Single-Cell Transcriptional Profiling Reveals Cellular Diversity and Intercommunication in the Mouse Heart

Cell Reports

Volumn 22, Issue 3, 2018, Pages 600-610

  Skelly, Daniel A ^a   Squiers, Galen T ^a   McLellan, Micheal A ^a,b   Bolisetty, Mohan T ^a   Robson, Paul ^a,c   Rosenthal, Nadia A ^a,b,d,e   Pinto, Alexander R ^a,d  

^a JACKSON LABORATORY   (United States)

^b TUFTS UNIVERSITY   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d MONASH UNIVERSITY   (Australia)

^e NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

10X; cardiac non myocyte; cell type markers; cell cell communication; cellulome; heart; mouse; sexual dimorphism; single cell RNA seq

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC CELLULOME; CARDIAC MUSCLE CELL; CELL COMMUNICATION; CELL POPULATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GLIA; MALE; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; RNA SEQUENCE; SEX DIFFERENCE; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; PROCEDURES; SINGLE CELL ANALYSIS; TRANSCRIPTION INITIATION;

ANIMALS; GENE EXPRESSION PROFILING; MICE; SINGLE-CELL ANALYSIS; TRANSCRIPTIONAL ACTIVATION;

EID: 85041654515     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.12.072     Document Type: Article

References (59)

1. Acharya, A., Baek, S.T., Huang, G., Eskiocak, B., Goetsch, S., Sung, C.Y., Banfi, S., Sauer, M.F., Olsen, G.S., Duffield, J.S., et al. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 139 (2012), 2139–2149.
2. Armulik, A., Genové, G., Betsholtz, C., Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21 (2011), 193–215.
3. Artis, D., Spits, H., The biology of innate lymphoid cells. Nature 517 (2015), 293–301.
4. Baban, B., Yin, L., Qin, X., Liu, J.Y., Shi, X., Mozaffari, M.S., The role of GILZ in modulation of adaptive immunity in a murine model of myocardial infarction. Exp. Mol. Pathol. 102 (2017), 408–414.
5. Bach, L.A., Endothelial cells and the IGF system. J. Mol. Endocrinol. 54 (2015), R1–R13.
6. Biassoni, R., Cantoni, C., Marras, D., Giron-Michel, J., Falco, M., Moretta, L., Dimasi, N., Human natural killer cell receptors: insights into their molecular function and structure. J. Cell. Mol. Med. 7 (2003), 376–387.
7. Bikfalvi, A., Klein, S., Pintucci, G., Rifkin, D.B., Biological roles of fibroblast growth factor-2. Endocr. Rev. 18 (1997), 26–45.
8. Blenck, C.L., Harvey, P.A., Reckelhoff, J.F., Leinwand, L.A., The importance of biological sex and estrogen in rodent models of cardiovascular health and disease. Circ. Res. 118 (2016), 1294–1312.
9. Bonecchi, R., Polentarutti, N., Luini, W., Borsatti, A., Bernasconi, S., Locati, M., Power, C., Proudfoot, A., Wells, T.N., Mackay, C., et al. Up-regulation of CCR1 and CCR3 and induction of chemotaxis to CC chemokines by IFN-gamma in human neutrophils. J. Immunol. 162 (1999), 474–479.
10. Breviario, F., Caveda, L., Corada, M., Martin-Padura, I., Navarro, P., Golay, J., Introna, M., Gulino, D., Lampugnani, M.G., Dejana, E., Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin. Arterioscler. Thromb. Vasc. Biol. 15 (1995), 1229–1239.
11. Butler, A., Satija, R., Integrated analysis of single cell transcriptomic data across conditions, technologies, and species. bioRxiv, 2017, 10.1101/164889.
12. Cavasin, M.A., Tao, Z.-Y., Yu, A.-L., Yang, X.-P., Testosterone enhances early cardiac remodeling after myocardial infarction, causing rupture and degrading cardiac function. Am. J. Physiol. Heart Circ. Physiol. 290 (2006), H2043–H2050.
13. Clarke, S.D., Regulation of fatty acid synthase gene expression: an approach for reducing fat accumulation. J. Anim. Sci. 71 (1993), 1957–1965.
14. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., Förster, I., Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8 (1999), 265–277.
15. Conway, J.G., McDonald, B., Parham, J., Keith, B., Rusnak, D.W., Shaw, E., Jansen, M., Lin, P., Payne, A., Crosby, R.M., et al. Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cFMS kinase inhibitor GW2580. Proc. Natl. Acad. Sci. USA 102 (2005), 16078–16083.
16. DeLaughter, D.M., Bick, A.G., Wakimoto, H., McKean, D., Gorham, J.M., Kathiriya, I.S., Hinson, J.T., Homsy, J., Gray, J., Pu, W., et al. Single-cell resolution of temporal gene expression during heart development. Dev. Cell 39 (2016), 480–490.
17. Deng, Y., Kim, B., He, X., Kim, S., Lu, C., Wang, H., Cho, S.G., Hou, Y., Li, J., Zhao, X., Lu, Q.R., Direct visualization of membrane architecture of myelinating cells in transgenic mice expressing membrane-anchored EGFP. Genesis 52 (2014), 341–349.
18. Doerflinger, N.H., Macklin, W.B., Popko, B., Inducible site-specific recombination in myelinating cells. Genesis 35 (2003), 63–72.
19. Eddleston, J., Herschbach, J., Wagelie-Steffen, A.L., Christiansen, S.C., Zuraw, B.L., The anti-inflammatory effect of glucocorticoids is mediated by glucocorticoid-induced leucine zipper in epithelial cells. J. Allergy Clin. Immunol. 119 (2007), 115–122.
20. Epelman, S., Lavine, K.J.J.J., Beaudin, A.E.E.E., Sojka, D.K.K.K., Carrero, J.A.A.A., Calderon, B., Brija, T., Gautier, E.L.L.L., Ivanov, S., Satpathy, A.T.T.T., et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40 (2014), 91–104.
21. Fang, L., Gao, X.-M., Moore, X.-L., Kiriazis, H., Su, Y., Ming, Z., Lim, Y.L., Dart, A.M., Du, X.-J., Differences in inflammation, MMP activation and collagen damage account for gender difference in murine cardiac rupture following myocardial infarction. J. Mol. Cell. Cardiol. 43 (2007), 535–544.
22. Fregoso, S.P.P., Hoover, D.B.B., Development of cardiac parasympathetic neurons, glial cells, and regional cholinergic innervation of the mouse heart. Neuroscience 221 (2012), 28–36.
23. Furtado, M.B., Costa, M.W., Pranoto, E.A., Salimova, E., Pinto, A.R., Lam, N.T., Park, A., Snider, P., Chandran, A., Harvey, R.P., et al. Cardiogenic genes expressed in cardiac fibroblasts contribute to heart development and repair. Circ. Res. 114 (2014), 1422–1434.
24. Gaengel, K., Genové, G., Armulik, A., Betsholtz, C., Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29 (2009), 630–638.
25. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., et al., Immunological Genome Consortium. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
26. Geijtenbeek, T.B., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Adema, G.J., van Kooyk, Y., Figdor, C.G., Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100 (2000), 575–585.
27. Glebova, N.O., Ginty, D.D., Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J. Neurosci. 24 (2004), 743–751.
28. Gokce, O., Stanley, G.M., Treutlein, B., Neff, N.F., Camp, J.G., Malenka, R.C., Rothwell, P.E., Fuccillo, M.V., Südhof, T.C., Quake, S.R., Cellular taxonomy of the mouse striatum as revealed by single-cell RNA-Seq. Cell Rep. 16 (2016), 1126–1137.
29. Hamilton, T.G., Klinghoffer, R.A., Corrin, P.D., Soriano, P., Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol. Cell. Biol. 23 (2003), 4013–4025.
30. He, L., Vanlandewijck, M., Raschperger, E., Andaloussi Mäe, M., Jung, B., Lebouvier, T., Ando, K., Hofmann, J., Keller, A., Betsholtz, C., Analysis of the brain mural cell transcriptome. Sci. Rep., 6, 2016, 35108.
31. Hughes, E.G., Kang, S.H., Fukaya, M., Bergles, D.E., Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16 (2013), 668–676.
32. Hulsmans, M., Clauss, S., Xiao, L., Aguirre, A.D., King, K.R., Hanley, A., Hucker, W.J., Wülfers, E.M., Seemann, G., Courties, G., et al. Macrophages facilitate electrical conduction in the heart. Cell 169 (2017), 510–522.e20.
33. Ilinykh, A., Pinto, A.R., The role of cardiac tissue macrophages in homeostasis and disease. 2017, Springer.
34. Ivey, M.J., Tallquist, M.D., Defining the cardiac fibroblast. Circ. J. 80 (2016), 2269–2276.
35. Kovacic, J.C., Mercader, N., Torres, M., Boehm, M., Fuster, V., Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition: from cardiovascular development to disease. Circulation 125 (2012), 1795–1808.
36. Kuijpers, T.W., Bende, R.J., Baars, P.A., Grummels, A., Derks, I.A.M., Dolman, K.M., Beaumont, T., Tedder, T.F., van Noesel, C.J.M., Eldering, E., van Lier, R.A., CD20 deficiency in humans results in impaired T cell-independent antibody responses. J. Clin. Invest. 120 (2010), 214–222.
37. Langlais, D., Barreiro, L.B., Gros, P., The macrophage IRF8/IRF1 regulome is required for protection against infections and is associated with chronic inflammation. J. Exp. Med. 213 (2016), 585–603.
38. Lohela, M., Bry, M., Tammela, T., Alitalo, K., VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. 2009, Elsevier Current Trends.
39. Macosko, E.Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A.R., Kamitaki, N., Martersteck, E.M., et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161 (2015), 1202–1214.
40. McDavid, A., Finak, G., Chattopadyay, P.K., Dominguez, M., Lamoreaux, L., Ma, S.S., Roederer, M., Gottardo, R., Data exploration, quality control and testing in single-cell qPCR-based gene expression experiments. Bioinformatics 29 (2013), 461–467.
41. Monnerat, G., Alarcón, M.L., Vasconcellos, L.R., Hochman-Mendez, C., Brasil, G., Bassani, R.A., Casis, O., Malan, D., Travassos, L.H., Sepúlveda, M., et al. Macrophage-dependent IL-1β production induces cardiac arrhythmias in diabetic mice. Nat. Commun., 7, 2016, 13344.
42. Nam, J., Onitsuka, I., Hatch, J., Uchida, Y., Ray, S., Huang, S., Li, W., Zang, H., Ruiz-Lozano, P., Mukouyama, Y.S., Coronary veins determine the pattern of sympathetic innervation in the developing heart. Development 140 (2013), 1475–1485.
43. Newman, P.J., Berndt, M.C., Gorski, J., White, G.C. 2nd, Lyman, S., Paddock, C., Muller, W.A., PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247 (1990), 1219–1222.
44. Panopoulos, A.D., Watowich, S.S., Granulocyte colony-stimulating factor: molecular mechanisms of action during steady state and ‘emergency’ hematopoiesis. Cytokine 42 (2008), 277–288.
45. Pilling, D., Fan, T., Huang, D., Kaul, B., Gomer, R.H., Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS ONE, 4, 2009, e7475.
46. Pinto, A.R., Paolicelli, R., Salimova, E., Gospocic, J., Slonimsky, E., Bilbao-Cortes, D., Godwin, J.W., Rosenthal, N.A., An abundant tissue macrophage population in the adult murine heart with a distinct alternatively-activated macrophage profile. PLoS ONE, 7, 2012, e36814.
47. Pinto, A.R., Chandran, A., Rosenthal, N.A., Godwin, J.W., Isolation and analysis of single cells from the mouse heart. J. Immunol. Methods 393 (2013), 74–80.
48. Pinto, A.R., Ilinykh, A., Ivey, M.J., Kuwabara, J.T., D'Antoni, M.L., Debuque, R., Chandran, A., Wang, L., Arora, K., Rosenthal, N.A., Tallquist, M.D., Revisiting cardiac cellular composition. Circ. Res. 118 (2016), 400–409.
49. Ramilowski, J.A., Goldberg, T., Harshbarger, J., Kloppmann, E., Lizio, M., Satagopam, V.P., Itoh, M., Kawaji, H., Carninci, P., Rost, B., Forrest, A.R., A draft network of ligand-receptor-mediated multicellular signalling in human. Nat. Commun., 6, 2015, 7866.
50. Reilkoff, R.A., Bucala, R., Herzog, E.L., Fibrocytes: emerging effector cells in chronic inflammation. Nat. Rev. Immunol. 11 (2011), 427–435.
51. Rensen, S.S.M., Doevendans, P.A.F.M., van Eys, G.J.J.M., Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth. Heart J. 15 (2007), 100–108.
52. Ronchetti, S., Migliorati, G., Riccardi, C., GILZ as a mediator of the anti-inflammatory effects of glucocorticoids. Front. Endocrinol. (Lausanne), 6, 2015, 170.
53. Ruffell, D., Mourkioti, F., Gambardella, A., Kirstetter, P., Lopez, R.G., Rosenthal, N., Nerlov, C., A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA 106 (2009), 17475–17480.
54. Ryan, J.C., Turck, J., Niemi, E.C., Yokoyama, W.M., Seaman, W.E., Molecular cloning of the NK1.1 antigen, a member of the NKR-P1 family of natural killer cell activation molecules. J. Immunol. 149 (1992), 1631–1635.
55. Ryckman, C., Vandal, K., Rouleau, P., Talbot, M., Tessier, P.A., Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J. Immunol. 170 (2003), 3233–3242.
56. Sevilla, L.M., Latorre, V., Carceller, E., Boix, J., Vodák, D., Mills, I.G., Pérez, P., Glucocorticoid receptor and Klf4 co-regulate anti-inflammatory genes in keratinocytes. Mol. Cell. Endocrinol. 412 (2015), 281–289.
57. Sudo, T., Nishikawa, S., Ogawa, M., Kataoka, H., Ohno, N., Izawa, A., Hayashi, S., Nishikawa, S., Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M. Oncogene 11 (1995), 2469–2476.
58. van den Brink, S.C., Sage, F., Vértesy, Á., Spanjaard, B., Peterson-Maduro, J., Baron, C.S., Robin, C., van Oudenaarden, A., Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations. Nat. Methods 14 (2017), 935–936.
59. Williams, A.F., Barclay, A.N., Clark, S.J., Paterson, D.J., Willis, A.C., Similarities in sequences and cellular expression between rat CD2 and CD4 antigens. J. Exp. Med. 165 (1987), 368–380.