Evolution toward beta common chain receptor usage links the matrix proteins of HIV-1 and its ancestors to human erythropoietin.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
12 01 2021
Historique:
entrez: 29 12 2020
pubmed: 30 12 2020
medline: 19 5 2021
Statut: ppublish

Résumé

The HIV-1 matrix protein p17 (p17) is a pleiotropic molecule impacting on different cell types. Its interaction with many cellular proteins underlines the importance of the viral protein as a major determinant of human specific adaptation. We previously showed the proangiogenic capability of p17. Here, by integrating functional analysis and receptor binding, we identify a functional epitope that displays molecular mimicry with human erythropoietin (EPO) and promotes angiogenesis through common beta chain receptor (βCR) activation. The functional EPO-like epitope was found to be present in the matrix protein of HIV-1 ancestors SIV originated in chimpanzees (SIVcpz) and gorillas (SIVgor) but not in that of HIV-2 and its ancestor SIVsmm from sooty mangabeys. According to biological data, evolution of the EPO-like epitope showed a clear differentiation between HIV-1/SIVcpz-gor and HIV-2/SIVsmm branches, thus highlighting this epitope on p17 as a divergent signature discriminating HIV-1 and HIV-2 ancestors. P17 is known to enhance HIV-1 replication. Similarly to other βCR ligands, p17 is capable of attracting and activating HIV-1 target cells and promoting a proinflammatory microenvironment. Thus, it is tempting to speculate that acquisition of an epitope on the matrix proteins of HIV-1 ancestors capable of triggering βCR may have represented a critical step to enhance viral aggressiveness and early human-to-human SIVcpz/gor dissemination. The hypothesis that the p17/βCR interaction and βCR abnormal stimulation may also play a role in sustaining chronic activation and inflammation, thus marking the difference between HIV-1 and HIV-2 in term of pathogenicity, needs further investigation.

Identifiants

pubmed: 33372148
pii: 2021366118
doi: 10.1073/pnas.2021366118
pmc: PMC7812818
pii:
doi:

Substances chimiques

EPO protein, human 0
Epitopes 0
HIV Antigens 0
gag Gene Products, Human Immunodeficiency Virus 0
p17 protein, Human Immunodeficiency Virus Type 1 0
Erythropoietin 11096-26-7

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

Competing interest statement: F.C. and A.C. are listed as inventors in a patent application related to this study.

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Auteurs

Francesca Caccuri (F)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy.

Pasqualina D'Ursi (P)

Institute of Technologies in Biomedicine, National Research Council, 20090 Segrate, Italy.

Matteo Uggeri (M)

Institute of Technologies in Biomedicine, National Research Council, 20090 Segrate, Italy.
Department of Pharmacy, University of Genova, 16132 Genova, Italy.

Antonella Bugatti (A)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy.

Pietro Mazzuca (P)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy.

Alberto Zani (A)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy.

Federica Filippini (F)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy.

Mario Salmona (M)

Istituti di Ricovero e Cura a Carattere Assistenziale Istituto di Ricerche Farmacologiche Mario Negri, 20156 Milan, Italy.

Domenico Ribatti (D)

Department of Basic Medical Sciences, Neurosciences and Sensory Organs, University of Bari Medical School, 70124 Bari, Italy.

Mark Slevin (M)

School of Healthcare Science, Manchester Metropolitan University, M15GD Manchester, United Kingdom.

Alessandro Orro (A)

Institute of Technologies in Biomedicine, National Research Council, 20090 Segrate, Italy.

Wuyuan Lu (W)

Institute of Human Virology, University of Maryland, Baltimore, MD 21201.

Pietro Liò (P)

Department of Computer Science and Technology, University of Cambridge, CB3 0FD Cambridge, United Kingdom.

Robert C Gallo (RC)

Institute of Human Virology, University of Maryland, Baltimore, MD 21201; rgallo@ihv.umaryland.edu arnaldo.caruso@unibs.it.

Arnaldo Caruso (A)

Department of Molecular and Translational Medicine, University of Brescia Medical School, 25123 Brescia, Italy; rgallo@ihv.umaryland.edu arnaldo.caruso@unibs.it.

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Classifications MeSH