Immunoglobulin G N-glycan markers of accelerated biological aging during chronic HIV infection

Leila B. Giron, Qin Liu, Opeyemi S. Adeniji, Xiangfan Yin, Toshitha Kannan, Jianyi Ding, David Y. Lu, Susan Langan, Jinbing Zhang, Joao L. L. C. Azevedo, Shuk Hang Li, Sergei Shalygin, Parastoo Azadi, David B. Hanna, Igho Ofotokun, Jason Lazar, Margaret A. Fischl, Sabina Haberlen, Bernard Macatangay, Adaora A. Adimora, Beth D. Jamieson, Charles Rinaldo, Daniel Merenstein, Nadia R. Roan, Olaf Kutsch, Stephen Gange, Steven M. Wolinsky, Mallory D. Witt, Wendy S. Post, Andrew Kossenkov, Alan L. Landay, Ian Frank, Phyllis C. Tien, Robert Gross, Todd T. Brown and Mohamed Abdel-Mohsen ()
Additional contact information
Leila B. Giron: The Wistar Institute
Qin Liu: The Wistar Institute
Opeyemi S. Adeniji: The Wistar Institute
Xiangfan Yin: The Wistar Institute
Toshitha Kannan: The Wistar Institute
Jianyi Ding: The Wistar Institute
David Y. Lu: The Wistar Institute
Susan Langan: Johns Hopkins University
Jinbing Zhang: Johns Hopkins University
Joao L. L. C. Azevedo: The Wistar Institute
Shuk Hang Li: University of Pennsylvania Perelman School of Medicine
Sergei Shalygin: University of Georgia
Parastoo Azadi: University of Georgia
David B. Hanna: Albert Einstein College of Medicine
Igho Ofotokun: Emory University School of Medicine
Jason Lazar: SUNY Downstate Health Sciences University
Margaret A. Fischl: University of Miami
Sabina Haberlen: Johns Hopkins University
Bernard Macatangay: University of Pittsburgh
Adaora A. Adimora: University of North Carolina
Beth D. Jamieson: Los Angeles
Charles Rinaldo: University of Pittsburgh
Daniel Merenstein: Georgetown University Medical Center
Nadia R. Roan: Gladstone Institutes
Olaf Kutsch: University of Alabama at Birmingham
Stephen Gange: Johns Hopkins University
Steven M. Wolinsky: Northwestern University
Mallory D. Witt: Lundquist Institute of Biomedical Research at Harbor-UCLA Medical Center
Wendy S. Post: Johns Hopkins University
Andrew Kossenkov: The Wistar Institute
Alan L. Landay: Rush University
Ian Frank: University of Pennsylvania Perelman School of Medicine
Phyllis C. Tien: University of California San Francisco
Robert Gross: University of Pennsylvania Perelman School of Medicine
Todd T. Brown: Johns Hopkins University
Mohamed Abdel-Mohsen: The Wistar Institute

Nature Communications, 2024, vol. 15, issue 1, 1-23

Abstract: Abstract People living with HIV (PLWH) experience increased vulnerability to premature aging and inflammation-associated comorbidities, even when HIV replication is suppressed by antiretroviral therapy (ART). However, the factors associated with this vulnerability remain uncertain. In the general population, alterations in the N-glycans on IgGs trigger inflammation and precede the onset of aging-associated diseases. Here, we investigate the IgG N-glycans in cross-sectional and longitudinal samples from 1214 women and men, living with and without HIV. PLWH exhibit an accelerated accumulation of pro-aging-associated glycan alterations and heightened expression of senescence-associated glycan-degrading enzymes compared to controls. These alterations correlate with elevated markers of inflammation and the severity of comorbidities, potentially preceding the development of such comorbidities. Mechanistically, HIV-specific antibodies glycoengineered with these alterations exhibit a reduced ability to elicit anti-HIV Fc-mediated immune activities. These findings hold potential for the development of biomarkers and tools to identify and prevent premature aging and comorbidities in PLWH.

Date: 2024
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DOI: 10.1038/s41467-024-47279-4

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