Generation of bivalent and bispecific kringle single domains by loop grafting as potent agonists against death receptors 4 and 5

Journal of Molecular Biology

Volumn 411, Issue 1, 2011, Pages 201-219

  Lee, Chang Han ^a   Park, Kyung Jin ^a   Kim, Sang Jick ^b   Kwon, Ohsuk ^b   Jeong, Ki Jun ^c   Kim, Ayeung ^a   Kim, Yong Sung ^a  

^a Ajou University   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

cell death; nonantibody protein scaffold; protein engineering; TRAIL receptor; yeast surface display

Indexed keywords

DEATH RECEPTOR 4; DEATH RECEPTOR 5;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL DEATH; CYSTINE KNOT MOTIF; KRINGLE DOMAIN; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN TARGETING; SURFACE PROPERTY; TUMOR CELL; YEAST;

EID: 79960697800     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.05.040     Document Type: Article

References (46)

1. Chan A.C., and Carter P.J. Therapeutic antibodies for autoimmunity and inflammation Nat. Rev. Immunol. 10 2010 301 316
2. Gronwall C., and Stahl S. Engineered affinity proteins-generation and applications J. Biotechnol. 140 2009 254 269
3. Cuesta A.M., Sainz-Pastor N., Bonet J., Oliva B., and Alvarez-Vallina L. Multivalent antibodies: when design surpasses evolution Trends Biotechnol. 28 2010 355 362
4. Cochran J.R. Engineered proteins pull double duty Sci. Transl. Med. 2 2010 17ps15
5. Yang A., Wilson N.S., and Ashkenazi A. Proapoptotic DR4 and DR5 signaling in cancer cells: toward clinical translation Curr. Opin. Cell Biol. 22 2010 837 844
6. Fox N.L., Humphreys R., Luster T.A., Klein J., and Gallant G. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) receptor-1 and receptor-2 agonists for cancer therapy Expert Opin. Biol. Ther. 10 2010 1 18
7. Griffith T.S., Rauch C.T., Smolak P.J., Waugh J.Y., Boiani N., and Lynch D.H. Functional analysis of TRAIL receptors using monoclonal antibodies J. Immunol. 162 1999 2597 2605 (Pubitemid 29309279)
8. Adams C., Totpal K., Lawrence D., Marsters S., Pitti R., and Yee S. Structural and functional analysis of the interaction between the agonistic monoclonal antibody Apomab and the proapoptotic receptor DR5 Cell Death Differ. 15 2008 751 761 (Pubitemid 351405080)
9. Lee S.H., Park D.W., Sung E.S., Park H.R., Kim J.K., and Kim Y.S. Humanization of an agonistic anti-death receptor 4 single chain variable fragment antibody and avidity-mediated enhancement of its cell death-inducing activity Mol. Immunol. 47 2010 816 824
10. Pavet V., Beyrath J., Pardin C., Morizot A., Lechner M.C., and Briand J.P. Multivalent DR5 peptides activate the TRAIL death pathway and exert tumoricidal activity Cancer Res. 70 2010 1101 1110
11. Lee H.W., Lee S.H., Lee H.W., Ryu Y.W., Kwon M.H., and Kim Y.S. Homomeric and heteromeric interactions of the extracellular domains of death receptors and death decoy receptors Biochem. Biophys. Res. Commun. 330 2005 1205 1212
12. Clancy L., Mruk K., Archer K., Woelfel M., Mongkolsapaya J., and Screaton G. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAIL-induced apoptosis Proc. Natl Acad. Sci. USA 102 2005 18099 18104 (Pubitemid 41798508)
13. Bouralexis S., Findlay D.M., Atkins G.J., Labrinidis A., Hay S., and Evdokiou A. Progressive resistance of BTK-143 osteosarcoma cells to Apo2L/TRAIL-induced apoptosis is mediated by acquisition of DcR2/TRAIL-R4 expression: resensitisation with chemotherapy Br. J. Cancer 89 2003 206 214 (Pubitemid 36897959)
14. Merino D., Lalaoui N., Morizot A., Schneider P., Solary E., and Micheau O. Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2 Mol. Cell. Biol. 26 2006 7046 7055 (Pubitemid 44477684)
15. Lee C.H., Park K.J., Sung E.S., Kim A., Choi J.D., and Kim J.S. Engineering of a human kringle domain into agonistic and antagonistic binding proteins functioning in vitro and in vivo Proc. Natl Acad. Sci. USA 107 2010 9567 9571
16. Cao Y., Cao R., and Veitonmaki N. Kringle structures and antiangiogenesis Curr. Med. Chem. Anticancer Agents 2 2002 667 681 (Pubitemid 35175266)
17. Ozhogina O.A., and Bominaar E.L. Characterization of the kringle fold and identification of a ubiquitous new class of disulfide rotamers J. Struct. Biol. 168 2009 223 233
18. Marti D.N., Schaller J., and Llinas M. Solution structure and dynamics of the plasminogen kringle 2-AMCHA complex: 3(1)-helix in homologous domains Biochemistry 38 1999 15741 15755 (Pubitemid 129520467)
19. Rios-Steiner J.L., Schenone M., Mochalkin I., Tulinsky A., and Castellino F.J. Structure and binding determinants of the recombinant kringle-2 domain of human plasminogen to an internal peptide from a group A streptococcal surface protein J. Mol. Biol. 308 2001 705 719 (Pubitemid 32568470)
20. Kim M.S., Lee S.H., Song M.Y., Yoo T.H., Lee B.K., and Kim Y.S. Comparative analyses of complex formation and binding sites between human tumor necrosis factor-alpha and its three antagonists elucidate their different neutralizing mechanisms J. Mol. Biol. 374 2007 1374 1388 (Pubitemid 350122551)
21. Gai S.A., and Wittrup K.D. Yeast surface display for protein engineering and characterization Curr. Opin. Struct. Biol. 17 2007 467 473 (Pubitemid 47454774)
22. Hernandez H., and Robinson C.V. Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry Nat. Protoc. 2 2007 715 726 (Pubitemid 47040033)
23. Wang L., Yang J.K., Kabaleeswaran V., Rice A.J., Cruz A.C., and Park A.Y. The Fas-FADD death domain complex structure reveals the basis of DISC assembly and disease mutations Nat. Struct. Mol. Biol. 17 2010 1324 1329
24. Sung E.S., Park K.J., Lee S.H., Jang Y.S., Park S.K., and Park Y.H. A novel agonistic antibody to human death receptor 4 induces apoptotic cell death in various tumor cells without cytotoxicity in hepatocytes Mol. Cancer Ther. 8 2009 2276 2285
25. Davidson D.J., Haskell C., Majest S., Kherzai A., Egan D.A., and Walter K.A. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78 Cancer Res. 65 2005 4663 4672 (Pubitemid 40740802)
26. Janin J., and Chothia C. The structure of protein-protein recognition sites J. Biol. Chem. 265 1990 16027 16030
27. Pfaff M., Tangemann K., Muller B., Gurrath M., Muller G., and Kessler H. Selective recognition of cyclic RGD peptides of NMR defined conformation by alpha IIb beta 3, alpha V beta 3, and alpha 5 beta 1 integrins J. Biol. Chem. 269 1994 20233 20238 (Pubitemid 24260416)
28. Ewert S., Honegger A., and Pluckthun A. Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering Methods 34 2004 184 199 (Pubitemid 39092813)
29. Kiss C., Fisher H., Pesavento E., Dai M., Valero R., and Ovecka M. Antibody binding loop insertions as diversity elements Nucleic Acids Res. e132 2006 34
30. Smith J.W., Tachias K., and Madison E.L. Protein loop grafting to construct a variant of tissue-type plasminogen activator that binds platelet integrin alpha IIb beta 3 J. Biol. Chem. 270 1995 30486 30490
31. Silverman A.P., Levin A.M., Lahti J.L., and Cochran J.R. Engineered cystine-knot peptides that bind alpha(v)beta(3) integrin with antibody-like affinities J. Mol. Biol. 385 2009 1064 1075
32. Kolmar H. Engineered cystine-knot miniproteins for diagnostic applications Expert Rev. Mol. Diagn. 10 2010 361 368
33. Krause S., Schmoldt H.U., Wentzel A., Ballmaier M., Friedrich K., and Kolmar H. Grafting of thrombopoietin-mimetic peptides into cystine knot miniproteins yields high-affinity thrombopoietin antagonists and agonists FEBS J. 274 2007 86 95 (Pubitemid 44952900)
34. Reiss S., Sieber M., Oberle V., Wentzel A., Spangenberg P., and Claus R. Inhibition of platelet aggregation by grafting RGD and KGD sequences on the structural scaffold of small disulfide-rich proteins Platelets 17 2006 153 157 (Pubitemid 43791626)
35. Silverman J., Liu Q., Bakker A., To W., Duguay A., and Alba B.M. Multivalent avimer proteins evolved by exon shuffling of a family of human receptor domains Nat. Biotechnol. 23 2005 1556 1561 (Pubitemid 41752934)
36. Eggel A., Baumann M.J., Amstutz P., Stadler B.M., and Vogel M. DARPins as bispecific receptor antagonists analyzed for immunoglobulin E receptor blockage J. Mol. Biol. 393 2009 598 607
37. Bostrom J., Yu S.F., Kan D., Appleton B.A., Lee C.V., and Billeci K. Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site Science 323 2009 1610 1614
38. Garcia-Rodriguez C., Levy R., Arndt J.W., Forsyth C.M., Razai A., and Lou J. Molecular evolution of antibody cross-reactivity for two subtypes of type A botulinum neurotoxin Nat. Biotechnol. 25 2007 107 116 (Pubitemid 46087909)
39. Kelley R.F., Totpal K., Lindstrom S.H., Mathieu M., Billeci K., and Deforge L. Receptor-selective mutants of apoptosis-inducing ligand 2/tumor necrosis factor-related apoptosis-inducing ligand reveal a greater contribution of death receptor (DR) 5 than DR4 to apoptosis signaling J. Biol. Chem. 280 2005 2205 2212
40. Kischkel F.C., Lawrence D.A., Chuntharapai A., Schow P., Kim K.J., and Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5 Immunity 12 2000 611 620
41. Sprick M.R., Weigand M.A., Rieser E., Rauch C.T., Juo P., and Blenis J. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2 Immunity 12 2000 599 609
42. Tarui T., Akakura N., Majumdar M., Andronicos N., Takagi J., and Mazar A.P. Direct interaction of the kringle domain of urokinase-type plasminogen activator (uPA) and integrin alpha V beta 3 induces signal transduction and enhances plasminogen activation Thromb. Haemost. 95 2006 524 534
43. Kim J.S., Yu H.K., Ahn J.H., Lee H.J., Hong S.W., and Jung K.H. Human apolipoprotein(a) kringle V inhibits angiogenesis in vitro and in vivo by interfering with the activation of focal adhesion kinases Biochem. Biophys. Res. Commun. 313 2004 534 540
44. Lee H.W., Lee S.H., Park K.J., Kim J.S., Kwon M.H., and Kim Y.S. Construction and characterization of a pseudo-immune human antibody library using yeast surface display Biochem. Biophys. Res. Commun. 346 2006 896 903
45. Sung E.S., Kim A., Park J.S., Chung J., Kwon M.H., and Kim Y.S. Histone deacetylase inhibitors synergistically potentiate death receptor 4-mediated apoptotic cell death of human T-cell acute lymphoblastic leukemia cells Apoptosis 15 2010 1256 1269
46. Park K.J., Lee S.H., Kim T.I., Lee H.W., Lee C.H., and Kim E.H. A human scFv antibody against TRAIL receptor 2 induces autophagic cell death in both TRAIL-sensitive and TRAIL-resistant cancer cells Cancer Res. 67 2007 7327 7334