CX
Atherosclerosis
CX3CR1
Glomerulonephritis
Gut microbiota
High-fat diet
SLE
Journal
Inflammation research : official journal of the European Histamine Research Society ... [et al.]
ISSN: 1420-908X
Titre abrégé: Inflamm Res
Pays: Switzerland
ID NLM: 9508160
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
received:
12
01
2023
accepted:
05
04
2023
revised:
31
03
2023
medline:
22
5
2023
pubmed:
16
4
2023
entrez:
15
4
2023
Statut:
ppublish
Résumé
Patients with systemic lupus erythematosus (SLE) often develop multi-organ damages including heart and kidney complications. We sought to better define the underlying mechanisms with a focus on the chemokine receptor CX We generated Cx3cr1-deficient MRL/lpr lupus-prone mice through backcrossing. We then employed heterozygous intercross to generate MRL/lpr littermates that were either sufficient or deficient of CX Cx3cr1 We uncovered novel, Cx3cr1 deficiency-mediated pathogenic mechanisms contributing to SLE-associated glomerulonephritis and cardiovascular disease.
Identifiants
pubmed: 37060359
doi: 10.1007/s00011-023-01731-1
pii: 10.1007/s00011-023-01731-1
doi:
Substances chimiques
CX3C Chemokine Receptor 1
0
Autoantibodies
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1083-1097Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL163948
Pays : United States
Organisme : NIH HHS
ID : AR067418
Pays : United States
Organisme : NIH HHS
ID : HL163948
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011;365:2110–21.
pubmed: 22129255
Lech M, Anders HJ. The pathogenesis of lupus nephritis. J Am Soc Nephrol. 2013;24:1357–66.
pubmed: 23929771
pmcid: 3752952
Restivo V, Candiloro S, Daidone M, Norrito R, Cataldi M, Minutolo G, et al. Systematic review and meta-analysis of cardiovascular risk in rheumatological disease: Symptomatic and non-symptomatic events in rheumatoid arthritis and systemic lupus erythematosus. Autoimmun Rev. 2021;21(1): 102925.
pubmed: 34454117
Skaggs BJ, Grossman J, Sahakian L, Perry L, FitzGerald J, Charles-Schoeman C, et al. A panel of biomarkers associates with increased risk for cardiovascular events in women with systemic lupus erythematosus. ACR Open Rheumatol. 2021;3:209–20.
pubmed: 33605563
pmcid: 8063147
Tektonidou MG, Wang Z, Dasgupta A, Ward MM. Burden of serious infections in adults with systemic lupus erythematosus: a national population-based study, 1996–2011. Arthritis Care Res (Hoboken). 2015;67:1078–85.
pubmed: 25732901
Imai T, Hieshima K, Haskell C, Baba M, Nagira M, Nishimura M, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell. 1997;91:521–30.
pubmed: 9390561
Bazan JF, Bacon KB, Hardiman G, Wang W, Soo K, Rossi D, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature. 1997;385:640–4.
pubmed: 9024663
Pan Y, Lloyd C, Zhou H, Dolich S, Deeds J, Gonzalo JA, et al. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature. 1997;387:611–7.
pubmed: 9177350
Garcia GE, Xia Y, Chen S, Wang Y, Ye RD, Harrison JK, et al. NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1β, TNF-α, and LPS. J Leukoc Biol. 2000;67:577–84.
pubmed: 10770292
Hirose S, Lin Q, Ohtsuji M, Nishimura H, Verbeek JS. Monocyte subsets involved in the development of systemic lupus erythematosus and rheumatoid arthritis. Int Immunol. 2019;31:687–96.
pubmed: 31063541
pmcid: 6794944
Qiu F, Li Y, Zhu Y, Li G, Lei F, Zhang S, et al. CX3CR1 might be a promising predictor of systemic lupus erythematosus patients with pulmonary fibrosis. Scand J Immunol. 2021;94: e13038.
pubmed: 33665864
Yajima N, Kasama T, Isozaki T, Odai T, Matsunawa M, Negishi M, et al. Elevated levels of soluble fractalkine in active systemic lupus erythematosus: potential involvement in neuropsychiatric manifestations. Arthritis Rheum. 2005;52:1670–5.
pubmed: 15934075
Segerer S, Hughes E, Hudkins KL, Mack M, Goodpaster T, Alpers CE. Expression of the fractalkine receptor (CX3CR1) in human kidney diseases. Kidney Int. 2002;62:488–95.
pubmed: 12110009
Nakatani K, Yoshimoto S, Iwano M, Asai O, Samejima K, Sakan H, et al. Fractalkine expression and CD16+ monocyte accumulation in glomerular lesions: association with their severity and diversity in lupus models. Am J Physiol Renal Physiol. 2010;299:F207–16.
pubmed: 20410215
Inoue A, Hasegawa H, Kohno M, Ito MR, Terada M, Imai T, et al. Antagonist of fractalkine (CX3CL1) delays the initiation and ameliorates the progression of lupus nephritis in MRL/lpr mice. Arthritis Rheum. 2005;52:1522–33.
pubmed: 15880599
Feng L, Chen S, Garcia GE, Xia Y, Siani MA, Botti P, et al. Prevention of crescentic glomerulonephritis by immunoneutralization of the fractalkine receptor CX3CR1 rapid communication. Kidney Int. 1999;56:612–20.
pubmed: 10432400
Liao X, Ren J, Reihl A, Pirapakaran T, Sreekumar B, Cecere TE, et al. Renal-infiltrating CD11c+ cells are pathogenic in murine lupus nephritis through promoting CD4+ T cell responses. Clin Exp Immunol. 2017. https://doi.org/10.1111/cei.13017 .
doi: 10.1111/cei.13017
pubmed: 28876451
pmcid: 5721231
Hochheiser K, Heuser C, Krause TA, Teteris S, Ilias A, Weisheit C, et al. Exclusive CX3CR1 dependence of kidney DCs impacts glomerulonephritis progression. J Clin Invest. 2013;123:4242–54.
pubmed: 23999431
pmcid: 3784547
Liu F, Dai S, Feng D, Qin Z, Peng X, Sakamuri S, et al. Distinct fate, dynamics and niches of renal macrophages of bone marrow or embryonic origins. Nat Commun. 2020;11:2280.
pubmed: 32385245
pmcid: 7210253
Cormican S, Griffin MD. Fractalkine (CX3CL1) and its receptor CX3CR1: a promising therapeutic target in chronic kidney disease? Front Immunol. 2021;12: 664202.
pubmed: 34163473
pmcid: 8215706
Grone HJ, Cohen CD, Grone E, Schmidt C, Kretzler M, Schlondorff D, et al. Spatial and temporally restricted expression of chemokines and chemokine receptors in the developing human kidney. J Am Soc Nephrol. 2002;13:957–67.
pubmed: 11912255
Landsman L, Bar-On L, Zernecke A, Kim KW, Krauthgamer R, Shagdarsuren E, et al. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood. 2009;113:963–72.
pubmed: 18971423
McDermott DH, Fong AM, Yang Q, Sechler JM, Cupples LA, Merrell MN, et al. Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans. J Clin Invest. 2003;111:1241–50.
pubmed: 12697743
pmcid: 152935
Mionnet C, Buatois V, Kanda A, Milcent V, Fleury S, Lair D, et al. CX3CR1 is required for airway inflammation by promoting T helper cell survival and maintenance in inflamed lung. Nat Med. 2010;16:1305–12.
pubmed: 21037587
Bonacina F, Martini E, Svecla M, Nour J, Cremonesi M, Beretta G, et al. Adoptive transfer of CX3CR1 transduced-T regulatory cells improves homing to the atherosclerotic plaques and dampens atherosclerosis progression. Cardiovasc Res. 2021;117:2069–82.
pubmed: 32931583
Dong L, Nordlohne J, Ge S, Hertel B, Melk A, Rong S, et al. T cell CX3CR1 mediates excess atherosclerotic inflammation in renal impairment. J Am Soc Nephrol. 2016;27:1753–64.
pubmed: 26449606
Dagkalis A, Wallace C, Hing B, Liversidge J, Crane IJ. CX3CR1-deficiency is associated with increased severity of disease in experimental autoimmune uveitis. Immunology. 2009;128:25–33.
pubmed: 19689733
pmcid: 2747136
Beli E, Dominguez JM 2nd, Hu P, Thinschmidt JS, Caballero S, Li Calzi S, et al. CX3CR1 deficiency accelerates the development of retinopathy in a rodent model of type 1 diabetes. J Mol Med (Berl). 2016;94:1255–65.
pubmed: 27344677
Kawamura N, Katsuura G, Yamada-Goto N, Novianti E, Inui A, Asakawa A. Reduced brain fractalkine-CX3CR1 signaling is involved in the impaired cognition of streptozotocin-treated mice. IBRO Rep. 2020;9:233–40.
pubmed: 32995659
pmcid: 7509139
Mai W, Liu X, Wang J, Zheng J, Wang X, Zhou W. Protective effects of CX3CR1 on autoimmune inflammation in a chronic EAE model for MS through modulation of antigen-presenting cell-related molecular MHC-II and its regulators. Neurol Sci. 2019;40:779–91.
pubmed: 30671738
Ridderstad Wollberg A, Ericsson-Dahlstrand A, Jureus A, Ekerot P, Simon S, Nilsson M, et al. Pharmacological inhibition of the chemokine receptor CX3CR1 attenuates disease in a chronic-relapsing rat model for multiple sclerosis. Proc Natl Acad Sci USA. 2014;111:5409–14.
pubmed: 24706865
pmcid: 3986185
Yadav AK, Kumar V, Jha V. Association of chemokine receptor CX3CR1 V249I and T280M polymorphisms with chronic kidney disease. Indian J Nephrol. 2016;26:275–9.
pubmed: 27512300
pmcid: 4964688
De Lema GP, Lucio-Cazaña FJ, Molina ANA, Luckow B, Schmid H, de Wit C, et al. Retinoic acid treatment protects MRL/lpr lupus mice from the development of glomerular disease. Kidney Int. 2004;66:1018–28.
Zhang H, Liao X, Sparks JB, Luo XM, Schloss PD. Dynamics of gut microbiota in autoimmune lupus. Appl Environ Microbiol. 2014;80:7551–60.
pubmed: 25261516
pmcid: 4249226
Mu Q, Zhang H, Liao X, Lin K, Liu H, Edwards MR, et al. Control of lupus nephritis by changes of gut microbiota. Microbiome. 2017;5:73.
pubmed: 28697806
pmcid: 5505136
Mu Q, Edwards MR, Swartwout BK, Cabana Puig X, Mao J, Zhu J, et al. Gut microbiota and bacterial DNA suppress autoimmunity by stimulating regulatory B cells in a murine model of lupus. Front Immunol. 2020;11: 593353.
pubmed: 33240280
pmcid: 7683516
Mu Q, Cabana-Puig X, Mao J, Swartwout B, Abdelhamid L, Cecere TE, et al. Pregnancy and lactation interfere with the response of autoimmunity to modulation of gut microbiota. Microbiome. 2019;7:105.
pubmed: 31311609
pmcid: 6635999
Mu Q, Swartwout BK, Edwards M, Zhu J, Lee G, Eden K, et al. Regulation of neonatal IgA production by the maternal microbiota. Proc Natl Acad Sci. 2021. https://doi.org/10.1073/pnas.2015691118 .
doi: 10.1073/pnas.2015691118
pubmed: 34257153
pmcid: 8307374
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30:2114–20.
pubmed: 24695404
pmcid: 4103590
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
pubmed: 27214047
pmcid: 4927377
McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8: e61217.
pubmed: 23630581
pmcid: 3632530
Martin BD, Witten D, Willis AD. Modeling microbial abundances and dysbiosis with beta-binomial regression. Ann Appl Stat. 2020;14:94–115.
pubmed: 32983313
pmcid: 7514055
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. Vegan: community ecology package. R Package Version 2.2–0; 2014. http://CRAN.Rproject.org/package=vegan .
Geng S, Zhang Y, Yi Z, Lu R, Li L. Resolving monocytes generated through TRAM deletion attenuate atherosclerosis. JCI Insight 2021; 6(20):e149651.
Geng S, Chen K, Yuan R, Peng L, Maitra U, Diao N, et al. The persistence of low-grade inflammatory monocytes contributes to aggravated atherosclerosis. Nat Commun. 2016;7:13436.
pubmed: 27824038
pmcid: 5105176
Liao X, Ren J, Wei CH, Ross AC, Cecere TE, Jortner BS, et al. Paradoxical effects of all-trans-retinoic acid on lupus-like disease in the MRL/lpr mouse model. PLoS One. 2015;10: e0118176.
pubmed: 25775135
pmcid: 4361690
Reilly CM, Olgun S, Goodwin D, Gogal RM Jr, Santo A, Romesburg JW, et al. Interferon regulatory factor-1 gene deletion decreases glomerulonephritis in MRL/lpr mice. Eur J Immunol. 2006;36:1296–308.
pubmed: 16541466
Cabana-Puig X, Bond JM, Wang Z, Dai R, Lu R, Lin A, et al. Phenotypic drift in lupus-prone MRL/lpr mice: potential roles of microRNAs and gut microbiota. Immunohorizons. 2022;6:36–46.
pubmed: 35039434
Schneider KM, Bieghs V, Heymann F, Hu W, Dreymueller D, Liao L, et al. CX3CR1 is a gatekeeper for intestinal barrier integrity in mice: limiting steatohepatitis by maintaining intestinal homeostasis. Hepatology. 2015;62:1405–16.
pubmed: 26178698
Medina-Contreras O, Geem D, Laur O, Williams IR, Lira SA, Nusrat A, et al. CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J Clin Invest. 2011;121:4787–95.
pubmed: 22045567
pmcid: 3226003
McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood. 2011;117:5403–12.
pubmed: 21444914
Qiao JH, Castellani LW, Fishbein MC, Lusis AJ. Immune-complex-mediated vasculitis increases coronary artery lipid accumulation in autoimmune-prone MRL mice. Arterioscler Thromb. 1993;13:932–43.
pubmed: 8499414
Geng S, Zhang Y, Lee C, Li L. Novel reprogramming of neutrophils modulates inflammation resolution during atherosclerosis. Sci Adv. 2019;5: eaav2309.
pubmed: 30775441
pmcid: 6365109
Pradhan K, Yi Z, Geng S, Li L. Development of exhausted memory monocytes and underlying mechanisms. Front Immunol. 2021;12: 778830.
pubmed: 34777396
pmcid: 8583871
Aicher A, Hayden-Ledbetter M, Brady WA, Pezzutto A, Richter G, Magaletti D, et al. Characterization of human inducible costimulator ligand expression and function. J Immunol. 2000;164:4689–96.
pubmed: 10779774
Wikenheiser DJ, Stumhofer JS. ICOS co-stimulation: friend or foe? Front Immunol. 2016;7:304.
pubmed: 27559335
pmcid: 4979228
Li H, Adamopoulos IE, Moulton VR, Stillman IE, Herbert Z, Moon JJ, et al. Systemic lupus erythematosus favors the generation of IL-17 producing double negative T cells. Nat Commun. 2020;11:2859.
pubmed: 32503973
pmcid: 7275084
Rodriguez-Rodriguez N, Flores-Mendoza G, Apostolidis SA, Rosetti F, Tsokos GC, Crispin JC. TCR-α/β CD4(–) CD8(–) double negative T cells arise from CD8(+) T cells. J Leukoc Biol. 2020;108:851–7.
pubmed: 32052478
Li H, Tsokos GC. Double-negative T cells in autoimmune diseases. Curr Opin Rheumatol. 2021;33:163–72.
pubmed: 33394752
pmcid: 8018563
Chen PM, Tsokos GC. The role of CD8+ T-cell systemic lupus erythematosus pathogenesis: an update. Curr Opin Rheumatol. 2021;33:586–91.
pubmed: 34183542
pmcid: 8567317
Shivakumar S, Tsokos GC, Datta SK. T cell receptor alpha/beta expressing double-negative (CD4–/CD8–) and CD4+ T helper cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J Immunol. 1989;143:103–12.
pubmed: 2525144
Crispin JC, Oukka M, Bayliss G, Cohen RA, Van Beek CA, Stillman IE, et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J Immunol. 2008;181:8761–6.
pubmed: 19050297
Mizui M, Koga T, Lieberman LA, Beltran J, Yoshida N, Johnson MC, et al. IL-2 protects lupus-prone mice from multiple end-organ damage by limiting CD4-CD8- IL-17-producing T cells. J Immunol. 2014;193:2168–77.
pubmed: 25063876
Cabeza-Cabrerizo M, Cardoso A, Minutti CM, Pereira da Costa M, Reis e Sousa C. Dendritic cells revisited. Annu Rev Immunol. 2021;39:131–66.
pubmed: 33481643
Gottschalk C, Kurts C. The debate about dendritic cells and macrophages in the kidney. Front Immunol. 2015;6:435.
pubmed: 26388867
pmcid: 4556034
Arnold IC, Mathisen S, Schulthess J, Danne C, Hegazy AN, Powrie F. CD11c(+) monocyte/macrophages promote chronic Helicobacter hepaticus-induced intestinal inflammation through the production of IL-23. Mucosal Immunol. 2016;9:352–63.
pubmed: 26242598
Lu L, Kuroishi T, Tanaka Y, Furukawa M, Nochi T, Sugawara S. Differential expression of CD11c defines two types of tissue-resident macrophages with different origins in steady-state salivary glands. Sci Rep. 2022;12:931.
pubmed: 35042931
pmcid: 8766464
Cao Q, Wang Y, Wang XM, Lu J, Lee VW, Ye Q, et al. Renal F4/80+ CD11c+ mononuclear phagocytes display phenotypic and functional characteristics of macrophages in health and in adriamycin nephropathy. J Am Soc Nephrol. 2015;26:349–63.
pubmed: 25012165
Borges da Silva H, Fonseca R, Pereira RM, Cassado Ados A, Alvarez JM, D’Imperio Lima MR. Splenic macrophage subsets and their function during blood-borne infections. Front Immunol. 2015;6:480.
pubmed: 26441984
pmcid: 4585205
Helmke A, Nordlohne J, Balzer MS, Dong L, Rong S, Hiss M, et al. CX3CL1-CX3CR1 interaction mediates macrophage-mesothelial cross talk and promotes peritoneal fibrosis. Kidney Int. 2019;95:1405–17.
pubmed: 30948201
Kassianos AJ, Wang X, Sampangi S, Afrin S, Wilkinson R, Healy H. Fractalkine-CX3CR1-dependent recruitment and retention of human CD1c+ myeloid dendritic cells by in vitro-activated proximal tubular epithelial cells. Kidney Int. 2015;87:1153–63.
pubmed: 25587706