Novel robust biomarkers for human bladder cancer based on activation of intracellular signaling pathways

Oncotarget

Volumn 5, Issue 19, 2014, Pages 9022-9032

  Lezhnina, Ksenia ^a,b   Kovalchuk, Olga ^c,d   Zhavoronkov, Alexander A ^b,e,f   Korzinkin, Mikhail B ^a   Zabolotneva, Anastasia A ^g   Shegay, Peter V ^h   Sokov, Dmitry G ⁱ   Gaifullin, Nurshat M ^j,k   Rusakov, Igor G ^h   Aliper, Alexander M ^a,b   Roumiantsev, Sergey A ^b   Alekseev, Boris Y ^h   Borisov, Nikolay M ^l   Buzdin, Anton A ^a,b,g  

^a Pathway Pharmaceuticals Limited   (Hong Kong)

^b Clinical Center of Pediatric Hematology Oncology and Immunology   (Russian Federation)

^c UNIVERSITY OF LETHBRIDGE   (Canada)

^d Canada Cancer and Aging Research Laboratories   (Canada)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^g SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^h P A Herzen Research Oncological Institute   (Russian Federation)

ⁱ Moscow Oncological Hospital No 62   (Russian Federation)

^j LOMONOSOV MOSCOW STATE UNIVERSITY   (Russian Federation)

^k Russian Postgraduate Medical Academy   (Russian Federation)

^l INSTITUTE OF BIOPHYSICS   (Russian Federation)

more..

Author keywords

AUC; Bladder cancer; Gene expression; Intracellular signaling pathway activation; Molecular markers; Transcriptome profiling

Indexed keywords

ACTIN; ANDROGEN RECEPTOR; AROMATIC HYDROCARBON RECEPTOR; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GLUCOCORTICOID RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTEGRIN LINKED KINASE; JANUS KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; MYOSIN; PROTEIN P53; PYRUVIC ACID; RNA POLYMERASE II; SMAD PROTEIN; SOMATOMEDIN C RECEPTOR; STAT PROTEIN; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKER; VASCULOTROPIN; WNT PROTEIN;

ADULT; AGED; ALGORITHM; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; BIOINFORMATICS; BLADDER CANCER; CANCER GROWTH; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DESMOSOME; DNA REPLICATION; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FOCAL ADHESION; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION PROFILING; GLYCOLYSIS; HUMAN; HUMAN TISSUE; INTERMEDIATE FILAMENT; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRESS FIBER; WNT SIGNALING PATHWAY; WOUND HEALING; BIOLOGY; BLADDER; BLADDER TUMOR; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; SIGNAL TRANSDUCTION;

ALGORITHMS; BIOMARKERS, TUMOR; COMPUTATIONAL BIOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTOME; URINARY BLADDER; URINARY BLADDER NEOPLASMS;

EID: 84910070046     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2493     Document Type: Article

References (85)

1. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J Clin, 2005, 2: 74-108.
2. Ploeg M., Aben K.K., Kiemeney L.A. The present and future burden of urinary bladder cancer in the world. World J Urol, 2009, 27: 289-293.
3. Kim W.J., Bae S.C. Molecular biomarkers in urothelial bladder cancer. Cancer Sci, 2008, 99: 646-652.
4. Majewski T., Lee S., Jeong J., Yoon D.S., Kram A., Kim M.S., Tuziak T., Bondaruk J., Lee S., Park W.S., Tang K.S., Chung W., Shen L., Ahmed S.S., Johnston D.A., Grossman H.B., Dinney C.P., Zhou J.H., Harris R.A., Snyder C., Filipek S., Narod S.A., Watson P., Lynch H.T., Gazdar A., Bar-Eli M., Wu X.F., McConkey D.J., Baggerly K., Issa J.P., Benedict W.F., Scherer S.E., Czerniak B. Understanding the development of human bladder cancer by using a whole-organ genomic mapping strategy. Lab Invest, 2008, 88: 694-721.
5. Sánchez-Carbayo M., Cordon-Cardo C. Applications of array technology: identification of molecular targets in bladder cancer. Br J Cancer, 2003, 89: 2172-2177.
6. Moskalev A.A., Aliper A.M., Smit-McBride Z., Buzdin A., Zhavoronkov A. Genetics and epigenetics of aging and longevity. Cell Cycle, 2014, 13:1063-1077.
7. Zabolotneva AA1, Zhavoronkov AA, Shegay PV, Gaifullin NM, Alekseev BY, Roumiantsev SA, Garazha AV, Kovalchuk O, Aravin A, Buzdin AA. A systematic experimental evaluation of microRNA markers of human bladder cancer. Front Genet, 2013, 4:247.
8. Zabolotneva A.A., Zhavoronkov A., Garazha A.V., Roumiantsev S.A., Buzdin A.A. Characteristic patterns of microRNA expression in human bladder cancer. Front Genet, 2013, 3: 310.
9. Aliper A.M., Frieden-Korovkina V.P., Buzdin A., Roumiantsev S.A., Zhavoronkov A. A role for G-CSF and GM-CSF in nonmyeloid cancers. Cancer Med, 2014, 3:737-746.
10. Buzdin A.A., Zhavoronkov A.A., Korzinkin M.B., Venkova L.S., Zenin A.A., Smirnov P.Y., Borisov N.M. Oncofinder, a new method for the analysis of intracellular signaling pathway activation using transcriptomic data. Front Genet, 2014, 5:55.
11. Zhavoronkov A., Buzdin A.A., Garazha A.V., Borisov N.M., Moskalev A.A. Signaling pathway cloud regulation for in silico screening and ranking of the potential geroprotective drugs. Front Genet, 2014, 5:49.
12. Drier Y., Sheffer M., Domany E. Pathway-based personalized analysis of cancer. PNAS, 2013, 110: 6388-6393.
13. Maftouh M., Belo A.I., Avan A., Funel N., Peters G.J., Giovannetti E., Van Die I. Galectin-4 expression is associated with reduced lymph node metastasis and modulation of Wnt/β-catenin signalling in pancreatic adenocarcinoma. Oncotarget, 2014, 5: 5335-5349.
14. Park H.J., Kim S.R., Kim S.S., Wee H.J., Bae M.K., Ryu M.H., Bae S.K. Visfatin promotes cell and tumor growth by upregulating Notch1 in breast cancer. Oncotarget, 2014, 5: 5087-5099.
15. Wang Y., Jin F., Higgins R., McKnight K. The current view for the silencing of the spindle assembly checkpoint. Cell Cycle, 2014, 13: 1694-1701.
16. Morozevich G.E., Kozlova N.I., Ushakova N.A., Preobrazhenskaya M.E., Berman A.E. Integrin a5ß1 simultaneously controls EGFR-dependent proliferation and Akt-dependent pro-survival signaling in epidermoid carcinoma cells. Aging, 2012, 4: 368-374.
17. Zamkova M., Khromova N., Kopnin B.P., Kopnin P. Ras-induced ROS upregulation affecting cell proliferation is connected with cell type-specific alterations of HSF1/SESN3/p21Cip1/WAF1 pathways. Cell Cycle, 2013, 12: 826-836.
18. Spirin P.V., Lebedev T.D., Orlova N.N, Gornostaeva A.S., Prokofjeva M.M., Nikitenko N.A., Dmitriev S.E., Buzdin A.A., Borisov N.M., Aliper A.M., Garazha A.V., Rubtsov P.M., Stocking C., Prassolov V.S. Silencing AML1-ETO gene expression leads to simultaneous activation of both pro-apoptotic and proliferation signaling. Leukemia. 2014, Apr 14 [Epub ahead of print].
19. Buzdin A.A., Zhavoronkov A., Korzinkin M., Roumiantsev S.A., Aliper A.M., Venkova L.S., Smirnov Ph., Borisov N.M. The OncoFinder algorithm for minimizing the errors introduced by the high-throughput methods of transcriptome analysis. Front Mol Biosci, 2014, 1: 8.
20. Borisov N.M., Terekhanova N.V., Aliper A.M., Venkova L.S., Smirnov P.Y., Roumiantsev S., Korzinkin M.B., Zhavoronkov A.A., Buzdin A.A. Signaling pathways activation profiles make better markers of cancer than expression of individual genes. Oncotarget, 2014, In press.
21. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 2003, 19: 185-193.
22. Boyd J.C. Mathematical tools for demonstrating the clinical usefulness of biochemical markers. Scand J Clin Lab Invest Suppl, 1997, 227: 46-63.
23. Cerella C., Teiten M.H., Radogna F., Dicato M., Diederich M. From nature to bedside: Pro-survival and cell death mechanisms as therapeutic targets in cancer treatment. Biotechnol Adv, 2014, 32: 1111-1122.
24. Moilanen E. Two faces of inflammation: an immunopharmacological view. Basic Clin Pharmacol Toxicol, 2014, 114: 2-6.
25. Saeidnia S, Abdollahi M. Antioxidants: friends or foe in prevention or treatment of cancer: the debate of the century. Toxicol Appl Pharmacol, 2013, 271: 49-63.
26. Sun H., Wang Z., Yakisich J.S. Natural products targeting autophagy via the PI3K/Akt/mTOR pathway as anticancer agents. Anticancer Agents Med Chem, 2013, 13: 1048-1056.
27. Sanguedolce F., Bufo P., Carrieri G., Cormio L. Predictive markers in bladder cancer: Do we have molecular markers ready for clinical use? Crit Rev Clin Lab Sci, 2014, 18: 1-14.
28. Mityaev M.V., Kopantzev E.P., Buzdin A.A., Vinogradova T.V., Sverdlov E.D. Enhancer element potentially involved in human survivin gene promoter regulation in lung cancer cell lines. Biochemistry (Mosc), 2010, 75: 182-191.
29. Mityaev M.V, Kopantzev E.P, Buzdin A.A., Vinogradova T.V, Sverdlov E.D. Functional significance of a putative sp1 transcription factor binding site in the survivin gene promoter. Biochemistry (Mosc), 2008, 73: 1183-1191.
30. Chao C.C. Mechanisms of p53 degradation. Clin Chim Acta, 2014, S0009-8981(14)00367-2.
31. Sipos F., Constantinovits M., Muzes G. Intratumoral functional heterogeneity and chemotherapy. World J Gastroenterol, 2014, 20: 2429-2432.
32. Loos B., Engelbrecht A.M., Lockshin R.A., Klionsky D.J., Zakeri Z. The variability of autophagy and cell death susceptibility: Unanswered questions. Autophagy, 2013, 9: 1270-1285.
33. Cotari J.W., Voisinne G., Altan-Bonnet G. Diversity training for signal transduction: leveraging cell-to-cell variability to dissect cellular signaling, differentiation and death. Curr Opin Biotechnol, 2013, 24: 760-766.
34. Bunnell C.A., Shulman L.N. Will we be able to care for cancer patients in the future? Oncology (Williston Park), 2010, 24: 1343-1348.
35. Jain K.K. Challenges of drug discovery for personalized medicine. Curr Opin Mol Ther. 2006, 8: 487-492.
36. Marcel V., Dichtel-Danjoy M.L., Sagne C., Hafsi H., Ma D., Ortiz-Cuaran S., Olivier M., Hall J, Mollereau B, Hainaut P, Bourdon J.C. Biological functions of p53 isoforms through evolution: lessons from animal and cellular models. Cell Death Differ, 2011, 18: 1815-1824.
37. Wiens M. Fundamental mechanisms of apoptosis in the simplest invertebrates, the Porifera. Z Gerontol Geriatr, 2004, 37: 190-199.
38. Green D.M., Swets J.A. Signal detection theory and psychophysics. New York: John Wiley & Sons Ltd, 1966. ISBN 0-471-32420-5.
39. Feng S., Cao Z., Wang X. Role of aryl hydrocarbon receptor in cancer. Biochim Biophys Acta, 2013, 1836:197-210.
40. Hsieh T.H., Tsai C.F., Hsu C.Y., Kuo P.L., Lee J.N., Chai C.Y., Wang S.C., Tsai E.M. Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway. FASEB J, 2012, 26: 778-787.
41. Kim D.W., Gazourian L., Quadri S.A., Romieu-Mourez R., Sherr D.H., Sonenshein G.E. The RelA NF-kappaB subunit and the aryl hydrocarbon receptor (AhR) cooperate to transactivate the c-myc promoter in mammary cells. Oncogene, 2000,19: 5498-5506.
42. Wang F., Samudio I., Safe S. Transcriptional activation of cathepsin D gene expression by 17beta-estradiol: mechanism of aryl hydrocarbon receptor-mediated inhibition. Mol Cell Endocrinol, 2001, 172: 91-103.
43. Nicotra G., Castino R., Follo C., Peracchio C., Valente G., Isidoro C. The dilemma: does tissue expression of cathepsin D reflect tumor malignancy? The question: does the assay truly mirror cathepsin D mis-function in the tumor? Cancer Biomark, 7: 47-64.
44. Nicotra G., Castino R., Follo C., Peracchio C., Valente G., Isidoro C. The dilemma: does tissue expression of cathepsin D reflect tumor malignancy? The question: does the assay truly mirror cathepsin D mis-function in the tumor? Cancer Biomark, 7: 47-64.
45. Janku F., Kaseb A.O., Tsimberidou A.M., Wolff R.A., Kurzrock R. Identification of novel therapeutic targets in the PI3K/AKT/mTOR pathway in hepatocellular carcinoma using targeted next generation sequencing. Oncotarget, 2014, 5: 3012-3022.
46. Ching C.B., Hansel D.E. Expanding therapeutic targets in bladder cancer: the PI3K/Akt/mTOR pathway. Lab Invest, 2010, 90: 1406-1414.
47. Chang C., Lee S.O., Yeh S., Chang T.M. Androgen receptor (AR) differential roles in hormone-related tumors including prostate, bladder, kidney, lung, breast and liver. Oncogene, 2014, 33: 3225-3234.
48. Rahmani A.H., Alzohairy M., Babiker A.Y., Khan A.A., Aly S.M., Rizvi M.A. Implication of androgen receptor in urinary bladder cancer: a critical mini review. Int J Mol Epidemiol Genet, 2013, 4: 150-155.
49. Bhoumik A., Takahashi S., Breitweiser W., Shiloh Y., Jones N., Ronai Z. ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol Cell, 2005, 18: 577-587.
50. Deng X., Ljunggren-Rose A., Maas K., Sriram S. Defective ATM-p53-mediated apoptotic pathway in multiple sclerosis. Ann Neurol, 2005, 58: 577-584.
51. Goeckeler Z.M., Wysolmerski R.B. Myosin phosphatase and cofilin mediate cAMP/cAMP-dependent protein kinase-induced decline in endothelial cell isometric tension and myosin II regulatory light chain phosphorylation. J Biol Chem, 2005, 280: 33083-33095.
52. Taylor S.S., Kim C., Vigil D., Haste N.M., Yang J., Wu J., Anand G.S. Dynamics of signaling by PKA. Biochim Biophys Acta, 2005, 1754: 25-37.
53. Mantamadiotis T., Papalexis N., Dworkin S. CREB signalling in neural stem/progenitor cells: recent developments and the implications for brain tumour biology. Bioessays, 2012, 34: 293-300.
54. Hong S.H., Goh S.H., Lee S.J., Hwang J.A., Lee J., Choi I.J., Seo H., Park J.H., Suzuki H., Yamamoto E., Kim I.H., Jeong J.S., Ju M.H., Lee D.H., Lee Y.S. Upregulation of adenylate cyclase 3 (ADCY3) increases the tumorigenic potential of cells by activating the CREB pathway. Oncotarget, 2013, 4: 1791-1803.
55. Roth M., Johnson P.R., Borger P., Bihl M.P., Rüdiger J.J., King G.G., Ge Q., Hostettler K., Burgess J.K., Black J.L., Tamm M. Dysfunctional interaction of C/EBPalpha and the glucocorticoid receptor in asthmatic bronchial smooth-muscle cells. N Engl J Med, 2004, 351: 560-574.
56. Jamieson C., Sharma M., Henderson B.R. Targeting the β-catenin nuclear transport pathway in cancer. Semin Cancer Biol, 2014, 27C: 20-29.
57. Oishi N., Yamashita T., Kaneko S. Molecular biology of liver cancer stem cells. Liver Cancer, 2014, 3: 71-84.
58. González-Moles M.A., Ruiz-ávila I., Gil-Montoya J.A., Plaza-Campillo J., Scully C. β-Catenin in oral cancer: An update on current knowledge. Oral Oncol, 2014, 50: 818-824.
59. Keith B., Johnson R.S., Simon M.C. HIF1a and HIF2a: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer, 2011, 12: 9-22.
60. Singh P., Alex J.M., Bast F. Insulin receptor (IR) and insulin-like growth factor receptor 1 (IGF-1R) signaling systems: novel treatment strategies for cancer. Med Oncol, 2014, 31: 805.
61. Chen H.X., Sharon E. IGF-1R as an anti-cancer target-trials and tribulations. Chin J Cancer, 2013, 32: 242-252.
62. Hannigan G., Troussard A.A., Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer, 2005, 5: 51-63.
63. Edwards L.A., Shabbits J.A., Bally M., Dedhar S. Integrin-linked kinase (ILK) in combination molecular targeting. Cancer Treat Res, 2004, 119: 59-75.
64. Fielding A.B., Dedhar S. The mitotic functions of integrin-linked kinase. Cancer Metastasis Rev, 2009, 28: 99-111.
65. Qin J., Wu C. ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling. Curr Opin Cell Biol, 2012, 24: 607-613.
66. Cordes N., van Beuningen D. Cell adhesion to the extracellular matrix protein fibronectin modulates radiation-dependent G2 phase arrest involving integrin-linked kinase (ILK) and glycogen synthase kinase-3beta (GSK-3beta) in vitro. Br J Cancer, 2003, 88: 1470-1479.
67. Peters D.J., Cammans M., Smit S., Spek W., van Lookeren Campagne M.M., Schaap P. Control of cAMP-induced gene expression by divergent signal transduction pathways. Dev Genet, 1991, 12: 25-34.
68. Incerpi S., Scapin S., D'Arezzo S., Spagnuolo S., Leoni S. Short-term effects of thyroid hormone in prenatal development and cell differentiation. Steroids, 2005, 70: 434-443.
69. Yoon M.J., Lee A.R., Jeong S.A., Kim Y.S., Kim J.Y., Kwon Y.J., Choi K.S. Release of Ca2+ from the endoplasmic reticulum and its subsequent influx into mitochondria trigger celastrol-induced paraptosis in cancer cells. Oncotarget, 2014, Jul 25 [Epub ahead of print].
70. Poehlmann T.G., Busch S., Mussil B., Winzer H., Weinert J., Mebes I., Schaumann A., Fitzgerald J.S., Markert U.R. The possible role of the Jak/STAT pathway in lymphocytes at the fetomaternal interface. Chem Immunol Allergy, 2005, 89: 26-35.
71. Grote K., Luchtefeld M., Schieffer B. JANUS under stress-role of JAK/STAT signaling pathway in vascular diseases. Vascul Pharmacol, 2005, 43: 357-363.
72. Zhang H.F., Lai R. STAT3 in Cancer-Friend or Foe? Cancers (Basel). 2014, 6: 1408-1440.
73. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell, 2006, 12: 471-484.
74. O'Reilly K.E., Rojo F., She Q.B., Solit D., Mills G.B., Smith D., Lane H., Hofmann F., Hicklin D.J., Ludwig D.L., Baselga J., Rosen N. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res, 2006, 66: 1500-1508.
75. Francoz S., Froment P., Bogaerts S., De Clercq S., Maetens M., Doumont G., Bellefroid E., Marine J.C. Mdm4 and Mdm2 cooperate to inhibit p53 activity in proliferating and quiescent cells in vivo. PNAS, 2006, 103: 3232-3237.
76. Ho C.C., Siu W.Y., Lau A., Chan W.M., Arooz T., Poon R.Y. Stalled replication induces p53 accumulation through distinct mechanisms from DNA damage checkpoint pathways. Cancer Res, 2006, 66: 2233-2241.
77. Sanders L.C., Matsumura F., Bokoch G.M., de Lanerolle P. Inhibition of myosin light chain kinase by p21-activated kinase. Science, 1999, 283: 2083-2085.
78. Geiduschek E.P., Kassavetis G.A. Transcription: adjusting to adversity by regulating RNA polymerase. Curr Biol, 2006, 16: R849-R851.
79. Wicks S.J., Lui S., Abdel-Wahab N., Mason R.M., Chantry A. Inactivation of smad-transforming growth factor beta signaling by Ca(2+)-calmodulin-dependent protein kinase II. Mol Cell Biol, 2000, 20: 8103-8111.
80. Xu J., Attisano L. Mutations in the tumor suppressors Smad2 and Smad4 inactivate transforming growth factor beta signaling by targeting Smads to the ubiquitin-proteasome pathway. PNAS, 2000, 97: 4820-4825.
81. Moustakas A., Pardali K., Gaal A., Heldin C.H. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol Lett, 2002, 82: 85-91.
82. López-Sáez J.F., de la Torre C., Pincheira J., Giménez-Martín G. Cell proliferation and cancer. Histol Histopathol, 1998, 13: 1197-1214.
83. Wierstra I. The transcription factor FOXM1 (Forkhead box M1): proliferation-specific expression, transcription factor function, target genes, mouse models, and normal biological roles. Adv Cancer Res, 2013, 118: 97-398.
84. Matsumoto T., Claesson-Welsh L. VEGF receptor signal transduction. Sci STKE, 2001, 2001: re21.
85. Jamieson C., Sharma M., Henderson B.R. Targeting the β-catenin nuclear transport pathway in cancer. Semin Cancer Biol, 2014, 27C: 20-29.