Interplay of mechanotransduction, FOXC2, connexins, and calcineurin signaling in lymphatic valve formation

Advances in Anatomy Embryology and Cell Biology

Volumn 214, Issue , 2014, Pages 67-80

  Sabine, Amélie ^a   Petrova, Tatiana V ^a,b,c  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; FORKHEAD TRANSCRIPTION FACTOR; GAP JUNCTION PROTEIN; TRANSCRIPTION FACTOR FOXC2;

ANIMAL; CALCIUM SIGNALING; GENE EXPRESSION REGULATION; HUMAN; LYMPH VESSEL; LYMPHANGIOGENESIS; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW;

ANIMALS; CALCINEURIN; CALCIUM SIGNALING; CONNEXINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MECHANOTRANSDUCTION, CELLULAR;

EID: 84958542717     PISSN: 03015556     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-7091-1646-3_6     Document Type: Review

References (52)

1. Bazigou, E., Lyons, O. T., Smith, A., Venn, G. E., Cope, C., Brown, N. A., & Makinen, T. (2011). Genes regulating lymphangiogenesis control venous valve formation and maintenance in mice. Journal of Clinical Investigation, 121(8), 2984-2992
2. Bazigou, E., & Makinen, T. (2013). Flow control in our vessels: Vascular valves make sure there is no way back. Cellular and Molecular Life Sciences, 70(6), 1055-1066
3. Bazigou, E., Xie, S., Chen, C., Weston, A., Miura, N., Sorokin, L., et al. (2009a). Integrin-Alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Developmental Cell, 17(2), 175-186
4. Bazigou, E., Xie, S., Chen, C., Weston, A., Miura, N., Sorokin, L., et al. (2009b). Integrin-Alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Developmental Cell, 17(2), 175-186. doi:10.1016/j.devcel.2009.06.017
5. Beis, D., Bartman, T., Jin, S. W., Scott, I. C., D'Amico, L. A., Ober, E. A., et al. (2005). Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development, 132(18), 4193-4204
6. Benayoun, B. A., Caburet, S., & Veitia, R. A. (2011). Forkhead transcription factors: Key players in health and disease. Trends in Genetics, 27(6), 224-232
7. Bouvree, K., Brunet, I., Del Toro, R., Gordon, E., Prahst, C., Cristofaro, B., et al. (2012). Semaphorin3A, Neuropilin-1, and PlexinA1 are required for lymphatic valve formation. Circulation Research, 111(4), 437-445
8. Brice, G., Ostergaard, P., Jeffery, S., Gordon, K., Mortimer, P., & Mansour, S. (2013). A novel mutation in GJA1 causing oculodentodigital syndrome and primary lymphoedema in a three generation family. Clinical Genetics, 64(4), 378-381
9. Butcher, J. T., Penrod, A. M., Garcia, A. J., & Nerem, R. M. (2004). Unique morphology and focal adhesion development of valvular endothelial cells in static and fluid flow environments. Arteriosclerosis, Thrombosis, and Vascular Biology, 24(8), 1429-1434
10. Butcher, J. T., Tressel, S., Johnson, T., Turner, D., Sorescu, G., Jo, H., & Nerem, R. M. (2006). Transcriptional profiles of valvular and vascular endothelial cells reveal phenotypic differences: Influence of shear stress. Arteriosclerosis, Thrombosis, and Vascular Biology, 26 (1), 69-77
11. Chang, C. P., Neilson, J. R., Bayle, J. H., Gestwicki, J. E., Kuo, A., Stankunas, K., et al. (2004). A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell, 118(5), 649-663
12. Chen, C. Y., Bertozzi, C., Zou, Z., Yuan, L., Lee, J. S., Lu, M., et al. (2012). Blood flow reprograms lymphatic vessels to blood vessels. Journal of Clinical Investigation, 122(6), 2006-2017
13. Chiu, J. J., & Chien, S. (2011). Effects of disturbed flow on vascular endothelium: Pathophysiological basis and clinical perspectives. Physiological Reviews, 91(1), 327-387
14. Dagenais, S. L., Hartsough, R. L., Erickson, R. P., Witte, M. H., Butler, M. G., & Glover, T. W. (2004). Foxc2 is expressed in developing lymphatic vessels and other tissues associated with lymphedema-distichiasis syndrome. Gene Expression Patterns, 4(6), 611-619
15. Danciu, T. E., Chupreta, S., Cruz, O., Fox, J. E., Whitman, M., & Iniguez-Lluhi, J. A. (2012). Small ubiquitin-like modifier (SUMO) modification mediates function of the inhibitory domains of developmental regulators FOXC1 and FOXC2. Journal of Biological Chemistry, 287(22), 18318-18329
16. de la Pompa, J. L., Timmerman, L. A., Takimoto, H., Yoshida, H., Elia, A. J., Samper, E., et al. (1998). Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature, 392(6672), 182-186
17. 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. Developmental Biology, 319(2), 309-320
18. Fang, J., Dagenais, S. L., Erickson, R. P., Arlt, M. F., Glynn, M. W., Gorski, J. L., et al. (2000). Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. American Journal of Human Genetics, 67(6), 1382-1388
19. Ferrell, R. E., Baty, C. J., Kimak, M. A., Karlsson, J. M., Lawrence, E. C., Franke-Snyder, M., et al. (2010). GJC2 missense mutations cause human lymphedema. American Journal of Human Genetics, 86(6), 943-948
20. Finegold, D. N., Baty, C. J., Knickelbein, K. Z., Perschke, S., Noon, S. E., Campbell, D., et al. (2012). Connexin 47 mutations increase risk for secondary lymphedema following breast cancer treatment. Clinical Cancer Research, 18(8), 2382-2390
21. Gale, N. W., Thurston, G., Hackett, S. F., Renard, R., Wang, Q., McClain, J., et al. (2002). Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Developmental Cell, 3(3), 411-423
22. Gnepp, D. R., & Green, F. H. (1980). Scanning electron microscopic study of canine lymphatic vessels and their valves. Lymphology, 13(2), 91-99
23. Hinton, R. B., & Yutzey, K. E. (2011). Heart valve structure and function in development and disease. Annual Review of Physiology, 73, 29-46
24. Hogan, P. G., Chen, L., Nardone, J., & Rao, A. (2003). Transcriptional regulation by calcium, calcineurin, and NFAT. Genes and Development, 17(18), 2205-2232
25. Holliday, C. J., Ankeny, R. F., Jo, H., & Nerem, R. M. (2011). Discovery of shear-And sidespecific mRNAs and miRNAs in human aortic valvular endothelial cells. American Journal of Physiology-Heart and Circulatory Physiology, 301(3), H856-H867
26. Iida, K., Koseki, H., Kakinuma, H., Kato, N., Mizutani-Koseki, Y., Ohuchi, H., et al. (1997). Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development, 124(22), 4627-4638
27. Ivanov, K. I., Agalarov, Y., Valmu, L., Samuilova, O., Liebl, J., Houhou, N., et al. (2013). Phosphorylation regulates FOXC2-mediated transcription in lymphatic endothelial cells. Molecular and Cellular Biology, 33(19), 3749-3761
28. Jurisic, G., Maby-El Hajjami, H., Karaman, S., Ochsenbein, A. M., Alitalo, A., Siddiqui, S. S., et al. (2012). An unexpected role of semaphorin3a-neuropilin-1 signaling in lymphatic vessel maturation and valve formation. Circulation Research, 111(4), 426-436
29. Kampmeier, O. F. (1928). The genetic history of the valves in the lymphatic system of man. The American Journal of Anatomy, 40(3), 413-457
30. Kanady, J. D., Dellinger, M. T., Munger, S. J., Witte, M. H., & Simon, A. M. (2011). Connexin37 and Connexin43 deficiencies in mice disrupt lymphatic valve development and result in lymphatic disorders including lymphedema and chylothorax. Developmental Biology, 354 (2), 253-266
31. Kazenwadel, J., Secker, G. A., Liu, Y. J., Rosenfeld, J. A., Wildin, R. S., Cuellar-Rodriguez, J., et al. (2012). Loss-of-function germline GATA2 mutations in patients with MDS/AML or MonoMAC syndrome and primary lymphedema reveal a key role for GATA2 in the lymphatic vasculature. Blood, 119(5), 1283-1291
32. Koltowska, K., Betterman, K. L., Harvey, N. L., & Hogan, B. M. (2013). Getting out and about: The emergence and morphogenesis of the vertebrate lymphatic vasculature. Development, 140 (9), 1857-1870
33. Kriederman, B. M., Myloyde, T. L., Witte, M. H., Dagenais, S. L., Witte, C. L., Rennels, M., et al. (2003). FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome. Human Molecular Genetics, 12(10), 1179-1185
34. Kulkarni, R. M., Greenberg, J. M., & Akeson, A. L. (2009). NFATc1 regulates lymphatic endothelial development. Mechanisms of Development, 126(5-6), 350-365
35. Kume, T. (2008). Foxc2 transcription factor: A newly described regulator of angiogenesis. Trends in Cardiovascular Medicine, 18(6), 224-228
36. Kume, T., Deng, K., & Hogan, B. L. (2000). Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development, 127(7), 1387-1395
37. Kume, T., Jiang, H., Topczewska, J. M., & Hogan, B. L. (2001). The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes and Development, 15(18), 2470-2482
38. Makinen, T., Adams, R. H., Bailey, J., Lu, Q., Ziemiecki, A., Alitalo, K., et al. (2005). PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes and Development, 19(3), 397-410
39. Mellor, R. H., Brice, G., Stanton, A. W., French, J., Smith, A., Jeffery, S., et al. (2007). Mutations in FOXC2 are strongly associated with primary valve failure in veins of the lower limb. Circulation, 115(14), 1912-1920
40. Mouta-Bellum, C., Kirov, A., Miceli-Libby, L., Mancini, M. L., Petrova, T. V., Liaw, L., et al. (2009). Organ-specific lymphangiectasia, arrested lymphatic sprouting, and maturation defects resulting from gene-Targeting of the PI3K regulatory isoforms p85alpha, p55alpha, and p50alpha. Developmental Dynamics, 238(10), 2670-2679
41. Norrmen, C., Ivanov, K. I., Cheng, J., Zangger, N., Delorenzi, M., Jaquet, M., et al. (2009). FOXC2 controls formation and maturation of lymphatic collecting vessels through cooperation with NFATc1. Journal of Cell Biology, 185(3), 439-457
42. Ostergaard, P., Simpson, M. A., Brice, G., Mansour, S., Connell, F. C., Onoufriadis, A., et al. (2011). Rapid identification of mutations in GJC2 in primary lymphoedema using whole exome sequencing combined with linkage analysis with delineation of the phenotype. Journal of Medical Genetics, 48(4), 251-255
43. Petrova, T. V., Karpanen, T., Norrmen, C., Mellor, R., Tamakoshi, T., Finegold, D., et al. (2004). Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nature Medicine, 10(9), 974-981
44. Pfenniger, A., Chanson, M., & Kwak, B. R. (2013). Connexins in atherosclerosis. Biochimica et Biophysica Acta, 1828(1), 157-166
45. Sabine, A., Agalarov, Y., Maby-El Hajjami, H., Jaquet, M., Hagerling, R., Pollmann, C., et al. (2012). Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Developmental Cell, 22(2), 430-445
46. Takemoto, M., He, L., Norlin, J., Patrakka, J., Xiao, Z., Petrova, T., et al. (2006). Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO Journal, 25(5), 1160-1174
47. Tammela, T., Saaristo, A., Holopainen, T., Lyytikka, J., Kotronen, A., Pitkonen, M., et al. (2007). Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nature Medicine, 13(12), 1458-1466
48. Tatin, F., Taddei, A., Weston, A., Fuchs, E., Devenport, D., Tissir, F., & Makinen, T. (2013). Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Developmental Cell, 26(1), 31-44
49. Vermot, J., Forouhar, A. S., Liebling, M., Wu, D., Plummer, D., Gharib, M., & Fraser, S. E. (2009). Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biology, 7(11), e1000246
50. Wei, C. J., Xu, X., & Lo, C. W. (2004). Connexins and cell signaling in development and disease. Annual Review of Cell and Developmental Biology, 20, 811-838
51. Wilting, J., Papoutsi, M., Christ, B., Nicolaides, K. H., von Kaisenberg, C. S., Borges, J., et al. (2002). The transcription factor Prox1 is a marker for lymphatic endothelial cells in normal and diseased human tissues. FASEB Journal, 16(10), 1271-1273
52. Zhou, F., Chang, Z., Zhang, L., Hong, Y. K., Shen, B., Wang, B., et al. (2010). Akt/Protein kinase B is required for lymphatic network formation, remodeling, and valve development. American Journal of Pathology, 177(4), 2124-2133