Selection of peptides binding to the alpha 5 beta 1 integrin from phage display library.
Open accessAbstract
The alpha 5 beta 1 integrin binds fibronectin through the integrin recognition sequence Arg-Gly-Asp (RGD). We have used a 6-amino acid peptide library expressed on filamentous phage to identify peptide ligands for alpha 5 beta 1. We found that this integrin selectively binds RGD-containing peptides from the library. Of the 32 different sequences obtained, 28 had the RGD motif, 3 contained sequences related to RGD, and only 1 had a clearly different sequence. One of the RGD-containing phage encoded a potentially cyclic insert CRGDCL. The cyclic peptide GAC*RGDC*LGA (where * denotes cysteines forming a disulfide bond) was 10-fold more efficient than any of the linear RGD-containing hexapeptides in inhibiting the binding of RGD-expressing phage to alpha 5 beta 1 or the attachment of alpha 5 beta 1-expressing cells to fibronectin. This peptide also inhibited cell attachment mediated by the alpha v beta 1, alpha v beta 3, and alpha v beta 5 integrins with about 10-fold higher efficiency than linear GRGDSP. One peptide containing an RGD-related sequence, NGRAHA, was also found to inhibit phage attachment and cell adhesion, especially adhesion mediated by the alpha v beta 5 integrin. These results indicate that novel and high affinity ligands for integrins can be isolated from a random peptide library.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
Integrins: Versatility, modulation, and signaling in cell adhesion
Hynes, R. O. (1992) · Cell · doi:10.1016/0092-8674(92)90115-s · Cited by 9,857 · see citing works
New Perspectives in Cell Adhesion: RGD and Integrins
Ruoslahti, E. I., & Pierschbacher, M. D. (1987) · Science · doi:10.1126/science.2821619 · Cited by 4,893 · see citing works
Self-citationPierschbacher, M. D., & Ruoslahti, E. I. (1984) · Nature · doi:10.1038/309030a0 · Cited by 3,670 · see citing works
Self-citationSearching for Peptide Ligands with an Epitope Library
Scott, J. K., & Smith, G. P. (1990) · Science · doi:10.1126/science.1696028 · Cited by 2,087 · see citing works
Integrins and other cell adhesion molecules
Albelda, S. Μ., & Buck, C. A. (1990) · The FASEB Journal · doi:10.1096/fasebj.4.11.2199285 · Cited by 1,975 · see citing works
Ruoslahti, E. I. (1991) · Journal of Clinical Investigation · doi:10.1172/jci114957 · Cited by 1,391 · see citing works
Self-citationPytela, R., Pierschbacher, M. D., & Ruoslahti, E. I. (1985) · Cell · doi:10.1016/0092-8674(85)90322-8 · Cited by 1,101 · see citing works
Self-citationPeptides on phage: a vast library of peptides for identifying ligands.
Cwirla, S. E., Peters, E. A., Barrett, R. W., & Dower, W. J. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6378 · Cited by 930 · see citing works
Random Peptide Libraries: a Source of Specific Protein Binding Molecules
Devlin, J. J., Panganiban, L. C., & Devlin, P. E. (1990) · Science · doi:10.1126/science.2143033 · Cited by 923 · see citing works
Antibody-selectable filamentous fd phage vectors: affinity purification of target genes
Parmley, S. F., & Smith, G. P. (1988) · Gene · doi:10.1016/0378-1119(88)90495-7 · Cited by 871 · see citing works
Giancotti, F. G., & Ruoslahtl, E. (1990) · Cell · doi:10.1016/0092-8674(90)90098-y · Cited by 739 · see citing works
Kornblihtt, A. R., Umezawa, K., Vibe‐Pedersen, K., & Baralle, F. E. (1985) · The EMBO Journal · doi:10.1002/j.1460-2075.1985.tb03847.x · Cited by 659 · see citing works
Pierschbacher, M. D., & Ruoslahti, E. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45376-8 · Cited by 651 · see citing works
Self-citationA Synthetic Peptide from Fibronectin Inhibits Experimental Metastasis of Murine Melanoma Cells
Humphries, M. J., Olden, K., & Yamada, K. M. (1986) · Science · doi:10.1126/science.3726541 · Cited by 628 · see citing works
Guan, J., & Hynes, R. O. (1990) · Cell · doi:10.1016/0092-8674(90)90715-q · Cited by 601 · see citing works
Plow, E. F., Pierschbacher, M. D., Ruoslahti, E. I., Marguerie, G. A., & Ginsberg, M. H. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.23.8057 · Cited by 579 · see citing works
Self-citation[46] Fibronectin: Purification, immunochemical properties, and biological activities
Ruoslahti, E. I., Hayman, E. G., Pierschbacher, M. D., & Engvall, E. (1982) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(82)82103-4 · Cited by 535 · see citing works
Self-citationChanges in integrin receptors on oncogenically transformed cells
Plantefaber, L. C., & Hynes, R. O. (1989) · Cell · doi:10.1016/0092-8674(89)90902-1 · Cited by 533 · see citing works
Pytela, R., Pierschbacher, M. D., & Ruoslahti, E. I. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.17.5766 · Cited by 513 · see citing works
Self-citationMain, A. L., Harvey, T. S., Baron, M., Boyd, J. W., & Campbell, I. D. (1992) · Cell · doi:10.1016/0092-8674(92)90600-h · Cited by 470 · see citing works
Kloczewiak, M. A., Timmons, S., Lukas, T. J., & Hawiger, J. (1984) · Biochemistry · doi:10.1021/bi00303a028 · Cited by 468 · see citing works
Elices, M. J., Urry, L. A., & Hemler, M. E. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.112.1.169 · Cited by 448 · see citing works
Suzuki, S., Oldberg, Å., Hayman, E. G., Pierschbacher, M. D., & Ruoslahti, E. I. (1985) · The EMBO Journal · doi:10.1002/j.1460-2075.1985.tb03965.x · Cited by 417 · see citing works
Self-citationFelici, F., Castagnoli, L., Musacchio, A., Jappelli, R., & Cesareni, G. (1991) · Journal of Molecular Biology · doi:10.1016/0022-2836(91)90213-p · Cited by 395 · see citing works
Scarborough, R. M., Naughton, M. A., Teng, W.-N., Rose, J. W., Phillips, D. R., Nannizzi, L., Arfsten, A. E., Campbell, A. M., & Charo, I. F. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)54042-4 · Cited by 375 · see citing works
Obara, M., Kang, M. S., & Yamada, K. M. (1988) · Cell · doi:10.1016/0092-8674(88)90580-6 · Cited by 374 · see citing works
Echistatin. A potent platelet aggregation inhibitor from the venom of the viper, Echis carinatus.
Gan, Z., Gould, R. J., Jacobs, J., Friedman, P. A., & Polokoff, M. A. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)77710-2 · Cited by 368 · see citing works
Humphries, M. J., Komoriya, A., Akiyama, S. K., Olden, K., & Yamada, K. M. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48327-5 · Cited by 347 · see citing works
Cheresh, D. A., Smith, J. W., Cooper, H. M., & Quaranta, V. (1989) · Cell · doi:10.1016/0092-8674(89)90172-4 · Cited by 341 · see citing works
Huang, T., Holt, J., ŁUKASIEWICZ, H., & Niewiarowski, S. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47710-1 · Cited by 324 · see citing works
Conformation/activity studies of rationally designed potent anti‐adhesive RGD peptides
Gurrath, M., Müller, G., Kessler, H., Aumailley, M., & Timpl, R. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb17495.x · Cited by 317 · see citing works
Gehlsen, K. R. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.106.3.925 · Cited by 305 · see citing works
Characterization of the integrin alpha v beta 6 as a fibronectin-binding protein.
Busk, M., Pytela, R., & Sheppard, D. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42622-1 · Cited by 293 · see citing works
A novel fibronectin receptor with an unexpected subunit composition (alpha v beta 1).
Vogel, B., Tarone, G., Giancotti, F. G., Gailit, J. O., & Ruoslahti, E. I. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39268-3 · Cited by 292 · see citing works
Self-citationPeptide ligands for a sugar-binding protein isolated from a random peptide library.
Oldenburg, K. R., Loganathan, D., Goldstein, I. J., Schultz, P. G., & Gallop, M. A. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.12.5393 · Cited by 280 · see citing works
O’Neil, K. T., Hoess, R. H., Jackson, S. A., Ramachandran, N. S., Mousa, S. A., & DeGrado, W. F. (1992) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340140411 · Cited by 278 · see citing works
[27] Arginine-glycine-aspartic acid adhesion receptors
Pytela, R., Pierschbacher, M. D., Argraves, W. S., Suzuki, S., & Ruoslahti, E. I. (1987) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(87)44196-7 · Cited by 263 · see citing works
Self-citationVogel, B., Lee, S. J., Hildebrand, A., Craig, W., Pierschbacher, M. D., Wong‐Staal, F., & Ruoslahti, E. I. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.2.461 · Cited by 262 · see citing works
Self-citationPlow, E., Srouji, A. H., Meyer, D., Marguerie, G. A., & Ginsberg, M. H. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)91019-7 · Cited by 250 · see citing works
Mould, A. P., Komoriya, A., Yamada, K. M., & Humphries, M. J. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)67834-8 · Cited by 245 · see citing works
A family of concanavalin A-binding peptides from a hexapeptide epitope library.
Scott, J. K., Loganathan, D., Easley, R. B., Gong, X., & Goldstein, I. J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.12.5398 · Cited by 238 · see citing works
Identification of a motif for HLA-DR1 binding peptides using M13 display libraries.
Hammer, J., Takács, B., & Sinigaglia, F. (1992) · The Journal of Experimental Medicine · doi:10.1084/jem.176.4.1007 · Cited by 222 · see citing works
Hautanen, A., Gailit, J. O., Mann, D. M., & Ruoslahti, E. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)94206-7 · Cited by 214 · see citing works
Self-citationSamanen, J. M., ALI, F. E. ‐., Romoff, T. T., Calvo, R. R., Sorenson, E., Vasko, J. A., Storer, B. L., Berry, D., Bennett, D., Strohsacker, M. W., et al. (1991) · Journal of Medicinal Chemistry · doi:10.1021/jm00114a022 · Cited by 193 · see citing works
Altieri, D. C., Plescia, J., & Plow, E. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53932-6 · Cited by 186 · see citing works
Zhang, Z., Morla, A., Vuori, K., Bauer, J. S., Juliano, R., & Ruoslahti, E. I. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.1.235 · Cited by 182 · see citing works
Self-citationAota, S., Nagai, T., & Yamada, K. M. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98498-x · Cited by 180 · see citing works
Morla, A. O., & Ruoslahti, E. I. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.118.2.421 · Cited by 166 · see citing works
Self-citationSantoro, S. A., & Lawing, W. J. (1987) · Cell · doi:10.1016/0092-8674(87)90083-3 · Cited by 165 · see citing works
Freed, E., Gailit, J. O., van der Geer, P., Ruoslahti, E. I., & Hunter, T. R. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb08445.x · Cited by 161 · see citing works
Self-citationNagai, T., Yamakawa, N., Aota, S., Yamada, S. S., Akiyama, S. K., Olden, K., & Yamada, K. M. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.6.1295 · Cited by 157 · see citing works
Bauer, J. S. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.2.477 · Cited by 143 · see citing works
Vectors—A survey of molecular cloning vectors and their uses
Short, J. M. (1988) · Genomics · doi:10.1016/0888-7543(88)90013-4 · Cited by 142 · see citing works
Increased tumorigenicity of fibronectin receptor deficient Chinese hamster ovary cell variants.
Schreiner, C. L., FISHER, M. S., Hussein, S., & Juliano, R. L. (1991) · PubMed · Cited by 129 · see citing works
SAIKI, I., Iida, J., Murata, J., Ogawa, R., Nishi, N., Sugimura, K., Tokura, S., & Azuma, I. (1989) · PubMed · Cited by 124 · see citing works
Peptide inhibitors of fibronectin, laminin, and other adhesion molecules: Unique and shared features
Yamada, K. M., & Kennedy, D. W. (1987) · Journal of Cellular Physiology · doi:10.1002/jcp.1041300105 · Cited by 114 · see citing works
Cardarelli, P. M., Yamagata, S., Taguchi, I., Gorcsan, F., Chiang, S.-L., & Lobl, T. J. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)50070-3 · Cited by 79 · see citing works
Barrett, R. W., Cwirla, S. E., Ackerman, M. S., Olson, A. M., Peters, E. A., & Dower, W. J. (1992) · Analytical Biochemistry · doi:10.1016/0003-2697(92)90252-3 · Cited by 77 · see citing works
Dalton, S. L., Marcantonio, E. E., & Assoian, R. K. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42425-8 · Cited by 63 · see citing works
Altering the antigenicity of proteins.
Alexander, H., Alexander, S. P. H., Getzoff, E. D., Tainer, J. A., Geysen, H. M., & Lerner, R. A. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.8.3352 · Cited by 42 · see citing works
Imura, Y., Stassen, J., Bunting, S., Stockmans, F., & Collen, D. (1992) · Blood · doi:10.1182/blood.v80.5.1247.1247 · Cited by 20 · see citing works
Lush, D. T. (1992) · Postgraduate Medicine · doi:10.1080/00325481.1992.11701234 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
RGD AND OTHER RECOGNITION SEQUENCES FOR INTEGRINS
Ruoslahti, E. (1996) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.12.1.697 · Cited by 3,191 · see citing works
Self-citationCancer Treatment by Targeted Drug Delivery to Tumor Vasculature in a Mouse Model
Arap, W., Pasqualini, R., & Ruoslahti, E. I. (1998) · Science · doi:10.1126/science.279.5349.377 · Cited by 2,040 · see citing works
Self-citationSmith, G. P., & Petrenko, V. A. (1997) · Chemical Reviews · doi:10.1021/cr960065d · Cited by 1,550 · see citing works
Tissue-Penetrating Delivery of Compounds and Nanoparticles into Tumors
Sugahara, K. N., Teesalu, T., Karmali, P. P., Kotamraju, V. R., Agemy, L., Girard, O. M., Hanahan, D., Mattrey, R. F., & Ruoslahti, E. I. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.10.013 · Cited by 1,140 · see citing works
Self-citationCoadministration of a Tumor-Penetrating Peptide Enhances the Efficacy of Cancer Drugs
Sugahara, K. N., Teesalu, T., Karmali, P. P., Kotamraju, V. R., Agemy, L., Greenwald, D. R., & Ruoslahti, E. I. (2010) · Science · doi:10.1126/science.1183057 · Cited by 1,080 · see citing works
Self-citationDmitriev, I. P., Krasnykh, V. N., Miller, C. R., Wang, M., Kashentseva, E. A., Mikheeva, G., Belousova, N., & Curiel, D. T. (1998) · Journal of Virology · doi:10.1128/jvi.72.12.9706-9713.1998 · Cited by 768 · see citing works
Gelatinase-mediated migration and invasion of cancer cells
Björklund, M., & Koivunen, E. (2005) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2005.03.001 · Cited by 663 · see citing works
Self-citationKim, S., Bell, K. S., Mousa, S. A., & Varner, J. A. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65005-5 · Cited by 632 · see citing works
Pfaff, M., Tangemann, K., Müller, B., Gurrath, M., Müller, G., Kessler, H., Timpl, R., & Engel, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31981-6 · Cited by 535 · see citing works
Self‐Assembled Peptide‐Based Nanomaterials for Biomedical Imaging and Therapy
Qi, G., Gao, Y., Wang, L., & Wang, H. (2018) · Advanced Materials · doi:10.1002/adma.201703444 · Cited by 531 · see citing works
Modulators of Protein–Protein Interactions
Milroy, L.-G., Grossmann, T. N., Hennig, S., Brunsveld, L., & Ottmann, C. (2014) · Chemical Reviews · doi:10.1021/cr400698c · Cited by 497 · see citing works
Koivunen, E., Wang, B., & Ruoslahti, E. (1995) · Nature Biotechnology · doi:10.1038/nbt0395-265 · Cited by 477 · see citing works
Self-citationMECHANOTRANSDUCTION INVOLVING MULTIMODULAR PROTEINS: Converting Force into Biochemical Signals
Viola Vogel, B. (2006) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.35.040405.102013 · Cited by 444 · see citing works
Elastin‐like polypeptides: Biomedical applications of tunable biopolymers
MacEwan, S. R., & Chilkoti, A. (2010) · Biopolymers · doi:10.1002/bip.21327 · Cited by 425 · see citing works
Zhang, Z., Vuori, K., Wang, H., Reed, J. C., & Ruoslahti, E. I. (1996) · Cell · doi:10.1016/s0092-8674(00)81082-x · Cited by 409 · see citing works
Self-citationCyclic Peptides as Therapeutic Agents and Biochemical Tools
Joo, S. H. (2012) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2012.20.1.019 · Cited by 359 · see citing works
Fibronectin-integrin interactions
Johansson, S. (1997) · Frontiers in bioscience · doi:10.2741/a178 · Cited by 315 · see citing works
Isolation of a highly specific ligand for the alpha 5 beta 1 integrin from a phage display library
Koivunen, E., Wang, B., & Ruoslahti, E. I. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.3.373 · Cited by 308 · see citing works
Self-citationExtracellular Matrix Cell Adhesion Peptides: Functional Applications in Orthopedic Materials
LeBaron, R. G., & Athanasiou, K. A. (2000) · Tissue Engineering · doi:10.1089/107632700320720 · Cited by 306 · see citing works
Isolation of High-Affinity Peptide Antagonists of 14-3-3 Proteins by Phage Display
Wang, B., Yang, H., Liu, Y., Jelı́nek, T., Zhang, L., Ruoslahti, E. I., & Fu, H. (1999) · Biochemistry · doi:10.1021/bi991353h · Cited by 304 · see citing works
Self-citationIdentification of a peptide blocking vascular endothelial growth factor (VEGF)‐mediated angiogenesis
Tournaire, R., Demangel, C., Malavaud, B. A., Vassy, R., Rouyre, S., Kraemer, M., Plouët, J., Derbin, C., Perret, G. Y., & Mazié, J. C. (2000) · The EMBO Journal · doi:10.1093/emboj/19.7.1525 · Cited by 295 · see citing works
Hamidouche, Z., Fromigué, O., Ringe, J., Häupl, T., Vaudin, P., Pagès, J., Srouji, S., Livne, E., & Marie, P. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812334106 · Cited by 291 · see citing works
Beta 1 integrin-dependent and -independent polymerization of fibronectin.
Wennerberg, K., Lohikangas, L., Gullberg, D., Pfaff, M., Johansson, S., & Fässler, R. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.132.1.227 · Cited by 290 · see citing works
From Combinatorial Chemistry to Cancer-Targeting Peptides
Aina, O. H., Liu, R., Sutcliffe-Goulden, J., Mařı́k, J., Pan, C.-X., & Lam, K. S. (2007) · Molecular Pharmaceutics · doi:10.1021/mp700073y · Cited by 285 · see citing works
Mizejewski, G. J. (2001) · Experimental Biology and Medicine · doi:10.1177/153537020122600503 · Cited by 270 · see citing works
Discovering Cell-Adhesion Peptides in Tissue Engineering: Beyond RGD
Huettner, N., Dargaville, T. R., & Forget, A. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.01.008 · Cited by 262 · see citing works
Targeted Delivery of Multifunctional Magnetic Nanoparticles
McCarthy, J. R., Kelly, K. A., Sun, E. Y., & Weissleder, R. (2007) · Nanomedicine · doi:10.2217/17435889.2.2.153 · Cited by 254 · see citing works
Pasqualini, R., Koivunen, E., & Ruoslahti, E. I. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.5.1189 · Cited by 235 · see citing works
Self-citationCombinatorial Peptide Libraries: Mining for Cell-Binding Peptides
Gray, B. P., & Brown, K. C. (2013) · Chemical Reviews · doi:10.1021/cr400166n · Cited by 229 · see citing works
The Human Integrin α8β1 Functions as a Receptor for Tenascin, Fibronectin, and Vitronectin
Schnapp, L. M., Hatch, N. E., Ramos, D. M., Klimanskaya, I. V., Sheppard, D., & Pytela, R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.39.23196 · Cited by 217 · see citing works
Dynamic Monitoring of Cell Adhesion and Spreading on Microelectronic Sensor Arrays
Atienza, J. M., Zhu, J., Wang, X., Xu, X., & Abassi, Y. A. (2005) · SLAS DISCOVERY · doi:10.1177/1087057105279635 · Cited by 215 · see citing works
Barker, T. H., Baneyx, G., Cardó‐Vila, M., Workman, G. A., Weaver, M. S., Menon, P. M., Dedhar, S., Rempel, S. A., Arap, W., Pasqualini, R., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m504663200 · Cited by 213 · see citing works
Spontaneous Formation of L-Isoaspartate and Gain of Function in Fibronectin
Curnis, F., Longhi, R., Crippa, L., Cattaneo, A., Dondossola, E., Bachi, A., & Corti, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604812200 · Cited by 211 · see citing works
Teesalu, T., Sugahara, K. N., & Ruoslahti, E. I. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00216 · Cited by 211 · see citing works
Self-citationAn Ephrin Mimetic Peptide That Selectively Targets the EphA2 Receptor
Koolpe, M., Dail, M., & Pasquale, E. B. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m208495200 · Cited by 211 · see citing works
Milner, R., & ffrench‐Constant, C. (1994) · Development · doi:10.1242/dev.120.12.3497 · Cited by 210 · see citing works
Crystal structure of the tenth type III cell adhesion module of human fibronectin
Dickinson, C. D., Veerapandian, B., Dai, X.-P., Hamlin, R. C., Xuong, N., Ruoslahti, E., & Ely, K. R. (1994) · Journal of Molecular Biology · doi:10.1016/0022-2836(94)90013-2 · Cited by 208 · see citing works
Self-citationKireeva, M. L., Lam, S. C.-T., & Lau, L. F. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.5.3090 · Cited by 203 · see citing works
Integrin-mediated cell adhesion: the extracellular face.
Loftus, J. C., Smith, J. W., & Ginsberg, M. H. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47235-3 · Cited by 202 · see citing works
Stimulus-responsive macromolecules and nanoparticles for cancer drug delivery
MacEwan, S. R., Callahan, D. J., & Chilkoti, A. (2010) · Nanomedicine · doi:10.2217/nnm.10.50 · Cited by 205 · see citing works
Tumor-targeting peptides from combinatorial libraries
Liu, R., Li, X., Xiao, W., & Lam, K. S. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2016.05.009 · Cited by 200 · see citing works
The neovasculature homing motif NGR: more than meets the eye
Corti, A., Curnis, F., Arap, W., & Pasqualini, R. (2008) · Blood · doi:10.1182/blood-2008-04-150862 · Cited by 198 · see citing works
Ligand-targeted theranostic nanomedicines against cancer
Yao, V. J., D’Angelo, S., Butler, K. S., Théron, C., Smith, T. L., Marchiò, S., Gelovani, J. G., Sidman, R. L., Dobroff, A. S., Brinker, C. J., et al. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.01.002 · Cited by 195 · see citing works
Cardote, T. A. F., & Ciulli, A. (2015) · ChemMedChem · doi:10.1002/cmdc.201500450 · Cited by 189 · see citing works
High-affinity urokinase receptor antagonists identified with bacteriophage peptide display.
Goodson, R. J., DOYLE, M. V., Kaufman, S., & Rosenberg, S. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.7129 · Cited by 190 · see citing works
Gouget, A., Senchou, V., Govers, F., Sanson, A., Barre, A., Rougé, P., Pont‐Lezica, R., & Canut, H. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.066464 · Cited by 189 · see citing works
A Role in Migration for the αvβ1 Integrin Expressed on Oligodendrocyte Precursors
Milner, R., Edwards, G. M., Streuli, C. H., & ffrench‐Constant, C. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-22-07240.1996 · Cited by 188 · see citing works
Asokan, A., Hamra, J. B., Govindasamy, L., Agbandje-McKenna, M., & Samulski, R. J. (2006) · Journal of Virology · doi:10.1128/jvi.00843-06 · Cited by 183 · see citing works
Lipid-Mediated Enhancement of Transfection by a Nonviral Integrin-Targeting Vector
Hart, S. L., Arancibia-Cárcamo, C. V., Wolfert, M. A., Mailhos, C., O’Reilly, N., Ali, R. R., Coutelle, C. C., George, A. J. T., Harbottle, R. P., Knight, A. M., et al. (1998) · Human Gene Therapy · doi:10.1089/hum.1998.9.4-575 · Cited by 176 · see citing works
De Novo Design of a Tumor-Penetrating Peptide
Alberici, L., Roth, L., Sugahara, K. N., Agemy, L., Kotamraju, V. R., Teesalu, T., Bordignon, C., Traversari, C., Rizzardi, G., & Ruoslahti, E. I. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1668 · Cited by 175 · see citing works
Self-citationPhage‐Enabled Nanomedicine: From Probes to Therapeutics in Precision Medicine
Sunderland, K. S., Yang, M., & Mao, C. (2016) · Angewandte Chemie International Edition · doi:10.1002/anie.201606181 · Cited by 171 · see citing works
Krätzschmar, J., Lum, L., & Blobel, C. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.9.4593 · Cited by 170 · see citing works
Peptide-based targeted therapeutics: Focus on cancer treatment
Araste, F., Abnous, K., Hashemi, M., Taghdisi, S. M., Ramezani, M., & Alibolandi, M. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.11.004 · Cited by 162 · see citing works
Kimura, R. H., Levin, A. M., Cochran, F. V., & Cochran, J. R. (2009) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.22441 · Cited by 154 · see citing works
Evans, J. P., Schultz, R. M., & Kopf, G. S. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.10.3267 · Cited by 154 · see citing works
iRGD Peptide as a Tumor-Penetrating Enhancer for Tumor-Targeted Drug Delivery
Kang, S., Lee, S., & Park, S. (2020) · Polymers · doi:10.3390/polym12091906 · Cited by 149 · see citing works
Rusnati, M., Tanghetti, E., Dell’Era, P., Gualandris, A., & Presta, M. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.12.2449 · Cited by 146 · see citing works
β1 Integrins Are Critically Involved in Neutrophil Locomotion in Extravascular Tissue In Vivo
Werr, J., Xie, X., Hedqvist, P., Ruoslahti, E. I., & Lindbom, L. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.12.2091 · Cited by 146 · see citing works
Self-citationDefinition of an Unexpected Ligand Recognition Motif for αvβ6 Integrin
Kraft, S., Diefenbach, B., Mehta, R., Jonczyk, A., Luckenbach, G. A., & Goodman, S. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.4.1979 · Cited by 145 · see citing works
Koolpe, M., Burgess, R., Dail, M., & Pasquale, E. B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500363200 · Cited by 143 · see citing works
Homing peptides as targeted delivery vehicles
Laakkonen, P. M., & Vuorinen, K. (2010) · Integrative Biology · doi:10.1039/c0ib00013b · Cited by 143 · see citing works
Milner, R., Wilby, M. J., Nishimura, S. L., Boylen, K., Edwards, G. M., Fawcett, J. W., Streuli, C. H., Pytela, R., & ffrench‐Constant, C. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8547 · Cited by 139 · see citing works
The Diverse Roles of Integrins and Their Ligands in AngiogenesisPreprint
Hynes, R. O., Lively, J. C., McCarty, J. H., Taverna, D., Francis, S., Hodivala‐Dilke, K., & XIAO, Q. (2002) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2002.67.143 · Cited by 138 · see citing works
Identification of receptor ligands with phage display peptide libraries.
Koivunen, E., Arap, W., Rajotte, D., Lahdenranta, J., & Pasqualini, R. (1999) · PubMed · Cited by 137 · see citing works
Self-citationTumor-Penetrating iRGD Peptide Inhibits Metastasis
Sugahara, K. N., Braun, G. B., de Mendoza, T. H., Kotamraju, V. R., French, R. P., Lowy, A. M., Teesalu, T., & Ruoslahti, E. I. (2014) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-14-0366 · Cited by 135 · see citing works
Self-citationChen, N., Leu, S.-J., Todorović, V., Lam, S. C.-T., & Lau, L. F. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406813200 · Cited by 132 · see citing works
Coburn, J., Chege, W., Magoun, L., Bodary, S. C., & Leong, J. M. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01654.x · Cited by 132 · see citing works
Transductional targeting of adenovirus vectors for gene therapy
Glasgow, J. N., Everts, M., & Curiel, D. (2006) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7700928 · Cited by 131 · see citing works
Design and Structure of Peptide and Peptidomimetic Antagonists of Protein- Protein Interaction
Sillerud, L. O., & Larson, R. A. (2005) · Current Protein and Peptide Science · doi:10.2174/1389203053545462 · Cited by 129 · see citing works
Mateu, M. G., Valero, M. L., Andreu, D., & Domingo, E. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.22.12814 · Cited by 128 · see citing works
Felding‐Habermann, B., Silletti, S., Mei, F. C., Siu, C., Yip, P. S. F., Brooks, P. C., Cheresh, D. A., O’Toole, T. E., Ginsberg, M. H., & Montgomery, A. M. P. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.6.1567 · Cited by 125 · see citing works
Engineered Cystine-Knot Peptides that Bind αvβ3 Integrin with Antibody-Like Affinities
Silverman, A. P., Levin, A. M., Lahti, J. L., & Cochran, J. R. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.11.004 · Cited by 124 · see citing works
Peptide Ligands for Integrin .alpha.v.beta.3 Selected from Random Phage Display Libraries
Healy, J. M., Murayama, O., Maeda, T., Yoshino, K., Sekiguchi, K., & Kikuchi, M. (1995) · Biochemistry · doi:10.1021/bi00012a012 · Cited by 124 · see citing works
αvβ3‐ or α5β1‐Integrin‐Selective Peptidomimetics for Surface Coating
Mas‐Moruno, C., Fraioli, R., Rechenmacher, F., Neubauer, S., Kapp, T. G., & Kessler, H. (2016) · Angewandte Chemie International Edition · doi:10.1002/anie.201509782 · Cited by 123 · see citing works
Review of Integrin‐Targeting Biomaterials in Tissue Engineering
Dhavalikar, P., Robinson, A., Lan, Z., Jenkins, D. M. R., Chwatko, M., Salhadar, K., Jose, A., Kar, R., Shoga, E., Kannapiran, A., et al. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000795 · Cited by 122 · see citing works
Selection of biologically active peptides by phage display of random peptide libraries
Cortese, R. (1996) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(96)80072-3 · Cited by 120 · see citing works
Identification of a Src SH3 domain binding motif by screening a random phage display library.
Cheadle, C., Ivashchenko, Y., South, V., Searfoss, G. H., French, S., Howk, R. S., Ricca, G. A., & Jaye, M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)51043-2 · Cited by 119 · see citing works
The pharmacology of the integrins
Cox, D. M., Aoki, T., Seki, J., Motoyama, Y., & Yoshida, K. (1994) · Medicinal Research Reviews · doi:10.1002/med.2610140203 · Cited by 119 · see citing works
Werr, J., Johansson, J., Eriksson, E. E., Hedqvist, P., Ruoslahti, E. I., & Lindbom, L. (2000) · Blood · doi:10.1182/blood.v95.5.1804.005k11_1804_1809 · Cited by 118 · see citing works
Self-citationIdentification of biologically active peptides using random libraries displayed on phage
Cortese, R., Monaci, P., Nicosia, A., Luzzago, A., Felici, F., Galfré, G., Pessi, A., Tramontano, A. L., & Sollazzo, M. (1995) · Current Opinion in Biotechnology · doi:10.1016/0958-1669(95)80012-3 · Cited by 118 · see citing works
Integrins in the Immune System
Shimizu, Y., Rose, D. M., & Ginsberg, M. H. (1999) · Advances in immunology · doi:10.1016/s0065-2776(08)60024-3 · Cited by 118 · see citing works
Lei, H., An, P., Shumei, S., Xiaoying, L., Luowen, H., Jian, W., Lin, M., Meisheng, L., Junshan, Y., & Chengchao, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203103200 · Cited by 116 · see citing works
Anti-neovascular therapy using novel peptides homing to angiogenic vessels
Oku, N., Asai, T., Watanabe, K., Kuromi, K., Nagatsuka, M., Kurohane, K., Kikkawa, H., Ogino, K., Tanaka, M., Ishikawa, D., et al. (2002) · Oncogene · doi:10.1038/sj.onc.1205347 · Cited by 116 · see citing works
Small binding proteins selected from a combinatorial repertoire of knottins displayed on phage
Smith, G. P., Patel, S. U., Windass, J. D., Thornton, J. M., Winter, G. P., & Griffiths, A. D. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1621 · Cited by 114 · see citing works
Saidak, Z., Le Henaff, C., Azzi, S., Marty, C., Da Nascimento, S., Sonnet, P., & Marie, P. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.621219 · Cited by 113 · see citing works
An artificial cell-cycle inhibitor isolated from a combinatorial library
Cohen, B. A., Colas, P., & Brent, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14272 · Cited by 112 · see citing works
Orecchia, A., Lacal, P. M., Schietroma, C., Morea, V., Zambruno, G., & Failla, C. M. (2003) · Journal of Cell Science · doi:10.1242/jcs.00673 · Cited by 110 · see citing works
Simnick, A. J., Valencia, C. A., Liu, R., & Chilkoti, A. (2010) · ACS Nano · doi:10.1021/nn901732h · Cited by 106 · see citing works
In Vivo Imaging of Molecularly Targeted Phage
Kelly, K. A., Waterman, P. R., & Weissleder, R. (2006) · Neoplasia · doi:10.1593/neo.06610 · Cited by 105 · see citing works
Targeting the EphA4 receptor in the nervous system with biologically active peptides
Murai, K. K., Nguyen, L. N., Koolpe, M., McLennan, R., Krull, C. E., & Pasquale, E. B. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2003.08.006 · Cited by 106 · see citing works
Mapping of Vascular ZIP Codes by Phage Display
Teesalu, T., Sugahara, K. N., & Ruoslahti, E. I. (2012) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-396962-0.00002-1 · Cited by 104 · see citing works
Self-citationPfaff, M., McLane, M. A., Beviglia, L., Niewiarowski, S., & Timpl, R. (1994) · Cell Communication & Adhesion · doi:10.3109/15419069409014213 · Cited by 99 · see citing works
Sánchez-Aparicio, P., Domı́nguez-Jiménez, C., & Garcı́a-Pardo, A. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.1.271 · Cited by 95 · see citing works
Targeted Delivery of IFNγ to Tumor Vessels Uncouples Antitumor from Counterregulatory Mechanisms
Curnis, F., Gasparri, A. M., Sacchi, A., Cattaneo, A., Magni, F., & Corti, A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4282 · Cited by 94 · see citing works
Uptake and intracellular fate of phage display vectors in mammalian cells
Ivanenkov, V. V., Felici, F., & Menon, A. G. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(98)00162-1 · Cited by 93 · see citing works
Dennis, M. S., & Lazarus, R. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31765-9 · Cited by 93 · see citing works
A Peptide Inhibiting the Collagen Binding Function of Integrin α2I Domain
Ivaska, J., Käpylä, J., Pentikäinen, O. T., Hoffrén, A., Hermonen, J., Huttunen, P., Johnson, M. S., & Heino, J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.6.3513 · Cited by 91 · see citing works
Widhe, M., Shalaly, N. D., & Hedhammar, M. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.10.013 · Cited by 90 · see citing works
Jackson, T., Blakemore, W. E., Newman, J. W. I., Knowles, N. J., Mould, A. P., Humphries, M. J., & King, A. M. Q. (2000) · Microbiology · doi:10.1099/0022-1317-81-5-1383 · Cited by 89 · see citing works
Wonder, E. A., Simón‐Gracia, L., Scodeller, P., Majzoub, R. N., Kotamraju, V. R., Ewert, K. K., Teesalu, T., & Safinya, C. R. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2018.02.052 · Cited by 86 · see citing works
- Authors
- Koivunen, E., Gay, D. A., & Ruoslahti, E.
- Affiliations
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1993-09
- Volume
- 268
- Issue
- 27
- Pages
- 20205-20210
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1506729263
- Cited by
- 344
- References
- 62
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 4 · 2023: 8 · 2022: 3 · 2021: 8 · 2020: 5 · 2019: 2 · 2018: 6 · 2017: 8 · 2016: 15 · 2015: 8 · 2014: 9 · 2013: 11 · 2012: 14
- FWCI
- 7.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p01ca028896-15, 5r35ca042507-07)
- National Cancer Institute (CA30199, CA 28896, CA-42507, P30CA030199)
- Topics
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Physical Sciences › Materials Science › Surfaces, Coatings and Films › Polymer Surface Interaction Studies
- Keywords
- alpha5beta1 integrin, RGD peptide, fibronectin, integrin ligands, cyclic RGD peptide, phage display, cell adhesion, peptide library screening
- MeSH terms
- Amino Acid Sequence, Animals, Bacteriophages, Base Sequence, Binding, Competitive, Fibronectins, Cricetinae, Kinetics, Molecular Sequence Data, Oligodeoxyribonucleotides, Oligopeptides, Transfection, Gene Library, Integrins, Polymerase Chain Reaction, Databases, Factual, CHO Cells, Receptors, Fibronectin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review