Role of the lymphatics in cancer metastasis and chemotherapy applications

Advanced Drug Delivery Reviews

Volumn 63, Issue 10-11, 2011, Pages 867-875

  McAllaster, Jennifer D ^a   Cohen, Mark S ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Lymphangiogenesis; Lymphatic anatomy; Lymphatic endothelial cells; Lymphatic metastasis; Lymphatic vasculature; Vascular endothelial growth factors

Indexed keywords

LYMPHANGIOGENESIS; LYMPHATIC ANATOMY; LYMPHATIC ENDOTHELIAL CELLS; LYMPHATIC METASTASIS; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULATURE;

CHEMOTHERAPY; DISEASES; ENDOTHELIAL CELLS;

PATHOLOGY;

ANGIOPOIETIN 2; ANTINEOPLASTIC AGENT; CHEMOKINE RECEPTOR CCR7; CISPLATIN; COMMON LYMPHATIC ENDOTHELIAL AND VASCULAR ENDOTHELIAL RECEPTOR 1; HOMEODOMAIN PROTEIN; HYALURONIC ACID; HYALURONIC ACID MEMBRANE RECEPTOR 1; LIPOSOME; MACROGOL; MANNOSE RECEPTOR; MEMBRANE RECEPTOR; MONOCLONAL ANTIBODY; NEUROPILIN 2; PACLITAXEL; PHOSPHATIDYLSERINE; PODOPLANIN; POLYGLACTIN; PROSPERO RELATED HOMEOBOX 1 PROTEIN; PROTEIN TYROSINE KINASE INHIBITOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER INVASION; CYTOKINE RELEASE; DRUG DELIVERY SYSTEM; DRUG TARGETING; ENDOTHELIUM CELL; FIBROSARCOMA; HUMAN; HYDROPHILICITY; LIPOPHILICITY; LUNG METASTASIS; LYMPH NODE METASTASIS; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; LYMPHATIC DRAINAGE; LYMPHATIC SYSTEM; LYMPHOCYTE MIGRATION; MALIGNANT NEOPLASTIC DISEASE; MEDICAL RESEARCH; MELANOMA; METASTASIS POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REVIEW; STOMACH CANCER; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL MARKERS; DRUG DELIVERY SYSTEMS; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; LYMPHATIC SYSTEM; NEOPLASMS;

EID: 80052183833     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2011.05.014     Document Type: Review

References (151)

1. Assellius G. De lactibus sive lacteis venis 1627, Mediolani, Milan.
2. Oliver G. Lymphatic vasculature development. Nat. Rev. Immunol. 2004, 4:35-45.
3. Sabin F.R. On the origin of the lymphatic system from the veins and the development of the lymph heart and thoracic duct in the pig. Am. J. Anat. 1902, 1:367-391.
4. Huntingon S.C., McClure C.F.W. The anatomy and development of the jugular lymph sacs in the domestic cat (Felis domestica). Am. J. Anat. 1910, 10:177-311.
5. Wilting J., Aref Y., Huang R., Tomarev S.I., Schweigerer L., Christ B., Valasek P., Papoutsi M. Dual origin of avian lymphatics. Dev. Biol. 2006, 292:165-173.
6. Srinivasan R.S., Dillard M.E., Lagutin O.V., Lin F.J., Tsai S., Tsai M.J., Samokhvalov I.M., Oliver G. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev. 2007, 21:242-243.
7. Wigle J.T., Harvey N., Detmar M., Lagutina I., Grosveld G., Gunn M.D., Jackson D.G., Oliver G. An essential role for Prox1 in the induction of the lymphatic endothelial cellphenotype. EMBO J. 2002, 21:1505-1513.
8. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
9. Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., Weinstein B.M. Live imaging of lymphatic development in the zebrafish. Nat Med. 2006, 12:711-716.
10. Rinderknacht M., Detmar M. Tumor lymphangiogenesis and melanoma metastasis. J. Cell. Physiol. 2008, 216(2):347-354.
11. Maby-El Hajjami H., Petrova T.V. Developmental and pathological lymphangiogenesis: from modles to human disease. Histochem. Cell Biol. 2008, 130(6):1063-1078.
12. Oliver G., Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev. 2002, 16:773-783.
13. Alitalo K., Tammela T., Petrova T.V. Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953.
14. 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.
15. Cardiovascular Physiology 2006, Lange. 6th ed. D.E. Mohrman, L.J. Heller (Eds.).
16. Moghimi S.M., Rajabi-Siahboomi A.R. Advanced colloid-based systems for efficient delivery of drugs and diagnostic agents to the lymphatic tissues. Prog. Biophys. Mol. Biol. 1996, 65:221-249.
17. Leak L.V. The structure of lymphatic capillaries in lymph formation. Fed. Proc. 1976, 35:1863-1871.
18. Gerli R., Solito R., Weber E., Agliano M. Specific adhesion molecules bind anchoring filaments and endothelial cells in human skin initial lymphatics. Lymphology 2000, 33:148-157.
19. Solito R., Alessandrini C., Fruschelli M., Pucci A.M., Gerli R. An immunological correlation between the anchoring filaments of initial lymph vessels and the neighboring elastic fibers: a unified morphofunctional concept. Lymphology 1997, 30:194-202.
20. Schmid-Schonbein G. The second valve system in lymphatics. Lymphat. Res. Biol. 2003, 1:25-29.
21. Trzewik J., Mallipattu S.K., Artmann G.M., Delano F.A., Schmid-Schonbein G.W. Evidence for a second valve system in lymphatics: endothelial microvalves. FASEB J. 2001, 15:1711-1717.
22. Rinderknecht M., Detmar M. Tumor lymphangiogenesis and melanoma metastasis. J. Cell Physiol. 2008, 216(2):347-354.
23. Sharma R., Wendt J.A., Rasmussen J.C., Adams K.E., Marshall M.V., Sevick-Muraca E.M. New Horizons for Imaging Lymphatic Function. Ann. N. Y. Acad. Sci. 2008, 1131:13-36.
24. Leake L.V., Burke J.F. Fine structure of the lymphatic capillary and the adjoining connective tissue area. Am. J. Anat. 1966, 118:785-809.
25. von der Weid P.Y., Zawieja D.C. Lymphatic smooth muscle: the motor unit of lymph drainage. Int. J. Biochem. Cell Biol. 2004, 36:1147-1153.
26. Casley-Smith J. The fine structure and functioning of tissue channels and lymphatics. Lymphology 1980, 13:177-183.
27. Moore Clinically oriented anatomy 1985, 42-45. Williams & Wilkins, Baltimore.
28. Tervala T., Suominen E., Saaristo A. Targeted treatment for lymphedema and lymphatic metastasis. Ann. N. Y. Acad. Sci. 2008, 1131:215-224.
29. Oliver G., Harvey N. A stepwise model of the development of lymphatic vasculature. Ann. N. Y. Acad. Sci. 2002, 979:159-165. discussion 188-196.
30. Jussila L., Alitalo K. Vascular growth factors and lymphangiogenesis. Physiol. Rev. 2002, 82:673-700.
31. Dumont D.J., Jussila L., Taipale J., Lymboussaki A., Mustonen T., Pajusola K., Breitman M., Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 1998, 282:946-949.
32. 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. Natl. Acad. Sci. U. S. A. 1995, 92:3566-3570.
33. Makinen T., Veikkola T., Mustjoki S., Karpanen T., Catimel B., Nice E.C., Wise L., Mercer A., Kowalski H., Kerjaschki D., Stacker S.A., Achen M.G., Alitalo K. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 2001, 20:4762-4773.
34. Veikkola T., Karkkainen M., Claesson-Welsh L., Alitalo K. Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res. 2000, 60:203-212.
35. 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. Natl. Acad. Sci. 1998, 95:548-553.
36. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahatinen 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 trosine kinases. EMBO J. 1996, 15:290-298.
37. Enholm B., Karpanen T., Jeltsch M., Kubo H., Stenback F., Prevo R., Jackson D.G., Yla-herttuala S., Alitalo K. Adeno-viral expression of bascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ. Res. 2001, 88:623-629.
38. Jeltsch M., Kaipainen A., Joukov V., Meng X., Lakso M., Rauvala H., Swartz M., Fukumura D., Jain R.K., Alitalo K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 1997, 276:1423-1425.
39. Kaipainen A., Korhonen J., Pajusola K., Aprelikova O., Persico M.G., Terman B.I., Alitalo K. The related FLT4, FLT1, and KDR receptor tyrosine kinases show distinct expression patterns in human fteal endothelial cells. J. Exp. Med. 1993, 178:2077-2088.
40. Oh S.J., Jeltsch M.M., Birkenhager R., McCarthy J.E., Weich H.A., Christ B., Alitalo K., Wilting J. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol. 1997, 188:96-109.
41. Nakamura K., Rockson S.G. Molecular targets for therapetic lymphangiogenesis in lmphatic dysfunction and disease. Lymphat. Res. Biol. 2008, 6(3-4):181-189.
42. Gale N.W., Thurston G., Hackett S.F., Renard R., Wang Q., McClain J., Martin C., Witte C., Witte M.H., Jackson D., Suri C., Campochiaro P.A., Wiegand S.J., Yancopoulos G.D. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell 2002, 3:411-423.
43. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Bucholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376:70-74.
44. Suri C., Jones P.F., Patan S., Bartunkova S., Maisonpierre P.C., Davis S., Sato T.N., Yancopoulos G.D. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-2280.
45. Hong Y.K., Harvey N., Noh Y.H., Schacht V., Kirakawa S., Detmar M., Oliver G. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 2002, 225:351-357.
46. Petrova T.V. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homebox transcription factor. EMBO J. 2002, 21:4593-4599.
47. Mishima K., Watabe T., Saito A., Yoshimatsu Y., Imaizumi N., Masui S., Hirashima M., Morisada T., Oike Y., Araie M., Niwa H., Kubo H., Suda T., Miyazono K. Prox1 induces lymphatic endothelial differentiation via integrin [alpha]9 and other signaling casades. Mol. Biol. Cell 2007, 18:1421-1429.
48. Grainger R.M. Embryonic lens induction: shedding light on vertebrate tissue determination. Trends Genet. 1992, 8:349-355.
49. Tammela T. The biology of vascular endothelial growth factors. Cardiovasc. Res. 2005, 65:550-563.
50. Karkkainen M.J., Saaristo A., Jussila L., Karila K.A., Lawrence E.C., Pajusola K., Bueler H., Eichmann A., Kauppinen R., Kettunen M.I., YlA-Herttuala S., Finegold D.N., Ferrell R.E., Alitalo K. A model for gene therapy of human hereditary lymphedema. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12677-12682.
51. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., Betsholtz C., Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
52. Enholm B., Karpanen T., Jeltsch M., Kubo H., Stenback F., Prevo R., Jackson D.G., Yla-herttuala S., Alitalo K. Adeno-viral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ. Res. 2001, 88:623-629.
53. Baldwin M.E., Halford M.M., Roufail S., Williams R.A., Hibbs M.L., Grail D., Kubo H., Stacker S.A., Achen M.G. Vascular endothelial growth factor d is dispensable for development of the lymphatic system. Mol. Cell. Biol. 2005, 25:2441-2449.
54. Achen M.G., Stacker S.A. Tumor lymphangiogenesis and metastatic spread-new players begin to emerge. Int. J. Cancer 2006, 119:1755-1760.
55. Schoppmann S.F., Birner P., Stockl J., Kalt R., Ullrich R., Caucig C., Kriehuber E., Nagy K., Alitalo K., Kerjaschki D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol. 2002, 161:947-956.
56. Cursiefen C., Chen L., Borges L.P., Jackson D., Cao J., Radziejewski C., D'Amore P.A., Dana M.R., Wiegand S.J., Streilein J.W. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Invest. 2004, 113:1040-1050.
57. 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.
58. Wirzenius M., Tammela T., Uutela M., He Y., Odorisio T., Zambruno G., Nagy J.A., Dvorak H.F., Yla-Herttuala S., Shibuya M., Alitalo K. Distinct vascular endothelial growth factor signals for lymphatic vessel enlargement and sprouting. J. Exp. Med. 2007, 204:1431-1440.
59. Yuan L. Abnormal lymphatic vessel development in neuropilin 2 mice. Development 2002, 129:4797-4806.
60. Wang J.F., Zhang X.F., Groopman J.E. Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. J. Biol. Chem. 2001, 276:41950-41957.
61. Huang X.Z. Fatal bilateral chylothorax in mice lacking the integrin a9b1. Mol. Cell. Biol. 2000, 20:5208-5215.
62. Banziger-Tobler N.E., Halin C., Kajiya K., Detmar M. Growth hormone promotes lymphangiogenesis. Am. J. Pathol. 2008, 173:586-597.
63. Bjorndahl M., Cao R., Nissen L.J., Clasper S., Johnson L.A., Xue Y., Zhou Z., Jackson D., Cao Y. Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15593-15598.
64. Hartveit E. Attenuated cells in breast stroma: the missing lymphatic system of the breast. Histopathology 1990, 16:533-543.
65. Ji R.C. Lymphatic endothelial cells, lymphangiogenesis, and extracellular matrix. Lymphat. Res. Biol. 2006, 4:83-100.
66. Koyama H., Kobayashi N., Harada M., Takeoka M., Kawai Y., Sano K., Fujimori M., Amano J., Ohhashi T., Kannagi R., Kimata K., Taniguchi S., Itano N. Significance of tumor-associated stroma in promotion of intratumoral lymphangiogenesis: pivotal role of a hyaluronan-rich tumor microenvironment. Am. J. Pathol. 2008, 172:179-193.
67. Dadras S.S., Lange-Asschenfeldt B., Velasco P., Nguyen L., Vora A., Muzikansky A., Jahnke K., Hauschild A., Hirakawa S., Mihm M.C., Detmar M. Tumor lymphangiogenesis predicts melanoma metastsis to sentinel lymph nodes. Mod. Pathol. 2005, 18:1232-1242.
68. Stacker S.A. Lymphangiogenesis and cancer metastasis. Nat. Rev. Cancer 2002, 2:573-583.
69. Achen M.G. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 2005, 7:121-127.
70. Ji R.C. Lymphatic endothelial cells, inflammatory lymphangiogenesis, and prospective players. Curr. Med. Chem. 2007, 14:2359-2368.
71. Dadras S.S., Paul T., Bertoncini J., Brown L.F., Muzikansky A., Jackson D.G., Ellwanger U., Garbe C., Mihm M.C., Detmar M. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am. J. Pathol. 2003, 162:1951-1960.
72. Hirakawa S., Brown L.F., Kodama S., Paavonen K., Alitalo K., Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 2007, 109:1010-1017.
73. Mandriota S.J., Jussila L., Jeltsch M., Compagni A., Baetens D., Prevo R., Banerji S., Huarte J., Montesano R., Jackson D.G., Orci L., Alitalo K., Christofori G., Pepper M.S. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J. 2001, 20:672-682.
74. Skobe M., Hawighorst T., Jackson D.G., Prevo R., Janes L., Velasco P., Riccardi L., Alitalo K., Claffey K., Detmar M. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med. 2001, 7:192-198.
75. Mandriota S.J., Jussila L., Jeltsch M., Compagni A., Baetens D., Prevo R., Banerji S., Huarte J., Montesano R., Jackson D.G., Orci L., Alitalo K., Christofori G., Pepper M.S. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J. 2001, 20:672-682.
76. Skobe M., Hawighorst T., Jackson D.G., Prevo R., Janes L., Velasco P., Riccardi L., Alitalo K., Claffey K., Detmar M. Induction of tumor lymphangiogenesis by VEGF-C promotoes breast cancer metastasis. Nat Med. 2001, 7:192-198.
77. Stacker S.A., Casesar C., Baldwin M.E., Thornton G.E., Williams R.A., Prevo R., Jackson D.G., Nishikawa S., Kubo H., Achen M.G. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med. 2001, 7:186-191.
78. Stacker S.A., Baldwin M.E., Achen M.G. The role of tumor lymphangiogenesis in metastatic spread. FASEB J. 2002, 16:922-934.
79. Achen M.C., Stacker S.A. Molecular control of lymphatic metastasis. Ann. N. Y. Acad. Sci. 2008, 1131:225-234.
80. Karpanen T. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 2001, 61:1786-1790.
81. Hoshida T. Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res. 2006, 66:8065-8075.
82. Harrell M.I., Iritani B.M., Ruddell A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am. J. Pathol. 2007, 170:774-786.
83. Padera T.P. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002, 296:1883-1886.
84. Pepper M.S. Lymphangiogenesis and tumor metastasis. Cell Tissue Res. 2003, 314:167-177.
85. Goydos J.S., Gorski D.H. Vascular endothelial growth factor C mRNA expression correlates with stage of progression in patients with melanoma. Clin. Cancer Res. 2003, 9:5962-5967.
86. Enholm B. Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoprotiens and hypoxia. Oncogene 1997, 14:2475-2483.
87. Schoppmann S.F. VEGF-C expressing tumor-associated macrophages in lymph node positive breast cancer: impact on lymphangiogenesis and survival. Surgery 2006, 139:839-846.
88. Das S., Skobe M. Lymphatic vessel activation in cancer. Ann. N. Y. Acad. Sci. 2008, 1131:235-241.
89. Ray P.S., Fox P.L. A post-transcriptional pathway represses monocyte VEGF-A expression and angiogenic activity. EMBO J. 2007, 26:3360-3372.
90. Chen L., Marble D.J., Agha R., Peterson J.D., Becker R.P., Jin T., Li J., Chan L.S. The progression of inflammation parallels the dermal angiogenesis in a keratin 14 IL-4-transgenic model of atopic dermatitis. Microcirculation 2008, 15:49-64.
91. Halin C., Tobler N.E., Vigl B., Brown L.F., Detmar M. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 2007, 110:3158-3167.
92. Dixelius J., Makinen T., Wirzenius M., Karkkainen M.J., Wernstedt C., Alitalo K., Claesson-Welsh L. 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. 2003, 278:40973-40979.
93. Hong Y.K., Lange-Asschenfeldt B., Velasco P., Hirakawa S., Kunstfeld R., Brown L.F., Bohlen P., Senger D.R., Detmar M. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins. FASEB J. 2004, 18:1111-1113.
94. Stacker S.A., Achen M.G. From anti-angiogenesis to anti-lymphangiogenesis: emerging trends in cancer therapy. Lymphat. Res. Biol. 2008, 6(3-4):165-172.
95. Qian C.N. Preparing the "soil": the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 2006, 66:10365-10367.
96. Van Den Eynden C.G. Induction of lymphangiogenesis in and around axillary lymph node metastases of patients with breast cancer. Br. J. Cancer 2006, 95:1362-1366.
97. Hirakawa S. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J. Exp. Med. 2005, 201:1089-1099.
98. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889, 1:571-573.
99. Van Den Eynden G.G. Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node. Clin. Cancer Res. 2007, 13:5391-5397.
100. Podrgrabinska S. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:16069-16074.
101. Gunn M.D., Tangemann K., Tam C., Cyster J.G., Rosen S.D., Williams L.T. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naïve T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:258-263.
102. Wiley H.E., Gonzalez E.B., Maki W., Wu M.T., Hwang S.T. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J. Natl. Cancer Inst. 2001, 93:1638-1643.
103. Irjala H. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J. Exp. Med. 2001, 194:1033-1042.
104. Irjala H. The same endothelial receptor controls lymphocyte traffic both in vascular and lymphatic vessels. Eur. J. Immunol. 2003, 33:815-824.
105. Irjala H. Mannose receptor (MR) and common lymphatic endothelial and vascular endothelial receptor (CLEVER)-1 direct the binding of cancer cells to the lymph vessel endothelium. Cancer Res. 2003, 63:4671-4676.
106. Laakkonen P. Vascular endothelial growth factor receptor 3 involvement in tumor angiogenesis and growth. Cancer Res. 2007, 67:593-599.
107. Roberts N. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res. 2006, 66:2650-2657.
108. Shimizu K., Kubo H., Yamguchi K., Kawashima K., Ueda Y., Matsuo K., Awane M., Shimahara Y., Takabayashi A., Yamaoka Y., Sataoh S. Suppression of VEGFR-3 signaling inhibits lymph node metastasis in gastric cancer. Cancer Sci. 2004, 95:328-333.
109. Krishnan J., Kirkin V., Steffen A., Hegen M., Weih D., Tomarev S., Wilting J., Sleeman J.P. Differential in vivo and in vitro expression of vascular endothelial growth factor (VEGF)-C and VEGF-D in tumors and its relationship to lymphatic metastasis in immunocompetent rats. Cancer Res. 2003, 63:713-722.
110. He Y., Kozaki K., Karpanen T., Koshikawa K., Yla-Herttuala S., Takahashi T., Alitalo K. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl. Cancer Inst. 2002, 94:819-825.
111. Chen Z., Varney M.L., Backora M.W., Cowan K., Solheim J.C., Talmadge J.E., Singh R.K. Down-regulation of vascular endothelial cell growth factor-C expression using small interfering RNA vectors in mammary tumors inhibits tumor lymphangiogenesis and spontaneous metastasis and enhances survival. Cancer Res. 2005, 65:9004-9011.
112. He X.W., Liu T., Chen Y.X., Cheng D.J., Li X.R., Xiao Y., Feng Y.L. Calcium carbonate nanoparticle delivering vascular endothelial growth factor-C siRNA effectively inhibits lymhangiogenesis and growth of gastric cancer in vivo. Cancer Gene Ther. 2008, 15:193-202.
113. Karpanen T., Wirzenius M., Makinen T., Veikkola T., Haisma H.J., Achen M.G., Stacker S.A., Pytowski B., Yla-herttuala S., Alitalo K. Lymphangiogenic growth factor responsiveness is modulated by postnatal lymphatic vessel maturation. Am. J. Pathol. 2006, 169:708-718.
114. Ruggeri B., Sing J., Gingrich D., Angeles T., Albom M., Chang H., Robinson C., Hunter K., Dobrzanski P., Jones-Bolin S., Aimone L., Klein-Szanto A., Herbert J.M., Bono F., Schaeffer P., Casellas P., Bourie B., Pili R., Isaacs J., Ator M., Hudkins R., Vaught J., Maljamo J., Dionne C. CEP-7055: a novel, orally active pan inhibitor of vascular endothelial growth factor receptor tyrosine kinases with potent antiangiogenic activity and antitumor efficacy in preclinical models. Cancer Res. 2003, 63:5978-5991.
115. Lin B., Podar K., Gupta D., Tai Y.T., Li S., Weller E., Hideshima T., Lentzsch S., Davies F., Li C., Weisberg E., Schlossman R.L., Richardson P.G., Griffin J.D., Wood J., Munshi N.C., Anderson K.C. The vascular endothelial growth factor receptor tyrosine kinase inhibitor PTK787/ZK222584 inhibits growth and migration of multiple myeloma cells in the bone marrow microenvironment. Cancer Res. 2002, 62:5019-5026.
116. Kirkin V., Thiele W., Baumann P., Mazitschek R., Rohde K., Fellbrich G., Weich H., Waltenberger J., Giannis A., Sleeman J.P. MAZ51, an indolinone that inhibits endothelial cell and tumor cell growth in vitro, suppresses tumor growth in vivo. Int. J. Cancer 2004, 112:986-993.
117. Caunt M., Mak J., Liang W.C., Stawicki S., Pan Q., Tong R.K., Kowalski J., Ho C., Reslan H.B., Ross J., Berry L., Kasman I., Zlot C., Cheng Z., Le Couter J., Filvaroff E.H., Plowman G., Peale F., French D., Carano R., Koch A.W., Wu Y., Watts R.J., Tessier-Lavigne M., Bagri A. Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 2008, 13:331-342.
118. Muller A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
119. Derek T.O. Particulates and Lymphatic Drug Delivery. Lymphatic transport of drugs 1992, 282. CRC. W.N. Charman (Ed.).
120. Charman W.N. Lymphatic Transport of Drugs 1992, 279-315. CRC Press, Boca Raton, FL.
121. Mangat S., Patel H.M. Lymph node localization of non-specific antibody-coated liposomes. Life Sci. 1985, 36:1917.
122. Weinstein J.N., Steller M.A., Covell D.G., Holton O.D., Keenan A.M., Sieber S.M., Parker R.J. Monoclonal anti-tumor antibodies in the lymphatics. Cancer Treat. Rep. 1984, 68:257-264.
123. Hirano K., Hunt C.A., Strubbe A., MacGregor R.D. Lymphatic transport of liposome-encapsulated drugs following intraperitoneal administration: effect of lipid composition. Pharm. Res. 1985, 2:271.
124. Ohsawa T., Matsukawa Y., Takakura Y., Hahida M., Sezaki H. Fate of lipid and encapsulated drug after intramuscular administration of liposomes prepared by the freeze-thawing method in rats. Chem. Pharm. Bull. 1985, 33:5013.
125. Ryman B.E., Jewkes R.F., Jeyasingh K., Osborne M.P., Patel H.M., Richardson V.J., Tattersall M.H.N., Tyrell D.A. Potential applications of liposomes to therapy. Ann. N. Y. Acad. Sci. 1978, 308:281.
126. Torchilin V.P. Affinity liposomes in vivo: factors influencing target accumulation. J. Mol. Recognit. 1996, 9:335-346.
127. Schmid-Schonbein G.W. Microlymphatics and lymph flow. Physiol. Rev. 1990, 10:148-162.
128. Gnepp D.R. Vascular endothelial markers of the human thoracic duct and lacteal. Lymphology 1987, 20:36-43.
129. Skandalakis J.E. I wish I had been there: highlights in the history of lymphatics. Am. Surg. 1995, 61:799-808.
130. Kanter M.A. The lymphatic system-an historical perspective. Plast. Reconstr. Surg. 1987, 79:131-139.
131. Tischendorf F. The lymphatic system and its history. Biochem. Exp. Biol. 1978, 14:86-97.
132. Swartz M.A. The physiology of the lymphatic system. Adv. Drug Deliv. Rev. 2001, 50:3-20.
133. Leeds S.E. Three centuries of history of the lymphatic system. Surg. Gynecol. Obstet. 1977, 1(144):927-934.
134. Brennan M.J., DePompolo R.W., Garden F.H. Focused review: postmastectomy lymphedema. Arch. Phys. Med. Rehabil. 1996, 77:S74-S80.
135. Hogan R.D., Unthank J.L. Mechanical control of initial lymphatic contractile behavior in bat's wing. Am. J. Physiol. 1986, 251:H357-H363.
136. Leak L.V., Burke J.F. Ultrastructural studies on the lymphatic anchoring filaments. J. Cell Biol. 1968, 36:129-149.
137. Aukland K., Reed R.K. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol. Rev. 1993, 73:785-810.
138. Adair T.H., Guyton A.C. Lymph formation and its modification in the lymphatic system. Experimental Biology of the Lymphatic Circulation 1985, 13-44. Elsevier, Amsterdam. M.G. Johnston (Ed.).
139. Adair T.H., Moffatt D.S., Paulson A.W., Guyton A.C. Quantitation of changes in lymph protein concentration during lymph node transit. Am. J. Physiol. 1982, 243:H351-H359.
140. Swartz M.A., Berk D.A., Jain R.K. Transport in lymphatic capillaries: macroscopic measurement using residence time distribution analysis. Am. J. Physiol. 1996, 270:H324-H329.
141. McGeown J.G., McHale N.G., Thornbury K.D. Effects of varying patterns of external compression on lymph flow in the hindlimb of the anaesthetized sheep. J. Physiol. 1988, 397:449-457.
142. Li B., Silver I., Szalai J.P., Johnston M.G. Pressure-volume relationships in sheep mesenteric lymphatic vessels in situ: response to hypovolemia. Microvasc. Res. 1998, 56:127-138.
143. Comper W.D., Laurent T.C. Physiological function of connective tissue polysaccharides. Physiol. Rev. 1978, 58:255.
144. Hardingham T.E., Fosang A.J. Proteoglycans: many forms and many functions. FASEB J. 1992, 6:861-870.
145. Negrini D., Passi A., De Luca G., Miserochi G. Proteoglycan involvement during development of lesional pulmonary edema. Am. J. Physiol. 1998, 274:L203-L211.
146. Passi A., Negrini D., Albertini R., De Luca G., Miserocchi G. Involvement of lung interstitial proteoglycans in development of hydraulic- and elastase-induced edema. Am. J. Physiol. 1998, 275:L631-L635.
147. Choi H.S., Seo S.A., Khang G., Rhee J.M., Lee H.B. Preparation and characterization of fentanyl-loaded PLGA microspheres: in vitro release profiles. Int. J. Pharm. 2002, 234:195-203.
148. Azouz S.M., Walpole J., Amirifeli S., Taylor K.N., Grinstaff M.W., Colson Y.L. Prevention of local tumor growth with paclitazel-loaded microspheres. J. Thorac. Cardiovasc. Surg. 2008, 135:1014-1021.
149. Liu J., Meisner D., Kwong E., Wu X.Y., Johnston M.R. A novel trans-lymphatic drug delivery system: implantable gelatin sponge impregnated with PLGA-paclitaxel microspheres. Biomaterials 2007, 28:3236-3244.
150. Fraser J.R., Laurent T.C. Turnover and metabolism of hyaluronan. CIBA Found. Symp. 1989, 143. 143:41.
151. Cai S., Xie Y., Bagby T.R., Cohen M.S., Forrest M.L. Intralymphatic chemotherapy using a hyaluronan-cisplatin conjugate. J. Surg. Res. 2008, 147:247-252.