Staphylococcus aureus leukocidin LukED and HIV-1 gp120 target different sequence determinants on CCR5

mBio

Volumn 7, Issue 6, 2016, Pages

  Tam, Kayan ^a   Schultz, Megan ^a   Reyes Robles, Tamara ^a   Vanwalscappel, Bénédicte ^a   Horton, Joshua ^a   Alonzo, Francis ^a   Wu, Beili ^b   Landau, Nathaniel R ^a   Torres, Victor J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; LEUKOCIDIN; STAPHYLOCOCCUS TOXIN; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR; BACTERIAL PROTEIN; EXOTOXIN; LUKD PROTEIN, STAPHYLOCOCCUS AUREUS; LUKE PROTEIN, STAPHYLOCOCCUS AUREUS;

ARTICLE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LETHALITY; MOLECULAR INTERACTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN TARGETING; RECEPTOR BINDING; STAPHYLOCOCCUS AUREUS; VIRUS ENTRY; VIRUS INFECTIVITY; CHEMISTRY; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY;

BACTERIAL PROTEINS; EXOTOXINS; HEK293 CELLS; HIV ENVELOPE PROTEIN GP120; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; LEUKOCIDINS; POINT MUTATION; RECEPTORS, CCR5; STAPHYLOCOCCUS AUREUS; VIRUS INTERNALIZATION;

EID: 85007564155     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02024-16     Document Type: Article

References (51)

1. Dantes R, Mu Y, Belflower R, Aragon D, Dumyati G, Harrison LH, Lessa FC, Lynfield R, Nadle J, Petit S, Ray SM, Schaffner W, Townes J, Fridkin S, Emerging Infections Program-Active Bacterial Core Surveillance MSI. 2013. National burden of invasive methicillin-resistant Staphylococcus aureus infections, United States, 2011. JAMA Intern Med 173: 1970-1978. http://dx.doi.org/10.1001/jamainternmed.2013.10423.
2. David MZ, Daum RS. 2010. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616-687. http://dx.doi.org/10.1128/CMR.00081-09.
3. CDC. 2015. Prevalence of diagnosed and undiagnosed HIV infection-United States, 2008-2012. MMWR Morb Mortal Wkly Rep 64: 657-662.
4. UNAIDS. 2016, Global AIDS update. UNAIDS report.
5. Alonzo F, III, Kozhaya L, Rawlings SA, Reyes-Robles T, DuMont AL, Myszka DG, Landau NR, Unutmaz D, Torres VJ. 2013. CCR5 is a receptor for Staphylococcus aureus leukotoxin ED. Nature 493: 51-55. http://dx.doi.org/10.1038/nature11724.
6. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381: 661-666. http://dx.doi.org/10.1038/381661a0.
7. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA. 1996. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
8. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J. 1996. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85: 1135-1148. http://dx.doi.org/10.1016/ S0092-8674(00)81313-6.
9. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85: 1149-1158. http://dx.doi.org/10.1016/S0092-8674(00)81314-8.
10. + cells is mediated by the chemokine receptor CC-CKR-5. Nature 381: 667-673. http://dx.doi.org/10.1038/381667a0.
11. Miller MA, Cloyd MW, Liebmann J, Rinaldo CR, Jr, Islam KR, Wang SZ, Mietzner TA, Montelaro RC. 1993. Alterations in cell membrane permeability by the lentivirus lytic peptide (LLP-1) of HIV-1 transmembrane protein. Virology 196: 89-100. http://dx.doi.org/10.1006/ viro.1993.1457.
12. Srinivas SK, Srinivas RV, Anantharamaiah GM, Segrest JP, Compans RW. 1992. Membrane interactions of synthetic peptides corresponding to amphipathic helical segments of the human immunodeficiency virus type-1 envelope glycoprotein. J Biol Chem 267: 7121-7127.
13. Rizzuto CD, Wyatt R, Hernández-Ramos N, Sun Y, Kwong PD, Hendrickson WA, Sodroski J. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280: 1949-1953. http://dx.doi.org/10.1126/science.280.5371.1949.
14. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M. 1996. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382: 722-725. http://dx.doi.org/10.1038/382722a0.
15. Rucker J, Samson M, Doranz BJ, Libert F, Berson JF, Yi Y, Smyth RJ, Collman RG, Broder CC, Vassart G, Doms RW, Parmentier M. 1996. Regions in beta-chemokine receptors CCR5 and CCR2b that determine HIV-1 cofactor specificity. Cell 87: 437-446. http://dx.doi.org/10.1016/ S0092-8674(00)81364-1.
16. Samson M, LaRosa G, Libert F, Paindavoine P, Detheux M, Vassart G, Parmentier M. 1997. The second extracellular loop of CCR5 is the major determinant of ligand specificity. J Biol Chem 272: 24934-24941. http:// dx.doi.org/10.1074/jbc.272.40.24934.
17. Blanpain C, Doranz BJ, Bondue A, Govaerts C, De Leener A, Vassart G, Doms RW, Proudfoot A, Parmentier M. 2003. The core domain of chemokines binds CCR5 extracellular domains while their amino terminus interacts with the transmembrane helix bundle. J Biol Chem 278: 5179-5187. http://dx.doi.org/10.1074/jbc.M205684200.
18. Maeda K, Das D, Ogata-Aoki H, Nakata H, Miyakawa T, Tojo Y, Norman R, Takaoka Y, Ding J, Arnold GF, Arnold E, Mitsuya H. 2006. Structural and molecular interactions of CCR5 inhibitors with CCR5. J Biol Chem 281: 12688-12698. http://dx.doi.org/10.1074/jbc .M512688200.
19. Reyes-Robles T, Lubkin A, Alonzo F, III, Lacy DB, Torres VJ. 2016. Exploiting dominant-negative toxins to combat Staphylococcus aureus pathogenesis. EMBO Rep 17: 428-440. http://dx.doi.org/10.15252/ embr.201540994.
20. Maeda K, Das D, Yin PD, Tsuchiya K, Ogata-Aoki H, Nakata H, Norman RB, Hackney LA, Takaoka Y, Mitsuya H. 2008. Involvement of the second extracellular loop and transmembrane residues of CCR5 in inhibitor binding and HIV-1 fusion: insights into the mechanism of allosteric inhibition. J Mol Biol 381: 956-974. http://dx.doi.org/10.1016/ j.jmb.2008.06.041.
21. Königs C, Pustowka A, Irving J, Kessel C, Klich K, Wegner V, Rowley MJ, Mackay IR, Kreuz W, Griesinger C, Dietrich U. 2007. Peptide mimotopes selected with HIV-1-blocking monoclonal antibodies against CCR5 represent motifs specific for HIV-1 entry. Immunol Cell Biol 85: 511-517. http://dx.doi.org/10.1038/sj.icb.7100077.
22. Dorr P, Westby M, Dobbs S, Griffin P, Irvine B, Macartney M, Mori J, Rickett G, Smith-Burchnell C, Napier C, Webster R, Armour D, Price D, Stammen B, Wood A, Perros M. 2005. 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 49: 4721-4732. http://dx.doi.org/10.1128/AAC.49.11.4721-4732.2005.
23. Tan Q, Zhu Y, Li J, Chen Z, Han GW, Kufareva I, Li T, Ma L, Fenalti G, Li J, Zhang W, Xie X, Yang H, Jiang H, Cherezov V, Liu H, Stevens RC, Zhao Q, Wu B. 2013. Structure of the CCR5 chemokine receptor-HIV entry inhibitor maraviroc complex. Science 341: 1387-1390. http:// dx.doi.org/10.1126/science.1241475.
24. Reyes-Robles T, Alonzo F, III, Kozhaya L, Lacy DB, Unutmaz D, Torres VJ. 2013. Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promote infection. Cell Host Microbe 14: 453-459. http://dx.doi.org/10.1016/ j.chom.2013.09.005.
25. Spaan AN, Reyes-Robles T, Badiou C, Cochet S, Boguslawski KM, Yoong P, Day CJ, de Haas CJ, van Kessel KP, Vandenesch F, Jennings MP, Le Van Kim C, Colin Y, van Strijp JA, Henry T, Torres VJ. 2015. Staphylococcus aureus targets the Duffy antigen receptor for chemokines (DARC) to lyse erythrocytes. Cell Host Microbe 18: 363-370. http:// dx.doi.org/10.1016/j.chom.2015.08.001.
26. Spaan AN, Henry T, van Rooijen WJ, Perret M, Badiou C, Aerts PC, Kemmink J, de Haas CJ, van Kessel KP, Vandenesch F, Lina G, van Strijp JA. 2013. The staphylococcal toxin Panton-Valentine leukocidin targets human C5a receptors. Cell Host Microbe 13: 584-594. http:// dx.doi.org/10.1016/j.chom.2013.04.006.
27. Guillet V, Roblin P, Werner S, Coraiola M, Menestrina G, Monteil H, Prévost G, Mourey L. 2004. Crystal structure of leucotoxin S component: new insight into the staphylococcal beta-barrel pore-forming toxins. J Biol Chem 279: 41028-41037. http://dx.doi.org/10.1074/jbc.M406904200.
28. Olson R, Nariya H, Yokota K, Kamio Y, Gouaux E. 1999. Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nat Struct Biol 6: 134-140. http://dx.doi.org/10.1038/5821.
29. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. 1996. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866. http://dx.doi.org/10.1126/ science.274.5294.1859.
30. Griffith JW, Sokol CL, Luster AD. 2014. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol 32: 659-702. http://dx.doi.org/10.1146/annurev-immunol-032713-120145.
31. +regulatory T cells to sites of Leishmania major infection favors pathogen persistence. J Exp Med 203: 2451-2460. http://dx.doi.org/10.1084/jem.20060956.
32. Lalani AS, Masters J, Zeng W, Barrett J, Pannu R, Everett H, Arendt CW, McFadden G. 1999. Use of chemokine receptors by poxviruses. Science 286: 1968-1971. http://dx.doi.org/10.1126/science.286.5446 .1968.
33. Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM. 2005. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 202: 1087-1098. http://dx.doi.org/10.1084/jem.20042530.
34. Glass WG, McDermott DH, Lim JK, Lekhong S, Yu SF, Frank WA, Pape J, Cheshier RC, Murphy PM. 2006. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J Exp Med 203: 35-40. http:// dx.doi.org/10.1084/jem.20051970.
35. Kindberg E, Mickiene A, Ax C, Akerlind B, Vene S, Lindquist L, Lundkvist A, Svensson L. 2008. A deletion in the chemokine receptor 5 (CCR5) gene is associated with tickborne encephalitis. J Infect Dis 197: 266-269. http://dx.doi.org/10.1086/524709.
36. Khan IA, Thomas SY, Moretto MM, Lee FS, Islam SA, Combe C, Schwartzman JD, Luster AD. 2006. CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog 2: e49. http://dx.doi.org/10.1371/journal.ppat.0020049.
37. Garcia-Perez J, Rueda P, Staropoli I, Kellenberger E, Alcami J, Arenzana-Seisdedos F, Lagane B. 2011. New insights into the mechanisms whereby low molecular weight CCR5 ligands inhibit HIV-1 infection. J Biol Chem 286: 4978-4990. http://dx.doi.org/10.1074/ jbc.M110.168955.
38. Watson C, Jenkinson S, Kazmierski W, Kenakin T. 2005. The CCR5 receptor-based mechanism of action of 873140, a potent allosteric noncompetitive HIV entry inhibitor. Mol Pharmacol 67: 1268-1282. http:// dx.doi.org/10.1124/mol.104.008565.
39. Alonzo F, III, Torres VJ. 2014. The bicomponent pore-forming leucocidins of Staphylococcus aureus. Microbiol Mol Biol Rev 78: 199-230. http://dx.doi.org/10.1128/MMBR.00055-13.
40. Spaan AN, Vrieling M, Wallet P, Badiou C, Reyes-Robles T, Ohneck EA, Benito Y, de Haas CJ, Day CJ, Jennings MP, Lina G, Vandenesch F, van Kessel KP, Torres VJ, van Strijp JA, Henry T. 2014. The staphylococcal toxins gamma-haemolysin AB and CB differentially target phagocytes by employing specific chemokine receptors. Nat Commun 5: 5438. http://dx.doi.org/10.1038/ncomms6438.
41. Vrieling M, Koymans KJ, Heesterbeek DA, Aerts PC, Rutten VP, de Haas CJ, van Kessel KP, Koets AP, Nijland R, van Strijp JA. 2015. Bovine Staphylococcus aureus secretes the leukocidin LukMF’ to kill migrating neutrophils through CCR1. mBio 6: e00335. http://dx.doi.org/10.1128/mBio.00335-15.
42. DuMont AL, Yoong P, Day CJ, Alonzo F, III, McDonald WH, Jennings MP, Torres VJ. 2013. Staphylococcus aureus LukAB cytotoxin kills human neutrophils by targeting the CD11b subunit of the integrin Mac-1. Proc Natl Acad Sci U S A 110: 10794-10799. http://dx.doi.org/10.1073/ pnas.1305121110.
43. Spaan AN, Schiepers A, de Haas CJ, van Hooijdonk DD, Badiou C, Contamin H, Vandenesch F, Lina G, Gerard NP, Gerard C, van Kessel KP, Henry T, van Strijp JA. 2015. Differential interaction of the staphylococcal toxins Panton-Valentine leukocidin and gamma-hemolysin CB with human C5a receptors. J Immunol 195: 1034-1043. http://dx.doi.org/10.4049/jimmunol.1500604.
44. DuMont AL, Torres VJ. 2014. Cell targeting by the Staphylococcus aureus pore-forming toxins: it’s not just about lipids. Trends Microbiol 22: 21-27. http://dx.doi.org/10.1016/j.tim.2013.10.004.
45. Laventie BJ, Guérin F, Mourey L, Tawk MY, Jover E, Maveyraud L, Prévost G. 2014. Residues essential for Panton-Valentine leukocidin S component binding to its cell receptor suggest both plasticity and adaptability in its interaction surface. PLoS One 9: e92094. http://dx.doi.org/10.1371/journal.pone.0092094.
46. DuMont AL, Yoong P, Liu X, Day CJ, Chumbler NM, James DB, Alonzo F, III, Bode NJ, Lacy DB, Jennings MP, Torres VJ. 2014. Identification of a crucial residue required for Staphylococcus aureus LukAB cytotoxicity and receptor recognition. Infect Immun 82: 1268-1276. http://dx.doi.org/10.1128/IAI.01444-13.
47. Alonzo F, III, Benson MA, Chen J, Novick RP, Shopsin B, Torres VJ. 2012. Staphylococcus aureus leucocidin ED contributes to systemic infection by targeting neutrophils and promoting bacterial growth in vivo. Mol Microbiol 83: 423-435. http://dx.doi.org/10.1111/j.1365-2958.2011.07942.x.
48. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. 2007. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13: 1405-1406. http:// dx.doi.org/10.1038/nm1207-1405.
49. DuMont AL, Yoong P, Surewaard BG, Benson MA, Nijland R, van Strijp JA, Torres VJ. 2013. Staphylococcus aureus elaborates leukocidin AB to mediate escape from within human neutrophils. Infect Immun 81: 1830-1841. http://dx.doi.org/10.1128/IAI.00095-13.
50. Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, Benito Y, Barbu EM, Vazquez V, Höök M, Etienne J, Vandenesch F, Bowden MG. 2007. Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315: 1130-1133. http://dx.doi.org/10.1126/ science.1137165.
51. Nocadello S, Minasov G, Shuvalova L, Dubrovska I, Sabini E, Bagnoli F, Grandi G, Anderson WF. 2016. Crystal structures of the components of the Staphylococcus aureus leukotoxin ED. Acta Crystallogr D Struct Biol 72: 113-120. http://dx.doi.org/10.1107/S2059798315023207.