Abnormal protein glycosylation and activated PI3K/Akt/mTOR pathway: Role in bladder cancer prognosis and targeted therapeutics

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Costa, Céu ^a,b,c   Pereira, Sofia ^a,b,c   Lima, Luís ^a,b,d   Peixoto, Andreia ^a   Fernandes, Elisabete ^a   Neves, Diogo ^a   Neves, Manuel ^a   Gaiteiro, Cristiana ^a   Tavares, Ana ^a   Da Costa, Rui M Gil ^a,b   Cruz, Ricardo ^a   Amaro, Teresina ^e   Oliveira, Paula A ^f   Ferreira, José Alexandre ^a,g   Santos, Lúcio L ^a,c  

^a PORTUGUESE ONCOLOGY INSTITUTE   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSIDADE FERNANDO PESSOA   (Portugal)

^d POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^e HOSPITAL PEDRO HISPANO   (Portugal)

^f UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^g UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RAPAMYCIN; S6 KINASE; SIALYL TN ANTIGEN; TN ANTIGEN; UNCLASSIFIED DRUG; AKT1 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; SIALOSYL-TN ANTIGEN; TARGET OF RAPAMYCIN KINASE; TUMOR ANTIGEN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER SPECIFIC SURVIVAL; CANCER STAGING; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; MUSCLE INVASIVE BLADDER CANCER; NONHUMAN; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RETROSPECTIVE STUDY; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR VOLUME; ANIMAL; GENE EXPRESSION REGULATION; GLYCOSYLATION; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; TREATMENT OUTCOME; URINARY BLADDER NEOPLASMS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOSYLATION; HUMANS; MALE; MICE; MICE, INBRED ICR; MIDDLE AGED; NEOPLASM STAGING; PHOSPHATIDYLINOSITOL 3-KINASES; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS C-AKT; RETROSPECTIVE STUDIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TREATMENT OUTCOME; URINARY BLADDER NEOPLASMS;

EID: 84954555869     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141253     Document Type: Article

References (38)

1. Pasin E, Josephson DY, Mitra AP, Cote RJ, Stein JP. Superficial bladder cancer: an update on etiology, molecular development, classification, and natural history. Rev Urol. 2008;10:31-43. PMID: 18470273
2. Babjuk M, Burger M, Zigeuner R, Shariat SF, Van Rhijn BWG, Compérat E, et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. Eur Urol. 2013;64:639-53. doi: 10.1016/j.eururo.2013.06.003 PMID: 23827737
3. Miakhil I, Parker SG, Kommu SS, Nethercliffe J. A review of molecular biomarkers for bladder cancer. Int J Med Biomed Res. 2013;2:186-194.
4. Dovedi SJ, Davies BR. Emerging targeted therapies for bladder cancer: a disease waiting for a drug. Cancer Metastasis Rev. 2009;28:355-67. doi: 10.1007/s10555-009-9192-9 PMID: 19997963
5. Ferreira JA, Videira PA, Lima L, Pereira S, Silva M, Carrascal M, et al. Overexpression of tumour-associated carbohydrate antigen sialyl-Tn in advanced bladdertumours. Mol Oncol. 2013;7:719-31. doi: 10.1016/j.molonc.2013.03.001 PMID: 23567325
6. Carrascal MA, Severino PF, Guadalupe Cabral M, Silva M, Ferreira JA, Calais F, et al. Sialyl Tnexpressing bladder cancer cells induce a tolerogenic phenotype in innate and adaptive immune cells. Mol Oncol. 2014;8:753-65. doi: 10.1016/j.molonc.2014.02.008 PMID: 24656965
7. Dall'Olio F, Malagolini N, Trinchera M, Chiricolo M. Mechanisms of cancer-associated glycosylation changes. Front Biosci (Landmark Ed). 2012;17:670-99.
8. Ma H, Zhou H, Song X, Shi S, Zhang J, Jia L. Modification of sialylation is associated with multidrug resistance in human acute myeloid leukemia. Oncogene. 2015;34:726-40. doi: 10.1038/onc.2014.7 PMID: 24531716
9. Porta C, Paglino C, Mosca A. Targeting PI3K/Akt/mTOR Signaling in Cancer. Front Oncol. 2014;4:1-11.
10. Ching CB, Hansel DE. Expanding therapeutic targets in bladder cancer: the PI3K/Akt/mTOR pathway. Lab Invest. Nature Publishing Group; 2010;90:1406-1414.
11. Wu X, Obata T, Khan Q, Highshaw RA, De Vere White R, Sweeney C. The phosphatidylinositol-3 kinase pathway regulates bladder cancer cell invasion. BJU Int. 2004;93:143-150. PMID: 14678387
12. Keniry M, Parsons R. The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene. 2008;27:5477-5485. doi: 10.1038/onc.2008.248 PMID: 18794882
13. Tamura M, Gu J, Tran H, Yamada KM. PTEN gene and integrin signaling in cancer. J Natl Cancer Inst. 1999;91:1820-1828. PMID: 10547389
14. Pinto-Leite R, Arantes-Rodrigues R, Palmeira C, Gaivão I, Cardoso ML, Colaço A, et al. Everolimus enhances gemcitabine-induced cytotoxicity in bladder-cancer cell lines. J Toxicol EnvHeal A. 2012;75:788-99.
15. Munari E, Fujita K, Faraj S, Chaux A, Gonzalez-Roibon N, Hicks J, et al. Dysregulation of mammalian target of rapamycin pathway in upper tract urothelial carcinoma. Hum Pathol. Elsevier Inc.; 2013;44:2668-2676.
16. Nishikawa M, Miyake H, Behnsawy HM, Fujisawa M. Significance of 4E-binding protein 1 as a therapeutic target for invasive urothelial carcinoma of the bladder. Urol Oncol. 2015;33:166.e9-15.
17. Chaux A, Compérat E, Varinot J, Hicks J, Lecksell K, Solus J, et al. High levels of phosphatase and tensin homolog expression are associated with tumor progression, tumor recurrence, and systemic metastases in pt1 urothelial carcinoma of the bladder: A tissue microarray study of 156 patients treated by transurethral resect. Urology. 2013;81:116-122. doi: 10.1016/j.urology.2012.09.007 PMID: 23273076
18. Oliveira PA, Arantes-Rodrigues R, Sousa-Diniz C, Colaço A, Lourenço L, De La Cruz P LF, et al. The effects of sirolimus on urothelial lesions chemically induced in ICR mice by BBN. Anticancer Res. 2009;29:3221-3226. PMID: 19661338
19. Lima L, Severino PF, Silva M, Miranda A, Tavares A, Pereira S et al. Response of high-risk of recurrence/progression bladdertumours expressing sialyl-Tn and sialyl-6-Tto BCG immunotherapy. Br J Cancer. 2013;109:2106-14. doi: 10.1038/bjc.2013.571 PMID: 24064971
20. Vasconcelos-Nóbrega C, Colaço A, Lopes C, Oliveira PA. BBN as an urothelial carcinogen. In Vivo (Brooklyn). 2012;26:727-739.
21. Palmeira C, Oliveira PA, Lameiras C, Amaro T, Silva VM, Lopes C, et al. Biological similarities between murine chemical-induced and natural human bladder carcinogenesis. Oncol Lett. 2010;1:373-377. PMID: 22966311
22. Azevedo R, Ferreira JA, Peixoto A, Neves M, Sousa N, Lima A et al. Emerging antibody-based therapeutic strategies for bladder cancer: A systematic review. J Control Release. 2015;
23. Flucke U, Zirbes T, Schröder W, Mönig S, Koch V, Schmitz K, et al. Expression of mucin-associated carbohydrate core antigens in esophageal squamous cell carcinomas. Anticancer Res. 2001;21:2189-2193. PMID: 11501845
24. Victorzon M, Nordling S, Nilsson O, Roberts P, Haglund C. Sialyl Tn antigen is an independent predictor of outcome in patients with gastric cancer. Int J Cancer. 1996;65:295-300. PMID: 8575847
25. Tsuchiya A, Kikuchi Y, Ando Y, Abe R. Correlation between expression of sialosyl-T antigen and survival in patients with gastric cancer. Br J Surg. 1995;82:960-962. PMID: 7648120
26. Pinho S, Marcos NT, Ferreira B, Carvalho AS, Oliveira MJ, Santos-Silva F, et al. Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett. 2007;249:157-70. PMID: 16965854
27. Julien S, Adriaenssens E, Ottenberg K, Furlan A, Courtand G, Vercoutter-Edouart AS, et al. ST6Gal-NAc I expression in MDA-MB-231 breast cancer cells greatly modifies their O-glycosylation pattern and enhances theirtumourigenicity. Glycobiology. 2006;16:54-64. PMID: 16135558
28. Lin J-C, Liao S-K, Lee E-H, Hung M-S, Sayion Y, Chen H-C, et al. Molecular events associated with epithelial to mesenchymal transition of nasopharyngeal carcinoma cells in the absence of Epstein-Barr virus genome. J Biomed Sci. 2009;16:105. doi: 10.1186/1423-0127-16-105 PMID: 19930697
29. Korkolopoulou P, Levidou G, Trigka EA, Prekete N, Karlou M, Thymara I, et al. A comprehensive immunohistochemical and molecular approach to the PI3K/AKT/mTOR (phosphoinositide 3-kinase/v-akt murine thymoma viral oncogene/mammalian target of rapamycin) pathway in bladder urothelial carcinoma. BJU Int. 2012;110:1237-1248.
30. Fahmy M, Mansure JJ, Brimo F, Yafi FA, Segal R, Althunayan A, et al. Relevance of the mammalian target of rapamycin pathway in the prognosis of patients with high-risk non-muscle invasive bladder cancer. Hum Pathol. Elsevier Inc; 2013;44:1766-1772.
31. Sun CH, Chang YH, Pan CC. Activation of the PI3K/Akt/mTOR pathway correlates with tumour progression and reduced survival in patients with urothelial carcinoma of the urinary bladder. Histopathology. 2011;58:1054-1063. doi: 10.1111/j.1365-2559.2011.03856.x PMID: 21707707
32. Saal LH, Johansson P, Holm K, Gruvberger-Saal SK, She Q-B, Maurer M, et al. Poor prognosis in carcinoma is associated with a gene expression signature of aberrant PTEN tumor suppressor pathway activity. Proc Natl Acad Sci USA. 2007;104:7564-7569. PMID: 17452630
33. Harris L, De La Cerda J, Tuziak T, Rosen D, Xiao L, Shen Y, et al. Analysis of the Expression of Biomarkers in Urinary Bladder Cancer Using a Tissue Microarray. Mol Carcinog. 2008;47:678-685. doi: 10.1002/mc.20420 PMID: 18288642
34. Calderaro J, Rebouissou S, De Koning L, Masmoudi A, Hérault A, Dubois T, et al. PI3K/AKT pathway activation in bladder carcinogenesis. Int J cancer. 2014;134:1776-84. doi: 10.1002/ijc.28518 PMID: 24122582
35. Ferreira J, Bernardo C, Amaro T, Costa C, Lopes P, Silva V, et al. Patient-derived sialyl-Tn positive invasive bladder cancer xenografts in nude mice: An exploratory model study. Eur Urol Suppl. European Association of Urology; 2014;13:e518.
36. Massari F, Ciccarese C, Santoni M, Brunelli M, Conti A, Modena A, Montironi R, Santini D, Cheng L, Martignoni G, Cascinu STG. The route to personalized medicine in bladder cancer: where do we stand? Target Oncol. 2015;
37. Kjeldsen T, Clausen H, Hirohashi S, Ogawa T, Iijima H, Hakomori S. Preparation and characterization of monoclonal antibodies directed to the tumor-associated O-linked sialosyl-2-6 alpha-N-acetylgalactosaminyl (sialosyl-Tn) epitope. Cancer Res. 1988;48:2214-2220. PMID: 2450649
38. Fernandes Eand Ferreira JA, Andreia P, Luís L, Barroso S, Sarmento B, et al. New trends in guided nanotherapies for digestive cancers: A systematic review. J Control Release. 2015;209:288-307. doi: 10.1016/j.jconrel.2015.05.003 PMID: 25957905