Distinct immune cell infiltration patterns in pancreatic ductal adenocarcinoma (PDAC) exhibit divergent immune cell selection and immunosuppressive mechanisms

S Shivan Sivakumar (Department of Immunology and Immunotherapy, School of Infection, Inflammation, and Immunology, College of Medicine and Health, University of Birmingham, Birmingham, United Kingdom) A Ashwin Jainarayanan E Edward Arbe-Barnes P Piyush Kumar Sharma M Maire Ni Leathlobhair S Sakina Amin D David J. Reiss L Lara Heij S Samarth Hegde A Assaf Magen F Felicia Tucci B Bo Sun S Shihong Wu N Nithishwer Mouroug Anand H Hubert Slawinski S Santiago Revale I Isar Nassiri J Jonathon Webber G Gerard D. Hoeltzel A Adam E. Frampton (Oncology Section, Surrey Cancer Research Institute, Department of Clinical and Experimental Medicine, FHMS, University of Surrey, The Leggett Building, Daphne Jackson Road, Guildford GU2 7WG, U.K.) G Georg Wiltberger U Ulf Neumann P Philip Charlton L Laura Spiers T Tim Elliott M Maria Wang S Suzana Couto (Genmab US, Inc., Building 2, 777 Scudders Mill Rd, Princeton, New Jersey 08540, United States) T Thomas Lila P Pallavur V. Sivakumar A Alexander V. Ratushny M Mark R. Middleton D Dimitra Peppa B Benjamin Fairfax M Miriam Merad M Michael L. Dustin E Enas Abu-Shah R Rachael Bashford-Rogers

Abstract

Abstract Pancreatic ductal adenocarcinoma has a dismal prognosis. A comprehensive analysis of single-cell multi-omic data from matched tumour-infiltrated CD45+ cells and peripheral blood in 12 patients, and two published datasets, reveals a complex immune infiltrate. Patients have either a myeloid-enriched or adaptive-enriched tumour microenvironment. Adaptive immune cell-enriched is intrinsically linked with highly distinct B and T cell clonal selection, diversification, and differentiation. Using TCR data, we see the largest clonal expansions in CD8 effector memory, senescent cells, and highly activated regulatory T cells which are induced within the tumour from naïve cells. We identify pathways that potentially lead to a suppressive microenvironment, including investigational targets TIGIT/PVR and SIRPA/CD47. Analysis of patients from the APACT clinical trial shows that myeloid enrichment had a shorter overall survival compared to those with adaptive cell enrichment. Strategies for rationale therapeutic development in this disease include boosting of B cell responses, targeting immunosuppressive macrophages, and specific Treg cell depletion approaches.

Article Details

Volume / Issue Vol. 16, Issue 1
Published February 06, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (37)

S

Shivan Sivakumar

Department of Immunology and Immunotherapy, School of Infection, Inflammation, and Immunology, College of Medicine and Health, University of Birmingham, Birmingham, United Kingdom

A

Ashwin Jainarayanan

E

Edward Arbe-Barnes

P

Piyush Kumar Sharma

M

Maire Ni Leathlobhair

S

Sakina Amin

D

David J. Reiss

L

Lara Heij

S

Samarth Hegde

A

Assaf Magen

F

Felicia Tucci

B

Bo Sun

S

Shihong Wu

N

Nithishwer Mouroug Anand

H

Hubert Slawinski

S

Santiago Revale

I

Isar Nassiri

J

Jonathon Webber

G

Gerard D. Hoeltzel

A

Adam E. Frampton

Oncology Section, Surrey Cancer Research Institute, Department of Clinical and Experimental Medicine, FHMS, University of Surrey, The Leggett Building, Daphne Jackson Road, Guildford GU2 7WG, U.K.

G

Georg Wiltberger

U

Ulf Neumann

P

Philip Charlton

L

Laura Spiers

T

Tim Elliott

M

Maria Wang

S

Suzana Couto

Genmab US, Inc., Building 2, 777 Scudders Mill Rd, Princeton, New Jersey 08540, United States

T

Thomas Lila

P

Pallavur V. Sivakumar

A

Alexander V. Ratushny

M

Mark R. Middleton

D

Dimitra Peppa

B

Benjamin Fairfax

M

Miriam Merad

M

Michael L. Dustin

E

Enas Abu-Shah

R

Rachael Bashford-Rogers