Monitoring changes in proteome during stepwise adaptation of a MDCK cell line from adherence to growth in suspension

Vaccine

Volumn 33, Issue 35, 2015, Pages 4269-4280

  Kluge, Sabine ^a   Benndorf, Dirk ^a   Genzel, Yvonne ^b   Scharfenberg, Klaus ^c   Rapp, Erdmann ^b   Reichl, Udo ^a,b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR DYNAMICS OF COMPLEX TECHNICAL SYSTEMS   (Germany)

^c UNIVERSITY OF APPLIED SCIENCES EMDEN LEER   (Germany)

Author keywords

2 D DIGE; Cell culture engineering; Cell line adaptation; Chemically defined medium; Gel map; MALDI TOF MS MS

Indexed keywords

LACTOYLGLUTATHIONE LYASE; PROTEOME; SULFOTRANSFERASE 1A1; MYOSIN; SERUM-FREE MEDIUM;

ANIMAL CELL; ARTICLE; CARCINOGENICITY; CELL ADHESION; CELL GROWTH; CELL METABOLISM; CELL SUSPENSION; CONTROLLED STUDY; INFORMATION PROCESSING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; ADAPTATION; ANIMAL; CELL PROLIFERATION; DOG; GENETICS; METABOLISM; PROCEDURES; SERUM-FREE MEDIUM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL ADHESION; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; DOGS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; LACTOYLGLUTATHIONE LYASE; MADIN DARBY CANINE KIDNEY CELLS; MYOSINS; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84940745261     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.02.077     Document Type: Article

References (65)

1. Kildegaard H.F., Baycin-Hizal D., Lewis N.E., Betenbaugh M.J. The emerging CHO systems biology era: harnessing the 'omics revolution for biotechnology. Curr Opin Biotechnol 2013, 2:1102-1107.
2. Bandaranayake A.D., Almo S.C. Recent advances in mammalian protein production. FEBS Lett 2014, 588:253-260.
3. Jordan I., Sandig V. Matrix and backstage: cellular substrates for viral vaccines. Viruses 2014, 6:1672-1700.
4. Hess R.D., Weber F., Watson K., Schmitt S. Regulatory, biosafety and safety challenges for novel cells as substrates for human vaccines. Vaccine 2012, 30:2715-2727.
5. Sinacore M.S., Drapeau D., Adamson S.R. Adaptation of mammalian cells to growth in serum-free media. Mol Biotechnol 2000, 15:249-257.
6. Cassio D. Long term culture of MDCK strains alters chromosome content. BMC Res Notes 2013, 6:162.
7. Boerner P., Rindler M.J., Chuman L., Saier M.H. Characterization of chemically and virally transformed variants of Madin-Darby canine kidney (MDCK) epithelial cells. J Cell Physiol 1985, 122:299-307.
8. Shin S.I., Freedman V.H., Risser R., Pollack R. Tumorigenicity of virus-transformed cells in nude mice is correlated specifically with anchorage independent growth in vitro. Proc Natl Acad Sci USA 1975, 72:4435-4439.
9. van Wielink R., Kant-Eenbergen H.C., Harmsen M.M., Martens D.E., Wijffels R.H., Coco-Martin J.M. Adaptation of a Madin-Darby canine kidney cell line to suspension growth in serum-free media and comparison of its ability to produce avian influenza virus to Vero and BHK21 cell lines. J Virol Methods 2011, 171:53-60.
10. Scharfenberg K., Wagner R. A reliable strategy for the achievement of cell lines growing in protein-free medium. Anim Cell Technol: Dev 21st Century [Proc Meet] 1995, 619-623.
11. Chu C., Lugovtsev V., Golding H., Betenbaugh M., Shiloach J. Conversion of MDCK cell line to suspension culture by transfecting with human siat7e gene and its application for influenza virus production. Proc Natl Acad Sci USA 2009, 106:14802-14807.
12. Mohamet L., Lea M.L., Ward C.M. Abrogation of E-cadherin-mediated cellular aggregation allows proliferation of pluripotent mouse embryonic stem cells in shake flask bioreactors. PLoS ONE 2010, 5:e12921.
13. Mise-Omata S., Obata Y., Iwase S., Mise N., Doi T.S. Transient strong reduction of PTEN expression by specific RNAi induces loss of adhesion of the cells. Biochem Biophys Res Commun 2005, 328:1034-1042.
14. Jaluria P., Konstantopoulos K., Betenbaugh M., Shiloach J. Egr1 and Gas6 facilitate the adaptation of HEK-293 cells to serum-free media by conferring enhanced viability and higher growth rates. Biotechnol Bioeng 2008, 99:1443-1452.
15. Lee K.H., Sburlati A., Renner W.A., Bailey J.E. Deregulated expression of cloned transcription factor E2F-1 in Chinese hamster ovary cells shifts protein patterns and activates growth in protein-free medium. Biotechnol Bioeng 1996, 50:273-279.
16. Genzel Y., Reichl U. Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines 2009, 8:1681-1692.
17. Gregersen J.P., Schmitt H.J., Trusheim H., Broker M. Safety of MDCK cell culture-based influenza vaccines. Future Microbiol 2011, 6:143-152.
18. Gröner A., Vorlop J. MDCK cells and methods for the propagation of influenza virus 1996, Kg NVaDGC, DE.
19. Gröner A., Vorlop J. Animal cells and processes for the replication of influenza viruses 1997, Co. CBG, US.
20. Schwartz R., Berry J.M., Subramanian A., Shi X. Non-tumorigenic MDCK cell line for propagating viruses 2010, Medimmune L, US.
21. Lohr V., Genzel Y., Behrendt I., Scharfenberg K., Reichl U. A new MDCK suspension line cultivated in a fully defined medium in stirred-tank and wave bioreactor. Vaccine 2010, 28:6256-6264.
22. Liu J., Mani S., Schwartz R., Richman L., Tabor D.E. Cloning and assessment of tumorigenicity and oncogenicity of a Madin-Darby canine kidney (MDCK) cell line for influenza vaccine production. Vaccine 2010, 28:1285-1293.
23. Li F., Vijayasankaran N., Shen A.Y., Kiss R., Amanullah A. Cell culture processes for monoclonal antibody production. mAbs 2010, 2:466-479.
24. Peschel B., Frentzel S., Laske T., Genzel Y., Reichl U. Comparison of influenza virus yields and apoptosis-induction in an adherent and a suspension MDCK cell line. Vaccine 2013, 31:5693-5699.
25. Luz-Hernández KRdl, Rojas-del Calvo L., Rabasa-Legón Y., Lage-Castellanos A., CastilloVitlloch A., Díaz J., et al. Metabolic and proteomic study of NSO myeloma cell line following the adaptation to protein-free medium. J Proteomics 2008, 71:133-147.
26. Jaluria P., Betenbaugh M., Konstantopoulos K., Frank B., Shiloach J. Application of microarrays to identify and characterize genes involved in attachment dependence in HeLa cells. Metab Eng 2007, 9:241-251.
27. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
28. Vester D., Rapp E., Gade D., Genzel Y., Reichl U. Quantitative analysis of cellular proteome alterations in human influenza A virus-infected mammalian cell lines. Proteomics 2009, 9:3316-3327.
29. Görg A., Obermaier C., Boguth G., Harder A., Scheibe B., Wildgruber R., et al. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 2000, 21:1037-1053.
30. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., et al. TM4: a free, open-source system for microarray data management and analysis. BioTechniques 2003, 34:374-378.
31. Team RDC R: a language and environment for statistical computing 2008, R Foundation for Statistical Computing, Vienna, Austria.
32. Benndorf D., Balcke G.U., Harms H., von Bergen M. Functional metaproteome analysis of protein extracts from contaminated soil and groundwater. ISME J 2007, 1:224-234.
33. Kluge S., Rourou S., Vester D., Majoul S., Benndorf D., Genzel Y., et al. Proteome analysis of virus-host cell interaction: rabies virus replication in Vero cells in two different media. Appl Microbiol Biotechnol 2013, 97:5493-5506.
34. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
35. Vizcaino J.A., Deutsch E.W., Wang R., Csordas A., Reisinger F., Rios D., et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 2014, 32:223-226.
36. Vizcaino J.A., Cote R.G., Csordas A., Dianes J.A., Fabregat A., Foster J.M., et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013, 41:D1063-D1069.
37. Rode C., Senkler M., Klodmann J., Winkelmann T., Braun H.P. GelMap-a novel software tool for building and presenting proteome reference maps. J Proteomics 2011, 74:2214-2219.
38. Consortium U. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 2014, 42:7486.
39. Croft D., Mundo A.F., Haw R., Milacic M., Weiser J., Wu G., et al. The reactome pathway knowledgebase. Nucleic Acids Res 2014, 42:D472-D477.
40. Croft D., O'Kelly G., Wu G., Haw R., Gillespie M., Matthews L., et al. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res 2011, 39:D691-D697.
41. Milacic M., Haw R., Rothfels K., Wu G., Croft D., Hermjakob H., et al. Annotating cancer variants and anti-cancer therapeutics in reactome. Cancers 2012, 4:1180-1211.
42. Vester D., Rapp E., Kluge S., Genzel Y., Reichl U. Virus-host cell interactions in vaccine production cell lines infected with different human influenza A virus variants: a proteomic approach. J Proteomics 2010, 73:1656-1669.
43. Rodrigues M.E., Costa A.R., Henriques M., Cunnah P., Melton D.W., Azeredo J., et al. Advances and drawbacks of the adaptation to serum-free culture of CHO-K1 cells for monoclonal antibody production. Appl Biochem Biotechnol 2013, 169:1279-1291.
44. Lee K., Nelson C.M. New insights into the regulation of epithelial-mesenchymal transition and tissue fibrosis. Int Rev Cell Mol Biol 2012, 294:171-221.
45. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994, 124:619-626.
46. Grossmann J. Molecular mechanisms of detachment-induced apoptosis - Anoikis. Apoptosis 2002, 7:247-260.
47. Rosenblatt J., Raff M.C., Cramer L.P. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 2001, 11:1847-1857.
48. Kondo T., Takeuchi K., Doi Y., Yonemura S., Nagata S., Tsukita S. ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis. J Cell Biol 1997, 139:749-758.
49. Marinari E., Mehonic A., Curran S., Gale J., Duke T., Baum B. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 2012, 484:542-545.
50. Emoto Y. Cellular aggregation facilitates anoikis in MDCK cells. J Physiol Sci 2008, 58:371-380.
51. Sanchez-Ruderisch H., Fischer C., Detjen K.M., Welzel M., Wimmel A., Manning J.C., et al. Tumor suppressor p16 INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J 2010, 277:3552-3563.
52. van den Brule F.A., Price J., Sobel M.E., Lambotte R., Castronovo V. Inverse expression of two laminin binding proteins, 67LR and galectin-3, correlates with the invasive phenotype of trophoblastic tissue. Biochem Biophys Res Commun 1994, 201:388-393.
53. Margadant C., van den Bout I., van Boxtel A.L., Thijssen V.L., Sonnenberg A. Epigenetic regulation of galectin-3 expression by beta1 integrins promotes cell adhesion and migration. J Biol Chem 2012, 287:44684-44693.
54. Gamage N.U., Duggleby R.G., Barnett A.C., Tresillian M., Latham C.F., Liyou N.E., et al. Structure of a human carcinogen-converting enzyme, SULT1A1. Structural and kinetic implications of substrate inhibition. J Biol Chem 2003, 278:7655-7662.
55. Grigoletto A., Lestienne P., Rosenbaum J. The multifaceted proteins Reptin and Pontin as major players in cancer. Biochim Biophys Acta 2011, 1815:147-157.
56. Saletta F., Suryo Rahmanto Y., Richardson D.R. The translational regulator eIF3a: the tricky eIF3 subunit!. Biochim Biophys Acta 2010, 1806:275-286.
57. de Hemptinne V., Rondas D., Toepoel M., Vancompernolle K. Phosphorylation on Thr-106 and NO-modification of glyoxalase I suppress the TNF-induced transcriptional activity of NF-kappaB. Mol Cell Biochem 2009, 325:169-178.
58. Weidle U.H., Eggle D., Klostermann S. L1-CAM as a target for treatment of cancer with monoclonal antibodies. Anticancer Res 2009, 29:4919-4931.
59. Yang Y., Kang P., Gao J., Xu C., Wang S., Jin H., et al. AU-binding factor 1 expression was correlated with metadherin expression and progression of hepatocellular carcinoma. Tumour Biol 2014, 35:2747-2751.
60. Zhu L., Wada M., Usagawa Y., Yasukochi Y., Yokoyama A., Wada N., et al. Overexpression of cathepsin D in malignant melanoma. Fukuoka igaku zasshi=Hukuoka acta medica 2013, 104:370-375.
61. Vepachedu R.S., Menon A., Hussain A.I., Liu J. Evaluation of tumorigenic potential of high yielding cloned MDCK cells for live-attenuated influenza vaccine using in vitro growth characteristics, metastatic gene expression and in vivo nude mice model. Biologicals 2012, 40:482-494.
62. Gnanasekar M., Thirugnanam S., Zheng G., Chen A., Ramaswamy K. Gene silencing of translationally controlled tumor protein (TCTP) by siRNA inhibits cell growth and induces apoptosis of human prostate cancer cells. Int J Oncol 2009, 34:1241-1246.
63. Chen W., Wang H., Tao S., Zheng Y., Wu W., Lian F., et al. Tumor protein translationally controlled 1 is a p53 target gene that promotes cell survival. Cell Cycle 2013, 12:2321-2328.
64. Bommer U.A., Thiele B.J. The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 2004, 36:379-385.
65. Wang H., Wang B., Liao Q., An H., Li W., Jin X., et al. Overexpression of RhoGDI, a novel predictor of distant metastasis, promotes cell proliferation and migration in hepatocellular carcinoma. FEBS Lett 2014, 588:503-508.