Interferon-α promotes HLA-B-restricted presentation of conventional and alternative antigens in human pancreatic β-cells

A Alexia Carré F Fatoumata Samassa Z Zhicheng Zhou J Javier Perez-Hernandez C Christiana Lekka A Anthony Manganaro M Masaya Oshima H Hanqing Liao R Robert Parker A Annalisa Nicastri B Barbara Brandao M Maikel L. Colli D Decio L. Eizirik J Jahnavi Aluri D Deep Patel M Marcus Göransson O Orlando Burgos Morales A Amanda Anderson L Laurie Landry F Farah Kobaisi R Raphael Scharfmann L Lorella Marselli P Piero Marchetti S Sylvaine You M Maki Nakayama (Cardiovascular Research Institute, Weill Cornell Medicine) S Sine R. Hadrup S Sally C. Kent S Sarah J. Richardson N Nicola Ternette R Roberto Mallone

Abstract

Abstract Interferon (IFN)-α is the earliest cytokine signature observed in individuals at risk for type 1 diabetes (T1D), but the effect of IFN-α on the antigen repertoire of HLA Class I (HLA-I) in pancreatic β-cells is unknown. Here we characterize the HLA-I antigen presentation in resting and IFN-α-exposed β-cells and find that IFN-α increases HLA-I expression and expands peptide repertoire to those derived from alternative mRNA splicing, protein cis-splicing and post-translational modifications. While the resting β-cell immunopeptidome is dominated by HLA-A-restricted peptides, IFN-α largely favors HLA-B and only marginally upregulates HLA-A, translating into increased HLA-B-restricted peptide presentation and activation of HLA-B-restricted CD8+ T cells. Lastly, islets of patients with T1D show preferential HLA-B hyper-expression when compared with non-diabetic donors, and islet-infiltrating CD8+ T cells reactive to HLA-B-restricted granule peptides are found in T1D donors. Thus, the inflammatory milieu of insulitis may skew the autoimmune response toward alternative epitopes presented by HLA-B, hence recruiting T cells with a distinct repertoire that may be relevant to T1D pathogenesis.

Article Details

Volume / Issue Vol. 16, Issue 1
Published January 17, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (30)

A

Alexia Carré

F

Fatoumata Samassa

Z

Zhicheng Zhou

J

Javier Perez-Hernandez

C

Christiana Lekka

A

Anthony Manganaro

M

Masaya Oshima

H

Hanqing Liao

R

Robert Parker

A

Annalisa Nicastri

B

Barbara Brandao

M

Maikel L. Colli

D

Decio L. Eizirik

J

Jahnavi Aluri

D

Deep Patel

M

Marcus Göransson

O

Orlando Burgos Morales

A

Amanda Anderson

L

Laurie Landry

F

Farah Kobaisi

R

Raphael Scharfmann

L

Lorella Marselli

P

Piero Marchetti

S

Sylvaine You

M

Maki Nakayama

Cardiovascular Research Institute, Weill Cornell Medicine

S

Sine R. Hadrup

S

Sally C. Kent

S

Sarah J. Richardson

N

Nicola Ternette

R

Roberto Mallone