Revisiting tumor angiogenesis: vessel co-option, vessel remodeling, and cancer cell-derived vasculature formation
Tóm tắt
Tumor growth and metastasis depend on the establishment of tumor vasculature to provide oxygen, nutrients, and other essential factors. The well-known vascular endothelial growth factor (VEGF) signaling is crucial for
sprouting angiogenesis as well as recruitment of circulating progenitor endothelial cells to tumor vasculature, which has become therapeutic targets in clinical practice. However, the survival benefits gained from targeting VEGF signaling have been very limited, with the inevitable development of treatment resistance. In this article, we discuss the most recent findings and understanding on how solid tumors evade VEGF-targeted therapy, with a special focus on vessel co-option, vessel remodeling, and tumor cell-derived vasculature establishment. Vessel co-option may occur in tumors independently of sprouting angiogenesis, and sprouting angiogenesis is not always required for tumor growth. The differences between vessel-like structure and tubule-like structure formed by tumor cells are also introduced. The exploration of the underlying mechanisms of these alternative angiogenic approaches would not only widen our knowledge of tumor angiogenesis but also provide novel therapeutic targets for better controlling cancer growth and metastasis.
Tài liệu tham khảo
McDonald DM, Baluk P. Imaging of angiogenesis in inflamed airways and tumors: newly formed blood vessels are not alike and may be wildly abnormal: Parker B. Francis lecture. Chest. 2005;128(6 Suppl):602S–8S. doi:10.1378/chest.128.6_suppl.602S-a.
Qin L, Bromberg-White JL, Qian CN. Opportunities and challenges in tumor angiogenesis research: back and forth between bench and bed. Adv Cancer Res. 2012;113:191–239. doi:10.1016/B978-0-12-394280-7.00006-3.
Qian CN, Huang D, Wondergem B, Teh BT. Complexity of tumor vasculature in clear cell renal cell carcinoma. Cancer. 2009;115(10 Suppl):2282–9. doi:10.1002/cncr.24238.
Yao X, Qian CN, Zhang ZF, Tan MH, Kort EJ, Yang XJ, et al. Two distinct types of blood vessels in clear cell renal cell carcinoma have contrasting prognostic implications. Clin Cancer Res. 2007;13(1):161–9. doi:10.1158/1078-0432.CCR-06-0774.
Al-Husein B, Abdalla M, Trepte M, Deremer DL, Somanath PR. Antiangiogenic therapy for cancer: an update. Pharmacotherapy. 2012;32(12):1095–111. doi:10.1002/phar.1147.
Stacker SA, Achen MG. The VEGF signaling pathway in cancer: the road ahead. Chin J Cancer. 2013;32(6):297–302. doi:10.5732/cjc.012.10319.
Ciliberto D, Staropoli N, Caglioti F, Gualtieri S, Fiorillo L, Chiellino S, et al. A systemic review and meta-analysis of randomized trials on the role of targeted therapy in the management of advanced gastric cancer: evidence does not translate? Cancer Biol Ther. 2015. doi:10.1080/15384047.2015.1056415.
Colagrande S, Regini F, Taliani GG, Nardi C, Inghilesi AL. Advanced hepatocellular carcinoma and sorafenib: diagnosis, indications, clinical and radiological follow-up. World J Hepatol. 2015;7(8):1041–53. doi:10.4254/wjh.v7.i8.1041.
Della Pepa C, Tonini G, Pisano C, Di Napoli M, Cecere SC, Tambaro R, et al. Ovarian cancer standard of care: are there real alternatives? Chin J Cancer. 2015;34(1):17–27. doi:10.5732/cjc.014.10274.
Gadducci A, Lanfredini N, Sergiampietri C. Antiangiogenic agents in gynecological cancer: state of art and perspectives of clinical research. Crit Rev Oncol Hematol. 2015. doi:10.1016/j.critrevonc.2015.05.009.
Chen YS, Chen ZP. Vasculogenic mimicry: a novel target for glioma therapy. Chin J Cancer. 2014;33(2):74–9. doi:10.5732/cjc.012.10292.
Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med. 2001;7(9):987–9. doi:10.1038/nm0901-987.
Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307(5706):58–62. doi:10.1126/science.1104819.
von Baumgarten L, Brucker D, Tirniceru A, Kienast Y, Grau S, Burgold S, et al. Bevacizumab has differential and dose-dependent effects on glioma blood vessels and tumor cells. Clin Cancer Res. 2011;17(19):6192–205. doi:10.1158/1078-0432.CCR-10-1868.
Qian CN. Hijacking the vasculature in ccRCC—co-option, remodelling and angiogenesis. Nat Rev Urol. 2013;10(5):300–4. doi:10.1038/nrurol.2013.26.
Motiejunaite R, Aranda J, Kazlauskas A. Pericytes prevent regression of endothelial cell tubes by accelerating metabolism of lysophosphatidic acid. Microvasc Res. 2014;93:62–71. doi:10.1016/j.mvr.2014.03.003.
Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, et al. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol. 2012;23(5):868–83. doi:10.1681/ASN.2011080851.
Franco M, Roswall P, Cortez E, Hanahan D, Pietras K. Pericytes promote endothelial cell survival through induction of autocrine VEGF-A signaling and Bcl-w expression. Blood. 2011;118(10):2906–17. doi:10.1182/blood-2011-01-331694.
Weisshardt P, Trarbach T, Durig J, Paul A, Reis H, Tilki D, et al. Tumor vessel stabilization and remodeling by anti-angiogenic therapy with bevacizumab. Histochem Cell Biol. 2012;137(3):391–401. doi:10.1007/s00418-011-0898-8.
Arjaans M, Oude Munnink TH, Oosting SF, Terwisscha van Scheltinga AG, Gietema JA, Garbacik ET, et al. Bevacizumab-induced normalization of blood vessels in tumors hampers antibody uptake. Cancer Res. 2013;73(11):3347–55. doi:10.1158/0008-5472.CAN-12-3518.
Franco M, Paez-Ribes M, Cortez E, Casanovas O, Pietras K. Use of a mouse model of pancreatic neuroendocrine tumors to find pericyte biomarkers of resistance to anti-angiogenic therapy. Horm Metab Res. 2011;43(12):884–9. doi:10.1055/s-0031-1284381.
Kim ES, Serur A, Huang J, Manley CA, McCrudden KW, Frischer JS, et al. Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc Natl Acad Sci USA. 2002;99(17):11399–404. doi:10.1073/pnas.172398399.
Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8(8):592–603. doi:10.1038/nrc2442.
Farnsworth RH, Lackmann M, Achen MG, Stacker SA. Vascular remodeling in cancer. Oncogene. 2014;33(27):3496–505. doi:10.1038/onc.2013.304.
Qian CN, Berghuis B, Tsarfaty G, Bruch M, Kort EJ, Ditlev J, et al. Preparing the “soil”: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 2006;66(21):10365–76. doi:10.1158/0008-5472.CAN-06-2977.
Qian CN, Resau JH, Teh BT. Prospects for vasculature reorganization in sentinel lymph nodes. Cell Cycle. 2007;6(5):514–7.
Sakai Y, Kobayashi M. Lymphocyte ‘homing’ and chronic inflammation. Pathol Int. 2015;65(7):344–54. doi:10.1111/pin.12294.
Jeong HS, Jones D, Liao S, Wattson DA, Cui CH, Duda DG, et al. Investigation of the lack of angiogenesis in the formation of lymph node metastases. J Natl Cancer Inst. 2015. doi:10.1093/jnci/djv155.
Lee SY, Chao-Nan Q, Seng OA, Peiyi C, Bernice WH, Swe MS, et al. Changes in specialized blood vessels in lymph nodes and their role in cancer metastasis. J Transl Med. 2012;10:206. doi:10.1186/1479-5876-10-206.
Farnsworth RH, Karnezis T, Shayan R, Matsumoto M, Nowell CJ, Achen MG, et al. A role for bone morphogenetic protein-4 in lymph node vascular remodeling and primary tumor growth. Cancer Res. 2011;71(20):6547–57. doi:10.1158/0008-5472.CAN-11-0200.
Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol. 2000;156(2):361–81. doi:10.1016/S0002-9440(10)64739-6.
Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, Margaryan NV, et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol. 2012;181(4):1115–25. doi:10.1016/j.ajpath.2012.07.013.
Qiao L, Liang N, Zhang J, Xie J, Liu F, Xu D, et al. Advanced research on vasculogenic mimicry in cancer. J Cell Mol Med. 2015;19(2):315–26. doi:10.1111/jcmm.12496.
Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010;468(7325):824–8. doi:10.1038/nature09557.
Soda Y, Myskiw C, Rommel A, Verma IM. Mechanisms of neovascularization and resistance to anti-angiogenic therapies in glioblastoma multiforme. J Mol Med (Berl). 2013;91(4):439–48. doi:10.1007/s00109-013-1019-z.
Xu Y, Li Q, Li XY, Yang QY, Xu WW, Liu GL. Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. J Exp Clin Cancer Res. 2012;31:16. doi:10.1186/1756-9966-31-16.
Hu CD, Choo R, Huang J. Neuroendocrine differentiation in prostate cancer: a mechanism of radioresistance and treatment failure. Front Oncol. 2015;5:90. doi:10.3389/fonc.2015.00090.
Jang YY, Sharkis SJ. Stem cell plasticity: a rare cell, not a rare event. Stem Cell Rev. 2005;1(1):45–51. doi:10.1385/SCR:1:1:045.
Zane M, Scavo E, Catalano V, Bonanno M, Todaro M, De Maria R, et al. Normal vs cancer thyroid stem cells: the road to transformation. Oncogene. 2015. doi:10.1038/onc.2015.138.
Tsarfaty I, Resau JH, Rulong S, Keydar I, Faletto DL, Vande Woude GF. The met proto-oncogene receptor and lumen formation. Science. 1992;257(5074):1258–61.
Cocola C, Sanzone S, Astigiano S, Pelucchi P, Piscitelli E, Vilardo L, et al. A rat mammary gland cancer cell with stem cell properties of self-renewal and multi-lineage differentiation. Cytotechnology. 2008;58(1):25–32. doi:10.1007/s10616-008-9173-9.
Ruffini F, Graziani G, Levati L, Tentori L, D’Atri S, Lacal PM. Cilengitide downmodulates invasiveness and vasculogenic mimicry of neuropilin 1 expressing melanoma cells through the inhibition of alphavbeta5 integrin. Int J Cancer. 2015;136(6):E545–58. doi:10.1002/ijc.29252.
Yang Z, Sun B, Li Y, Zhao X, Zhao X, Gu Q, et al. ZEB2 promotes vasculogenic mimicry by TGF-beta1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma. Exp Mol Pathol. 2015;98(3):352–9. doi:10.1016/j.yexmp.2015.03.030.
Cao Z, Shang B, Zhang G, Miele L, Sarkar FH, Wang Z, et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta. 2013;1836(2):273–86. doi:10.1016/j.bbcan.2013.08.001.
Lirdprapamongkol K, Chiablaem K, Sila-Asna M, Surarit R, Bunyaratvej A, Svasti J. Exploring stemness gene expression and vasculogenic mimicry capacity in well- and poorly-differentiated hepatocellular carcinoma cell lines. Biochem Biophys Res Commun. 2012;422(3):429–35. doi:10.1016/j.bbrc.2012.05.009.
Liu YR, Sun B, Zhao XL, Gu Q, Liu ZY, Dong XY, et al. Basal caspase-3 activity promotes migration, invasion, and vasculogenic mimicry formation of melanoma cells. Melanoma Res. 2013;23(4):243–53. doi:10.1097/CMR.0b013e3283625498.
Wan HY, Li QQ, Zhang Y, Tian W, Li YN, Liu M, et al. MiR-124 represses vasculogenic mimicry and cell motility by targeting amotL1 in cervical cancer cells. Cancer Lett. 2014;355(1):148–58. doi:10.1016/j.canlet.2014.09.005.
Wagenblast E, Soto M, Gutierrez-Angel S, Hartl CA, Gable AL, Maceli AR, et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature. 2015;520(7547):358–62. doi:10.1038/nature14403.
Maddipati R, Stanger BZ. Pancreatic cancer metastases harbor evidence of polyclonality. Cancer Discov. 2015. doi:10.1158/2159-8290.CD-15-0120.
Li XJ, Ong CK, Cao Y, Xiang YQ, Shao JY, Ooi A, et al. Serglycin is a theranostic target in nasopharyngeal carcinoma that promotes metastasis. Cancer Res. 2011;71(8):3162–72. doi:10.1158/0008-5472.CAN-10-3557.
Li XJ, Peng LX, Shao JY, Lu WH, Zhang JX, Chen S, et al. As an independent unfavorable prognostic factor, IL-8 promotes metastasis of nasopharyngeal carcinoma through induction of epithelial-mesenchymal transition and activation of AKT signaling. Carcinogenesis. 2012;33(7):1302–9. doi:10.1093/carcin/bgs181.
Li XJ, Qian CN. Serglycin in human cancers. Chin J Cancer. 2011;30(9):585–9. doi:10.5732/cjc.011.10314.