РОЛЬ ТИМИН ДНК-ГЛИКОЗИЛАЗЫ ЧЕЛОВЕКА В ЭПИГЕНЕТИЧЕСКОЙ РЕГУЛЯЦИИ ТРАНСКРИПЦИИ И СТАБИЛЬНОСТИ ГЕНОМА

Авторы

  • Д. Манапқызы Казахский национальный университет имени аль-Фараби, Казахстан, Алматы
  • М.К. Сапарбаев Лаборатория Механизмов ДНК Рапарации и Карциногенеза СИЕ 9019, Институт Густава Русси, Вильжюиф, Франция
  • С.М. Тайпакова Казахский национальный университет имени аль-Фараби, Казахстан, Алматы

DOI:

https://doi.org/10.26577/eb.2023.v97.i4.01
        139 92

Ключевые слова:

Тимин ДНК-гликозилаза, репарация ДНК, деметилирование ДНК, раковые заболевания

Аннотация

Тимин ДНК-гликозилаза (TDG) привлекла к себе внимание благодаря своей способности удалять тимин, т.е. нормальное основание ДНК, из G:T неправильных пар. Это указывало на его функцию в эксцизионной репарации оснований ДНК в восстановлении пар оснований G:C после дезаминирования 5-метилцитозина. Из-за очевидной каталитической неэффективности, некоторые считали TDG плохим ферментом репарации ДНК без важной биологической функции. Однако было продемонстрировано, что этот фермент может действовать как ключевой игрок в транскрипционной регуляции через взаимодействие с различными ядерными рецепторами и факторами транскрипции что указывает на ее функцию в регуляции генов, которая, по-видимому, имеет решающее значение в процессах развития. Другие показали, что TDG участвует в эпигенетической регуляции экспрессии генов защищая CpG-богатые промоторы от de novo ДНК метилирования и может инициировать аберрантную репарацию. Недавние исследования на животных выявили связь между потерей TDG и началом и началом опухолеобразования. Таким образом целью данного обзора является собрать воедино результаты различных экспериментов, в которых исследовалась тимин ДНК-гликозилаза с момента ее открытия, и оценить их влияние ля определения возможных физиологических ролей этого фермента.

Библиографические ссылки

Akan P., Deloukas P. (2008) DNA Sequence and Structural Properties as Predictors of Human and Mouse Promoters. Gene, vol. 410, pp. 165–176.

Arlt V.M., Stiborova M. and Schmeiser H.H. (2002) Aristolochic acid as a probable human cancer hazard in herbal remedies: a review. Mutagenesis, vol. 17, pp. 265–277.

Attaluri S., Bonala R.R., Yang I.Y., Lukin M.A., Wen Y., Grollman A.P., Moriya M., Iden C.R. and Johnson,F. (2010) DNA adducts of aristolochic acid II: total synthesis and site-specific mutagenesis studies in mammalian cells. Nucleic Acids Res., vol. 38, pp. 339–352.

Bellacosa A., (2001) Role of MED1 (MBD4) gene in DNA repair and human cancer. J. Cell Physiol., vol. 187, pp. 137–144.

Bennett M. T., Rodgers M. T., Hebert A. S., Ruslander L. E., Eisele L., Drohat A. C. (2006) Specificity of human thymine DNA glycosylase depends on N-glycosidic bond stability. J. Am. Chem. Soc., vol. 128, pp. 12510-12519.

Bhattacharyya S., Yu Y., Suzuki M., Campbell N., Mazdo J., Vasanthakumar A., Bhagat T.D., Nischal S., Christopeit M., Parekh S., et al. (2013) Genome-Wide Hydroxymethylation Tested Using the HELP-GT Assay Shows Redistribution in Cancer. Nucleic Acids Res., vol. 41. pp. 157.

Bhutani N., Burns D.M., Blau H.M. (2011) DNA Demethylation Dynamics. Cell. vol.146. pp. 866–872.

Bird A. (2002) DNA Methylation Patterns and Epigenetic Memory. Genes Dev., vol.16, pp. 6–21.

Bird A., Taggart M., Frommer M., Miller O.J., Macleod D. A. (1985) Fraction of the Mouse Genome That Is Derived from Islands of Nonmethylated, CpG-Rich DNA. Cell, vol.40, pp. 91–99.

Bird A.P. (1980) DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res., vol. 8, pp. 1499–1504.

Bostick M., Kim J.K., Estève P.O., Clark A., Pradhan S., Jacobsen S.E. (2007) UHRF1 Plays a Role in Maintaining DNA Methylation in Mammalian Cells. Science, vol. 317. pp .1760–1764.

Chen K., Zhang J., Guo Z., Ma Q., Xu Z., Zhou Y., Xu Z., Li Z., Liu Y., Ye X., et al. (2016) Loss of 5-Hydroxymethylcytosine Is Linked to Gene Body Hypermethylation in Kidney Cancer. Cell Res., vol. 26, pp.103–118.

Christmann M., Tomicic M.T. and Kaina B. (2002) Phosphorylation of mismatch repair proteins MSH2 and MSH6 affecting MutSalpha mismatch-binding activity. Nucleic Acids Res., vol. 30. pp.1959–1966.

Cortazar D., Kunz C., Saito Y., Steinacher R., Schar P. (2007) The enigmatic thymine DNA glycosylase. DNA Repair (Amsterdam), vol. 6, pp. 489–504.

Cortellino S, Xu J, Sannai M, et al. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell, vol. 146, pp. 67–79.

Deaton A.M.; Bird A. (2011) CpG Islands, and the Regulation of Transcription. Genes Dev., vol. 25, pp. 1010–1022.

Fernando R.C., Schmeiser H.H., Scherf H.R. and Wiessler M. (1993) Formation and persistence of specific purine DNA adducts by 32P-postlabelling in target and non-target organs of rats treated with aristolochic acid I. IARC Sci. Publ., pp. 167–171.

Fromme J.C.; Verdine G.L. (2004) Base Excision Repair. Adv. Protein Chem. vol. 69, pp.1–41.

Gallinari P., Jiricny J. (1996) A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature, vol. 383, pp. 735-738.

Gopalakrishna R. and Jaken S. (2000) Protein kinase C signaling and oxidative stress. Free Radic. Biol. Med., vol. 28, pp. 1349–1361.

Greenblatt M.S., Bennett W.P., Hollstein M., Harris C.C. (1994) Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res., vol. 54, pp. 4855–4878.

Griner E.M. and Kazanietz M.G. (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer, vol. 7, pp. 281–294.

Grollman A.P., Scarborough J. and Jelakovic B. In: Fishbein J.C. (2009) Advances in Molecular Toxicology. The Netherlands, Elsevier, AmsterdaM, vol. 3. pp. 211–222.

Grollman A.P., Shibutani S., Moriya M., Miller F., Wu L., Moll U., Suzuki N., Fernandes A., Rosenquist T., Medverec Z. et al. (2007) Aristolochic acid and the etiology of endemic (Balkan) nephropathy. Proc. Natl Acad. Sci. USA, vol. 104, pp. 12129–12134.

Hang B., Medina M., Fraenkel-Conrat H., Singer B., (1998) A 55-kDa protein isolated from human cells shows DNA glycosylase activity toward 3, N4-ethenocytosine and the G/T mismatch. Proc Natl Acad Sci USA, vol. 95, pp.13561-13566.

Hardeland U., Bentele M., Jiricny J., Schar P. (2003) The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res., vol. 31, pp. 2261-2271.

Hardeland U., Steinacher R., Jiricny J., Schar P., (2002) Modification of the human thymine–DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J, vol. 21. pp.1456–1464.

Hasan S., El-Andaloussi N., Hardeland U., Hassa P.O., Burki C., Imhof R., Schar P. and Hottiger M.O. (2002) Acetylation regulates the DNA end-trimming activity of DNA polymerase beta. Mol. Cell, vol. 10, pp.1213–1222.

Hasan S., Stucki M., Hassa P.O., Imhof R., Gehrig P., Hunziker P., Hubscher U. and Hottiger M.O. (2001) Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol. Cell, vol. 7, pp. 1221–1231.

Hashimoto H., Liu Y., Upadhyay A. K., Chang Y., Howerton S. B., Vertino P. M., Zhang X., Cheng X. (2012) Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res., vol. 40, no 11, pp. 4841-9.

Hassan H.M.; Isovic M.; Kolendowski B.; Bauer-Maison N.; Onabote O.; Cecchini M.; Haig A.; Maleki Vareki S.; Underhill T.M.; Torchia J. (2020) Loss of Thymine DNA Glycosylase Causes Dysregulation of Bile Acid Homeostasis and Hepatocellular Carcinoma. Cell Rep., vol. 31, pp.107475.

Hendrich B., Hardeland U., Ng H. H., Jiricny J., Bird A. (1999) The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature, vol. 401, pp. 301-304.

Hitomi K., Iwai S. and Tainer J.A. (2007) The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst), vol. 6, pp. 410–428.

Jelakovic B., Karanovic S., Vukovic L., Miller F., Edwards K., Nikolic J., Tomic K., Slade N., Brdar B., Turesky R. et al. (2011) Aristolactam-DNA adducts in the renal cortex: biomarkers of environmental exposure to aristolochic acid. Kidney Int. (in press)

Kalkhoven E., (2004) CBP and p300: HATs for different occasions. Biochem. Pharmacol., vol. 68, pp.1145–1155.

Kim E.J., Um S.J. (2008) Thymine–DNA Glycosylase Interacts with and Functions as a Coactivator of P53 Family Proteins. Biochem. Biophys. Res. Commun. vol. 377. pp. 838–842.

Kohli R.M., Zhang Y. (2013) TET Enzymes, TDG and the Dynamics of DNA Demethylation. Nature, vol. 502, pp. 472–479.

Kondo E., Gu Z., Horii A., Fukushige S., (2005) The thymine DNA glycosylase MBD4 represses transcription and is associated with methylated p16(INK4a) and hMLH1 genes. Mol. Cell. Biol., vol. 25, pp. 4388–4396.

Krokan H.E. and Bjoras M. (2013) Base excision repair. Cold Spring Harb. Perspect. Biol., vol. 5, pp. 012583.

Kudo Y., Tateishi K., Yamamoto K., Yamamoto S., Asaoka Y., Ijichi H., Nagae G., Yoshida H., Aburatani H., Koike K. (2012) Loss of 5-Hydroxymethylcytosine Is Accompanied with Malignant Cellular Transformation. Cancer Sci., vol. 103, pp. 670–676.

Li W.Q., Hu N., Hyland P.L., Gao Y., Wang Z.M., Yu K., Su H., Wang C.Y., Wang L.M., Chanock S.J., et al. (2013) Genetic Variants in DNA Repair Pathway Genes and Risk of Esophageal Squamous Cell Carcinoma and Gastric Adenocarcinoma in a Chinese Population. Carcinogenesis, vol. 34, pp.1536–1542.

Lim K.C., Lakshmanan G., Crawford S.E., et al. (2000) Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat Genet., vol. 25, pp. 209–212.

Maiti A., Morgan M.T., Pozharski E., Drohat A.C. (2008) Crystal structure of human thymine DNA glycosylase bound to DNA elucidates sequence-specific mismatch recognition. PNAS, vol. 105, pp. 8890-8895

Mancuso P., Tricarico R., Bhattacharjee V., Cosentino L., Kadariya Y., Jelinek J., Nicolas E., Einarson M., Beeharry N., Devarajan K., et al. (2019) Thymine DNA Glycosylase as a Novel Target for Melanoma. Oncogene, vol. 38, pp. 3710–3728.

Mark M., Ghyselinck N.B., Chambon P. (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol., vol. 46, pp. 451–480.

Messerschmidt D.M., Knowles B.B., Solter D. (2014) DNA Methylation Dynamics during Epigenetic Reprogramming in the Germline and Preimplantation Embryos. Genes Dev., vol. 28, pp. 812–828.

Millar C.B., Guy J., Sansom O.J., Selfridge J., MacDougall E., Hendrich B., Keightley P.D., Bishop S.M., Clarke A.R., Bird A. (2002) Enhanced CpG mutability and tumorigenesis in MBD4-deficient mice. Science, vol. 297, pp. 403–405

Mohan R.D., Rao A., Gagliardi J. and Tini M. (2007) SUMO-1-dependent allosteric regulation of thymine DNA glycosylase alters subnuclear localization and CBP/p300 recruitment. Mol. Cell. Biol., vol. 27, pp. 229–243.

Morgan M.T., Bennett M.T., Drohat A.C. (2007) Excision of 5-halogenated uracils by human thymine DNA glycosylase: Robust activity for DNA contexts other than CpG. J Biol Chem., vol. 282, pp. 27578–27586.

Moriya M., Slade N., Brdar B., Medverec Z., Tomic K., Jelakovic B., Wu L., Truong S., Fernandes A. and Grollman A.P. (2011) TP53 mutational signature for aristolochic acid: an environmental carcinogen. Int. J. Cancer, vol. 129, pp. 1532–1536.

Neddermann P., Jiricny J. (1993) The purification of a mismatch-specific thymine-DNA glycosylase from HeLa cells. J Biol Chem., vol. 268, pp. 21218-21224.

Neri F., Incarnato D., Krepelova A., Rapelli S., Anselmi F., Parlato C., Medana C., Dal Bello F., Oliviero S. (2015) Single-Base Resolution Analysis of 5-Formyl and 5-Carboxyl Cytosine Reveals Promoter DNA Methylation Dynamics. Cell Rep., vol. 10, pp. 674–683.

Nortier J.L., Martinez M.C., Schmeiser H.H., Arlt V.M., Bieler C.A., Petein M., Depierreux M.F., De Pauw L., Abramowicz D., Vereerstraeten P., et al. (2000) Urothelial carcinoma associated with the use of a Chinese herb (Aristolochia fangchi). N. Engl. J. Med., vol. 42, no 3, pp.1686–1692.

Okano M., Bell D.W., Haber D.A., Li E. (1999) DNA Methyltransferases Dnmt3a and Dnmt3b Are Essential for De Novo Methylation and Mammalian Development. Cell, vol. 99, pp. 247–257.

Petronzelli F., Riccio A., Markham G. D., Seeholzer S. H., Genuardi M., Karbowski M., Yeung A. T., Matsumoto Y., Bellacosa A. (2000) Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain. J. Cell. Physiol., vol. 185, pp. 473-480.

Pfeifer G.P., (2006) Mutagenesis at methylated CpG sequences. Curr. Top/ Microbiol. Immunol., vol. 301, pp. 259–281.

Popov A.V., Grin I.R., Dvornikova A.P., Matkarimov B.T., Groisman R., Saparbaev M., Zharkov D.O. (2019) Reading Targeted DNA Damage in the Active Demethylation Pathway: Role of Accessory Domains of Eukaryotic AP Endonucleases and Thymine-DNA Glycosylases. JM, vol.432, pp. 1747-1768

Rai K, Huggins IJ, James SR, et al. (2008) DNA demethylation in zebrafish involves the coupling of adeaminase, a glycosylase, and gadd45. Cell, vol. 35, pp. 1201–1212.

Reddy Parine N., Alanazi I.O., Shaik J.P., Aldhaian S., Aljebreen A.M., Alharbi O., Almadi M.A., Azzam N.A., Alanazi M. (2019) TDG Gene Polymorphisms and Their Possible Association with Colorectal Cancer: A Case Control Study. J. Oncol., 709 1815.

Ruczinski I., Jorgensen T.J., Shugart Y.Y., Schaad Y.B., Kessing B., Hoffman-Bolton J., Helzlsouer K.J., Kao W.H.L., Wheless L., Francis L., et al. (2012) A Population-Based Study of DNA Repair Gene Variants in Relation to Non-Melanoma Skin Cancer as a Marker of a Cancer-Prone Phenotype. Carcinogenesis, vol.33, pp.1692–1698

Ryan D., David W., Torchia J. and Tini M. (2010) Opposing regulatory roles of phosphorylation and acetylation in DNA mispair processing by thymine DNA glycosylase. Nucleic Acids Res., vol 38, no 4, pp. 1135–1148.

Saito Y., Ono T., Takeda N., et al. (2012) Embryonic lethality in mice lacking mismatch-specific thymine DNA glycosylase is partially prevented by DOPS, a precursor of noradrenaline. J Exp Med., vol. 226, pp. 75–83.

Sanyal A.J., Yoon S.K., Lencioni R. (2010) The Etiology of Hepatocellular Carcinoma and Consequences for Treatment. Oncologist, vol.15, pp.14–22.

Scharer O.D., Kawate T., Gallinari P., Jiricny J., Verdine G.L. (1997) Investigation of the mechanisms of DNA binding of the human G/T glycosylase using designed inhibitors. Proc. Natl. Acad. Sci. USA, vol. 94, pp. 4878–4883.

Schmeiser H.H., Scherf H.R. and Wiessler M. (1991) Activating mutations at codon 61 of the c-Ha-ras gene in thin-tissue sections of tumors induced by aristolochic acid in rats and mice. Cancer Lett., vol. 59, pp.139–143.

Steinacher R., Schar P. (2005) Functionality of human thymine DNA glycosylase requires SUMO-Regulated changes in protein conformation.Curr Biol., vol.15, pp.616–623.

Stiborova M., Frei E., Sopko B., Sopkova K., Markova V., Lankova M., Kumstyrova T., Wiessler M. and Schmeiser H.H. (2003) Human cytosolic enzymes involved in the metabolic activation of carcinogenic aristolochic acid: evidence for reductive activation by human NAD(P)H:quinone oxidoreductase. Carcinogenesis, vol. 24, pp. 1695–1703.

Talhaoui I., Couve S., Gros L., Ishchenko A.A., Matkarimov B., Saparbaev M.K., (2014) Aberrant repair initiated by mismatch-specific thymine-DNA glycosylases provide a mechanism for the mutational bias observed in CpG islands. Nucleic Acids Res., vol. 42, pp. 6300–6313.

Talhaoui I., Couve S., Ishchenko A. A., Kunz C., Schar P., Saparbaev M. (2013.) 7,8-Dihydro-8-oxoadenine, a highly mutagenic adduct, is repaired by Escherichia coli and human mismatch-specific uracil/thymine-DNA glycosylases. Nucleic Acids Res.

Talhaoui I., Matkarimov B.T., Tchenio T.,Zharkov D.O., Saparbaev M., Aberrant base excision repair pathway of oxidatively damaged DNA:Implications for degenerative diseases. (2017) Free Rad. Bio. & Medicine, vol.107, pp. 266 -277

Tanaka Y., Naruse I., Hongo T., et al. (2000) Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech Dev., vol. 95, pp.133–145.

Thillainadesan G., Chitilian J.M., Isovic M., Ablack J.N.G., Mymryk J.S., Tini M., Torchia J. (2012) TGF-β-Dependent Active Demethylation and Expression of the P15ink4b Tumor Suppressor Are Impaired by the ZNF217 CoREST. Complex. Mol. Cell., vol. 46, pp.636–649.

Tini M., Benecke A., Um S.J., Torchia J., Evans R.M. and Chambon P. (2002) Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cel., vol. 9, pp. 265–277.

Tokui T., Inagaki M., Nishizawa K., Yatani R., Kusagawa M., Ajiro K., Nishimoto Y., Date T. and Matsukage A. (1991) Inactivation of DNA polymerase beta by in vitro phosphorylation with protein kinase C. J. Biol. Chem., vol. 266, pp. 10820–10824.

Um S., Harbers M., Benecke A., Pierrat B., Losson R. and Chambon P. (1998) Retinoic acid receptors interact physically and functionally with the T:G mismatch-specific thymine-DNA glycosylase. J. Biol. Chem., vol. 273, pp. 20728–20736.

Vanherweghem J.L., Debelle F., Muniz Martinez M.C. and Nortier J. In: De Broe M.E., Porter G.A., Bennet W.M. and Verpooten G.A. (eds). (2003) Clinical Nephrotoxins, 2nd edn. Dordrecht Kluwer, Netherlands, pp. 588–601.

Vasovcak P., Krepelova A., Menigatti M., Puchmajerova A., Skapa P., Augustinakova A., Amann G., Wernstedt A., Jiricny J., Marra G., et al. (2012) Unique Mutational Profile Associated with a Loss of TDG Expression in the Rectal Cancer of a Patient with a Constitutional PMS2 Deficiency. DNA Repair., vol. 11, pp. 616–623.

Vermot J., Niederreither K., Garnier J.M., et al. (2003) Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice.Proc Natl Acad Sci USA, vol.100, pp. 1763–1768.

Wu P., et al. (2003) Mismatch repair in methylated DNA. Structure and activity of the mismatch-specific thymine glycosylase domain of methyl-CpG-binding protein MBD4. J Biol Chem., vol. 278, pp. 5285–5291

Xu J., Cortellino S., Tricarico R., Chang W.C., Scher G., Devarajan K., Slifker M., Moore R., Bassi M.R., Caretti E., et al. (2017) Thymine DNA Glycosylase (TDG) Is Involved in the Pathogenesis of Intestinal Tumors with Reduced APC Expression. Oncotarget, vol. 8, pp. 89988–89997.

Xu X., Yu T., Shi J., Chen X., Zhang W., Lin T., Liu Z., Wang Y., Zeng Z., Wang C., et al. (2014) Thymine DNA Glycosylase Is a Positive Regulator of Wnt Signaling in Colorectal Cancer. J. Biol. Chem., vol. 289, pp. 8881–8890.

Yang F., Huang X., Yi T., Yen Y. Moore D.D., HuangW. (2007) Spontaneous Development of Liver Tumors in the Absence of the Bile Acid Receptor Farnesoid X Receptor. Cancer Res., vol.67, pp. 863–867.

Yao T.P., Oh S.P., Fuchs M., et al. (1998) Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell, vol. 93, pp. 361–372.

Yoon J. H., Iwai S., O’Connor T. R., Pfeifer G. P. (2003) Human thymine DNA glycosylase (TDG) and methyl-CpG-binding protein 4 (MBD4) excise thymine glycol (Tg) from a Tg:G mispair. Nucleic Acids Res., vol. 31, pp. 5399-5404.

Загрузки

Как цитировать

Манапқызы, Д., Сапарбаев, М. ., & Тайпакова, С. . (2023). РОЛЬ ТИМИН ДНК-ГЛИКОЗИЛАЗЫ ЧЕЛОВЕКА В ЭПИГЕНЕТИЧЕСКОЙ РЕГУЛЯЦИИ ТРАНСКРИПЦИИ И СТАБИЛЬНОСТИ ГЕНОМА. Вестник КазНУ. Серия биологическая, 97(4), 4–18. https://doi.org/10.26577/eb.2023.v97.i4.01