Peptide-Derivatized SB105-A10 Dendrimer Inhibits the Infectivity of R5 and X4 HIV-1 Strains in Primary PBMCs and Cervicovaginal Histocultures

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Bon, Isabella ^a   Lembo, David ^b   Rusnati, Marco ^c   Clò, Alberto ^a   Morini, Silvia ^a   Miserocchi, Anna ^a   Bugatti, Antonella ^c   Grigolon, Sonia ^d   Musumeci, Giuseppina ^a   Landolfo, Santo ^e   Re, Maria Carla ^a,f   Gibellini, Davide ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF BRESCIA   (Italy)

^d Spider Biotech srl   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTYLSERYLLEUCYLARGINYLVALYLARGINYLISOLEUCYLLYSYLLYSINE; DENDRIMER; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MICROBICIDE; PROTEOHEPARAN SULFATE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG PROTEIN BINDING; HETEROSEXUALITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; PERIPHERAL BLOOD MONONUCLEAR CELL; SEXUAL TRANSMISSION; SURFACE PLASMON RESONANCE; TISSUE CULTURE; UTERINE CERVIX; VAGINA; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; CERVIX UTERI; DENDRIMERS; FEMALE; FLOW CYTOMETRY; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; LEUKOCYTES, MONONUCLEAR; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN BINDING; SPECIES SPECIFICITY; TISSUE CULTURE TECHNIQUES; VAGINA; VIRUS REPLICATION;

EID: 84885024058     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076482     Document Type: Article

References (96)

1. Quinn TC, (2009) HIV epidemiology and the effects of antiviral therapy on long-term consequences. AIDS 22: S7-S12.
2. WHO (2011) Global HIV/AIDS Response: Epidemic update and health sector progress towards Universal Access Progress report 2011. Available: http://www.who.int/hiv/data/en/Accessed 2013 May10.
3. Bekker LG, Beyrer C, Quinn TC, (2012) Behavioral and biomedical combination strategies for HIV prevention. Cold Spring Harb Perspect Med 2: a007435.
4. Broder S, (2010) The development of antiretroviral therapy and its impact on the HIV-1/AIDS pandemic. Antiviral Res 85: 1-18.
5. Marsden MD, Zack JA, (2009) Eradication of HIV: current challenges and new directions. J Antimicrob Chemother 63: 7-10.
6. Maldarelli F, (2011) Targeting viral reservoirs: ability of antiretroviral therapy to stop viral replication. Curr Opin HIV AIDS 6: 49-56.
7. Wilson LE, Gallant JE, (2009) HIV/AIDS: the management of treatment-experienced HIV-infected patients: new drugs and drug combinations. Clin Infect Dis 48: 214-221.
8. Dahl V, Josefsson L, Palmer S, (2012) HIV reservoirs, latency, and reactivation: prospects for eradication. Antivir Res 85: 286-294.
9. Lederman MM, Offord RE, Hartley O, (2006) Microbicides and other topical strategies to prevent vaginal transmission of HIV. Nat Rev Immunol 6: 371-382.
10. Coates T, Richter L, Caceres C, (2008) Behavioural strategies to reduce HIV transmission: How to make them work better. Lancet 372: 669-684.
11. Girard MP, Plotkin SA, (2012) HIV vaccine development at the turn of the 21st century. Curr Opin HIV AIDS 7: 4-9.
12. Girard MP, Osmanov S, Assossouc OM, Kieny MP, (2011) Human immunodeficiency virus (HIV) immunopathogenesis and vaccine development: A review. Vaccine 29: 6191-6218.
13. Cohen MS, (2004) HIV and sexually transmitted diseases: lethal synergy. Top HIV Med 12: 104-107.
14. Higgins JA, Hoffman S, Dworkin SL, (2010) Rethinking gender, heterosexual men, and women's vulnerability to HIV/AIDS. Am J Public Health 100: 435-445.
15. Lederman MM, Jump R, Pilch-Cooper HA, Root M, Sieg SF, (2008) Topical application of entry inhibitors as "virustats" to prevent sexual transmission of HIV infection. Retrovirology 5: 116.
16. Klasse PJ, Shattock R, Moore JP, (2008) Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu Rev Med 59: 455-471.
17. Kuhmann SE, Hartley O, (2008) Targeting chemokine receptors in HIV: a status report. Annu Rev Pharmacol Toxicol 48: 425-461.
18. Smith RJ, Bodine EN, Wilson DP, Blower SM, (2005) Evaluating the potential impact of vaginal microbicides to reduce the risk of acquiring HIV in female sex workers. AIDS 19: 413-421.
19. Foss AM, Vickerman PT, Alary M, Watts CH, (2009) How much could a microbicide's sexually transmitted infection efficacy contribute to reducing HIV risk and the level of condom use needed to lower risk? Model estimates. Sex Transm Infect 85: 276-282.
20. De Clerq E, (2010) Antiretroviral drugs. Curr Opin Pharmacol 10: 507-515.
21. McGowan I, (2010) Microbicides for HIV prevention: reality or hope? Curr Opin Infect Dis 23: 26-31.
22. Morris GC, Lacey CJ, (2010) Microbicides and HIV prevention: lessons from the past, looking to the future. Curr Opin Infect Dis 23: 57-63.
23. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, et al. (2010) CAPRISA 004 Trial Group. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 329: 1168-1174.
24. McEnery R, (2011) Oral tenofovir arm of VOICE trial discontinued early. IAVI Rep 15: 21.
25. Van Damme L, Corneli A, Ahmed K, Agot K, Lombaard J, et al. (2012) FEM-PrEP Study Group. Preexposure prophylaxis for HIV infection among African women. N Engl J Med 367: 411-422.
26. Thigpen MC, Kebaabetswe PM, Paxton LA, Smith DK, Rose CE, et al. (2012) TDF2 Study Group. Antiretroviral preexposure prophylaxis for heterosexual HIV transmission in Botswana. N Engl J Med 367: 423-434.
27. Baeten JM, Donnell D, Ndase P, Mugo NR, Campbell JD, et al. (2012) Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med 367: 399-410.
28. Grobler A, Abdool Karim S, (2012) Declining adherence is a more likely explanation than frailty of the apparent decline in efficacy in the CAPRISA 004 trial. AIDS 26: 2261.
29. Van der Straten A, Van Damme L, Haberer JE, Bangsberg DR, (2012) Unraveling the divergent results of pre-exposure prophylaxis trials for HIV prevention. AIDS 26: F13-F19.
30. Cloninger MJ, (2002) Biological applications of dendrimers. Curr Opin Chem Biol 6: 742-748.
31. McCarthy TD, Karellas P, Henderson SA, Giannis M, O′Keefe DF, et al. (2005) Dendrimers as drugs, discovery and preclinical and clinical development of dendrimer-based microbicides for HIV and STI prevention. Mol. Pharm 2: 312-318.
32. Rosa Borges A, Schengrund CL, (2005) Dendrimers and antivirals, a review. Curr Drug Targets Infect Disord 5: 247-254.
33. Heegaard PM, Boas U, (2006) Dendrimer based anti-infective and antiinflammatory drugs. Rec Pat Anti-Infect Drug Discov 1: 331-351.
34. Dezzutti CS, James VN, Ramos A, Sullivan ST, Siddig A, et al. (2004) In vitro comparison of topical microbicides for prevention of human immunodeficiency virus type 1 transmission. Antimicrob Agents Chemother 48: 3834-3844.
35. Abner SR, Guenthner PC, Guarner J, Hancock KA, Cummins JE Jr, et al. (2005) A human colorectal explant culture to evaluate topical microbicides for the prevention of HIV infection. J Infect Dis 192: 1545-1556.
36. Telwatte S, Moore K, Johnson A, Tyssen D, Sterjovski J, et al. (2011) Virucidal activity of the dendrimer microbicide SPL7013 against HIV-1. Antiviral Res 90: 195-199.
37. Jiang YH, Emau P, Cairns JS, Flanary L, Morton WR, et al. (2005) SPL7013 gel as a topical microbicide for prevention of vaginal transmission of SHIV89.6P in macaques. AIDS Res Hum Retroviruses 21: 207-213.
38. Pini A, Giuliani A, Falciani C, Runci Y, Ricci C, et al. (2005) Antimicrobial activity of novel dendrimeric peptides obtained by phage display selection and rational modification. Antimicrob Agents Chemother 49: 2665-2672.
39. Luganini A, Giuliani A, Pirri G, Pizzuto L, Landolfo S, et al. (2010) Peptide-derivatized dendrimers inhibit human cytomegalovirus infection by blocking virus binding to cell surface heparan sulfate. Antiviral Res 85: 532-540.
40. Donalisio M, Rusnati M, Civra A, Bugatti A, Allemand D, et al. (2010) Identification of a dendrimeric heparan sulfate-binding peptide that inhibits infectivity of genital types of human papillomaviruses. Antimicrob Agents Chemother 54: 4290-4299.
41. Donalisio M, Rusnati M, Cagno V, Civra A, Bugatti A, et al. (2012) Inhibition of human respiratory syncytial virus infectivity by a dendrimeric heparan sulfate-binding peptide. Antimicrob Agents Chemother 56: 5278-5288.
42. Gartner S, Popovic M (1990) Virus Isolation and production. In AldoviniA, WalkerBD. Editors.HIV techniques, Stockton Press NY pp 53-69.
43. Svicher V, D′Arrigo R, Alteri C, Andreoni M, Angarano G, et al. (2010) Performance of genotypic tropism testing in clinical practice using the enhanced sensitivity version of Trofile as reference assay, results from the OSCAR Study Group. New Microbiol 33: 195-206.
44. Tyagi M, Rusnati M, Presta M, Giacca M, (2001) Internalization of HIV-1 Tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276: 3254-3261.
45. Gibellini D, Vitone F, Gori E, La Placa M, Re MC, (2004) Quantitative detection of human immunodeficiency virus type 1 (HIV-1) viral load by SYBR green real-time RT-PCR technique in HIV-1 seropositive patients. J Virol Meth 115: 183-189.
46. Gibellini D, Vitone F, Schiavone P, Ponti C, La Placa M, et al. (2004) Quantitative detection of human immunodeficiency virus type 1 (HIV-1) proviral DNA in peripheral blood mononuclear cells by SYBR green real-time PCR technique. J Clin Virol 29: 282-289.
47. Mondor I, Ugolini S, Sattentau QJ, (1998) Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J Virol 72: 3623-3634.
48. Moulard M, Lortat-Jacob H, Mondor I, Roca G, Wyatt R, et al. (2000) Selective interactions of polyanions with basic surfaces on human immunodeficiency virus type 1 gp120. J Virol 74: 1948-1960.
49. Tilton JC, Doms RW, (2010) Entry inhibitors in the treatment of HIV-1 infection. Antivir Res 85: 91-100.
50. Sattentau QJ, Moore JP, Vignaux F, Traincard F, Poignard P, (1993) Conformational changes induced in the envelope glycoproteins of the human and simian immunodeficiency viruses by soluble receptor binding. J Virol 67: 7383-7393.
51. Wyatt R, Moore J, Accola M, Desjardin E, Robinson J, et al. (1995) Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J Virol 69: 5723-5733.
52. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
53. Rizzuto CD, Wyatt R, Hernández-Ramos N, Sun Y, Kwong PD, et al. (1998) A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280: 1949-1953.
54. Basmaciogullari S, Babcock GJ, Van Ryk D, Wojtowicz W, Sodroski J, (2002) Identification of conserved and variable structures in the human immunodeficiency virus gp120 glycoprotein of importance for CXCR4 binding. J Virol 76: 10791-10800.
55. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, Wiley DC, (1997) Atomic structure of the ectodomain from HIV-1 gp41. Nature 387: 426-430.
56. Liu S, Wu S, Jiang S, Liu S, Wu S, et al. (2007) HIV entry inhibitors targeting gp41, from polypeptides to small-molecule compounds. Curr Pharm Des 13: 143-162.
57. Chang DK, Chang-Sheng Hsu CS, (2007) Biophysical evidence of two docking sites of the carboxyl heptad repeat region within the amino heptad repeat region of gp41 of human immunodeficiency virus type 1. Antivir Res 74: 51-58.
58. Blumenthal R, Durell S, Viard M, (2012) HIV entry and envelope glycoprotein-mediated fusion. J Biol Chem 287: 40841-40849.
59. Kilby JM, Lalezari JP, Eron JJ, Carlson M, Cohen C, et al. (2002) The safety, plasma pharmacokinetics, and antiviral activity of subcutaneous enfuvirtide (T-20), a peptide inhibitor of gp41-mediated virus fusion, in HIV-infected adults. AIDS Res Hum Retroviruses 18: 685-693.
60. Lalezari JP, Eron JJ, Carlson M, Cohen C, DeJesus E, et al. (2003) A phase II clinical study of the long-term safety and antiviral activity of enfuvirtide-based antiretroviral therapy. AIDS 17: 691-698.
61. Wild C, Greenwell T, Matthews T, (1993) A synthetic peptide from HIV-1 gp41 is a potent inhibitor of virus-medated cell-cell fusion. AIDS Res Hum Retroviruses 9: 1051-1053.
62. Pang W, Wang RR, Yang LM, Liu CM, Tien P, et al. (2008) Recombinant protein of heptad-repeat HR212, a stable fusion inhibitor with potent anti-HIV action in vitro. Virology 377: 80-87.
63. Cai L, Jiang S, (2010) Development of peptide and small-molecule HIV-1 fusion inhibitors that target gp41. Chem Med Chem. 5: 1813-1824.
64. Cole AL, Yang OO, Warren AD, Waring AJ, Lehrer RI, et al. (2006) HIV-1 adapts to a retrocyclin with cationic amino acid substitutions that reduce fusion efficiency of gp41. J Immunol 176: 6900-6905.
65. Cole AL, Herasimtschuk A, Gupta P, Waring AJ, Lehrer RI, et al. (2007) The retrocyclin analogue RC-101 prevents human immunodeficiency virus type 1 infection of a model human cervicovaginal tissue construct. Immunology 121: 140-145.
66. Hansen JE, Nielsen CM, Nielsen C, Heegaard P, Mathiesen LR, et al. (1989) Correlation between carbohydrate structures on the envelope glycoprotein gp120 of HIV-1 and HIV-2 and syncytium inhibition with lectins. AIDS 3: 635-641.
67. Balzarini J, Schols D, Neyts J, Van Damme E, Peumans W, et al. (1991) Alpha-(1-3)- and alpha-(1-6)-D-mannose-specific plant lectins are markedly inhibitory to human immunodeficiency virus and cytomegalovirus infections in vitro. Antimicrob. Agents Chemother 35: 410-416.
68. Calarese DA, Scanlan CN, Zwick MB, Deechongkit S, Mimura Y, et al. (2003) Antibody domain exchange is an immunological solution tocarbohydrate cluster recognition. Science 300: 2065-2071.
69. Tsai CC, Emau P, Jiang Y, Tian B, Morton WR, et al. (2003) Cyanovirin-N gel as a topical microbicide prevents rectal transmission of SHIV89.6P in macaques. AIDS Res Hum Retroviruses. 19: 535-541.
70. Mori T, O′Keefe BR, Sowder RC 2nd, Bringans S, Gardella R, et al. (2005) Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp. J Biol Chem 280: 9345-9553.
71. Huskens D, Vermeire K, Profy AT, Schols D, (2009) The candidate sulfonated microbicide, PRO 2000, has potential multiple mechanisms of action against HIV-1. Antiviral Res 84: 38-47.
72. Cummins JE Jr, Guarner J, Flowers L, Guenthner PC, Bartlett J, et al. (2007) Preclinical testing of candidate topical microbicides for anti-human immunodeficiency virus type 1 activity and tissue toxicity in a human cervical explant culture. Antimicrob Agents Chemother 5: 521770-1779.
73. Lackman-Smith C, Osterling C, Luckenbaugh K, Mankowski M. Snyder B, et al. (2008) Development of a comprehensive human immunodeficiency virus type 1 screening algorithm for discovery and preclinical testing of topical microbicides. Antimicrob Agents Chemother 52: 1768-1781.
74. Tyssen D. Henderson SA, Johnson A, Sterjovski J, Moore K, et al. (2010) Structure activity relationship of dendrimer microbicides with dual action antiviral activity. PLoS ONE 5: e12309.
75. Asaftei S, Huskens D, Schols D (2012) HIV-1 X4 activities of polycationic "Viologen" based dendrimers by interaction with the chemokine receptor CXCR4, study of structure-activity relationship. J. Med. Chem. 55, 10405-10413.
76. Roan NR, Münch J, Arhel N, Mothes W, Neidleman J, et al. (2009) The cationic properties of SEVI underlie its ability to enhance human immunodeficiency virus infection. J Virol 83: 73-80.
77. Salvador B, Sexton NR, Carrion R Jr, Nunneley J, Patterson JL, et al. (2013) Filoviruses utilize glycosaminoglycans for their attachment to target cells. J Virol 87: 3295-3304.
78. Sarrazin S, Lamanna WC, Esko JD, (2011) Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 3: 7.
79. Spillmann D, (2001) Heparan sulfate, anchor for viral intruders? Biochimie 83: 811-817.
80. Shieh MT, Dunn DW, Montgomery RI, Esko JD, Spear PG, (1992) Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol 116: 1273-1281.
81. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M, (2001) Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75: 1565-1570.
82. Feldman SA, Audet S, Beeler JA, (2000) The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. J Virol 74: 6442-6447.
83. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, et al. (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003 278: 41003-41012.
84. Chen Y, Maguire T, Hileman RE, Fromm JR, Esko J, et al. (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3: 866-871.
85. Jones KS, Petrow-Sadowski C, Bertolette DC, Huang Y, Ruscetti FW, (2005) Heparan sulfate proteoglycans mediate attachment and entry of human T-cell leukemia virus type 1 virions into CD4+ T cells. J Virol 79: 12692-12702.
86. Patel M, Yanagishita M, Roderiquez G, Bou-Habib DC, Oravecz T, et al. (1993) Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T-cell lines. AIDS Res Hum Retroviruses 9: 167-174.
87. Ugolini S, Mondor I, Sattentau QJ, (1997) HIV-1 attachment, another look. Trends Microbiol 7: 144-149.
88. Vivès RR, Imberty A, Sattentau QJ, Lortat-Jacob H, (2005) Heparan sulfate targets the HIV-1 envelope glycoprotein gp120 coreceptor binding site. J Biol Chem 280: 21353-21357.
89. Roderiquez G, Oravecz T, Yanagishita M, Bou-Habib DC, Mostowski H, et al. (1995) Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp120-gp41. J Virol 69: 2233-2239.
90. Ohshiro Y. Murakami T, Matsuda K, Nishioka K, Yoshida K, et al. (1996) Role of cell surface glycosaminoglycans of human T cells in human immunodeficiency virus type-1 (HIV-1) infection. Microbiol Immunol 40: 827-835.
91. Mondor I, Ugolini S, Sattentau QJ, (1998) Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J Virol 72: 3623-3634.
92. Saphire ACS, Bobardt MD, Zhang Z, David G, Gallay PA, (2001) Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J Virol 75: 9187-9200.
93. Argyris EG, Acheampong E, Nunnari G, Mukhtar M, Williams KJ, et al. (2003) Human immunodeficiency virus type 1 enters primary human brain microvascular endothelial cells by a mechanism involving cell surface proteoglycans independent of lipid rafts. J Virol 77: 12140-12151.
94. Cladera J, Martin I, O′Shea P, (2001) The fusion domain of HIV gp41 interacts specifically with heparan sulfate on the T-lymphocyte cell surface. EMBO J 20: 19-26.
95. Abraham BK, Gulick R, (2012) Next-generation oral preexposure prophylaxis, beyond tenofovir Curr Opin HIV AIDS. 7: 600-606.
96. Baeten JM, Donnell D, Ndase P, (2012) Partners PrEP Study Team. Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med 367: 399-410.