Cloning, chromosomal characterization and FISH mapping of the NAD+-dependent histone deacetylase gene sirtuin 5 in the mouse

Voelter-Mahlknecht,Susanne; Mahlknecht,Ulrich

doi:10.3892/ijo.2013.1939

Cloning, chromosomal characterization and FISH mapping of the NAD+-dependent histone deacetylase gene sirtuin 5 in the mouse

Authors:
- Susanne Voelter-Mahlknecht
- Ulrich Mahlknecht
View Affiliations

Affiliations: Institute of Occupational and Social Medicine and Health Services Research, University of Tuebingen, D-72074 Tuebingen, Germany, Department of Hematology/Oncology, St. Lukas Klinik Solingen, D-42697 Solingen, Germany
Published online on: May 14, 2013 https://doi.org/10.3892/ijo.2013.1939
Pages: 237-245

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Sirtuin 5 (SIRT5) is a nicotinamide adenine dinucleotide (NAD+)-dependent deacetylase, belonging to the silent information regulator 2 (Sir2) family of sirtuin histone deacetylases (sirtuins). The yeast Sir2 protein and its mammalian derivatives are important in epigenetic gene silencing, DNA repair and recombination, cell cycle, microtubule organization and in the regulation of aging. In mammals, 7 sirtuin isoforms have been identified to date of which three (SIRT3, SIRT4 and SIRT5) are localized in the mitochondria, which serve as the center of energy management and the initiation of cellular apoptosis. In the study presented herein, we report the genomic organization and chromosomal localization of the murine sirt5 gene. We have isolated and characterized the murine sirt5 genomic sequence, which spans a region of 24,449 bp and which has one single genomic locus. The murine sirt5 gene consists of 8 exons and encodes a 310-aa protein with a predictive molecular weight of 34.1 kDa and an isoelectric point of 8.90. For the murine sirt5 gene only one single genomic locus has been identified. The gene has been localized to mouse chromosome 13A4 and is flanked by STS-marker 164522 (synonymous WI MRC-RH: 506859).

View Figures

View References

1.	Imai S, Armstrong CM, Kaeberlein M and Guarente L: Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 403:795–800. 2000. View Article : Google Scholar : PubMed/NCBI
2.	Schuetz A, Min J, Antoshenko T, et al: Structural basis of inhibition of the human NAD⁺-dependent deacetylase SIRT5 by suramin. Stucture. 15:377–389. 2007. View Article : Google Scholar : PubMed/NCBI
3.	Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L and Boeke JD: The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 9:2888–2902. 1995. View Article : Google Scholar : PubMed/NCBI
4.	Voelter-Mahlknecht S and Mahlknecht U: Cloning, chromosomal characterization and mapping of the NAD-dependent histone deacetylases gene sirtuin 1. Int J Mol Med. 17:59–67. 2006.PubMed/NCBI
5.	Vaziri H, Dessain SK, Ng Eaton E, et al: hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 107:149–159. 2001. View Article : Google Scholar : PubMed/NCBI
6.	North BJ, Marshall BL, Borra MT, Denu JM and Verdin E: The human Sir2 ortholog, SIRT2, is an NAD⁺-dependent tubulin deacetylase. Mol Cell. 11:437–444. 2003. View Article : Google Scholar : PubMed/NCBI
7.	Starai VJ, Celic I, Cole RN, Boeke JD and Escalante-Semerena JC: Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science. 298:2390–2392. 2002. View Article : Google Scholar : PubMed/NCBI
8.	Sauve AA and Schramm VL: SIR2: the biochemical mechanism of NAD(+)-dependent protein deacetylation and ADP-ribosyl enzyme intermediates. Curr Med Chem. 11:807–826. 2004.
9.	Liszt G, Ford E, Kurtev M and Guarente L: Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem. 280:21313–21320. 2005. View Article : Google Scholar : PubMed/NCBI
10.	Mahlknecht U and Hoelzer D: Histone acetylation modifiers in the pathogenesis of malignant disease. Mol Med. 6:623–644. 2000.PubMed/NCBI
11.	Mahlknecht U, Ottmann OG and Hoelzer D: When the band begins to play: histone acetylation caught in the crossfire of gene control. Mol Carcinog. 27:268–271. 2000. View Article : Google Scholar : PubMed/NCBI
12.	Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P and Reinberg D: Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol Cell. 16:93–105. 2004. View Article : Google Scholar : PubMed/NCBI
13.	Blander G, Olejnik J, Krzymanska-Olejnik E, et al: SIRT1 shows no substrate specificity in vitro. J Biol Chem. 280:9780–9785. 2005. View Article : Google Scholar : PubMed/NCBI
14.	Blander G and Guarente L: The Sir2 family of protein deacetylases. Annu Rev Biochem. 73:417–435. 2004. View Article : Google Scholar : PubMed/NCBI
15.	Straight AF, Shou W, Dowd GJ, et al: Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell. 97:245–256. 1999. View Article : Google Scholar : PubMed/NCBI
16.	Fritze CE, Verschueren K, Strich R and Easton Esposito R: Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J. 16:6495–6509. 1997. View Article : Google Scholar : PubMed/NCBI
17.	Haigis MC, Mostoslavsky R, Haigis KM, et al: SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell. 126:941–954. 2006. View Article : Google Scholar : PubMed/NCBI
18.	Hede K: Histone deacetylase inhibitors sit at crossroads of diet, aging, cancer. J Natl Cancer Inst. 98:377–379. 2006. View Article : Google Scholar : PubMed/NCBI
19.	Mahlknecht U, Ho AD, Letzel S and Voelter-Mahlknecht S: Assignment of the NAD-dependent deacetylase sirtuin 5 gene (SIRT5) to human chromosome band 6p23 by in situ hybridization. Cytogenet Genome Res. 112:208–212. 2006. View Article : Google Scholar : PubMed/NCBI
20.	Frye RA: Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun. 273:793–798. 2000. View Article : Google Scholar : PubMed/NCBI
21.	Birnboim HC and Doly J: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513–1523. 1979. View Article : Google Scholar : PubMed/NCBI
22.	Mahlknecht U, Hoelzer D and Bucala R: Sequencing of genomic DNA. Biotechniques. 27:406–408. 1999.
23.	Altschul SF, Madden TL, Schaffer AA, et al: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402. 1997. View Article : Google Scholar : PubMed/NCBI
24.	Mahlknecht U and Voelter-Mahlknecht S: Genomic organization and localization of the NAD-dependent histone deacetylase gene sirtuin 3 (Sirt3) in the mouse. Int J Oncol. 38:813–822. 2011. View Article : Google Scholar : PubMed/NCBI
25.	Wilbur WJ and Lipman DJ: Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci USA. 80:726–730. 1983. View Article : Google Scholar : PubMed/NCBI
26.	Needleman SB and Wunsch CD: A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 48:443–453. 1970. View Article : Google Scholar : PubMed/NCBI
27.	Fitzgerald M and Shenk T: The sequence 5′-AAUAAA-3′forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell. 24:251–260. 1981.
28.	Su AI, Wiltshire T, Batalov S, et al: A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA. 101:6062–6067. 2004. View Article : Google Scholar : PubMed/NCBI
29.	Su AI, Cooke MP, Ching KA, et al: Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA. 99:4465–4470. 2002. View Article : Google Scholar : PubMed/NCBI
30.	Walker JR, Su AI, Self DW, et al: Applications of a rat multiple tissue gene expression data set. Genome Res. 14:742–749. 2004. View Article : Google Scholar : PubMed/NCBI
31.	Huang JY, Hirschey MD, Shimazu T, Ho L and Verdin E: Mitochondrial sirtuins. Biochim Biophys Acta. 1804:1645–1651. 2010. View Article : Google Scholar : PubMed/NCBI
32.	Fulco M, Schiltz RL, Iezzi S, et al: Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell. 12:51–62. 2003. View Article : Google Scholar : PubMed/NCBI
33.	Brunet A, Sweeney LB, Sturgill JF, et al: Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 303:2011–2015. 2004. View Article : Google Scholar : PubMed/NCBI
34.	Luo J, Nikolaev AY, Imai S, et al: Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell. 107:137–148. 2001. View Article : Google Scholar : PubMed/NCBI
35.	Yeung F, Hoberg JE, Ramsey CS, et al: Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23:2369–2380. 2004. View Article : Google Scholar : PubMed/NCBI
36.	Motta MC, Divecha N, Lemieux M, et al: Mammalian SIRT1 represses forkhead transcription factors. Cell. 116:551–563. 2004. View Article : Google Scholar : PubMed/NCBI
37.	Michishita E, McCord RA, Berber E, et al: SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature. 452:492–496. 2008. View Article : Google Scholar : PubMed/NCBI
38.	Ford E, Voit R, Liszt G, Magin C, Grummt I and Guarente L: Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev. 20:1075–1080. 2006. View Article : Google Scholar : PubMed/NCBI
39.	Michishita E, Park JY, Burneskis JM, Barrett JC and Horikawa I: Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cel. l6:4623–4635. 2005. View Article : Google Scholar : PubMed/NCBI
40.	Haigis MC and Sinclair DA: Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol. 5:253–295. 2010. View Article : Google Scholar : PubMed/NCBI
41.	Nakamura Y, Ogura M, Tanaka D and Inagaki N: Localization of mouse mitochondrial SIRT proteins: shift of SIRT3 to nucleus by co-expression with SIRT5. Biochem Biophys Res Commun. 366:174–179. 2008. View Article : Google Scholar : PubMed/NCBI
42.	Nakagawa T, Lomb DJ, Haigis MC and Guarente L: SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell. 137:560–570. 2009. View Article : Google Scholar : PubMed/NCBI
43.	Schlicker C, Gertz M, Papatheodorou P, Kachholz B, Becker CF and Steegborn C: Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J Mol Biol. 382:790–801. 2008. View Article : Google Scholar : PubMed/NCBI
44.	Gertz M and Steegborn C: Function and regulation of the mitochondrial sirtuin isoform Sirt5 in Mammalia. Biochim Biophys Acta. 1804:1658–1665. 2010. View Article : Google Scholar : PubMed/NCBI
45.	Nakahata Y, Kaluzova M, Grimaldi B, et al: The NAD^+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 134:329–340. 2008.PubMed/NCBI
46.	Nakamura Y, Ogura M, Ogura K, Tanaka D and Inagaki N: SIRT5 deacetylates and activates urate oxidase in liver mitochondria of mice. FEBS Lett. 586:4076–4081. 2012. View Article : Google Scholar : PubMed/NCBI
47.	North BJ, Schwer B, Ahuja N, Marshall B and Verdin E: Preparation of enzymatically active recombinant class III protein deacetylases. Methods. 36:338–345. 2005. View Article : Google Scholar : PubMed/NCBI
48.	Lieber CS, Leo MA, Wang X and Decarli LM: Alcohol alters hepatic FoxO1, p53, and mitochondrial SIRT5 deacetylation function. Biochem Biophys Res Commun. 373:246–252. 2008. View Article : Google Scholar : PubMed/NCBI
49.	Shepard BD and Tuma PL: Alcohol-induced protein hyperacetylation: mechanisms and consequences. World J Gastroenterol. 15:1219–1230. 2009. View Article : Google Scholar : PubMed/NCBI
50.	Singer MF, Thayer RE, Grimaldi G, Lerman MI and Fanning TG: Homology between the KpnI primate and BamH1 (M1F-1) rodent families of long interspersed repeated sequences. Nucleic Acids Res. 11:5739–5745. 1983. View Article : Google Scholar : PubMed/NCBI
51.	Mitelman F, Mertens F and Johansson B: A breakpoint map of recurrent chromosomal rearrangements in human neoplasia. Nat Genet. 15:417–474. 1997. View Article : Google Scholar : PubMed/NCBI
52.	Michan S and Sinclair D: Sirtuins in mammals: insights into their biological function. Biochem J. 404:1–13. 2007. View Article : Google Scholar : PubMed/NCBI