DEVELOPMENT OF THE LYMPHATIC SYSTEM IN NATURALLY-HISTORICAL ASPECT. PART 1
From the point of view of phylogenesis, the appearance of the lymphatic system was logical: the evolutionary leap in the sizes and volumes of animals was accompanied by complication and the emergence of a more effective cardiovascular system, vital for feeding an increased number of tissues and organs. By increasing the efficiency of the cardiovascular system, in the first place, it is meant to increase the cardiac output and the level of systolic pressure: without effective muscular organ the sufficient perfusion of tissues would be impossible. According to Starling's theory (on water metabolism in the microcirculatory bed), the amount of “leaked” fluid at the level of arterioles is higher than reabsorbed at the level of venules (which again is explained by the increased ratio of cardiac output and body size). Here is the point why the lymphatic system appear - the function of it consists in the return of water from the intercellular space, the reabsorption of which is not adapted to the cardiovascular system. It should be noted that the removal of tissue metabolism products with the help of the lymphatic system comes to the fore after restoring the equilibrium of the liquid in the body. As is known, other organs and systems such as the lungs, liver, Обзоры 57 Вопросы реконструктивной и пластической хирургии № 3 (66) сентябрь’ 2018 kidneys are of greatest importance in the utilization of protein, carbohydrate and fat metabolism products etc. For the above-described reason (the impossibility of an effective reabsorption of the liquid at the level of venules and the need to maintain the homeostasis of the cardiovascular system), the lymphatic system is a venous derivative. Evidently, there was a need for the emergence of a “drainage” system, whose roots would begin in the intercellular space and the fluid flow would have direction, similar to the venous (toward the right atrium). From the point of view of ontogenesis, thanks to modern genetic, immunological techniques, and the possibility of conducting live studies on biological models in vivo, a mixed model of the origin of the lymphatic system has been finally established (from the endothelial cells of the cardinal vein and other mesenchymal angioblasts with a distinctive set of markers, from yet unidentified sources). This indicates a much greater complexity of the lymphatic system than previously thought.
Download file
Counter downloads: 335
Keywords
лимфатическая система, лимфатические сосуды, лимфатические эндотелиальные клетки, нокаут гена, нокдаун гена, первичная лимфедема, эмбриология, анатомия, лимфология, лимфовенулярные анастомозы, lymphatic system, lymphatic vessels, lymphatic endothelial cells, gene knockout, gene knockdown, primary lymphedema, embryology, anatomy, lymphology, lymphovenular anastomosesAuthors
| Name | Organization | |
| Dudnikov A.V. | Institute of Microsurgery; Siberian State Medical University | ya.alex1994@yandex.ru |
| Baytinger V.F. | Institute of Microsurgery | |
| Kurochkina O.S. | Institute of Microsurgery |
References
Scallan J. P., Zawieja S.D., Castorena[1]Gonzalez J.A., Davis M.J. Lymphatic pumping: mechanics, mechanisms and malfunction. The Journal of Physiology, 2016, 594(20), 5749-5768.
Semo J., Nicenboim J., Yaniv K. Development of the lymphatic system: new questions and paradigms. Development, 2016, 143(6), 924-935.
Engeset A., Olszewski W., Jaeger P.M., Sokolowski J., Theodorsen L. Twenty[1]Four Hour Variation in Flow and Composition of Leg Lymph in Normal Men. Acta Physiologica, 1977. 99(2), 140-148.
Smith R.O. Lymphatic contractility: a possible intrinsic mechanism of lymphatic vessels for the transport of lymph. Journal of Experimental Medicine, 1949.90(5), 497-509.
Gashev A.A., Davis M.J., Delp M.D., Zawieja D.C. Regional variations of contractile activity in isolated rat lymphatics. Microcirculation, 2004. 11(6), 477-492.
Davis M.J., Scallan J.P., Wolpers J.H., Muthuchamy M., Gashev A.A., Zawieja D.C. Intrinsic increase in lymphangion muscle contractility in response to elevated afterload. American Journal of Physiology-Heart and Circulatory Physiology, 2012. 303(7), H795-H808.
Gashev A.A., Davis M.J., Zawieja D.C. Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct. The Journal of Physiology, 2002. 540(3), 1023-1037.
Zawieja D.C., von der Weid P.Y., Gashev A.A. Microlymphatic biology. 2008. In Microcirculation. pp. 125-158.
Zawieja D.C., Davis K.L., Schuster R., Hinds W.M., Granger H.J. Distribution, propagation, and coordination of contractile activity in lymphatics. American Journal of Physiology-Heart and Circulatory Physiology, 1993. 264(4), H1283-H1291.
Ikomi F., Kawai Y., Ohhashi T. Recent advance in lymph dynamic analysis in lymphatics and lymph nodes. Annals of Vascular Diseases, 2012. 5(3), 258-268.
Ny A., Koch M., Schneider M., Neven E., Tong R. T., Maity S., Terclavers S. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nature Medicine, 2005. 11(9), 998.
Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., Weinstein B. M. Live imaging of lymphatic development in the zebrafish. Nature Medicine, 2006. 12(6), 711.
Kuchler A.M., Gjini E., Peterson-Maduro J., Cancilla B., Wolburg H., Schulte-Merker S. Development of the zebrafish lymphatic system requires VEGFC signaling. Current Biology, 2006. 16(12), 1244-1248.
Tilney N.L. Patterns of lymphatic drainage in the adult laboratory rat. Journal of Anatomy, 1971. 109(Pt 3), 369.
Walls J.R., Coultas L., Rossant J., Henkelman R.M. Three-dimensional analysis of vascular development in the mouse embryo. PloS One, 2008. 3(8), e2853.
Isogai S., Lawson N. D., Torrealday S., Horiguchi M., & Weinstein B.M. Angiogenic network formation in the developing vertebrate trunk. Development, 2003. 130(21), 5281-5290.
Koltowska K., Lagendijk A.K., Pichol-Thievend C., Fischer J.C., Francois M., Ober E.A., Hogan B.M. Vegfc regulates bipotential precursor division and Prox1 expression to promote lymphatic identity in zebrafish. Cell Reports, 2015. 13(9), 1828-1841.
Nicenboim J., Malkinson G., Lupo T., Asaf L., Sela Y., Mayseless O., Jerafi-Vider A. Lymphatic vessels arise from specialized angioblasts within a venous niche. Nature, 2015. 522(7554), 56.
Wigle J. T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell, 1999. 98(6), 769-778.
Yang Y., Garcia-Verdugo J.M., Soriano-Navarro M., Srinivasan R.S., Scallan J.P., Singh M.K., Oliver G. Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood, 2012. 120(11), 2340-2348.
Harvey N.L., Srinivasan R.S., Dillard M.E., Johnson N.C., Witte M.H., Boyd K., Oliver G. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nature Genetics, 2005. 37(10), 1072.
Hong Y.K., Harvey N., Noh Y.H., Schacht V., Hirakawa S., Detmar M., Oliver G. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Developmental Dynamics, 2002. 225(3), 351- 357. Обзоры 63 Вопросы реконструктивной и пластической хирургии № 3 (66) сентябрь’ 2018
Kim H., Nguyen V.P., Petrova T.V., Cruz M., Alitalo K., Dumont D.J. Embryonic vascular endothelial cells are malleable to reprogramming via Prox1 to a lymphatic gene signature. BMC Developmental Biology, 2010. 10(1), 72.
Srinivasan R.S., Dillard M.E., Lagutin O.V., Lin F.J., Tsai S., Tsai M.J., Oliver G. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes & Development, 2007. 21(19), 2422-2432.
Srinivasan R.S., Oliver G. Prox1 dosage controls the number of lymphatic endothelial cell progenitors and the formation of the lymphovenous valves. Genes & Development, 2011. 25(20), 2187-2197.
Hogan B.M., Bos F.L., Bussmann J., Witte M., Chi N. C., Duckers H.J., Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nature Genetics, 2009. 41(4), 396.
Lim A.H., Suli A., Yaniv K., Weinstein B., Li D.Y., Chien C.B. Motoneurons are essential for vascular pathfinding. Development, 2011. 138(17), 3847-3857.
Del Giacco L., Pistocchi A., Ghilardi A. Prox1b Activity is essential in zebrafish lymphangiogenesis. PLoS One, 2010. 5(10), e13170.
Francois M., Caprini A., Hosking B., Orsenigo F., Wilhelm D., Browne C., Davidson T. Sox18 induces development of the lymphatic vasculature in mice. Nature, 2008. 456(7222), 643.
Deng Y., Atri D., Eichmann A., Simons M. Endothelial ERK signaling controls lymphatic fate specification. The Journal of Clinical Investigation, 2013. 123(3), 1202-1215.
Duong T., Koltowska K., Pichol-Thievend C., Le Guen L., Fontaine F., Smith K.A.,.Koopman P. VEGFD regulates blood vascular development by modulating SOX18 activity. Blood, 2014. 123(7), 1102-1112.
Cermenati S., Moleri S., Cimbro S., Corti P., Del Giacco L., Amodeo R., Beltrame M. Sox18 and Sox7 play redundant roles in vascular development. Blood, 2008. 111(5), 2657-2666.
Cermenati S., Moleri S., Neyt C., Bresciani E., Carra S., Grassini D.R., Hogan B.M. Sox18 Genetically Interacts With VegfC to Regulate Lymphangiogenesis in ZebrafishSignificance. Arteriosclerosis, Thrombosis, and Vascular Biology, 2013. 33(6), 1238-1247.
You L.R., Lin F.J., Lee C.T., DeMayo F.J., Tsai M.J., Tsai S.Y. Suppression of Notch signalling by the COUPTFII transcription factor regulates vein identity. Nature, 2005. 435(7038), 98.
Srinivasan R.S., Geng X., Yang Y., Wang Y., Mukatira S., Studer M., Oliver G. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes & Development, 2010. 24(7), 696-707.
Clevers H. Wnt/.-catenin signaling in development and disease. Cell, 2006. 127(3), 469-480.
Wang R.N., Green J., Wang Z., Deng Y., Qiao M., Peabody M., Idowu O. Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes & Diseases, 2014. 1(1), 87-105.
Dunworth W.P., Cardona-Costa J., Bozkulak E.C., Kim J.D., Meadows S., Fischer J.C., Jin S.W. Bone morphogenetic protein 2 signaling negatively modulates lymphatic development in vertebrate embryosNovelty and Significance. Circulation Research, 2014. 114(1), 56-66.
Levet S., Ciais D., Merdzhanova G., Mallet C., Zimmers T.A., Lee S.J., Vittet D. Bone morphogenetic protein (BMP9) controls lymphatic vessel maturation and valve formation. Blood, 2013. 122(4), 598-607.
Yoshimatsu Y., Lee Y.G., Akatsu Y., Taguchi L., Suzuki H.I., Cunha S.I., Oh S.P. Bone morphogenetic protein-9 inhibits lymphatic vessel formation via activin receptor-like kinase 1 during development and cancer progression. Proceedings of the National Academy of Sciences, 2013. 110(47), 18940-18945.
Wiley D.M., Kim J.D., Hao J., Hong C.C., Bautch V.L., Jin S.W. Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nature Cell Biology, 2011. 13(6), 686.
Kashiwada T., Fukuhara S., Terai K., Tanaka T., Wakayama Y., Ando K., Gemma A.-catenin-dependent transcription is central to Bmp-mediated formation of venous vessels. Development, 2015. 142(3), 497-509.
Kim J.D., Kim J. Alk3/Alk3b and Smad5 Mediate BMP signaling during lymphatic development in Zebrafish. Molecules and cells, 2014. 37(3), 270.
Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Betsholtz C. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature Immunology, 2004. 5(1), 74.
eltsch M., Kaipainen A., Joukov V., Meng X., Lakso M., Rauvala H., Alitalo K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science, 1997. 276(5317), 1423-1425.
Kukk E., Lymboussaki A., Taira S., Kaipainen A., Jeltsch M., Joukov V., Alitalo K. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development, 1996. 122(12), 3829-3837.
Kaipainen A., Korhonen J., Mustonen T., Van Hinsbergh V.W., Fang G.H., Dumont D., Alitalo K. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proceedings of the National Academy of Sciences, 1995. 92(8), 3566-3570.
Makinen T., Veikkola T., Mustjoki S., Karpanen, T., Catimel B., Nice E. C., Stacker S. A. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF[1]C/D receptor VEGFR[1]3. The EMBO Journal, 2001. 20(17), 4762-4773.
Tammela T., Zarkada G., Wallgard E., Murtomaki A., Suchting S., Wirzenius M., Freitas C. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature, 2008. 454(7204), 656.
Covassin L.D., Villefranc J.A., Kacergis M.C., Weinstein B.M., Lawson N.D. Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proceedings of the National Academy of Sciences, 2006. 103(17), 6554-6559.
Siekmann A.F., Lawson N.D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature, 2007. 445(7129), 781.
van Impel A., Zhao Z., Hermkens D.M., Roukens M.G., Fischer J.C., Peterson-Maduro J., Schulte-Merker S. Divergence of zebrafish and mouse lymphatic cell fate specification pathways. Development, 2014. 141(6), 1228- 1238.
Dumont D.J., Jussila L., Taipale J., Lymboussaki A., Mustonen T., Pajusola K., Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science, 1998. 282(5390), 946-949.
Haiko P., Makinen T., Keskitalo S., Taipale J., Karkkainen M.J., Baldwin M.E., Alitalo K. Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Molecular and Cellular Biology, 2008). 28(15), 4843-4850.
Le Guen L., Karpanen T., Schulte D., Harris N. C., Koltowska K., Roukens G., Schulte-Merker S. Ccbe1 regulates Vegfc-mediated induction of Vegfr3 signaling during embryonic lymphangiogenesis. Development, 2014. 141(6), 1239-1249.
Srinivasan R.S., Escobedo N., Yang Y., Interiano A., Dillard M.E., Finkelstein D., Oliver G. The Prox1-Vegfr3 feedback loop maintains the identity and the number of lymphatic endothelial cell progenitors. Genes & Development, 2014. 28(19), 2175-2187.
Koltowska K., Paterson S., Bower N.I., Baillie G. J., Lagendijk A.K., Astin J.W., Simons C. mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish. Genes & Development, 2015. 29(15), 1618-1630.
Dieterich L.C., Klein S., Mathelier A., Sliwa-Primorac A., Ma Q., Hong Y.K., Kawaji H. DeepCAGE transcriptomics reveal an important role of the transcription factor MAFB in the lymphatic endothelium. C ell Reports, 2015. 13(7), 1493-1504.
Bos F.L., Caunt M., Peterson-Maduro J., Planas-Paz L., Kowalski J., Karpanen T., van Es J. H. CCBE1 Is Essential for Mammalian Lymphatic Vascular Development and Enhances the Lymphangiogenic Effect of Vascular Endothelial Growth Factor-C In VivoNovelty and Significance. Circulation Research, 2011. 109(5), 486-491.
Alders M., Hogan B.M., Gjini E., Salehi F., Al-Gazali L., Hennekam E. A., Prescott T. E. Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nature genetics, 2009. 41(12), 1272.
Zheng W., Tammela T., Yamamoto M., Anisimov A., Holopainen T., Kaijalainen S., Alitalo K. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood, 2011. 118(4), 1154-1162.
Fatima A., Culver A., Culver F., Liu T., Dietz W.H., Thomson B.R., Kume T. Murine Notch1 is required for lymphatic vascular morphogenesis during development. Developmental Dynamics, 2014). 243(7), 957-964.
Niessen K., Zhang G., Ridgway J. B., Chen H., Kolumam G., Siebel C.W., Yan M. The Notch1-Dll4 signaling pathway regulates mouse postnatal lymphatic development. Blood, 2011. 118(7), 1989-1997.
Geudens I., Herpers R., Hermans K., Segura I., De Almodovar C. R., Bussmann J., Claes F. Role of delta-like- 4/Notch in the formation and wiring of the lymphatic network in zebrafish. Arteriosclerosis, Thrombosis, and Vascular Biology, 2010. 30(9), 1695-1702.
