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BioMed Research International
Volume 2015, Article ID 237969, 15 pages
http://dx.doi.org/10.1155/2015/237969
Research Article

A Heparan Sulfate-Binding Cell Penetrating Peptide for Tumor Targeting and Migration Inhibition

1Institute of Molecular and Cellular Biology, National Tsing Hua University, Hsinchu 30013, Taiwan
2Biomedical Science and Engineering Center, National Tsing Hua University, Hsinchu 30013, Taiwan
3Institute of Bioinformatics and Structural Biology, National Tsing Hua University, Hsinchu 30013, Taiwan
4Department of Medical Science, National Tsing Hua University, Hsinchu 30013, Taiwan

Received 18 August 2014; Revised 31 October 2014; Accepted 14 November 2014

Academic Editor: Hao-Teng Chang

Copyright © 2015 Chien-Jung Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Adachi, T. Taki, M. Higashiyama, N. Kohno, H. Inufusa, and M. Miyake, “Significance of integrin α5 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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Regberg, A. Srimanee, and Ü. Langel, “Applications of cell-penetrating peptides for tumor targeting and future cancer therapies,” Pharmaceuticals, vol. 5, no. 9, pp. 991–1007, 2012. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Console, C. Marty, C. García-Echeverría, R. Schwendener, and K. Ballmer-Hofer, “Antennapedia and HIV transactivator 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  12. S.-L. Fang, T.-C. Fan, H.-W. Fu et al., “A novel cell-penetrating peptide derived from human eosinophil cationic protein,” PLoS ONE, vol. 8, no. 3, Article ID e57318, 2013. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Capila and R. J. Linhardt, “Heparin-protein interactions,” Angewandte Chemie—International Edition, vol. 41, no. 3, pp. 391–412, 2002. View at Google Scholar
  19. C. Combet, C. Blanchet, C. Geourjon, and G. Deléage, “NPS@: network protein sequence analysis,” Trends in Biochemical Sciences, vol. 25, no. 3, pp. 147–150, 2000. View at Publisher · View at Google Scholar · View at Scopus
  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 3D structure world,” Genetica, vol. 106, no. 1-2, pp. 149–158, 1999. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Chaloin, P. Vidal, P. Lory et al., “Design of carrier peptide-oligonucleotide conjugates with rapid membrane translocation and nuclear localization properties,” Biochemical and Biophysical Research Communications, vol. 243, no. 2, pp. 601–608, 1998. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  30. F. J. Byfield, Q. Wen, K. Leszczyńska 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Drin, S. Cottin, E. Blanc, A. R. Rees, and J. Temsamani, “Studies on the internalization mechanism of cationic cell-penetrating peptides,” The Journal of Biological Chemistry, vol. 278, no. 33, pp. 31192–31201, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Magzoub, S. Sandgren, P. Lundberg et al., “N-terminal peptides from unprocessed prion proteins enter cells by macropinocytosis,” Biochemical and Biophysical Research Communications, vol. 348, no. 2, pp. 379–385, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Fajloun, R. Kharrat, L. Chen et al., “Chemical synthesis and characterization of maurocalcine, a scorpion toxin that activates Ca2+ release channel/ryanodine receptors,” FEBS Letters, vol. 469, no. 2-3, pp. 179–185, 2000. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Hibino, M. Shibuya, M. P. Hoffman et al., “Laminin α5 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Lamalice, F. Le Boeuf, and J. Huot, “Endothelial cell migration during angiogenesis,” Circulation Research, vol. 100, no. 6, pp. 782–794, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Hibino, M. Shibuya, J. A. Engbring, M. Mochizuki, M. Nomizu, and H. K. Kleinman, “Identification of an active site on the laminin α5 chain globular domain that binds to CD44 and inhibits malignancy,” Cancer Research, vol. 64, no. 14, pp. 4810–4816, 2004. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Nicoli, G. De Sena, and M. Presta, “Fibroblast growth factor 2-induced angiogenesis in zebrafish: the zebrafish yolk membrane (ZFYM) angiogenesis assay,” Journal of Cellular and Molecular Medicine, vol. 13, no. 8, pp. 2061–2068, 2009. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  57. F. D. Nascimento, L. Sancey, A. Pereira et al., “The natural cell-penetrating 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. View at Publisher · View at Google Scholar · View at Scopus
  58. D. Görlich and I. W. Mattaj, “Nucleocytoplasmic transport,” Science, vol. 271, no. 5255, pp. 1513–1518, 1996. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  61. D. Derossi, A. H. Joliot, G. Chassaing, and A. Prochiantz, “The third helix of the Antennapedia homeodomain translocates through biological membranes,” The Journal of Biological Chemistry, vol. 269, no. 14, pp. 10444–10450, 1994. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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 lipid membrane,” Biochemistry, vol. 37, no. 47, pp. 16582–16590, 1998. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Elmquist, M. Lindgren, T. Bartfai, and Ü. Langel, “Ve-cadherin-derived cell-penetrating peptide, pVEC with carrier functions,” Experimental Cell Research, vol. 269, no. 2, pp. 237–244, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Eiríksdóttir, I. Mäger, T. Lehto, S. El Andaloussi, and Ü. Langel, “Cellular internalization kinetics of (luciferin-)cell-penetrating peptide conjugates,” Bioconjugate Chemistry, vol. 21, no. 9, pp. 1662–1672, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. I. Mäger, E. Eiríksdóttir, K. Langel, S. EL Andaloussi, and Ü. 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  71. F. J. Byfield, Q. Wen, K. Leszczyńska 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus