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Anti-PD-1 immunotherapy leads to tuberculosis reactivation via dysregulation of TNF-α

Anti-PD-1 immunotherapy leads to tuberculosis reactivation via dysregulation of TNF-α
Anti-PD-1 immunotherapy leads to tuberculosis reactivation via dysregulation of TNF-α
Previously, we developed a 3-dimensional cell culture model of human tuberculosis (TB) and demonstrated its potential to interrogate the host-pathogen interaction (Tezera et al., 2017a). Here, we use the model to investigate mechanisms whereby immune checkpoint therapy for cancer paradoxically activates TB infection. In patients, PD-1 is expressed in Mycobacterium tuberculosis (Mtb)-infected lung tissue but is absent in areas of immunopathology. In the microsphere model, PD-1 ligands are up-regulated by infection, and the PD-1/PD-L1 axis is further induced by hypoxia. Inhibition of PD-1 signalling increases Mtb growth, and augments cytokine secretion. TNF-α is responsible for accelerated Mtb growth, and TNF-α neutralisation reverses augmented Mtb growth caused by anti-PD-1 treatment. In human TB, pulmonary TNF-α immunoreactivity is increased and circulating PD-1 expression negatively correlates with sputum TNF-α concentrations. Together, our findings demonstrate that PD-1 regulates the immune response in TB, and inhibition of PD-1 accelerates Mtb growth via excessive TNF-α secretion.
2050-084X
Tezera, Liku B.
c5598dbf-23a8-4934-96a4-7c783bf9e776
Bielecka, Magdalena K
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Ogongo, Paul
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Walker, Naomi F.
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Ellis, Matthew
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Garay-Baquero, Diana J.
da9136fe-3d47-4d04-8ab3-96bfe17a773c
Thomas, Kristian
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Reichmann, Michaela T.
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Johnston, David A.
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Wilkinson, Katalin Andrea
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Ahmed, Mohamed
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Jogai, Sanjay
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Jayasinghe, Suwan N.
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Wilkinson, Robert J.
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Mansour, Salah
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Thomas, Gareth J.
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Ottensmeier, Christian H.
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Leslie, Alasdair
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Elkington, Paul T.
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Tezera, Liku B.
c5598dbf-23a8-4934-96a4-7c783bf9e776
Bielecka, Magdalena K
90391ea3-aa1f-4104-a893-568c138718a2
Ogongo, Paul
8ad3eded-41c5-4a27-b5a4-aa0e924b23ae
Walker, Naomi F.
e586ffdf-ae4b-46fa-83a1-db72501d17c1
Ellis, Matthew
afbca752-ced4-40dd-b0af-d9ecffbd5b63
Garay-Baquero, Diana J.
da9136fe-3d47-4d04-8ab3-96bfe17a773c
Thomas, Kristian
e9b90898-c510-43a0-af9a-4ddf24345e80
Reichmann, Michaela T.
d887f227-13a8-4384-a1c5-d3c229cd0642
Johnston, David A.
b41163c9-b9d2-425c-af99-2a357204014e
Wilkinson, Katalin Andrea
535eb90d-f8fc-4f97-b590-34005b45f03e
Ahmed, Mohamed
dadd35d9-b0c3-423e-a322-7dabee95bd9d
Jogai, Sanjay
18c2f36b-4572-46d5-b17d-a6d2cdaa916c
Jayasinghe, Suwan N.
49b9ed49-c926-4e85-8a85-bc38bcb9a155
Wilkinson, Robert J.
efcf7079-ebfa-4270-b7a4-a578ffd91178
Mansour, Salah
4aecba5a-8387-4f7b-b766-0a9c309ccb8b
Thomas, Gareth J.
2ff54aa9-a766-416b-91ee-cf1c5be74106
Ottensmeier, Christian H.
42b8a398-baac-4843-a3d6-056225675797
Leslie, Alasdair
967978bd-5a04-4b8a-8339-3dea7daf9a80
Elkington, Paul T.
60828c7c-3d32-47c9-9fcc-6c4c54c35a15

Tezera, Liku B., Bielecka, Magdalena K, Ogongo, Paul, Walker, Naomi F., Ellis, Matthew, Garay-Baquero, Diana J., Thomas, Kristian, Reichmann, Michaela T., Johnston, David A., Wilkinson, Katalin Andrea, Ahmed, Mohamed, Jogai, Sanjay, Jayasinghe, Suwan N., Wilkinson, Robert J., Mansour, Salah, Thomas, Gareth J., Ottensmeier, Christian H., Leslie, Alasdair and Elkington, Paul T. (2020) Anti-PD-1 immunotherapy leads to tuberculosis reactivation via dysregulation of TNF-α. eLife, 9, [e52668]. (doi:10.7554/eLife.52668).

Record type: Article

Abstract

Previously, we developed a 3-dimensional cell culture model of human tuberculosis (TB) and demonstrated its potential to interrogate the host-pathogen interaction (Tezera et al., 2017a). Here, we use the model to investigate mechanisms whereby immune checkpoint therapy for cancer paradoxically activates TB infection. In patients, PD-1 is expressed in Mycobacterium tuberculosis (Mtb)-infected lung tissue but is absent in areas of immunopathology. In the microsphere model, PD-1 ligands are up-regulated by infection, and the PD-1/PD-L1 axis is further induced by hypoxia. Inhibition of PD-1 signalling increases Mtb growth, and augments cytokine secretion. TNF-α is responsible for accelerated Mtb growth, and TNF-α neutralisation reverses augmented Mtb growth caused by anti-PD-1 treatment. In human TB, pulmonary TNF-α immunoreactivity is increased and circulating PD-1 expression negatively correlates with sputum TNF-α concentrations. Together, our findings demonstrate that PD-1 regulates the immune response in TB, and inhibition of PD-1 accelerates Mtb growth via excessive TNF-α secretion.

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More information

Accepted/In Press date: 19 February 2020
e-pub ahead of print date: 24 February 2020
Published date: 5 March 2020

Identifiers

Local EPrints ID: 438296
URI: http://eprints.soton.ac.uk/id/eprint/438296
ISSN: 2050-084X
PURE UUID: 2da789b6-89a8-4a73-870a-29cb0480e360
ORCID for Liku B. Tezera: ORCID iD orcid.org/0000-0002-7898-6709
ORCID for Diana J. Garay-Baquero: ORCID iD orcid.org/0000-0002-9450-8504
ORCID for Michaela T. Reichmann: ORCID iD orcid.org/0000-0002-3015-9827
ORCID for David A. Johnston: ORCID iD orcid.org/0000-0001-6703-6014
ORCID for Salah Mansour: ORCID iD orcid.org/0000-0002-5982-734X
ORCID for Paul T. Elkington: ORCID iD orcid.org/0000-0003-0390-0613

Catalogue record

Date deposited: 04 Mar 2020 17:33
Last modified: 12 Nov 2024 03:01

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Contributors

Author: Liku B. Tezera ORCID iD
Author: Magdalena K Bielecka
Author: Paul Ogongo
Author: Naomi F. Walker
Author: Matthew Ellis
Author: Diana J. Garay-Baquero ORCID iD
Author: Kristian Thomas
Author: Michaela T. Reichmann ORCID iD
Author: David A. Johnston ORCID iD
Author: Katalin Andrea Wilkinson
Author: Mohamed Ahmed
Author: Sanjay Jogai
Author: Suwan N. Jayasinghe
Author: Robert J. Wilkinson
Author: Salah Mansour ORCID iD
Author: Alasdair Leslie

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