A heparan sulfate-binding cell penetrating peptide for tumor targeting and migration inhibition

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Chen, Chien Jung ^a   Tsai, Kang Chiao ^a   Kuo, Ping Hsueh ^a   Chang, Pei Lin ^a   Wang, Wen Ching ^a   Chuang, Yung Jen ^a   Chang, Margaret Dah Tsyr ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PENETRATING PEPTIDE; HEPARAN SULFATE; MAGNETIC NANOPARTICLE; RIBONUCLEASE; EOSINOPHIL CATIONIC PROTEIN; RNASE3 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MIGRATION; CONTROLLED STUDY; INTERNALIZATION; MIGRATION INHIBITION; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; CELL MEMBRANE; CELL MOTION; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; MOUSE; NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CELL-PENETRATING PEPTIDES; EOSINOPHIL CATIONIC PROTEIN; HEPARITIN SULFATE; HUMANS; MICE; NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84929631281     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/237969     Document Type: Article

References (75)

1. K. R. Kampen, "The mechanisms that regulate the localization and overexpression of VEGF receptor-2 are promising therapeutic targets in cancer biology, " Anti-Cancer Drugs, vol. 23, no. 4, pp. 347-354, 2012.
2. R. Sasisekharan, Z. Shriver, G. Venkataraman, and U. Narayanasami, "Roles of heparan-sulphate glycosaminoglycans in cancer, " Nature Reviews Cancer, vol. 2, no. 7, pp. 521-528, 2002.
3. M. Adachi, T. Taki, M. Higashiyama, N. Kohno, H. Inufusa, and M. Miyake, "Significance of integrin 5 gene expression as a prognostic factor in node-negative non-small cell lung cancer, " Clinical Cancer Research, vol. 6, no. 1, pp. 96-101, 2000.
4. E. H. Knelson, J. C. Nee, and G. C. Blobe, "Heparan sulfate signaling in cancer, " Trends in Biochemical Sciences, vol. 39, no. 6, pp. 277-288, 2014.
5. A. Ori, M. C. Wilkinson, and D. G. Fernig, "A systems biology approach for the investigation of the heparin/heparan sulfate interactome, " The Journal of Biological Chemistry, vol. 286, no. 22, pp. 19892-19904, 2011.
6. N. Sasaki, N. Higashi, T. Taka, M. Nakajima, and T. Irimura, "Cell surface localization of heparanase on macrophages regulates degradation of extracellular matrix heparan sulfate, " The Journal of Immunology, vol. 172, no. 6, pp. 3830-3835, 2004.
7. J. Regberg, A. Srimanee, and U. Langel, "Applications of cellpenetrating peptides for tumor targeting and future cancer therapies, " Pharmaceuticals, vol. 5, no. 9, pp. 991-1007, 2012.
8. V. Kersemans, K. Kersemans, and B. Cornelissen, "Cell penetrating peptides for in vivo molecular imaging applications, " Current Pharmaceutical Design, vol. 14, no. 24, pp. 2415-2427, 2008.
9. S. Console, C. Marty, C. Garcá-Echeverrá, R. Schwendener, and K. Ballmer-Hofer, "Antennapedia andHIVtransactivator of transcription (TAT) "protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans, " The Journal of Biological Chemistry, vol. 278, no. 37, pp. 35109-35114, 2003.
10. S. Deshayes, T. Plénat, P. Charnet, G. Divita, G. Molle, and F. Heitz, "Formation of transmembrane ionic channels of primary amphipathic cell-penetrating peptides. Consequences on the mechanism of cell penetration, " Biochimica et Biophysica Acta, vol. 1758, no. 11, pp. 1846-1851, 2006.
11. B. G. Bitler and J. A. Schroeder, "Anti-cancer therapies that utilize cell penetrating peptides, " Recent Patents on Anti-Cancer Drug Discovery, vol. 5, no. 2, pp. 99-108, 2010.
12. S.-L. Fang, T.-C. Fan, H.-W. Fu et al., "A novel cell-penetrating peptide derived fromhuman eosinophil cationic protein, " PLoS ONE, vol. 8, no. 3, Article ID e57318, 2013.
13. P.-C. Lien, P.-H. Kuo, C.-J. Chen et al., "In silico prediction and in vitro characterization of multifunctional human RNase3, " BioMed Research International, vol. 2013, Article ID 170398, 12 pages, 2013.
14. C.-J. Chen, P.-H. Kuo, T.-J. Hung et al., "In vitro characterization and in vivo application of a dual functional peptide, " in Proceedings of the 7th International Conference on Complex, Intelligent, and Software Intensive Systems (CISIS '13), pp. 576-581, Taichung, Taiwan, July 2013.
15. K. R. Kidd and B. M. Weinstein, "Fishing for novel angiogenic therapies, " British Journal of Pharmacology, vol. 140, no. 4, pp. 585-594, 2003.
16. G. N. Serbedzija, E. Flynn, and C. E. Willett, "Zebrafish angiogenesis: a new model for drug screening, " Angiogenesis, vol. 3, no. 4, pp. 353-359, 1999.
17. S. Y. Yang, J. L. Wu, C. H. Tso et al., "A novel quantitative immunomagnetic reduction assay for Nervous necrosis virus, " Journal of Veterinary Diagnostic Investigation, vol. 24, no. 5, pp. 911-917, 2012.
18. I. Capila and R. J. Linhardt, "Heparin-protein interactions, " Angewandte Chemie-International Edition, vol. 41, no. 3, pp. 391-412, 2002.
19. C. Combet, C. Blanchet, C. Geourjon, and G. Deleáge, "NPS@: network protein sequence analysis, " Trends in Biochemical Sciences, vol. 25, no. 3, pp. 147-150, 2000.
20. J. L. Sussman, E. E. Abola, D. Lin, J. Jiang, N. O. Manning, and J. Prilusky, "The protein data bank: Bridging the gap between the sequence and 3Dstructure world, " Genetica, vol. 106, no. 1-2, pp. 149-158, 1999.
21. Y. G. Choi and A. L. N. Rao, "Molecular studies on bromovirus capsid protein: VII. Selective packaging of BMV RNA4 by specific N-terminal arginine residues, " Virology, vol. 275, no. 1, pp. 207-217, 2000.
22. S. Futaki, T. Suzuki, W. Ohashi et al., "Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery, " Journal of Biological Chemistry, vol. 276, no. 8, pp. 5836-5840, 2001.
23. J. P. M. Langedijk, "Translocation activity of C-terminal domain of pestivirus Erns and ribotoxin L3 loop, " Journal of Biological Chemistry, vol. 277, no. 7, pp. 5308-5314, 2002.
24. L. Chaloin, P. Vidal, P. Lory et al., "Design of carrier peptideoligonucleotide conjugates with rapid membrane translocation and nuclear localization properties, " Biochemical and Biophysical Research Communications, vol. 243, no. 2, pp. 601-608, 1998.
25. E. Vivès, P. Brodin, and B. Lebleu, "A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus, " Journal of Biological Chemistry, vol. 272, no. 25, pp. 16010-16017, 1997.
26. J. S. Wadia, R. V. Stan, and S. F. Dowdy, "Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis, " Nature Medicine, vol. 10, no. 3, pp. 310-315, 2004.
27. T. Sugita, T. Yoshikawa, Y. Mukai et al., "Comparative study on transduction and toxicity of protein transduction domains, " British Journal of Pharmacology, vol. 153, no. 6, pp. 1143-1152, 2008.
28. S. Kameyama, M. Horie, T. Kikuchi et al., "Acid wash in determining cellular uptake of fab/cell-permeating peptide conjugates, " Biopolymers, vol. 88, no. 2, pp. 98-107, 2007.
29. G. Elliott and P. O'Hare, "Intercellular trafficking and protein delivery by a herpesvirus structural protein, " Cell, vol. 88, no. 2, pp. 223-233, 1997.
30. F. J. Byfield, Q. Wen, K. Leszczýnska et al., "Cathelicidin LL-37 peptide regulates endothelial cell stiffness and endothelial barrier permeability, " The American Journal of Physiology-Cell Physiology, vol. 300, no. 1, pp. C105-C112, 2011.
31. S. Pochet, S. Tandel, S. Querriére et al., "Modulation by LL-37 of the responses of salivary glands to purinergic agonists, " Molecular Pharmacology, vol. 69, no. 6, pp. 2037-2046, 2006.
32. G. Drin, S. Cottin, E. Blanc, A. R. Rees, and J. Temsamani, "Studies on the internalization mechanism of cationic cellpenetrating peptides, "The Journal of Biological Chemistry, vol. 278, no. 33, pp. 31192-31201, 2003.
33. M. Magzoub, S. Sandgren, P. Lundberg et al., "N-terminal peptides fromunprocessed prion proteins enter cells by macropinocytosis, " Biochemical and Biophysical Research Communications, vol. 348, no. 2, pp. 379-385, 2006.
34. F. D. Nascimento, M. A. F. Hayashi, A. Kerkis et al., "Crotamine mediates gene delivery into cells through the binding to heparan sulfate proteoglycans, " The Journal of Biological Chemistry, vol. 282, no. 29, pp. 21349-21360, 2007.
35. Z. Fajloun, R. Kharrat, L. Chen et al., "Chemical synthesis and characterization ofmaurocalcine, a scorpion toxin that activates Ca2+ release channel/ryanodine receptors, " FEBS Letters, vol. 469, no. 2-3, pp. 179-185, 2000.
36. A. Mosbah, R. Kharrat, Z. Fajloun et al., "A new fold in the scorpion toxin family, associated with an activity on a ryanodine-sensitive calcium channel, " Proteins, vol. 40, no. 3, pp. 436-442, 2000.
37. E. Vives, "Cellular utake of the Tat peptide: an endocytosis mechanism following ionic interactions, " Journal of Molecular Recognition, vol. 16, no. 5, pp. 265-271, 2003.
38. M. Tyagi, M. Rusnati, M. Presta, and M. Giacca, "Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans, " The Journal of Biological Chemistry, vol. 276, no. 5, pp. 3254-3261, 2001.
39. T.-W. Pai, M. D.-T. Chang, W.-S. Tzou et al., "REMUS: a tool for identification of unique peptide segments as epitopes, " Nucleic Acids Research, vol. 34, pp. W198-W201, 2006.
40. D. Jha, R. Mishra, S. Gottschalk et al., "CyLoP-1: a novel cysteine-rich cell-penetrating peptide for cytosolic delivery of cargoes, " Bioconjugate Chemistry, vol. 22, no. 3, pp. 319-328, 2011.
41. G. Dom, C. Shaw-Jackson, C. Matis et al., "Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation, "Nucleic Acids Research, vol. 31, no. 2, pp. 556-561, 2003.
42. H. Park, Y. Kim, Y. Lim, I. Han, and E.-S. Oh, "Syndecan-2 mediates adhesion and proliferation of colon carcinoma cells, " The Journal of Biological Chemistry, vol. 277, no. 33, pp. 29730-29736, 2002.
43. K. Nackaerts, E. Verbeken, G. Deneffe, B. Vanderschueren, M. Demedts, and G. David, "Heparan sulfate proteoglycan expression in human lung-cancer cells, " International Journal of Cancer, vol. 74, no. 3, pp. 335-345, 1997.
44. R. D. Sanderson, "Heparan sulfate proteoglycans in invasion and metastasis, " Seminars in Cell and Developmental Biology, vol. 12, no. 2, pp. 89-98, 2001.
45. S. Hibino, M. Shibuya, M. P. Hoffman et al., "Laminin 5 chain metastasis-and angiogenesis-inhibiting peptide blocks fibroblast growth factor 2 activity by binding to the heparan sulfate chains of CD44, " Cancer Research, vol. 65, no. 22, pp. 10494-10501, 2005.
46. M. M. Fuster, L. Wang, J. Castagnola et al., "Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis, " The Journal of Cell Biology, vol. 177, no. 3, pp. 539-549, 2007.
47. L. Jakobsson, J. Kreuger, K. Holmborn et al., "Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis, " Developmental Cell, vol. 10, no. 5, pp. 625-634, 2006.
48. L. Lamalice, F. LeBoeuf, andJ. Huot, "Endothelial cell migration during angiogenesis, " Circulation Research, vol. 100, no. 6, pp. 782-794, 2007.
49. S. Hibino, M. Shibuya, J. A. Engbring, M. Mochizuki, M. Nomizu, and H. K. Kleinman, "Identification of an active site on the laminin 5 chain globular domain that binds to CD44 and inhibits malignancy, " Cancer Research, vol. 64, no. 14, pp. 4810-4816, 2004.
50. T.-Y. Lee, J. Folkman, and K. Javaherian, "HSPG-Binding peptide corresponding to the exon 6a-encoded domain of VEGF inhibits tumor growth by blocking angiogenesis in Murine model, " PLoS ONE, vol. 5, no. 4, Article ID e9945, 2010.
51. S. Nicoli, G. De Sena, andM. Presta, "Fibroblast growth factor 2-induced angiogenesis in zebrafish: the zebrafish yolkmembrane (ZFYM) angiogenesis assay, " Journal of Cellular and Molecular Medicine, vol. 13, no. 8, pp. 2061-2068, 2009.
52. M.-W. Kuo, C.-H. Wang, H.-C. Wu, S.-J. Chang, and Y.-J. Chuang, "Soluble THSD7A is an N-glycoprotein that promotes endothelial cell migration and tube formation in angiogenesis, " PLoS ONE, vol. 6, no. 12, Article ID e29000, 2011.
53. R. Kumar, I. Roy, T. Y. Ohulchanskky et al., "In vivo biodistribution and clearance studies using multimodal organically modified silica nanoparticles, " ACS Nano, vol. 4, no. 2, pp. 699-708, 2010.
54. S. Nagayama, K.-I. Ogawara, Y. Fukuoka, K. Higaki, and T. Kimura, "Time-dependent changes in opsonin amount associated on nanoparticles alter their hepatic uptake characteristics, " International Journal of Pharmaceutics, vol. 342, no. 1-2, pp. 215-221, 2007.
55. B. Zhang, B. Yang, C. Zhai, B. Jiang, and Y. Wu, "The role of exendin-4-conjugated superparamagnetic iron oxide nanoparticles in beta-cell-targeted MRI, " Biomaterials, vol. 34, no. 23, pp. 5843-5852, 2013.
56. D. Sarko, B. Beijer, R. G. Boy et al., "The pharmacokinetics of cell-penetrating peptides, " Molecular Pharmaceutics, vol. 7, no. 6, pp. 2224-2231, 2010.
57. F. D. Nascimento, L. Sancey, A. Pereira et al., "The natural cellpenetrating peptide crotamine targets tumor tissue in vivo and triggers a lethal calcium-dependent pathway in cultured cells, " Molecular Pharmaceutics, vol. 9, no. 2, pp. 211-221, 2012.
58. D. Görlich and I. W. Mattaj, "Nucleocytoplasmic transport, " Science, vol. 271, no. 5255, pp. 1513-1518, 1996.
59. D. Kalderon, B. L. Roberts, W. D. Richardson, and A. E. Smith, "A short amino acid sequence able to specify nuclear location, " Cell, vol. 39, no. 3, pp. 499-509, 1984.
60. D. A. Jans, D. A. Jans, P. Jans, and P. Jans, "Negative charge at the casein kinase II site flanking the nuclear localization signal of the SV40 large T-antigen is mechanistically important for enhanced nuclear import, " Oncogene, vol. 9, no. 10, pp. 2961-2968, 1994.
61. D. Derossi, A. H. Joliot, G. Chassaing, and A. Prochiantz, "The third helix of the Antennapedia homeodomain translocates through biologicalmembranes, "The Journal of Biological Chemistry, vol. 269, no. 14, pp. 10444-10450, 1994.
62. T.-C. Fan, H.-T. Chang, I.-W. Chen, H.-Y. Wang, and M. D.-T. Chang, "A heparan sulfate-facilitated and raft-dependent macropinocytosis of eosinophil cationic protein, " Traffic, vol. 8, no. 12, pp. 1778-1795, 2007.
63. M. C. Schmidt, B. Rothen-Rutishauser, B. Rist et al., "Translocation of human calcitonin in respiratory nasal epithelium is associated with self-assembly in lipidmembrane, " Biochemistry, vol. 37, no. 47, pp. 16582-16590, 1998.
64. N. Sakamoto and A. S. Rosenberg, "Apolipoprotein B binding domains: evidence that they are cell-penetrating peptides that efficiently deliver antigenic peptide for cross-presentation of cytotoxic T cells, " Journal of Immunology, vol. 186, no. 8, pp. 5004-5011, 2011.
65. S. Lang, B. Rothen-Rutishauser, J. C. Perriard, M. C. Schmidt, and H. P. Merkle, "Permeation and pathways of human calcitonin (hCT) across excised bovine nasal mucosa, " Peptides, vol. 19, no. 3, pp. 599-607, 1998.
66. A. Elmquist, M. Lindgren, T. Bartfai, and U. Langel, "Vecadherin-derived cell-penetrating peptide, pVEC with carrier functions, " Experimental Cell Research, vol. 269, no. 2, pp. 237-244, 2001.
67. E. Eiŕksdóttir, I. Mäger, T. Lehto, S. El Andaloussi, and U. Langel, "Cellular internalization kinetics of (luciferin-)cellpenetrating peptide conjugates, " Bioconjugate Chemistry, vol. 21, no. 9, pp. 1662-1672, 2010.
68. I. Mäger, E. Eiŕksdóttir, K. Langel, S. EL Andaloussi, and U. Langel, "Assessing the uptake kinetics and internalization mechanisms of cell-penetrating peptides using a quenched fluorescence assay, " Biochimica et Biophysica Acta, vol. 1798, no. 3, pp. 338-343, 2010.
69. F. Duchardt, I. R. Ruttekolk, W. P. R. Verdurmen et al., "A cell-penetrating peptide derived from human lactoferrin with conformation-dependent uptake efficiency, " The Journal of Biological Chemistry, vol. 284, no. 52, pp. 36099-36108, 2009.
70. H. Noguchi, S. Matsumoto, T. Okitsu et al., "PDX-1 protein is internalized by lipid raft-dependent macropinocytosis, " Cell Transplantation, vol. 14, no. 9, pp. 637-645, 2005.
71. F. J. Byfield, Q. Wen, K. Leszczýnska et al., "Cathelicidin LL-37 peptide regulates endothelial cell stiffness and endothelial barrier permeability, " American Journal of Physiology-Cell Physiology, vol. 300, no. 1, pp. C105-C112, 2011.
72. R. Berges, J. Balzeau, A. C. Peterson, and J. Eyer, "A tubulin binding peptide targets glioma cells disrupting their microtubules, blocking migration, and inducing apoptosis, "Molecular Therapy, vol. 20, no. 7, pp. 1367-1377, 2012.
73. C. Lépinoux-Chambaud and J. Eyer, "The NFL-TBS. 40-63 anti-glioblastoma peptide enters selectively in glioma cells by endocytosis, " International Journal of Pharmaceutics, vol. 454, no. 2, pp. 738-747, 2013.
74. H. Jia, M. Lohr, S. Jezequel et al., "Cysteine-rich and basic domain HIV-1 Tat peptides inhibit angiogenesis and induce endothelial cell apoptosis, " Biochemical and Biophysical Research Communications, vol. 283, no. 2, pp. 469-479, 2001.
75. R. R. Mehta, T. Yamada, B. N. Taylor et al., "A cell penetrating peptide derived from azurin inhibits angiogenesis and tumor growth by inhibiting phosphorylation of VEGFR-2, FAK and Akt, " Angiogenesis, vol. 14, no. 3, pp. 355-369, 2011.