CRF19_cpx is an Evolutionary fit HIV-1 Variant Strongly Associated With Rapid Progression to AIDS in Cuba

CRF19; Cuba; HIV-1; Progression to AIDS; Variant; CXCL9 chemokine; Fas ligand; RANTES; Pol protein; Article; CD4 lymphocyte count; Human immunodeficiency virus 1 infection; Acquired Immunodeficiency Syndrome; HIV Infections; Human immunodeficiency virus 1; Adult; Biological Evolution; Coinfection; Drug Resistance, Viral; Female; Genetic Variation; Humans; Male; Retrospective Studies; Sexual Behavior; Viral Load; Young Adult

Abstract :

[en] Background: Clinicians reported an increasing trend of rapid progression (RP) (AIDS within 3. years of infection) in Cuba. Methods: Recently infected patients were prospectively sampled, 52 RP at AIDS diagnosis (AIDS-RP) and 21 without AIDS in the same time frame (non-AIDS). 22 patients were sampled at AIDS diagnosis (chronic-AIDS) retrospectively assessed as >. 3. years infected. Clinical, demographic, virological, epidemiological and immunological data were collected. Pol and env sequences were used for subtyping, transmission cluster analysis, and prediction of resistance, co-receptor use and evolutionary fitness. Host, immunological and viral predictors of RP were explored through data mining. Findings: Subtyping revealed 26 subtype B strains, 6 C, 6 CRF18_cpx, 9 CRF19_cpx, 29 BG-recombinants and other subtypes/URFs. All patients infected with CRF19 belonged to the AIDS-RP group. Data mining identified CRF19, oral candidiasis and RANTES levels as the strongest predictors of AIDS-RP. CRF19 was more frequently predicted to use the CXCR4 co-receptor, had higher fitness scores in the protease region, and patients had higher viral load at diagnosis. Interpretation: CRF19 is a recombinant of subtype D (C-part of Gag, PR, RT and nef), subtype A (N-part of Gag, Integrase, Env) and subtype G (Vif, Vpr, Vpu and C-part of Env). Since subtypes D and A have been associated with respectively faster and slower disease progression, our findings might indicate a fit PR driving high viral load, which in combination with co-infections may boost RANTES levels and thus CXCR4 use, potentially explaining the fast progression. We propose that CRF19 is evolutionary very fit and causing rapid progression to AIDS in many newly infected patients in Cuba. © 2015.

Disciplines :

Immunology & infectious disease

Author, co-author :

Kouri, V.; Virology Department, Institute of Tropical Medicine Pedro Kourí, Autopista Novia del Mediodía, Marianao 13, Havana City, Cuba

Khouri, R.; KU Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium, LIMI-LIP, Centro de Pesquisa Gonçalo Moniz, FIOCRUZ, Salvador-Bahia, Brazil

Alemán, Y.; Virology Department, Institute of Tropical Medicine Pedro Kourí, Autopista Novia del Mediodía, Marianao 13, Havana City, Cuba

Abrahantes, Y.; Virology Department, Institute of Tropical Medicine Pedro Kourí, Autopista Novia del Mediodía, Marianao 13, Havana City, Cuba

Vercauteren, J.; KU Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium

Pineda-Peña, A.-C.; KU Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium, Clinical and Molecular Infectious Diseases Group, Faculty of Sciences and Mathematics, Universidad del Rosario, Bogotá, Colombia

Theys, K.; KU Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium

Megens, S.; KU Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium

Moutschen, Michel ; Université de Liège - ULiège > Département des sciences cliniques > GIGA-R:Immunopath. - Maladies infect. et médec. inter. gén.

Pfeifer, N.; Department of Computational Biology and Applied Algorithmics, Max Planck Institute for Informatics, Campus E1 4, Saarbrücken, Germany

More authors (6 more)

Language :

English

Title :

CRF19_cpx is an Evolutionary fit HIV-1 Variant Strongly Associated With Rapid Progression to AIDS in Cuba

Publication date :

2015

Journal title :

EBioMedicine

eISSN :

2352-3964

Publisher :

Elsevier

Volume :

Issue :

Pages :

244-254

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 04 March 2019

Statistics

Number of views

67 (4 by ULiège)

Number of downloads

49 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Abrahantes Rodríguez Y., Pérez Avila J., Kouri Cardellá V., Fonseca Gómez C., Baly Gil A., Tápanes Fernandez T. Factors linked to rapid progression to AIDS in Cuban subjects. Rev. Cubana Med. Trop. 2010, 62:146-153.
Alemu A., Shiferaw Y., Addis Z., Mathewos B., Birhan W. Effect of malaria on HIV/AIDS transmission and progression. Parasites Vectors 2013, 6:18.
Annunziato F., Galli G., Nappi F., et al. Limited expression of R5-tropic HIV-1 in CCR5-positive type 1-polarized T cells explained by their ability to produce RANTES, MIP-1alpha, and MIP-1beta. Blood 2000, 95:1167-1174.
Eberle J., Noah C., Wolf E., Stürmer M., Braun P., Korn K., Däumer M., Thielen A., Berg T., Obermeier M., Ehret R., WaLter H., Lengauer T., Verheyen J., Sierra S., Kaiser R. Empfehlungen zur Bestimmung des HIV-1-Korezeptor-Gebrauchs, (DAIG Recommendations for the HIV-1 Tropism Testing) (last accessed 2/3/2015). http://www.daignet.de/site-content/hiv-therapie/leitlinien-1/Empfehlungen%20zur%20Bestimmung%20des%20HIV_1_Korezeptor_Gebrauchs.pdf.
Baeten J.M., Chohan B., Lavreys L., et al. HIV-1 subtype D infection is associated with faster disease progression than subtype A in spite of similar plasma HIV-1 loads. J. Infect. Dis. 2007, 195:1177-1180.
Bártolo I., Camacho R., Barroso H., Bezerra V., Taveira N. Rapid clinical progression to AIDS and death in a persistently seronegative HIV-1 infected heterosexual young man. AIDS 2009, 23:2359-2362.
Bennett D.E., Camacho R.J., Otelea D., et al. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS ONE 2009, 4:e4724.
Casado G., Thomson M.M., Sierra M., Nájera R. Identification of a novel HIV-1 circulating ADG intersubtype recombinant form (CRF19_cpx) in Cuba. J. Acquir. Immune Defic. Syndr. 2005, 40:532-537.
Casado C., Colombo S., Rauch A., et al. Host and viral genetic correlates of clinical definitions of HIV-1 disease progression. PLoS ONE 2010, 5:e11079.
De Oliveira T., Deforche K., Cassol S., et al. An automated genotyping system for analysis of HIV-1 and other microbial sequences. Bioinformatics 2005, 21:3797-3800.
Deacon N.J., Tsykin A., Solomon A., et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 1995, 270:988-991.
Deforche K., Silander T., Camacho R., et al. Analysis of HIV-1 pol sequences using Bayesian Networks: implications for drug resistance. Bioinformatics 2006, 22:2975-2979.
Delatorre E., Bello G. Phylodynamics of the HIV-1 epidemic in Cuba. PLoS ONE 2013, 8:e72448.
Demarest J.F., Jack N., Cleghorn F.R., et al. Immunologic and virologic analyses of an acutely HIV type 1-infected patient with extremely rapid disease progression. AIDS Res. Hum. Retroviruses 2001, 17:1333-1344.
Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
Esbjörnsson J., Månsson F., Martínez-arias W., et al. Frequent CXCR4 Tropism of HIV-1 Subtype A and CRF02_AG During Late-stage Disease - Indication of an Evolving Epidemic in West Africa 2010, 1-13.
Frahm N., Korber B.T., Adams C.M., et al. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 2004, 78:2187-2200.
Frentz D., Wensing A.M.J., Albert J., et al. Limited cross-border infections in patients newly diagnosed with HIV in Europe. Retrovirology 2013, 10:36.
Friedman N.G.M., WA Data analysis with bayesian networks: a bootstrap approach. UAI'99 Proceedings of the Fifteenth Conference on Uncertainty in Artificial Intelligence 1999, 196-205.
Giorgi J.V., Hultin L.E., McKeating J.A., et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine co-receptor usage. J. Infect. Dis. 1999, 179:859-870.
Helleberg M., Afzal S., Kronborg G., et al. Mortality attributable to smoking among HIV-1-infected individuals: a nationwide, population-based cohort study. Clin. Infect. Dis. 2013, 56:727-734.
Hernandez M.D., Sherman K.E. HIV/hepatitis C coinfection natural history and disease progression. Curr. Opin. HIV AIDS 2011, 6:478-482.
Huang C., Levitz S.M. Stimulation of macrophage inflammatory protein-1alpha, macrophage inflammatory protein-1beta, and RANTES by Candida albicans and Cryptococcus neoformans in peripheral blood mononuclear cells from persons with and without human immunodeficiency virus infec. J. Infect. Dis. 2000, 181:791-794.
Jensen M.A., Li F.-S., van 't Wout A.B., et al. Improved co-receptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J. Virol. 2003, 77:13376-13388.
Kaleebu P., French N., Mahe C., et al. Effect of human immunodeficiency virus (HIV) type 1 envelope subtypes A and D on disease progression in a large cohort of HIV-1-positive persons in Uganda. J. Infect. Dis. 2002, 185:1244-1250.
Kaleebu P., Nankya I.L., Yirrell D.L., et al. Relation between chemokine receptor use, disease stage, and HIV-1 subtypes A and D: results from a rural Ugandan cohort. J. Acquir. Immune Defic. Syndr. 2007, 45:28-33.
Kiwanuka N., Laeyendecker O., Robb M., et al. Effect of human immunodeficiency virus Type 1 (HIV-1) subtype on disease progression in persons from Rakai, Uganda, with incident HIV-1 infection. J. Infect. Dis. 2008, 197:707-713.
Lajoie J., Fontaine J., Tremblay C., Routy J.-P., Poudrier J., Roger M. Persistence of high levels of blood soluble human leukocyte antigen-G is associated with rapid progression of HIV infection. AIDS 2009, 23:1437-1440.
Le Clerc S., Limou S., Coulonges C., et al. Genomewide association study of a rapid progression cohort identifies new susceptibility alleles for AIDS (ANRS Genomewide Association Study 03). J. Infect. Dis. 2009, 200:1194-1201.
Leigh Brown A.J., Lycett S.J., Weinert L., Hughes G.J., Fearnhill E., Dunn D.T. Transmission network parameters estimated from HIV sequences for a nationwide epidemic. J. Infect. Dis. 2011, 204:1463-1469.
Lemey P., Derdelinckx I., Rambaut A., et al. Molecular footprint of drug-selective pressure in a human immunodeficiency virus transmission chain. J. Virol. 2005, 79:11981-11989.
Lemey P., Kosakovsky Pond S.L., Drummond A.J., et al. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput. Biol. 2007, 3:e29.
Lengauer T., Sander O., Sierra S., Thielen A., Kaiser R. Bioinformatics prediction of HIV co-receptor usage. Nat. Biotechnol. 2007, 25:1407-1410.
Leslie A.J., Pfafferott K.J., Chetty P., et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 2004, 10:282-289.
Li G., Verheyen J., Rhee S.-Y., Voet A., Vandamme A.-M., Theys K. Functional conservation of HIV-1 Gag: implications for rational drug design. Retrovirology 2013, 10:126.
Li X., Xue Y., Zhou L., et al. Evidence that HIV-1 CRF01_AE is associated with low CD4+ T cell count and CXCR4 co-receptor usage in recently infected young men who have sex with men (MSM) in Shanghai, China. PLoS ONE 2014, 9:e89462.
Limou S., Le Clerc S., Coulonges C., et al. Genomewide association study of an AIDS-nonprogression cohort emphasizes the role played by HLA genes (ANRS Genomewide Association Study 02). J. Infect. Dis. 2009, 199:419-426.
Liovat A.-S., Rey-Cuillé M.-A., Lécuroux C., et al. Acute plasma biomarkers of T cell activation set-point levels and of disease progression in HIV-1 infection. PLoS ONE 2012, 7:e46143.
Mann J.K., Byakwaga H., Kuang X.T., et al. Ability of HIV-1 Nef to downregulate CD4 and HLA class I differs among viral subtypes. Retrovirology 2013, 10:100.
Martinez-Picado J., Prado J.G., Fry E.E., et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 2006, 80:3617-3623.
Murphy K., Hoover D.R., Shi Q., et al. Association of self-reported race with AIDS death in continuous HAART users in a cohort of HIV-infected women in the United States. AIDS 2013, 27:2413-2423.
Ng O.T., Laeyendecker O., Redd A.D., et al. HIV type 1 polymerase gene polymorphisms are associated with phenotypic differences in replication capacity and disease progression. J. Infect. Dis. 2014, 209:66-73.
Pawlowski A., Jansson M., Sköld M., Rottenberg M.E., Källenius G. Tuberculosis and HIV co-infection. PLoS Pathog. 2012, 8:e1002464.
Pérez L., Thomson M.M., Bleda M.J., et al. HIV type 1 molecular epidemiology in Cuba: high genetic diversity, frequent mosaicism, and recent expansion of BG intersubtype recombinant forms. AIDS Res. Hum. Retroviruses 2006, 22:724-733.
Pérez L., Kourí V., Alemán Y., et al. Antiretroviral drug resistance in HIV-1 therapy-naive patients in Cuba. Infect. Genet. Evol. 2013, 16:144-150.
Pineda-Peña A.-C., Faria N.R., Imbrechts S., et al. Automated subtyping of HIV-1 genetic sequences for clinical and surveillance purposes: performance evaluation of the new REGA version 3 and seven other tools. Infect. Genet. Evol. 2013, 19:337-348.
Price M.N., Dehal P.S., Arkin A.P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 2010, 5:e9490.
Pushker R., Jacqué J.-M., Shields D.C. Meta-analysis to test the association of HIV-1 nef amino acid differences and deletions with disease progression. J. Virol. 2010, 84:3644-3653.
Ragonnet-Cronin M., Hodcroft E., Hué S., et al. Automated analysis of phylogenetic clusters. BMC Bioinforma. 2013, 14:317.
Roberts L., Passmore J.S., Williamson C., et al. Disease progression 2011, 24:819-831.
Rutledge T.F., Boyd M.F. Morbidity and Mortality Weekly Report Revised Surveillance Case Definitions for HIV Infection Among Adults, Adolescents, and Children Aged <18Months and for HIV Infection and AIDS Among Children Aged 18 Months to <13Years - United States 2008, 57. (depa. 2008).
Sapsutthipas S., Tsuchiya N., Pathipavanich P., et al. CRF01_AE-specific neutralizing activity observed in plasma derived from HIV-1-infected Thai patients residing in northern Thailand: comparison of neutralizing breadth and potency between plasma derived from rapid and slow progressors. PLoS ONE 2013, 8:e53920.
Secor W.E. The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr. Opin. HIV AIDS 2012, 7:254-259.
Sierra M., Thomson M.M., Posada D., et al. Identification of 3 phylogenetically related HIV-1 BG intersubtype circulating recombinant forms in Cuba. J. Acquir. Immune Defic. Syndr. 2007, 45:151-160.
Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
Struck D., Perez-Bercoff D., Devaux C.S.J. COMET: a novel approach to HIV-1 subtype prediction. 8th European HIV Drug Resistance Workshop 2010.
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
Theys K., Deforche K., Vercauteren J., et al. Treatment-associated polymorphisms in protease are significantly associated with higher viral load and lower CD4 count in newly diagnosed drug-naive HIV-1 infected patients. Retrovirology 2012, 9:81.
Thomson M.M., Nájera R. Molecular epidemiology of HIV-1 variants in the global AIDS pandemic: an update. AIDS Rev. 2005, 7:210-224.
Tscherning C., Alaeus A., Fredriksson R., et al. Differences in chemokine co-receptor usage between genetic subtypes of HIV-1. Virology 1998, 241:181-188.
Van Laethem K., Schrooten Y., Lemey P., et al. A genotypic resistance assay for the detection of drug resistance in the human immunodeficiency virus type 1 envelope gene. J. Virol. Methods 2005, 123:25-34.
Vandekerckhove L.P.R., Wensing A.M.J., Kaiser R., et al. European guidelines on the clinical management of HIV-1 tropism testing. Lancet Infect. Dis. 2011, 11:394-407.
Vaughan H.E., Cane P., Pillay D., Tedder R.S. Characterization of HIV type 1 clades in the Caribbean using pol gene sequences. AIDS Res. Hum. Retroviruses 2003, 19:929-932.
Wang B. Viral factors in non-progression. Front. Immunol. 2013, 4:355.