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Development and Patterning of the Cardiac Lymphatic Network

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The Cardiac Lymphatic System

Abstract

An overview of the prenatal development of the cardiac lymphatic system can be achieved only when it is seen in the general context of prenatal morphogenesis of the heart. Moreover, since it was found that the development of the cardiac lymphatic network follows, in time and place, that of the coronary blood vessels, cardiac lymphangiogenesis cannot be fully understood without knowledge about the essential steps in the development of the blood supply of the developing heart. We therefore start this chapter with short descriptions of both the morphogenesis of the human embryonic heart and the development of its blood supply, and we will then focus on the development of the cardiac lymphatic system.

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References

  1. Vincent SD, Buckingham ME (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90:1–41

    Article  PubMed  Google Scholar 

  2. Van den Berg G, Moorman AFM (2009) Concepts of cardiac development in retrospect. Pediatr Cardiol 30:580–587

    Article  PubMed  Google Scholar 

  3. Davis CL (1927) The development of the human heart from its first appearance to the stage found in embryos of twenty paired somites. Contrib Embryol 19:245–284

    Google Scholar 

  4. Männer J (2009) The anatomy of cardiac looping: a step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin Anat 22:21–35

    Article  PubMed  Google Scholar 

  5. Moorman A, Webb S, Brown NA, Lamers W, Anderson RH (2003) Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 89:806–814

    Article  PubMed  Google Scholar 

  6. Licata JM (1954) The human embryonic heart in the ninth week. Am J Anat 94:73–125

    Article  CAS  PubMed  Google Scholar 

  7. Kampmeier OF (1928) On the lymph flow of the human heart, with reference to the development of the channels and the first appearance, distribution, and physiology of their valves. Am Heart J 4:210–222

    Article  Google Scholar 

  8. Rychter Z, Jelinek R, Klika E, Antalikova L (1971) Development of the lymph bed in the wall of the chick embryo heart. Physiol Bohemoslov 20:533–539

    CAS  PubMed  Google Scholar 

  9. Britten S, Soenksen DM, Bustillo M, Coulam CB (1994) Very early (24–56 days from the last menstrual period) embryonic heart rate in normal pregnancies. Hum Reprod 9:2424–2426

    CAS  PubMed  Google Scholar 

  10. Wisser J, Dirschedl P (1994) Embryonic heart rate in dated human embryos. Early Hum Dev 37:107–115

    Article  CAS  PubMed  Google Scholar 

  11. Männer J, Thrane L, Norozi K, Yelbuz TM (2008) High resolution in vivo imaging of the cross-sectional deformations of contracting embryonic heart loops using optical coherence tomography. Dev Dyn 237:953–961

    Article  PubMed  Google Scholar 

  12. Icardo JM, Fernandez-Terán A (1987) Morphological study of ventricular trabeculation in the embryonic heart. Acta Anat 130:264–274

    Article  CAS  PubMed  Google Scholar 

  13. Männer J, Thrane L, Norozi K, Yelbuz TM (2009) In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function. Dev Dyn 238:3273–3284

    Article  PubMed  Google Scholar 

  14. Hirakow R (1989) Epicardial formation in staged human embryos. Acta Anat Nippon 67:616–622

    Google Scholar 

  15. Männer J, Pérez-Pomarez JM, Macías D, Muñoz-Chápuli R (2001) The origin, formation, and developmental significance of the epicardium: a review. Cells Tissues Organs 169:89–103

    Article  PubMed  Google Scholar 

  16. Peshkovsky C, Totong R, Yelon D (2011) Dependence of cardiac trabeculation on neuregulin signaling and blood flow in zebrafish. Dev Dyn 240:446–456

    Article  PubMed  Google Scholar 

  17. Hutchins GM, Kessler-Hanna A, Moore GW (1988) Development of the coronary arteries in the embryonic human heart. Circulation 77:1250–1257

    Article  CAS  PubMed  Google Scholar 

  18. Rudbeck O (1653) Nova exercitatio anatomica exhibens Ductus Hepaticos Aquosos et Vasa Glandularum Serosa, nunc primum in venta, aeneisque figuris delineata. Arosia

    Google Scholar 

  19. Mascagni P (1787) Vasorum Lymphaticorum Corporis Humani Descriptio et Iconographia. Pazzini Carli, Siena, Italy

    Google Scholar 

  20. Rusznyak I, Földi M, Szabo G (1969) Lymphologie: Physiologie und Pathologie der Lymphgefässe und des Lymphkreislaufes. G. Fischer, Stuttgart, Germany, p 625

    Google Scholar 

  21. Eberth CJ, Belajeff A (1886) Über die lymphgefässe des Herzens. Arch Pathol Anat 37:124

    Google Scholar 

  22. Sacchi G, Weber E, Aglianò M, Cavina N, Comparini L (1999) Lymphatic vessels of the human heart: precollectors and collecting vessels: a morpho-structural study. J Submicrosc Cytol Pathol 31:515–525

    CAS  PubMed  Google Scholar 

  23. Kubik S (2003) Anatomy of the lymphatic system. In: Földi M, Földi E, Kubik S (eds) Textbook of lymphology. Urban und Fischer Verlag/Elsevier GmbH, München, Germany, pp 2–166

    Google Scholar 

  24. Van der Putte SCJ (1975) The development of the lymphatic system in man. Adv Anat Embryol Cell Biol 51:1–60

    Google Scholar 

  25. Breier G, Breviario F, Caveda L et al (1966) Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 87:630–641

    Google Scholar 

  26. Wigle JT, Oliver G (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98:769–778

    Article  CAS  PubMed  Google Scholar 

  27. Cash JR (1917) On the development of the lymphatics in the heart of the embryo pig. Anat Rec 13:451–464

    Article  Google Scholar 

  28. Klika E, Antalikova L, Rychter Z, Jelinek R (1972) Inception and manner of development of the lymph vessels in the chick embryo heart. Lymphology 5:137–148

    CAS  PubMed  Google Scholar 

  29. Riquet M, Briere J, Dupont P, Pennhouat G, Hidden G (1993) The embryonic and early fetal development of the lymphatics of the heart and lungs in humans. Surg Radiol Anat 15:369–370

    Article  CAS  PubMed  Google Scholar 

  30. Wilting J, Buttler K, Schulte I, Papoutsi M, Schweigerer L, Männer J (2007) The proepicardium of avian embryo delivers hemangioblasts but not lymphangioblasts to the developing heart. Dev Biol 305:451–459

    Article  CAS  PubMed  Google Scholar 

  31. Kuratani S, Tanaka S (1990) Peripheral development of the avian vagus nerve with special reference to the morphological innervation of heart and lung. Anat Embryol 182:435–445

    Article  CAS  PubMed  Google Scholar 

  32. Verberne ME, Gittenberger-de Groot AC, Poelmann RE (1998) Lineage and development of the parasympathetic nervous system of the embryonic chick heart. Anat Embryol 198:171–184

    Article  CAS  PubMed  Google Scholar 

  33. Mäkinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, Pulkkanen KJ et al (2001) Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 7:199–205

    Article  PubMed  Google Scholar 

  34. Xu Y, Yuan L, Mak J, Pardanaud L, Caunt M, Kasman I et al (2010) Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J Cell Biol 188:115–130

    Article  CAS  PubMed  Google Scholar 

  35. Le Douarin NM (2008) Developmental patterning deciphered in avian chimeras. Dev Growth Differ 50(suppl 1):S11–S28

    Article  PubMed  Google Scholar 

  36. Vajda J, Tomcsik M, van Doorenmaalen WJ (1972) Connections between the venous system of the heart and the epicardiac lymphatic network. Acta Anat (Basel) 83(2):262–274

    Article  CAS  Google Scholar 

  37. Sabin FR (1902) On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am J Anat 1:367–389

    Article  Google Scholar 

  38. François M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C et al (2008) Sox18 induces development of the lymphatic vasculature in mice. Nature 456:643–647

    Article  PubMed  Google Scholar 

  39. Schoppmann SF, Birner P, Stöckl J, Kalt R, Ullrich R, Caucig C et al (2002) Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161:947–956

    Article  CAS  PubMed  Google Scholar 

  40. Buttler K, Kreysing A, von Kaisenberg CS, Schweigerer L, Gale N, Papoutsi M et al (2006) Mesenchymal cells with leukocyte and lymphendothelial characteristics in murine embryos. Dev Dyn 235:1554–1562

    Article  CAS  PubMed  Google Scholar 

  41. Barozzi P, Luppi M, Facchetti F, Mecucci C, Alù M, Sarid R et al (2003) Post-transplant Kaposi sarcoma originates from the seeding of donor-derived progenitors. Nat Med 9:554–561

    Article  CAS  PubMed  Google Scholar 

  42. Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, Bartel G et al (2006) Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12:230–234

    Article  CAS  PubMed  Google Scholar 

  43. Juszynski M, Ciszek B, Stachurska E, Jablonska A, Ratajska A (2008) Development of lymphatic vessels in mouse embryonic and postnatal hearts. Dev Dyn 237:2973–2986

    Article  PubMed  Google Scholar 

  44. Karunamuni G, Yang K, Doughman YQ, Wikenheiser J, Bader D, Barnett J et al (2010) Expression of lymphatic markers during avian and mouse cardiogenesis. Anat Rec 293:259–270

    Article  CAS  Google Scholar 

  45. Flaht A, Jankowska-Steifer E, Radomska DM, Madej M, Gula G, Kujawa M et al (2012) Cellular phenotypes and spatio-temporal patterns of lymphatic vessel development in embryonic mouse hearts. Dev Dyn 241:1473–1486

    Article  CAS  PubMed  Google Scholar 

  46. Laine GA, Allen SJ (1991) Left ventricular myocardial edema. Lymph flow, interstitial fibrosis, and cardiac function. Circ Res 68:1713–1721

    Article  CAS  PubMed  Google Scholar 

  47. Cui Y (2010) Impact of lymphatic vessels on the heart. Thorac Cardiovasc Surg 58:1–7

    Article  CAS  PubMed  Google Scholar 

  48. Friedrich MG (2010) Myocardial edema: a new clinical entity? Nat Rev Cardiol 7:292–296

    PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, University Medicine Gottingen, Kreuzbergring 36, Goettingen, 37075, Germany

    Jörg Wilting

  2. Department of Anatomy and Embryology, University Medicine Gottingen, Kreuzbergring 36, Goettingen, 37075, Germany

    Jörg Männer

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  1. Jörg Wilting
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  2. Jörg Männer
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Correspondence to Jörg Wilting .

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Editors and Affiliations

  1. School of Medicine, Case Western Reserve University, 10900 Euclid Ave, Cleveland, 44106, Ohio, USA

    Ganga Karunamuni

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Wilting, J., Männer, J. (2013). Development and Patterning of the Cardiac Lymphatic Network. In: Karunamuni, G. (eds) The Cardiac Lymphatic System. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6774-8_2

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