The apelin-APJ system induces tumor arteriogenesis in hepatocellular carcinoma

Anticancer Research

Volumn 34, Issue 10, 2014, Pages 5313-5320

  Muto, Jun ^a,b   Shirabe, Ken ^a   Yoshizumi, Tomoharu ^a   Ikegami, Toru ^a   Aishima, Shinichi ^a   Ishigami, Kousei ^a   Yonemitsu, Yoshikazu ^b   Ikeda, Tetsuo ^a   Soejima, Yuji ^a   Maehara, Yoshihiko ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Apelin; APJ; Arteriogenesis; Hepatocellular carcinoma

Indexed keywords

ANTINEOPLASTIC AGENT; APELIN; F 13A; MESSENGER RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; APELIN-13, ALA(13)-; APLN PROTEIN, HUMAN; APLNR PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; SIGNAL PEPTIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SMOOTH MUSCLE; TUMOR GROWTH; ANGIOGRAPHY; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; LIVER NEOPLASMS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; TUMOR VOLUME;

ANGIOGRAPHY; ANIMALS; CARCINOMA, HEPATOCELLULAR; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; MICE; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, G-PROTEIN-COUPLED; TUMOR BURDEN;

EID: 84917738155     PISSN: 02507005     EISSN: 17917530     Source Type: Journal    
DOI: None     Document Type: Article

References (31)

1. Zhu AX, Duda DG, Sahani DV and Jain RK: HCC and angiogenesis: possible targets and future directions. Nat Rev Clin Oncol 8: 292-301, 2011.
2. Sonoda T, Shirabe K, Takenaka K, Kanematsu T, Yasumori K and Sugimachi K: Angiographically undetected small hepatocellular carcinoma: clinicopathological characteristics, follow-up and treatment. Hepatology 10: 1003-1007, 1989.
3. Tanigawa N, Lu C, Mitsui T and Miura S: Quantitation of sinusoid-like vessels in hepatocellular carcinoma: its clinical and prognostic significance. Hepatology 26: 1216-1223, 1997.
4. Carr BI: Hepatocellular carcinoma: current management and future trends. Gastroenterology 127: S218-224, 2004.
5. Muto J, Shirabe K, Sugimachi K and Maehara Y: Review of angiogenesis in hepatocellular carcinoma. Hepatology research: the official journal of the Japan Society of Hepatology 2014.
6. Matsui O, Kobayashi S, Sanada J, Kouda W, Ryu Y, Kozaka K, Kitao A, Nakamura K and Gabata T: Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging 36: 264-272, 2011.
7. Zhu AX: Systemic treatment of hepatocellular carcinoma: dawn of a new era? Ann Surg Oncol 17: 1247-1256, 2010.
8. Sugimachi K, Tanaka S, Taguchi K, Aishima S, Shimada M and Tsuneyoshi M: Angiopoietin switching regulates angiogenesis and progression of human hepatocellular carcinoma. J Clin Pathol 56: 854-860, 2003.
9. Mitsuhashi N, Shimizu H, Ohtsuka M, Wakabayashi Y, Ito H, Kimura F, Yoshidome H, Kato A, Nukui Y and Miyazaki M: Angiopoietins and Tie-2 expression in angiogenesis and proliferation of human hepatocellular carcinoma. Hepatology 37: 1105-1113, 2003.
10. Yang XR, Xu Y, Yu B, Zhou J, Qiu SJ, Shi GM, Zhang BH, Wu WZ, Shi YH, Wu B, Yang GH, Ji Y and Fan J: High expression levels of putative hepatic stem/progenitor cell biomarkers related to tumour angiogenesis and poor prognosis of hepatocellular carcinoma. Gut 59: 953-962, 2010.
11. O'Dowd BF, Heiber M, Chan A, Heng HH, Tsui LC, Kennedy JL, Shi X, Petronis A, George SR and Nguyen T: A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene 136: 355-360, 1993.
12. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, Kawamata Y, Fukusumi S, Hinuma S, Kitada C, Kurokawa T, Onda H and Fujino M: Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 251: 471-476, 1998.
13. Eyries M, Siegfried G, Ciumas M, Montagne K, Agrapart M, Lebrin F and Soubrier F: Hypoxia-induced apelin expression regulates endothelial cell proliferation and regenerative angiogenesis. Circ Res 103: 432-440, 2008.
14. Kidoya H, Ueno M, Yamada Y, Mochizuki N, Nakata M, Yano T, Fujii R and Takakura N: Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J 27: 522-534, 2008.
15. Dai T, Ramirez-Correa G and Gao WD: Apelin increases contractility in failing cardiac muscle. Eur J Pharmacol 553: 222-228, 2006.
16. Zhong JC, Huang DY, Liu GF, Jin HY, Yang YM, Li YF, Song XH and Du K: Effects of all-trans retinoic acid on orphan receptor APJ signaling in spontaneously hypertensive rats. Cardiovasc Res 65: 743-750, 2005.
17. Cui RR, Mao DA, Yi L, Wang C, Zhang XX, Xie H, Wu XP, Liao XB, Zhou H, Meng JC, Yuan LQ and Liao EY: Apelin suppresses apoptosis of human vascular smooth muscle cells via APJ/PI3-K/Akt signaling pathways. Amino Acids 39: 1193-1200, 2010.
18. Hashimoto T, Kihara M, Ishida J, Imai N, Yoshida S, Toya Y, Fukamizu A, Kitamura H and Umemura S: Apelin stimulates myosin light chain phosphorylation in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 26: 1267-1272, 2006.
19. Kidoya H, Naito H and Takakura N: Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischemia. Blood 115: 3166-3174, 2010.
20. Berta J, Kenessey I, Dobos J, Tovari J, Klepetko W, Jan Ankersmit H, Hegedus B, Renyi-Vamos F, Varga J, Lorincz Z, Paku S, Ostoros G, Rozsas A, Timar J and Dome B: Apelin expression in human non-small cell lung cancer: role in angiogenesis and prognosis. J Thorac Oncol 5: 1120-1129, 2010.
21. Heo K, Kim YH, Sung HJ, Li HY, Yoo CW, Kim JY, Park JY, Lee UL, Nam BH, Kim EO, Kim SY, Lee SH, Park JB and Choi SW: Hypoxia-induced up-regulation of apelin is associated with a poor prognosis in oral squamous cell carcinoma patients. Oral Oncol 2012.
22. Wang Z, Greeley GH Jr. and Qiu S: Immunohistochemical localization of apelin in human normal breast and breast carcinoma. J Mol Histol 39: 121-124, 2008.
23. Sorli SC, van den Berghe L, Masri B, Knibiehler B and Audigier Y: Therapeutic potential of interfering with apelin signalling. Drug Discov Today 11: 1100-1106, 2006.
24. Sorli SC, Le Gonidec S, Knibiehler B and Audigier Y: Apelin is a potent activator of tumour neoangiogenesis. Oncogene 26: 7692-7699, 2007.
25. Kayashima H, Toshima T, Okano S, Taketomi A, Harada N, Yamashita Y, Tomita Y, Shirabe K and Maehara Y: Intratumoral neoadjuvant immunotherapy using IL-12 and dendritic cells is an effective strategy to control recurrence of murine hepatocellular carcinoma in immunosuppressed mice. J Immunol 185: 698-708, 2010.
26. Fujita N, Aishima S, Iguchi T, Nishihara Y, Yamamoto H, Taketomi A, Oda Y, Honda H and Tsuneyoshi M: Down-regulation of artery in moderately differentiated hepatocellular carcinoma related to tumor development. Hum Pathol 41: 838-847, 2010.
27. Kim HC, Kim TK, Sung KB, Yoon HK, Kim PN, Ha HK, Kim AY, Kim HJ and Lee MG: CT during hepatic arteriography and portography: an illustrative review. Radiographics 22: 1041-1051, 2002.
28. Park YN, Kim YB, Yang KM, Park C. Increased expression of vascular endothelial growth factor and angiogenesis in the early stage of multistep hepatocarcinogenesis. Arch Pathol Lab Med 124: 1061-1065, 2000.
29. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, Politi LS, Gentner B, Brown JL, Naldini L and De Palma M: Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 19: 512-526, 2011.
30. Kidoya H, Kunii N, Naito H, Muramatsu F, Okamoto Y, Nakayama T and Takakura N: The apelin/APJ system induces maturation of the tumor vasculature and improves the efficiency of immune therapy. Oncogene 2011.
31. Zhang ZB, Cai L, Zheng SG, Xiong Y and Dong JH: Overexpression of caveolin-1 in hepatocellular carcinoma with metastasis and worse prognosis: correlation with vascular endothelial growth factor, microvessel density and unpaired artery. Pathology oncology research: POR 15: 495-502, 2009.