Macrophage Jak2 deficiency accelerates atherosclerosis through defects in cholesterol efflux.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
15 02 2022
Historique:
received: 05 09 2020
accepted: 26 01 2022
entrez: 16 2 2022
pubmed: 17 2 2022
medline: 5 4 2022
Statut: epublish

Résumé

Atherosclerosis is a chronic inflammatory condition in which macrophages play a major role. Janus kinase 2 (JAK2) is a pivotal molecule in inflammatory and metabolic signaling, and Jak2

Identifiants

pubmed: 35169231
doi: 10.1038/s42003-022-03078-5
pii: 10.1038/s42003-022-03078-5
pmc: PMC8847578
doi:

Substances chimiques

Cholesterol 97C5T2UQ7J
Jak2 protein, mouse EC 2.7.10.2
Janus Kinase 2 EC 2.7.10.2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

132

Subventions

Organisme : CIHR
ID : MOP-142193
Pays : Canada
Organisme : CIHR
ID : PJT-159505
Pays : Canada

Informations de copyright

© 2022. The Author(s).

Références

Ross, R. Atherosclerosis–an inflammatory disease. N. Engl. J. Med. 340, 115–126 (1999).
pubmed: 9887164 doi: 10.1056/NEJM199901143400207
Blankenberg, S., Barbaux, S. & Tiret, L. Adhesion molecules and atherosclerosis. Atherosclerosis 170, 191–203 (2003).
pubmed: 14612198 doi: 10.1016/S0021-9150(03)00097-2
Kojima, Y., Weissman, I. L. & Leeper, N. J. The role of efferocytosis in atherosclerosis. Circulation 135, 476–489 (2017).
pubmed: 28137963 pmcid: 5302553 doi: 10.1161/CIRCULATIONAHA.116.025684
Valanti, E. K., Dalakoura-Karagkouni, K. & Sanoudou, D. Current and emerging reconstituted HDL-apoA-I and HDL-apoE approaches to treat atherosclerosis. J. Pers. Med. 8, https://doi.org/10.3390/jpm8040034 (2018).
Feig, J. E. et al. HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc. Natl Acad. Sci. USA 108, 7166–7171 (2011).
pubmed: 21482781 pmcid: 3084076 doi: 10.1073/pnas.1016086108
Rohatgi, A. et al. HDL cholesterol efflux capacity and incident cardiovascular events. N. Engl. J. Med. 371, 2383–2393 (2014).
pubmed: 25404125 pmcid: 4308988 doi: 10.1056/NEJMoa1409065
Murray, P. J. The JAK-STAT signaling pathway: input and output integration. J. Immunol. 178, 2623–2629 (2007).
pubmed: 17312100 doi: 10.4049/jimmunol.178.5.2623
Tang, C., Liu, Y., Kessler, P. S., Vaughan, A. M. & Oram, J. F. The macrophage cholesterol exporter ABCA1 functions as an anti-inflammatory receptor. J. Biol. Chem. 284, 32336–32343 (2009).
pubmed: 19783654 pmcid: 2781648 doi: 10.1074/jbc.M109.047472
de Jonge, W. J. et al. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nat. Immunol. 6, 844–851 (2005).
pubmed: 16025117 doi: 10.1038/ni1229
Desai, H. R. et al. Macrophage JAK2 deficiency protects against high-fat diet-induced inflammation. Sci. Rep. 7, 7653 (2017).
pubmed: 28794431 pmcid: 5550513 doi: 10.1038/s41598-017-07923-0
Wang, W. et al. Macrophage inflammation, erythrophagocytosis, and accelerated atherosclerosis in Jak2 (V617F) mice. Circ. Res. 123, e35–e47 (2018).
pubmed: 30571460 pmcid: 6309796 doi: 10.1161/CIRCRESAHA.118.313283
Robbins, C. S. et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat. Med. 19, 1166–1172 (2013).
pubmed: 23933982 pmcid: 3769444 doi: 10.1038/nm.3258
Jongstra-Bilen, J. et al. Oxidized low-density lipoprotein loading of macrophages downregulates TLR-induced proinflammatory responses in a gene-specific and temporal manner through transcriptional control. J. Immunol. 199, 2149–2157 (2017).
pubmed: 28784845 doi: 10.4049/jimmunol.1601363
Spann, N. J. et al. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151, 138–152 (2012).
pubmed: 23021221 pmcid: 3464914 doi: 10.1016/j.cell.2012.06.054
Tang, C., Vaughan, A. M. & Oram, J. F. Janus kinase 2 modulates the apolipoprotein interactions with ABCA1 required for removing cellular cholesterol. J. Biol. Chem. 279, 7622–7628 (2004).
pubmed: 14668333 doi: 10.1074/jbc.M312571200
Tang, C., Vaughan, A. M., Anantharamaiah, G. M. & Oram, J. F. Janus kinase 2 modulates the lipid-removing but not protein-stabilizing interactions of amphipathic helices with ABCA1. J. Lipid Res. 47, 107–114 (2006).
pubmed: 16210729 doi: 10.1194/jlr.M500240-JLR200
Vaughan, A. M., Tang, C. & Oram, J. F. ABCA1 mutants reveal an interdependency between lipid export function, apoA-I binding activity, and Janus kinase 2 activation. J. Lipid Res. 50, 285–292 (2009).
pubmed: 18776170 pmcid: 2636916 doi: 10.1194/jlr.M800366-JLR200
Yancey, P. G. et al. Importance of different pathways of cellular cholesterol efflux. Arterioscler Thromb. Vasc. Biol. 23, 712–719 (2003).
pubmed: 12615688 doi: 10.1161/01.ATV.0000057572.97137.DD
Duffy, D. & Rader, D. J. Update on strategies to increase HDL quantity and function. Nat. Rev. Cardiol. 6, 455–463 (2009).
pubmed: 19488077 doi: 10.1038/nrcardio.2009.94
Beyea, M. M. et al. Selective up-regulation of LXR-regulated genes ABCA1, ABCG1, and APOE in macrophages through increased endogenous synthesis of 24(S),25-epoxycholesterol. J. Biol. Chem. 282, 5207–5216 (2007).
pubmed: 17186944 doi: 10.1074/jbc.M611063200
Yu, L., Cao, G., Repa, J. & Stangl, H. Sterol regulation of scavenger receptor class B type I in macrophages. J. Lipid Res. 45, 889–899 (2004).
pubmed: 14967816 doi: 10.1194/jlr.M300461-JLR200
Schwartz, D. M. et al. JAK inhibition as a therapeutic strategy for immune and inflammatory diseases. Nat. Rev. Drug Discov. 17, 78 (2017).
pubmed: 29282366 pmcid: 6168198 doi: 10.1038/nrd.2017.267
Kralovics, R. et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N. Engl. J. Med. 352, 1779–1790 (2005).
pubmed: 15858187 doi: 10.1056/NEJMoa051113
Jaiswal, S. et al. Clonal hematopoiesis and risk of atherosclerotic cardiovascular disease. N. Engl. J. Med. 377, 111–121 (2017).
pubmed: 28636844 pmcid: 6717509 doi: 10.1056/NEJMoa1701719
Libby, P., Ridker, P. M. & Hansson, G. K. Progress and challenges in translating the biology of atherosclerosis. Nature 473, 317–325 (2011).
pubmed: 21593864 doi: 10.1038/nature10146
Yang, X. et al. Inhibition of JAK2/STAT3/SOCS3 signaling attenuates atherosclerosis in rabbit. BMC Cardiovasc Disord. 20, 133 (2020).
pubmed: 32169038 pmcid: 7071770 doi: 10.1186/s12872-020-01391-7
Action to Control Cardiovascular Risk in Diabetes Study, G. et al. Effects of intensive glucose lowering in type 2 diabetes. N. Engl. J. Med. 358, 2545–2559 (2008).
doi: 10.1056/NEJMoa0802743
Seimon, T. A. et al. Macrophage deficiency of p38alpha MAPK promotes apoptosis and plaque necrosis in advanced atherosclerotic lesions in mice. J. Clin. Investig. 119, 886–898 (2009).
pubmed: 19287091 pmcid: 2662559
Vergadi, E., Ieronymaki, E., Lyroni, K., Vaporidi, K. & Tsatsanis, C. Akt signaling pathway in macrophage activation and M1/M2 polarization. J. Immunol. 198, 1006–1014 (2017).
pubmed: 28115590 doi: 10.4049/jimmunol.1601515
Wang, F. et al. Myeloid beta-catenin deficiency exacerbates atherosclerosis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb. Vasc. Biol. 38, 1468–1478 (2018).
pubmed: 29724817 pmcid: 6023740 doi: 10.1161/ATVBAHA.118.311059
Chithra, P. K., Jayalekshmy, A. & Helen, A. Petroleum ether extract of Njavara rice (Oryza sativa) bran upregulates the JAK2-STAT3-mediated anti-inflammatory profile in macrophages and aortic endothelial cells promoting regression of atherosclerosis. Biochem Cell Biol. 95, 652–662 (2017).
pubmed: 28700834 doi: 10.1139/bcb-2017-0090
Wang, J. L. et al. ApoA-1 mimetic peptide ELK-2A2K2E decreases inflammatory factor levels through the ABCA1-JAK2-STAT3-TTP axis in THP-1-derived macrophages. J. Cardiovasc Pharm. 72, 60–67 (2018).
doi: 10.1097/FJC.0000000000000594
Feng, L. et al. Seselin ameliorates inflammation via targeting Jak2 to suppress the proinflammatory phenotype of macrophages. Br. J. Pharm. 176, 317–333 (2019).
doi: 10.1111/bph.14521
Oram, J. F., Lawn, R. M., Garvin, M. R. & Wade, D. P. ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J. Biol. Chem. 275, 34508–34511 (2000).
pubmed: 10918070 doi: 10.1074/jbc.M006738200
Oram, J. F. & Lawn, R. M. ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 42, 1173–1179 (2001).
pubmed: 11483617 doi: 10.1016/S0022-2275(20)31566-2
Huang, L., Fan, B., Ma, A., Shaul, P. W. & Zhu, H. Inhibition of ABCA1 protein degradation promotes HDL cholesterol efflux capacity and RCT and reduces atherosclerosis in mice. J. Lipid Res. 56, 986–997 (2015).
pubmed: 25761370 pmcid: 4409288 doi: 10.1194/jlr.M054742
Khera, A. V. et al. Cholesterol efflux capacity, high-density lipoprotein particle number, and incident cardiovascular events: an analysis from the JUPITER Trial (justification for the use of statins in prevention: an intervention trial evaluating rosuvastatin). Circulation 135, 2494–2504 (2017).
pubmed: 28450350 pmcid: 5490983 doi: 10.1161/CIRCULATIONAHA.116.025678
Suzuki, S. et al. Verapamil increases the apolipoprotein-mediated release of cellular cholesterol by induction of ABCA1 expression via Liver X receptor-independent mechanism. Arterioscler Thromb. Vasc. Biol. 24, 519–525 (2004).
pubmed: 14726413 doi: 10.1161/01.ATV.0000117178.94087.ba
Jiang, T. et al. Leonurine prevents atherosclerosis via promoting the expression of ABCA1 and ABCG1 in a ppargamma/lxralpha signaling pathway-dependent manner. Cell Physiol. Biochem 43, 1703–1717 (2017).
pubmed: 29045950 doi: 10.1159/000484031
Joseph, S. B. et al. Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc. Natl Acad. Sci. USA 99, 7604–7609 (2002).
pubmed: 12032330 pmcid: 124297 doi: 10.1073/pnas.112059299
Verschuren, L., de Vries-van der Weij, J., Zadelaar, S., Kleemann, R. & Kooistra, T. LXR agonist suppresses atherosclerotic lesion growth and promotes lesion regression in apoE*3Leiden mice: time course and mechanisms. J. Lipid Res. 50, 301–311 (2009).
pubmed: 18757914 doi: 10.1194/jlr.M800374-JLR200
Grisouard, J., Hao-Shen, H., Dirnhofer, S., Wagner, K. U. & Skoda, R. C. Selective deletion of Jak2 in adult mouse hematopoietic cells leads to lethal anemia and thrombocytopenia. Haematologica 99, e52–e54 (2014).
pubmed: 24510341 pmcid: 3971094 doi: 10.3324/haematol.2013.100016
Fidler, T. P. et al. The AIM2 inflammasome exacerbates atherosclerosis in clonal haematopoiesis. Nature https://doi.org/10.1038/s41586-021-03341-5 (2021).
Vainchenker, W. & Constantinescu, S. N. A unique activating mutation in JAK2 (V617F) is at the origin of polycythemia vera and allows a new classification of myeloproliferative diseases. Hematol. Am. Soc. Hematol. Educ Program 195–200 https://doi.org/10.1182/asheducation-2005.1.195 (2005).
Tang, Y. et al. Inhibition of JAK2 suppresses myelopoiesis and atherosclerosis in Apoe(-/-) mice. Cardiovasc Drugs Ther. 34, 145–152 (2020).
pubmed: 32086626 pmcid: 7125070 doi: 10.1007/s10557-020-06943-9
Krempler, A. et al. Generation of a conditional knockout allele for the Janus kinase 2 (Jak2) gene in mice. Genesis 40, 52–57 (2004).
pubmed: 15354294 doi: 10.1002/gene.20063
Tasian, S. K. et al. Potent efficacy of combined PI3K/mTOR and JAK or ABL inhibition in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood 129, 177–187 (2017).
pubmed: 27777238 pmcid: 5234216 doi: 10.1182/blood-2016-05-707653
Wang, L. et al. Pten deletion in RIP-Cre neurons protects against type 2 diabetes by activating the anti-inflammatory reflex. Nat. Med. 20, 484–492 (2014).
pubmed: 24747746 doi: 10.1038/nm.3527
Sivasubramaniyam, T. et al. Hepatic JAK2 protects against atherosclerosis through circulating IGF-1. JCI Insight 2, https://doi.org/10.1172/jci.insight.93735 (2017).
Carson, F. C. C. Histotechnology A Self Instructional Text, 4th edition (American Society for Clinical Pathology Press, 2016).
Zhu, S. N., Chen, M., Jongstra-Bilen, J. & Cybulsky, M. I. GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J. Exp. Med. 206, 2141–2149 (2009).
pubmed: 19752185 pmcid: 2757868 doi: 10.1084/jem.20090866
Zhang, K. et al. Polarized macrophages have distinct roles in the differentiation and migration of embryonic spinal-cord-derived neural stem cells after grafting to injured sites of spinal cord. Mol. Ther. 23, 1077–1091 (2015).
pubmed: 25794051 pmcid: 4817764 doi: 10.1038/mt.2015.46
Hafiane, A. & Genest, J. HDL-mediated cellular cholesterol efflux assay method. Ann. Clin. Lab. Sci. 45, 659–668 (2015).
pubmed: 26663796

Auteurs

Idit Dotan (I)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.
Institute of Endocrinology, Beilinson Campus, Rabin Medical Center, Petach Tikva, Israel.

Jiaqi Yang (J)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Jiro Ikeda (J)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Ziv Roth (Z)

Program in Cell Biology, Peter Gilgan Centre for Research and Learning, Hospital for Sick Children, Toronto, Canada.

Evan Pollock-Tahiri (E)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Harsh Desai (H)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Tharini Sivasubramaniyam (T)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Sonia Rehal (S)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Josh Rapps (J)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Yu Zhe Li (YZ)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Helen Le (H)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Gedaliah Farber (G)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Edouard Alchami (E)

Department of Immunology, University of Toronto, Toronto, Canada.

Changting Xiao (C)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Saraf Karim (S)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Marcela Gronda (M)

Princess Margaret Cancer Centre, University Health Network, Toronto, Canada.

Michael F Saikali (MF)

Department of Pharmaceutical Sciences, University of Toronto, Toronto, Canada.

Amit Tirosh (A)

Endocrine Cancer Genomics Center, Sheba Medical Center, Tel Hashomer, Israel.

Kay-Uwe Wagner (KU)

Department of Oncology, Wayne State University School of Medicine and Tumor Biology Program, Barbara Ann Karmanos Cancer Institute, Detroit, MI, USA.

Jacques Genest (J)

Research Institute of the McGill University Health Centre, Royal Victoria Hospital, Montreal, QC, Canada.

Aaron D Schimmer (AD)

Princess Margaret Cancer Centre, University Health Network, Toronto, Canada.

Vikas Gupta (V)

Princess Margaret Cancer Centre, University Health Network, Toronto, Canada.

Mark D Minden (MD)

Princess Margaret Cancer Centre, University Health Network, Toronto, Canada.

Carolyn L Cummins (CL)

Department of Pharmaceutical Sciences, University of Toronto, Toronto, Canada.

Gary F Lewis (GF)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.

Clinton Robbins (C)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.
Department of Immunology, University of Toronto, Toronto, Canada.

Jenny Jongstra-Bilen (J)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.
Department of Immunology, University of Toronto, Toronto, Canada.

Myron Cybulsky (M)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada.
Department of Immunology, University of Toronto, Toronto, Canada.

Minna Woo (M)

Toronto General Hospital Research Institute, University Health Network, Toronto, Canada. mwoo@uhnresearch.ca.
Department of Immunology, University of Toronto, Toronto, Canada. mwoo@uhnresearch.ca.
Division of Endocrinology and Metabolism, Department of Medicine, University Health Network and Sinai Health System, University of Toronto, Toronto, Canada. mwoo@uhnresearch.ca.

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