Improving drug penetrability with iRGD leverages the therapeutic response to sorafenib and doxorubicin in hepatocellular carcinoma

Cancer Research

Volumn 75, Issue 15, 2015, Pages 3147-3154

  Schmithals, Christian ^a   Köberle, Verena ^a   Korkusuz, Hüdayi ^a   Pleli, Thomas ^a   Kakoschky, Bianca ^a   Augusto, Eduardo Alonso ^a   Ibrahim, Ahmed Atef ^a,b   Arencibia, Jose M ^a   Vafaizadeh, Vida ^c   Groner, Bernd ^c   Korf, Horst Werner ^a   Kronenberger, Bernd ^a   Zeuzem, Stefan ^a   Vogl, Thomas J ^a   Waidmann, Oliver ^a   Piiper, Albrecht ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b NATIONAL RESEARCH CENTRE   (Egypt)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; DOXORUBICIN; GADOLINIUM PENTETATE; PEPTIDE IRGD; SORAFENIB; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; EVANS BLUE; N-END CYSTEINE PEPTIDE TUMOR-HOMING PEPTIDE; NICOTINAMIDE; OLIGOPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BYSTANDER EFFECT; CANCER INHIBITION; CANCER TISSUE; CONTROLLED STUDY; DRUG EFFICACY; DRUG PENETRATION; DRUG POTENTIATION; DRUG RESPONSE; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOMA, HEPATOCELLULAR; CHEMISTRY; DIAGNOSTIC USE; DRUG DELIVERY SYSTEM; DRUG EFFECTS; HEPG2 CELL LINE; INTRAVENOUS DRUG ADMINISTRATION; LIVER NEOPLASMS; NUDE MOUSE; PROTEIN MOTIF; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

ADMINISTRATION, INTRAVENOUS; AMINO ACID MOTIFS; ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, HEPATOCELLULAR; DOXORUBICIN; DRUG DELIVERY SYSTEMS; EVANS BLUE; GADOLINIUM DTPA; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; MALE; MICE, NUDE; MICE, TRANSGENIC; NIACINAMIDE; OLIGOPEPTIDES; PHENYLUREA COMPOUNDS; TISSUE DISTRIBUTION;

EID: 84942894500     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0395     Document Type: Article

References (30)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Hernandez-Gea V, Toffanin S, Friedman SL, Llovet JM. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology 2013;144:512-27.
3. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. SHARP Investigators Study Group. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
4. Sugahara KN, Teesalu T, Karmali PP, Kotamraju VR, Agemy L, Girard OM, et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 2009;16:510-20.
5. Sugahara KN, Teesalu T, Karmali PP, Kotamraju VR, Agemy L, Greenwald DR, et al. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 2010;328:1031-5.
6. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010;10:9-22.
7. Ruoslahti E. Specialization of tumour vasculature. Nat Rev Cancer 2002;2:83-99.
8. Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci USA 2009;106:16157-62.
9. Teesalu T, Sugahara KN, Ruoslahti E. Tumor-penetrating peptides. Front Oncol 2013;3:216.
10. Sugahara KN, Braun GB, de Mendoza TH, Kotamraju VR, French RP, Lowy AM, et al. Tumor-penetrating iRGD peptide inhibits metastasis. Mol Cancer Ther 2015;14:120-8.
11. Pang HB, Braun GB, Friman T, Aza-Blanc P, Ruidiaz ME, Sugahara KN, et al. An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability. Nat Commun 2014;5:4904.
12. Puig-Saus C, Rojas LA, Laborda E, Figueras A, Alba R, Fillat C, et al. iRGD tumor-penetrating peptide-modified oncolytic adenovirus shows enhanced tumor transduction, intratumoral dissemination and antitumor efficacy. Gene Ther 2014;21:767-74.
13. Zhu Z, Xie C, Liu Q, Zhen X, Zheng X, Wu W, et al. The effect of hydrophilic chain length and iRGD on drug delivery from poly(e-caprolactone)-poly (N-vinylpyrrolidone) nanoparticles. Biomaterials 2011;32:9525-35.
14. Akashi Y, Oda T, Ohara Y, Miyamoto R, Kurokawa T, Hashimoto S, et al. Anticancer effects of gemcitabine are enhanced by co-administered iRGD peptide in murine pancreatic cancer models that overexpressed neuropilin-1. Br J Cancer 2014;110:1481-7.
15. Kadonosono T, Yamano A, Goto T, Niibori M, Kuchimaru T, Kizaka- Kondoh S. Cell penetrating peptides improve tumor delivery of cargos through neuropilin-1-dependent extravasation. J Control Release 2015; 201C:14-21.
16. Murakami H, Sanderson ND, Nagy P, Marino PA, Merlino G, Thorgeirsson SS. Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: interaction of c-myc and transforming growth factor a in hepatic oncogenesis. Cancer Res 1993;53:1719-23.
17. Haupenthal J, Bihrer V, Korkusuz H, Kollmar O, Schmithals C, Kriener S, et al. Reduced efficacy of the Plk1 inhibitor BI 2536 on the progression of hepatocellular carcinoma due to low intratumoral drug levels. Neoplasia 2012;14:410-9.
18. Watcharin W, Schmithals C, Pleli T, Köberle V, Korkusuz H, Hübner F, et al. Detection of hepatocellular carcinoma in transgenic mice by Gd-DTPAand rhodamine 123-conjugated human serum albumin nanoparticles in T1 magnetic resonance imaging. J Control Release 2015;199:63-71.
19. Korkusuz H, Ulbrich K, Welzel K, Koeberle V, Watcharin W, Bahr U, et al. Transferrin-coated gadolinium nanoparticles as MRI contrast agent. Mol Imaging Biol 2013;15:148-54.
20. Yau T, Chan P, Epstein R, Poon RT. Management of advanced hepatocellular carcinoma in the era of targeted therapy. Liver Int 2009;29:10-17.
21. Asghar U, Meyer T. Are there opportunities for chemotherapy in the treatment of hepatocellular cancer? J Hepatol 2012;56:686-95.
22. Ruoslahti E, Bhatia SN, Sailor MJ. Targeting of drugs and nanoparticles to tumors. J Cell Biol 2010;188:759-68.
23. Chauhan VP, Jain RK. Strategies for advancing cancer nanomedicine. Nat Mater 2013;12:958-62.
24. Chen R, Braun GB, Luo X, Sugahara KN, Teesalu T, Ruoslahti E. Application of a proapoptotic peptide to intratumorally spreading cancer therapy. Cancer Res 2013;73:1352-61.
25. Pellet-Many C, Frankel P, Jia H, Zachary I. Neuropilins: structure, function and role in disease. Biochem J 2008;411:211-26.
26. Nejjari M, Hafdi Z, Gouysse G, Fiorentino M, B-eatrix O, Dumortier J, et al. Expression, regulation, and function of alpha V integrins in hepatocellular carcinoma: an in vivo and in vitro study. Hepatology 2002;36:418-26.
27. Berg-e M, Allanic D, Bonnin P, de Montrion C, Richard J, Suc M, et al. Neuropilin-1 is upregulated in hepatocellular carcinoma and contributes to tumour growth and vascular remodelling. J Hepatol 2011;55: 866-75.
28. Edwards S, Lalor PF, Tuncer C, Adams DH. Vitronectin in human hepatic tumours contributes to the recruitment of lymphocytes in an avb3-independent manner. Br J Cancer 2006;95:1545-54.
29. Dong YW, Wang R, Cai QQ, Qi B, Wu W, Zhang YH, et al. Sulfatide epigenetically regulates miR-223 and promotes the migration of human hepatocellular carcinoma cells. J Hepatol 2014;60:792-801.
30. Pang HB, Braun GB, She ZG, Kotamraju VR, Sugahara KN, Teesalu T, et al. A free cysteine prolongs the half-life of a homing peptide and improves its tumor-penetrating activity. J Control Release 2014;175:48-53.