Microarray and proteomics expression profiling identifies several candidates, including the Valosin-Containing Protein (VCP), involved in regulating high cellular growth rate in production CHO cell lines

Biotechnology and Bioengineering

Volumn 106, Issue 1, 2010, Pages 42-56

  Doolan, Padraig ^a   Meleady, Paula ^a   Barron, Niall ^a   Henry, Michael ^a   Gallagher, Ross ^a   Gammell, Patrick ^b   Melville, Mark ^b   Sinacore, Martin ^c   McCarthy, Kevin ^b   Leonard, Mark ^b   Charlebois, Timothy ^b   Clynes, Martin ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b PFIZER INC   (United States)

^c BIOGEN   (United States)

Author keywords

CHO; Growth rate; Microarray; Proteomics; VCP

Indexed keywords

CELLULAR GROWTH RATE; CHINESE HAMSTER OVARY CELLS; CHO; CHO CELL; DATA SETS; EXPRESSION PROFILING; FUNCTIONAL VALIDATION; GENE KNOCK DOWN; GENE TRANSCRIPTS; HIGH GROWTH RATE; HIGH RATE; OVER-EXPRESSION; PHASE CULTURE; PRIORITY LIST; PRODUCTION CELLS; PRODUCTION CULTURE; PROTEOMICS; SCALE-UP; SLOW GROWTH RATES; STATISTICAL ANALYSIS;

CELL GROWTH; CELL PROLIFERATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GROWTH KINETICS; GROWTH RATE; MOLECULAR BIOLOGY; PROTEINS; RNA;

CELL CULTURE;

ACTIN RELATED PROTEIN; ALPHA ENOLASE; COMPLEMENTARY DNA; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 27; MONOCLONAL ANTIBODY; SMALL INTERFERING RNA; VALOSIN CONTAINING PROTEIN;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CHO CELL; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GROWTH RATE; NONHUMAN; PHENOTYPE; PROTEOMICS; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; EPITHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SILENCING; PROTEOME; RNA, SMALL INTERFERING; UP-REGULATION;

CRICETULUS GRISEUS;

EID: 77951555640     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22670     Document Type: Article

References (74)

1. Altamirano C, Paredes C, Cairo JJ, Godia F. 2000. Improvement of CHOcell culture medium formulation: Simultaneous substitution of glucose and glutamine. Biotechnol Prog 16:69-75.
2. Anderson L, Seilhamer J. 1997. A comparison of selectedmRNA and protein abundances in human liver. Electrophoresis 18:533-537.
3. Ansell R, Granath K, Hohmann S, Thevelein JM, Adler L. 1997. The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16:2179-2187.
4. Arden N, Majors BS, Ahn SH, Oyler G, Betenbaugh MJ. 2007. Inhibiting the apoptosis pathway using MDM2 in mammalian cell cultures. Biotechnol Bioeng 97:601-614.
5. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, Parthasarathy S, Petros JA, Lambeth JD. 2001. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci USA 98:5550-5555.
6. Asai T, Tomita Y, Nakatsuka S, Hoshida Y, Myoui A, Yoshikawa H, Aozasa K. 2002. VCP (p97) regulates NFkappaB signaling pathway, which is important for metastasis of osteosarcoma cell line. Jpn J Cancer Res 93:296-304.
7. Baik JY, Lee MS, An SR, Yoon SK, Joo EJ, Kim YH, Park HW, Lee GM. 2006. Initial transcriptome and proteome analyses of low culture temperature-induced expression in CHO cells producing erythropoietin. Biotechnol Bioeng 93:361-371.
8. Baik JY, Joo EJ, Kim YH, Lee GM. 2008. Limitations to the comparative proteomic analysis of thrombopoietin producing Chinese hamster ovary cells treated with sodium butyrate. J Biotechnol 133:461-468.
9. Bandyopadhyay A, Matsumoto T, Maitra U. 2000. Fission yeast Int6 is not essential for global translation initiation, but deletion of int6(+) causes hypersensitivity to caffeine and affects spore formation. Mol Biol Cell 11:4005-4018.
10. Berrios J, Diaz-Barrera A, Bazan C, Altamirano C. 2009. Relationship between tissue plasminogen activator production and specific growth rate in Chinese Hamster Ovary cells cultured in mannose at low temperature. Biotechnol Lett 10:1493-1497
11. Bertram C, von Neuhoff N, Skawran B, Steinemann D, Schlegelberger B, Hass R. 2008. The differentiation/retrodifferentiation program of human U937 leukemia cells is accompanied by changes of VCP/p97. BMC Cell Biol 9:12.
12. Butler M. 2005. Animal cell cultures: Recent achievements and perspectives in the production of biopharmaceuticals. Appl Microbiol Biotechnol 68:283-291.
13. Clerch B, Rivera E, Llagostera M. 1996. Identification of a pKM101 region which confers a slow growth rate and interferes with susceptibility to quinolone in Escherichia coli AB1157. J Bacteriol 178:5568-5572.
14. Dai RM, Chen E, Longo DL, Gorbea CM, Li CC. 1998. Involvement of valosin-containing protein, an ATPase Co-purified with IkappaBalpha and 26S proteasome, in ubiquitin-proteasome-mediated degradation of IkappaBalpha. J Biol Chem 273:3562-3573.
15. De Leon Gatti M, Wlaschin KF, Nissom PM, Yap M, Hu WS. 2007. Comparative transcriptional analysis of mouse hybridoma and recombinant Chinese hamster ovary cells undergoing butyrate treatment. J Biosci Bioeng 103:82-91. (Pubitemid 46216907)
16. de Nobel H, Lawrie L, Brul S, Klis F, Davis M, Alloush H, Coote P. 2001. Parallel and comparative analysis of the proteome and transcriptome of sorbic acid-stressed Saccharomyces cerevisiae. Yeast 18:1413-1428.
17. Doolan P, Melville M, Gammell P, Sinacore M, Meleady P, McCarthy K, Francullo L, Leonard M, Charlebois T, Clynes M. 2008. Transcriptional profiling of gene expression changes in a PACE-transfected CHO DUKX cell line secreting high levels of rhBMP-2. Mol Biotechnol 39:187-199.
18. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868. (Pubitemid 29003722)
19. Ferrer M, Chernikova TN, Yakimov MM, Golyshin PN, Timmis KN. 2003. Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21:1266-1267. (Pubitemid 37356602)
20. Figueroa B, Jr., Ailor E, Osborne D, Hardwick JM, Reff M, Betenbaugh MJ. 2007. Enhanced cell culture performance using inducible anti-apoptotic genes E1B-19K and Aven in the production of a monoclonal antibody with Chinese hamster ovary cells. Biotechnol Bioeng 97:877-892. (Pubitemid 47051057)
21. Freemerman AJ, Powis G. 2000. A redox-inactive thioredoxin reduces growth and enhances apoptosis in WEHI7.2 cells. Biochem Biophys Res Commun 274:136-141. (Pubitemid 30496769)
22. Fussenegger M, Schlatter S, Datwyler D, Mazur X, Bailey JE. 1998. Controlled proliferation by multigene metabolic engineering enhances the productivity of Chinese hamster ovary cells. Nat Biotechnol 16:468-472. (Pubitemid 28211201)
23. Gervais M, Dugourd C, Muller L, Ardidie C, Canton B, Loviconi L, Corvol P, Chneiweiss H, Monnot C. 2006. Akt down-regulates ERK1/2 nuclear localization and angiotensin II-induced cell proliferation through PEA-15. Mol Biol Cell 17:3940-3951. (Pubitemid 44330878)
24. Gupta P, Aggarwal N, Batra P, Mishra S, Chaudhuri TK. 2006. Co-expression of chaperonin GroEL/GroES enhances in vivo folding of yeast mitochondrial aconitase and alters the growth characteristics of Escherichia coli. Int J Biochem Cell Biol 38:1975-1985. (Pubitemid 44425254)
25. Gygi SP, Rochon Y, Franza BR, Aebersold R. 1999. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720-1730. (Pubitemid 29098230)
26. Hayduk EJ, Lee KH. 2005. Cytochalasin D can improve heterologous protein productivity in adherent Chinese hamster ovary cells. Biotechnol Bioeng 90:354-364.
27. Horman S, Del Bino G, Fokan D, Mosselmans R, Galand P. 2000. Effect of the serine protease inhibitor N-tosyl-l-phenylalanine-chloromethyl ketone (TPCK) on MCF-7 mammary tumour cells growth and differentiation. Cell Biol Int 24:153-161.
28. Hwang SO, Lee GM. 2009. Effect of Akt overexpression on programmed cell death in antibody-producing Chinese hamster ovary cells. J Biotechnol 139:89-94.
29. Ifandi V, Al-Rubeai M. 2003. Stable transfection of CHO cells with the c-myc gene results in increased proliferation rates, reduces serum dependency, and induces anchorage independence. Cytotechnology 41:1-10. (Pubitemid 36875117)
30. Ifandi V, Al-Rubeai M. 2005. Regulation of cell proliferation and apoptosis in CHO-K1 cells by the coexpression of c-Myc and Bcl-2. Biotechnol Prog 21:671-677.
31. Jaluria P, Betenbaugh M, Konstantopoulos K, Shiloach J. 2007. Enhancement of cell proliferation in various mammalian cell lines by gene insertion of a cyclin-dependent kinase homolog. BMC Biotechnol 7:71.
32. Kaufmann H, Mazur X, Fussenegger M, Bailey JE. 1999. Influence of low temperature on productivity, proteome and protein phosphorylation of CHO cells. Biotechnol Bioeng 63:573-582.
33. Klein JB, Barati MT, Wu R, Gozal D, Sachleben LR, Jr., Kausar H, Trent JO, Gozal E, Rane MJ. 2005. Akt-mediated valosin-containing protein 97 phosphorylation regulates its association with ubiquitinated proteins. J Biol Chem 280:31870-31881.
34. Korke R, Rink A, Seow TK, Chung MC, Beattie CW, Hu WS. 2002. Genomic and proteomic perspectives in cell culture engineering. J Biotechnol 94:73-92.
35. Korke R, Gatti Mde L, Lau AL, Lim JW, Seow TK, Chung MC, Hu WS. 2004. Large scale gene expression profiling of metabolic shift of mammalian cells in culture. J Biotechnol 107:1-17.
36. Krampe B, Swiderek H, Al-Rubeai M. 2008. Transcriptome and proteome analysis of antibody-producing mouse myeloma NS0 cells cultivated at different cell densities in perfusion culture. Biotechnol Appl Biochem 50:133-141.
37. Kumar N, Gammell P, Clynes M. 2007. Proliferation control strategies to improve productivity and survival during CHO based production culture: A summary of recent methods employed and the effects of proliferation control in product secreting CHO cell lines. Cytotechnology 53:33-46.
38. Lee MS, Kim KW, Kim YH, Lee GM. 2003. Proteome analysis of antibody-expressing CHO cells in response to hyperosmotic pressure. Biotechnol Prog 19:1734-1741.
39. Lipscomb ML, Palomares LA, Hernandez V, Ramirez OT, Kompala DS. 2005. Effect of production method and gene amplification on the glycosylation pattern of a secreted reporter protein in CHO cells. Biotechnol Prog 21:40-49.
40. Livingstone M, Ruan H, Weiner J, Clauser KR, Strack P, Jin S, Williams A, Greulich H, Gardner J, Venere M, Mochan TA, DiTullio RA, Jr., Moravcevic K, Gorgoulis VG, Burkhardt A, Halazonetis TD. 2005. Valosin-containing protein phosphorylation at Ser784 in response to DNA damage. Cancer Res 65:7533-7540.
41. Maddika S, Ande SR, Panigrahi S, Paranjothy T, Weglarczyk K, Zuse A, Eshraghi M, Manda KD, Wiechec E, Los M. 2007. Cell survival, cell death and cell cycle pathways are interconnected: Implications for cancer therapy. Drug Resist Updat 10:13-29.
42. Mairesse N, Bernaert D, Del Bino G, Horman S, Mosselmans R, Robaye B, Galand P. 1998. Expression of HSP27 results in increased sensitivity to tumor necrosis factor, etoposide, and H2O2 in an oxidative stress-resistant cell line. J Cell Physiol 177:606-617.
43. Majors BS, Arden N, Oyler GA, Chiang GG, Pederson NE, Betenbaugh MJ. 2008. E2F-1 overexpression increases viable cell density in batch cultures of Chinese hamster ovary cells. J Biotechnol 138:103-106.
44. Meleady P, Henry M, Gammell P, Doolan P, Sinacore M, Melville M, Francullo L, Leonard M, Charlebois T, Clynes M. 2008. Proteomic profiling of CHO cells with enhanced rhBMP-2 productivity following co-expression of PACEsol. Proteomics 8:2611-2624.
45. Naryzhny SN, Lee H. 2001. Protein profiles of the Chinese hamster ovary cells in the resting and proliferating stages. Electrophoresis 22:1764-1775.
46. Nicolet CM, Craig EA. 1989. Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol Cell Biol 9:3638-3646.
47. Nissom PM, Sanny A, Kok YJ, Hiang YT, Chuah SH, Shing TK, Lee YY, Wong KT, Hu WS, Sim MY, Philp R. 2006. Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol Biotechnol 34:125-140.
48. Pascoe DE, Arnott D, Papoutsakis ET, Miller WM, Andersen DC. 2007. Proteome analysis of antibody-producing CHO cell lines with different metabolic profiles. Biotechnol Bioeng 98:391-410.
49. Peng RW, Fussenegger M. 2009. Molecular engineering of exocytic vesicle traffic enhances the productivity of Chinese hamster ovary cells. Biotechnol Bioeng 102:1170-1181.
50. Prentice HL, Ehrenfels BN, Sisk WP. 2007. Improving performance of mammalian cells in fed-batch processes through "bioreactor evolution." Biotechnol Prog 23:458-464.
51. Qiu Y, Tomita Y, Zhang B, Nakamichi I, Morii E, Aozasa K. 2007. Pre-B-cell leukemia transcription factor 1 regulates expression of valosin-containing protein, a gene involved in cancer growth. Am J Pathol 170:152-159.
52. Seth G, Philp RJ, Lau A, Jiun KY, Yap M, Hu WS. 2007a. Molecular portrait of high productivity in recombinant NS0 cells. Biotechnol Bioeng 97:933-951.
53. Seth G, Charaniya S, Wlaschin KF, Hu WS. 2007b. In pursuit of a super producer-alternative paths to high producing recombinant mammalian cells. Curr Opin Biotechnol 18:557-564.
54. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, Hirano T. 1999. Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11:709-719.
55. Stansfield SH, Allen EE, Dinnis DM, Racher AJ, Birch JR, James DC. 2007. Dynamic analysis of GS-NS0 cells producing a recombinant monoclonal antibody during fed-batch culture. Biotechnol Bioeng 97:410-424.
56. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102:15545-15550. (Pubitemid 41528093)
57. Tigges M, Fussenegger M. 2006. Xbp1-based engineering of secretory capacity enhances the productivity of Chinese hamster ovary cells. Metab Eng 8:264-272.
58. Tome ME, Baker AF, Powis G, Payne CM, Briehl MM. 2001. Catalase-overexpressing thymocytes are resistant to glucocorticoid-induced apoptosis and exhibit increased net tumor growth. Cancer Res 61:2766-2773.
59. Tsujimoto Y, Tomita Y, Hoshida Y, Kono T, Oka T, Yamamoto S, Nonomura N, Okuyama A, Aozasa K. 2004. Elevated expression of valosin-containing protein (p97) is associated with poor prognosis of prostate cancer. Clin Cancer Res 10:3007-3012. (Pubitemid 38619676)
60. Van Dyk DD, Misztal DR, Wilkins MR, Mackintosh JA, Poljak A, Varnai JC, Teber E, Walsh BJ, Gray PP. 2003. Identification of cellular changes associated with increased production of human growth hormone in a recombinant Chinese hamster ovary cell line. Proteomics 3:147-156.
61. Vandermoere F, El Yazidi-Belkoura I, Slomianny C, Demont Y, Bidaux G, Adriaenssens E, Lemoine J, Hondermarck H. 2006. The valosin-containing protein (VCP) is a target of Akt signaling required for cell survival. J Biol Chem 281:14307-14313. (Pubitemid 43848359)
62. Vandermoere F, El Yazidi-Belkoura I, Demont Y, Slomianny C, Antol J, Lemoine J, Hondermarck H. 2007. Proteomics exploration reveals that actin is a signaling target of the kinase Akt. Mol Cell Proteomics 6:114-124. (Pubitemid 46152696)
63. Wang Q, Song C, Li CC. 2004. Molecular perspectives on p97-VCP: Progress in understanding its structure and diverse biological functions. J Struct Biol 146:44-57. (Pubitemid 38369017)
64. Watanabe S, Shuttleworth J, Al-Rubeai M. 2002. Regulation of cell cycle and productivity in NS0 cells by the over-expression of p21CIP1. Biotechnol Bioeng 77:1-7.
65. Wojcik C, Yano M, DeMartino GN. 2004. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J Cell Sci 117:281-292. (Pubitemid 38128906)
66. Wojcik C, Rowicka M, Kudlicki A, Nowis D, McConnell E, Kujawa M, DeMartino GN. 2006. Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol Biol Cell 17:4606-4618. (Pubitemid 44665732)
67. Wong DC, Wong KT, Lee YY, Morin PN, Heng CK, Yap MG. 2006. Transcriptional profiling of apoptotic pathways in batch and fed-batch CHO cell cultures. Biotechnol Bioeng 94:373-382. (Pubitemid 43799536)
68. Wurm FM. 2004. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat Biotechnol 22:1393-1398. (Pubitemid 39482858)
69. Yamamoto S, Tomita Y, Hoshida Y, Sakon M, Kameyama M, Imaoka S, Sekimoto M, Nakamori S, Monden M, Aozasa K. 2004. Expression of valosin-containing protein in colorectal carcinomas as a predictor for disease recurrence and prognosis. Clin Cancer Res 10:651-657. (Pubitemid 38174005)
70. Yamamoto S, Tomita Y, Uruno T, Hoshida Y, Qiu Y, Iizuka N, Nakamichi I, Miyauchi A, Aozasa K. 2005. Increased expression of valosin-containing protein (p97) is correlated with disease recurrence in follicular thyroid cancer. Ann Surg Oncol 12:925-934. (Pubitemid 41504226)
71. Yee JC, de Leon Gatti M, Philp RJ, Yap M, Hu WS. 2007. Genomic and proteome exploration of CHO and hybridoma cells under sodium butyrate treatment. Biotechnol Bioeng 99:1186-1204. (Pubitemid 351462776)
72. Yokota M, Tanji Y. 2008. Analysis of cell-cycle-dependent production of tissue plasminogen activator analogue (pamiteplase) by CHO cells. Biochem Eng J 39:297-304. (Pubitemid 351324181)
73. Yoshida K, Kobayashi K, Miwa Y, Kang CM, Matsunaga M, Yamaguchi H, Tojo S, Yamamoto M, Nishi R, Ogasawara N, Nakayama T, Fujita Y. 2001. Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucleic Acids Res 29:683-692.
74. Zhang B, Tomita Y, Qiu Y, He J, Morii E, Noguchi S, Aozasa K. 2007. E74-like factor 2 regulates valosin-containing protein expression. Biochem Biophys Res Commun 356:536-541.