Biopharmaceutical discovery and production in yeast

Current Opinion in Biotechnology

Volumn 30, Issue , 2014, Pages 120-127

  Meehl, Michael A ^a   Stadheim, Terrance A ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS;

BIOPHARMACEUTICALS; CRITICAL QUALITY; MAMMALIAN HOSTS; POST-TRANSLATIONAL MODIFICATIONS; PRODUCTION SYSTEM; YEAST EXPRESSION;

YEAST;

ALD 403; ANTIBODY; BECAPLERMIN; CALCITONIN GENE RELATED PEPTIDE; CLAZAKIZUMAB; ECALLANTIDE; GLYCAN; INSULIN; OCRIPLASMIN; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RECOMBINANT HUMAN INSULIN; UNCLASSIFIED DRUG; WART VIRUS VACCINE; BIOLOGICAL PRODUCT; RECOMBINANT PROTEIN; GLYCOPROTEIN; PROTEIN DERIVATIVE; RECOMBINANT DNA; RECOMBINANT VACCINE;

ANTIBODY ENGINEERING; ANTIBODY PRODUCTION; BIOENGINEERING; BIOTECHNOLOGICAL PRODUCTION; DRUG MANUFACTURE; DRUG MARKETING; FUNGAL STRAIN; GENE EXPRESSION SYSTEM; GENETIC ENGINEERING; GLYCOSYLATION; HUMAN; NONHUMAN; PHARMACEUTICAL ENGINEERING; PHARMACEUTICS; PRIORITY JOURNAL; REVIEW; YEAST; ANIMAL; GENETICS; METABOLISM; PLANT; PROCEDURES; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE; BIOTECHNOLOGY; DRUG QUALITY; DRUG RESEARCH; DRUG SYNTHESIS; GLYCOENGINEERING; PICHIA ANGUSTA; PICHIA PASTORIS; PROTEIN GLYCOSYLATION; VACCINE PRODUCTION;

ANIMALS; BIOLOGICAL PRODUCTS; GLYCOSYLATION; PLANTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; TECHNOLOGY, PHARMACEUTICAL; YEASTS;

EID: 84903945178     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2014.06.007     Document Type: Review

References (78)

1. Gurramkonda C., Polez S., Skoko N., Adnan A., Gabel T., Chugh D., Swaminathan S., Khanna N., Tisminetzky S., Rinas U. Application of simple fed-batch technique to high-level secretory production of insulin precursor using Pichia pastoris with subsequent purification and conversion to human insulin. Microb Cell Fact 2010, 9:31.
2. Xie T., Liu Q., Xie F., Liu H., Zhang Y. Secretory expression of insulin precursor in Pichia pastoris and simple procedure for producing recombinant human insulin. Prep Biochem Biotechnol 2008, 38:308-317.
3. Berlec A., Strukelj B. Current state and recent advances in biopharmaceutical production in Escherichia coli, yeasts and mammalian cells. J Ind Microbiol Biotechnol 2013, 40:257-274.
4. Celik E., Calik P. Production of recombinant proteins by yeast cells. Biotechnol Adv 2012, 30:1108-1118.
5. Frenzel A., Hust M., Schirrmann T. Expression of recombinant antibodies. Front Immunol 2013, 4:217.
6. Mattanovich D., Branduardi P., Dato L., Gasser B., Sauer M., Porro D. Recombinant protein production in yeasts. Methods Mol Biol 2012, 824:329-358.
7. Spadiut O., Capone S., Krainer F., Glieder A., Herwig C. Microbials for the production of monoclonal antibodies and antibody fragments. Trends Biotechnol 2014, 32:54-60.
8. Mullard A. 2012 FDA drug approvals. Nat Rev Drug Discov 2013, 12:87-90.
9. Syed Y.Y., Dhillon S. Ocriplasmin: a review of its use in patients with symptomatic vitreomacular adhesion. Drugs 2013, 73:1617-1625.
10. Mease P., Strand V., Shalamberidze L., Dimic A., Raskina T., Xu L.A., Liu Y., Smith J. A phase II, double-blind, randomised, placebo-controlled study of BMS945429 (ALD518) in patients with rheumatoid arthritis with an inadequate response to methotrexate. Ann Rheum Dis 2012, 71:1183-1189.
11. Jung S.T., Kang T.H., Kelton W., Georgiou G. Bypassing glycosylation: engineering aglycosylated full-length IgG antibodies for human therapy. Curr Opin Biotechnol 2011, 22:858-867.
12. Barnard G.C., Kull A.R., Sharkey N.S., Shaikh S.S., Rittenhour A.M., Burnina I., Jiang Y., Li F., Lynaugh H., Mitchell T., et al. High-throughput screening and selection of yeast cell lines expressing monoclonal antibodies. J Ind Microbiol Biotechnol 2010, 37:961-971.
13. Potgieter T.I., Cukan M., Drummond J.E., Houston-Cummings N.R., Jiang Y., Li F., Lynaugh H., Mallem M., McKelvey T.W., Mitchell T., et al. Production of monoclonal antibodies by glycoengineered Pichia pastoris. J Biotechnol 2009, 139:318-325.
14. Zha D. Glycoengineered Pichia-based expression of monoclonal antibodies. Methods Mol Biol 2013, 988:31-43.
15. Hamilton S.R., Cook W.J., Gomathinayagam S., Burnina I., Bukowski J., Hopkins D., Schwartz S., Du M., Sharkey N.J., Bobrowicz P., et al. Production of sialylated O-linked glycans in Pichia pastoris. Glycobiology 2013, 23:1192-1203.
16. Hamilton S.R., Davidson R.C., Sethuraman N., Nett J.H., Jiang Y., Rios S., Bobrowicz P., Stadheim T.A., Li H., Choi B.K., et al. Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 2006, 313:1441-1443.
17. Hamilton S.R., Gerngross T.U. Glycosylation engineering in yeast: the advent of fully humanized yeast. Curr Opin Biotechnol 2007, 18:387-392.
18. Liu L., Li H., Hamilton S.R., Gomathinayagam S., Rayfield W.J., van Maanen M., Yin K.C., Hong L., Prueksaritanont T. The impact of sialic acids on the pharmacokinetics of a PEGylated erythropoietin. J Pharm Sci 2012, 101:4414-4418.
19. Liu L., Gomathinayagam S., Hamuro L., Prueksaritanont T., Wang W., Stadheim T.A., Hamilton S.R. The impact of glycosylation on the pharmacokinetics of a TNFR2:Fc fusion protein expressed in glycoengineered Pichia pastoris. Pharm Res 2013, 30:803-812.
20. Liu L., Stadheim A., Hamuro L., Pittman T., Wang W., Zha D., Hochman J., Prueksaritanont T. Pharmacokinetics of IgG1 monoclonal antibodies produced in humanized Pichia pastoris with specific glycoforms: a comparative study with CHO produced materials. Biologicals 2011, 39:205-210.
21. Choi B.K., Actor J.K., Rios S., d'Anjou M., Stadheim T.A., Warburton S., Giaccone E., Cukan M., Li H., Kull A., et al. Recombinant human lactoferrin expressed in glycoengineered Pichia pastoris: effect of terminal N-acetylneuraminic acid on in vitro secondary humoral immune response. Glycoconj J 2008, 25:581-593.
22. Li H., Sethuraman N., Stadheim T.A., Zha D., Prinz B., Ballew N., Bobrowicz P., Choi B.K., Cook W.J., Cukan M., et al. Optimization of humanized IgGs in glycoengineered Pichia pastoris. Nat Biotechnol 2006, 24:210-215.
23. Li H., d'Anjou M. Pharmacological significance of glycosylation in therapeutic proteins. Curr Opin Biotechnol 2009, 20:678-684.
24. Sethuraman N., Stadheim T.A. Challenges in therapeutic glycoprotein production. Curr Opin Biotechnol 2006, 17:341-346.
25. Alessandri L., Ouellette D., Acquah A., Rieser M., Leblond D., Saltarelli M., Radziejewski C., Fujimori T., Correia I. Increased serum clearance of oligomannose species present on a human IgG1 molecule. MAbs 2012, 4:509-520.
26. Goetze A.M., Liu Y.D., Zhang Z., Shah B., Lee E., Bondarenko P.V., Flynn G.C. High-mannose glycans on the Fc region of therapeutic IgG antibodies increase serum clearance in humans. Glycobiology 2011, 21:949-959.
27. Yu M., Brown D., Reed C., Chung S., Lutman J., Stefanich E., Wong A., Stephan J.P., Bayer R. Production, characterization, and pharmacokinetic properties of antibodies with N-linked mannose-5 glycans. MAbs 2012, 4:475-487.
28. Rabinovich G.A., van Kooyk Y., Cobb B.A. Glycobiology of immune responses. Ann N Y Acad Sci 2012, 1253:1-15.
29. Banerjee K., Michael E., Eggink D., van Montfort T., Lasnik A.B., Palmer K.E., Sanders R.W., Moore J.P., Klasse P.J. Occluding the mannose moieties on human immunodeficiency virus type 1 gp120 with griffithsin improves the antibody responses to both proteins in mice. AIDS Res Hum Retroviruses 2012, 28:206-214.
30. de Vries R.P., Smit C.H., de Bruin E., Rigter A., de Vries E., Cornelissen L.A., Eggink D., Chung N.P., Moore J.P., Sanders R.W., et al. Glycan-dependent immunogenicity of recombinant soluble trimeric hemagglutinin. J Virol 2012, 86:11735-11744.
31. Yuen C.T., Storring P.L., Tiplady R.J., Izquierdo M., Wait R., Gee C.K., Gerson P., Lloyd P., Cremata J.A. Relationships between the N-glycan structures and biological activities of recombinant human erythropoietins produced using different culture conditions and purification procedures. Br J Haematol 2003, 121:511-526.
32. Shields R.L., Lai J., Keck R., O'Connell L.Y., Hong K., Meng Y.G., Weikert S.H., Presta L.G. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002, 277:26733-26740.
33. Van Patten S.M., Hughes H., Huff M.R., Piepenhagen P.A., Waire J., Qiu H., Ganesa C., Reczek D., Ward P.V., Kutzko J.P., et al. Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of Gaucher disease. Glycobiology 2007, 17:467-478.
34. Beck A., Cochet O., Wurch T. GlycoFi's technology to control the glycosylation of recombinant therapeutic proteins. Expert Opin Drug Discov 2010, 5:95-111.
35. Bobrowicz P., Davidson R.C., Li H., Potgieter T.I., Nett J.H., Hamilton S.R., Stadheim T.A., Miele R.G., Bobrowicz B., Mitchell T., et al. Engineering of an artificial glycosylation pathway blocked in core oligosaccharide assembly in the yeast Pichia pastoris: production of complex humanized glycoproteins with terminal galactose. Glycobiology 2004, 14:757-766.
36. Choi B.K., Bobrowicz P., Davidson R.C., Hamilton S.R., Kung D.H., Li H., Miele R.G., Nett J.H., Wildt S., Gerngross T.U. Use of combinatorial genetic libraries to humanize N-linked glycosylation in the yeast Pichia pastoris. Proc Natl Acad Sci U S A 2003, 100:5022-5027.
37. Jacobs P.P., Geysens S., Vervecken W., Contreras R., Callewaert N. Engineering complex-type N-glycosylation in Pichia pastoris using GlycoSwitch technology. Nat Protoc 2009, 4:58-70.
38. Nett J.H., Stadheim T.A., Li H., Bobrowicz P., Hamilton S.R., Davidson R.C., Choi B.K., Mitchell T., Bobrowicz B., Rittenhour A., et al. A combinatorial genetic library approach to target heterologous glycosylation enzymes to the endoplasmic reticulum or the Golgi apparatus of Pichia pastoris. Yeast 2011, 28:237-252.
39. Davidson R.C., Nett J.H., Renfer E., Li H., Stadheim T.A., Miller B.J., Miele R.G., Hamilton S.R., Choi B.K., Mitchell T.I., et al. Functional analysis of the ALG3 gene encoding the Dol-P-Man: Man5GlcNAc2-PP-Dol mannosyltransferase enzyme of P. pastoris. Glycobiology 2004, 14:399-407.
40. Nett J.H., Gomathinayagam S., Hamilton S.R., Gong B., Davidson R.C., Du M., Hopkins D., Mitchell T., Mallem M.R., Nylen A., et al. Optimization of erythropoietin production with controlled glycosylation-PEGylated erythropoietin produced in glycoengineered Pichia pastoris. J Biotechnol 2012, 157:198-206.
41. Zhang N., Liu L., Dumitru C.D., Cummings N.R., Cukan M., Jiang Y., Li Y., Li F., Mitchell T., Mallem M.R., et al. Glycoengineered Pichia produced anti-HER2 is comparable to trastuzumab in preclinical study. MAbs 2011, 3:289-298.
42. Arico C., Bonnet C., Javaud C. N-glycosylation humanization for production of therapeutic recombinant glycoproteins in Saccharomyces cerevisiae. Methods Mol Biol 2013, 988:45-57.
43. Parsaie Nasab F., Aebi M., Bernhard G., Frey A.D. A combined system for engineering glycosylation efficiency and glycan structure in Saccharomyces cerevisiae. Appl Environ Microbiol 2013, 79:997-1007.
44. Wang H., Song H.L., Wang Q., Qiu B.S. Expression of glycoproteins bearing complex human-like glycans with galactose terminal in Hansenula polymorpha. World J Microbiol Biotechnol 2013, 29:447-458.
45. Cheon S.A., Kim H., Oh D.B., Kwon O., Kang H.A. Remodeling of the glycosylation pathway in the methylotrophic yeast Hansenula polymorpha to produce human hybrid-type N-glycans. J Microbiol 2012, 50:341-348.
46. Oh D.B., Park J.S., Kim M.W., Cheon S.A., Kim E.J., Moon H.Y., Kwon O., Rhee S.K., Kang H.A. Glycoengineering of the methylotrophic yeast Hansenula polymorpha for the production of glycoproteins with trimannosyl core N-glycan by blocking core oligosaccharide assembly. Biotechnol J 2008, 3:659-668.
47. Liu B., Gong X., Chang S., Yang Y., Song M., Duan D., Wang L., Ma Q., Wu J. Disruption of the OCH1 and MNN1 genes decrease N-glycosylation on glycoprotein expressed in Kluyveromyces lactis. J Biotechnol 2009, 143:95-102.
48. De Pourcq K., Tiels P., Van Hecke A., Geysens S., Vervecken W., Callewaert N. Engineering Yarrowia lipolytica to produce glycoproteins homogeneously modified with the universal Man3GlcNAc2 N-glycan core. PLoS ONE 2012, 7:e39976.
49. De Pourcq K., Vervecken W., Dewerte I., Valevska A., Van Hecke A., Callewaert N. Engineering the yeast Yarrowia lipolytica for the production of therapeutic proteins homogeneously glycosylated with Man(8)GlcNAc(2) and Man(5)GlcNAc(2). Microb Cell Fact 2012, 11:53.
50. Vervecken W., Kaigorodov V., Callewaert N., Geysens S., De Vusser K., Contreras R. In vivo synthesis of mammalian-like, hybrid-type N-glycans in Pichia pastoris. Appl Environ Microbiol 2004, 70:2639-2646.
51. Jacobs P.P., Inan M., Festjens N., Haustraete J., Van Hecke A., Contreras R., Meagher M.M., Callewaert N. Fed-batch fermentation of GM-CSF-producing glycoengineered Pichia pastoris under controlled specific growth rate. Microb Cell Fact 2010, 9:93.
52. Choi B.K., Warburton S., Lin H., Patel R., Boldogh I., Meehl M., d'Anjou M., Pon L., Stadheim T.A., Sethuraman N. Improvement of N-glycan site occupancy of therapeutic glycoproteins produced in Pichia pastoris. Appl Microbiol Biotechnol 2012, 95:671-682.
53. Nett J.H., Cook W.J., Chen M.T., Davidson R.C., Bobrowicz P., Kett W., Brevnova E., Potgieter T.I., Mellon M.T., Prinz B., et al. Characterization of the Pichia pastoris protein-O-mannosyltransferase gene family. PLoS ONE 2013, 8:e68325.
54. Loibl M., Strahl S. Protein O-mannosylation: what we have learned from baker's yeast. Biochim Biophys Acta 2013, 1833:2438-2446.
55. Cukan M.C., Hopkins D., Burnina I., Button M., Giaccone E., Houston-Cummings N.R., Jiang Y., Li F., Mallem M., Mitchell T., et al. Binding of DC-SIGN to glycoproteins expressed in glycoengineered Pichia pastoris. J Immunol Methods 2012, 386:34-42.
56. Ahlen G., Strindelius L., Johansson T., Nilsson A., Chatzissavidou N., Sjoblom M., Rova U., Holgersson J. Mannosylated mucin-type immunoglobulin fusion proteins enhance antigen-specific antibody and T lymphocyte responses. PLoS ONE 2012, 7:e46959.
57. Argyros R., Nelson S., Kull A., Chen M.T., Stadheim T.A., Jiang B. A phenylalanine to serine substitution within an O-protein mannosyltransferase led to strong resistance to PMT-inhibitors in Pichia pastoris. PLoS ONE 2013, 8:e62229.
58. Orchard M.G., Neuss J.C., Galley C.M., Carr A., Porter D.W., Smith P., Scopes D.I., Haydon D., Vousden K., Stubberfield C.R., et al. Rhodanine-3-acetic acid derivatives as inhibitors of fungal protein mannosyl transferase 1 (PMT1). Bioorg Med Chem Lett 2004, 14:3975-3978.
59. Kuroda K., Kobayashi K., Kitagawa Y., Nakagawa T., Tsumura H., Komeda T., Shinmi D., Mori E., Motoki K., Fuju K., et al. Efficient antibody production upon suppression of O mannosylation in the yeast Ogataea minuta. Appl Environ Microbiol 2008, 74:446-453.
60. Amano K., Chiba Y., Kasahara Y., Kato Y., Kaneko M.K., Kuno A., Ito H., Kobayashi K., Hirabayashi J., Jigami Y., et al. Engineering of mucin-type human glycoproteins in yeast cells. Proc Natl Acad Sci U S A 2008, 105:3232-3237.
61. Chigira Y., Oka T., Okajima T., Jigami Y. Engineering of a mammalian O-glycosylation pathway in the yeast Saccharomyces cerevisiae: production of O-fucosylated epidermal growth factor domains. Glycobiology 2008, 18:303-314.
62. Suga M., Hatakeyama T. High-efficiency electroporation by freezing intact yeast cells with addition of calcium. Curr Genet 2003, 43:206-211.
63. Cregg J.M. DNA-mediated transformation. Methods Mol Biol 2007, 389:27-42.
64. Wu S., Letchworth G.J. High efficiency transformation by electroporation of Pichia pastoris pretreated with lithium acetate and dithiothreitol. Biotechniques 2004, 36:152-154.
65. Aw R., Polizzi K.M. Can too many copies spoil the broth?. Microb Cell Fact 2013, 12:128.
66. Baek D.S., Kim Y.S. Construction of a large synthetic human Fab antibody library on yeast cell surface by optimized yeast mating. J Microbiol Biotechnol 2014, (Epub ahead of print).
67. Blaise L., Wehnert A., Steukers M.P., van den Beucken T., Hoogenboom H.R., Hufton S.E. Construction and diversification of yeast cell surface displayed libraries by yeast mating: application to the affinity maturation of Fab antibody fragments. Gene 2004, 342:211-218.
68. Chen M.T., Lin S., Shandil I., Andrews D., Stadheim T.A., Choi B.K. Generation of diploid Pichia pastoris strains by mating and their application for recombinant protein production. Microb Cell Fact 2012, 11:91.
69. Ioannidis J.P., Karassa F.B., Druyts E., Thorlund K., Mills E.J. Biologic agents in rheumatology: unmet issues after 200 trials and $200 billion sales. Nat Rev Rheumatol 2013, 9:665-673.
70. Doerner A., Rhiel L., Zielonka S., Kolmar H. Therapeutic antibody engineering by high efficiency cell screening. FEBS Lett 2014, 588:278-287.
71. Gera N., Hussain M., Rao B.M. Protein selection using yeast surface display. Methods 2013, 60:15-26.
72. Zhang L., Liang S., Zhou X., Jin Z., Jiang F., Han S., Zheng S., Lin Y. Screening for glycosylphosphatidylinositol-modified cell wall proteins in Pichia pastoris and their recombinant expression on the cell surface. Appl Environ Microbiol 2013, 79:5519-5526.
73. Shaheen H.H., Prinz B., Chen M.T., Pavoor T., Lin S., Houston-Cummings N.R., Moore R., Stadheim T.A., Zha D. A dual-mode surface display system for the maturation and production of monoclonal antibodies in glyco-engineered Pichia pastoris. PLoS ONE 2013, 8:e70190.
74. Puri V., Streaker E., Prabakaran P., Zhu Z., Dimitrov D.S. Highly efficient selection of epitope specific antibody through competitive yeast display library sorting. MAbs 2013, 5:533-539.
75. Tillotson B.J., Cho Y.K., Shusta E.V. Cells and cell lysates: a direct approach for engineering antibodies against membrane proteins using yeast surface display. Methods 2013, 60:27-37.
76. Tillotson B.J., de Larrinoa I.F., Skinner C.A., Klavas D.M., Shusta E.V. Antibody affinity maturation using yeast display with detergent-solubilized membrane proteins as antigen sources. Protein Eng Des Sel 2013, 26:101-112.
77. Xu Y., Roach W., Sun T., Jain T., Prinz B., Yu T.Y., Torrey J., Thomas J., Bobrowicz P., Vasquez M., et al. Addressing polyspecificity of antibodies selected from an in vitro yeast presentation system: a FACS-based, high-throughput selection and analytical tool. Protein Eng Des Sel 2013, 26:663-670.
78. Ceroni A., Maass K., Geyer H., Geyer R., Dell A., Haslam S.M. GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans. J Proteome Res 2008, 7:1650-1659.