Role of T cells during the cerebral infection with Trypanosoma brucei.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
09 2021
Historique:
received: 22 03 2021
accepted: 25 08 2021
revised: 21 10 2021
pubmed: 30 9 2021
medline: 15 12 2021
entrez: 29 9 2021
Statut: epublish

Résumé

The infection by Trypanosoma brucei brucei (T.b.b.), a protozoan parasite, is characterized by an early-systemic stage followed by a late stage in which parasites invade the brain parenchyma in a T cell-dependent manner. Here we found that early after infection effector-memory T cells were predominant among brain T cells, whereas, during the encephalitic stage T cells acquired a tissue resident memory phenotype (TRM) and expressed PD1. Both CD4 and CD8 T cells were independently redundant for the penetration of T.b.b. and other leukocytes into the brain parenchyma. The role of lymphoid cells during the T.b.b. infection was studied by comparing T- and B-cell deficient rag1-/- and WT mice. Early after infection, parasites located in circumventricular organs, brain structures with increased vascular permeability, particularly in the median eminence (ME), paced closed to the sleep-wake regulatory arcuate nucleus of the hypothalamus (Arc). Whereas parasite levels in the ME were higher in rag1-/- than in WT mice, leukocytes were instead reduced. Rag1-/- infected mice showed increased levels of meca32 mRNA coding for a blood /hypothalamus endothelial molecule absent in the blood-brain-barrier (BBB). Both immune and metabolic transcripts were elevated in the ME/Arc of WT and rag1-/- mice early after infection, except for ifng mRNA, which levels were only increased in WT mice. Finally, using a non-invasive sleep-wake cycle assessment method we proposed a putative role of lymphocytes in mediating sleep alterations during the infection with T.b.b. Thus, the majority of T cells in the brain during the early stage of T.b.b. infection expressed an effector-memory phenotype while TRM cells developed in the late stage of infection. T cells and parasites invade the ME/Arc altering the metabolic and inflammatory responses during the early stage of infection and modulating sleep disturbances.

Identifiants

pubmed: 34587172
doi: 10.1371/journal.pntd.0009764
pii: PNTD-D-21-00411
pmc: PMC8530334
doi:

Substances chimiques

Homeodomain Proteins 0
RAG-1 protein 128559-51-3

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0009764

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

J Exp Med. 2016 Jul 25;213(8):1571-87
pubmed: 27377586
Front Immunol. 2018 Dec 11;9:2877
pubmed: 30619260
J Biol Chem. 1994 Sep 23;269(38):23757-63
pubmed: 8089148
Brain Behav Immun. 2005 Mar;19(2):127-37
pubmed: 15664785
Nat Med. 2015 Jul;21(7):688-97
pubmed: 26121195
Brain Res Bull. 2019 Feb;145:59-74
pubmed: 30016726
Nature. 2018 Oct;562(7725):63-68
pubmed: 30232458
J Biol Chem. 2011 Jul 29;286(30):26873-87
pubmed: 21622562
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19408-13
pubmed: 20962277
Brain Res Rev. 2007 Nov;56(1):119-47
pubmed: 17659349
J Neurosci. 2013 Sep 4;33(36):14288-300
pubmed: 24005282
Am J Trop Med Hyg. 2010 Jun;82(6):983-90
pubmed: 20519589
Brain Res Bull. 1995;37(2):123-9
pubmed: 7606487
J Sleep Res. 2021 Jun;30(3):e13187
pubmed: 32902030
Nat Commun. 2019 Feb 19;10(1):837
pubmed: 30783092
J Exp Med. 2004 Feb 16;199(4):559-65
pubmed: 14769854
J Neurosci. 2009 Mar 25;29(12):3885-96
pubmed: 19321785
Acta Neuropathol. 2010 Dec;120(6):689-705
pubmed: 20830478
Infect Immun. 2002 Jan;70(1):185-91
pubmed: 11748181
Neuropathol Appl Neurobiol. 2009 Jun;35(3):232-46
pubmed: 19473292
Nature. 2013 Apr 11;496(7444):238-42
pubmed: 23535595
Front Cell Neurosci. 2015 Mar 12;9:80
pubmed: 25814932
J Biol Rhythms. 2012 Feb;27(1):48-58
pubmed: 22306973
Cell Metab. 2013 Apr 2;17(4):607-17
pubmed: 23562080
Lancet Neurol. 2015 Mar;14(3):318-28
pubmed: 25728441
J Neurosci Res. 1988 Sep;21(1):56-61
pubmed: 3216412
Autoimmun Rev. 2018 Sep;17(9):906-911
pubmed: 30005862
Eur J Immunol. 1994 Sep;24(9):2213-8
pubmed: 7916297
Front Neuroanat. 2018 Feb 27;12:13
pubmed: 29535612
Nature. 1991 Sep 12;353(6340):180-4
pubmed: 1832488
J Infect Dis. 2012 Jan 15;205(2):320-32
pubmed: 22116836
Curr Top Microbiol Immunol. 2002;265:227-57
pubmed: 12014192
Nat Immunol. 2015 Apr;16(4):406-14
pubmed: 25706747
Nat Neurosci. 2011 Oct 09;14(11):1418-20
pubmed: 21983682
Proc Natl Acad Sci U S A. 2010 Oct 19;107(42):17872-9
pubmed: 20923878
Prog Neurobiol. 2010 Jun;91(2):152-71
pubmed: 19995590
J Immunol. 2014 Apr 1;192(7):2961-4
pubmed: 24600038
Cell. 2015 May 7;161(4):737-49
pubmed: 25957682
PLoS Negl Trop Dis. 2016 Dec 21;10(12):e0005242
pubmed: 28002454
Nat Protoc. 2014 Jan;9(1):209-22
pubmed: 24385150
Neuroscience. 2015 Apr 2;290:185-95
pubmed: 25595977
J Autoimmun. 2019 Jun;100:1-6
pubmed: 30948158
Neuron. 2020 Jul 22;107(2):306-319.e9
pubmed: 32407670
J Biol Chem. 1996 Dec 20;271(51):32529-37
pubmed: 8955077
PLoS Pathog. 2016 Feb 25;12(2):e1005442
pubmed: 26915097
J Infect Dis. 2009 Nov 15;200(10):1556-65
pubmed: 19827943
J Clin Invest. 2004 Sep;114(5):689-94
pubmed: 15343387
J Virol. 2016 May 27;90(12):5785-96
pubmed: 27053560
Science. 2003 Apr 11;300(5617):339-42
pubmed: 12690202
Nat Rev Immunol. 2015 Aug;15(8):486-99
pubmed: 26205583
Front Neurosci. 2015 Oct 27;9:390
pubmed: 26578857
Nat Commun. 2013;4:2049
pubmed: 23804023
Front Biosci. 2008 May 01;13:4529-43
pubmed: 18508527
Neurosci Lett. 2011 Jan 7;487(2):187-90
pubmed: 20951768
PLoS Negl Trop Dis. 2017 Aug 18;11(8):e0005854
pubmed: 28821016
Cell Metab. 2015 Jan 6;21(1):65-80
pubmed: 25565206
J Comp Neurol. 2013 Oct 15;521(15):3389-405
pubmed: 23649873
Nat Immunol. 2013 Dec;14(12):1294-301
pubmed: 24162776
Physiol Genomics. 2007 Jan 17;28(2):232-8
pubmed: 16985007
Nature. 2012 Feb 29;483(7388):227-31
pubmed: 22388819
Nature. 1992 Oct 29;359(6398):843-5
pubmed: 1279431
Sleep. 2008 Mar;31(3):348-54
pubmed: 18363311
Immunol Lett. 1995 Feb;45(1-2):53-60
pubmed: 7622189

Auteurs

Gabriela C Olivera (GC)

Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.

Leonie Vetter (L)

Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.

Chiara Tesoriero (C)

Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.

Federico Del Gallo (F)

Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.

Gustav Hedberg (G)

Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.

Juan Basile (J)

Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.

Martin E Rottenberg (ME)

Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden.

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