Delivery of antibodies to the cytosol: Debunking the myths

mAbs

Volumn 6, Issue 4, 2014, Pages 943-956

  Marschall, Andrea L J ^a   Zhang, Congcong ^b   Frenzel, André ^a   Schirrmann, Thomas ^c   Hust, Michael ^a   Perez, Franck ^d,e   Dübel, Stefan ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^c YUMAB GmbH   (Germany)

^d INSTITUT CURIE   (France)

^e INSTITUT CURIE   (France)

Author keywords

Cell penetrating peptides; CPP; Electroporation; Electrotransfer; Profection; Protein delivery; Protein transduction domain; PTD; Transbody; Transfection; Yumab

Indexed keywords

CELL PENETRATING PEPTIDE; CRE RECOMBINASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 FC RECEPTOR; PROFECTION REAGENT; REAGENT; UNCLASSIFIED DRUG; IMMUNOGLOBULIN CONSTANT REGION; IMMUNOGLOBULIN G; INTEGRASE;

ARTICLE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ELECTROPORATION; EMBRYO; ENDOSOME; FEMALE; FLOW CYTOMETRY; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; MICROSCOPY; DRUG DELIVERY SYSTEM; GENETICS; IMMUNOGLOBULIN CONSTANT REGION; METABOLISM; PHARMACOLOGY; PROCEDURES; PROTEIN TRANSPORT;

CYTOSOL; DRUG DELIVERY SYSTEMS; ENDOSOMES; HELA CELLS; HUMANS; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN G; INTEGRASES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84903790801     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.29268     Document Type: Article

References (55)

1. Blose SH, Meltzer DI, Feramisco JR. 10-nm filaments are induced to collapse in living cells microinjected with monoclonal and polyclonal antibodies against tubulin. J Cell Biol 1984; 98:847-58; PMID:6538204; http://dx.doi.org/10.1083/jcb.98.3.847
2. Gawlitta W, Osborn M, Weber K. Coiling of intermediate filaments induced by microinjection of a vimentin-specific antibody does not interfere with locomotion and mitosis. Eur J Cell Biol 1981; 26:83-90; PMID:7198976
3. Kallajoki M, Harborth J, Weber K, Osborn M. Microinjection of a monoclonal antibody against SPN antigen, now identified by peptide sequences as the NuMA protein, induces micronuclei in PtK2 cells. J Cell Sci 1993; 104:139-50; PMID:8449992
4. Lin JJ, Feramisco JR. Disruption of the in vivo distribution of the intermediate filaments in fibroblasts through the microinjection of a specific monoclonal antibody. Cell 1981; 24:185-93; PMID:7016335; http://dx.doi.org/10. 1016/0092-8674(81)90514-6
5. Warn RM, Flegg L, Warn A. An investigation of microtubule organization and functions in living Drosophila embryos by injection of a fluorescently labeled antibody against tyrosinated alpha-tubulin. J Cell Biol 1987; 105:1721-30; PMID:3117804; http://dx.doi.org/10.1083/jcb.105.4.1721
6. Marschall AL, Frenzel A, Schirrmann T, Schüngel M, Dübel S. Targeting antibodies to the cytoplasm. MAbs 2011; 3:3-16; PMID:21099369; http://dx.doi.org/10.4161/mabs.3.1.14110
7. Stocks MR. Intrabodies: production and promise. Drug Discov Today 2004; 9:960-6; PMID:15539139; http://dx.doi.org/10.1016/S1359-6446(04)03269-6
8. Stocks M. Intrabodies as drug discovery tools and therapeutics. Curr Opin Chem Biol 2005; 9:359-65; PMID:15979379; http://dx.doi.org/10.1016/j.cbpa.2005. 06.003
9. Caussinus E, Kanca O, Affolter M. Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat Struct Mol Biol 2012; 19:117-21; PMID:22157958; http://dx.doi.org/10.1038/nsmb.2180
10. Ernst A, Avvakumov G, Tong J, Fan Y, Zhao Y, Alberts P, Persaud A, Walker JR, Neculai AM, Neculai D, et al. A strategy for modulation of enzymes in the ubiquitin system. Science 2013; 339:590-5; PMID:23287719; http://dx.doi.org/10. 1126/science.1230161
11. Grebien F, Hantschel O, Wojcik J, Kaupe I, Kovacic B, Wyrzucki AM, Gish GD, Cerny-Reiterer S, Koide A, Beug H, et al. Targeting the SH2-kinase interface in Bcr-Abl inhibits leukemogenesis. Cell 2011; 147:306-19; PMID:22000011; http://dx.doi.org/10.1016/j.cell.2011.08.046
12. Kummer L, Parizek P, Rube P, Millgramm B, Prinz A, Mittl PR, Kaufholz M, Zimmermann B, Herberg FW, Plückthun A. Structural and functional analysis of phosphorylation-specific binders of the kinase ERK from designed ankyrin repeat protein libraries. Proc Natl Acad Sci U S A 2012; 109:E2248-57; PMID:22843676; http://dx.doi.org/10.1073/pnas.1205399109
13. Böldicke T. Blocking translocation of cell surface molecules from the ER to the cell surface by intracellular antibodies targeted to the ER. J Cell Mol Med 2007; 11:54-70; PMID:17367501; http://dx.doi.org/10.1111/j.1582- 4934.2007.00002.x
14. Strebe N, Guse A, Schüngel M, Schirrmann T, Hafner M, Jostock T, Hust M, Müller W, Dübel S. Functional knockdown of VCAM-1 at the posttranslational level with ER retained antibodies. J Immunol Methods 2009; 341:30-40; PMID:19038261; http://dx.doi.org/10.1016/j.jim.2008.10.012
15. Zhang C, Helmsing S, Zagrebelsky M, Schirrmann T, Marschall AL, Schüngel M, Korte M, Hust M, Dübel S. Suppression of p75 neurotrophin receptor surface expression with intrabodies influences Bcl-xL mRNA expression and neurite outgrowth in PC12 cells. PLoS One 2012; 7:e30684; PMID:22292018; http://dx.doi.org/10.1371/journal.pone.0030684
16. Postupalenko V, Sibler AP, Desplancq D, Nominé Y, Spehner D, Schultz P, Weiss E, Zuber G. Intracellular delivery of functionally active proteins using self-assembling pyridylthiourea-polyethylenimine. J Control Release 2014; 178:86-94; PMID:24476809; http://dx.doi.org/10.1016/j.jconrel. 2014.01.017
17. Kaczmarczyk SJ, Sitaraman K, Young HA, Hughes SH, Chatterjee DK. Protein delivery using engineered virus-like particles. Proc Natl Acad Sci U S A 2011; 108:16998-7003; PMID:21949376; http://dx.doi.org/10.1073/pnas.1101874108
18. Voelkel C, Galla M, Maetzig T, Warlich E, Kuehle J, Zychlinski D, Bode J, Cantz T, Schambach A, Baum C. Protein transduction from retroviral Gag precursors. Proc Natl Acad Sci U S A 2010; 107:7805-10; PMID:20385817; http://dx.doi.org/10.1073/pnas.0914517107
19. Heitz F, Morris MC, Divita G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 2009; 157:195-206; PMID:19309362; http://dx.doi.org/10.1111/j.1476-5381.2009.00057.x
20. Mueller J, Kretzschmar I, Volkmer R, Boisguerin P. Comparison of cellular uptake using 22 CPPs in 4 different cell lines. Bioconjug Chem 2008; 19:2363-74; PMID:19053306; http://dx.doi.org/10.1021/bc800194e
21. Ye D, Xu D, Singer AU, Juliano RL. Evaluation of strategies for the intracellular delivery of proteins. Pharm Res 2002; 19:1302-9; PMID:12403066; http://dx.doi.org/10.1023/A:1020346607764
22. Behr JP. The Proton Sponge: a Trick to Enter Cells the Viruses Did not Exploit. Chimia (Aarau) 1997; 51:34-6
23. Khalil IA, Kogure K, Akita H, Harashima H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 2006; 58:32-45; PMID:16507881; http://dx.doi.org/10.1124/pr.58.1.8
24. Fischer PM. Cellular uptake mechanisms and potential therapeutic utility of peptidic cell delivery vectors: progress 2001-2006. Med Res Rev 2007; 27:755-95; PMID:17019680; http://dx.doi.org/10.1002/med.20093
25. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003; 278:585-90; PMID:12411431; http://dx.doi.org/10.1074/jbc.M209548200
26. Schmidt N, Mishra A, Lai GH, Wong GC. Arginine-rich cell-penetrating peptides. FEBS Lett 2010; 584:1806-13; PMID:19925791; http://dx.doi.org/10.1016/ j.febslet.2009.11.046
27. Cronican JJ, Beier KT, Davis TN, Tseng JC, Li W, Thompson DB, Shih AF, May EM, Cepko CL, Kung AL, et al. A class of human proteins that deliver functional proteins into mammalian cells in vitro and in vivo. Chem Biol 2011; 18:833-8; PMID:21802004; http://dx.doi.org/10.1016/j.chembiol.2011.07.003
28. Rongrong L, Lixia W, Zhongping L. Effect of deletion mutation on the recombination activity of Cre recombinase. Acta Biochim Pol 2005; 52:541-4; PMID:15912212
29. Moutel S, El Marjou A, Vielemeyer O, Nizak C, Benaroch P, Dübel S, Perez F. A multi-Fc-species system for recombinant antibody production. BMC Biotechnol 2009; 9:14; PMID:19245715; http://dx.doi.org/10.1186/1472-6750-9-14
30. Vielemeyer O, Nizak C, Jimenez AJ, Echard A, Goud B, Camonis J, Rain JC, Perez F. Characterization of single chain antibody targets through yeast two hybrid. BMC Biotechnol 2010; 10:59; PMID:20727208; http://dx.doi.org/10.1186/ 1472-6750-10-59
31. Tanaka T, Rabbitts TH. Functional intracellular antibody fragments do not require invariant intradomain disulfide bonds. J Mol Biol 2008; 376:749-57; PMID:18187153; http://dx.doi.org/10.1016/j.jmb.2007.11.085
32. Loonstra A, Vooijs M, Beverloo HB, Allak BA, van Drunen E, Kanaar R, Berns A, Jonkers J. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc Natl Acad Sci U S A 2001; 98:9209-14; PMID:11481484; http://dx.doi.org/10.1073/pnas.161269798
33. Pfeifer A, Brandon EP, Kootstra N, Gage FH, Verma IM. Delivery of the Cre recombinase by a self-deleting lentiviral vector: efficient gene targeting in vivo. Proc Natl Acad Sci U S A 2001; 98:11450-5; PMID:11553794; http://dx.doi.org/10.1073/pnas.201415498
34. Lin Q, Jo D, Gebre-Amlak KD, Ruley HE. Enhanced cell-permeant Cre protein for site-specific recombination in cultured cells. BMC Biotechnol 2004; 4:25; PMID:15500682; http://dx.doi.org/10.1186/1472-6750-4-25
35. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10:310-5; PMID:14770178; http://dx.doi.org/10.1038/nm996
36. Will E, Klump H, Heffner N, Schwieger M, Schiedlmeier B, Ostertag W, Baum C, Stocking C. Unmodified Cre recombinase crosses the membrane. Nucleic Acids Res 2002; 30:e59; PMID:12060697; http://dx.doi.org/10.1093/nar/gnf059
37. Dalkara D, Zuber G, Behr JP. Intracytoplasmic delivery of anionic proteins. Mol Ther 2004; 9:964-9; PMID:15194063; http://dx.doi.org/10.1016/j. ymthe.2004.03.007
38. Bieber T, Meissner W, Kostin S, Niemann A, Elsasser HP. Intracellular route and transcriptional competence of polyethylenimine-DNA complexes. J Control Release 2002; 82:441-54; PMID:12175756; http://dx.doi.org/10.1016/S0168- 3659(02)00129-3
39. Gilleron J, Querbes W, Zeigerer A, Borodovsky A, Marsico G, Schubert U, Manygoats K, Seifert S, Andree C, Stöter M, et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat Biotechnol 2013; 31:638-46; PMID:23792630; http://dx.doi.org/10.1038/nbt.2612
40. Sahay G, Querbes W, Alabi C, Eltoukhy A, Sarkar S, Zurenko C, Karagiannis E, Love K, Chen D, Zoncu R, et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nat Biotechnol 2013; 31:653-8; PMID:23792629; http://dx.doi.org/10.1038/nbt.2614
41. Chu CJ, Dijkstra J, Lai MZ, Hong K, Szoka FC. Efficiency of cytoplasmic delivery by pH-sensitive liposomes to cells in culture. Pharm Res 1990; 7:824-34; PMID:2172955; http://dx.doi.org/10.1023/A:1015908831507
42. Dalkara D, Chandrashekhar C, Zuber G. Intracellular protein delivery with a dimerizable amphiphile for improved complex stability and prolonged protein release in the cytoplasm of adherent cell lines. J Control Release 2006; 116:353-9; PMID:17097756; http://dx.doi.org/10.1016/j.jconrel.2006.10.005
43. Tinsley JH, Zawieja DC, Wu MH, Ustinova EE, Xu W, Yuan SY. Protein transfection of intact microvessels specifically modulates vasoreactivity and permeability. J Vasc Res 2001; 38:444-52; PMID:11561146; http://dx.doi.org/10. 1159/000051077
44. Tinsley JH, Hawker J, Yuan Y. Efficient protein transfection of cultured coronary venular endothelial cells. Am J Physiol 1998; 275:H1873-8; PMID:9815096
45. Todorova R. Estimation of methods of protein delivery into mammalian cells - a comparative study by electroporation and bioporter assay. Prikl Biokhim Mikrobiol 2009; 45:493-6; PMID:19764622
46. van der Gun BT, Monami A, Laarmann S, Raskó T, Slaska-Kiss K, Weinhold E, Wasserkort R, de Leij LF, Ruiters MH, Kiss A, et al. Serum insensitive, intranuclear protein delivery by the multipurpose cationic lipid SAINT-2. J Control Release 2007; 123:228-38; PMID:17884225; http://dx.doi.org/ 10.1016/j.jconrel.2007.08.014
47. Weill CO, Biri S, Adib A, Erbacher P. A practical approach for intracellular protein delivery. Cytotechnology 2008; 56:41-8; PMID:19002840; http://dx.doi.org/10.1007/s10616-007-9102-3
48. Zelphati O, Wang Y, Kitada S, Reed JC, Felgner PL, Corbeil J. Intracellular delivery of proteins with a new lipid-mediated delivery system. J Biol Chem 2001; 276:35103-10; PMID:11447231; http://dx.doi.org/10.1074/jbc. M104920200
49. Samba-Louaka A, Nougayrède JP, Watrin C, Oswald E, Taieb F. The enteropathogenic Escherichia coli effector Cif induces delayed apoptosis in epithelial cells. Infect Immun 2009; 77:5471-7; PMID:19786559; http://dx.doi.org/10.1128/IAI.00860-09
50. Zassler B, Blasig IE, Humpel C. Protein delivery of caspase-3 induces cell death in malignant C6 glioma, primary astrocytes and immortalized and primary brain capillary endothelial cells. J Neurooncol 2005; 71:127-34; PMID:15690127; http://dx.doi.org/10.1007/s11060-004-1364-4
51. Freund G, Sibler AP, Desplancq D, Oulad-Abdelghani M, Vigneron M, Gannon J, Van Regenmortel MH, Weiss E. Targeting endogenous nuclear antigens by electrotransfer of monoclonal antibodies in living cells. MAbs 2013; 5:518-22; PMID:23765067; http://dx.doi.org/10.4161/mabs.25084
52. Bradbury AR, Sidhu S, Dübel S, McCafferty J. Beyond natural antibodies: the power of in vitro display technologies. Nat Biotechnol 2011; 29:245-54; PMID:21390033; http://dx.doi.org/10.1038/nbt.1791
53. Colwill K, Gräslund S; Renewable Protein Binder Working Group. A roadmap to generate renewable protein binders to the human proteome. Nat Methods 2011; 8:551-8; PMID:21572409; http://dx.doi.org/10.1038/nmeth.1607
54. Dübel S. Recombinant human antibodies for target discovery. Presentation and abstract. MIPTEC conference. Congress Centre Basel, 2012.
55. Jäger V, Büssow K, Wagner A, Weber S, Hust M, Frenzel A, Schirrmann T. High level transient production of recombinant antibodies and antibody fusion proteins in HEK293 cells. BMC Biotechnol 2013; 13:52; PMID:23802841; http://dx.doi.org/10.1186/1472-6750-13-52