Combinatorial synthesis and screening of cancer cell-specific nanomedicines targeted via phage fusion proteins

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Gillespie, James W ^a   Gross, Amanda L ^a   Puzyrev, Anatoliy T ^a   Bedi, Deepa ^a   Petrenko, Valery A ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Breast cancer; Doxorubicin; Liposomal drug delivery; Pancreatic cancer; Phage display; Targeted nanomedicines

Indexed keywords

COAT PROTEIN; DOXORUBICIN; LIPOSOME;

ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; DNA SEQUENCE; DRUG TARGETING; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MTT ASSAY; NANOMEDICINE; PARTICLE SIZE; POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ZETA POTENTIAL;

EID: 84936997116     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00628     Document Type: Article

References (47)

1. Bedi, D., Gillespie, J. W., and Petrenko, V. A. (2014). Selection of pancreatic cancer cell-binding landscape phages and their use in development of anticancer nanomedicines. Protein Eng. Des. Sel. 27, 235-243. doi: 10.1093/protein/gzu020
2. Brigati, J. R., and Petrenko, V. A. (2005). Thermostability of landscape phage probes. Anal. Bioanal. Chem. 382, 1346-1350. doi: 10.1007/s00216-005-3289-y
3. Brigati, J. R., Samoylova, T. I., Jayanna, P. K., and Petrenko, V. A. (2008). "Phage display for generating peptide reagents," in Current Protocols in Protein Science, eds J. E. Coligan, B.M. Dunn, D. W. Speicher, and P. T.Wingfield (New Jersey, NJ: John Wiley & Sons, Inc), 1-27.
4. DeSantis, C. E., Lin, C. C., Mariotto, A. B., Siegel, R. L., Stein, K. D., Kramer, J. L., et al. (2014). Cancer treatment and survivorship statistics. CA Cancer J. Clin. 4, 252-271. doi: 10.3322/caac.21235
5. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). (2005). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365, 1687-1717. doi: 10.1016/S0140-6736(05)66544-0
6. Fagbohun, O. A., Bedi, D., Grabchenko, N. I., DeInnocentes, P. A., Bird, R. C., and Petrenko, V. A. (2012). Landscape phages and their fusion proteins targeted to breast cancer cells. Protein Eng. Des. Sel. 25, 271-283. doi: 10.1093/protein/gzs013
7. Fang, J., Nakamura, H., and Maeda, H. (2011). The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 63, 136-151. doi: 10.1016/j.addr.2010.04.009
8. Florent, J.-C., and Monneret, C. (2008). "Doxorubicin conjugates for selective delivery to tumors," in Topics in Current Chemistry, ed K. Krohn (Berlin: Springer), 99-140.
9. Gabizon, A., Shmeeda, H., and Barenholz, Y. (2003). Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies. Clin. Pharmacokinet. 42, 419-436. doi: 10.2165/00003088-200342050-00002
10. Gray, B. P., McGuire, M. J., and Brown, K. C. (2013). A liposomal drug platform overrides Peptide ligand targeting to a cancer biomarker, irrespective of ligand affinity or density. PLoS ONE 8:e72938. doi: 10.1371/journal.pone.0072938
11. Hrkach, J., Hoff Von, D., Mukkaram Ali, M., Andrianova, E., Auer, J., Campbell, T., et al. (2012). Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci. Transl. Med. 4, 128ra39. doi: 10.1126/scitranslmed.3003651
12. Jayanna, P. K., Bedi, D., DeInnocentes, P. A., Bird, R. C., and Petrenko, V. A. (2010a). Landscape phage ligands for PC3 prostate carcinoma cells. Protein Eng. Des. Sel. 23, 423-430. doi: 10.1093/protein/gzq011
13. Jayanna, P. K., Bedi, D., Gillespie, J. W., DeInnocentes, P. A., Wang, T., Torchilin, V. P., et al. (2010b). Landscape phage fusion protein-mediated targeting of nanomedicines enhances their prostate tumor cell association and cytotoxic efficiency. Nanomedicine 6, 538-546. doi: 10.1016/j.nano.2010.01.005
14. Jayanna, P. K., Torchilin, V. P., and Petrenko, V. A. (2009). Liposomes targeted by fusion phage proteins. Nanomedicine 5, 83-89. doi: 10.1016/j.nano.2008.07.006
15. Kung, V. T., and Redemann, C. T. (1986). Synthesis of carboxyacyl derivatives of phosphatidylethanolamine and use as an efficient method for conjugation of protein to liposomes. Biochim. Biophys. Acta 862, 435-439. doi: 10.1016/0005-2736(86)90247-6
16. Kuzmicheva, G. A., Jayanna, P. K., Sorokulova, I. B., and Petrenko, V. A. (2009). Diversity and censoring of landscape phage libraries. Protein Eng. Des. Sel. 22, 9-18. doi: 10.1093/protein/gzn060
17. Lee, D.-H., Rötger, C., Appeldoorn, C. C. M., Reijerkerk, A., Gladdines, W., Gaillard, P. J., et al. (2014). Glutathione PEGylated liposomal methylprednisolone (2B3-201) attenuates CNS inflammation and degeneration in murine myelin oligodendrocyte glycoprotein induced experimental autoimmune encephalomyelitis. J. Neuroimmunol. 274, 96-101. doi: 10.1016/j.jneuroim.2014.06.025
18. Li, W., Suez, I., and Szoka, F. C. (2007). Reconstitution of the M13 major coat protein and its transmembrane peptide segment on a DNA template. Biochemistry 46, 8579-8591. doi: 10.1021/bi700165m
19. Loughrey, H., Bally, M. B., and Cullis, P. R. (1987). A non-covalent method of attaching antibodies to liposomes. Biochim. Biophys. Acta 901, 157-160. doi: 10.1016/0005-2736(87)90267-7
20. Lukyanova, N. Y., Rusetskya, N. V., Tregubova, N. A., and Chekhun, V. F. (2009). Molecular profile and cell cycle in MCF-7 cells resistant to cisplatin and doxorubicin. Exp. Oncol. 31, 87-91.
21. Manning, M., Chrysogelos, S., and Griffith, J. (1981). Mechanism of coliphage M13 contraction: intermediate structures trapped at low temperatures. J. Virol. 40, 912-919. doi: 10.1016/0042-6822(70)90137-6
22. Marvin, D. A., Symmons, M. F., and Straus, S. K. (2014). Structure and assembly of filamentous bacteriophages. Prog. Biophys. Mol. Biol. 114, 80-122. doi: 10.1016/j.pbiomolbio.2014.02.003
23. Olofsson, L., Ankarloo, J., and Nicholls, I. A. (1998). Phage viability in organic media: insights into phage stability. J. Mol. Recogn. 11, 91-93.
24. Petrenko, V. A. (2008). Landscape phage as a molecular recognition interface for detection devices. Microelectronics J. 39, 202-207. doi: 10.1016/j.mejo.2006.11.007
25. Petrenko, V. A., and Jayanna, P. K. (2014). Phage protein-targeted cancer nanomedicines. FEBS Lett. 588, 341-349. doi: 10.1016/j.febslet.2013.11.011
26. Petrenko, V. A., and Smith, G. P. (2000). Phages from landscape libraries as substitute antibodies. Protein Eng. 13, 589-592. doi: 10.1093/protein/13.8.589
27. Petrenko, V. A., Smith, G. P., Gong, X., and Quinn, T. (1996). A library of organic landscapes on filamentous phage. Protein Eng. 9, 797-801. doi: 10.1093/protein/9.9.797
28. Pidgeon, C., and Hunt, C. A. (1981). Calculating number and surface area of liposomes in any suspension. J. Pharm. Sci. 70, 173-176. doi: 10.1002/jps.2600700215
29. Riihimäki, M., Thomsen, H., Brandt, A., Sundquist, J., and Hemminki, K. (2012). Death causes in breast cancer patients. Ann. Oncol. 23, 604-610. doi: 10.1093/annonc/mdr160
30. Romanov, V. I., Durand, D. B., and Petrenko, V. A. (2001). Phage display selection of peptides that affect prostate carcinoma cells attachment and invasion. Prostate 47, 239-251. doi: 10.1002/pros.1068
31. Samoylova, T. I., Petrenko, V. A., Morrison, N. E., Globa, L. P., Baker, H. J., and Cox, N. R. (2003). Phage probes for malignant glial cells. Mol. Cancer Ther. 2, 1129-1137.
32. Schwind, P., Kramer, H., Kremser, A., Ramsberger, U., and Rasched, I. (1992). Subtilisin removes the surface layer of the phage fd coat. Eur. J. Biochem. 210, 431-436. doi: 10.1111/j.1432-1033.1992.tb17438.x
33. Shroff, K., and Kokkoli, E. (2012). PEGylated liposomal doxorubicin targeted to α5β1-expressing MDA-MB-231 breast cancer cells. Langmuir 28, 4729-4736. doi: 10.1021/la204466g
34. Siegel, R. L., Miller, K. D., and Jemal, A. (2015). Cancer statistics. CA Cancer J. Clin. 65, 5-29. doi: 10.3322/caac.21254
35. Smith, G. P. (1993). Surface display and peptide libraries. Gene 128, 1-2. doi: 10.1016/0378-1119(93)90145-S
36. Smith, G. P., and Petrenko, V. A. (1997). Phage Display. Chem. Rev. 97, 391-410. doi: 10.1021/cr960065d
37. Smith, G. P., Petrenko, V. A., and Matthews, L. J. (1998). Cross-linked filamentous phage as an affinity matrix. J. Immunol. Methods 215, 151-161. doi: 10.1016/S0022-1759(98)00087-8
38. Soekarjo, M., Eisenhawer, M., Kuhn, A., and Vogel, H. (1996). Thermodynamics of the membrane insertion process of the M13 procoat protein, a lipid bilayer traversing protein containing a leader sequence. Biochemistry 35, 1232-1241. doi: 10.1021/bi951087h
39. Spidlen, J., Breuer, K., Rosenberg, C., Kotecha, N., and Brinkman, R. R. (2012). FlowRepository: a resource of annotated flow cytometry datasets associated with peer-reviewed publications. Cytometry A 81, 727-731. doi: 10.1002/cyto.a.22106
40. Spruijt, R. B., Wolfs, C. J., and Hemminga, M. A. (1989). Aggregation-related conformational change of the membrane-associated coat protein of bacteriophage M13. Biochemistry 28, 9158-9165. doi: 10.1021/bi00449a030
41. Wang, R., Xiao, R., Zeng, Z., Xu, L., and Wang, J. (2012). Application of poly(ethylene glycol)-distearoylphosphatidylethanolamine (PEG-DSPE) block copolymers and their derivatives as nanomaterials in drug delivery. Int. J. Nanomedicine 7, 4185-4198. doi: 10.2147/IJN.S34489
42. Wang, S., Konorev, E. A., Kotamraju, S., Joseph, J., Kalivendi, S., and Kalyanaraman, B. (2004). Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. intermediacy of H(2)O(2)- and p53-dependent pathways. J. Biol. Chem. 279, 25535-43. doi: 10.1074/jbc.M400944200
43. Wang, T., D'Souza, G. G. M., Bedi, D., Fagbohun, O. A., Potturi, L. P., Papahadjopoulos-Sternberg, B., et al. (2010a). Enhanced binding and killing of target tumor cells by drug-loaded liposomes modified with tumor-specific phage fusion coat protein. Nanomedicine 5, 563-574. doi: 10.2217/nnm.10.30
44. Wang, T., Hartner, W. C., Gillespie, J. W., Praveen, K. P., Yang, S., Mei, L. A., et al. (2014). Enhanced tumor delivery and antitumor activity in vivo of liposomal doxorubicin modified with MCF-7-specific phage fusion protein. Nanomedicine 10, 421-430. doi: 10.1016/j.nano.2013.08.009
45. Wang, T., Kulkarni, N., Bedi, D., D'Souza, G. G. M., Papahadjopoulos-Sternberg, B., Petrenko, V. A., et al. (2011). In vitro optimization of liposomal nanocarriers prepared from breast tumor cell specific phage fusion protein. J. Drug Target. 19, 597-605. doi: 10.3109/1061186X.2010.550920
46. Wang, T., Yang, S., Petrenko, V. A., and Torchilin, V. P. (2010b). Cytoplasmic delivery of liposomes into MCF-7 breast cancer cells mediated by cell-specific phage fusion coat protein. Mol. Pharm. 7, 1149-1158. doi: 10.1021/mp1000229
47. Zacher, A. N., Stock, C. A., Golden, J. W., and Smith, G. P. (1980). A new filamentous phage cloning vector: fd-tet. Gene 9, 127-140. doi: 10.1016/0378-1119(80)90171-7