Intracellular Delivery of Functional Proteins and Native Drugs by Cell-Penetrating Poly(disulfide)s

Journal of the American Chemical Society

Volumn 137, Issue 37, 2015, Pages 12153-12160

  Fu, Jiaqi ^a   Yu, Changmin ^a   Li, Lin ^a,b   Yao, Shao Q ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NANJING TECH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; CYTOLOGY; MAMMALS; MOLECULAR BIOLOGY; MOLECULES; PROTEINS;

BIOACTIVE COMPOUNDS; BIOLOGICAL STUDIES; DELIVERY PROTOCOLS; FUNCTIONAL PROTEINS; GENETIC MANIPULATIONS; INTRACELLULAR DELIVERY; SMALL-MOLECULE DRUGS; TRANSDUCTION METHOD;

CELLS;

CASPASE 3; CELL PENETRATING PEPTIDE; CELL PENETRATING POLYDISULFIDE; NANOCARRIER; UNCLASSIFIED DRUG; BIOMIMETIC MATERIAL; DISULFIDE; DRUG CARRIER; PROTEIN;

ARTICLE; CONJUGATE; CYTOTOXICITY; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MAMMAL CELL; PROTEIN BINDING; PROTEIN TRANSPORT; SYNTHESIS; CHEMISTRY; DRUG DESIGN; INTRACELLULAR SPACE; METABOLISM;

BIOMIMETIC MATERIALS; CELL-PENETRATING PEPTIDES; DISULFIDES; DRUG CARRIERS; DRUG DESIGN; HELA CELLS; HUMANS; INTRACELLULAR SPACE; PROTEIN TRANSPORT; PROTEINS;

EID: 84942455856     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.5b08130     Document Type: Article

References (59)

1. Torres, A. G.; Gait, M. J. Trends Biotechnol. 2012, 30, 185-190 10.1016/j.tibtech.2011.12.002
2. Fu, A.; Tang, R.; Hardie, J.; Farkas, M. E.; Rotello, V. M. Bioconjugate Chem. 2014, 25, 1602-1608 10.1021/bc500320j
3. van den Berg, A.; Dowdy, S. F. Curr. Opin. Biotechnol. 2011, 22, 888-893 10.1016/j.copbio.2011.03.008
4. Lindsay, M. A. Curr. Opin. Pharmacol. 2002, 2, 587-594 10.1016/S1471-4892(02)00199-6
5. Mintzer, M. A.; Simanek, E. E. Chem. Rev. 2009, 109, 259-302 10.1021/cr800409e
6. Nguyen, J.; Szoka, F. C. Acc. Chem. Res. 2012, 45, 1153-1162 10.1021/ar3000162
7. Kostarelos, K.; Miller, A. D. Chem. Soc. Rev. 2005, 34, 970-994 10.1039/b307062j
8. Sun, T.; Zhang, Y. S.; Pang, B.; Hyun, D. C.; Yang, M.; Xia, Y. Angew. Chem., Int. Ed. 2014, 53, 12320-12364 10.1002/anie.201403036
9. Williams, H. D.; Trevaskis, N. L.; Charman, S. A.; Shanker, R. M.; Charman, W. N.; Pouton, C. W.; Porter, C. J. Pharmacol. Rev. 2013, 65, 315-499 10.1124/pr.112.005660
10. Jorgensen, W. L.; Duffy, E. M. Adv. Drug Delivery Rev. 2002, 54, 355-366 10.1016/S0169-409X(02)00008-X
11. Heitz, F.; Morris, M. C.; Divita, G. Br. J. Pharmacol. 2009, 157, 195-206 10.1111/j.1476-5381.2009.00057.x
12. Montrose, K.; Yang, Y.; Sun, X.; Wiles, S.; Krissansen, G. W. Sci. Rep. 2013, 3, 1661-1667 10.1038/srep01661
13. Nischan, N.; Herce, H. D.; Natale, F.; Bohlke, N.; Budisa, N.; Cardoso, M. C.; Hackenberger, C. P. R. Angew. Chem., Int. Ed. 2015, 54, 1950-1953 10.1002/anie.201410006
14. Zuris, J. A.; Thompson, D. B.; Shu, Y.; Guilinger, J. P.; Bessen, J. L.; Hu, J. H.; Maeder, M. L.; Joung, J. K.; Chen, Z. Y.; Liu, D. R. Nat. Biotechnol. 2015, 33, 73-80 10.1038/nbt.3081
15. Cronican, J. J.; Thompson, D. B.; Beier, K. T.; McNaughton, B. R.; Cepko, C. L.; Liu, D. R. ACS Chem. Biol. 2010, 5, 747-752 10.1021/cb1001153
16. Allen, T. M.; Cullis, P. R. Adv. Drug Delivery Rev. 2013, 65, 36-48 10.1016/j.addr.2012.09.037
17. Sarker, S. R.; Hokama, R.; Takeoka, S. Mol. Pharmaceutics 2014, 11, 164-174 10.1021/mp400363z
18. Han, D. H.; Na, H. K.; Choi, W. H.; Lee, J. H.; Kim, Y. K.; Won, C.; Lee, S. H.; Kim, K. P.; Kuret, J.; Min, D. H.; Lee, M. J. Nat. Commun. 2014, 5, 5633 10.1038/ncomms6633
19. Tunnemann, G.; Martin, R. M.; Haupt, S.; Patsch, C.; Edenhofer, F.; Cardoso, M. C. FASEB J. 2006, 20, 1775-1784 10.1096/fj.05-5523com
20. Richard, J. P.; Melikov, K.; Vives, E.; Ramos, C.; Verbeure, B.; Gait, M. J.; Chernomordik, L. V.; Lebleu, B. J. Biol. Chem. 2003, 278, 585-590 10.1074/jbc.M209548200
21. Michaudel, Q.; Journot, G.; Regueiro-Ren, A.; Goswami, A.; Guo, Z.; Tully, T. P.; Zou, L.; Ramabhadran, R. O.; Houk, K. N.; Baran, P. S. Angew. Chem., Int. Ed. 2014, 53, 12091-12096 10.1002/anie.201407016
22. Nicolas, J.; Mura, S.; Brambilla, D.; Mackiewicz, N.; Couvreur, P. Chem. Soc. Rev. 2013, 42, 1147-1235 10.1039/C2CS35265F
23. Li, Z.; Barnes, J. C.; Bosoy, A.; Stoddart, J. F.; Zink, J. I. Chem. Soc. Rev. 2012, 41, 2590-2605 10.1039/c1cs15246g
24. Coll, C.; Bernardos, A.; Martinez-Manez, R.; Sancenon, F. Acc. Chem. Res. 2013, 46, 339-349 10.1021/ar3001469
25. Zhang, P.; Cheng, F.; Zhou, R.; Cao, J.; Li, J.; Burda, C.; Min, Q.; Zhu, J. Angew. Chem., Int. Ed. 2014, 53, 2371-2375 10.1002/anie.201308920
26. Slowing, I. I.; Trewyn, B. G.; Lin, V. S. Y. J. Am. Chem. Soc. 2006, 128, 14792-14793 10.1021/ja0645943
27. Yu, C.; Qian, L.; Uttamchandani, M.; Li, L.; Yao, S. Q. Angew. Chem., Int. Ed. 2015, 54, 10574-10578 10.1002/anie.201504913
28. Bang, E.-K.; Gasparini, G.; Molinard, G.; Roux, A.; Sakai, N.; Matile, S. J. J. Am. Chem. Soc. 2013, 135, 2088-2091 10.1021/ja311961k
29. Gasparini, G.; Bang, E.-K.; Molinard, G.; Tulumello, D. V.; Ward, S.; Kelley, S. O.; Roux, A.; Sakai, N.; Matile, S. J. Am. Chem. Soc. 2014, 136, 6069-6074 10.1021/ja501581b
30. Chuard, N.; Gasparini, G.; Roux, A.; Sakai, N.; Matile, S. Org. Biomol. Chem. 2015, 13, 64-67 10.1039/C4OB02060J
31. Gasparini, G.; Sargsyan, G.; Bang, E. K.; Sakai, N.; Matile, S. Angew. Chem., Int. Ed. 2015, 54, 7328-7331 10.1002/anie.201502358
32. Son, S.; Namgung, R.; Kim, J.; Singha, K.; Kim, W. J. Acc. Chem. Res. 2012, 45, 1100-1112 10.1021/ar200248u
33. Gasparini, G.; Bang, E.-K.; Montenegro, J.; Matile, S. Chem. Commun. 2015, 51, 10389-10402 10.1039/C5CC03472H
34. Marschall, A. L.; Frenzel, A.; Schirrmann, T.; Schüngel, M.; Dübel, S. mAbs 2011, 3, 3-16 10.4161/mabs.3.1.14110
35. Khalili, H.; Godwin, A.; Choi, J. W.; Lever, R.; Brocchini, S. Bioconjugate Chem. 2012, 23, 2262-2277 10.1021/bc300372r
36. Polytherics Home Page. http://www.polytherics.com (accessed Sept 2, 2015).
37. Click Chemistry Tools Home Page. https://www.clickchemistrytools.com (accessed Sept 2, 2015).
38. Devaraj, N. K.; Weissleder, R. Acc. Chem. Res. 2011, 44, 816-827 10.1021/ar200037t
39. Li, Z.; Wang, D.; Li, L.; Pan, S.; Na, Z.; Tan, C. Y. J.; Yao, S. Q. J. Am. Chem. Soc. 2014, 136, 9990-9998 10.1021/ja502780z
40. Zhang, C.; Tan, C. Y. J.; Ge, J.; Na, Z.; Chen, G. Y. J.; Uttamchandani, M.; Sun, H.; Yao, S. Q. Angew. Chem., Int. Ed. 2013, 52, 14060-14064 10.1002/anie.201307803
41. Katz, B. A. J. Mol. Biol. 1997, 274, 776-800 10.1006/jmbi.1997.1444
42. Fuchs, S. M.; Raines, R. T. ACS Chem. Biol. 2007, 2, 167-170 10.1021/cb600429k
43. McNaughton, B. R.; Cronican, J. J.; Thompson, D. B.; Liu, D. R. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 6111-6116 10.1073/pnas.0807883106
44. ThermoFisher Home Page. http://www.thermofisher.com/order/catalog/product/89850 (accessed Sept 3, 2015).
45. Zelphati, O.; Wang, Y.; Kitada, S.; Reed, J. C.; Felgner, P. L.; Corbeil, J. J. Biol. Chem. 2001, 276, 35103-35110 10.1074/jbc.M104920200
46. Denault, J. B.; Salvesen, G. S. Chem. Rev. 2002, 102, 4489-4499 10.1021/cr010183n
47. Yang, X. H.; Sladek, T. L.; Liu, X.; Butler, B. R.; Froelich, C. J.; Thor, A. D. Cancer Res. 2001, 61, 348-354
48. Ng, S. L.; Yang, P.-Y.; Chen, K. Y.-T.; Srinivasan, R.; Yao, S. Q. Org. Biomol. Chem. 2008, 6, 844-847 10.1039/b718304f
49. Li, J.; Yao, S. Q. Org. Lett. 2009, 11, 405-408 10.1021/ol802700w
50. Hu, M.; Li, L.; Wu, H.; Su, Y.; Yang, P.-Y.; Uttamchandani, M.; Xu, Q.-H.; Yao, S. Q. J. Am. Chem. Soc. 2011, 133, 12009-12020 10.1021/ja200808y
51. Na, Z.; Peng, B.; Ng, S.; Pan, S.; Lee, J.-S.; Shen, H. M.; Yao, S. Q. Angew. Chem., Int. Ed. 2015, 54, 2515-2519 10.1002/anie.201410678
52. Chaitanya, G. V.; Alexander, J. S.; Babu, P. P. Cell Commun. Signaling 2010, 8, 31 10.1186/1478-811X-8-31
53. Weiner, L. M.; Surana, R.; Wang, S. Nat. Rev. Immunol. 2010, 10, 317-327 10.1038/nri2744
54. Lyon, R. P.; Meyer, D. L.; Setter, J. R.; Senter, P. D. Methods Enzymol. 2012, 502, 123-138 10.1016/B978-0-12-416039-2.00006-9
55. Shaunak, S.; Godwin, A.; Choi, J.-W.; Balan, S.; Pedone, E.; Vijayarangam, D.; Heidelberger, S.; Teo, I.; Zloh, M.; Brocchini, S. Nat. Chem. Biol. 2006, 2, 312-313 10.1038/nchembio786
56. Badescu, G.; Bryant, P.; Bird, M.; Henseleit, K.; Swierkosz, J.; Parekh, V.; Tommasi, R.; Pawlisz, E.; Jurlewicz, K.; Farys, M.; Camper, N.; Sheng, X. B.; Fisher, M.; Grygorash, R.; Kyle, A.; Abhilash, A.; Frigerio, M.; Edwards, J.; Godwin, A. Bioconjugate Chem. 2014, 25, 1124-1136 10.1021/bc500148x
57. Zhao, Y. L.; Li, Z.; Kabehie, S.; Botros, Y. Y.; Stoddart, J. F.; Zink, J. I. J. Am. Chem. Soc. 2010, 132, 13016-13025 10.1021/ja105371u
58. Tacar, O.; Sriamornsak, P.; Dass, C. R. J. Pharm. Pharmacol. 2013, 65, 157-170 10.1111/j.2042-7158.2012.01567.x
59. Norton, J. T.; Titus, S. A.; Dexter, D.; Austin, C. P.; Zheng, W.; Huang, S. J. Biomol. Screening 2009, 14, 1045-1053 10.1177/1087057109343120