A Tale of Two Models: Mouse and Zebrafish as Complementary Models for Lymphatic Studies

다국어 초록 (Multilingual Abstract)

Lymphatic vessels provide essential roles in maintaining fluid homeostasis and lipid absorption. Dysfunctions of the lymphatic vessels lead to debilitating pathological conditions, collectively known as lymphedema. In addition, lymphatic vessels are a critical moderator for the onset and progression of diverse human diseases including metastatic cancer and obesity. Despite their clinical impor-tance, there is no currently effective pharmacological therapy to regulate functions of lymphatic vessels. Recent efforts to manipulate the Vascular Endothelial Growth Factor-C (VEGFC) pathway, which is arguably the most important signaling pathway regulating lymphatic endo-thelial cells, to alleviate lymphedema yielded largely mixed results, necessitating identification of new targetable signaling pathways for therapeutic intervention for lym-phedema. Zebrafish, a relatively new model system to investigate lymphatic biology, appears to be an ideal model to identify novel therapeutic targets for lymphatic biology. In this review, we will provide an overview of our current understanding of the lymphatic vessels in verte-brates, and discuss zebrafish as a promising in vivo model to study lymphatic vessels.

참고문헌 (Reference)

1 Okuda KS., "lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish" 139 : 2381-2391, 2012

2 Chikly B., "Who discovered the lymphatic system" 30 : 186-193, 1997

3 Pollmann C., "Visualization of lymphatic vessel development, growth, and function" 214 : 167-186, 2014

4 Lindeman RE., "Vertebrate maternal-effect genes : Insights into fertilization, early cleavage divisions, and germ cell determinant localization from studies in the zebrafish" 77 : 299-313, 2010

5 Ellertsdóttir E., "Vascular morphogenesis in the zebrafish embryo" 341 : 56-65, 2010

6 Karkkainen MJ., "Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins" 5 : 74-80, 2004

7 Gore AV., "Vascular development in the zebrafish" 2 : a006684-, 2012

8 Kukk E., "VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development" 122 : 3829-3837, 1996

9 Wilkinson RN., "The zebrafish as a model of vascular development and disease" 124 : 93-122, 2014

10 Francois M., "The transcriptional control of lymphatic vascular development" 26 : 146-155, 2011

11 Aoyagi T., "The role of sphingosine-1-phosphate in breast cancer tumor-induced lymphangiogenesis" 10 : 97-106, 2012

12 Srinivasan RS., "The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells" 24 : 696-707, 2010

13 Kerjaschki D., "The lymphatic vasculature revisited" 124 : 874-877, 2014

14 Alitalo K., "The lymphatic vasculature in disease" 17 : 1371-1380, 2011

15 van der Putte SC., "The development of the lymphatic system in man" 51 : 3-60, 1975

16 Dejana E., "The control of vascular integrity by endothelial cell junctions : molecular basis and pathological implications" 16 : 209-221, 2009

17 Connell FC., "The classification and diagnostic algorithm for primary lymphatic dysplasia : an update from 2010 to include molecular findings" 84 : 303-314, 2013

18 Niessen K., "The Notch1-Dll4 signaling pathway regulates mouse postnatal lymphatic development" 118 : 1989-1997, 2011

19 Blackburn PR., "The CRISPR system--keeping zebrafish gene targeting fresh" 10 : 116-118, 2013

20 Meng X., "Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases" 26 : 695-701, 2008

21 James JM., "TGFβ signaling is required for sprouting lymphangiogenesis during lymphatic network development in the skin" 140 : 3903-3914, 2013

22 Yoon CM., "Sphingosine-1-phosphate promotes lymphangiogenesis by stimulating S1P1/Gi/PLC/Ca2+ signaling pathways" 112 : 1129-1138, 2008

23 François M., "Sox18 induces development of the lymphatic vasculature in mice" 456 : 643-647, 2008

24 Geudens I., "Role of delta-like-4/Notch in the formation and wiring of the lymphatic network in zebrafish" 30 : 1695-1702, 2010

25 Kimple AJ., "Regulators of G-protein signaling and their Gα substrates : promises and challenges in their use as drug discovery targets" 63 : 728-749, 2011

26 Marcelo KL., "Regulation of endothelial cell differentiation and specification" 112 : 1272-1287, 2013

27 Abtahian F., "Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk" 299 : 247-251, 2003

28 Wigle JT., "Prox1 function is required for the development of the murine lymphatic system" 98 : 769-778, 1999

29 Lee S., "Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors" 169 : 681-691, 2005

30 김한솔, "Platelets Take the Lead in Lymphatic Separation" LIPPINCOTT WILLIAMS WILKINS 106 (106): 1184-1186, 2010

31 McColl BK., "Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D" 198 : 863-868, 2003

32 Sabin FR., "On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig" 1 : 367-389, 1902

33 Murtomaki A., "Notch1 functions as a negative regulator of lymphatic endothelial cell differentiation in the venous endothelium" 140 : 2365-2376, 2013

34 Zheng W., "Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor" 118 : 1154-1162, 2011

35 Campbell JM., "New and TALENted genome engineering toolbox" 113 : 571-587, 2013

36 Alders M., "Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans" 41 : 1272-1274, 2009

37 Prevo R., "Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium" 276 : 19420-19430, 2001

38 Heasman J., "Morpholino oligos : making sense of antisense?" 243 : 209-214, 2002

39 Corey DR, "Morpholino antisense oligonucleotides: tools for investigating vertebrate development" 2 : REVIEWS101-, 2001

40 Ekker SC., "Morphants : a new systematic vertebrate functional genomics approach" 17 : 302-306, 2000

41 Smrcka AV., "Molecular targeting of Gα and Gβγ subunits : a potential approach for cancer therapeutics" 34 : 290-298, 2013

42 Venkatakrishnan AJ., "Molecular signatures of G-protein-coupled receptors" 494 : 185-194, 2013

43 Karkkainen MJ., "Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema" 25 : 153-159, 2000

44 Wagner DS., "Maternal control of development at the midblastula transition and beyond : mutants from the zebrafish II" 6 : 781-790, 2004

45 Guermazi A., "Lymphography: an old technique retains its usefulness" 23 : 1541-1558, 2003

46 Zuther JE, "Lymphedema management: the comprehensive guide for practitioners" Thieme 2012

47 Oliver G., "Lymphatic vasculature development" 4 : 35-45, 2004

48 Yang Y., "Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos" 120 : 2340-2348, 2012

49 Lohela M., "Lymphangiogenic growth factors, receptors and therapies" 90 : 167-184, 2003

50 Bruyère F., "Lymphangiogenesis : in vitro and in vivo models" 24 : 8-21, 2010

51 Tammela T., "Lymphangiogenesis : Molecular mechanisms and future promise" 140 : 460-476, 2010

52 Yaniv K., "Live imaging of lymphatic development in the zebrafish" 12 : 711-716, 2006

53 Srinivasan RS., "Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature" 21 : 2422-2432, 2007

54 Banerji S., "LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan" 144 : 789-801, 1999

55 Bazigou E., "Integrin-alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis" 17 : 175-186, 2009

56 Oka M., "Inhibition of endogenous TGF-beta signaling enhances lymphangiogenesis" 111 : 4571-4579, 2008

57 Lawson ND., "In vivo imaging of embryonic vascular development using transgenic zebrafish" 248 : 307-318, 2002

58 Bedell VM., "In vivo genome editing using a high-efficiency TALEN system" 491 : 114-118, 2012

59 Kamei M., "Imaging blood vessels in the zebrafish" 100 : 27-54, 2010

60 Pistocchi A., "Identification and expression pattern of zebrafish prox2 during embryonic development" 237 : 3916-3920, 2008

61 Jeltsch M., "Hyperplasia of lymphatic vessels in VEGF-C transgenic mice" 276 : 1423-1425, 1997

62 Doyon Y., "Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases" 26 : 702-708, 2008

63 Koltowska K., "Getting out and about : the emergence and morphogenesis of the vertebrate lymphatic vasculature" 140 : 1857-1870, 2013

64 Brouillard P., "Genetics of lymphatic anomalies" 124 : 898-904, 2014

65 Dorsam RT., "G-protein-coupled receptors and cancer" 9 : 79-94, 2007

66 Gilman AG., "G proteins : transducers of receptor-generated signals" 56 : 615-649, 1987

67 Möhle R., "G protein-coupled receptor crosstalk and signaling in hematopoietic stem and progenitor cells" 1266 : 63-67, 2012

68 Goldsmith ZG., "G protein regulation of MAPK networks" 26 : 3122-3142, 2007

69 Achen MG., "Focus on lymphangiogenesis in tumor metastasis" 7 : 121-127, 2005

70 Bazigou E., "Flow control in our vessels : vascular valves make sure there is no way back" 70 : 1055-1066, 2013

71 김준대, "Essential Role of Apelin Signaling During Lymphatic Development in Zebrafish" LIPPINCOTT WILLIAMS & WILKINS 34 : 338-345, 2014

72 Oliver G., "Endothelial cell plasticity : how to become and remain a lymphatic endothelial cell" 137 : 363-372, 2010

73 Hwang WY., "Efficient genome editing in zebrafish using a CRISPR-Cas system" 31 : 227-229, 2013

74 Abrams EW., "Early zebrafish development : it’s in the maternal genes" 19 : 396-403, 2009

75 Nithianandarajah-Jones GN., "ERK5 : structure, regulation and function" 24 : 2187-2196, 2012

76 Simon MI., "Diversity of G proteins in signal transduction" 252 : 802-808, 1991

77 van Impel A., "Divergence of zebrafish and mouse lymphatic cell fate specification pathways" 141 : 1228-1238, 2014

78 Wiley DM., "Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein" 13 : 686-692, 2011

79 Pfeiffer F., "Distinct molecular composition of blood and lymphatic vascular endothelial cell junctions establishes specific functional barriers within the peripheral lymph node" 38 : 2142-2155, 2008

80 Küchler AM., "Development of the zebrafish lymphatic system requires VEGFC signaling" 16 : 1244-1248, 2006

81 Wang Y., "Current views on the function of the lymphatic vasculature in health and disease" 24 : 2115-2126, 2010

82 Murdaca G., "Current views on diagnostic approach and treatment of lymphedema" 125 : 134-140, 2012

83 김준대, "Context-Dependent Proangiogenic Function of Bone Morphogenetic Protein Signaling Is Mediated by Disabled Homolog 2" CELL PRESS 23 (23): 441-448, 2012

84 Meens MJ., "Connexins in lymphatic vessel physiology and disease" 588 : 1271-1277, 2014

85 Irrthum A., "Congenital hereditary lymphedema caused by a mutation that inactivates VEGFR3 tyrosine kinase" 67 : 295-301, 2000

86 Cha YR., "Chemokine signaling directs trunk lymphatic network formation along the preexisting blood vasculature" 22 : 824-836, 2012

87 Jin SW., "Cellular and molecular analyses of vascular tube and lumen formation in zebrafish" 132 : 5199-5209, 2005

88 Bos FL., "CCBE1 is essential for mammalian lymphatic vascular development and enhances the lymphangiogenic effect of vascular endothelial growth factor-C in vivo" 109 : 486-491, 2011

89 Jeltsch M., "CCBE1 enhances lymphangiogenesis via ADAMTS3-mediated VEGF-C activation" 129 : 1962-1971, 2014

90 Levet S., "Bone morphogenetic protein 9(BMP9)controls lymphatic vessel maturation and valve formation" 122 : 598-607, 2013

91 Dunworth WP., "Bone morphogenetic protein 2 signaling negatively modulates lymphatic development in vertebrate embryos" 114 : 56-66, 2013

92 Neufeld, S., "Blood and lymphatic vascular tube formation in mouse" (14) : S1084-S9521, 2014

93 Kidoya H., "Biology of the apelin-APJ axis in vascular formation" 152 : 125-131, 2012

94 DeWire SM., "Biased ligands for better cardiovascular drugs : dissecting G-protein-coupled receptor pharmacology" 109 : 205-216, 2011

95 Eichmann A., "Avian VEGF-C : cloning, embryonic expression pattern and stimulation of the differentiation of VEGFR2-expressing endothelial cell precursors" 125 : 743-752, 1998

96 Kohli V., "Arterial and venous progenitors of the major axial vessels originate at distinct locations" 25 : 196-206, 2013

97 Karpinich NO., "Apelin signaling : new G protein-coupled receptor pathway in lymphatic vascular development" 34 : 239-241, 2014

98 Wigle JT., "An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype" 21 : 1505-1513, 2002

99 김준대, "Alk3/Alk3b and Smad5 Mediate BMP Signaling during Lymphatic Development in Zebrafish" 한국분자세포생물학회 37 (37): 270-274, 2014

100 Fritz-Six KL., "Adrenomedullin signaling is necessary for murine lymphatic vascular development" 118 : 40-50, 2008

101 Karpinich NO., "Adrenomedullin gene dosage correlates with tumor and lymph node lymphangiogenesis" 27 : 590-600, 2013

102 Enholm B., "Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin" 88 : 623-629, 2001

103 Larrivée B., "ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway" 22 : 489-500, 2012

104 Bill BR., "A primer for morpholino use in zebrafish" 6 : 69-77, 2009

105 Hägerling R., "A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy" 32 : 629-644, 2013

106 Ny A., "A genetic Xenopus laevis tadpole model to study lymphangiogenesis" 11 : 998-1004, 2005