Redox-responsive nanocapsules for intracellular protein delivery

Biomaterials

Volumn 32, Issue 22, 2011, Pages 5223-5230

  Zhao, Muxun ^a   Biswas, Anuradha ^a   Hu, Biliang ^b   Joo, Kye Il ^b   Wang, Pin ^b   Gu, Zhen ^a,c   Tang, Yi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Southern California ^*  (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Apoptosis; Degradable material; Disulfide; Endocytosis; Nanogels

Indexed keywords

APOPTOSIS; DEGRADABLE MATERIAL; DISULFIDE; ENDOCYTOSIS; NANOGELS;

CELL CULTURE; CELL DEATH; MEDICAL APPLICATIONS; MOLECULAR BIOLOGY; NANOCAPSULES; POLYMERS;

PROTEINS;

CASPASE 3; CROSS LINKING REAGENT; DISULFIDE; GLUTATHIONE; NANOCAPSULE; POLYMER; PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL FREE SYSTEM; CELL STRAIN MCF 7; CONTROLLED DRUG RELEASE; CONTROLLED STUDY; CYTOSOL; DISSOCIATION; DRUG DELIVERY SYSTEM; ENCAPSULATION; HELA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; OXIDATION REDUCTION POTENTIAL; POLYMERIZATION; PRIORITY JOURNAL;

APOPTOSIS; CELL LINE; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; HUMANS; MATERIALS TESTING; MOLECULAR STRUCTURE; NANOCAPSULES; OXIDATION-REDUCTION; PROTEINS;

EID: 79956078790     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.03.060     Document Type: Article

References (55)

1. Cotter T.G. Apoptosis and cancer: the genesis of a research field. Nat Rev Cancer 2009, 9:501-507.
2. Zhou H., Wu S., Joo J.Y., Zhu S., Han D.W., Lin T., et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, 4:381-384.
3. Ford K.G., Souberbielle B.E., Darling D., Farzaneh F. Protein transduction: an alternative to genetic intervention?. Gene Ther 2001, 8:1-4.
4. Gupta B., Levchenko T.S., Torchilin V.P. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev 2005, 57:637-651.
5. Hirakura T., Yasugi K., Nemoto T., Sato M., Shimoboji T., Aso Y., et al. Hybrid hyaluronan hydrogel encapsulating nanogel as a protein nanocarrier: new system for sustained delivery of protein with a chaperone-like function. J Control Release 2010, 142:483-489.
6. Frokjaer S., Otzen D.E. Protein drug stability: a formulation challenge. Nat Rev Drug Discov 2005, 4:298-306.
7. Murthy N., Campbell J., Fausto N., Hoffman A.S., Stayton P.S. Bioinspired pH-responsive polymers for the intracellular delivery of biomolecular drugs. Bioconjug Chem 2003, 14:412-419.
8. Haag R., Kratz F. Polymer therapeutics: concepts and applications. Angew Chem Int Ed 2006, 45:1198-1215.
9. Salmaso S., Bersani S., Semenzato A., Caliceti P. Nanotechnologies in protein delivery. J Nanosci Nanotechno 2006, 6:2736-2753.
10. Lu Y.J., Yang J., Sega E. Issues related to targeted delivery of proteins and peptides. AAPS J 2006, 8:E466-E478.
11. Yan Y., Johnston A.P.R., Dodds S.J., Kamphuis M.M.J., Ferguson C., Parton R.G., et al. Uptake and intracellular fate of disulfide-bonded polymer hydrogel capsules for doxorubicin delivery to colorectal cancer cells. ACS Nano 2010, 4:2928-2936.
12. Heath J.R., Davis M.E. Nanotechnology and cancer. Annu Rev Med 2008, 59:251-265.
13. Davis M.E., Chen Z., Shin D.M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008, 7:771-782.
14. Zelphati O., Wang Y., Kitada S., Reed J.C., Felgner P.L., Corbeil J. Intracellular delivery of proteins with a new lipid-mediated delivery system. J Biol Chem 2001, 276:35103-35110.
15. Martins S., Sarmento B., Ferreira D.C., Souto E.B. Lipid-based colloidal carriers for peptide and protein delivery - liposomes versus lipid nanoparticles. Int J Nanomed 2007, 2:595-607.
16. Mehnert W., Mader K. Solid lipid nanoparticles - production, characterization and applications. Adv Drug Deliv Rev 2001, 47:165-196.
17. Hu F.Q., Hong Y., Yuan H. Preparation and characterization of solid lipid nanoparticles containing peptide. Int J Pharm 2004, 273:29-35.
18. Gu Z., Yan M., Hu B., Joo K.I., Biswas A., Huang Y., et al. Protein nanocapsule weaved with enzymatically degradable polymeric network. Nano Lett 2009, 9:4533-4538.
19. Bachelder E.M., Beaudette T.T., Broaders K.E., Dashe J., Frechet J.M. Acetal-derivatized dextran: an acid-responsive biodegradable material for therapeutic applications. J Am Chem Soc 2008, 130:10494-10495.
20. Thornton P.D., Mart R.J., Ulijn R.V. Enzyme-responsive polymer hydrogel particles for controlled release. Adv Mater 2007, 19:1252.
21. Kim B., Peppas N.A. Poly(ethylene glycol)-containing hydrogels for oral protein delivery applications. Biomed Microdevices 2003, 5:333-341.
22. Murthy N., Xu M.C., Schuck S., Kunisawa J., Shastri N., Frechet J.M.J. A macromolecular delivery vehicle for protein-based vaccines: acid-degradable protein-loaded microgels. Proc Natl Acad Sci U S A 2003, 100:4995-5000.
23. Nochi T., Yuki Y., Takahashi H., Sawada S., Mejima M., Kohda T., et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nat Mater 2010, 9:572-578.
24. Ayame H., Morimoto N., Akiyoshi K. Self-assembled cationic nanogels for intracellular protein delivery. Bioconjug Chem 2008, 19:882-890.
25. Lee A.L., Wang Y., Ye W.H., Yoon H.S., Chan S.Y., Yang Y.Y. Efficient intracellular delivery of functional proteins using cationic polymer core/shell nanoparticles. Biomaterials 2008, 29:1224-1232.
26. Shu S., Zhang X., Wu Z., Wang Z., Li C. Gradient cross-linked biodegradable polyelectrolyte nanocapsules for intracellular protein drug delivery. Biomaterials 2010, 31:6039-6049.
27. Lee Y., Ishii T., Cabral H., Kim H.J., Seo J.H., Nishiyama N., et al. Charge-conversional polyionic complex micelles-efficient nanocarriers for protein delivery into cytoplasm. Angew Chem Int Ed Engl 2009, 48:5309-5312.
28. Lee Y., Ishii T., Kim H., Nishiyama N., Hayakawa Y., Itaka K., et al. Efficient delivery of bioactive antibodies into the cytoplasm of living cells by charge-conversional polyion complex micells. Angew Chem Int Ed 2010, 49:1-5.
29. Akagi T., Wang X., Uto T., Baba M., Akashi M. Protein direct delivery to dendritic cells using nanoparticles based on amphiphilic poly(amino acid) derivatives. Biomaterials 2007, 28:3427-3436.
30. Medintz I.L., Pons T., Delehanty J.B., Susumu K., Brunel F.M., Dawson P.E., et al. Intracellular delivery of quantum dot-protein cargos mediated by cell penetrating peptides. Bioconjug Chem 2008, 19:1785-1795.
31. Ghosh P., Yang X., Arvizo R., Zhu Z.J., Agasti S.S., Mo Z., et al. Intracellular delivery of a membrane-impermeable enzyme in active form using functionalized gold nanoparticles. J Am Chem Soc 2010, 132:2642-2645.
32. Slowing I.I., Trewyn B.G., Lin V.S. Mesoporous silica nanoparticles for intracellular delivery of membrane-impermeable proteins. J Am Chem Soc 2007, 129:8845-8849.
33. Bale S.S., Kwon S.J., Shah D.A., Banerjee A., Dordick J.S., Kane R.S. Nanoparticle-mediated cytoplasmic delivery of proteins to target cellular machinery. ACS Nano 2010, 4:1493-1500.
34. Shimkunas R.A., Robinson E., Lam R., Lu S., Xu X.Y., Zhang X.Q., et al. Nanodiamond-insulin complexes as pH-dependent protein delivery vehicles. Biomaterials 2009, 30:5720-5728.
35. Kam N.W.S., Jessop T.C., Wender P.A., Dai H.J. Nanotube molecular transporters: internalization of carbon nanotube-protein conjugates into mammalian cells. J Am Chem Soc 2004, 126:6850-6851.
36. Crinelli R., Carloni E., Menotta M., Giacomini E., Bianchi M., Ambrosi G., et al. Oxidized ultrashort nanotubes as carbon scaffolds for the construction of cell-penetrating NF-kappa b decoy molecules. ACS Nano 2010, 4:2791-2803.
37. Kam N.W.S., Liu Z.A., Dai H.J. Carbon nanotubes as intracellular transporters for proteins and DNA: an investigation of the uptake mechanism and pathway. Angew Chem Int Ed 2006, 45:577-581.
38. Abbing A., Blaschke U.K., Grein S., Kretschmar M., Stark C.M., Thies M.J., et al. Efficient intracellular delivery of a protein and a low molecular weight substance via recombinant polyomavirus-like particles. J Biol Chem 2004, 279:27410-27421.
39. Cronican J.J., Thompson D.B., Beier K.T., McNaughton B.R., Cepko C.L., Liu D.R. Potent delivery of functional proteins into mammalian cells in vitro and in vivo using a supercharged protein. ACS Chem Biol 2010, 5:747-752.
40. Lim Y.T., Cho M.Y., Lee J.M., Chung S.J., Chung B.H. Simultaneous intracellular delivery of targeting antibodies and functional nanoparticles with engineered protein G system. Biomaterials 2009, 30:1197-1204.
41. Christian D.A., Cai S., Bowen D.M., Kim Y., Pajerowski J.D., Discher D.E. Polymersome carriers: from self-assembly to sirna and protein therapeutics. Eur J Pharm Biopharm 2009, 71:463-474.
42. Parveen S., Sahoo S.K. Nanomedicine - clinical applications of polyethylene glycol conjugated proteins and drugs. Clin Pharmacokinet 2006, 45:965-988.
43. Zhang Z.H., Cao W.G., Jin H.L., Lovell J.F., Yang M., Ding L.L., et al. Biomimetic nanocarrier for direct cytosolic drug delivery. Angew Chem Int Ed 2009, 48:9171-9175.
44. Biswas A., Joo K., Liu J., Zhao M., Fan G., Wang P., et al. Endoprotease-mediated intracellular protein delivery using nanocapsules. ACS Nano 2011, 5:1385-1394.
45. Meister A., Tate S.S. Glutathione and related gamma-glutamyl compounds: biosynthesis and utilization. Annu Rev Biochem 1976, 45:559-604.
46. Bauhuber S., Hozsa C., Breunig M., Gopferich A. Delivery of nucleic acids via disulfide-based carrier systems. Adv Mater 2009, 21:3286-3306.
47. Takae S., Miyata K., Oba M., Ishii T., Nishiyama N., Itaka K., et al. PEG-detachable polyplex micelles based on disulfide-linked block catiomers as bioresponsive nonviral gene vectors. J Am Chem Soc 2008, 130:6001-6009.
48. You Y.Z., Manickam D.S., Zhou Q.H., Oupicky D. Reducible poly(2-dimethylaminoethyl methaerylate): synthesis, cytotoxicity, and gene delivery activity. J Control Release 2007, 122:217-225.
49. Kakizawa Y., Harada A., Kataoka K. Glutathione-sensitive stabilization of block copolymer micelles composed of antisense DNA and thiolated poly(ethylene glycol)-block-poly(l-lysine): a potential carrier for systemic delivery of antisense DNA. Biomacromolecules 2001, 2:491-497.
50. Lee Y., Mo H., Koo H., Park J.Y., Cho M.Y., Jin G.W., et al. Visualization of the degradation of a disulfide polymer, linear poly(ethylenimine sulfide), for gene delivery. Bioconjug Chem 2007, 18:13-18.
51. Talanian R.V., Quinlan C., Trautz S., Hackett M.C., Mankovich J.A., Banach D., et al. Substrate specificities of caspase family proteases. J Biol Chem 1997, 272:9677-9682.
52. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992, 119:493-501.
53. Peer D., Karp J.M., Hong S., FaroKHzad O.C., Margalit R., Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007, 2:751-760.
54. Joerger A.C., Fersht A.R. Structure-function-rescue: the diverse nature of common p53 cancer mutants. Oncogene 2007, 26:2226-2242.
55. Noteborn M.H. Proteins selectively killing tumor cells. Eur J Pharmacol 2009, 625:165-173.