An anti-hapten camelid antibody reveals a cryptic binding site with significant energetic contributions from a nonhypervariable loop

Protein Science

Volumn 20, Issue 7, 2011, Pages 1196-1207

  Fanning, Sean W ^a   Horn, James R ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Anti hapten antibody; Binding thermodynamics; Camelid antibody; CDR grafting; Hapten; Single domain antibody; VHH; VHH structure

Indexed keywords

HAPTEN ANTIBODY; LIGAND; METHOTREXATE;

ARTICLE; ARTIODACTYLA; BINDING AFFINITY; BINDING SITE; COMPLEMENTARITY DETERMINING REGION; CRYSTAL STRUCTURE; ENERGY METABOLISM; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; THERMODYNAMICS;

ANIMALS; CAMELIDS, NEW WORLD; CAMELS; COMPLEMENTARITY DETERMINING REGIONS; CRYSTALLOGRAPHY, X-RAY; HAPTENS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOSUPPRESSIVE AGENTS; METHOTREXATE; MODELS, MOLECULAR; PROTEIN CONFORMATION; THERMODYNAMICS;

CAMELIDAE;

EID: 79959327631     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.648     Document Type: Article

References (42)

1. Zhang H, Zhang Y, Wang S (2008) Development of flow-through and dip-stick immunoassays for screening of sulfonamide residues. J Immunol Methods 337:1-6.
2. Yau KYF, Groves MAT, Li SH, Sheedy C, Lee H, Tanha J, MacKenzie CR, Jermutus L, Hall JC (2003) Selection of hapten-specific single-domain antibodies from a nonimmunized llama ribosome display library. J Immunol Methods 281:161-175. (Pubitemid 37324578)
3. Song SS, Lin F, Liu LQ, Kuang H, Wang LB, Xu CL (2010) Immunoaffinity removal and immunoassay for rhodamine B in chilli powder. Int J Food Sci Tech 45:2589-2595.
4. Hofstetter O, Lindstrom H, Hofstetter H (2002) Direct resolution of enantiomers in high-performance immunoaffinity chromatography under isocratic conditions. Anal Chem 74:2119-2125. (Pubitemid 34465411)
5. Curd J, Smith TW, Jaton JC, Haber E (1971) Isolation of digoxin-specific antibody and its uses in reversing effects of digoxin. Proc Natl Acad Sci USA 68:2401.
6. Smith TW, Butler VP, Haber E, Fozzard H, Marcus FI, Bremner WF, Schulman IC, Phillips A (1982) Treatment of life-threatening digitalis intoxication with digoxin-specific Fab antibody fragments - experience in 26 cases. New Engl J Med 307:1357-1362. (Pubitemid 13233011)
7. Fox BS, Kantak KM, Edwards MA, Black KM, Bollinger BK, Botka AJ, French TL, Thompson TL, Schad VC, Greenstein JL, Gefter ML, Exley MA, Swain PA, Briner TJ (1996) Efficacy of a therapeutic cocaine vaccine in rodent models. Nat Med 2:1129-1132. (Pubitemid 26338633)
8. Monnet C, Bettsworth F, Stura EA, Le Du MH, Menez R, Derrien L, Zinn-Justin S, Gilquin B, Sibai G, Battail-Poirot N, Jolivet M, Menez A, Arnaud M, Ducancel F, Charbonnier JB (2002) Highly specific anti-estradiol antibodies: structural characterisation and binding diversity. J Mol Biol 315:699-712. (Pubitemid 34729320)
9. Burmester J, Spinelli S, Pugliese L, Krebber A, Honegger A, Jung S, Schimmele B, Cambillau C, Pluckthun A (2001) Selection, characterization and x-ray structure of anti-ampicillin single-chain Fv fragments from phage-displayed murine antibody libraries. J Mol Biol 309:671-685. (Pubitemid 32595100)
10. Scotti C, Gherardi E (2006) Structural basis of affinity maturation of the TEPC15/Vkappa45.1 anti-2-phenyl-5-oxazolone antibodies. J Mol Biol 359:1161-1169. (Pubitemid 43903496)
11. Nakasako M, Oka T, Mashumo M, Takahashi H, Shimada I, Yamaguchi Y, Kato K, Arata Y (2005) Conformational dynamics of complementarity-determining region H3 of an anti-dansyl Fv fragment in the presence of its hapten. J Mol Biol 351:627-640. (Pubitemid 41021945)
12. Guddat LW, Shan L, Anchin JM, Linthicum DS, Edmundson AB (1994) Local and transmitted conformational changes on complexation of an anti-sweetener Fab. J Mol Biol 236:247-274. (Pubitemid 24148962)
13. Niemi MH, Takkinen K, Amundsen LK, Soderlund H, Rouvinen J, Hoyhtya M (2011) The testosterone binding mechanism of an antibody derived from a naive human scFv library. J Mol Recogn 24:209-219.
14. Midelfort KS, Hernandez HH, Lippow SM, Tidor B, Drennan CL, Wittrup KD (2004) Substantial energetic improvement with minimal structural perturbation in a high affinity mutant antibody. J Mol Biol 343:685-701. (Pubitemid 39311615)
15. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R (1993) Naturally occurring antibodies devoid of light chains. Nature 363:446-448. (Pubitemid 23179389)
16. Muyldermans S (2001) Single domain camel antibodies: current status. J Biotechnol 74:277-302.
17. Doyle PJ, Arbabi-Ghahroudi M, Gaudette N, Furzer G, Savard ME, Gleddie S, McLean MD, Mackenzie CR, Hall JC (2008) Cloning, expression, and characterization of a single-domain antibody fragment with affinity for 15-acetyl-deoxynivalenol. Mol Immunol 45:3703-3713.
18. Ladenson RC, Crimmins DL, Landt Y, Ladenson JH (2006) Isolation and characterization of a thermally stable recombinant anti-caffeine heavy-chain antibody fragment. Anal Chem 78:4501-4508.
19. Spinelli S, Frenken LGJ, Hermans P, Verrips T, Brown K, Tegoni M, Cambillau C (2000) Camelid heavy-chain variable domains provide efficient combining sites to haptens. Biochemistry 39:1217-1222. (Pubitemid 30090687)
20. Spinelli S, Tegoni M, Frenken L, van Vliet C, Cambillau C (2001) Lateral recognition of a dye hapten by a llama VHH domain. J Mol Biol 311:123-129. (Pubitemid 32735319)
21. De Genst EJ, Guilliams T, Wellens J, O'Day EM, Waudby CA, Meehan S, Dumoulin M, Hsu ST, Cremades N, Verschueren KH, Pardon E, Wyns L, Steyaert J, Christodoulou J, Dobson CM (2010) Structure and properties of a complex of alpha-synuclein and a single-domain camelid antibody. J Mol Biol 402:326-343.
22. Alvarez-Rueda N, Behar G, Ferre V, Pugniere M, Roquet F, Gastinel L, Jacquot C, Aubry J, Baty D, Barbet J, Birkle S (2007) Generation of llama single-domain antibodies against methotrexate, a prototypical hapten. Mol Immunol 44:1680-1690.
23. Bond CJ, Wiesmann C, Marsters JC, Jr, Sidhu SS (2005) A structure-based database of antibody variable domain diversity. J Mol Biol 348:699-709.
24. Ewert S, Honegger A, Pluckthun A (2004) Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering. Methods 34:184-199. (Pubitemid 39092813)
25. Saerens D, Pellis M, Loris R, Pardon E, Dumoulin M, Matagne A, Wyns L, Muyldermans S, Conrath K (2005) Identification of a universal VHH framework to graft non-canonical antigen-binding loops of camel single-domain antibodies. J Mol Biol 352:597-607. (Pubitemid 41225471)
26. Decanniere K, Desmyter A, Lauwereys M, Ghahroudi MA, Muyldermans S, Wyns L (1999) A single-domain antibody fragment in complex with RNase A: non-canonical loop structures and nanomolar affinity using two CDR loops. Structure 7:361-370. (Pubitemid 29190470)
27. Koide A, Tereshko V, Uysal S, Margalef K, Kossiakoff AA, Koide S (2007) Exploring the capacity of minimalist protein interfaces: interface energetics and affinity maturation to picomolar K(D) of a single-domain antibody with a flat paratope. J Mol Biol 373:941-953. (Pubitemid 47498439)
28. Tereshko V, Uysal S, Koide A, Margalef K, Koide S, Kossiakoff AA (2008) Toward chaperone-assisted crystallography: protein engineering enhancement of crystal packing and X-ray phasing capabilities of a camelid single-domain antibody (VHH) scaffold. Protein Sci 17:1175-1187. (Pubitemid 351930915)
29. Stites WE (1997) Protein-protein interactions: interface structure, binding, thermodynamics, and mutational analysis. Chem Rev 97:1233-1250.
30. Franklin MC, Carey KD, Vajdos FF, Leahy DJ, de Vos AM, Sliwkowski MX (2004) Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex. Cancer Cell 5:317-328. (Pubitemid 38482068)
31. Turnbull WB, Daranas AH (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J Am Chem Soc 125:14859-14866.
32. Sonneson GJ, Horn JR (2009) Hapten-induced dimerization of a single-domain VHH camelid antibody. Biochemistry 48:6693-6695.
33. Baca M, Presta LG, O'Connor SJ, Wells JA (1997) Antibody humanization using monovalent phage display. J Biol Chem 272:10678-10684. (Pubitemid 27181078)
34. Kunkel TA (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci USA 82:488-492.
35. Mandelbaum-Shavit F, Grossowicz N (1973) Carriermediated transport of folate in a mutant of Pediococcus cerevisiae. J Bacteriol 114:485-490.
36. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4:2411-2423.
37. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. (Pubitemid 27085611)
38. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Cryst 40:658-674. (Pubitemid 47080256)
39. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Cryst D50:760-763.
40. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Cryst D60:2126-2132. (Pubitemid 41742764)
41. DeLano WL (2002) The PyMOL Molecular Graphics System. San Carlos, CA, USA: DeLano Scientific.
42. Hubbard SJ, Thornton JM (1993) "NACCESS," Computer Program. Department of Biochemistry and Molecular Biology, University College London.