Identification of bacteria-derived HLA-bound peptides in melanoma

Shelly Kalaora, Adi Nagler, Deborah Nejman, Michal Alon, Chaya Barbolin, Eilon Barnea, Steven L. C. Ketelaars, Kuoyuan Cheng, Kevin Vervier, Noam Shental, Yuval Bussi, Ron Rotkopf, Ronen Levy, Gil Benedek, Sophie Trabish, Tali Dadosh, Smadar Levin-Zaidman, Leore T. Geller, Kun Wang, Polina Greenberg, Gal Yagel, Aviyah Peri, Garold Fuks, Neerupma Bhardwaj, Alexandre Reuben, Leandro Hermida, Sarah B. Johnson, Jessica R. Galloway-Peña, William C. Shropshire, Chantale Bernatchez, Cara Haymaker, Reetakshi Arora, Lior Roitman, Raya Eilam, Adina Weinberger, Maya Lotan-Pompan, Michal Lotem, Arie Admon, Yishai Levin, Trevor D. Lawley, David J. Adams, Mitchell P. Levesque, Michal J. Besser, Jacob Schachter, Ofra Golani, Eran Segal, Naama Geva-Zatorsky, Eytan Ruppin, Pia Kvistborg, Scott N. Peterson, Jennifer A. Wargo, Ravid Straussman and Yardena Samuels ()
Additional contact information
Shelly Kalaora: Weizmann Institute of Science
Adi Nagler: Weizmann Institute of Science
Deborah Nejman: Weizmann Institute of Science
Michal Alon: Weizmann Institute of Science
Chaya Barbolin: Weizmann Institute of Science
Eilon Barnea: Technion – Israel Institute of Technology
Steven L. C. Ketelaars: The Netherlands Cancer Institute
Kuoyuan Cheng: National Institutes of Health (NIH)
Kevin Vervier: Wellcome Sanger Institute
Noam Shental: Open University of Israel
Yuval Bussi: Weizmann Institute of Science
Ron Rotkopf: Weizmann Institute of Science
Ronen Levy: Weizmann Institute of Science
Gil Benedek: Hadassah Medical Center
Sophie Trabish: Weizmann Institute of Science
Tali Dadosh: Weizmann Institute of Science
Smadar Levin-Zaidman: Weizmann Institute of Science
Leore T. Geller: Weizmann Institute of Science
Kun Wang: National Institutes of Health (NIH)
Polina Greenberg: Weizmann Institute of Science
Gal Yagel: Weizmann Institute of Science
Aviyah Peri: Weizmann Institute of Science
Garold Fuks: Weizmann Institute of Science
Neerupma Bhardwaj: Technion – Israel Institute of Technology
Alexandre Reuben: The University of Texas MD Anderson Cancer Center
Leandro Hermida: National Institutes of Health (NIH)
Sarah B. Johnson: The University of Texas MD Anderson Cancer Center
Jessica R. Galloway-Peña: Texas A&M University
William C. Shropshire: MD Anderson Cancer Center
Chantale Bernatchez: The University of Texas MD Anderson Cancer Center
Cara Haymaker: The University of Texas MD Anderson Cancer Center
Reetakshi Arora: The University of Texas MD Anderson Cancer Center
Lior Roitman: Weizmann Institute of Science
Raya Eilam: Weizmann Institute of Science
Adina Weinberger: Weizmann Institute of Science
Maya Lotan-Pompan: Weizmann Institute of Science
Michal Lotem: Hadassah Hebrew University Medical Center
Arie Admon: Technion – Israel Institute of Technology
Yishai Levin: The Nancy and Stephen Grand Israel National Center for Personalized Medicine, Weizmann Institute of Science
Trevor D. Lawley: Wellcome Sanger Institute
David J. Adams: Wellcome Sanger Institute
Mitchell P. Levesque: University of Zurich Hospital, University of Zurich
Michal J. Besser: Chaim Sheba Medical Center
Jacob Schachter: Chaim Sheba Medical Center
Ofra Golani: Weizmann Institute of Science
Eran Segal: Weizmann Institute of Science
Naama Geva-Zatorsky: Technion – Israel Institute of Technology
Eytan Ruppin: National Institutes of Health (NIH)
Pia Kvistborg: The Netherlands Cancer Institute
Scott N. Peterson: Sanford Burnham Prebys Medical Discovery Institute
Jennifer A. Wargo: The University of Texas MD Anderson Cancer Center
Ravid Straussman: Weizmann Institute of Science
Yardena Samuels: Weizmann Institute of Science

Nature, 2021, vol. 592, issue 7852, 138-143

Abstract: Abstract A variety of species of bacteria are known to colonize human tumours1–11, proliferate within them and modulate immune function, which ultimately affects the survival of patients with cancer and their responses to treatment12–14. However, it is not known whether antigens derived from intracellular bacteria are presented by the human leukocyte antigen class I and II (HLA-I and HLA-II, respectively) molecules of tumour cells, or whether such antigens elicit a tumour-infiltrating T cell immune response. Here we used 16S rRNA gene sequencing and HLA peptidomics to identify a peptide repertoire derived from intracellular bacteria that was presented on HLA-I and HLA-II molecules in melanoma tumours. Our analysis of 17 melanoma metastases (derived from 9 patients) revealed 248 and 35 unique HLA-I and HLA-II peptides, respectively, that were derived from 41 species of bacteria. We identified recurrent bacterial peptides in tumours from different patients, as well as in different tumours from the same patient. Our study reveals that peptides derived from intracellular bacteria can be presented by tumour cells and elicit immune reactivity, and thus provides insight into a mechanism by which bacteria influence activation of the immune system and responses to therapy.

Date: 2021
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DOI: 10.1038/s41586-021-03368-8

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