Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity

Joshua R. Kane; David J. Stanley; Judd F. Hultquist; Jeffrey R. Johnson; Nicole Mietrach; Jennifer M. Binning; Stefán R. Jónsson; Sarah Barelier; Billy W. Newton; Tasha L. Johnson; Kathleen E. Franks-Skiba; Ming Li; William L. Brown; Hörour I. Gunnarsson; Adalbjorg Adalbjornsdóttir; James S. Fraser; Reuben S. Harris; Valgerour Andrésdóttir; John D. Gross; Nevan J. Krogan

doi:10.1016/j.celrep.2015.04.038

Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity

Joshua R. Kane, David J. Stanley, Judd F. Hultquist, Jeffrey R. Johnson, Nicole Mietrach, Jennifer M. Binning, Stefán R. Jónsson, Sarah Barelier, Billy W. Newton, Tasha L. Johnson, Kathleen E. Franks-Skiba, Ming Li, William L. Brown, Hörour I. Gunnarsson, Adalbjorg Adalbjornsdóttir, James S. Fraser, Reuben S. Harris, Valgerour Andrésdóttir, John D. Gross, Nevan J. Krogan

Biochemistry, Molecular Biology, and Biophysics (CBS)

Research output: Contribution to journal › Article › peer-review

40 Scopus citations

Abstract

HIV-1 encodes the accessory protein Vif, which hijacks a host Cullin-RING ubiquitin ligase (CRL) complex as well as the non-canonical cofactor CBFβ, to antagonize APOBEC3 antiviral proteins. Non-canonical cofactor recruitment to CRL complexes by viral factors, to date, has only been attributed to HIV-1 Vif. To further study this phenomenon, we employed a comparative approach combining proteomic, biochemical, structural, and virological techniques to investigate Vif complexes across the lentivirus genus, including primate (HIV-1 and simian immunodeficiency virus macaque [SIVmac]) and non-primate (FIV, BIV, and MVV) viruses. We find that CBFβ is completely dispensable for the activity of non-primate lentiviral Vif proteins. Furthermore, we find that BIV Vif requires no cofactor and that MVV Vif requires a novel cofactor, cyclophilin A (CYPA), for stable CRL complex formation and anti-APOBEC3 activity. We propose modular conservation of Vif complexes allows for potential exaptation of functions through the acquisition of non-CRL-associated host cofactors while preserving anti-APOBEC3 activity.

Original language	English (US)
Pages (from-to)	1236-1250
Number of pages	15
Journal	Cell reports
Volume	11
Issue number	8
DOIs	https://doi.org/10.1016/j.celrep.2015.04.038
State	Published - May 26 2015

Bibliographical note

Funding Information:
The authors wish to thank members of the N.J.K., J.D.G., J.S.F., R.S.H., and V.A. labs; P. Hartley for assisting in stable line generation; R. LaRue for cloning of MVV, BIV, FIV, and SIVmac Vif plasmids; S. Jäger, S. Chen, M. Eckhardt, and D. Gordon for reagents; Z. Rizvi for CYPA cloning; S.J., C. Mahon, and G. Jang for expertise and advice in affinity purifications; E. Verschueren and P. Cimermančič for advice on AP-MS scoring; and M. Shales for assistance in figure construction. We would kindly thank S.J. Kim for help in collecting SAXS profiles and D. Schneidman for her assistance in generating the HIV E3 model and analyzing the SAXS data using the AllosMod-FoXS server. The following reagents were obtained through the NIH AIDS Reagent Program, Division of AIDS, NIAID, NIH: Jurkat Clone E6-1 from Dr. A. Weiss and Jurkat T cells CYPA −/− from Drs. D. Braaten and J. Luban. J.R.K. was supported by an NSF graduate research fellowship. This work was supported by NIH grants to N.J.K (P50 GM082250, P50 GM081879, and P01 AI090935) and to R.S.H. (R01 AI064046 and P01 GM091743) and a grant from the Icelandic Research Fund to V.A. (141085-051).

Publisher Copyright:
© 2015 The Authors.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Publisher link

10.1016/j.celrep.2015.04.038

Find It

Find It at U of M Libraries

Cite this

Kane, J. R., Stanley, D. J., Hultquist, J. F., Johnson, J. R., Mietrach, N., Binning, J. M., Jónsson, S. R., Barelier, S., Newton, B. W., Johnson, T. L., Franks-Skiba, K. E., Li, M., Brown, W. L., Gunnarsson, H. I., Adalbjornsdóttir, A., Fraser, J. S., Harris, R. S., Andrésdóttir, V., Gross, J. D., & Krogan, N. J. (2015). Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity. Cell reports, 11(8), 1236-1250. https://doi.org/10.1016/j.celrep.2015.04.038

Kane, JR, Stanley, DJ, Hultquist, JF, Johnson, JR, Mietrach, N, Binning, JM, Jónsson, SR, Barelier, S, Newton, BW, Johnson, TL, Franks-Skiba, KE, Li, M, Brown, WL, Gunnarsson, HI, Adalbjornsdóttir, A, Fraser, JS, Harris, RS, Andrésdóttir, V, Gross, JD & Krogan, NJ 2015, 'Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity', Cell reports, vol. 11, no. 8, pp. 1236-1250. https://doi.org/10.1016/j.celrep.2015.04.038

@article{ec6bc6a5e6894451ae36285c03c0a93a,

title = "Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity",

abstract = "HIV-1 encodes the accessory protein Vif, which hijacks a host Cullin-RING ubiquitin ligase (CRL) complex as well as the non-canonical cofactor CBFβ, to antagonize APOBEC3 antiviral proteins. Non-canonical cofactor recruitment to CRL complexes by viral factors, to date, has only been attributed to HIV-1 Vif. To further study this phenomenon, we employed a comparative approach combining proteomic, biochemical, structural, and virological techniques to investigate Vif complexes across the lentivirus genus, including primate (HIV-1 and simian immunodeficiency virus macaque [SIVmac]) and non-primate (FIV, BIV, and MVV) viruses. We find that CBFβ is completely dispensable for the activity of non-primate lentiviral Vif proteins. Furthermore, we find that BIV Vif requires no cofactor and that MVV Vif requires a novel cofactor, cyclophilin A (CYPA), for stable CRL complex formation and anti-APOBEC3 activity. We propose modular conservation of Vif complexes allows for potential exaptation of functions through the acquisition of non-CRL-associated host cofactors while preserving anti-APOBEC3 activity.",

author = "Kane, {Joshua R.} and Stanley, {David J.} and Hultquist, {Judd F.} and Johnson, {Jeffrey R.} and Nicole Mietrach and Binning, {Jennifer M.} and J{\'o}nsson, {Stef{\'a}n R.} and Sarah Barelier and Newton, {Billy W.} and Johnson, {Tasha L.} and Franks-Skiba, {Kathleen E.} and Ming Li and Brown, {William L.} and Gunnarsson, {H{\"o}rour I.} and Adalbjorg Adalbjornsd{\'o}ttir and Fraser, {James S.} and Harris, {Reuben S.} and Valgerour Andr{\'e}sd{\'o}ttir and Gross, {John D.} and Krogan, {Nevan J.}",

note = "Funding Information: The authors wish to thank members of the N.J.K., J.D.G., J.S.F., R.S.H., and V.A. labs; P. Hartley for assisting in stable line generation; R. LaRue for cloning of MVV, BIV, FIV, and SIVmac Vif plasmids; S. J{\"a}ger, S. Chen, M. Eckhardt, and D. Gordon for reagents; Z. Rizvi for CYPA cloning; S.J., C. Mahon, and G. Jang for expertise and advice in affinity purifications; E. Verschueren and P. Cimerman{\v c}i{\v c} for advice on AP-MS scoring; and M. Shales for assistance in figure construction. We would kindly thank S.J. Kim for help in collecting SAXS profiles and D. Schneidman for her assistance in generating the HIV E3 model and analyzing the SAXS data using the AllosMod-FoXS server. The following reagents were obtained through the NIH AIDS Reagent Program, Division of AIDS, NIAID, NIH: Jurkat Clone E6-1 from Dr. A. Weiss and Jurkat T cells CYPA −/− from Drs. D. Braaten and J. Luban. J.R.K. was supported by an NSF graduate research fellowship. This work was supported by NIH grants to N.J.K (P50 GM082250, P50 GM081879, and P01 AI090935) and to R.S.H. (R01 AI064046 and P01 GM091743) and a grant from the Icelandic Research Fund to V.A. (141085-051). Publisher Copyright: {\textcopyright} 2015 The Authors.",

year = "2015",

month = may,

day = "26",

doi = "10.1016/j.celrep.2015.04.038",

language = "English (US)",

volume = "11",

pages = "1236--1250",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "8",

}

TY - JOUR

T1 - Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity

AU - Kane, Joshua R.

AU - Stanley, David J.

AU - Hultquist, Judd F.

AU - Johnson, Jeffrey R.

AU - Mietrach, Nicole

AU - Binning, Jennifer M.

AU - Jónsson, Stefán R.

AU - Barelier, Sarah

AU - Newton, Billy W.

AU - Johnson, Tasha L.

AU - Franks-Skiba, Kathleen E.

AU - Li, Ming

AU - Brown, William L.

AU - Gunnarsson, Hörour I.

AU - Adalbjornsdóttir, Adalbjorg

AU - Fraser, James S.

AU - Harris, Reuben S.

AU - Andrésdóttir, Valgerour

AU - Gross, John D.

AU - Krogan, Nevan J.

N1 - Funding Information: The authors wish to thank members of the N.J.K., J.D.G., J.S.F., R.S.H., and V.A. labs; P. Hartley for assisting in stable line generation; R. LaRue for cloning of MVV, BIV, FIV, and SIVmac Vif plasmids; S. Jäger, S. Chen, M. Eckhardt, and D. Gordon for reagents; Z. Rizvi for CYPA cloning; S.J., C. Mahon, and G. Jang for expertise and advice in affinity purifications; E. Verschueren and P. Cimermančič for advice on AP-MS scoring; and M. Shales for assistance in figure construction. We would kindly thank S.J. Kim for help in collecting SAXS profiles and D. Schneidman for her assistance in generating the HIV E3 model and analyzing the SAXS data using the AllosMod-FoXS server. The following reagents were obtained through the NIH AIDS Reagent Program, Division of AIDS, NIAID, NIH: Jurkat Clone E6-1 from Dr. A. Weiss and Jurkat T cells CYPA −/− from Drs. D. Braaten and J. Luban. J.R.K. was supported by an NSF graduate research fellowship. This work was supported by NIH grants to N.J.K (P50 GM082250, P50 GM081879, and P01 AI090935) and to R.S.H. (R01 AI064046 and P01 GM091743) and a grant from the Icelandic Research Fund to V.A. (141085-051). Publisher Copyright: © 2015 The Authors.

PY - 2015/5/26

Y1 - 2015/5/26

N2 - HIV-1 encodes the accessory protein Vif, which hijacks a host Cullin-RING ubiquitin ligase (CRL) complex as well as the non-canonical cofactor CBFβ, to antagonize APOBEC3 antiviral proteins. Non-canonical cofactor recruitment to CRL complexes by viral factors, to date, has only been attributed to HIV-1 Vif. To further study this phenomenon, we employed a comparative approach combining proteomic, biochemical, structural, and virological techniques to investigate Vif complexes across the lentivirus genus, including primate (HIV-1 and simian immunodeficiency virus macaque [SIVmac]) and non-primate (FIV, BIV, and MVV) viruses. We find that CBFβ is completely dispensable for the activity of non-primate lentiviral Vif proteins. Furthermore, we find that BIV Vif requires no cofactor and that MVV Vif requires a novel cofactor, cyclophilin A (CYPA), for stable CRL complex formation and anti-APOBEC3 activity. We propose modular conservation of Vif complexes allows for potential exaptation of functions through the acquisition of non-CRL-associated host cofactors while preserving anti-APOBEC3 activity.

AB - HIV-1 encodes the accessory protein Vif, which hijacks a host Cullin-RING ubiquitin ligase (CRL) complex as well as the non-canonical cofactor CBFβ, to antagonize APOBEC3 antiviral proteins. Non-canonical cofactor recruitment to CRL complexes by viral factors, to date, has only been attributed to HIV-1 Vif. To further study this phenomenon, we employed a comparative approach combining proteomic, biochemical, structural, and virological techniques to investigate Vif complexes across the lentivirus genus, including primate (HIV-1 and simian immunodeficiency virus macaque [SIVmac]) and non-primate (FIV, BIV, and MVV) viruses. We find that CBFβ is completely dispensable for the activity of non-primate lentiviral Vif proteins. Furthermore, we find that BIV Vif requires no cofactor and that MVV Vif requires a novel cofactor, cyclophilin A (CYPA), for stable CRL complex formation and anti-APOBEC3 activity. We propose modular conservation of Vif complexes allows for potential exaptation of functions through the acquisition of non-CRL-associated host cofactors while preserving anti-APOBEC3 activity.

UR - http://www.scopus.com/inward/record.url?scp=84929953567&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84929953567&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2015.04.038

DO - 10.1016/j.celrep.2015.04.038

M3 - Article

C2 - 25981045

AN - SCOPUS:84929953567

SN - 2211-1247

VL - 11

SP - 1236

EP - 1250

JO - Cell Reports

JF - Cell Reports

IS - 8

ER -

Lineage-Specific Viral Hijacking of Non-canonical E3Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity

Abstract

Bibliographical note

UN SDGs

Publisher link

Find It

Other files and links

Fingerprint

Cite this