Cancer‑associated fibroblast regulation of tumor neo‑angiogenesis as a therapeutic target in cancer (Review)
- Authors:
- Fang‑Tao Wang
- Wei Sun
- Jing‑Tao Zhang
- Yue‑Zu Fan
-
Affiliations: Department of Surgery, Tongji Hospital, Tongji University School of Medicine, Shanghai 200065, P.R. China, Department of Surgery, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai 200072, P.R. China - Published online on: January 25, 2019 https://doi.org/10.3892/ol.2019.9973
- Pages: 3055-3065
-
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Folkman J: Anti-angiogenesis: New concept for therapy of solid tumors. Ann Surg. 175:409–416. 1972. View Article : Google Scholar : PubMed/NCBI | |
Huang G and Chen L: Tumor vasculature and microenvironment normalization: A possible mechanism of antiangiogenesis therapy. Cancer Biother Radiopharm. 23:661–667. 2008. View Article : Google Scholar : PubMed/NCBI | |
Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS and Hendrix MJ: Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. Am J Pathol. 155:739–752. 1999. View Article : Google Scholar : PubMed/NCBI | |
Folberg R, Hendrix M and Maniotis A: Vasculogenic mimicry and tumor angiogenesis. Am J Pathol. 156:361–381. 2000. View Article : Google Scholar : PubMed/NCBI | |
Senger D and Davis G: Angiogenesis. Cold Spring Harb Perspect Biol. 3:a0050902011. View Article : Google Scholar : PubMed/NCBI | |
Rhee J and Hoff P: Angiogenesis inhibitors in the treatment of cancer. Expert Opin Pharmacother. 6:1701–1711. 2005. View Article : Google Scholar : PubMed/NCBI | |
Fan YZ and Sun W: Molecular regulation of vasculogenic mimicry in tumors and potential tumor-target therapy. World J Gastrointest Surg. 2:117–127. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chen HX and Cleck JN: Adverse effects of anticancer agents that target the VEGF pathway. Nat Rev Clin Oncol. 6:465–477. 2009. View Article : Google Scholar : PubMed/NCBI | |
Higa GM and Abraham J: Biological mechanisms of bevacizumab-associated adverse events. Expert Rev Anticancer Ther. 9:999–1007. 2009. View Article : Google Scholar : PubMed/NCBI | |
Liotta LA and Kohn EC: The microenvironment of the tumour-host interface. Nature. 411:375–379. 2001. View Article : Google Scholar : PubMed/NCBI | |
Reisfeld RA: The tumor microenvironment: A target for combination therapy of breast cancer. Crit Rev Oncog. 18:115–133. 2013. View Article : Google Scholar : PubMed/NCBI | |
Micke P and Ostman A: Tumour-stroma interaction: Cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung Cancer. 45:(Suppl 2). S163–S175. 2004. View Article : Google Scholar : PubMed/NCBI | |
Franco OE, Shaw AK, Strand DW and Hayward SW: Cancer associated fibroblasts in cancer pathogenesis. Semin Cell Dev Biol. 21:33–39. 2010. View Article : Google Scholar : PubMed/NCBI | |
O'Reilly MS: Antiangiogenesis and vascular endothelial growth factor/vascular endothelial growth factor receptor targeting as part of a combined-modality approach to the treatment of cancer. Int J Radiat Oncol Biol Phys. 69:S64–S66. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hajitou A, Sounni NE, Devy L, Grignet-Debrus C, Lewalle JM, Li H, Deroanne C, Lu H, Colige A, Nusgens BV, et al: Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: Effect on in vivo mammary tumor growth and angiogenesis. Cancer Res. 61:3450–3457. 2001.PubMed/NCBI | |
Sato M, Arap W and Pasqualini R: Molecular targets on blood vessels for cancer therapies in clinical trials. Oncology (Williston Park). 21:1346–1355, 1367, 1370 passim. 2007.PubMed/NCBI | |
Zhang JT, Fan YZ, Chen CQ, Zhao ZM and Sun W: Norcantharidin: A potential antiangiogenic agent for gallbladder cancers in vitro and in vivo. Int J Oncol. 40:1501–1514. 2012.PubMed/NCBI | |
Ma J and Waxman DJ: Combination of antiangiogenesis with chemotherapy for more effective cancer treatment. Mol Cancer Ther. 7:3670–3684. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kamrava M, Bernstein MB, Camphausen K and Hodge J: Combining radiation, immunotherapy, and antiangiogenesis agents in the management of cancer: The Three Musketeers or just another quixotic combination? Mol Biosyst. 5:1262–1270. 2009. View Article : Google Scholar : PubMed/NCBI | |
Frenkel S, Barzel I, Levy J, Lin AY, Bartsch DJ, Majumdar D, Folberg R and Pe'er J: Demonstrating circulation in vasculogenic mimicry patterns of uveal melanoma by confocal indocyanine green angiography. Eye (Lond). 22:948–952. 2008. View Article : Google Scholar : PubMed/NCBI | |
Xu Y, Li Q, Li XY, Yang QY, Xu WW and Liu GL: Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. J Exp Clin Cancer Res. 31:162012. View Article : Google Scholar : PubMed/NCBI | |
Sun W, Fan YZ, Zhang WZ and Ge CY: A pilot histomorphology and hemodynamic of vasculogenic mimicry in gallbladder carcinomas in vivo and in vitro. J Exp Clin Cancer Res. 30:462011. View Article : Google Scholar : PubMed/NCBI | |
Lu XS, Sun W, Ge CY, Zhang WZ and Fan YZ: Contribution of the PI3K/MMPs/Ln-5γ2 and EphA2/FAK/Paxillin signaling pathways to tumor growth and vasculogenic mimicry of gallbladder carcinomas. Int J Oncol. 42:2103–2115. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang JT, Sun W, Zhang WZ, Ge CY, Liu ZY, Zhao ZM, Lu XS and Fan YZ: Norcantharidin inhibits tumor growth and vasculogenic mimicry of human gallbladder carcinomas by suppression of the PI3-K/MMPs/Ln-5γ2 signaling pathway. BMC Cancer. 14:1932014. View Article : Google Scholar : PubMed/NCBI | |
Wang H, Sun W, Zhang WZ, Ge CY, Zhang JT, Liu ZY and Fan YZ: Inhibition of tumor vasculogenic mimicry and prolongation of host survival in highly aggressive gallbladder cancers by norcantharidin via blocking the ephrin type a receptor 2/focal adhesion kinase/paxillin signaling pathway. PLoS One. 9:e969822014. View Article : Google Scholar : PubMed/NCBI | |
Zhu W, Sun W, Zhang JT, Liu ZY, Li XP and Fan YZ: Norcantharidin enhances TIMP-2 anti-vasculogenic mimicry activity for human gallbladder cancers through downregulating MMP-2 and MT1-MMP. Int J Oncol. 46:627–640. 2015. View Article : Google Scholar : PubMed/NCBI | |
Han H, Du L, Cao Z, Zhang B and Zhou Q: Triptonide potently suppresses pancreatic cancer cell-mediated vasculogenic mimicry by inhibiting expression of VE-cadherin and chemokine ligand 2 genes. Eur J Pharmacol. 818:593–603. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Zhao M, Zhisheng Z, Lin C, Yayun Q, Xuanyi W, Feng J, Haibo W, Youyang S, Tadashi H, et al: COE inhibits vasculogenic mimicry in hepatocellular carcinoma via suppressing Notch1 signaling. J Ethnopharmacol. 208:165–173. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang F, Zhang CM, Li S, Wang KK, Guo BB, Fu Y, Liu LY, Zhang Y, Jiang HY and Wu CJ: Low dosage of arsenic trioxide inhibits vasculogenic mimicry in hepatoblastoma without cell apoptosis. Mol Med Rep. 17:1573–1582. 2018.PubMed/NCBI | |
Li S, Zhang Q, Zhou L, Guan Y, Chen S, Zhang Y and Han X: Inhibitory effects of compound DMBT on hypoxia-induced vasculogenic mimicry in human breast cancer. Biomed Pharmacother. 96:982–992. 2017. View Article : Google Scholar : PubMed/NCBI | |
Angara K, Rashid MH, Shankar A, Ara R, Iskander A, Borin TF, Jain M, Achyut BR and Arbab AS: Vascular mimicry in glioblastoma following anti-angiogenic and anti-20-HETE therapies. Histol Histopathol. 32:917–928. 2017.PubMed/NCBI | |
Xue W, Du XS, Wu H, Liu H, Xie T, Tong HP, Chen X, Guo Y and Zhang WG: Aberrant glioblastoma neovascularization patterns and their correlation with DCE-MRI-derived parameters following temozolomide and bevacizumab treatment. Sci Rep. 7:138942017. View Article : Google Scholar : PubMed/NCBI | |
Zang M, Hu L, Zhang B, Zhu Z, Li J, Zhu Z, Yan M and Liu B: Luteolin suppresses angiogenesis and vasculogenic mimicry formation through inhibiting Notchl-VEGF signaling in gastric cancer. Biochem Biophys Res Commun. 490:913–919. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu W, Lv C, Zhang B, Zhou Q and Cao Z: MicroRNA-27b functions as a new inhibitor of ovarian cancer-mediated vasculogenic mimicry through suppression of VE-cadherin expression. RNA. 23:1019–1027. 2017. View Article : Google Scholar : PubMed/NCBI | |
Orimo A, Gupta P, Sgroi D, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey V, Richardson A and Weinberg R: Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 121:335–348. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sugimoto H, Mundel T, Kieran M and Kalluri R: Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther. 5:1640–1646. 2006. View Article : Google Scholar : PubMed/NCBI | |
Johansson A, Ansell A, Jerhammar F, Lindh M, Grénman R, Munck-Wikland E, Östman A and Roberg K: Cancer-associated fibroblasts induce matrix metalloproteinase-mediated cetuximab resistance in head and neck squamous cell carcinoma cells. Mol Cancer Res. 10:1158–1168. 2012. View Article : Google Scholar : PubMed/NCBI | |
Affolter A, Schmidtmann I, Mann WJ and Brieger J: Cancer-associated fibroblasts do not respond to combined irradiation and kinase inhibitor treatment. Oncol Rep. 29:785–790. 2013. View Article : Google Scholar : PubMed/NCBI | |
Al-Ansari MM, Hendrayani SF, Tulbah A, Al-Tweigeri T, Shehata AL and Aboussekhra A: p16INK4A represses breast stromal fibroblasts migration/invasion and their VEGF-A-dependent promotion of angiogenesis through Akt inhibition. Neoplasia. 14:1269–1277. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gao Q, Wang XY, Qiu SJ, Zhou J, Shi YH, Zhang BH and Fan J: Tumor stroma reaction-related gene signature predicts clinical outcome in human hepatocellular carcinoma. Cancer Sci. 102:1522–1531. 2011. View Article : Google Scholar : PubMed/NCBI | |
Herrera M, Herrera A, Domínguez G, Silva J, García V, García J, Gómez I, Soldevilla B, Muñoz C, Provencio M, et al: Cancer-associated fibroblast and M2 macrophage markers together predict outcome in colorectal cancer patients. Cancer Sci. 104:437–444. 2013. View Article : Google Scholar : PubMed/NCBI | |
Madar S, Goldstein I and Rotter V: ‘Cancer associated fibroblasts’ -more than meets the eye. Trends Mol Med. 19:447–453. 2013. View Article : Google Scholar : PubMed/NCBI | |
Gonda TA, Varro A, Wang TC and Tycko B: Molecular biology of cancer-associated fibroblasts: Can these cells be targeted in anti-cancer therapy? Semin Cell Dev Biol. 21:2–10. 2010. View Article : Google Scholar : PubMed/NCBI | |
Mertens J, Fingas CD, Christensen JD, Smoot RL, Bronk SF, Werneburg NW, Gustafson MP, Dietz AB, Roberts LR, Sirica AE and Gores GJ: Therapeutic effects of deleting cancer-associated fibroblasts in cholangiocarcinoma. Cancer Res. 73:897–907. 2013. View Article : Google Scholar : PubMed/NCBI | |
Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, et al: Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 324:1457–1461. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK and Seed B: Tumor induction of VEGF promoter activity in stromal cells. Cell. 94:715–725. 1998. View Article : Google Scholar : PubMed/NCBI | |
Okabe H, Beppu T, Hayashi H, Ishiko T, Masuda T, Otao R, Horlad H, Jono H, Ueda M, Shinriki S, et al: Hepatic stellate cells accelerate the malignant behavior of cholangiocarcinoma cells. Ann Surg Oncol. 18:1175–1184. 2011. View Article : Google Scholar : PubMed/NCBI | |
Guo X, Oshima H, Kitmura T, Taketo M and Oshima M: Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem. 283:19864–19871. 2008. View Article : Google Scholar : PubMed/NCBI | |
Vartanian AA, Burova OS, Stepanova EV, Baryshnikov AY and Lichinitser MR: Melanoma vasculogenic mimicry is strongly related to reactive oxygen species level. Melanoma Res. 17:370–379. 2007. View Article : Google Scholar : PubMed/NCBI | |
Liu Z, Sun B, Qi L, Li H, Gao J and Leng X: Zinc finger E-box binding homeobox 1 promotes vasculogenic mimicry in colorectal cancer through induction of epithelial-to-mesenchymal transition. Cancer Sci. 103:813–820. 2012. View Article : Google Scholar : PubMed/NCBI | |
Carmeliet P and Jain R: Molecular mechanisms and clinical applications of angiogenesis. Nature. 473:298–307. 2011. View Article : Google Scholar : PubMed/NCBI | |
Noma K, Smalley KS, Lioni M, Naomoto Y, Tanaka N, El-Deiry W, King AJ, Nakagawa H and Herlyn M: The essential role of fibroblasts in esophageal squamous cell carcinoma-induced angiogenesis. Gastroenterology. 134:1981–1993. 2008. View Article : Google Scholar : PubMed/NCBI | |
Suzuki H, Onimaru M, Yonemitsu Y, Maehara Y, Nakamura S and Sueishi K: Podoplanin in cancer cells is experimentally able to attenuate prolymphangiogenic and lymphogenous metastatic potentials of lung squamoid cancer cells. Mol Cancer. 9:2872010. View Article : Google Scholar : PubMed/NCBI | |
Schoppmann SF, Jesch B, Riegler MF, Maroske F, Schwameis K, Jomrich G and Birner P: Podoplanin expressing cancer associated fibroblasts are associated with unfavourable prognosis in adenocarcinoma of the esophagus. Clin Exp Metastasis. 30:441–446. 2013. View Article : Google Scholar : PubMed/NCBI | |
Pula B, Jethon A, Piotrowska A, Gomulkiewicz A, Owczarek T, Calik J, Wojnar A, Witkiewicz W, Rys J, Ugorski M, et al: Podoplanin expression by cancer-associated fibroblasts predicts poor outcome in invasive ductal breast carcinoma. Histopathology. 59:1249–1260. 2011. View Article : Google Scholar : PubMed/NCBI | |
Pula B, Wojnar A, Witkiewicz W, Dziegiel P and Podhorska-Okolow M: Podoplanin expression in cancer-associated fibroblasts correlates with VEGF-C expression in cancer cells of invasive ductal breast carcinoma. Neoplasma. 60:516–524. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tang D, Yuan Z, Xue X, Lu Z, Zhang Y, Wang H, Chen M, An Y, Wei J, Zhu Y, et al: High expression of Galectin-1 in pancreatic stellate cells plays a role in the development and maintenance of an immunosuppressive microenvironment in pancreatic cancer. Int J Cancer. 130:2337–2348. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wu MH, Hong TM, Cheng HW, Pan SH, Liang YR, Hong HC, Chiang WF, Wong TY, Shieh DB, Shiau AL, et al: Galectin-1-mediated tumor invasion and metastasis, up-regulated matrix metalloproteinase expression, and reorganized actin cytoskeletons. Mol Cancer Res. 7:311–318. 2009. View Article : Google Scholar : PubMed/NCBI | |
Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijn S, Verhofstad N, Nakabeppu Y, Baum L, Bakkers J, et al: Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA. 103:15975–15980. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bektas S, Bahadir B, Ucan BH and Ozdamar SO: CD24 and galectin-1 expressions in gastric adenocarcinoma and clinicopathologic significance. Pathol Oncol Res. 16:569–577. 2010. View Article : Google Scholar : PubMed/NCBI | |
Tang D, Gao J, Wang S, Ye N, Chong Y, Huang Y, Wang J, Li B, Yin W and Wang D: Cancer-associated fibroblasts promote angiogenesis in gastric cancer through galectin-1 expression. Tumour Biol. 37:1889–1899. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hooper AT, Shmelkov SV, Gupta S, Milde T, Bambino K, Gillen K, Goetz M, Chavala S, Baljevic M, Murphy A, et al: Angiomodulin is a specific marker of vasculature and regulates vascular endothelial growth factor-A-dependent neoangiogenesis. Circ Res. 105:201–208. 2009. View Article : Google Scholar : PubMed/NCBI | |
Komiya E, Furuya M, Watanabe N, Miyagi Y, Higashi S and Miyazaki K: Elevated expression of angiomodulin (AGM/IGFBP-rP1) in tumor stroma and its roles in fibroblast activation. Cancer Sci. 103:691–699. 2012. View Article : Google Scholar : PubMed/NCBI | |
Komiya E, Sato H, Watanabe N, Ise M, Higashi S, Miyagi Y and Miyazaki K: Angiomodulin, a marker of cancer vasculature, is upregulated by vascular endothelial growth factor and increases vascular permeability as a ligand of integrin αvβ3. Cancer Med. 3:537–549. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ren J, Guo H, Wu H, Tian T, Dong D, Zhang Y, Sui Y, Zhang Y, Zhao D, Wang S, et al: GPER in CAFs regulates hypoxia-driven breast cancer invasion in a CTGF-dependent manner. Oncol Rep. 33:1929–1937. 2015. View Article : Google Scholar : PubMed/NCBI | |
De Francesco E, Lappano R, Santolla M, Marsico S, Caruso A and Maggiolini M: HIF-1α/GPER signaling mediates the expression of VEGF induced by hypoxia in breast cancer associated fibroblasts (CAFs). Breast Cancer Res. 15:R642013. View Article : Google Scholar : PubMed/NCBI | |
Hayashi Y, Tsujii M, Kodama T, Akasaka T, Kondo J, Hikita H, Inoue T, Tsujii Y, Maekawa A, Yoshii S, et al: p53 functional deficiency in human colon cancer cells promotes fibroblast-mediated angiogenesis and tumor growth. Carcinogenesis. 37:972–984. 2016. View Article : Google Scholar : PubMed/NCBI | |
Jo M, Nishikawa T, Nakajima T, Okada Y, Yamaguchi K, Mitsuyoshi H, Yasui K, Minami M, Iwai M, Kagawa K, et al: Oxidative stress is closely associated with tumor angiogenesis of hepatocellular carcinoma. J Gastroenterol. 46:809–821. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang S, Ma N, Kawanishi S, Hiraku Y, Oikawa S, Xie Y, Zhang Z, Huang G and Murata M: Relationships of alpha-SMA-positive fibroblasts and SDF-1-positive tumor cells with neoangiogenesis in nasopharyngeal carcinoma. Biomed Res Int 2014. 5073532014. | |
Orimo A and Weinberg R: Stromal fibroblasts in cancer: A novel tumor-promoting cell type. Cell Cycle. 5:1597–1601. 2006. View Article : Google Scholar : PubMed/NCBI | |
Matsuo Y, Ochi N, Sawai H, Yasuda A, Takahashi H, Funahashi H, Takeyama H, Tong Z and Guha S: CXCL8/IL-8 and CXCL12/SDF-1 alpha co-operatively promote invasiveness and angiogenesis in pancreatic cancer. Int J Cancer. 124:853–861. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yang J, Lu Y, Lin YY, Zheng ZY, Fang JH, He S and Zhuang SM: Vascular mimicry formation is promoted by paracrine TGF-β and SDF1 of cancer-associated fibroblasts and inhibited by miR-101 in hepatocellular carcinoma. Cancer Lett. 383:18–27. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fang D, Sun L, Lin S, Zhou L, Su N, Yuan S and Yu B: Vinorelbine inhibits angiogenesis and 95D migration via reducing hypoxic fibroblast stromal cell-derived factor 1 secretion. Exp Biol Med (Maywood). 237:1045–1055. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhou B, Zhuang XM, Wang YY, Lin ZY, Zhang DM, Fan S, Li JS and Chen WL: Tumor necrosis factor α induces myofibroblast differentiation in human tongue cancer and promotes invasiveness and angiogenesis via secretion of stromal cell-derived factor-1. Oral Oncol. 51:1095–1102. 2015. View Article : Google Scholar : PubMed/NCBI | |
Katoh H, Hosono K, Ito Y, Suzuki T, Ogawa Y, Kubo H, Kamata H, Mishima T, Tamaki H, Sakagami H, et al: COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am J Pathol. 176:1469–1483. 2010. View Article : Google Scholar : PubMed/NCBI | |
Massagué J: TGFβ signalling in context. Nat Rev Mol Cell Biol. 13:616–630. 2012. View Article : Google Scholar : PubMed/NCBI | |
Meulmeester E and Ten Dijke P: The dynamic roles of TGF-β in cancer. J Pathol. 223:205–218. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sánchez-Elsner T, Botella L, Velasco B, Corbí A, Attisano L and Bernabéu C: Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression. J Biol Chem. 276:38527–38535. 2001. View Article : Google Scholar : PubMed/NCBI | |
Schnegg C, Yang MH, Ghosh SK and Hsu MY: Induction of vasculogenic mimicry overrides VEGF-A silencing and enriches stem-like cancer cells in melanoma. Cancer Res. 75:1682–1690. 2015. View Article : Google Scholar : PubMed/NCBI | |
Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, Margaryan NV and Hendrix MJ: Tumor cell vasculogenic mimicry: From controversy to therapeutic promise. Am J Pathol. 181:1115–1125. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kirschmann DA, Seftor EA, Hardy KM, Seftor RE and Hendrix MJ: Molecular pathways: Vasculogenic mimicry in tumor cells: Diagnostic and therapeutic implications. Clin Cancer Res. 18:2726–2732. 2012. View Article : Google Scholar : PubMed/NCBI | |
Barcellos-de-Souza P, Comito G, Pons-Segura C, Taddei ML, Gori V, Becherucci V, Bambi F, Margheri F, Laurenzana A, Del Rosso M, et al: Mesenchymal stem cells are recruited and activated into carcinoma-associated fibroblasts by prostate cancer microenvironment-derived TGF-β1. Stem Cells. 34:2536–2547. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gonzalez-Zubeldia I, Dotor J, Redrado M, Bleau A, Manrique I, de Aberasturi A, Villalba M and Calvo A: Co-migration of colon cancer cells and CAFs induced by TGFβ1 enhances liver metastasis. Cell Tissue Res. 359:829–839. 2015. View Article : Google Scholar : PubMed/NCBI | |
Xu Z, Wang S, Wu M, Zeng W, Wang X and Dong Z: TGFβ1 and HGF protein secretion by esophageal squamous epithelial cells and stromal fibroblasts in oesophageal carcinogenesis. Oncol Lett. 6:401–406. 2013. View Article : Google Scholar : PubMed/NCBI | |
Saito H, Tsujitani S, Oka S, Kondo A, Ikeguchi M, Maeta M and Kaibara N: The expression of transforming growth factor-beta1 is significantly correlated with the expression of vascular endothelial growth factor and poor prognosis of patients with advanced gastric carcinoma. Cancer. 86:1455–1462. 1999. View Article : Google Scholar : PubMed/NCBI | |
Xu LN, Xu BN, Cai J, Yang JB and Lin N: Tumor-associated fibroblast-conditioned medium promotes tumor cell proliferation and angiogenesis. Genet Mol Res. 12:5863–5871. 2013. View Article : Google Scholar : PubMed/NCBI | |
Guido C, Whitaker-Menezes D, Capparelli C, Balliet R, Lin Z, Pestell R, Howell A, Aquila S, Andò S, Martinez-Outschoorn U, et al: Metabolic reprogramming of cancer-associated fibroblasts by TGF-β drives tumor growth: Connecting TGF-β signaling with ‘Warburg-like’ cancer metabolism and L-lactate production. Cell Cycle. 11:3019–3035. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ding S, Merkulova-Rainon T, Han ZC and Tobelem G: HGF receptor up-regulation contributes to the angiogenic phenotype of human endothelial cells and promotes angiogenesis in vitro. Blood. 101:4816–4822. 2003. View Article : Google Scholar : PubMed/NCBI | |
Sulpice E, Ding S, Muscatelli-Groux B, Bergé M, Han Z, Plouet J, Tobelem G and Merkulova-Rainon T: Cross-talk between the VEGF-A and HGF signalling pathways in endothelial cells. Biol Cell. 101:525–539. 2009. View Article : Google Scholar : PubMed/NCBI | |
Spina A, De Pasquale V, Cerulo G, Cocchiaro P, Della Morte R, Avallone L and Pavone L: HGF/c-MET axis in tumor microenvironment and metastasis formation. Biomedicines. 3:71–88. 2015. View Article : Google Scholar : PubMed/NCBI | |
Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, Klein-Szanto AJ, Diehl A, Herlyn M, Han M, Nakagawa H and Rustgi AK: Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc Natl Acad Sci USA. 107:11026–11031. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wu X, Chen X, Zhou Q, Li P, Yu B, Li J, Qu Y, Yan J, Yu Y, Yan M, et al: Hepatocyte growth factor activates tumor stromal fibroblasts to promote tumorigenesis in gastric cancer. Cancer Lett. 335:128–135. 2013. View Article : Google Scholar : PubMed/NCBI | |
Jia C, Wang T, Liu W, Fu B, Hua X, Wang G, Li T, Li X, Wu X, Tai Y, et al: Cancer-associated fibroblasts from hepatocellular carcinoma promote malignant cell proliferation by HGF secretion. PLoS One. 8:e632432013. View Article : Google Scholar : PubMed/NCBI | |
Tyan SW, Kuo WH, Huang CK, Pan CC, Shew JY, Chang KJ, Lee EY and Lee WH: Breast cancer cells induce cancer-associated fibroblasts to secrete hepatocyte growth factor to enhance breast tumorigenesis. PLoS One. 6:e153132011. View Article : Google Scholar : PubMed/NCBI | |
Ren Y, Cao B, Law S, Xie Y, Lee PY, Cheung L, Chen Y, Huang X, Chan HM, Zhao P, et al: Hepatocyte growth factor promotes cancer cell migration and angiogenic factors expression: A prognostic marker of human esophageal squamous cell carcinomas. Clin Cancer Res. 11:6190–6197. 2005. View Article : Google Scholar : PubMed/NCBI | |
Oshima Y, Yajima S, Yamazaki K, Matsushita K, Tagawa M and Shimada H: Angiogenesis-related factors are molecular targets for diagnosis and treatment of patients with esophageal carcinoma. Ann Thorac Cardiovasc Surg. 16:389–393. 2010.PubMed/NCBI | |
Bergsten E, Uutela M, Li X, Pietras K, Ostman A, Heldin C, Alitalo K and Eriksson U: PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat Cell Biol. 3:512–516. 2001. View Article : Google Scholar : PubMed/NCBI | |
Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana C and Fidler I: Targeting the expression of platelet-derived growth factor receptor by reactive stroma inhibits growth and metastasis of human colon carcinoma. Am J Pathol. 169:2054–2065. 2006. View Article : Google Scholar : PubMed/NCBI | |
Crawford Y, Kasman I, Yu L, Zhong C, Wu X, Modrusan Z, Kaminker J and Ferrara N: PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell. 15:21–34. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ostman A: PDGF receptors-mediators of autocrine tumor growth and regulators of tumor vasculature and stroma. Cytokine Growth Factor Rev. 15:275–286. 2004. View Article : Google Scholar : PubMed/NCBI | |
Pietras K, Rubin K, Sjöblom T, Buchdunger E, Sjöquist M, Heldin C and Ostman A: Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy. Cancer Res. 62:5476–5484. 2002.PubMed/NCBI | |
Pietras K, Gustafson AM, Sjoblom T, Buchdunger E, McSheehy P, Sjoquist M, Wartmann M, Reed R, Heldin CH, Rubin K, et al: PDGF receptor inhibition in tumor stroma, with STI571 or PDGF B-chain aptamers, enhances the effects of chemotherapy in experimental solid tumors by increasing tumor drug uptake. Eur J Cancer. 38:S91. 2002. View Article : Google Scholar | |
Pietras K, Pahler J, Bergers G and Hanahan D: Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med. 5:e192008. View Article : Google Scholar : PubMed/NCBI | |
Zi F, He J, He D, Li Y, Yang L and Cai Z: Fibroblast activation protein α in tumor microenvironment: Recent progression and implications (review). Mol Med Rep. 11:3203–3211. 2015. View Article : Google Scholar : PubMed/NCBI | |
Santos AM, Jung J, Aziz N, Kissil JL and Puré E: Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest. 119:3613–3625. 2009. View Article : Google Scholar : PubMed/NCBI | |
Patsouras D, Papaxoinis K, Kostakis A, Safioleas MC, Lazaris AC and Nicolopoulou-Stamati P: Fibroblast activation protein and its prognostic significance in correlation with vascular endothelial growth factor in pancreatic adenocarcinoma. Mol Med Rep. 11:4585–4590. 2015. View Article : Google Scholar : PubMed/NCBI | |
Koczorowska MM, Tholen S, Bucher F, Lutz L, Kizhakkedathu JN, De Wever O, Wellner U, Biniossek ML, Stahl A, Lassmann S and Schilling O: Fibroblast activation protein-α, a stromal cell surface protease, shapes key features of cancer associated fibroblasts through proteome and degradome alterations. Mol Oncol. 10:40–58. 2016. View Article : Google Scholar : PubMed/NCBI | |
LeBeau AM, Brennen WN, Aggarwal S and Denmeade SR: Targeting the cancer stroma with a fibroblast activation protein-activated promelittin protoxin. Mol Cancer Ther. 8:1378–1386. 2009. View Article : Google Scholar : PubMed/NCBI | |
Liao D, Luo Y, Markowitz D, Xiang R and Reisfeld RA: Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One. 4:e79652009. View Article : Google Scholar : PubMed/NCBI | |
Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D and Brown PO: Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA. 99:12877–12882. 2002. View Article : Google Scholar : PubMed/NCBI | |
Simian M, Hirai Y, Navre M, Werb Z, Lochter A and Bissell MJ: The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development. 128:3117–3131. 2001.PubMed/NCBI | |
Vosseler S, Lederle W, Airola K, Obermueller E, Fusenig NE and Mueller MM: Distinct progression-associated expression of tumor and stromal MMPs in HaCaT skin SCCs correlates with onset of invasion. Int J Cancer. 125:2296–2306. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lederle W, Hartenstein B, Meides A, Kunzelmann H, Werb Z, Angel P and Mueller M: MMP13 as a stromal mediator in controlling persistent angiogenesis in skin carcinoma. Carcinogenesis. 31:1175–1184. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zigrino P, Kuhn I, Bäuerle T, Zamek J, Fox JW, Neumann S, Licht A, Schorpp-Kistner M, Angel P and Mauch C: Stromal expression of MMP-13 is required for melanoma invasion and metastasis. J Invest Dermatol. 129:2686–2693. 2009. View Article : Google Scholar : PubMed/NCBI | |
Benyahia Z, Dussault N, Cayol M, Sigaud R, Berenguer-Daizé C, Delfino C, Tounsi A, Garcia S, Martin P, Mabrouk K and Ouafik L: Stromal fibroblasts present in breast carcinomas promote tumor growth and angiogenesis through adrenomedullin secretion. Oncotarget. 8:15744–15762. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kayamori K, Katsube K, Sakamoto K, Ohyama Y, Hirai H, Yukimori A, Ohata Y, Akashi T, Saitoh M, Harada K, et al: NOTCH3 is induced in cancer-associated fibroblasts and promotes angiogenesis in oral squamous cell carcinoma. PLoS One. 11:e01541122016. View Article : Google Scholar : PubMed/NCBI | |
Tasiopoulou V, Magouliotis D, Solenov EI, Vavougios G, Molyvdas PA, Gourgoulianis KI, Hatzoglou C and Zarogiannis SG: Transcriptional over-expression of chloride intracellular channels 3 and 4 in malignant pleural mesothelioma. Comput Biol Chem. 59:Pt A. 111–116. 2015. View Article : Google Scholar : PubMed/NCBI | |
Macpherson IR, Rainero E, Mitchell LE, van den Berghe PV, Speirs C, Dozynkiewicz MA, Chaudhary S, Kalna G, Edwards J, Timpson P and Norman JC: CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J Cell Sci. 127:3893–3901. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dozynkiewicz MA, Jamieson NB, Macpherson I, Grindlay J, van den Berghe P, von Thun A, Morton JP, Gourley C, Timpson P, Nixon C, et al: Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell. 22:131–145. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hernandez-Fernaud JR, Ruengeler E, Casazza A, Neilson LJ, Pulleine E, Santi A, Ismail S, Lilla S, Dhayade S, MacPherson IR, et al: Secreted CLIC3 drives cancer progression through its glutathione-dependent oxidoreductase activity. Nat Commun. 8:142062017. View Article : Google Scholar : PubMed/NCBI | |
Calvo F, Ranftl R, Hooper S, Farrugia AJ, Moeendarbary E, Bruckbauer A, Batista F, Charras G and Sahai E: Cdc42EP3/BORG2 and septin network enables mechano-transduction and the emergence of cancer-associated fibroblasts. Cell Rep. 13:2699–2714. 2015. View Article : Google Scholar : PubMed/NCBI | |
Paggetti J, Haderk F, Seiffert M, Janji B, Distler U, Ammerlaan W, Kim YJ, Adam J, Lichter P, Solary E, et al: Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood. 126:1106–1117. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bai YP, Shang K, Chen H, Ding F, Wang Z, Liang C, Xu Y, Sun MH and Li YY: FGF-1/-3/FGFR4 signaling in cancer-associated fibroblasts promotes tumor progression in colon cancer through Erk and MMP-7. Cancer Sci. 106:1278–1287. 2015. View Article : Google Scholar : PubMed/NCBI | |
Núñez-Gómez E, Pericacho M, Ollauri-Ibáñez C, Bernabéu C and López-Novoa J: The role of endoglin in post-ischemic revascularization. Angiogenesis. 20:1–24. 2017. View Article : Google Scholar : PubMed/NCBI | |
Romero D, O'Neill C, Terzic A, Contois L, Young K, Conley BA, Bergan RC, Brooks PC and Vary CP: Endoglin regulates cancer-stromal cell interactions in prostate tumors. Cancer Res. 71:3482–3493. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mendel DB, Laird AD, Smolich BD, Blake RA, Liang C, Hannah AL, Shaheen RM, Ellis LM, Weitman S, Shawver LK and Cherrington JM: Development of SU5416, a selective small molecule inhibitor of VEGF receptor tyrosine kinase activity, as an anti-angiogenesis agent. Anticancer Drug Des. 15:29–41. 2000.PubMed/NCBI | |
Wang LL, Li JJ, Zheng ZB, Liu HY, Du GJ and Li S: Antitumor activities of a novel indolin-2-ketone compound, Z24: More potent inhibition on bFGF-induced angiogenesis and bcl-2 over-expressing cancer cells. Eur J Pharmacol. 502:1–10. 2004. View Article : Google Scholar : PubMed/NCBI | |
Brennen WN, Isaacs JT and Denmeade SR: Rationale behind targeting fibroblast activation protein-expressing carcinoma-associated fibroblasts as a novel chemotherapeutic strategy. Mol Cancer Ther. 11:257–266. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yamamoto Y, Matsui J, Matsushima T, Obaishi H, Miyazaki K, Nakamura K, Tohyama O, Semba T, Yamaguchi A, Hoshi SS, et al: Lenvatinib, an angiogenesis inhibitor targeting VEGFR/FGFR, shows broad antitumor activity in human tumor xenograft models associated with microvessel density and pericyte coverage. Vasc Cell. 6:182014. View Article : Google Scholar : PubMed/NCBI | |
Taguchi A, Kawana K, Tomio K, Yamashita A, Isobe Y, Nagasaka K, Koga K, Inoue T, Nishida H, Kojima S, et al: Matrix metalloproteinase (MMP)-9 in cancer-associated fibroblasts (CAFs) is suppressed by omega-3 polyunsaturated fatty acids in vitro and in vivo. PLoS One. 9:e896052014. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Shen Y, Li S, Lv M, Zhang X and Yang J, Wang F and Yang J: Importance of the interaction between immune cells and tumor vasculature mediated by thalidomide in cancer treatment (Review). Int J Mol Med. 38:1021–1029. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hu-Lowe DD, Chen E, Zhang L, Watson KD, Mancuso P, Lappin P, Wickman G, Chen JH, Wang J, Jiang X, et al: Targeting activin receptor-like kinase 1 inhibits angiogenesis and tumorigenesis through a mechanism of action complementary to anti-VEGF therapies. Cancer Res. 71:1362–1373. 2011. View Article : Google Scholar : PubMed/NCBI | |
Huijbers EJ, van Beijnum JR, Thijssen VL, Sabrkhany S, Nowak-Sliwinska P and Griffioen A: Role of the tumor stroma in resistance to anti-angiogenic therapy. Drug Resist Updat. 25:26–37. 2016. View Article : Google Scholar : PubMed/NCBI | |
di Tomaso E, London N, Fuja D, Logie J, Tyrrell JA, Kamoun W, Munn LL and Jain RK: PDGF-C induces maturation of blood vessels in a model of glioblastoma and attenuates the response to anti-VEGF treatment. PLoS One. 4:e51232009. View Article : Google Scholar : PubMed/NCBI | |
Hainsworth JD, Spigel DR, Sosman JA, Burris HA III, Farley C, Cucullu H, Yost K, Hart LL, Sylvester L, Waterhouse DM and Greco FA: Treatment of advanced renal cell carcinoma with the combination bevacizumab/erlotinib/imatinib: A phase I/II trial. Clin Genitourin Cancer. 5:427–432. 2007. View Article : Google Scholar : PubMed/NCBI | |
Li M, Li M, Yin T, Shi H, Wen Y, Zhang B, Chen M, Xu G, Ren K and Wei Y: Targeting of cancer-associated fibroblasts enhances the efficacy of cancer chemotherapy by regulating the tumor microenvironment. Mol Med Rep. 13:2476–2484. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kinugasa Y, Matsui T and Takakura N: CD44 expressed on cancer-associated fibroblasts is a functional molecule supporting the stemness and drug resistance of malignant cancer cells in the tumor microenvironment. Stem Cells. 32:145–156. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang W, Ma JL, Jia WD and Xu GL: Periostin: A putative mediator involved in tumour resistance to anti-angiogenic therapy? Cell Biol Int. 35:1085–1088. 2011. View Article : Google Scholar : PubMed/NCBI |