Lymphatic function and responses in periodontal disease

Experimental Cell Research

Volumn 325, Issue 2, 2014, Pages 130-137

  Berggreen, Ellen ^a   Wiig, Helge ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Edema; Lymph flow; Lymphatic growth factors; Periodontitis; Porphyromonas gingivalis; Vascular endothelial growth factor c

Indexed keywords

SECONDARY LYMPHOID TISSUE CHEMOKINE; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3;

ALVEOLAR BONE; BODY FLUID; CELL MIGRATION; DENDRITIC CELL; ENZYME ACTIVITY; EXTRAVASATION; GINGIVA; HUMAN; HUMORAL IMMUNITY; IMMUNOCOMPETENT CELL; INFLAMMATION; INTERSTITIAL FLUID; LAMINA PROPRIA; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; NONHUMAN; PERIODONTAL DISEASE; PERIODONTITIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); MUS; PORPHYROMONAS GINGIVALIS;

EDEMA; LYMPH FLOW; LYMPHATIC GROWTH FACTORS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

ANIMALS; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; MICE; PERIODONTAL DISEASES;

EID: 84902793442     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.12.006     Document Type: Review

References (58)

1. Alitalo K., Tammela T., Petrova T.V. Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953.
2. Norrmen C., Tammela T., Petrova T.V., Alitalo K. Biological basis of therapeutic lymphangiogenesis. Circulation 2011, 123:1335-1351.
3. Wiig H., Swartz M.A. Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer. Physiol. Rev. 2012, 92:1005-1060.
4. Mumprecht V., Detmar M. Lymphangiogenesis and cancer metastasis. J. Cell. Mol. Med. 2009, 13:1405-1416.
5. Schmid-Schonbein G.W. Microlymphatics and lymph flow. Physiol. Rev. 1990, 70:987-1028.
6. Keene D.R., Sakai L.Y., Lunstrum G.P., Morris N.P., Burgeson R.E. Type VII collagen forms an extended network of anchoring fibrils. J. Cell Biol. 1987, 104:611-621.
7. Leak L.V. The structure of lymphatic capillaries in lymph formation. Fed. Proc. 1976, 35:1863-1871.
8. Baluk P., Fuxe J., Hashizume H., Romano T., Lashnits E., Butz S., Vestweber D., Corada M., Molendini C., Dejana E., McDonald D.M. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 2007, 204:2349-2362.
9. Levick J.R., Michel C.C. Microvascular fluid exchange and the revised Starling principle. Cardiovasc. Res. 2010, 87:198-210.
10. Muthuchamy M., Zawieja D. Molecular regulation of lymphatic contractility. Ann. N.Y. Acad. Sci. 2008, 1131:89-99.
11. von der Weid P.Y., Muthuchamy M. Regulatory mechanisms in lymphatic vessel contraction under normal and inflammatory conditions. Pathophysiology 2010, 17:263-276.
12. Zawieja D.C., Gashev A.A. Microlymphatic biology. Compre. Physiol. 2011, 125-158. (v.d.W.P.-Y.).
13. Adair T.H., Moffatt D.S., Paulsen A.W., Guyton A.C. Quantitation of changes in lymph protein concentration during lymph node transit. Am. J. Physiol. 1982, 243:H351-359.
14. Randolph G.J., Angeli V., Swartz M.A. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 2005, 5:617-628.
15. Swartz M.A., Hubbell J.A., Reddy S.T. Lymphatic drainage function and its immunological implications: from dendritic cell homing to vaccine design. Sem. Immunol. 2008, 20:147-156.
16. Randolph G.J., Ochando J., Partida-Sanchez S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 2008, 26:293-316.
17. Jackson D.G. Immunological functions of hyaluronan and its receptors in the lymphatics. Immunol. Rev. 2009, 230:216-231.
18. Desch K., Li J., Kim S., Laventhal N., Metzger K., Siemieniak D., Ginsburg D. Analysis of informed consent document utilization in a minimal-risk genetic study. Ann. Intern. Med. 2011, 155:316-322.
19. Tammela T., Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010, 140:460-476.
20. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
21. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., Jones M., Jackson D.G. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 1999, 144:789-801.
22. Breiteneder-Geleff S., Soleiman A., Kowalski H., Horvat R., Amann G., Kriehuber E., Diem K., Weninger W., Tschachler E., Alitalo K., Kerjaschki D. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am. J. Pathol. 1999, 154:385-394.
23. Kaipainen A., Korhonen J., Mustonen T., van Hinsbergh V.W., Fang G.H., Dumont D., Breitman M., Alitalo K. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Nat. Acad. Sci. U.S.A. 1995, 92:3566-3570.
24. Jurisic G., Detmar M. Lymphatic endothelium in health and disease. Cell Tissue Res. 2009, 335:97-108.
25. Schulte-Merker S., Sabine A., Petrova T.V. Lymphatic vascular morphogenesis in development, physiology, and disease. J. Cell Biol. 2011, 193:607-618.
26. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahtinen I., Kukk E., Saksela O., Kalkkinen N., Alitalo K. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 1996, 15:290-298.
27. Achen M.G., Jeltsch M., Kukk E., Makinen T., Vitali A., Wilks A.F., Alitalo K., Stacker S.A. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc. Nat. Acad. Sci. U.S.A. 1998, 95:548-553.
28. Wiig H., Keskin D., Kalluri R. Interaction between the extracellular matrix and lymphatics: consequences for lymphangiogenesis and lymphatic function. Matrix Biol. 2010, 29:645-656.
29. Kim H., Kataru R.P., Koh G.Y. Regulation and implications of inflammatory lymphangiogenesis. Trends Immunol. 2012, 33:350-356.
30. Kajiya K., Sawane M., Huggenberger R., Detmar M. Activation of the VEGFR-3 pathway by VEGF-C attenuates UVB-induced edema formation and skin inflammation by promoting lymphangiogenesis. J. Invest. Dermatol. 2009, 129:1292-1298.
31. Huggenberger R., Ullmann S., Proulx S.T., Pytowski B., Alitalo K., Detmar M. Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J. Exp. Med. 2010, 207:2255-2269.
32. Huggenberger R., Siddiqui S.S., Brander D., Ullmann S., Zimmermann K., Antsiferova M., Werner S., Alitalo K., Detmar M. An important role of lymphatic vessel activation in limiting acute inflammation. Blood 2011, 117:4667-4678.
33. Kataru R.P., Jung K., Jang C., Yang H., Schwendener R.A., Baik J.E., Han S.H., Alitalo K., Koh G.Y. Critical role of CD11b+ macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 2009, 113:5650-5659.
34. Guo R., Zhou Q., Proulx S.T., Wood R., Ji R.C., Ritchlin C.T., Pytowski B., Zhu Z., Wang Y.J., Schwarz E.M., Xing L. Inhibition of lymphangiogenesis and lymphatic drainage via vascular endothelial growth factor receptor 3 blockade increases the severity of inflammation in a mouse model of chronic inflammatory arthritis. Arthritis Rheum. 2009, 60:2666-2676.
35. Zhou Q., Guo R., Wood R., Boyce B.F., Liang Q., Wang Y.J., Schwarz E.M., Xing L. Vascular endothelial growth factor C attenuates joint damage in chronic inflammatory arthritis by accelerating local lymphatic drainage in mice. Arthritis Rheum. 2011, 63:2318-2328.
36. Ushijima N., Inoue K., Domon T., Yoshida S. Distribution and organization of lymphatic vessels in the mouse gingiva: an immunohistochemical study with LYVE-1. Arch. Oral Biol. 2008, 53:652-658.
37. Bletsa A., Virtej A., Berggreen E. Vascular endothelial growth factors and receptors are up-regulated during development of apical periodontitis. J. Endodont. 2012, 38:628-635.
38. Virtej A., Loes S.S., Berggreen E., Bletsa A. Localization and signaling patterns of vascular endothelial growth factors and receptors in human periapical lesions. J. Endodont. 2013, 39:605-611.
39. Staszyk C., Duesterdieck K.F., Gasse H., Bienert A. Immunohistochemical identification of lymphatic vessels in the periodontium of equine cheek teeth. J. Vet. Dent. 2005, 22:227-232.
40. Makinen T., Jussila L., Veikkola T., Karpanen T., Kettunen M.I., Pulkkanen K.J., Kauppinen R., Jackson D.G., Kubo H., Nishikawa S., Yla-Herttuala S., Alitalo K. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat. Med. 2001, 7:199-205.
41. Mkonyi L.E., Bletsa A., Fristad I., Wiig H., Berggreen E. Importance of lymph vessels in the transcapillary fluid balance in the gingiva studied in a transgenic mouse model. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H275-283.
42. Mkonyi L.E., Bakken V., Sovik J.B., Mauland E.K., Fristad I., Barczyk M.M., Bletsa A., Berggreen E. Lymphangiogenesis is induced during development of periodontal disease. J. Dent. Res. 2012, 91:71-77.
43. Johnson N.C., Dillard M.E., Baluk P., McDonald D.M., Harvey N.L., Frase S.L., Oliver G. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008, 22:3282-3291.
44. Oliver G., Srinivasan R.S. Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development 2010, 137:363-372.
45. Del Fabbro M., Francetti L., Bulfamante G., Cribiu M., Miserocchi G., Weinstein R.L. Fluid dynamics of gingival tissues in transition from physiological condition to inflammation. J. Periodontol. 2001, 72:65-73.
46. Fjaertoft M., Johannessen A.C., Heyeraas K.J. Micropuncture measurements of interstitial fluid pressure in normal and inflamed gingiva in rats. J. Periodontal. Res. 1992, 27:534-538.
47. Aarli V., Heyeraas K.J. Effect of venous stasis and hypoproteinemia in gingival fluid formation in rats. J. Periodontal. Res. 1995, 30:231-237.
48. Mkonyi L.E., Bletsa A., Bolstad A.I., Bakken V., Wiig H., Berggreen E. Gingival lymphatic drainage protects against Porphyromonas gingivalis-induced bone loss in mice. Am. J. Pathol. 2012, 181:907-916.
49. Cueni L.N., Detmar M. New insights into the molecular control of the lymphatic vascular system and its role in disease. J. Invest. Dermatol. 2006, 126:2167-2177.
50. Baluk P., Yao L.C., Feng J., Romano T., Jung S.S., Schreiter J.L., Yan L., Shealy D.J., McDonald D.M. TNF-alpha drives remodeling of blood vessels and lymphatics in sustained airway inflammation in mice. J. Clin. Invest. 2009, 119:2954-2964.
51. Baluk P., Hogmalm A., Bry M., Alitalo K., Bry K., McDonald D.M. Transgenic overexpression of interleukin-1beta induces persistent lymphangiogenesis but not angiogenesis in mouse airways. Am. J. Pathol. 2013, 182:1434-1447.
52. Thomas S.N., Rutkowski J.M., Pasquier M., Kuan E.L., Alitalo K., Randolph G.J., Swartz M.A. Impaired humoral immunity and tolerance in K14-VEGFR-3-Ig mice that lack dermal lymphatic drainage. J. Immunol. 2012, 189:2181-2190.
53. Baluk P., Tammela T., Ator E., Lyubynska N., Achen M.G., Hicklin D.J., Jeltsch M., Petrova T.V., Pytowski B., Stacker S.A., Yla-Herttuala S., Jackson D.G., Alitalo K., McDonald D.M. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest. 2005, 115:247-257.
54. Kuroshima S., Sawa Y., Yamaoka Y., Notani K., Yoshida S., Inoue N. Expression of cys-cys chemokine ligand 21 on human gingival lymphatic vessels. Tissue Cell 2004, 36:121-127.
55. Vassileva G., Soto H., Zlotnik A., Nakano H., Kakiuchi T., Hedrick J.A., Lira S.A. The reduced expression of 6Ckine in the plt mouse results from the deletion of one of two 6Ckine genes. J. Exp. Med. 1999, 190:1183-1188.
56. Reynolds J.J. Collagenases and tissue inhibitors of metalloproteinases: a functional balance in tissue degradation. Oral Dis. 1996, 2:70-76.
57. Nomura T., Ishii A., Oishi Y., Kohma H., Hara K. Tissue inhibitors of metalloproteinases level and collagenase activity in gingival crevicular fluid: the relevance to periodontal diseases. Oral Dis. 1998, 4:231-240.
58. H. Wiig, Pathophysiology of tissue fluid accumulation in inflammation. J. Physiol. 2011 Jun 15, 589(Pt 12), 2945-2953. Epub 2011 Apr 11. http://dx.doi.org/10.1113/jphysiol.2011.206136.