Pancheva S, Shishkov S, Ilieva D. Effect of combined acyclovir and ribavirin on experimental herpes simplex virus type 1 keratoconjunctivitis in rabbits. Acta Microbiol Bulg 1993; 29: 61-64.
56. Balzarini J. Effect of antimetabolite drugs of nucleotide metabolism on the anti-human immunodeficiency virus activity of nucleoside reverse transcriptase inhibitors. Pharmacol Ther 2000; 87: 175-187.
57. López M, Benito JM, Lozano S, et al. Enhanced HIV-specific immune responses in chronically HIV-infected patients receiving didanosine plus hydroxyurea. AIDS 2004; 18: 1251-1261.
58. Lori F, Malykh AG, Foli A, et al. Combination of a drug targeting the cell with a drug targeting the virus controls human immunodeficiency virus type 1 resistance. AIDS Res Hum Retroviruses 1997; 13: 1403-1409.
59. Lori F, Lisziewicz J. Rationale for the use of hydroxyurea as an anti-human immunodeficiency virus drug. Clin Infect Dis 2000; 30, Suppl 2: S193-S197.
60. Lori F, Pollard RB, Whitman L, et al. Lowering the dose of hydroxyurea minimizes toxicity and maximizes anti-HIV potency. AIDS Res Hum Retroviruses 2005; 21: 263-272.
61. Lackman-Smith C, Osterling C, Luckenbaugh K, et al. Development of a comprehensive human immunodeficiency virus type 1 screening algorithm for discovery and preclinical testing of topical microbicides. Antimicrob Agents Chemother 2008; 52: 1768-1781.
62. Rusconi S, Moonis M, Merrill DP, et al. Naphthalene sulfonate polymers with CD4-blocking and anti-human immunodeficiency virus type 1 activities. Antimicrob Agents Chemother 1996; 40:234-236.
63. Cheshenko N, Keller MJ, MasCasullo V, et al. Candidate topical microbicides bind herpes simplex virus glycoprotein B and prevent viral entry and cell-to-cell spread. Antimicrob Agents Chemother 2004; 48: 2025-2036.
64. Huskens D, Vermeire K, Profy AT, Schols D. The candidate sulfonated microbicide, PRO 2000, has potential multiple mechanisms of action against HIV-1. Antiviral Res 2009; 84: 38-47.
65. Buckheit RW Jr, Hartman TL, Watson KM, Chung SG, Cho EH. Comparative evaluation of the inhibitory activities of a series of pyrimidinedione congeners that inhibit human immunodeficiency virus types 1 and 2. Antimicrob Agents Chemother 2008; 52: 225-236.
66. Watson KM, Buckheit CE, Buckheit RW Jr. Comparative evaluation of virus transmission inhibition by dual-acting pyrimidinedione microbicides using the microbicide transmission and sterilization assay. Antimicrob Agents Chemother 2008; 52: 2787-2796.
67. Watson-Buckheit K, Yang L, Buckheit RW Jr. Development of dual-acting pyrimidinediones as novel and highly potent topical anti-HIV microbicides. Antimicrob Agents Chemother 2011; in press.
68. Esposito F, Kharlamova T, Distinto S, et al. Alizarine derivatives as new dual inhibitors of the HIV-1 reverse transcriptase-associated DNA polymerase and RNase H activities effective also on the RNase H activity of non-nucleoside resistant reverse transcriptases. FEBS J 2011; 278: 1444-1457.
69. Cates, W. Jr. After CAPRISA 004: time to re-evaluate the HIV lexicon. Lancet 2010; 376: 495-496.
70. Andrei G, Lisco A, Vanpouille C, et al. Topical tenofovir as dualtargeted anti-human immunodeficiency virus and antiherpesvirusmicrobicide. Cell Host Microbe 2011; 10: 379-389.
71. Lisco A, Vanpouille C, Tchesnokov EP, et al. Acyclovir is activated into a HIV-1 reverse transcriptase inhibitor in herpesvirus-infected human tissues. Cell Host Microbe 2008; 4:260-270.
72. Tchesnokov EP, Obikhod A, Massud I, et al. Mechanisms associated with HIV-1 resistance to acyclovir by the V75I mutation in reverse transcriptase. J Biol Chem 2009; 284: 21496-21504.
73. Derudas M, Carta D, Brancale A, et al. The application of phosphoramidate protide technology to acyclovir confers anti-HIV inhibition. J Med Chem 2009; 52:5520-5530.
74. Vanpouille C, Lisco A, Derudas M, et al. A new class of dualtargeted antivirals: monophosphorylated acyclovir prodrug derivatives suppress both human immunodeficiency virus type 1 and herpes simplex virus type 2. J Infect Dis 2010; 201: 635-643.
75. Buckheit RW Jr, Watson KM, Morrow KM, Ham AS. Development of topical microbicides to prevent the sexual transmission of HIV. Antiviral Res 2010; 85: 142-158.