Endothelial cells are progenitors of cardiac pericytes and vascular smooth muscle cells

Nature Communications

Volumn 7, Issue , 2016, Pages

  Chen, Qi ^a   Zhang, Hui ^b   Liu, Yang ^a   Adams, Susanne ^a   Eilken, Hanna ^a   Stehling, Martin ^c   Corada, Monica ^d   Dejana, Elisabetta ^d,e   Zhou, Bin ^b   Adams, Ralf H ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Chinese Academy of Sciences   (China)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; FRIZZLED 4 PROTEIN; FRIZZLED PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CELLS AND CELL COMPONENTS; GROWTH; MUSCLE; PHYSIOLOGY; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC MUSCLE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; CORONARY BLOOD VESSEL; DEVELOPMENTAL STAGE; EMBRYO; ENDOCARDIUM; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HEART; HEART FUNCTION; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PERICYTE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; VASCULAR ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE CELL; WNT SIGNALING PATHWAY; ANIMAL; ANIMAL MODEL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; SMOOTH MUSCLE CELL; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE;

MURINAE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOCARDIUM; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEART; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, ANIMAL; MUSCLE, SMOOTH, VASCULAR; MYOCARDIUM; MYOCYTES, SMOOTH MUSCLE; PERICYTES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA;

EID: 84982313678     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12422     Document Type: Article

References (70)

1. Hill, J. A. & Olson, E. N. Cardiac plasticity. N. Engl. J. Med. 358, 1370-1380 (2008).
2. Kathiresan, S. & Srivastava, D. Genetics of human cardiovascular disease. Cell 148, 1242-1257 (2012).
3. Daneman, R., Zhou, L., Kebede, A. A. & Barres, B. A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468, 562-566 (2010).
4. Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
5. Hall, C. N. et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508, 55-60 (2014).
6. Hill, R. A. et al. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron 87, 95-110 (2015).
7. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2011).
8. Volz, K. S. et al. Pericytes are progenitors for coronary artery smooth muscle. eLife 4, e10036 (2015).
9. Adams, R. H. & Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478 (2007).
10. Campagnolo, P. et al. Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121, 1735-1745 (2010).
11. Avolio, E. et al. Combined intramyocardial delivery of human pericytes and cardiac stem cells additively improves the healing of mouse infarcted hearts through stimulation of vascular and muscular repair. Circ. Res. 116, e81-e94 (2015).
12. Avolio, E. et al. Expansion and characterization of neonatal cardiac pericytes provides a novel cellular option for tissue engineering in congenital heart disease. J. Am. Heart Assoc. 4, e002043 (2015).
13. Katare, R. et al. Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132. Circ. Res. 109, 894-906 (2011).
14. Chen, W. C. et al. Human myocardial pericytes: multipotent mesodermal precursors exhibiting cardiac specificity. Stem Cells 33, 557-573 (2015).
15. Chen, C. W. et al. Human pericytes for ischemic heart repair. Stem Cells 31, 305-316 (2013).
16. Kramann, R. et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 16, 51-66 (2015).
17. Crisan, M. et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313 (2008).
18. Crisan, M., Corselli, M., Chen, W. C. & Peault, B. Perivascular cells for regenerative medicine. J. Cell Mol. Med. 16, 2851-2860 (2012).
19. Cai, C. L. et al. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454, 104-108 (2008).
20. Zhou, B. et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454, 109-113 (2008).
21. Mellgren, A. M. et al. Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 103, 1393-1401 (2008).
22. Smith, C. L., Baek, S. T., Sung, C. Y. & Tallquist, M. D. Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ. Res. 108, e15-e26 (2011).
23. de Lange, F. J. et al. Lineage and morphogenetic analysis of the cardiac valves. Circ. Res. 95, 645-654 (2004).
24. Etchevers, H. C., Vincent, C., Le Douarin, N. M. & Couly, G. F. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128, 1059-1068 (2001).
25. Tian, X. et al. Vessel formation. De novo formation of a distinct coronary vascular population in neonatal heart. Science 345, 90-94 (2014).
26. Tian, X. et al. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 23, 1075-1090 (2013).
27. Chen, H. I. et al. The sinus venosus contributes to coronary vasculature through VEGFC-stimulated angiogenesis. Development 141, 4500-4512 (2014).
28. Wu, B. et al. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell 151, 1083-1096 (2012).
29. Lamouille, S., Xu, J. & Derynck, R. Molecular mechanisms of epithelial mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196 (2014).
30. Sanz, E. et al. Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc. Natl Acad. Sci. USA 106, 13939-13944 (2009).
31. Lin, C. J., Lin, C. Y., Chen, C. H., Zhou, B. & Chang, C. P. Partitioning the heart: mechanisms of cardiac septation and valve development. Development 139, 3277-3299 (2012).
32. Liebner, S. et al. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. The Journal of Cell Biology 166, 359-367 (2004).
33. Niehrs, C. The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol. 13, 767-779 (2012).
34. Clevers, H., Loh, K. M. & Nusse, R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 1248012 (2014).
35. Song, S., Ewald, A. J., Stallcup, W., Werb, Z. & Bergers, G. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat. Cell Biol. 7, 870-879 (2005).
36. Trost, A. et al. Neural crest origin of retinal and choroidal pericytes. Invest. Ophthalmol. Vis. Sci. 54, 7910-7921 (2013).
37. Zachariah, M. A. & Cyster, J. G. Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328, 1129-1135 (2010).
38. Muller, S. M. et al. Neural crest origin of perivascular mesenchyme in the adult thymus. J. Immunol. 180, 5344-5351 (2008).
39. Foster, K. et al. Contribution of neural crest-derived cells in the embryonic and adult thymus. J. Immunol. 180, 3183-3189 (2008).
40. Que, J. et al. Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc. Natl Acad. Sci. USA 105, 16626-16630 (2008).
41. Asahina, K., Zhou, B., Pu, W. T. & Tsukamoto, H. Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53, 983-995 (2011).
42. Chien, K. R., Domian, I. J. & Parker, K. K. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 322, 1494-1497 (2008).
43. Red-Horse, K., Ueno, H., Weissman, I. L. & Krasnow, M. A. Coronary arteries form by developmental reprogramming of venous cells. Nature 464, 549-553 (2010).
44. Luxan, G., D'Amato, G., MacGrogan, D. & de la Pompa, J. L. Endocardial notch signaling in cardiac development and disease. Circ. Res. 118, e1-e18 (2016).
45. Cai, X. et al. Tbx20 acts upstream of Wnt signaling to regulate endocardial cushion formation and valve remodeling during mouse cardiogenesis. Development 140, 3176-3187 (2013).
46. Hurlstone, A. F. et al. The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 425, 633-637 (2003).
47. Yuan, K. et al. Activation of the Wnt/planar cell polarity pathway is required for pericyte recruitment during pulmonary angiogenesis. Am. J. Pathol. 185, 69-84 (2015).
48. Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E. & Speck, N. A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457, 887-891 (2009).
49. Kissa, K. & Herbomel, P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115 (2010).
50. Bertrand, J. Y. et al. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111 (2010).
51. Boisset, J. C. et al. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120 (2010).
52. Zhu, P. et al. Transdifferentiation of pulmonary arteriolar endothelial cells into smooth muscle-like cells regulated by myocardin involved in hypoxia-induced pulmonary vascular remodelling. Int. J. Exp. Pathol. 87, 463-474 (2006).
53. Frid, M. G., Kale, V. A. & Stenmark, K. R. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circ. Res. 90, 1189-1196 (2002).
54. Qiao, L. et al. Endothelial fate mapping in mice with pulmonary hypertension. Circulation 129, 692-703 (2014).
55. Cooley, B. C. et al. TGF-beta signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling. Sci. Transl. Med. 6, 227ra234 (2014).
56. Ubil, E. et al. Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature 514, 585-590 (2014).
57. Medici, D. et al. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 16, 1400-1406 (2010).
58. Zeisberg, E. M. et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 13, 952-961 (2007).
59. Chen, Q. et al. Haemodynamics-driven developmental pruning of brain vasculature in zebrafish. PLoS Biol. 10, e1001374 (2012).
60. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
61. 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, 4013-4025 (2003).
62. Zhu, X., Bergles, D. E. & Nishiyama, A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145-157 (2008).
63. Ye, X. et al. Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization. Cell 139, 285-298 (2009).
64. Brault, V. et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (2001).
65. Carpenter, A. C., Rao, S., Wells, J. M., Campbell, K. & Lang, R. A. Generation of mice with a conditional null allele for Wntless. Genesis 48, 554-558 (2010).
66. Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486 (2010).
67. Maretto, S. et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl Acad. Sci. USA 100, 3299-3304 (2003).
68. Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242 (2001).
69. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. & McMahon, A. P. Modification of gene activity in mouse embryos in utero by a tamoxifeninducible form of Cre recombinase. Curr. Biol. 8, 1323-1326 (1998).
70. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140 (2010).