Tumor Lymphangiogenesis and Lymphangiogenic Growth Factors

Archives of Medical Research

Volumn 39, Issue 4, 2008, Pages 365-372

  Da, Ming Xu ^a   Wu, Zhuang ^b   Tian, Hong Wei ^a  

^a GANSU PROVINCIAL HOSPITAL   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Lymphangiogenesis; Lymphangiogenic growth factors; Lymphatic metastasis

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN RECEPTOR; CYCLOOXYGENASE 2; FIBROBLAST GROWTH FACTOR 2; GROWTH FACTOR; NITRIC OXIDE; PLATELET DERIVED GROWTH FACTOR; SCATTER FACTOR; SOMATOMEDIN; TIE 1 RECEPTOR; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3;

CANCER GROWTH; CANCER INHIBITION; HUMAN; INFLAMMATION; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; METASTASIS; REVIEW;

ANGIOPOIETIN-1; ANIMALS; CYCLOOXYGENASE 2; FIBROBLAST GROWTH FACTOR 2; HEPATOCYTE GROWTH FACTOR; HUMANS; INFLAMMATION; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; NEOPLASMS; NITRIC OXIDE; PLATELET-DERIVED GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SOMATOMEDINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 41049091680     PISSN: 01884409     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.arcmed.2007.12.005     Document Type: Review

References (95)

1. Hayes D.F. Prognostic and predictive factors revisited. Breast 14 (2005) 493-499
2. Pepper M.S. Lymphangiogenesis and tumor metastasis: myth or reality?. Clin Cancer Res 7 (2001) 462-468
3. Jackson D.G., Prevo R., Clasper S., and Banerji S. LYVE-1, the lymphatics and tumor lymphangiogenesis. Trends Immunol 22 (2001) 317-321
4. Karpanen T., and Alitalo K. Lymphatic vessels as targets for tumor therapy?. J Exp Med 194 (2001) 37-42
5. Stacker S.A., Achen M.G., Jussila L., Baldwin M.E., and Alitalo K. Lymphangiogenesis and cancer metastasis. Nat Rev Cancer 2 (2002) 573-583
6. Carmeliet P., and Jain R.K. Angiogenesis in cancer and other diseases. Nature 407 (2000) 249-257
7. Ji R.C. Lymphatic endothelial cells, lymphangiogenesis, and extracellular matrix. Lymph Res Biol 4 (2006) 83-100
8. Saharinen P., Tammela T., Karkkainen M.J., and Alitalo K. Lymphatic vasculature: development, molecular regulation and role in tumor metastasis and inflammation. Trends Immunol 25 (2004) 387-395
9. Padera T.P., Kadambi A., Tomaso E., Carreira C.M., Brown E.B., Boucher Y., et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296 (2002) 1883-1886
10. Dadras S.S., Paul T., Bertoncini J., Brown L.F., Muzikansky A., Jackson D.G., et al. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 162 (2003) 1951-1960
11. Stacker S.A., Caesar C., Baldwin M.E., Thornton G.E., Williams R.A., Prevo R., et al. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7 (2001) 186-191
12. Karpanen T., Egeblad M., Karkkainen M.J., Kubo H., Yla-Herttuala S., Jaattela M., et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61 (2001) 1786-1790
13. Stacker S.A., Baldwin M.E., and Achen M.G. The role of tumor lymphangiogenesis in metastatic spread. FASEB J 16 (2002) 922-934
14. Dadras S.S., Lange-Asschenfeldt B., Velasco P., Nguyen L., Vora A., Muzikansky A., et al. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 18 (2005) 1232-1242
15. Hirakawa S., Kodama S., Kunstfeld R., Kajiya K., Brown L.F., and Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201 (2005) 1089-1099
16. Harrell M.I., Iritani B.M., and Ruddell A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 170 (2007) 774-786
17. Rubbia-Brandt L., Terris B., Giostra E., Dousset B., Morel P., and Pepper M.S. Lymphatic vessel density and vascular endothelial growth factor-C expression correlate with malignant behavior in human pancreatic endocrine tumors. Clin Cancer Res 10 (2004) 6919-6928
18. Gombos Z., Xu X., Chu C.S., Zhang P.J., and Acs G. Peritumoral lymphatic vessel density and vascular endothelial growth factor C expression in early-stage squamous cell carcinoma of the uterine cervix. Clin Cancer Res 11 (2005) 8364-8371
19. Maula S.M., Luukkaa M., Grenman R., Jackson D., Jalkanen S., and Ristamaki R. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res 63 (2003) 1920-1926
20. Hall F.T., Freeman J.L., Asa S.L., Jackson D.G., and Beasley N.J. Intratumoral lymphatics and lymph node metastases in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 129 (2003) 716-719
21. Kyzas P.A., Geleff S., Batistatou A., Agnantis N.J., and Stefanou D. Evidence for lymphangiogenesis and its prognostic implications in head and neck squamous cell carcinoma. J Pathol 206 (2005) 170-177
22. Wong S.Y., Haack H., Crowley D., Barry M., Bronson R.T., and Hynes R.O. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res 65 (2005) 9789-9798
23. Taipale J., Makinen T., Arighi E., Kukk E., Karkkainen M., and Alitalo K. Vascular endothelial growth factor-3. Curr Top Microbiol Immunol 237 (1999) 85-96
24. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahtinen I., Kukk E., et al. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt-4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15 (1996) 290-298
25. Achen M.G., Jeltsch M., Kukk E., Makinen T., Vitali A., Wilks A.F., et al. 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 USA 95 (1998) 548-553
26. Achen M.G., and Stacker S.A. Tumor lymphangiogenesis and metastatic spread-new players begin to emerge. Int J Cancer 119 (2006) 1755-1760
27. Su J.L., Yang P.C., Shih J.Y., Yang C.Y., Wei L.H., Hsieh C.Y., et al. The VEGF-C/VEGFR-3 axis promotes invasion and metastasis of cancer cells. Cancer Cell 9 (2006) 209-223
28. Lin J., Lalani A.S., Harding T.C., Gonzalez M., Wu W.W., Luan B., et al. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res 65 (2005) 6901-6909
29. He Y., Rajantie I., Pajusola K., Jeltsch M., Holopainen T., Yla-Herttuala S., et al. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res 65 (2005) 4739-4746
30. Alitalo K., and Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cells 1 (2002) 219-227
31. Arinaga M., Noguchi T., Takeno S., Chujo M., Miura T., and Uchida Y. Clinical significance of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in patients with non-small cell lung carcinoma. Cancer 97 (2003) 457-464
32. Kojima H., Shijubo N., Yamada G., Ichimiya S., Abe S., Satoh M., et al. Clinical significance of vascular endothelial growth factor-C and vascular endothelial growth factor receptor 3 in patients with T1 lung adenocarcinoma. Cancer 104 (2005) 1668-1677
33. Ogawa E., Takenaka K., Yanagihara K., Kurozumi M., Manabe T., Wada H., et al. Clinical significance of VEGF-C status in tumor cells and stromal macrophages in non-small cell lung cancer patients. Br J Cancer 91 (2004) 498-503
34. Achen M.G., Williams R.A., Baldwin M.E., Lai P., Roufail S., Alitalo K., et al. The angiogenic and lymphangiogenic factor vascular endothelial growth factor-D exhibits a paracrine mode of action in cancer. Growth Factors 20 (2002) 99-107
35. Han S.L., Tang H.J., Hua Y.W., Ji S.Q., and Lin D.X. Expression of COX-2 in stomach cancers and its relation to their biological features. Dig Surg 20 (2003) 107-114
36. Ohno R., Yoshinaga K., Fujita T., Hasegawa K., Iseki H., Tsunozaki H., et al. Depth of invasion parallels increased cyclooxygenase-2 levels in patients with gastric carcinoma. Cancer 91 (2001) 1876-1881
37. Chen C.N., Sung C.T., Lin M.T., Lee P.H., and Chang K.J. Clinicopathologic association of cyclooxygenase 1 and cyclooxygenase 2 expression in gastric adenocarcinoma. Ann Surg 233 (2001) 183-188
38. Zha S., Yegnasubramanian V., Nelson W.G., Isaacs W.B., and Marzo A.M. Cyclooxygenases in cancer: progress and perspective. Cancer Lett 215 (2004) 1-20
39. Su J.L., Shih J.Y., Yen M.L., Jeng Y.M., Chang C.C., Hsieh C.Y., et al. Cyclooxygenase-2 induces EP1-and HER-2/Neu-dependent vascular endothelial growth factor-C up-regulation: a novel mechanism of lymphangiogenesis in lung adenocarcinoma. Cancer Res 64 (2004) 554-564
40. Timoshenko A.V., Chakraborty C., Wagner G.F., and Lala P.K. COX-2-mediated stimulation of the lymphangiogenic factor VEGF-C in human breast cancer. Br J Cancer 94 (2006) 1154-1163
41. Da M.X., Wu X.T., Wang J., Guo T.K., Zhao Z.G., Luo T., et al. Expression of cyclooxygenase-2 and vascular endothelial growth factor-c correlates with lymphangiogenesis and lymphatic invasion in human gastric cancer. Arch Med Res 39 (2008) 92-99
42. Alitalo K., Mohla S., and Ruoslahti E. Lymphangiogenesis and cancer: meeting report. Cancer Res 64 (2004) 9225-9229
43. Barnes N.L.P., Waenberg F., Farnie G., White D., Jiang W., Anderson E., et al. Cyclooxygenase-2 inhibition:effects on tumour growth, cell cycling and lymphangiogenesis in a xenograft model of breast cancer. Br J Cancer 96 (2007) 575-582
44. Dailey L., Ambrosetti D., Mansukhani A., and Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 16 (2005) 233-247
45. Chang L.K., Garcia-Cardena G., Farnebo F., Fannon M., Chen E.J., Butterfield C., et al. Dose dependent response of FGF-2 for lymphangiogenesis. Proc Natl Acad Sci USA 101 (2004) 11658-11663
46. Cao R., Eriksson A., Kubo H., Alitalo K., Cao Y., and Thyberg J. Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability. Circ Res 94 (2004) 664-670
47. Kubo H., Cao R., Brakenhielm E., Makinen T., Cao Y., and Alitalo K. Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci USA 99 (2002) 8868-8873
48. Matsuo M., Yamada S., Koizumi K., Sakurai H., and Saiki I. Tumour-derived fibroblast growth factor-2 exerts lymphangiogenic effects through Akt/mTOR/p70S6kinase pathway in rat lymphatic endothelial cells. Eur J Cancer 43 (2007) 1748-1754
49. Thurston G. Role of angiopoietins and Tie receptor tyrosine kinases in angiogenesis and lymphangiogenesis. Cell Tissue Res 314 (2003) 61-68
50. Gale N.W., Thurston G., Hackett S.F., Renard R., Wang Q., McClain J., 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) 411-423
51. Morisada T., Oike Y., Yamada Y., Urano T., Akao M., Kubota Y., et al. Angiopoietin-1 promotes LYVE-1-positive lymphatic vessel formation. Blood 105 (2005) 4649-4656
52. Tammela T., Saaristo A., Lohela M., Morisada T., Tornberg J., Norrmen C., et al. Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105 (2005) 4642-468
53. Pietras K., Sjoblom T., Rubin K., Heldin C.-H., and Ostman A. PDGF receptors as cancer drug targets. Cancer Cell 3 (2003) 439-443
54. Heldin C.H., Eriksson U., and Ostman A. New members of the platelet-derived growth factor family of mitogens. Arch Biochem Biophys 398 (2002) 284-290
55. Cao R., Bjorndahl M.A., Religa P., Clasper S., Garvin S., Galter D., et al. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6 (2004) 333-345
56. Bjorndahl M., Cao R., Nissen L.J., Clasper S., Johnson L.A., Xue Y., et al. Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc Natl Acad Sci USA 102 (2005) 15593-1558
57. Foulstone E., Prince S., Zaccheo O., Burns J.L., Harper J., Jacobs C., et al. Insulin-like growth factor ligands, receptors, and binding proteins in cancer. J Pathol 205 (2005) 145-153
58. Kern P.A., Svoboda M.E., Eckel R.H., and Van Wyk J.J. Insulin-like growth factor action and production in adipocytes and endothelial cells from human adipose tissue. Diabetes 38 (1989) 710-717
59. Lee O.H., Bae S.K., Bae M.H., Lee Y.M., Moon E.J., Cha H.J., et al. Identification of angiogenic properties of insulin-like growth factor II in in vitro angiogenesis models. Br J Cancer 82 (2000) 385-391
60. Clemmons D.R. Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8 (1997) 45-62
61. Baserga R., Hongo A., Rubini M., Prisco M., and Valentinis B. The IGF-I receptor in cell growth, transformation and apoptosis. Biochim Biophys Acta 1332 (1997) 105-126
62. Flossmann-Kast B.B., Jehle P.M., Hoeflich A., Adler G., and Lutz M.P. Src stimulates insulin-like growth factor I (IGF-I)-dependent cell proliferation by increasing IGF-I receptor number in human pancreatic carcinoma cells. Cancer Res 58 (1998) 3551-3554
63. Jenkins P.J., and Bustin S.A. Evidence for a link between IGF-I and cancer. Eur J Endocrinol 151 (2004) S17-S22
64. Tang Y., Zhang D., Fallavollita L., and Brodt P. Vascular endothelial growth factor C expression and lymph node metastasis are regulated by the type I insulin-like growth factor receptor. Cancer Res 63 (2003) 1166-1171
65. Kajiya K., Hirakawa S., Ma B., Drinnenberg I., and Detmar M. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 24 (2005) 2885-2895
66. Birchmeier C., Birchmeier W., Gherardi E., and Vande Woude G.F. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 4 (2003) 915-925
67. Danilkovitch-Miagkova A., and Zbar B. Dysregulation of Met receptor tyrosine kinase activity in invasive tumors. J Clin Invest 109 (2002) 863-867
68. Cao R., Bjorndahl M.A., Gallego M.I., Chen S., Religa P., Hansen A.J., et al. Hepatocyte growth factor is a lymphangiogenic factor with an indirect mechanism of action. Blood 107 (2006) 3531-3536
69. Ferrara N., Gerber H.-P., and LeCouter J. The biology of VEGF and its receptors. Nat Med 9 (2003) 669-676
70. Saaristo A., Veikkola T., Enholm B., Hytönen M., Arola J., Pajusola K., et al. Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J 16 (2002) 1041-1049
71. Cursiefen C., Chen L., Borges L.P., Jackson D., Cao J., Radziejewski C., et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113 (2004) 1040-1050
72. Hong Y.K., Lange-Asschenfeldt B., Velasco P., Hirakawa S., Kunstfeld R., Brown L.F., et al. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the α1β1 and α2-β1 integrins. FASEB J 18 (2004) 1111-1113
73. Bjorndahl M.A., Cao R., Burton J.B., Brakenhielm E., Religa P., Galter D., et al. Vascular endothelial growth factor promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 65 (2005) 9261-9268
74. Ishigami S.I., Arii S., Furutani M., Niwano M., Harada T., Mizumoto M., et al. Predictive value of vascular endothelial growth factor (VEGF) in metastasis and prognosis of human colorectal cancer. Br J Cancer 78 (1998) 1379-1384
75. Shih C.H., Ozawa S., Ando N., Ueda M., and Kitajima M. Vascular endothelial growth factor expression predicts outcome and lymph node metastasis in squamous cell carcinoma of the esophagus. Clin Cancer Res 6 (2000) 1161-1168
76. O-charoenrat P., Rhys-Evans P., and Eccles S.A. Expression of vascular endothelial growth factor family members in head and neck squamous cell carcinoma correlates with lymph node metastasis. Cancer 92 (2001) 556-568
77. Gannon G., Mandriota S.J., Cui L., Baetens D., Pepper M.S., and Christofori G. Overexpression of vascular endothelial growth factor-A165 enhances tumor angiogenesis but not metastasis during b-cell carcinogenesis. Cancer Res 62 (2002) 603-608
78. Alitalo K., Tammela T., and Petrova T.V. Lymphangiogenesis in development and human disease. Nature 438 (2005) 946-953
79. Stuehr D.J. Mammalian nitric oxide synthases. Biochim Biophys Acta 1411 (1999) 217-230
80. Kim-Shapiro D.B., Schechter A.N., and Gladwin M.T. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler. Thromb Vasc Biol 26 (2006) 697-705
81. Morbidelli L., Donnini S., and Ziche M. Role of nitric oxide in the modulation of angiogenesis. Curr Pharm Des 9 (2003) 521-530
82. Pyriochou A., Beis D., Koika V., Potytarchou C., Papadimitriou E., Zhou Z., et al. Soluble guanylyl cyclase activation promotes angiogenesis. J Pharmacol Exp Ther 319 (2006) 663-671
83. Ohhashi T., Mizuno R., Ikomi F., and Kawai Y. Current topics of physiology and pharmacology in the lymphatic system. Pharmacol Ther 105 (2005) 165-188
84. Franchi A., Massi D., Santucci M., Masini E., Degl Innocenti D.R., Magnelli L., et al. Inducible nitric oxide synthase activity correlates with lymphangiogenesis and vascular endothelial growth factor-C expression in head and neck squamous cell carcinoma. J Pathol 208 (2006) 439-445
85. Nakamura Y., Yasuoka H., Zuo H., Takamura Y., Miyauchi A., Nakamura M., et al. Nitric oxide in papillary thyroid carcinoma: induction of vascular endothelial growth factor D and correlation with lymph node metastasis. J Clin Endocrinol Metab 91 (2006) 1582-1585
86. Kajiya K., Huggenberger R., Drinnenberg I., Ma B., and Detmar M. Nitric oxide mediates lymphatic vessel activation via soluble guanylate cyclase α1β1-impact on inflammation. FASEB J 22 (2008) 000-000. Published online September 13, 2007 (doi: 10.1096/fj.07-8873)
87. Mouta C., and Heroult M. Inflammatory triggers of lymphangiogenesis. Lymphat Res Biol 1 (2003) 201-218
88. Schoppmann S.F., Birner P., Stockl J., Kalt R., Ullrich R., Caucig C., et al. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161 (2002) 947-956
89. Kerjaschki D. The crucial role of macrophages in lymphangiogenesis. J Clin Invest 115 (2005) 2316-2319
90. Maruyama K., Ii M., Cursiefen C., Jackson D.G., Keino H., Tomita M., et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115 (2005) 2363-2372
91. Kunstfeld R., Hirakawa S., Hong Y.K., Schacht V., Lange-Asschenfeldt B., Velasco P., et al. 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) 1048-1057
92. Kerjaschki D., Huttary N., Raab I., Regele H., Bojarski-Nagy K., Bartel G., et al. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12 (2006) 230-234
93. Baluk P., Tammela T., Ator E., Lyubynska N., Achen M.G., Hicklin D.J., et al. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115 (2005) 247-257
94. Kajiya K., Hirakawa S., and Detmar M. Vascular endothelial growth factor-A mediates ultraviolet B-induced impairment of lymphatic vessel function. Am J Pathol 169 (2006) 1496-1503
95. Halin C., Tobler N.E., Vigl B., Brown L.F., and Detmar M. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 110 (2007) 3158-3167