Cancer Letters
Volume 290, Issue 2 , Pages 192-203 , 28 April 2010

Selective death of human breast cancer cells by lytic immunoliposomes: Correlation with their HER2 expression level

  • Enrique Barrajón-Catalán

      Affiliations

    • Molecular and Cellular Biology Institute (IBMC), Miguel Hernández University, Avda. de la Universidad s/n, E-03202 Elche, Alicante, Spain
    • Both authors contributed evenly.
  • ,
  • María P. Menéndez-Gutiérrez

      Affiliations

    • Molecular and Cellular Biology Institute (IBMC), Miguel Hernández University, Avda. de la Universidad s/n, E-03202 Elche, Alicante, Spain
    • Both authors contributed evenly.
    • Present address: National Center for Cardiovascular Research Foundation, Regenerative Cardiology Department, C/ Melchor Fernández Almagro, 3, 28029 Madrid, Spain.
  • ,
  • Alberto Falco

      Affiliations

    • Molecular and Cellular Biology Institute (IBMC), Miguel Hernández University, Avda. de la Universidad s/n, E-03202 Elche, Alicante, Spain
  • ,
  • Alfredo Carrato

      Affiliations

    • Elche University Hospital, Biomedical Research Foundation (FIBElx), Camí de la Almazara 11, Ed. Anexo II, 03203 Elche, Alicante, Spain
  • ,
  • Miguel Saceda

      Affiliations

    • Elche University Hospital, Biomedical Research Foundation (FIBElx), Camí de la Almazara 11, Ed. Anexo II, 03203 Elche, Alicante, Spain
  • ,
  • Vicente Micol

      Affiliations

    • Molecular and Cellular Biology Institute (IBMC), Miguel Hernández University, Avda. de la Universidad s/n, E-03202 Elche, Alicante, Spain
    • Corresponding Author InformationCorresponding author. Tel.: +34 96 6658430; fax: +34 96 6658758.

Received 25 June 2009 ,Revised 7 September 2009 ,Accepted 14 September 2009.

References 

  1. Sznol M, Holmlund J. Antigen-specific agents in development. Semin. Oncol. 1997;24:173–186
  2. Noble CO, Kirpotin DB, Hayes ME, Mamot C, Hong K, Park JW, et al. Development of ligand-targeted liposomes for cancer therapy. Expert Opin. Ther. Targets. 2004;8:335–353
  3. Park JW, Hong K, Kirpotin DB, Papahadjopoulos D, Benz CC. Immunoliposomes for cancer treatment. Adv. Pharmacol. 1997;40:399–435
  4. Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol. Rev. 1999;51:691–743
  5. Papahadjopoulos D, Allen TM, Gabizon A, Mayhew E, Matthay K, Huang SK, et al. Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc. Natl. Acad. Sci. USA. 1991;88:11460–11464
  6. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 2000;19:3159–3167
  7. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987;235:177–182
  8. Press MF, Cordon-Cardo C, Slamon DJ. Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene. 1990;5:953–962
  9. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. New Engl. J. Med. 2001;344:783–792
  10. Kirpotin D, Park JW, Hong K, Zalipsky S, Li WL, Carter P, et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry. 1997;36:66–75
  11. Park JW, Hong K, Kirpotin DB, Colbern G, Shalaby R, Baselga J, et al. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res. 2002;8:1172–1181
  12. Patrzykat A, Douglas SE. Antimicrobial peptides: cooperative approaches to protection. Protein Peptide Lett. 2005;12:19–25
  13. Lohner K, Blondelle SE. Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics. Comb. Chem. High Throughput Screen. 2005;8:241–256
  14. Bechinger B. Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J. Membrane Biol. 1997;156:197–211
  15. Allende D, Simon SA, McIntosh TJ. Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 2005;88:1828–1837
  16. Hoskin DW, Ramamoorthy A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta. 2008;1778:357–375
  17. Son DJ, Lee JW, Lee YH, Song HS, Lee CK, Hong JT. Therapeutic application of anti-arthritis, pain-releasing, and anti-cancer effects of bee venom and its constituent compounds. Pharmacol. Ther. 2007;115:246–270
  18. Raghuraman H, Chattopadhyay A. Melittin: a membrane-active peptide with diverse functions. Biosci. Rep. 2007;27:189–223
  19. Holle L, Song W, Holle E, Wei Y, Wagner T, Yu X. A matrix metalloproteinase 2 cleavable melittin/avidin conjugate specifically targets tumor cells in vitro and in vivo. Int. J. Oncol. 2003;22:93–98
  20. Moon DO, Park SY, Heo MS, Kim KC, Park C, Ko WS, et al. Key regulators in bee venom-induced apoptosis are Bcl-2 and caspase-3 in human leukemic U937 cells through downregulation of ERK and Akt. Int. Immunopharmacol. 2006;6:1796–1807
  21. Sui SF, Wu H, Guo Y, Chen KS. Conformational changes of melittin upon insertion into phospholipid monolayer and vesicle. J. Biochem. 1994;116:482–487
  22. Lin JH, Baumgaertner A. Stability of a melittin pore in a lipid bilayer: a molecular dynamics study. Biophys. J. 2000;78:1714–1724
  23. Hu H, Chen D, Liu Y, Deng Y, Yang S, Qiao M, et al. Target ability and therapy efficacy of immunoliposomes using a humanized antihepatoma disulfide-stabilized Fv fragment on tumor cells. J. Pharm. Sci. 2006;95:192–199
  24. Menendez JA, Vazquez-Martin A, Colomer R, Brunet J, Carrasco-Pancorbo A, Garcia-Villalba R, et al. Olive oil’s bitter principle reverses acquired autoresistance to trastuzumab (Herceptin) in HER2-overexpressing breast cancer cells. BMC Cancer. 2007;7:80
  25. Tanner M, Kapanen AI, Junttila T, Raheem O, Grenman S, Elo J, et al. Characterization of a novel cell line established from a patient with Herceptin-resistant breast cancer. Mol. Cancer. Ther. 2004;3:1585–1592
  26. Olson F, Hunt CA, Szoka FC, Vail WJ, Papahadjopoulos D. Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. Biochim. Biophys. Acta. 1979;557:9–23
  27. Vemuri S, Rhodes CT. Preparation and characterization of liposomes as therapeutic delivery systems: a review. Pharm. Acta Helv. 1995;70:95–111
  28. Huwyler J, Wu D, Pardridge WM. Brain drug delivery of small molecules using immunoliposomes. Proc. Natl. Acad. Sci. USA. 1996;93:14164–14169
  29. Hansen CB, Kao GY, Moase EH, Zalipsky S, Allen TM. Attachment of antibodies to sterically stabilized liposomes: evaluation, comparison and optimization of coupling procedures. Biochim. Biophys. Acta. 1995;1239:133–144
  30. Dynamic light scattering: an introduction in 30min, Malvern Instruments technical note (MRK656-01), Malvern Instruments Ltd., 2008. Available from: <http://www.malvern.com/common/downloads/campaign/MRK656-01.pdf>.
  31. Villari V, Micali N. Light scattering as spectroscopic tool for the study of disperse systems useful in pharmaceutical sciences. J. Pharm. Sci. 2008;97:1703–1730
  32. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 1983;65:55–63
  33. Fiske CH, Subbarow Y. The colorimetric determination of phosphorus. J. Biol. Chem. 1925;66:375–400
  34. Lewis GD, Figari I, Fendly B, Wong WL, Carter P, Gorman C, et al. Differential responses of human tumor cell lines to anti-p185HER2 monoclonal antibodies. Cancer. Immunol. Immunother. 1993;37:255–263
  35. Lam PB, Burga LN, Wu BP, Hofstatter EW, Lu KP, Wulf GM. Prolyl isomerase Pin1 is highly expressed in Her2-positive breast cancer and regulates erbB2 protein stability. Mol. Cancer. 2008;7:91
  36. Cooley S, Burns LJ, Repka T, Miller JS. Natural killer cell cytotoxicity of breast cancer targets is enhanced by two distinct mechanisms of antibody-dependent cellular cytotoxicity against LFA-3 and HER2/neu. Exp. Hematol. 1999;27:1533–1541
  37. Pegram MD, Lipton A, Hayes DF, Weber BL, Baselga JM, Tripathy D, et al. Phase II study of receptor-enhanced chemosensitivity using recombinant humanized anti-p185HER2/neu monoclonal antibody plus cisplatin in patients with HER2/neu-overexpressing metastatic breast cancer refractory to chemotherapy treatment. J. Clin. Oncol. 1998;16:2659–2671
  38. Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, et al. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res. 2006;66:1630–1639
  39. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, Arteaga CL. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res. 2001;61:8887–8895
  40. Baselga J, Albanell J. Mechanism of action of anti-HER2 monoclonal antibodies. Ann. Oncol. 2001;12(Suppl. 1):S35–S41
  41. Sun WQ, Leopold AC, Crowe LM, Crowe JH. Stability of dry liposomes in sugar glasses. Biophys. J. 1996;70:1769–1776
  42. Zuba-Surma EK, Kucia M, Abdel-Latif A, Lillard J, Ratajczak MZ. The ImageStream system: a key step to a new era in imaging. Folia Histochem. Cytobiol. 2007;45:279–290
  43. Kikumori T, Kobayashi T, Sawaki M, Imai T. Anti-cancer effect of hyperthermia on breast cancer by magnetite nanoparticle-loaded anti-HER2 immunoliposomes. Breast Cancer Res. Treat. 2009;113:435–441
  44. Kullberg M, Mann K, Owens JL. A two-component drug delivery system using Her-2-targeting thermosensitive liposomes. J. Drug. Target. 2009;17:98–107
  45. Utsugi T, Schroit AJ, Connor J, Bucana CD, Fidler IJ. Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes. Cancer Res. 1991;51:3062–3066
  46. Gawronska B, Leuschner C, Enright FM, Hansel W. Effects of a lytic peptide conjugated to beta HCG on ovarian cancer: studies in vitro and in vivo. Gynecol. Oncol. 2002;85:45–52
  47. Hansel W, Enright F, Leuschner C. Destruction of breast cancers and their metastases by lytic peptide conjugates in vitro and in vivo. Mol. Cell. Endocrinol. 2006;260–262:183–189
  48. Chu ST, Cheng HH, Huang CJ, Chang HC, Chi CC, Su HH, et al. Phospholipase A2-independent Ca2+ entry and subsequent apoptosis induced by melittin in human MG63 osteosarcoma cells. Life Sci. 2007;80:364–369
  49. Arora AS, de Groen PC, Croall DE, Emori Y, Gores GJ. Hepatocellular carcinoma cells resist necrosis during anoxia by preventing phospholipase-mediated calpain activation. J. Cell Physiol. 1996;167:434–442
  50. Saini SS, Chopra AK, Peterson JW. Melittin activates endogenous phospholipase D during cytolysis of human monocytic leukemia cells. Toxicon. 1999;37:1605–1619
  51. Yan B, Wang H, Zhuo D, Li F, Kon T, Dewhirst M, et al. Apoptotic DNA fragmentation factor maintains chromosome stability in a P53-independent manner. Oncogene. 2006;25:5370–5376
  52. Wyllie AH. Apoptosis: an overview. Br. Med. Bull. 1997;53:451–465
  53. Kim HW, Kwon YB, Ham TW, Roh DH, Yoon SY, Kang SY, et al. General pharmacological profiles of bee venom and its water soluble fractions in rodent models. J. Vet. Sci. 2004;5:309–318

PII: S0304-3835(09)00598-9

doi: 10.1016/j.canlet.2009.09.010

Cancer Letters
Volume 290, Issue 2 , Pages 192-203 , 28 April 2010