Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types

Genome Research

Volumn 27, Issue 3, 2017, Pages 451-461

  Carmona, Santiago J ^a,b   Teichmann, Sarah A ^c   Ferreira, Lauren ^c,d,e   MacAulay, Iain C ^c   Stubbington, Michael J T ^c   Cvejic, Ana ^c,d,e   Gfeller, David ^a,b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CD28 ANTIGEN; CD4 ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; CD8ALPHA ANTIGEN; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR4; CYTOPLASM PROTEIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DEATH RECEPTOR; FAS LIGAND; FC RECEPTOR; GRANULYSIN; GRANZYME B; HERPESVIRUS ENTRY MEDIATOR LIGAND; IMMUNOGLOBULIN RECEPTOR; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 1; INTERLEUKIN 10 RECEPTOR BETA; INTERLEUKIN 2 RECEPTOR BETA; MEMBRANE PROTEIN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; NUCLEAR PROTEIN; PROTEIN KINASE LCK; PROTEIN KINASE SYK; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL HETEROGENEITY; CELL POPULATION; CELLS BY BODY ANATOMY; COMPARATIVE STUDY; GENE CLUSTER; GENE EXPRESSION; GENE LOCUS; GENETIC CONSERVATION; HUMAN; HUMAN CELL; MOLECULAR EVOLUTION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SINGLE CELL ANALYSIS; T LYMPHOCYTE; TELEOST; TRANSCRIPTOMICS; ZEBRA FISH; ANIMAL; CELL CULTURE; CONSERVED SEQUENCE; CYTOLOGY; GENETICS; IMMUNOLOGY;

ANIMALS; CELLS, CULTURED; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; KILLER CELLS, NATURAL; MICE; RECEPTORS, IGG; SINGLE-CELL ANALYSIS; TRANSCRIPTOME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85016468947     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.207704.116     Document Type: Article

References (61)

1. Bailey M, Christoforidou Z, Lewis M. 2013. Evolution of immune systems: specificity and autoreactivity. Autoimmun Rev 12: 643-647.
2. Bezman NA, Kim CC, Sun JC, Min-Oo G, Hendricks DW, Kamimura Y, Best JA, Goldrath AW, Lanier LL, Immunological Genome Project Consortium. 2012. Molecular definition of the identity and activation of natural killer cells. Nat Immunol 13: 1000-1009.
3. Bielczyk-Maczyńska E, Serbanovic-Canic J, Ferreira L, Soranzo N, Stemple DL, Ouwehand WH, Cvejic A. 2014. A loss of function screen of identified genome-wide association study Loci reveals new genes controlling hematopoiesis. PLoS Genet 10: e1004450.
4. Björklund AK, Forkel M, Picelli S, Konya V, Theorell J, Friberg D, Sandberg R, Mjösberg J. 2016. The heterogeneity of human CD127+ innate lymphoid cells revealed by single-cell RNA sequencing. Nat Immunol 17: 451-460.
5. Boehm T. 2012. Evolution of vertebrate immunity. Curr Biol 22: R722-R732.
6. Brennecke P, Anders S, Kim JK, Kolodziejczyk AA, Zhang X, Proserpio V, Baying B, Benes V, Teichmann SA, Marioni JC, et al. 2013. Accounting for technical noise in single-cell RNA-seq experiments. Nat Methods 10: 1093-1095.
7. Buettner F, Natarajan KN, Casale FP, Proserpio V, Scialdone A, Theis FJ, Teichmann SA, Marioni JC, Stegle O. 2015. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat Biotechnol 33: 155-160.
8. Carrillo-Bustamante P, Kes mir C, de Boer RJ. 2016. The evolution of natural killer cell receptors. Immunogenetics 68: 3-18.
9. Chambers SM, Boles NC, Lin K-YK, Tierney MP, Bowman TV, Bradfute SB, Chen AJ, Merchant AA, Sirin O, Weksberg DC, et al. 2007. Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell 1: 578-591.
10. Dybkaer K, Iqbal J, Zhou G, Geng H, Xiao L, Schmitz A, d'Amore F, Chan WC. 2007. Genome wide transcriptional analysis of resting and IL2 activated human natural killer cells: gene expression signatures indicative of novel molecular signaling pathways. BMC Genomics 8: 230.
11. Flajnik MF, Kasahara M. 2010. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11: 47-59.
12. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Ferrer-Admettla A, Pattini L, Nielsen R. 2011. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet 7: e1002355.
13. Gibbings D, Befus AD. 2009. CD4 and CD8: an inside-out coreceptor model for innate immune cells. J Leukoc Biol 86: 251-259.
14. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652.
15. Grün D, Lyubimova A, Kester L, Wiebrands K, Basak O, Sasaki N, Clevers H, van Oudenaarden A. 2015. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature 525: 251-255.
16. Guiet R, Poincloux R, Castandet J, Marois L, Labrousse A, Le Cabec V, Maridonneau-Parini I. 2008. Hematopoietic cell kinase (Hck) isoforms and phagocyte duties-from signaling and actin reorganization to migration and phagocytosis. Eur J Cell Biol 87: 527-542.
17. Guo P, Hirano M, Herrin BR, Li J, Yu C, Sadlonova A, Cooper MD. 2009. Dual nature of the adaptive immune system in lampreys. Nature 459: 796-801.
18. Haire RN, Cannon JP, O'Driscoll ML, Ostrov DA, Mueller MG, Turner PM, Litman RT, Litman GW, Yoder JA. 2012. Genomic and functional characterization of the diverse immunoglobulin domain-containing protein (DICP) family. Genomics 99: 282-291.
19. Horton TL, Ritchie P, Watson MD, Horton JD. 1996. NK-like activity against allogeneic tumour cells demonstrated in the spleen of control and thymectomized Xenopus. Immunol Cell Biol 74: 365-373.
20. Iwanami N. 2014. Zebrafish as a model for understanding the evolution of the vertebrate immune system and human primary immunodeficiency. Exp Hematol 42: 697-706.
21. Jansen CA, van de Haar PM, van Haarlem D, van Kooten P, de Wit S, van Eden W, Viertlböck BC, Göbel TW, Vervelde L. 2010. Identification of new populations of chicken natural killer (NK) cells. Dev Comp Immunol 34: 759-767.
22. Kaufman, C.K., Mosimann, C., Fan, Z.P., Yang, S., Thomas, A.J., Ablain, J.,Tan J.L., Fogley R.D., Van Rooijen E., Hagedorn E.J., Ciarlo C., White R.M., Matos D.A., Puller A.-C., Santoriello C., Liao E.C., Young R.A., Zon L.I.A zebrafish melanoma model reveals emergence of neural crest identity during melanoma initiation. Science, 351(6272), 2016.
23. Kharchenko PV, Silberstein L, Scadden DT. 2014. Bayesian approach to single-cell differential expression analysis. Nat Methods 11: 740-742.
24. Kikuchi-Maki A, Catina TL, Campbell KS. 2005. Cutting edge: KIR2DL4 transduces signals into human NK cells through association with the Fc receptor protein. J Immunol 174: 3859-3863.
25. Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, Siepel A. 2008. Patterns of positive selection in six mammalian genomes. PLoS Genet 4: e1000144.
26. Langenau DM, Zon LI. 2005. The zebrafish: a new model of T-cell and thymic development. Nat Rev Immunol 5: 307-317.
27. Langenau DM, Ferrando AA, Traver D, Kutok JL, Hezel J-PD, Kanki JP, Zon LI, Look AT, Trede NS. 2004. In vivo tracking of T cell development, ablation, and engraftment in transgenic zebrafish. Proc Natl Acad Sci 101: 7369-7374.
28. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
29. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNASeq data with or without a reference genome. BMC Bioinformatics 12: 323.
30. Macaulay IC, Svensson V, Labalette C, Ferreira L, Hamey F, Voet T, Teichmann SA, Cvejic A. 2016. Single-cell RNA-sequencing reveals a continuous spectrum of differentiation in hematopoietic cells. Cell Rep 14: 966-977.
31. Meeker ND, Smith ACH, Frazer JK, Bradley DF, Rudner LA, Love C, Trede NS. 2010. Characterization of the zebrafish T cell receptor locus. Immunogenetics 62: 23-29.
32. Moore FE, Garcia EG, Lobbardi R, Jain E, Tang Q, Moore JC, Cortes M, Molodtsov A, Kasheta M, Luo CC, et al. 2016. Single-cell transcriptional analysis of normal, aberrant, and malignant hematopoiesis in zebrafish. J Exp Med 213: 979-992.
33. Parker HS, Leek JT, Favorov AV, Considine M, Xia X, Chavan S, Chung CH, Fertig EJ. 2014. Preserving biological heterogeneity with a permuted surrogate variable analysis for genomics batch correction. Bioinformatics 30: 2757-2763.
34. Pereiro P, Varela M, Diaz-Rosales P, Romero A, Dios S, Figueras A, Novoa B. 2015. Zebrafish Nk-lysins: first insights about their cellular and functional diversification. Dev Comp Immunol 51: 148-159.
35. Picelli S, Faridani OR, Björklund AK, Winberg G, Sagasser S, Sandberg R. 2014. Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc 9: 171-181.
36. Pierson E, Yau C. 2015. ZIFA: dimensionality reduction for zero-inflated single-cell gene expression analysis. Genome Biol 16: 241.
37. Pilbeam K, Basse P, Brossay L, Vujanovic N, Gerstein R, Vallejo AN, Borghesi L. 2008. The ontogeny and fate of NK cells marked by permanent DNA rearrangements. J Immunol 180: 1432-1441.
38. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www. R-project.org/.
39. Renshaw SA, Trede NS. 2012. A model 450 million years in the making: zebrafish and vertebrate immunity. Dis Model Mech 5: 38-47.
40. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43: e47.
41. Saliba A-E, Westermann AJ, Gorski SA, Vogel J. 2014. Single-cell RNAseq: advances and future challenges. Nucleic Acids Res 42: 8845-8860.
42. Schorpp M, Bialecki M, Diekhoff D, Walderich B, Odenthal J, Maischein HM, Zapata AG, Boehm T. 2006. Conserved functions of Ikaros in vertebrate lymphocyte development: genetic evidence for distinct larval and adult phases of T cell development and two lineages of B cells in zebrafish. J Immunol 177: 2463-2476.
43. Schulte R, Wilson NK, Prick JCM, Cossetti C, Maj MK, Göttgens B, Kent DG. 2015. Index sorting resolves heterogeneous murine hematopoietic stem cell populations. Exp Hematol 43: 803-811.
44. Shapiro E, Biezuner T, Linnarsson S. 2013. Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat Rev Genet 14: 618-630.
45. Shay T, Kang J. 2013. Immunological Genome Project and systems immunology. Trends Immunol 34: 602-609.
46. Shay T, Jojic V, Zuk O, Rothamel K, Puyraimond-Zemmour D, Feng T, Wakamatsu E, Benoist C, Koller D, Regev A, et al. 2013. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proc Natl Acad Sci 110: 2946-2951.
47. Shen L, Stuge TB, Bengtén E, Wilson M, Chinchar VG, Naftel JP, Bernanke JM, Clem LW, Miller NW. 2004. Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev Comp Immunol 28: 139-152.
48. Shimizu C, Kawamoto H, Yamashita M, Kimura M, Kondou E, Kaneko Y, Okada S, Tokuhisa T, Yokoyama M, Taniguchi M, et al. 2001. Progression of T cell lineage restriction in the earliest subpopulation of murine adult thymus visualized by the expression of lck proximal promoter activity. Int Immunol 13: 105-117.
49. Stubbington MJT, Lönnberg T, Proserpio V, Clare S, Speak AO, Dougan G, Teichmann SA. 2016. T cell fate and clonality inference from singlecell transcriptomes. Nat Methods 13: 329-332.
50. Sun JC, Lanier LL. 2009. Natural killer cells remember: an evolutionary bridge between innate and adaptive immunity? Eur J Immunol 39: 2059-2064.
51. Sun JC, Beilke JN, Lanier LL. 2009. Adaptive immune features of natural killer cells. Nature 457: 557-561.
52. Trapnell C. 2015. Defining cell types and states with single-cell genomics. Genome Res 25: 1491-1498.
53. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
54. Vu Manh T-P, Marty H, Sibille P, Le Vern Y, Kaspers B, Dalod M, Schwartz-Cornil I, Quéré P. 2014. Existence of conventional dendritic cells in Gallus gallus revealed by comparative gene expression profiling. J Immunol 192: 4510-4517.
55. Ward AC, McPhee DO, Condron MM, Varma S, Cody SH, Onnebo SMN, Paw BH, Zon LI, Lieschke GJ. 2003. The zebrafish spi1 promoter drives myeloid-specific expression in stable transgenic fish. Blood 102: 3238-3240.
56. Watkins NA, Gusnanto A, de Bono B, De S, Miranda-Saavedra D, Hardie DL, Angenent WGJ, Attwood AP, Ellis PD, ErberW, et al. 2009. A HaemAtlas: characterizing gene expression in differentiated human blood cells. Blood 113: e1-9.
57. Yates A, Akanni W, Amode MR, Barrell D, Billis K, Carvalho-Silva D, Cummins C, Clapham P, Fitzgerald S, Gil L, et al. 2016. Ensembl 2016. Nucleic Acids Res 44: D710-D716.
58. Ye J, Ma N, Madden TL, Ostell JM. 2013. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res 41: W34-W40.
59. Yoder JA. 2004. Investigating the morphology, function and genetics of cytotoxic cells in bony fish. Comp Biochem Physiol C Toxicol Pharmacol 138: 271-280.
60. Yoder JA, Litman GW. 2011. The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 63: 123-141.
61. Yoder JA, Litman RT, Mueller MG, Desai S, Dobrinski KP, Montgomery JS, Buzzeo MP, Ota T, Amemiya CT, Trede NS, et al. 2004. Resolution of the novel immune-type receptor gene cluster in zebrafish. Proc Natl Acad Sci 101: 15706-15711.