Polyanionic carbosilane dendrimer-conjugated antiviral drugs as efficient microbicides: Recent trends and developments in HIV treatment/therapy

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 6, 2015, Pages 1481-1498

  Sepúlveda Crespo, Daniel ^a,b   Gómez, Rafael ^c   De La Mata, Francisco Javier ^c   Jiménez, José Luis ^b   Muñoz Fernández, M Ángeles ^a,b  

^a BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^c UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

HIV 1 HSV 2; Maraviroc; Microbicide; Polyanionic carbosilane dendrimers; Tenofovir

Indexed keywords

DRUG DOSAGE; DRUG INTERACTIONS;

CARBOSILANE DENDRIMER; HIV-1/HSV-2; MARAVIROC; MICROBICIDE; TENOFOVIR;

DENDRIMERS;

ANTIVIRUS AGENT; CD209 ANTIGEN; CD4 ANTIGEN; DENDRIMER; GLYCOPROTEIN GP 120; GLYCOSPHINGOLIPID; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; MARAVIROC; MICROBICIDE; POLYANION; POLYANIONIC CARBOSILANE DENDRIMER; SILANE DERIVATIVE; TENOFOVIR; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; ANTIINFECTIVE AGENT; CARBOSILANE; POLYANIONS; POLYMER;

ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; BINDING AFFINITY; BIOCOMPATIBILITY; CD4+ T LYMPHOCYTE; CHEMICAL STRUCTURE; CLINICAL RESEARCH; CYTOTOXICITY; DRUG EFFICACY; EC50; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MONOTHERAPY; NONHUMAN; PRE-EXPOSURE PROPHYLAXIS; REVIEW; SEXUAL TRANSMISSION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS TRANSMISSION; CHEMISTRY; DRUG EFFECTS; PHYSIOLOGY; VIRUS REPLICATION;

ANTI-HIV AGENTS; ANTI-INFECTIVE AGENTS; DENDRIMERS; HIV-1; HUMANS; POLYMERS; SILANES; VIRUS REPLICATION;

EID: 84937127376     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.03.008     Document Type: Review

References (138)

1. Richman D.D. HIV chemotherapy. Nature 2001, 410:995-1001.
2. Harris M., Nosyk B., Harrigan R., Lima V.D., Cohen C., Montaner J. Cost-effectiveness of antiretroviral therapy for multidrug-resistant HIV: past, present, and future. AIDS Res Treat 2012, 2012:595762.
3. Hajizadeh M., Sia D., Heymann S.J., Nandi A. Socioeconomic inequalities in HIV/AIDS prevalence in sub-Saharan African countries: evidence from the Demographic Health Surveys. Int J Equity Health 2014, 13:18-40.
4. Maartens G., Celum C., Lewin S.R. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet 2014, 384:258-271.
5. Shen R., Richter H.E., Smith P.D. Interactions between HIV-1 and mucosal cells in the female reproductive tract. Am J Reprod Immunol 2014, 71:608-617.
6. Murphy E.M., Greene M.E., Mihailovic A., Olupot-Olupot P. Was the "ABC" approach (abstinence, being faithful, using condoms) responsible for Uganda's decline in HIV?. PLoS Med 2006, 3:e379-e384.
7. Gupta G.R. How men's power over women fuels the HIV epidemic. BMJ 2002, 324:183-184.
8. Smith P.L., Tanner H., Dalgleish A. Developments in HIV-1 immunotherapy and therapeutic vaccination. F1000Prime Rep 2014, 6:43-55.
9. Cottrell M.L., Kashuba A.D. Topical microbicides and HIV prevention in the female genital tract. J Clin Pharmacol 2014, 54:603-615.
10. Peterson L., Nanda K., Opoku B.K., Ampofo W.K., Owusu-Amoako M., Boakye A.Y., et al. SAVVY (C31G) gel for prevention of HIV infection in women: a phase 3, double-blind, randomized, placebo-controlled trial in Ghana. PLoS One 2007, 2:e1312-e1320.
11. Van Damme L., Ramjee G., Alary M., Vuylsteke B., Chandeying V., Rees H., 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.
12. Pirrone V., Wigdahl B., Krebs F.C. The rise and fall of polyanionic inhibitors of the human immunodeficiency virus type 1. Antiviral Res 2011, 90:168-182.
13. Ensign L.M., Cone R., Hanes J. Nanoparticle-based drug delivery to the vagina: a review. J Control Release 2014, 190C:500-514.
14. Kumar L., Verma S., Prasad D.N., Bhardwaj A., Vaidya B., Jain A.K. Nanotechnology: a magic bullet for HIV AIDS treatment. Artif Cells Nanomedicine Biotechnol 2014, 43:71-86.
15. Gajbhiye V., Palanirajan V.K., Tekade R.K., Jain N.K. Dendrimers as therapeutic agents: a systematic review. J Pharm Pharmacol 2009, 61:989-1003.
16. Sanchez-Rodriguez J., Vacas-Cordoba E., Gomez R., De La Mata F.J., Munoz-Fernandez M.A. Nanotech-derived topical microbicides for HIV prevention: the road to clinical development. Antivir Res 2015, 113C:33-48.
17. Tyssen D., Henderson S.A., Johnson A., Sterjovski J., Moore K., La J., et al. Structure activity relationship of dendrimer microbicides with dual action antiviral activity. PLoS One 2010, 5:e12309-e12324.
18. D'Cruz O.J., Uckun F.M. Vaginal microbicides and their delivery platforms. Expert Opin Drug Deliv 2014, 11:723-740.
19. Kizima L., Rodriguez A., Kenney J., Derby N., Mizenina O., Menon R., et al. A potent combination microbicide that targets SHIV-RT, HSV-2 and HPV. PLoS One 2014, 9:e94547-e94562.
20. Coates T.J., Richter L., Caceres C. Behavioural strategies to reduce HIV transmission: how to make them work better. Lancet 2008, 372:669-684.
21. Freeman E.E., Weiss H.A., Glynn J.R., Cross P.L., Whitworth J.A., Hayes R.J. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006, 20:73-83.
22. Chaowanachan T., Krogstad E., Ball C., Woodrow K.A. Drug synergy of tenofovir and nanoparticle-based antiretrovirals for HIV prophylaxis. PLoS One 2013, 8:e61416-e61429.
23. Cooper D.A., Heera J., Ive P., Botes M., Dejesus E., Burnside R., et al. Efficacy and safety of maraviroc vs. efavirenz in treatment-naive patients with HIV-1: 5-year findings. AIDS 2014, 28:717-725.
24. Ferir G., Palmer K.E., Schols D. Synergistic activity profile of griffithsin in combination with tenofovir, maraviroc and enfuvirtide against HIV-1 clade C. Virology 2011, 417:253-258.
25. Vacas-Cordoba E., Galan M., de la Mata F.J., Gomez R., Pion M., Munoz-Fernandez M.A. Enhanced activity of carbosilane dendrimers against HIV when combined with reverse transcriptase inhibitor drugs: searching for more potent microbicides. Int J Nanomedicine 2014, 9:3591-3600.
26. Sepulveda-Crespo D., Lorente R., Leal M., Gomez R., De la Mata F.J., Jimenez J.L., et al. Synergistic activity profile of carbosilane dendrimer G2-STE16 in combination with other dendrimers and antiretrovirals as topical anti-HIV-1 microbicide. Nanomedicine 2014, 10:609-618.
27. Cordoba E.V., Arnaiz E., De La Mata F.J., Gomez R., Leal M., Pion M., et al. Synergistic activity of carbosilane dendrimers in combination with maraviroc against HIV in vitro. AIDS 2013, 27:2053-2058.
28. Sepulveda-Crespo D., Sánchez-Rodríguez J., Serramía M.J., Gomez R., De la Mata F.J., Jimenez J.L., et al. Triple combination of carbosilane dendrimers, tenofovir and maraviroc as potential microbicide to prevent HIV-1 sexual transmission. Nanomedicine (Lond) 2015, 10. [Epub ahead of print].
29. Chou T.C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006, 58:621-681.
30. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
31. De Clercq E. Clinical potential of the acyclic nucleoside phosphonates cidofovir, adefovir, and tenofovir in treatment of DNA virus and retrovirus infections. Clin Microbiol Rev 2003, 16:569-596.
32. Sokal D.C., Karim Q.A., Sibeko S., Yende-Zuma N., Mansoor L.E., Baxter C., et al. Safety of tenofovir gel, a vaginal microbicide, in South African women: results of the CAPRISA 004 Trial. Antivir Ther 2013, 18:301-310.
33. Celum C., Baeten J.M. Tenofovir-based pre-exposure prophylaxis for HIV prevention: evolving evidence. Curr Opin Infect Dis 2012, 25:51-57.
34. FACTS FACTS 001 Study Design In. http://www.facts-consortium.co.za/.
35. Clinical Trials Implementation effectiveness and safety of tenofovir gel provision through family planning services In. http://clinicaltrials.gov/show/NCT01691768.
36. MTN MTN-008 Expanded Safety Study of Tenofovir Gel in Pregnant and Breastfeeding Women In. http://www.mtnstopshiv.org/news/studies/mtn008.
37. Anton P.A., Cranston R.D., Kashuba A., Hendrix C.W., Bumpus N.N., Richardson-Harman N., et al. RMP-02/MTN-006: a phase 1 rectal safety, acceptability, pharmacokinetic, and pharmacodynamic study of tenofovir 1% gel compared with oral tenofovir disoproxil fumarate. AIDS Res Hum Retroviruses 2012, 28:1412-1421.
38. McGowan I., Hoesley C., Cranston R.D., Andrew P., Janocko L., Dai J.Y., et al. A phase 1 randomized, double blind, placebo controlled rectal safety and acceptability study of tenofovir 1% gel (MTN-007). PLoS One 2013, 8:e6014-e6023.
39. McGowan I. The development of rectal microbicides for HIV prevention. Expert Opin Drug Deliv 2014, 11:69-82.
40. MTN MTN-013/IPM 026: Phase I Safety and Drug Absorption Trial of a Combination Dapivirine-Maraviroc Vaginal Ring In. http://www.mtnstopshiv.org/news/studies/mtn013.
41. Dorr P., Westby M., Dobbs S., Griffin P., Irvine B., Macartney M., 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.
42. Malcolm R.K., Fetherston S.M., McCoy C.F., Boyd P., Major I. Vaginal rings for delivery of HIV microbicides. Int J Womens Health 2012, 4:595-605.
43. MTN Rectal Microbicides Fact Sheet In. http://www.mtnstopshiv.org/node/2864.
44. Tomalia D.A. Birth of a new macromolecular architecture: dendrimers as quantized building blocks for nanoscale synthetic polymer chemistry. Prog Polym Sci 2005, 30:294-324.
45. Tomalia D.A. Dendrons/dendrimers: quantized, nano-element like building blocks for soft-soft and soft-hard nano-compound synthesis. Soft Matter 2010, 6:456-474.
46. Tomalia D.A., Baker H., Dewald J., Hall M., Kallos S., Roeck J., et al. A new class of polymers: starburst-dendritic macromolecules. Polym J 1985, 17:117-132.
47. Kaminskas L.M., Boyd B.J., Porter C.J. Dendrimer pharmacokinetics: the effect of size, structure and surface characteristics on ADME properties. Nanomedicine (Lond) 2011, 6:1063-1084.
48. Abbasi E., Aval S.F., Akbarzadeh A., Milani M., Nasrabadi H.T., Joo S.W., et al. Dendrimers: synthesis, applications, and properties. Nanoscale Res Lett 2014, 9:247-257.
49. Ina M. Dendrimer: a novel drug delivery system. J Drug Deliv Ther 2011, 1:70-74.
50. Tripathy S., Das M.K. Dendrimers and their applications as novel drug delivery carriers. J Appl Pharm Sci 2013, 3:142-149.
51. Kannan R.M., Nance E., Kannan S., Tomalia D.A. Emerging concepts in dendrimer-based nanomedicine: from design principles to clinical applications. J Intern Med 2014, 276:579-617.
52. Lombardo D. Modeling dendrimers charge interaction in solution: relevance in biosystems. Biochem Res Int 2014, 2014:837651.
53. Mintzer M.A., Grinstaff M.W. Biomedical applications of dendrimers: a tutorial. Chem Soc Rev 2011, 40:173-190.
54. Tomalia D.A. Birth of a new macromolecular architecture: dendrimers as quantized building blocks for nanoscale synthetic organic chemistry. Aldrichimica Acta 2004, 37:39-57.
55. Svenson S., Tomalia D.A. Dendrimers in biomedical applications-reflections on the field. Adv Drug Deliv Rev 2005, 57:2106-2129.
56. Ma C.Q., Mena-Osteritz E., Wunderlin M., Schulz G., Bauerle P. 2,2':3',2″-Terthiophene-based all-thiophene dendrons and dendrimers: synthesis, structural characterization, and properties. Chemistry 2012, 18:12880-12901.
57. Gautam S.P., Gupta A.K., Agrawal S., Sureka S. Spectroscopic characterization of dendrimers. Int J Pharm Pharm Sci 2012, 4:77-80.
58. Hedden R.C., Bauer B.J. Structure and dimensions of PAMAM/PEG dendrimer-star polymers. Macromolecules 2003, 36:1829-1835.
59. Wang X., Guerrand L., Wu B., Boldon L., Chen W.-R., Liu L. Characterizations of polyamidoamine dendrimers with scattering techniques. Polymers 2012, 4:600-616.
60. Li J., Piehler L.T., Qin D., Baker J.R., Tomalia D.A. Visualization and characterization of poly(amidoamine) dendrimers by atomic force microscopy. Langmuir 2000, 16:5613-5616.
61. Hawker C.J., Fréchet J.M.J. Preparation of polymers with controlled molecular architecture. A new convergent approach to dendritic macromolecules. J Am Chem Soc 1990, 112:7638-7647.
62. Madaan K., Kumar S., Poonia N., Lather V., Pandita D. Dendrimers in drug delivery and targeting: drug-dendrimer interactions and toxicity issues. J Pharm Bioallied Sci 2014, 6:139-150.
63. Son D.Y. A durable template for carbosilane dendrimer synthesis. Chem Commun (Camb) 2013, 49:10209-10210.
64. Sánchez-Nieves J., Ortega P., Muñoz-Fernandez M.A., Gomez R., De la Mata F.J. Synthesis of carbosilane dendrons and dendrimers derived from 1,3,5-trihydroxybenzene. Tetrahedron 2010, 66:9203-9213.
65. Galan M., Sanchez Rodriguez J., Jimenez J.L., Relloso M., Maly M., de la Mata F.J., et al. Synthesis of new anionic carbosilane dendrimers via thiol-ene chemistry and their antiviral behaviour. Org Biomol Chem 2014, 12:3222-3237.
66. Dufes C., Uchegbu I.F., Schatzlein A.G. Dendrimers in gene delivery. Adv Drug Deliv Rev 2005, 57:2177-2202.
67. Esfand R., Tomalia D.A. Poly(amidoamine) (PAMAM) dendrimers: from biomimicry to drug delivery and biomedical applications. Drug Discov Today 2001, 6:427-436.
68. Kaczorowska M.A., Cooper H.J. Electron capture dissociation, electron detachment dissociation, and collision-induced dissociation of polyamidoamine (PAMAM) dendrimer ions with amino, amidoethanol, and sodium carboxylate surface groups. J Am Soc Mass Spectrom 2008, 19:1312-1319.
69. Bosman A.W., Janssen H.M., Meijer E.W. About dendrimers: structure, physical properties, and applications. Chem Rev 1999, 99:1665-1688.
70. de Gennes P.G., Hervet H. Statistics of "starburst" polymers. J Phys Lett 1983, 44:351-360.
71. Duncan R., Izzo L. Dendrimer biocompatibility and toxicity. Adv Drug Deliv Rev 2005, 57:2215-2237.
72. Greish K., Thiagarajan G., Herd H., Price R., Bauer H., Hubbard D., et al. Size and surface charge significantly influence the toxicity of silica and dendritic nanoparticles. Nanotoxicology 2012, 6:713-723.
73. Domanski D.M., Klajnert B., Bryszewska M. Influence of PAMAM dendrimers on human red blood cells. Bioelectrochemistry 2004, 63:189-191.
74. Jevprasesphant R., Penny J., Jalal R., Attwood D., McKeown N.B., D'Emanuele A. The influence of surface modification on the cytotoxicity of PAMAM dendrimers. Int J Pharm 2003, 252:263-266.
75. Chonco L., Pion M., Vacas E., Rasines B., Maly M., Serramia M.J., et al. Carbosilane dendrimer nanotechnology outlines of the broad HIV blocker profile. J Control Release 2012, 161:949-958.
76. Vacas Cordoba E., Arnaiz E., Relloso M., Sanchez-Torres C., Garcia F., Perez-Alvarez L., et al. Development of sulphated and naphthylsulphonated carbosilane dendrimers as topical microbicides to prevent HIV-1 sexual transmission. AIDS 2013, 27:1219-1229.
77. Lozach P.Y., Burleigh L., Staropoli I., Amara A. The C type lectins DC-SIGN and L-SIGN: receptors for viral glycoproteins. Methods Mol Biol 2007, 379:51-68.
78. Arce E., Nieto P.M., Diaz V., Castro R.G., Bernad A., Rojo J. Glycodendritic structures based on Boltorn hyperbranched polymers and their interactions with Lens culinaris lectin. Bioconjug Chem 2003, 14:817-823.
79. Tabarani G., Reina J.J., Ebel C., Vives C., Lortat-Jacob H., Rojo J., et al. Mannose hyperbranched dendritic polymers interact with clustered organization of DC-SIGN and inhibit gp120 binding. FEBS Lett 2006, 580:2402-2408.
80. Sattin S., Daghetti A., Thepaut M., Berzi A., Sanchez-Navarro M., Tabarani G., et al. Inhibition of DC-SIGN-mediated HIV infection by a linear trimannoside mimic in a tetravalent presentation. ACS Chem Biol 2010, 5:301-312.
81. Berzi A., Reina J.J., Ottria R., Sutkeviciute I., Antonazzo P., Sanchez-Navarro M., et al. A glycomimetic compound inhibits DC-SIGN-mediated HIV infection in cellular and cervical explant models. AIDS 2012, 26:127-137.
82. Varga N., Sutkeviciute I., Ribeiro-Viana R., Berzi A., Ramdasi R., Daghetti A., et al. A multivalent inhibitor of the DC-SIGN dependent uptake of HIV-1 and dengue virus. Biomaterials 2014, 35:4175-4184.
83. Rojo J., Delgado R. Glycodendritic structures: promising new antiviral drugs. J Antimicrob Chemother 2004, 54:579-581.
84. Harouse J.M., Collman R.G., Gonzalez-Scarano F. Human immunodeficiency virus type 1 infection of SK-N-MC cells: domains of gp120 involved in entry into a CD4-negative, galactosyl ceramide/3' sulfo-galactosyl ceramide-positive cell line. J Virol 1995, 69:7383-7390.
85. Kensinger R.D., Yowler B.C., Benesi A.J., Schengrund C.L. Synthesis of novel, multivalent glycodendrimers as ligands for HIV-1 gp120. Bioconjug Chem 2004, 15:349-358.
86. Kensinger R.D., Catalone B.J., Krebs F.C., Wigdahl B., Schengrund C.L. Novel polysulfated galactose-derivatized dendrimers as binding antagonists of human immunodeficiency virus type 1 infection. Antimicrob Agents Chemother 2004, 48:1614-1623.
87. Morales-Serna J.A., Boutureira O., Serra A., Matheu M.I., Diaz Y., Castillon S. Synthesis of hyperbranched β-galceramide-containing dendritic polymers that bind HIV-1 rgp120. Eur J Org Chem 2010, 2010:2657-2660.
88. Blanzat M., Turrin C.O., Aubertin A.M., Couturier-Vidal C., Caminade A.M., Majoral J.P., et al. Dendritic catanionic assemblies: in vitro anti-HIV activity of phosphorus-containing dendrimers bearing galbeta1cer analogues. Chembiochem 2005, 6:2207-2213.
89. Perez-Anes A., Stefaniu C., Moog C., Majoral J.P., Blanzat M., Turrin C.O., et al. Multivalent catanionic GalCer analogs derived from first generation dendrimeric phosphonic acids. Bioorg Med Chem 2010, 18:242-248.
90. Blanzat M., Turrin C.O., Perez E., Rico-Lattes I., Caminade A.M., Majoral J.P. Phosphorus-containing dendrimers bearing galactosylceramide analogs: self-assembly properties. Chem Commun (Camb) 2002, 1864-1865.
91. Perez-Anes A., Spataro G., Coppel Y., Moog C., Blanzat M., Turrin C.O., et al. Phosphonate terminated PPH dendrimers: influence of pendant alkyl chains on the in vitro anti-HIV-1 properties. Org Biomol Chem 2009, 7:3491-3498.
92. Han S., Kanamoto T., Nakashima H., Yoshida T. Synthesis of a new amphiphilic glycodendrimer with antiviral functionality. Carbohydr Polym 2012, 90:1061-1068.
93. Han S., Yoshida D., Kanamoto T., Nakashima H., Uryu T., Yoshida T. Sulfated oligosaccharide cluster with polylysine core scaffold as a new anti-HIV dendrimer. Carbohydr Polym 2010, 80:1111-1115.
94. Lundquist J.J., Toone E.J. The cluster glycoside effect. Chem Rev 2002, 102:555-578.
95. Han S., Baigude H., Yoshida T., Uryu T. Synthesis of new spherical and hemispherical oligosaccharides with polylysine core scaffold. Carbohydr Polym 2007, 68:26-34.
96. Degroote S., Wolthoorn J., van Meer G. The cell biology of glycosphingolipids. Semin Cell Dev Biol 2004, 15:375-387.
97. Rosa Borges A., Wieczorek L., Johnson B., Benesi A.J., Brown B.K., Kensinger R.D., et al. Multivalent dendrimeric compounds containing carbohydrates expressed on immune cells inhibit infection by primary isolates of HIV-1. Virology 2010, 408:80-88.
98. Clayton R., Hardman J., LaBranche C.C., McReynolds K.D. Evaluation of the synthesis of sialic acid-PAMAM glycodendrimers without the use of sugar protecting groups, and the anti-HIV-1 properties of these compounds. Bioconjug Chem 2011, 22:2186-2197.
99. Pierson T.C., Doms R.W. HIV-1 entry and its inhibition. Curr Top Microbiol Immunol 2003, 281:1-27.
100. Huang C.C., Tang M., Zhang M.Y., Majeed S., Montabana E., Stanfield R.L., et al. Structure of a V3-containing HIV-1 gp120 core. Science 2005, 310:1025-1028.
101. Meshcheryakova D., Andreev S., Tarasova S., Sidorova M., Vafina M., Kornilaeva G., et al. CD4-derived peptide and sulfated polysaccharides have similar mechanisms of anti-HIV activity based on electrostatic interactions with positively charged gp120 fragments. Mol Immunol 1993, 30:993-1001.
102. Rizzuto C.D., Wyatt R., Hernandez-Ramos N., Sun Y., Kwong P.D., Hendrickson W.A., et al. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 1998, 280:1949-1953.
103. Witvrouw M., Fikkert V., Pluymers W., Matthews B., Mardel K., Schols D., et al. Polyanionic (i.e., polysulfonate) dendrimers can inhibit the replication of human immunodeficiency virus by interfering with both virus adsorption and later steps (reverse transcriptase/integrase) in the virus replicative cycle. Mol Pharmacol 2000, 58:1100-1108.
104. Nandy B., Bindu D.H., Dixit N.M., Maiti P.K. Simulations reveal that the HIV-1 gp120-CD4 complex dissociates via complex pathways and is a potential target of the polyamidoamine (PAMAM) dendrimer. J Chem Phys 2013, 139:24905-24909.
105. McCarthy T.D., Karellas P., Henderson S.A., Giannis M., O'Keefe D.F., Heery G., et al. Dendrimers as drugs: discovery and preclinical and clinical development of dendrimer-based microbicides for HIV and STI prevention. Mol Pharm 2005, 2:312-318.
106. Rupp R., Rosenthal S.L., Stanberry L.R. VivaGel (SPL7013 Gel): a candidate dendrimer-microbicide for the prevention of HIV and HSV infection. Int J Nanomedicine 2007, 2:561-566.
107. Price C.F., Tyssen D., Sonza S., Davie A., Evans S., Lewis G.R., et al. SPL7013 Gel (VivaGel(R)) retains potent HIV-1 and HSV-2 inhibitory activity following vaginal administration in humans. PLoS One 2011, 6:e24095-e24107.
108. Telwatte S., Moore K., Johnson A., Tyssen D., Sterjovski J., Aldunate M., et al. Virucidal activity of the dendrimer microbicide SPL7013 against HIV-1. Antiviral Res 2011, 90:195-199.
109. Moscicki A.B., Kaul R., Ma Y., Scott M.E., Daud I.I., Bukusi E.A., et al. Measurement of mucosal biomarkers in a phase 1 trial of intravaginal 3% StarPharma LTD 7013 gel (VivaGel) to assess expanded safety. J Acquir Immune Defic Syndr 2012, 59:134-140.
110. Rasines B., Sanchez-Nieves J., Maiolo M., Maly M., Chonco L., Jimenez J.L., et al. Synthesis, structure and molecular modelling of anionic carbosilane dendrimers. Dalton Trans 2012, 41:12733-12748.
111. Arnáiz E., Vacas Cordoba E., Galan M., Pion M., Gomez R., Munoz-Fernandez M.A., et al. Synthesis of anionic carbosilane dendrimers via "click chemistry" and their antiviral properties against HIV. J Polym Sci A1 2014, 52:1099-1112.
112. Galan M., Sanchez-Rodriguez J., Cangiotti M., Garcia-Gallego S., Jimenez J.L., Gomez R., et al. Antiviral properties against HIV of water soluble copper carbosilane dendrimers and their EPR characterization. Curr Med Chem 2012, 19:4984-4994.
113. Neira J.L. The capsid protein of human immunodeficiency virus: designing inhibitors of capsid assembly. FEBS J 2009, 276:6110-6117.
114. Domenech R., Abian O., Bocanegra R., Correa J., Sousa-Herves A., Riguera R., et al. Dendrimers as potential inhibitors of the dimerization of the capsid protein of HIV-1. Biomacromolecules 2010, 11:2069-2078.
115. Bishop J.R., Schuksz M., Esko J.D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007, 446:1030-1037.
116. Bon I., Lembo D., Rusnati M., Clo A., Morini S., Miserocchi A., et al. Peptide-derivatized SB105-A10 dendrimer inhibits the infectivity of R5 and X4 HIV-1 strains in primary PBMCs and cervicovaginal histocultures. PLoS One 2013, 8:e76482-e76495.
117. Asaftei S., De Clercq E. "Viologen" dendrimers as antiviral agents: the effect of charge number and distance. J Med Chem 2010, 53:3480-3488.
118. Asaftei S., Huskens D., Schols D. HIV-1 X4 activities of polycationic "viologen" based dendrimers by interaction with the chemokine receptor CXCR4: study of structure-activity relationship. J Med Chem 2012, 55:10405-10413.
119. Kumar P.D., Kumar P.V., Selvam T.P., Rao K.S. PEG conjugated PAMAM dendrimers with a anti-HIV drug stavudine for prolong release. Res Biotechnol 2013, 4:10-18.
120. Kumar P.D., Kumar P.V., Selvam T.P., Rao K.S. Prolonged drug delivery system of PEGylated PAMAM dendrimers with a anti-HIV drug. Res Pharm 2013, 3:8-17.
121. Dutta T., Garg M., Jain N.K. Targeting of efavirenz loaded tuftsin conjugated poly(propyleneimine) dendrimers to HIV infected macrophages in vitro. Eur J Pharm Sci 2008, 34:181-189.
122. Dutta T., Jain N.K. Targeting potential and anti-HIV activity of lamivudine loaded mannosylated poly (propyleneimine) dendrimer. Biochim Biophys Acta 2007, 1770:681-686.
123. Gajbhiye V., Ganesh N., Barve J., Jain N.K. Synthesis, characterization and targeting potential of zidovudine loaded sialic acid conjugated-mannosylated poly(propyleneimine) dendrimers. Eur J Pharm Sci 2013, 48:668-679.
124. Pyreddy S., Kumar P.D., Kumar P.V. Polyethylene glycolated PAMAM dendrimers-Efavirenz conjugates. Int J Pharm Invest 2014, 4:15-18.
125. Balandya E., Sheth S., Sanders K., Wieland-Alter W., Lahey T. Semen protects CD4+ target cells from HIV infection but promotes the preferential transmission of R5 tropic HIV. J Immunol 2010, 185:7596-7604.
126. Grivel J.C., Shattock R.J., Margolis L.B. Selective transmission of R5 HIV-1 variants: where is the gatekeeper?. J Transl Med 2011, 9(Suppl. 1):S1-S6.
127. Sarrami-Forooshani R., Mesman A.W., van Teijlingen N.H., Sprokholt J.K., van der Vlist M., Ribeiro C.M., et al. Human immature Langerhans cells restrict CXCR4-using HIV-1 transmission. Retrovirology 2014, 11:52.
128. Kahle E., Campbell M., Lingappa J., Donnell D., Celum C., Ondondo R., et al. HIV-1 subtype C is not associated with higher risk of heterosexual HIV-1 transmission: a multinational study among HIV-1 serodiscordant couples. AIDS 2014, 28:235-243.
129. Sanchez-Rodriguez J., Vacas-Cordoba E., Gomez R., De La Mata F.J., Munoz-Fernandez M.A. Nanotech-derived topical microbicides for HIV prevention: the road to clinical development. Antiviral Res 2015, 113C:33-48.
130. Abdool Karim S.S., Baxter C. Overview of microbicides for the prevention of human immunodeficiency virus. Best Pract Res Clin Obstet Gynaecol 2012, 26:427-439.
131. Zirafi O., Kim K., Roan N.R., Kluge S.F., Müller J.A., Jiang S., et al. Semen enhances HIV infectivity and impairs the antiviral efficacy of microbicides. Sci Transl Med 2014, 6:262-273.
132. Herold B.C., Mesquita P.M., Madan R.P., Keller M.J. 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 2011, 65:325-333.
133. Denton P.W., Garcia J.V. Humanized mouse models of HIV infection. AIDS Rev 2011, 13:135-148.
134. Lanham M., Wilcher R., Montgomery E.T., Pool R., Schuler S., Lenzi R., et al. Engaging male partners in women's microbicide use: evidence from clinical trials and implications for future research and microbicide introduction. J Int AIDS Soc 2014, 17:19159-19170.
135. Nunes R., Sarmento B., das Neves J. Formulation and delivery of anti-HIV rectal microbicides: advances and challenges. J Control Release 2014, 194C:278-294.
136. Rohan L.C., Devlin B., Yang H. Microbicide dosage forms. Curr Top Microbiol Immunol 2014, 383:27-54.
137. Kuhn B., Gerber P., Schulz-Gasch T., Stahl M. Validation and use of the MM-PBSA approach for drug discovery. J Med Chem 2005, 48:4040-4048.
138. Myszka D.G., Sweet R.W., Hensley P., Brigham-Burke M., Kwong P.D., Hendrickson W.A., et al. Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci U S A 2000, 97:9026-9031.