Lymphatic System: Morphology and Pathology Update
Authors:
I. Kholová
Authors‘ workplace:
Pathology, Laboratory Centre, Tampere University Hospital, Tampere, Finland
Published in:
Čes.-slov. Patol., 46, 2010, No. 4, p. 98-103
Category:
Reviews Article
Overview
The lymphatic system is crucial for the maintenance of tissue fluid balance, immune surveillance, and fatty acids absorption in the intestine. The lymphatic vessels are also involved in the pathogenesis of tumor metastasis, lymphedema, and various inflammatory processes. Recently, several markers specific for lymphatic endothelium were found. Progress in the field of lymphatic growth factors and their receptors, and molecular lymphatic biology has helped to understand better the lymphatic vasculature. This review summarizes the updates on lymphatic system research and possible applications in routine pathological diagnostics.
Key words:
lymphangiogenesis – lymphatic system
Sources
1. Achen, M.G., McColl, B.K., Stacker, S.A.: Focus on lymphangiogenesis in tumor metastasis. Cancer Cell, 7, 2005, s. 121–127.
2. Asellius, G.: De lactibus sive lacteis venis. Milan: Mediolani, 1627.
3. Baldwin, M.E., Halford, M.M., Roufail, S. et al.: Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Mol. Cell. Biol., 25, 2005, s. 2441–2449.
4. Baluk, P., Tammela, T., Ator, E. et al.: Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest., 115, 2005, s. 247–257.
5. Bandarchi, B., Ma, L., Marginean, C., Hafezi, S., Zubovits, J., Rasty, G: D2-40, a novel immunohistochemical marker in differentiating dermatofibroma from dermatofibrosarcoma protuberans. Mod. Pathol., 23, 2010, s. 434–438.
6. Banerji, S., Ni, J., Wang S.X. et al.: LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell. Biol, 144, 1999, s. 789–801.
7. Beham, A.: Lymphangioma. In: Tumours of soft tissue and bone. Ed. Fletcher, Ch.D.M., Unni, K.K., Mertens, F. IARCPress, Lyon, 2002, s. 162–163.
8. Bellini, C., Boccardo, F., Campisi, C., Bonioli, E.: Congenital pulmonary lymphangiectasia. Orp. J. Rare Dis., 43, 2006, s. 43.
9. Bhardwaj, S., Roy, H., Gruchala, M. et al.: Angiogenic responses of vascular endothelial growth factors in periadventitial tissue. Hum. Gene Ther., 14, 2003, s. 1451–1462.
10. Breiteneder-Geleff, S., Soleiman, A., Kowalski, H. et al.: Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am. J. Pathol., 154, 1999, s. 385–394.
11. Cursiefen, C., Chen, L., Borges, L.P. et al.: VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Invest., 113, 2004, s. 1040–1050.
12. Dixelius, J., Makinen, T., Wirzenius, M. et al.: Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. J. Biol. Chem., 278, 2003, s. 40973–40979.
13. Eliskova, M., Eliska, O.: Light microscopy of the lymphatics of the human atrial wall and lymphatic drainage of supraventricular pacemakers. Int. Angiol., 8, 1989, s. 1–6.
14. Gale, N.W., Thurston, G., Hackett, S.F. et al.: Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell, 3, 2002, s. 411–423.
15. Harvey, N.L.: The link between lymphatic function and adipose biology. Ann. N. Y. Acad., 1131, 2008, s. 82–88.
16. Hirakawa, S., Kodama, S., Kunstfeld, R., Kajiya, K., Brown, L.F., Detmar, M.: VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastases. J. Exp. Med., 201, 2005, s. 1089–1099.
17. Hohman, D.W., Noghrehkar, D., Ratnayake, S.: Lymphangioleiomyomatosis: a review. Eur. J. Intern. Med., 19, 2008, s. 319-324.
18. Huang, X.Z., Wu, J.F., Ferrando, R. et al.: Fatal bilateral chylothorax in mice lacking integrin α91. Mol. Cell. Biol., 20, 2000, s. 5208–5215.
19. Huntington, G.C., McClure, C.F.W.: The anatomy and development of the jugular lymph sacs in the domestic cat (Felis domestica). Am. J. Anat., 10, 1910, s. 177–311.
20. Cho, C.-H., Koh, Y.J., Han, J. et al.: Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ. Res., 100, 2007, s. 47–57.
21. Chung, K.C., Kim, H.J., Jeffers, L.L.: Lymphangiosarcoma (Stewart-Treves syndrome) in postmastectomy patients. J. Hand Surg. Am., 25, 2000, s. 1163–1168.
22. Jussila, L., Valtola, R., Partanen, T.A. et al.: Lymphatic endothelium and Kaposi’s sarcoma spindle cells detected by antibodies against the vascular endothelial growth factor receptor-3. Cancer Res., 58, 1998, s. 1599–1604.
23. Kahn, H.J., Bailey, D., Marks, A.: Monoclonal antibody D2-40, a new marker of lymphatic endothelium, reacts with Kaposi’s sarcoma and subset of angiosarcomas. Mod. Pathol, 15, 2002, s. 434–440.
24. Kajiya, K., Detmar, M.: An important role of lymphatic vessels in the control of UVB-induced edema formation and inflammation. J. Invest. Dermatol., 126, 2006, 919–921.
25. Karkkainen, M.J., Haiko, P., Sainio K. et al.: Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol., 5, 2004, s. 74–80.
26. Karpanen, T., Alitalo K.: Molecular biology and pathology of lymphangiogenesis. Annu. Rev. Pathol. Mech. Dis., 3, 2008, s. 367–397.
27. Karpanen, T., Heckman, C.A., Keskitalo, S., et al.: Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J., 20, 2006, s. 1462–1472.
28. Kato S., Yasunaga, A., Uchida U.: Enzyme-histochemical method for identification of lymphatic capillaries. Lymphology, 24, 1991, s. 125–129.
29. Kerjaschki, D., Huttary, N., Raab, I. et al.: Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat. Med. 12, 2004, 230–234.
30. Kerjaschki, D., Regele, H.M., Moosberger, I. et al.: Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J. Am. Soc. Nephrol., 15, 2004, 603–612.
31. Kholová, I., Koota, S., Kaskenpaa, N. et al.: Adenovirus-mediated gene transfer of human vascular endothelial growth factor-d induces transient angiogenic effects in mouse hind limb muscle. Hum. Gene Ther., 2007, 18, s. 232–244.
32. Kunstfeld, R., Hirakawa, S., Hong, Y.K.: Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood, 104, 2004, s. 1048–1057.
33. Lakomec, J., Knuutila, S.: Kaposi sarcoma. In: Tumours of soft tissue and bone. Ed. Fletcher, Ch.D.M., Unni, K.K., Mertens, F. IARCPress, Lyon, 2002, s. 170–172.
34. Lewis, F.: The development of the lymphatic system in rabbits. Am. J. Anat., 5, 1905, s. 95–111.
35. Machnik, A., Neuhofer, W., Jantsch, J. et al.: Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat. Med., 15, 2009, s. 545–552.
36. Makinen, T., Adams, R.H., Bailey, J. et al.: PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev., 19, 2005, s. 397–410.
37. Mulvenna, P.M., Gillham, L., Regnard, C.F.: Lymphangiosarcomata - experience in a lymphoedema clinic. Palliat. Med., 9, 1995, s. 55–59.
38. Nagy, J.A., Vasile, E., Feng, D. et al.: Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J. Exp. Med., 196, 2002, s. 1497–1506.
39. Nilsson, I., Bahram, F., Li, X. et al.: VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J., 29, 2010, s. 1377–1388.
40. Nykänen, A.I., Sandelin, H., Krebs, R. et al.: Targeting lymphatic vessel activation and CCL21 production by vascular endothelial growth factor receptor-3 inhibition has novel immunomodulatory and antiatherosclerotic effects in cardiac allografts. Circulation, 121, 2010, s. 1413–1422.
41. Oliver G.: Lymphatic vasculature development. Nat. Rev. Immunol., 4, 2004, s. 35–45.
42. Petrova, T.V., Makinen, T., Makela, T.P. et al.: Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J., 21, 2002, s. 4593–4599.
43. Pharr, K.M., Debrah, A.Y., Specht, S., Hoerauf, A.: Filariasis and lymphoedema. Parasite Immunol., 31, 2009, s. 664–672.
44. Pratz, K.W., Dingli, D., Smyrk, T.C., Lust, J.A.: Intestinal lymphangiectasia with protein-losing enteropathy in Waldenström macroglobulinemia. Medicine (Baltimore), 86, 2007, s. 210–214.
45. Purhonen, S., Palm, J., Rossi D. et al.: Bone-marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc. Natl. Acad. Sci. USA., 312, 2008, s. 6620–6625.
46. Rissanen, T.T., Markkanen, J.E., Gruchala, M. et al.: VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ. Res., 92, 2003, s. 1098–1106.
47. Ristimäki, A., Narko, K., Enholm, B., Joukov, V., Alitalo, K.: Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem., 273, 1998, s. 8413-8418.
48. Saban, M.R., Memet, S., Jackson, D.G. et al.: Visualization of lymphatic vessels through NF-κB activity. Blood, 104, 2004, s. 3228–3230.
49. Sabin, F.R.: On the origin of lymphatic system from the veins and the development of the lymph hearts and thoracic ducts in the pig. Am. J. Anat., 1, 1902, s. 367–389.
50. Schacht, V., Ramirex, M.I., Hong, Y.K. et al.: T1α/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J., 22, 2003, s. 3546–3456.
51. Šteiner, I., Krbal, L., Dominik, J.: Blood vessels and lymphatics in calcific aortic stenosis – in support of its inflammatory pathogenesis. Ces.-slov. Patol., 46, 2010, s. 33–36.
52. Tammela, T., Alitalo, K.: Lymphangiogenesis: molecular mechanisms and future promise. Cell, 140, 2010, s. 460–476.
53. Tammela, T., Saaristo, A., Holopainen, T. et al.: Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat. Med., 13, 2007, s. 1458-1466.
54. Taveira-DaSilva, A.M., Steagall, W.K., Moss, J.: Lymphangioleiomyomatosis. Cancer Control., 13, 2006, s. 276-285.
55. Tobler, N.E., Detmar, M.: Tumor and lymph node lymphangiogenesis – impact on cancer metastais. J. Leukoc. Biol., 80, 2006, s. 691–696.
56. Upreti, L., Dev, A., Puri, S.K.: Imaging in renal lymphangiectasia: report of two cases and review of literature. Clin. Radiol., 2008, 63, s. 1057–1062.
57. Van Balkom, I.D., Alders, M., Allanson, J. et al.: Lymphedema-lymphangiectasia-mental retardation (Hennekam) syndrome: a review. Am. J. Med. Genet., 112, 2002, s. 412–421.
58. Verma, S.B.: Lymphangiectasias of the skin: victims of confusing nomenclature. Clin. Exp. Dermatol., 34, 2009, s. 566–569.
59. Vignes, S., Bellanger, J.: Primary intestinal lymphangiectasia (Waldmann’s disease). Orphanet J. Rare Dis., 3, 2008, s. 5.
60. Warren, A.G., Brorson, H., Borud, L.J., Slavin, S.A.: Lymphedema: a comprehensive review. Ann. Plast. Surg., 56, 2007, s. 464–472.
61. Wigle, J.T., Oliver, G.: Prox1 function is required for the development of the murine lymphatic system. Cell, 98, 1999, s. 769–778.
62. Wigle, J.T., Harvey, N., Detmar, M. et al.: An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J., 21, 2002, s. 1505–1513.
63. Wilting, J., Aref, Y., Huang, R. et al.: Dual origin of avian lymphatics. Dev. Biol., 292, 2006, s. 165–173.
64. Xu, X., Lin, H., LV, H., Zhang, M., Zhang, Y.: Adventitial lymphatic vessels – an important role in atherosclerosis. Med. Hypotheses, 69, 2007, s. 1238–1241.
65. Yuan L., Moyon, D., Pardanaud, L. et al.: Abnormal lymphatic development in neuropilin 2 mutant mice. Development, 129, 2002, s. 4797–4806.
Labels
Anatomical pathology Forensic medical examiner ToxicologyArticle was published in
Czecho-Slovak Pathology
2010 Issue 4
Most read in this issue
- Muir-Torre Syndrome – a Phenotypic Variant of Lynch Syndrome
- Lymphatic System: Morphology and Pathology Update
- IgG4-related Systemic Sclerosing Disease: a Review
- Prolonged Treatment of Chronic Renal Insufficiency, Acquired Cystic Kidney Disease, Simultaneous Precancerous Lesions and Multiple Tumors of Left Kidney