Angiogenesis in biliary tract cancer: targeting and therapeutic potential

References

• Khan SA, Davidson BR, Goldin RD, et al. Guidelines for the diagnosis and treatment of cholangiocarcinoma: an update. Gut. 2012;61(12):1657–1669.1.
   PubMed Web of Science ®Google Scholar
• Vijgen S, Terris B, Rubbia-Brandt L. Pathology of intrahepatic cholangiocarcinoma. Hepatobiliary Surg Nutr. 2017;6(1):22–34.
   PubMed Web of Science ®Google Scholar
• Mansour JC, Aloia TA, Crane CH, et al. Hilar cholangiocarcinoma: expert consensus statement. HPB. 2015;17(8):691–699.
   PubMed Web of Science ®Google Scholar
• Bragazzi MC, Ridola L, Safarikia S, et al. New insights into cholangiocarcinoma: multiple stems and related cell lineages of origin. Ann Gastroenterol. 2018;31(1):42–55.
   PubMed Web of Science ®Google Scholar
• Mammola CL, Vetuschi A, Pannarale L, et al. Epidermal growth factor-like domain multiple 7 (EGFL7): expression and possible effect on biliary epithelium growth in cholangiocarcinoma. Eur J Histochem. 2018;62(4):2971.
   Web of Science ®Google Scholar
• Howlader N, Noone AM, Krapcho M, et al. Eds., SEER cancer statistics review, 1975–2013, national cancer institute. Bethesda, MD, based on November 2015 SEER data submission, posted to the SEER web site. April 2016. Available online: http://seer.cancer.gov/csr/1975_2013/
   Google Scholar
• Valle J, Wasan H, Palmer DH, et al. ABC-02 Trial Investigators. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362(14):1273–1281.
   PubMed Web of Science ®Google Scholar
• Neuzillet C, Casadei-Gardini A, Brieau B, et al. AGEO (association des gastro-entérologues oncologues) Investigators; GICO (Italian group of cholangiocarcinoma) investigators. fluropyrimidine single agent or doublet chemotherapy as second line treatment in advanced biliary tract cancer. Int J Cancer. 2020 Jun 11;147(11):3177–3188. Epub ahead of print. PMID: 32525595.
   PubMed Web of Science ®Google Scholar
• Fornaro L, Vivaldi C, Cereda S, et al. GICO group (Gruppo Italiano COlangiocarcinoma). Second-line chemotherapy in advanced biliary cancer progressed to first-line platinum-gemcitabine combination: a multicenter survey and pooled analysis with published data. J Exp Clin Cancer Res. 2015;34(1):156.
   PubMed Web of Science ®Google Scholar
• Enjoji M, Nakamuta M, Yamaguchi K, et al. Clinical significance of serum levels of vascular endothelial growth factor and its receptor in biliary disease and carcinoma. World J Gastroenterol. 2005;11(8):1167–1171.
   PubMed Web of Science ®Google Scholar
• Glaser SS, Gaudio E, Alpini G. Vascular factors, angiogenesis and biliary tract disease. Curr Opin Gastroenterol. 2010;26(3):246–250.
   PubMed Web of Science ®Google Scholar
• Simone V, Brunetti O, Lupo L, et al., Targeting angiogenesis in biliary tract cancers: an open option. Int J Mol Sci. 2017; 18(2): 418.
   Web of Science ®Google Scholar
• Yoon JH, Canbay AE, Werneburg NW, et al. Oxysterols induce cyclooxygenase-2 expression in cholangiocytes: implications for biliary tract carcinogenesis. Hepatology. 2004;39(3):732–738.
   PubMed Web of Science ®Google Scholar
• Jaiswal M, LaRusso NF, Gores GJ. Nitric oxide in gastrointestinal epithelial cell carcinogenesis: linking inflammation to oncogenesis. Am J Physiol Gastrointest Liver Physiol. 2001;281(3):G626–G634.
   PubMed Web of Science ®Google Scholar
• Leyva-Illades D, McMillin M, Quinn M, et al. Cholangiocarcinoma pathogenesis: role of the tumor microenvironment. Transl. Gastrointest. Cancer. 2012;1(1):71–80.
   PubMedGoogle Scholar
• Hasita H, Komohara Y, Okabe H, et al. Significance of alternatively activated macrophages in patients with intrahepatic cholangiocarcinoma. Cancer Sci. 2010;101(8):1913–1919.
   PubMed Web of Science ®Google Scholar
• Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307(5706):58–62.
   PubMed Web of Science ®Google Scholar
• Yoshikawa D, Ojima H, Iwasaki M, et al., Clinicopathological and prognostic significance of EGFR, VEGF, and HER2 expression in cholangiocarcinoma. Br J Cancer. 2008; 98(2): 418–425.
   PubMed Web of Science ®Google Scholar
• Tang D, Nagano H, Yamamoto H, et al. Angiogenesis in cholangiocellular carcinoma: expression of vascular endothelial growth factor, angiopoietin-1/2, thrombospondin-1 and clinicopathological significance. Oncol Rep. 2006;15(3):525–532.
   PubMed Web of Science ®Google Scholar
• Wiggers JK, Ruys AT, Groot Koerkamp B, et al. Differences in immunohistochemical biomarkers between intra- and extrahepatic cholangiocarcinoma: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2014;29(8):1582–1594.
   PubMed Web of Science ®Google Scholar
• Vidal-Vanaclocha F. The prometastatic microenvironment of the liver. Cancer Microenviron. 2008;1(1):113–129.
   PubMedGoogle Scholar
• Chen Y, Chen Y, Yu G, et al. Lymphangiogenic and angiogentic microvessel density in gallbladder carcinoma. Hepatogastroenterology. 2011;58(105):20–25.
   PubMedGoogle Scholar
• Thelen A, Scholz A, Weichert W, et al. Tumor-associated angiogenesis and lymphangiogenesis correlate with progression of intrahepatic cholangiocarcinoma. Am J Gastroenterol. 2010;105(5):1123–1132.
   PubMed Web of Science ®Google Scholar
• Thelen A, Scholz A, Benckert C, et al. Microvessel density correlates with lymph node metastases and prognosis in hilar cholangiocarcinoma. J Gastroenterol. 2008;43(12):959–966.
   PubMed Web of Science ®Google Scholar
• Boonjaraspinyo S, Boonmars T, Wu Z, et al. Platelet-derived growth factor may be a potential diagnostic and prognostic marker for cholangiocarcinoma. Tumour Biol. 2012;33(5):1785–1802.
   PubMedGoogle Scholar
• Voigtländer T, David S, Thamm K, et al. Angiopoietin-2 and biliary diseases: elevated serum, but not bile levels are associated with cholangiocarcinoma. PLoS One. 2014;9(5):e97046.
   PubMed Web of Science ®Google Scholar
• Fava G, Demorrow S, Gaudio E, et al. Endothelin inhibits cholangiocarcinoma growth by a decrease in the vascular endothelial growth factor expression. Liver Int. 2009;29(7):1031–1042.
   PubMed Web of Science ®Google Scholar
• Vaeteewoottacharn K, Kariya R, Dana P, et al. Inhibition of carbonic anhydrase potentiates bevacizumab treatment in cholangiocarcinoma. Tumour Biol. 2016;37(7):9023–9035.
   PubMedGoogle Scholar
• Sugiyama H, Onuki K, Ishige K, et al. Potent in vitro and in vivo antitumor activity of sorafenib against human intrahepatic cholangiocarcinoma cells. J Gastroenterol. 2011;46(6):779–789.
   PubMed Web of Science ®Google Scholar
• Kim DH, Jeong YI, Chung CW, et al. Preclinical evaluation of sorafenib-eluting stent for suppression of human cholangiocarcinoma cells. Int J Nanomed. 2013;8:1697–1711.
   PubMed Web of Science ®Google Scholar
• Yoshikawa D, Ojima H, Kokubu A, et al. Vandetanib (ZD6474), an inhibitor of VEGFR and EGFR signalling, as a novel molecular-targeted therapy against cholangiocarcinoma. Br J Cancer. 2009;100(8):1257–1266.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Ojima H, Shimizu H, et al. Axitinib (AG-013736), an oralspecific VEGFR TKI, shows potential therapeutic utility against cholangiocarcinoma. Jpn J Clin Oncol. 2014;44(6):570–578.
   PubMed Web of Science ®Google Scholar
• Masoud GN, Li WHIF. 1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B. 2015;5(5):378–389.
   PubMed Web of Science ®Google Scholar
• Horiuchi H, Kawamata H, Fujimori T, et al. A MEK inhibitor (U0126) prolongs survival in nude mice bearing human gallbladder cancer cells with K-Ras mutation: analysis in a novel orthotopic inoculation model. Int J Oncol. 2003;23(4):957–963.
   PubMed Web of Science ®Google Scholar
• Cavalloni G, Peraldo-Neia C, Varamo C, et al. Preclinical activity of EGFR and MEK1/2 inhibitors in the treatment of biliary tract carcinoma. Oncotarget. 2016;7(32):52354–52363.
   Google Scholar
• Nakamura H, Arai Y, Totoki Y, et al., Genomic spectra of biliary tract cancer. Nat Genet. 2015; 47(9): 1003–1010.
   PubMed Web of Science ®Google Scholar
• Zhu AX, Meyerhardt JA, Blaszkowsky LS, et al. Efficacy and safety of gemcitabine, oxaliplatin, and bevacizumab in advanced biliary-tract cancers and correlation of changes in 18-fluorodeoxyglucose PET with clinical outcome: a phase 2 study. Lancet Oncol. 2010;11(1):48–54.
   PubMed Web of Science ®Google Scholar
• Lubner SJ, Mahoney MR, Kolesar JL, et al. Report of a multicenter phase II trial testing a combination of biweekly bevacizumab and daily erlotinib in patients with unresectable biliary cancer: a phase II consortium study. J Clin Oncol. 2010;28(21):3491–3497.
   PubMed Web of Science ®Google Scholar
• Guion-Dusserre JF, Lorgis V, Vincent J, et al. FOLFIRI plus bevacizumab as a second-line therapy for metastatic intrahepatic cholangiocarcinoma. World J Gastroenterol. 2015;21(7):2096–2101.
   PubMed Web of Science ®Google Scholar
• Larsen FO, Markussen A, Diness LV, et al. Efficacy and safety of capecitabine, irinotecan, gemcitabine, and bevacizumab as second-line treatment in advanced biliary tract cancer: a phase II study. Oncology. 2018;94(1):19–24.
   PubMed Web of Science ®Google Scholar
• Valle JW, Wasan H, Lopes A, et al. Cediranib or placebo in combination with cisplatin and gemcitabine chemotherapy for patients with advanced biliary tract cancer (ABC-03): a randomised phase 2 trial. Lancet Oncol. 2015;16(8):967–978.
   PubMed Web of Science ®Google Scholar
• Peng H, Zhang Q, Li J, et al. Apatinib inhibits VEGF signaling and promotes apoptosis in intrahepatic cholangiocarcinoma. Oncotarget. 2016 Mar 29;7(13):17220–17229.
   PubMedGoogle Scholar
• Shroff RT, Yarchoan M, O’Connor A, et al. The oral VEGF receptor tyrosine kinase inhibitor pazopanib in combination with the MEK inhibitor trametinib in advanced cholangiocarcinoma. Br J Cancer. 2017;116(11):1402–1407.
   PubMed Web of Science ®Google Scholar
• Sun W, Patel A, Normolle D, et al. A phase 2 trial of regorafenib as a single agent in patients with chemotherapy-refractory, advanced, and metastatic biliary tract adenocarcinoma. Cancer. 2019;125(6):902–909.
   PubMed Web of Science ®Google Scholar
• Kim RD, Stewart Poklepovic A, Nixon AB, et al. Multi institutional phase II trial of single agent regorafenib in refractory advanced biliary cancers. J Clin Oncol. 2018;36(15_suppl):4082.
   Web of Science ®Google Scholar
• Bengala C, Bertolini F, Malavasi N, et al. Sorafenib in patients with advanced biliary tract carcinoma: a phase II trial. Br J Cancer. 2010;102(1):68–72.
   PubMed Web of Science ®Google Scholar
• El-Khoueiry AB, Rankin CJ, Ben-Josef E, et al. SWOG 0514: a phase II study of sorafenib in patients with unresectable or metastatic gallbladder carcinoma and cholangiocarcinoma. Investig New Drugs. 2012;30(4):1646–1651.
   PubMed Web of Science ®Google Scholar
• Moehler M, Maderer A, Schimanski C, et al. Working group of internal oncology. gemcitabine plus sorafenib versus gemcitabine alone in advanced biliary tract cancer: a double-blind placebo-controlled multicentre phase II AIO study with biomarker and serum programme. Eur J Cancer. 2014;50(18):3125–3135.
   PubMed Web of Science ®Google Scholar
• Lee JK, Capanu M, O’Reilly EM, et al. A phase II study of gemcitabine and cisplatin plus sorafenib in patients with advanced biliary adenocarcinomas. Br J Cancer. 2013;109(4):915–919.
   PubMed Web of Science ®Google Scholar
• El-Khoueiry AB, Rankin C, Siegel AB, et al. S0941: a phase 2 SWOG study of sorafenib and erlotinib in patients with advanced gallbladder carcinoma or cholangiocarcinoma. Br J Cancer. 2014;110(4):882–887.
   PubMed Web of Science ®Google Scholar
• Kessler ER, Eckhardt SG, Pitts TM, et al. Phase I trial of vandetanib in combination with gemcitabine and capecitabine in patients with advanced solid tumors with an expanded cohort in pancreatic and biliary cancers. Invest New Drugs. 2016;34(2):176–183.
   PubMed Web of Science ®Google Scholar
• Santoro A, Gebbia V, Pressiani T, et al. A randomized, multicenter, phase II study of vandetanib monotherapy versus vandetanib in combination with gemcitabine versus gemcitabine plus placebo in subjects with advanced biliary tract cancer: the VanGogh study. Ann Oncol. 2015;26(3):542–547.
   PubMed Web of Science ®Google Scholar
• Yi JH, Thongprasert S, Lee J, et al. A phase II study of sunitinib as a second-line treatment in advanced biliary tract carcinoma: a multicentre, multinational study. Eur J Cancer. 2012;48(2):196–201.
   PubMed Web of Science ®Google Scholar
• Gabrilovich D, Ishida T, Oyama T, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 1998;92(11):4150–4166.
   PubMed Web of Science ®Google Scholar
• Hack SP, Spahn J, Chen M, et al. IMbrave 050: a Phase III trial of atezolizumab plus bevacizumab in high-risk hepatocellular carcinoma after curative resection or ablation. Future Oncol. 2020 May;16(15):975–989.
   PubMed Web of Science ®Google Scholar
• Osada T, Chong G, Tansik R, et al. The effect of anti-VEGF therapy on immature myeloid cell and dendritic cells in cancer patients. Cancer Immunol Immunother. 2008;57(8):1115–1124.
   PubMed Web of Science ®Google Scholar
• Allen E, Jabouille A, Rivera LB, et al., Combined antiangiogenic and anti-PD-L1 therapy stimulates tumor immunity through HEV formation. Sci Transl Med. 2017; 9(385): eaak9679.
   Web of Science ®Google Scholar
• Tian L, Goldstein A, Wang H, et al., Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming. Nature. 2017; 544(7649): 250–254.
   PubMed Web of Science ®Google Scholar
• Arkenau HT, Martin-Liberal J, Calvo E, et al. Ramucirumab plus pembrolizumab in patients with previously treated advanced or metastatic biliary tract cancer: nonrandomized, open-label, phase I trial (JVDF). Oncologist. 2018;23(12):1407–e136.
   PubMed Web of Science ®Google Scholar
• Haitao Z”Lenvatinib combined pembrolizumab as a second-line treatment in advanced hepatobiliary tumors: a single-center, single-arm, non-randomized clinical study”. NCT03895970.
   Google Scholar
• Haitao H,“Axitinib plus toripalimab as second-line treatment in hepatobiliary malignant tumors”. NCT04010071.
   Google Scholar
• Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017 Dec;14(12):749–762. Epub 2017 Oct 4. PMID: 28975929.
   PubMed Web of Science ®Google Scholar
• Sadot E, Simpson AL, Do RKG, et al. Cholangiocarcinoma: correlation between molecular profiling and imaging phenotypes. PLoS One. 2015;10(7):1–12.
   Web of Science ®Google Scholar
• Segal E, Sirlin CB, Ooi C, et al. Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol. 2007;25(6):675–680.
   PubMed Web of Science ®Google Scholar
• Peng YT, Zhou CY, Lin P, et al., Preoperative ultrasound radiomics signatures for noninvasive evaluation of biological characteristics of intrahepatic cholangiocarcinoma. Acad Radiol. 2020 Jun;27(6):785–797. Epub 2019 Sep 5. PMID: 31494003.
   PubMed Web of Science ®Google Scholar