Hippo Signaling Plays an Essential Role in Cell State Transitions during Cardiac Fibroblast Development

Developmental Cell

Volumn 45, Issue 2, 2018, Pages 153-169.e6

  Xiao, Yang ^a,b,c   Hill, Matthew C ^b   Zhang, Min ^b,d   Martin, Thomas J ^b   Morikawa, Yuka ^a   Wang, Suya ^e   Moise, Alexander R ^e,f   Wythe, Joshua D ^b   Martin, James F ^a,b,c  

^a TEXAS HEART INSTITUTE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^d SHANGHAI CHILDREN S MEDICAL CENTER   (China)

^e UNIVERSITY OF KANSAS   (United States)

^f NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

Author keywords

epicardium; fibroblast differentiation; Hippo signaling; single cell RNA sequencing

Indexed keywords

DHRS3 PROTEIN; DPP4 PROTEIN; LATS1 KINASE; LATS2 KINASE; PHOSPHOTRANSFERASE; PROTEIN; UNCLASSIFIED DRUG; YAP PROTEIN; ALCOHOL DEHYDROGENASE; DHRS3 PROTEIN, MOUSE; DIPEPTIDYL PEPTIDASE IV; DPP4 PROTEIN, MOUSE; HIPPO PROTEIN, MOUSE; LATS1 PROTEIN, MOUSE; LATS2 PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL MUTANT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORONARY BLOOD VESSEL; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVITY; EPICARDIUM; EXTRACELLULAR MATRIX; FEMALE; GENE DELETION; HEART DEVELOPMENT; HEART FIBROBLAST; HIPPO SIGNALING; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA SEQUENCE; TRANSCRIPTOMICS; VASCULAR REMODELING; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; EMBRYOLOGY; FIBROBLAST; GENE EXPRESSION PROFILING; GENETICS; HEART; KNOCKOUT MOUSE; METABOLISM; ORGANOGENESIS; PERICARDIUM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALCOHOL OXIDOREDUCTASES; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DIPEPTIDYL PEPTIDASE 4; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; GENE EXPRESSION PROFILING; HEART; MICE; MICE, KNOCKOUT; ORGANOGENESIS; PERICARDIUM; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; TUMOR SUPPRESSOR PROTEINS;

EID: 85045577248     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2018.03.019     Document Type: Article

References (86)

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., Genove, G., Betsholtz, C., Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21 (2011), 193–215.
3. Billings, S.E., Pierzchalski, K., Butler Tjaden, N.E., Pang, X.Y., Trainor, P.A., Kane, M.A., Moise, A.R., The retinaldehyde reductase DHRS3 is essential for preventing the formation of excess retinoic acid during embryonic development. FASEB J. 27 (2013), 4877–4889.
4. Bosada, F.M., Devasthali, V., Jones, K.A., Stankunas, K., Wnt/beta-catenin signaling enables developmental transitions during valvulogenesis. Development 143 (2016), 1041–1054.
5. Braitsch, C.M., Combs, M.D., Quaggin, S.E., Yutzey, K.E., Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardium-derived cells into smooth muscle in the developing heart. Dev. Biol. 368 (2012), 345–357.
6. Cai, C.L., Martin, J.C., Sun, Y., Cui, L., Wang, L., Ouyang, K., Yang, L., Bu, L., Liang, X., Zhang, X., et al. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454 (2008), 104–108.
7. Cambier, L., Plate, M., Sucov, H.M., Pashmforoush, M., Nkx2-5 regulates cardiac growth through modulation of Wnt signaling by R-spondin3. Development 141 (2014), 2959–2971.
8. Campione, M., Ros, M.A., Icardo, J.M., Piedra, E., Christoffels, V.M., Schweickert, A., Blum, M., Franco, D., Moorman, A.F., Pitx2 expression defines a left cardiac lineage of cells: evidence for atrial and ventricular molecular isomerism in the iv/iv mice. Dev. Biol. 231 (2001), 252–264.
9. Cavallero, S., Shen, H., Yi, C., Lien, C.L., Kumar, S.R., Sucov, H.M., CXCL12 signaling is essential for maturation of the ventricular coronary endothelial plexus and establishment of functional coronary circulation. Dev. Cell 33 (2015), 469–477.
10. Choy, M., Lam, S., Sitagliptin: a novel drug for the treatment of type 2 diabetes. Cardiol. Rev. 15 (2007), 264–271.
11. + progenitor cells. J. Immunol. 169 (2002), 7000–7008.
12. Cruciat, C.M., Niehrs, C., Secreted and transmembrane wnt inhibitors and activators. Cold Spring Harb. Perspect. Biol., 5, 2013, a015081.
13. 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.
14. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
15. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. Role of YAP/TAZ in mechanotransduction. Nature 474 (2011), 179–183.
16. Dyer, L.A., Patterson, C., Isolation of embryonic ventricular endothelial cells. J. Vis. Exp., 2013, 10.3791/50463.
17. Fang, W., Hartmann, N., Chow, D.T., Riegel, A.T., Wellstein, A., Pleiotrophin stimulates fibroblasts and endothelial and epithelial cells and is expressed in human cancer. J. Biol. Chem. 267 (1992), 25889–25897.
18. Ghersi, G., Zhao, Q., Salamone, M., Yeh, Y., Zucker, S., Chen, W.T., The protease complex consisting of dipeptidyl peptidase IV and seprase plays a role in the migration and invasion of human endothelial cells in collagenous matrices. Cancer Res. 66 (2006), 4652–4661.
19. Gong, C., Qu, S., Lv, X.B., Liu, B., Tan, W., Nie, Y., Su, F., Liu, Q., Yao, H., Song, E., BRMS1L suppresses breast cancer metastasis by inducing epigenetic silence of FZD10. Nat. Commun., 5, 2014, 5406.
20. Guadix, J.A., Ruiz-Villalba, A., Lettice, L., Velecela, V., Munoz-Chapuli, R., Hastie, N.D., Perez-Pomares, J.M., Martinez-Estrada, O.M., Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 138 (2011), 1093–1097.
21. Habets, P.E., Moorman, A.F., Clout, D.E., van Roon, M.A., Lingbeek, M., van Lohuizen, M., Campione, M., Christoffels, V.M., Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev. 16 (2002), 1234–1246.
22. Halder, G., Johnson, R.L., Hippo signaling: growth control and beyond. Development 138 (2011), 9–22.
23. Hanna, M., Liu, H., Amir, J., Sun, Y., Morris, S.W., Siddiqui, M.A., Lau, L.F., Chaqour, B., Mechanical regulation of the proangiogenic factor CCN1/CYR61 gene requires the combined activities of MRTF-A and CREB-binding protein histone acetyltransferase. J. Biol. Chem. 284 (2009), 23125–23136.
24. Harrison, M.R., Bussmann, J., Huang, Y., Zhao, L., Osorio, A., Burns, C.G., Burns, C.E., Sucov, H.M., Siekmann, A.F., Lien, C.L., Chemokine-guided angiogenesis directs coronary vasculature formation in zebrafish. Dev. Cell 33 (2015), 442–454.
25. Hathaway, C.K., Grant, R., Hagaman, J.R., Hiller, S., Li, F., Xu, L., Chang, A.S., Madden, V.J., Bagnell, C.R., Rojas, M., et al. Endothelin-1 critically influences cardiac function via superoxide-MMP9 cascade. Proc. Natl. Acad. Sci. USA 112 (2015), 5141–5146.
26. He, L., Tian, X., Zhang, H., Wythe, J.D., Zhou, B., Fabp4-CreER lineage tracing reveals two distinctive coronary vascular populations. J. Cell. Mol. Med. 18 (2014), 2152–2156.
27. Heallen, T., Morikawa, Y., Leach, J., Tao, G., Willerson, J.T., Johnson, R.L., Martin, J.F., Hippo signaling impedes adult heart regeneration. Development 140 (2013), 4683–4690.
28. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R.L., Martin, J.F., Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332 (2011), 458–461.
29. Hindley, C.J., Condurat, A.L., Menon, V., Thomas, R., Azmitia, L.M., Davis, J.A., Pruszak, J., The Hippo pathway member YAP enhances human neural crest cell fate and migration. Sci. Rep., 6, 2016, 23208.
30. Hinkel, R., Trenkwalder, T., Petersen, B., Husada, W., Gesenhues, F., Lee, S., Hannappel, E., Bock-Marquette, I., Theisen, D., Leitner, L., et al. MRTF-A controls vessel growth and maturation by increasing the expression of CCN1 and CCN2. Nat. Commun., 5, 2014, 3970.
31. 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. C/EBP transcription factors mediate epicardial activation during heart development and injury. Science 338 (2012), 1599–1603.
32. Ito, S., Nagata, K., Biology of Hsp47 (Serpin H1), a collagen-specific molecular chaperone. Semin. Cell Dev. Biol. 62 (2017), 142–151.
33. Janky, R., Verfaillie, A., Imrichova, H., Van de Sande, B., Standaert, L., Christiaens, V., Hulselmans, G., Herten, K., Naval Sanchez, M., Potier, D., et al. iRegulon: from a gene list to a gene regulatory network using large motif and track collections. PLoS Comput. Biol., 10, 2014, e1003731.
34. Jensen, B., Boukens, B.J., Postma, A.V., Gunst, Q.D., van den Hoff, M.J., Moorman, A.F., Wang, T., Christoffels, V.M., Identifying the evolutionary building blocks of the cardiac conduction system. PLoS One, 7, 2012, e44231.
35. Jiang, R., Lan, Y., Norton, C.R., Sundberg, J.P., Gridley, T., The Slug gene is not essential for mesoderm or neural crest development in mice. Dev. Biol. 198 (1998), 277–285.
36. Jiang, X., Rowitch, D.H., Soriano, P., McMahon, A.P., Sucov, H.M., Fate of the mammalian cardiac neural crest. Development 127 (2000), 1607–1616.
37. Katz, T.C., Singh, M.K., Degenhardt, K., Rivera-Feliciano, J., Johnson, R.L., Epstein, J.A., Tabin, C.J., Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 22 (2012), 639–650.
38. Khurana, S., Margamuljana, L., Joseph, C., Schouteden, S., Buckley, S.M., Verfaillie, C.M., Glypican-3-mediated inhibition of CD26 by TFPI: a novel mechanism in hematopoietic stem cell homing and maintenance. Blood 121 (2013), 2587–2595.
39. Leek, J.T., Johnson, W.E., Parker, H.S., Jaffe, A.E., Storey, J.D., The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics 28 (2012), 882–883.
40. Lepilina, A., Coon, A.N., Kikuchi, K., Holdway, J.E., Roberts, R.W., Burns, C.G., Poss, K.D., A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127 (2006), 607–619.
41. Li, G., Xu, A., Sim, S., Priest, J.R., Tian, X., Khan, T., Quertermous, T., Zhou, B., Tsao, P.S., Quake, S.R., et al. Transcriptomic profiling maps anatomically patterned subpopulations among single embryonic cardiac cells. Dev. Cell 39 (2016), 491–507.
42. Li, P., Cavallero, S., Gu, Y., Chen, T.H., Hughes, J., Hassan, A.B., Bruning, J.C., Pashmforoush, M., Sucov, H.M., IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138 (2011), 1795–1805.
43. Liebner, S., Cattelino, A., Gallini, R., Rudini, N., Iurlaro, M., Piccolo, S., Dejana, E., Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J. Cell Biol. 166 (2004), 359–367.
44. Liu, Q., Hu, T., He, L., Huang, X., Tian, X., Zhang, H., He, L., Pu, W., Zhang, L., Sun, H., et al. Genetic targeting of sprouting angiogenesis using Apln-CreER. Nat. Commun., 6, 2015, 6020.
45. Lu, M.H., Huang, C.C., Pan, M.R., Chen, H.H., Hung, W.C., Prospero homeobox 1 promotes epithelial-mesenchymal transition in colon cancer cells by inhibiting E-cadherin via miR-9. Clin. Cancer Res. 18 (2012), 6416–6425.
46. Ma, L., Lu, M.F., Schwartz, R.J., Martin, J.F., Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132 (2005), 5601–5611.
47. Maaten, L., Hinton, G., Visualizing data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
48. 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.
49. Majkut, S., Idema, T., Swift, J., Krieger, C., Liu, A., Discher, D.E., Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 23 (2013), 2434–2439.
50. 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.
51. McKean, D.M., Homsy, J., Wakimoto, H., Patel, N., Gorham, J., DePalma, S.R., Ware, J.S., Zaidi, S., Ma, W., Patel, N., et al. Loss of RNA expression and allele-specific expression associated with congenital heart disease. Nat. Commun., 7, 2016, 12824.
52. Morikawa, Y., Zhang, M., Heallen, T., Leach, J., Tao, G., Xiao, Y., Bai, Y., Li, W., Willerson, J.T., Martin, J.F., Actin cytoskeletal remodeling with protrusion formation is essential for heart regeneration in Hippo-deficient mice. Sci. Signal., 8, 2015, ra41.
53. Mukouyama, Y.S., James, J., Nam, J., Uchida, Y., Whole-mount confocal microscopy for vascular branching morphogenesis. Methods Mol. Biol. 843 (2012), 69–78.
54. Muzumdar, M.D., Tasic, B., Miyamichi, K., Li, L., Luo, L., A global double-fluorescent Cre reporter mouse. Genesis 45 (2007), 593–605.
55. Nusse, R., Clevers, H., Wnt/beta-Catenin signaling, disease, and emerging therapeutic modalities. Cell 169 (2017), 985–999.
56. Ou, X., O'Leary, H.A., Broxmeyer, H.E., Implications of DPP4 modification of proteins that regulate stem/progenitor and more mature cell types. Blood 122 (2013), 161–169.
57. 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., et al. Revisiting cardiac cellular composition. Circ. Res. 118 (2016), 400–409.
58. Puig-Hervas, M.T., Temtamy, S., Aglan, M., Valencia, M., Martinez-Glez, V., Ballesta-Martinez, M.J., Lopez-Gonzalez, V., Ashour, A.M., Amr, K., Pulido, V., et al. Mutations in PLOD2 cause autosomal-recessive connective tissue disorders within the Bruck syndrome–osteogenesis imperfecta phenotypic spectrum. Hum. Mutat. 33 (2012), 1444–1449.
59. Qiu, X., Hill, A., Packer, J., Lin, D., Ma, Y.A., Trapnell, C., Single-cell mRNA quantification and differential analysis with Census. Nat. Methods 14 (2017), 309–315.
60. Ramjee, V., Li, D., Manderfield, L.J., Liu, F., Engleka, K.A., Aghajanian, H., Rodell, C.B., Lu, W., Ho, V., Wang, T., et al. Epicardial YAP/TAZ orchestrate an immunosuppressive response following myocardial infarction. J. Clin. Invest. 127 (2017), 899–911.
61. Red-Horse, K., Ueno, H., Weissman, I.L., Krasnow, M.A., Coronary arteries form by developmental reprogramming of venous cells. Nature 464 (2010), 549–553.
62. Rudat, C., Grieskamp, T., Rohr, C., Airik, R., Wrede, C., Hegermann, J., Herrmann, B.G., Schuster-Gossler, K., Kispert, A., Upk3b is dispensable for development and integrity of urothelium and mesothelium. PLoS One, 9, 2014, e112112.
63. Rudat, C., Kispert, A., Wt1 and epicardial fate mapping. Circ. Res. 111 (2012), 165–169.
64. Rutkovskiy, A., Valen, G., Vaage, J., Cardiac aquaporins. Basic Res. Cardiol., 108, 2013, 393.
65. Salazar, V.S., Gamer, L.W., Rosen, V., BMP signalling in skeletal development, disease and repair. Nat. Rev. Endocrinol. 12 (2016), 203–221.
66. Satija, R., Farrell, J.A., Gennert, D., Schier, A.F., Regev, A., Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33 (2015), 495–502.
67. Shamloo, A., Mohammadaliha, N., Heilshorn, S.C., Bauer, A.L., A comparative study of collagen matrix density effect on endothelial sprout formation using experimental and computational approaches. Ann. Biomed. Eng. 44 (2016), 929–941.
68. Shaul, Y.D., Freinkman, E., Comb, W.C., Cantor, J.R., Tam, W.L., Thiru, P., Kim, D., Kanarek, N., Pacold, M.E., Chen, W.W., et al. Dihydropyrimidine accumulation is required for the epithelial-mesenchymal transition. Cell 158 (2014), 1094–1109.
69. Shekhar, K., Lapan, S.W., Whitney, I.E., Tran, N.M., Macosko, E.Z., Kowalczyk, M., Adiconis, X., Levin, J.Z., Nemesh, J., Goldman, M., et al. Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell 166 (2016), 1308–1323.e30.
70. Singh, A., Ramesh, S., Cibi, D.M., Yun, L.S., Li, J., Li, L., Manderfield, L.J., Olson, E.N., Epstein, J.A., Singh, M.K., Hippo signaling mediators Yap and Taz are required in the epicardium for coronary vasculature development. Cell Rep. 15 (2016), 1384–1393.
71. Singhal, N., Martin, P.T., A role for Galgt1 in skeletal muscle regeneration. Skelet. Muscle, 5, 2015, 3.
72. Skelly, D.A., Squiers, G.T., McLellan, M.A., Bolisetty, M.T., Robson, P., Rosenthal, N.A., Pinto, A.R., Single-cell transcriptional profiling reveals cellular diversity and intercommunication in the mouse heart. Cell Rep. 22 (2018), 600–610.
73. Smart, N., Bollini, S., Dubé K.N., Vieira, J.M., Zhou, B., Davidson, S., Yellon, D., Riegler, J., Price, A.N., Lythgoe, M.F., et al. De novo cardiomyocytes from within the activated adult heart after injury. Nature 474 (2011), 640–644.
74. Sridurongrit, S., Larsson, J., Schwartz, R., Ruiz-Lozano, P., Kaartinen, V., Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev. Biol. 322 (2008), 208–218.
75. Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N.J., Livak, K.J., Mikkelsen, T.S., Rinn, J.L., The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32 (2014), 381–386.
76. Tripathi, S., Pohl, M.O., Zhou, Y., Rodriguez-Frandsen, A., Wang, G., Stein, D.A., Moulton, H.M., DeJesus, P., Che, J., Mulder, L.C., et al. Meta- and orthogonal integration of influenza “OMICs” data defines a role for UBR4 in virus budding. Cell Host Microbe 18 (2015), 723–735.
77. Tse, J.R., Engler, A.J., Preparation of hydrogel substrates with tunable mechanical properties. Curr. Protoc. Cell Biol., Chapter 10, 2010 Unit 10 16.
78. Ulmer, B., Hagenlocher, C., Schmalholz, S., Kurz, S., Schweickert, A., Kohl, A., Roth, L., Sela-Donenfeld, D., Blum, M., Calponin 2 acts as an effector of noncanonical Wnt-mediated cell polarization during neural crest cell migration. Cell Rep. 3 (2013), 615–621.
79. Viragh, S., Challice, C.E., The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec. 201 (1981), 157–168.
80. Volz, K.S., Jacobs, A.H., Chen, H.I., Poduri, A., McKay, A.S., Riordan, D.P., Kofler, N., Kitajewski, J., Weissman, I., Red-Horse, K., Pericytes are progenitors for coronary artery smooth muscle. Elife, 4, 2015, 10.7554/eLife.10036.
81. Wang, S., Yu, J., Jones, J.W., Pierzchalski, K., Kane, M.A., Trainor, P.A., Xavier-Nieto, J., Moise, A.R., Retinoic acid signaling promotes the cytoskeleton rearrangement of embryonic epicardial cells. FASEB J., 2018, 10.1096/fj.201701038R.
82. Wessels, A., Perez-Pomares, J.M., The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 276 (2004), 43–57.
83. Xin, M., Kim, Y., Sutherland, L.B., Qi, X., McAnally, J., Schwartz, R.J., Richardson, J.A., Bassel-Duby, R., Olson, E.N., Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci. Signal., 4, 2011, ra70.
84. Zhang, H., Pu, W., Li, G., Huang, X., He, L., Tian, X., Liu, Q., Zhang, L., Wu, S.M., Sucov, H.M., et al. Endocardium minimally contributes to coronary endothelium in the embryonic ventricular free walls. Circ. Res. 118 (2016), 1880–1893.
85. 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. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 121 (2011), 1894–1904.
86. Zhou, B., Ma, Q., Rajagopal, S., Wu, S.M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K.R., et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454 (2008), 109–113.