A diabetic milieu increases ACE2 expression and cellular susceptibility to SARS-CoV-2 infections in human kidney organoids and patient cells

Baer, 2008, Human renal cells from the thick ascending limb and early distal tubule: characterization of primary isolated and cultured cells by reverse transcription polymerase chain reaction, Nephrology (Carlton), 13, 316, 10.1111/j.1440-1797.2008.00927.x Baer, 1997, Isolation of proximal and distal tubule cells from human kidney by immunomagnetic separation. Technical note, Kidney Int., 52, 1321, 10.1038/ki.1997.457 Bastard, 2021, Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine, J. Exp. Med., 218, 10.1084/jem.20202486 Becker, 2008, Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice, Proc. Natl. Acad. Sci. USA, 105, 19944, 10.1073/pnas.0808116105 Bonnet, 2007, A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth, Cancer Cell, 11, 37, 10.1016/j.ccr.2006.10.020 Braun, 2020, SARS-CoV-2 renal tropism associates with acute kidney injury, Lancet, 396, 597, 10.1016/S0140-6736(20)31759-1 Bülow, 2019, Extracellular matrix in kidney fibrosis: more than just a scaffold, J. Histochem. Cytochem., 67, 643, 10.1369/0022155419849388 Cantuti-Castelvetri, 2020, Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity, Science, 370, 856, 10.1126/science.abd2985 Chen, 2017, A convenient method for quantifying collagen fibers in atherosclerotic lesions by ImageJ software, Int. J. Clin. Exp. Med., 10, 14927 Clarke, 2012, Angiotensin-converting enzyme 2: the first decade, Int. J. Hypertens., 2012, 307315, 10.1155/2012/307315 Clement, 2019, CRISPResso2 provides accurate and rapid genome editing sequence analysis, Nat. Biotechnol., 37, 224, 10.1038/s41587-019-0032-3 Codo, 2020, Elevated glucose levels favor SARS-CoV-2 infection and monocyte response through a HIF-1α/glycolysis-dependent axis, Cell Metab, 32, 437, 10.1016/j.cmet.2020.07.007 Cook, 2021, Targeting glucose metabolism of cancer cells with dichloroacetate to radiosensitize high-grade gliomas, Int. J. Mol. Sci., 22, 7265, 10.3390/ijms22147265 Crackower, 2002, Angiotensin-converting enzyme 2 is an essential regulator of heart function, Nature, 417, 822, 10.1038/nature00786 Daly, 2020, Neuropilin-1 is a host factor for SARS-CoV-2 infection, Science, 370, 861, 10.1126/science.abd3072 Deng, 2020, Single-cell RNA sequencing data suggest a role for angiotensin-converting enzyme 2 in kidney impairment in patients infected with 2019-novel coronavirus, Chin. Med. J. (Engl), 133, 1129, 10.1097/CM9.0000000000000783 Dhillon, 2021, The nuclear receptor ESRRA protects from kidney disease by coupling metabolism and differentiation, Cell Metab, 33, 379, 10.1016/j.cmet.2020.11.011 Diao, 2021, Human kidney is a target for novel severe acute respiratory syndrome coronavirus 2 infection, Nat. Commun., 12, 2506, 10.1038/s41467-021-22781-1 El Jamal, 2021, Tissue-based SARS-CoV-2 detection in fatal COVID-19 infections: sustained direct viral-induced damage is not necessary to drive disease progression, Hum. Pathol., 114, 110, 10.1016/j.humpath.2021.04.012 Eleftheriadis, 2013, Dichloroacetate at therapeutic concentration alters glucose metabolism and induces regulatory T-cell differentiation in alloreactive human lymphocytes, J. Basic Clin. Physiol. Pharmacol., 24, 271, 10.1515/jbcpp-2013-0001 Ellinghaus, 2020, The ABO blood group locus and a chromosome 3 gene cluster associate with SARS-CoV-2 respiratory failure in an Italian-Spanish genome-wide association analysis, Preprint at MedRxiv Friederich-Persson, 2020, Mitochondrial angiotensin II receptors regulate oxygen consumption in kidney mitochondria from healthy and type 1 diabetic rats, Am. J. Physiol. Renal Physiol., 318, F683, 10.1152/ajprenal.00417.2019 Friederich, 2008, Diabetes-induced up-regulation of uncoupling protein-2 results in increased mitochondrial uncoupling in kidney proximal tubular cells, Biochim. Biophys. Acta, 1777, 935, 10.1016/j.bbabio.2008.03.030 Garreta, 2019, Fine tuning the extracellular environment accelerates the derivation of kidney organoids from human pluripotent stem cells, Nat. Mater., 18, 397, 10.1038/s41563-019-0287-6 Genuth, 2002, Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus, JAMA, 287, 2563, 10.1001/jama.287.19.2563 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 Haga, 2008, Modulation of TNF-alpha-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-alpha production and facilitates viral entry, Proc. Natl. Acad. Sci. USA, 105, 7809, 10.1073/pnas.0711241105 Härdtner, 2013, High glucose activates the alternative ACE2/Ang-(1–7)/Mas and APN/Ang IV/IRAP RAS axes in pancreatic β-cells, Int. J. Mol. Med., 32, 795, 10.3892/ijmm.2013.1469 Hoffmann, 2020, SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor, Cell, 181, 271, 10.1016/j.cell.2020.02.052 Imai, 2005, Angiotensin-converting enzyme 2 protects from severe acute lung failure, Nature, 436, 112, 10.1038/nature03712 Jansen, 2021, SARS-CoV-2 infects the human kidney and drives fibrosis in kidney organoids, Cell Stem Cell, 29, 217, 10.1016/j.stem.2021.12.010 Jiang, 2020, Hypertension and renin-angiotensin system blockers are not associated with expression of angiotensin-converting enzyme 2 (ACE2) in the kidney, Eur. Heart J., 41, 4580, 10.1093/eurheartj/ehaa794 Khalili, 2021, Prevalence, risk factors and outcomes associated with acute kidney injury in patients hospitalized for COVID-19: a comparative study between diabetic and nondiabetic patients, J. Diabetes Res., 2021, 6666086 Korotkevich, 2021, Fast gene set enrichment analysis, Preprint at bioRxiv Kuba, 2005, A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury, Nat. Med., 11, 875, 10.1038/nm1267 Kuleshov, 2016, Enrichr: a comprehensive gene set enrichment analysis web server 2016 update, Nucleic Acids Res., 44, W90, 10.1093/nar/gkw377 Legrand, 2021, Pathophysiology of COVID-19-associated acute kidney injury, Nat. Rev. Nephrol., 17, 751, 10.1038/s41581-021-00452-0 Lely, 2004, Renal ACE2 expression in human kidney disease, J. Pathol., 204, 587, 10.1002/path.1670 Li, 2018, The role of peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) in kidney disease, Semin. Nephrol., 38, 121, 10.1016/j.semnephrol.2018.01.003 Lim, 2021, COVID-19 and diabetes mellitus: from pathophysiology to clinical management, Nat. Rev. Endocrinol., 17, 11, 10.1038/s41574-020-00435-4 Lin, 2021, Single-cell analysis of angiotensin-converting enzyme II expression in human kidneys and bladders reveals a potential route of 2019 novel coronavirus infection, Chin. Med. J. (Engl), 134, 935, 10.1097/CM9.0000000000001439 Lindström, 2018, Progressive recruitment of mesenchymal progenitors reveals a time-dependent process of cell fate acquisition in mouse and human nephrogenesis, Dev. Cell, 45, 651, 10.1016/j.devcel.2018.05.010 Lindström, 2018, Conserved and divergent features of human and mouse kidney organogenesis, J. Am. Soc. Nephrol., 29, 785, 10.1681/ASN.2017080887 Maksimowski, 2020, Kidney ACE2 expression: implications for chronic kidney disease, PLoS One, 15, 10.1371/journal.pone.0241534 Marco, 2019, Engineering human pluripotent stem cells (hPSCs) lines with CRISPR/Cas9 for inducible knock out in kidney organoids Marco, 2020, Engineering human pluripotent stem cells (hPSCs) lines with CRISPR/Cas9 for inducible knock out in kidney organoids Menon, 2020, SARS-CoV-2 receptor networks in diabetic and COVID-19-associated kidney disease, Kidney Int., 98, 1502, 10.1016/j.kint.2020.09.015 Mizuiri, 2008, Expression of ACE and ACE2 in individuals with diabetic kidney disease and healthy controls, Am. J. Kidney Dis., 51, 613, 10.1053/j.ajkd.2007.11.022 Monteil, 2020, Inhibition of SARS-CoV-2 infections in engineered human tissues using clinical-grade soluble human ACE2, Cell, 181, 905, 10.1016/j.cell.2020.04.004 Monteil, 2021, Human soluble ACE2 improves the effect of remdesivir in SARS-CoV-2 infection, EMBO Mol. Med., 13, 10.15252/emmm.202013426 Nadim, 2020, COVID-19-associated acute kidney injury: consensus report of the 25th Acute Disease Quality Initiative (ADQI) Workgroup, Nat. Rev. Nephrol., 16, 747, 10.1038/s41581-020-00356-5 Peña Silva, 2012, Impact of ACE2 deficiency and oxidative stress on cerebrovascular function with aging, Stroke, 43, 3358, 10.1161/STROKEAHA.112.667063 Puelles, 2020, Multiorgan and renal tropism of SARS-CoV-2, N. Engl. J. Med., 383, 590, 10.1056/NEJMc2011400 Reich, 2008, Decreased glomerular and tubular expression of ACE2 in patients with type 2 diabetes and kidney disease, Kidney Int., 74, 1610, 10.1038/ki.2008.497 Sandooja, 2020, Heightened ACE activity and unfavorable consequences in COVID-19 diabetic subjects, Int. J. Endocrinol., 2020, 7847526, 10.1155/2020/7847526 Santoriello, 2020, Postmortem kidney pathology findings in patients with COVID-19, J. Am. Soc. Nephrol., 31, 2158, 10.1681/ASN.2020050744 Sas, 2016, Tissue-specific metabolic reprogramming drives nutrient flux in diabetic complications, JCI Insight, 1, 10.1172/jci.insight.86976 Shilts, 2021, No evidence for basigin/CD147 as a direct SARS-CoV-2 spike binding receptor, Sci. Rep., 11, 413, 10.1038/s41598-020-80464-1 Soler, 2007, ACE2 inhibition worsens glomerular injury in association with increased ACE expression in streptozotocin-induced diabetic mice, Kidney Int., 72, 614, 10.1038/sj.ki.5002373 Soler, 2013, ACE2 alterations in kidney disease, Nephrol. Dial. Transplant., 28, 2687, 10.1093/ndt/gft320 Stuart, 2019, Comprehensive integration of single-cell data, Cell, 177, 1888, 10.1016/j.cell.2019.05.031 Triana, 2021, Single-cell analyses reveal SARS-CoV-2 interference with intrinsic immune response in the human gut, Mol. Syst. Biol., 17, 10.15252/msb.202110232 Ugwueze, 2020, COVID-19 and diabetes mellitus: the link and clinical implications, Dubai Diabetes Endocrinol. J., 26, 69, 10.1159/000511354 van der Made, 2020, Presence of genetic variants among young men with severe COVID-19, JAMA, 324, 663, 10.1001/jama.2020.13719 Vasquez-Muñoz, 2021, Oscillatory pattern of glycemic control in patients with diabetes mellitus, Sci Rep., 11, 5789, 10.1038/s41598-021-84822-5 Volbeda, 2021, Comparison of renal histopathology and gene expression profiles between severe COVID-19 and bacterial sepsis in critically ill patients, Crit. Care, 25, 202, 10.1186/s13054-021-03631-4 Walls, 2020, Structure, function, and antigenicity of the SARS-CoV-2 Spike glycoprotein, Cell, 181, 281, 10.1016/j.cell.2020.02.058 Wan, 2020, Receptor recognition by the novel coronavirus from Wuhan: an analysis based on decade-long structural studies of SARS coronavirus, J. Virol., 94, 10.1128/JVI.00127-20 Wang, 2020, CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells, Signal Transduct. Target. Ther., 5, 283, 10.1038/s41392-020-00426-x Wrapp, 2020, Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation, Science, 367, 1260, 10.1126/science.abb2507 2003, Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study, JAMA, 290, 2159, 10.1001/jama.290.16.2159 Wysocki, 2014, ACE2 deficiency increases NADPH-mediated oxidative stress in the kidney, Physiol. Rep., 2, 10.1002/phy2.264 Yang, 2015, Visit-to-visit glucose variability predicts the development of end-stage renal disease in type 2 diabetes: 10-year follow-up of Taiwan diabetes study, Med. (Baltim.), 94 Ye, 2004, Increased ACE 2 and decreased ACE protein in renal tubules from diabetic mice: a renoprotective combination?, Hypertension, 43, 1120, 10.1161/01.HYP.0000126192.27644.76 Ye, 2006, Glomerular localization and expression of angiotensin-converting enzyme 2 and angiotensin-converting enzyme: implications for albuminuria in diabetes, J. Am. Soc. Nephrol., 17, 3067, 10.1681/ASN.2006050423 Zhang, 2020, Single-cell landscape of immunological responses in patients with COVID-19, Nat. Immunol., 21, 1107, 10.1038/s41590-020-0762-x Zhang, 2020, Inborn errors of type I IFN immunity in patients with life-threatening COVID-19, Science, 370, eabd4570, 10.1126/science.abd4570 Zhou, 2020, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, 579, 270, 10.1038/s41586-020-2012-7 Zou, 2020, Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection, Front. Med., 14, 185, 10.1007/s11684-020-0754-0