P2X-selective purinergic antagonists are strong inhibitors of HIV-1 fusion during both cell-to-cell and cell-free infection

Journal of Virology

Volumn 88, Issue 19, 2014, Pages 11504-11515

  Swartz, Talia H ^a   Esposito, Anthony M ^a   Durham, Natasha D ^a   Hartmann, Boris M ^a   Chen, Benjamin K ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE RECEPTOR BLOCKING AGENT; CHEMOKINE RECEPTOR CXCR4; GAG PROTEIN; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2Y RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR5; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; PURINERGIC RECEPTOR BLOCKING AGENT;

ARTICLE; CD4+ T LYMPHOCYTE; CELL INTERACTION; CELL TRANSFER; CONTROLLED STUDY; DOSE RESPONSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INTERNALIZATION; LYMPHOCYTE; NONHUMAN; PROTEIN LOCALIZATION; TARGET CELL; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS TRANSMISSION; CELL FUSION; CELL LINE; DRUG EFFECT; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; STRUCTURE ACTIVITY RELATION; VIRION; VIROLOGY; VIRUS REPLICATION;

CD4-POSITIVE T-LYMPHOCYTES; CELL FUSION; CELL LINE; HEK293 CELLS; HIV FUSION INHIBITORS; HIV-1; HUMANS; PURINERGIC ANTAGONISTS; RECEPTORS, CCR5; RECEPTORS, CXCR4; RECEPTORS, PURINERGIC P2X; STRUCTURE-ACTIVITY RELATIONSHIP; VIRION; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84906990853     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01158-14     Document Type: Article

References (67)

1. Guaraldi G, Orlando G, Zona S, Menozzi M, Carli F, Garlassi E, Berti A, Rossi E, Roverato A, Palella F. 2011. Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin. Infect. Dis. 53:1120-1126. http://dx.doi.org/10.1093/cid/cir627.
2. Ofotokun I, McIntosh E, Weitzmann MN. 2012. HIV: inflammation and bone. Curr. HIV/AIDS Rep. 9:16-25. http://dx.doi.org/10.1007/s11904 -011-0099-z.
3. Sigel K, Dubrow R, Silverberg M, Crothers K, Braithwaite S, Justice A. 2011 Cancer screening in patients infected with HIV. Curr. HIV/AIDS Rep. 8:142-152. http://dx.doi.org/10.1007/s11904-011-0085-5.
4. Hunt PW, Sinclair E, Rodriguez B, Shive C, Clagett B, Funderburg N, Robinson J, Huang Y, Epling L, Martin JN, Deeks SG, Meinert CL, Van Natta ML, Jabs DA, Lederman MM. 21 April 2014. Gut epithelial barrier dysfunction and innate immune activation predict mortality in treated HIV infection. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jiu238.
5. Belete HA, Hubmayr RD, Wang S, Singh RD. 2011. The role of purinergic signaling on deformation induced injury and repair responses of alveolar epithelial cells. PLoS One 6:e27469. http://dx.doi.org/10.1371 /journal.pone.0027469.
6. Busillo JM, Azzam KM, Cidlowski JA. 2011. Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J. Biol. Chem. 286:38703-38713. http://dx.doi.org/10.1074/jbc .M111.275370.
7. Deli T, Csernoch L. 2008. Extracellular ATP and cancer: an overview with special reference to P2 purinergic receptors. Pathol. Oncol. Res. 14:219-231. http://dx.doi.org/10.1007/s12253-008-9071-7.
8. McIlvain HB, Ma L, Ludwig B, Manners MT, Martone RL, Dunlop J, Kaftan EJ, Kennedy JD, Whiteside GT. 2010. Purinergic receptormediated morphological changes in microglia are transient and independent from inflammatory cytokine release. Eur. J. Pharmacol. 643:202-210. http://dx.doi.org/10.1016/j.ejphar.2010.06.046.
9. Pillai S, Bikle DD. 1992. Adenosine triphosphate stimulates phosphoinositie metabolism, mobilizes intracellular calcium, and inhibits terminal differentiation of human epidermal keratinocytes. J. Clin. Invest. 90:42-51. http://dx.doi.org/10.1172/JCI115854.
10. Reigada D, Lu W, Zhang M, Mitchell CH. 2008. Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 157:396-404. http://dx.doi.org /10.1016/j.neuroscience.2008.08.036.
11. Paoletti A, Raza SQ, Voisin L, Law F, Pipoli da Fonseca J, Caillet M, Kroemer G, Perfettini JL. 2012. Multifaceted roles of purinergic receptors in viral infection. Microbes Infect. 14:1278-1283. http://dx.doi.org/10 .1016/j.micinf.2012.05.010.
12. Se´ror C, Melki MT, Subra F, Raza SQ, Bras M, Saidi H, Nardacci R, Voisin L, Paoletti A, Law F, Martins I, Amendola A, Abdul-Sater AA, Ciccosanti F, Delelis O, Niedergang F, Thierry S, Said-Sadier N, Lamaze C, Metivier D, Estaquier J, Fimia GM, Falasca L, Casetti R, Modjtahedi N, Kanellopoulos J, Mouscadet JF, Ojcius DM, Piacentini M, Gougeon ML, Kroemer G, Perfettini JL. 2011. Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J. Exp. Med. 208:1823-1834. http://dx.doi.org/10.1084/jem.20101805.
13. Blanco J, Bosch B, Fernandez-Figueras MT, Barretina J, Clotet B, Este JA. 2004. High level of coreceptor-independent HIV transfer induced by contacts between primary CD4 T cells. J. Biol. Chem. 279:51305-51314. http://dx.doi.org/10.1074/jbc.M408547200.
14. Chen P, Hubner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595. http://dx.doi.org/10.1128/JVI.00381-07.
15. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293. http://dx.doi.org/10.1084/jem.20030648.
16. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FY, Li XD, Asmuth DM, Huser T, Chen BK. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747. http://dx.doi.org/10.1126/science.1167525.
17. Durham ND, Yewdall AW, Chen P, Lee R, Zony C, Robinson JE, Chen BK. 2012. Neutralization resistance of virological synapse-mediated HIV-1 infection is regulated by the gp41 cytoplasmic tail. J. Virol. 86: 7484-7495. http://dx.doi.org/10.1128/JVI.00230-12.
18. Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, Baltimore D. 2011 Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature 477:95-98. http://dx.doi.org/10.1038 /nature10347.
19. Agosto LM, Zhong P, Munro J, Mothes W. 2014. Highly active antiretroviral therapies are effective against HIV-1 cell-to-cell transmission. PLoS Pathog. 10:e1003982. http://dx.doi.org/10.1371/journal.ppat.1003982.
20. Jolly C, Mitar I, Sattentau QJ. 2007. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J. Virol. 81:13916-13921. http://dx.doi .org/10.1128/JVI.01585-07.
21. Hazleton JE, Berman JW, Eugenin EA. 2012. Purinergic receptors are required for HIV-1 infection of primary human macrophages. J. Immunol. 188:4488-4495. http://dx.doi.org/10.4049/jimmunol.1102482.
22. Orellana JA, Velasquez S, Williams DW, Saez JC, Berman JW, Eugenin EA. 2013. Pannexin1 hemichannels are critical for HIV infection of human primary CD4± T lymphocytes. J. Leukoc. Biol. 94:399-407. http: //dx.doi.org/10.1189/jlb.0512249.
23. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661-671. http://dx.doi.org/10.1016/S1074-7613 (00)80065-5.
24. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM, Bilska M, Kothe DL, Salazar-Gonzalez JF, Wei X, Decker JM, Hahn BH, Montefiori DC. 2005 Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125. http://dx.doi.org/10 .1128/JVI.79.16.10108-10125.2005.
25. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
26. Dale BM, McNerney GP, Thompson DL, Hubner W, de Los Reyes K, Chuang FY, Huser T, Chen BK. 2011. Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host Microbe 10:551-562. http://dx.doi.org /10.1016/j.chom.2011.10.015.
27. Koo BK, Stange DE, Sato T, Karthaus W, Farin HF, Huch M, van Es JH, Clevers H. 2012. Controlled gene expression in primary Lgr5 organoid cultures. Nat. Methods 9:81-83. http://dx.doi.org/10.1038/nchembio .1138.
28. Cavrois M, De Noronha C, Greene WC. 2002. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat. Biotechnol. 20:1151-1154. http://dx.doi.org/10.1038/nbt745.
29. Barat C, Gilbert C, Imbeault M, Tremblay MJ. 2008. Extracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4± T lymphocytes. Retrovirology 5:30. http://dx.doi.org/10.1186/1742-4690-5-30.
30. Blanco J, Barretina J, Henson G, Bridger G, De Clercq E, Clotet B, Este JA. 2000. The CXCR4 antagonist AMD3100 efficiently inhibits cellsurface-expressed human immunodeficiency virus type 1 envelopeinduced apoptosis. Antimicrob. Agents Chemother. 44:51-56. http://dx .doi.org/10.1128/AAC.44.1.51-56.2000.
31. Tovar-y-Romo LB, Kolson DL, Bandaru VV, Drewes JL, Graham DR, Haughey NJ. 2013. Adenosine triphosphate released from HIV-infected macrophages regulates glutamatergic tone and dendritic spine density on neurons. J. Neuroimmune Pharmacol. 8:998-1009. http://dx.doi.org/10 .1007/s11481-013-9471-7.
32. Eugenin EA. 2014. Role of connexin/pannexin containing channels in infectious diseases. FEBS Lett. 588:1389-1395. http://dx.doi.org/10.1016 /j.febslet.2014.01.030.
33. Velasquez S, Eugenin EA. 2014. Role of pannexin-1 hemichannels and purinergic receptors in the pathogenesis of human diseases. Front. Physiol. 5:96.
34. Gunosewoyo H, Kassiou M. 2010. P2X purinergic receptor ligands: recently patented compounds. Expert Opin. Ther. Patents 20:625-646. http: //dx.doi.org/10.1517/13543771003702424.
35. Gum RJ, Wakefield B, Jarvis MF. 2012. P2X receptor antagonists for pain management: examination of binding and physicochemical properties. Purinergic Signal. 8:41-56. http://dx.doi.org/10.1007/s11302-011-9272-5.
36. De Clercq E. 1979. Suramin: a potent inhibitor of the reverse transcriptase of RNA tumor viruses. Cancer Lett. 8:9-22. http://dx.doi.org/10.1016 /0304-3835(79)90017-X.
37. De Clercq E. 1987. Suramin in the treatment of AIDS: mechanism of action. Antiviral Res. 7:1-10. http://dx.doi.org/10.1016/0166-3542(87) 90034-9.
38. Riteau N, Baron L, Villeret B, Guillou N, Savigny F, Ryffel B, Rassendren F, Le Bert M, Gombault A, Couillin I. 2012. ATP release and purinergic signaling: a common pathway for particle-mediated inflammasome activation. Cell Death Dis. 3:e403. http://dx.doi.org/10.1038 /cddis.2012.144.
39. Riteau N, Gasse P, Fauconnier L, Gombault A, Couegnat M, Fick L, Kanellopoulos J, Quesniaux VF, Marchand-Adam S, Crestani B, Ryffel B, Couillin I. 2010. Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 182:774-783. http://dx.doi.org/10.1164/rccm.201003-0359OC.
40. Wang Q, Imamura R, Motani K, Kushiyama H, Nagata S, Suda T. 2013. Pyroptotic cells externalize eat-me and release find-me signals and are efficiently engulfed by macrophages. Int. Immunol. 25:363-372. http://dx .doi.org/10.1093/intimm/dxs161.
41. Gombault A, Baron L, Couillin I. 2012. ATP release and purinergic signaling in NLRP3 inflammasome activation. Front. Immunol. 3:414. http://dx.doi.org/10.3389/fimmu.2012.00414.
42. Eltom S, Stevenson CS, Rastrick J, Dale N, Raemdonck K, Wong S, Catley MC, Belvisi MG, Birrell MA. 2011. P2X7 receptor and caspase 1 activation are central to airway inflammation observed after exposure to tobacco smoke. PLoS One 6:e24097. http://dx.doi.org/10.1371/journal .pone.0024097.
43. + for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 282:18810-18818. http://dx.doi.org/10.1074/jbc.M610762200.
44. Harder J, Franchi L, Munoz-Planillo R, Park JH, Reimer T, Nunez G. 2009 Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-kappa B activation but proceeds independently of TLR signaling and P2X7 receptor. J. Immunol. 183:5823-5829. http://dx.doi.org/10.4049/jimmunol.0900444.
45. Jorgensen NR, Husted LB, Skarratt KK, Stokes L, Tofteng CL, Kvist T, Jensen JE, Eiken P, Brixen K, Fuller S, Clifton-Bligh R, Gartland A, Schwarz P, Langdahl BL, Wiley JS. 2012. Single-nucleotide polymorphisms in the P2X7 receptor gene are associated with post-menopausal bone loss and vertebral fractures. Eur. J. Hum. Genet. 20:675-681. http: //dx.doi.org/10.1038/ejhg.2011.253.
46. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, Santiago ML, Hebbeler AM, Greene WC. 2010. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143: 789-801. http://dx.doi.org/10.1016/j.cell.2010.11.001.
47. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, Hunt PW, Hatano H, Sowinski S, Munoz-Arias I, Greene WC. 2014. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505:509-514. http://dx.doi.org/10.1038/nature12940.
48. Ali Z, Laurijssens B, Ostenfeld T, McHugh S, Stylianou A, Scott-Stevens P, Hosking L, Dewit O, Richardson JC, Chen C. 2013. Pharmacokinetic and pharmacodynamic profiling of a P2X7 receptor allosteric modulator GSK1482160 in healthy human subjects. Br. J. Clin. Pharmacol. 75:197-207. http://dx.doi.org/10.1111/j.1365-2125.2012.04320.x.
49. Stock TC, Bloom BJ, Wei N, Ishaq S, Park W, Wang X, Gupta P, Mebus CA. 2012. Efficacy and safety of CE-224,535, an antagonist of P2X7 receptor, in treatment of patients with rheumatoid arthritis inadequately controlled by methotrexate. J. Rheumatol. 39:720-727. http://dx.doi.org/10 .3899/jrheum.110874.
50. Elsby R, Fox L, Stresser D, Layton M, Butters C, Sharma P, Smith V, Surry D. 2011. In vitro risk assessment of AZD9056 perpetrating a transporter-mediated drug-drug interaction with methotrexate. Eur. J. Pharm. Sci. 43:41-49. http://dx.doi.org/10.1016/j.ejps.2011.03.006.
51. Keystone EC, Wang MM, Layton M, Hollis S, McInnes IB, D1520C00001 Study Team. 2012. Clinical evaluation of the efficacy of the P2X7 purinergic receptor antagonist AZD9056 on the signs and symptoms of rheumatoid arthritis in patients with active disease despite treatment with methotrexate or sulphasalazine. Ann. Rheum. Dis. 71:1630-1635. http: //dx.doi.org/10.1136/annrheumdis-2011-143578.
52. Wagner MC. 2011. The therapeutic potential of adenosine triphosphate as an immune modulator in the treatment of HIV/AIDS: a combination approach with HAART. Curr. HIV Res. 9:209-222. http://dx.doi.org/10 .2174/157016211796320289.
53. Sorrell ME, Hauser KF. 2014. Ligand-gated purinergic receptors regulate HIV-1 Tat and morphine related neurotoxicity in primary mouse striatal neuron-glia co-cultures. J. Neuroimmune Pharmacol. 9:233-244. http: //dx.doi.org/10.1007/s11481-013-9507-z.
54. Damer S, Niebel B, Czeche S, Nickel P, Ardanuy U, Schmalzing G, Rettinger J, Mutschler E, Lambrecht G. 1998. NF279: a novel potent and selective antagonist of P2X receptor-mediated responses. Eur. J. Pharmacol. 350:R5-R6. http://dx.doi.org/10.1016/S0014-2999(98)00316-1.
55. Klapperstuck M, Buttner C, Nickel P, Schmalzing G, Lambrecht G, Markwardt F. 2000. Antagonism by the suramin analogue NF279 on human P2X(1) and P2X(7) receptors. Eur. J. Pharmacol. 387:245-252. http://dx.doi.org/10.1016/S0014-2999(99)00826-2.
56. Rettinger J, Schmalzing G, Damer S, Muller G, Nickel P, Lambrecht G.2000 The suramin analogue NF279 is a novel and potent antagonist selective for the P2X(1) receptor. Neuropharmacology 39:2044-2053. http: //dx.doi.org/10.1016/S0028-3908(00)00022-8.
57. Busch W, Brodt R, Ganser A, Helm EB, Stille W. 1985. Suramin treatment for AIDS. Lancet ii:1247.
58. Kaplan LD, Wolfe PR, Volberding PA, Feorino P, Levy JA, Abrams DI, Kiprov D, Wong R, Kaufman L, Gottlieb MS. 1987. Lack of response to suramin in patients with AIDS and AIDS-related complex. Am. J. Med. 82:615-620. http://dx.doi.org/10.1016/0002-9343(87)90108-2.
59. Hui EK, Nayak DP. 2002. Role of G protein and protein kinase signalling in influenza virus budding in MDCK cells. J. Gen. Virol. 83:3055-3066.
60. Croci R, Tarantino D, Milani M, Pezzullo M, Rohayem J, Bolognesi M, Mastrangelo E. 2014. PPNDS inhibits murine norovirus RNA-dependent RNA-polymerase mimicking two RNA stacking bases. FEBS Lett. 588: 1720-1725. http://dx.doi.org/10.1016/j.febslet.2014.03.021.
61. Lambrecht G, Rettinger J, Baumert HG, Czeche S, Damer S, Ganso M, Hildebrandt C, Niebel B, Spatz-Kumbel G, Schmalzing G, Mutschler E. 2000. The novel pyridoxal-5′-phosphate derivative PPNDS potently antagonizes activation of P2X(1) receptors. Eur. J. Pharmacol. 387:R19-R21. http://dx.doi.org/10.1016/S0014-2999(99)00834-1.
62. Suzuki E, Kessler M, Montgomery K, Arai AC. 2004. Divergent effects of the purinoceptor antagonists suramin and pyridoxal-5′-phosphate-6-(2′-naphthylazo-6′-nitro-4′,8′-disulfonate) (PPNDS) on alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors. Mol. Pharmacol. 66:1738-1747. http://dx.doi.org/10.1124/mol.104.003038.
63. Wood CR, Hennessey TM. 2003. PPNDS is an agonist, not an antagonist, for the ATP receptor of Paramecium. J. Exp. Biol. 206:627-636. http://dx .doi.org/10.1242/jeb.00105.
64. Soto F, Lambrecht G, Nickel P, Stuhmer W, Busch AE. 1999. Antagonistic properties of the suramin analogue NF023 at heterologously expressed P2X receptors. Neuropharmacology 38:141-149. http://dx.doi .org/10.1016/S0028-3908(98)00158-0.
65. Ziyal R, Ziganshin AU, Nickel P, Ardanuy U, Mutschler E, Lambrecht G, Burnstock G. 1997. Vasoconstrictor responses via P2X-receptors are selectively antagonized by NF023 in rabbit isolated aorta and saphenous artery. Br. J. Pharmacol. 120:954-960. http://dx.doi.org/10.1038/sj.bjp .0700984.
66. Borsani E, Albertini R, Colleoni M, Sacerdote P, Trovato AE, Lonati C, Labanca M, Panerai AE, Rezzani R, Rodella LF. 2008. PPADS, a purinergic antagonist reduces Fos expression at spinal cord level in a mouse model of mononeuropathy. Brain Res. 1199:74-81. http://dx.doi.org/10 .1016/j.brainres.2007.12.066.
67. Martucci C, Trovato AE, Costa B, Borsani E, Franchi S, Magnaghi V, Panerai AE, Rodella LF, Valsecchi AE, Sacerdote P, Colleoni M. 2008. The purinergic antagonist PPADS reduces pain related behaviours and interleukin-1 beta, interleukin-6, iNOS and nNOS overproduction in central and peripheral nervous system after peripheral neuropathy in mice. Pain 137:81-95. http://dx.doi.org/10.1016/j.pain.2007.08.017.