Artículo

Cerda-Opazo, P.; Valenzuela-Valderrama, M.; Wichmann, I.; Rodríguez, A.; Contreras-Reyes, D.; Fernández, E.A.; Carrasco-Aviño, G.; Corvalán, A.H.; Quest, A.F.G. "Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer" (2018) Oncotarget. 9(16):12853-12867
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Abstract:

BACKGROUND: The objective of the study was to determine the relationship between Survivin and Reprimo transcript/protein expression levels, and gastric cancer outcome. METHODS: In silico correlations between an agnostic set of twelve p53-dependent apoptosis and cell-cycle genes were explored in the gastric adenocarcinoma TCGA database, using cBioPortal. Findings were validated by regression analysis of RNAseq data. Separate regression analyses were performed to assess the impact of p53 status on Survivin and Reprimo. Quantitative reverse-transcription PCR (RT-qPCR) and immunohistochemistry confirmed in silico findings on fresh-frozen and paraffinembedded gastric cancer tissues, respectively. Wild-type (AGS, SNU-1) and mutated p53 (NCI-N87) cell lines transfected with pEGFP-Survivin or pCMV6-Reprimo were evaluated by RT-qPCR and Western blotting. Kaplan-Meier method and Long-Rank test were used to assess differences in patient outcome. RESULTS: cBioPortal analysis revealed an inverse correlation between Survivin and Reprimo expression (Pearson's r= -0.3, Spearman's ρ= -0.55). RNAseq analyses confirmed these findings (Spearman's ρ= -0.37, p < 4.2e-09) and revealed p53 dependence in linear regression models (p < 0.05). mRNA and protein levels validated these observations in clinical samples (p < 0.001). In vitro analysis in cell lines demonstrated that increasing Survivin reduced Reprimo, while increasing Reprimo reduced Survivin expression, but only did so in p53 wild-type gastric cells (p < 0.05). Survivin-positive but Reprimo-negative patients displayed shorter overall survival rates (p=0.047, Long Rank Test) (HR=0.32; 95%IC: 0.11-0.97; p=0.044). CONCLUSIONS: TCGA RNAseq data analysis, evaluation of clinical samples and studies in cell lines identified an inverse relationship between Survivin and Reprimo. Elevated Survivin and reduced Reprimo protein expression correlated with poor patient prognosis in gastric cancer. © Cerda-Opazo et al.

Registro:

Documento: Artículo
Título:Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer
Autor:Cerda-Opazo, P.; Valenzuela-Valderrama, M.; Wichmann, I.; Rodríguez, A.; Contreras-Reyes, D.; Fernández, E.A.; Carrasco-Aviño, G.; Corvalán, A.H.; Quest, A.F.G.
Filiación:Lab. de Comunicaciones Celulares, Centro de Estudios en Ejercicio, Metabolismo y Cancer (CEMC), Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas (ICBM), Facultad De Medicina, Universidad de Chile, Santiago, Chile
Gastric Cancer Research Group - Laboratory of Oncology, UC Center for Investigational Oncology (CITO), Pontificia Universidad Católica de Chile, Santiago, Chile
Advanced Center for Chronic Diseases (ACCDiS), Santiago, Chile
Facultad de Ciencias de la Salud, Universidad Central de Chile, Santiago, Chile
CIDIE - CONICET - Facultad de Ingeniería, Campus Universitario, Universidad Católica de Córdoba, Córdoba, Argentina
Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina
National Bioinformatics Consortia (BIA) of Argentina, Buenos Aires, Argentina
Departamento de Anatomía Patológica, Hospital Clínico José Joaquín Aguirre, Universidad de Chile, Santiago, Chile
Core Biodata, Advanced Center for Chronic Diseases (ACCDiS), Santiago, Chile
Palabras clave:Gastric cancer; Reprimo; Survivin; TCGA
Año:2018
Volumen:9
Número:16
Página de inicio:12853
Página de fin:12867
DOI: http://dx.doi.org/10.18632/oncotarget.24402
Título revista:Oncotarget
Título revista abreviado:Oncotarget
ISSN:19492553
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19492553_v9_n16_p12853_CerdaOpazo

Referencias:

  • Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D.M., Bray, F., Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012 (2015) Int J Cancer, 136, pp. E359-E386. , https://doi.org/10.1002/ijc.29210
  • Bass, A.J., Thorsson, V., Shmulevich, I., Reynolds, S.M., Miller, M., Bernard, B., Hinoue, T., Shen, R., Comprehensive molecular characterization of gastric adenocarcinoma (2014) Nature, 513, pp. 202-209. , https://doi.org/10.1038/nature13480
  • Garg, H., Suri, P., Gupta, J.C., Talwar, G.P., Dubey, S., Survivin: a unique target for tumor therapy (2016) Cancer Cell Int, 16, p. 49. , https://doi.org/10.1186/s12935-016-0326-1
  • Cheung, C.H., Huang, C.C., Tsai, F.Y., Lee, J.Y., Cheng, S.M., Chang, Y.C., Huang, Y.C., Chang, J.Y., Survivin-biology and potential as a therapeutic target in oncology (2013) Onco Targets Ther, 6, pp. 1453-1462. , https://doi.org/10.2147/ott.s33374
  • Valenzuela, M., Bravo, D., Canales, J., Sanhueza, C., Diaz, N., Almarza, O., Toledo, H., Quest, A.F., Helicobacter pylori-induced loss of survivin and gastric cell viability is attributable to secreted bacterial gamma-glutamyl transpeptidase activity (2013) J Infect Dis, 208, pp. 1131-1141. , https://doi.org/10.1093/infdis/jit286
  • Valenzuela, M., Perez-Perez, G., Corvalan, A.H., Carrasco, G., Urra, H., Bravo, D., Toledo, H., Quest, A.F., Helicobacter pyloriinduced loss of the inhibitor-of-apoptosis protein survivin is linked to gastritis and death of human gastric cells (2010) J Infect Dis, 202, pp. 1021-1030. , https://doi.org/10.1086/656143
  • Chun-Lai, T., Murad, S., Erlandsson, M.C., Hussein, H., Sulaiman, W., Dhaliwal, J.S., Bokarewa, M.I., Recognizing rheumatoid arthritis: oncoprotein survivin opens new possibilities: a population-based case-control study (2015) Medicine (Baltimore), 94, p. e468. , https://doi.org/10.1097/md.0000000000000468
  • Bertazza, L., Mocellin, S., Marchet, A., Pilati, P., Gabrieli, J., Scalerta, R., Nitti, D., Survivin gene levels in the peripheral blood of patients with gastric cancer independently predict survival (2009) J Transl Med, 7, p. 111. , https://doi.org/10.1186/1479-5876-7-111
  • Jiang, Y., Saavedra, H.I., Holloway, M.P., Leone, G., Altura, R.A., Aberrant regulation of survivin by the RB/E2F family of proteins (2004) J Biol Chem, 279, pp. 40511-40520. , https://doi.org/10.1074/jbc.M404496200
  • Xu, R., Zhang, P., Huang, J., Ge, S., Lu, J., Qian, G., Sp1 and Sp3 regulate basal transcription of the survivin gene (2007) Biochem Biophys Res Commun, 356, pp. 286-292. , https://doi.org/10.1016/j.bbrc.2007.02.140
  • Hoffman, W.H., Biade, S., Zilfou, J.T., Chen, J., Murphy, M., Transcriptional repression of the anti-apoptotic survivin gene by wild type p53 (2002) J Biol Chem, 277, pp. 3247-3257. , https://doi.org/10.1074/jbc.M106643200
  • Busuttil, R.A., Zapparoli, G.V., Haupt, S., Fennell, C., Wong, S.Q., Pang, J.M., Takeno, E.A., Boussioutas, A., Role of p53 in the progression of gastric cancer (2014) Oncotarget, 5, pp. 12016-12026. , https://doi.org/10.18632/oncotarget.2434
  • Jung, C.L., Mun, H., Jo, S.Y., Oh, J.H., Lee, C., Choi, E.K., Jang, S.J., Suh, Y.A., Suppression of gain-of-function mutant p53 with metabolic inhibitors reduces tumor growth in vivo (2016) Oncotarget, 7, pp. 77664-77682. , https://doi.org/10.18632/oncotarget.12758
  • Tsuji, N., Furuse, K., Asanuma, K., Furuya, M., Kondoh, K., Kamagata, C., Sasaki, M., Watanabe, N., Mutations of the p53 gene and loss of heterozygosity at chromosome 17p13.1 are associated with increased survivin expression in breast cancer (2004) Breast Cancer Res Treat, 87, pp. 23-31. , https://doi.org/10.1023/B:BREA.0000041575.73262.aa
  • Xu, Y., Fang, F., Ludewig, G., Jones, G., Jones, D., A mutation found in the promoter region of the human survivin gene is correlated to overexpression of survivin in cancer cells (2004) DNA Cell Biol, 23, pp. 527-537. , https://doi.org/10.1089/dna.2004.23.527
  • Yeo, K.S., Mohidin, T.B., Ng, C.C., Epstein-Barr virus-encoded latent membrane protein-1 upregulates 14-3-3sigma and Reprimo to confer G(2)/M phase cell cycle arrest (2012) C R Biol, 335, pp. 713-721. , https://doi.org/10.1016/j.crvi.2012.11.002
  • Malik, S., Jiang, S., Garee, J.P., Verdin, E., Lee, A.V., O'Malley, B.W., Zhang, M., Oesterreich, S., Histone deacetylase 7 and FoxA1 in estrogen-mediated repression of RPRM (2010) Mol Cell Biol, 30, pp. 399-412. , https://doi.org/10.1128/mcb.00907-09
  • Xu, M., Knox, A.J., Michaelis, K.A., Kiseljak-Vassiliades, K., Kleinschmidt-DeMasters, B.K., Lillehei, K.O., Wierman, M.E., Reprimo (RPRM) is a novel tumor suppressor in pituitary tumors and regulates survival, proliferation, and tumorigenicity (2012) Endocrinology, 153, pp. 2963-2973. , https://doi.org/10.1210/en.2011-2021
  • Luo, J., Zhu, Y., Yang, G., Gong, L., Wang, B., Liu, H., Loss of reprimo and S100A2 expression in human gastric adenocarcinoma (2011) Diagn Cytopathol, 39, pp. 752-757. , https://doi.org/10.1002/dc.21461
  • Saavedra, K., Valbuena, J., Olivares, W., Marchant, M.J., Rodriguez, A., Torres-Estay, V., Carrasco-Avino, G., Corvalan, A.H., Loss of expression of reprimo, a p53-induced cell cycle arrest gene, correlates with invasive stage of tumor progression and p73 expression in gastric cancer (2015) PLoS One, 10. , https://doi.org/10.1371/journal.pone.0125834
  • Garcia-Bloj, B., Moses, C., Sgro, A., Plani-Lam, J., Arooj, M., Duffy, C., Thiruvengadam, S., Corvalan, A.H., Waking up dormant tumor suppressor genes with zinc fingers, TALEs and the CRISPR/dCas9 system (2016) Oncotarget, 7, pp. 60535-60554. , https://doi.org/10.18632/oncotarget.11142
  • Schneider, B.G., Peng, D.F., Camargo, M.C., Piazuelo, M.B., Sicinschi, L.A., Mera, R., Romero-Gallo, J., El-Rifai, W., Promoter DNA hypermethylation in gastric biopsies from subjects at high and low risk for gastric cancer (2010) Int J Cancer, 127, pp. 2588-2597. , https://doi.org/10.1002/ijc.25274
  • Wang, Q.P., Wang, Y., Wang, X.D., Mo, X.M., Gu, J., Lu, Z.Y., Pan, Z.L., Zhu, Y.X., Survivin up-regulates the expression of breast cancer resistance protein (BCRP) through attenuating the suppression of p53 on NF-kappaB expression in MCF-7/5-FU cells (2013) Int J Biochem Cell Biol, 45, pp. 2036-2044. , https://doi.org/10.1016/j.biocel.2013.06.026
  • Huang, G., Meng, L., Tsai, R.Y., p53 configures the G2/M arrest response of nucleostemin-deficient cells (2015) Cell Death Dis, 1. , https://doi.org/10.1038/cddiscovery.2015.60
  • Shi, Y., Chen, C., Zhang, X., Liu, Q., Xu, J.L., Zhang, H.R., Yao, X.H., Liu, L., Primate-specific miR-663 functions as a tumor suppressor by targeting PIK3CD and predicts the prognosis of human glioblastoma (2014) Clin Cancer Res, 20, pp. 1803-1813. , https://doi.org/10.1158/1078-0432.ccr-13-2284
  • Figueiredo, C., Costa, S., Karameris, A., Machado, J.C., Pathogenesis of gastric cancer (2015) Helicobacter, 20, pp. 30-35. , https://doi.org/10.1111/hel.12254
  • Cerami, E., Gao, J., Dogrusoz, U., Gross, B.E., Sumer, S.O., Aksoy, B.A., Jacobsen, A., Goldberg, A.P., The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data (2012) Cancer Discov, 2, pp. 401-404. , https://doi.org/10.1158/2159-8290.cd-12-0095
  • Torres, V.A., Tapia, J.C., Rodriguez, D.A., Parraga, M., Lisboa, P., Montoya, M., Leyton, L., Quest, A.F., Caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin (2006) J Cell Sci, 119, pp. 1812-1823. , https://doi.org/10.1242/jcs.02894
  • Li, N., Xie, C., Lu, N.H., p53, a potential predictor of helicobacter pylori infection-associated gastric carcinogenesis? (2016) Oncotarget, 7, pp. 66276-66286. , https://doi.org/10.18632/oncotarget.11414
  • Mihmanli, M., Ilhan, E., Idiz, U.O., Alemdar, A., Demir, U., Recent developments and innovations in gastric cancer (2016) World J Gastroenterol, 22, pp. 4307-4320. , https://doi.org/10.3748/wjg.v22.i17.4307
  • Boidot, R., Vegran, F., Lizard-Nacol, S., Transcriptional regulation of the survivin gene (2014) Mol Biol Rep, 41, pp. 233-240. , https://doi.org/10.1007/s11033-013-2856-0
  • Jaiswal, P.K., Goel, A., Mittal, R.D., Survivin: a molecular biomarker in cancer (2015) Indian J Med Res, 141, pp. 389-397. , https://doi.org/10.4103/0971-5916.159250
  • Karar, J., Maity, A., PI3K/AKT/mTOR pathway in angiogenesis (2011) Front Mol Neurosci, 4, p. 51. , https://doi.org/10.3389/fnmol.2011.00051
  • Fernandez, J.G., Rodriguez, D.A., Valenzuela, M., Calderon, C., Urzua, U., Munroe, D., Rosas, C., Quest, A.F., Survivin expression promotes VEGF-induced tumor angiogenesis via PI3K/Akt enhanced beta-catenin/Tcf-Lef dependent transcription (2014) Mol Cancer, 13, p. 209. , https://doi.org/10.1186/1476-4598-13-209
  • Li, B., Senbabaoglu, Y., Peng, W., Yang, M.L., Xu, J., Li, J.Z., Genomic estimates of aneuploid content in glioblastoma multiforme and improved classification (2012) Clin Cancer Res, 18, pp. 5595-5605. , https://doi.org/10.1158/1078-0432.ccr-12-1427
  • Sanhueza, C., Wehinger, S., Castillo Bennett, J., Valenzuela, M., Owen, G.I., Quest, A.F., The twisted survivin connection to angiogenesis (2015) Mol Cancer, 14, p. 198. , https://doi.org/10.1186/s12943-015-0467-1
  • Abraham, A.G., O'Neill, E., Pi3k/Akt-mediated regulation of p53 in cancer (2014) Biochem Soc Trans, 42, pp. 798-803. , https://doi.org/10.1042/bst20140070
  • Bernal, C., Aguayo, F., Villarroel, C., Vargas, M., Diaz, I., Ossandon, F.J., Santibanez, E., Corvalan, A.H., Reprimo as a potential biomarker for early detection in gastric cancer (2008) Clin Cancer Res, 14, pp. 6264-6269. , https://doi.org/10.1158/1078-0432.ccr-07-4522
  • Gao, J., Aksoy, B.A., Dogrusoz, U., Dresdner, G., Gross, B., Sumer, S.O., Sun, Y., Schultz, N., Integrative analysis of complex cancer genomics and clinical profiles using the cbioportal (2013) Sci Signal, 6. , https://doi.org/10.1126/scisignal.2004088
  • Zhu, Y., Qiu, P., Ji, Y., TCGA-assembler: open-source software for retrieving and processing tcga data (2014) Nat Methods, 11, pp. 599-600. , https://doi.org/10.1038/nmeth.2956
  • Carrasco, G., Diaz, J., Valbuena, J.R., Ibanez, P., Rodriguez, P., Araya, G., Rodriguez, C., Corvalan, A.H., Overexpression of p73 as a tissue marker for high-risk gastritis (2010) Clin Cancer Res, 16, pp. 3253-3259. , https://doi.org/10.1158/1078-0432.ccr-09-2491
  • Japanese classification of gastric carcinoma: 3rd English edition (2011) Gastric Cancer, 14, pp. 101-112. , https://doi.org/10.1007/s10120-011-0041-5
  • Washington, K., 7th edition of the AJCC cancer staging manual: stomach (2010) Ann Surg Oncol, 17, pp. 3077-3079. , https://doi.org/10.1245/s10434-010-1362-z
  • García, C.C., Benavides, C.C., Apablaza, S.P., Rubilar, P.O., Covacevich, S.R., Peñaloza, P.M., Guerra, J.C., Romero, S.C., [Surgical treatment of gastric cancer: results in 423 cases] [Article in Spanish] (2007) Rev Med Chil, 135, pp. 687-695
  • Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Wittwer, C.T., The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments (2009) Clin Chem, 55, pp. 611-622. , https://doi.org/10.1373/clinchem.2008.112797
  • Da, C.L., Xin, Y., Zhao, J., Luo, X.D., Significance and relationship between yes-associated protein and survivin expression in gastric carcinoma and precancerous lesions (2009) World J Gastroenterol, 15, pp. 4055-4061
  • Ando, K., Oki, E., Saeki, H., Yan, Z., Tsuda, Y., Hidaka, G., Kasagi, Y., Maehara, Y., Discrimination of p53 immunohistochemistrypositive tumors by its staining pattern in gastric cancer (2015) Cancer Med, 4, pp. 75-83. , https://doi.org/10.1002/cam4.346

Citas:

---------- APA ----------
Cerda-Opazo, P., Valenzuela-Valderrama, M., Wichmann, I., Rodríguez, A., Contreras-Reyes, D., Fernández, E.A., Carrasco-Aviño, G.,..., Quest, A.F.G. (2018) . Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer. Oncotarget, 9(16), 12853-12867.
http://dx.doi.org/10.18632/oncotarget.24402
---------- CHICAGO ----------
Cerda-Opazo, P., Valenzuela-Valderrama, M., Wichmann, I., Rodríguez, A., Contreras-Reyes, D., Fernández, E.A., et al. "Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer" . Oncotarget 9, no. 16 (2018) : 12853-12867.
http://dx.doi.org/10.18632/oncotarget.24402
---------- MLA ----------
Cerda-Opazo, P., Valenzuela-Valderrama, M., Wichmann, I., Rodríguez, A., Contreras-Reyes, D., Fernández, E.A., et al. "Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer" . Oncotarget, vol. 9, no. 16, 2018, pp. 12853-12867.
http://dx.doi.org/10.18632/oncotarget.24402
---------- VANCOUVER ----------
Cerda-Opazo, P., Valenzuela-Valderrama, M., Wichmann, I., Rodríguez, A., Contreras-Reyes, D., Fernández, E.A., et al. Inverse expression of survivin and reprimo correlates with poor patient prognosis in gastric cancer. Oncotarget. 2018;9(16):12853-12867.
http://dx.doi.org/10.18632/oncotarget.24402