Effector Memory-Expressing CD45RA (TEMRA) CD8
adhesion molecule
cell activation
cell adhesion
chemokine
chronic allograft rejection
endothelium
immunology
kidney transplantation
lymphocytes
purinergic P2X4 receptors
Journal
Journal of the American Society of Nephrology : JASN
ISSN: 1533-3450
Titre abrégé: J Am Soc Nephrol
Pays: United States
ID NLM: 9013836
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
10
03
2022
accepted:
22
08
2022
pubmed:
25
10
2022
medline:
3
12
2022
entrez:
24
10
2022
Statut:
ppublish
Résumé
The mechanisms regulating CD8 We used single-cell proteomic profiling and functional testing of CD8 We showed that humoral rejection of a kidney allograft is associated with an accumulation of cytolytic TEMRA CD8 Our findings highlight the active role of TEMRA CD8
Sections du résumé
BACKGROUND
The mechanisms regulating CD8
METHODS
We used single-cell proteomic profiling and functional testing of CD8
RESULTS
We showed that humoral rejection of a kidney allograft is associated with an accumulation of cytolytic TEMRA CD8
CONCLUSIONS
Our findings highlight the active role of TEMRA CD8
Identifiants
pubmed: 36280286
pii: 00001751-202212000-00010
doi: 10.1681/ASN.2022030286
pmc: PMC9731633
doi:
Substances chimiques
P-Selectin
0
Receptors, Purinergic P2X4
0
Leukocyte Common Antigens
EC 3.1.3.48
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2211-2231Investigateurs
Gilles Blancho
(G)
Julien Branchereau
(J)
Diego Cantarovich
(D)
Agnès Chapelet
(A)
Jacques Dantal
(J)
Clément Deltombe
(C)
Lucile Figueres
(L)
Claire Garandeau
(C)
Magali Giral
(M)
Caroline Gourraud-Vercel
(C)
Maryvonne Hourmant
(M)
Georges Karam
(G)
Clarisse Kerleau
(C)
Christophe Masset
(C)
Delphine Kervela
(D)
Sabine Lebot
(S)
Aurélie Meurette
(A)
Simon Ville
(S)
Christine Kandell
(C)
Anne Moreau
(A)
Karine Renaudin
(K)
Anne Cesbron
(A)
Florent Delbos
(F)
Alexandre Walencik
(A)
Anne Devis
(A)
Informations de copyright
Copyright © 2022 by the American Society of Nephrology.
Références
Kapoor R, Ho P-R, Campbell N, Chang I, Deykin A, Forrestal F, et al.; ASCEND investigators: Effect of natalizumab on disease progression in secondary progressive multiple sclerosis (ASCEND): A phase 3, randomised, double-blind, placebo-controlled trial with an open-label extension. Lancet Neurol 17: 405–415, 2018
Lebwohl M, Tyring SK, Hamilton TK, Toth D, Glazer S, Tawfik NH, et al.; Efalizumab Study Group: A novel targeted T-cell modulator, efalizumab, for plaque psoriasis. N Engl J Med 349: 2004–2013, 2003
Feagan BG, Rutgeerts P, Sands BE, Hanauer S, Colombel J-F, Sandborn WJ, et al.; GEMINI 1 Study Group: Vedolizumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med 369: 699–710, 2013
Sandborn WJ, Feagan BG, Rutgeerts P, Hanauer S, Colombel J-F, Sands BE, et al.; GEMINI 2 Study Group: Vedolizumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med 369: 711–721, 2013
Schulz O, Hammerschmidt SI, Moschovakis GL, Förster R: Chemokines and chemokine receptors in lymphoid tissue dynamics. Annu Rev Immunol 34: 203–242, 2016
Randolph GJ, Ivanov S, Zinselmeyer BH, Scallan JP: The lymphatic system: Integral roles in immunity. Annu Rev Immunol 35: 31–52, 2017
Mueller SN, Gebhardt T, Carbone FR, Heath WR: Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 31: 137–161, 2013
Abram CL, Lowell CA: The ins and outs of leukocyte integrin signaling. Annu Rev Immunol 27: 339–362, 2009
Lowe JB: Glycosylation in the control of selectin counter-receptor structure and function. Immunol Rev 186: 19–36, 2002
Ledderose C, Liu K, Kondo Y, Slubowski CJ, Dertnig T, Denicoló S, et al.: Purinergic P2X4 receptors and mitochondrial ATP production regulate T cell migration. J Clin Invest 128: 3583–3594, 2018
McKinney EF, Lyons PA, Carr EJ, Hollis JL, Jayne DRW, Willcocks LC, et al.: A CD8+ T cell transcription signature predicts prognosis in autoimmune disease. Nat Med 16: 586–591, 2010
McKinney EF, Lee JC, Jayne DRW, Lyons PA, Smith KGC: T-cell exhaustion, co-stimulation and clinical outcome in autoimmunity and infection. Nature 523: 612–616, 2015
Néel A, Bucchia M, Néel M, Tilly G, Caristan A, Yap M, et al.: Dampening of CD8+ T cell response by B cell depletion therapy in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol 71: 641–650, 2019
Tasaki S, Suzuki K, Nishikawa A, Kassai Y, Takiguchi M, Kurisu R, et al.: Multiomic disease signatures converge to cytotoxic CD8 T cells in primary Sjögren’s syndrome. Ann Rheum Dis 76: 1458–1466, 2017
Fuschiotti P, Medsger Jr. TA, Morel PA: Effector CD8+ T cells in systemic sclerosis patients produce abnormally high levels of interleukin-13 associated with increased skin fibrosis. Arthritis Rheum 60: 1119–1128, 2009
Gross CC, Meyer C, Bhatia U, Yshii L, Kleffner I, Bauer J, et al.: CD8 + T cell-mediated endotheliopathy is a targetable mechanism of neuro-inflammation in Susac syndrome. Nat Commun 10: 5779, 2019
Yap M, Boeffard F, Clave E, Pallier A, Danger R, Giral M, et al.: Expansion of highly differentiated cytotoxic terminally differentiated effector memory CD8+ T cells in a subset of clinically stable kidney transplant recipients: A potential marker for late graft dysfunction. J Am Soc Nephrol 25: 1856–1868, 2014
Jacquemont L, Tilly G, Yap M, Doan-Ngoc T-M, Danger R, Guérif P, et al.: Terminally differentiated effector memory CD8 + T cells identify kidney transplant recipients at high risk of graft failure. J Am Soc Nephrol 31: 876–891, 2020
Setoguchi R: IL-15 boosts the function and migration of human terminally differentiated CD8+ T cells by inducing a unique gene signature. Int Immunol 28: 293–305, 2016
Tilly G, Doan-Ngoc T-M, Yap M, Caristan A, Jacquemont L, Danger R, et al.: IL-15 harnesses pro-inflammatory function of TEMRA CD8 in kidney-transplant recipients. Front Immunol 8: 778, 2017
Trombetta JJ, Gennert D, Lu D, Satija R, Shalek AK, Regev A: Preparation of single-cell RNA-seq libraries for next generation sequencing. Curr Protoc Mol Biol 107: 4.22.1–4.22.17, 2014
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al.: Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578, 2012
Law CW, Chen Y, Shi W, Smyth GK: voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 15: R29, 2014
Yu G, Wang L-G, Han Y, He Q-Y: clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS 16: 284–287, 2012
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al.: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545–15550, 2005
Creelan BC, Wang C, Teer JK, Toloza EM, Yao J, Kim S, et al.: Tumor-infiltrating lymphocyte treatment for anti-PD-1-resistant metastatic lung cancer: A phase 1 trial. Nat Med 27: 1410–1418, 2021
Spiegel JY, Patel S, Muffly L, Hossain NM, Oak J, Baird JH, et al.: CAR T cells with dual targeting of CD19 and CD22 in adult patients with recurrent or refractory B cell malignancies: A phase 1 trial. Nat Med 27: 1419–1431, 2021
Lee JB, Khan DH, Hurren R, Xu M, Na Y, Kang H, et al.: Venetoclax enhances T cell-mediated antileukemic activity by increasing ROS production. Blood 138: 234–245, 2021
Rossi J, Paczkowski P, Shen Y-W, Morse K, Flynn B, Kaiser A, et al.: Preinfusion polyfunctional anti-CD19 chimeric antigen receptor T cells are associated with clinical outcomes in NHL. Blood 132: 804–814, 2018
Xue Q, Bettini E, Paczkowski P, Ng C, Kaiser A, McConnell T, et al.: Single-cell multiplexed cytokine profiling of CD19 CAR-T cells reveals a diverse landscape of polyfunctional antigen-specific response. J Immunother Cancer 5: 85, 2017
Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, et al.: QuPath: Open source software for digital pathology image analysis. Sci Rep 7: 16878, 2017
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al.: Fiji: An open-source platform for biological-image analysis. Nat Methods 9: 676–682, 2012
Rieckmann JC, Geiger R, Hornburg D, Wolf T, Kveler K, Jarrossay D, et al.: Social network architecture of human immune cells unveiled by quantitative proteomics. Nat Immunol 18: 583–593, 2017
Buggert M, Vella LA, Nguyen S, Wu VH, Chen Z, Sekine T, et al.: The identity of human tissue-emigrant CD8 + T cells. Cell 183: 1946–1961, 2020
Bengsch B, Ohtani T, Khan O, Setty M, Manne S, O’Brien S, et al.: Epigenomic-guided mass cytometry profiling reveals disease-specific features of exhausted CD8 T cells. Immunity 48: 1029–1045, 2018
Callemeyn J, Lerut E, de Loor H, Arijs I, Thaunat O, Koenig A, et al.: Transcriptional changes in kidney allografts with histology of antibody-mediated rejection without anti-HLA donor-specific antibodies. J Am Soc Nephrol 31: 2168–2183, 2020
Griffith JW, Sokol CL, Luster AD: Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu Rev Immunol 32: 659–702, 2014
Xu J, Torres E, Mora AL, Shim H, Ramirez A, Neujahr D, et al.: Attenuation of obliterative bronchiolitis by a CXCR4 antagonist in the murine heterotopic tracheal transplant model. J Heart Lung Transplant 27: 1302–1310, 2008
Scimone ML, Felbinger TW, Mazo IB, Stein JV, Von Andrian UH, Weninger W: CXCL12 mediates CCR7-independent homing of central memory cells, but not naive T cells, in peripheral lymph nodes. J Exp Med 199: 1113–1120, 2004
Busillo JM, Benovic JL: Regulation of CXCR4 signaling. Biochim Biophys Acta 1768: 952–963, 2007
Trebak M, Kinet J-P: Calcium signalling in T cells. Nat Rev Immunol 19: 154–169, 2019
North RA: Molecular physiology of P2X receptors. Physiol Rev 82: 1013–1067, 2002
Schenk U, Westendorf AM, Radaelli E, Casati A, Ferro M, Fumagalli M, et al.: Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal 1: ra6, 2008
Woehrle T, Yip L, Elkhal A, Sumi Y, Chen Y, Yao Y, et al.: Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116: 3475–3484, 2010
Filippini A, Taffs RE, Sitkovsky MV: Extracellular ATP in T-lymphocyte activation: Possible role in effector functions. Proc Natl Acad Sci U S A 87: 8267–8271, 1990
Ley K, Kansas GS: Selectins in T-cell recruitment to non-lymphoid tissues and sites of inflammation. Nat Rev Immunol 4: 325–335, 2004
van der Windt GJW, O’Sullivan D, Everts B, Huang SC-C, Buck MD, Curtis JD, et al.: CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc Natl Acad Sci U S A 110: 14336–14341, 2013
Andresen L, Skovbakke SL, Persson G, Hagemann-Jensen M, Hansen KA, Jensen H, et al.: 2-deoxy D-glucose prevents cell surface expression of NKG2D ligands through inhibition of N-linked glycosylation. J Immunol 188: 1847–1855, 2012
Zygmunt BM, Węgrzyn A, Gajska W, Yevsa T, Chodaczek G, Guzmán CA: Mannose metabolism is essential for Th1 cell differentiation and IFN-γ production. J Immunol 201: 1400–1411, 2018
Chen S, Springer TA: An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J Cell Biol 144: 185–200, 1999
McEver RP: Selectins: Initiators of leucocyte adhesion and signalling at the vascular wall. Cardiovasc Res 107: 331–339, 2015
Constantin G, Majeed M, Giagulli C, Piccio L, Kim JY, Butcher EC, et al.: Chemokines trigger immediate β2 integrin affinity and mobility changes: Differential regulation and roles in lymphocyte arrest under flow. Immunity 13: 759–769, 2000
Walling BL, Kim M: LFA-1 in T cell migration and differentiation. Front Immunol 9: 952, 2018
Arazi A, Rao DA, Berthier CC, Davidson A, Liu Y, Hoover PJ, et al.; Accelerating Medicines Partnership in SLE network: The immune cell landscape in kidneys of patients with lupus nephritis. Nat Immunol 20: 902–914, 2019
Wu H, Malone AF, Donnelly EL, Kirita Y, Uchimura K, Ramakrishnan SM, et al.: Single-cell transcriptomics of a human kidney allograft biopsy specimen defines a diverse inflammatory response. J Am Soc Nephrol 29: 2069–2080, 2018
Lamarthée B, Callemeyn J, Herck YV, Antoranz A, Anglicheau D, Becker JU, et al: Transcriptional and spatial profiling of the kidney allograft unravels a central role for FcyRIII+ innate immune cells in rejection. Medrxiv. (Preprint posted July 10, 2022)
Georg P, Astaburuaga-García R, Bonaguro L, Brumhard S, Michalick L, Lippert LJ, et al.; PA-COVID-19 Study Group: Complement activation induces excessive T cell cytotoxicity in severe COVID-19. Cell 185: 493–512, 2022
Nolz JC, Richer MJ: Control of memory CD8 + T cell longevity and effector functions by IL-15. Mol Immunol 117: 180–188, 2020
Nolz JC, Harty JT: IL-15 regulates memory CD8+ T cell O-glycan synthesis and affects trafficking. J Clin Invest 124: 1013–1026, 2014
Pavlakis M, Strehlau J, Lipman M, Shapiro M, Maslinski W, Strom TB: Intragraft IL-15 transcripts are increased in human renal allograft rejection. Transplantation 62: 543–545, 1996
Strehlau J, Pavlakis M, Lipman M, Shapiro M, Vasconcellos L, Harmon W, et al.: Quantitative detection of immune activation transcripts as a diagnostic tool in kidney transplantation. Proc Natl Acad Sci U S A 94: 695–700, 1997
Shinozaki M, Hirahashi J, Lebedeva T, Liew FY, Salant DJ, Maron R, et al.: IL-15, a survival factor for kidney epithelial cells, counteracts apoptosis and inflammation during nephritis. J Clin Invest 109: 951–960, 2002
Weiler M, Rogashev B, Einbinder T, Hausmann MJ, Kaneti J, Chaimovitz C, et al.: Interleukin-15, a leukocyte activator and growth factor, is produced by cortical tubular epithelial cells. J Am Soc Nephrol 9: 1194–1201, 1998
Oppenheimer-Marks N, Brezinschek RI, Mohamadzadeh M, Vita R, Lipsky PE: Interleukin 15 is produced by endothelial cells and increases the transendothelial migration of T cells In vitro and in the SCID mouse-human rheumatoid arthritis model In vivo. J Clin Invest 101: 1261–1272, 1998
Heil M, Land WG: Danger signals - damaged-self recognition across the tree of life. Front Plant Sci 5: 578, 2014
Salles ÉM, Menezes MN, Siqueira R, Borges da Silva H, Amaral EP, Castillo-Méndez SI, et al.: P2X7 receptor drives Th1 cell differentiation and controls the follicular helper T cell population to protect against Plasmodium chabaudi malaria. PLoS Pathog 13: e1006595, 2017
Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, et al.: ATP drives lamina propria T(H)17 cell differentiation. Nature 455: 808–812, 2008
Schenk U, Frascoli M, Proietti M, Geffers R, Traggiai E, Buer J, et al.: ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci Signal 4: ra12, 2011
Borges da Silva H, Beura LK, Wang H, Hanse EA, Gore R, Scott MC, et al.: The purinergic receptor P2RX7 directs metabolic fitness of long-lived memory CD8 + T cells. Nature 559: 264–268, 2018
Liu K, Vergani A, Zhao P, Ben Nasr M, Wu X, Iken K, et al.: Inhibition of the purinergic pathway prolongs mouse lung allograft survival. Am J Respir Cell Mol Biol 51: 300–310, 2014
Wanhainen KM, Jameson SC, da Silva HB: Self-regulation of memory CD8 T cell metabolism through extracellular ATP signaling. Immunometabolism 1: e190009, 2019
Solini A, Usuelli V, Fiorina P: The dark side of extracellular ATP in kidney diseases. J Am Soc Nephrol 26: 1007–1016, 2015
Patel MS, Miranda-Nieves D, Chen J, Haller CA, Chaikof EL: Targeting P-selectin glycoprotein ligand-1/P-selectin interactions as a novel therapy for metabolic syndrome. Transl Res 183: 1–13, 2017
Friedrich M, Bock D, Philipp S, Ludwig N, Sabat R, Wolk K, et al.: Pan-selectin antagonism improves psoriasis manifestation in mice and man. Arch Dermatol Res 297: 345–351, 2006
Krishnamurthy VR, Sardar MYR, Ying Y, Song X, Haller C, Dai E, et al.: Glycopeptide analogues of PSGL-1 inhibit P-selectin in vitro and in vivo. Nat Commun 6: 6387, 2015