Complement activation and increased expression of Syk, mucin-1 and CaMK4 in kidneys of patients with COVID-19

Clinical Immunology - Tập 229 - Trang 108795 - 2021
Simin Jamaly1,2, Maria G. Tsokos1, Rhea Bhargava1, Olga R. Brook3, Jonathan L. Hecht4, Reza Abdi5, Vaishali R. Moulton1, Abhigyan Satyam1, George C. Tsokos1
1Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
2Department of Medical Biology, Faculty of Health Science, UiT Arctic University of Norway, N-9037 Tromsø, Norway
3Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
4Department of Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
5Transplantation Research Center, Renal Division, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, United States

Tài liệu tham khảo

Zhou, 2020, Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study, Lancet, 395, 1054, 10.1016/S0140-6736(20)30566-3 Gasmi, 2020, Individual risk management strategy and potential therapeutic options for the COVID-19 pandemic, Clin. Immunol., 215, 108409, 10.1016/j.clim.2020.108409 Guan, 2020, Clinical characteristics of coronavirus disease 2019 in China, N. Engl. J. Med., 382, 1708, 10.1056/NEJMoa2002032 Grasselli, 2020, Baseline characteristics and outcomes of 1591 patients infected with SARS-CoV-2 admitted to ICUs of the Lombardy region, Italy, JAMA, 323, 1574, 10.1001/jama.2020.5394 Goyal, 2020, Clinical characteristics of Covid-19 in New York City, N. Engl. J. Med., 382, 2372, 10.1056/NEJMc2010419 Llitjos, 2020, High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients, J. Thromb. Haemost., 18, 1743, 10.1111/jth.14869 Helms, 2020, Neurologic features in severe SARS-CoV-2 infection, N. Engl. J. Med., 382, 2268, 10.1056/NEJMc2008597 Fabrizi, 2020, COVID-19 and acute kidney injury: a systematic review and meta-analysis, Pathogens, 9, 10.3390/pathogens9121052 Argenziano, 2020, Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series, BMJ (Clinical research ed.), 369 Fisher, 2020, AKI in hospitalized patients with and without COVID-19: a comparison study, J. Am. Soc. Nephrol., 31, 2145, 10.1681/ASN.2020040509 Hirsch, 2020, Acute kidney injury in patients hospitalized with COVID-19, Kidney Int., 98, 209, 10.1016/j.kint.2020.05.006 Chan, 2021, AKI in hospitalized patients with COVID-19, J. Am. Soc. Nephrol., 32, 151, 10.1681/ASN.2020050615 Coca, 2012, Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis, Kidney Int., 81, 442, 10.1038/ki.2011.379 Nugent, 2021, Assessment of acute kidney injury and longitudinal kidney function after hospital discharge among patients with and without COVID-19, JAMA Netw. Open, 4, 10.1001/jamanetworkopen.2021.1095 Delorey, 2021, COVID-19 tissue atlases reveal SARS-CoV-2 pathology and cellular targets, Nature, 595, 107, 10.1038/s41586-021-03570-8 Gavriilaki, 2020, Severe COVID-19 infection and thrombotic microangiopathy: success does not come easily, Br. J. Haematol., 189, e227, 10.1111/bjh.16783 Satyam, 2020, Curb complement to cure COVID-19, Clin. Immunol., 221, 108603, 10.1016/j.clim.2020.108603 Song, 2020, COVID-19, microangiopathy, hemostatic activation, and complement, J. Clin. Invest., 130, 3950 Noris, 2020, The case of complement activation in COVID-19 multiorgan impact, Kidney Int., 98, 314, 10.1016/j.kint.2020.05.013 Pfister, 2020, Complement activation in kidneys of patients with COVID-19, Front. Immunol., 11, 594849, 10.3389/fimmu.2020.594849 de Nooijer, 2021, Complement activation in the disease course of coronavirus disease 2019 and its effects on clinical outcomes, J. Infect. Dis., 223, 214, 10.1093/infdis/jiaa646 Skendros, 2020, Complement and tissue factor–enriched neutrophil extracellular traps are key drivers in COVID-19 immunothrombosis, J. Clin. Invest., 130, 6151, 10.1172/JCI141374 Mastaglio, 2020, The first case of COVID-19 treated with the complement C3 inhibitor AMY-101, Clin. Immunol., 215, 108450, 10.1016/j.clim.2020.108450 Mastellos, 2020, Complement C3 vs C5 inhibition in severe COVID-19: early clinical findings reveal differential biological efficacy, Clin. Immunol., 220, 108598, 10.1016/j.clim.2020.108598 Al-Bataineh, 2017, Novel roles for mucin 1 in the kidney, Curr. Opin. Nephrol. Hypertens., 26, 384, 10.1097/MNH.0000000000000350 Kost-Alimova, 2020, A High-content screen for mucin-1-reducing compounds identifies fostamatinib as a candidate for rapid repurposing for acute lung injury, Cell Rep. Med., 1, 100137, 10.1016/j.xcrm.2020.100137 Pamuk, 2010, Spleen tyrosine kinase inhibition prevents tissue damage after ischemia-reperfusion, Am. J. Physiol. Gastroint. Liver Physiol., 299, G391, 10.1152/ajpgi.00198.2010 Pamuk, 2015, Spleen tyrosine kinase (Syk) inhibitor fostamatinib limits tissue damage and fibrosis in a bleomycin-induced scleroderma mouse model, Clin. Exp. Rheumatol., 33, S15 Braselmann, 2006, R406, an orally available spleen tyrosine kinase inhibitor blocks fc receptor signaling and reduces immune complex-mediated inflammation, J. Pharmacol. Exp. Ther., 319, 998, 10.1124/jpet.106.109058 Antenucci, 2018, Phosphorylated immunoreceptor tyrosine-based activation motifs and integrin cytoplasmic domains activate spleen tyrosine kinase via distinct mechanisms, J. Biol. Chem., 293, 4591, 10.1074/jbc.RA117.000660 Chauhan, 2012, Immune complexes and late complement proteins trigger activation of Syk tyrosine kinase in human CD4(+) T cells, Clin. Exp. Immunol., 167, 235, 10.1111/j.1365-2249.2011.04505.x Strich, 2020, Fostamatinib inhibits neutrophils extracellular traps induced by COVID-19 patient plasma: a potential therapeutic, J. Infect. Dis., 223, 981, 10.1093/infdis/jiaa789 Kitamoto, 2013, MUC1 enhances hypoxia-driven angiogenesis through the regulation of multiple proangiogenic factors, Oncogene, 32, 4614, 10.1038/onc.2012.478 Chakraborty, 2006, Hypoxia regulates cross-talk between syk and lck leading to breast cancer progression and angiogenesis *, J. Biol. Chem., 281, 11322, 10.1074/jbc.M512546200 Jang, 2021, Spleen tyrosine kinase regulates crosstalk of hypoxia-inducible factor-1α and nuclear factor (erythroid-derived2)-like 2 for B cell survival, Int. Immunopharmacol., 95, 107509, 10.1016/j.intimp.2021.107509 Serebrovska, 2020, Hypoxia, HIF-1α, and COVID-19: from pathogenic factors to potential therapeutic targets, Acta Pharmacol. Sin., 41, 1539, 10.1038/s41401-020-00554-8 Gusarova, 2011, Hypoxia leads to Na,K-ATPase downregulation via Ca(2+) release-activated Ca(2+) channels and AMPK activation, Mol. Cell. Biol., 31, 3546, 10.1128/MCB.05114-11 Racioppi, 2008, Calcium/calmodulin-dependent kinase IV in immune and inflammatory responses: novel routes for an ancient traveller, Trends Immunol., 29, 600, 10.1016/j.it.2008.08.005 Greka, 2011, Balancing calcium signals through TRPC5 and TRPC6 in podocytes, J. Am. Soc. Nephrol., 22, 1969, 10.1681/ASN.2011040370 Ichinose, 2016, Lupus nephritis IgG induction of calcium/calmodulin-dependent protein kinase IV expression in podocytes and alteration of their function, Arthritis Rheum., 68, 944, 10.1002/art.39499 Maeda, 2018, CaMK4 compromises podocyte function in autoimmune and nonautoimmune kidney disease, J. Clin. Invest., 128, 3445, 10.1172/JCI99507 Brook, 2021, Feasibility and safety of ultrasound-guided minimally invasive autopsy in COVID-19 patients, Abdominal Radiol., 46, 1263, 10.1007/s00261-020-02753-7 Matsumoto, 2017, C3a enhances the formation of intestinal organoids through C3aR1, Front. Immunol., 8, 10.3389/fimmu.2017.01046 Satyam, 2020, Complement deposition on the surface of RBC after trauma serves a biomarker of moderate trauma severity: a prospective study, Shock, 53, 16, 10.1097/SHK.0000000000001348 Satyam, 2019, Complement and coagulation cascades in trauma, Acute Med. Surgery, 6, 329, 10.1002/ams2.426 Satyam, 2017, Intracellular activation of complement 3 is responsible for intestinal tissue damage during mesenteric ischemia, J. Immunol., 198, 788, 10.4049/jimmunol.1502287 Kudose, 2020, Kidney biopsy findings in patients with COVID-19, J. Am. Soc. Nephrol., 31, 1959, 10.1681/ASN.2020060802 Golmai, 2020, Histopathologic and Ultrastructural findings in postmortem kidney biopsy material in 12 patients with AKI and COVID-19, J. Am. Soc. Nephrol., 31, 1944, 10.1681/ASN.2020050683 Santoriello, 2020, Postmortem kidney pathology findings in patients with COVID-19, J. Am. Soc. Nephrol., 31, 2158, 10.1681/ASN.2020050744 Tsokos, 2004, Autoimmunity, complement activation, tissue injury and reciprocal effects, Curr. Dir. Autoimmun., 7, 149, 10.1159/000075691 Wang, 2021, Diverse functional autoantibodies in patients with COVID-19, Nature, 595, 283, 10.1038/s41586-021-03631-y Satyam, 2021, Activation of classical and alternative complement pathways in the pathogenesis of lung injury in COVID-19, Clin. Immunol., 226, 108716, 10.1016/j.clim.2021.108716 Gavriilaki, 2021, Genetic justification of severe COVID-19 using a rigorous algorithm, Clin. Immunol., 226, 108726, 10.1016/j.clim.2021.108726 Pastor, 2013, Complement factor H gene (CFH) polymorphisms C-257T, G257A and haplotypes are associated with protection against severe dengue phenotype, possible related with high CFH expression, Hum. Immunol., 74, 1225, 10.1016/j.humimm.2013.05.005 Gibier, 2017, Dual role of MUC1 mucin in kidney ischemia-reperfusion injury: Nephroprotector in early phase, but pro-fibrotic in late phase, Biochim. Biophys. Acta (BBA) - Mol. Basis Dis., 1863, 1336, 10.1016/j.bbadis.2017.03.023 Pastor-Soler, 2015, Muc1 is protective during kidney ischemia-reperfusion injury, Am. J. Physiol. Renal. Physiol., 15, F1452, 10.1152/ajprenal.00066.2015 Otomo, 2015, Cutting edge: nanogel-based delivery of an inhibitor of CaMK4 to CD4+ T cells suppresses experimental autoimmune encephalomyelitis and lupus-like disease in mice, J. Immunol., 195, 5533, 10.4049/jimmunol.1501603 Geahlen, 2014, Getting Syk: spleen tyrosine kinase as a therapeutic target, Trends Pharmacol. Sci., 35, 414, 10.1016/j.tips.2014.05.007 Schuringa, 2001, C-Jun and c-Fos cooperate with STAT3 in IL-6-induced transactivation of the IL-6 respone element (IRE), Cytokine, 14, 78, 10.1006/cyto.2001.0856 McAdoo, 2020, Spleen tyrosine kinase inhibition is an effective treatment for established vasculitis in a pre-clinical model, Kidney Int., 97, 1196, 10.1016/j.kint.2019.12.014 McAdoo, 2018, Role of the spleen tyrosine kinase pathway in driving inflammation in IgA nephropathy, Semin. Nephrol., 38, 496, 10.1016/j.semnephrol.2018.05.019 Shi, 2006, Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis, Blood, 107, 4554, 10.1182/blood-2005-09-3616 Leroy, 2002, Expression of human mucin genes in normal kidney and renal cell carcinoma, Histopathology, 40, 450, 10.1046/j.1365-2559.2002.01408.x d’Alessandro, 2020, Serum KL-6 levels in pulmonary Langerhans’ cell histiocytosis, Eur. J. Clin. Investig., 50, 10.1111/eci.13242 Syrkina, 2017, Dual role of the extracellular domain of human Mucin MUC1 in metastasis, J. Cell. Biochem., 118, 4002, 10.1002/jcb.26056 Merle, 2015, Complement system part I - molecular mechanisms of activation and regulation, Front. Immunol., 6, 262, 10.3389/fimmu.2015.00262 Elsner, 1994, C3a activates reactive oxygen radical species production and intracellular calcium transients in human eosinophils, Eur. J. Immunol., 24, 518, 10.1002/eji.1830240304 Nie, 2016, Mucin-1 increases renal TRPV5 activity in vitro, and urinary level associates with calcium nephrolithiasis in patients, J. Am. Soc. Nephrol., 27, 3447, 10.1681/ASN.2015101100 Kulathu, 2008, The kinase Syk as an adaptor controlling sustained calcium signalling and B-cell development, EMBO J., 27, 1333, 10.1038/emboj.2008.62 Rao, 2013, Spleen tyrosine kinase (Syk)-dependent calcium signals mediate efficient CpG-induced exocytosis of tumor necrosis factor alpha (TNFalpha) in innate immune cells, J. Biol. Chem., 288, 12448, 10.1074/jbc.M113.454405 Ferretti, 2018, Calcium/Calmodulin kinase IV controls the function of both T cells and kidney resident cells, Front. Immunol., 9, 2113, 10.3389/fimmu.2018.02113 Li, 2019, MiR-129-5p inhibits liver cancer growth by targeting calcium calmodulin-dependent protein kinase IV (CAMK4), Cell Death Dis., 10, 789, 10.1038/s41419-019-1923-4 Satyam, 2020, Cell-derived extracellular matrix-rich biomimetic substrate supports podocyte proliferation, differentiation, and maintenance of native phenotype, Adv. Funct. Mater., 30, 1908752, 10.1002/adfm.201908752