Heterologous protein production capacity of mammalian cells cultivated as monolayers and microtissues

Biotechnology and Bioengineering

Volumn 93, Issue 1, 2006, Pages 169-180

  Sanchez Bustamante, Carlota Diaz ^a   Kelm, Jens M ^a   Mitta, Barbara ^a   Fussenegger, Martin ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Cell based therapies; Lentivirus; Proliferation control; Tissue engineering; Vascularization

Indexed keywords

BACTERIA; BIOTECHNOLOGY; DRUG PRODUCTS; GENES; MONOLAYERS; PROTEINS; TISSUE; TISSUE CULTURE;

CELL-BASED THERAPIES; LENTIVIRUS; PROLIFERATION CONTROL; TISUE ENGINEERING; VASCULARIZATION;

CELLS;

ALKALINE PHOSPHATASE; AMYLASE; MACROLIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE THERAPY; GEOBACILLUS STEAROTHERMOPHILUS; HUMAN; HUMAN CELL; LENTIVIRINAE; MAMMAL CELL; MONOLAYER CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN PROCESSING; TISSUE ENGINEERING; VASCULARIZATION; VIRUS PARTICLE;

ALKALINE PHOSPHATASE; ANIMALS; BACILLUS STEAROTHERMOPHILUS; BACTERIAL PROTEINS; CELL CULTURE TECHNIQUES; CELL LINE; CRICETINAE; FEMALE; HUMANS; PREGNANCY PROTEINS; RECOMBINANT PROTEINS; TISSUE CULTURE TECHNIQUES;

ANIMALIA; GEOBACILLUS STEAROTHERMOPHILUS; LENTIVIRUS; MAMMALIA;

EID: 30944447267     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.20679     Document Type: Article

References (87)

1. Abbott A. 2003. Cell culture: Biology's new dimension. Nature 424:870-872.
2. Al-Rubeai M. 1998. Apoptosis and cell culture technology. Adv Biochem Eng Biotechnol 59:225-249.
3. Andersen DC, Krummen L. 2002. Recombinant protein expression for therapeutic applications. Curr Opin Biotechnol 13:117-123.
4. Baker KN, Rendall MH, Hills AE, Hoare M, Freedman RB, James DC. 2001. Metabolic control of recombinant protein N-glycan processing in NS0 and CHO cells. Biotechnol Bioeng 73:188-202.
5. Balcarcel RR, Stephanopoulos G. 2001. Rapamycin reduces hybridoma cell death and enhances monoclonal antibody production. Biotechnol Bioeng 76:1-10.
6. Berger J, Hauber J, Hauber R, Geiger R, Cullen BR. 1988. Secreted placental alkaline phosphatase: A powerful new quantitative indicator of gene expression in eukaryotic cells. Gene 66:1-10.
7. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. 2002. The organizing principle: Microenvironmental influences in the normal and malignant breast. Differentiation 70:537-546.
8. Carvalhal AV, Santos SS, Calado J, Haury M, Carrondo MJ. 2003. Cell growth arrest by nucleotides, nucleosides, and bases as a tool for improved production of recombinant proteins. Biotechnol Prog 19:69-83.
9. Chen K, Liu Q, Xie L, Sharp PA, Wang DI. 2001. Engineering of a mammalian cell line for reduction of lactate formation and high monoclonal antibody production. Biotechnol Bioeng 72:55-61.
10. Cruz HJ, Moreira JL, Carrondo MJ. 1999. Metabolic shifts by nutrient manipulation in continuous cultures of BHK cells. Biotechnol Bioeng 66:104-113.
11. Cukierman E, Pankov R, Stevens DR, Yamada KM. 2001. Taking cell-matrix adhesions to the third dimension. Science 294:1708-1712.
12. Dang CV, Semenza GL. 1999. Oncogenic alterations of metabolism. Trends Biochem Sci 24:68-72.
13. Desoize B, Jardillier J. 2000. Multicellular resistance: A paradigm for clinical resistance? Crit Rev Oncol Hematol 36:193-207.
14. deZengotita VM, Miller WM, Aunins JG, Zhou W. 2000. Phosphate feeding improves high-cell-concentration NS0 myeloma culture performance for monoclonal antibody production. Biotechnol Bioeng 69:566-576.
15. Dove A. 2002. Uncorking the biomanufacturing bottleneck. Nat Biotechnol 20:777-779.
16. Duguay D, Foty RA, Steinberg MS. 2003. Cadherin-mediated cell adhesion and tissue segregation: Qualitative and quantitative determinants. Dev Biol 253:309-323.
17. Fox SR, Patel UA, Yap MG, Wang DI. 2004. Maximizing interferon-gamma production by Chinese hamster ovary cells through temperature shift optimization: Experimental and modeling. Biotechnol Bioeng 85:177-184.
18. Freyer JP. 1998. Decreased mitochondrial function in quiescent cells isolated from multicellular tumor spheroids. J Cell Physiol 176:138-149.
19. Fussenegger M. 2001. The impact of mammalian gene regulation concepts on functional genomic research, metabolic engineering, and advanced gene therapies. Biotechnol Prog 17:1-51.
20. Fussenegger M, Bailey JE. 1998. Molecular regulation of cell-cycle progression and apoptosis in mammalian cells: Implications for biotechnology. Biotechnol Prog 14:807-833.
21. 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.
22. Geserick C, Bonarius HP, Kongerslev L, Hauser H, Mueller PP. 2000. Enhanced productivity during controlled proliferation of BHK cells in continuously perfused bioreactors. Biotechnol Bioeng 69:266-274.
23. Girotto D, Urbani S, Brun P, Renier D, Barbucci R, Abatangelo G. 2003. Tissue-specific gene expression in chondrocytes grown on three-dimensional hyaluronic acid scaffolds. Biomaterials 24:3265-3275.
24. Griffith LG, Naughton G. 2002. Tissue engineering-Current challenges and expanding opportunities. Science 295:1009-1014.
25. Grill J, Lamfers ML, van Beusechem VW, Dirven CM, Pherai DS, Kater M, Van der Valk P, Vogels R, Vandertop WP, Pinedo HM, Curiel DT, Gerritsen WR. 2002. The organotypic multicellular spheroid is a relevant three-dimensional model to study adenovirus replication and penetration in human tumors in vitro. Mol Ther 6:609-614.
26. Hesse F, Wagner R. 2000. Developments and improvements in the manufacturing of human therapeutics with mammalian cell cultures. Trends Biotechnol 18:173-180.
27. Ingber DE. 2002. Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation. Differentiation 70:547-560.
28. Irani N, Wirth M, van Den Heuvel J, Wagner R. 1999. Improvement of the primary metabolism of cell cultures by introducing a new cytoplasmic pyruvate carboxylase reaction. Biotechnol Bioeng 66:238-246.
29. Jacks T, Weinberg RA. 2002. Taking the study of cancer cell survival to a new dimension. Cell 111:923-925.
30. Juliano RL. 2002. Signal transduction by cell adhesion receptors and the cytoskeleton: Functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42: 283-323.
31. 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.
32. Kaufmann H, Mazur X, Marone R, Bailey JE, Fussenegger M. 2001. Comparative analysis of two controlled proliferation strategies regarding product quality, influence on tetracycline-regulated gene expression, and productivity. Biotechnol Bioeng 72:592-602.
33. Kelm JM, Fussenegger M. 2004. Microscale tissue engineering using gravity-enforced cell assembly. Trends Biotechnol 22:195-202.
34. Kelm JM, Timmins NE, Brown CJ, Fussenegger M, Nielsen LK. 2003. Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types. Biotechnol Bioeng 83:173-180.
35. Kelm JM, Ehler E, Nielsen LK, Schlatter S, Perriard JC, Fussenegger M. 2004. Design of artificial myocardial microtissues. Tissue Eng 10:201-214.
36. Kelm JM, Diaz Sanchez-Bustamante C, Ehler E, Hoerstrup SP, Djonov V, Ittner L, Fussenegger M. 2005. VEGF profiling and angiogenesis in human microtissues. J Biotechnol 118:213-229.
37. Khalil M, Shariat-Panahi A, Tootle R, Ryder T, McCloskey P, Roberts E, Hodgson H, Selden C. 2001. Human hepatocyte cell lines proliferating as cohesive spheroid colonies in alginate markedly upregulate both synthetic and detoxificatory liver function. J Hepatol 34:68-77.
38. Kim NS, Lee GM. 2000. Overexpression of bcl-2 inhibits sodium butyrate-induced apoptosis in Chinese hamster ovary cells resulting in enhanced humanized antibody production. Biotechnol Bioeng 71:184-193.
39. Kim MS, Kim NS, Sung YH, Lee GM. 2002. Biphasic culture strategy based on hyperosmotic pressure for improved humanized antibody production in Chinese hamster ovary cell culture. In Vitro Cell Dev Biol Anim 38:314-319.
40. Knibbs RN, Dame M, Allen MR, Ding Y, Hillegas WJ, Varani J, Stoolman LM. 2003. Sustained high-yield production of recombinant proteins in transiently transfected COS-7 cells grown on trimethylamine-coated (hillex) microcarrier beads. Biotechnol Prog 19:9-13.
41. Kramer BP, Fussenegger M. 2005. Hysteresis in a synthetic mammalian gene network. Proc Natl Acad Sci USA 102:9517-9522.
42. Kretzmer G. 2002. Industrial processes with animal cells. Appl Microbiol Biotechnol 59:135-142.
43. Kunz-Schughart LA, Habbersett RC, Freyer JP. 1997. Mitochondrial function in oncogene-transfected rat fibroblasts isolated from multicellular spheroids. Am J Physiol 273:C1487-C1495.
44. Kunz-Schughart LA, Doetsch J, Mueller-Klieser W, Groebe K. 2000. Proliferative activity and tumorigenic conversion: Impact on cellular metabolism in 3-D culture. Am J Physiol Cell Physiol 278:C765-C780.
45. Kunz-Schughart LA, Habbersett RC, Freyer JP. 2001. Impact of proliferate activity and tumorigenic conversion on mitochondrial function of fibroblasts in 2D and 3D culture. Cell Biol Int 25:919-930.
46. Kunz-Schughart LA, Wenninger S, Neumeier T, Seidl P, Knuechel R. 2003. Three-dimensional tissue structure affects sensitivity of fibroblasts to TGF-beta 1. Am J Physiol Cell Physiol 284:C209-C219.
47. Li S, Lao J, Chen BP, Li YS, Zhao Y, Chu J, Chen KD, Tsou TC, Peck K, Chien S. 2003. Genomic analysis of smooth muscle cells in 3-dimensional collagen matrix. FASEB J 17:97-99.
48. Lysaght MJ, Reyes J. 2001. The growth of tissue engineering. Tissue Eng 7:485-493.
49. Martin I, Dozin B, Quarto R, Cancedda R, Beltrame F. 1997. Computer-based technique for cell aggregation analysis and cell aggregation in in vitro chondrogenesis. Cytometry 28:141-146.
50. Mastrangelo AJ, Hardwick JM, Zou S, Betenbaugh MJ. 2000. Part II. Overexpression of bcl-2 family members enhances survival of mammalian cells in response to various culture insults. Biotechnol Bioeng 67:555-564.
51. Mazur X, Fussenegger M, Renner WA, Bailey JE. 1998. Higher productivity of growth-arrested Chinese hamster ovary cells expressing the cyclin-dependent kinase inhibitor p27. Biotechnol Prog 14:705-713.
52. Meents H, Enenkel B, Eppenberger HM, Werner RG, Fussenegger M. 2002a. Impact of coexpression and coamplification of sICAM and antiapoptosis determinants bcl-2/bcl-x(L) on productivity, cell survival, and mitochondria number in CHO-DG44 grown in suspension and serum-free media. Biotechnol Bioeng 80:706-716.
53. Meents H, Enenkel B, Werner RG, Fussenegger M. 2002b. p27Kip1-mediated controlled proliferation technology increases constitutive sICAM production in CHO-DUKX adapted for growth in suspension and serum-free media. Biotechnol Bioeng 79:619-627.
54. Messerli JM, van der Voort HT, Rungger-Brandle E, Perriard JC. 1993. Three-dimensional visualization of multi-channel volume data: The amSFP algorithm. Cytometry 14:725-735.
55. Mitta B, Rimann M, Ehrengruber MU, Ehrbar M, Djonov V, Kelm J, Fussenegger M. 2002. Advanced modular self-inactivating lentiviral expression vectors for multigene interventions in mammalian cells and in vivo transduction. Nucleic Acids Res 30:e113.
56. Mueller PP, Schlenke P, Nimtz M, Conradt HS, Hauser H. 1999. Recombinant glycoprotein product quality in proliferation-controlled BHK-21 cells. Biotechnol Bioeng 65:529-536.
57. Mueller-Klieser W. 1997. Three-dimensional cell cultures: From molecular mechanisms to clinical applications. Am J Physiol 273:C1109-C1123.
58. Muschler J, Levy D, Boudreau R, Henry M, Campbell K, Bissell MJ. 2002. A role for dystroglycan in epithelial polarization: Loss of function in breast tumor cells. Cancer Res 62:7102-7109.
59. Muschler GF, Nakamoto C, Griffith LG. 2004. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am 86A:1541-1558.
60. Petroll WM, Cavanagh HD, Jester JV. 2004. Dynamic three-dimensional visualization of collagen matrix remodeling and cytoskeletal organization in living corneal fibroblasts. Scanning 26:1-10.
61. Proud CG. 2005. eIF2 and the control of cell physiology. Semin Cell Dev Biol 16:3-12.
62. Radisky D, Muschler J, Bissell MJ. 2002. Order and disorder: The role of extracellular matrix in epithelial cancer. Cancer Invest 20:139-153.
63. Reiser J, Harmison G, Kluepfel-Stahl S, Brady RO, Karlsson S, Schubert M. 1996. Transduction of nondividing cells using pseudotyped defective high-liter HIV type 1 particles. Proc Natl Acad Sci USA 93:15266-15271.
64. Roskelley CD, Srebrow A, Bissell MJ. 1995. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr Opin Cell Biol 7:736-747.
65. Santini MT, Rainaldi G, Indovina PL. 2000. Apoptosis, cell adhesion, and the extracellular matrix in the three-dimensional growth of multicellular tumor spheroids. Crit Rev Oncol Hematol 36:75-87.
66. Schlatter S, Bailey JE, Fussenegger M. 2001. Novel surface tagging technology for selection of complex proliferation-controlled mammalian cell phenotypes. Biotechnol Bioeng 75:597-606.
67. Schlatter S, Rimann M, Kelm J, Fussenegger M. 2002. SAMY, a novel mammalian reporter gene derived from Bacillus stearothermophilus alpha-amylase. Gene 282:19-31.
68. Schmeichel KL, Bissell MJ. 2003. Modeling tissue-specific signaling and organ function in three dimensions. J Cell Sci 116:2377-2388.
69. Schuetz EG, Li D, Omiecinski CJ, Muller-Eberhard U, Kleinman HK, Elswick B, Guzelian PS. 1988. Regulation of gene expression in adult rat hepatocytes cultured on a basement membrane matrix. J Cell Physiol 134:309-323.
70. Sheehan DC, Hrapchak BB. 1980. Theory and practice of histotechnology. Ohio: Battelle Press.
71. Siegwart P, Cote J, Male K, Luong JH, Perrier M, Kamen A. 1999. Adaptive control at low glucose concentration of HEK-293 cell serum-free cultures. Biotechnol Prog 15:608-616.
72. Smith PG, Burchill SA, Brooke D, Coletta PL, Whitehouse A. 2005. Efficient infection and persistence of a herpesvirus saimiri-based gene delivery vector into human tumor xenografts and multicellular spheroid cultures. Cancer Gene Ther 12:248-256.
73. St. Croix B, Florenes VA, Rak JW, Flanagan M, Bhattacharya N, Slingerland JM, Kerbel RS. 1996. Impact of the cyclin-dependent kinase inhibitor p27Kip1 on resistance of tumor cells to anticancer agents. Nat Med 2:1204-1210.
74. Timmins NE, Dietmair S, Nielsen LK. 2004. Hanging-drop multicellular spheroids as a model of tumour angiogenesis. Angiogenesis 7:97-103.
75. 1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17:176-180.
76. Vournakis JN, Runstadler PW, Jr. 1991. Optimization of the microenvironment for mammalian cell culture in flexible collagen microspheres in a fluidized-bed bioreactor. Biotechnology 17:305-326.
77. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. 1997. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137:231-245.
78. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ. 2002. Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2:205-216.
79. Weber W, Fux C, Daoud-el Baba M, Keller B, Weber CC, Kramer BP, Heinzen C, Aubel D, Bailey JE, Fussenegger M. 2002. Macrolide-based transgene control in mammalian cells and mice. Nat Biotechnol 20:901-907.
80. Weber W, Rimann M, Spielmann M, Keller B, Daoud-El Baba M, Aubel D, Weber CC, Fussenegger M. 2004. Gas-inducible transgene expression in mammalian cells and mice. Nat Biotechnol 22:1440-1444.
81. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. 2004. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692:103-119.
82. Wu MH, Dimopoulos G, Mantalaris A, Varley J. 2004. The effect of hyperosmotic pressure on antibody production and gene expression in the GS-NS0 cell line. Biotechnol Appl Biochem 40:41-46.
83. Wurm FM. 2004. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat Biotechnol 22:1393-1398.
84. Yamada KM, Pankov R, Cukierman E. 2003. Dimensions and dynamics in integrin function. Braz J Med Biol Res 36:959-966.
85. Zahir N, Weaver VM. 2004. Death in the third dimension: Apoptosis regulation and tissue architecture. Curr Opin Genet Dev 14:71-80.
86. Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107-117.
87. Zhang S. 2004. Beyond the petri dish. Nat Biotechnol 22:151-152.