The role of histone modifications and DNA methylation in renal cell carcinoma development

Abstract

Epigenetic mechanisms of gene regulation play a key role in carcinogenesis. This review will focus on the recent advances of epigenetic investigations in the development of human cancer. The role of histone modifications, genomic imprinting and DNA methylation in renal cell carcinoma development and progression will be considered.

About the authors

Lilia R Kutlyeva

Institute of Biochemistry and Genetics, Ufa Research Scientific Center RAS, Ufa, Republic of Bashkortostanб RF

Email: mingazovaliliya@mail.ru Ufa

Irina R Gilayzova

Institute of Biochemistry and Genetics, Ufa Research Scientific Center RAS, Ufa, Republic of Bashkortostanб RF

Email: gilyasova_irina@mail.ru Ufa

Rita I Khusainova

Institute of Biochemistry and Genetics, Ufa Research Scientific Center RAS, Ufa, Republic of Bashkortostanб RF

Email: ritakh@mail.ru

Elsa K Khusnutdinova

Institute of Biochemistry and Genetics, Ufa Research Scientific Center RAS, Ufa, Republic of Bashkortostanб RF

Email: ekkh@anrb.ru

References

  1. Гранов А. М., Якубович Е. И., Лавникевич Д. М. и др., 2008. Гендерные различия в метилировании 5'-фланкирующей области гена DUSP9 у больных со светлоклеточной карциномой почки // Мед. акад. журнал. Т. 8. № 3. С. 55–61.
  2. Евдокимов А. А., Зиновьев В. В., Кузнецов В. В. и др., 2009. Конструирование олигонуклеотидных ингибиторов ДНК-метилтрансферазы I человека // Молекулярная биология. Т. 43, № 3. C. 455–463
  3. Курынин Р. В., Михайленко Д. С., Залетаев Д. В. и др., 2008. Молекулярные маркеры в диагностике и лечении рака почки // Молекулярная медицина. № 4. С. 24–28.
  4. Лебедев И. Н., Саженова Е. А., 2008. Эпимутации импринтированных генов в геноме человека: классификация, причины возникновения, связь с наследственной патологией // Генетика. Т. 44. № 10. С. 1356–1373.
  5. Лихтенштейн А. В., Киселева Н. П., 2001. Метилирование ДНК и канцерогенез // Биохимия. № 66. C. 293–317.
  6. Логинов В. И., Ходырев Д. С., Пронина И. В. и др., 2009. Два СpG-островка гена SEMA3B: метилирование при светлоклеточном раке почки // Молекулярная биология. № 6. С. 1088–1092.
  7. Михайленко Д. С., Немцова М. В., 2007. Молекулярно-генетические маркеры рака почки // Российский онкологический журнал. № 4. С. 48–51.
  8. Назаренко С. А., 2002. Эпигенетическая регуляция активности генов и ее эволюция // Эволюционная биология. Материалы II Международной конференции «Проблема вида и видообразование». Томск: Томский государственный университет. Т. 2. C. 412.
  9. Пальцев М. А., Залетаев Д. В., 2009. Системы генетических и эпигенетических маркеров в диагностике онкологических заболеваний. М.: Медицина. С. 384.
  10. Смирнихина С. А., Лавров А. В., 2009. Методы оценки метилирования остатков цитозина в ДНК //Молекулярная биология. Т. 43. № 3. С. 474–479.
  11. Стрельников В. В., Кузнецова Е. Б., Танас А. А., 2010. Методы анализа метилирования ДНК // Введение в молекулярную диагностику / под ред. М. А. Пальцева. Москва, ОАО Издательство «Медицина». C. 368.
  12. Ahmad S. T., Arjumand W., Seth A., Saini A. K. et al., 2011. Methylation of the APAF-1 and DAPK-1 promoter region correlates with progression of renal cell carcinoma in North Indian population // Tumour Biol. (Epub ahead of print)
  13. Arita K., Ariyoshi M., Tochio H. et al., 2008. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism // Nature. Vol. 455. P. 818–821.
  14. Awakura Y., Nakamura E., Kamoto T. et al., 2008. Methylation-associated silencing of SFRP1 in renal cell carcinoma // Oncology Reports. Vol. 20. P. 1257–1263.
  15. Bannister A. J., Schneider R., Myers F. A. et al., 2005. Spatial distribution of di-and tri-methyl lysine 36 of histone H3 at active genes // J. Biol. Chem. Vol. 280. P. 17732–17736.
  16. Bannister A. J., Schneider R., Kouzarides T., 2010. Histone methylation: dynamic or static? // Nat. Rev. Cancer. Vol. 10(7). P.457–469.
  17. Bártová E., Krejcí J., Harnicarová A. et al., 2008. Histone modifications and nuclear architecture: a review // J. Histochem. Cytochem. Vol. 56 (8). P. 711–21.
  18. Bouzinba-Segard H., Guais A., Francastel C., 2006. Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function // Proc Natl Acad Sci USA. Vol. 103. P. 8709–8714.
  19. Caldwell G., Jones C., Gensberg K. et al., 2004. The Wnt antagonist sFRP1 in colorectal tumorigenesis //Cancer Res. Vol. 64. P. 883–888.
  20. Cheng J. C., Matsen F. A., Gonzales F. A. et al., 2003. Inhibition of DNA methylation and reactivation of silenced genes by zebularine // J. Natl. Cancer Inst. Vol. 95. P. 399–409.
  21. Cheung H., Lee T., Rennert O. et al., 2009. DNA methylation of cancer genome // Birth Defects Research (Part C). Vol. 87. P. 335–350.
  22. Chi P., Allis C. D., Wang G. G. 2010. Covalent histone modifications — miswritten, misinterpreted and miserased in human cancers // Nat Rev Cancer. Vol. 10. P. 457–469.
  23. Christoph F., Weikert St., Kempkensteffen C. et al., 2006. Promoter hypermethylation profile of kidney cancer with new proapoptotic p53 target genes and clinical implications // Clin. Cancer Res. Vol. 12
  24. Dahl E., Wiesmann F., Woenekhaus M. et al., 2007. Frequent loss of SFRP1 expression in multiple human solid tumours: association with aberrant promoter methylation in renal cell carcinoma // Oncogene. Vol. 26. P. 5680–5690.
  25. Dalgliesh G.L., Furge K., Greenman C. et al., 2010. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes // Nature. Vol. 4639. P. 360–363.
  26. Di Lorenzo A., Bedford M.T., 2011. Histone arginine methylation // FEBS Lett. Vol. 585 (13). P. 2024–2031.
  27. Duns G., van den Berg E., van Duivenbode I. et al., 2010. Histone methyltransferase gene SETD2 is a novel tumor suppressor gene in clear cell renal cell carcinoma // Cancer Res. Vol. 70. P. 4287–4291.
  28. El-Osta A., 2003. DNMT cooperativity — the developing links between methylation, chromatin structure and cancer // Bioessays. Vol. 25. P. 1071–1084.
  29. Esteve P., Chin H., Pradhan S., 2005. Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. // Proc Natl Acad Sci USA. Vol. 102. P. 1000–1005.
  30. Fabbri M., Garzon R., Cimmino A. et al., 2007. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B // Proc Natl Acad Sci USA. Vol. 104. P. 15805–15810.
  31. Fan T., Schmidtmann A., Xi S. et al., 2008. DNA hypomethylation caused by Lsh deletion promotes erythroleukemia development // Epigenetics. Vol. 3. P. 134–142.
  32. Foltz G., Ryu G., Yoon J. et al., 2006. Genome-wide analysis of epigenetic silencing identifies BEX1 and BEX2 as candidate tumor suppressor genes in malignant glioma // Cancer Res. Vol. 66. P. 6665–6674.
  33. Gama-Sosa M. A., Slagel V. A., Trewyn R. W. et al., 1983. The 5-methylcytosine content of DNA from human tumors // Nucleic. Acids Res. Vol. 11. P. 6883–6894.
  34. Goll M. G., Bestor T. H., 2005 Eukaryotic cytosine methyltransferases // Ann. Rev. Biochem. Vol. 74. P. 481–514.
  35. Gonzalgo M., Yegnasubramanian S., Yan G. et al., 2004. Molecular profiling and classification of sporadic renal cell carcinoma by quantitative methylation analysis // Clin. Cancer Res. Vol. 10. P. 7276–7283.
  36. Gowher H., Liebert K., Herman A., Xu G., 2005. Mechanism of stimulation of catalytic activity of Dnmt3A and Dnmt3B DNA- (cytosine-C5)-methyltransferases by Dnmt3L // J. Bid Chem. Vol. 280. P. 13 341–13 348.
  37. Huang J., Dorsey J., Chuikov S. et al., 2010. G9a and Glp methylate lysine 373 in the tumor suppressor p53 // J. Biol. Chem. Vol. 285. Р. 9636–9641.
  38. Ito Y., Koessler T., Ibrahim A. E. et al., 2008. Somatically acquired hypomethylation of IGF2 in breast and colorectal cancer. // Hum. Mol. Genet. Vol. 17. P. 2633–2643.
  39. Jemal A., Bray F., Center M. M, Ferlay J. et al., 2011. Global cancer statistics. // CA Cancer J. Clin. Vol. 61(2). P. 69–90.
  40. Kato K., Maesawa C., Itabashi T. et al., 2009. DNA hypomethylation at the CpG island is involved in aberrant expression of the L1 cell adhesion molecule gene in colorectal cancer // Int. J. Oncol. Vol. 35. P. 467–476.
  41. Kawada Y., Nakamura M., Ishida E. et al., 2001. Aberrations of the p14 (ARF) and p16 (INK4a) genes in renal cell carcinomas // J. J. Cancer Res. Vol. 92. P. 1293–1299.
  42. Kawamoto K., Hirata H., Kikuno N. et al., 2008. DNA methylation and histone modifications cause silencing of Wnt antagonist gene in human renal cell carcinoma cell lines // Int. J. Cancer. Vol. 123. P. 535–542.
  43. Kim J. K., Samaranayake M., Pradhan S., 2009. Epigenetic mechanisms in mammals // Cell Mol. Life Sci. Vol. 66. P. 596–612.
  44. Klose R.J, Zhang Y., 2007. Regulation of histone methylation by demethylimination and demethylation. //Nat. Rev. Mol. Cell Biol. Vol. 8 (4). P. 307–318.
  45. Kondo M., Suzuki H., Ueda R. et al., 1995. Frequent loss of imprinting of the H19 gene is often associated with its overexpression in human lung cancers // Oncogene. Vol. 10. P. 1193–1198.
  46. Kurdistani S. K., 2011 Histone modifications in cancer biology and prognosis. Prog. Drug Res. 67. P. 91–106.
  47. Larkin J., Goh X. Y., Vetter M. et al., 2012. Epigenetic regulation in RCC: opportunities for therapeutic intervention? // Nat. Rev. Urol. Vol. 9 (3). P. 147–155.
  48. Lim J., Kim S., Gabrielson E., Park Y. B. et al., 2005. Activation of human cancer / testis antigen gene, XAGE-1, in tumor cells is correlated with CpG island hypomethylation // Int. J. Cancer. Vol. 116. P. 200–206.
  49. Lujambio A., Calin G., Villanueva A. et al., 2008. A microRNA DNA methylation signature for human cancer metastasis // Proc. Natl. Acad. Sci. USA. Vol. 105. P. 13556–13561.
  50. Majid Sh., Dar A. A., Ahmad A. E. et al., 2009. BTG3 tumor suppressor gene promoter demethylation, histone modification and cell cycle arrest by genistein in renal cancer // Carcinogenesis. Vol. 4. P. 662–670.
  51. Martin C., Zhang Y., 2005. The diverse functions of histone lysine methylation // Nat. Rev. Mol. Cell Biol. Vol. 6 (11). P. 838–849.
  52. Martinez-Garcia E., Licht J. D., 2010. Deregulation of H3K27 methylation in cancer // Nat. Genet. Vol. 42. P. 100–101.
  53. Moore L. E., Pfeiffer R. M., Poscablo C. et al., 2008. Genomic DNA hypomethylation as a biomarker for bladder cancer susceptibility in the Spanish Bladder Cancer Study: a case-control study // Lancet Oncol. Vol. 9. P. 359–366.
  54. Morris M. R., Hesson L., Wagner K. et al., 2003. Multigene methylation analysis of Wilms' tumour and adult renal cell carcinoma // Oncogene. Vol. 22. P. 6794–6801.
  55. Morris M. R., Ricketts C., Gentle D. et al., 2010. Identification of candidate tumour suppressor genes frequently methylated in renal cell carcinoma // Oncogene. Vol. 29. P. 2104–2117.
  56. Morris M. R., Ricketts C. J., Gertle D. et al., 2011. Genome-wide methylation analysis identifies epigenetically inactivated candidate tumour suppressor genes in renal cell carcinoma // Oncogene. Vol. 30. P. 1390–1401.
  57. Nakagawa T., Kanai Y., Ushijima S. et al., 2005. DNA hypomethylation on pericentromeric satellite regions significantly correlates with loss of heterozygosity on chromosome 9 in urothelial carcinomas // J. Urol. Vol. 173. P. 243–246.
  58. Nonomura N., Nishimura K., Tsuneharu M. et al., 1997. Loss of imprinting of the insulin-like growth factor II gene in renal cell carcinoma // Cancer Res. Vol. 57. P. 2575–2577.
  59. Ongenaert M., Van Neste L., De Mey et al., 2008. PubMeth: a cancer methylation database combining text-mining and expert annotation // Nucleic Acids Res. Vol. 36. P. 842–846.
  60. Paiva F., Duarte-Pereira S., Costa V. L. et al., 2010. Functional and epigenetic characterization of the KRT19 gene in renal cell neoplasms // DNA Cell Biol. Vol. 30. P. 85–90.
  61. Park P. J., 2009. ChIP-seq: advantages and challenges of a maturing technology // Nat. Rev. Genet. Vol.10. P. 669–80.
  62. Poke F. S., Qadi A., Holloway A., 2010. Reversing aberrant methylation patterns in cancer // Current Medicinal Chemistry. Vol. 17. P. 1246–1254.
  63. Raj K., Mufti G. J., 2006. Azacytidine (Vidaza (®) in the treatment of myelodysplastic syndromes // Ther. Clin. Risk Manag. Vol. 2. P. 377–388.
  64. Ramsahoye B., Biniszkiewicz D., Lyko F. et al., 2000. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a // Proc. Natl. Acad. Sci USA. Vol. 97. P. 5237–5242.
  65. Reik W., Walter J., 2001 Genomic imprinting: parental influence on the genome // Nat. Rev. Genet. Vol. 2. P. 21–32.
  66. Ricketts C. J., Morris M. R., Gentle D., 2012. Genome-wide CpG island methylation analysis implicates novel genes in the pathogenesis of renal cell carcinoma //Epigenetics. Vol. 7. P. 278–90.
  67. Robertson K., Ait-Si-Ali S., Yokochi T. et al., 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters // Nat. Genet. 2000. Vol. 25. P. 338–342.
  68. Roman-Gomez J., Jimenez-Velasco A., Agirre X. et al., 2005. Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia // J. Clin. Oncol. Vol. 23. P. 7043–7049.
  69. Ronald F., Morris M., Gentle D. et al., 2009. CpG methylation profiling in VHL related and VHL unrelated renal cell carcinoma // Molecular cancer. Vol. 8. P. 31.
  70. Ruthenburg A. J., Li H., Patel D. J. et al., 2007. Multivalent engagement of chromatin modifications by linked binding modules // Nat. Rev. Mol. Cell Biol. Vol. 12. P. 983–994.
  71. Saxonov S., Berg P., Brutlag D., 2006. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. // Proc. Natl. Acad. Sci. USA. Vol. 103. P. 1412–1417.
  72. Scelfo R. A., Schwienbacher C., Veronese A. et al., 2002. Loss of methylation at chromosome 11p15.5 is common in human adult tumors // Oncogene. Vol. 21. P. 2564–2572.
  73. Schulte J., Lim S., Scramm A. et al., 2009. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy // Cancer Res. Vol. 69. P. 2065–2071.
  74. Sims R. J. 3rd, Nishioka K., Reinberg D., 2003. Histone lysine methylation: a signature for chromatin function // Trends Genet. Vol. 19. P. 629–639.
  75. Stephens K. E., Miaskowski C. A., Levine J. D. et al., 2012. Epigenetic Regulation and Measurement of Epigenetic Changes // Biol. Res. Nurs.
  76. Suzuki K., Suzuki I., Leodolter A. et al., 2006. Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage // Cancer Cell. Vol. 9. P. 199–207.
  77. Takai D., Gonzales F. A., Tsai Y. C. et al, 2001. Large scale mapping of methylcytosines in CTCF-binding sites in the human H19 promoter and aberrant hypomethylation in human bladder cancer // Hum. Mol. Genet. Vol. 10. P. 2619–2626.
  78. Tang S. H., Yang D. H., Huang W. et al., 2006. Hypomethylated P4 promoter induces expression of the insulin-like growth factor-II gene in hepatocellular carcinoma in a Chinese population // Clin. Cancer Res. Vol. 12. P. 4171–4177.
  79. Van Haaften G., Dalgliesh G. L., Davies H. et al., 2009. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer // Nat. Genet. Vol. 41. P. 521–523.
  80. Varela I., Tarpey P., Raine K. et al., 2011. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma // Nature. Vol. 469. P. 539–542.
  81. Vidaurreta M., Maestro M., Sanz-Casla M. et al., 2008. Inactivation of p16 by CpG hypermethylation in renal cell carcinoma // Urologic Oncology: Seminars and Original Investigations. Vol. 26. P. 239–245.
  82. Wang Q., Williamson M., Bott S. et al., 2007. Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer // Oncogene. 2007. Vol. 26. P. 6560–6565.
  83. Yamada Y., Jackson-Grusby L., Linhart H. et al., 2005. Opposing effects of DNA hypomethylation on intestinal and liver carcinogenesis // Proc Natl Acad Sci USA. Vol. 102. P. 13580–13585.
  84. Yanagawa N., Tamura G., Honda T., et al., 2004. Demethylation of the synuclein gamma gene CpG island in primary gastric cancers and gastric cancer cell lines // Clin. Cancer Res. 2004. Vol. 10. P. 2447–2451.
  85. Yehezkel S., Segev Y., Viegas-Pequignot E. et al., 2008. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions // Hum. Mol. Genet. Vol. 17. P. 2776–2789.
  86. Yoo K. H., Park Y. K., Kim H. S. et al., 2010. Epigenetic inactivation of HOXA5 and MSH2 gene in clear cell renal cell carcinoma // Pathology International. Vol. 60. P. 661–666.
  87. Zhang Q., Ying J., Li J. et al., 2010. Aberrant promoter methylation of DLEC1, a critical 3p22 tumor suppressor for renal cell carcinoma, is associated with more advanced tumor stage // The J. of Urology. Vol. 184. P. 731–737.
  88. Zhao W., Liu H., Liu W. et al., 2006. Abnormal activation of the synuclein-gamma gene in hepatocellular carcinomas by epigenetic alteration // Int. J. Oncol. Vol. 28. P. 1081–1088.
  89. Zhou L., Cheng X., Connoly B. A. et al., 2002. Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases. // J. Mol. Biol. Vol. 321. P. 591–599.
  90. Zhu H., Geiman T. M., Xi S., Schmidtmann A. et al., 2006. Lsh is involved in de novo methylation of DNA. // EMBO J. Vol. 25. P. 335–345.
  91. Aravin A., Sachidanandam R., Bouc’his D. et al., 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice // Mol. Cell. Vol. 31. P. 785–799.
  92. Costa V., Henrique R., Ribeiro F. et al., 2007. Quantitative promoter methylation analysis of multiple cancer-related genes in renal cell tumors // BMC Cancer. Vol. 7. P. 133.
  93. Stresemann C., Brueckner B., Musch T. et al., 2006. Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines // Cancer Res. Vol. 66. P. 2794–2800.

Statistics

Views

Abstract: 520

PDF (Russian): 445

Dimensions

Article Metrics

Metrics Loading ...

PlumX


Copyright (c) 2012 Kutlyeva L.R., Gilayzova I.R., Khusainova R.I., Khusnutdinova E.K.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies