Single epicardial cell transcriptome sequencing identifies caveolin 1 as an essential factor in zebrafish heart regeneration

Development (Cambridge)

Volumn 143, Issue 2, 2016, Pages 232-243

  Cao, Jingli ^a   Navis, Adam ^a   Cox, Ben D ^a   Dickson, Amy L ^a   Gemberling, Matthew ^a   Karra, Ravi ^a   Bagnat, Michel ^a   Poss, Kenneth D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Caveolin 1; Epicardium; Heart regeneration; Single cell sequencing; Zebrafish

Indexed keywords

CAVEOLIN 1; SCAFFOLD PROTEIN; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EPICARDIUM; GENE; GENE EXPRESSION; GENOME; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART REGENERATION; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; REGENERATION; REGULATORY SEQUENCE; REPORTER GENE; VASCULAR ENDOTHELIUM; ZEBRA FISH; ANIMAL; CARDIAC MUSCLE CELL; CYTOLOGY; GENETICS; HEART; METABOLISM; PERICARDIUM; PHYSIOLOGY;

ANIMALS; CAVEOLIN 1; HEART; MYOCYTES, CARDIAC; PERICARDIUM; REGENERATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84954512505     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.130534     Document Type: Article

References (61)

1. Bollini, S., Vieira, J. M. N., Howard, S., Dube, K. N., Balmer, G. M., Smart, N. and Riley, P. R. (2014). Re-activated adult epicardial progenitor cells are a heterogeneous population molecularly distinct from their embryonic counterparts. Stem Cells Dev. 23, 1719-1730.
2. Cavallero, S., Shen, H., Yi, C., Lien, C.-L., Kumar, S. R. and Sucov, H. M. (2015). CXCL12 signaling is essential for maturation of the ventricular coronary endothelial plexus and establishment of functional coronary circulation. Dev. Cell 33, 469-477.
3. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J. and Voytas, D. F. (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82.
4. Chablais, F. and Jazwinska, A. (2012). The regenerative capacity of the zebrafish heart is dependent on TGFbeta signaling. Development 139, 1921-1930.
5. Chen, Y.-G. (2009). Endocytic regulation of TGF-beta signaling. Cell Res. 19, 58-70.
6. Cho, K. A., Ryu, S. J., Oh, Y. S., Park, J. H., Lee, J. W., Kim, H.-P., Kim, K. T., Jang, I. S. and Park, S. C. (2004). Morphological adjustment of senescent cells by modulating caveolin-1 status. J. Biol. Chem. 279, 42270-42278.
7. Choi, W.-Y., Gemberling, M., Wang, J., Holdway, J. E., Shen, M.-C., Karlstrom, R. O. and Poss, K. D. (2013). In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development 140, 660-666.
8. Cohen, A. W., Park, D. S., Woodman, S. E., Williams, T. M., Chandra, M., Shirani, J., Pereira de Souza, A., Kitsis, R. N., Russell, R. G., Weiss, L. M. et al. (2003). Caveolin-1 null mice develop cardiac hypertrophy with hyperactivation of p42/44 MAP kinase in cardiac fibroblasts. Am. J. Physiol. Cell Physiol. 284, C457-C474.
9. Dahlem, T. J., Hoshijima, K., Jurynec, M. J., Gunther, D., Starker, C. G., Locke, S., Weis, A. M., Voytas, D. F. and Grunwald, D. J. (2012). Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet. 8, e1002861.
10. Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F. and Wrana, J. L. (2003). Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 5, 410-421.
11. Doyle, E. L., Booher, N. J., Standage, D. S., Voytas, D. F., Brendel, V. P., Vandyk, J. K. and Bogdanove, A. J. (2012). TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res. 40, W117-W122.
12. Echarri, A., Muriel, O. and Del Pozo, M. A. (2007). Intracellular trafficking of raft/ caveolae domains: insights from integrin signaling. Semin. Cell Dev. Biol. 18, 627-637.
13. Fang, P.-K., Solomon, K. R., Zhuang, L., Qi, M., McKee, M., Freeman, M. R. and Yelick, P. C. (2006). Caveolin-1alpha and -1beta perform nonredundant roles in early vertebrate development. Am. J. Pathol. 169, 2209-2222.
14. Fujimoto, T., Kogo, H., Nomura, R. and Une, T. (2000). Isoforms of caveolin-1 and caveolar structure. J. Cell Sci. 113, 3509-3517.
15. Gabor, K. A., Stevens, C. R., Pietraszewski, M. J., Gould, T. J., Shim, J., Yoder, J. A., Lam, S. H., Gong, Z., Hess, S. T. and Kim, C. H. (2013). Super resolution microscopy reveals that caveolin-1 is required for spatial organization of CRFB1 and subsequent antiviral signaling in zebrafish. PLoS ONE 8, e68759.
16. Gemberling, M., Karra, R., Dickson, A. L. and Poss, K. D. (2015). Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. Elife 4, e05871.
17. Grande-Garcia, A. and del Pozo, M. A. (2008). Caveolin-1 in cell polarization and directional migration. Eur. J. Cell Biol. 87, 641-647.
18. Gvaramia, D., Blaauboer, M. E., Hanemaaijer, R. and Everts, V. (2013). Role of caveolin-1 in fibrotic diseases. Matrix Biol. 32, 307-315.
19. Harrison, M. R. M., Bussmann, J., Huang, Y., Zhao, L., Osorio, A., Burns, C. G., Burns, C. E., Sucov, H. M., Siekmann, A. F. and Lien, C.-L. (2015). Chemokine-guided angiogenesis directs coronary vasculature formation in zebrafish. Dev. Cell 33, 442-454.
20. Huang, G. N., Thatcher, J. E., McAnally, J., Kong, Y., Qi, X., Tan, W., DiMaio, J. M., Amatruda, J. F., Gerard, R. D., Hill, J. A. et al. (2012). C/EBP transcription factors mediate epicardial activation during heart development and injury. Science 338, 1599-1603.
21. Ieda, M., Fu, J.-D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G. and Srivastava, D. (2010). Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142, 375-386.
22. Jopling, C., Sleep, E., Raya, M., Martı, M., Raya, A. and Izpisua Belmonte, J. C. (2010). Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609.
23. Kikuchi, K., Holdway, J. E., Werdich, A. A., Anderson, R. M., Fang, Y., Egnaczyk, G. F., Evans, T., MacRae, C. A., Stainier, D. Y. R. and Poss, K. D. (2010). Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464, 601-605.
24. Kikuchi, K., Gupta, V., Wang, J., Holdway, J. E., Wills, A. A., Fang, Y. and Poss, K. D. (2011a). tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 138, 2895-2902.
25. Kikuchi, K., Holdway, J. E., Major, R. J., Blum, N., Dahn, R. D., Begemann, G. and Poss, K. D. (2011b). Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 20, 397-404.
26. Knouse, K. A., Wu, J., Whittaker, C. A. and Amon, A. (2014). Single cell sequencing reveals low levels of aneuploidy across mammalian tissues. Proc. Natl. Acad. Sci. USA 111, 13409-13414.
27. Langmead, B. and Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359.
28. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
29. Lee, E. K., Lee, Y. S., Han, I.-O. and Park, S. H. (2007). Expression of Caveolin-1 reduces cellular responses to TGF-beta1 through down-regulating the expression of TGF-beta type II receptor gene in NIH3T3 fibroblast cells. Biochem. Biophys. Res. Commun. 359, 385-390.
30. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G. and Poss, K. D. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619.
31. Li, B. and Dewey, C. N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.
32. Lien, C.-L., Schebesta, M., Makino, S., Weber, G. J. and Keating, M. T. (2006). Gene expression analysis of zebrafish heart regeneration. PLoS Biol. 4, e260.
33. Miyasato, S. K., Loeffler, J., Shohet, R., Zhang, J., Lindsey, M. and Le Saux, C. J. (2011). Caveolin-1 modulates TGF-beta1 signaling in cardiac remodeling. Matrix Biol. 30, 318-329.
34. Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D. et al. (2011). Tumour evolution inferred by single-cell sequencing. Nature 472, 90-94.
35. Navis, A., Marjoram, L. and Bagnat, M. (2013). Cftr controls lumen expansion and function of Kupffer’s vesicle in zebrafish. Development 140, 1703-1712.
36. Nixon, S. J., Carter, A., Wegner, J., Ferguson, C., Floetenmeyer, M., Riches, J., Key, B., Westerfield, M. and Parton, R. G. (2007). Caveolin-1 is required for lateral line neuromast and notochord development. J. Cell Sci. 120, 2151-2161.
37. Nohe, A., Keating, E., Underhill, T. M., Knaus, P. and Petersen, N. O. (2005). Dynamics and interaction of caveolin-1 isoforms with BMP-receptors. J. Cell Sci. 118, 643-650.
38. Parton, R. G. and del Pozo, M. A. (2013). Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 14, 98-112.
39. Parton, R. G., Hanzal-Bayer, M. and Hancock, J. F. (2006). Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J. Cell Sci. 119, 787-796.
40. Pollen, A. A., Nowakowski, T. J., Shuga, J., Wang, X., Leyrat, A. A., Lui, J. H., Li, N., Szpankowski, L., Fowler, B., Chen, P. et al. (2014). Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 32, 1053-1058.
41. Poss, K. D., Wilson, L. G. and Keating, M. T. (2002). Heart regeneration in zebrafish. Science 298, 2188-2190.
42. Qian, L., Huang, Y., Spencer, C. I., Foley, A., Vedantham, V., Liu, L., Conway, S. J., Fu, J.-D. and Srivastava, D. (2012). In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598.
43. Razani, B., Engelman, J. A., Wang, X. B., Schubert, W., Zhang, X. L., Marks, C. B., Macaluso, F., Russell, R. G., Li, M., Pestell, R. G. et al. (2001). Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 276, 38121-38138.
44. Rossi, A., Kontarakis, Z., Gerri, C., Nolte, H., Holper, S., Kruger, M. and Stainier, D. Y. R. (2015). Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524, 230-233.
45. Shalek, A. K., Satija, R., Adiconis, X., Gertner, R. S., Gaublomme, J. T., Raychowdhury, R., Schwartz, S., Yosef, N., Malboeuf, C., Lu, D. et al. (2013). Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 498, 236-240.
46. Shivshankar, P., Halade, G. V., Calhoun, C., Escobar, G. P., Mehr, A. J., Jimenez, F., Martinez, C., Bhatnagar, H., Mjaatvedt, C. H., Lindsey, M. L. et al. (2014). Caveolin-1 deletion exacerbates cardiac interstitial fibrosis by promoting M2 macrophage activation in mice after myocardial infarction. J. Mol. Cell Cardiol. 76, 84-93.
47. Shvets, E., Ludwig, A. and Nichols, B. J. (2014). News from the caves: update on the structure and function of caveolae. Curr. Opin. Cell Biol. 29, 99-106.
48. Smart, N., Risebro, C. A., Melville, A. A. D., Moses, K., Schwartz, R. J., Chien, K. R. and Riley, P. R. (2007). Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445, 177-182.
49. Smart, N., Bollini, S., Dube, K. N., Vieira, J. M., Zhou, B., Davidson, S., Yellon, D., Riegler, J., Price, A. N., Lythgoe, M. F. et al. (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature 474, 640-644.
50. Song, K., Nam, Y.-J., Luo, X., Qi, X., Tan, W., Huang, G. N., Acharya, A., Smith, C. L., Tallquist, M. D., Neilson, E. G. et al. (2012). Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485, 599-604.
51. Suster, M. L., Sumiyama, K. and Kawakami, K. (2009). Transposon-mediated BAC transgenesis in zebrafish and mice. BMC Genomics 10, 477.
52. Tourkina, E., Richard, M., Gooz, P., Bonner, M., Pannu, J., Harley, R., Bernatchez, P. N., Sessa, W. C., Silver, R. M. and Hoffman, S. (2008). Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L843-L861.
53. Wang, X. M., Zhang, Y., Kim, H. P., Zhou, Z., Feghali-Bostwick, C. A., Liu, F., Ifedigbo, E., Xu, X., Oury, T. D., Kaminski, N. et al. (2006). Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J. Exp. Med. 203, 2895-2906.
54. Wang, J., Panakova, D., Kikuchi, K., Holdway, J. E., Gemberling, M., Burris, J. S., Singh, S. P., Dickson, A. L., Lin, Y.-F., Sabeh, M. K. et al. (2011). The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138, 3421-3430.
55. Wang, J., Karra, R., Dickson, A. L. and Poss, K. D. (2013). Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev. Biol. 382, 427-435.
56. Wang, J., Cao, J., Dickson, A. L. and Poss, K. D. (2015). Epicardial regeneration is guided by cardiac outflow tract and Hedgehog signalling. Nature 522, 226-230.
57. Wills, A. A., Holdway, J. E., Major, R. J. and Poss, K. D. (2008). Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 135, 183-192.
58. Yan, L., Yang, M., Guo, H., Yang, L., Wu, J., Li, R., Liu, P., Lian, Y., Zheng, X., Yan, J. et al. (2013). Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1131-1139.
59. Zhao, Y.-Y., Liu, Y., Stan, R.-V., Fan, L., Gu, Y., Dalton, N., Chu, P.-H., Peterson, K., Ross, J., Jr and Chien, K. R. (2002). Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc. Natl. Acad. Sci. USA 99, 11375-11380.
60. Zhou, B. and Pu, W. T. (2012). Isolation and characterization of embryonic and adult epicardium and epicardium-derived cells. Methods Mol. Biol. 843, 155-168.
61. Zhou, B., Honor, L. B., He, H., Ma, Q., Oh, J.-H., Butterfield, C., Lin, R.-Z., Melero-Martin, J. M., Dolmatova, E., Duffy, H. S. et al. (2011). Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 121, 1894-1904.