Enhanced cellular entry and efficacy of tat conjugates by rational design of the auxiliary segment

Molecular Pharmaceutics

Volumn 11, Issue 3, 2014, Pages 964-973

  Zhang, Pengcheng ^a   Lock, Lye Lin ^a   Cheetham, Andrew G ^a   Cui, Honggang ^a  

^a Johns Hopkins University   (United States)

Author keywords

cell penetrating peptide; cellular uptake; multidrug resistant; nanobeacon

Indexed keywords

6 CARBOXYFLUORESCEIN; ANTINEOPLASTIC AGENT; DOXORUBICIN; TAT 5 CARBOXYFLUORESCEIN CONJUGATE; TAT DOXORUBICIN CONJUGATE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; 4-CARBOXYFLUORESCEIN; FLUORESCEIN DERIVATIVE; PEPTIDE FRAGMENT;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL MEMBRANE; CELL STRAIN MCF 7; CELL TRANSPORT; CONJUGATE; COVALENT BOND; CYTOTOXICITY; DRUG CONJUGATION; FLOW CYTOMETRY; FLUORESCENCE IMAGING; HYDROPHOBICITY; INTERNALIZATION; MEMBRANE PERMEABILITY; PALMITOYLATION; PRIORITY JOURNAL; UTERINE CERVIX CANCER; APOPTOSIS; BREAST NEOPLASMS; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; HUMAN; LIPOYLATION; METABOLISM; PATHOLOGY; TUMOR CELL CULTURE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; DOXORUBICIN; FEMALE; FLOW CYTOMETRY; FLUORESCEINS; HUMANS; LIPOYLATION; PEPTIDE FRAGMENTS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TUMOR CELLS, CULTURED;

EID: 84901743395     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400619v     Document Type: Article

References (66)

1. Overington, J. P.; Al-Lazikani, B.; Hopkins, A. L. Opinion-How Many Drug Targets Are There? Nat. Rev. Drug Discovery 2006, 5, 993-996
2. Whitehead, K. A.; Langer, R.; Anderson, D. G. Knocking Down Barriers: Advances in Sirna Delivery Nat. Rev. Drug Discovery 2009, 8, 129-138
3. McCormick, F. Cancer Gene Therapy: Fringe or Cutting Edge? Nat. Rev. Cancer 2001, 1, 130-141
4. Lindgren, M.; Hallbrink, M.; Prochiantz, A.; Langel, U. Cell-Penetrating Peptides Trends Pharmacol. Sci. 2000, 21, 99-103
5. Leeson, P. D.; Springthorpe, B. The Influence of Drug-Like Concepts on Decision-Making in Medicinal Chemistry Nat. Rev. Drug Discovery 2007, 6, 881-890
6. Barabasi, A. L.; Gulbahce, N.; Loscalzo, J. Network Medicine: A Network-Based Approach to Human Disease Nat. Rev. Genet. 2011, 12, 56-68
7. Hanahan, D.; Weinberg, R. A. Hallmarks of Cancer: The Next Generation Cell 2011, 144, 646-674
8. Coster, H. G. L. A Quantitative Analysis of Voltage-Current Relationships of Fixed Charge Membranes and Associated Property of Punch-Through Biophys. J. 1965, 5, 669-686
9. Sharei, A.; Zoldan, J.; Adamo, A.; Sim, W. Y.; Cho, N.; Jackson, E.; Mao, S.; Schneider, S.; Han, M. J.; Lytton-Jean, A.; Basto, P. A.; Jhunjhunwala, S.; Lee, J.; Heller, D. A.; Kang, J. W.; Hartoularos, G. C.; Kim, K. S.; Anderson, D. G.; Langer, R.; Jensen, K. F. A Vector-Free Microfluidic Platform for Intracellular Delivery Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 2082-2087
10. Zheng, D.; Seferos, D. S.; Giljohann, D. A.; Patel, P. C.; Mirkin, C. A. Aptamer Nano-Flares for Molecular Detection in Living Cells Nano Lett. 2009, 9, 3258-3261
11. Zheng, D.; Giljohann, D. A.; Chen, D. L.; Massich, M. D.; Wang, X. Q.; Iordanov, H.; Mirkin, C. A.; Paller, A. S. Topical Delivery of Sirna-Based Spherical Nucleic Acid Nanoparticle Conjugates for Gene Regulation Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 11975-11980
12. Gullotti, E.; Yeo, Y. Beyond the Imaging: Limitations of Cellular Uptake Study in the Evaluation of Nanoparticles J. Controlled Release 2012, 164, 170-176
13. Xu, P. S.; Gullotti, E.; Tong, L.; Highley, C. B.; Errabelli, D. R.; Hasan, T.; Cheng, J. X.; Kohane, D. S.; Yeo, Y. Intracellular Drug Delivery by Poly(Lactic-Co-Glycolic Acid) Nanoparticles, Revisited Mol. Pharmaceutics 2009, 6, 190-201
14. Jones, C. H.; Chen, C. K.; Jiang, M.; Fang, L.; Cheng, C.; Pfeifer, B. A. Synthesis of Cationic Polylactides with Tunable Charge Densities as Nanocarriers for Effective Gene Delivery Mol. Pharmaceutics 2013, 10, 1138-1145
15. Panyam, J.; Labhasetwar, V. Biodegradable Nanoparticles for Drug and Gene Delivery to Cells and Tissue Adv. Drug Delivery Rev. 2003, 55, 329-347
16. Gao, Y.; Berciu, C.; Kuang, Y.; Shi, J.; Nicastro, D.; Xu, B. Probing Nanoscale Self-Assembly of Nonfluorescent Small Molecules inside Live Mammalian Cells ACS Nano 2013, 7, 9055-9063
17. Yu, Y.; Chen, C. K.; Law, W. C.; Mok, J.; Zou, J.; Prasad, P. N.; Cheng, C. Well-Defined Degradable Brush Polymer-Drug Conjugates for Sustained Delivery of Paclitaxel Mol. Pharmaceutics 2013, 10, 867-874
18. Koren, E.; Torchilin, V. P. Cell-Penetrating Peptides: Breaking through to the Other Side Trends Mol. Med. 2012, 18, 385-393
19. Vives, E.; Brodin, P.; Lebleu, B. A Truncated Hiv-1 Tat Protein Basic Domain Rapidly Translocates through the Plasma Membrane and Accumulates in the Cell Nucleus J. Biol. Chem. 1997, 272, 16010-16017
20. Brooks, H.; Lebleu, B.; Vives, E. Tat Peptide-Mediated Cellular Delivery: Back to Basics Adv. Drug Delivery Rev. 2005, 57, 559-577
21. Zhang, K.; Fang, H.; Chen, Z.; Taylor, J. S.; Wooley, K. L. Shape Effects of Nanoparticles Conjugated with Cell-Penetrating Peptides (Hiv Tat Ptd) on Cho Cell Uptake Bioconjugate Chem. 2008, 19, 1880-1887
22. Zhang, P.; Cheetham, A. G.; Lock, L. L.; Cui, H. Cellular Uptake and Cytotoxicity of Drug-Peptide Conjugates Regulated by Conjugation Site Bioconjugate Chem. 2013, 24, 604-613
23. Aroui, S.; Ram, N.; Appaix, F.; Ronjat, M.; Kenani, A.; Pirollet, F.; De Waard, M. Maurocalcine as a Non Toxic Drug Carrier Overcomes Doxorubicin Resistance in the Cancer Cell Line Mda-Mb 231 Pharm. Res. 2009, 26, 836-845
24. Richard, J. P.; Melikov, K.; Brooks, H.; Prevot, P.; Lebleu, B.; Chernomordik, L. V. Cellular Uptake of Unconjugated Tat Peptide Involves Clathrin-Dependent Endocytosis and Heparan Sulfate Receptors J. Biol. Chem. 2005, 280, 15300-15306
25. Mishra, A.; Lai, G. H.; Schmidt, N. W.; Sun, V. Z.; Rodriguez, A. R.; Tong, R.; Tang, L.; Cheng, J.; Deming, T. J.; Kamei, D. T.; Wong, G. C. Translocation of Hiv Tat Peptide and Analogues Induced by Multiplexed Membrane and Cytoskeletal Interactions Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16883-16888
26. Lock, L. L.; Cheetham, A. G.; Zhang, P. C.; Cui, H. G. Design and Construction of Supramolecular Nanobeacons for Enzyme Detection ACS Nano 2013, 7, 4924-4932
27. Zhang, P. C.; Cheetham, A. G.; Lin, Y.-A.; Cui, H. G. Self-Assembled Tat Nanofibers as Effective Drug Carrier and Transporter ACS Nano 2013, 7, 5965-5977
28. Daniels, D. S.; Schepartz, A. Intrinsically Cell-Permeable Miniature Proteins Based on a Minimal Cationic PPII Motif J. Am. Chem. Soc. 2007, 129, 14578-14579
29. Takayama, K.; Nakase, I.; Michiue, H.; Takeuchi, T.; Tomizawa, K.; Matsui, H.; Futaki, S. Enhanced Intracellular Delivery Using Arginine-Rich Peptides by the Addition of Penetration Accelerating Sequences (Pas) J. Controlled Release 2009, 138, 128-133
30. Takayama, K.; Hirose, H.; Tanaka, G.; Pujals, S.; Katayama, S.; Nakase, I.; Futaki, S. Effect of the Attachment of a Penetration Accelerating Sequence and the Influence of Hydrophobicity on Octaarginine-Mediated Intracellular Delivery Mol. Pharmaceutics 2012, 9, 1222-1230
31. Ye, G.; Nam, N. H.; Kumar, A.; Saleh, A.; Shenoy, D. B.; Amiji, M. M.; Lin, X.; Sun, G.; Parang, K. Synthesis and Evaluation of Tripodal Peptide Analogues for Cellular Delivery of Phosphopeptides J. Med. Chem. 2007, 50, 3604-3617
32. Nasrolahi Shirazi, A.; Oh, D.; Tiwari, R. K.; Sullivan, B.; Gupta, A.; Bothun, G. D.; Parang, K. Peptide Amphiphile Containing Arginine and Fatty Acyl Chains as Molecular Transporters Mol. Pharmaceutics 2013, 10, 4717-4727
33. Missirlis, D.; Teesalu, T.; Black, M.; Tirrell, M. The Non-Peptidic Part Determines the Internalization Mechanism and Intracellular Trafficking of Peptide Amphiphiles PLoS One 2013, 8, e54611
34. Futaki, S.; Ohashi, W.; Suzuki, T.; Niwa, M.; Tanaka, S.; Ueda, K.; Harashima, H.; Sugiura, Y. Stearylated Arginine-Rich Peptides: A New Class of Transfection Systems Bioconjugate Chem. 2001, 12, 1005-1011
35. Lehto, T.; Abes, R.; Oskolkov, N.; Suhorutsenko, J.; Copolovici, D. M.; Mager, I.; Viola, J. R.; Simonson, O. E.; Ezzat, K.; Guterstam, P.; Eriste, E.; Smith, C. I. E.; Lebleu, B.; El Andaloussi, S.; Langel, U. Delivery of Nucleic Acids with a Stearylated (Rxr)(4) Peptide Using a Non-Covalent Co-Incubation Strategy J. Controlled Release 2010, 141, 42-51
36. Li, G. H.; Li, W. X.; Mumper, R. J.; Nath, A. Molecular Mechanisms in the Dramatic Enhancement of Hiv-1 Tat Transduction by Cationic Liposomes FASEB J. 2012, 26, 2824-2834
37. Duncan, R.; Cable, H. C.; Lloyd, J. B.; Rejmanova, P.; Kopecek, J. Degradation of Side-Chains of N-(2-Hydroxypropyl)Methacrylamide Copolymers by Lysosomal Thiol-Proteinases Biosci. Rep. 1982, 2, 1041-1046
38. Duncan, R.; Cable, H. C.; Lloyd, J. B.; Rejmanova, P.; Kopecek, J. Polymers Containing Enzymatically Degradable Bonds. 7. Design of Oligopeptide Side-Chains in Poly[N-(2-Hydroxypropyl)-Methacrylamide] Co-Polymers to Promote Efficient Degradation by Lysosomal-Enzymes Makromol. Chem. 1983, 184, 1997-2008
39. Teich, N.; Bodeker, H.; Keim, V. Cathepsin B Cleavage of the Trypsinogen Activation Peptide BMC Gastroenterol. 2002, 2, 16
40. Duncan, R. Polymer Conjugates as Anticancer Nanomedicines Nat. Rev. Cancer 2006, 6, 688-701
41. Chu-Kung, A. F.; Nguyen, R.; Bozzelli, K. N.; Tirrell, M. Chain Length Dependence of Antimicrobial Peptide-Fatty Acid Conjugate Activity J. Colloid Interface Sci. 2010, 345, 160-167
42. Hartgerink, J. D.; Beniash, E.; Stupp, S. I. Self-Assembly and Mineralization of Peptide-Amphiphile Nanofibers Science 2001, 294, 1684-1688
43. Fry, H. C.; Garcia, J. M.; Medina, M. J.; Ricoy, U. M.; Gosztola, D. J.; Nikiforov, M. P.; Palmer, L. C.; Stupp, S. I. Self-Assembly of Highly Ordered Peptide Amphiphile Metalloporphyrin Arrays J. Am. Chem. Soc. 2012, 134, 14646-14649
44. Sur, S.; Matson, J. B.; Webber, M. J.; Newcomb, C. J.; Stupp, S. I. Photodynamic Control of Bioactivity in a Nanofiber Matrix ACS Nano 2012, 6, 10776-10785
45. Black, M.; Trent, A.; Kostenko, Y.; Lee, J. S.; Olive, C.; Tirrell, M. Self-Assembled Peptide Amphiphile Micelles Containing a Cytotoxic T-Cell Epitope Promote a Protective Immune Response in Vivo Adv. Mater. 2012, 24, 3845-3849
46. Ghose, A. K.; Viswanadhan, V. N.; Wendoloski, J. J. A Knowledge-Based Approach in Designing Combinatorial or Medicinal Chemistry Libraries for Drug Discovery. 1. A Qualitative and Quantitative Characterization of Known Drug Databases J. Comb. Chem. 1999, 1, 55-68
47. Missirlis, D.; Farine, M.; Kastantin, M.; Ananthanarayanan, B.; Neumann, T.; Tirrell, M. Linker Chemistry Determines Secondary Structure of P53(14-29) in Peptide Amphiphile Micelles Bioconjugate Chem. 2010, 21, 465-475
48. Missirlis, D.; Chworos, A.; Fu, C. J.; Khant, H. A.; Krogstad, D. V.; Tirrell, M. Effect of the Peptide Secondary Structure on the Peptide Amphiphile Supramolecular Structure and Interactions Langmuir 2011, 27, 6163-6170
49. Mier, W.; Zitzmann, S.; Kramer, S.; Reed, J.; Knapp, E. M.; Altmann, A.; Eisenhut, M.; Haberkorn, U. Influence of Chelate Conjugation on a Newly Identified Tumor-Targeting Peptide J. Nucl. Med. 2007, 48, 1545-1552
50. Duchardt, F.; Ruttekolk, I. R.; Verdurmen, W. P. R.; Lortat-Jacob, H.; Burck, J.; Hufnagel, H.; Fischer, R.; van den Heuvel, M.; Lowik, D. W. P. M.; Vuister, G. W.; Ulrich, A.; de Waard, M.; Brock, R. A Cell-Penetrating Peptide Derived from Human Lactoferrin with Conformation-Dependent Uptake Efficiency J. Biol. Chem. 2009, 284, 36099-36108
51. Lin, B. F.; Missirlis, D.; Krogstad, D. V.; Tirrell, M. Structural Effects and Lipid Membrane Interactions of the Ph-Responsive Gala Peptide with Fatty Acid Acylation Biochemistry 2012, 51, 4658-4668
52. Missirlis, D.; Khant, H.; Tirrell, M. Mechanisms of Peptide Amphiphile Internalization by Sjsa-1 Cells in Vitro Biochemistry 2009, 48, 3304-3314
53. Persidis, A. Cancer Multidrug Resistance Nat. Biotechnol. 1999, 17, 94-95
54. Akiyama, S. I.; Fojo, A.; Hanover, J. A.; Pastan, I.; Gottesman, M. M. Isolation and Genetic Characterization of Human Kb-Cell Lines Resistant to Multiple-Drugs Somatic Cell Mol. Genet. 1985, 11, 117-126
55. Cao, N.; Feng, S. S. Doxorubicin Conjugated to D-Alpha-Tocopheryl Polyethylene Glycol 1000 Succinate (Tpgs): Conjugation Chemistry, Characterization, in Vitro and in Vivo Evaluation Biomaterials 2008, 29, 3856-3865
56. van Lummel, M.; van Blitterswijk, W. J.; Vink, S. R.; Veldman, R. J.; van der Valk, M. A.; Schipper, D.; Dicheva, B. M.; Eggermont, A. M. M.; ten Hagen, T. L. M.; Verheij, M.; Koning, G. A. Enriching Lipid Nanovesicles with Short-Chain Glucosylceramide Improves Doxorubicin Delivery and Efficacy in Solid Tumors FASEB J. 2011, 25, 280-289
57. Bhatia, S.; Frangioni, J. V.; Hoffman, R. M.; Iafrate, A. J.; Polyak, K. The Challenges Posed by Cancer Heterogeneity Nat. Biotechnol. 2012, 30, 604-610
58. Bock, C.; Lengauer, T. Managing Drug Resistance in Cancer: Lessons from HIV Therapy Nat. Rev. Cancer 2012, 12, 494-501
59. Turk, V.; Turk, B.; Turk, D. Lysosomal Cysteine Proteases: Facts and Opportunities EMBO J. 2001, 20, 4629-4633
60. Hurley, L. H. DNA and Its Associated Processes as Targets for Cancer Therapy Nat. Rev. Cancer 2002, 2, 188-200
61. Patel, E. N.; Wang, J.; Kim, K. J.; Borok, Z.; Crandall, E. D.; Shen, W. C. Conjugation with Cationic Cell-Penetrating Peptide Increases Pulmonary Absorption of Insulin Mol. Pharmaceutics 2009, 6, 492-503
62. van Hell, A. J.; Fretz, M. M.; Crommelin, D. J. A.; Hennink, W. E.; Mastrobattista, E. Peptide Nanocarriers for Intracellular Delivery of Photosensitizers J. Controlled Release 2010, 141, 347-353
63. Khalil, I. A.; Kogure, K.; Akita, H.; Harashima, H. Uptake Pathways and Subsequent Intracellular Trafficking in Nonviral Gene Delivery Pharmacol. Rev. 2006, 58, 32-45
64. Jedeszko, C.; Sloane, B. F. Cysteine Cathepsins in Human Cancer Biol. Chem. 2004, 385, 1017-1027
65. Maguire, T. M.; Shering, S. G.; Duggan, C. M.; McDermott, E. W.; O'Higgins, N. J.; Duffy, M. J. High Levels of Cathepsin B Predict Poor Outcome in Patients with Breast Cancer Int. J. Biol. Markers 1998, 13, 139-144
66. Gao, Y.; Shi, J.; Yuan, D.; Xu, B. Imaging Enzyme-Triggered Self-Assembly of Small Molecules inside Live Cells Nat. Commun. 2012, 3, 1033