Cellular phenotypes and spatio-temporal patterns of lymphatic vessel development in embryonic mouse hearts

Developmental Dynamics

Volumn 241, Issue 9, 2012, Pages 1473-1486

  Flaht, A ^a   Jankowska Steifer, E ^a   Radomska, D M ^a   Madej, M ^a   Gula, G ^a   Kujawa, M ^a   Ratajska, A ^a  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Cardiac lymphangiogenesis; CD11b; CD31; CD45; CD68; F4 80; Flk 1; Lymphangioblasts; Lyve 1; Mouse embryonic heart; Prox 1

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CD68 ANTIGEN; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL MATURATION; CONTROLLED STUDY; HEART DEVELOPMENT; LYMPHANGIOGENESIS; MEDIASTINUM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; BODY PATTERNING; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HEART; HOMEODOMAIN PROTEINS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MODELS, BIOLOGICAL; MYOCARDIUM; ORGANOGENESIS; PHENOTYPE; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84865349160     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23827     Document Type: Article

References (80)

1. Albelda SM, Muller WA, Buck CA, Newman PJ. 1991. Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 114: 1059-1068.
2. Albrecht I, Christophori G. 2011. Molecular mechanisms of lymphangiogenesis in development and cancer. Int J Dev Biol 55: 483-494.
3. Arnaout MA. 1990. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75: 1037-1050.
4. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, Hicklin DJ, Jeltsch M, Petrova TV, Pytowski B, Stacker SA, Ylä-Herttuala S, Jackson DG, Alitalo K, McDonald DM. 2005. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115: 247-257.
5. Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM. 2007. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med 204: 2349-2362.
6. Banerji S, Ni J, Wang S-X, Clasper S, Su J, Tammi R, Jones M, Jackson DG. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronian. J Cell Biol 144: 789-801.
7. Boensch C, Kuo MD, Connolly DT, Huang SS, Huang JS. 1995. Identification, purification, and characterization of cell-surface retention sequence-binding proteins from human SK-Hep cells and bovine liver plasma membranes. J Biol Chem 270: 1807-1816.
8. Burgio VL, Zupo S, Roncella S, Zocchi M, Ruco LP, Baroni CD. 1994. Characterization of EN4 monoclonal antibody: a reagent with CD31 specificity. Clin Exp Immunol 96: 170-176.
9. Burke Z, Oliver G. 2002. Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech Dev 118: 147-155.
10. Butler MG, Isogai S, Weinstein BM. 2009. Lymphatic development. Birth Defects Res C 87: 222-231.
11. Buttler K, Kreysing A, von Kaisenberg CS, Schweigerer L, Gale N, Papoutsi M, Wilting J. 2006. Mesenchymal cells with leukocyte and lymphendothelial characteristics in murine embryos. Dev Dyn 235: 1554-1562.
12. Buttler K, Ezaki T, Wilting J. 2008. Proliferating mesodermal cells in murine embryos exhibiting macrophage and lymphoendothelial characterisctics. BMC Dev Biol 8: 43.
13. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq D, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
14. Cho C-H, Koh YJ, Han J, Sung H-K, Lee HJ, Morisada T, Schwendener RA, Brekken RA, Kang G, Oike Y, Choi T-S, Suda T, Yoo O-J, Koh GY. 2007. Angiogenic role of Lyve-1-positive macrophages in adipose tissue. Circ Res 100: e47-e57.
15. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ, Streilein JW. 2004. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113: 1040-1050.
16. Damert A, Miquerol L, Gertsenstein M, Risau W, Nagy A. 2002. Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 129: 1881-1892.
17. De Beer MC, Zhao Z, Webb NR, van der Westhuyzen DR, de Villiers WJ. 2003. Lack of a direct role for macrosialin in oxidized LDL metabolism. J Lipid Res 44: 674-685.
18. Dent JA, Polson AG, Klymkowsky MW. 1989. A whole-mount immunohistochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development 105: 61-74.
19. Eichmann A, Corbel C, Nataf V, Vaigot P, Breant C, Le Douarin NM. 1997. Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci USA 94: 5141-5146.
20. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442.
21. Flotte TJ, Springer TA, Thorbecke GJ. 1983. Dentritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets. Am J Pathol 111: 112-124.
22. Gahmberg CG, Valmu L, Fagerholm S, Kotovuori P, Ihanus E, Tian L, Pessa-Morikawa T. 1998. Leukocyte integrins and inflammation. Cell Mol Life Sci 54: 549-555.
23. Gordon EJ, Gale NW, Harvey N. 2008. Expression of the hyaluronian receptor LYVE-1 is not restricted to the lymphatic vasculature; Lyve-1 is also expressed on embryonic blood vessels. Dev Dyn 237: 1901-1907.
24. Gordon EJ, Rao S, Pollard JW, Nutt SL, Lang RA, Harvey NL. 2010. Macrophages define dermal lymphatic vessel calibre during development by regulating lymphatic endothelial cell proliferation. Development 137: 3899-910. Erratum in: Development 2011;138:797.
25. Gottfried E, Kunz-Schughart LA, Weber A, Rehli M, Peuker A, Müller A, Kastenberger M, Brockhoff G, Andreesen R, Kreutz M. 2008. Expression of CD68 in non-myeloid cell types. Scand J Immunol 67: 453-463.
26. Holness CL, Simmons DL. 1993. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81: 1607-1613.
27. Holness CL, da Silva RP, Fawcett J, Gordon S, Simmons DL. 1993. Macrosialin, a mouse macrophage-restricted glycoprotein, is a member of the lamp/ lgp family. J Biol Chem 268: 9661-9666.
28. Hou W-H, Liu I-H, Tsai CC, Johnson FE, Huang SS, Huang JS. 2011. CRSBP-1/LYVE-1 ligands disrupt lymphatic intercellular adhesion by inducing tyrosine phosphorylation and internalization of VE-cadherin. J Cell Sci 124: 1231-1244.
29. Huang SS, Tang FM, Huang YH, Liu IH, Hsu SC, Chen ST Huang JS. 2003. Cloning, expression, characterization, and role in autocrine cell growth of cell-surface retention sequence binding protein-1. J Biol Chem 278: 43855-43869.
30. Huntington GS, McClure CFW. 1910. The anatomy and development of the jugular lymph sacs in the domestic cat (Felis domestica). Am J Anat 10: 177-311.
31. Jackson DG. 2004. Biology of the lymphatic marker LYVE-1 and applications in research into lymphatic trafficking and lymphangiogenesis. APMIS 112: 526-38.
32. Jackson DG, Prevo R, Clasper S, Banerji S. 2001. Lyve-1, the lymphatic system and tumor lymphangiogenesis. Trends Immunol 22: 317-321.
33. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F. 1998. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125: 4575-4583.
34. Jeon B-H, Jang C, Han J, Kataru RP, Piao L, Jung K, Cha HJ, Schwendener RA, Jang KY, Kim K-S, Alitalo K, Koh GY. 2008. Profound but dysfunctional lymphangiogenesis via vascular endothelial growth factor ligands from CD11b+ macrophages in advanced ovarian cancer. Cancer Res 68: 1100-1109.
35. Ji R-C. 2012. Macrophages are important mediators of either tumor- or inflammation-induced lymphangiogenesis. Cell Mol Life Sci 69: 897-914.
36. Juszyński M, Ciszek B, Stachurska E, Jablońska A, Ratajska A. 2008. Development of lymphatic vessels in mouse embryonic and early postnatal hearts. Dev Dyn 237: 2973-2986.
37. Kampmeier OF. 1912. The value of the injection method in the study of lymphatic development. Anat Rec 6: 223-233.
38. Karunamuni G, Yang K, Qiu Doughman Y, Wikenheiser J, Bader D, Barnett J, Austin A, Parsons-Wingerter P, Watanabe M. 2010. Expression of lymphatic markers during avian and mouse cardiogenesis. Anat Rec 293: 259-270.
39. Kataru RP, Jung K, Jang C, Yang H, Schwendener RA, Baik JE, Han SH, Alitalo K, Koh GY. 2009. Critical role of CD11b+ macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 113: 5650-5659.
40. Kattan J, Dettman RW, Bristow J. 2004. Formation and remodeling of the coronary vascular bed in the embryonic avian heart. Dev Dyn 230: 34-43.
41. Kim KE, Koh Y-J, Jeon B-H, Jang C, Han J, Kataru RP, Schwendener RA, Kim J-M, Koh GY. 2009. Role of CD11b macrophages in intraperitoneal lipopolysaccharide-induced aberrant lymphangiogenesis and lymphatic function in the diaphragm. Am J Pathol 175: 1733-1745.
42. Klika E, Antaliková L, Rychter Z, Jelínek R. 1972. Inception and manner of development of the lymph vessels in the chick embryo heart. Lymphology 5: 137-148.
43. Lee H-W, Qin Y-X, Kim Y-M, Park E-Y, Hwang J-S, Huo G-H, Yang C-W, Kim W-Y, Kim J. 2011. Expression of lymphatic endothelium-specific hyaluronian receptor LYVE-1 in the developing mouse kidney. Cell Tissue Res 343: 429-444.
44. Leenen PJ, de Bruijn MF, Voerman JS, Campbell PA, van Ewijk W. 1994. Markers of macrophage development detected by monoclonal antibodies. J Immunol Methods 174: 5-19.
45. Lewis CE, Pollard JW. 2006. Distinct role of macrophages in different tumor microenvironments. Cancer Res 66: 605-612.
46. Liao HJ, Kume T, McKay C, Xu MJ, Ihle JN, Carpenter G. 2002. Absence of erythrogenesis and vasculogenesis in Plcg1- deficient mice. J Biol Chem 277: 9335-9341.
47. Liu Y, Shaw SK, Ma S, Yang L, Lunscinskas FW, Parkos CA. 2004. Regulation of leukocyte transmigration: cell surface interactions and signaling events. J Immunol 172: 7-13.
48. Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, Tomita M, Van Rooijen N, Takenaka H, D'Amore PA, Stein-Streilein J, Losordo DW, Streilen JW. 2005. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115: 2363-2372.
49. Maruyama K, Asai J, li M, Thorne T, Losordo DW, D'Amore PA. 2007. Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol 170: 1178-1191.
50. McCaffery P, Dräger UC. 2000. Regulation of retinoic acid signaling in the embryonic nervous system: a master differentiation factor. Cytokine Growth Factor Rev 11: 233-249.
51. Mouta Carreira C, Nasser SM, di Tomaso E, Padera TP, Boucher Y, Tomarev SI, Jain RK. 2001. LYVE-1 is not restricted to the lymph vessels: expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis. Cancer Res 61: 8079-8084.
52. Ny A, Koch M, Schneider M, Neven E, Tong RT, Maity S, Fischer C, Plaisance S, Lambrechts D, Heligon C, Terclavers S, Ciesiolka M, Kalin R, Man WY, Senn I, Wyns S, Lupu F, Brandli A, Vleminckx K, Collen D, Dewerchin M, Conway EM, Moons L, Jain RK, Carmeliet P. 2005. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nature Med 11: 998-1004.
53. Pérez-Pomares JM, Carmona R, González-Iriarte M, Atencia G, Wessels A, Muñoz-Chapuli R. 2002. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int J Dev Biol 46: 1005-1013.
54. Poelmann RE, Gittenberger-de Groot AC, Mentink MMT, Bökenkamp R, Hogers B. 1993. Development of the cardiac coronary vescular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ Res 73: 559-568.
55. Prevo R, Banerji S, Ferguson D, Clasper S, Jackson DG. 2001. Mouse LYVE-1 is an endocytic receptor for hyaluronian in lymphatic endothelium. J Biol Chem 276: 19420-19430.
56. Pusztaszeri MP, Seelentag W, Bosman FT. 2006. Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J Histochem Cytochem 54: 385-395.
57. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. 1996. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc Natl Acad Sci USA 93: 14833-14838.
58. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. 2010. Coronary arteries form by developmental reprogramming of venous cells. Nature 464: 549-554.
59. Religa P, Cao R, Bjorndahl M, Zhou Z, Zhu Z, Cao Y. 2005. Presence of bone marrow-derived circulating progenitor endothelial cells in the newly formed lymphatic vessels. Blood 106: 4184-4190.
60. Rodriguez-Niedenführ M, Papoutsi M, Christ B, Nicolaides KH, von Kaisenberg CS, Tomarev SI, Wilting J. 2001. Prox1 is a marker of ectodermal placodes, endodermal compartments, lymphatic endothelium and lymphangioblasts. Anat Embryol (Berl) 204: 399-406.
61. Sabin FR. 1902. On the origin of the lymphatics system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am J Anat 1: 367-391.
62. Sabin FR. 1904. On the development of the superficial lymphatics in the skin of the pig. Am J Anat 3: 183-195.
63. Saito N, Pulford KA, Breton-Gorius J, Masse JM, Mason DY, Cramer EM. 1991. Ultrastructural localization of the CD68 macrophage-associated antigen in human blood neutrophils and monocytes. Am J Pathol 139: 1053-1059.
64. Schledzewski K, Falkowski M, Moldenhauer G, Metharom P, Kzhyshkowska J, Ganss R, Demory A, Falkowska-Hansen B, Kurzen H, Ugurel S, Geginat G, Arnold B, Goerdt S. 2006. Lymphatic endothelium specific hyaluronian receptor Lyve-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of lymphangiogenesis. J Pathol 209: 67-77.
65. Schoppmann SF, Birner P, Stöckl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K, Kerjaschki D. 2002. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161: 947-956.
66. Schulte-Merker S, Sabine A, Petrova TV. 2011. Lymphatic vascular morphogenesis in development, physiology, and disease. J Cell Biol 193: 607-618.
67. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu X, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66.
68. Shalaby F, Ho J, Stanford WL, Fischer K-D, Schuh AC, Schwartz L, Bernstein A, Rossant J. 1997. A requirement for flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89: 981-990.
69. Solovjov DA, Pluskota E, Plow EF. 2005. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem 280: 1336-1345.
70. Srinivasan RS, Dillard ME, Lagutin OV, Lin F-J, Tsai S, Tsai M-J, Samokhvalov IM, Oliver G. 2007. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21: 2422-2432.
71. Tomanek RJ. 2005. Formation of coronary vasculature during development. Angiogenesis 8: 273-284.
72. Van den Berg TK, Kraal G. 2005. A function for the macrophage F4/80 molecule in tolerance induction. Trends Immunol 26: 506-509.
73. Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P. 1997. Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc Natl Acad Sci USA 94: 6273-6278.
74. Vrancken Peeters MPFM, Gittenberger-de Groot AC, Mentink MMT, Hungerford JE, Little CD, Poelmann RE. 1997. The development of the coronary vessels and their differentiation into arteries and veins in the embryonic quail heart. Dev Dyn 208: 338-348.
75. Wigle JT, Oliver G. 1999. Prox1 function is required for development of the murine lymphatic system. Cell 98: 769-778.
76. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G. 2002. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21: 1505-1513.
77. Wilting J, Aref Y, Huang R, Tomarev SI, Schweigerer L, Christ B, Valasek P, Papoutsi M. 2006. Dual origin of avian lymphatics. Dev Biol 292: 165-173.
78. Wilting J, Buttler K, Schulte I, Papoutsi M, Schweigerer L, Männer J. 2007. The proepicardium delivers hemangioblasts but not lymphangioblasts to the developing heart. Dev Biol 305: 451-459.
79. Wirzenius M, Tammela T, Uutela M, He Y, Odorisio T, Zambruno G, Nagy JA, Dvorak HF, Yla-Herttuala S, Shibuya M, Alitalo K. 2007. Distinct vascular endothelial growth factor signals for lymphatic vessel enlargement and sprouting. J Exp Med 204: 1431-1440.
80. Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein BM. 2006. Live imaging of the lymphatic development in the zebrafish. Nature Med 12: 711-716.