Biopolym. Cell. 2011; 27(1):25-35.
http://dx.doi.org/10.7124/bc.00007E
Reviews
Genetic and epigenetic changes of genes on chromosome 3 in human urogenital tumors
1Gordiyuk V. V.
  1. Institute of Molecular Biology and Genetics, NAS of Ukraine
    150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

Numerous disorders of genes and alterations of their expression are observed on a short arm of human chromosome 3, particularly in 3p14, 3p21, 3p24 compact regions in epithelial tumors. These aberrations affect the key biological processes specific for cancerogenesis. Such genes or their products could be used for diagnostics and prognosis of cancer. Genetical and epigenetical changes of a number of genes on chromosome 3 in human urogenital cancer, their role in cellular processes and signal pathways and perspectives as molecular markers of cancer diseases are analyzed in the review
Keywords: human chromosome 3, tumor suppressor genes, DNA methylation, microRNA, urogenital cancer, molecular oncomarker
Full text: (PDF, in English) (PDF, in Russian)

References

[1] Lubinski J., Hadaczek P., Podolski J., Toloczko A., Sikorski A., McCue P., Druck T., Huebner K. Common regions of deletion in chromosome regions 3p12 and 3p14.2 in primary clear cell renal carcinomas Cancer Res 1994 54, N 14 P. 3710–3713.
[2] Gordiyuk V. V. Genetic and epigenetic changes in malignant cells of tumors of urogenital organs Biopolym. Cell 2010 26, N 6 P. 450– 460.
[3] van Gils W., Kilic E., Bruggenwirth H. T., Vaarwater J., Verbiest M. M., Beverloo B., van Til-Berg M. E., Paridaens D., Luyten G. P., de Klein A. Regional deletion and amplification on chromosome 6 in a uveal melanoma case without abnormalities on chromosomes 1p, 3 and 8 Melanoma Res 2008 18, N 1 P. 10–15.
[4] Darai-Ramqvist E., Sandlund A., Muller S., Klein G., Imreh S., Kost-Alimova M. Segmental duplications and evolutionary plasticity at tumor chromosome break-prone regions Genome Res 2008 18, N 3 P. 370–379.
[5] Wang X., Zheng B., Zhang R. R., Li S., Chen X., Mulvihill J. J., Lu X., Pang H., Liu H. Automated analysis of fluorescent in situ hybridization (FISH) labeled genetic biomarkers in assisting cervical cancer diagnosis Technol. Cancer Res. Treat 2010 9, N 3 P. 231–242.
[6] Yoshimoto T., Matsuura K., Karnan S., Tagawa H., Nakada C., Tanigawa M., Tsukamoto Y., Uchida T., Kashima K., Akizuki S., Takeuchi I., Sato F., Mimata H., Seto M., Moriyama M. High-resolution analysis of DNA copy number alterations and gene expression in renal clear cell carcinoma J. Pathol 2007 213, N 4 P. 392–401.
[7] Hadaczek P., Podolski J., Toloczko A., Kurzawski G., Sikorski A., Rabbitts P., Huebner K., Lubinski J. Losses at 3p common deletion sites in subtypes of kidney tumours: histopathological correlations Virchows Arch 1996 429, N 1 P. 37–42.
[8] Durkin S. G., Ragland R. L., Arlt M. F., Mulle J. G., Warren S. T., Glover T. W. Replication stress induces tumor-like microdeletions in FHIT/FRA3B Proc. Natl Acad. Sci. USA 2008 105, N 1 P. 246–251.
[9] Hintzy M. C., Camparo P., Vasiliu V., Peyromaure M., Vieillefond A. Renal carcinoma associated with MiTF/TFE translocation: report of six cases in young adults Prog. Urol 2008. 18, N 5 P. 275–280.
[10] Cody N. A., Ouellet V., Manderson E. N., Quinn M. C., FilaliMouhim A., Tellis P., Zietarska M., Provencher D. M., MesMasson A. M., Chevrette M., Tonin P. N. Transfer of chromosome 3 fragments suppresses tumorigenicity of an ovarian cancer cell line monoallelic for chromosome 3p Oncogene 2007 26, N 4 P. 618–632.
[11] Hong F. Z., Wang B., Li H. M., Liew C. T. Hypermethylation of fragile histidine triad gene and 3p14 allelic deletion in ovarian carcinomas Zhonghua Bing Li Xue Za Zhi 2005 34, N 5 P. 257–261.
[12] Fouts R. L., Sandusky G. E., Zhang S., Eckert G. J., Koch M. O., Ulbright T. M., Eble J. N., Cheng L. Down-regulation of fragile histidine triad expression in prostate carcinoma Cancer 2003 97, N 6 P. 1447–1452.
[13] Cross N. A., Chandrasekharan S., Jokonya N., Fowles A., Hamdy F. C., Buttle D. J., Eaton C. L. The expression and regulation of ADAMTS-1, -4, -5, -9, and -15, and TIMP-3 by TGFbeta1 in prostate cells: relevance to the accumulation of versican Prostate 2005 63, N 3 P. 269–275.
[14] Banham A. H., Beasley N., Campo E., Fernandez P. L., Fidler C., Gatter K., Jones M., Mason D. Y., Prime J. E., Trougouboff P., Wood K., Cordell J. L. The FOXP1 winged helix transcription factor is a novel candidate tumor suppressor gene on chromosome 3p Cancer Res 2001 61, N 24 P. 8820–8829.
[15] Taylor B. S., Schultz N., Hieronymus H., Gopalan A., Xiao Y., Carver B. S., Arora V. K., Kaushik P., Cerami E., Reva B., Antipin Y., Mitsiades N., Landers T., Dolgalev I., Major J. E., Wilson M., Socci N. D., Lash A. E., Heguy A., Eastham J. A., Scher H. I., Reuter V. E., Scardino P. T., Sander C., Sawyers C. L., Gerald W. L. Integrative genomic profiling of human prostate cancer Cancer Cell 2010 18, N 1 P. 11–22.
[16] Kanjanavirojkul N., Limpaiboon T., Patarapadungkit N., Yuenyao P., Pairojkul C. Chromosome 3p alterations in northeastern Thai women with cervical carcinoma Asian. Pac. J. Cancer Prev 2005 6, N 4 P. 501–504.
[17] Ki K. D., Lee S. K., Tong S. Y., Lee J. M., Song D. H., Chi S. G. Role of 5'-CpG island hypermethylation of the FHIT gene in cervical carcinoma J. Gynecol. Oncol 2008 19, N 2 P. 117–122.
[18] Kashuba V. I., Skripkina I. Ia., Saraev D. V., Gordiiuk V. V., Vinnitskaia A. B., Tsyba L. A., Pogrebnoi P. V., Blinov V. M., Zabarovskii E. R., Ryndich A. V. Identification of changes in gene loci potentially associated with cervical cancer using NotI microarrays Ukr. Biokhim. Zh 2006 78, N 2 P. 113–120.
[19] Gordiyuk V. V., Gerashchenko G. V., Skrypkina I. Ya., Simonchuk O. V., Pavlova T. V., Ugrin D. D., Manzhura E. P., Vakulenko G. O., Zabarovsky E. R., Rynditch A. V., Kashuba V. I. Identification of chromosome 3 epigenetic and genetic abnormalities and gene expression changes in ovarian cancer Biopolym. Cell 2008 24, N 4 P. 223–332.
[20] Loginov V. I., Bazov I. V., Khodyrev D. S., Pronina I. V., Kazubskaia T. P., Ermilova V. D., Gar'kavtseva R. F., Zbarovskii E. R., Braga E. A. Human chromosome 3P regions of putative tumor-suppressor genes in renal, breast, and ovarian carcinomas Russian Journal of Genetics 2008 44, N 2 P. 209-214.
[21] Angeloni D. Molecular analysis of deletions in human chromosome 3p21 and the role of resident cancer genes in disease Brief. Funct. Genomic Proteomic 2007 6, N 1 P. 19–39.
[22] Pfeifer G. P., Dammann R. Methylation of the tumor suppressor gene RASSF1A in human tumors Biochemistry (Mosc) 2005 70, N 5 P. 576–583.
[23] Shaheduzzaman S., Vishwanath A., Furusato B., Cullen J., Chen Y., Bacez L., Nau M., Ravindranath L., Kim K. H., Mohammed A., Chen Y., Ehrich M., Srikantan V., Sesterhenn I. A., McLeod D., Vahey M., Petrovics G., Dobi A., Srivastava S. Silencing of Lactotransferrin expression by methylation in prostate cancer progression Cancer. Biol. Ther 2007 6, N 7 P. 1088–1095.
[24] Loginov V. I., Khodyrev D. S., Pronina I. V., Kazubskaia T. P., Ermilova V. D., Gar'kavtseva R. F., Braga E. A. Methylation of promoter region of RASSF1A gene and frequencies of allelic imbalances in chromosome 3 critical regions are correlated with progression of clear cell renal cell carcinoma Mol. Biol. 2009 43, N 3 P. 394-402.
[25] Awakura Y., Nakamura E., Ito N., Kamoto T., Ogawa O. Methylation-associated silencing of TU3A in human cancers Int. J. Oncol 2008 33, N 4 P. 893–899.
[26] Li J., Wang F., Haraldson K., Protopopov A., Duh F. M., Geil L., Kuzmin I., Minna J. D., Stanbridge E., Braga E., Kashuba V. I., Klein G., Lerman M. I., Zabarovsky E. R. Functional characterization of the candidate tumor suppressor gene NPRL2/G21 located in 3p21.3C Cancer Res 2004 64, N 18 P. 6438–6443.
[27] Rubio-Del-Campo A., Salinas-Sanchez A. S., Sanchez-Sanchez F., Gimenez-Bachs J. M., Donate-Moreno M. J., Pastor-Navarro H., Carrion-Lypez P., Escribano J. Implications of mismatch repair genes hMLH1 and hMSH2 in patients with sporadic renal cell carcinoma BJU Int 2008 102, N 4 P. 504–509.
[28] Arai E., Ushijima S., Tsuda H., Fujimoto H., Hosoda F., Shibata T., Kondo T., Imoto I., Inazawa J., Hirohashi S., Kanai Y. Genetic clustering of clear cell renal cell carcinoma based on array-comparative genomic hybridization: its association with DNA methylation alteration and patient outcome Clin. Cancer Res 2008 14, N 17 P. 5531–5539.
[29] Senchenko V., Liu J., Braga E., Mazurenko N., Loginov W., Seryogin Y., Bazov I., Protopopov A., Kisseljov F. L., Kashuba V., Lerman M. I., Klein G., Zabarovsky E. R. Deletion mapping using quantitative real-time PCR identifies two distinct 3p21.3 regions affected in most cervical carcinomas Oncogene 2003 22, N 19 P. 2984–2992.
[30] Lai H. C., Lin Y. W., Chang C. C., Wang H. C., Chu T. W., Yu M. H., Chu T. Y. Hypermethylation of two consecutive tumor suppressor genes, BLU and RASSF1A, located at 3p21.3 in cervical neoplasias Gynecol. Oncol 2007 104, N 3 P. 629–635.
[31] Zhang H., Zhang S., Cui J., Zhang A., Shen L., Yu. H. Expression and promoter methylation status of mismatch repair gene hMLH1 and hMSH2 in epithelial ovarian cancer Aust. NZJ Obstet. Gynaecol 2008 48, N 5 P. 505–509.
[32] Kwong J., Lee J. Y., Wong K. K., Zhou X., Wong D. T., Lo K. W., Welch W. R., Berkowitz R. S., Mok S. C. Candidate tumorsuppressor gene DLEC1 is frequently downregulated by promoter hypermethylation and histone hypoacetylation in human epithelial ovarian cancer Neoplasia 2006 8, N 4 P. 268–278.
[33] Birch A. H., Quinn M. C., Filali-Mouhim A., Provencher D. M., Mes-Masson A. M., Tonin P. N. Transcriptome analysis of serous ovarian cancers identifies differentially expressed chromosome 3 genes Mol. Carcinog 2008 47, N 1 P. 56–65.
[34] de Caceres I., Battagli C., Esteller M., Herman J. G., Dulaimi E., Edelson M. I., Bergman C., Ehya H., Eisenberg B. L., Cairns P. Tumor cell-specific BRCA1 and RASSF1A hypermethylation in serum, plasma, and peritoneal fluid from ovarian cancer patients Cancer Res 2004 64, N 18 P. 6476– 6481.
[35] Nykopp T. K., Rilla K., Sironen R., Tammi M. I., Tammi R. H., Hamalainen K., Heikkinen A. M., Komulainen M., Kosma V. M., Anttila M. Expression of hyaluronan synthases (HAS1-3) and hyaluronidases (HYAL1-2) in serous ovarian carcinomas: inverse correlation between HYAL1 and hyaluronan content BMC Cancer 2009 12, N 9 P. 143.
[36] Salama M. E., Worsham M. J., DePeralta-Venturina M. Malignant papillary renal tumors with extensive clear cell change: a molecular analysis by microsatellite analysis and fluorescence in situ hybridization Arch. Pathol. Lab. Med 2003 127, N 9 P. 1176–1181.
[37] Guo Z., Wu F., Asplund A., Hu X., Mazurenko N., Kisseljov F., Ponten J., Wilander E. Analysis of intratumoral heterogeneity of chromosome 3p deletions and genetic evidence of polyclonal origin of cervical squamous carcinoma Mod. Pathol 2001 14, N 2 P. 54–61.
[38] Muller I., Urban K., Pantel K., Schwarzenbach H. Comparison of genetic alterations detected in circulating microsatellite DNA in blood plasma samples of patients with prostate cancer and benign prostatic hyperplasia Ann. N. Y. Acad. Sci 2006 1075 P. 222–229.
[39] Haudenschild D. R., Curtiss S. B., Moseley T. A., Reddi A. H. Generation of interleukin-17 receptor-like protein (IL-17RL) in prostate by alternative splicing of RNA Prostate 2006 66, N 12 P. 1268–1274.
[40] Balachandar V., Kumar B. L., Sasikala K., Manikantan P., Sangeetha R., Devi S. M. Identification of a high frequency of chromosomal rearrangements in the centromeric regions of prostate cancer patients J. Zhejiang Univ. Sci. B 2007 8, N 9 P. 638–646.
[41] Dasgupta S., Chakraborty S. B., Roy A., Roychowdhury S., Panda C. K. Differential deletions of chromosome 3p are associated with the development of uterine cervical carcinoma in Indian patients Mol. Pathol 2003 56, N 5 P. 263–269.
[42] Braga E., Senchenko V., Bazov I., Loginov W., Liu J., Ermilova V., Kazubskaya T., Garkavtseva R., Mazurenko N., Kisseljov F., Lerman M. I., Klein G., Kisselev L., Zabarovsky E. R. Critical tumor-suppressor gene regions on chromosome 3P in major human epithelial malignancies: allelotyping and quantitative real-time PCR Int. J. Cancer 2002 100, N 5 P. 534–541.
[43] Rokman A., Baffoe-Bonnie A. B., Gillanders E., Fredriksson H., Autio V., Ikonen T., Gibbs K. D., Jr., Jones M., Gildea D., Freas-Lutz D., Markey C., Matikainen M. P., Koivisto P. A., Tammela T. L., Kallioniemi O. P., Trent J., Bailey-Wilson J. E., Schleutker J. Hereditary prostate cancer in Finland: finemapping validates 3p26 as a major predisposition locus Hum Genet 2005 116, N 1–2 P. 43–50.
[44] Voelter-Mahlknecht S., Ho A. D., Mahlknecht U. Chromosomal organization and localization of the novel class IV human histone deacetylase 11 gene Int. J. Mol. Med 2005 16, N 4 P. 589–598.
[45] Villagra A., Cheng F., Wang H. W., Suarez I., Glozak M., Maurin M., Nguyen D., Wright K. L., Atadja P. W., Bhalla K., Pinilla-Ibarz J., Seto E., Sotomayor E. M. The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance Nat. Immunol 2009 10, N 1 P. 92–100.
[46] Wilting S. M., de Wilde J., Meijer C. J., Berkhof J., Yi Y., van Wieringen W. N., Braakhuis B. J., Meijer G. A., Ylstra B., Snijders P. J., Steenbergen R. D. Integrated genomic and transcriptional profiling identifies chromosomal loci with altered gene expression in cervical cancer Genes Chromosomes Cancer 2008 47, N 10 P. 890–905.
[47] Goyama S., Nitta E., Yoshino T., Kako S., Watanabe-Okochi N., Shimabe M., Imai Y., Takahashi K., Kurokawa M. EVI-1 interacts with histone methyltransferases SUV39H1 and G9a for transcriptional repression and bone marrow immortalization Leukemia 2010 24, N 1 P. 81–88.
[48] Andersson S., Sowjanya P., Wangsa D., Hjerpe A., Johansson B., Auer G., Gravitt P. E., Larsson C., Wallin K. L., Ried T., Heselmeyer-Haddad K. Detection of genomic amplification of the human telomerase gene TERC, a potential marker for triage of women with HPV-positive, abnormal Pap smears Am. J. Pathol 2009 175, N 5 P. 1831–1847.
[49] Woenckhaus J., Steger K., Sturm K., Kunstedt K., Franke F. E., Fenic I. Prognostic value of PIK3CA and phosphorylated AKT expression in ovarian cancer Virchows Arch 2007 450, N 4 P. 387–395.
[50] Sattler H. P., Lensch R., Rohde V., Zimmer E., Meese E., Bonkhoff H., Retz M., Zwergel T., Bex A., Stoeckle M., Wullich B. Novel amplification unit at chromosome 3q25-q27 in human prostate cancer Prostate 2000 45, N 3 P. 207– 215.
[51] Jung V., Kindich R., Kamradt J., Jung M., Muller M., Schulz W. A., Engers R., Unteregger G., Stockle M., Zimmermann R., Wullich B. Genomic and expression analysis of the 3q25-q26 amplification unit reveals TLOC1/SEC62 as a probable target gene in prostate cancer Mol. Cancer Res 2006 4, N 3 P. 169–176.
[52] Peters D. G., Kudla D. M., Deloia J. A., Chu T. J., Fairfull L., Edwards R. P., Ferrell R. E. Comparative gene expression analysis of ovarian carcinoma and normal ovarian epithelium by serial analysis of gene expression Cancer Epidemiol. Biomarkers Prev 2005 14, N 7 P. 1717–1723.
[53] Feng Q., Balasubramanian A., Hawes S. E., Toure P., Sow P. S., Dem A., Dembele B., Critchlow C. W., Xi L., Lu H., McIntosh M. W., Young A. M., Kiviat N. B. Detection of hypermethylated genes in women with and without cervical neoplasia J. Natl Cancer Inst 2005 97, N 4 P. 273–282.
[54] Choi C. H., Lee K. M., Choi J. J., Kim T. J., Kim W. Y., Lee J. W., Lee S. J., Lee J. H., Bae D. S., Kim B. G. Hypermethylation and loss of heterozygosity of tumor suppressor genes on chromosome 3p in cervical cancer Cancer Lett 2007 255, N 1–P. 26–33.
[55] Anedchenko E. A., Kiseleva N. P., Dmitriev A. A., Kiselev F. L., Zabarovskii E. R., Senchenko V. N. Tumor suppressor gene RBSP3 in cervical carcinoma: copy number and transcriptional level Mol. Biol. (Mosk) 2007 41, N 1:77-85 .
[56] Kuroki T., Trapasso F., Yendamuri S., Matsuyama A., Alder H., Mori M., Croce C. M. Allele loss and promoter hypermethylation of VHL, RAR-beta, RASSF1A, and FHIT tumor suppressor genes on chromosome 3p in esophageal squamous cell carcinoma Cancer Res 2003 63, N 13 P. 3724– 3728.
[57] Zhang L., Volinia S., Bonome T., Calin G. A., Greshock J., Yang N., Liu C. G., Giannakakis A., Alexiou P., Hasegawa K., Johnstone C. N., Megraw M. S., Adams S., Lassus H., Huang J., Kaur S., Liang S., Sethupathy P., Leminen A., Simossis V. A., Sandaltzopoulos R., Naomoto Y., Katsaros D., Gimotty P. A., DeMichele A., Huang Q., Butzow R., Rustgi A. K., Weber B. L., Birrer M. J., Hatzigeorgiou A. G., Croce C. M., Coukos G. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer Proc. Natl Acad. Sci. USA 2008 105, N 19 P. 7004–7009.
[58] Theodore S. C., Rhim J. S., Turner T., Yates C. MiRNA 26a expression in a novel panel of African American prostate cancer cell lines Ethn. Dis 2010 20, N 1 P. 96–100.
[59] Wang G., Wang Y., Feng W., Wang X., Yang J. Y., Zhao Y., Wang Y., Liu Y. Transcription factor and microRNA regulation in androgen-dependent and -independent prostate cancer cells BMC Genomics 2008 16, N 9 P. 22.
[60] Juan D., Alexe G., Antes T., Liu H., Madabhushi A., Delisi C., Ganesan S., Bhanot G., Liou L. S. Identification of a microRNA panel for clear-cell kidney cancer Urology 2010 75, N 4 P. 835–841.
[61] Shen J., DiCioccio R., Odunsi K., Lele S. B., Zhao H. Novel genetic variants in miR-191 gene and familial ovarian cancer BMC Cancer 2010 18, N 10 P. 47.
[62] Lui W. O., Pourmand N., Patterson B. K., Fire A. Patterns of known and novel small RNAs in human cervical cancer Cancer Res 2007 67, N 13 P. 6031–6043.
[63] Altuvia Y., Landgraf P., Lithwick G., Elefant N., Pfeffer S., Aravin A., Brownstein M. J., Tuschl T., Margalit H. Clustering and conservation patterns of human microRNAs Nucl. Acids Res 2005 33, N 8 P. 2697–2706.
[64] Goatly A., Bacon C. M., Nakamura S., Ye H., Kim I., Brown P. J., Ruskone-Fourmestraux A., Cervera P., Streubel B., Banham A. H., Du M. Q. FOXP1 abnormalities in lymphoma: translocation breakpoint mapping reveals insights into deregulated transcriptional control Mod. Pathol 2008 21, N 7 P. 902–911.
[65] Hua K., Din J., Cao Q., Feng W., Zhang Y., Yao L., Huang Y., Zhao Y., Feng Y. Estrogen and progestin regulate HIF-1alpha expression in ovarian cancer cell lines via the activation of Akt signaling transduction pathway Oncol. Rep 2009 21, N 4 P. 893–898.
[66] Lee S., Garner E. I., Welch W. R., Berkowitz R. S., Mok S. C. Over-expression of hypoxia-inducible factor 1 alpha in ovarian clear cell carcinoma Gynecol. Oncol 2007 106, N 2 P. 311–317.
[67] Fenwick C., Na S. Y., Voll R. E., Zhong H., Im S. Y., Lee J. W., Ghosh S. A subclass of Ras proteins that regulate the degradation of IkappaB Science 2000 287, N 5454 P. 869–873.
[68] Tokinaga K., Okuda H., Nomura A., Ashida S., Furihata M., Shuin T. Hypermethylation of the RASSF1A tumor suppressor gene in Japanese clear cell renal cell carcinoma Oncol. Rep 2004 12, N 4 P. 805–810.
[69] Thaler S., Hahnel P. S., Schad A., Dammann R., Schuler M. RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEKERK pathway and inhibition of Akt Cancer Res 2009 69, N 5 P. 1748–1757.
[70] Winn R. A., Van Scoyk M., Hammond M., Rodriguez K., Crossno J. T., Jr., Heasley L. E., Nemenoff R. A. Antitumorigenic effect of Wnt 7a and Fzd 9 in non-small cell lung cancer cells is mediated through ERK-5-dependent activation of peroxisome proliferator-activated receptor gamma J. Biol. Chem 2006 281, N 37 P. 26943–26950.
[71] Yamadori T., Baba Y., Matsushita M., Hashimoto S., Kurosaki M., Kurosaki T., Kishimoto T., Tsukada S. Bruton's tyrosine kinase activity is negatively regulated by Sab, the Btk-SH3 domain-binding protein Proc. Natl Acad. Sci. USA 1999 96, N 11 P. 6341–6346.
[72] Kashuba V. I., Li J., Wang F., Senchenko V. N., Protopopov A., Malyukova A., Kutsenko A. S., Kadyrova E., Zabarovska V. I., Muravenko O. V., Zelenin A. V., Kisselev L. L., Kuzmin I., Minna J. D., Winberg G., Ernberg I., Braga E., Lerman M. I., Klein G., Zabarovsky E. R. RBSP3 (HYA22) is a tumor suppressor gene implicated in major epithelial malignancies Proc. Natl Acad. Sci. USA 2004 101, N 14–P. 4906–4911.
[73] Otsubo T., Akiyama Y., Yanagihara K., Yuasa Y. SOX2 is frequently downregulated in gastric cancers and inhibits cell growth through cell-cycle arrest and apoptosis Br. J. Cancer 2008 98, N 4 P. 824–831.
[74] Wellbrock C., Rana S., Paterson H., Pickersgill H., Brummelkamp T., Marais R. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF PLoS One 2008 3, N 7 P. e2734.
[75] Zhou Y., Zeng Z., Zhang W., Xiong W., Wu M., Tan Y., Yi W., Xiao L., Li X., Huang C., Cao L., Tang K., Li X., Shen S., Li G. Lactotransferrin: a candidate tumor suppressor-deficient expression in human nasopharyngeal carcinoma and inhibition of NPC cell proliferation by modulating the mitogen-activated protein kinase pathway Int. J. Cancer 2008 123, N 9 P. 2065–2072.
[76] Semba S., Trapasso F., Fabbri M., McCorkell K. A., Volinia S., Druck T., Iliopoulos D., Pekarsky Y., Ishii H., Garrison P. N., Barnes L. D., Croce C. M., Huebner K. Fhit modulation of the Akt-survivin pathway in lung cancer cells: Fhit-tyrosine 114 (Y114) is essential Oncogene 2006 25, N 20 P. 2860–2872.
[77] Kurata A., Katayama R., Watanabe T., Tsuruo T., Fujita N. TUSC4/NPRL2, a novel PDK1-interacting protein, inhibits PDK1 tyrosine phosphorylation and its downstream signaling Cancer Sci 2008 99, N 9 P. 1827–1834.
[78] Takayama K., Horie-Inoue K., Ikeda K., Urano T., Murakami K., Hayashizaki Y., Ouchi Y., Inoue S. FOXP1 is an androgen-responsive transcription factor that negatively regulates androgen receptor signaling in prostate cancer cells Biochem. Biophys. Res. Communs 2008 374, N 2 P. 388– 393.
[79] Chen X., Han S., Wang S., Zhou X., Zhang M., Dong J., Shi X., Qian N., Wang X., Wei Q., Shen H., Hu Z. Interactions of IL12A and IL-12B polymorphisms on the risk of cervical cancer in Chinese women Clin. Cancer Res 2009 15, N 1 P. 400–405.
[80] Dangi-Garimella S., Yun J., Eves E. M., Newman M., Erkeland S. J., Hammond S. M., Minn A. J., Rosner M. R. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7 EMBO J 2009 28, N 4 P. 347–358.
[81] Witwer K. W., Sisk J. M., Gama L., Clements J. E. MicroRNA regulation of IFN-beta protein expression: rapid and sensitive modulation of the innate immune response J. Immunol 2010 184, N 5 P. 2369–2376.
[82] Willner J., Wurz K., Allison K. H., Galic V., Garcia R. L., Goff B. A., Swisher E. M. Alternate molecular genetic pathways in ovarian carcinomas of common histological types Hum. Pathol 2007 38, N 4 P. 607–613.
[83] Balch C., Huang T. H., Brown R., Nephew K. P. The epigenetics of ovarian cancer drug resistance and resensitization Am. J. Obstet. Gynecol 2004 191, N 5 P. 1552–1572.
[84] Hara T., Noma T., Yamashiro Y., Naito K., Nakazawa A. Quantitative analysis of telomerase activity and telomerase reverse transcriptase expression in renal cell carcinoma Urol. Res 2001 29, N 1 P. 1–6.
[85] Bantis A., Patsouris E., Gonidi M., Kavantzas N., Tsipis A., Athanassiadou A. M., Aggelonidou E., Athanassiadou P. Telomerase RNA expression and DNA ploidy as prognostic markers of prostate carcinomas Tumori 2009 95, N 6 P. 744–752.
[86] Schaefer A., Jung M., Mollenkopf H. J., Wagner I., Stephan C., Jentzmik F., Miller K., Lein M., Kristiansen G., Jung K. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma Int. J. Cancer 2010 126, N 5 P. 1166–1176.
[87] Wiley A., Katsaros D., Chen H., de la Longrais R. I. A., Beeghly A., Puopolo M., Singal R., Zhang Y., Amoako A., Zelterman D., Yu H. Aberrant promoter methylation of multiple genes in malignant ovarian tumors and in ovarian tumors with low malignant potential Cancer 2006 107, N 2 P. 299– 308.
[88] Chan M. W., Wei S. H., Wen P., Wang Z., Matei D. E., Liu J. C., Liyanarachchi S., Brown R., Nephew K. P., Yan P. S., Huang T. H. Hypermethylation of 18S and 28S ribosomal DNAs predicts progression-free survival in patients with ovarian cancer Clin. Cancer Res 2005 11, N 20 P. 7376–7383.
[89] Nanjundan M., Nakayama Y., Cheng K. W., Lahad J., Liu J., Lu K., Kuo W. L., Smith-McCune K., Fishman D., Gray J. W., Mills G. B. Amplification of MDS1/EVI1 and EVI1, located in the 3q26.2 amplicon, is associated with favorable patient prognosis in ovarian cancer Cancer Res 2007 67, N 7 P. 3074–3084.
[90] Grady W. M. Epigenetic events in the colorectum and in colon cancer Biochem. Soc. Trans 2005 33, N 4 P. 684– 688.
[91] Yoon M. S., Suh D. S., Choi K. U., Sol M. Y., Shin D. H., Park W. Y., Lee J. H., Jeong S. M., Kim W. G., Shin N. R. High-hroughput DNA hypermethylation profiling in different ovarian epithelial cancer subtypes using universal bead array Oncol. Rep 2010 24, N 4 P. 917–925.
[92] Farley J., Ozbun L. L., Birrer M. J. Genomic analysis of epithelial ovarian cancer Cell Res 2008 18, N 5 P. 538– 548.
[93] Fridman E., Dotan Z., Barshack I., David M. B., Dov A., Tabak S., Zion O., Benjamin S., Benjamin H., Kuker H., Avivi C., Rosenblatt K., Polak-Charcon S., Ramon J., Rosenfeld N., Spector Y. Accurate molecular classification of renal tumors using microRNA expression J. Mol. Diagn 2010 12, N 5 P. 687–696.
[94] Li S. S., Sharief F. S. The prostatic acid phosphatase (ACPP) gene is localized to human chromosome 3q21-q23 Genomics 1993 17, N 3 P. 765–766.
[95] Zhang H. L., Yang L. F., Zhu Y., Yao X. D., Zhang S. L., Dai B., Zhu Y. P., Shen Y. J., Shi G. H., Ye D. W. Serum miRNA21: Elevated levels in patients with metastatic hormonerefractory prostate cancer and potential predictive factor for the efficacy of docetaxel-based chemotherapy. Prostate. 2011;71(3):326-31
[96] Kahn S. L., Ronnett B. M., Gravitt P. E., Gustafson K. S. Quantitative methylation-specific PCR for the detection of aberrant DNA methylation in liquid-based Pap tests Cancer 2008 114, N 1 P. 57–64.
[97] Hausler S. F., Keller A., Chandran P. A., Ziegler K., Zipp K., Heuer S., Krockenberger M., Engel J. B., Honig A., Scheffler M., Dietl J., Wischhusen J. Whole blood-derived miRNA profiles as potential new tools for ovarian cancer screening Br. J. Cancer 2010 103, N 5 P. 693–700.
[98] Skvortsova T. E., Vlassov V. V., Laktionov P. P. Binding and penetration of methylated DNA into primary and transformed human cells Ann. N. Y. Acad. Sci 2008 1137 P. 36–40.
[99] Jones P. A., Martienssen R. A blueprint for a Human Epigenome Project: the AACR Human Epigenome Workshop Cancer Res 2005 65, N 24 P. 11241–11246.