The antimicrobial peptide, Lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo

International Journal of Cancer

Volumn 119, Issue 3, 2006, Pages 493-500

  Eliassen, Liv Tone ^a   Berge, Gerd ^a   Leknessund, Arild ^a   Wikman, Mari ^a   Lindin, Inger ^a   Løkke, Cecilie ^a   Ponthan, Frida ^b   Johnsen, John Inge ^b   Sveinbjørnsson, Baldur ^a   Kogner, Per ^b   Flægstad, Trond ^a   Rekdal, Øystein ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Bovine lactoferricin; Cell death; Mitochondria; Neuroblastoma

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 6; CASPASE 7; CASPASE 9; CASPASE INHIBITOR; FLUORESCENT DYE; LACTOFERRICIN B; POLYPEPTIDE ANTIBIOTIC AGENT;

ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL DEATH; CELL MEMBRANE; CELL STRAIN; CELL STRAIN SHSY 5Y; CONTROLLED STUDY; CYTOTOXICITY; ENZYME DEGRADATION; FIBROBLAST; FLUORESCENCE; GENE AMPLIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE DAMAGE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NEUROBLASTOMA CELL; NONHUMAN; ONCOGENE C MYB; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; TUMOR XENOGRAFT;

ANIMALS; ANTI-INFECTIVE AGENTS; BLOTTING, WESTERN; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; HUMANS; INHIBITORY CONCENTRATION 50; LACTOFERRIN; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEUROBLASTOMA; RATS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33745441169     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21886     Document Type: Article

References (56)

1. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003;3:203-16.
2. Cruciani RA, Barker JL, Zasloff M, Chen HC, Colamonici O. Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc Natl Acad Sci USA 1991;88:3792-6.
3. Chen HM, Wang W, Smith D, Chan SC. Effects of the anti-bacterial peptide cecropin B and its analogs, cecropins B-1 and B-2, on liposomes, bacteria, and cancer cells. Biochim Biophys Acta 1997;1336:171-9.
4. Baker MA, Maloy WL, Zasloff M, Jacob LS. Anticancer efficacy of Magainin 2 and analogue peptides. Cancer Res 1993;53:3052-7.
5. Eliassen LT, Berge G, Sveinbjørnsson B, Svendsen JS, Vorland LH, Rekdal Ø. Evidence for a direct antitumor mechanism of action of bovine lactoferricin. Anticancer Res 2002;22:2703-10.
6. Johnstone SA, Gelmon K, Mayer LD, Hancock RE, Bally MB. In vitro characterization of the anticancer activity of membrane-active cationic peptides. I. Peptide-mediated cytotoxicity and peptide-enhanced cytotoxic activity of doxorubicin against wild-type and p-glycoprotein over-expressing tumor cell lines. Anticancer Drug Des 2000;15:151-4.
7. Ohsaki Y, Gazdar AF, Chen HC, Johnson BE. Antitumor activity of magainin analogues against human lung cancer cell lines. Cancer Res 1992;52:3534-8.
8. 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;51:3062-6.
9. Yang N, Lejon T, Rekdal Ø. Antitumor activity and specificity as a function of substitutions in the lipophilic sector of helical lactoferrin-derived peptides. J Pept Sci 2003;9:300-11.
10. Yang N, Stensen W, Svendesen JS, Rekdal Ø. Enhanced antitumor activity and selectivity of lactoferrin-derived peptides. J Pept Res 2002;60:187-97.
11. Papo N, Shahar M, Eisenbach L, Shai Y. A novel lytic peptide composed of DL-amino acids selectively kills cancer cells in culture and in mice. J Biol Chem 2003;278:21018-23.
12. Sitaram N, Nagaraj R. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim Biophys Acta 1999;1462:29-54.
13. Matsuzaki K, Sugishita K, Ishibe N, Ueha M, Nakata S, Miyajima K, Epand RM. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 1998;37:11856-63.
14. Epand RM, Vogel HJ. Diversity of antimicrobial peptides and their mechanisms of action. Biochim Biophys Acta 1999;1462:11-28.
15. Andreu D, Rivas L. Animal antimicrobial peptides: an overview. Biopolymers 1998;47:415-33.
16. Mai JC, Mi Z, Kim SH, Ng B, Robbins PD. A proapoptotic peptide for the treatment of solid tumors. Cancer Res 2001;61:7709-12.
17. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, Rio GD, Krajewski S, Lombardo CR, Rao R, Ruoslahti E, Bredesen DE, Pasqualini R. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 1999;5:1032-8.
18. Takeshima K, Chikushi A, Lee KK, Yonehara S, Matsuzaki K. Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J Biol Chem 2003;278:1310-15.
19. Risso A, Braidot E, Sordano MC, Vianello A, Macri F, Skerlavaj B, Zanetti M, Gennaro R, Bernardi P. BMAP-28, an antibiotic peptide of innate immunity, induces cell death through opening of the mitochondrial permeability transition pore. Mol Cell Biol 2002;22:1926-35.
20. Vogel HJ, Schibli DJ, Jing W, Lohmeier-Vogel EM, Epand RF, Epand RM. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem Cell Biol 2002;80:49-63.
21. Yoo YC, Watanabe S, Watanabe R, Hata K, Shimazaki K, Azuma I. Bovine lactoferrin and lactoferricin inhibit tumor metastasis in mice. Adv Exp Med Biol 1998;443:285-91.
22. Yoo YC, Watanabe R, Koike Y, Mitobe M, Shimazaki K, Watanabe S, Azuma I. Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-derived peptide: involvement of reactive oxygen species. Biochem Biophys Res Commun 1997;237:624-28.
23. Mader JS, Salsman J, Conrad DM, Hoskin DW. Bovine lactoferricin selectively induces apoptosis in human leukemia and carcinoma cell lines. Mol Cancer Ther 2005;4:612-24.
24. Strøm MB, Rekdal O, Svendsen JS. Antibacterial activity of 15-residue lactoferricin derivatives. J Pept Res 2000;56:265-74.
25. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
26. Ponthan F, Johnsen JI, Klevenvall L, Castro J, Kogner P. The synthetic retinoid RO 13-6307 induces neuroblastoma differentiation in vitro and inhibits neuroblastoma tumour growth in vivo. Int J Cancer 2003;104:418-24.
27. Bozzola JJ, Russel LD. Specimen preparation for transmission electron microscopy. In: Bozzola JJ, Russel LD, eds. Electron microscopy. Sudbury, MA: Jones & Barlett, 1992 p. 15-38.
28. Haukland HH, Ulvatne H, Sandvik K, Vorland LH. The antimicrobial peptides lactoferricin B and magainin 2 cross over the bacterial cytoplasmic membrane and reside in the cytoplasm. FEBS Lett 2001;508:389-93.
29. Johnsen JI, Pettersen I, Ponthan F, Sveinbjornsson B, Flægstad T, Kogner P. Synergistic induction of apoptosis in neuroblastoma cells using a combination of cytostatic drugs with interferon-γ and TRAIL. Int J Oncol 2004;25:1849-57.
30. Nilsson S, Pahlman S, Arnberg H, Letocha H, Westlin JE. Characterization and uptake of radiolabelled meta-iodobenzylguanidine (MIBG) in a human neuroblastoma heterotransplant model in athymic rats. Acta Oncol 1993;32:887-91.
31. Blankenberg FG, Katsikis PD, Tait JF, Davis RE, Naumovski L, Ohtsuki K, Kopiwoda S, Abrams MJ, Darkes M, Robbins RC, Maecker HT, Strauss HW. In vivo detection and imaging of phosphatidylserine expression during programmed cell death. Proc Natl Acad Sci USA 1998;95:6349-54.
32. Bombeli T, Karsan A, Tait JF, Harlan JM. Apoptotic vascular endothelial cells become procoagulant. Blood 1997;89:2429-42.
33. Zwaal RF, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997;89:1121-32.
34. Williamson P, Schlegel RA. Back and forth: the regulation and function of transbilayer phospholipid movement in eukaryotic cells. Mol Membr Biol 1994;11:199-216.
35. Raval GN, Patel DD, Parekh LJ, Patel JB, Shah MH, Patel PS. Evaluation of serum sialic acid, sialyltransferase and sialoproteins in oral cavity cancer. Oral Dis 2003;9:119-28.
36. Miyagi T, Wada T, Yamaguchi K, Hata K. Sialidase and malignancy: a minireview. Glycoconj J 2004;20:189-98.
37. Cappelli G, Paladini S, D'Agata A. Tumor markers in the diagnosis of pancreatic cancer. Tumori 1999;85 (Suppl 1):S19-S21.
38. - ions in micellar-packaged gramicidin A. Biochim Biophys Acta 1995;1238:12-21.
39. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 1998;60:619-42.
40. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997;90:405-13.
41. Teitz T, Wei T, Valentine MB, Vanin EF, Grenet J, Valentine VA. Behm FG, Look AT, Lahti JM, Kidd VJ. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 2000;6:529-35.
42. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 2003;304:463-70.
43. Tronstad KJ, Gjertsen BT, Krakstad C, Berge K, Brustugun OT, Doskeland SO, Berge RK. Mitochondrial-targeted fatty acid analog induces apoptosis with selective loss of mitochondrial glutathione in promyelocytic leukemia cells. Chem Biol 2003;10:609-18.
44. Risso A, Zanetti M, Gennaro R. Cytotoxicity and apoptosis mediated by two peptides of innate immunity. Cell Immunol 1998;189:107-15.
45. Hovius R, Lambrechts H, Nicolay K, de Kruijff B. Improved methods to isolate and subfractionate rat liver mitochondria. Lipid composition of the inner and outer membrane. Biochim Biophys Acta 1990;1021:217-26.
46. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B. Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1997;1325:108-16.
47. Villa AM, Doglia SM. Mitochondria in tumor cells studied by laser scanning confocal microscopy. J Biomed Opt 2004;9:385-94.
48. Parlo RA, Coleman PS. Enhanced rate of citrate export from cholesterol-rich hepatoma mitochondria. The truncated Krebs cycle and other metabolic ramifications of mitochondrial membrane cholesterol. J Biol Chem 1984;259:9997-10003.
49. Son KN, Park J, Chung CK, Chung DK, Yu DY, Lee KK, Kim J. Human lactoferrin activates transcription of IL-1β gene in mammalian cells. Biochem Biophys Res Commun 2002;290:236-41.
50. He J, Furmanski P. Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature 1995;373:721-4.
51. Garre C, Bianchi-Scarra G, Sirito M, Musso M, Ravazzolo R. Lactoferrin binding sites and nuclear localization in K562(S) cells. J Cell Physiol 1992;153:477-82.
52. Baumrucker CR, Schanbacher F, Shang Y, Green MH. Lactoferrin interaction with retinoid signaling: cell growth and apoptosis in mammary cells. Domest Anim Endocrinol, in press.
53. Ashida K, Sasaki H, Suzuki YA, Lonnerdal B. Cellular internalization of lactoferrin in intestinal epithelial cells. Biometals 2004;17:311-15.
54. Kanyshkova TG, Semenov DV, Buneva VN, Nevinsky GA. Human milk lactoferrin binds two DNA molecules with different affinities. FEBS Lett 1999;451:235-7.
55. Hugosson M, Andreu D, Boman HG, Glaser E. Antibacterial peptides and mitochondrial presequences affect mitochondrial coupling, respiration and protein import. Eur J Biochem 1994;223:1027-33.
56. Diaz-Achirica P, Prieto S, Ubach J, Andreu D, Rial E, Rivas L. Permeabilization of the mitochondrial inner membrane by short cecropin-A-melittin hybrid peptides. Eur J Biochem 1994;224:257-63.