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Molecular Cancer
Published in: Molecular Cancer 1/2015

Open Access 01-12-2015 | Review

The twisted survivin connection to angiogenesis

Authors: C. Sanhueza, S. Wehinger, J. Castillo Bennett, M. Valenzuela, G. I. Owen, A. F. G. Quest

Published in: Molecular Cancer | Issue 1/2015

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Abstract

Survivin, a member of the inhibitor of apoptosis family of proteins (IAPs) that controls cell division, apoptosis, metastasis and angiogenesis, is overexpressed in essentially all human cancers. As a consequence, the gene/protein is considered an attractive target for cancer treatment. Here, we discuss recent findings related to the regulation of survivin expression and its role in angiogenesis, particularly in the context of hypoxia. We propose a novel role for survivin in cancer, whereby expression of the protein in tumor cells promotes VEGF synthesis, secretion and angiogenesis. Mechanistically, we propose the existence of a positive feed-back loop involving PI3-kinase/Akt activation and enhanced β-Catenin-TCF/LEF-dependent VEGF expression followed by secretion. Finally, we elaborate on the possibility that this mechanism operating in cancer cells may contribute to enhanced tumor vascularization by vasculogenic mimicry together with conventional angiogenesis.
Literature
1.
2.
Lladser A, Sanhueza C, Kiessling R, Quest AF. Is survivin the potential Achilles’ heel of cancer? Adv Cancer Res. 2011;111:1–37.PubMedCrossRef
3.
Fernandez JG, Rodriguez DA, Valenzuela M, Calderon C, Urzua U, Munroe D, et al. Survivin expression promotes VEGF-induced tumor angiogenesis via PI3K/Akt enhanced beta-catenin/Tcf-Lef dependent transcription. Mol Cancer. 2014;13:209.PubMedCentralPubMedCrossRef
4.
Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer. 2008;8:61–70.PubMedCrossRef
5.
6.
Chen P, Zhu J, Liu DY, Li HY, Xu N, Hou M. Over-expression of survivin and VEGF in small-cell lung cancer may predict the poorer prognosis. Med Oncol. 2014;31:775.PubMedCrossRef
7.
Sun YW, Xuan Q, Shu QA, Wu SS, Chen H, Xiao J, et al. Correlation of tumor relapse and elevated expression of survivin and vascular endothelial growth factor in superficial bladder transitional cell carcinoma. Genet Mol Res. 2013;12:1045–53.PubMedCrossRef
8.
Zhang HY, Meng X, Du ZX, Fang CQ, Liu GL, Wang HQ, et al. Significance of survivin, caspase-3, and VEGF expression in thyroid carcinoma. Clin Exp Med. 2009;9:207–13.PubMedCrossRef
9.
Li YH, Hu CF, Shao Q, Huang MY, Hou JH, Xie D, et al. Elevated expressions of survivin and VEGF protein are strong independent predictors of survival in advanced nasopharyngeal carcinoma. J Transl Med. 2008;6:1.PubMedCentralPubMedCrossRef
10.
Carreau A, El Hafny-Rahbi B, Matejuk A, Grillon C, Kieda C. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med. 2011;15:1239–53.PubMedCentralPubMedCrossRef
11.
Carrera S, Senra J, Acosta MI, Althubiti M, Hammond EM, de Verdier PJ, et al. The role of the HIF-1alpha transcription factor in increased cell division at physiological oxygen tensions. PLoS One. 2014;9:e97938.PubMedCentralPubMedCrossRef
12.
13.
Movsas B, Chapman JD, Hanlon AL, Horwitz EM, Pinover WH, Greenberg RE, et al. Hypoxia in human prostate carcinoma: an Eppendorf PO2 study. Am J Clin Oncol. 2001;24:458–61.PubMedCrossRef
14.
Koong AC, Mehta VK, Le QT, Fisher GA, Terris DJ, Brown JM, et al. Pancreatic tumors show high levels of hypoxia. Int J Radiat Oncol Biol Phys. 2000;48:919–22.PubMedCrossRef
15.
Becker A, Hansgen G, Bloching M, Weigel C, Lautenschlager C, Dunst J. Oxygenation of squamous cell carcinoma of the head and neck: comparison of primary tumors, neck node metastases, and normal tissue. Int J Radiat Oncol Biol Phys. 1998;42:35–41.PubMedCrossRef
16.
Vaupel P, Schlenger K, Knoop C, Hockel M. Oxygenation of human tumors: evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements. Cancer Res. 1991;51:3316–22.PubMed
17.
Lawrentschuk N, Poon AM, Foo SS, Putra LG, Murone C, Davis ID, et al. Assessing regional hypoxia in human renal tumours using 18 F-fluoromisonidazole positron emission tomography. BJU Int. 2005;96:540–6.PubMedCrossRef
18.
Vaupel P, Hockel M, Mayer A. Detection and characterization of tumor hypoxia using pO2 histography. Antioxid Redox Signal. 2007;9:1221–35.PubMedCrossRef
19.
Denko NC, Fontana LA, Hudson KM, Sutphin PD, Raychaudhuri S, Altman R, et al. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene. 2003;22:5907–14.PubMedCrossRef
20.
Vaupel P, Harrison L. Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist. 2004;9 Suppl 5:4–9.PubMedCrossRef
21.
Vaupel P. Hypoxia and aggressive tumor phenotype: implications for therapy and prognosis. Oncologist. 2008;13 Suppl 3:21–6.PubMedCrossRef
22.
Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer. 2012;12:9–22.
23.
24.
Pries AR, Hopfner M, le Noble F, Dewhirst MW, Secomb TW. The shunt problem: control of functional shunting in normal and tumour vasculature. Nat Rev Cancer. 2010;10:587–93.PubMedCentralPubMedCrossRef
25.
Yasui H, Matsumoto S, Devasahayam N, Munasinghe JP, Choudhuri R, Saito K, et al. Low-field magnetic resonance imaging to visualize chronic and cycling hypoxia in tumor-bearing mice. Cancer Res. 2010;70:6427–36.PubMedCentralPubMedCrossRef
26.
Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer. 2004;4:437–47.PubMedCrossRef
27.
28.
29.
Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A. 1995;92:5510–4.PubMedCentralPubMedCrossRef
30.
Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A. 1997;94:4273–8.PubMedCentralPubMedCrossRef
31.
Makino Y, Kanopka A, Wilson WJ, Tanaka H, Poellinger L. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J Biol Chem. 2002;277:32405–8.PubMedCrossRef
32.
Wiesener MS, Jurgensen JS, Rosenberger C, Scholze CK, Horstrup JH, Warnecke C, et al. Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 2003;17:271–3.PubMed
33.
34.
Tanaka A, Jin Y, Lee SJ, Zhang M, Kim HP, Stolz DB, et al. Hyperoxia-induced LC3B interacts with the Fas apoptotic pathway in epithelial cell death. Am J Respir Cell Mol Biol. 2012;46:507–14.PubMedCentralPubMedCrossRef
35.
Huang LE, Gu J, Schau M, Bunn HF. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A. 1998;95:7987–92.PubMedCentralPubMedCrossRef
36.
Sutter CH, Laughner E, Semenza GL. Hypoxia-inducible factor 1alpha protein expression is controlled by oxygen-regulated ubiquitination that is disrupted by deletions and missense mutations. Proc Natl Acad Sci U S A. 2000;97:4748–53.PubMedCentralPubMedCrossRef
37.
Fandrey J, Gorr TA, Gassmann M. Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res. 2006;71:642–51.PubMedCrossRef
38.
Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130–8.PubMedCrossRef
39.
Schroedl C, McClintock DS, Budinger GR, Chandel NS. Hypoxic but not anoxic stabilization of HIF-1alpha requires mitochondrial reactive oxygen species. Am J Physiol Lung Cell Mol Physiol. 2002;283:L922–31.PubMedCrossRef
40.
Paul SA, Simons JW, Mabjeesh NJ. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol. 2004;200:20–30.PubMedCrossRef
41.
Klimova T, Chandel NS. Mitochondrial complex III regulates hypoxic activation of HIF. Cell Death Differ. 2008;15:660–6.PubMedCrossRef
42.
Pawlus MR, Hu CJ. Enhanceosomes as integrators of hypoxia inducible factor (HIF) and other transcription factors in the hypoxic transcriptional response. Cell Signal. 2013;25:1895–903.PubMedCentralPubMedCrossRef
43.
Pawlus MR, Wang L, Ware K, Hu CJ. Upstream stimulatory factor 2 and hypoxia-inducible factor 2alpha (HIF2alpha) cooperatively activate HIF2 target genes during hypoxia. Mol Cell Biol. 2012;32:4595–610.PubMedCentralPubMedCrossRef
44.
45.
46.
47.
Koh MY, Lemos Jr R, Liu X, Powis G. The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res. 2011;71:4015–27.PubMedCentralPubMedCrossRef
48.
49.
Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell. 2007;11:335–47.PubMedCentralPubMedCrossRef
50.
51.
Hielscher A, Gerecht S. Hypoxia and free radicals: role in tumor progression and the use of engineering-based platforms to address these relationships. Free Radic Biol Med. 2015;79:281–91.PubMedCrossRef
52.
Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998;95:11715–20.PubMedCentralPubMedCrossRef
53.
Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005;1:401–8.PubMedCrossRef
54.
Bell EL, Klimova TA, Eisenbart J, Schumacker PT, Chandel NS. Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia. Mol Cell Biol. 2007;27:5737–45.PubMedCentralPubMedCrossRef
55.
Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol. 2008;28:718–31.PubMedCentralPubMedCrossRef
56.
57.
Kaelin Jr WG, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30:393–402.PubMedCrossRef
58.
Lluis JM, Buricchi F, Chiarugi P, Morales A, Fernandez-Checa JC. Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-{kappa}B via c-SRC and oxidant-dependent cell death. Cancer Res. 2007;67:7368–77.PubMedCrossRef
59.
Pan Y, Mansfield KD, Bertozzi CC, Rudenko V, Chan DA, Giaccia AJ, et al. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol Cell Biol. 2007;27:912–25.PubMedCentralPubMedCrossRef
60.
Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell. 2005;7:77–85.PubMedCrossRef
61.
Pollard PJ, Briere JJ, Alam NA, Barwell J, Barclay E, Wortham NC, et al. Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet. 2005;14:2231–9.PubMedCrossRef
62.
Catalano V, Turdo A, Di Franco S, Dieli F, Todaro M, Stassi G. Tumor and its microenvironment: a synergistic interplay. Semin Cancer Biol. 2013;23:522–32.PubMedCrossRef
63.
Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science. 2008;320:661–4.PubMedCrossRef
64.
Calvani M, Comito G, Giannoni E, Chiarugi P. Time-dependent stabilization of hypoxia inducible factor-1alpha by different intracellular sources of reactive oxygen species. PLoS One. 2012;7:e38388.PubMedCentralPubMedCrossRef
65.
Lluis JM, Llacuna L, von Montfort C, Barcena C, Enrich C, Morales A, et al. GD3 synthase overexpression sensitizes hepatocarcinoma cells to hypoxia and reduces tumor growth by suppressing the cSrc/NF-kappaB survival pathway. PLoS One. 2009;4(e8059).
66.
Delle Monache S, Sanita P, Calgani A, Schenone S, Botta L, Angelucci A. Src inhibition potentiates antitumoral effect of paclitaxel by blocking tumor-induced angiogenesis. Exp Cell Res. 2014;328:20–31.PubMedCrossRef
67.
Bouis D, Kusumanto Y, Meijer C, Mulder NH, Hospers GA. A review on pro- and anti-angiogenic factors as targets of clinical intervention. Pharmacol Res. 2006;53:89–103.PubMedCrossRef
68.
69.
Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S, Waltenberger J, et al. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem. 2002;277:3101–8.PubMedCrossRef
70.
Xia C, Meng Q, Liu LZ, Rojanasakul Y, Wang XR, Jiang BH. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 2007;67:10823–30.PubMedCrossRef
71.
auf dem Keller U, Kumin A, Braun S, Werner S. Reactive oxygen species and their detoxification in healing skin wounds. J Investig Dermatol Symp Proc. 2006;11:106–11.PubMedCrossRef
72.
Yasuda M, Ohzeki Y, Shimizu S, Naito S, Ohtsuru A, Yamamoto T, et al. Stimulation of in vitro angiogenesis by hydrogen peroxide and the relation with ETS-1 in endothelial cells. Life Sci. 1999;64:249–58.PubMedCrossRef
73.
Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991;51:794–8.PubMed
74.
Yamagishi S, Amano S, Inagaki Y, Okamoto T, Takeuchi M, Inoue H. Pigment epithelium-derived factor inhibits leptin-induced angiogenesis by suppressing vascular endothelial growth factor gene expression through anti-oxidative properties. Microvasc Res. 2003;65:186–90.PubMedCrossRef
75.
Al-Shabrawey M, Bartoli M, El-Remessy AB, Platt DH, Matragoon S, Behzadian MA, et al. Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy. Am J Pathol. 2005;167:599–607.PubMedCentralPubMedCrossRef
76.
Koch AE, Cho M, Burrows JC, Polverini PJ, Leibovich SJ. Inhibition of production of monocyte/macrophage-derived angiogenic activity by oxygen free-radical scavengers. Cell Biol Int Rep. 1992;16:415–25.PubMedCrossRef
77.
Cai T, Fassina G, Morini M, Aluigi MG, Masiello L, Fontanini G, et al. N-acetylcysteine inhibits endothelial cell invasion and angiogenesis. Lab Invest. 1999;79:1151–9.PubMed
78.
Wheeler MD, Smutney OM, Samulski RJ. Secretion of extracellular superoxide dismutase from muscle transduced with recombinant adenovirus inhibits the growth of B16 melanomas in mice. Mol Cancer Res. 2003;1:871–81.PubMed
79.
Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation. 2005;111:2347–55.PubMedCrossRef
80.
Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, et al. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A. 2002;99:715–20.PubMedCentralPubMedCrossRef
81.
Wang Y, Zang QS, Liu Z, Wu Q, Maass D, Dulan G, et al. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. Am J Physiol Cell Physiol. 2011;301:C695–704.PubMedCentralPubMedCrossRef
82.
West XZ, Malinin NL, Merkulova AA, Tischenko M, Kerr BA, Borden EC, et al. Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature. 2010;467:972–6.PubMedCentralPubMedCrossRef
83.
Mutoh A, Ueda S. Peroxidized unsaturated fatty acids stimulate Toll-like receptor 4 signaling in endothelial cells. Life Sci. 2013;92:984–92.PubMedCrossRef
84.
85.
Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23:1011–27.PubMedCrossRef
86.
Chen YQ, Zhao CL, Li W. Effect of hypoxia-inducible factor-1alpha on transcription of survivin in non-small cell lung cancer. J Exp Clin Cancer Res. 2009;28:29.PubMedCentralPubMedCrossRef
87.
Peng XH, Karna P, Cao Z, Jiang BH, Zhou M, Yang L. Cross-talk between epidermal growth factor receptor and hypoxia-inducible factor-1alpha signal pathways increases resistance to apoptosis by up-regulating survivin gene expression. J Biol Chem. 2006;281:25903–14.PubMedCentralPubMedCrossRef
88.
Yang L, Cao Z, Li F, Post DE, Van Meir EG, Zhong H, et al. Tumor-specific gene expression using the survivin promoter is further increased by hypoxia. Gene Ther. 2004;11:1215–23.PubMedCentralPubMedCrossRef
89.
Valenzuela M, Perez-Perez G, Corvalan AH, Carrasco G, Urra H, Bravo D, et al. Helicobacter pylori-induced loss of the inhibitor-of-apoptosis protein survivin is linked to gastritis and death of human gastric cells. J Infect Dis. 2010;202:1021–30.PubMedCrossRef
90.
91.
92.
Hu Y, Kirito K, Yoshida K, Mitsumori T, Nakajima K, Nozaki Y, et al. Inhibition of hypoxia-inducible factor-1 function enhances the sensitivity of multiple myeloma cells to melphalan. Mol Cancer Ther. 2009;8:2329–38.PubMedCrossRef
93.
Li W, Chen YQ, Shen YB, Shu HM, Wang XJ, Zhao CL, et al. HIF-1alpha knockdown by miRNA decreases survivin expression and inhibits A549 cell growth in vitro and in vivo. Int J Mol Med. 2013;32:271–80.PubMedCentralPubMed
94.
Wu XY, Fu ZX, Wang XH. Effect of hypoxia-inducible factor 1-alpha on Survivin in colorectal cancer. Mol Med Rep. 2010;3:409–15.PubMed
95.
Sun XP, Dong X, Lin L, Jiang X, Wei Z, Zhai B, et al. Up-regulation of survivin by AKT and hypoxia-inducible factor 1alpha contributes to cisplatin resistance in gastric cancer. FEBS J. 2014;281:115–28.PubMedCrossRef
96.
Jutooru I, Chadalapaka G, Abdelrahim M, Basha MR, Samudio I, Konopleva M, et al. Methyl 2-cyano-3,12-dioxooleana-1,9-dien-28-oate decreases specificity protein transcription factors and inhibits pancreatic tumor growth: role of microRNA-27a. Mol Pharmacol. 2010;78:226–36.PubMedCentralPubMedCrossRef
97.
Pathi SS, Jutooru I, Chadalapaka G, Sreevalsan S, Anand S, Thatcher GR, et al. GT-094, a NO-NSAID, inhibits colon cancer cell growth by activation of a reactive oxygen species-microRNA-27a: ZBTB10-specificity protein pathway. Mol Cancer Res. 2011;9:195–202.PubMedCentralPubMedCrossRef
98.
Pathi SS, Lei P, Sreevalsan S, Chadalapaka G, Jutooru I, Safe S. Pharmacologic doses of ascorbic acid repress specificity protein (Sp) transcription factors and Sp-regulated genes in colon cancer cells. Nutr Cancer. 2011;63:1133–42.PubMedCentralPubMedCrossRef
99.
Bhowmick R, Girotti AW. Cytoprotective signaling associated with nitric oxide upregulation in tumor cells subjected to photodynamic therapy-like oxidative stress. Free Radic Biol Med. 2013;57:39–48.PubMedCentralPubMedCrossRef
100.
Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, et al. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell. 2002;9:1031–44.PubMedCrossRef
101.
Lampiasi N, Azzolina A, Umezawa K, Montalto G, McCubrey JA, Cervello M. The novel NF-kappaB inhibitor DHMEQ synergizes with celecoxib to exert antitumor effects on human liver cancer cells by a ROS-dependent mechanism. Cancer Lett. 2012;322:35–44.PubMedCrossRef
102.
Yang X, Li X, An L, Bai B, Chen J. Silibinin induced the apoptosis of Hep-2 cells via oxidative stress and down-regulating survivin expression. Eur Arch Otorhinolaryngol. 2013;270:2289–97.PubMedCrossRef
103.
Zheng WX, Wang F, Cao XL, Pan HY, Liu XY, Hu XM, et al. Baicalin protects PC-12 cells from oxidative stress induced by hydrogen peroxide via anti-apoptotic effects. Brain Inj. 2014;28:227–34.PubMedCrossRef
104.
Zhu W, Cromie MM, Cai Q, Lv T, Singh K, Gao W. Curcumin and vitamin E protect against adverse effects of benzo[a]pyrene in lung epithelial cells. PLoS One. 2014;9:e92992.PubMedCentralPubMedCrossRef
105.
Ahamed M, Akhtar MJ, Raja M, Ahmad I, Siddiqui MK, AlSalhi MS, et al. ZnO nanorod-induced apoptosis in human alveolar adenocarcinoma cells via p53, survivin and bax/bcl-2 pathways: role of oxidative stress. Nanomedicine. 2011;7:904–13.PubMedCrossRef
106.
Valenzuela M, Bravo D, Canales J, Sanhueza C, Diaz N, Almarza O, et al. Helicobacter pylori-induced loss of survivin and gastric cell viability is attributable to secreted bacterial gamma-glutamyl transpeptidase activity. J Infect Dis. 2013;208:1131–41.PubMedCrossRef
107.
Xu GC, Zhang P, Leng F, Pan L, Li ZY, Yu DD, et al. Inhibition of lymphatic metastases by a survivin dominant-negative mutant. Oncol Res. 2012;20:579–87.PubMedCrossRef
108.
Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst. 1990;82:4–6.PubMedCrossRef
109.
Taeger J, Moser C, Hellerbrand C, Mycielska ME, Glockzin G, Schlitt HJ, et al. Targeting FGFR/PDGFR/VEGFR impairs tumor growth, angiogenesis, and metastasis by effects on tumor cells, endothelial cells, and pericytes in pancreatic cancer. Mol Cancer Ther. 2011;10:2157–67.PubMedCrossRef
110.
Welti J, Loges S, Dimmeler S, Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest. 2013;123:3190–200.PubMedCentralPubMedCrossRef
111.
Samuel S, Fan F, Dang LH, Xia L, Gaur P, Ellis LM. Intracrine vascular endothelial growth factor signaling in survival and chemoresistance of human colorectal cancer cells. Oncogene. 2011;30:1205–12.PubMedCentralPubMedCrossRef
112.
Goteri G, Lucarini G, Pieramici T, Filosa A, Pugnaloni A, Montik N, et al. Endothelial cell survivin is involved in the growth of ovarian endometriotic cysts. Anticancer Res. 2005;25:4313–8.PubMed
113.
Gupta K, Kshirsagar S, Li W, Gui L, Ramakrishnan S, Gupta P, et al. VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res. 1999;247:495–504.PubMedCrossRef
114.
Thirunavukkarasu M, Han Z, Zhan L, Penumathsa SV, Menon VP, Maulik N. Adeno-sh-beta-catenin abolishes ischemic preconditioning-mediated cardioprotection by downregulation of its target genes VEGF, Bcl-2, and survivin in ischemic rat myocardium. Antioxid Redox Signal. 2008;10:1475–84.PubMedCentralPubMedCrossRef
115.
Kaga S, Zhan L, Altaf E, Maulik N. Glycogen synthase kinase-3beta/beta-catenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. J Mol Cell Cardiol. 2006;40:138–47.PubMedCrossRef
116.
Nogueira-Ferreira R, Vitorino R, Ferreira-Pinto MJ, Ferreira R, Henriques-Coelho T. Exploring the role of post-translational modifications on protein-protein interactions with survivin. Arch Biochem Biophys. 2013;538:64–70.PubMedCrossRef
117.
Boidot R, Vegran F, Lizard-Nacol S. Transcriptional regulation of the survivin gene. Mol Biol Rep. 2014;41:233–40.PubMedCrossRef
118.
Aoki Y, Feldman GM, Tosato G. Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood. 2003;101:1535–42.PubMedCrossRef
119.
Asanuma H, Torigoe T, Kamiguchi K, Hirohashi Y, Ohmura T, Hirata K, et al. Survivin expression is regulated by coexpression of human epidermal growth factor receptor 2 and epidermal growth factor receptor via phosphatidylinositol 3-kinase/AKT signaling pathway in breast cancer cells. Cancer Res. 2005;65:11018–25.PubMedCrossRef
120.
Ohashi H, Takagi H, Oh H, Suzuma K, Suzuma I, Miyamoto N, et al. Phosphatidylinositol 3-kinase/Akt regulates angiotensin II-induced inhibition of apoptosis in microvascular endothelial cells by governing survivin expression and suppression of caspase-3 activity. Circ Res. 2004;94:785–93.PubMedCrossRef
121.
Kim YS, Jin HO, Seo SK, Woo SH, Choe TB, An S, et al. Sorafenib induces apoptotic cell death in human non-small cell lung cancer cells by down-regulating mammalian target of rapamycin (mTOR)-dependent survivin expression. Biochem Pharmacol. 2011;82:216–26.PubMedCrossRef
122.
Fukuda S, Pelus LM. Activated H-Ras regulates hematopoietic cell survival by modulating Survivin. Biochem Biophys Res Commun. 2004;323:636–44.PubMedCrossRef
123.
Liu C, Liang B, Wang Q, Wu J, Zou MH. Activation of AMP-activated protein kinase alpha1 alleviates endothelial cell apoptosis by increasing the expression of anti-apoptotic proteins Bcl-2 and survivin. J Biol Chem. 2010;285:15346–55.PubMedCentralPubMedCrossRef
124.
Kumar P, Coltas IK, Kumar B, Chepeha DB, Bradford CR, Polverini PJ. Bcl-2 protects endothelial cells against gamma-radiation via a Raf-MEK-ERK-survivin signaling pathway that is independent of cytochrome c release. Cancer Res. 2007;67:1193–202.PubMedCrossRef
125.
Kanwar JR, Kamalapuram SK, Kanwar RK. Targeting survivin in cancer: the cell-signalling perspective. Drug Discov Today. 2011;16:485–94.PubMedCrossRef
126.
Hoffman WH, Biade S, Zilfou JT, Chen J, Murphy M. Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem. 2002;277:3247–57.PubMedCrossRef
127.
Fossey SL, Liao AT, McCleese JK, Bear MD, Lin J, Li PK, et al. Characterization of STAT3 activation and expression in canine and human osteosarcoma. BMC Cancer. 2009;9:81.PubMedCentralPubMedCrossRef
128.
Weerasinghe P, Garcia GE, Zhu Q, Yuan P, Feng L, Mao L, et al. Inhibition of Stat3 activation and tumor growth suppression of non-small cell lung cancer by G-quartet oligonucleotides. Int J Oncol. 2007;31:129–36.PubMed
129.
Kim KW, Mutter RW, Cao C, Albert JM, Shinohara ET, Sekhar KR, et al. Inhibition of signal transducer and activator of transcription 3 activity results in down-regulation of Survivin following irradiation. Mol Cancer Ther. 2006;5:2659–65.PubMedCrossRef
130.
Wu ZX, Song TB, Li DM, Zhang XT, Wu XL. Overexpression of PTEN suppresses growth and induces apoptosis by inhibiting the expression of survivin in bladder cancer cells. Tumour Biol. 2007;28:9–15.PubMedCrossRef
131.
Li W, Wang H, Kuang CY, Zhu JK, Yu Y, Qin ZX, et al. An essential role for the Id1/PI3K/Akt/NFkB/survivin signalling pathway in promoting the proliferation of endothelial progenitor cells in vitro. Mol Cell Biochem. 2012;363:135–45.PubMedCentralPubMedCrossRef
132.
Takada Y, Khuri FR, Aggarwal BB. Protein farnesyltransferase inhibitor (SCH 66336) abolishes NF-kappaB activation induced by various carcinogens and inflammatory stimuli leading to suppression of NF-kappaB-regulated gene expression and up-regulation of apoptosis. J Biol Chem. 2004;279:26287–99.PubMedCrossRef
133.
Zhang G, Zhu H, Wang Y, Yang S, Liu M, Zhang W, et al. Kruppel-like factor 4 represses transcription of the survivin gene in esophageal cancer cell lines. Biol Chem. 2009;390:463–9.PubMedCrossRef
134.
Zhu N, Gu L, Findley HW, Chen C, Dong JT, Yang L, et al. KLF5 Interacts with p53 in regulating survivin expression in acute lymphoblastic leukemia. J Biol Chem. 2006;281:14711–8.PubMedCrossRef
135.
Wagner M, Schmelz K, Dorken B, Tamm I. Transcriptional regulation of human survivin by early growth response (Egr)-1 transcription factor. Int J Cancer. 2008;122:1278–87.PubMedCrossRef
136.
Huang CL, Liu D, Nakano J, Yokomise H, Ueno M, Kadota K, et al. E2F1 overexpression correlates with thymidylate synthase and survivin gene expressions and tumor proliferation in non small-cell lung cancer. Clin Cancer Res. 2007;13:6938–46.PubMedCrossRef
137.
Xu R, Zhang P, Huang J, Ge S, Lu J, Qian G. Sp1 and Sp3 regulate basal transcription of the survivin gene. Biochem Biophys Res Commun. 2007;356:286–92.PubMedCrossRef
138.
Zhong Q, Zhou Y, Ye W, Cai T, Zhang X, Deng DY. Hypoxia-inducible factor 1-alpha-AA-modified bone marrow stem cells protect PC12 cells from hypoxia-induced apoptosis, partially through VEGF/PI3K/Akt/FoxO1 pathway. Stem Cells Dev. 2012;21:2703–17.PubMedCentralPubMedCrossRef
139.
Ma H, Nguyen C, Lee KS, Kahn M. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene. 2005;24:3619–31.PubMedCrossRef
140.
Hossain MM, Banik NL, Ray SK. Survivin knockdown increased anti-cancer effects of (-)-epigallocatechin-3-gallate in human malignant neuroblastoma SK-N-BE2 and SH-SY5Y cells. Exp Cell Res. 2012;318:1597–610.PubMedCentralPubMedCrossRef
141.
Shen J, Sun H, Meng Q, Yin Q, Zhang Z, Yu H, et al. Simultaneous inhibition of tumor growth and angiogenesis for resistant hepatocellular carcinoma by co-delivery of sorafenib and survivin small hairpin RNA. Mol Pharm. 2014;11:3342–51.PubMedCrossRef
142.
Ma A, Lin R, Chan PK, Leung JC, Chan LY, Meng A, et al. The role of survivin in angiogenesis during zebrafish embryonic development. BMC Dev Biol. 2007;7:50.PubMedCentralPubMedCrossRef
143.
Delvaeye M, De Vriese A, Zwerts F, Betz I, Moons M, Autiero M, et al. Role of the 2 zebrafish survivin genes in vasculo-angiogenesis, neurogenesis, cardiogenesis and hematopoiesis. BMC Dev Biol. 2009;9:25.PubMedCentralPubMedCrossRef
144.
Wang P, Zhen H, Zhang J, Zhang W, Zhang R, Cheng X, et al. Survivin promotes glioma angiogenesis through vascular endothelial growth factor and basic fibroblast growth factor in vitro and in vivo. Mol Carcinog. 2012;51:586–95.PubMedCrossRef
145.
Shu MG, Guo XT, Zhen HN, Han Y, Chen FL, Li LW, et al. Enhancing skin flap survival by a cell-permeable wild-type survivin. Med Hypotheses. 2007;69:888–91.PubMedCrossRef
146.
Furuya M, Tsuji N, Kobayashi D, Watanabe N. Interaction between survivin and aurora-B kinase plays an important role in survivin-mediated up-regulation of human telomerase reverse transcriptase expression. Int J Oncol. 2009;34:1061–8.PubMed
147.
Wang Z, Fukuda S, Pelus LM. Survivin regulates the p53 tumor suppressor gene family. Oncogene. 2004;23:8146–53.PubMedCrossRef
148.
Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg PT. Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell. 2002;13:3064–77.PubMedCentralPubMedCrossRef
149.
Zhu LB, Jiang J, Zhu XP, Wang TF, Chen XY, Luo QF, et al. Knockdown of Aurora-B inhibits osteosarcoma cell invasion and migration via modulating PI3K/Akt/NF-kappaB signaling pathway. Int J Clin Exp Pathol. 2014;7:3984–91.PubMedCentralPubMed
150.
Shan RF, Zhou YF, Peng AF, Jie ZG. Inhibition of Aurora-B suppresses HepG2 cell invasion and migration via the PI3K/Akt/NF-kappaB signaling pathway. Exp Ther Med. 2014;8:1005–9.PubMedCentralPubMed
151.
Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, et al. Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J Biol Chem. 2003;278:31277–85.PubMedCrossRef
152.
Sharma M, Chuang WW, Sun Z. Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3beta inhibition and nuclear beta-catenin accumulation. J Biol Chem. 2002;277:30935–41.PubMedCrossRef
153.
Adluri RS, Thirunavukkarasu M, Zhan L, Akita Y, Samuel SM, Otani H, et al. Thioredoxin 1 enhances neovascularization and reduces ventricular remodeling during chronic myocardial infarction: a study using thioredoxin 1 transgenic mice. J Mol Cell Cardiol. 2011;50:239–47.PubMedCentralPubMedCrossRef
154.
Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, et al. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem. 2007;282:11221–9.PubMedCentralPubMedCrossRef
155.
Bai XM, Jiang H, Ding JX, Peng T, Ma J, Wang YH, et al. Prostaglandin E2 upregulates survivin expression via the EP1 receptor in hepatocellular carcinoma cells. Life Sci. 2010;86:214–23.PubMedCrossRef
156.
Krysan K, Dalwadi H, Sharma S, Pold M, Dubinett S. Cyclooxygenase 2-dependent expression of survivin is critical for apoptosis resistance in non-small cell lung cancer. Cancer Res. 2004;64:6359–62.PubMedCrossRef
157.
Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science. 2005;310:1504–10.PubMedCrossRef
158.
Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155:739–52.PubMedCentralPubMedCrossRef
159.
160.
Kirschmann DA, Seftor EA, Hardy KM, Seftor RE, Hendrix MJ. Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res. 2012;18:2726–32.PubMedCentralPubMedCrossRef
161.
Francescone R, Scully S, Bentley B, Yan W, Taylor SL, Oh D, et al. Glioblastoma-derived tumor cells induce vasculogenic mimicry through Flk-1 protein activation. J Biol Chem. 2012;287:24821–31.PubMedCentralPubMedCrossRef
162.
Yao X, Ping Y, Liu Y, Chen K, Yoshimura T, Liu M, et al. Vascular endothelial growth factor receptor 2 (VEGFR-2) plays a key role in vasculogenic mimicry formation, neovascularization and tumor initiation by Glioma stem-like cells. PLoS One. 2013;8:e57188.PubMedCentralPubMedCrossRef
163.
Dunleavey JM, Xiao L, Thompson J, Kim MM, Shields JM, Shelton SE, et al. Vascular channels formed by subpopulations of PECAM1+ melanoma cells. Nat Commun. 2014;5:5200.PubMedCentralPubMedCrossRef
164.
Gao Y, Zhao XL, Gu Q, Wang JY, Zhang SW, Zhang DF, et al. Correlation of vasculogenic mimicry with clinicopathologic features and prognosis of ovarian carcinoma. Zhonghua Bing Li Xue Za Zhi. 2009;38:585–9.PubMed
165.
Bai XL, Zhang Q, Ye LY, Liang F, Sun X, Chen Y, et al. Myocyte enhancer factor 2C regulation of hepatocellular carcinoma via vascular endothelial growth factor and Wnt/beta-catenin signaling. Oncogene. 2015;34:4089–97.
166.
Clapp C, Martinez de la Escalera G. Aquaporin-1: a novel promoter of tumor angiogenesis. Trends Endocrinol Metab. 2006;17:1–2.PubMedCrossRef
167.
Du J, Sun B, Zhao X, Gu Q, Dong X, Mo J, et al. Hypoxia promotes vasculogenic mimicry formation by inducing epithelial-mesenchymal transition in ovarian carcinoma. Gynecol Oncol. 2014;133:575–83.PubMedCrossRef
168.
Fan YL, Zheng M, Tang YL, Liang XH. A new perspective of vasculogenic mimicry: EMT and cancer stem cells (Review). Oncol Lett. 2013;6:1174–80.PubMedCentralPubMed
169.
Zhang X, Song Q, Wei C, Qu J. LRIG1 inhibits hypoxia-induced vasculogenic mimicry formation via suppression of the EGFR/PI3K/AKT pathway and epithelial-to-mesenchymal transition in human glioma SHG-44 cells. Cell Stress Chaperones. 2015;20:631–41.PubMedPubMedCentralCrossRef
170.
Yang Z, Sun B, Li Y, Zhao X, Gu Q, An J, et al. ZEB2 promotes vasculogenic mimicry by TGF-beta1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma. Exp Mol Pathol. 2015;98:352–9.PubMedCrossRef
171.
Wang L, Lin L, Chen X, Sun L, Liao Y, Huang N, et al. Metastasis-associated in colon cancer-1 promotes vasculogenic mimicry in gastric cancer by upregulating TWIST1/2. Oncotarget. 2015;6:11492–506.PubMedCentralPubMedCrossRef
172.
Wang W, Lin P, Sun B, Zhang S, Cai W, Han C, et al. Epithelial-mesenchymal transition regulated by EphA2 contributes to vasculogenic mimicry formation of head and neck squamous cell carcinoma. Biomed Res Int. 2014;2014:803914.PubMedCentralPubMed
173.
174.
Liao A, Shi R, Jiang Y, Tian S, Li P, Song F, et al. SDF-1/CXCR4 Axis regulates cell cycle progression and epithelial-mesenchymal transition via up-regulation of survivin in glioblastoma. Mol Neurobiol. 2014. doi:10.​1007/​s12035-014-9006-0
175.
Tang NN, Zhu H, Zhang HJ, Zhang WF, Jin HL, Wang L, et al. HIF-1alpha induces VE-cadherin expression and modulates vasculogenic mimicry in esophageal carcinoma cells. World J Gastroenterol. 2014;20:17894–904.PubMedCentralPubMed
176.
Tsuneki M, Madri JA. CD44 regulation of endothelial cell proliferation and apoptosis via modulation of CD31 and VE-cadherin expression. J Biol Chem. 2014;289:5357–70.PubMedCentralPubMedCrossRef
177.
Iurlaro M, Demontis F, Corada M, Zanetta L, Drake C, Gariboldi M, et al. VE-cadherin expression and clustering maintain low levels of survivin in endothelial cells. Am J Pathol. 2004;165:181–9.PubMedCentralPubMedCrossRef
178.
Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med. 1997;3:917–21.PubMedCrossRef
179.
180.
Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, Marchisio PC, et al. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature. 1998;396:580–4.PubMedCrossRef
181.
182.
Zhang LQ, Wang J, Jiang F, Xu L, Liu FY, Yin R. Prognostic value of survivin in patients with non-small cell lung carcinoma: a systematic review with meta-analysis. PLoS One. 2012;7:e34100.PubMedCentralPubMedCrossRef
183.
Liu JL, Gao W, Kang QM, Zhang XJ, Yang SG. Prognostic value of survivin in patients with gastric cancer: a systematic review with meta-analysis. PLoS One. 2013;8:e71930.PubMedCentralPubMedCrossRef
184.
Gasowska-Bodnar A, Bodnar L, Dabek A, Cichowicz M, Jerzak M, Cierniak S, et al. Survivin expression as a prognostic factor in patients with epithelial ovarian cancer or primary peritoneal cancer treated with neoadjuvant chemotherapy. Int J Gynecol Cancer. 2014;24:687–96.PubMedCrossRef
185.
Siamakpour-Reihani S, Owzar K, Jiang C, Turner T, Deng Y, Bean SM, et al. Prognostic significance of differential expression of angiogenic genes in women with high-grade serous ovarian carcinoma. Gynecol Oncol. 2015;139:23–9.PubMedCrossRef
186.
187.
Tamm I, Kornblau SM, Segall H, Krajewski S, Welsh K, Kitada S, et al. Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin Cancer Res. 2000;6:1796–803.PubMed
188.
Fulda S. Inhibitor of Apoptosis (IAP) proteins in hematological malignancies: molecular mechanisms and therapeutic opportunities. Leukemia. 2014;28:1414–22.PubMedCrossRef
189.
Fulda S, Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat Rev Drug Discov. 2012;11:109–24.PubMedCrossRef
190.
Raetz EA, Morrison D, Romanos-Sirakis E, Gaynon P, Sposto R, Bhojwani D, et al. A phase I study of EZN-3042, a novel survivin messenger ribonucleic acid (mRNA) antagonist, administered in combination with chemotherapy in children with relapsed acute lymphoblastic leukemia (ALL): a report from the therapeutic advances in childhood leukemia and lymphoma (TACL) consortium. J Pediatr Hematol Oncol. 2014;36:458–63.PubMedCentralPubMedCrossRef
191.
Kelly RJ, Thomas A, Rajan A, Chun G, Lopez-Chavez A, Szabo E, et al. A phase I/II study of sepantronium bromide (YM155, survivin suppressor) with paclitaxel and carboplatin in patients with advanced non-small-cell lung cancer. Ann Oncol. 2013;24:2601–6.PubMedCentralPubMedCrossRef
192.
Tibes R, McDonagh KT, Lekakis L, Bogenberger JM, Kim S, Frazer N, et al. Phase I study of the novel Cdc2/CDK1 and AKT inhibitor terameprocol in patients with advanced leukemias. Invest New Drugs. 2015;33:389–96.PubMedCrossRef
193.
Berntsen A, Trepiakas R, Wenandy L, Geertsen PF, thor Straten P, Andersen MH, et al. Therapeutic dendritic cell vaccination of patients with metastatic renal cell carcinoma: a clinical phase 1/2 trial. J Immunother. 2008;31:771–80.PubMedCrossRef
194.
Wang D, Zhang B, Gao H, Ding G, Wu Q, Zhang J, et al. Clinical research of genetically modified dendritic cells in combination with cytokine-induced killer cell treatment in advanced renal cancer. BMC Cancer. 2014;14:251.PubMedCentralPubMedCrossRef
195.
Berinstein NL, Karkada M, Oza AM, Odunsi K, Villella JA, Nemunaitis JJ, et al. Survivin-targeted immunotherapy drives robust polyfunctional T cell generation and differentiation in advanced ovarian cancer patients. Oncoimmunology. 2015;4:e1026529.PubMedPubMedCentralCrossRef
196.
Ellebaek E, Engell-Noerregaard L, Iversen TZ, Froesig TM, Munir S, Hadrup SR, et al. Metastatic melanoma patients treated with dendritic cell vaccination, Interleukin-2 and metronomic cyclophosphamide: results from a phase II trial. Cancer Immunol Immunother. 2012;61:1791–804.PubMedCrossRef
Metadata
Title
The twisted survivin connection to angiogenesis
Authors
C. Sanhueza
S. Wehinger
J. Castillo Bennett
M. Valenzuela
G. I. Owen
A. F. G. Quest
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2015
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-015-0467-1

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