Discovery of functional antibodies targeting ion channels

Journal of Biomolecular Screening

Volumn 20, Issue 4, 2015, Pages 454-467

  Wilkinson, Trevor C I ^a   Gardener, Matthew J ^a   Williams, Wendy A ^a  

^a MEDIMMUNE   (United States)

Author keywords

antigens; ion channels; monoclonal antibodies; screening

Indexed keywords

ANTIGEN; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; ION CHANNEL; MONOCLONAL ANTIBODY; PROTEIN EAG 1; PURINERGIC P2X7 RECEPTOR; SODIUM CHANNEL NAV1.7; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; ANTIBODY;

ANTIBODY SPECIFICITY; BINDING AFFINITY; DRUG SCREENING; DRUG SELECTIVITY; DRUG TARGETING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVIEW; ANIMAL; IMMUNOLOGY;

ANIMALS; ANTIBODIES; HUMANS; ION CHANNELS;

EID: 84925759142     PISSN: 10870571     EISSN: 1552454X     Source Type: Journal    
DOI: 10.1177/1087057114560698     Document Type: Review

References (109)

1. Wickenden A., Priest B., Erdemli G.. Ion Channel Drug Discovery: Challenges and Future Directions. Future Med. Chem. 2012 ; 4: 661-679
2. Bagal S. K., Brown A. D., Cox P. J., et al. Ion Channels as Therapeutic Targets: A Drug Discovery Perspective. J. Med. Chem. 2013 ; 56: 593-624
3. Overington J. P., Al-Lazikani B., Hopkins A. L.. How Many Drug Targets Are There?. Nat. Rev. Drug. Disc. 2006 ; 5: 993-996
4. McGivern J. G.. Ziconotide: A Review of Its Pharmacology and Use in the Treatment of Pain. Neuropsych. Treat. Dis. 2007 ; 3: 69-85
5. Tradtrantip L., Namkung W., Verkman A. S.. Crofelemer, An Antisecretory Antidiarrheal Proanthocyanidin Oligomer Extracted from Croton lechleri, Targets Two Distinct Intestinal Chloride Channels. Mol. Pharmacol. 2010 ; 77: 69-78
6. Bosmans F., Swartz K. J.. Targeting Voltage Sensors in Sodium Channels with Spider Toxins. Trends Pharmacol. Sci. 2010 ; 31: 175-182
7. Beck A., Wurch T., Bailly C., et al. Strategies and Challenges for the Next Generation of Therapeutic Antibodies. Nat. Rev. Immunol. 2010 ; 10: 345-352
8. Pederson S. F., Stock C.. Ion Channels and Transporters in Cancer: Pathophysiology, Regulation and Clinical Potential. Cancer Res. 2013 ; 73: 1658-1661
9. Imbrici P., Camerino D. C., Tricarico D.. Major Channels Involved in Neuropsychiatric Disorders and Therapeutic Perspectives. Frontiers Genet. 2013 ; 4: 1-17
10. Srivastava R., Aslam M., Kalluri S. R., et al. Potassium Channel KIR4.1 as an Immune Target for Multiple Sclerosis. New Eng. J. Med. 2012 ; 367: 115-123
11. Huber S. M.. Oncochannels. Cell Calcium. 2013 ; 53: 241-255
12. Wemmie J. A., Taugher R. J., Kreple C. J.. Acid-Sensing Ion Channels in Pain and Disease. Nature Rev. Neurosci. 2013 ; 14: 461-471
13. Wulff H., Castle N. A., Pardo L. A.. Voltage-Gated Potassium Channels as Therapeutic Targets. Nat. Rev. Drug. Disc. 2009 ; 8: 982-1001
14. Perret D., Luo Z. D.. Targeting Voltage-Gated Calcium Channels for Neuropathic Pain Management. Neurotherapeutics. 2009 ; 6: 679-692
15. Mathie A.. Ion Channels as Novel Therapeutic Targets in the Treatment of Pain. J. Pharm. Pharmacol. 2010 ; 62: 1089-1095
16. Bennett D. L. H., Woods C. G.. Painful and Painless Channelopathies. Lancet Neurol. 2014 ; 13: 587-599
17. Lambert E. H., Eaton L. M., Rooke E. D.. Defect of Neuromuscular Conduction Associated with Malignant Neoplasm. Am. J. Physiol. 1956 ; 187: 612-613
18. Meriney S. D., Hulsizer S. C., Lennon V. A., et al. Lambert-Eaton Myasthenic Syndrome Immunoglobulins React with Multiple Types of Calcium Channels in Small-Cell Lung Carcinoma. Ann. Neurol. 1996 ; 40: 739-749
19. Newsom-Davis J., Buckley C., Clover L., et al. Autoimmune Disorders of Neuronal Potassium Channels. Ann. N.Y. Acad. Sci. 2003 ; 998: 202-210
20. Rana S. S., Ramanathan R. S., Small G., et al. Paraneoplastic Isaacs' Syndrome: A Case Series and Review of the Literature. J. Clin. Neuromusc. Dis. 2012 ; 13: 228-233
21. Yu F. K., Yarov-Yarovoy V., Gutman G. A., et al. Overview of Molecular Relationships in the Voltage-Gated Ion Channel Superfamily. Pharmacol. Rev. 2005 ; 57: 387-395
22. Li S., Gosling M., Poll C. T., et al. Therapeutic Scope of Modulation of Non-Voltage Gated Cation Channels. Drug Disc. Today. 2005 ; 10: 129-137
23. Kaczorowski G. J., McManus O. B., Priest B. T., et al. Ion Channels as Drug Targets: The Next GPCR's. J. Gen. Physiol. 2008 ; 131: 399-405
24. Eckford P. D. W., Li C., Ramjeesingh M., et al. Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Potentiator VX-770 (Ivacaftor) Opens the Defective Channel Gate of Mutant CFTR in a Phosphorylation-Dependent but ATP-Independent Manner. J. Biol. Chem. 2012 ; 287: 36639-36649
25. Sermet-Gaudelus I.. Ivacaftor Treatment in Patients with Cystic Fibrosis and the G551D-CFTR Mutation. Eur. Respir. Rev. 2013 ; 22: 66-71
26. Dimitrov D. Therapeutic Proteins: Methods and Protocols, Methods in Molecular Biology. Voynov V. Caravella J. A., ed. Humana Press: Totowa, NJ ; 2012: 1-26.
27. Carter P. J.. Potent Antibody Therapeutics by Design. Nat. Rev. Immunol. 2006 ; 6: 343-357
28. Hogarth P. M., Pietersz G. A.. Fc Receptor-Targeted Therapies for the Treatment of Inflammation, Cancer and Beyond. Nat. Rev. Drug. Disc. 2012 ; 11: 311-331
29. Nelson A. L., Dhimolea E., Reichart J. M.. Development Trends for Human Monoclonal Antibody Therapeutics. Nat. Rev. Drug. Disc. 2010 ; 9: 767-774
30. Reichart J. M.. Marketed Therapeutic Antibodies Compendium. mAbs. 2012 ; 4: 413-415
31. Groves M. A. T., Amanuel L., Campbell J. I., et al. Antibody VH and VL Recombination Using Phage and Ribosome Display Technologies Reveals Distinct Structural Routes to Affinity Improvements with VH-VL Interface Residues Providing Important Structural Diversity. mAbs. 2014 ; 6: 236-245
32. Atwal J. K., Chen Y., Chiu C., et al. A Therapeutic Antibody Targeting BACE1 Inhibits Amyloid-β Production in Vivo. Science Trans. Med. 2011 ; 3: 1-12
33. Yu Y. J., Zhang Y., Kenrick M., et al. Boosting Brain Uptake of a Therapeutic Antibody by Reducing its Affinity for a Transcytosis Target. Science Trans. Med. 2011 ; 3: 1-8
34. Niewoehner J., Bohrmann B., Collin L., et al. Increased Brain Penetration and Potency of a Therapeutic Antibody Using a Monovalent Molecular Shuttle. Neuron. 2014 ; 81: 49-60
35. Vaughan T. J., Williams A. J., Pritchard K., et al. Human Antibodies with Sub-Nanomolar Affinities Isolated from a Large Non-Immunised Phage Display Library. Nature Biotech. 1996 ; 14: 309-314
36. Schwimmer L. J., Huang B., Giang H., et al. Discovery of Diverse and Functional Antibodies from Large Human Repertoire Antibody Libraries. J. Immunol. Meth. 2013 ; 391: 60-71
37. Muyldermans S.. Nanobodies: Natural Single-Domain Antibodies. Ann. Rev. Biochem. 2013 ; 82: 775-797
38. Muji-Deli A., de Wit R. H., Verkaar F., et al. GPCR-Targeting Nanobodies: Attractive Research Tools, Diagnostics, and Therapeutics. Trends Pharm. Sci. 2014 ; 35: 247-255
39. Skerra A.. Alternative Non-Antibody Scaffolds for Molecular Recognition. Curr. Opin. Biotech. 2007 ; 18: 295-304
40. Gebauer M., Skerra A.. Engineered Protein Scaffolds as Next-Generation Antibody Therapeutics. Curr. Opin. Chem. Biol. 2009 ; 13: 245-255
41. Ablynx nv. Characterization of Anti-Kv1.3 Nanobodies and Activity in Inflammatory Model Systems. http://www.ablynx.com (accessed Jun 26, 2014).
42. Kawate T., Michel J. C., Birdsong W. T., et al. Crystal Structure of the ATP Gated P2X(4) Ion Channel in the Closed State. Nature. 2009 ; 460: 592-598
43. Mayer M. L.. Emerging Models of Glutamate Receptor Ion Channel Structure and Function. Structure. 2011 ; 19: 1370-1380
44. Buell G., Chessell I. P., Michel A. D., et al. Blockade of P2X7 Receptor Function with a Monoclonal Antibody. Blood. 1998 ; 92: 3251-3528
45. Ebersbach H., Proetzel G., Zhang C.. Antigen Presentation for the Generation of Binding Molecules. Meth. Mol Biol. 2012 ; 901: 1-10
46. Chiarelli P., Fazio V. M.. Mouse Monoclonal Antibodies in Biological Research: Strategies for High-Throughput Production. Biotechnol. Lett. 2008 ; 30: 1303-1310
47. Ebersbach H., Geisse S.. Antigen Generation and Display in Therapeutic Antibody Drug Discovery - a Neglected but Critical Player. Biotechnol. J. 2012 ; 7: 1-11
48. Chames P., Hoogenboom H. R., Henderikx P.. Selection of Antibodies against Biotinylated Peptides. Meth. Mol. Biol. 2002 ; 178: 147-157
49. Sommerfelt M. A.. Circular CCR5 Peptide Conjugates and Uses Thereof (WO2008074895). Exp. Opin. Ther. Patents. 2009 ; 19: 1323-1328
50. Zhang Y., Pool C., Sadler K., et al. Selection of Active scFv to G-Protein-Coupled Receptor CCR5 Using Surface Antigen-Mimicking Peptides. Biochemistry. 2004 ; 43: 12575-12584
51. Pepscan. Antibody Discovery to G-Protein Coupled Receptors. http://www.pepscan.com (accessed Jun 14, 2014).
52. Naylor J., Beech D. J.. Extracellular Ion Channel Inhibitor Antibodies. Open Drug Disc. J. 2009 ; 1: 36-42
53. Xu S-Z., Zeng F., Lei M., et al. Generation of Functional Ion-Channel Tools by E3 Targeting. Nat. Biotech. 2005 ; 23: 1289-1293
54. Gómez-Varela D., Zwick-Wallasch E., Knötgen H., et al. Monoclonal Antibody Blockade of the Human Eag1 Potassium Channel Function Exerts Antitumor Activity. Cancer Res. 2007 ; 67: 7343-7349
55. Klionsky L., Tamir R., Holzinger B., et al. A Polyclonal Antibody to the Prepore Loop of Transient Receptor Potential Vanilloid Type 1 Blocks Channel Activation. J. Pharm. Exp. Ther. 2006 ; 319: 192-198
56. Clare J. J. Expression and Analysis of Recombinant Ion Channels. Clare J. J. Tresize D. J., ed. Wiley-VCH: Weinheim, Germany ; 2006 :
57. Maue R. A.. Understanding Ion Channel Biology Suing Epitope Tags: Progress, Pitfalls and Promise. J. Cell. Physiol. 2007 ; 213: 618-625
58. Kawate T., Gouaux E.. Fluorescence-Detection Size-Exclusion Chromatography for Precrystallization Screening of Integral Membrane Proteins. Structure. 2006 ; 14: 673-681
59. Agharkar A., Rzadkowolski J., McBroom M., et al. Detergent Screening of the Human Voltage-Gated Proton Channel Using Fluorescence-Detection Size-Exclusion Chromatography. Prot. Sci. 2014 ; 23: 1136-1147
60. Stojilkovic S. S., Yan Z., Obsil T., et al. Structural Insights into the Function of P2X4: An ATP Gated Cation Channel of Neuroendocrine Cells. Cell. Mol. Neurobiol. 2010 ; 30: 1251-1258
61. Clontech. Tet-on 3G Tetracycline Inducible Expression System. http://www.clontech.com (accessed Jun 27, 2014).
62. Corin K., Baaske P., Geissler S., et al. Structure and Function Analyses of the Purified GPCR Human Vomeronasal Type 1 Receptor 1. Scientific Reports. 2011 ; 172: 1-6
63. Gaillet B., Gilbert R., Broussau S., et al. High-Level Recombinant Protein Production in CHO Cells Using Lentiviral Vectors and the Cumate Gene-Switch. Biotechnol. Bioeng. 2010 ; 106: 203-215
64. Johansson T., Norris T., Peilot-Sjögren H.. Yellow Fluorescent Protein-Based Assay to Measure GABAA Channel Activation and Allosteric Modulation in CHO-K1 Cells. PLoS One. 2013 ; 8: e59429
65. Willis S., Davidoff C., Schilling J., et al. Virus-Like Particles as Quantitative Probes of Membrane Protein Interactions. Biochemistry. 2008 ; 47: 6988-6990
66. Sulli C., Banik S. S. R., Schilling J., et al. Detection of Proton Movement Directly across Viral Membranes to Identify Novel Influenza Virus M2 Inhibitors. J. Virol. 2013 ; 87: 10679-10686
67. Integral Molecular. http://www.integralmolecular.com (accessed Nov 6, 2014).
68. Doyle D. A., Cabral J. M., Pfuetzner R. A., et al. The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity. Science. 1998 ; 280: 69-77
69. Robertson N., Jazayeri A., Errey J., et al. The Properties of Thermostabilised G Protein-Coupled Receptors (StaRs) and Their Use in Drug Discovery. Neuropharmacology. 2011 ; 60: 36-44
70. Magnani F., Shibata Y., Serano-Vega M. J., et al. Co-Evolving Stability and Conformational Homogeneity of the Human Adenosine A2a Receptor. Proc. Natl. Acad. Sci. 2008 ; 105: 10744-10749
71. Abdul-Hussein S., Andrell J., Tate C. G.. Thermostabilisation of the Serotonin Transporter in a Cocaine-Bound Conformation. J. Mol. Biol. 2013 ; 425: 2198-2207
72. Hutchings C. J., Cseke G., Osborne G., et al. Monoclonal Anti-β1-Adrenergic Receptor Antibodies Activate G Protein Signalling in the Absence of β-Arrestin Recruitment. mAbs. 2014 ; 6: 246-261
73. Chowdhury P. S.. DNA Immunization as a Means to Generate Antibodies to Proteins. Methods. Mol. Biol. 2003 ; 207: 57-62
74. Chowdhury P. S., Gallo M., Pastan I.. Generation of High Titer Antisera in Rabbits by DNA Immunization. J. Immunol. Methods. 2001 ; 249: 147-154
75. Hazen M., Bhakta S., Vij R., et al. An Improved and Robust DNA Immunization Method to Develop Antibodies against Extra-Cellular Loops of Multi-Transmembrane Proteins. mAbs. 2014 ; 6: 95-107
76. Lee K. J., Wang W., Padaki R., et al. Mouse Monoclonal Antibodies to Transient Receptor Potential Ankyrin 1 Act as Antagonists of Multiple Modes of Channel Activation. J. Pharm. Exp. Ther. 2014 ; 350: 223-231
77. Sin H., Li M.. 2013. Antibody Therapeutics Targeting Ion Channels: Are We There Yet?. Acta Pharmacologica Sinica. 2013 ; 34: 199-204
78. Brass D., Grably M. R., Bronstein-Sitton N., et al. Using Antibodies against P2Y and P2X Receptors in Purinergic Signaling Research. Purinergic Sig. 2012 ; 8: 61-79
79. Smith A. J., Hancock M. K., Bi K., et al. Feasibility of Implementing Cell-Based Pathway Reporter Assays in Early High-Throughput Screening Assay Cascades for Antibody Drug Discovery. J. Biomol. Screening. 2012 ; 17: 713-726
80. Lee J-H., Park C-K., Chen G., et al. A Monoclonal Antibody That Targets a Nav1.7 Channel Voltage Sensor for Pain and Itch Relief. Cell. 2014 ; 157: 1-12
81. Sohma Y., Fujita R., Katoh S., et al. Recognition of Liposome-Bound Antigens by Antipeptide Antibody. Appl. Biochem. Biotech. 1993 ; 38: 179-188
82. Yao F., Theopold C., Hoeller D., et al. Highly Efficient Regulation of Gene Expression by Tetracycline in a Replication-Defective Herpes Simplex Viral Vector. Mol. Ther. 2006 ; 13: 1133-1141
83. Lee R., Tran M., Nocerini M., et al. 2008. A High-Throughput Hybridoma Selection Method Using Fluorometric Microvolume Assay Technology. J. Biomol. Screening. 2008 ; 13: 210-217
84. Neher E., Sakmann B.. Single-Channel Currents Recorded from Membrane of Denervated Frog Muscle Fibres. Nature. 1976 ; 260: 799-802
85. Neher E., Sakmann B., Steinbach J. H.. The Extracellular Patch Clamp: A Method for Resolving Currents through Individual Open Channels in Biological Membranes. Pflug Archiv Eur. J. Physiol. 1978 ; 375 (2). 219-228
86. Dunlop J., Bowlby M., Peri R., et al. High-Throughput Electrophysiology: An Emerging Paradigm for Ion-Channel Screening and Physiology. Nat. Rev. Drug Disc. 2008 ; 7: 358-368
87. Trivedi T., Liu J., Liu R, et al. Advances in Functional Assays for High-Throughput Screening of Ion Channels Targets. Expert Opin. Drug Disc.. 2010 ; 5 (10). 995-1006
88. Kuryshev Y. A., Brown A. M., Duzic E., et al. Evaluating State Dependence and Subtype Selectivity of Calcium Channel Modulators in Automated Electrophysiology Assays. Assay Drug Dev Tech. 2014 ; 12: 110-119
89. Cariuk P., Gardener M. J., Vaughan T. J.. Evolution of Biologics Screening Technologies. Pharmaceuticals. 2013 ; 6: 681-688
90. McManus O. B.. HTS Assays for Developing the Molecular Pharmacology of Ion Channels. Curr. Opin. Pharmacol. 2014 ; 15: 91-96
91. Falconer M., Smith F., Surah-Narwal S., et al. High-Throughput Screening for Ion Channel Modulators. J. Biomol. Screen. 2002 ; 7: 460-465
92. North R. A., Jarvis M. F.. P2X Receptors as Drug Targets. Mol. Pharmacol. 2013 ; 83: 759-769
93. Roy M-L., Dumaine R., Brown A.M.. HERG, a Primary Ventricular Target of the Nonsedating Antihistamine Terfanidine. Circulation. 1996 ; 94: 817-823
94. Srikanth S., Gwack Y.. Orai1, STIM1 and Their Associating Partners. J. Physiol. 2012 ; 590: 4169-4177
95. Lin F-F., Elliott R., Colombero A., et al. Generation and Characterization of Fully Human Monoclonal Antibodies against Human Orai1 for Autoimmune Disease. J. Pharm. Exp. Ther. 2013 ; 345: 225-238
96. Cox J. H., Hussell S., Sondergaard H., et al. Antibody-Mediated Targeting of the Orai1 Calcium Channel Inhibits T Cell Function. Plos One. 2013 ; 8: 1-11
97. Jakobovits A., Amado R. G., Yang X., et al. From Xenomouse Technology to Panitimumab, the First Fully Human Antibody Product from Transgenic Mice. Nat. Biotech. 2007 ; 10: 1134-1143
98. Moran M. M., McAlexander M. A., Bíró T., et al. Transient Receptor Potential Channels as Therapeutic Targets. Nat. Rev. Drug Disc. 2011 ; 10: 601-620
99. Dib-Haji S. D., Yang Y., Black J. A., et al. The Nav1.7 Sodium Channel: From Molecule to Man. Nat. Rev. Neurosci. 2013 ; 14: 49-62
100. Catterall W. A.. Structure and Function of Voltage-Gated Sodium Channels at Atomic Resolution. Exp. Physiol. 2014 ; 99: 35-51
101. Clare J. J.. Targeting Voltage-Gated Sodium Channels for Pain Therapy. Expert Opin. Investig. Drugs. 2010 ; 19: 45-62
102. Wu M-T., Huang P-Y., Yen C-T., et al. A Novel SCN9A Mutation Responsible for Primary Erythromelalgia and Is Resistant to the Treatment of Sodium Channel Blockers. Plos One. 2013 ; 8: e55212
103. Catterall W. A.. Ion Channel Voltage Sensors: Structure, Function and Pathophysiology. Neuron. 2010 ; 67: 915-928
104. Minassian N. A., Gibbs A., Shih A. Y., et al. Analysis of the Structural and Molecular Basis of Voltage-Sensitive Sodium Channel Inhibition by the Spider Toxin Huwentoxin-IV (μ-TRTX-Hh2a). J. Biol. Chem. 2013 ; 288: 22707-22720
105. Liu Z., Cai T., Zhu Q., et al. Structure and Function of Hainantoxin-III, a Selective Antagonist of Neuronal Tetrodotoxin-Sensitive Voltage Gated Sodium Channels Isolated from the Chinese Bird Spider Ornithoctonus hainana. J. Biol. Chem. 2013 ; 288: 20392-20403
106. Sobolevsky A. I., Rosconi M. P., Gouaux E. C.. X-Ray Structure, Symmetry and Mechanism of an AMPA-Subtype Glutamate Receptor. Nature. 2009 ; 462: 745-756
107. Tang L., Gamel El-Din T. M., Payendah J., et al. Structural Basis for Ca2+ Selectivity of a Voltage-Gated Calcium Channel. Nature. 2014 ; 505: 56-61
108. Harris L. J., Larson S. B., Hasel K. W., et al. Refined Structure of an Intact IgG2a Monoclonal Antibody. Biochemistry. 1997 ; 36: 1581-1597
109. Miller S., Rao S., Wang W., et al. Antibodies to the Extracellular Pore Loop of TRPM8 Act as Antagonists of Channel Activation. Plos One. 2014 ; 9: e107151