A new biological strategy for high productivity of recombinant proteins in animal cells by the use of hypoxia-response enhancer

Biotechnology and Bioengineering

Volumn 67, Issue 2, 2000, Pages 157-164

  Masuda, Seiji ^a   Moon, Sung Kwon ^a   Kambe, Taiho ^a   Nagao, Masaya ^a   Sasaki, Ryuzo ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Chinese hamster ovary cell; Erythropoietin; Hypoxia response enhancer; Lactate dehydrogenase A; Low oxygen concentration

Indexed keywords

ANIMAL CELL CULTURE; CATALYST ACTIVITY; ENZYMES; GENES; ONCOLOGY; OXYGEN; PHYSIOLOGICAL MODELS;

HUMAN ERYTHROPROTEIN; HYPOXIA-RESPONSE ENHANCER; RECOMBINANT PROTEINS;

GENETIC ENGINEERING;

RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION; GENE SEQUENCE; HYPOXIA; NONHUMAN; PROMOTER REGION; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS;

ANIMALS; BASE SEQUENCE; CARBOHYDRATES; CELL HYPOXIA; CHO CELLS; COBALT; CRICETINAE; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); ERYTHROPOIETIN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; OXYGEN; PROMOTER REGIONS (GENETICS); PROTEIN ENGINEERING; RECOMBINANT PROTEINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0034688276     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0290(20000120)67:2<157::AID-BIT5>3.0.CO;2-B     Document Type: Article

References (59)

1. Archibald AL, McClenaghan M, Hornsey V, Simons JP, Clark AJ. 1990. High-level expression of biologically active human α 1-antitrypsin in the milk of transgenic mice. Proc Natl Acad Sci USA 87:5178-5182.
2. Beck I, Ramirez S, Weinmann R, Caro J. 1991. Enhancer element at the 3′-flanking region controls transcriptional response to hypoxia in the human erythropoietin gene. J Biol Chem 266:15563-15566.
3. Born C, Biselli M, Wandrey C, 1997. Oxygen transfer from the gasphase to the immobilized cells in membrane aerated fluidized beds. In: Funatsu K, Shirai Y, Matsushita T, editors. Animal Cell Technology: Basic & Applied Aspects. Dordrecht, The Netherlands: Kluwer Academic Publishers. Vol 8, p 83-87.
4. Bunn HF, Poyton RO. 1996. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76:839-885.
5. Chung KC, Huang D, Chen Y, Short S, Short ML, Zhang Z, Jungmann RA. 1995. Identification of a silencer module which selectively represses cyclic AMP-responsive element-dependent gene expression. Mol Cell Biol 15:6139-6149.
6. Ebert BL, Firth JD, Ratcliffe PJ. 1995. Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences. J Biol Chem 270:29083-29089.
7. Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. 1994. Oxygen-regulated control elements in the phosphoglycerate kinase I and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc Natl Acad Sci USA 91:6496-6500.
8. Firth JD, Ebert BL, Ratcliffe PJ. 1995. Hypoxic regulation of lactate dehydrogenase A. J Biol Chem 270:21021-21027.
9. Forsythe JA, Jiang B-H, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613.
10. Goldberg MA, Glass GA, Cunningham JM, Bunn HF. 1987. The regulated expression of erythropoietin by two human hepatoma cell lines. Proc Natl Acad Sci USA 84:7972-7976.
11. Goldberg MA, Dunning SP, Bunn HF. 1988. Regulation of the erythropoietin gene: Evidence that the oxygen sensor is a heme protein. Science 242:1412-1415.
12. Goldwasser E, Gross M. 1975. Erythropoietin: Assay and study of its mode of action. Methods Enzymol 37:109-121.
13. Goto M, Akai K, Murakami A, Hashimoto C, Tsuda E, Ueda M, Kawanishi G, Takahashi N, Ishimoto A, Chiba H, Sasaki R. 1988. Production of recombinant erythropoietin in mammalian cells: Host cell dependency of the biological activity of the cloned glycoprotein. Bio/Technology 6:67-71.
14. Goto M, Murakami A, Akai K, Kawanishi G, Ueda M, Chiba H, Sasaki R. 1989. Characterization and use of monoclonal antibodies directed against human erythropoietin that recognize different antigenic determinants. Blood 74:1415-1423.
15. Gordon K, Lee E, Vitale JA, Smith AE, Westphal H, Hennighausen L. 1987. Production of human tissue plasminogen activator in transgenic mouse milk, Bio/Technology 5:1183-1187.
16. Guillemin K, Krasnow MA. 1997. The hypoxic response: Huffing and HIFing. Cell 89:9-12.
17. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95:7987-7992.
18. Jänne J, Hyttinen J-M, Peura T, Tolvanen M, Alhonen L, Sinervirta R, Halmekytö M. 1994. Transgenic bioreactors. Int J Biochem 26: 859-870.
19. Jiang B-H, Rue E, Wang GL, Roe R, Semenza GL. 1996. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 271:17771-17778.
20. Kambe T, Tada J, Chikuma M, Masuda S, Nagao M, Tsuchiya T, Ratcliffe PJ, Sasaki R. 1998. Embryonal carcinoma P19 cells produce erythropoietin constitutively but express lactate dehydrogenase in an oxygen-dependent manner. Blood 91:1185-1195.
21. Kelly BD, Chiou TW, Rosenberg M, Wang DIC. 1993. In: Rehm HJ, Reed G, Puhler A, Stadler P, editors. Industrial animal cell culture: Biotechnology. Weinheim: VCH. Vol 3, p 23-38.
22. Kondo A. Suzuki J, Kuraya N, Hase S, Kato I, Ikenaka T. 1990. Improved method for fluorescence labeling of sugar chains with sialic acid residues. Agric Biol Chem 54:2169-2170.
23. Korhonen V-P, Tolvanen M, Hyttinen J-M, Uusi-Oukari M, Sinervirta R, Alhonen L, Jauhiainen M, Jänne OA, Jänne J. 1997. Expression of bovine β-lactoglobulin/human erythropoietin fusion protein in the milk of transgenic mice and rabbits. Eur J Biochem 245:482-489.
24. Lee PJ, Jiang B-H, Chin BY, Lyer NV, Alam J, Semenza GL, Choi AMK. 1997. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in resonse to hypoxia. J Biol Chem 272:5375-5381.
25. Levy AP, Levy NS, Wegner S, Goldberg MA. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270:13333-13340.
26. Li H, Ko HP, Whitlock JP Jr. 1996. Induction of phosphoglycerate kinase I gene expression by hypoxia: Roles of ARNT aqnd HIF1α. J Biol Chem 271:21262-21267.
27. Liu Y, Cox SR, Morita T, Kourembanas S. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells: identification of a 5′ enhancer. Cir Res 77:638-643.
28. Marken CL, Shaklee JB, Whitt GS. 1975. Evolution of a gene: Multiple genes for LDH isozymes provide a model of the evolution of gene structure, function, and regulation. Science 189:102-114.
29. Massoud M, Attal J, Thepot D, Pointu H, Stinnakre MG, Theron MC, Lopez C, Houdebine LM. 1996. The deleterious effects of human erythropoietin gene driven by the rabbit whey acidic protein gene promoter in transgenic rabbits. Reprod Nutr Dev 36:555-563.
30. Maxwell PH, Pugh CW, Ratcliffe PJ. 1993. Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: Evidence for a widespread oxygen-sensing mechanism. Proc Natl Acad Sci USA 90: 2423-2427.
31. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. 1995. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182: 1683-1693.
32. Moon SK, Takeuchi S, Kambe T, Tsuchiya T, Masuda S, Nagao M, Sasaki R. 1997. Erythropoietin enhancer stimulates production of a recombinant protein by Chinese hamster ovary (CHO) cells under hypoxic condition. Cytotechnology 25:79-88.
33. Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R. 1997. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76:105-116.
34. Okano M, Suga H, Masuda S, Nagao M, Narita H, Ikura K, Sasaki R. 1993. Characterization of erythropoietin isolated from rat serum: Biochemical comparison of rat and human erythropoietins. Biosci Biotechnol Biochem 57:1882-1885.
35. Prunkard D, Cottingham I, Garner I, Bruce S, Dalrymple M, Lasser G, Bishop P, Foster D. 1996. High-level expression of recombinant human fibrinogen in the milk of transgenic mice Nat Biotechnol 14: 867-871.
36. Pugh CW, Tan CC, Jones RW, Ratcliffe PJ. 1991. Functional analysis of an oxygen-regulated transcriptional enhancer lying 3′ to the mouse erythropoietin gene. Proc Natl Acad Sci USA 88:10553-10557.
37. Ratcliffe PJ, O'Rourke JF, Maxwell PH, Pugh CW. 1998. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 201:1153-1162.
38. Rodriguez A, Castro FO, Aguilar A, Ramos B, Del-Barco DG, Lleonart R, De-la-Fuente J. 1995. Expression of active human erythropoietin in the mammary gland of lactating transgenic mice and rabbits. Biol Res 28:141-153.
39. Rolfs A, Kvietikova I, Gassmann M, Wenger RH. 1997. Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J Biol Chem 272:20055-20062.
40. Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, Sasaki R. 1998. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA 95:4635-4640.
41. Salceda S, Caro J. 1997. Hypoxia-inducible factor1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. J Biol Chem 272:22642-22647.
42. Sasaki R, Yanagawa S, Chiba H. 1987. Isolation of human erythropoietin with monoclonal antibodies. Methods Enzymol 147:328-340.
43. Semenza GL, Wang GL. 1992. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12:5447-5454.
44. Semenza GL, Roth PH, Fang H-M, Wang GL. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269:23757-23763.
45. Semenza GL, Jiang B-H, Leung SW, Passantino R, Concordet J-P, Maire P, Giallongo A. 1996. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essen-tial binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537.
46. Semenza GL. 1998. Hypoxia-inducible factor 1 and the molecular physiology of oxygen homeostasis. J Lab Clin Med 131:207-214.
47. Shweiki D, Itin A, Soffer D, Keshet E. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843-845.
48. Trocha M, von Rohr R. 1997. Large-scale bubble bed aeration for animal cell cultures. In: Carrondo MJT, Griffiths B, Moreira JLP, editors. Animal Cell Technology. Dordrecht, The Netherlands: Kluwer Academic Publishers, p 399-404.
49. Tsuda E, Kawanishi G, Ueda M, Masuda S, Sasaki R. 1990. The role of carbohydrate in recombinant human erythropoietin. Eur J Biochem 188:405-411.
50. Uusi-Oukari M, Hyttinen J-M, Korhonen VP, Vasti A, Alhonen L, Jänne OA, Jänne J. 1997. Bovine a s1-casein gene sequences direct high level expression of human granulocyte-macrophage colony-stimulating factor in the milk of transgenic mice. Transgenic Res 6: 75-84.
51. Velander WH, Page RL, Morcol T, Russell CG, Canseco R, Young JM, Drohan WN, Gwazdauskas FC, Wilkins TD, Johnson JL. 1992. Production of biologically active human protein C in the milk of transgenic mice. Ann NY Acad Sci 665:391-403.
52. Wang GL, Semenza GL. 1993a. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90:4304-4308.
53. Wang GL, Semenza GL. 1993b. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem 268:21513-21518.
54. Wang GL, Semenza GL. 1995. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270:1230-1237.
55. 2 tension. Proc Natl Acad Sci USA 92:5510-5514.
56. Wenger RH, Gassmann M. 1997. Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 378:609-616.
57. Wright G, Carver A, Cottom D, Reeves D, Scott A, Simons P, Wilmut I, Garner I, Colman A. 1991. High level expression of active human α-1-antitrypsin in the milk of transgenic sheep. Bio/Technology 9: 830-834.
58. Yamaguchi K, Akai K, Kawanishi G, Ueda M, Masuda S, Sasaki R. 1991. Effects of site-directed removal of N-glycosylation sites in human erythropoietin on its production and biological properties. J Biol Chem 266:20434-20439.
59. Yasuda Y, Masuda S, Chikuma M, Inoue K, Nagao M, Sasaki R. 1998. Estrogen-dependent production of erythropoietin in uterus and its implication in uterine angiogenesis. J Biol Chem 273:25381-25387.