High-yield production of functional soluble single-domain antibodies in the cytoplasm of Escherichia coli

Microbial Cell Factories

Volumn 12, Issue 1, 2013, Pages

  Zarschler, Kristof ^a   Witecy, Stefanie ^a   Kapplusch, Franz ^a   Foerster, Christian ^a,b   Stephan, Holger ^a  

^a INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DISULFIDE; EPITOPE; HEXAHISTIDINE; NANOBODY; THIOL GROUP;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; BINDING AFFINITY; CELL DENSITY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOPLASM; DISULFIDE BOND; ESCHERICHIA COLI; GENETIC ENGINEERING; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; ISOTOPE LABELING; MELTING POINT; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

AMINO ACID SEQUENCE; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; PROTEIN ENGINEERING; SINGLE-DOMAIN ANTIBODIES;

EID: 84886153348     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-12-97     Document Type: Article

References (64)

1. Gschwind A, Fischer OM, Ullrich A. The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 2004, 4:361-370. 10.1038/nrc1360, 15122207.
2. Holbro T, Civenni G, Hynes NE. The ErbB receptors and their role in cancer progression. Exp Cell Res 2003, 284:99-110. 10.1016/S0014-4827(02)00099-X, 12648469.
3. Zeineldin R, Muller CY, Stack MS, Hudson LG. Targeting the EGF receptor for ovarian cancer therapy. J Oncol 2010, 2010:414676. 2801454, 20066160.
4. Rapidis AD, Wolf GT. Immunotherapy of head and neck cancer: current and future considerations. J Oncol 2009, 2009:346345. 2723756, 19680453.
5. Lurje G, Lenz HJ. EGFR signaling and drug discovery. Oncology 2009, 77:400-410. 10.1159/000279388, 20130423.
6. Burgess AW. EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 2008, 26:263-274. 10.1080/08977190802312844, 18800267.
7. Elbakri A, Nelson PN, Abu Odeh RO. The state of antibody therapy. Hum Immunol 2010, 71:1243-1250. 10.1016/j.humimm.2010.09.007, 20849901.
8. Holliger P, Hudson PJ. Engineered antibody fragments and the rise of single domains. Nat Biotechnol 2005, 23:1126-1136. 10.1038/nbt1142, 16151406.
9. Feldwisch J, Tolmachev V. Engineering of affibody molecules for therapy and diagnostics. Methods Mol Biol 2012, 899:103-126. 10.1007/978-1-61779-921-1_7, 22735949.
10. Lofblom J, Feldwisch J, Tolmachev V, Carlsson J, Stahl S, Frejd FY. Affibody molecules: engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett 2010, 584:2670-2680. 10.1016/j.febslet.2010.04.014, 20388508.
11. Orlova A, Feldwisch J, Abrahmsen L, Tolmachev V. Update: affibody molecules for molecular imaging and therapy for cancer. Cancer Biother Radiopharm 2007, 22:573-584. 10.1089/cbr.2006.004-U, 17979560.
12. Rahbarizadeh F, Ahmadvand D, Sharifzadeh Z. Nanobody; an old concept and new vehicle for immunotargeting. Immunol Invest 2011, 40:299-338. 10.3109/08820139.2010.542228, 21244216.
13. Vaneycken I, D'Huyvetter M, Hernot S, De Vos J, Xavier C, Devoogdt N, Caveliers V, Lahoutte T. Immuno-imaging using nanobodies. Curr Opin Biotechnol 2011, 22:877-881. 10.1016/j.copbio.2011.06.009, 21726996.
14. De Vos J, Devoogdt N, Lahoutte T, Muyldermans S. Camelid single-domain antibody-fragment engineering for (pre)clinical in vivo molecular imaging applications: adjusting the bullet to its target. Expert Opin Biol Ther 2013, 13:1149-1160. 10.1517/14712598.2013.800478, 23675652.
15. Huang L, Gainkam LO, Caveliers V, Vanhove C, Keyaerts M, De Baetselier P, Bossuyt A, Revets H, Lahoutte T. SPECT imaging with 99mTc-labeled EGFR-specific nanobody for in vivo monitoring of EGFR expression. Mol Imaging Biol 2008, 10:167-175. 10.1007/s11307-008-0133-8, 18297364.
16. Bell A, Wang ZJ, Arbabi-Ghahroudi M, Chang TA, Durocher Y, Trojahn U, Baardsnes J, Jaramillo ML, Li S, Baral TN, et al. Differential tumor-targeting abilities of three single-domain antibody formats. Cancer Lett 2010, 289:81-90. 10.1016/j.canlet.2009.08.003, 19716651.
17. Gainkam LO, Huang L, Caveliers V, Keyaerts M, Hernot S, Vaneycken I, Vanhove C, Revets H, De Baetselier P, Lahoutte T. Comparison of the biodistribution and tumor targeting of two 99mTc-labeled anti-EGFR nanobodies in mice, using pinhole SPECT/micro-CT. J Nucl Med 2008, 49:788-795. 10.2967/jnumed.107.048538, 18413403.
18. Roovers RC, Laeremans T, Huang L, De Taeye S, Verkleij AJ, Revets H, De Haard HJ, Vanbergenen Henegouwen PM. Efficient inhibition of EGFR signaling and of tumour growth by antagonistic anti-EFGR Nanobodies. Cancer Immunol Immunother 2007, 56:303-317.
19. Gainkam LO, Keyaerts M, Caveliers V, Devoogdt N, Vanhove C, Van Grunsven L, Muyldermans S, Lahoutte T. Correlation between epidermal growth factor receptor-specific nanobody uptake and tumor burden: a tool for noninvasive monitoring of tumor response to therapy. Mol Imaging Biol 2011, 13:940-948. 10.1007/s11307-010-0428-4, 20865332.
20. Roovers RC, Vosjan MJ, Laeremans T, El Khoulati R, De Bruin RC, Ferguson KM, Verkleij AJ, Van Dongen GA, Van Bergen En Henegouwen PM. A biparatopic anti-EGFR nanobody efficiently inhibits solid tumour growth. Int J Cancer 2011, 129:2013-2024. 10.1002/ijc.26145, 21520037.
21. Baral TN, Arbabi-Ghahroudi M. Expression of single-domain antibodies in bacterial systems. Methods Mol Biol 2012, 911:257-275.
22. De Vooght L, Caljon G, Stijlemans B, De Baetselier P, Coosemans M, Van den Abbeele J. Expression and extracellular release of a functional anti-trypanosome Nanobody(R) in Sodalis glossinidius, a bacterial symbiont of the tsetse fly. Microb Cell Fact 2012, 11:23. 10.1186/1475-2859-11-23, 3311065, 22335892.
23. Gorlani A, De Haard H, Verrips T. Expression of VHHs in Saccharomyces cerevisiae. Methods Mol Biol 2012, 911:277-286.
24. Joosten V, Lokman C, Van Den Hondel CA, Punt PJ. The production of antibody fragments and antibody fusion proteins by yeasts and filamentous fungi. Microb Cell Fact 2003, 2:1. 10.1186/1475-2859-2-1, 149433, 12605725.
25. De Buck S, Virdi V, De Meyer T, De Wilde K, Piron R, Nolf J, Van Lerberge E, De Paepe A, Depicker A. Production of camel-like antibodies in plants. Methods Mol Biol 2012, 911:305-324.
26. Agrawal V, Slivac I, Perret S, Bisson L, St-Laurent G, Murad Y, Zhang J, Durocher Y. Stable expression of chimeric heavy chain antibodies in CHO cells. Methods Mol Biol 2012, 911:287-303.
27. Gomez-Sebastian S, Nunez MC, Garaicoechea L, Alvarado C, Mozgovoj M, Lasa R, Kahl A, Wigdorovitz A, Parreno V, Escribano JM. Rotavirus A-specific single-domain antibodies produced in baculovirus-infected insect larvae are protective in vivo. BMC Biotechnol 2012, 12:59. 10.1186/1472-6750-12-59, 3444942, 22953695.
28. Andersen DC, Krummen L. Recombinant protein expression for therapeutic applications. Curr Opin Biotechnol 2002, 13:117-123. 10.1016/S0958-1669(02)00300-2, 11950561.
29. Demain AL, Vaishnav P. Production of recombinant proteins by microbes and higher organisms. Biotechnol Adv 2009, 27:297-306.
30. Talelli M, Oliveira S, Rijcken CJ, Pieters EH, Etrych T, Ulbrich K, Van Nostrum RC, Storm G, Hennink WE, Lammers T. Intrinsically active nanobody-modified polymeric micelles for tumor-targeted combination therapy. Biomaterials 2013, 34:1255-1260. 10.1016/j.biomaterials.2012.09.064, 23122804.
31. VanderMeel R, Oliveira S, Altintas I, Haselberg R, van der Veeken J, Roovers RC, Henegouwen PM VBE, Storm G, Hennink WE, Schiffelers RM, Kok RJ. Tumor-targeted nanobullets: anti-EGFR nanobody-liposomes loaded with anti-IGF-1R kinase inhibitor for cancer treatment. J Control Release 2012, 159:281-289. 10.1016/j.jconrel.2011.12.027, 22227023.
32. De Marco A. Biotechnological applications of recombinant single-domain antibody fragments. Microb Cell Fact 2011, 10:44. 10.1186/1475-2859-10-44, 3123181, 21658216.
33. Bessette PH, Aslund F, Beckwith J, Georgiou G. Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci U S A 1999, 96:13703-13708. 10.1073/pnas.96.24.13703, 24128, 10570136.
34. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R. Naturally occurring antibodies devoid of light chains. Nature 1993, 363:446-448. 10.1038/363446a0, 8502296.
35. Muyldermans S, Atarhouch T, Saldanha J, Barbosa JA, Hamers R. Sequence and structure of VH domain from naturally occurring camel heavy chain immunoglobulins lacking light chains. Protein Eng 1994, 7:1129-1135. 10.1093/protein/7.9.1129, 7831284.
36. De Marco A. Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli. Microb Cell Fact 2009, 8:26. 10.1186/1475-2859-8-26, 2689190, 19442264.
37. Makino T, Skretas G, Georgiou G. Strain engineering for improved expression of recombinant proteins in bacteria. Microb Cell Fact 2011, 10:32. 10.1186/1475-2859-10-32, 3120638, 21569582.
38. Sorensen HP, Mortensen KK. Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb Cell Fact 2005, 4:1. 10.1186/1475-2859-4-1, 544838, 15629064.
39. Levy R, Weiss R, Chen G, Iverson BL, Georgiou G. Production of correctly folded Fab antibody fragment in the cytoplasm of Escherichia coli trxB gor mutants via the coexpression of molecular chaperones. Protein Expr Purif 2001, 23:338-347. 10.1006/prep.2001.1520, 11676610.
40. Krause M, Ukkonen K, Haataja T, Ruottinen M, Glumoff T, Neubauer A, Neubauer P, Vasala A. A novel fed-batch based cultivation method provides high cell-density and improves yield of soluble recombinant proteins in shaken cultures. Microb Cell Fact 2010, 9:11. 10.1186/1475-2859-9-11, 2841585, 20167131.
41. Arbabi Ghahroudi M, Desmyter A, Wyns L, Hamers R, Muyldermans S. Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett 1997, 414:521-526. 10.1016/S0014-5793(97)01062-4, 9323027.
42. Tanha J, Dubuc G, Hirama T, Narang SA, MacKenzie CR. Selection by phage display of llama conventional V(H) fragments with heavy chain antibody V(H)H properties. J Immunol Methods 2002, 263:97-109. 10.1016/S0022-1759(02)00027-3, 12009207.
43. Matz J, Kessler P, Bouchet J, Combes O, Ramos OH, Barin F, Baty D, Martin L, Benichou S, Chames P. Straightforward selection of broadly neutralizing single-domain antibodies targeting the conserved CD4 and coreceptor binding sites of HIV-1 gp120. J Virol 2013, 87:1137-1149. 10.1128/JVI.00461-12, 3554102, 23152508.
44. Thomassen YE, Verkleij AJ, Boonstra J, Verrips CT. Specific production rate of VHH antibody fragments by Saccharomyces cerevisiae is correlated with growth rate, independent of nutrient limitation. J Biotechnol 2005, 118:270-277. 10.1016/j.jbiotec.2005.05.010, 15979755.
45. Thomassen YE, Meijer W, Sierkstra L, Verrips CT. Large-scale production of VHH antibody fragments by Saccharomyces cerevisiae. Enzyme Microb Technol 2002, 30:273-278.
46. Arbabi-Ghahroudi M, Tanha J, MacKenzie R. Prokaryotic expression of antibodies. Cancer Metastasis Rev 2005, 24:501-519. 10.1007/s10555-005-6193-1, 16408159.
47. Katsuda T, Sonoda H, Kumada Y, Yamaji H. Production of antibody fragments in Escherichia coli. Methods Mol Biol 2012, 907:305-324.
48. Guglielmi L, Martineau P. Expression of single-chain Fv fragments in E. coli cytoplasm. Methods Mol Biol 2009, 562:215-224. 10.1007/978-1-60327-302-2_17, 3101525, 19554299.
49. Mahgoub IO. Expression and characterization of a functional single-chain variable fragment (scFv) protein recognizing MCF7 breast cancer cells in E. coli cytoplasm. Biochem Genet 2012, 50:625-641. 10.1007/s10528-012-9506-4, 22552770.
50. Sonoda H, Kumada Y, Katsuda T, Yamaji H. Functional expression of single-chain Fv antibody in the cytoplasm of Escherichia coli by thioredoxin fusion and co-expression of molecular chaperones. Protein Expr Purif 2010, 70:248-253. 10.1016/j.pep.2009.11.003, 19913620.
51. Venturi M, Seifert C, Hunte C. High level production of functional antibody Fab fragments in an oxidizing bacterial cytoplasm. J Mol Biol 2002, 315:1-8. 10.1006/jmbi.2001.5221, 11771962.
52. Ukkonen K, Vasala A, Ojamo H, Neubauer P. High-yield production of biologically active recombinant protein in shake flask culture by combination of enzyme-based glucose delivery and increased oxygen transfer. Microb Cell Fact 2011, 10:107. 10.1186/1475-2859-10-107, 3258199, 22152005.
53. Järviluoma A, Strandin T, Lülf S, Bouchet J, Mäkelä AR, Geyer M, Benichou S, Saksela K. High-affinity target binding engineered via fusion of a single-domain antibody fragment with a ligand-tailored SH3 domain. PLoS ONE 2012, 7:e40331. 10.1371/journal.pone.0040331, 3390362, 22792285.
54. Matsumura M, Signor G, Matthews BW. Substantial increase of protein stability by multiple disulphide bonds. Nature 1989, 342:291-293. 10.1038/342291a0, 2812028.
55. Pace CN. Conformational stability of globular proteins. Trends Biochem Sci 1990, 15:14-17. 10.1016/0968-0004(90)90124-T, 2107612.
56. Salvati A, Pitek AS, Monopoli MP, Prapainop K, Bombelli FB, Hristov DR, Kelly PM, Aberg C, Mahon E, Dawson KA. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat Nanotechnol 2013, 8:137-143. 10.1038/nnano.2012.237, 23334168.
57. Bjorkelund H, Gedda L, Andersson K. Comparing the epidermal growth factor interaction with four different cell lines: intriguing effects imply strong dependency of cellular context. PLoS One 2011, 6:e16536. 10.1371/journal.pone.0016536, 3031572, 21304974.
58. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000, 28:1102-1104.
59. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein Identification and Analysis Tools on the ExPASy Server. The proteomics protocols handbook 2005, 571-607. Totowa, NJ: Humana Press, Walker JM.
60. Needleman SB, Wunsch CD. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 1970, 48:443-453. 10.1016/0022-2836(70)90057-4, 5420325.
61. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685. 10.1038/227680a0, 5432063.
62. Pace CN, Scholtz JM. Measuring the conformational stability of a protein. Protein structure: a practical approach 1996, 299-321. Oxford: IRL Press, Creighton TE.
63. Tavare R, Torres Martin De Rosales R, Blower PJ, Mullen GE. Efficient site-specific radiolabeling of a modified C2A domain of synaptotagmin I with [99mTc(CO)3]+: a new radiopharmaceutical for imaging cell death. Bioconjug Chem 2009, 20:2071-2081. 10.1021/bc900160j, 19874007.
64. Alberto R, Schibli R, Egli A, Schubiger AP, Abram U, Kaden TA. A novel organometallic aqua complex of technetium for the labeling of biomolecules: synthesis of [99mTc(OH2)3(CO)3] + from [99mTcO4]- in aqueous solution and its reaction with a bifunctional ligand. J Am Chem Soc 1998, 120:7987-7988.