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BioMed Research International
Volume 2014, Article ID 152659, 10 pages
http://dx.doi.org/10.1155/2014/152659
Research Article

Chlorotoxin-Fc Fusion Inhibits Release of MMP-2 from Pancreatic Cancer Cells

Division of Chemistry and Biotechnology, Graduate School of Natural Science and Technology, Okayama University, Okayama 7008530, Japan

Received 29 October 2013; Accepted 11 December 2013; Published 8 January 2014

Academic Editor: Andrei Surguchov

Copyright © 2014 Samah El-Ghlban 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. D. Hariharan, A. Saied, and H. M. Kocher, “Analysis of mortality rates for pancreatic cancer across the world,” HPB, vol. 10, no. 1, pp. 58–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Ellenrieder, B. Alber, U. Lacher et al., “Role of MT-MMPs and MMP-2 in pancreatic cancer progression,” International Journal of Cancer, vol. 85, no. 1, pp. 14–20, 2000. View at Google Scholar
  3. D. Destouches, E. Huet, M. Sader et al., “Multivalent pseudopeptides targeting cell surface nucleoproteins inhibit cancer cell invasion through tissue inhibitor of metalloproteinases 3 (TIMP-3) release,” The Journal of Biological Chemistry, vol. 287, no. 52, pp. 43685–43693, 2012. View at Google Scholar
  4. J. Yue, K. Zhang, and J. Chen, “Role of integrins in regulating proteases to mediate extracellular matrix remodeling,” Cancer Microenvironment, vol. 5, no. 3, pp. 275–283, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. L. M. Coussens, B. Fingleton, and L. M. Matrisian, “Matrix metalloproteinase inhibitors and cancer: trials and tribulations,” Science, vol. 295, no. 5564, pp. 2387–2392, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. L. A. Liotta, P. S. Steeg, and W. G. Stetler-Stevenson, “Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation,” Cell, vol. 64, no. 2, pp. 327–336, 1991. View at Google Scholar · View at Scopus
  7. W. C. Parks, C. L. Wilson, and Y. S. López-Boado, “Matrix metalloproteinases as modulators of inflammation and innate immunity,” Nature Reviews Immunology, vol. 4, no. 8, pp. 617–629, 2004. View at Google Scholar · View at Scopus
  8. M. W. Roomi, V. Ivanov, T. Kalinovsky, A. Niedzwiecki, and M. Rath, “Inhibition of glioma cell line A-172 MMP activity and cell invasion in vitro by a nutrient mixture,” Medical Oncology, vol. 24, no. 2, pp. 231–238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Wild-Bode, M. Weller, and W. Wick, “Molecular determinants of glioma cell migration and invasion,” Journal of Neurosurgery, vol. 94, no. 6, pp. 978–984, 2001. View at Google Scholar · View at Scopus
  10. M. Seiki, “Membrane-type matrix metalloproteinases,” APMIS, vol. 107, no. 1, pp. 137–143, 1999. View at Google Scholar · View at Scopus
  11. H. Sato, T. Takino, Y. Okada et al., “A matrix metalloproteinase expressed on the surface of invasive tumour cells,” Nature, vol. 370, no. 6484, pp. 61–65, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Itoh and M. Seiki, “MT1-MMP: a potent modifier of pericellular microenvironment,” Journal of Cellular Physiology, vol. 206, no. 1, pp. 1–8, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. P. D. Brown, R. E. Bloxidge, S. A. Stuart, K. C. Gatter, and J. Carmichael, “Association between expression of activated 72-kilodalton gelatinase and tumor spread in non-small-cell lung carcinoma,” Journal of the National Cancer Institute, vol. 85, no. 7, pp. 574–578, 1993. View at Google Scholar · View at Scopus
  14. Y. Okada, T. Morodomi, J. J. Enghild et al., “Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties,” European Journal of Biochemistry, vol. 194, no. 3, pp. 721–730, 1990. View at Google Scholar · View at Scopus
  15. T. Kinoshita, H. Sato, T. Takino, M. Itoh, T. Akizawa, and M. Seiki, “Processing of a precursor of 72-kilodalton type IV collagenase/gelatinase A by a recombinant membrane-type 1 matrix metalloproteinase,” Cancer Research, vol. 56, no. 11, pp. 2535–2538, 1996. View at Google Scholar · View at Scopus
  16. H. Sato and T. Takino, “Coordinate action of membrane-type matrix metalloproteinase-1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion,” Cancer Science, vol. 101, no. 4, pp. 843–847, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Hernandez-Barrantes, M. Toth, M. M. Bernardo et al., “Binding of active (57 kDa) membrane type 1-matrix metalloproteinase (MT1-MMP) to tissue inhibitor of metalloproteinase (TIMP)-2 regulates MT1-MMP processing and pro-MMP-2 activation,” The Journal of Biological Chemistry, vol. 275, no. 16, pp. 12080–12089, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. DeBin, J. E. Maggio, and G. R. Strichartz, “Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion,” American Journal of Physiology: Cell Physiology, vol. 264, no. 2, pp. C361–C369, 1993. View at Google Scholar · View at Scopus
  19. A. N. Mamelak and D. B. Jacoby, “Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601),” Expert Opinion on Drug Delivery, vol. 4, no. 2, pp. 175–186, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Deshane, C. C. Garner, and H. Sontheimer, “Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2,” The Journal of Biological Chemistry, vol. 278, no. 6, pp. 4135–4144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Soroceanu, Y. Gillespie, M. B. Khazaeli, and H. Sontheimer, “Use of chlorotoxin for targeting of primary brain tumors,” Cancer Research, vol. 58, no. 21, pp. 4871–4879, 1998. View at Google Scholar · View at Scopus
  22. S. A. Lyons, J. O'Neal, and H. Sontheimer, “Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin,” GLIA, vol. 39, no. 2, pp. 162–173, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. D. B. Jacoby, E. Dyskin, M. Yalcin et al., “Potent pleiotropic anti-angiogenic effects of TM601, a synthetic chlorotoxin peptide,” Anticancer Research, vol. 30, no. 1, pp. 39–46, 2010. View at Google Scholar · View at Scopus
  24. M. Veiseh, P. Gabikian, S. B. Bahrami et al., “Tumor paint: a chlorotoxin: Cy5. 5 bioconjugate for intraoperative visualization of cancer foci,” Cancer Research, vol. 67, no. 14, pp. 6882–6888, 2007. View at Google Scholar
  25. C. Sun, O. Veiseh, J. Gunn et al., “In vivo MRI detection of gliomas by chlorotoxin-conjugated superparamagnetic nanoprobes,” Small, vol. 4, no. 3, pp. 372–379, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. O. Veiseh, C. Sun, C. Fang et al., “Specific targeting of brain tumors with an optical/magnetic resonance imaging nanoprobe across the blood-brain barrier,” Cancer Research, vol. 69, no. 15, pp. 6200–6207, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. X.-X. Meng, J.-Q. Wan, M. Jing, S.-G. Zhao, W. Cai, and E.-Z. Liu, “Specific targeting of gliomas with multifunctional superparamagnetic iron oxide nanoparticle optical and magnetic resonance imaging contrast agents,” Acta Pharmacologica Sinica, vol. 28, no. 12, pp. 2019–2026, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. O. Veiseh, F. M. Kievit, J. W. Gunn, B. D. Ratner, and M. Zhang, “A ligand-mediated nanovector for targeted gene delivery and transfection in cancer cells,” Biomaterials, vol. 30, no. 4, pp. 649–657, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Kasai, K. Nakamura, A. Vaidyanath et al., “Chlorotoxin fused to IgG-Fc inhibits glioblastoma cell motility via receptor-mediated endocytosis,” Journal of Drug Delivery, vol. 2012, Article ID 975763, 10 pages, 2012. View at Publisher · View at Google Scholar
  30. T. Hashizume, T. Fukuda, T. Nagaoka et al., “Cell type dependent endocytic internalization of ErbB2 with an artificial peptide ligand that binds to ErbB2,” Cell Biology International, vol. 32, no. 7, pp. 814–826, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Hagemann, S. C. Robinson, M. Schulz, L. Trümper, F. R. Balkwill, and C. Binder, “Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-α dependent up-regulation of matrix metalloproteases,” Carcinogenesis, vol. 25, no. 8, pp. 1543–1549, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Mayor and R. E. Pagano, “Pathways of clathrin-independent endocytosis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 8, pp. 603–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Kirkham and R. G. Parton, “Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers,” Biochimica et Biophysica Acta, vol. 1745, no. 3, pp. 273–286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Falcone, E. Cocucci, P. Podini, T. Kirchhausen, E. Clementi, and J. Meldolesi, “Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events,” Journal of Cell Science, vol. 119, no. 22, pp. 4758–4769, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. L. Gong, G. M. Xu, W. D. Huang, and L. B. Chen, “Expression of matrix metalloproteinases and the tissue inhibitors of metalloproteinases and their local invasiveness and metastasis in Chinese human pancreatic cancer,” Journal of Surgical Oncology, vol. 73, no. 2, pp. 95–99, 2000. View at Google Scholar
  36. T. M. Gress, F. Muller-Pillasch, M. M. Lerch, H. Friess, H. Buchler, and G. Adler, “Expression and in-situ localization of genes coding for extracellular matrix proteins and extracellular matrix degrading proteases in pancreatic cancer,” International Journal of Cancer, vol. 62, no. 4, pp. 407–413, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Yamamoto, F. Itoh, S. Iku et al., “Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human pancreatic adenocarcinomas: clinicopathologic and prognostic significance of matrilysin expression,” Journal of Clinical Oncology, vol. 19, no. 4, pp. 1118–1127, 2001. View at Google Scholar · View at Scopus
  38. U. B. Hofmann, J. R. Westphal, A. A. Kraats, D. J. Ruiter, and G. N. Muijen, “Expression of integrin αvβ3 correlates with activation of membranetype matrix metalloproteinase-1 (MT1-MMP) and matrix metalloproteinase-2 (MMP-2) in human melanoma cells in vitro and in vivo,” International Journal of Cancer, vol. 87, no. 1, pp. 12–19, 2000. View at Google Scholar
  39. E. I. Deryugina, B. Ratnikov, E. Monosov et al., “MT1-MMP initiates activation of pro-MMP-2 and integrin αvβ3 promotes maturation of MMP-2 in breast carcinoma cells,” Experimental Cell Research, vol. 263, no. 2, pp. 209–223, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Nagase, “Cell surface activation of progelatinase A (proMMP-2) and cell migration,” Cell Research, vol. 8, no. 3, pp. 179–186, 1998. View at Google Scholar · View at Scopus
  41. A. Y. Strongin, I. Collier, G. Bannikov, B. L. Marmer, G. A. Grant, and G. I. Goldberg, “Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease,” The Journal of Biological Chemistry, vol. 270, no. 10, pp. 5331–5338, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. M. B. Mcferrin and H. Sontheimer, “A role for ion channels in glioma cell invasion,” Neuron Glia Biology, vol. 2, no. 1, pp. 39–49, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Osenkowski, M. Toth, and R. Fridman, “Processing, shedding, and endocytosis of membrane type 1-Matrix metalloproteinase (MT1-MMP),” Journal of Cellular Physiology, vol. 200, no. 1, pp. 2–10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. B. G. Gálvez, S. Matías-Román, M. Yáñez-Mó, F. Sánchez-Madrid, and A. G. Arroyo, “ECM regulates MT1-MMP localization with β1 or αvβ3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells,” Journal of Cell Biology, vol. 159, no. 3, pp. 509–521, 2002. View at Google Scholar
  45. F.-T. Mu, J. M. Callaghan, O. Steele-Mortimer et al., “EEA1, an early endosome-associated protein. EEA1 is a conserved α- helical peripheral membrane protein flanked by cysteine 'fingers' and contains a calmodulin-binding IQ motif,” The Journal of Biological Chemistry, vol. 270, no. 22, pp. 13503–13511, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. I. G. Mills, A. T. Jones, and M. J. Clague, “Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes,” Current Biology, vol. 8, no. 15, pp. 881–884, 1998. View at Google Scholar · View at Scopus
  47. B. Sönnichsen, S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial, “Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11,” Journal of Cell Biology, vol. 149, no. 4, pp. 901–913, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. X. Yang, E. D. Staren, J. M. Howard, T. Iwamura, J. E. Bartsch, and H. E. Appert, “Invasiveness and MMP expression in pancreatic carcinoma,” Journal of Surgical Research, vol. 98, no. 1, pp. 33–39, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Koshiba, R. Hosotani, M. Wada et al., “Involvement of matrix metalloproteinase-2 activity in invasion and metastasis of pancreatic carcinoma,” Cancer, vol. 82, no. 4, pp. 642–650, 1998. View at Google Scholar
  50. L. Bello, V. Lucini, G. Carrabba et al., “Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2,” Cancer Research, vol. 61, no. 24, pp. 8730–8736, 2001. View at Google Scholar · View at Scopus
  51. U. B. Hofmann, J. R. Westphal, E. T. Waas, J. C. Becker, D. J. Ruiter, and G. N. P. Van Muijen, “Coexpression of integrin α(v)β3 and matrix metalloproteinase-2 (MMP-2) coincides with MMP-2 activation: correlation with melanoma progression,” Journal of Investigative Dermatology, vol. 115, no. 4, pp. 625–632, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. E. I. Deryugina, M. A. Bourdon, K. Jungwirth, J. W. Smith, and A. Y. Strongin, “Functional activation of integrin αvβ3 in tumor cells expressing membrane type 1 matrix metalloprotease,” International Journal of Cancer, vol. 86, no. 1, pp. 15–23, 2000. View at Google Scholar