Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells

Wippermann A, Klausing S, Rupp O, Albaum S, Büntemeyer H, Noll T, Hoffrogge R (2014)
Applied Microbiology and Biotechnology 98(2): 579-589.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
Optimizing productivity and growth rates of recombinant Chinese hamster ovary (CHO) cells requires insight into the regulation of cellular processes. In this regard, the elucidation of the epigenetic process of DNA methylation, known to influence transcription by a differential occurrence in CpG islands in promoter regions, is increasingly gaining importance. However, DNA methylation has not yet been investigated on a genomic scale in CHO cells and suitable tools have not existed until now. Based on the genomic and transcriptomic CHO data currently available, we developed a customized oligonucleotide microarray covering 19598 CpG islands (89 % of total bioinformatically identified CpG islands) in the CHO genome. We applied our CHO-specific CpG island microarray to investigate the effect of butyrate treatment on differential DNA methylation in CHO cultures in a time-dependent approach. Supplementation of butyrate is known to enhance cell specific productivities in CHO cells and leads to alterations of epigenetic silencing events. Gene ontology clusters regarding, e.g., chromatin modification or DNA repair, were significantly overrepresented 24 h after butyrate addition. Functional classifications furthermore indicated that several major signaling systems such as the Wnt/beta-catenin pathway were affected by butyrate treatment. Our novel CHO-specific CpG island microarray will provide valuable information in future studies of cellular processes associated with productivity and product characteristics.
Erscheinungsjahr
Zeitschriftentitel
Applied Microbiology and Biotechnology
Band
98
Ausgabe
2
Seite(n)
579-589
ISSN
eISSN
PUB-ID

Zitieren

Wippermann A, Klausing S, Rupp O, et al. Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells. Applied Microbiology and Biotechnology. 2014;98(2):579-589.
Wippermann, A., Klausing, S., Rupp, O., Albaum, S., Büntemeyer, H., Noll, T., & Hoffrogge, R. (2014). Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells. Applied Microbiology and Biotechnology, 98(2), 579-589. doi:10.1007/s00253-013-5282-2
Wippermann, A., Klausing, S., Rupp, O., Albaum, S., Büntemeyer, H., Noll, T., and Hoffrogge, R. (2014). Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells. Applied Microbiology and Biotechnology 98, 579-589.
Wippermann, A., et al., 2014. Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells. Applied Microbiology and Biotechnology, 98(2), p 579-589.
A. Wippermann, et al., “Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells”, Applied Microbiology and Biotechnology, vol. 98, 2014, pp. 579-589.
Wippermann, A., Klausing, S., Rupp, O., Albaum, S., Büntemeyer, H., Noll, T., Hoffrogge, R.: Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells. Applied Microbiology and Biotechnology. 98, 579-589 (2014).
Wippermann, Anna, Klausing, Sandra, Rupp, Oliver, Albaum, Stefan, Büntemeyer, Heino, Noll, Thomas, and Hoffrogge, Raimund. “Establishment of a CpG island microarray for analyses of genome-wide DNA methylation in Chinese hamster ovary cells”. Applied Microbiology and Biotechnology 98.2 (2014): 579-589.

11 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

CHO-Omics Review: The Impact of Current and Emerging Technologies on Chinese Hamster Ovary Based Bioproduction.
Stolfa G, Smonskey MT, Boniface R, Hachmann AB, Gulde P, Joshi AD, Pierce AP, Jacobia SJ, Campbell A., Biotechnol J 13(3), 2018
PMID: 29072373
CRISPR-Based Targeted Epigenetic Editing Enables Gene Expression Modulation of the Silenced Beta-Galactoside Alpha-2,6-Sialyltransferase 1 in CHO Cells.
Marx N, Grünwald-Gruber C, Bydlinski N, Dhiman H, Ngoc Nguyen L, Klanert G, Borth N., Biotechnol J 13(10), 2018
PMID: 29802757
Integrative analysis of DNA methylation and gene expression in butyrate-treated CHO cells.
Wippermann A, Rupp O, Brinkrolf K, Hoffrogge R, Noll T., J Biotechnol 257(), 2017
PMID: 27890772
Label-free protein quantification of sodium butyrate treated CHO cells by ESI-UHR-TOF-MS.
Müller B, Heinrich C, Jabs W, Kaspar-Schönefeld S, Schmidt A, Rodrigues de Carvalho N, Albaum SP, Baessmann C, Noll T, Hoffrogge R., J Biotechnol 257(), 2017
PMID: 28363874
Mechanisms underlying epigenetic and transcriptional heterogeneity in Chinese hamster ovary (CHO) cell lines.
Veith N, Ziehr H, MacLeod RA, Reamon-Buettner SM., BMC Biotechnol 16(), 2016
PMID: 26800878
Comprehensive genome and epigenome characterization of CHO cells in response to evolutionary pressures and over time.
Feichtinger J, Hernández I, Fischer C, Hanscho M, Auer N, Hackl M, Jadhav V, Baumann M, Krempl PM, Schmidl C, Farlik M, Schuster M, Merkel A, Sommer A, Heath S, Rico D, Bock C, Thallinger GG, Borth N., Biotechnol Bioeng 113(10), 2016
PMID: 27072894
2D-DIGE screening of high-productive CHO cells under glucose limitation--basic changes in the proteome equipment and hints for epigenetic effects.
Wingens M, Gätgens J, Schmidt A, Albaum SP, Büntemeyer H, Noll T, Hoffrogge R., J Biotechnol 201(), 2015
PMID: 25612871
Microarray profiling of preselected CHO host cell subclones identifies gene expression patterns associated with increased production capacity.
Harreither E, Hackl M, Pichler J, Shridhar S, Auer N, Łabaj PP, Scheideler M, Karbiener M, Grillari J, Kreil DP, Borth N., Biotechnol J 10(10), 2015
PMID: 26315449
Toward product attribute control: developments from genome sequencing.
Baik JY, Lee KH., Curr Opin Biotechnol 30(), 2014
PMID: 24874795
Advancing biopharmaceutical process science through transcriptome analysis.
Vishwanathan N, Le H, Le T, Hu WS., Curr Opin Biotechnol 30(), 2014
PMID: 25014889

64 References

Daten bereitgestellt von Europe PubMed Central.

Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation.
Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, Doderlein G, Maltry N, Wu W, Lyko F, Niehrs C., Nature 445(7128), 2007
PMID: 17268471
Unraveling the Chinese hamster ovary cell line transcriptome by next-generation sequencing.
Becker J, Hackl M, Rupp O, Jakobi T, Schneider J, Szczepanowski R, Bekel T, Borth N, Goesmann A, Grillari J, Kaltschmidt C, Noll T, Puhler A, Tauch A, Brinkrolf K., J. Biotechnol. 156(3), 2011
PMID: 21945585
Effects of high passage cultivation on CHO cells: a global analysis.
Beckmann TF, Kramer O, Klausing S, Heinrich C, Thute T, Buntemeyer H, Hoffrogge R, Noll T., Appl. Microbiol. Biotechnol. 94(3), 2012
PMID: 22331235
Controlling the false discovery rate: a practical and powerful approach to multiple testing
Benjamini Y, Hochberg Y., 1995
BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing.
Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T., Bioinformatics 21(21), 2005
PMID: 16141249
Quantitative comparison of genome-wide DNA methylation mapping technologies.
Bock C, Tomazou EM, Brinkman AB, Muller F, Simmer F, Gu H, Jager N, Gnirke A, Stunnenberg HG, Meissner A., Nat. Biotechnol. 28(10), 2010
PMID: 20852634
Suppression of histone deacetylation in vivo and in vitro by sodium butyrate.
Boffa LC, Vidali G, Mann RS, Allfrey VG., J. Biol. Chem. 253(10), 1978
PMID: 649576
Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk?
Bordonaro M, Lazarova DL, Sartorelli AC., Cell Cycle 7(9), 2008
PMID: 18418037
UHRF1 plays a role in maintaining DNA methylation in mammalian cells.
Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE., Science 317(5845), 2007
PMID: 17673620
Linking DNA methylation and histone modification: patterns and paradigms.
Cedar H, Bergman Y., Nat. Rev. Genet. 10(5), 2009
PMID: 19308066
Interplay between gene expression noise and regulatory network architecture.
Chalancon G, Ravarani CN, Balaji S, Martinez-Arias A, Aravind L, Jothi R, Babu MM., Trends Genet. 28(5), 2012
PMID: 22365642
Butyrate induces reactive oxygen species production and affects cell cycle progression in human gingival fibroblasts.
Chang MC, Tsai YL, Chen YW, Chan CP, Huang CF, Lan WC, Lin CC, Lan WH, Jeng JH., J. Periodont. Res. 48(1), 2012
PMID: 22834967
The combined effect of sodium butyrate and low culture temperature on the production, sialylation, and biological activity of an antibody produced in CHO cells
Chen F, Kou T, Fan L, Zhou Y, Ye Z, Zhao L, Tan W-S., 2011
Non-coding RNAs, epigenetics and complexity.
Costa FF., Gene 410(1), 2008
PMID: 18226475
Inhibition of histone deacetylase activity by butyrate.
Davie JR., J. Nutr. 133(7 Suppl), 2003
PMID: 12840228
EMMA 2--a MAGE-compliant system for the collaborative analysis and integration of microarray data.
Dondrup M, Albaum SP, Griebel T, Henckel K, Junemann S, Kahlke T, Kleindt CK, Kuster H, Linke B, Mertens D, Mittard-Runte V, Neuweger H, Runte KJ, Tauch A, Tille F, Puhler A, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19200358
Expression of recombinant plasmids in mammalian cells is enhanced by sodium butyrate.
Gorman CM, Howard BH, Reeves R., Nucleic Acids Res. 11(21), 1983
PMID: 6316266
Computational identification of microRNA gene loci and precursor microRNA sequences in CHO cell lines.
Hackl M, Jadhav V, Jakobi T, Rupp O, Brinkrolf K, Goesmann A, Puhler A, Noll T, Borth N, Grillari J., J. Biotechnol. 158(3), 2012
PMID: 22306111
Helping Wingless take flight: how WNT proteins are secreted.
Hausmann G, Banziger C, Basler K., Nat. Rev. Mol. Cell Biol. 8(4), 2007
PMID: 17342185
Transgene copy number distribution profiles in recombinant CHO cell lines revealed by single cell analyses.
He L, Winterrowd C, Kadura I, Frye C., Biotechnol. Bioeng. 109(7), 2012
PMID: 22234778
Identification of c-MYC as a target of the APC pathway.
He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW., Science 281(5382), 1998
PMID: 9727977
Wnt signalling: variety at the core.
Hoppler S, Kavanagh CL., J. Cell. Sci. 120(Pt 3), 2007
PMID: 17251379

AUTHOR UNKNOWN, 0
Public biotech 2011--the numbers.
Huggett B, Lahteenmaki R., Nat. Biotechnol. 30(8), 2012
PMID: 22871710
CpG islands--'a rough guide'.
Illingworth RS, Bird AP., FEBS Lett. 583(11), 2009
PMID: 19376112
Structural basis of Wnt recognition by Frizzled.
Janda CY, Waghray D, Levin AM, Thomas C, Garcia KC., Science 337(6090), 2012
PMID: 22653731

AUTHOR UNKNOWN, 0
A mechanistic understanding of production instability in CHO cell lines expressing recombinant monoclonal antibodies.
Kim M, O'Callaghan PM, Droms KA, James DC., Biotechnol. Bioeng. 108(10), 2011
PMID: 21538334
Alternative splicing: a pivotal step between eukaryotic transcription and translation.
Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ., Nat. Rev. Mol. Cell Biol. 14(3), 2013
PMID: 23385723
Sodium butyrate inhibits c-myc splicing and interferes with signal transduction in ovarian carcinoma cells.
Krupitza G, Harant H, Dittrich E, Szekeres T, Huber H, Dittrich C., Carcinogenesis 16(5), 1995
PMID: 7767986
Principles and challenges of genomewide DNA methylation analysis.
Laird PW., Nat. Rev. Genet. 11(3), 2010
PMID: 20125086
Multivariate analysis of cell culture bioprocess data--lactate consumption as process indicator.
Le H, Kabbur S, Pollastrini L, Sun Z, Mills K, Johnson K, Karypis G, Hu WS., J. Biotechnol. 162(2-3), 2012
PMID: 22974585
MethPrimer: designing primers for methylation PCRs.
Li LC, Dahiya R., Bioinformatics 18(11), 2002
PMID: 12424112
The Wnt signaling pathway in development and disease.
Logan CY, Nusse R., Annu. Rev. Cell Dev. Biol. 20(), 2004
PMID: 15473860
Wnt/beta-catenin signaling: components, mechanisms, and diseases.
MacDonald BT, Tamai K, He X., Dev. Cell 17(1), 2009
PMID: 19619488
Correlation between butyrate-induced histone hyperacetylation turn-over and c-myc expression.
Mariani MR, Carpaneto EM, Ulivi M, Allfrey VG, Boffa LC., J. Steroid Biochem. Mol. Biol. 86(2), 2003
PMID: 14568568
G1 cell-cycle control and cancer.
Massague J., Nature 432(7015), 2004
PMID: 15549091
Exposing the DNA methylome iceberg.
Ndlovu MN, Denis H, Fuks F., Trends Biochem. Sci. 36(7), 2011
PMID: 21497094
DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45.
Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR., Cell 135(7), 2008
PMID: 19109892
Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production.
Saemann MD, Bohmig GA, Osterreicher CH, Burtscher H, Parolini O, Diakos C, Stockl J, Horl WH, Zlabinger GJ., FASEB J. 14(15), 2000
PMID: 11024006

AUTHOR UNKNOWN, 0
MicroRNAs and epigenetics.
Sato F, Tsuchiya S, Meltzer SJ, Shimizu K., FEBS J. 278(10), 2011
PMID: 21395977
Genome-wide mapping of RNA Pol-II promoter usage in mouse tissues by ChIP-seq.
Sun H, Wu J, Wickramasinghe P, Pal S, Gupta R, Bhattacharyya A, Agosto-Perez FJ, Showe LC, Huang TH, Davuluri RV., Nucleic Acids Res. 39(1), 2010
PMID: 20843783
Comprehensive analysis of CpG islands in human chromosomes 21 and 22.
Takai D, Jones PA., Proc. Natl. Acad. Sci. U.S.A. 99(6), 2002
PMID: 11891299
Post-translational modifications of protein biopharmaceuticals.
Walsh G., Drug Discov. Today 15(17-18), 2010
PMID: 20599624
The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line.
Xu X, Nagarajan H, Lewis NE, Pan S, Cai Z, Liu X, Chen W, Xie M, Wang W, Hammond S, Andersen MR, Neff N, Passarelli B, Koh W, Fan HC, Wang J, Gui Y, Lee KH, Betenbaugh MJ, Quake SR, Famili I, Palsson BO, Wang J., Nat. Biotechnol. 29(8), 2011
PMID: 21804562
Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation.
Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP., Nucleic Acids Res. 30(4), 2002
PMID: 11842121
Histone deacetylase inhibitor promotes differentiation of embryonic stem cells into neural cells in adherent monoculture.
Yao X, Zhang JR, Huang HR, Dai LC, Liu QJ, Zhang M., Chin. Med. J. 123(6), 2010
PMID: 20368096
Genomic and proteomic exploration of CHO and hybridoma cells under sodium butyrate treatment.
Yee JC, de Leon Gatti M, Philp RJ, Yap M, Hu WS., Biotechnol. Bioeng. 99(5), 2008
PMID: 17929327
Butyrate induces cell apoptosis through activation of JNK MAP kinase pathway in human colon cancer RKO cells.
Zhang Y, Zhou L, Bao YL, Wu Y, Yu CL, Huang YX, Sun Y, Zheng LH, Li YX., Chem. Biol. Interact. 185(3), 2010
PMID: 20346929

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 24146078
PubMed | Europe PMC

Suchen in

Google Scholar