Inhibition of cancer cell proliferation and breast tumor targeting of phlip-monomethyl auristatin e conjugates

Molecular Pharmaceutics

Volumn 12, Issue 4, 2015, Pages 1250-1258

  Burns, Kelly E ^a   Robinson, Matthew K ^b   Thévenin, Damien ^a  

^a LEHIGH UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

cytotoxicity; in vivo imaging; peptide; targeted drug delivery; tumor acidity

Indexed keywords

DOXORUBICIN; DRUG CARRIER; PEPTIDE DERIVATIVE; PH INSERTION PEPTIDE; UNCLASSIFIED DRUG; VEDOTIN; VINBLASTINE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; AMINOBENZOIC ACID DERIVATIVE; AURISTATIN; MEMBRANE PROTEIN; OLIGOPEPTIDE; PEPTIDE; PHLIP PROTEIN; PHOSPHATIDYLCHOLINE; TRYPTOPHAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CELL KILLING; CELL MEMBRANE; CELL PROLIFERATION; CELL VIABILITY; CONJUGATE; CONTROLLED STUDY; DEPOLYMERIZATION; DRUG CONJUGATION; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG SOLUBILITY; DRUG TARGETING; FEMALE; HELA CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC50; LIPID BILAYER; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; TRIPLE NEGATIVE BREAST CANCER; TUMOR XENOGRAFT; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; CIRCULAR DICHROISM; DRUG DELIVERY SYSTEM; MEDICINAL CHEMISTRY; METABOLISM; PROCEDURES; SPECTROFLUOROMETRY; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

AMINOBENZOATES; ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; CHEMISTRY, PHARMACEUTICAL; CIRCULAR DICHROISM; DRUG DELIVERY SYSTEMS; FEMALE; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MICE; NEOPLASM TRANSPLANTATION; OLIGOPEPTIDES; PEPTIDES; PHOSPHATIDYLCHOLINES; SPECTROMETRY, FLUORESCENCE; TRIPLE NEGATIVE BREAST NEOPLASMS; TRYPTOPHAN;

EID: 84926432293     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500779k     Document Type: Article

References (45)

1. Gerlinger, M.; Rowan, A. J.; Horswell, S.; Larkin, J.; Endesfelder, D.; Gronroos, E.; Martinez, P.; Matthews, N.; Stewart, A.; Tarpey, P.; Varela, I.; Phillimore, B.; Begum, S.; McDonald, N. Q.; Butler, A.; Jones, D.; Raine, K.; Latimer, C.; Santos, C. R.; Nohadani, M.; Eklund, A. C.; Spencer-Dene, B.; Clark, G.; Pickering, L.; Stamp, G.; Gore, M.; Szallasi, Z.; Downward, J.; Futreal, P. A.; Swanton, C. Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing N. Engl. J. Med. 2012, 366, 883-892
2. Manyak, M. J. Indium-111 Capromab Pendetide in the Management of Recurrent Prostate Cancer Expert Rev. Anticancer Ther. 2008, 8, 175-181
3. Warburg, O. On the Origin of Cancer Cells Science 1956, 123, 309-314
4. Kim, J.-W.; Dang, C. V. Cancers Molecular Sweet Tooth and the Warburg Effect Cancer Res. 2006, 66, 8927-8930
5. Chiche, J.; Brahimi-Horn, M. C.; Pouysségur, J. Tumour Hypoxia Induces a Metabolic Shift Causing Acidosis: A Common Feature in Cancer J. Cell. Mol. Med. 2010, 14, 771-794
6. Griffiths, J. R. Are Cancer Cells Acidic? Br. J. Cancer 1991, 64, 425-427
7. Vaupel, P.; Kallinowski, F.; Okunieff, P. Blood Flow, Oxygen and Nutrient Supply, and Metabolic Microenvironment of Human Tumors: A Review Cancer Res. 1989, 49, 6449-6465
8. Wike-Hooley, J. L.; Haveman, J.; Reinhold, H. S. The Relevance of Tumour pH to the Treatment of Malignant Disease Radiother. Oncol. 1984, 2, 343-366
9. Cairns, R.; Papandreou, I.; Denko, N. Overcoming Physiologic Barriers to Cancer Treatment by Molecularly Targeting the Tumor Microenvironment Mol. Cancer Res. 2006, 4, 61-70
10. Rofstad, E. K.; Mathiesen, B.; Kindem, K.; Galappathi, K. Acidic Extracellular pH Promotes Experimental Metastasis of Human Melanoma Cells in Athymic Nude Mice Cancer Res. 2006, 66, 6699-6707
11. Gillies, R. J.; Robey, I.; Gatenby, R. A. Causes and Consequences of Increased Glucose Metabolism of Cancers J. Nucl. Med. 2008, 49, 24S-42S
12. Estrella, V.; Chen, T.; Lloyd, M.; Wojtkowiak, J.; Cornnell, H. H.; Ibrahim-Hashim, A.; Bailey, K.; Balagurunathan, Y.; Rothberg, J. M.; Sloane, B. F.; Johnson, J.; Gatenby, R. A.; Gillies, R. J. Acidity Generated by the Tumor Microenvironment Drives Local Invasion Cancer Res. 2013, 73, 1524-1535
13. Hanahan, D.; Weinberg, R. A. Hallmarks of Cancer: The Next Generation Cell 2011, 144, 646-674
14. Reshetnyak, Y. K.; Yao, L.; Zheng, S.; Kuznetsov, S.; Engelman, D. M.; Andreev, O. A. Measuring Tumor Aggressiveness and Targeting Metastatic Lesions with Fluorescent pHLIP Mol. Imaging Biol. 2011, 13, 1146-1156
15. Andreev, O. A.; Engelman, D. M.; Reshetnyak, Y. K. Targeting Acidic Diseased Tissue: New Technology Based on Use of the pH (Low) Insertion Peptide (pHLIP) Chim Oggi 2009, 27, 34-37
16. Va¯vere, A. L.; Biddlecombe, G. B.; Spees, W. M.; Garbow, J. R.; Wijesinghe, D.; Andreev, O. A.; Engelman, D. M.; Reshetnyak, Y. K.; Lewis, J. S. A Novel Technology for the Imaging of Acidic Prostate Tumors by Positron Emission Tomography Cancer Res. 2009, 69, 4510-4516
17. Reshetnyak, Y. K.; Segala, M.; Andreev, O. A.; Engelman, D. M. A Monomeric Membrane Peptide That Lives in Three Worlds: In Solution, Attached to, and Inserted Across Lipid Bilayers Biophys. J. 2007, 93, 2363-2372
18. Reshetnyak, Y. K.; Andreev, O. A.; Segala, M.; Markin, V. S.; Engelman, D. M. Energetics of Peptide (pHLIP) Binding to and Folding Across a Lipid Bilayer Membrane Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 15340-15345
19. Thévenin, D.; An, M.; Engelman, D. M. pHLIP-Mediated Translocation of Membrane-Impermeable Molecules into Cells Chem. Biol. 2009, 16, 754-762
20. An, M.; Wijesinghe, D.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. pH-(Low)-Insertion-Peptide (pHLIP) Translocation of Membrane Impermeable Phalloidin Toxin Inhibits Cancer Cell Proliferation Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 20246-20250
21. Wijesinghe, D.; Engelman, D. M.; Andreev, O. A.; Reshetnyak, Y. K. Tuning a Polar Molecule for Selective Cytoplasmic Delivery by a pH (Low) Insertion Peptide Biochemistry 2011, 50, 10215-10222
22. Reshetnyak, Y. K.; Andreev, O. A.; Lehnert, U.; Engelman, D. M. Translocation of Molecules into Cells by pH-Dependent Insertion of a Transmembrane Helix Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6460-6465
23. Zoonens, M.; Reshetnyak, Y. K.; Engelman, D. M. Bilayer Interactions of pHLIP, a Peptide That Can Deliver Drugs and Target Tumors Biophys. J. 2008, 95, 225-235
24. Adochite, R.-C.; Moshnikova, A.; Carlin, S. D.; Guerrieri, R. A.; Andreev, O. A.; Lewis, J. S.; Reshetnyak, Y. K. Targeting Breast Tumors with pH (Low) Insertion Peptides Mol. Pharmaceutics 2014, 11, 2896-2905
25. Karabadzhak, A. G.; An, M.; Yao, L.; Langenbacher, R.; Moshnikova, A.; Adochite, R.-C.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. pHLIP-FIRE, a Cell Insertion-Triggered Fluorescent Probe for Imaging Tumors Demonstrates Targeted Cargo Delivery in Vivo ACS Chem. Biol. 2014, 9, 2545-2553
26. Sørlie, T.; Perou, C. M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M. B.; van de Rijn, M.; Jeffrey, S. S.; Thorsen, T.; Quist, H.; Matese, J. C.; Brown, P. O.; Botstein, D.; Lønning, P. E.; Børresen-Dale, A. L. Gene Expression Patterns of Breast Carcinomas Distinguish Tumor Subclasses with Clinical Implications Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10869-10874
27. Paik, S.; Shak, S.; Tang, G.; Kim, C.; Baker, J.; Cronin, M.; Baehner, F. L.; Walker, M. G.; Watson, D.; Park, T.; Hiller, W.; Fisher, E. R.; Wickerham, D. L.; Bryant, J.; Wolmark, N. A Multigene Assay To Predict Recurrence of Tamoxifen-Treated, Node-Negative Breast Cancer N. Engl. J. Med. 2004, 351, 2817-2826
28. Slamon, D. J.; Clark, G. M.; Wong, S. G.; Levin, W. J.; Ullrich, A.; McGuire, W. L. Human Breast Cancer: Correlation of Relapse and Survival with Amplification of the HER-2/Neu Oncogene Science 1987, 235, 177-182
29. Sorlie, T.; Tibshirani, R.; Parker, J.; Hastie, T.; Marron, J. S.; Nobel, A.; Deng, S.; Johnsen, H.; Pesich, R.; Geisler, S.; Demeter, J.; Perou, C. M.; Lønning, P. E.; Brown, P. O.; Børresen-Dale, A.-L.; Botstein, D. Repeated Observation of Breast Tumor Subtypes in Independent Gene Expression Data Sets Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 8418-8423
30. Carey, L. A.; Perou, C. M.; Livasy, C. A.; Dressler, L. G.; Cowan, D.; Conway, K.; Karaca, G.; Troester, M. A.; Tse, C. K.; Edmiston, S.; Deming, S. L.; Geradts, J.; Cheang, M. C. U.; Nielsen, T. O.; Moorman, P. G.; Earp, H. S.; Millikan, R. C. Race, Breast Cancer Subtypes, and Survival in the Carolina Breast Cancer Study JAMA 2006, 295, 2492-2502
31. Perou, C. M.; Sørlie, T.; Eisen, M. B.; van de Rijn, M.; Jeffrey, S. S.; Rees, C. A.; Pollack, J. R.; Ross, D. T.; Johnsen, H.; Akslen, L. A.; Fluge, O.; Pergamenschikov, A.; Williams, C.; Zhu, S. X.; Lønning, P. E.; Børresen-Dale, A. L.; Brown, P. O.; Botstein, D. Molecular Portraits of Human Breast Tumours Nature 2000, 406, 747-752
32. Dent, R.; Trudeau, M.; Pritchard, K. I.; Hanna, W. M.; Kahn, H. K.; Sawka, C. A.; Lickley, L. A.; Rawlinson, E.; Sun, P.; Narod, S. A. Triple-Negative Breast Cancer: Clinical Features and Patterns of Recurrence Clin. Cancer Res. 2007, 13, 4429-4434
33. Stewart, J. C. Colorimetric Determination of Phospholipids with Ammonium Ferrothiocyanate Anal. Biochem. 1980, 104, 10-14
34. Anticancer Agents from Natural Products, 1 st ed.; Cragg, G. M.; Kingston, D. G.; Newman, D. J., Eds.; Taylor & Francis: Boca Raton, FL, 2005.
35. Doronina, S. O.; Toki, B. E.; Torgov, M. Y.; Mendelsohn, B. A.; Cerveny, C. G.; Chace, D. F.; DeBlanc, R. L.; Gearing, R. P.; Bovee, T. D.; Siegall, C. B.; Francisco, J. A.; Wahl, A. F.; Meyer, D. L.; Senter, P. D. Development of Potent Monoclonal Antibody Auristatin Conjugates for Cancer Therapy Nat. Biotechnol. 2003, 21, 778-784
36. Doronina, S. O.; Mendelsohn, B. A.; Bovee, T. D.; Cerveny, C. G.; Alley, S. C.; Meyer, D. L.; Oflazoglu, E.; Toki, B. E.; Sanderson, R. J.; Zabinski, R. F.; Wahl, A. F.; Senter, P. D. Enhanced Activity of Monomethylauristatin F Through Monoclonal Antibody Delivery: Effects of Linker Technology on Efficacy and Toxicity Bioconjugate Chem. 2006, 17, 114-124
37. Minko, T.; Dharap, S. S.; Pakunlu, R. I.; Wang, Y. Molecular Targeting of Drug Delivery Systems to Cancer Curr. Drug Targets 2004, 5, 389-406
38. Lambert, J. M.; Chari, R. V. J. Ado-Trastuzumab Emtansine (T-DM1): An Antibody-Drug Conjugate (ADC) for HER2-Positive Breast Cancer J. Med. Chem. 2014, 57, 6949-6964
39. Musial-Siwek, M.; Karabadzhak, A.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. Tuning the Insertion Properties of pHLIP Biochim. Biophys. Acta 2010, 1798, 1041-1046
40. Moshnikova, A.; Moshnikova, V.; Andreev, O. A.; Reshetnyak, Y. K. Antiproliferative Effect of pHLIP-Amanitin Biochemistry 2013, 52, 1171-1178
41. Alley, S. C.; Okeley, N. M.; Senter, P. D. Antibody-Drug Conjugates: Targeted Drug Delivery for Cancer Curr. Opin. Chem. Biol. 2010, 14, 529-537
42. Alley, S. C.; Zhang, X.; Okeley, N. M.; Anderson, M.; Law, C.-L.; Senter, P. D.; Benjamin, D. R. The Pharmacologic Basis for Antibody-Auristatin Conjugate Activity J. Pharmacol. Exp. Ther. 2009, 330, 932-938
43. Miller, J.; Doss, M.; McQuillen, R.; Shaller, C. C.; Tolner, B.; Yu, J. Q.; Chester, K.; Robinson, M. K. Impact of Expression System on the Function of the C6.5 Diabody PET Radiotracer Tumour Biol. 2012, 33, 617-627
44. Robinson, M. K.; Shaller, C.; Garmestani, K.; Plascjak, P. S.; Hodge, K. M.; Yuan, Q.-A.; Marks, J. D.; Waldmann, T. A.; Brechbiel, M. W.; Adams, G. P. Effective Treatment of Established Human Breast Tumor Xenografts in Immunodeficient Mice with a Single Dose of the Alpha-Emitting Radioisotope Astatine-211 Conjugated to Anti-HER2/Neu Diabodies Clin. Cancer Res. 2008, 14, 875-882
45. Cao, Y.; Marks, J. W.; Liu, Z.; Cheung, L. H.; Hittelman, W. N.; Rosenblum, M. G. Design Optimization and Characterization of Her2/Neu-Targeted Immunotoxins: Comparative in Vitro and in Vivo Efficacy Studies Oncogene 2014, 33, 429-439