Linkages between HIV-1 specificity for CCR5 or CXCR4 and in vitro usage of alternative coreceptors during progressive HIV-1 subtype C infection

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Cashin, Kieran ^a,b   Jakobsen, Martin R ^c   Sterjovski, Jasminka ^a,d   Roche, Michael ^a,d   Ellett, Anne ^a   Flynn, Jacqueline K ^a,d   Borm, Katharina ^a,e   Gouillou, Maelenn ^a   Churchill, Melissa J ^a,d   Gorry, Paul R ^a,b,d  

^a BURNET INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c AARHUS UNIVERSITY   (Denmark)

^d MONASH UNIVERSITY   (Australia)

^e LA TROBE UNIVERSITY   (Australia)

Author keywords

Alternative coreceptor; CCR5; CXCR4; Env; HIV 1; Pathogenesis; Subtype C

Indexed keywords

CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR4; FORMYLPEPTIDE RECEPTOR LIKE 1; VIRUS ENVELOPE PROTEIN;

ARTICLE; DISEASE COURSE; DISEASE SEVERITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS 1 SUBTYPE C; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN STRUCTURE; UNINDEXED SEQUENCE; VIRUS ENTRY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; DENMARK; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENOTYPE; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; RECEPTORS, CCR5; RECEPTORS, CXCR4; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, HIV; RECEPTORS, LIPOXIN; SEQUENCE ANALYSIS, DNA; VIRAL TROPISM; VIRUS INTERNALIZATION;

EID: 84883745292     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-98     Document Type: Article

References (44)

1. Gorry PR, Ancuta P. Coreceptors and HIV-1 pathogenesis. Current HIV/AIDS Reports 2011, 8:45-53. 10.1007/s11904-010-0069-x, 21188555.
2. Farzan M, Choe H, Martin K, Marcon L, Hofmann W, Karlsson G, Sun Y, Barrett P, Marchand N, Sullivan N, et al. Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. J Exp Med 1997, 186(3):405-411. 10.1084/jem.186.3.405, 2198994, 9236192.
3. Gorry PR, Dunfee RL, Mefford ME, Kunstman K, Morgan T, Moore JP, Mascola JR, Agopian K, Holm GH, Mehle A, et al. Changes in the V3 region of gp120 contribute to unusually broad coreceptor usage of an HIV-1 isolate from a CCR5 Delta32 heterozygote. Virology 2007, 362(1):163-178. 10.1016/j.virol.2006.11.025, 1973138, 17239419.
4. McKnight A, Dittmar MT, Moniz-Periera J, Ariyoshi K, Reeves JD, Hibbitts S, Whitby D, Aarons E, Proudfoot AE, Whittle H, et al. A broad range of chemokine receptors are used by primary isolates of human immunodeficiency virus type 2 as coreceptors with CD4. J Virol 1998, 72(5):4065-4071. 109635, 9557695.
5. Reeves JD, Hibbitts S, Simmons G, McKnight A, Azevedo-Pereira JM, Moniz-Pereira J, Clapham PR. Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4-negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo. J Virol 1999, 73(9):7795-7804. 104307, 10438870.
6. Jiang C, Parrish NF, Wilen CB, Li H, Chen Y, Pavlicek JW, Berg A, Lu X, Song H, Tilton JC, et al. Primary infection by a human immunodeficiency virus with atypical coreceptor tropism. J Virol 2011, 85(20):10669-10681. 10.1128/JVI.05249-11, 3187499, 21835785.
7. Clapham PR, Reeves JD, Simmons G, Dejucq N, Hibbitts S, McKnight A. HIV coreceptors, cell tropism and inhibition by chemokine receptor ligands. Mol Membr Biol 1999, 16(1):49-55. 10.1080/096876899294751, 10332737.
8. Jakobsen MR, Cashin K, Roche M, Sterjovski J, Ellett A, Borm K, Flynn J, Erikstrup C, Gouillou M, Gray LR, et al. Longitudinal analysis of CCR5 and CXCR4 usage alterations in a cohort of antiretroviral therapy naive subjects with progressive HIV-1 subtype C infection. PLoS One 2013, 8(6):e65950. 10.1371/journal.pone.0065950, 3688867, 23824043.
9. Jakobsen MR, Ellett A, Churchill MJ, Gorry PR. Viral tropism, fitness and pathogenicity of HIV-1 subtype C. Future Virol 2010, 5:219-231.
10. Nedellec R, Coetzer M, Shimizu N, Hoshino H, Polonis VR, Morris L, Martensson UE, Binley J, Overbaugh J, Mosier DE. Virus entry via the alternative coreceptors CCR3 and FPRL1 differs by human immunodeficiency virus type 1 subtype. J Virol 2009, 83(17):8353-8363. 10.1128/JVI.00780-09, 2738165, 19553323.
11. Coetzer M, Nedellec R, Cilliers T, Meyers T, Morris L, Mosier DE. Extreme genetic divergence is required for coreceptor switching in HIV-1 subtype C. J Acquir Immune Defic Syndr 2011, 56:9-15. 10.1097/QAI.0b013e3181f63906, 3006070, 20921899.
12. Isaacman-Beck J, Hermann EA, Yi Y, Ratcliffe SJ, Mulenga J, Allen S, Hunter E, Derdeyn CA, Collman RG. Heterosexual transmission of human immunodeficiency virus type 1 subtype C: macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol 2009, 83(16):8208-8220. 10.1128/JVI.00296-09, 2715751, 19515785.
13. Riddick NE, Hermann EA, Loftin LM, Elliott ST, Wey WC, Cervasi B, Taafe J, Engram JC, Li B, Else JG, et al. A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor usage in vivo. PLoS Pathogens 2010, 6:e1001064. 10.1371/journal.ppat.1001064, 2928783, 20865163.
14. Elliott ST, Riddick NE, Francella N, Paiardini M, Vanderford TH, Li B, Apetrei C, Sodora DL, Derdeyn CA, Silvestri G, et al. Cloning and analysis of sooty mangabey alternative coreceptors that support simian immunodeficiency virus SIVsmm entry independently of CCR5. J Virol 2012, 86(2):898-908. 10.1128/JVI.06415-11, 3255830, 22090107.
15. Chen Z, Kwon D, Jin Z, Monard S, Telfer P, Jones MS, Lu CY, Aguilar RF, Ho DD, Marx PA. Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J Exp Med 1998, 188(11):2057-2065. 10.1084/jem.188.11.2057, 2212380, 9841919.
16. Bjorndal A, Deng H, Jansson M, Fiore JR, Colognesi C, Karlsson A, Albert J, Scarlatti G, Littman DR, Fenyo EM. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J Virol 1997, 71(10):7478-7487. 192094, 9311827.
17. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR. Change in coreceptor use coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 1997, 185(4):621-628. 10.1084/jem.185.4.621, 2196142, 9034141.
18. Arien KK, Vanham G, Arts EJ. Is HIV-1 evolving to a less virulent form in humans?. Nat Rev Microbiol 2007, 5(2):141-151. 10.1038/nrmicro1594, 17203103.
19. Parker ZF, Iyer SS, Wilen CB, Parrish NF, Chikere KC, Lee FH, Didigu CA, Berro R, Klasse PJ, Lee B, et al. Transmitted/Founder and Chronic HIV-1 Envelope Proteins are Distinguished by Differential Utilization of CCR5. J Virol 2013, 87:2401-2411. 10.1128/JVI.02964-12, 3571396, 23269796.
20. Ping LH, Joseph SB, Anderson JA, Abrahams MR, Salazar-Gonzalez JF, Kincer LP, Treurnicht FK, Arney L, Ojeda S, Zhang M, et al. Comparison of Viral Env Proteins from Acute and Chronic Infections with Subtype C Human Immunodeficiency Virus Type 1 Identifies Differences in Glycosylation and CCR5 Utilization and Suggests a New Strategy for Immunogen Design. J Virol 2013, 87(13):7218-7233. 10.1128/JVI.03577-12, 23616655.
21. Alexander M, Lynch R, Mulenga J, Allen S, Derdeyn CA, Hunter E. Donor and recipient envs from heterosexual human immunodeficiency virus subtype C transmission pairs require high receptor levels for entry. J Virol 2010, 84(8):4100-4104. 10.1128/JVI.02068-09, 2849512, 20147398.
22. Li M, Salazar-Gonzalez JF, Derdeyn CA, Morris L, Williamson C, Robinson JE, Decker JM, Li Y, Salazar MG, Polonis VR, et al. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J Virol 2006, 80(23):11776-11790. 10.1128/JVI.01730-06, 1642599, 16971434.
23. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009, 206(6):1273-1289. 10.1084/jem.20090378, 2715054, 19487424.
24. Abebe A, Demissie D, Goudsmit J, Brouwer M, Kuiken CL, Pollakis G, Schuitemaker H, Fontanet AL, Rinke de Wit TF. HIV-1 subtype C syncytium- and non-syncytium-inducing phenotypes and coreceptor usage among Ethiopian patients with AIDS. Aids 1999, 13(11):1305-1311. 10.1097/00002030-199907300-00006, 10449282.
25. Bjorndal A, Sonnerborg A, Tscherning C, Albert J, Fenyo EM. Phenotypic characteristics of human immunodeficiency virus type 1 subtype C isolates of Ethiopian AIDS patients. AIDS Res Hum Retroviruses 1999, 15(7):647-653. 10.1089/088922299310944, 10331443.
26. Cilliers T, Nhlapo J, Coetzer M, Orlovic D, Ketas T, Olson WC, Moore JP, Trkola A, Morris L. The CCR5 and CXCR4 coreceptors are both used by human immunodeficiency virus type 1 primary isolates from subtype C. J Virol 2003, 77(7):4449-4456. 10.1128/JVI.77.7.4449-4456.2003, 150635, 12634405.
27. Connell BJ, Michler K, Capovilla A, Venter WD, Stevens WS, Papathanasopoulos MA. Emergence of X4 usage among HIV-1 subtype C: evidence for an evolving epidemic in South Africa. Aids 2008, 22(7):896-899. 10.1097/QAD.0b013e3282f57f7a, 18427209.
28. Johnston ER, Zijenah LS, Mutetwa S, Kantor R, Kittinunvorakoon C, Katzenstein DA. High frequency of syncytium-inducing and CXCR4-tropic viruses among human immunodeficiency virus type 1 subtype C-infected patients receiving antiretroviral treatment. J Virol 2003, 77(13):7682-7688. 10.1128/JVI.77.13.7682-7688.2003, 164829, 12805470.
29. Michler K, Connell BJ, Venter WD, Stevens WS, Capovilla A, Papathanasopoulos MA. Genotypic characterization and comparison of full-length envelope glycoproteins from South African HIV type 1 subtype C primary isolates that utilize CCR5 and/or CXCR4. AIDS Res Hum Retroviruses 2008, 24(5):743-751. 10.1089/aid.2007.0304, 18507530.
30. Ping LH, Nelson JA, Hoffman IF, Schock J, Lamers SL, Goodman M, Vernazza P, Kazembe P, Maida M, Zimba D, et al. Characterization of V3 sequence heterogeneity in subtype C human immunodeficiency virus type 1 isolates from Malawi: underrepresentation of X4 variants. J Virol 1999, 73(8):6271-6281. 112705, 10400718.
31. van Rensburg EJ, Smith TL, Zeier M, Robson B, Sampson C, Treurnicht F, Engelbrecht S. Change in co-receptor usage of current South African HIV-1 subtype C primary isolates. Aids 2002, 16(18):2479-2480. 10.1097/00002030-200212060-00015, 12461424.
32. Chikere K, Chou T, Gorry PR, Lee B. Affinofile profiling: how efficiency of CD4/CCR5 usage impacts the biological and pathogenic phenotype of HIV. Virology 2013, 435:81-91. 10.1016/j.virol.2012.09.043, 23217618.
33. Johnston SH, Lobriz MA, Nguyen S, Lassen K, Delair S, Posta F, Bryson YJ, Arts EJ, Chou T, Lee B. A quantitative affinity-profiling system that reveals distinct CD4/CCR5 usage patterns among human immunodeficiency virus type 1 and simian immunodeficiency virus strains. J Virol 2009, 83:11016-11026. 10.1128/JVI.01242-09, 2772777, 19692480.
34. Sterjovski J, Roche M, Churchill MJ, Ellett A, Farrugia W, Gray LR, Cowley D, Poumbourios P, Lee B, Wesselingh S, et al. An altered and more efficient mechanism of CCR5 engagement contributes to macrophage tropism of CCR5-using HIV-1 envelopes. Virology 2010, 404:269-278. 10.1016/j.virol.2010.05.006, 3096480, 20570309.
35. Shimizu N, Tanaka A, Oue A, Mori T, Ohtsuki T, Apichartpiyakul C, Uchiumi H, Nojima Y, Hoshino H. Broad usage spectrum of G protein-coupled receptors as coreceptors by primary isolates of HIV. Aids 2009, 23(7):761-769.
36. Gao F, Morrison SG, Robertson DL, Thornton CL, Craig S, Karlsson G, Sodroski J, Morgado M, Galvao-Castro B, von Briesen H, et al. Molecular cloning and analysis of functional envelope genes from human immunodeficiency virus type 1 sequence subtypes A through G. The WHO and NIAID Networks for HIV Isolation and Characterization. J Virol 1996, 70(3):1651-1667. 189989, 8627686.
37. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 1998, 72(4):2855-2864. 109730, 9525605.
38. Gray L, Churchill MJ, Keane N, Sterjovski J, Ellett AM, Purcell DFJ, Poumbourios P, Kol C, Wang B, Saksena N, et al. Genetic and functional analysis of R5X4 human immunodeficiency virus type 1 envelope glycoprotiens derived from two individuals homozygous for the CCR5delta32 allele. J Virol 2006, 80(7):3684-3691. 10.1128/JVI.80.7.3684-3691.2006, 1440368, 16537640.
39. Yang X, Wyatt R, Sodroski J. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J Virol 2001, 75(3):1165-1171. 10.1128/JVI.75.3.1165-1171.2001, 114022, 11152489.
40. Sterjovski J, Churchill MJ, Ellett A, Gray LR, Roche MJ, Dunfee RL, Purcell DF, Saksena N, Wang B, Sonza S, et al. Asn 362 in gp120 contributes to enhanced fusogenicity by CCR5-restricted HIV-1 envelope glycoprotein variants from patients with AIDS. Retrovirology 2007, 4:89. 10.1186/1742-4690-4-89, 2225424, 18076768.
41. Cashin K, Roche M, Sterjovski J, Ellett A, Gray LR, Cunningham AL, Ramsland PA, Churchill MJ, Gorry PR. Alternative coreceptor requirements for efficient CCR5- and CXCR4-mediated HIV-1 entry into macrophages. J Virol 2011, 85:10699-10709. 10.1128/JVI.05510-11, 3187472, 21835796.
42. Roche M, Jakobsen MR, Ellett A, Salimiseyedabad H, Jubb B, Westby M, Lee B, Lewin SR, Churchill MJ, Gorry PR. HIV-1 predisposed to acquiring resistance to maraviroc (MVC) and other CCR5 antagonists in vitro has an inherent, low-level ability to utilize MVC-bound CCR5 for entry. Retrovirology 2011, 8(1):89. 10.1186/1742-4690-8-89, 3217884, 22054077.
43. Roche M, Jakobsen MR, Sterjovski J, Ellett A, Posta F, Lee B, Jubb B, Westby M, Lewin SR, Ramsland PA, et al. HIV-1 escape from the CCR5 antagonist maraviroc associated with an altered and less efficient mechanism of gp120-CCR5 engagement that attenuates macrophage-tropism. J Virol 2011, 85:4330-4342. 10.1128/JVI.00106-11, 3126252, 21345957.
44. Etemad-Moghadam B, Sun Y, Nicholson EK, Fernandes M, Liou K, Gomila R, Lee J, Sodroski J. Envelope glycoprotein determinants of increased fusogenicity in a pathogenic simian-human immunodeficiency virus (SHIV-KB9) passaged in vivo. J Virol 2000, 74(9):4433-4440. 10.1128/JVI.74.9.4433-4440.2000, 111962, 10756060.