Advances in single-cell sequencing: insights from organ transplantation

Ying Wang; Jian-Ye Wang; Angelika Schnieke; Konrad Fischer

doi:10.1186/s40779-021-00336-1

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Advances in single-cell sequencing: insights from organ transplantation

REVIEW | Updated：2023-02-28

- Advances in single-cell sequencing: insights from organ transplantation
- Military Medical Research Vol. 9, Issue 1, Pages: 86-97(2022)
- Affiliations：
  
  1.Chair of Livestock Biotechnology, School of Life Sciences Weihenstephan, Technical University of Munich, Liesel Beckman Str 1, 85354 Freising, Germany
  2.Department of Surgery, School of Medicine, Technical University of Munich, 81675 Munich, Germany
- Author bio：
  
  * konrad.fischer@wzw.tum.de
- Funds：
- DOI：10.1186/s40779-021-00336-1
  CLC：
- Published：2022-02
- Accepted：
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Wang et al.: Advances in single-cell sequencing: insights from organ transplantation. Mil Med Res, 2021, 8: 45.
DOI：

Wang et al.: Advances in single-cell sequencing: insights from organ transplantation. Mil Med Res, 2021, 8: 45. DOI： 10.1186/s40779-021-00336-1.

摘要

Abstract

Single-cell RNA sequencing (scRNA-seq) is a comprehensive technical tool to analyze intracellular and intercellular interaction data by whole transcriptional profile analysis. Here

we describe the application in biomedical research

focusing on the immune system during organ transplantation and rejection. Unlike conventional transcriptome analysis

this method provides a full map of multiple cell populations in one specific tissue and presents a dynamic and transient unbiased method to explore the progression of allograft dysfunction

starting from the stress response to final graft failure. This promising sequencing technology remarkably improves individualized organ rejection treatment by identifying decisive cellular subgroups and cell-specific interactions.

关键词

Keywords

references

Hao S , Yan KK , Ding L , Qian C , Chi H , Yu J . Network approaches for dissecting the immune system . iScience . 2020 ; 23 ( 8 ): 101354 .

Stubbington MJT , Rozenblatt-Rosen O , Regev A , Teichmann SA . Singlecell transcriptomics to explore the immune system in health and disease . Science . 2017 ; 358 ( 6359 ): 58 - 63 .

Ingulli E . Mechanism of cellular rejection in transplantation . Pediatr Nephrol . 2010 ; 25 ( 1 ): 61 - 74 .

Menon MC , Keung KL , Murphy B , O’connell PJ . The use of genomics and pathway analysis in our understanding and prediction of clinical renal transplant injury . Transplantation . 2016 ; 100 ( 7 ): 1405 - 14 .

Claeys E , Vermeire K . Immunosuppressive drugs in organ transplantation to prevent allograft rejection: mode of action and side effects . J Immunol Sci . 2019 ; 3 ( 4 ): 14 - 21 .

Nankivell BJ , Borrows RJ , Fung CLS , O’connell PJ , Allen RDM , Chapman JR . The natural history of chronic allograft nephropathy . N Engl J Med . 2003 ; 349 ( 24 ): 2326 - 33 .

El-Zoghby ZM , Stegall MD , Lager DJ , Kremers WK , Amer H , Gloor JM , et al . Identifying specific causes of kidney allograft loss . Am J Transplant . 2009 ; 9 ( 3 ): 527 - 35 .

Maguire O , Tario JD Jr , Shanahan TC , Wallace PK , Minderman H . Flow cytometry and solid organ transplantation: a perfect match . Immunol Invest . 2014 ; 43 ( 8 ): 756 - 74 .

Colvin RB . Antibody-mediated renal allograft rejection: diagnosis and pathogenesis . J Am Soc Nephrol . 2007 ; 18 ( 4 ): 1046 - 56 .

Malone AF , Wu H , Humphreys BD . Bringing renal biopsy interpretation into the molecular age with single-cell RNA sequencing . Semin Nephrol . 2018 ; 38 ( 1 ): 31 - 9 .

Sellares J , Reeve J , Loupy A , Mengel M , Sis B , Skene A , et al . Molecular diagnosis of antibody-mediated rejection in human kidney transplants . Am J Transplant . 2013 ; 13 ( 4 ): 971 - 83 .

Halloran PF , Pereira AB , Chang J , Matas A , Picton M , De Freitas D , et al . Microarray diagnosis of antibody-mediated rejection in kidney transplant biopsies: an international prospective study (INTERCOM) . Am J Transplant . 2013 ; 13 ( 11 ): 2865 - 74 .

Thareja G , Yang H , Hayat S , Mueller FB , Lee JR , Lubetzky M , et al . Single nucleotide variant counts computed from RNA sequencing and cellular traffic into human kidney allografts . Am J Transplant . 2018 ; 18 ( 10 ): 2429 - 42 .

Roedder S , Sigdel T , Salomonis N , Hsieh S , Dai H , Bestard O , et al . The kSORT assay to detect renal transplant patients at high risk for acute rejection: results of the multicenter AART study . PLoS Med . 2014 ; 11 ( 11 ): e1001759 .

Higdon LE , Schaffert S , Khatri P , Maltzman JS . Single cell immune profiling in transplantation research . Am J Transplant . 2019 ; 19 ( 5 ): 1278 - 87 .

Roy AL . Transcriptional regulation in the immune system: one cell at a time . Front Immunol . 2019 ; 10 : 1355 .

Giladi A , Amit I . Single-cell genomics: a stepping stone for future immunology discoveries . Cell . 2018 ; 172 ( 1–2 ): 14 - 21 .

Neu KE , Tang Q , Wilson PC , Khan AA . Single-cell genomics: approaches and utility in immunology . Trends Immunol . 2017 ; 38 ( 2 ): 140 - 9 .

Chen HI , Jin Y , Huang Y , Chen Y . Detection of high variability in gene expression from single-cell RNA-seq profiling . BMC Genom . 2016 ; 17 ( Suppl 7 ): 508 .

Clatworthy MR . How to find a resident kidney macrophage: the singlecell sequencing solution . J Am Soc Nephrol . 2019 ; 30 ( 5 ): 715 - 6 .

Malone AF , Humphreys BD . Single-cell transcriptomics and solid organ transplantation . Transplantation . 2019 ; 103 ( 9 ): 1776 - 82 .

Macparland SA , Liu JC , Ma XZ , Innes BT , Bartczak AM , Gage BK , et al . Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations . Nat Commun . 2018 ; 9 ( 1 ): 4383 .

Wang W , Penland L , Gokce O , Croote D , Quake SR . High fidelity hypothermic preservation of primary tissues in organ transplant preservative for single cell transcriptome analysis . BMC Genom . 2018 ; 19 ( 1 ): 140 .

Guillaumet-Adkins A , Rodriguez-Esteban G , Mereu E , Mendez-Lago M , Jaitin DA , Villanueva A , et al . Single-cell transcriptome conservation in cryopreserved cells and tissues . Genome Biol . 2017 ; 18 ( 1 ): 45 .

Codeluppi S , Borm LE , Zeisel A , La Manno G , Van Lunteren JA , Svensson CI , et al . Spatial organization of the somatosensory cortex revealed by osmFISH . Nat Methods . 2018 ; 15 ( 11 ): 932 - 5 .

Ståhl PL , Salmén F , Vickovic S , Lundmark A , Navarro JF , Magnusson J , et al . Visualization and analysis of gene expression in tissue sections by spatial transcriptomics . Science . 2016 ; 353 : 78 - 82 .

Ziegenhain C , Vieth B , Parekh S , Reinius B , Guillaumet-Adkins A , Smets M , et al . Comparative analysis of single-cell RNA sequencing methods . Mol Cell . 2017 ; 65 ( 4 ): 631-43.e4 .

Lafzi A , Moutinho C , Picelli S , Heyn H . Tutorial: guidelines for the experimental design of single-cell RNA sequencing studies . Nat Protoc . 2018 ; 13 ( 12 ): 2742 - 57 .

Munoz-Manchado AB , Bengtsson Gonzales C , Zeisel A , Munguba H , Bekkouche B , Skene NG , et al . Diversity of interneurons in the dorsal striatum revealed by single-cell RNA sequencing and PatchSeq . Cell Rep . 2018 ; 24 ( 8 ): 2179-90.e7 .

Attaf N , Cervera-Marzal I , Dong C , Gil L , Renand A , Spinelli L , et al . FB5P-seq: FACS-based 5-prime end single-cell RNA-seq for integrative analysis of transcriptome and antigen receptor repertoire in B and T cells . Front Immunol . 2020 ; 11 : 216 .

Picelli S , Faridani OR , Björklund ÅK , Winberg G , Sagasser S , Sandberg R . Full-length RNA-seq from single cells using Smart-seq2 . Nat Protoc . 2014 ; 9 ( 1 ): 171 - 81 .

Picelli S , Björklund ÅK , Faridani OR , Sagasser S , Winberg G , Sandberg R . Smart-seq2 for sensitive full-length transcriptome profiling in single cells . Nat Methods . 2013 ; 10 ( 11 ): 1096 - 8 .

Sasagawa Y , Nikaido I , Hayashi T , Danno H , Uno KD , Imai T , et al . Quartz-Seq: a highly reproducible and sensitive single-cell RNA sequencing method, reveals non-genetic gene-expression heterogeneity . Genome Biol . 2013 ; 14 ( 4 ): R31 .

Sasagawa Y , Danno H , Takada H , Ebisawa M , Tanaka K , Hayashi T , et al . Quartz-Seq2: a high-throughput single-cell RNA-sequencing method that effectively uses limited sequence reads . Genome Biol . 2018 ; 19 ( 1 ): 29 .

Klein AM , Mazutis L , Akartuna I , Tallapragada N , Veres A , Li V , et al . Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells . Cell . 2015 ; 161 ( 5 ): 1187 - 201 .

Hashimshony T , Senderovich N , Avital G , Klochendler A , De Leeuw Y , Anavy L , et al . CEL-Seq2: sensitive highly-multiplexed single-cell RNASeq . Genome Biol . 2016 ; 17 : 77 .

Hashimshony T , Wagner F , Sher N , Yanai I . CEL-Seq: Single-cell RNA-Seq by multiplexed linear amplification . Cell Rep . 2012 ; 2 ( 3 ): 666 - 73 .

Macosko EZ , Basu A , Satija R , Nemesh J , Shekhar K , Goldman M , et al . Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets . Cell . 2015 ; 161 ( 5 ): 1202 - 14 .

Chen G , Ning B , Shi T . Single-cell RNA-seq technologies and related computational data analysis . Front Genet . 2019 ; 10 : 317 .

Kolodziejczyk AA , Kim JK , Svensson V , Marioni JC , Teichmann SA . The technology and biology of single-cell RNA sequencing . Mol Cell . 2015 ; 58 ( 4 ): 610 - 20 .

Gupta RK , Kuznicki J . Biological and medical importance of cellular heterogeneity deciphered by single-cell RNA sequencing . Cells . 2020 ; 9 ( 8 ): E1751 .

Zou A , Ramanathan S , Dale RC , Brilot F . Single-cell approaches to investigate B cells and antibodies in autoimmune neurological disorders . Cell Mol Immunol . 2021 ; 18 ( 2 ): 294 - 306 .

Sheng K , Cao W , Niu Y , Deng Q , Zong C . Effective detection of variation in single-cell transcriptomes using MATQ-seq . Nat Methods . 2017 ; 14 ( 3 ): 267 - 70 .

Woodsworth DJ , Castellarin M , Holt RA . Sequence analysis of T-cell repertoires in health and disease . Genome Med . 2013 ; 5 ( 10 ): 98 .

Salomon R , Kaczorowski D , Valdes-Mora F , Nordon RE , Neild A , Farbehi N , et al . Droplet-based single cell RNAseq tools: a practical guide . Lab Chip . 2019 ; 19 ( 10 ): 1706 - 27 .

Ni J , Hu C , Li H , Li X , Fu Q , Czajkowsky DM , et al . Significant improvement in data quality with simplified SCRB-seq . Acta Biochim Biophys Sin (Shanghai) . 2020 ; 52 ( 4 ): 457 - 9 .

Islam S , Kjallquist U , Moliner A , Zajac P , Fan JB , Lonnerberg P , et al . Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq . Genome Res . 2011 ; 21 ( 7 ): 1160 - 7 .

Keren-Shaul H , Kenigsberg E , Jaitin DA , David E , Paul F , Tanay A , et al . MARS-seq2.0: an experimental and analytical pipeline for indexed sorting combined with single-cell RNA sequencing . Nat Protoc . 2019 ; 14 ( 6 ): 1841 - 62 .

Hicks SC , Townes FW , Teng M , Irizarry RA . Missing data and technical variability in single-cell RNA-sequencing experiments . Biostatistics . 2018 ; 19 ( 4 ): 562 - 78 .

Leek JT , Scharpf RB , Bravo HC , Simcha D , Langmead B , Johnson WE , et al . Tackling the widespread and critical impact of batch effects in high-throughput data . Nat Rev Genet . 2010 ; 11 ( 10 ): 733 - 9 .

Risso D , Ngai J , Speed TP , Dudoit S . Normalization of RNA-seq data using factor analysis of control genes or samples . Nat Biotechnol . 2014 ; 32 ( 9 ): 896 - 902 .

Aran D , Looney AP , Liu L , Wu E , Fong V , Hsu A , et al . Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage . Nat Immunol . 2019 ; 20 ( 2 ): 163 - 72 .

Zhang X , Lan Y , Xu J , Quan F , Zhao E , Deng C , et al . Cell Marker: a manually curated resource of cell markers in human and mouse . Nucleic Acids Res . 2019 ; 47 ( D1 ): D721 - 8 .

Liao J , Yu Z , Chen Y , Bao M , Zou C , Zhang H , et al . Single-cell RNA sequencing of human kidney . Sci Data . 2020 ; 7 ( 1 ): 4 .

Kharchenko PV , Silberstein L , Scadden DT . Bayesian approach to single-cell differential expression analysis . Nat Methods . 2014 ; 11 ( 7 ): 740 - 2 .

Ilicic T , Kim JK , Kolodziejczyk AA , Bagger FO , Mccarthy DJ , Marioni JC , et al . Classification of low quality cells from single-cell RNA-seq data . Genome Biol . 2016 ; 17 : 29 .

Liu Y , Hu J , Liu D , Zhou S , Liao J , Liao G , et al . Single-cell analysis reveals immune landscape in kidneys of patients with chronic transplant rejection . Theranostics . 2020 ; 10 ( 19 ): 8851 - 62 .

Prabhakaran S , Azizi E , Carr A , Pe’er D . Dirichlet process mixture model for correcting technical variation in single-cell gene expression data . JMLR Workshop Conf Proc . 2016 ; 48 : 1070 - 9 .

Bacher R , Kendziorski C . Design and computational analysis of singlecell RNA-sequencing experiments . Genome Biol . 2016 ; 17 : 63 .

van der Maaten L , Hinton G . Visualizing data using t-SNE . J Mach Learn Res . 2008 ; 9 : 2579 - 605 .

Levine JH , Simonds EF , Bendall SC , Davis KL , El Amir AD , Tadmor MD , et al . Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis . Cell . 2015 ; 162 ( 1 ): 184 - 97 .

Becht E , Mcinnes L , Healy J , Dutertre CA , Kwok IWH , Ng LG , et al . Dimensionality reduction for visualizing single-cell data using UMAP . Nat Biotechnol . 2018 ; 37 : 38 - 44 .

Xu C , Su Z . Identification of cell types from single-cell tran-scriptomes using a novel clustering method . Bioinformatics . 2015 ; 31 ( 12 ): 1974 - 80 .

Pierson E , Yau C . ZIFA: Dimensionality reduction for zero-inflated singlecell gene expression analysis . Genome Biol . 2015 ; 16 : 241 .

Korsunsky I , Millard N , Fan J , Slowikowski K , Zhang F , Wei K , et al . Fast, sensitive and accurate integration of single-cell data with Harmony . Nat Methods . 2019 ; 16 ( 12 ): 1289 - 96 .

Trapnell C , Cacchiarelli D , Grimsby J , Pokharel P , Li S , Morse M , et al . The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells . Nat Biotechnol . 2014 ; 32 ( 4 ): 381 - 6 .

Qiu X , Hill A , Packer J , Lin D , Ma YA , Trapnell C . Single-cell mRNA quantification and differential analysis with Census . Nat Methods . 2017 ; 14 ( 3 ): 309 - 15 .

Ji Z , Ji H . TSCAN: pseudo-time reconstruction and evaluation in singlecell RNA-seq analysis . Nucleic Acids Res . 2016 ; 44 ( 13 ): e117 .

Setty M , Tadmor MD , Reich-Zeliger S , Angel O , Salame TM , Kathail P , et al . Wishbone identifies bifurcating developmental trajectories from single-cell data . Nat Biotechnol . 2016 ; 34 ( 6 ): 637 - 45 .

Street K , Risso D , Fletcher RB , Das D , Ngai J , Yosef N , et al . Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics . BMC Genom . 2018 ; 19 ( 1 ): 477 .

Haghverdi L , Büttner M , Wolf FA , Buettner F , Theis FJ . Diffusion pseudotime robustly reconstructs lineage branching . Nat Methods . 2016 ; 13 ( 10 ): 845 - 8 .

Bendall SC , Davis KL , Amir EAD , Tadmor MD , Simonds EF , Chen TJ , et al . Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development . Cell . 2014 ; 157 ( 3 ): 714 - 25 .

Saelens W , Cannoodt R , Todorov H , Saeys Y . A comparison of single-cell trajectory inference methods . Nat Biotechnol . 2019 ; 37 ( 5 ): 547 - 54 .

Dangi A , Yu S , Luo X . Emerging approaches and technologies in transplantation: the potential game changers . Cell Mol Immunol . 2019 ; 16 ( 4 ): 334 - 42 .

Noé A , Cargill TN , Nielsen CM , Russell AJC , Barnes E . The application of single-cell RNA sequencing in vaccinology . J Immunol Res . 2020 ; 2020 : 8624963 .

See P , Lum J , Chen J , Ginhoux F . A single-cell sequencing guide for immunologists . Front Immunol . 2018 ; 9 : 2425 .

de Simone M , Rossetti G , Pagani M . Single cell T cell receptor sequencing: techniques and future challenges . Front Immunol . 2018 ; 9 : 1638 .

Zheng P , Tamaresis J , Thangavelu G , Xu L , You X , Blazar BR , et al . Recipient-specific T-cell repertoire reconstitution in the gut following murine hematopoietic cell transplant . Blood Adv . 2020 ; 4 ( 17 ): 4232 - 43 .

Stubbington MJT , Lönnberg T , Proserpio V , Clare S , Speak AO , Dougan G , et al . T cell fate and clonality inference from single-cell transcriptomes . Nat Methods . 2016 ; 13 ( 4 ): 329 - 32 .

Morris H , Dewolf S , Robins H , Sprangers B , Locascio SA , Shonts BA , et al . Tracking donor-reactive T cells: evidence for clonal deletion in tolerant kidney transplant patients . Sci Transl Med . 2015 ; 7 ( 272 ): 272ra10 .

DeWolf S , Sykes M . Alloimmune T cells in transplantation . J Clin Invest . 2017 ; 127 ( 7 ): 2473 - 81 .

Alachkar H , Mutonga M , Kato T , Kalluri S , Kakuta Y , Uemura M , et al . Quantitative characterization of T-cell repertoire and biomarkers in kidney transplant rejection . BMC Nephrol . 2016 ; 17 ( 1 ): 181 .

Yew PY , Alachkar H , Yamaguchi R , Kiyotani K , Fang H , Yap KL , et al . Quantitative characterization of T-cell repertoire in allogeneic hematopoietic stem cell transplant recipients . Bone Marrow Transplant . 2015 ; 50 ( 9 ): 1227 - 34 .

Halloran PF , Pereira AB , Chang J , Matas A , Picton M , De Freitas D , et al . Potential impact of microarray diagnosis of T cell-mediated rejection in kidney transplants: the INTERCOM study . Am J Transplant . 2013 ; 13 ( 9 ): 2352 - 63 .

Stewart BJ , Ferdinand JR , Clatworthy MR . Using single-cell technologies to map the human immune system: implications for nephrology . Nat Rev Nephrol . 2020 ; 16 ( 2 ): 112 - 28 .

Reinders ME , Rabelink TJ , Briscoe DM . Angiogenesis and endothelial cell repair in renal disease and allograft rejection . J Am Soc Nephrol . 2006 ; 17 ( 4 ): 932 - 42 .

Sis B , Jhangri GS , Bunnag S , Allanach K , Kaplan B , Halloran PF . Endothelial gene expression in kidney transplants with alloantibody indicates antibody-mediated damage despite lack of C4d staining . Am J Transplant . 2009 ; 9 ( 10 ): 2312 - 23 .

Malone AF , Wu H , Fronick C , Fulton R , Gaut JP , Humphreys BD . Harnessing expressed single nucleotide variation and single cell rna sequencing to define immune cell chimerism in the rejecting kidney transplant . J Am Soc Nephrol . 2020 ; 31 ( 9 ): 1977 - 86 .

Bellan C , Amato T , Carmellini M , Onorati M , D’amuri A , Leoncini L , et al . Analysis of the IgVH genes in T cell-mediated and antibody-mediated rejection of the kidney graft . J Clin Pathol . 2011 ; 64 ( 1 ): 47 - 53 .

Dangi A , Natesh NR , Husain I , Ji Z , Barisoni L , Kwun J , et al . Single cell transcriptomics of mouse kidney transplants reveals a myeloid cell pathway for transplant rejection . JCI Insight . 2020 ; 5 ( 20 ): e141321 .

Varma E , Luo X , Muthukumar T . Dissecting the human kidney allograft transcriptome: single-cell RNA sequencing . Curr Opin Organ Transplant . 2021 ; 26 ( 1 ): 43 - 51 .

Lei H , Reinke P , Volk HD , Lv Y , Wu R . Mechanisms of immune tolerance in liver transplantation-crosstalk between alloreactive T cells and liver cells with therapeutic prospects . Front Immunol . 2019 ; 10 : 2667 .

Dai H , Zheng Y , Thomson AW , Rogers NM . Transplant tolerance induction: insights from the liver . Front Immunol . 2020 ; 11 : 1044 .

Feng S , Bucuvalas J . Tolerance after liver transplantation: Where are we? Liver Transpl . 2017 ; 23 ( 12 ): 1601 - 14 .

Thomson AW , Vionnet J , Sanchez-Fueyo A . Understanding, predicting and achieving liver transplant tolerance: from bench to bedside . Nat Rev Gastroenterol Hepatol . 2020 ; 17 ( 12 ): 719 - 39 .

Choudhary NS , Saigal S , Bansal RK , Saraf N , Gautam D , Soin AS . Acute and chronic rejection after liver transplantation: what a clinician needs to know . J Clin Exp Hepatol . 2017 ; 7 ( 4 ): 358 - 66 .

Feng S , Bucuvalas JC , Demetris AJ , Burrell BE , Spain KM , Kanaparthi S , et al . Evidence of chronic allograft injury in liver biopsies from long-term pediatric recipients of liver transplants . Gastroenterology . 2018 ; 155 ( 6 ): 1838-51.e7 .

Misharin AV , Morales-Nebreda L , Reyfman PA , Cuda CM , Walter JM , Mcquattie-Pimentel AC , et al . Monocyte-derived alveolar macrophages drive lung fibrosis and persist in the lung over the life span . J Exp Med . 2017 ; 214 ( 8 ): 2387 - 404 .

Mccubbrey AL , Barthel L , Mohning MP , Redente EF , Mould KJ , Thomas SM , et al . Deletion of c-FLIP from CD11bhi macrophages prevents development of bleomycin-induced lung fibrosis . Am J Respir Cell Mol Biol . 2018 ; 58 ( 1 ): 66 - 78 .

Reyfman PA , Walter JM , Joshi N , Anekalla KR , Mcquattie-Pimentel AC , Chiu S , et al . Single-cell transcriptomic analysis of human lung provides insights into the pathobiology of pulmonary fibrosis . Am J Respir Crit Care Med . 2018 ; 199 ( 12 ): 1517 - 36 .

Mould KJ , Moore CM , Mcmanus SA , Mccubbrey AL , Mcclendon JD , Griesmer CL , et al . Airspace macrophages and monocytes exist in transcriptionally distinct subsets in healthy adults . Am J Respir Crit Care Med . 2021 ; 203 ( 8 ): 946 - 56 .

Snyder ME , Finlayson MO , Connors TJ , Dogra P , Senda T , Bush E , et al . Generation and persistence of human tissue-resident memory T cells in lung transplantation . Sci Immunol . 2019 ; 4 ( 33 ): eaav5581 .

Dong F , Hao S , Zhang S , Zhu C , Cheng H , Yang Z , et al . Differentiation of transplanted haematopoietic stem cells tracked by single-cell transcriptomic analysis . Nat Cell Biol . 2020 ; 22 ( 6 ): 630 - 9 .

Fujisaki J , Wu J , Carlson AL , Silberstein L , Putheti P , Larocca R , et al . In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche . Nature . 2011 ; 474 ( 7350 ): 216 - 9 .

Beilhack A , Schulz S , Baker J , Beilhack GF , Wieland CB , Herman EI , et al . In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets . Blood . 2005 ; 106 ( 3 ): 1113 - 22 .

DiRienzo CG , Murphy GF , Jones SC , Korngold R , Friedman TM . T-cell receptor Valpha spectratype analysis of a CD4-mediated T-cell response against minor histocompatibility antigens involved in severe graft versus-host disease . Biol Blood Marrow Transplant . 2006 ; 12 ( 8 ): 818 - 27 .

Divito SJ , Aasebo AT , Matos TR , Hsieh PC , Collin M , Elco CP , et al . Peripheral host T cells survive hematopoietic stem cell transplantation and promote graft-versus-host disease . J Clin Invest . 2020 ; 130 ( 9 ): 4624 - 36 .

Habib N , Avraham-Davidi I , Basu A , Burks T , Shekhar K , Hofree M , et al . Massively parallel single-nucleus RNA-seq with DroNc-seq . Nat Methods . 2017 ; 14 ( 10 ): 955 - 8 .

Babel N , Stervbo U , Reinke P , Volk HD . The identity card of T cells-clinical utility of T-cell receptor repertoire analysis in transplantation . Transplantation . 2019 ; 103 ( 8 ): 1544 - 55 .

Chen H , Ye F , Guo G . Revolutionizing immunology with single-cell RNA sequencing . Cell Mol Immunol . 2019 ; 16 ( 3 ): 242 - 9 .

Denisenko E , Guo BB , Jones M , Hou R , De Kock L , Lassmann T , et al . Systematic assessment of tissue dissociation and storage biases in single-cell and single-nucleus RNA-seq workflows . Genome Biol . 2020 ; 21 ( 1 ): 130 .

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 . 2019 ; 30 ( 1 ): 23 - 32 .

Slyper M , Porter CBM , Ashenberg O , Waldman J , Drokhlyansky E , Wakiro I , et al . A single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors . Nat Med . 2020 ; 26 ( 5 ): 792 - 802 .

Roy AL , Conroy RS . Toward mapping the human body at a cellular resolution . Mol Biol Cell . 2018 ; 29 ( 15 ): 1779 - 85 .

Vegh P , Haniffa M . The impact of single-cell RNA sequencing on understanding the functional organization of the immune system . Brief Funct Genom . 2018 ; 17 ( 4 ): 265 - 72 .

Zeng T , Dai H . Single-cell rna sequencing-based computational analysis to describe disease heterogeneity . Front Genet . 2019 ; 10 : 629 .

Schlitzer A , Sivakamasundari V , Chen J , Sumatoh HR , Schreuder J , Lum J , et al . Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow . Nat Immunol . 2015 ; 16 ( 7 ): 718 - 28 .

Pang WW , Price EA , Sahoo D , Beerman I , Maloney WJ , Rossi DJ , et al . Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age . Proc Natl Acad Sci USA . 2011 ; 108 ( 50 ): 20012 - 7 .

Jaitin DA , Kenigsberg E , Keren-Shaul H , Elefant N , Paul F , Zaretsky I , et al . Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types . Science . 2014 ; 343 ( 6172 ): 776 - 9 .

Miyamoto DT , Zheng Y , Wittner BS , Lee RJ , Zhu H , Broderick KT , et al . RNA-Seq of single prostate CTCs implicates noncanonical Wnt signaling in antiandrogen resistance . Science . 2015 ; 349 ( 6254 ): 1351 - 6 .

Keren-Shaul H , Spinrad A , Weiner A , Matcovitch-Natan O , Dvir-Szternfeld R , Ulland TK , et al . A unique microglia type associated with restricting development of Alzheimer’s disease . Cell . 2017 ; 169 ( 7 ): 1276-90.e17 .

Myklebust JH , Brody J , Kohrt HE , Kolstad A , Czerwinski DK , Walchli S , et al . Distinct patterns of B-cell receptor signaling in non-Hodgkin lymphomas identified by single-cell profiling . Blood . 2017 ; 129 ( 6 ): 759 - 70 .

Young RM , Staudt LM . Targeting pathological B cell receptor signalling in lymphoid malignancies . Nat Rev Drug Discov . 2013 ; 12 ( 3 ): 229 - 43 .

Zheng GX , Terry JM , Belgrader P , Ryvkin P , Bent ZW , Wilson R , et al . Massively parallel digital transcriptional profiling of single cells . Nat Commun . 2017 ; 8 : 14049 .

Bjorklund AK , Forkel M , Picelli S , Konya V , Theorell J , Friberg D , et al . The heterogeneity of human CD127(+) innate lymphoid cells revealed by single-cell RNA sequencing . Nat Immunol . 2016 ; 17 ( 4 ): 451 - 60 .

Paul F , Arkin Y , Giladi A , Jaitin DA , Kenigsberg E , Keren-Shaul H , et al . Transcriptional heterogeneity and lineage commitment in myeloid progenitors . Cell . 2016 ; 164 ( 1–2 ): 325 .

Ye Y , Song H , Zhang J , Shi S . Understanding the biology and pathogenesis of the kidney by single-cell transcriptomic analysis . Kidney Dis (Basel) . 2018 ; 4 ( 4 ): 214 - 25 .

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