The CXCL12/CXCR4 Axis Plays a Critical Role in Coronary Artery Development

Developmental Cell

Volumn 33, Issue 4, 2015, Pages 455-468

  Ivins, Sarah ^a   Chappell, Joel ^a   Vernay, Bertrand ^a   Suntharalingham, Jenifer ^a   Martineau, Alexandrine ^b   Mohun, Timothy J ^b   Scambler, Peter J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CRE RECOMBINASE; NOTCH1 RECEPTOR; STROMAL CELL DERIVED FACTOR 1; CXCL12 PROTEIN, MOUSE; CXCR4 PROTEIN, MOUSE;

ANIMAL TISSUE; ANTIBODY LABELING; AORTA ENDOTHELIUM; AORTA VALVE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORONARY ARTERY; CORONARY BLOOD VESSEL; DEVELOPMENTAL STAGE; EMBRYO; ENDOTHELIUM CELL; GENE MUTATION; HEART DEVELOPMENT; HEART VENTRICLE WALL; HETEROZYGOTE; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PULMONARY VALVE; SIGNAL TRANSDUCTION; TUNICA MEDIA; VASCULAR SMOOTH MUSCLE CELL; VASCULARIZATION; ANIMAL; ANIMAL EMBRYO; AORTA; CELL CULTURE; CYTOLOGY; EMBRYOLOGY; FEMALE; HEART; KNOCKOUT MOUSE; MALE; METABOLISM; ORGANOGENESIS; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

MURINAE;

ANIMALS; AORTA; CELLS, CULTURED; CHEMOKINE CXCL12; CORONARY VESSELS; EMBRYO, MAMMALIAN; ENDOTHELIUM, VASCULAR; FEMALE; HEART; IN SITU HYBRIDIZATION; MALE; MICE; MICE, KNOCKOUT; ORGANOGENESIS; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84929914270     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.03.026     Document Type: Article

References (61)

1. Aikawa E., Kawano J. Formation of coronary arteries sprouting from the primitive aortic sinus wall of the chick embryo. Experientia 1982, 38:816-818.
2. Anastasia A., Deinhardt K., Wang S., Martin L., Nichol D., Irmady K., Trinh J., Parada L., Rafii S., Hempstead B.L., Kermani P. Trkb signaling in pericytes is required for cardiac microvessel stabilization. PLoS ONE 2014, 9:e87406.
3. Ando K., Nakajima Y., Yamagishi T., Yamamoto S., Nakamura H. Development of proximal coronary arteries in quail embryonic heart:multiple capillaries penetrating the aortic sinus fuse to form main coronary trunk. Circ. Res. 2004, 94:346-352.
4. Ara T., Nakamura Y., Egawa T., Sugiyama T., Abe K., Kishimoto T., Matsui Y., Nagasawa T. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc. Natl. Acad. Sci. USA 2003, 100:5319-5323.
5. Ara T., Tokoyoda K., Okamoto R., Koni P.A., Nagasawa T. The role of CXCL12 in the organ-specific process of artery formation. Blood 2005, 105:3155-3161.
6. Balabanian K., Lagane B., Infantino S., Chow K.Y., Harriague J., Moepps B., Arenzana-Seisdedos F., Thelen M., Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J.Biol. Chem. 2005, 280:35760-35766.
7. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J.Neurosci. 2005, 25:3995-4003.
8. Bernanke D.H., Velkey J.M. Development of the coronary blood supply: changing concepts and current ideas. Anat. Rec. 2002, 269:198-208.
9. Bogers A.J., Gittenberger-de Groot A.C., Poelmann R.E., Péault B.M., Huysmans H.A. Development of the origin of the coronary arteries, a matter of ingrowth or outgrowth?. Anat. Embryol. (Berl.) 1989, 180:437-441.
10. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., Penfold M.E., Sunshine M.J., Littman D.R., Kuo C.J., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J.Exp. Med. 2006, 203:2201-2213.
11. Chen H.I., Poduri A., Numi H., Kivela R., Saharinen P., McKay A.S., Raftrey B., Churko J., Tian X., Zhou B., et al. VEGF-C and aortic cardiomyocytes guide coronary artery stem development. J.Clin. Invest. 2014, 124:4899-4914.
12. Chen H.I., Sharma B., Akerberg B.N., Numi H.J., Kivelä R., Saharinen P., Aghajanian H., McKay A.S., Bogard P.E., Chang A.H., et al. The sinus venosus contributes to coronary vasculature through VEGFC-stimulated angiogenesis. Development 2014, 141:4500-4512.
13. del Monte G., Casanova J.C., Guadix J.A., MacGrogan D., Burch J.B., Pérez-Pomares J.M., de la Pompa J.L. Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ. Res. 2011, 108:824-836.
14. Escot S., Blavet C., Härtle S., Duband J.L., Fournier-Thibault C. Misregulation of SDF1-CXCR4 signaling impairs early cardiac neural crest cell migration leading to conotruncal defects. Circ. Res. 2013, 113:505-516.
15. Fernández B., Durán A.C., Fernández M.C., Fernández-Gallego T., Icardo J.M., Sans-Coma V. The coronary arteries of the C57BL/6 mouse strains: implications for comparison with mutant models. J.Anat. 2008, 212:12-18.
16. González-Iriarte M., Carmona R., Pérez-Pomares J.M., Macías D., Costell M., Muñoz-Chápuli R. Development of the coronary arteries in a murine model of transposition of great arteries. J.Mol. Cell. Cardiol. 2003, 35:795-802.
17. Greenbaum A., Hsu Y.M., Day R.B., Schuettpelz L.G., Christopher M.J., Borgerding J.N., Nagasawa T., Link D.C. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013, 495:227-230.
18. Hauser M. Congenital anomalies of the coronary arteries. Heart 2005, 91:1240-1245.
19. Holtwick R., Gotthardt M., Skryabin B., Steinmetz M., Potthast R., Zetsche B., Hammer R.E., Herz J., Kuhn M. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc. Natl. Acad. Sci. USA 2002, 99:7142-7147.
20. Jones E.A., le Noble F., Eichmann A. What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology (Bethesda) 2006, 21:388-395.
21. Kasemeier-Kulesa J.C., McLennan R., Romine M.H., Kulesa P.M., Lefcort F. CXCR4 controls ventral migration of sympathetic precursor cells. J.Neurosci. 2010, 30:13078-13088.
22. Kattan J., Dettman R.W., Bristow J. Formation and remodeling of the coronary vascular bed in the embryonic avian heart. Dev. Dyn. 2004, 230:34-43.
23. 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 2012, 22:639-650.
24. Kiefer F., Siekmann A.F. The role of chemokines and their receptors in angiogenesis. Cell. Mol. Life Sci. 2011, 68:2811-2830.
25. Kisanuki Y.Y., Hammer R.E., Miyazaki J., Williams S.C., Richardson J.A., Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis invivo. Dev. Biol. 2001, 230:230-242.
26. Li W., Kohara H., Uchida Y., James J.M., Soneji K., Cronshaw D.G., Zou Y.R., Nagasawa T., Mukouyama Y.S. Peripheral nerve-derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev. Cell 2013, 24:359-371.
27. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 1998, 95:9448-9453.
28. Ma Q., Zhou B., Pu W.T. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev. Biol. 2008, 323:98-104.
29. Mikawa T., Fischman D.A. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc. Natl. Acad. Sci. USA 1992, 89:9504-9508.
30. Mohun T.J., Weninger W.J. Episcopic three-dimensional imaging of embryos. Cold Spring Harb. Protoc. 2012, 2012:641-646.
31. Morabito C.J., Kattan J., Bristow J. Mechanisms of embryonic coronary artery development. Curr. Opin. Cardiol. 2002, 17:235-241.
32. Moses K.A., DeMayo F., Braun R.M., Reecy J.L., Schwartz R.J. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 2001, 31:176-180.
33. Nagasawa T., Hirota S., Tachibana K., Takakura N., Nishikawa S., Kitamura Y., Yoshida N., Kikutani H., Kishimoto T. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382:635-638.
34. Nie Y., Waite J., Brewer F., Sunshine M.J., Littman D.R., Zou Y.R. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J.Exp. Med. 2004, 200:1145-1156.
35. Petit I., Jin D., Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol. 2007, 28:299-307.
36. Poelmann R.E., Gittenberger-de Groot A.C., Mentink M.M., Bökenkamp R., Hogers B. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ. Res. 1993, 73:559-568.
37. Ramsbottom S.A., Sharma V., Rhee H.J., Eley L., Phillips H.M., Rigby H.F., Dean C., Chaudhry B., Henderson D.J. Vangl2-regulated polarisation of second heart field-derived cells is required for outflow tract lengthening during cardiac development. PLoS Genet. 2014, 10:e1004871.
38. Ratajska A., Fiejka E. Prenatal development of coronary arteries in the rat: morphologic patterns. Anat. Embryol. (Berl.) 1999, 200:533-540.
39. Red-Horse K., Ueno H., Weissman I.L., Krasnow M.A. Coronary arteries form by developmental reprogramming of venous cells. Nature 2010, 464:549-553.
40. Sierro F., Biben C., Martínez-Muñoz L., Mellado M., Ransohoff R.M., Li M., Woehl B., Leung H., Groom J., Batten M., et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA 2007, 104:14759-14764.
41. Song N., Huang Y., Shi H., Yuan S., Ding Y., Song X., Fu Y., Luo Y. Overexpression of platelet-derived growth factor-BB increases tumor pericyte content via stromal-derived factor-1alpha/CXCR4 axis. Cancer Res. 2009, 69:6057-6064.
42. Tachibana K., Hirota S., Iizasa H., Yoshida H., Kawabata K., Kataoka Y., Kitamura Y., Matsushima K., Yoshida N., Nishikawa S., et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 1998, 393:591-594.
43. Takabatake Y., Sugiyama T., Kohara H., Matsusaka T., Kurihara H., Koni P.A., Nagasawa Y., Hamano T., Matsui I., Kawada N., et al. The CXCL12 (SDF-1)/CXCR4 axis is essential for the development of renal vasculature. J.Am. Soc. Nephrol. 2009, 20:1714-1723.
44. Teicher B.A., Fricker S.P. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin. Cancer Res. 2010, 16:2927-2931.
45. Theveneau E., Marchant L., Kuriyama S., Gull M., Moepps B., Parsons M., Mayor R. Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 2010, 19:39-53.
46. Tian X., Hu T., He L., Zhang H., Huang X., Poelmann R.E., Liu W., Yang Z., Yan Y., Pu W.T., Zhou B. Peritruncal coronary endothelial cells contribute to proximal coronary artery stems and their aortic orifices in the mouse heart. PLoS ONE 2013, 8:e80857.
47. Tian X., Hu T., Zhang H., He L., Huang X., Liu Q., Yu W., He L., Yang Z., Zhang Z., et al. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 2013, 23:1075-1090.
48. Tomanek R.J. Formation of the coronary vasculature during development. Angiogenesis 2005, 8:273-284.
49. Tomanek R.J., Holifield J.S., Reiter R.S., Sandra A., Lin J.J. Role of VEGF family members and receptors in coronary vessel formation. Dev. Dyn. 2002, 225:233-240.
50. Tomanek R.J., Ishii Y., Holifield J.S., Sjogren C.L., Hansen H.K., Mikawa T. VEGF family members regulate myocardial tubulogenesis and coronary artery formation in the embryo. Circ. Res. 2006, 98:947-953.
51. Tomanek R.J., Hansen H.K., Christensen L.P. Temporally expressed PDGF and FGF-2 regulate embryonic coronary artery formation and growth. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1237-1243.
52. Van den Akker N.M., Winkel L.C., Nisancioglu M.H., Maas S., Wisse L.J., Armulik A., Poelmann R.E., Lie-Venema H., Betsholtz C., Gittenberger-de Groot A.C. PDGF-B signaling is important for murine cardiac development: its role in developing atrioventricular valves, coronaries, and cardiac innervation. Dev. Dyn. 2008, 237:494-503.
53. Verzi M.P., McCulley D.J., De Val S., Dodou E., Black B.L. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 2005, 287:134-145.
54. Vrancken Peeters M.P., Gittenberger-de Groot A.C., Mentink M.M., Hungerford J.E., Little C.D., Poelmann R.E. The development of the coronary vessels and their differentiation into arteries and veins in the embryonic quail heart. Dev. Dyn. 1997, 208:338-348.
55. Waldo K.L., Willner W., Kirby M.L. Origin of the proximal coronary artery stems and a review of ventricular vascularization in the chick embryo. Am. J. Anat. 1990, 188:109-120.
56. Wesselhoeft H., Fawcett J.S., Johnson A.L. Anomalous origin of the left coronary artery from the pulmonary trunk. Its clinical spectrum, pathology, and pathophysiology, based on a review of 140 cases with seven further cases. Circulation 1968, 38:403-425.
57. Wu B., Zhang Z., Lui W., Chen X., Wang Y., Chamberlain A.A., Moreno-Rodriguez R.A., Markwald R.R., O'Rourke B.P., Sharp D.J., et al. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell 2012, 151:1083-1096.
58. Yu S., Crawford D., Tsuchihashi T., Behrens T.W., Srivastava D. The chemokine receptor CXCR7 functions to regulate cardiac valve remodeling. Dev. Dyn. 2011, 240:384-393.
59. Zangi L., Lui K.O., von Gise A., Ma Q., Ebina W., Ptaszek L.M., Später D., Xu H., Tabebordbar M., Gorbatov R., et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol. 2013, 31:898-907.
60. Zernecke A., Schober A., Bot I., von Hundelshausen P., Liehn E.A., Möpps B., Mericskay M., Gierschik P., Biessen E.A., Weber C. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ. Res. 2005, 96:784-791.
61. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.