Efficient Delivery of Structurally Diverse Protein Cargo into Mammalian Cells by a Bacterial Toxin

Molecular Pharmaceutics

Volumn 12, Issue 8, 2015, Pages 2962-2971

  Auger, Anick ^a   Park, Minyoung ^a,b   Nitschke, Felix ^a   Minassian, Lori M ^a   Beilhartz, Greg L ^a   Minassian, Berge A ^a,c   Melnyk, Roman A ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

diphtheria toxin; intracellular protein delivery; toxin translocation

Indexed keywords

AMYLASE; DIPHTHERIA TOXIN; GLYCOGEN; PEPTIDE FRAGMENT;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL SPECIFICITY; CHIMERA; DRUG DELIVERY SYSTEM; INVESTIGATIVE PROCEDURES; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; TARGET CELL; CHEMISTRY; DIFFERENTIAL SCANNING CALORIMETRY; HEK293 CELL LINE; HUMAN; METABOLISM; PROTEIN FOLDING;

ALPHA-AMYLASES; CALORIMETRY, DIFFERENTIAL SCANNING; DIPHTHERIA TOXIN; DRUG DELIVERY SYSTEMS; GLYCOGEN; HEK293 CELLS; HUMANS; PEPTIDE FRAGMENTS; PROTEIN FOLDING;

EID: 84938343485     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00233     Document Type: Article

References (56)

1. Frankel, A. D.; Pabo, C. O. Cellular uptake of the tat protein from human immunodeficiency virus Cell 1988, 55, 1189-1193 10.1016/0092-8674(88)90263-2
2. Garcia-Echeverria, C.; Jiang, L.; Ramsey, T. M.; Sharma, S. K.; Chen, Y. P. A new Antennapedia-derived vector for intracellular delivery of exogenous compounds Bioorg. Med. Chem. Lett. 2001, 11, 1363-1366 10.1016/S0960-894X(01)00208-6
3. Heitz, F.; Morris, M. C.; Divita, G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics Br. J. Pharmacol. 2009, 157, 195-206 10.1111/j.1476-5381.2009.00057.x
4. Karagiannis, E. D. Rational design of a biomimetic cell penetrating peptide library ACS Nano 2013, 7, 8616-8626 10.1021/nn4027382
5. Zelphati, O. Intracellular delivery of proteins with a new lipid-mediated delivery system J. Biol. Chem. 2001, 276, 35103-35110 10.1074/jbc.M104920200
6. Hasadsri, L.; Kreuter, J.; Hattori, H.; Iwasaki, T.; George, J. M. Functional protein delivery into neurons using polymeric nanoparticles J. Biol. Chem. 2009, 284, 6972-6981 10.1074/jbc.M805956200
7. Lewin, M. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells Nat. Biotechnol. 2000, 18, 410-414 10.1038/74464
8. Panyam, J.; Labhasetwar, V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue Adv. Drug Delivery Rev. 2003, 55, 329-347 10.1016/S0169-409X(02)00228-4
9. Worsdorfer, B.; Pianowski, Z.; Hilvert, D. Efficient in vitro encapsulation of protein cargo by an engineered protein container J. Am. Chem. Soc. 2012, 134, 909-911 10.1021/ja211011k
10. Gaj, T.; Liu, J.; Anderson, K. E.; Sirk, S. J.; Barbas, C. F., 3rd. Protein delivery using Cys2-His2 zinc-finger domains ACS Chem. Biol. 2014, 9, 1662-1667 10.1021/cb500282g
11. Gaj, T.; Guo, J.; Kato, Y.; Sirk, S. J.; Barbas, C. F., 3rd. Targeted gene knockout by direct delivery of zinc-finger nuclease proteins Nat. Methods 2012, 9, 805-807 10.1038/nmeth.2030
12. Thompson, D. B.; Villasenor, R.; Dorr, B. M.; Zerial, M.; Liu, D. R. Cellular uptake mechanisms and endosomal trafficking of supercharged proteins Chem. Biol. 2012, 19, 831-843 10.1016/j.chembiol.2012.06.014
13. Thompson, D. B.; Cronican, J. J.; Liu, D. R. Engineering and identifying supercharged proteins for macromolecule delivery into mammalian cells Methods Enzymol. 2012, 503, 293-319 10.1016/B978-0-12-396962-0.00012-4
14. Zhao, M. Redox-responsive nanocapsules for intracellular protein delivery Biomaterials 2011, 32, 5223-5230 10.1016/j.biomaterials.2011.03.060
15. Greenfield, L. Nucleotide sequence of the structural gene for diphtheria toxin carried by corynebacteriophage beta Proc. Natl. Acad. Sci. U. S. A. 1983, 80, 6853-6857 10.1073/pnas.80.22.6853
16. Naglich, J. G.; Metherall, J. E.; Russell, D. W.; Eidels, L. Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor Cell 1992, 69, 1051-1061 10.1016/0092-8674(92)90623-K
17. Moya, M.; Dautry-Varsat, A.; Goud, B.; Louvard, D.; Boquet, P. Inhibition of coated pit formation in Hep2 cells blocks the cytotoxicity of diphtheria toxin but not that of ricin toxin J. Cell Biol. 1985, 101, 548-559 10.1083/jcb.101.2.548
18. Donovan, J. J.; Simon, M. I.; Draper, R. K.; Montal, M. Diphtheria toxin forms transmembrane channels in planar lipid bilayers Proc. Natl. Acad. Sci. U. S. A. 1981, 78, 172-176 10.1073/pnas.78.1.172
19. Donovan, J. J.; Simon, M. I.; Montal, M. Insertion of diphtheria toxin into and across membranes: role of phosphoinositide asymmetry Nature 1982, 298, 669-672 10.1038/298669a0
20. Donovan, J. J.; Simon, M. I.; Montal, M. Requirements for the translocation of diphtheria toxin fragment A across lipid membranes J. Biol. Chem. 1985, 260, 8817-8823
21. Lai, B.; Zhao, G.; London, E. Behavior of the deeply inserted helices in diphtheria toxin T domain: helices 5, 8, and 9 interact strongly and promote pore formation, while helices 6/7 limit pore formation Biochemistry 2008, 47, 4565-4574 10.1021/bi7025134
22. Olsnes, S.; Falnes, P. O. Probing pores with peptide plugs. Topology of membrane-inserted diphtheria toxin J. Gen. Physiol. 2000, 115, 417-420 10.1085/jgp.115.4.417
23. Sharpe, J. C.; London, E. Diphtheria toxin forms pores of different sizes depending on its concentration in membranes: probable relationship to oligomerization J. Membr. Biol. 1999, 171, 209-221 10.1007/s002329900572
24. Sandvig, K.; Olsnes, S. Rapid entry of nicked diphtheria toxin into cells at low pH. Characterization of the entry process and effects of low pH on the toxin molecule J. Biol. Chem. 1981, 256, 9068-9076
25. Collier, R. J.; Pappenheimer, A. M., Jr. Studies on the Mode of Action of Diphtheria Toxin. Ii. Effect of Toxin on Amino Acid Incorporation in Cell-Free Systems J. Exp. Med. 1964, 120, 1019-1039 10.1084/jem.120.6.1019
26. Collier, R. J. Effect of diphtheria toxin on protein synthesis: inactivation of one of the transfer factors J. Mol. Biol. 1967, 25, 83-98 10.1016/0022-2836(67)90280-X
27. Williams, D. P. Diphtheria toxin receptor binding domain substitution with interleukin-2: genetic construction and properties of a diphtheria toxin-related interleukin-2 fusion protein Protein Eng., Des. Sel. 1987, 1, 493-498 10.1093/protein/1.6.493
28. Jean, L. F.; Murphy, J. R. Diphtheria toxin receptor-binding domain substitution with interleukin 6: genetic construction and interleukin 6 receptor-specific action of a diphtheria toxin-related interleukin 6 fusion protein Protein Eng., Des. Sel. 1991, 4, 989-994 10.1093/protein/4.8.989
29. Aullo, P. A recombinant diphtheria toxin related human CD4 fusion protein specifically kills HIV infected cells which express gp120 but selects fusion toxin resistant cells which carry HIV EMBO J. 1992, 11, 575-583
30. Madshus, I. H.; Olsnes, S.; Stenmark, H. Membrane translocation of diphtheria toxin carrying passenger protein domains Infect. Immun. 1992, 60, 3296-3302
31. Stenmark, H.; Moskaug, J. O.; Madshus, I. H.; Sandvig, K.; Olsnes, S. Peptides fused to the amino-terminal end of diphtheria toxin are translocated to the cytosol J. Cell Biol. 1991, 113, 1025-1032 10.1083/jcb.113.5.1025
32. Wiedlocha, A.; Madshus, I. H.; Mach, H.; Middaugh, C. R.; Olsnes, S. Tight folding of acidic fibroblast growth factor prevents its translocation to the cytosol with diphtheria toxin as vector EMBO J. 1992, 11, 4835-4842
33. Klingenberg, O.; Olsnes, S. Ability of methotrexate to inhibit translocation to the cytosol of dihydrofolate reductase fused to diphtheria toxin Biochem. J. 1996, 313 (Pt 2) 647-653
34. Ainavarapu, S. R.; Li, L.; Badilla, C. L.; Fernandez, J. M. Ligand binding modulates the mechanical stability of dihydrofolate reductase Biophys. J. 2005, 89, 3337-3344 10.1529/biophysj.105.062034
35. Passonneau, J. V.; Gatfield, P. D.; Schulz, D. W.; Lowry, O. H. An enzymic method for measurement of glycogen Anal. Biochem. 1967, 19, 315-326 10.1016/0003-2697(67)90167-4
36. Francis, J. W. A survival motor neuron:tetanus toxin fragment C fusion protein for the targeted delivery of SMN protein to neurons Brain Res. 2004, 995, 84-96 10.1016/j.brainres.2003.09.063
37. Fu, H.; Blanke, S. R.; Mattheakis, L. C.; Collier, R. J. Selection of diphtheria toxin active-site mutants in yeast. Rediscovery of glutamic acid-148 as a key residue Adv. Exp. Med Biol. 1997, 419, 45-52
38. Murphy, J. R. Mechanism of diphtheria toxin catalytic domain delivery to the eukaryotic cell cytosol and the cellular factors that directly participate in the process Toxins 2011, 3, 294-308 10.3390/toxins3030294
39. Stepanenko, O. V. Comparative studies on the structure and stability of fluorescent proteins EGFP, zFP506, mRFP1, "dimer", and DsRed1 Biochemistry 2004, 43, 14913-14923 10.1021/bi048725t
40. Verkhusha, V. V. High stability of Discosoma DsRed as compared to Aequorea EGFP Biochemistry 2003, 42, 7879-7884 10.1021/bi034555t
41. Lemichez, E. Membrane translocation of diphtheria toxin fragment A exploits early to late endosome trafficking machinery Mol. Microbiol. 1997, 23, 445-457 10.1111/j.1365-2958.1997.tb02669.x
42. Falnes, P. O.; Wesche, J.; Olsnes, S. Ability of the Tat basic domain and VP22 to mediate cell binding, but not membrane translocation of the diphtheria toxin A-fragment Biochemistry 2001, 40, 4349-4358 10.1021/bi002443l
43. Kiyokawa, T.; Williams, D. P.; Snider, C. E.; Strom, T. B.; Murphy, J. R. Protein engineering of diphtheria-toxin-related interleukin-2 fusion toxins to increase cytotoxic potency for high-affinity IL-2-receptor-bearing target cells Protein Eng., Des. Sel. 1991, 4, 463-468 10.1093/protein/4.4.463
44. Choudhary, S.; Mathew, M.; Verma, R. S. Therapeutic potential of anticancer immunotoxins Drug Discovery Today 2011, 16, 495-503 10.1016/j.drudis.2011.04.003
45. Alewine, C.; Hassan, R.; Pastan, I. Advances in Anticancer Immunotoxin Therapy Oncologist 2015, 20, 176 10.1634/theoncologist.2014-0358
46. Mazor, R. Identification and elimination of an immunodominant T-cell epitope in recombinant immunotoxins based on Pseudomonas exotoxin A Proc. Natl. Acad. Sci. U. S. A. 2012, 109, E3597-3603 10.1073/pnas.1218138109
47. Barth, H.; Hofmann, F.; Olenik, C.; Just, I.; Aktories, K. The N-terminal part of the enzyme component (C2I) of the binary Clostridium botulinum C2 toxin interacts with the binding component C2II and functions as a carrier system for a Rho ADP-ribosylating C3-like fusion toxin Infect. Immun. 1998, 66, 1364-1369
48. Ballard, J. D.; Collier, R. J.; Starnbach, M. N. Anthrax toxin-mediated delivery of a cytotoxic T-cell epitope in vivo Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 12531-12534 10.1073/pnas.93.22.12531
49. Leppla, S. H.; Arora, N.; Varughese, M. Anthrax toxin fusion proteins for intracellular delivery of macromolecules J. Appl. Microbiol. 1999, 87, 284 10.1046/j.1365-2672.1999.00890.x
50. Bachran, C. Anthrax toxin-mediated delivery of the Pseudomonas exotoxin A enzymatic domain to the cytosol of tumor cells via cleavable ubiquitin fusions mBio 2013, 4, e00201 10.1128/mBio.00201-13
51. Liao, X.; Rabideau, A. E.; Pentelute, B. L. Delivery of antibody mimics into mammalian cells via anthrax toxin protective antigen ChemBioChem 2014, 15, 2458-2466 10.1002/cbic.201402290
52. Benson, E. L.; Huynh, P. D.; Finkelstein, A.; Collier, R. J. Identification of residues lining the anthrax protective antigen channel Biochemistry 1998, 37, 3941-3948 10.1021/bi972657b
53. Krantz, B. A. A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore Science 2005, 309, 777-781 10.1126/science.1113380
54. Zornetta, I. Imaging the cell entry of the anthrax oedema and lethal toxins with fluorescent protein chimeras Cell. Microbiol. 2010, 12, 1435-1445 10.1111/j.1462-5822.2010.01480.x
55. Nagata, S.; Pastan, I. Removal of B cell epitopes as a practical approach for reducing the immunogenicity of foreign protein-based therapeutics Adv. Drug Delivery Rev. 2009, 61, 977-985 10.1016/j.addr.2009.07.014
56. King, C. Removing T-cell epitopes with computational protein design Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 8577-8582 10.1073/pnas.1321126111