Vascular-homing peptides for targeted drug delivery and molecular imaging: Meeting the clinical challenges

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1846, Issue 1, 2014, Pages 1-12

  D'Onofrio, Nunzia ^a   Caraglia, Michele ^a   Grimaldi, Anna ^a   Marfella, Raffaele ^a   Servillo, Luigi ^a   Paolisso, Giuseppe ^a   Balestrieri, Maria Luisa ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Cancer; Endothelium; Peptides; Phage display

Indexed keywords

CANCER; ENDOTHELIUM; PEPTIDES; PHAGE DISPLAY;

ANGIOGENESIS INHIBITORS; ANIMALS; DRUG DELIVERY SYSTEMS; DRUG DISCOVERY; ENDOTHELIUM, VASCULAR; HUMANS; MOLECULAR IMAGING; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PEPTIDE LIBRARY; PEPTIDES;

ALPHAVBETA5 INTEGRIN; AMYLOID PRECURSOR PROTEIN; ARGINYLGLYCYLASPARTIC ACID; ASPARAGINYLGLYCINYLARGININE; CAPECITABINE; CETUXIMAB; CILENGITIDE; DOXORUBICIN; EPHRIN A4; EPHRIN A5; EPHRIN B2; FIBROBLAST GROWTH FACTOR 8; FLUOROURACIL; GANCICLOVIR; GELATINASE A; INTERLEUKIN 11 RECEPTOR; LIPOSOME; MELPHALAN; MICROSOMAL AMINOPEPTIDASE; NANOPARTICLE; OXALIPLATIN; PACLITAXEL; PEMETREXED; PROHIBITIN; TEMOZOLOMIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR TARGETING AGENT; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BIOPANNING; BLOOD VESSEL; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER SURVIVAL; CELL ADHESION; CELL HOMING; CELL PROLIFERATION; COLORECTAL CANCER; DRUG DELIVERY SYSTEM; DRUG RECEPTOR BINDING; DRUG SCREENING; DRUG TOLERABILITY; ENDOTHELIUM CELL; GLIOBLASTOMA; HEAD AND NECK CARCINOMA; HUMAN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER CANCER; LOW DRUG DOSE; MALIGNANT NEOPLASTIC DISEASE; MASS SPECTROMETRY; MELANOMA; METASTATIC COLORECTAL CANCER; MOLECULAR IMAGING; NON SMALL CELL LUNG CANCER; NONHUMAN; OVARY CANCER; PHAGE DISPLAY; PHAGEMID; PLEURA MESOTHELIOMA; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TARGETING; RESTRICTION MAPPING; RESTRICTION SITE; REVIEW; SOLID TUMOR; SQUAMOUS CELL CARCINOMA; TUMOR VASCULARIZATION;

EID: 84898968794     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2014.03.004     Document Type: Review

References (122)

1. Trepel M., Pasqualini R., Arap W. Screening phage-display peptide libraries for vascular targeted peptides. Methods Enzymol. 2008, 445:83-106.
2. Laakkonen P., Zhang L., Ruoslahti E. Peptide targeting of tumor lymph vessels. Ann. N. Y. Acad. Sci. 2008, 1131:37-43.
3. de Nigris F., Balestrieri M.L., Napoli C. Targeting c-Myc, Ras and IGF cascade to treat cancer and vascular disorders. Cell Cycle 2006, 5:1621-1628.
4. Johannessen T.C., Wagner M., Straume O., Bjerkvig R., Eikesdal H.P. Tumor vasculature: the Achilles' heel of cancer?. Expert Opin. Ther. Targets 2013, 7:7-20.
5. Balestrieri M.L., Napoli C. Novel challenges in exploring peptide ligands and corresponding tissue-specific endothelial receptors. Eur. J. Cancer 2007, 43:1242-1250.
6. Pasqualini R., Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature 1996, 380:364-366.
7. Bábíčková J., Tóthová L., Boor P., Celec P. In vivo phage display - a discovery tool in molecular biomedicine. Biotechnol. Adv. 2013, 31:1247-1259.
8. Nicol C.G., Denby L., Lopez-Franco O., Masson R., Halliday C.A., Nicklin S.A., Kritz A., Work L.M., Baker A.H. Use of in vivo phage display to engineer novel adenoviruses for targeted delivery to the cardiac vasculature. FEBS Lett. 2009, 583:2100-2107.
9. Ueberberg S., Schneider S. Phage library-screening: a powerful approach for generation of targeting-agents specific for normal pancreatic islet-cells and islet-cell carcinoma in vivo. Regul. Pept. 2010, 160:1-8.
10. Bratkovic T. Progress in phage display: evolution of the technique and its applications. Cell. Mol. Life Sci. 2010, 67:749-767.
11. Molek P., Strukelj B., Bratkovic T. Peptide phage display as a tool for drug discovery: targeting membrane receptors. Molecules 2011, 16:857-887.
12. Pavoni E., Vaccaro P., D'Alessio V., De Santis R., Minenkova O. Simultaneous display of two large proteins on the head and tail of bacteriophage lambda. BMC Biotechnol. Sep 30 2013, 13:79. 10.1186/1472-6750-13-79.
13. Qi H., Lu H., Qiu H.J., Petrenko V., Liu A. Phagemid vectors for phage display: properties, characteristics and construction. J. Mol. Biol. 2012, 3417:129-143.
14. Hust M., Frenzel A., Meyer T., Schirrmann T., Dubel S. Construction of human naive antibody gene libraries. Methods Mol. Biol. 2012, 907:85-107.
15. Newton J.R., Kelly K.A., Mahmood U., Weissleder R., Deutscher S.L. In vivo selection of phage for the optical Imaging of PC-3 human prostate carcinoma in mice. Neoplasia 2006, 8:772-780.
16. Akita N., Maruta F., Seymour L.W., Kerr D.J., Parker A.L., Asai T., Oku N., Nakayama J., Miyagawa S. Identification of oligopeptides binding to peritoneal tumors of gastric cancer. Cancer Sci. 2006, 97:1075-1081.
17. Bussolati B., Grange C., Tei L., Deregibus M.C., Ercolani M., Aime S., Camussi G. Targeting of human renal tumor-derived endothelial cells with peptides obtained by phage display. J. Mol. Med. (Berl.) 2007, 85:897-906.
18. Arap W., Pasqualini R., Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 1998, 279:377-380.
19. Jia W.D., Sun H.C., Zhang J.B., Xu Y., Qian Y.B., Pang J.Z., Wang L., Qin L.X., Liu Y.K., Tang Z.Y. A novel peptide that selectively binds highly metastatic hepatocellular carcinoma cell surface is related to invasion and metastasis. Cancer Lett. 2007, 247:234-242.
20. Arap W., Kolonin M.G., Trepel M., Lahdenranta J., Cardò-Villa M., Giordano R.J., Mintz P.J., Ardelt P.U., Yao V.J., Vidal C.I., Chen L., Flamm A., Valtanen H., Weavind L.M., Hicks M.E., Pollock R.E., Botz G.H., Bucana C.D., Koivunen E., Cahill D., Troncoso P., Baggerly K.A., Pentz R.D., Do K.A., Logothetis C.J., Pasqualini R. Steps toward mapping the human vasculature by phage display. Nat. Med. 2002, 8:121-127.
21. Arap W., Pasqualini R. The human vascular mapping project. Selection and utilization of molecules for tumor endothelial targeting. Haemostasis 2001, 31:30-31.
22. Castel G., Chtéoui M., Heyd B., Tordo N. Phage display of combinatorial peptide libraries: application to antiviral research. Molecules 2011, 16:3499-3518.
23. Zurita A.J., Troncoso P., Cardo-Vila M., Logothetis C.J., Pasqualini R., Arap W. Combinatorial screenings in patients: the interleukin-11 receptor alpha as a candidate target in the progression of human prostate cancer. Cancer Res. 2004, 64:435-439.
24. Sugahara K.N., Teesalu T., Karmali P.P., Kotamraju V.R., Agemy L., Girard O.M., Hanahan D., Mattrey R.F., Ruoslahti E. Tissue penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 2009, 16:510-520.
25. Pasqualini R., Koivunen E., Ruoslahti E. Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat. Biotechnol. 1997, 15:542-546.
26. Curnis F., Sacchi A., Borgna L., Magni F., Gasparri A., Corti A. Enhancement of tumor necrosis factor a antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat. Biotechnol. 2000, 18:1185-1190.
27. Soudy R., Ahmed S., Kaur K. NGR peptide ligands for targeting CD13/APN identified through peptide array screening resemble fibronectin sequences. ACS Comb. Sci. 2012, 14:590-599.
28. Dechantsreiter M.A., Planker E., Mathä B., Lohof E., Hölzemann G., Jonczyk A., Goodman S.L., Kessler H. N-Methylated cyclic RGD peptides as highly active and selective alpha(V)beta(3) integrin antagonists. J. Med. Chem. 1999, 42:3033-3040.
29. Belvisi L., Riccioni T., Marcellini M., Vesci L., Chiarucci I., Efrati D., Potenza D., Scolastico C., Manzoni L., Lombardo K., Stasi M.A., Orlandi A., Ciucci A., Nico B., Ribatti D., Giannini G., Presta M., Carminati P., Pisano C. Biological and molecular properties of a new alpha(v)beta3/alpha(v)beta5 integrin antagonist. Mol. Cancer Ther. 2005, 4:1670-1680.
30. Marra M., Santini D., Meo G., Vincenzi B., Zappavigna S., Baldi A., Rosolowski M., Tonini G., Loeffler M., Lupu R., Addeo S.R., Abbruzzese A., Budillon A., Caraglia M. Cyr61 downmodulation potentiates the anticancer effects of zoledronic acid in androgen-independent prostate cancer cells. Int. J. Cancer 2009, 125:2004-2013.
31. Menendez J.A., Vellon L., Mehmi I., Teng P.K., Griggs D.W., Lupu R. A novel CYR61-triggered 'CYR61-alphavbeta3 integrin loop' regulates breast cancer cell survival and chemosensitivity through activation of ERK1/ERK2 MAPK signaling pathway. Oncogene 2005, 24:761-779.
32. Kimball K.J., Preuss M.A., Barnes M.N., Wang M., Siegal G.P., Wan W., Kuo H., Saddekni S., Stockard C.R., Grizzle W.E., Harris R.D., Aurigemma R., Curiel D.T., Alvarez R.D. A phase I study of a tropism-modified conditionally replicative adenovirus for recurrent malignant gynecologic diseases. Clin. Cancer Res. 2010, 16:5277-5287.
33. Laverman P., Sosabowski J.K., Boerman O.C., Oyen W.J. Radiolabelled peptides for oncological diagnosis. Eur. J. Nucl. Med. Mol. Imaging 2012, 39:S78-S92.
34. Scaringi C., Enrici R.M., Minniti G. Combining molecular targeted agents with radiation therapy for malignant gliomas. Onco Targets Ther. 2013, 6:1079-1095.
35. Ning S., Chen Z., Dirks A., Husbeck B., Hsu M., Bedogni B., O'Neill M., Powell M.B., Knox S.J. Targeting integrins and PI3K/Akt-mediated signal transduction pathways enhances radiation-induced anti-angiogenesis. Radiat. Res. 2007, 168:125-133.
36. Abdollahi A., Griggs D.W., Zieher H., Roth A., Lipson K.E., Saffrich R., Gröne H.J., Hallahan D.E., Reisfeld R.A., Debus J., Niethammer A.G., Huber P.E. Inhibition of alpha(v)beta3 integrin survival signaling enhances antiangiogenic and antitumor effects of radiotherapy. Clin. Cancer Res. 2005, 11:6270-6279.
37. Domingo-Espin J., Petegnief V., de Vera N., Conchillo-Solé O., Saccardo P., Unzueta U., Vazquez E., Cedano J., Negro L., Daura X., Peluffo H., Planas A.M., Villaverde A., Ferrer-Miralles N. RGD-based cell ligands for cell-targeted drug delivery act as potent trophic factors. Nanomedicine 2012, 8:1263-1266.
38. Koivunen E., Wang B., Ruoslahti E. Isolation of a highly specific ligand for the alpha 5 beta 1 integrin from a phage display library. J. Cell Biol. 1994, 124:373-380.
39. Larsen C.C., Kligman F., Tang C., Kottke-Marchant K., Marchant R.E. A biomimetic peptide fluorosurfactant polymer for endothelialization of ePTFE with limited platelet adhesion. Biomaterials 2007, 28:3537-3548.
40. Meyers S.R., Kenan D.J., Khoo X., Grinstaff M.W. Bioactive stent surface coating that promotes endothelialization while preventing platelet adhesion. Biomacromolecules 2011, 12:533-539.
41. Dudash L.A., Kligman F.L., Bastijanic J.M., Kottke-Marchant K., Marchant R.E. Cross-reactivity of cell-selective CRRETAWAC peptide with human and porcine endothelial cells. J. Biomed. Mater. Res. A Sep 30 2013, 10.1002/jbm.a.34960.
42. Koivunen E., Ranta T.M., Annila A., Taube S., Uppala A., Jokinen M., van Willigen G., Ihanus E., Gahmberg C.G. Inhibition of beta(2) integrin-mediated leukocyte cell adhesion by leucine-leucine-glycine motif-containing peptides. J. Cell Biol. 2001, 153:905-916.
43. Stefanidakis M., Bjorklund M., Ihanus E., Gahmberg C.G., Koivunen E. Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins. J. Biol. Chem. 2003, 278:34674-34684.
44. Suojanen J., Reunanen J., Ranta T.M., Peñate-Medina O., Salo T., Saris P., Sorsa T. Peptides against mac-1 do not sufficiently target leukemia or lymphoma in vivo. Anticancer Res. 2014, 34:645-650.
45. Corti A., Curnis F. Tumor vasculature targeting through NGR peptide-based drug delivery systems. Curr. Pharm. Biotechnol. 2011, 12:1128-1134.
46. Jiang W., Jin G., Ma D., Wang F., Fu T., Chen X., Jia K., Marikar F.M., Hua Z. Modification of cyclic NGR tumor neovasculature-homing motif sequence to human plasminogen kringle 5 improves inhibition of tumor growth. PLoS One 2012, 7:e37132.
47. Faintuch B.L., Oliveira E.A., Targino R.C., Moro A.M. Radiolabeled NGR phage display peptide sequence for tumor targeting. Appl. Radiat. Isot. 2014, 86:41-45.
48. Cardo-Vila M., Zurita A.J., Giordano R.J., Sun J., Rangel R., Guzman-Rojas L., Anobom C.D., Valente A.P., Almeida F.C., Lahdenranta J., Kolonin M.G., Arap W., Pasqualini R. A ligand peptide motif selected from a cancer patient is a receptor-interacting site within human interleukin- 11. PLoS One 2008, 3:e3452.
49. Qinghua W., Jianli X., Lu L., Zexuan Y., Guansheng T., Hailin G., Jianwei J. A radiolabeled nonapeptide probe targeting PC-3 cells and bone metastases of prostate cancer in mice. Contrast Media Mol. Imaging 2012, 7:223-230.
50. Staquicini F.I., Cardó-Vila M., Kolonin M.G., Trepel M., Edwards J.K., Nunes D.N., Sergeeva A., Efstathiou E., Sun J., Almeida N.F., Tu S.M., Botz G.H., Wallace M.J., O'Connell D.J., Krajewski S., Gershenwald J.E., Molldrem J.J., Flamm A.L., Koivunen E., Pentz R.D., Dias-Neto E., Setubal J.C., Cahill D.J., Troncoso P., Do K.A., Logothetis C.J., Sidman R.L., Pasqualini R., Arap W. Vascular ligand-receptor mapping by direct combinatorial selection in cancer patients. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18637-18642.
51. Krag D.N., Shukla G.S., Shen G.P., Pero S., Ashikaga T., Fuller S., Weaver D.L., Burdette-Radoux S., Thomas C. Selection of tumor binding ligands in cancer patients with phage display libraries. Cancer Res. 2006, 66:7724-7733.
52. Dienst A., Grunow A., Unruh M., Rabausch B., Nor J.E., Fries J.W., Gottstein C. Specific occlusion of murine and human tumor vasculature by VCAM-1-targeted recombinant fusion proteins. J. Natl. Cancer Inst. 2005, 97:733-747.
53. Kelly K.A., Allport J.R., Tsourkas A., Shinde-Patil V.R., Josephson L., Weissleder R. Detection of vascular adhesion molecule-1 expression using a novel multimodal nanoparticle. Circ. Res. 2005, 96:327-336.
54. Matsuo A.L., Tanaka A.S., Juliano M.A., Rodrigues E.G., Travassos L.R. A novel melanoma-targeting peptide screened by phage display exhibits antitumor activity. J. Mol. Med. 2010, 88:1255-1264.
55. Giordano R.J., Anobom C.D., Cardo-Vila M., Kalil J., Valente A.P., Pasqualini R., Almeida F.C., Arap W. Structural basis for the interaction of a vascular endothelial growth factor mimic peptide motif and its corresponding receptors. Chem. Biol. 2005, 12:1075-1083.
56. Hetian L., Ping A., Shumei S., Xiaoying L., Luowen H., Jian W., Lin M., Meisheng L., Junshan Y., Chengchao S. A novel peptide isolated from a phage display library inhibits tumor growth and metastasis by blocking the binding of vascular endothelial growth factor to its kinase domain receptor. J. Biol. Chem. 2002, 277:43137-43142.
57. El-Mousawi M., Tchistiakova L., Yurchenko L., Pietrzynski G., Moreno M., Stanimirovic D., Ahmad D., Alakhov V. A vascular endothelial growth factor high affinity receptor 1-specific peptide with antiangiogenic activity identified using a phage display peptide library. J. Biol. Chem. 2003, 278:46681-46691.
58. Maruta F., Parker A.L., Fisher K.D., Hallissey M.T., Ismail T., Rowlands D.C., Chandler L.A., Kerr D.J., Seymour L.W. Identification of FGF receptor-binding peptides for cancer gene therapy. Cancer Gene Ther. 2002, 9:543-552.
59. Wang W., Chen X., Li T., Li Y., Wang R., He D., Luo W., Li X., Wu X. Screening a phage display library for a novel FGF8b-binding peptide with anti-tumor effect on prostate cancer. Exp. Cell Res. 2013, 319:1156-1164.
60. Hajitou A., Pasqualini R., Arap W. Vascular Targeting: recent advances and therapeutic perspectives. Trends Cardiovasc. Med. 2006, 16:80-88.
61. Mueller J., Gaertner F.C., Blechert B., Janssen K.P., Essler M. Targeting of tumor blood vessels: a phage-displayed tumor-homing peptide specifically binds to matrix metalloproteinase-2-processed collagen IV and blocks angiogenesis in vivo. Mol. Cancer Res. 2009, 7:1078-1085.
62. Marchiò S., Lahdenranta J., Schlingemann R.O., Valdembri D., Wesseling P., Arap M.A., Hajitou A., Ozawa M.G., Trepel M., Giordano R.J., Nanus D.M., Dijkman H.B., Oosterwijk E., Sidman R.L., Cooper M.D., Bussolino F., Pasqualini R., Arap W. Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 2004, 5:151-162.
63. Burg M.A., Pasqualini R., Arap W. NG2 proteoglycan-binding peptides target tumor neovasculature. Cancer Res. 1999, 59:2869-2874.
64. Erdag B., Balcioglu K.B., Kumbasar A., Celikbicak O., Zeder-Lutz G., Altschuh D., Salih B., Baysal K. Novel short peptides isolated from phage display library inhibit vascular endothelial growth factor activity. Mol. Biotechnol. 2007, 35:51-63.
65. Raiter A., Weiss C., Bechor Z., Ben-Dor I., Battler A., Kaplan B., Hardy B. Activation of GRP78 on endothelial cell membranes by an ADAM15-derived peptide induces angiogenesis. J. Vasc. Res. 2010, 47:399-411.
66. Hoffman J.A., Giraudo E., Singh M., Zhang L., Inoue M., Porkka K., Hanahan D., Ruoslahti E. Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma. Cancer Cell 2003, 4:383-391.
67. Joyce J.A., Laakkonen P., Bernasconi M., Bergers G., Ruoslahti E., Hanahan D. Stage-specific vascular markers revealed by phage display in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 2003, 4:393-403.
68. Hajitou A. Targeted systemic gene therapy and molecular imaging of cancer contribution of the vascular-Targeted AAAVP vector. Adv. Genet. 2010, 69:65-82.
69. Kanki S., Jaalouk D.E., Lee S., Yu A.Y., Gannon J., Lee R.T. Identification of targeting peptides for ischemic myocardium by in vivo phage display. J. Mol. Cell. Cardiol. 2011, 50:841-848.
70. Lee G.Y., Kim J.H., Oh G.T., Lee B.H., Kwon I.C., Kim I.S. Molecular targeting of atherosclerotic plaques by a stabilin-2-specific peptide ligand. J. Control. Release 2011, 155:211-217.
71. Kolonin M.G., Saha P.K., Chan L., Pasqualini R., Arap W. Reversal of obesity by targeted ablation of adipose tissue. Nat. Med. 2004, 10:625-632.
72. Staquicini F.I., Ozawa M.G., Moya C.A., Driessen W.H., Barbu E.M., Nishimori H., Soghomonyan S., Flores L.G., Liang X., Paolillo V., Alauddin M.M., Basilion J.P., Furnari F.B., Bogler O., Lang F.F., Aldape K.D., Fuller G.N., Höök M., Gelovani J.G., Sidman R.L., Cavenee W.K., Pasqualini R., Arap W. Systemic combinatorial peptide selection yields a non-canonical iron-mimicry mechanism for targeting tumors in a mouse model of human glioblastoma. J. Clin. Invest. 2011, 121:161-173.
73. Yang Y., Zizheng W., Tongxin D. Mouse thymus targeted peptide isolated by in vivo phage display can inhibit bioactivity of thymus output in vivo. J. Biomol. Screen. 2008, 13:968-974.
74. Yao V.J., Ozawa M.G., Trepel M., Arap W., McDonald D.M., Pasqualini R. Targeting pancreatic islets with phage display assisted by laser pressure catapult microdissection. Am. J. Pathol. 2005, 166:625-636.
75. Koolpe M., Burgess R., Dail M., Pasquale E.B. EphB receptor-binding peptides identified by phage display enable design of an antagonist with ephrin-like affinity. J. Biol. Chem. 2005, 280:17301-17311.
76. Han X., Xu Y., Yang Y., Xi J., Tian W., Duggineni S., Huang Z., An J. Discovery and characterization of a novel cyclic peptide that effectively inhibits ephrin binding to the EphA4 receptor and displays anti-angiogenesis activity. PLoS One 2013, 8:e80183.
77. Dai X., Cai C., Xiao F., Xiong Y., Huang Y., Zhang Q., Xiang Q., Lou G., Lian M., Su Z., Zheng Q. Identification of a novel aFGF-binding peptide with anti-tumor effect on breast cancer from phage display library. Biochem. Biophys. Res. Commun. Feb 12 2014, 12. (pii: S0006-291X(14)00274-5). 10.1016/j.bbrc.2014.02.022.
78. Larimer B.M., Thomas W.D., Smith G.P., Deutscher S.L. Affinity maturation of an ERBB2-targeted SPECT imaging peptide by in vivo phage display. Mol. Imaging Biol. Feb 19 2014, 10.1007/s11307-014-0724-5.
79. Veleva A.N., Nepal D.B., Frederick C.B., Schwab J., Lockyer P., Yuan H., Lalush D.S., Patterson C. Efficient in vivo selection of a novel tumor-associated peptide from a phage display library. Molecules 2011, 16:900-914.
80. Patterson C., Frederick C.B., Yuan H., Dyer L.A., Lockyer P., Lalush D.S., Veleva A.N. Development of a new positron emission tomography tracer for targeting tumor angiogenesis: synthesis, small animal imaging, and radiation dosimetry. Molecules 2013, 18:5594-5610.
81. Fan X., Venegas R., Fey R., van der Heyde H., Bernard M.A., Lazarides E., Woods C.M. An in vivo approach to structure activity relationship analysis of peptide ligands. Pharm. Res. 2007, 24:868-879.
82. Denby L., Work L.M., Von Seggern D.J., Wu E., McVey J.H., Nicklin S.A., Baker A.H. Development of renal-targeted vectors through combined in vivo phage display and capsid engineering of adenoviral fibers from serotype 19p. Mol. Ther. 2007, 15:1647-1654.
83. Lee T.Y., Lin C.T., Kuo S.Y., Chang D.K., Wu H.C. Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery. Cancer Res. 2007, 67:10958-10965.
84. Matsuo A.L., Juliano M.A., Figueiredo C.R., Batista W.L., Tanaka A.S., Travassos L.R. A new phage-display tumor-homing peptide fused to antiangiogenic peptide generates a novel bioactive molecule with antimelanoma activity. Mol. Cancer Res. 2011, 9:1471-1478.
85. Zhi M., Wu K.C., Dong L., Hao Z.M., Deng T.Z., Hong L., Liang S.H., Zhao P.T., Qiao T.D., Wang Y., Xu X., Fan D.M. Characterization of a specific phage-displayed peptide binding to vasculature of human gastric cancer. Cancer Biol. Ther. 2004, 3:1232-1235.
86. Yang M., Liu C., Niu M., Hu Y., Guo M., Zhang J., Luo Y., Yuan W., Yang M., Yun M., Guo L., Yan J., Liu D., Liu J., Jiang Y. Phage-display library biopanning and bioinformatic analysis yielded a high-affinity peptide to inflamed vascular endothelium both in vitro and in vivo. J. Control. Release 2014, 174:72-80.
87. Ma C., Yin G., Yan D., He X., Zhang L., Wei Y., Huang Z. A novel peptide specifically targeting ovarian cancer identified by in vivo phage display. J. Pept. Sci. 2013, 19:730-736.
88. Staniszewska M., Gu X., Romano C., Kazlauskas A. A phage display-based approach to investigate abnormal neovessels of the retina. Invest. Ophthalmol. Vis. Sci. 2012, 3:4371-4379.
89. Balestrieri M.L., Fiorito C., Crimi E., Felice F., Schiano C., Milone L., Casamassimi A., Giovane A., Grimaldi V., del Giudice V., Minucci P.B., Mancini F.P., Servillo L., D'Armiento F.P., Farzati B., Napoli C. Effect of red wine antioxidants and minor polyphenolic constituents on endothelial progenitor cells after physical training in mice. Int. J. Cardiol. 2008, 126:295-297.
90. Chen B., Cao S., Zhang Y., Wang X., Liu J., Hui X., Wan Y., Du W., Wang L., Wu K., Fan D. A novel peptide (GX1) homing to gastric cancer vasculature inhibits angiogenesis and cooperates with TNF alpha in anti-tumor therapy. BMC Cell Biol. 2009, 10:63.
91. van Rooy I., Cakir-Tascioglu S., Couraud P.O., Romero I.A., Weksler B., Storm G., Hennink W.E., Schiffelers R.M., Mastrobattista E. Identification of peptide ligands for targeting to the blood-brain barrier. Pharm. Res. 2010, 27:673-682.
92. Li J., Zhang Q., Pang Z., Wang Y., Liu Q., Guo L., Jiang X. Identification of peptide sequences that target to the brain using in vivo phage display. Amino Acids 2012, 42:2373-2381.
93. Chang D.K., Chiu C.Y., Kuo S.Y., Lin W.C., Lo A., Wang Y.P., Li P.C., Wu H.C. Antiangiogenic targeting liposomes increase therapeutic efficacy for solid tumors. J. Biol. Chem. 2009, 284:12905-12916.
94. Cao Q., Liu S., Niu G., Chen K., Yan Y., Liu Z., Chen X. Phage display peptide probes for imaging early response to bevacizumab treatment. Amino Acids 2011, 41:1103-1112.
95. Loi M., Marchio S., Becherini P., Di Paolo D., Soster M., Curnis F., Brignole C., Pagnan G., Perri P., Caffa I., Longhi R., Nico B., Bussolino F., Gambini C., Ribatti D., Cilli M., Arap W., Pasqualini R., Allen T.M., Corti A., Ponzoni M., Pastorino F. Combined targeting of perivascular and endothelial tumor cells enhances anti-tumor efficacy of liposomal chemotherapy in neuroblastoma. J. Control. Release 2010, 145:66-73.
96. Liguori A., Fiorito C., Balestrieri M.L., Crimi E., Bruzzese G., Williams-Ignarro S., D'Amora M., Sommese L., Grimaldi V., Minucci P.B., Giovane A., Farzati B., Ignarro L.J., Napoli C. Functional impairment of hematopoietic progenitor cells in patients with coronary heart disease. Eur. J. Haematol. 2008, 80:258-264.
97. Greig J.A., Shirley R., Graham D., Denby L., Dominiczak A.F., Work L.M., Baker A.H. Vascular-targeting antioxidant therapy in a model of hypertension and stroke. J. Cardiovasc. Pharmacol. 2010, 56:642-650.
98. Dunehoo A.L., Anderson M., Majumdar S., Kobayashi N., Berkland C., Siahaan T.J. Cell adhesion molecules for targeted drug delivery. J. Pharm. Sci. 2006, 95:1856-1872.
99. Stupp R., Hegi M.E., Neyns B., Goldbrunner R., Schlegel U., Clement P.M., Grabenbauer G.G., Ochsenbein A.F., Simon M., Dietrich P.Y., Pietsch T., Hicking C., Tonn J.C., Diserens A.C., Pica A., Hermisson M., Krueger S., Picard M., Weller M. Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma. J. Clin. Oncol. 2010, 28:2712-2718.
100. Reardon D.A., Nabors L.B., Stupp R., Mikkelsen T. Cilengitide: an integrin-targeting arginine-glycine-aspartic acid peptide with promising activity for glioblastoma multiforme. Expert Opin. Investig. Drugs 2008, 17:1225-1235.
101. Leblond P., Dewitte A., Le Tinier F., Bal-Mahieu C., Baroncini M., Sarrazin T., Lartigau E., Lansiaux A., Meignan S. Cilengitide targets pediatric glioma and neuroblastoma cells through cell detachment and anoikis induction. Anticancer Drugs 2013, 24:818-825.
102. Lautenschlaeger T., Perry J., Peereboom D., Li B., Ibrahim A., Huebner A., Meng W., White J., Chakravarti A. In vitro study of combined cilengitide and radiation treatment in breast cancer cell lines. Radiat. Oncol. 2013, 8:246.
103. Cabarcas S.M., Sun L., Mathews L., Thomas S., Zhang X., Farrar W.L. The differentiation of pancreatic tumor-initiating cells by vitronectin can be blocked by cilengitide. Pancreas 2013, 42:861-870.
104. 18F-FDG PET and gene expression analysis. J. Cancer Res. Clin. Oncol. 2013, 139:573-583.
105. Ten Hagen T.L., Seynhaeve A.L., de Wiel-Ambagtsheer G.a., de Bruijn E.A., van Tiel S.T., Ruegg C., Meyring M., Grell M., Goodman S.L., Eggermont A.M. The αVβ3/αVβ5 integrin inhibitor cilengitide augments tumor response to melphalan isolated limb perfusion in a sarcoma model. Int. J. Cancer 2013, 132:2694-2704.
106. MacDonald T.J., Vezina G., Stewart C.F., Turner D., Pierson C.R., Chen L., Pollack I.F., Gajjar A., Kieran M.W. Phase II study of cilengitide in the treatment of refractory or relapsed high-grade gliomas in children: a report from the Children's Oncology Group. Neuro Oncol. 2013, 15:1438-1444.
107. Vermorken J.B., Guigay J., Mesia R., Trigo J.M., Keilholz U., Kerber A., Bethe U., Picard M., Brummendorf T.H. Phase I/II trial of cilengitide with cetuximab, cisplatin and 5-fluorouracil in recurrent and/or metastatic squamous cell cancer of the head and neck: findings of the phase I part. Br. J. Cancer 2011, 104:1691-1696.
108. Manegold C., Vansteenkiste J., Cardenal F., Schuette W., Woll P.J., Ulsperger E., Kerber A., Eckmayr J., von Pawel J. Randomized phase II study of three doses of the integrin inhibitor cilengitide versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer. Invest. New Drugs 2013, 31:175-182.
109. Alva A., Slovin S., Daignault S., Carducci M., Dipaola R., Pienta K., Agus D., Cooney K., Chen A., Smith D.C., Hussain M. Phase II study of cilengitide (EMD 121974, NSC 707544) in patients with non-metastatic castration resistant prostate cancer, NCI-6735. A study by the DOD/PCF prostate cancer clinical trials consortium. Invest. New Drugs 2012, 30:749-757.
110. Hu P., Yan J., Sharifi J., Bai T., Khawli L.A., Epstein A.L. Comparison of three different targeted tissue factor fusion proteins for inducing tumor vessel thrombosis. Cancer Res. 2003, 63:5046-5053.
111. Wang R.E., Niu Y., Wu H., Cai J. Development of NGR-based anti cancer agents for targeted therapeutics and imaging. Anticancer Agents Med. Chem. 2012, 12:76-86.
112. Gregorc V., Zucali P.A., Santoro A., Ceresoli G.L., Citterio G., De Pas T.M., Zilembo N., De Vincenzo F., Simonelli M., Rossoni G., Spreafico A., Grazia Viganò M., Fontana F., De Braud F.G., Bajetta E., Caligaris-Cappio F., Bruzzi P., Lambiase A., Bordignon C. Phase II study of asparagine-glycine-arginine-human tumor necrosis factor alpha, a selective vascular targeting agent, in previously treated patients with malignant pleural mesothelioma. J. Clin. Oncol. 2010, 28:2604-2611.
113. Gregorc V., Santoro A., Bennicelli E., Punt C.J., Citterio G., Timmer-Bonte J.N., Caligaris Cappio F., Lambiase A., Bordignon C., van Herpen C.M. Phase Ib study of NGR-hTNF, a selective vascular targeting agent, administered at low doses in combination with doxorubicin to patients with advanced solid tumours. Br. J. Cancer 2009, 101:219-224.
114. Santoro A., Pressiani T., Citterio G., Rossoni G., Donadoni G., Pozzi F., Rimassa L., Personeni N., Bozzarelli S., Rossoni G., Colombi S., De Braud F.G., Caligaris-Cappio F., Lambiase A., Bordignon C. Activity and safety of NGR-hTNF, a selective vascular-targeting agent, in previously treated patients with advanced hepatocellular carcinoma. Br. J. Cancer 2010, 10:837-844.
115. Santoro A., Rimassa L., Sobrero A.F., Citterio G., Sclafani F., Carnaghi C., Rimassa L., Personeni N., Bozzarelli S., Rossoni G., Colombi S., De Braud F.G., Caligaris-Cappio F., Lambiase A., Bordignon C. Phase II study of NGR-hTNF, a selective vascular targeting agent, in patients with metastatic colorectal cancer after failure of standard therapy. Eur. J. Cancer 2010, 46:2746-2752.
116. Curnis F., Sacchi A., Corti A. Improving chemotherapeutic drug penetration in tumors by vascular targeting and barrier alteration. J. Clin. Invest. 2002, 110:475-482.
117. Lorusso D., Scambia G., Amadio G., di Legge A., Pietragalla A., De Vincenzo R., Masciullo V., Di Stefano M., Mangili G., Citterio G., Mantori M., Lambiase A., Bordignon C. Phase II study of NGR-hTNF in combination with doxorubicin in relapsed ovarian cancer patients. Br. J. Cancer 2010, 107:37-42.
118. Mammoliti S., Andretta V., Bennicelli E., Caprioni F., Comandini D., Fornarini G., Guglielmi A., Pessino A., Sciallero S., Sobrero A.F., Mazzola G., Lambiase A., Bordignon C. Two doses of NGR-hTNF in combination with capecitabine plus oxaliplatin in colorectal cancer patients failing standard therapies. Ann. Oncol. 2011, 22:973-978.
119. Knetsch P.A., Petrik M., Griessinger C.M., Rangger C., Fani M., Kesenheimer C., von Guggenberg E., Pichler B.J., Virgolini I., Decristoforo C., Haubner R. [68Ga]NODAGA-RGD for imaging αvβ3 integrin expression. Eur. J. Nucl. Med. Mol. Imaging 2011, 38:1303-1312.
120. Ariztia E.V., Lee C.J., Gogoi R., Fishman D.A. The tumor microenvironment: key to early detection. Crit. Rev. Clin. Lab. Sci. 2006, 43:393-425.
121. Petrenko V.A., Jayanna P.K. Phage protein-targeted cancer nanomedicines. FEBS Lett. 2014, 588:341-349.
122. Wang T., Hartner W.C., Gillespie J.W., Praveen K.P., Yang S., Mei L.A., Petrenko V.A., Torchilin V.P. Enhanced tumor delivery and antitumor activity in vivo of liposomal doxorubicin modified with MCF-7-specific phage fusion protein. Nanomedicine 2014, 10:421-430.