Lymphangiogenesis: A new player in cancer progression

World Journal of Gastroenterology

Volumn 16, Issue 32, 2010, Pages 4003-4012

  Nagahashi, Masayuki ^a   Ramachandran, Subramaniam ^a   Rashid, Omar M ^a   Takabe, Kazuaki ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Biomarkers; Colorectal neoplasms; Lymphangiogenesis; Lymphatic metastasis; Lymphatic vessels; Monoclonal antibody d2 40; Therapy related neoplasms; Vascular endothelial growth factor

Indexed keywords

ANGIOGENESIS; CANCER CHEMOTHERAPY; CANCER GROWTH; COLORECTAL CANCER; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LYMPHANGIOGENESIS; METASTASIS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TREATMENT OUTCOME;

EID: 77956646251     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v16.i32.4003     Document Type: Review

References (116)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009; 59: 225-249
2. Sundlisaeter E, Dicko A, Sakariassen PØ, Sondenaa K, Enger PØ, Bjerkvig R. Lymphangiogenesis in colorectal cancer--prognostic and therapeutic aspects. Int J Cancer 2007; 121: 1401-1409
3. Vather R, Sammour T, Kahokehr A, Connolly AB, Hill AG. Lymph node evaluation and long-term survival in Stage II and Stage III colon cancer: a national study. Ann Surg Oncol 2009; 16: 585-593
4. Compton CC, Greene FL. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 2004; 54: 295-308
5. Haq AI, Schneeweiss J, Kalsi V, Arya M. The Dukes staging system: a cornerstone in the clinical management of colorectal cancer. Lancet Oncol 2009; 10: 1128
6. Royston D, Jackson DG. Mechanisms of lymphatic metastasis in human colorectal adenocarcinoma. J Pathol 2009; 217: 608-619
7. Belluco C, Esposito G, Bertorelle R, Del Mistro A, Fassina A, Vieceli G, Chieco-Bianchi L, Nitti D, Lise M. Absence of the cell cycle inhibitor p27Kip1 protein predicts poor outcome in patients with stage I-III colorectal cancer. Ann Surg Oncol 1999; 6: 19-25
8. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, editors. AJCC Cancer Staging Manual. 7th ed. New York: Springer-Verlag, 2010
9. Gill S, Blackstock AW, Goldberg RM. Colorectal cancer. Mayo Clin Proc 2007; 82: 114-129
10. Willett CG, Duda DG, Czito BG, Bendell JC, Clark JW, Jain RK. Targeted therapy in rectal cancer. Oncology (Williston Park) 2007; 21: 1055-1065; discussion 1065, 1070, 1075 passim
11. Ortega J, Vigil CE, Chodkiewicz C. Current progress in targeted therapy for colorectal cancer. Cancer Control 2010; 17: 7-15
12. Fakih M. The role of targeted therapy in the treatment of advanced colorectal cancer. Curr Treat Options Oncol 2008; 9: 357-374
13. Kawakami M, Yanai Y, Hata F, Hirata K. Vascular endothelial growth factor C promotes lymph node metastasis in a rectal cancer orthotopic model. Surg Today 2005; 35: 131-138
14. He XW, Yu X, Liu T, Yu SY, Chen DJ. Vector-based RNA interference against vascular endothelial growth factor-C inhibits tumor lymphangiogenesis and growth of colorectal cancer in vivo in mice. Chin Med J (Engl) 2008; 121: 439-444
15. Moehler M, Frings C, Mueller A, Gockel I, Schimanski CC, Biesterfeld S, Galle PR, Holtmann MH. VEGF-D expression correlates with colorectal cancer aggressiveness and is downregulated by cetuximab. World J Gastroenterol 2008; 14: 4156-4167
16. Jia YT, Li ZX, He YT, Liang W, Yang HC, Ma HJ. Expression of vascular endothelial growth factor-C and the relationship between lymphangiogenesis and lymphatic metastasis in colorectal cancer. World J Gastroenterol 2004; 10: 3261-3263
17. Lu Y, Yang Q, Du Y, Feng G, Yang C. Expression analysis of lymphangiogenic factors in human colorectal cancer with quantitative RT-PCR. Cancer Invest 2007; 25: 393-396
18. He XW, Liu T, Xiao Y, Feng YL, Cheng DJ, Tingting G, Zhang L, Zhang Y, Chen YX, Tingting G, Zhang L. Vascular endothelial growth factor-C siRNA delivered via calcium carbonate nanoparticle effectively inhibits lymphangiogenesis and growth of colorectal cancer in vivo. Cancer Biother Radiopharm 2009; 24: 249-259
19. Lui Z, Ma Q, Wang X, Zhang Y. Inhibiting tumor growth of colorectal cancer by blocking the expression of vascular endothelial growth factor receptor 3 using interference vectorbased RNA interference. Int J Mol Med 2010; 25: 59-64
20. Zhong D, Li Y, Peng Q, Zhou J, Zhou Q, Zhang R, Liang H. Expression of Tiam1 and VEGF-C correlates with lymphangiogenesis in human colorectal carcinoma. Cancer Biol Ther 2009; 8: 689-695
21. Parr C, Jiang WG. Quantitative analysis of lymphangiogenic markers in human colorectal cancer. Int J Oncol 2003; 23: 533-539
22. Yan G, Zhou XY, Cai SJ, Zhang GH, Peng JJ, Du X. Lymphangiogenic and angiogenic microvessel density in human primary sporadic colorectal carcinoma. World J Gastroenterol 2008; 14: 101-107
23. Tsirlis TD, Papastratis G, Masselou K, Tsigris C, Papachristodoulou A, Kostakis A, Nikiteas NI. Circulating lymphangio- genic growth factors in gastrointestinal solid tumors, could they be of any clinical significance? World J Gastroenterol 2008; 14: 2691-2701
24. Gordon MS, Mendelson DS, Kato G. Tumor angiogenesis and novel antiangiogenic strategies. Int J Cancer 2010; 126: 1777-1787
25. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186
26. Folkman J, Merler E, Abernathy C, Williams G. Isolation of a tumor factor responsible for angiogenesis. J Exp Med 1971; 133: 275-288
27. Rosenthal RA, Megyesi JF, Henzel WJ, Ferrara N, Folkman J. Conditioned medium from mouse sarcoma 180 cells contains vascular endothelial growth factor. Growth Factors 1990; 4: 53-59
28. Folkman J, Shing Y. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv Exp Med Biol 1992; 313: 355-364
29. Cao Y, Liu Q. Therapeutic targets of multiple angiogenic factors for the treatment of cancer and metastasis. Adv Cancer Res 2007; 97: 203-224
30. Detmar M. Tumor angiogenesis. J Investig Dermatol Symp Proc 2000; 5: 20-23
31. Stacker SA, Achen MG. From anti-angiogenesis to anti-lymphangiogenesis: emerging trends in cancer therapy. Lymphat Res Biol 2008; 6: 165-172
32. Chikly B. Who discovered the lymphatic system. Lymphology 1997; 30: 186-193
33. Weiss L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev 2000; 19: I-XI, 193-383
34. Sleeman J, Schmid A, Thiele W. Tumor lymphatics. Semin Cancer Biol 2009; 19: 285-297
35. 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
36. Jeltsch M, Tammela T, Alitalo K, Wilting J. Genesis and pathogenesis of lymphatic vessels. Cell Tissue Res 2003; 314: 69-84
37. 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: 1751
38. Beasley NJ, Prevo R, Banerji S, Leek RD, Moore J, van Trappen P, Cox G, Harris AL, Jackson DG. Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res 2002; 62: 1315-1320
39. Schoppmann SF, Birner P, Stöckl 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
40. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005; 201: 1089-1099
41. Tammela T, Alitalo K. Lymphangiogenesis: Molecular mechanisms and future promise. Cell 2010; 140: 460-476
42. Wissmann C, Detmar M. Pathways targeting tumor lymphangiogenesis. Clin Cancer Res 2006; 12: 6865-6868
43. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S, Mihm MC, Detmar M. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 2005; 18: 1232-1242
44. Wilting J, Hawighorst T, Hecht M, Christ B, Papoutsi M. Development of lymphatic vessels: tumour lymphangiogenesis and lymphatic invasion. Curr Med Chem 2005; 12: 3043-3053
45. Ding MX, Lin XQ, Fu XY, Zhang N, Li JC. Expression of vascular endothelial growth factor-C and angiogenesis in esophageal squamous cell carcinoma. World J Gastroenterol 2006; 12: 4582-4585
46. Liu C, Liang P, Wang Y, Zhou P, Li X, Han ZY, Liu SP. Assessment of hepatic VX(2) tumors with combined percutaneous transhepatic lymphosonography and contrast-enhanced ultrasonographic imaging. World J Gastroenterol 2008; 14: 3908-3913
47. Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 2002; 1: 219-227
48. Saad RS, Kordunsky L, Liu YL, Denning KL, Kandil HA, Silverman JF. Lymphatic microvessel density as prognostic marker in colorectal cancer. Mod Pathol 2006; 19: 1317-1323
49. Ishigami SI, Arii S, Furutani M, Niwano M, Harada T, Mizumoto M, Mori A, Onodera H, Imamura M. Predictive value of vascular endothelial growth factor (VEGF) in metastasis and prognosis of human colorectal cancer. Br J Cancer 1998; 78: 1379-1384
50. Jackson DG. The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1. Trends Cardiovasc Med 2003; 13: 1-7
51. Schoppmann SF, Birner P, Studer P, Breiteneder-Geleff S. Lymphatic microvessel density and lymphovascular invasion assessed by anti-podoplanin immunostaining in human breast cancer. Anticancer Res 2001; 21: 2351-2355
52. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999; 98: 769-778
53. Castro EC, Galambos C. Prox-1 and VEGFR3 antibodies are superior to D2-40 in identifying endothelial cells of lymphatic malformations--a proposal of a new immunohistochemical panel to differentiate lymphatic from other vascular malformations. Pediatr Dev Pathol 2009; 12: 187-194
54. Paavonen K, Puolakkainen P, Jussila L, Jahkola T, Alitalo K. Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am J Pathol 2000; 156: 1499-1504
55. Podgrabinska S, Braun P, Velasco P, Kloos B, Pepper MS, Skobe M. Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci USA 2002; 99: 16069-16074
56. Matsuo M, Koizumi K, Yamada S, Tomi M, Takahashi R, Ueda M, Terasaki T, Obinata M, Hosoya K, Ohtani O, Saiki I. Establishment and characterization of conditionally immortalized endothelial cell lines from the thoracic duct and inferior vena cava of tsA58/EGFP double-transgenic rats. Cell Tissue Res 2006; 326: 749-758
57. Nisato RE, Harrison JA, Buser R, Orci L, Rinsch C, Montesano R, Dupraz P, Pepper MS. Generation and characterization of telomerase-transfected human lymphatic endothelial cells with an extended life span. Am J Pathol 2004; 165: 11-24
58. Yamaguchi T, Ichise T, Iwata O, Hori A, Adachi T, Nakamura M, Yoshida N, Ichise H. Development of a new method for isolation and long-term culture of organ-specific blood vascular and lymphatic endothelial cells of the mouse. FEBS J 2008; 275: 1988-1998
59. Hayes H, Kossmann E, Wilson E, Meininger C, Zawieja D. Development and characterization of endothelial cells from rat microlymphatics. Lymphat Res Biol 2003; 1: 101-119
60. Whitehurst B, Eversgerd C, Flister M, Bivens CM, Pickett B, Zawieja DC, Ran S. Molecular profile and proliferative responses of rat lymphatic endothelial cells in culture. Lymphat Res Biol 2006; 4: 119-142
61. Bruyère F, Noël A. Lymphangiogenesis: in vitro and in vivo models. FASEB J 2010; 24: 8-21
62. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, Alitalo K. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 1998; 95: 14389-14394
63. Cursiefen C, Schlötzer-Schrehardt U, Küchle M, Sorokin L, Breiteneder-Geleff S, Alitalo K, Jackson D. Lymphatic vessels in vascularized human corneas: immunohistochemical investigation using LYVE-1 and podoplanin. Invest Ophthalmol Vis Sci 2002; 43: 2127-2135
64. Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, Tomita M, Van Rooijen N, Takenaka H, D'Amore PA, Stein-Streilein J, Losordo DW, Streilein JW. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 2005; 115: 2363-2372
65. Karpanen T, Alitalo K. Molecular biology and pathology of lymphangiogenesis. Annu Rev Pathol 2008; 3: 367-397
66. Shin WS, Rockson SG. Animal models for the molecular and mechanistic study of lymphatic biology and disease. Ann N Y Acad Sci 2008; 1131: 50-74
67. Rutkowski JM, Boardman KC, Swartz MA. Characterization of lymphangiogenesis in a model of adult skin regeneration. Am J Physiol Heart Circ Physiol 2006; 291: H1402-H1410
68. Tabibiazar R, Cheung L, Han J, Swanson J, Beilhack A, An A, Dadras SS, Rockson N, Joshi S, Wagner R, Rockson SG. Inflammatory manifestations of experimental lymphatic insufficiency. PLoS Med 2006; 3: e254
69. Dale MM. The effect of Freund's adjuvants on lymphatics in the mouse's ear. Br J Exp Pathol 1960; 41: 86-88
70. Mancardi S, Stanta G, Dusetti N, Bestagno M, Jussila L, Zweyer M, Lunazzi G, Dumont D, Alitalo K, Burrone OR. Lymphatic endothelial tumors induced by intraperitoneal injection of incomplete Freund's adjuvant. Exp Cell Res 1999; 246: 368-375
71. Nakamura ES, Koizumi K, Kobayashi M, Saiki I. Inhibition of lymphangiogenesis-related properties of murine lymphatic endothelial cells and lymph node metastasis of lung cancer by the matrix metalloproteinase inhibitor MMI270. Cancer Sci 2004; 95: 25-31
72. Yanai Y, Furuhata T, Kimura Y, Yamaguchi K, Yasoshima T, Mitaka T, Mochizuki Y, Hirata K. Vascular endothelial growth factor C promotes human gastric carcinoma lymph node metastasis in mice. J Exp Clin Cancer Res 2001; 20: 419-428
73. Mattila MM, Ruohola JK, Karpanen T, Jackson DG, Alitalo K, Härkönen PL. VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 2002; 98: 946-951
74. Hirakawa S, Brown LF, 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
75. Cao R, Björndahl MA, Religa P, Clasper S, Garvin S, Galter D, Meister B, Ikomi F, Tritsaris K, Dissing S, Ohhashi T, Jackson DG, Cao Y. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 2004; 6: 333-345
76. Chang LK, Garcia-Cardeña G, Farnebo F, Fannon M, Chen EJ, Butterfield C, Moses MA, Mulligan RC, Folkman J, Kaipainen A. Dose-dependent response of FGF-2 for lymphangiogenesis. Proc Natl Acad Sci USA 2004; 101: 11658-1166
77. Cao Y. Direct role of PDGF-BB in lymphangiogenesis and lymphatic metastasis. Cell Cycle 2005; 4: 228-230
78. Morisada T, Oike Y, Yamada Y, Urano T, Akao M, Kubota Y, Maekawa H, Kimura Y, Ohmura M, Miyamoto T, Nozawa S, Koh GY, Alitalo K, Suda T. Angiopoietin-1 promotes LYVE-1-positive lymphatic vessel formation. Blood 2005; 105: 4649-4656
79. Cao R, Björndahl MA, Gallego MI, Chen S, Religa P, Hansen AJ, Cao Y. Hepatocyte growth factor is a lymphangiogenic factor with an indirect mechanism of action. Blood 2006; 107: 3531-3536
80. Yoon CM, Hong BS, Moon HG, Lim S, Suh PG, Kim YK, Chae CB, Gho YS. Sphingosine-1-phosphate promotes lymphangiogenesis by stimulating S1P1/Gi/PLC/Ca2+ signaling pathways. Blood 2008; 112: 1129-1138
81. Anelli V, Gault CR, Snider AJ, Obeid LM. Role of sphingosine kinase-1 in paracrine/transcellular angiogenesis and lymphangiogenesis in vitro. FASEB J 2010; Epub ahead of print
82. Spiegel S, Milstien S. Functions of the multifaceted family of sphingosine kinases and some close relatives. J Biol Chem 2007; 282: 2125-2129
83. Takabe K, Paugh SW, Milstien S, Spiegel S. Inside-out signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol Rev 2008; 60: 181-195
84. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, Spiegel S. Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 2010; 285: 10477-10486
85. Pham TH, Baluk P, Xu Y, Grigorova I, Bankovich AJ, Pappu R, Coughlin SR, McDonald DM, Schwab SR, Cyster JG. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J Exp Med 2010; 207: 17-27
86. Straume O, Jackson DG, Akslen LA. Independent prognostic impact of lymphatic vessel density and presence of low-grade lymphangiogenesis in cutaneous melanoma. Clin Cancer Res 2003; 9: 250-256
87. Shields JD, Borsetti M, Rigby H, Harper SJ, Mortimer PS, Levick JR, Orlando A, Bates DO. Lymphatic density and metastatic spread in human malignant melanoma. Br J Cancer 2004; 90: 693-700
88. Kyzas PA, Geleff S, Batistatou A, Agnantis NJ, Stefanou D. Evidence for lymphangiogenesis and its prognostic implications in head and neck squamous cell carcinoma. J Pathol 2005; 206: 170-177
89. Fernández MI, Bolenz C, Trojan L, Steidler A, Weiss C, Alken P, Grobholz R, Michel MS. Prognostic implications of lymphangiogenesis in muscle-invasive transitional cell carcinoma of the bladder. Eur Urol 2008; 53: 571-578
90. Miyata Y, Kanda S, Ohba K, Nomata K, Hayashida Y, Eguchi J, Hayashi T, Kanetake H. Lymphangiogenesis and angiogenesis in bladder cancer: prognostic implications and regulation by vascular endothelial growth factors-A, -C, and -D. Clin Cancer Res 2006; 12: 800-806
91. Renyi-Vamos F, Tovari J, Fillinger J, Timar J, Paku S, Kenessey I, Ostoros G, Agocs L, Soltesz I, Dome B. Lymphangiogenesis correlates with lymph node metastasis, prognosis, and angiogenic phenotype in human non-small cell lung cancer. Clin Cancer Res 2005; 11: 7344-7353
92. Bono P, Wasenius VM, Heikkilä P, Lundin J, Jackson DG, Joensuu H. High LYVE-1-positive lymphatic vessel numbers are associated with poor outcome in breast cancer. Clin Cancer Res 2004; 10: 7144-7149
93. Williams CS, Leek RD, Robson AM, Banerji S, Prevo R, Harris AL, Jackson DG. Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer. J Pathol 2003; 200: 195-206
94. Van Trappen PO, Steele D, Lowe DG, Baithun S, Beasley N, Thiele W, Weich H, Krishnan J, Shepherd JH, Pepper MS, Jackson DG, Sleeman JP, Jacobs IJ. Expression of vascular endothelial growth factor (VEGF)-C and VEGF-D, and their receptor VEGFR-3, during different stages of cervical carcinogenesis. J Pathol 2003; 201: 544-554
95. Nagahashi M, Shirai Y, Wakai T, Sakata J, Ajioka Y, Hatakeyama K. Perimuscular connective tissue contains more and larger lymphatic vessels than the shallower layers in human gallbladders. World J Gastroenterol 2007; 13: 4480-4483
96. Nagahashi M, Shirai Y, Wakai T, Sakata J, Ajioka Y, Nomura T, Tsuchiya Y, Hatakeyama K. Depth of invasion determines the postresectional prognosis for patients with T1 extrahepatic cholangiocarcinoma. Cancer 2010; 116: 400-405
97. Onogawa S, Kitadai Y, Tanaka S, Kuwai T, Kuroda T, Chayama K. Regulation of vascular endothelial growth factor (VEGF)-C and VEGF-D expression by the organ microenvi-ronment in human colon carcinoma. Eur J Cancer 2004; 40: 1604-1609
98. Gao J, Knutsen A, Arbman G, Carstensen J, Frånlund B, Sun XF. Clinical and biological significance of angiogenesis and lymphangiogenesis in colorectal cancer. Dig Liver Dis 2009; 41: 116-122
99. Sundlisaeter E, Røsland GV, Hertel JK, Sakariassen PØ, Almås B, Dicko A, Søndenaa K. Increased lymphatic vascular density is seen before colorectal cancers reach stage II and growth factor FGF-2 is downregulated in tumor tissue compared with normal mucosa. APMIS 2009; 117: 212-221
100. Kazama S, Kitayama J, Watanabe T, Nagawa H. Expression pattern of vascular endothelial growth factor-C in human colorectal normal mucosa and neoplastic mucosa. Hepatogastroenterology 2004; 51: 391-395
101. Miyazaki T, Okada N, Ishibashi K, Ogata K, Ohsawa T, Ishiguro T, Nakada H, Yokoyama M, Matsuki M, Kato H, Kuwano H, Ishida H. Clinical significance of plasma level of vascular endothelial growth factor-C in patients with colorectal cancer. Jpn J Clin Oncol 2008; 38: 839-843
102. Duff SE, Jeziorska M, Kumar S, Haboubi N, Sherlock D, O'Dwyer ST, Jayson GC. Lymphatic vessel density, microvessel density and lymphangiogenic growth factor expression in colorectal cancer. Colorectal Dis 2007; 9: 793-800
103. Duffy MJ, van Dalen A, Haglund C, Hansson L, Holinski-Feder E, Klapdor R, Lamerz R, Peltomaki P, Sturgeon C, Topolcan O. Tumour markers in colorectal cancer: European Group on Tumour Markers (EGTM) guidelines for clinical use. Eur J Cancer 2007; 43: 1348-1360
104. Graziano F, Cascinu S. Prognostic molecular markers for planning adjuvant chemotherapy trials in Dukes' B colorectal cancer patients: how much evidence is enough? Ann Oncol 2003; 14: 1026-1038
105. Nagahashi M, Ajioka Y, Lang I, Szentirmay Z, Kasler M, Nakadaira H, Yokoyama N, Watanabe G, Nishikura K, Wakai T, Shirai Y, Hatakeyama K, Yamamoto M. Genetic changes of p53, K-ras, and microsatellite instability in gallbladder carcinoma in high-incidence areas of Japan and Hungary. World J Gastroenterol 2008; 14: 70-75
106. Hsu JY, Wakelee HA. Monoclonal antibodies targeting vascular endothelial growth factor: current status and future challenges in cancer therapy. BioDrugs 2009; 23: 289-304
107. Je Y, Schutz FA, Choueiri TK. Risk of bleeding with vascular endothelial growth factor receptor tyrosine-kinase inhibitors sunitinib and sorafenib: a systematic review and metaanalysis of clinical trials. Lancet Oncol 2009; 10: 967-974
108. Wolpin BM, Meyerhardt JA, Mamon HJ, Mayer RJ. Adjuvant treatment of colorectal cancer. CA Cancer J Clin 2007; 57: 168-185
109. Sporn MB, Dunlop NM, Newton DL, Smith JM. Prevention of chemical carcinogenesis by vitamin A and its synthetic analogs (retinoids). Fed Proc 1976; 35: 1332-1338
110. Gerner EW, Meyskens FL Jr. Combination chemoprevention for colon cancer targeting polyamine synthesis and inflammation. Clin Cancer Res 2009; 15: 758-761
111. Zilli M, Iacobelli S. Chemoprophylaxis in gastrointestinal tumors. Eur Rev Med Pharmacol Sci 2010; 14: 285-291
112. Chu AJ, Chou TH, Chen BD. Prevention of colorectal cancer using COX-2 inhibitors: basic science and clinical applications. Front Biosci 2004; 9: 2697-2713
113. Wang L, Chen W, Xie X, He Y, Bai X. Celecoxib inhibits tumor growth and angiogenesis in an orthotopic implantation tumor model of human colon cancer. Exp Oncol 2008; 30: 42-51
114. Soumaoro LT, Uetake H, Takagi Y, Iida S, Higuchi T, Yasuno M, Enomoto M, Sugihara K. Coexpression of VEGF-C and Cox-2 in human colorectal cancer and its association with lymph node metastasis. Dis Colon Rectum 2006; 49: 392-398
115. Kubo H, Hosono K, Suzuki T, Ogawa Y, Kato H, Kamata H, Ito Y, Amano H, Kato T, Sakagami H, Hayashi I, Sugimoto Y, Narumiya S, Watanabe M, Majima M. Host prostaglandin EP3 receptor signaling relevant to tumor-associated lymphangiogenesis. Biomed Pharmacother 2010; 64: 101-106
116. Liu H, Yang Y, Xiao J, Lv Y, Liu Y, Yang H, Zhao L. Inhibition of cyclooxygenase-2 suppresses lymph node metastasis via VEGF-C. Anat Rec (Hoboken) 2009; 292: 1577-1583