SPOCK1 as a potential cancer prognostic marker promotes the proliferation and metastasis of gallbladder cancer cells by activating the PI3K/AKT pathway

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• 作者：Yi-Jun Shu (1) (2)
  Hao Weng (1) (2)
  Yuan-Yuan Ye (1) (2)
  Yun-Ping Hu (1) (2)
  Run-Fa Bao (1) (2)
  Yang Cao (1) (2)
  Xu-An Wang (1) (2)
  Fei Zhang (1) (2)
  Shan-Shan Xiang (1) (2)
  Huai-Feng Li (1) (2)
  Xiang-Song Wu (1) (2)
  Mao-Lan Li (1) (2)
  Lin Jiang (1) (2)
  Wei Lu (1) (2)
  Bao-San Han (1) (2)
  Zhi-Gang Jie (3)
  Ying-Bin Liu (1) (2)
  
  1. Laboratory of General Surgery and Department of General Surgery ; Xinhua Hospital ; Affiliated with Shanghai Jiao Tong University ; School of Medicine ; No. 1665 Kongjiang Road ; Shanghai ; 200092 ; China
  2. Institute of Biliary Tract Disease ; Shanghai Jiao Tong University School of Medicine ; No. 1665 Kongjiang Road ; Shanghai ; 200092 ; China
  3. The Department of General Surgery ; First affiliated hospital of Nanchang University ; No.17 Yongwaizheng street ; Nanchang ; 330006 ; Jiangxi ; China
  
• 关键词：Gallbladder cancer ; SPOCK1 ; Tumor progression ; RNA interference ; Epithelial ; mesenchymal transition
• 刊名：Molecular Cancer
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：14
• 期：1
• 全文大小：3,545 KB
• 参考文献：1. Wu XS, Shi LB, Li ML, Ding Q, Weng H, Wu WG, et al. Evaluation of two inflammation-based prognostic scores in patients with resectable gallbladder carcinoma. Ann Surg Oncol. 2014;21:449鈥?7. lank" title="It opens in new window">CrossRef
  2. Li M, Zhang S, Wang Z, Zhang B, Wu X, Weng H, et al. Prognostic significance of nemo-like kinase (NLK) expression in patients with gallbladder cancer. Tumour Biol. 2013;34:3995鈥?000. lank" title="It opens in new window">CrossRef
  3. Li M, Zhang Z, Li X, Ye J, Wu X, Tan Z, et al. Whole-exome and targeted gene sequencing of gallbladder carcinoma identifies recurrent mutations in the ErbB pathway. Nat Genet. 2014;46:872鈥?. lank" title="It opens in new window">CrossRef
  4. Tan Z, Li M, Wu W, Zhang L, Ding Q, Wu X, et al. NLK is a key regulator of proliferation and migration in gallbladder carcinoma cells. Mol Cell Biochem. 2012;369:27鈥?3. lank" title="It opens in new window">CrossRef
  5. Dong P, Zhang Y, Gu J, Wu W, Li M, Yang J, et al. Wogonin, an active ingredient of Chinese herb medicine Scutellaria baicalensis, inhibits the mobility and invasion of human gallbladder carcinoma GBC-SD cells by inducing the expression of maspin. J Ethnopharmacol. 2011;137:1373鈥?0. lank" title="It opens in new window">CrossRef
  6. Dong P, He XW, Gu J, Wu WG, Li ML, Yang JH, et al. Vimentin significantly promoted gallbladder carcinoma metastasis. Chin Med J (Engl). 2011;124:4236鈥?4.
  7. Chen L, Hu L, Chan TH, Tsao GS, Xie D, Huo KK, et al. Chromodomain helicase/adenosine triphosphatase DNA binding protein 1-like (CHD1l) gene suppresses the nucleus-to-mitochondria translocation of nur77 to sustain hepatocellular carcinoma cell survival. Hepatology. 2009;50:122鈥?. lank" title="It opens in new window">CrossRef
  8. Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science. 2009;325:1240鈥?. lank" title="It opens in new window">CrossRef
  9. Chen L, Chan TH, Yuan YF, Hu L, Huang J, Ma S, et al. CHD1L promotes hepatocellular carcinoma progression and metastasis in mice and is associated with these processes in human patients. J Clin Invest. 2010;120:1178鈥?1. lank" title="It opens in new window">CrossRef
  10. Colin C, Baeza N, Bartoli C, Fina F, Eudes N, Nanni I, et al. Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using Suppression Subtractive Hybridization. Oncogene. 2006;25:2818鈥?6. lank" title="It opens in new window">CrossRef
  11. Hartmann U, Hulsmann H, Seul J, Roll S, Midani H, Breloy I, et al. Testican-3: a brain-specific proteoglycan member of the BM-40/SPARC/osteonectin family. J Neurochem. 2013;125:399鈥?09. lank" title="It opens in new window">CrossRef
  12. Hausser HJ, Decking R, Brenner RE. Testican-1, an inhibitor of pro-MMP-2 activation, is expressed in cartilage. Osteoarthritis Cartilage. 2004;12:870鈥?. lank" title="It opens in new window">CrossRef
  13. Pinheiro C, Longatto-Filho A, Scapulatempo C, Ferreira L, Martins S, Pellerin L, et al. Increased expression of monocarboxylate transporters 1, 2, and 4 in colorectal carcinomas. Virchows Arch. 2008;452:139鈥?6. lank" title="It opens in new window">CrossRef
  14. Butte JM, Matsuo K, Gonen M, D鈥橝ngelica MI, Waugh E, Allen PJ, et al. Gallbladder cancer: differences in presentation, surgical treatment, and survival in patients treated at centers in three countries. J Am Coll Surg. 2011;212:50鈥?1. lank" title="It opens in new window">CrossRef
  15. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev. 1999;13:2905鈥?7. lank" title="It opens in new window">CrossRef
  16. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2:277鈥?8. lank" title="It opens in new window">CrossRef
  17. Cifuentes-Diaz C, Alliel PM, Charbonnier F, de la Porte S, Molgo J, Goudou D, et al. Regulated expression of the proteoglycan SPOCK in the neuromuscular system. Mech Dev. 2000;94:277鈥?2. lank" title="It opens in new window">CrossRef
  18. Li Y, Chen L, Chan TH, Liu M, Kong KL, Qiu JL, et al. SPOCK1 is regulated by CHD1L and blocks apoptosis and promotes HCC cell invasiveness and metastasis in mice. Gastroenterology. 2013;144:179鈥?1. e174. lank" title="It opens in new window">CrossRef
  19. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559鈥?4. lank" title="It opens in new window">CrossRef
  20. Harlozinska A. Progress in molecular mechanisms of tumor metastasis and angiogenesis. Anticancer Res. 2005;25:3327鈥?3.
  21. Miao L, Wang Y, Xia H, Yao C, Cai H, Song Y. SPOCK1 is a novel transforming growth factor-beta target gene that regulates lung cancer cell epithelial-mesenchymal transition. Biochem Biophys Res Commun. 2013;440:792鈥?. lank" title="It opens in new window">CrossRef
  22. Xia H, Ooi LL, Hui KM. MicroRNA-216a/217-induced epithelial-mesenchymal transition targets PTEN and SMAD7 to promote drug resistance and recurrence of liver cancer. Hepatology. 2013;58:629鈥?1. lank" title="It opens in new window">CrossRef
  23. Xia H, Hui KM. MicroRNAs involved in regulating epithelial-mesenchymal transition and cancer stem cells as molecular targets for cancer therapeutics. Cancer Gene Ther. 2012;19:723鈥?0. lank" title="It opens in new window">CrossRef
  24. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57鈥?0. lank" title="It opens in new window">CrossRef
  25. Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov. 2009;8:627鈥?4. lank" title="It opens in new window">CrossRef
  26. Zhen Y, Liu Z, Yang H, Yu X, Wu Q, Hua S, et al. Tumor suppressor PDCD4 modulates miR-184-mediated direct suppression of C-MYC and BCL2 blocking cell growth and survival in nasopharyngeal carcinoma. Cell Death Dis. 2013;4:e872. lank" title="It opens in new window">CrossRef
  27. Yu X, Zhen Y, Yang H, Wang H, Zhou Y, Wang E, et al. Loss of connective tissue growth factor as an unfavorable prognosis factor activates miR-18b by PI3K/AKT/C-Jun and C-Myc and promotes cell growth in nasopharyngeal carcinoma. Cell Death Dis. 2013;4:e634. lank" title="It opens in new window">CrossRef
  28. Yuan TL, Cantley LC. PI3K pathway alterations in cancer: variations on a theme. Oncogene. 2008;27:5497鈥?10. lank" title="It opens in new window">CrossRef
  29. Kumar PS, Shiras A, Das G, Jagtap JC, Prasad V, Shastry P. Differential expression and role of p21cip/waf1 and p27kip1 in TNF-alpha-induced inhibition of proliferation in human glioma cells. Mol Cancer. 2007;6:42. lank" title="It opens in new window">CrossRef
  30. Wen W, Ding J, Sun W, Fu J, Chen Y, Wu K, et al. Cyclin G1-mediated epithelial-mesenchymal transition via phosphoinositide 3-kinase/Akt signaling facilitates liver cancer progression. Hepatology. 2012;55:1787鈥?8. lank" title="It opens in new window">CrossRef
  31. Blackhall FH, Merry CL, Davies EJ, Jayson GC. Heparan sulfate proteoglycans and cancer. Br J Cancer. 2001;85:1094鈥?. lank" title="It opens in new window">CrossRef
  32. Jiang X, Couchman JR. Perlecan and tumor angiogenesis. J Histochem Cytochem. 2003;51:1393鈥?10. lank" title="It opens in new window">CrossRef
  33. Vlodavsky I, Friedmann Y. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest. 2001;108:341鈥?. lank" title="It opens in new window">CrossRef
  
• 刊物主题：Cancer Research; Oncology;
• 出版者：BioMed Central
• ISSN：1476-4598

文摘

Background Gallbladder cancer (GBC) is a leading cause of cancer-related death worldwide, and its prognosis remains poor, with 5-year survival of approximately 5%. In this study, we analyzed the involvement of a novel proteoglycan, Sparc/osteonectin, cwcv, and kazal-like domains proteoglycan 1 (SPOCK1), in the tumor progression and prognosis of human GBC. Methods SPOCK1 expression levels were measured in fresh samples and stored specimens of GBC and adjacent nontumor tissues. The effect of SPOCK1 on cell growth, DNA replication, migration and invasion were explored by Cell Counting Kit-8, colony formation, EdU retention assay, wound healing, and transwell migration assays, flow cytometric analysis, western blotting, and in vivo tumorigenesis and metastasis in nude mice. Results SPOCK1 mRNA and protein levels were increased in human GBC tissues compared with those in nontumor tissues. Immunohistochemical analysis indicated that SPOCK1 levels were increased in tumors that became metastatic, compared with those that did not, which was significantly associated with histological differentiation and patients with shorter overall survival periods. Knockdown of SPOCK1 expression by lentivirus-mediated shRNA transduction resulted in significant inhibition of GBC cell growth, colony formation, DNA replication, and invasion in vitro. The knockdown cells also formed smaller xenografted tumors than control GBC cells in nude mice. Overexpression of SPOCK1 had the opposite effects. In addition, SPOCK1 promoted cancer cell migration and epithelial-mesenchymal transition by regulating the expression of relevant genes. We found that activation of the PI3K/Akt pathway was involved in the oncogenic functions of SPOCK1 in GBC. Conclusions SPOCK1 activates PI3K/Akt signaling to block apoptosis and promote proliferation and metastasis by GBC cells in vitro and in vivo. Levels of SPOCK1 increase with the progression of human GBC. SPOCK1 acts as an oncogene and may be a prognostic factor or therapeutic target for patients with GBC.