Analyze Diet
Frontiers in immunology2022; 13; 929922; doi: 10.3389/fimmu.2022.929922

Single-cell gene expression analysis of cryopreserved equine bronchoalveolar cells.

Abstract: The transcriptomic profile of a cell population can now be studied at the cellular level using single-cell mRNA sequencing (scRNA-seq). This novel technique provides the unprecedented opportunity to explore the cellular composition of the bronchoalveolar lavage fluid (BALF) of the horse, a species for which cell type markers are poorly described. Here, scRNA-seq technology was applied to cryopreserved equine BALF cells. Analysis of 4,631 cells isolated from three asthmatic horses in remission identified 16 cell clusters belonging to six major cell types: monocytes/macrophages, T cells, B/plasma cells, dendritic cells, neutrophils and mast cells. Higher resolution analysis of the constituents of the major immune cell populations allowed deep annotation of monocytes/macrophages, T cells and B/plasma cells. A significantly higher lymphocyte/macrophage ratio was detected with scRNA-seq compared to conventional cytological differential cell count. For the first time in horses, we detected a transcriptomic signature consistent with monocyte-lymphocyte complexes. Our findings indicate that scRNA-seq technology is applicable to cryopreserved equine BALF cells, allowing the identification of its major (cytologically differentiated) populations as well as previously unexplored T cell and macrophage subpopulations. Single-cell gene expression analysis has the potential to facilitate understanding of the immunological mechanisms at play in respiratory disorders of the horse, such as equine asthma.
Publication Date: 2022-08-29 PubMed ID: 36105804PubMed Central: PMC9467276DOI: 10.3389/fimmu.2022.929922Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study explores the use of single-cell mRNA sequencing (scRNA-seq) to analyze the cellular composition of fluid found in horse lungs, particularly in those with asthma. It showed that this technique can identify the major cell types as well as previously unexplored cell subgroups, which can further our understanding of the immunological functionalities in equine respiratory ailments.

Methodology

  • The researchers employed scRNA-seq technology to conduct the gene-expression analysis of cryopreserved bronchoalveolar lavage fluid (BALF) cells of horses. BALF is the liquid obtained from a washout of the bronchoalveolar space. BALF cells being analyzed for this study were retrieved from three horses with asthma in remission.

Findings

  • A total of 4,631 cells were analyzed through this process, and the results identified 16 distinct clusters of cells that belonged to six major cell types. These cell types include monocytes/macrophages, T cells, B/plasma cells, dendritic cells, neutrophils, and mast cells.
  • Deeper analysis of the major immune cell groups allowed researchers to deeply annotate or describe monocytes/macrophages, T cells, and B/plasma cells, enabling a more detailed understanding of these cell types.
  • The researchers found that the lymphocyte/macrophage ratio detected with scRNA-seq was significantly higher than that detected using conventional cytological differential cell count methods.

Novel Discoveries

  • For the first time in equine studies, the researchers identified a transcriptomic signature consistent with monocyte-lymphocyte complexes, indicating new areas for future research.

Implications

  • This study’s results demonstrate that scRNA-seq technology can be utilized with cryopreserved equine BALF cells and can enhance the identification of its major populations and previously unexplored subpopulations of cells, such as T cells and macrophages.
  • This use of single-cell gene expression analysis has the potential to advance our comprehension of the immunological mechanisms driving respiratory disorders in horses, notably equine asthma, enhancing diagnostic and treatment strategies.

Cite This Article

APA
Sage SE, Nicholson P, Peters LM, Leeb T, Jagannathan V, Gerber V. (2022). Single-cell gene expression analysis of cryopreserved equine bronchoalveolar cells. Front Immunol, 13, 929922. https://doi.org/10.3389/fimmu.2022.929922

Publication

ISSN: 1664-3224
NlmUniqueID: 101560960
Country: Switzerland
Language: English
Volume: 13
Pages: 929922
PII: 929922

Researcher Affiliations

Sage, Sophie E
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Nicholson, Pamela
  • Next Generation Sequencing Platform, University of Bern, Bern, Switzerland.
Peters, Laureen M
  • Clinical Diagnostic Laboratory, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Leeb, Tosso
  • Next Generation Sequencing Platform, University of Bern, Bern, Switzerland.
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Jagannathan, Vidhya
  • Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Gerber, Vinzenz
  • Swiss Institute of Equine Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, Bern, Switzerland.

MeSH Terms

  • Animals
  • Asthma
  • Bronchoalveolar Lavage Fluid
  • Horse Diseases
  • Horses
  • Single-Cell Analysis
  • Transcriptome

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 94 references
  1. Nayak R, Hasija Y. A hitchhiker's guide to single-cell transcriptomics and data analysis pipelines.. Genomics 2021 Mar;113(2):606-619.
    doi: 10.1016/j.ygeno.2021.01.007pubmed: 33485955google scholar: lookup
  2. Chua RL, Lukassen S, Trump S, Hennig BP, Wendisch D, Pott F, Debnath O, Thürmann L, Kurth F, Völker MT, Kazmierski J, Timmermann B, Twardziok S, Schneider S, Machleidt F, Müller-Redetzky H, Maier M, Krannich A, Schmidt S, Balzer F, Liebig J, Loske J, Suttorp N, Eils J, Ishaque N, Liebert UG, von Kalle C, Hocke A, Witzenrath M, Goffinet C, Drosten C, Laudi S, Lehmann I, Conrad C, Sander LE, Eils R. COVID-19 severity correlates with airway epithelium-immune cell interactions identified by single-cell analysis.. Nat Biotechnol 2020 Aug;38(8):970-979.
    doi: 10.1038/s41587-020-0602-4pubmed: 32591762google scholar: lookup
  3. He J, Cai S, Feng H, Cai B, Lin L, Mai Y, Fan Y, Zhu A, Huang H, Shi J, Li D, Wei Y, Li Y, Zhao Y, Pan Y, Liu H, Mo X, He X, Cao S, Hu F, Zhao J, Wang J, Zhong N, Chen X, Deng X, Chen J. Single-cell analysis reveals bronchoalveolar epithelial dysfunction in COVID-19 patients.. Protein Cell 2020 Sep;11(9):680-687.
    doi: 10.1007/s13238-020-00752-4pmc: PMC7363016pubmed: 32671793google scholar: lookup
  4. Liao M, Liu Y, Yuan J, Wen Y, Xu G, Zhao J, Cheng L, Li J, Wang X, Wang F, Liu L, Amit I, Zhang S, Zhang Z. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19.. Nat Med 2020 Jun;26(6):842-844.
    doi: 10.1038/s41591-020-0901-9pubmed: 32398875google scholar: lookup
  5. Couetil LL, Thompson CA. Airway Diagnostics: Bronchoalveolar Lavage, Tracheal Wash, and Pleural Fluid.. Vet Clin North Am Equine Pract 2020 Apr;36(1):87-103.
    doi: 10.1016/j.cveq.2019.12.006pubmed: 32145836google scholar: lookup
  6. Tomlinson JE, Wagner B, Felippe MJB, Van de Walle GR. Multispectral fluorescence-activated cell sorting of B and T cell subpopulations from equine peripheral blood.. Vet Immunol Immunopathol 2018 May;199:22-31.
    doi: 10.1016/j.vetimm.2018.03.010pubmed: 29678226google scholar: lookup
  7. Davis EG, Wilkerson MJ, Rush BR. Flow cytometry: clinical applications in equine medicine.. J Vet Intern Med 2002 Jul-Aug;16(4):404-10.
  8. Vargas A, Boivin R, Cano P, Murcia Y, Bazin I, Lavoie JP. Neutrophil extracellular traps are downregulated by glucocorticosteroids in lungs in an equine model of asthma.. Respir Res 2017 Dec 12;18(1):207.
    doi: 10.1186/s12931-017-0689-4pmc: PMC5727947pubmed: 29233147google scholar: lookup
  9. Lavoie JP, Cesarini C, Lavoie-Lamoureux A, Moran K, Lutz S, Picandet V, Jean D, Marcoux M. Bronchoalveolar lavage fluid cytology and cytokine messenger ribonucleic Acid expression of racehorses with exercise intolerance and lower airway inflammation.. J Vet Intern Med 2011 Mar-Apr;25(2):322-9.
  10. Hughes KJ, Nicolson L, Da Costa N, Franklin SH, Allen KJ, Dunham SP. Evaluation of cytokine mRNA expression in bronchoalveolar lavage cells from horses with inflammatory airway disease.. Vet Immunol Immunopathol 2011 Mar 15;140(1-2):82-9.
    doi: 10.1016/j.vetimm.2010.11.018pubmed: 21194756google scholar: lookup
  11. Beekman L, Tohver T, Léguillette R. Comparison of cytokine mRNA expression in the bronchoalveolar lavage fluid of horses with inflammatory airway disease and bronchoalveolar lavage mastocytosis or neutrophilia using REST software analysis.. J Vet Intern Med 2012 Jan-Feb;26(1):153-61.
  12. Couëtil LL, Cardwell JM, Gerber V, Lavoie JP, Léguillette R, Richard EA. Inflammatory Airway Disease of Horses--Revised Consensus Statement.. J Vet Intern Med 2016 Mar-Apr;30(2):503-15.
    doi: 10.1111/jvim.13824pmc: PMC4913592pubmed: 26806374google scholar: lookup
  13. Mould KJ, Jackson ND, Henson PM, Seibold M, Janssen WJ. Single cell RNA sequencing identifies unique inflammatory airspace macrophage subsets.. JCI Insight 2019 Mar 7;4(5).
    doi: 10.1172/jci.insight.126556pmc: PMC6483508pubmed: 30721157google scholar: lookup
  14. Lee JS, Koh JY, Yi K, Kim YI, Park SJ, Kim EH, Kim SM, Park SH, Ju YS, Choi YK, Park SH. Single-cell transcriptome of bronchoalveolar lavage fluid reveals sequential change of macrophages during SARS-CoV-2 infection in ferrets.. Nat Commun 2021 Jul 27;12(1):4567.
    doi: 10.1038/s41467-021-24807-0pmc: PMC8316405pubmed: 34315893google scholar: lookup
  15. Fastrès A, Pirottin D, Fievez L, Marichal T, Desmet CJ, Bureau F, Clercx C. Characterization of the Bronchoalveolar Lavage Fluid by Single Cell Gene Expression Analysis in Healthy Dogs: A Promising Technique.. Front Immunol 2020;11:1707.
    doi: 10.3389/fimmu.2020.01707pmc: PMC7406785pubmed: 32849601google scholar: lookup
  16. Lavoie JP, Bullone M, Rodrigues N, Germim P, Albrecht B, von Salis-Soglio M. Effect of different doses of inhaled ciclesonide on lung function, clinical signs related to airflow limitation and serum cortisol levels in horses with experimentally induced mild to severe airway obstruction.. Equine Vet J 2019 Nov;51(6):779-786.
    doi: 10.1111/evj.13093pmc: PMC7379559pubmed: 30854685google scholar: lookup
  17. Stuart T, Butler A, Hoffman P, Hafemeister C, Papalexi E, Mauck WM 3rd, Hao Y, Stoeckius M, Smibert P, Satija R. Comprehensive Integration of Single-Cell Data.. Cell 2019 Jun 13;177(7):1888-1902.e21.
    doi: 10.1016/j.cell.2019.05.031pmc: PMC6687398pubmed: 31178118google scholar: lookup
  18. Luecken MD, Theis FJ. Current best practices in single-cell RNA-seq analysis: a tutorial.. Mol Syst Biol 2019 Jun 19;15(6):e8746.
    doi: 10.15252/msb.20188746pmc: PMC6582955pubmed: 31217225google scholar: lookup
  19. Ramseyer A, Gaillard C, Burger D, Straub R, Jost U, Boog C, Marti E, Gerber V. Effects of genetic and environmental factors on chronic lower airway disease in horses.. J Vet Intern Med 2007 Jan-Feb;21(1):149-56.
  20. Laumen E, Doherr MG, Gerber V. Relationship of horse owner assessed respiratory signs index to characteristics of recurrent airway obstruction in two Warmblood families.. Equine Vet J 2010 Mar;42(2):142-8.
    doi: 10.2746/042516409X479586pubmed: 20156250google scholar: lookup
  21. Couetil L, Cardwell JM, Leguillette R, Mazan M, Richard E, Bienzle D, Bullone M, Gerber V, Ivester K, Lavoie JP, Martin J, Moran G, Niedźwiedź A, Pusterla N, Swiderski C. Equine Asthma: Current Understanding and Future Directions.. Front Vet Sci 2020;7:450.
    doi: 10.3389/fvets.2020.00450pmc: PMC7438831pubmed: 32903600google scholar: lookup
  22. Moyo NA, Marchi E, Steinbach F. Differentiation and activation of equine monocyte-derived dendritic cells are not correlated with CD206 or CD83 expression.. Immunology 2013 Aug;139(4):472-83.
    doi: 10.1111/imm.12094pmc: PMC3719064pubmed: 23461413google scholar: lookup
  23. Worah K, Mathan TSM, Vu Manh TP, Keerthikumar S, Schreibelt G, Tel J, Duiveman-de Boer T, Sköld AE, van Spriel AB, de Vries IJM, Huynen MA, Wessels HJ, Gloerich J, Dalod M, Lasonder E, Figdor CG, Buschow SI. Proteomics of Human Dendritic Cell Subsets Reveals Subset-Specific Surface Markers and Differential Inflammasome Function.. Cell Rep 2016 Sep 13;16(11):2953-2966.
  24. Ogawa T, Shichino S, Ueha S, Ogawa S, Matsushima K. Complement protein C1q activates lung fibroblasts and exacerbates silica-induced pulmonary fibrosis in mice.. Biochem Biophys Res Commun 2022 May 7;603:88-93.
    doi: 10.1016/j.bbrc.2022.02.090pubmed: 35278885google scholar: lookup
  25. Morse C, Tabib T, Sembrat J, Buschur KL, Bittar HT, Valenzi E, Jiang Y, Kass DJ, Gibson K, Chen W, Mora A, Benos PV, Rojas M, Lafyatis R. Proliferating SPP1/MERTK-expressing macrophages in idiopathic pulmonary fibrosis.. Eur Respir J 2019 Aug;54(2).
    doi: 10.1183/13993003.02441-2018pmc: PMC8025672pubmed: 31221805google scholar: lookup
  26. Chun KR, Bae EM, Kim JK, Suk K, Lee WH. Suppression of the lipopolysaccharide-induced expression of MARCKS-related protein (MRP) affects transmigration in activated RAW264.7 cells.. Cell Immunol 2009;256(1-2):92-8.
    doi: 10.1016/j.cellimm.2009.01.011pubmed: 19246034google scholar: lookup
  27. Shimizu Y, Dobashi K. CC-chemokine CCL15 expression and possible implications for the pathogenesis of IgE-related severe asthma.. Mediators Inflamm 2012;2012:475253.
    doi: 10.1155/2012/475253pmc: PMC3508751pubmed: 23258953google scholar: lookup
  28. Hollingsworth JW, Li Z, Brass DM, Garantziotis S, Timberlake SH, Kim A, Hossain I, Savani RC, Schwartz DA. CD44 regulates macrophage recruitment to the lung in lipopolysaccharide-induced airway disease.. Am J Respir Cell Mol Biol 2007 Aug;37(2):248-53.
    doi: 10.1165/rcmb.2006-0363OCpmc: PMC1976546pubmed: 17446529google scholar: lookup
  29. Wei J, Marisetty A, Schrand B, Gabrusiewicz K, Hashimoto Y, Ott M, Grami Z, Kong LY, Ling X, Caruso H, Zhou S, Wang YA, Fuller GN, Huse J, Gilboa E, Kang N, Huang X, Verhaak R, Li S, Heimberger AB. Osteopontin mediates glioblastoma-associated macrophage infiltration and is a potential therapeutic target.. J Clin Invest 2019 Jan 2;129(1):137-149.
    doi: 10.1172/JCI121266pmc: PMC6307970pubmed: 30307407google scholar: lookup
  30. Evren E, Ringqvist E, Tripathi KP, Sleiers N, Rives IC, Alisjahbana A, Gao Y, Sarhan D, Halle T, Sorini C, Lepzien R, Marquardt N, Michaëlsson J, Smed-Sörensen A, Botling J, Karlsson MCI, Villablanca EJ, Willinger T. Distinct developmental pathways from blood monocytes generate human lung macrophage diversity.. Immunity 2021 Feb 9;54(2):259-275.e7.
    doi: 10.1016/j.immuni.2020.12.003pubmed: 33382972google scholar: lookup
  31. Schyns J, Bai Q, Ruscitti C, Radermecker C, De Schepper S, Chakarov S, Farnir F, Pirottin D, Ginhoux F, Boeckxstaens G, Bureau F, Marichal T. Non-classical tissue monocytes and two functionally distinct populations of interstitial macrophages populate the mouse lung.. Nat Commun 2019 Sep 3;10(1):3964.
    doi: 10.1038/s41467-019-11843-0pmc: PMC6722135pubmed: 31481690google scholar: lookup
  32. Kim C, Jin J, Weyand CM, Goronzy JJ. The Transcription Factor TCF1 in T Cell Differentiation and Aging.. Int J Mol Sci 2020 Sep 5;21(18).
    doi: 10.3390/ijms21186497pmc: PMC7554785pubmed: 32899486google scholar: lookup
  33. Szabo PA, Levitin HM, Miron M, Snyder ME, Senda T, Yuan J, Cheng YL, Bush EC, Dogra P, Thapa P, Farber DL, Sims PA. Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease.. Nat Commun 2019 Oct 17;10(1):4706.
    doi: 10.1038/s41467-019-12464-3pmc: PMC6797728pubmed: 31624246google scholar: lookup
  34. Sanchez CG, Teixeira FK, Czech B, Preall JB, Zamparini AL, Seifert JR, Malone CD, Hannon GJ, Lehmann R. Regulation of Ribosome Biogenesis and Protein Synthesis Controls Germline Stem Cell Differentiation.. Cell Stem Cell 2016 Feb 4;18(2):276-90.
    doi: 10.1016/j.stem.2015.11.004pmc: PMC4744108pubmed: 26669894google scholar: lookup
  35. Zhang Y, Reynolds JM, Chang SH, Martin-Orozco N, Chung Y, Nurieva RI, Dong C. MKP-1 is necessary for T cell activation and function.. J Biol Chem 2009 Nov 6;284(45):30815-24.
    doi: 10.1074/jbc.M109.052472pmc: PMC2781480pubmed: 19748894google scholar: lookup
  36. Gavins FN, Hickey MJ. Annexin A1 and the regulation of innate and adaptive immunity.. Front Immunol 2012;3:354.
    doi: 10.3389/fimmu.2012.00354pmc: PMC3515881pubmed: 23230437google scholar: lookup
  37. Truong KL, Schlickeiser S, Vogt K, Boës D, Stanko K, Appelt C, Streitz M, Grütz G, Stobutzki N, Meisel C, Iwert C, Tomiuk S, Polansky JK, Pascher A, Babel N, Stervbo U, Sauer I, Gerlach U, Sawitzki B. Killer-like receptors and GPR56 progressive expression defines cytokine production of human CD4(+) memory T cells.. Nat Commun 2019 May 22;10(1):2263.
    doi: 10.1038/s41467-019-10018-1pmc: PMC6531457pubmed: 31118448google scholar: lookup
  38. Bai Y, Hu M, Chen Z, Wei J, Du H. Single-Cell Transcriptome Analysis Reveals RGS1 as a New Marker and Promoting Factor for T-Cell Exhaustion in Multiple Cancers.. Front Immunol 2021;12:767070.
    doi: 10.3389/fimmu.2021.767070pmc: PMC8692249pubmed: 34956194google scholar: lookup
  39. Ohkura N, Sakaguchi S. Transcriptional and epigenetic basis of Treg cell development and function: its genetic anomalies or variations in autoimmune diseases.. Cell Res 2020 Jun;30(6):465-474.
    doi: 10.1038/s41422-020-0324-7pmc: PMC7264322pubmed: 32367041google scholar: lookup
  40. Schumann K, Raju SS, Lauber M, Kolb S, Shifrut E, Cortez JT, Skartsis N, Nguyen VQ, Woo JM, Roth TL, Yu R, Nguyen MLT, Simeonov DR, Nguyen DN, Targ S, Gate RE, Tang Q, Bluestone JA, Spitzer MH, Ye CJ, Marson A. Functional CRISPR dissection of gene networks controlling human regulatory T cell identity.. Nat Immunol 2020 Nov;21(11):1456-1466.
    doi: 10.1038/s41590-020-0784-4pmc: PMC7577958pubmed: 32989329google scholar: lookup
  41. Zhang H, Madi A, Yosef N, Chihara N, Awasthi A, Pot C, Lambden C, Srivastava A, Burkett PR, Nyman J, Christian E, Etminan Y, Lee A, Stroh H, Xia J, Karwacz K, Thakore PI, Acharya N, Schnell A, Wang C, Apetoh L, Rozenblatt-Rosen O, Anderson AC, Regev A, Kuchroo VK. An IL-27-Driven Transcriptional Network Identifies Regulators of IL-10 Expression across T Helper Cell Subsets.. Cell Rep 2020 Nov 24;33(8):108433.
  42. Wheaton JD, Yeh CH, Ciofani M. Cutting Edge: c-Maf Is Required for Regulatory T Cells To Adopt RORγt(+) and Follicular Phenotypes.. J Immunol 2017 Dec 15;199(12):3931-3936.
    doi: 10.4049/jimmunol.1701134pmc: PMC5728164pubmed: 29127150google scholar: lookup
  43. Ren J, Han L, Tang J, Liu Y, Deng X, Liu Q, Hao P, Feng X, Li B, Hu H, Wang H. Foxp1 is critical for the maintenance of regulatory T-cell homeostasis and suppressive function.. PLoS Biol 2019 May;17(5):e3000270.
  44. Remedios KA, Zirak B, Sandoval PM, Lowe MM, Boda D, Henley E, Bhattrai S, Scharschmidt TC, Liao W, Naik HB, Rosenblum MD. The TNFRSF members CD27 and OX40 coordinately limit T(H)17 differentiation in regulatory T cells.. Sci Immunol 2018 Dec 21;3(30).
    doi: 10.1126/sciimmunol.aa⁂pubmed: 30578350google scholar: lookup
  45. van Aalderen MC, van den Biggelaar M, Remmerswaal EBM, van Alphen FPJ, Meijer AB, Ten Berge IJM, van Lier RAW. Label-free Analysis of CD8(+) T Cell Subset Proteomes Supports a Progressive Differentiation Model of Human-Virus-Specific T Cells.. Cell Rep 2017 May 2;19(5):1068-1079.
    doi: 10.1016/j.celrep.2017.04.014pubmed: 28467900google scholar: lookup
  46. Slade CD, Reagin KL, Lakshmanan HG, Klonowski KD, Watford WT. Placenta-specific 8 limits IFNγ production by CD4 T cells in vitro and promotes establishment of influenza-specific CD8 T cells in vivo.. PLoS One 2020;15(7):e0235706.
  47. Pfaender S, Mar KB, Michailidis E, Kratzel A, Boys IN, V'kovski P, Fan W, Kelly JN, Hirt D, Ebert N, Stalder H, Kleine-Weber H, Hoffmann M, Hoffmann HH, Saeed M, Dijkman R, Steinmann E, Wight-Carter M, McDougal MB, Hanners NW, Pöhlmann S, Gallagher T, Todt D, Zimmer G, Rice CM, Schoggins JW, Thiel V. LY6E impairs coronavirus fusion and confers immune control of viral disease.. Nat Microbiol 2020 Nov;5(11):1330-1339.
    doi: 10.1038/s41564-020-0769-ypmc: PMC7916999pubmed: 32704094google scholar: lookup
  48. Eberlein J, Davenport B, Nguyen TT, Victorino F, Jhun K, van der Heide V, Kuleshov M, Ma'ayan A, Kedl R, Homann D. Chemokine Signatures of Pathogen-Specific T Cells I: Effector T Cells.. J Immunol 2020 Oct 15;205(8):2169-2187.
    doi: 10.4049/jimmunol.2000253pmc: PMC7541659pubmed: 32948687google scholar: lookup
  49. Athanasiadis EI, Botthof JG, Andres H, Ferreira L, Lio P, Cvejic A. Single-cell RNA-sequencing uncovers transcriptional states and fate decisions in haematopoiesis.. Nat Commun 2017 Dec 11;8(1):2045.
    doi: 10.1038/s41467-017-02305-6pmc: PMC5725498pubmed: 29229905google scholar: lookup
  50. Zhang JY, Wang XM, Xing X, Xu Z, Zhang C, Song JW, Fan X, Xia P, Fu JL, Wang SY, Xu RN, Dai XP, Shi L, Huang L, Jiang TJ, Shi M, Zhang Y, Zumla A, Maeurer M, Bai F, Wang FS. Single-cell landscape of immunological responses in patients with COVID-19.. Nat Immunol 2020 Sep;21(9):1107-1118.
    doi: 10.1038/s41590-020-0762-xpubmed: 32788748google scholar: lookup
  51. Holm D, Fink DR, Steffensen MA, Schlosser A, Nielsen O, Moeller JB, Holmskov U. Characterization of a novel human scavenger receptor cysteine-rich molecule SCART1 expressed by lymphocytes.. Immunobiology 2013 Mar;218(3):408-17.
    doi: 10.1016/j.imbio.2012.05.025pubmed: 22795646google scholar: lookup
  52. Kisielow J, Kopf M, Karjalainen K. SCART scavenger receptors identify a novel subset of adult gammadelta T cells.. J Immunol 2008 Aug 1;181(3):1710-6.
    doi: 10.4049/jimmunol.181.3.1710pubmed: 18641307google scholar: lookup
  53. Patel RS, Tomlinson JE, Divers TJ, Van de Walle GR, Rosenberg BR. Single-cell resolution landscape of equine peripheral blood mononuclear cells reveals diverse cell types including T-bet(+) B cells.. BMC Biol 2021 Jan 22;19(1):13.
    doi: 10.1186/s12915-020-00947-5pmc: PMC7820527pubmed: 33482825google scholar: lookup
  54. Yoon HS, Scharer CD, Majumder P, Davis CW, Butler R, Zinzow-Kramer W, Skountzou I, Koutsonanos DG, Ahmed R, Boss JM. ZBTB32 is an early repressor of the CIITA and MHC class II gene expression during B cell differentiation to plasma cells.. J Immunol 2012 Sep 1;189(5):2393-403.
    doi: 10.4049/jimmunol.1103371pmc: PMC3424359pubmed: 22851713google scholar: lookup
  55. Travaglini KJ, Nabhan AN, Penland L, Sinha R, Gillich A, Sit RV, Chang S, Conley SD, Mori Y, Seita J, Berry GJ, Shrager JB, Metzger RJ, Kuo CS, Neff N, Weissman IL, Quake SR, Krasnow MA. A molecular cell atlas of the human lung from single-cell RNA sequencing.. Nature 2020 Nov;587(7835):619-625.
    doi: 10.1038/s41586-020-2922-4pmc: PMC7704697pubmed: 33208946google scholar: lookup
  56. Morris SA. The evolving concept of cell identity in the single cell era.. Development 2019 Jun 27;146(12).
    doi: 10.1242/dev.169748pubmed: 31249002google scholar: lookup
  57. Xia B, Yanai I. A periodic table of cell types.. Development 2019 Jun 27;146(12).
    doi: 10.1242/dev.169854pmc: PMC6602355pubmed: 31249003google scholar: lookup
  58. Koczera P, Martin L, Marx G, Schuerholz T. The Ribonuclease A Superfamily in Humans: Canonical RNases as the Buttress of Innate Immunity.. Int J Mol Sci 2016 Aug 5;17(8).
    doi: 10.3390/ijms17081278pmc: PMC5000675pubmed: 27527162google scholar: lookup
  59. Kang H, Bienzle D, Lee GKC, Piché É, Viel L, Odemuyiwa SO, Beeler-Marfisi J. Flow cytometric analysis of equine bronchoalveolar lavage fluid cells in horses with and without severe equine asthma.. Vet Pathol 2022 Jan;59(1):91-99.
    doi: 10.1177/03009858211042588pmc: PMC8679174pubmed: 34521286google scholar: lookup
  60. Hodge SJ, Hodge GL, Holmes M, Reynolds PN. Flow cytometric characterization of cell populations in bronchoalveolar lavage and bronchial brushings from patients with chronic obstructive pulmonary disease.. Cytometry B Clin Cytom 2004 Sep;61(1):27-34.
    doi: 10.1002/cyto.b.20020pubmed: 15351979google scholar: lookup
  61. Pickles K, Pirie RS, Rhind S, Dixon PM, McGorum BC. Cytological analysis of equine bronchoalveolar lavage fluid. Part 2: Comparison of smear and cytocentrifuged preparations.. Equine Vet J 2002 May;34(3):292-6.
    doi: 10.2746/042516402776186155pubmed: 12108750google scholar: lookup
  62. Fastrès A, Pirottin D, Fievez L, Tutunaru AC, Bolen G, Merveille AC, Marichal T, Desmet CJ, Bureau F, Clercx C. Identification of Pro-Fibrotic Macrophage Populations by Single-Cell Transcriptomic Analysis in West Highland White Terriers Affected With Canine Idiopathic Pulmonary Fibrosis.. Front Immunol 2020;11:611749.
    doi: 10.3389/fimmu.2020.611749pmc: PMC7770158pubmed: 33384697google scholar: lookup
  63. Karagianni AE, Kapetanovic R, Summers KM, McGorum BC, Hume DA, Pirie RS. Comparative transcriptome analysis of equine alveolar macrophages.. Equine Vet J 2017 May;49(3):375-382.
    doi: 10.1111/evj.12584pmc: PMC5412682pubmed: 27096353google scholar: lookup
  64. Brand HK, Ahout IM, de Ridder D, van Diepen A, Li Y, Zaalberg M, Andeweg A, Roeleveld N, de Groot R, Warris A, Hermans PW, Ferwerda G, Staal FJ. Olfactomedin 4 Serves as a Marker for Disease Severity in Pediatric Respiratory Syncytial Virus (RSV) Infection.. PLoS One 2015;10(7):e0131927.
  65. Gong F, Li R, Zheng X, Chen W, Zheng Y, Yang Z, Chen Y, Qu H, Mao E, Chen E. OLFM4 Regulates Lung Epithelial Cell Function in Sepsis-Associated ARDS/ALI via LDHA-Mediated NF-κB Signaling.. J Inflamm Res 2021;14:7035-7051.
    doi: 10.2147/JIR.S335915pmc: PMC8694847pubmed: 34955649google scholar: lookup
  66. Kobayashi S, Tayama S, Phung HT, Kagawa Y, Miyazaki H, Takahashi Y, Maruyama T, Ishii N, Owada Y. Fatty acid-binding protein 5 limits ILC2-mediated allergic lung inflammation in a murine asthma model.. Sci Rep 2020 Oct 6;10(1):16617.
    doi: 10.1038/s41598-020-73935-ypmc: PMC7538993pubmed: 33024217google scholar: lookup
  67. Zhang S, Yu M, Guo Q, Li R, Li G, Tan S, Li X, Wei Y, Wu M. Annexin A2 binds to endosomes and negatively regulates TLR4-triggered inflammatory responses via the TRAM-TRIF pathway.. Sci Rep 2015 Nov 3;5:15859.
    doi: 10.1038/srep15859pmc: PMC4630631pubmed: 26527544google scholar: lookup
  68. Hiroshima Y, Hsu K, Tedla N, Wong SW, Chow S, Kawaguchi N, Geczy CL. S100A8/A9 and S100A9 reduce acute lung injury.. Immunol Cell Biol 2017 May;95(5):461-472.
    doi: 10.1038/icb.2017.2pmc: PMC5454315pubmed: 28074060google scholar: lookup
  69. Viola A, Munari F, Sánchez-Rodríguez R, Scolaro T, Castegna A. The Metabolic Signature of Macrophage Responses.. Front Immunol 2019;10:1462.
    doi: 10.3389/fimmu.2019.01462pmc: PMC6618143pubmed: 31333642google scholar: lookup
  70. Jo M, Kim JH, Song GJ, Seo M, Hwang EM, Suk K. Astrocytic Orosomucoid-2 Modulates Microglial Activation and Neuroinflammation.. J Neurosci 2017 Mar 15;37(11):2878-2894.
  71. Lee YS, Choi JW, Hwang I, Lee JW, Lee JH, Kim AY, Huh JY, Koh YJ, Koh GY, Son HJ, Masuzaki H, Hotta K, Alfadda AA, Kim JB. Adipocytokine orosomucoid integrates inflammatory and metabolic signals to preserve energy homeostasis by resolving immoderate inflammation.. J Biol Chem 2010 Jul 16;285(29):22174-85.
    doi: 10.1074/jbc.M109.085464pmc: PMC2903347pubmed: 20442402google scholar: lookup
  72. Sanjurjo L, Amézaga N, Aran G, Naranjo-Gómez M, Arias L, Armengol C, Borràs FE, Sarrias MR. The human CD5L/AIM-CD36 axis: A novel autophagy inducer in macrophages that modulates inflammatory responses.. Autophagy 2015;11(3):487-502.
  73. Sanjurjo L, Aran G, Téllez É, Amézaga N, Armengol C, López D, Prats C, Sarrias MR. CD5L Promotes M2 Macrophage Polarization through Autophagy-Mediated Upregulation of ID3.. Front Immunol 2018;9:480.
    doi: 10.3389/fimmu.2018.00480pmc: PMC5858086pubmed: 29593730google scholar: lookup
  74. Mitsi E, Kamng'ona R, Rylance J, Solórzano C, Jesus Reiné J, Mwandumba HC, Ferreira DM, Jambo KC. Human alveolar macrophages predominately express combined classical M1 and M2 surface markers in steady state.. Respir Res 2018 Apr 18;19(1):66.
    doi: 10.1186/s12931-018-0777-0pmc: PMC5907303pubmed: 29669565google scholar: lookup
  75. Takiguchi H, Yang CX, Yang CWT, Sahin B, Whalen BA, Milne S, Akata K, Yamasaki K, Yang JSW, Cheung CY, Vander Werff R, McNagny KM, Leitao Filho FS, Shaipanich T, van Eeden SF, Obeidat M, Leung JM, Sin DD. Macrophages with reduced expressions of classical M1 and M2 surface markers in human bronchoalveolar lavage fluid exhibit pro-inflammatory gene signatures.. Sci Rep 2021 Apr 15;11(1):8282.
    doi: 10.1038/s41598-021-87720-ypmc: PMC8050093pubmed: 33859282google scholar: lookup
  76. Karagianni AE, Lisowski ZM, Hume DA, Scott Pirie R. The equine mononuclear phagocyte system: The relevance of the horse as a model for understanding human innate immunity.. Equine Vet J 2021 Mar;53(2):231-249.
    doi: 10.1111/evj.13341pubmed: 32881079google scholar: lookup
  77. Ross EA, Devitt A, Johnson JR. Macrophages: The Good, the Bad, and the Gluttony.. Front Immunol 2021;12:708186.
    doi: 10.3389/fimmu.2021.708186pmc: PMC8397413pubmed: 34456917google scholar: lookup
  78. Byrne AJ, Powell JE, O'Sullivan BJ, Ogger PP, Hoffland A, Cook J, Bonner KL, Hewitt RJ, Wolf S, Ghai P, Walker SA, Lukowski SW, Molyneaux PL, Saglani S, Chambers DC, Maher TM, Lloyd CM. Dynamics of human monocytes and airway macrophages during healthy aging and after transplant.. J Exp Med 2020 Mar 2;217(3).
    doi: 10.1084/jem.20191236pmc: PMC7062517pubmed: 31917836google scholar: lookup
  79. Schulz D, Severin Y, Zanotelli VRT, Bodenmiller B. In-Depth Characterization of Monocyte-Derived Macrophages using a Mass Cytometry-Based Phagocytosis Assay.. Sci Rep 2019 Feb 13;9(1):1925.
    doi: 10.1038/s41598-018-38127-9pmc: PMC6374473pubmed: 30760760google scholar: lookup
  80. Silva MT. Macrophage phagocytosis of neutrophils at inflammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation.. J Leukoc Biol 2011 May;89(5):675-83.
    doi: 10.1189/jlb.0910536pubmed: 21169518google scholar: lookup
  81. Niedzwiedz A, Jaworski Z, Tykalowski B, Smialek M. Neutrophil and macrophage apoptosis in bronchoalveolar lavage fluid from healthy horses and horses with recurrent airway obstruction (RAO).. BMC Vet Res 2014 Jan 24;10:29.
    doi: 10.1186/1746-6148-10-29pmc: PMC3903020pubmed: 24460911google scholar: lookup
  82. Lee Y, Kiupel M, Soboll Hussey G. Characterization of respiratory dendritic cells from equine lung tissues.. BMC Vet Res 2017 Nov 6;13(1):313.
    doi: 10.1186/s12917-017-1240-zpmc: PMC5674750pubmed: 29110660google scholar: lookup
  83. Burel JG, Pomaznoy M, Lindestam Arlehamn CS, Weiskopf D, da Silva Antunes R, Jung Y, Babor M, Schulten V, Seumois G, Greenbaum JA, Premawansa S, Premawansa G, Wijewickrama A, Vidanagama D, Gunasena B, Tippalagama R, deSilva AD, Gilman RH, Saito M, Taplitz R, Ley K, Vijayanand P, Sette A, Peters B. Circulating T cell-monocyte complexes are markers of immune perturbations.. Elife 2019 Jun 25;8.
    doi: 10.7554/eLife.46045pmc: PMC6592685pubmed: 31237234google scholar: lookup
  84. Burel JG, Pomaznoy M, Lindestam Arlehamn CS, Seumois G, Vijayanand P, Sette A, Peters B. The Challenge of Distinguishing Cell-Cell Complexes from Singlet Cells in Non-Imaging Flow Cytometry and Single-Cell Sorting.. Cytometry A 2020 Nov;97(11):1127-1135.
    doi: 10.1002/cyto.a.24027pmc: PMC7666012pubmed: 32400942google scholar: lookup
  85. Restifo NP, Gattinoni L. Lineage relationship of effector and memory T cells.. Curr Opin Immunol 2013 Oct;25(5):556-63.
    doi: 10.1016/j.coi.2013.09.003pmc: PMC3858177pubmed: 24148236google scholar: lookup
  86. Looringh van Beeck FA, Reinink P, Hermsen R, Zajonc DM, Laven MJ, Fun A, Troskie M, Schoemaker NJ, Morar D, Lenstra JA, Vervelde L, Rutten VP, van Eden W, Van Rhijn I. Functional CD1d and/or NKT cell invariant chain transcript in horse, pig, African elephant and guinea pig, but not in ruminants.. Mol Immunol 2009 Apr;46(7):1424-31.
  87. Dossa RG, Alperin DC, Garzon D, Mealey RH, Brown WC, Jervis PJ, Besra GS, Cox LR, Hines SA. In contrast to other species, α-Galactosylceramide (α-GalCer) is not an immunostimulatory NKT cell agonist in horses.. Dev Comp Immunol 2015 Mar;49(1):49-58.
    doi: 10.1016/j.dci.2014.11.005pubmed: 25445911google scholar: lookup
  88. Tan TCJ, Knight J, Sbarrato T, Dudek K, Willis AE, Zamoyska R. Suboptimal T-cell receptor signaling compromises protein translation, ribosome biogenesis, and proliferation of mouse CD8 T cells.. Proc Natl Acad Sci U S A 2017 Jul 25;114(30):E6117-E6126.
    doi: 10.1073/pnas.1700939114pmc: PMC5544288pubmed: 28696283google scholar: lookup
  89. Tang R, Liu X, Liang C, Hua J, Xu J, Wang W, Meng Q, Liu J, Zhang B, Yu X, Shi S. Deciphering the Prognostic Implications of the Components and Signatures in the Immune Microenvironment of Pancreatic Ductal Adenocarcinoma.. Front Immunol 2021;12:648917.
    doi: 10.3389/fimmu.2021.648917pmc: PMC7987951pubmed: 33777046google scholar: lookup
  90. Yang B, Fan J, Huang J, Guo E, Fu Y, Liu S, Xiao R, Liu C, Lu F, Qin T, He C, Wang Z, Qin X, Hu D, You L, Li X, Wang T, Wu P, Chen G, Zhou J, Li K, Sun C. Clinical and molecular characteristics of COVID-19 patients with persistent SARS-CoV-2 infection.. Nat Commun 2021 Jun 9;12(1):3501.
    doi: 10.1038/s41467-021-23621-ypmc: PMC8190301pubmed: 34108465google scholar: lookup
  91. Kaelin CB, McGowan KA, Barsh GS. Developmental genetics of color pattern establishment in cats.. Nat Commun 2021 Sep 7;12(1):5127.
    doi: 10.1038/s41467-021-25348-2pmc: PMC8423757pubmed: 34493721google scholar: lookup
  92. Madissoon E, Wilbrey-Clark A, Miragaia RJ, Saeb-Parsy K, Mahbubani KT, Georgakopoulos N, Harding P, Polanski K, Huang N, Nowicki-Osuch K, Fitzgerald RC, Loudon KW, Ferdinand JR, Clatworthy MR, Tsingene A, van Dongen S, Dabrowska M, Patel M, Stubbington MJT, Teichmann SA, Stegle O, Meyer KB. scRNA-seq assessment of the human lung, spleen, and esophagus tissue stability after cold preservation.. Genome Biol 2019 Dec 31;21(1):1.
    doi: 10.1186/s13059-019-1906-xpmc: PMC6937944pubmed: 31892341google scholar: lookup
  93. Guillaumet-Adkins A, Rodríguez-Esteban G, Mereu E, Mendez-Lago M, Jaitin DA, Villanueva A, Vidal A, Martinez-Marti A, Felip E, Vivancos A, Keren-Shaul H, Heath S, Gut M, Amit I, Gut I, Heyn H. Single-cell transcriptome conservation in cryopreserved cells and tissues.. Genome Biol 2017 Mar 1;18(1):45.
    doi: 10.1186/s13059-017-1171-9pmc: PMC5333448pubmed: 28249587google scholar: lookup
  94. Schiller HB, Montoro DT, Simon LM, Rawlins EL, Meyer KB, Strunz M, Vieira Braga FA, Timens W, Koppelman GH, Budinger GRS, Burgess JK, Waghray A, van den Berge M, Theis FJ, Regev A, Kaminski N, Rajagopal J, Teichmann SA, Misharin AV, Nawijn MC. The Human Lung Cell Atlas: A High-Resolution Reference Map of the Human Lung in Health and Disease.. Am J Respir Cell Mol Biol 2019 Jul;61(1):31-41.
    doi: 10.1165/rcmb.2018-0416TRpmc: PMC6604220pubmed: 30995076google scholar: lookup

Citations

This article has been cited 2 times.
  1. Kang H, Lee GKC, Bienzle D, Arroyo LG, Sears W, Lillie BN, Beeler-Marfisi J. Equine alveolar macrophages and monocyte-derived macrophages respond differently to an inflammatory stimulus.. PLoS One 2023;18(3):e0282738.
    doi: 10.1371/journal.pone.0282738pubmed: 36920969google scholar: lookup
  2. Sage SE, Nicholson P, Leeb T, Gerber V, Jagannathan V. Long-Read Transcriptome of Equine Bronchoalveolar Cells.. Genes (Basel) 2022 Sep 25;13(10).
    doi: 10.3390/genes13101722pubmed: 36292607google scholar: lookup