Integrin α4 Induces Lymphangiogenesis and Metastasis via Upregulation of VEGF-C in Human Colon Cancer

Anatomical Record

Volumn 299, Issue 6, 2016, Pages 741-747

  Lv, Xiao Hong ^a   Liu, Bao Quan ^a   Li, Xue Mei ^a   Wang, Xiang Chen ^a   Li, Xin Lei ^a   Ahmed, Naila ^a   Zhang, Ya Fang ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Colon cancer; Integrin 4; Lymphatic metastasis; Vascular endothelial growth factor C; VEGFR 3

Indexed keywords

ALPHA4 INTEGRIN; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 3; VERY LATE ACTIVATION ANTIGEN 4;

ADULT; AGED; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CAPILLARY DENSITY; COLON CANCER; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; SURVIVAL TIME; UPREGULATION; COLON TUMOR; LYMPH VESSEL; METABOLISM; MICROVASCULATURE; MIDDLE AGED; MORTALITY; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; SURVIVAL RATE; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; COLONIC NEOPLASMS; FEMALE; HUMANS; INTEGRIN ALPHA4; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; LYMPHATIC VESSELS; MALE; MICROVESSELS; MIDDLE AGED; PROGNOSIS; SURVIVAL RATE; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; YOUNG ADULT;

EID: 84963502578     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.23338     Document Type: Article

References (34)

1. Avraamides CJ, Garmy-Susini B, Varner JA. 2008. Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 8:604-617.
2. Cao R, Ji H, Feng N, Zhang Y, Yang X, Andersson P, Sun Y, Tritsaris K, Hansen JA, Dissing S, and Cao Y. 2012. Collaborative interplay between FGF-2 and VEGF-C promotes lymphangiogenesis and metastasis. Proc Natl Acad Sci USA 109:15894-15899.
3. Cekaite L, Rantala JK, Bruun J, Guriby M, Ågesen TH, Danielsen SA, Lind GE, Nesbakken A, Kallioniemi O, Lothe RA, and Skotheim RI. 2012. MiR-9, -31, and -182 deregulation promote proliferation and tumor cell survival in colon cancer. Neoplasia 14:868-879.
4. Delforge M, Raets V, Van Duppen V, Vandenberghe P, and Boogaerts M. 2005. CD34+ marrow progenitors from MDS patients with high levels of intramedullary apoptosis have reduced expression of alpha4beta1 and alpha5beta1 integrins. Leukemia 19:57-63.
5. Garmy-Susini B, Avraamides CJ, Schmid MC, Foubert P, Ellies LG, Barnes L, Feral C, Papayannopoulou T, Lowy A, Blair SL, Cheresh D, Ginsberg M, and Varner JA . 2010. Integrin α4β1 signaling is required for lymphangiogenesis and tumor metastasis. Cancer Res 70:3042-3051.
6. Garmy-Susini B, Jin H, Zhu Y, Sung R-J, Hwang R, Varner J. 2005. Integrin α4β1-VCAM-1-mediated adhesion between endothelial and mural cells is required for blood vessel maturation. J Clin Invest 115:1542-1551.
7. Goel HL, Li J, Kogan S, Languino LR. 2008. Integrins in prostate cancer progression. Endocr Relat Cancer 15:657-664.
8. Gogineni A, Caunt M, Crow A, Lee CV, Fuh G, Bruggen NV, Ye W, Weimer RM. 2013. Inhibition of VEGF-C modulates distal lymphatic remodeling and secondary metastasis. PLos One 8:e68755.
9. Gou H, Chen X, Zhu J, Jiang M, Yang Y, Cao D, Hou M. 2011. Expressions of COX-2 and VEGF-C in gastric cancer: correlations with lymphangiogenesis and prognostic implications. J Exp Clin Cancer Res 30:14-21.
10. Gupta BK, Maher DM, Ebeling MC, Sundram V, Koch MD, Lynch DW, Bohlmeyer T, Watanabe A, Aburatani H, Puumala SE, Jaggi M, and Chauhan SC . 2012. Increased expression and aberrant localization of mucin 13 in metastatic colon cancer. J Histochem Cytochem 60:822-831.
11. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. 2007. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109:1010-1017.
12. Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H, Swartz M, Fukumura D, Jain RK, Alitalo K. 1997. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276:1423-1425.
13. Kang P, Wan M, Huang P, Li C, Wang Z, Zhong X, Hu Z, Tai S, Cui Y. 2014. The Wnt antagonist sFRP1 as a favorable prognosticator in human biliary tract carcinoma. PLos One 9:e90308.
14. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K . 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5:74-80.
15. Kawamura L, Carvalho FM, Alves BG, Bacchi CE, Goes JC, Calil MA, Baracat EC, Carvalho JP. 2010. Association between intratumoral lymphatic microvessel density (LMVD) and clinicopathologic features in endometrial cancer: a retrospective cohort study. World J Surg Oncol 8:89-95.
16. Leu ST, Jacques SA, Wingerd KL, Hikita ST, Tolhurst EC, Pring JL, Wiswell D, Kinney L, Goodman NL, Jackson DY, Clegg DO . 2004. Integrin alpha4beta1 function is required for cell survival in developing retina. Dev Biol 276:416-430.
17. Li X, Liu B, Xiao J, Yuan Y, Ma J, Zhang Y. 2011. Roles of VEGF-C and Smad4 in the lymphangiogenesis, lymphatic metastasis, and prognosis in colon cancer. J Gastrointest Surg 15:2001-2010.
18. Millard M, Odde S, Neamati N. 2011. Integrin targeted therapeutics. Theranostics 1:154-188.
19. Min Y, Ghose S, Boelte K, Li J, Yang L, Lin PC. 2011. C/EBP-δ regulates VEGF-C autocrine signaling in lymphangiogenesis and metastasis of lung cancer through HIF-1α. Oncogene 30:4901-4909.
20. Niu G, Chen X. 2011. Why integrin as a primary target for imaging and therapy. Theranostics 1:30-47.
21. Pinco KA, He W, Yang JT. 2002. α4β1 integrin regulates lamellipodia protrusion via a focal complex/focal adhesion-independent mechanism. Mol Biol Cell 13:3203-3217.
22. Ran S, Volk L, Hall K, Flister MJ. 2010. Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 17:229-251.
23. Rebhun RB, Cheng H, Gershenwald JE, Fan D, Fidler IJ, and Langley RR. 2010. Constitutive expression of the α4 integrin correlates with tumorigenicity and lymph node metastasis of the B16 murine melanoma. Neoplasia 12:173-182.
24. Siegel R, Ward E, Brawley O, Jemal A. 2011. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61:212-236.
25. Su JL, Chen PS, Chien MH, Chen PB, Chen YH, Lai CC, Hung MC, Kuo ML. 2008. Further evidence for expression and function of the VEGF-C/VEGFR-3 axis in cancer cells. Cancer cell 13:557-560.
26. Tanaka T, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Katada T, Shiozaki M, Naganawa Y, Fujii Y, and Takeyama H. 2010. Research vascular endothelial growth factor C (VEGF-C) in esophageal cancer correlates with lymph node metastasis and poor patient prognosis. J Exp Clin Cancer Res 29:83-89.
27. Testaz S, Duband JL. 2001. Central role of the alpha4beta1 integrin in the coordination of avian truncal neural crest cell adhesion, migration, and survival. Dev Dyn 222:127-140.
28. Wang C-A, Jedlicka P, Patrick AN, Micalizzi DS, Lemmer KC, Deitsch E, Casás-Selves M, Chuck Harrell J, and Ford HL. 2012. SIX1 induces lymphangiogenesis and metastasis via upregulation of VEGF-C in mouse models of breast cancer. J Clin Invest 122:1895-1906.
29. Wang L, Shirure VS, Burdick MM, Wu S. 2011. UVB-irradiation regulates VLA-4-mediated melanoma cell adhesion to endothelial VCAM-1 under flow conditions. Mol Carcinog 50:58-65.
30. Wu L, Bernard-Trifilo JA, Lim Y, Lim S-T, Mitra SK, Uryu S, Chen M, Pallen CJ, Cheung N-KV, Mikolon D, Mielgo A, Stupack DG, Schlaepfer DD . 2008. Distinct FAK-Src activation events promote α5β1 and α4β1 integrin-stimulated neuroblastoma cell motility. Oncogene 27:1439-1448.
31. Wu Q, She H, Liang J, Huang Y, Yang Q, Yang Q, and Zhang Z. 2012. Expression and clinical significance of extracellular matrix protein 1 and vascular endothelial growth factor-C in lymphatic metastasis of human breast cancer. BMC Cancer 12:47-58.
32. Xie L-X, Zhai T, Yang L, Yang E, Zhang X, Chen J, and Zhang H. 2013. Lymphangiogenesis and prognostic significance of vascular endothelial growth factor C in gastro-oesophageal junction adenocarcinoma. Int J Exp Pathol 94:39-46.
33. Yang H, Kim C, Kim M, Schwendener RA, Alitalo K, Heston W, Kim I, Kim W, and Koh GY. 2011. Soluble vascular endothelial growth factor receptor-3 suppresses lymphangiogenesis and lymphatic metastasis in bladder cancer. Mol Cancer 10:36-47.
34. Zhang C, Hao L, Wang L, Xiao Y, Ge H, Zhu Z, Luo Y, Zhang Y, and Zhang Y. 2010. Research article Elevated IGFIR expression regulating VEGF and VEGF-C predicts lymph node metastasis in human colorectal cancer. BMC Cancer 10:184-194.