FRET based quantification and screening technology platform for the interactions of leukocyte function-associated antigen-1 (LFA-1) with InterCellular adhesion molecule-1 (ICAM-1)

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Chakraborty, Sandeep ^a   Núñez, David ^b,c   Hu, Shih Yang ^a   Domingo, María Pilar ^b,c   Pardo, Julian ^c,d,e,f   Karmenyan, Artashes ^a   Gálvez, Eva Ma ^b,c   Chiou, Arthur ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTO DE CARBOQUÍMICA   (Spain)

^c INSTITUTO ARAGONÉS DE CIENCIAS DE LA SALUD   (Spain)

^d UNIVERSITY OF ZARAGOZA   (Spain)

^e ARAID   (Spain)

^f Instituto de Nanociencia y Materiales de Aragón   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ARTICLE; BINDING AFFINITY; BINDING ASSAY; CONTROLLED STUDY; DISSOCIATION CONSTANT; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; PROCESS DEVELOPMENT; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STEADY STATE;

EID: 84904480125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102572     Document Type: Article

References (65)

1. Hynes RO (2002) Integrins: bidirectional, allosteric signalling machines. Cell 110: 673-687.
2. Xingyuan M, Wenyun Z, Tianwen W (2006) Leukocyte function-associated antigen-1: structure, function and application prospects. Protein Peptide Lett 13: 397-400.
3. 2) integrin. PNAS 92: 10277-10281.
4. Hogg N, Patzak I, Willenbrock F (2011) The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol 11: 416-426.
5. Rahman A, Fazal F (2009) Hug tightly and say goodbye: role of endothelial ICAM-1 in leukocyte transmigration. Antioxid Redox Signaling 11(4): 823-839.
6. Long EO (2011) ICAM-1: getting a grip on leukocyte adhesion. J. Immunol 186: 5021-5023.
7. de Fougerolles AD, Stacker SA, Schwarting R, Springer TA (1991) Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1. J Exp Med 174: 253-267.
8. Fawcett J, Holness CLL, Needham LA, Turley H, Gatter KC, et al. (1992) Molecular cloning of ICAM-3, a third ligand for LFA-1, constitutively expressed on resting leukocytes. Nature 360: 481-484.
9. Estecha A, Aguilera-Montilla N, Sanchez-Mateos P, Puig-Kröger A (2012) RUNX3 regulates intercellular adhesion molecule-3 (ICAM-3) expression during macrophage differenctiation and monocyte extravasation. PloS ONE 7(3): e33313.
10. Ihanus E, Uotila L, Stefanidakis M, Bailly P, Cartron J, et al. (2003) Characterization of ICAM-4 binding to the I domains of the CD11a/CD18 and CD11b/CD18 leukocyte integrins. Eur J Biochem 270(8): 1710-1723. (Pubitemid 36532530)
11. Yang H (2012) Structure, expression, and function of ICAM-5. Comp Funct Genomics 2012: 368938.
12. Shimoka M, Lu C, Palframan R, von Andrian UH, Takagi J, et al. (2001) Reversibly locking a protein fold in an active conformation with a disulfide bond: integrin aL I domains with high affinity and antagonist activity in vivo. PNAS 98: 6009-6014. (Pubitemid 32488184)
13. de Stolpe AV, der Saaq PTV (1996) Intercellular adhesion molecule-1. J Mol Med 74(1): 13-33.
14. Springer TA (1990) Adhesion receptors of the immune system. Nature 346: 425-434.
15. Diamond MS, Staunton DE, de Fougerolles AR, Stacker SA, Garcia-Aguilar J, et al. (1990) ICAM-1 (CD54): A counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol 111(6, 2): 3129-3139.
16. Fuchs R, Blaas D (2010) Uncoating of human rhinovirus. Rev Med Virol 20: 281-297.
17. Xiao C, Bator-Kelly CM, Rieder E, Chipman PR, Craig A, et al. (2005) The crystal structure of Coxsackievirus A21 and its interaction with ICAM-1. Structure 13: 1019-1033. (Pubitemid 40943333)
18. Bernabeu M, Lopez FJ, Ferrer M, Martin-Jular L, Razaname A, et al. (2012) Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor. Cell Microbiol 14(3): 386-400.
19. Shimoka M, Xiao T, Liu JH, Yang Y, Dong Y, et al. (2003) Structures of the αI I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112: 99-111. (Pubitemid 36106422)
20. Luo BH, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25: 619-647. (Pubitemid 46697919)
21. Dransfield I, Cabañas C, Craig A, Hogg N (1992) Divalent cation regulation of the function of the leukocyte integrin LFA-1. J Cell Biol 116 (1): 219-226.
22. Huang C, Springer TA (1995) A binding interface on the I-domain of lymphocyte function-associated antigen-1 (LFA-1) required for specific interaction with intercellular adhesion molecule 1 (ICAM-1). J Biol Chem 270 (32): 19008-19016.
23. Kinashi T (2007) Integrin regulation of lymphocyte trafficking: lessons from structural and signaling studies. Adv Immunol 93: 185-227.
24. Dustin ML (2009) The cellular context of T cell signalling. Immunity 30(4): 482-492.
25. Yusuf-Makagiansar H, Anderson ME, Yakovleva TV, Murray JS, Siahaan TJ (2002) Inhibition of LFA-1/ICAM-1 and VLA-4/VCAM-1 as a therapeutic approach to inflammation and autoimmune diseases. Med Res Rev 22(2): 146-167. (Pubitemid 34160583)
26. Steinman L (1996) A few autoreactive cells in an autoimmune infiltrate control a vast population of nonspecific cells: a tale of smart bombs and the infantry. PNAS 93: 2253-2256.
27. Lou J, Chofflon M, Julliard C, Donati Y, Mili N, et al. (1997) Brain microvascular endothelial cells and leukocytes derived from patients with multiple sclerosis exhibit increased adhesion capacity. NeuroReport 8(3): 629-633. (Pubitemid 27128206)
28. Barbeau B, Fortin JF, Genois N, Tremblay MJ (1998) Modulation of human immunodeficiency virus type 1-induced syncytium formation by the conformational state of LFA-1 determined by a new luciferase-based syncytium quantitative assay. J Virol 72(9): 7125-7136. (Pubitemid 28377841)
29. Zhu XW, Gong JP (2013) Expression and role of ICAM-1 in the occurrence and development of hepatocellular carcinoma. Asian Pacific J Caner Prev 14(3): 1579-1583.
30. Zheng Y, Yang J, Qian J, Qiu P, Hanabuchi S, et al. (2013) PSGL-1/selectin and ICAM-1/CD18 interactions are involved in macrophage-induced drug resistance in myeloma. Leukemia 27 (3): 702-710.
31. Isobe M, Yagita H, Okumura K (1992) Specific acceptance of cardiac allograft after treatment with antibodies to ICAM-1 and LFA-1. Science 255: 1125-1127.
32. Gottileb AB, Krugger JG, Wittkowski K (2002) Psoriasis as a model for T-cell mediated disease: immunobiologicand clinical effects of treatment with multiple doses of efalizumab, an anti-CD11a antibody. Arch Dermatol 138 (5): 591-600.
33. Kavanaugh AF, David LS, Nicholas LA, Norris SH, Rothlein R, et al. (1994) Treatment of refractory rheumatoid arthritis with a monoclonal antibody to intracellular adhesion molecule-1. Arthritis Rheum 37: 992-999. (Pubitemid 24222089)
34. Weitz-Schimdt G (2002) Statins as anti-inflammatory agents. Trends Pharmacol Sci 23(10): 482-487.
35. Zhou CL, Lu R, Lin G, Yao Z (2011) The latest developments in synthetic peptides with immunoregulatory activities. Peptides 32(2): 408-414.
36. Tibbetts SA, Jois DSS, Siahaan TJ, Benedict SH, Chan MA (2000) Linear and cyclic LFA-1 and ICAM-1 peptides inhibit T-cell adhesion and function. Peptides 21: 1161-1167.
37. Anderson ME, Siahaan TJ (2003) Targeting ICAM-1/LFA-1 interaction for controlling autoimmune diseases: designing peptide and small molecule inhibitors. Peptides 24: 487-501. (Pubitemid 36561224)
38. Sun Y, Rombola C, Jyothikumar V, Periasamy A (2013) Förster resonance energy transfer microscopy and spectroscopy for localizing protein-protien interactions in living cells. Cytometry A 83A: 780-793.
39. Heib AR, D'Arcy S, Kramer MA, White AE, Luger K (2012) Fluorescence strategies for high-throughput quantification of protein interactions. Nucl Acids Res 40(5): e33.
40. rd ed. New York: Plenum. 443 p.
41. Tominaga Y, Kita Y, Satoh A, Asai S, Kato K, et al. (1998) Affinity and Kinetic analysis of the molecular interaction of ICAM-1 and leukocyte function-associated antigen-1. J Immunol 161: 4016-4022. (Pubitemid 28468979)
42. Pierce MM, Raman CS, Nall BT (1999) Isothermal titration calorimetry of protein-protein interactions. Methods 19: 213-221. (Pubitemid 29515856)
43. Hulme E, Trevethick M (2010) Ligand binding assays at equilibrium: validation and interpretation. Br J Pharmacol 161: 1219-1237.
44. Grünwald D, Cardoso MC, Leonhardt H (2005) Diffusion and binding properties investigated by fluorescence correlation spectroscopy (FCS). Curr Pharm Biotechnol 6: 381-386. (Pubitemid 41644881)
45. Tsuganezawa K, Shinohara Y, Ogawa N, Tsuboi S, Okada N, et al. (2013) Two-colored fluorescence correlation spectroscopy screening for LC3-P62 interaction inhibitors. J Biomol Screen 18(9): 1103-1109.
46. Chen H, Puhl HLIII, Ikeda SR (2007) Estimating protein-protein interactions affinity in living cells using quantitative Forster resonance energy transfer measurements. J Biomed Opt 12 (5): 054011.
47. Martin SF, Tatham MH, Hay RT, Samuel IDW (2008) Quantitative analysis of multi-protein interactions using FRET: application to the SUMO pathway. Protein Sci. 17: 777-784. (Pubitemid 351480871)
48. Song Y, Madahar V, Liao J (2010) Development of FRET assay into quantitative and high-throughput screening technology platforms for protein-protien interactions. Ann Biomed Eng 39(4): 1224-1234.
49. Song Y, Rodgers VGJ, Schultz JS, Liao J (2012) Protein interactions affinity determination by quantitative FRET technology. Biotechnol Bioeng 109(11): 2875-2883.
50. Núñez D, Domingo MP, Sanchez-Martínez D, Cebolla V, Chiou A, et al. (2013) Recombinant production of human ICAM-1 chimeras by single step on column refolding and purification. Process Biochem 48: 708-715.
51. Medintz IL, Clapp AR, Mattoussi H, Goldman ER, Fisher B, et al. (2003) Self-assembled nanoscale biosensors based on quantum dot FRET donors. Nat Mater 2: 630-638.
52. Bojarski P, kulak L, Walczewska-Szewc K, Synak A, Marzullo VM, et al. (2011) Long-distance FRET analysis: a monte carlo simulation study. J Phys Chem B 115: 10120-10125.
53. Maliwal BP, Raut S, Fudala R, D'Auria S, Marzullo VM, et al. (2012) Extending förster resonance energy transfer measurements beyond 100 Å using common organic fluorophores: enhanced transfer in the presence of multiple acceptors. J Biomed Opt 17(1): 011006.
54. Table 1.5 Fluorescence quantum yields (QY) and lifetimes (τ) for alexa fluor dyes. Available: http://www.lifetechnologies.com/tw/zt/home/ references/molecular-probes-the-handbook/tables/fluorescence-quantum-yields-and- lifetimes-for-alexa-fluor-dyes.html. Accessed 26 May 2014.
55. Wu SH, Núnez D, Hu SY, Domingo MP, Chen YC, et al. (2014) The effect of acidic pH on the inhibitory efficacy of peptides against the interaction ICAM-1/LFA-1 studied by surface plasmon resonance (SPR). Biosens Bioelectron 56: 159-166.
56. Lichlyter DJ, Grant SA, Soykan O (2003) Development of a novel FRET immunosensor technique. Biosens Bioelectron 19: 219-226. (Pubitemid 37377968)
57. Corsini A, Maggi FM, Catapano AL (1995) Pharmacology of competitive inhibitors of HMG-CoA reductase. Pharmacol Res 31: 9-27.
58. Kallen J, Welzenbach K, Ramage P, Geyl D, Kriwacki R, et al. (1999) Structural basis for LFA-1 inhibition upon lovastatin binding to the CD11a I-domain. J Mol Biol 292(1): 1-9. (Pubitemid 29425648)
59. Giguère JF, Tremblay MJ (2004) Statin compounds reduce human immunodeficiency virus type 1 replication by preventing the interaction between virion-associated host intercellular adhesion molecule 1 and its natural cell surface ligand LFA-1. J Virol 78(21): 12062-12065.
60. Liu L, Gei G, Liu Z, He Z, Xiao S, et al. (2008) Two photon excitation fluorescence resonance energy transfer with small organic molecule as energy donor for bioassay. Bioconjugate Chem 19: 574-579. (Pubitemid 351294932)
61. Bossis G, Chmielarska K, Gärtner U, Pichler A, Stieger E, et al. (2005) A fluorescence resonance energy transfer-based assay to study SUMO modification in solution. Methods Enzymol 398: 20-32. (Pubitemid 41578871)
62. Stankovic-Valentin N, Kozaczkiewicz L, Curth K, Melchior F (2009) An in vitro FRET-based assay for the analysis of SUMO conjugation and isopeptidase cleavage. Methods Mol Biol 497: 241-251.
63. Berney C, Danuser G (2003) FRET or no FRET: a quantitative comparison. Biophys J 84: 3992-4010. (Pubitemid 36637892)
64. Ciubotaru M, Kriatchko AN, Swanson PC, Bright FV, Schatz DG (2007) Fluorescence resonance energy transfer analysis of recombination signal sequence configuration in the RAG1/2 synaptic complex. Mol Cell Biol 27 (13): 4745-4758. (Pubitemid 47016128)
65. Fairclough RH, Cantor CR (1978) The use of singlet-singlet energy transfer to study macromolecular assemblies. Methods Enzymol 48: 347-379.