Murine Notch1 is required for lymphatic vascular morphogenesis during development

Developmental Dynamics

Volumn 243, Issue 7, 2014, Pages 957-964

  Fatima, Anees ^a   Culver, Austin ^a   Culver, Ford ^a   Liu, Ting ^a   Dietz, William H ^a   Thomson, Benjamin R ^a   Hadjantonakis, Anna Katerina ^b   Quaggin, Susan E ^a   Kume, Tsutomu ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Lymphangiogenesis; Lymphatic vessel development; Notch; Prox1

Indexed keywords

CHEMOKINE; CONNEXIN 37; CYTOKINE; NOTCH1 RECEPTOR; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENE DELETION; GENE EXPRESSION PROFILING; KNOCKOUT MOUSE; LYMPH VESSEL; LYMPHANGIOGENESIS; MORPHOGENESIS; MOUSE; MUTANT; NONHUMAN; NOTCH1 GENE; PHENOTYPE; PRIORITY JOURNAL; RNA SEQUENCE; SIGNAL TRANSDUCTION; SKIN; SMOOTH MUSCLE FIBER; UPREGULATION; ANIMAL; EMBRYOLOGY; FEMALE; FLOW CYTOMETRY; GENETICS; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; PHYSIOLOGY; PREGNANCY;

MURINAE; MUS;

ANIMALS; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MALE; MICE; MORPHOGENESIS; PREGNANCY; RECEPTOR, NOTCH1;

EID: 84902551210     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24129     Document Type: Article

References (41)

1. Alitalo K. 2011. The lymphatic vasculature in disease. Nat Med 17:1371-1380.
2. Aranguren XL, Beerens M, Coppiello G, Wiese C, Vandersmissen I, Lo Nigro A, Verfaillie CM, Gessler M, Luttun A. 2013. COUP-TFII orchestrates venous and lymphatic endothelial identity by homo- or hetero-dimerisation with PROX1. J Cell Sci 126:1164-1175.
3. Blanco R, Gerhardt H. 2013. VEGF and Notch in tip and stalk cell selection. Cold Spring Harb Perspect Med 3:a006569.
4. Choi I, Lee S, Hong YK. 2012. The new era of the lymphatic system: no longer secondary to the blood vascular system. Cold Spring Harb Perspect Med 2:a006445.
5. Dellinger M, Hunter R, Bernas M, Gale N, Yancopoulos G, Erickson R, Witte M. 2008. Defective remodeling and maturation of the lymphatic vasculature in Angiopoietin-2 deficient mice. Dev Biol 319:309-320.
6. Ehling M, Adams S, Benedito R, Adams RH. 2013. Notch controls retinal blood vessel maturation and quiescence. Development 140:3051-3061.
7. Francois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C, Paavonen K, Karnezis T, Shayan R, Downes M, Davidson T, Tutt D, Cheah KS, Stacker SA, Muscat GE, Achen MG, Dejana E, Koopman P. 2008. Sox18 induces development of the lymphatic vasculature in mice. Nature 456:643-647.
8. Geudens I, Herpers R, Hermans K, Segura I, Ruiz de Almodovar C, Bussmann J, De Smet F, Vandevelde W, Hogan BM, Siekmann A, Claes F, Moore JC, Pistocchi AS, Loges S, Mazzone M, Mariggi G, Bruyere F, Cotelli F, Kerjaschki D, Noel A, Foidart JM, Gerhardt H, Ny A, Langenberg T, Lawson ND, Duckers HJ, Schulte-Merker S, Carmeliet P, Dewerchin M. 2010. Role of delta-like-4/Notch in the formation and wiring of the lymphatic network in zebrafish. Arterioscler Thromb Vasc Biol 30:1695-1702.
9. Gridley T. 2010. Notch signaling in the vasculature. Curr Top Dev Biol 92:277-309.
10. He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, Yla-Herttuala S, Harding T, Jooss K, Takahashi T, Alitalo K. 2005. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res 65:4739-4746.
11. Huppert SS, Le A, Schroeter EH, Mumm JS, Saxena MT, Milner LA, Kopan R. 2000. Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature 405:966-970.
12. James JM, Nalbandian A, Mukouyama YS. 2013. TGFbeta signaling is required for sprouting lymphangiogenesis during lymphatic network development in the skin. Development 140:3903-3914.
13. Johnson NC, Dillard ME, Baluk P, McDonald DM, Harvey NL, Frase SL, Oliver G. 2008. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev 22:3282-3291.
14. Kang J, Yoo J, Lee S, Tang W, Aguilar B, Ramu S, Choi I, Otu HH, Shin JW, Dotto GP, Koh CJ, Detmar M, Hong YK. 2010. An exquisite cross-control mechanism among endothelial cell fate regulators directs the plasticity and heterogeneity of lymphatic endothelial cells. Blood 116:140-150.
15. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K. 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5:74-80.
16. Koltowska K, Betterman KL, Harvey NL, Hogan BM. 2013. Getting out and about: the emergence and morphogenesis of the vertebrate lymphatic vasculature. Development 140:1857-1870.
17. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP, Gallahan D, Closson V, Kitajewski J, Callahan R, Smith GH, Stark KL, Gridley T. 2000. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14:1343-1352.
18. Kume T. 2009. Novel insights into the differential functions of Notch ligands in vascular formation. J Angiogenes Res 1:8.
19. Lutter S, Xie S, Tatin F, Makinen T. 2012. Smooth muscle-endothelial cell communication activates Reelin signaling and regulates lymphatic vessel formation. J Cell Biol 197:837-849.
20. Makinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA. 2005. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19:397-410.
21. Martinez-Corral I, Makinen T. 2013. Regulation of lymphatic vascular morphogenesis: Implications for pathological (tumor)lymphangiogenesis. Exp Cell Res 319:1618-1625.
22. Murtomaki A, Uh MK, Choi YK, Kitajewski C, Borisenko V, Kitajewski J, Shawber CJ. 2013. Notch1 functions as a negative regulator of lymphatic endothelial cell differentiation in the venous endothelium. Development 140:2365-2376.
23. Niessen K, Zhang G, Ridgway JB, Chen H, Kolumam G, Siebel CW, Yan M. 2011. The Notch1-Dll4 signaling pathway regulates mouse postnatal lymphatic development. Blood 118:1989-1997.
24. Nowotschin S, Xenopoulos P, Schrode N, Hadjantonakis AK. 2013. A bright single-cell resolution live imaging reporter of Notch signaling in the mouse. BMC Dev Biol 13:15.
25. Petrova TV, Karpanen T, Norrmen C, Mellor R, Tamakoshi T, Finegold D, Ferrell R, Kerjaschki D, Mortimer P, Yla-Herttuala S, Miura N, Alitalo K. 2004. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 10:974-981.
26. Sabine A, Petrova TV. 2014. Interplay of mechanotransduction, FOXC2, connexins, and calcineurin signaling in lymphatic valve formation. Adv Anat Embryol Cell Biol 214:67-80.
27. Sabine A, Agalarov Y, Maby-El Hajjami H, Jaquet M, Hagerling R, Pollmann C, Bebber D, Pfenniger A, Miura N, Dormond O, Calmes JM, Adams RH, Makinen T, Kiefer F, Kwak BR, Petrova TV. 2012. Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev Cell 22:430-445.
28. Schulte-Merker S, Sabine A, Petrova TV. 2011. Lymphatic vascular morphogenesis in development, physiology, and disease. J Cell Biol 193:607-618.
29. Simons M, Eichmann A. 2013. Physiology. Lymphatics are in my veins. Science 341:622-624.
30. Srinivasan RS, Dillard ME, Lagutin OV, Lin FJ, Tsai S, Tsai MJ, Samokhvalov IM, Oliver G. 2007. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21:2422-2432.
31. Srinivasan RS, Geng X, Yang Y, Wang Y, Mukatira S, Studer M, Porto MP, Lagutin O, Oliver G. 2010. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev 24:696-707.
32. Tammela T, Alitalo K. 2010. Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140:460-476.
33. Tung JJ, Tattersall IW, Kitajewski J. 2012. Tips, stalks, tubes: notch-mediated cell fate determination and mechanisms of tubulogenesis during angiogenesis. Cold Spring Harb Perspect Med 2:a006601.
34. Veikkola T, Jussila L, Makinen T, Karpanen T, Jeltsch M, Petrova TV, Kubo H, Thurston G, McDonald DM, Achen MG, Stacker SA, Alitalo K. 2001. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 20:1223-1231.
35. Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769-778.
36. 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.
37. 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.
38. Xu Y, Yuan L, Mak J, Pardanaud L, Caunt M, Kasman I, Larrivee B, Del Toro R, Suchting S, Medvinsky A, Silva J, Yang J, Thomas JL, Koch AW, Alitalo K, Eichmann A, Bagri A. 2010. Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J Cell Biol 188:115-130.
39. Yang X, Klein R, Tian X, Cheng HT, Kopan R, Shen J. 2004. Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol 269:81-94.
40. Yang Y, Garcia-Verdugo JM, Soriano-Navarro M, Srinivasan RS, Scallan JP, Singh MK, Epstein JA, Oliver G. 2012. Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood 120:2340-2348.
41. Zheng W, Tammela T, Yamamoto M, Anisimov A, Holopainen T, Kaijalainen S, Karpanen T, Lehti K, Yla-Herttuala S, Alitalo K. 2011. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 118:1154-1162.