Reconstitution of EBV-directed T cell immunity by adoptive transfer of peptide-stimulated T cells in a patient after allogeneic stem cell transplantation for AITL.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
04 2022
Historique:
received: 16 12 2021
accepted: 31 03 2022
revised: 04 05 2022
pubmed: 23 4 2022
medline: 7 5 2022
entrez: 22 4 2022
Statut: epublish

Résumé

Reconstitution of the T cell repertoire after allogeneic stem cell transplantation is a long and often incomplete process. As a result, reactivation of Epstein-Barr virus (EBV) is a frequent complication that may be treated by adoptive transfer of donor-derived EBV-specific T cells. We generated donor-derived EBV-specific T cells by stimulation with peptides representing defined epitopes covering multiple HLA restrictions. T cells were adoptively transferred to a patient who had developed persisting high titers of EBV after allogeneic stem cell transplantation for angioimmunoblastic T-cell lymphoma (AITL). T cell receptor beta (TCRβ) deep sequencing showed that the T cell repertoire of the patient early after transplantation (day 60) was strongly reduced and only very low numbers of EBV-specific T cells were detectable. Manufacturing and in vitro expansion of donor-derived EBV-specific T cells resulted in enrichment of EBV epitope-specific, HLA-restricted T cells. Monitoring of T cell clonotypes at a molecular level after adoptive transfer revealed that the dominant TCR sequences from peptide-stimulated T cells persisted long-term and established an EBV-specific TCR clonotype repertoire in the host, with many of the EBV-specific TCRs present in the donor. This reconstituted repertoire was associated with immunological control of EBV and with lack of further AITL relapse.

Identifiants

pubmed: 35452490
doi: 10.1371/journal.ppat.1010206
pii: PPATHOGENS-D-21-02534
pmc: PMC9067708
doi:

Substances chimiques

Epitopes 0
Peptides 0
Peptide T 106362-33-8

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010206

Déclaration de conflit d'intérêts

I have read the journal’s policy and the authors of this manuscript have the following competing interests: AMo receives project funding from Biosyngen Pte. Ltd. for preclinical development of EBV-specific TCRs not related to this study.

Références

J Virol. 2006 Nov;80(21):10357-64
pubmed: 17041216
Curr Opin Oncol. 2014 Nov;26(6):677-83
pubmed: 25162331
Br J Cancer. 2018 Feb 20;118(4):534-545
pubmed: 29360818
Int J Hematol. 2019 Apr;109(4):499-504
pubmed: 30604313
Nat Med. 2013 Mar;19(3):372-7
pubmed: 23435170
Biol Blood Marrow Transplant. 2009 Jul;15(7):795-803
pubmed: 19539210
PLoS Pathog. 2012 Sep;8(9):e1002889
pubmed: 23028307
Infection. 2008 Mar;36(2):158-62
pubmed: 18379728
Blood. 2010 Apr 8;115(14):2960-70
pubmed: 20103780
Blood. 2010 Feb 4;115(5):925-35
pubmed: 19880495
Br J Haematol. 2019 Oct;187(2):206-218
pubmed: 31219185
Eur J Immunol. 2004 Sep;34(9):2500-9
pubmed: 15307182
Haematologica. 2016 Jul;101(7):803-11
pubmed: 27365460
Cancer Res. 2012 Mar 1;72(5):1116-25
pubmed: 22282657
Bone Marrow Transplant. 2020 Sep;55(9):1754-1762
pubmed: 32066862
Cytotherapy. 2019 Sep;21(9):935-942
pubmed: 31320195
J Exp Med. 2006 Apr 17;203(4):995-1006
pubmed: 16549597
Blood. 1992 Oct 1;80(7):1804-12
pubmed: 1327284
Clin Case Rep. 2021 May 05;9(5):e04083
pubmed: 34084501
PLoS Pathog. 2014 Aug 28;10(8):e1004333
pubmed: 25165855
Oncoimmunology. 2021 Aug 2;10(1):1955545
pubmed: 34377592
J Transl Med. 2018 May 9;16(1):124
pubmed: 29743075
Molecules. 2019 Mar 12;24(5):
pubmed: 30871092
Blood. 2003 Jun 1;101(11):4290-7
pubmed: 12576337
Hematol Oncol. 2020 Aug;38(3):272-276
pubmed: 32083758
Biol Blood Marrow Transplant. 2004 Mar;10(3):143-55
pubmed: 14993880
Nature. 1999 Oct 14;401(6754):708-12
pubmed: 10537110
Int J Cancer. 2002 May 1;99(1):93-9
pubmed: 11948498
J Cell Biol. 1991 Jul;114(2):343-9
pubmed: 1712790
J Clin Exp Hematop. 2010;50(1):59-63
pubmed: 20505277
J Exp Med. 1997 May 5;185(9):1605-17
pubmed: 9151898
Ther Adv Hematol. 2020 Apr 28;11:2040620720910964
pubmed: 32523657
Curr Top Microbiol Immunol. 2001;258:221-9
pubmed: 11443864
J Virol. 2001 Sep;75(18):8649-59
pubmed: 11507210
Am J Transplant. 2015 Aug;15(8):2170-9
pubmed: 25873100
Clin Infect Dis. 2006 Jun 15;42(12):1743-8
pubmed: 16705581
J Immunol. 2000 Nov 1;165(9):4831-41
pubmed: 11046006
Blood. 2002 Dec 1;100(12):4059-66
pubmed: 12393655
Nat Rev Clin Oncol. 2012 Sep;9(9):510-9
pubmed: 22801669
Blood. 2001 Aug 15;98(4):972-8
pubmed: 11493441
Leukemia. 2003 Dec;17(12):2257-317
pubmed: 14671650
J Biol Chem. 2007 Aug 17;282(33):23799-810
pubmed: 17540778
Blood. 1992 Apr 1;79(7):1789-95
pubmed: 1373088
J Immunol. 1999 Feb 1;162(3):1827-35
pubmed: 9973448
J Clin Invest. 2020 Feb 3;130(2):733-747
pubmed: 31689242
Blood. 2004 Feb 15;103(4):1408-16
pubmed: 14563644
Br J Haematol. 2007 Jul;138(1):44-53
pubmed: 17555446
Bone Marrow Transplant. 2013 Nov;48(11):1465-71
pubmed: 23749107
J Am Acad Dermatol. 2019 Oct;81(4):989-997
pubmed: 30240776
Bone Marrow Transplant. 2020 Jan;55(1):25-39
pubmed: 31089285
Annu Rev Immunol. 1997;15:405-31
pubmed: 9143694
Cancer Cell. 2014 Oct 13;26(4):565-76
pubmed: 25220446
PLoS One. 2013 Oct 25;8(10):e78686
pubmed: 24205294
J Virol. 1993 Dec;67(12):7428-35
pubmed: 7693972
J Clin Invest. 2005 Sep;115(9):2546-55
pubmed: 16110323
J Immunother Cancer. 2021 Jul;9(7):
pubmed: 34210819
J Exp Med. 1995 Jun 1;181(6):2221-8
pubmed: 7539044
Ann Transl Med. 2015 Apr;3(5):62
pubmed: 25992361
Hematol Rep. 2017 Sep 27;9(3):7088
pubmed: 29071053
Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10391-6
pubmed: 10468618
J Virol. 1995 Aug;69(8):4872-9
pubmed: 7609055
Biol Blood Marrow Transplant. 2017 Sep;23(9):1437-1446
pubmed: 28495643
Cancer Med. 2020 Jan;9(2):678-688
pubmed: 31793218
J Gen Virol. 1994 Sep;75 ( Pt 9):2489-93
pubmed: 7521394
J Clin Oncol. 2013 Jan 1;31(1):39-48
pubmed: 23169501
J Exp Med. 1996 Nov 1;184(5):1791-800
pubmed: 8920867
J Immunol. 2005 Sep 15;175(6):3826-34
pubmed: 16148129
Blood. 2014 Oct 16;124(16):2514-22
pubmed: 25185261
PLoS Pathog. 2014 May 22;10(5):e1004068
pubmed: 24853673
Antivir Ther. 2004 Jun;9(3):453-9
pubmed: 15259909
Int Immunol. 2006 Apr;18(4):591-601
pubmed: 16507598
J Immunol. 2002 Aug 15;169(4):2172-9
pubmed: 12165547
Science. 1992 Jul 10;257(5067):238-41
pubmed: 1352912
Hum Gene Ther. 2021 Sep;32(17-18):919-935
pubmed: 33798008
BMC Immunol. 2021 Sep 28;22(1):65
pubmed: 34583647
Front Immunol. 2018 Oct 04;9:2291
pubmed: 30337929
J Immunol. 2011 Jun 15;186(12):7039-49
pubmed: 21555537
Eur J Immunol. 2000 Sep;30(9):2531-9
pubmed: 11009086

Auteurs

María Fernanda Lammoglia Cobo (MF)

Department of Hematology, Oncology, and Tumor Immunology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Julia Ritter (J)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Regina Gary (R)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Volkhard Seitz (V)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
HS Diagnomics GmbH, Berlin, Germany.

Josef Mautner (J)

Department of Medicine III, LMU-Klinikum, Munich, Germany.
German Centre for Infection Research, Munich, Germany.

Michael Aigner (M)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Simon Völkl (S)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Stefanie Schaffer (S)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Stephanie Moi (S)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Anke Seegebarth (A)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Heiko Bruns (H)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Wolf Rösler (W)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Kerstin Amann (K)

Department of Nephropathology, Institute of Pathology, University of Erlangen, Erlangen, Germany.

Maike Büttner-Herold (M)

Department of Nephropathology, Institute of Pathology, University of Erlangen, Erlangen, Germany.

Steffen Hennig (S)

HS Diagnomics GmbH, Berlin, Germany.

Andreas Mackensen (A)

Department of Internal Medicine 5 -Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany.

Michael Hummel (M)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Andreas Moosmann (A)

Department of Medicine III, LMU-Klinikum, Munich, Germany.
German Centre for Infection Research, Munich, Germany.

Armin Gerbitz (A)

Division of Medical Oncology and Hematology, Princess Margaret Cancer Center, Toronto, Ontario, Canada.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH