Myeloid Heterogeneity in Kidney Disease as Revealed through Single-Cell RNA Sequencing.
RNA
basic science
chronic kidney disease
dendritic cells
kidney disease
macrophage
monocytes
myeloid cells
scRNA-sequencing
sequence analysis
Journal
Kidney360
ISSN: 2641-7650
Titre abrégé: Kidney360
Pays: United States
ID NLM: 101766381
Informations de publication
Date de publication:
25 11 2021
25 11 2021
Historique:
received:
02
06
2021
accepted:
27
08
2021
entrez:
4
4
2022
pubmed:
5
4
2022
medline:
8
4
2022
Statut:
epublish
Résumé
Kidney disease represents a global health burden of increasing prevalence and is an independent risk factor for cardiovascular disease. Myeloid cells are a major cellular compartment of the immune system; they are found in the healthy kidney and in increased numbers in the damaged and/or diseased kidney, where they act as key players in the progression of injury, inflammation, and fibrosis. They possess enormous plasticity and heterogeneity, adopting different phenotypic and functional characteristics in response to stimuli in the local milieu. Although this inherent complexity remains to be fully understood in the kidney, advances in single-cell genomics promise to change this. Specifically, single-cell RNA sequencing (scRNA-seq) has had a transformative effect on kidney research, enabling the profiling and analysis of the transcriptomes of single cells at unprecedented resolution and throughput, and subsequent generation of cell atlases. Moving forward, combining scRNA- and single-nuclear RNA-seq with greater-resolution spatial transcriptomics will allow spatial mapping of kidney disease of varying etiology to further reveal the patterning of immune cells and nonimmune renal cells. This review summarizes the roles of myeloid cells in kidney health and disease, the experimental workflow in currently available scRNA-seq technologies, and published findings using scRNA-seq in the context of myeloid cells and the kidney.
Identifiants
pubmed: 35372996
doi: 10.34067/KID.0003682021
pii: 02200512-202111000-00022
pmc: PMC8785845
doi:
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1844-1851Subventions
Organisme : British Heart Foundation
ID : FS/19/55/34890
Pays : United Kingdom
Informations de copyright
Copyright © 2021 by the American Society of Nephrology.
Déclaration de conflit d'intérêts
L. Denby reports receiving research funding from GlaxoSmithKline and Regulus Therapeutics. The remaining author has nothing to disclose.
Références
GBD Chronic Kidney Disease Collaboration: Global, regional, and national burden of chronic kidney disease, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet 395: 709–733, 2020 https://doi.org/10.1016/S0140-6736(20)30045-3
doi: 10.1016/S0140-6736(20)30045-3
Park J, Shrestha R, Qiu C, Kondo A, Huang S, Werth M, Li M, Barasch J, Suszták K: Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Science 360: 758–763, 2018 https://doi.org/10.1126/science.aar2131
doi: 10.1126/science.aar2131
Tecklenborg J, Clayton D, Siebert S, Coley SM: The role of the immune system in kidney disease. Clin Exp Immunol 192: 142–150, 2018 https://doi.org/10.1111/cei.13119
doi: 10.1111/cei.13119
Bassler K, Schulte-Schrepping J, Warnat-Herresthal S, Aschenbrenner AC, Schultze JL: The myeloid cell compartment-cell by cell. Annu Rev Immunol 37: 269–293, 2019 https://doi.org/10.1146/annurev-immunol-042718-041728
doi: 10.1146/annurev-immunol-042718-041728
Xu L, Sharkey D, Cantley LG: Tubular GM-CSF promotes late MCP-1/CCR2-mediated fibrosis and inflammation after ischemia/reperfusion injury. J Am Soc Nephrol 30: 1825–1840, 2019 https://doi.org/10.1681/ASN.2019010068
doi: 10.1681/ASN.2019010068
Stewart BJ, Ferdinand JR, Clatworthy MR: Using single-cell technologies to map the human immune system - Implications for nephrology. Nat Rev Nephrol 16: 112–128, 2020 https://doi.org/10.1038/s41581-019-0227-3
doi: 10.1038/s41581-019-0227-3
Stubbington MJT, Rozenblatt-Rosen O, Regev A, Teichmann SA: Single-cell transcriptomics to explore the immune system in health and disease. Science 358: 58–63, 2017 https://doi.org/10.1126/science.aan6828
doi: 10.1126/science.aan6828
Berry MR, Mathews RJ, Ferdinand JR, Jing C, Loudon KW, Wlodek E, Dennison TW, Kuper C, Neuhofer W, Clatworthy MR: Renal sodium gradient orchestrates a dynamic antibacterial defense zone. Cell 170: 860–874.e19, 2017 https://doi.org/10.1016/j.cell.2017.07.022
doi: 10.1016/j.cell.2017.07.022
Stewart BJ, Ferdinand JR, Young MD, Mitchell TJ, Loudon KW, Riding AM, Richoz N, Frazer GL, Staniforth JUL, Vieira Braga FA, Botting RA, Popescu DM, Vento-Tormo R, Stephenson E, Cagan A, Farndon SJ, Polanski K, Efremova M, Green K, Del Castillo Velasco-Herrera M, Guzzo C, Collord G, Mamanova L, Aho T, Armitage JN, Riddick ACP, Mushtaq I, Farrell S, Rampling D, Nicholson J, Filby A, Burge J, Lisgo S, Lindsay S, Bajenoff M, Warren AY, Stewart GD, Sebire N, Coleman N, Haniffa M, Teichmann SA, Behjati S, Clatworthy MR: Spatiotemporal immune zonation of the human kidney. Science 365: 1461–1466, 2019 https://doi.org/10.1126/science.aat5031
doi: 10.1126/science.aat5031
Conway BR, O’Sullivan ED, Cairns C, O’Sullivan J, Simpson DJ, Salzano A, Connor K, Ding P, Humphries D, Stewart K, Teenan O, Pius R, Henderson NC, Bénézech C, Ramachandran P, Ferenbach D, Hughes J, Chandra T, Denby L: Kidney single-cell atlas reveals myeloid heterogeneity in progression and regression of kidney disease. J Am Soc Nephrol 31: 2833–2854, 2020 https://doi.org/10.1681/ASN.2020060806
doi: 10.1681/ASN.2020060806
Kurts C, Ginhoux F, Panzer U: Kidney dendritic cells: Fundamental biology and functional roles in health and disease. Nat Rev Nephrol 16: 391–407, 2020 https://doi.org/10.1038/s41581-020-0272-y
doi: 10.1038/s41581-020-0272-y
Mass E, Ballesteros I, Farlik M, Halbritter F, Günther P, Crozet L, Jacome-Galarza CE, Händler K, Klughammer J, Kobayashi Y, Gomez-Perdiguero E, Schultze JL, Beyer M, Bock C, Geissmann F: Specification of tissue-resident macrophages during organogenesis. Science 353: aaf4238, 2016 https://doi.org/10.1126/science.aaf4238
doi: 10.1126/science.aaf4238
Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F: A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86–90, 2012 https://doi.org/10.1126/science.1219179
doi: 10.1126/science.1219179
Park J, Liu CL, Kim J, Susztak K: Understanding the kidney one cell at a time. Kidney Int 96: 862–870, 2019 https://doi.org/10.1016/j.kint.2019.03.035
doi: 10.1016/j.kint.2019.03.035
Rao DA, Arazi A, Wofsy D, Diamond B: Design and application of single-cell RNA sequencing to study kidney immune cells in lupus nephritis. Nat Rev Nephrol 16: 238–250, 2020 https://doi.org/10.1038/s41581-019-0232-6
doi: 10.1038/s41581-019-0232-6
Li H, Humphreys BD: Single cell technologies: Beyond microfluidics. Kidney 360 2: 1196–1204, 2021 https://doi.org/10.34067/KID.0001822021
doi: 10.34067/KID.0001822021
O’Flanagan CH, Campbell KR, Zhang AW, Kabeer F, Lim JLP, Biele J, Eirew P, Lai D, McPherson A, Kong E, Bates C, Borkowski K, Wiens M, Hewitson B, Hopkins J, Pham J, Ceglia N, Moore R, Mungall AJ, McAlpine JN, Shah SP, Aparicio S; CRUK IMAXT Grand Challenge Team: Dissociation of solid tumor tissues with cold active protease for single-cell RNA-seq minimizes conserved collagenase-associated stress responses. Genome Biol 20: 210, 2019 https://doi.org/10.1186/s13059-019-1830-0
doi: 10.1186/s13059-019-1830-0
Dangi A, Natesh NR, Husain I, Ji Z, Barisoni L, Kwun J, Shen X, Thorp EB, Luo X: Single cell transcriptomics of mouse kidney transplants reveals a myeloid cell pathway for transplant rejection. JCI Insight 5: e141321, 2020 https://doi.org/10.1172/jci.insight.141321
doi: 10.1172/jci.insight.141321
Wu H, Kirita Y, Donnelly EL, Humphreys BD: Advantages of single-nucleus over single-cell RNA sequencing of adult kidney: Rare cell types and novel cell states revealed in fibrosis. J Am Soc Nephrol 30: 23–32, 2019 https://doi.org/10.1681/ASN.2018090912
doi: 10.1681/ASN.2018090912
Nistala R, Meuth A, Smith C, Annayya A: Reliable and high efficiency extraction of kidney immune cells. J Vis Exp 114: 54368, 2016 https://doi.org/10.3791/54368
doi: 10.3791/54368
Peterson VM, Zhang KX, Kumar N, Wong J, Li L, Wilson DC, Moore R, McClanahan TK, Sadekova S, Klappenbach JA: Multiplexed quantification of proteins and transcripts in single cells. Nat Biotechnol 35: 936–939, 2017 https://doi.org/10.1038/nbt.3973
doi: 10.1038/nbt.3973
Stoeckius M, Hafemeister C, Stephenson W, Houck-Loomis B, Chattopadhyay PK, Swerdlow H, Satija R, Smibert P: Simultaneous epitope and transcriptome measurement in single cells. Nat Methods 14: 865–868, 2017 https://doi.org/10.1038/nmeth.4380
doi: 10.1038/nmeth.4380
Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML, Snyder MP, Chang HY, Greenleaf WJ: Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523: 486–490, 2015 https://doi.org/10.1038/nature14590
doi: 10.1038/nature14590
Muto Y, Wilson PC, Ledru N, Wu H, Dimke H, Waikar SS, Humphreys BD: Single cell transcriptional and chromatin accessibility profiling redefine cellular heterogeneity in the adult human kidney. Nat Commun 12: 2190, 2021 https://doi.org/10.1038/s41467-021-22368-w
doi: 10.1038/s41467-021-22368-w
Miao Z, Balzer MS, Ma Z, Liu H, Wu J, Shrestha R, Aranyi T, Kwan A, Kondo A, Pontoglio M, Kim J, Li M, Kaestner KH, Suszták K: Single cell regulatory landscape of the mouse kidney highlights cellular differentiation programs and disease targets. Nat Commun 12: 2277, 2021 https://doi.org/10.1038/s41467-021-22266-1
doi: 10.1038/s41467-021-22266-1
Ferreira RM, Sabo AR, Winfree S, Collins KS, Janosevic D, Gulbronson C, Cheng Y, Casbon L, Barwinska D, Ferkowicz MJ, Xuei X, Zhang C, Dunn KW, Kelly KJ, Sutton TA, Hato T, Dagher PC, El-Achkar TM, Eadon MT: Integration of spatial and single-cell transcriptomics localizes epithelial cell –immune cross-talk in acute kidney injury. JCI Insight 6: e147703, 2021
Menon R, Otto EA, Hoover P, Eddy S, Mariani L, Godfrey B, Berthier CC, Eichinger F, Subramanian L, Harder J, Ju W, Nair V, Larkina M, Naik AS, Luo J, Jain S, Sealfon R, Troyanskaya O, Hacohen N, Hodgin JB, Kretzler M; Kidney Precision Medicine Project Kpmp; Nephrotic Syndrome Study Network (NEPTUNE): Single cell transcriptomics identifies focal segmental glomerulosclerosis remission endothelial biomarker. JCI Insight 5: e133267, 2020 https://doi.org/10.1172/jci.insight.133267
doi: 10.1172/jci.insight.133267
Salei N, Rambichler S, Salvermoser J, Papaioannou NE, Schuchert R, Pakalniškytė D, Li N, Marschner JA, Lichtnekert J, Stremmel C, Cernilogar FM, Salvermoser M, Walzog B, Straub T, Schotta G, Anders HJ, Schulz C, Schraml BU: The kidney contains ontogenetically distinct dendritic cell and macrophage subtypes throughout development that differ in their inflammatory properties. J Am Soc Nephrol 31: 257–278, 2020 https://doi.org/10.1681/ASN.2019040419
doi: 10.1681/ASN.2019040419
Tabula Muris Consortium: A single-cell transcriptomic atlas characterizes ageing tissues in the mouse. Nature 583: 590–595, 2020 https://doi.org/10.1038/s41586-020-2496-1
doi: 10.1038/s41586-020-2496-1
Clatworthy MR: How to find a resident kidney macrophage: The single-cell sequencing solution. J Am Soc Nephrol 30: 715–716, 2019 https://doi.org/10.1681/ASN.2019030245
doi: 10.1681/ASN.2019030245
Zimmerman KA, Bentley MR, Lever JM, Li Z, Crossman DK, Song CJ, Liu S, Crowley MR, George JF, Mrug M, Yoder BK: Single-cell RNA sequencing identifies candidate renal resident macrophage gene expression signatures across species. J Am Soc Nephrol 30: 767–781, 2019 https://doi.org/10.1681/ASN.2018090931
doi: 10.1681/ASN.2018090931
Wu H, Malone AF, Donnelly EL, Kirita Y, Uchimura K, Ramakrishnan SM, Gaut JP, Humphreys BD: Single-cell transcriptomics of a human kidney allograft biopsy specimen defines a diverse inflammatory response. J Am Soc Nephrol 29: 2069–2080, 2018 https://doi.org/10.1681/ASN.2018020125
doi: 10.1681/ASN.2018020125
Lu X, Li N, Shushakova N, Schmitt R, Menne J, Susnik N, Meier M, Leitges M, Haller H, Gueler F, Rong S: C57BL/6 and 129/Sv mice: Genetic difference to renal ischemia-reperfusion. J Nephrol 25: 738–743, 2012 https://doi.org/10.5301/jn.5000053
doi: 10.5301/jn.5000053
O’Sullivan J, Finnie SL, Teenan O, Cairns C, Boyd A, Bailey MA, Thomson A, Hughes J, Bénézech C, Conway BR, Denby L: Refining the mouse subtotal nephrectomy in male 129S2/SV mice for consistent modeling of progressive kidney disease with renal inflammation and cardiac dysfunction. Front Physiol 10: 1365, 2019 https://doi.org/10.3389/fphys.2019.01365
doi: 10.3389/fphys.2019.01365
do Valle Duraes F, Lafont A, Beibel M, Martin K, Darribat K, Cuttat R, Waldt A, Naumann U, Wieczorek G, Gaulis S, Pfister S, Mertz KD, Jianping L, Roma G, Warncke M: Immune cell landscaping reveals a protective role for regulatory T cells during kidney injury and fibrosis. JCI Insight 5: e130651, 2020 https://doi.org/10.1172/jci.insight.130651
doi: 10.1172/jci.insight.130651
Kirita Y, Wu H, Uchimura K, Wilson PC, Humphreys BD: Cell profiling of mouse acute kidney injury reveals conserved cellular responses to injury. Proc Natl Acad Sci U S A 117: 15874–15883, 2020 https://doi.org/10.1073/pnas.2005477117
doi: 10.1073/pnas.2005477117
Ramachandran P, Pellicoro A, Vernon MA, Boulter L, Aucott RL, Ali A, Hartland SN, Snowdon VK, Cappon A, Gordon-Walker TT, Williams MJ, Dunbar DR, Manning JR, van Rooijen N, Fallowfield JA, Forbes SJ, Iredale JP: Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc Natl Acad Sci U S A 109: E3186–E3195, 2012 https://doi.org/10.1073/pnas.1119964109
doi: 10.1073/pnas.1119964109
Janosevic D, Myslinski J, McCarthy TW, Zollman A, Syed F, Xuei X, Gao H, Liu YL, Collins KS, Cheng YH, Winfree S, El-Achkar TM, Maier B, Melo Ferreira R, Eadon MT, Hato T, Dagher PC: The orchestrated cellular and molecular responses of the kidney to endotoxin define a precise sepsis timeline. eLife 10: e62270, 2021 https://doi.org/10.7554/eLife.62270
doi: 10.7554/eLife.62270
Dhillon P, Park J, Hurtado Del Pozo C, Li L, Doke T, Huang S, Zhao J, Kang HM, Shrestra R, Balzer MS, Chatterjee S, Prado P, Han SY, Liu H, Sheng X, Dierickx P, Batmanov K, Romero JP, Prósper F, Li M, Pei L, Kim J, Montserrat N, Suszták K: The nuclear receptor ESRRA protects from kidney disease by coupling metabolism and differentiation. Cell Metab 33: 379–394.e8, 2021 https://doi.org/10.1016/j.cmet.2020.11.011
doi: 10.1016/j.cmet.2020.11.011
Wilson PC, Wu H, Kirita Y, Uchimura K, Ledru N, Rennke HG, Welling PA, Waikar SS, Humphreys BD: The single-cell transcriptomic landscape of early human diabetic nephropathy. Proc Natl Acad Sci U S A 116: 19619–19625, 2019 https://doi.org/10.1073/pnas.1908706116
doi: 10.1073/pnas.1908706116
Calle P, Hotter G: Macrophage phenotype and fibrosis in diabetic nephropathy. Int J Mol Sci 21: 2806, 2020 https://doi.org/10.3390/ijms21082806
doi: 10.3390/ijms21082806
Kuppe C, Ibrahim MM, Kranz J, Zhang X, Ziegler S, Perales-Patón J, Jansen J, Reimer KC, Smith JR, Dobie R, Wilson-Kanamori JR, Halder M, Xu Y, Kabgani N, Kaesler N, Klaus M, Gernhold L, Puelles VG, Huber TB, Boor P, Menzel S, Hoogenboezem RM, Bindels EMJ, Steffens J, Floege J, Schneider RK, Saez-Rodriguez J, Henderson NC, Kramann R: Decoding myofibroblast origins in human kidney fibrosis. Nature 589: 281–286, 2021 https://doi.org/10.1038/s41586-020-2941-1
doi: 10.1038/s41586-020-2941-1
Arazi A, Rao DA, Berthier CC, Davidson A, Liu Y, Hoover PJ, Chicoine A, Eisenhaure TM, Jonsson AH, Li S, Lieb DJ, Zhang F, Slowikowski K, Browne EP, Noma A, Sutherby D, Steelman S, Smilek DE, Tosta P, Apruzzese W, Massarotti E, Dall’Era M, Park M, Kamen DL, Furie RA, Payan-Schober F, Pendergraft WF 3rd, McInnis EA, Buyon JP, Petri MA, Putterman C, Kalunian KC, Woodle ES, Lederer JA, Hildeman DA, Nusbaum C, Raychaudhuri S, Kretzler M, Anolik JH, Brenner MB, Wofsy D, Hacohen N, Diamond B; Accelerating Medicines Partnership in SLE network: The immune cell landscape in kidneys of patients with lupus nephritis [published correction appears in Nat Immunol 20: 1404, 2019]. Nat Immunol 20: 902–914, 2019 https://doi.org/10.1038/s41590-019-0398-x
doi: 10.1038/s41590-019-0398-x