Targeting heat shock proteins on cancer cells: Selection, characterization, and cell-penetrating properties of a peptidic GRP78 ligand

Biochemistry

Volumn 45, Issue 31, 2006, Pages 9434-9444

  Kim, Youngsoo ^a   Lillo, Antonietta M ^a   Steiniger, Sebastian C J ^a   Liu, Ying ^a   Ballatore, Carlo ^b   Anichini, Andrea ^c   Mortarini, Roberta ^c   Kaufmann, Gunnar F ^a   Zhou, Bin ^a   Felding Habermann, Brunhilde ^a   Janda, Kim D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Acidophil LLC   (United States)

^c NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CYTOLOGY; ELECTROSTATICS; MONOCLONAL ANTIBODIES; TOXICITY; TUMORS;

CANCER CELLS; HEAT SHOCK PROTEINS; HUMAN MELANOMA CELL LINE ME6652/4; PEPTIDIC GRP78 LIGAND;

PROTEINS;

CELL RECEPTOR; CYCLOPEPTIDE; CYSTEINYLTHREONYLVALYLALANYLLEUCYLPROLYLGLYCYLGLYCYLTYROSYLVALYLARGINYLVALY LCYSTEINE; GLUCOSE REGULATED PROTEIN; HEAT SHOCK PROTEIN; MONOCLONAL ANTIBODY; PACLITAXEL; QUANTUM DOT; TUMOR MARKER; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CULTURE MEDIUM; DRUG CONJUGATION; DRUG CYTOTOXICITY; DRUG SELECTIVITY; ENDOPLASMIC RETICULUM; EVALUATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INTERNALIZATION; MELANOMA; MELANOMA CELL; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; WHOLE CELL;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; HEAT-SHOCK PROTEINS; HUMANS; LIGANDS; MELANOMA; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PACLITAXEL; PEPTIDE LIBRARY; PEPTIDES, CYCLIC; PROTEIN TRANSPORT;

EID: 33747145206     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060264j     Document Type: Article

References (54)

1. Foerg, C., Ziegler, U., Fernandez-Carneado, J., Giralt, E., Rennert, R., Beck-Sickinger, A. G., and Merkle, H. P. (2005) Decoding the entry of two novel cell-penetrating peptides in HeLa cells: lipid raft-mediated endocytosis and endosomal escape, Biochemistry 44, 72-81.
2. Ziegler, A., Nervi, P., Durrenberger, M., and Seelig, J. (2005) The cationic cell-penetrating peptide CPP(TAT) derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: optical, biophysical, and metabolic evidence, Biochemistry 44, 138-148.
3. Richard, J. P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M. J., Chernomordik, L. V., and Lebleu, B. (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake, J. Biol. Chem. 278, 585-590.
4. Ruoslahti, E., Duza, T., and Zhang, L. (2005) Vascular homing peptides with cell-penetrating properties, Curr. Pharm. Des. 11, 3655-3660.
5. Barry, M. A., Dower, W. J., and Johnston, S. A. (1996) Toward cell-targeting gene therapy vectors: selection of cell-binding peptides from random peptide-presenting phage libraries, Nat. Med. 2, 299-305.
6. Landon, L. A., and Deutscher, S. L. (2003) Combinatorial discovery of tumor targeting peptides using phage display, J. Cell. Biochem. 90, 509-517.
7. Joliot, A., and Prochiantz, A. (2004) Transduction peptides: from technology to physiology, Nat. Cell Biol. 6, 189-196.
8. Fennelly, D., and Schneider, J. (1995) Role of chemotherapy dose intensification in the treatment of advanced ovarian cancer, Oncology (Willision Park) 9, 911-921; discussion 922, 924, 926.
9. Alexandrescu, D. T., Dutcher, J. P., and Wiernik, P. H. (2005) Metastatic melanoma: is biochemotherapy the future?, Med. Oncol. 22, 101-111.
10. Tsuchiya, Y., Sawada, S., Tsukada, K., and Saiki, I. (2002) A new pseudo-peptide of Arg-Gly-Asp (RGD) inhibits intrahepatic metastasis of orthotopically implanted murine hepatocellular carcinoma, Int. J. Oncol. 20, 319-324.
11. Kato, M., and Mrksich, M. (2004) Using model substrates to study the dependence of focal adhesion formation on the affinity of integrin-ligand complexes, Biochemistry 43, 2699-2707.
12. Aumailley, M., Gurrath, M., Muller, G., Calvete, J., Timpl, R., and Kessler, H. (1991) Arg-Gly-Asp constrained within cyclic pentapeptides. Strong and selective inhibitors of cell adhesion to vitronectin and laminin fragment P1, FEBS Lett. 291, 50-54.
13. Suzuki, N., Nakatsuka, H., Mochizuki, M., Nishi, N., Kadoya, Y., Utani, A., Oishi, S., Fujii, N., Kleinman, H. K., and Nomizu, M. (2003) Biological activities of homologous loop regions in the laminin alpha chain G domains, J. Biol. Chem. 278, 45697-45705.
14. Gurrath, M., Muller, G., Kessler, H., Aumailley, M., and Timpl, R. (1992) Conformation/activity studies of rationally designed potent anti-adhesive RGD peptides, Eur. J. Biochem. 210, 911-921.
15. Macario, A. J., and Conway de Macario, E. (2005) Sick chaperones, cellular stress, and disease, N. Engl. J. Med. 353, 1489-1501.
16. Delpino, A., Piselli, P., Vismara, D., Vendetti, S., and Colizzi, V. (1998) Cell surface localization of the 78 kD glucose regulated protein (GRP 78) induced by thapsigargin, Mol. Membr. Biol. 75, 21-26.
17. 2+ depletion. A comparative analysis with A23187 and the endoplasmic reticulum Ca(2+)-ATPase inhibitor thapsigargin, J. Biol. Chem. 268, 12003-12009.
18. Lee, A. S. (1992) Mammalian stress response: induction of the glucose-regulated protein family, Curr. Opin. Cell Biol. 4, 267-273.
19. Fernandez, P. M., Tabbara, S. O., Jacobs, L. K., Manning, F. C., Tsangaris, T. N., Schwartz, A. M., Kennedy, K. A., and Patierno, S. R. (2000) Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions, Breast Cancer Res. Treat. 59, 15-26.
20. Song, M. S., Park, Y. K., Lee, J. H., and Park, K. (2001) Induction of glucose-regulated protein 78 by chronic hypoxia in human gastric tumor cells through a protein kinase C-epsilon/ERK/AP-1 signaling cascade, Cancer Res. 61, 8322-8330.
21. Reddy, R. K., Mao, C., Baumeister, P., Austin, R. C., Kaufman, R. J., and Lee, A. S. (2003) Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation, J. Biol. Chem. 278, 20915-20924.
22. Chatterjee, S., Cheng, M. F., Berger, R. B., Berger, S. J., and Berger, N. A. (1995) Effect of inhibitors of poly(ADP-ribose) polymerase on the induction of GRP78 and subsequent development of resistance to etoposide, Cancer Res. 55, 868-873.
23. Fujihara, S. M., and Nadler, S. G. (1999) Intranuclear targeted delivery of functional NF-kappaB by 70 kDa heat shock protein, EMBO J. 18, 411-419.
24. Kim, Y., Lillo, A., Moss, J. A., and Janda, K. D. (2005) A contiguous stretch of methionine residues mediates the energy-dependent internalization mechanism of a cell-penetrating peptide, Mol. Pharm. 2, 528-535.
25. Moss, J. A., Lillo, A., Kim, Y. S., Gao, C., Ditzel, H., and Janda, K. D. (2005) A dimerization "switch" in the internalization mechanism of a cell-penetrating peptide, J. Am. Chem. Soc. 127, 538-539.
26. Anichini, A., Mortarini, R., Fossati, G., and Parmiani, G. (1986) Phenotypic profile of clones from early cultures of human metastatic melanomas and its modulation by recombinant Interferon gamma, Int. J. Cancer 38, 505-511.
27. Anichini, A., Mortarini, R., Supino, R., and Parmiani, G. (1990) Human melanoma cells with high susceptibility to cell-mediated lysis can be identified on the basis of ICAM-1 phenotype, VLA profile and invasive ability, Int. J. Cancer 46, 508-515.
28. Gao, C., Mao, S., Ditzel, H. J., Farnaes, L., Wirsching, P., Lerner, R. A., and Janda, K. D. (2002) A cell-penetrating peptide from a novel pVII-pIX phage-displayed random peptide library, Bioorg. Med. Chem. 10, 4057-4065.
29. Gao, C., Brummer, O., Mao, S., and Janda, K. D. (1999) Selection of human metalloantibodies from a combinatorial phage single-chain antibody library, J. Am. Chem. Soc. 121, 6517-6518.
30. Chan, W. C., and White, P. D. (2000) Fmoc Solid-Phase Peptide Synthesis, Oxford University Press, Oxford.
31. Zanon, M., Piris, A., Bersani, I., Vegetti, C., Molla, A., Scarito, A., and Anichini, A. (2004) Apoptosis protease activator protein-1 expression is dispensable for response of human melanoma cells to distinct proapoptotic agents, Cancer Res. 64, 7386-7394.
32. Finney, D. A., and Sklar, L. A. (1983) Ligand/receptor internalization: a kinetic, flow cytometric analysis of the internalization of N-formyl peptides by human neutrophils, Cytometry 4, 54-60.
33. Sklar, L. A. (1987) Real-time spectroscopic analysis of ligand-receptor dynamics, Annu. Rev. Biophys. Biophys. Chem. 16, 479-506.
34. Kwon, S., and Carson, J. H. (1998) Fluorescence quenching and dequenching analysis of RNA interactions in vitro and in vivo, Anal. Biochem. 264, 133-140.
35. Fotin-Mleczek, M., Fischer, R., and Brock, R. (2005) Endocytosis and cationic cell-penetrating peptides-a merger of concepts and methods, Curr. Pharm. Des. 11, 3613-3628.
36. Letoha, T., Gaal, S., Somlai, C., Czajlik, A., Perczel, A., and Penke, B. (2003) Membrane translocation of penetratin and its derivatives in different cell lines, J. Mol. Recognit. 16, 272-279.
37. Tyagi, M., Rusnati, M., Presta, M., and Giacca, M. (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans, J. Biol. Chem. 276, 3254-3261.
38. Goncalves, E., Kitas, E., and Seelig, J. (2005) Binding of oligoarginine to membrane lipids and heparan sulfate: structural and thermodynamic characterization of a cell-penetrating peptide, Biochemistry 44, 2692-2702.
39. Lensink, M. F., Christiaens, B., Vandekerckhove, J., Prochiantz, A., and Rosseneu, M. (2005) Penetratin-membrane association: W48/R52/W56 shield the peptide from the aqueous phase, Biophys. J. 88, 939-952.
40. Ziegler, A., Blatter, X. L., Seelig, A., and Seelig, J. (2003) Protein transduction domains of HIV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic analysis, Biochemistry 42, 9185-9194.
41. Ohvo, H., and Slotte, J. P. (1996) Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate, Biochemistry 35, 8018-8024.
42. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes, Nature 387, 569-572.
43. Brown, D. A., and London, E. (1998) Functions of lipid rafts in biological membranes, Annu. Rev. Cell Dev. Biol. 14, 111-136.
44. Pike, L. J. (2003) Lipid rafts: bringing order to chaos, J. Lipid Res. 44, 655-667.
45. Fittipaldi, A., Ferrari, A., Zoppe, M., Arcangeli, C., Pellegrini, V., Beltram, F., and Giacca, M. (2003) Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins, J. Biol. Chem. 278, 34141-34149.
46. Sandgren, S., Wittrup, A., Cheng, F., Jonsson, M., Eklund, E., Busch, S., and Belting, M. (2004) The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis, J. Biol. Chem. 279, 17951-17956.
47. Kauer, J. C., Erickson-Viitanen, S., Wolfe, H. R., Jr., and DeGrado, W. F. (1986) p-Benzoyl-L-phenylalanine, a new photoreactive amino acid. Photolabeling of calmodulin with a synthetic calmodulin-binding peptide, J. Biol. Chem. 261, 10695-10700.
48. Arap, M. A., Lahdenranta, J., Mintz, P. J., Hajitou, A., Sarkis, A. S., Arap, W., and Pasqualini, R. (2004) Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands, Cancer Cell 6, 275-284.
49. Blond-Elguindi, S., Cwirla, S. E., Dower, W. J., Lipshutz, R. J., Sprang, S. R., Sambrook, J. F., and Gething, M.-J. H. (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP, Cell 75, 717.
50. El-Andaloussi, S., Holm, T., and Langel, U. (2005) Cell-penetrating peptides: mechanisms and applications, Curr. Pharm. Des. 11, 3597-3611.
51. Misra, U. K., Gonzalez-Gronow, M., Gawdi, G., Hart, J. P., Johnson, C. E., and Pizzo, S. V. (2002) The role of Grp 78 in alpha 2-macroglobulin-induced signal transduction. Evidence from RNA interference that the low-density lipoprotein receptor-related protein is associated with, but not necessary for, GRP 78-mediated signal transduction, J. Biol. Chem. 277, 42082-42087.
52. Misra, U. K., Deedwania, R., and Pizzo, S. V. (2005) Binding of activated alpha2-macroglobulin to its cell surface receptor GRP78 in 1-LN prostate cancer cells regulates PAK-2-dependent activation of LIMK, J. Biol. Chem. 280, 26278-26286.
53. Mintz, P. J., Kim, J., Do, K. A., Wang, X., Zinner, R. G., Cristofanilli, M., Arap, M. A., Hong, W. K., Troncoso, P., Logothetis, C. J., Pasqualini, R., and Arap, W. (2003) Fingerprinting the circulating repertoire of antibodies from cancer patients, Nat. Biotechnol. 21, 57-63.
54. Denmeade, S. R., and Isaacs, J. T. (2005) The SERCA pump as a therapeutic target-Making a "smart bomb" for prostate cancer, Cancer Biol. Ther. 4, 14-22.