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Erschienen in: Tumor Biology 12/2016

13.11.2015 | Original Article

VEGF-activated miR-144 regulates autophagic survival of prostate cancer cells against Cisplatin

verfasst von: Feng Liu, Jihong Wang, Qiang Fu, Xinru Zhang, Ying Wang, Jialin Liu, Jianwen Huang, Xiangguo Lv

Erschienen in: Tumor Biology | Ausgabe 12/2016

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Abstract

Cisplatin is a commonly used chemotherapy drug for prostate cancer (PC). However, some PCs are resistant to cisplatin treatment, while the molecular mechanisms underlying the resistance of PCs to cisplatin are not completely understood. In this study, we found that cisplatin dose-dependently activated Beclin-1 in two PC cell lines, PC3 and LNCap. Autophagy suppression significantly increased the cisplatin-induced cell death of these PC cells in a CCK-8 assay. Moreover, microRNA (miR)-144 levels were significantly downregulated in cisplatin-treated PC cells, in a VEGF-dependent manner. Bioinformatics analysis showed that miR-144 targeted the 3′-UTR of Beclin-1 mRNA to inhibit its translation, which was confirmed by luciferase reporter assay. In PC patients after cisplatin treatment, low miR-144 levels appeared to predict poor outcome of patients’ survival. Together, these data suggest that cisplatin may induce VEGF to suppress miR-144 levels in PC cells, which subsequently upregulates Beclin-1 to increase autophagic cell survival against cisplatin-induced cell death. Upregulation of miR-144 or suppression of cell autophagy may improve the outcome of cisplatin therapy in PC.
Literatur
1.
Zurück zum Zitat Saylor PJ. Prostate cancer: the androgen receptor remains front and centre. Nat Rev Clin Oncol. 2013;10:126–8.CrossRefPubMed Saylor PJ. Prostate cancer: the androgen receptor remains front and centre. Nat Rev Clin Oncol. 2013;10:126–8.CrossRefPubMed
2.
Zurück zum Zitat Alva A, Hussain M. The changing natural history of metastatic prostate cancer. Cancer J. 2013;19:19–24.CrossRefPubMed Alva A, Hussain M. The changing natural history of metastatic prostate cancer. Cancer J. 2013;19:19–24.CrossRefPubMed
3.
Zurück zum Zitat Beltran H, Rubin MA. New strategies in prostate cancer: Translating genomics into the clinic. Clin Cancer Res. 2013;19:517–23.CrossRefPubMed Beltran H, Rubin MA. New strategies in prostate cancer: Translating genomics into the clinic. Clin Cancer Res. 2013;19:517–23.CrossRefPubMed
4.
Zurück zum Zitat Xin L. Cells of origin for cancer: an updated view from prostate cancer. Oncogene. 2013;32:3655–63.CrossRefPubMed Xin L. Cells of origin for cancer: an updated view from prostate cancer. Oncogene. 2013;32:3655–63.CrossRefPubMed
5.
Zurück zum Zitat Huang S, Liao Q, Li L, Xin D. Pttg1 inhibits smad3 in prostate cancer cells to promote their proliferation. Tumour Biol. 2014;35:6265–70.CrossRefPubMed Huang S, Liao Q, Li L, Xin D. Pttg1 inhibits smad3 in prostate cancer cells to promote their proliferation. Tumour Biol. 2014;35:6265–70.CrossRefPubMed
6.
Zurück zum Zitat Xia Q, Li C, Bian P, Wang J, Dong S. Targeting smad3 for inhibiting prostate cancer metastasis. Tumour Biol. 2014;35:8537–41.CrossRefPubMed Xia Q, Li C, Bian P, Wang J, Dong S. Targeting smad3 for inhibiting prostate cancer metastasis. Tumour Biol. 2014;35:8537–41.CrossRefPubMed
7.
Zurück zum Zitat Lin R, Feng J, Dong S, Pan R, Zhuang H, Ding Z. Regulation of autophagy of prostate cancer cells by beta-catenin signaling. Cell Physiol Biochem. 2015;35:926–32.CrossRefPubMed Lin R, Feng J, Dong S, Pan R, Zhuang H, Ding Z. Regulation of autophagy of prostate cancer cells by beta-catenin signaling. Cell Physiol Biochem. 2015;35:926–32.CrossRefPubMed
8.
Zurück zum Zitat Li T, Zhao X, Mo Z, Huang W, Yan H, Ling Z, et al. Formononetin promotes cell cycle arrest via downregulation of akt/cyclin d1/cdk4 in human prostate cancer cells. Cell Physiol Biochem. 2014;34:1351–8.CrossRefPubMed Li T, Zhao X, Mo Z, Huang W, Yan H, Ling Z, et al. Formononetin promotes cell cycle arrest via downregulation of akt/cyclin d1/cdk4 in human prostate cancer cells. Cell Physiol Biochem. 2014;34:1351–8.CrossRefPubMed
9.
Zurück zum Zitat Gillies K, Wertman J, Charette N, Dupre DJ. Anterograde trafficking of cxcr4 and ccr2 receptors in a prostate cancer cell line. Cell Physiol Biochem. 2013;32:74–85.CrossRefPubMed Gillies K, Wertman J, Charette N, Dupre DJ. Anterograde trafficking of cxcr4 and ccr2 receptors in a prostate cancer cell line. Cell Physiol Biochem. 2013;32:74–85.CrossRefPubMed
10.
Zurück zum Zitat Dhar S, Kolishetti N, Lippard SJ, Farokhzad OC. Targeted delivery of a cisplatin prodrug for safer and more effective prostate cancer therapy in vivo. Proc Natl Acad Sci U S A. 2011;108:1850–5.CrossRefPubMedPubMedCentral Dhar S, Kolishetti N, Lippard SJ, Farokhzad OC. Targeted delivery of a cisplatin prodrug for safer and more effective prostate cancer therapy in vivo. Proc Natl Acad Sci U S A. 2011;108:1850–5.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Villar J, Quadri HS, Song I, Tomita Y, Tirado OM, Notario V. Pcph/entpd5 expression confers to prostate cancer cells resistance against cisplatin-induced apoptosis through protein kinase calpha-mediated bcl-2 stabilization. Cancer Res. 2009;69:102–10.CrossRefPubMedPubMedCentral Villar J, Quadri HS, Song I, Tomita Y, Tirado OM, Notario V. Pcph/entpd5 expression confers to prostate cancer cells resistance against cisplatin-induced apoptosis through protein kinase calpha-mediated bcl-2 stabilization. Cancer Res. 2009;69:102–10.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Dhar S, Gu FX, Langer R, Farokhzad OC, Lippard SJ. Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized pt(iv) prodrug-plga-peg nanoparticles. Proc Natl Acad Sci U S A. 2008;105:17356–61.CrossRefPubMedPubMedCentral Dhar S, Gu FX, Langer R, Farokhzad OC, Lippard SJ. Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized pt(iv) prodrug-plga-peg nanoparticles. Proc Natl Acad Sci U S A. 2008;105:17356–61.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Huang CY, Huang SP, Lin VC, Yu CC, Chang TY, Lu TL, et al. Genetic variants of the autophagy pathway as prognostic indicators for prostate cancer. Sci Rep. 2015;5:14045.CrossRefPubMedPubMedCentral Huang CY, Huang SP, Lin VC, Yu CC, Chang TY, Lu TL, et al. Genetic variants of the autophagy pathway as prognostic indicators for prostate cancer. Sci Rep. 2015;5:14045.CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Shi Y, Han JJ, Tennakoon JB, Mehta FF, Merchant FA, Burns AR, et al. Androgens promote prostate cancer cell growth through induction of autophagy. Mol Endocrinol. 2013;27:280–95.CrossRefPubMed Shi Y, Han JJ, Tennakoon JB, Mehta FF, Merchant FA, Burns AR, et al. Androgens promote prostate cancer cell growth through induction of autophagy. Mol Endocrinol. 2013;27:280–95.CrossRefPubMed
20.
Zurück zum Zitat Ouyang DY, Xu LH, He XH, Zhang YT, Zeng LH, Cai JY, et al. Autophagy is differentially induced in prostate cancer lncap, du145 and pc-3 cells via distinct splicing profiles of atg5. Autophagy. 2013;9:20–32.CrossRefPubMedPubMedCentral Ouyang DY, Xu LH, He XH, Zhang YT, Zeng LH, Cai JY, et al. Autophagy is differentially induced in prostate cancer lncap, du145 and pc-3 cells via distinct splicing profiles of atg5. Autophagy. 2013;9:20–32.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Lian J, Karnak D, Xu L. The bcl-2-beclin 1 interaction in (−)-gossypol-induced autophagy versus apoptosis in prostate cancer cells. Autophagy. 2010;6:1201–3.CrossRefPubMedPubMedCentral Lian J, Karnak D, Xu L. The bcl-2-beclin 1 interaction in (−)-gossypol-induced autophagy versus apoptosis in prostate cancer cells. Autophagy. 2010;6:1201–3.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Ferrara N, Gerber HP, LeCouter J. The biology of vegf and its receptors. Nat Med. 2003;9:669–76.CrossRefPubMed Ferrara N, Gerber HP, LeCouter J. The biology of vegf and its receptors. Nat Med. 2003;9:669–76.CrossRefPubMed
26.
Zurück zum Zitat Xiao X, Prasadan K, Guo P, El-Gohary Y, Fischbach S, Wiersch J, et al. Pancreatic duct cells as a source of vegf in mice. Diabetologia. 2014;57:991–1000.CrossRefPubMedPubMedCentral Xiao X, Prasadan K, Guo P, El-Gohary Y, Fischbach S, Wiersch J, et al. Pancreatic duct cells as a source of vegf in mice. Diabetologia. 2014;57:991–1000.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Xiao X, Guo P, Chen Z, El-Gohary Y, Wiersch J, Gaffar I, et al. Hypoglycemia reduces vascular endothelial growth factor a production by pancreatic beta cells as a regulator of beta cell mass. J Biol Chem. 2013;288:8636–46.CrossRefPubMedPubMedCentral Xiao X, Guo P, Chen Z, El-Gohary Y, Wiersch J, Gaffar I, et al. Hypoglycemia reduces vascular endothelial growth factor a production by pancreatic beta cells as a regulator of beta cell mass. J Biol Chem. 2013;288:8636–46.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Bagri A, Kouros-Mehr H, Leong KG, Plowman GD. Use of anti-vegf adjuvant therapy in cancer: Challenges and rationale. Trends Mol Med. 2010;16:122–32.CrossRefPubMed Bagri A, Kouros-Mehr H, Leong KG, Plowman GD. Use of anti-vegf adjuvant therapy in cancer: Challenges and rationale. Trends Mol Med. 2010;16:122–32.CrossRefPubMed
29.
Zurück zum Zitat Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P, et al. Inhibition of vascular endothelial growth factor (vegf) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol. 2004;165:35–52.CrossRefPubMedPubMedCentral Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P, et al. Inhibition of vascular endothelial growth factor (vegf) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol. 2004;165:35–52.CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Shima DT, Adamis AP, Ferrara N, Yeo KT, Yeo TK, Allende R, et al. Hypoxic induction of endothelial cell growth factors in retinal cells: Identification and characterization of vascular endothelial growth factor (vegf) as the mitogen. Mol Med. 1995;1:182–93.PubMedPubMedCentral Shima DT, Adamis AP, Ferrara N, Yeo KT, Yeo TK, Allende R, et al. Hypoxic induction of endothelial cell growth factors in retinal cells: Identification and characterization of vascular endothelial growth factor (vegf) as the mitogen. Mol Med. 1995;1:182–93.PubMedPubMedCentral
31.
Zurück zum Zitat Cheng SY, Nagane M, Huang HS, Cavenee WK. Intracerebral tumor-associated hemorrhage caused by overexpression of the vascular endothelial growth factor isoforms vegf121 and vegf165 but not vegf189. Proc Natl Acad Sci U S A. 1997;94:12081–7.CrossRefPubMedPubMedCentral Cheng SY, Nagane M, Huang HS, Cavenee WK. Intracerebral tumor-associated hemorrhage caused by overexpression of the vascular endothelial growth factor isoforms vegf121 and vegf165 but not vegf189. Proc Natl Acad Sci U S A. 1997;94:12081–7.CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Huez I, Creancier L, Audigier S, Gensac MC, Prats AC, Prats H. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol Cell Biol. 1998;18:6178–90.CrossRefPubMedPubMedCentral Huez I, Creancier L, Audigier S, Gensac MC, Prats AC, Prats H. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol Cell Biol. 1998;18:6178–90.CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Pereira DM, Rodrigues PM, Borralho PM, Rodrigues CM. Delivering the promise of miRNA cancer therapeutics. Drug Discov Today. 2013;18:282–9.CrossRefPubMed Pereira DM, Rodrigues PM, Borralho PM, Rodrigues CM. Delivering the promise of miRNA cancer therapeutics. Drug Discov Today. 2013;18:282–9.CrossRefPubMed
35.
Zurück zum Zitat Mei Q, Li F, Quan H, Liu Y, Xu H. Busulfan inhibits growth of human osteosarcoma through mir-200 family microRNAs in vitro and in vivo. Cancer Sci. 2014;105:755–62.CrossRefPubMedPubMedCentral Mei Q, Li F, Quan H, Liu Y, Xu H. Busulfan inhibits growth of human osteosarcoma through mir-200 family microRNAs in vitro and in vivo. Cancer Sci. 2014;105:755–62.CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Wang F, Xiao W, Sun J, Han D, Zhu Y. Mirna-181c inhibits egfr-signaling-dependent mmp9 activation via suppressing akt phosphorylation in glioblastoma. Tumour Biol. 2014;35:8653–8.CrossRefPubMed Wang F, Xiao W, Sun J, Han D, Zhu Y. Mirna-181c inhibits egfr-signaling-dependent mmp9 activation via suppressing akt phosphorylation in glioblastoma. Tumour Biol. 2014;35:8653–8.CrossRefPubMed
37.
Zurück zum Zitat Liu G, Jiang C, Li D, Wang R, Wang W. Mirna-34a inhibits egfr-signaling-dependent mmp7 activation in gastric cancer. Tumour Biol. 2014;35:9801–6.CrossRefPubMed Liu G, Jiang C, Li D, Wang R, Wang W. Mirna-34a inhibits egfr-signaling-dependent mmp7 activation in gastric cancer. Tumour Biol. 2014;35:9801–6.CrossRefPubMed
38.
Zurück zum Zitat Zhao M, Huang J, Gui K, Xiong M, Cai G, Xu J, et al. The downregulation of mir-144 is associated with the growth and invasion of osteosarcoma cells through the regulation of tagln expression. Int J Mol Med. 2014;34:1565–72.PubMed Zhao M, Huang J, Gui K, Xiong M, Cai G, Xu J, et al. The downregulation of mir-144 is associated with the growth and invasion of osteosarcoma cells through the regulation of tagln expression. Int J Mol Med. 2014;34:1565–72.PubMed
39.
Zurück zum Zitat Cao T, Li H, Hu Y, Ma D, Cai X. Mir-144 suppresses the proliferation and metastasis of hepatocellular carcinoma by targeting e2f3. Tumour Biol. 2014;35:10759–64.CrossRefPubMed Cao T, Li H, Hu Y, Ma D, Cai X. Mir-144 suppresses the proliferation and metastasis of hepatocellular carcinoma by targeting e2f3. Tumour Biol. 2014;35:10759–64.CrossRefPubMed
40.
41.
Zurück zum Zitat Hassan F, Nuovo GJ, Crawford M, Boyaka PN, Kirkby S, Nana-Sinkam SP, et al. Mir-101 and mir-144 regulate the expression of the cftr chloride channel in the lung. PLoS One. 2012;7, e50837.CrossRefPubMedPubMedCentral Hassan F, Nuovo GJ, Crawford M, Boyaka PN, Kirkby S, Nana-Sinkam SP, et al. Mir-101 and mir-144 regulate the expression of the cftr chloride channel in the lung. PLoS One. 2012;7, e50837.CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat Iwaya T, Yokobori T, Nishida N, Kogo R, Sudo T, Tanaka F, et al. Downregulation of mir-144 is associated with colorectal cancer progression via activation of mtor signaling pathway. Carcinogenesis. 2012;33:2391–7.CrossRefPubMed Iwaya T, Yokobori T, Nishida N, Kogo R, Sudo T, Tanaka F, et al. Downregulation of mir-144 is associated with colorectal cancer progression via activation of mtor signaling pathway. Carcinogenesis. 2012;33:2391–7.CrossRefPubMed
43.
Zurück zum Zitat Akiyoshi S, Fukagawa T, Ueo H, Ishibashi M, Takahashi Y, Fabbri M, et al. Clinical significance of mir-144-zfx axis in disseminated tumour cells in bone marrow in gastric cancer cases. Br J Cancer. 2012;107:1345–53.CrossRefPubMedPubMedCentral Akiyoshi S, Fukagawa T, Ueo H, Ishibashi M, Takahashi Y, Fabbri M, et al. Clinical significance of mir-144-zfx axis in disseminated tumour cells in bone marrow in gastric cancer cases. Br J Cancer. 2012;107:1345–53.CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Kalimutho M, Del Vecchio Blanco G, Di Cecilia S, Sileri P, Cretella M, Pallone F, et al. Differential expression of mir-144* as a novel fecal-based diagnostic marker for colorectal cancer. J Gastroenterol. 2011;46:1391–402.CrossRefPubMed Kalimutho M, Del Vecchio Blanco G, Di Cecilia S, Sileri P, Cretella M, Pallone F, et al. Differential expression of mir-144* as a novel fecal-based diagnostic marker for colorectal cancer. J Gastroenterol. 2011;46:1391–402.CrossRefPubMed
45.
Zurück zum Zitat Huang SQ, Liao QJ, Wang XW, Xin DQ, Chen SX, Wu QJ, et al. Rnai-mediated knockdown of pituitary tumor- transforming gene-1 (pttg1) suppresses the proliferation and invasive potential of pc3 human prostate cancer cells. Braz J Med Biol Res. 2012;45:995–1001.CrossRefPubMedPubMedCentral Huang SQ, Liao QJ, Wang XW, Xin DQ, Chen SX, Wu QJ, et al. Rnai-mediated knockdown of pituitary tumor- transforming gene-1 (pttg1) suppresses the proliferation and invasive potential of pc3 human prostate cancer cells. Braz J Med Biol Res. 2012;45:995–1001.CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Horoszewicz JS, Leong SS, Carter WA. Differential susceptibility of spleen focus-forming virus and murine leukemia viruses to ansamycin antibiotics. Antimicrob Agents Chemother. 1977;12:4–10.CrossRefPubMedPubMedCentral Horoszewicz JS, Leong SS, Carter WA. Differential susceptibility of spleen focus-forming virus and murine leukemia viruses to ansamycin antibiotics. Antimicrob Agents Chemother. 1977;12:4–10.CrossRefPubMedPubMedCentral
Metadaten
Titel
VEGF-activated miR-144 regulates autophagic survival of prostate cancer cells against Cisplatin
verfasst von
Feng Liu
Jihong Wang
Qiang Fu
Xinru Zhang
Ying Wang
Jialin Liu
Jianwen Huang
Xiangguo Lv
Publikationsdatum
13.11.2015
Verlag
Springer Netherlands
Erschienen in
Tumor Biology / Ausgabe 12/2016
Print ISSN: 1010-4283
Elektronische ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-4383-1

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