The anticancer activity of lytic peptides is inhibited by heparan sulfate on the surface of the tumor cells

BMC Cancer

Volumn 9, Issue , 2009, Pages

  Fadnes, Bodil ^a,b   Rekdal, Øystein ^a,c   Uhlin Hansen, Lars ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^c LYTIX BIOPHARMA AS   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; CHONDROITIN SULFATE; HEPARAN SULFATE; LACTOFERRICIN; SODIUM CHLORATE; CHLORATE; HEPARIN; LACTOFERRICIN B; LACTOFERRIN; PEPTIDE FRAGMENT;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL SURFACE; CHO CELL; COLORIMETRY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; ANIMAL; BIOSYNTHESIS; CATTLE; CELL STRAIN HT29; CRICETULUS; DRUG ANTAGONISM; DRUG POTENTIATION; HAMSTER; LYMPHOMA; METABOLISM; NEOPLASM; PROTEIN SECONDARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; CATTLE; CELL LINE, TUMOR; CHLORATES; CHO CELLS; CRICETINAE; CRICETULUS; DRUG SYNERGISM; HEPARIN; HEPARITIN SULFATE; HT29 CELLS; HUMANS; LACTOFERRIN; LYMPHOMA; NEOPLASMS; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY;

EID: 67650065476     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-9-183     Document Type: Article

References (77)

1. Boman HG Peptide antibiotics and their role in innate immunity Annu Rev Immunol 1995, 13:61-92 10.1146/annurev.iy.13.040195.000425 7612236
2. Hultmark D Engstrom A Bennich H Kapur R Boman HG Insect immunity: isolation and structure of cecropin D and four minor antibacterial components from Cecropia pupae Eur J Biochem 1982, 127(1):207-217 10.1111/j.1432-1033.1982.tb06857.x 7140755
3. Cornet B Bonmatin JM Hetru C Hoffmann JA Ptak M Vovelle F Refined three-dimensional solution structure of insect defensin A Structure 1995, 3(5):435-448 10.1016/S0969-2126(01)00177-0 7663941
4. Li ZQ Merrifield RB Boman IA Boman HG Effects on electrophoretic mobility and antibacterial spectrum of removal of two residues from synthetic sarcotoxin IA and addition of the same residues to cecropin B FEBS Lett 1988, 231(2):299-302 10.1016/0014-5793(88)80837-8 3360136
5. Bechinger B Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin J Membr Biol 1997, 156(3):197-211 10.1007/s002329900201 9096062
6. Polozov IV Polozova AI Tytler EM Anantharamaiah GM Segrest JP Woolley GA Epand RM Role of lipids in the permeabilization of membranes by class L amphipathic helical peptides Biochemistry 1997, 36(30):9237-9245 10.1021/ bi970045l 9230057
7. Eliassen LT Berge G Sveinbjornsson B Svendsen JS Vorland LH Rekdal O Evidence for a direct antitumor mechanism of action of bovine lactoferricin Anticancer Res 2002, 22(5):2703-2710 12529985
8. Eliassen LT Berge G Leknessund A Wikman M Lindin I Lokke C Ponthan F Johnsen JI Sveinbjornsson B Kogner P et al The antimicrobial peptide, lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo Int J Cancer 2006, 119(3):493-500 10.1002/ijc.21886 16572423
9. 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(23):21018-21023 10.1074/jbc.M211204200 12646578
10. Chen Y Xu X Hong S Chen J Liu N Underhill CB Creswell K Zhang L RGD-Tachyplesin inhibits tumor growth Cancer Res 2001, 61(6):2434-2438 11289111
11. Dennison SR Whittaker M Harris F Phoenix DA Anticancer alpha-helical peptides and structure/function relationships underpinning their interactions with tumour cell membranes Curr Protein Pept Sci 2006, 7(6):487-499 10.2174/138920306779025611 17168782
12. Mader JS Hoskin DW Cationic antimicrobial peptides as novel cytotoxic agents for cancer treatment Expert Opin Investig Drugs 2006, 15(8):933-946 10.1517/13543784.15.8.933 16859395
13. 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(2):151-160 10901303
14. Cruciani RA Barker JL Durell SR Raghunathan G Guy HR Zasloff M Stanley EF Magainin 2, a natural antibiotic from frog skin, forms ion channels in lipid bilayer membranes Eur J Pharmacol 1992, 226(4):287-296 10.1016/ 0922-4106(92)90045-W 1383011
15. Ohsaki Y Gazdar AF Chen HC Johnson BE Antitumor activity of magainin analogues against human lung cancer cell lines Cancer Res 1992, 52(13):3534-3538 1319823
16. Kim S Kim SS Bang YJ Kim SJ Lee BJ In vitro activities of native and designed peptide antibiotics against drug sensitive and resistant tumor cell lines Peptides 2003, 24(7):945-953 10.1016/S0196-9781(03)00194-3 14499271
17. Matsuzaki K Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes Biochim Biophys Acta 1999, 1462(1-2):1-10 10590299
18. Pouny Y Shai Y Interaction of D-amino acid incorporated analogues of pardaxin with membranes Biochemistry 1992, 31(39):9482-9490 10.1021/ bi00154a022 1390731
19. Oren Z Shai Y Mode of action of linear amphipathic alpha-helical antimicrobial peptides Biopolymers 1998, 47(6):451-463 10.1002/ (SICI)1097-0282(1998)47:6<451::AID-BIP4>3.0.CO;2-F 10333737
20. Ellerby HM Arap W Ellerby LM Kain R Andrusiak R Rio GD Krajewski S Lombardo CR Rao R Ruoslahti E et al Anti-cancer activity of targeted pro-apoptotic peptides Nat Med 1999, 5(9):1032-1038 10.1038/12469 10470080
21. Yeaman MR Yount NY Mechanisms of antimicrobial peptide action and resistance Pharmacol Rev 2003, 55(1):27-55 10.1124/pr.55.1.2 12615953
22. 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(11):3062-3066 2032247
23. Bucana CD Hoyer LC Schroit AJ Kleinerman E Fidler IJ Ultrastructural studies of the interaction between liposome-activated human blood monocytes and allogeneic tumor cells in vitro Am J Pathol 1983, 112(1):101-111 1916313 6859224
24. Sugimura M Donato R Kakkar VV Scully MF Annexin V as a probe of the contribution of anionic phospholipids to the procoagulant activity of tumour cell surfaces Blood Coagul Fibrinolysis 1994, 5(3):365-373 8075308
25. Rao LV Tait JF Hoang AD Binding of annexin V to a human ovarian carcinoma cell line (OC-2008). Contrasting effects on cell surface factor VIIa/tissue factor activity and prothrombinase activity Thromb Res 1992, 67(5):517-531 10.1016/0049-3848(92)90013-Z 1448786
26. Kim YJ Varki A Perspectives on the significance of altered glycosylation of glycoproteins in cancer Glycoconj J 1997, 14(5):569-576 10.1023/ A:1018580324971 9298689
27. Dube DH Bertozzi CR Glycans in cancer and inflammation - potential for therapeutics and diagnostics Nat Rev Drug Discov 2005, 4(6):477-488 10.1038/nrd1751 15931257
28. Kjellen L Lindahl U Proteoglycans: Structures and interactions Annu Rev Biochem 1991, 60:443-475 10.1146/annurev.bi.60.070191.002303 1883201
29. Sugahara K Mikami T Uyama T Mizuguchi S Nomura K Kitagawa H Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate Curr Opin Struct Biol 2003, 13(5):612-620 10.1016/ j.sbi.2003.09.011 14568617
30. Tkachenko E Rhodes JM Simons M Syndecans: New kids on the signaling block Circ Res 2005, 96(5):488-500 10.1161/01.RES.0000159708.71142.c8 15774861
31. Rabenstein DL Heparin and heparan sulfate: Structure and function Nat Prod Rep 2002, 19(3):312-331 10.1039/b100916h 12137280
32. Zsila F Gedeon G Binding of anti-prion agents to glycosaminoglycans: evidence from electronic absorption and circular dichroism spectroscopy Biochem Biophys Res Commun 2006, 346(4):1267-1274 10.1016/ j.bbrc.2006.06.033 16793017
33. Kleeff J Ishiwata T Kumbasar A Friess H Buchler MW Lander AD Korc M The cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer J Clin Invest 1998 102 9 1662 1673 509114 9802880 10.1172/JCI4105
34. Matsuda K Maruyama H Guo F Kleeff J Itakura J Matsumoto Y Lander AD Korc M Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells Cancer Res 2001, 61(14):5562-5569 11454708
35. Sanderson RD Heparan sulfate proteoglycans in invasion and metastasis Semin Cell Dev Biol 2001, 12(2):89-98 10.1006/scdb.2000.0241 11292374
36. Jayson GC Lyon M Paraskeva C Turnbull JE Deakin JA Gallagher JT Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro J Biol Chem 1998, 273(1):51-57 10.1074/jbc.273.1.51 9417046
37. Safaiyan F Lindahl U Salmivirta M Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells Eur J Biochem 1998, 252(3):576-582 10.1046/j.1432-1327.1998.2520576.x 9546676
38. 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(4):612-624 10.1158/1535-7163.MCT-04-0077 15827335
39. 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, 443:285-291 9781371
40. Jenssen H Andersen JH Uhlin-Hansen L Gutteberg TJ Rekdal O Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate Antiviral Res 2004, 61(2):101-109 10.1016/ j.antiviral.2003.09.001 14670583
41. Esko JD Stewart TE Taylor WH Animal cell mutants defective in glycosaminoglycan biosynthesis Proc Natl Acad Sci USA 1985, 82(10):3197-3201 397742 3858816 10.1073/pnas.82.10.3197
42. Bai X Wei G Sinha A Esko JD Chinese hamster ovary cell mutants defective in glycosaminoglycan assembly and glucuronosyltransferase I J Biol Chem 1999, 274(19):13017-13024 10.1074/jbc.274.19.13017 10224052
43. Eliassen LT Haug BE Berge G Rekdal O Enhanced antitumour activity of 15-residue bovine lactoferricin derivatives containing bulky aromatic amino acids and lipophilic N-terminal modifications J Pept Sci 2003, 9(8):510-517 10.1002/psc.472 12952392
44. Keller KM Brauer PR Keller JM Modulation of cell surface heparan sulfate structure by growth of cells in the presence of chlorate Biochemistry 1989, 28(20):8100-8107 10.1021/bi00446a021 2532538
45. Yanagishita M Hascall VC Proteoglycans synthesized by rat ovarian granulosa cells in culture. Isolation, fractionation, and characterization of proteoglycans associated with the cell layer J Biol Chem 1984, 259(16):10260-10269 6469964
46. Shively JE Conrad HE Formation of anhydrosugars in the chemical depolymerization of heparin Biochemistry 1976, 15(18):3932-3942 10.1021/ bi00663a005 9127
47. Greve H Cully Z Blumberg P Kresse H Influence of chlorate on proteoglycan biosynthesis by cultured human fibroblasts J Biol Chem 1988, 263(26):12886-12892 3417641
48. Uhlin-Hansen L Yanagishita M Differential effect of brefeldin A on the biosynthesis of heparan sulfate and chondroitin/dermatan sulfate proteoglycans in rat ovarian granulosa cells in culture J Biol Chem 1993, 268(23):17370-17376 8349620
49. Stringer SE Gallagher JT Heparan sulphate Int J Biochem Cell Biol 1997, 29(5):709-714 10.1016/S1357-2725(96)00170-7 9251237
50. Risso A Zanetti M Gennaro R Cytotoxicity and apoptosis mediated by two peptides of innate immunity Cell Immunol 1998, 189(2):107-115 10.1006/ cimm.1998.1358 9790724
51. Schroder-Borm H Bakalova R Andra J The NK-lysin derived peptide NK-2 preferentially kills cancer cells with increased surface levels of negatively charged phosphatidylserine FEBS Lett 2005, 579(27):6128-6134 10.1016/j.febslet.2005.09.084 16269280
52. Klaassen CD Boles JW Sulfation and sulfotransferases 5: The importance of 3'-phosphoadenosine 5'-phosphosulfate (PAPS) in the regulation of sulfation Faseb J 1997, 11(6):404-418 9194521
53. Safaiyan F Kolset SO Prydz K Gottfridsson E Lindahl U Salmivirta M Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate J Biol Chem 1999, 274(51):36267-36273 10.1074/ jbc.274.51.36267 10593915
54. Zhang L Lawrence R Frazier BA Esko JD CHO glycosylation mutants: proteoglycans Methods Enzymol 2006, 416:205-221 10.1016/ S0076-6879(06)16013-9 17113868
55. Smetsers TF Westerlo van de EM ten Dam GB Overes IM Schalkwijk J van Muijen GN van Kuppevelt TH Human single-chain antibodies reactive with native chondroitin sulfate detect chondroitin sulfate alterations in melanoma and psoriasis J Invest Dermatol 2004, 122(3):707-716 10.1111/ j.0022-202X.2004.22316.x 15086557
56. Molist A Romaris M Lindahl U Villena J Touab M Bassols A Changes in glycosaminoglycan structure and composition of the main heparan sulphate proteoglycan from human colon carcinoma cells (perlecan) during cell differentiation Eur J Biochem 1998, 254(2):371-377 10.1046/ j.1432-1327.1998.2540371.x 9660193
57. Guibinga GH Miyanohara A Esko JD Friedmann T Cell surface heparan sulfate is a receptor for attachment of envelope protein-free retrovirus-like particles and VSV-G pseudotyped MLV-derived retrovirus vectors to target cells Mol Ther 2002, 5(5 Pt 1):538-546 10.1006/ mthe.2002.0578 11991744
58. Ueda M Matsumoto S Hayashi S Kobayashi N Noguchi H Cell surface heparan sulfate proteoglycans mediate the internalization of PDX-1 protein Cell Transplant 2008, 17(1-2):91-97 10.3727/000000008783906892 18468239
59. Bernfield M Kokenyesi R Kato M Hinkes MT Spring J Gallo RL Lose EJ Biology of the syndecans: A family of transmembrane heparan sulfate proteoglycans Annu Rev Cell Biol 1992, 8:365-393 10.1146/ annurev.cb.08.110192.002053 1335744
60. Fransson LA Glypicans Int J Biochem Cell Biol 2003, 35(2):125-129 10.1016/S1357-2725(02)00095-X 12479862
61. Tumova S Woods A Couchman JR Heparan sulfate proteoglycans on the cell surface: Versatile coordinators of cellular functions Int J Biochem Cell Biol 2000, 32(3):269-288 10.1016/S1357-2725(99)00116-8 10716625
62. Rees SG Hughes W Embery G Interaction of glucuronic acid and iduronic acid-rich glycosaminoglycans and their modified forms with hydroxyapatite Biomaterials 2002, 23(2):481-489 10.1016/ S0142-9612(01)00130-2 11761169
63. Schmidtchen A Frick IM Andersson E Tapper H Bjorck L Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37 Mol Microbiol 2002, 46(1):157-168 10.1046/ j.1365-2958.2002.03146.x 12366839
64. Baranska-Rybak W Sonesson A Nowicki R Schmidtchen A Glycosaminoglycans inhibit the antibacterial activity of LL-37 in biological fluids J Antimicrob Chemother 2006, 57(2):260-265 10.1093/jac/dki460 16387752
65. Schmidtchen A Frick IM Bjorck L Dermatan sulphate is released by proteinases of common pathogenic bacteria and inactivates antibacterial alpha-defensin Mol Microbiol 2001, 39(3):708-713 10.1046/ j.1365-2958.2001.02251.x 11169110
66. Jenssen H Andersen JH Mantzilas D Gutteberg TJ A wide range of medium-sized, highly cationic, alpha-helical peptides show antiviral activity against herpes simplex virus Antiviral Res 2004, 64(2):119-126 15498607
67. Andersen JH Jenssen H Sandvik K Gutteberg TJ Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface J Med Virol 2004, 74(2):262-271 10.1002/ jmv.20171 15332275
68. Roseanu A Chelu F Trif M Motas C Brock JH Inhibition of binding of lactoferrin to the human promonocyte cell line THP-1 by heparin: The role of cell surface sulphated molecules Biochim Biophys Acta 2000, 1475(1):35-38 10806335
69. Ashikari-Hada S Habuchi H Kariya Y Itoh N Reddi AH Kimata K Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library J Biol Chem 2004, 279(13):12346-12354 10.1074/jbc.M313523200 14707131
70. Yuguchi Y Kominato R Ban T Urakawa H Kajiwara K Takano R Kamei K Hara S Structural observation of complexes of FGF-2 and regioselectively desulfated heparin in aqueous solutions Int J Biol Macromol 2005, 35(1-2):19-25 10.1016/j.ijbiomac.2004.11.003 15769511
71. Kusche M Torri G Casu B Lindahl U Biosynthesis of heparin. Availability of glucosaminyl 3-O-sulfation sites J Biol Chem 1990, 265(13):7292-7300 2332430
72. Mahalingam Y Gallagher JT Couchman JR Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties J Biol Chem 2007, 282(5):3221-3230 10.1074/ jbc.M604938200 17130131
73. Rintala M Inki P Klemi P Jalkanen M Grenman S Association of syndecan-1 with tumor grade and histology in primary invasive cervical carcinoma Gynecol Oncol 1999, 75(3):372-378 10.1006/gyno.1999.5595 10600292
74. Harada K Masuda S Hirano M Nakanuma Y Reduced expression of syndecan-1 correlates with histologic dedifferentiation, lymph node metastasis, and poor prognosis in intrahepatic cholangiocarcinoma Human Pathology 2003, 34(9):857-863 10.1016/S0046-8177(03)00336-8 14562280
75. Kurokawa H Zhang M Matsumoto S Yamashita Y Tanaka T Takamori K Igawa K Yoshida M Fukuyama H Takahashi T et al Reduced syndecan-1 expression is correlated with the histological grade of malignancy at the deep invasive front in oral squamous cell carcinoma J Oral pathol Med 2006, 35(5):301-306 10.1111/j.1600-0714.2006.00412.x 16630294
76. Bame K Heparanase: Endoglycosidases that degrade heparan sulfate proteoglycans Glycobiology 2001, 11(6):91-98 10.1093/glycob/11.6.91R
77. Ilan N Elkin M Vlodavsky I Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis Int J Biochem Cell Biol 2006, 38(12):2018-2039 10.1016/j.biocel.2006.06.004 16901744