A novel luminescence-based method for the detection of functionally active antibodies to muscarinic acetylcholine receptors of the M3 type (mAchR3) in patients' sera

Clinical and Experimental Immunology

Volumn 177, Issue 1, 2014, Pages 179-189

  Preuss, B ^a   Tunaru, S ^b   Henes, J ^a   Offermanns, S ^b   Klein, R ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Aequorin GFP; Anti mAchR3 antibodies; CHO cells; Luminometer; Sj gren's disease

Indexed keywords

AEQUORIN; ANTIBODY; ATROPINE; CALCIUM ION; CARBACHOL; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN G; MUSCARINIC M3 RECEPTOR; MUSCARINIC M3 RECEPTOR ANTIBODY; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; ANTIBODY DETECTION; ANTIBODY ISOLATION; ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; BLOOD DONOR; CALCIUM CELL LEVEL; CELL DENSITY; CHO CELL LINE; CONTROLLED STUDY; ENERGY TRANSFER; FEMALE; GENETIC TRANSFECTION; HUMAN; LUMINESCENCE; MAJOR CLINICAL STUDY; MALE; MICROFLUOROMETRY; MYASTHENIA GRAVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SJOEGREN SYNDROME; SYSTEMIC SCLEROSIS;

AEQUORIN/GFP; ANTI-MACHR3 ANTIBODIES; CHO CELLS; LUMINOMETER; SJÖGREN'S DISEASE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; AUTOANTIBODIES; CALCIUM SIGNALING; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; LUMINESCENT MEASUREMENTS; MIDDLE AGED; MYASTHENIA GRAVIS; PREVALENCE; RECEPTOR, MUSCARINIC M3; REPRODUCIBILITY OF RESULTS; SCLERODERMA, SYSTEMIC; SENSITIVITY AND SPECIFICITY; SEROLOGIC TESTS; SJOGREN'S SYNDROME; YOUNG ADULT;

EID: 84904241351     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12324     Document Type: Article

References (67)

1. Bahn RS. Graves' ophthalmopathy. N Engl J Med 2010; 362:726-738.
2. Gomez AM, Van Den Broeck J, Vrolix K etal. Antibody effector mechanisms in myasthenia gravis-pathogenesis at the neuromuscular junction. Autoimmunity 2010; 43:353-370.
3. Jahns R, Schlipp A, Boivin V, Lohse MJ. Targeting receptor antibodies in immune cardiomyopathy. Semin Thromb Hemost 2010; 36:212-218.
4. Bacman S, Sterin-Borda L, Camusso JJ, Arana R, Hubscher O, Borda E. Circulating antibodies against rat parotid gland M3 muscarinic receptors in primary Sjogren's syndrome. Clin Exp Immunol 1996; 104:454-459.
5. Baroni SS, Santillo M, Bevilacqua F etal. Stimulatory autoantibodies to the PDGF receptor in systemic sclerosis. N Engl J Med 2006; 354:2667-2676.
6. Perez Leiros C, Sterin-Borda L, Hubscher O, Arana R, Borda ES. Activation of nitric oxide signaling through muscarinic receptors in submandibular glands by primary Sjogren syndrome antibodies. Clin Immunol 1999; 90:190-195.
7. Watson EL, Abel PW, DiJulio D etal. Identification of muscarinic receptor subtypes in mouse parotid gland. Am J Physiol 1996; 271:C905-913.
8. Cha S, Singson E, Cornelius J, Yagna JP, Knot HJ, Peck AB. Muscarinic acetylcholine type-3 receptor desensitization due to chronic exposure to Sjogren's syndrome-associated autoantibodies. J Rheumatol 2006; 33:296-306.
9. Dawson L, Tobin A, Smith P, Gordon T. Antimuscarinic antibodies in Sjogren's syndrome: where are we, and where are we going? Arthritis Rheum 2005; 52:2984-2995.
10. Dawson LJ, Stanbury J, Venn N, Hasdimir B, Rogers SN, Smith PM. Antimuscarinic antibodies in primary Sjogren's syndrome reversibly inhibit the mechanism of fluid secretion by human submandibular salivary acinar cells. Arthritis Rheum 2006; 54:1165-1173.
11. Koo NY, Li J, Hwang SM etal. Functional epitope of muscarinic type 3 receptor which interacts with autoantibodies from Sjogren's syndrome patients. Rheumatology 2008; 47:828-833.
12. Kovacs L, Feher E, Bodnar I etal. Demonstration of autoantibody binding to muscarinic acetylcholine receptors in the salivary gland in primary Sjogren's syndrome. Clin Immunol 2008; 128:269-276.
13. Nikolov NP, Illei GG. Pathogenesis of Sjogren's syndrome. Curr Opin Rheumatol 2009; 21:465-470.
14. Orman B, Sterin-Borda L, De Couto Pita A, Reina S, Borda E. Anti-brain cholinergic auto antibodies from primary Sjogren syndrome sera modify simultaneously cerebral nitric oxide and prostaglandin biosynthesis. Int Immunopharmacol 2007; 7:1535-1543.
15. Park K, Park S, Jackson MW. The inhibitory effects of antimuscarinic autoantibodies in the sera of primary Sjogren syndrome patients on the gastrointestinal motility. Mol Immunol 2013; 56:583-587.
16. Bonner TI, Buckley NJ, Young AC, Brann MR. Identification of a family of muscarinic acetylcholine receptor genes. Science 1987; 237:527-532.
17. Bonner TI, Young AC, Brann MR, Buckley NJ. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron 1988; 1:403-410.
18. Liao CF, Themmen AP, Joho R, Barberis C, Birnbaumer M, Birnbaumer L. Molecular cloning and expression of a fifth muscarinic acetylcholine receptor. J Biol Chem 1989; 264:7328-7337.
19. Offermanns S, Wieland T, Homann D etal. Transfected muscarinic acetylcholine receptors selectively couple to Gi-type G proteins and Gq/11. Mol Pharmacol 1994; 45:890-898.
20. Abrams P, Andersson KE, Buccafusco JJ etal. Muscarinic receptors: their distribution and function in body systems, and the implications for treating overactive bladder. Br J Pharmacol 2006; 148:565-578.
21. Cavill D, Waterman SA, Gordon TP. Antibodies raised against the second extracellular loop of the human muscarinic M3 receptor mimic functional autoantibodies in Sjogren's syndrome. Scand J Immunol 2004; 59:261-266.
22. Goldblatt F, Gordon TP, Waterman SA. Antibody-mediated gastrointestinal dysmotility in scleroderma. Gastroenterology 2002; 123:1144-1150.
23. Waterman SA, Gordon TP, Rischmueller M. Inhibitory effects of muscarinic receptor autoantibodies on parasympathetic neurotransmission in Sjogren's syndrome. Arthritis Rheum 2000; 43:1647-1654.
24. Park K, Haberberger RV, Gordon TP, Jackson MW. Antibodies interfering with the type 3 muscarinic receptor pathway inhibit gastrointestinal motility and cholinergic neurotransmission in Sjogren's syndrome. Arthritis Rheum 2011; 63:1426-1434.
25. Bacman S, Perez Leiros C, Sterin-Borda L, Hubscher O, Arana R, Borda E. Autoantibodies against lacrimal gland M3 muscarinic acetylcholine receptors in patients with primary Sjogren's syndrome. Invest Ophthalmol Vis Sci 1998; 39:151-156.
26. Berra A, Sterin-Borda L, Bacman S, Borda E. Role of salivary IgA in the pathogenesis of Sjogren syndrome. Clin Immunol 2002; 104:49-57.
27. Li J, Ha YM, Ku NY etal. Inhibitory effects of autoantibodies on the muscarinic receptors in Sjogren's syndrome. Lab Invest 2004; 84:1430-1438.
28. Tsuboi H, Matsumoto I, Wakamatsu E etal. New epitopes and function of anti-M3 muscarinic acetylcholine receptor antibodies in patients with Sjögren's syndrome. Clin Exp Immunol 2010; 162:53-61.
29. Dawson LJ, Allison HE, Stanbury J, Fitzgerald D, Smith PM. Putative anti-muscarinic antibodies cannot be detected in patients with primary Sjogren's syndrome using conventional immunological approaches. Rheumatology 2004; 43:1488-1495.
30. Jin M, Hwang SM, Davies AJ etal. Autoantibodies in primary Sjogren's syndrome patients induce internalization of muscarinic type 3 receptors. Biochim Biophys Acta 2012; 1822:161-167.
31. Persson KE, Lee CT, Marsh K, Beeson JG. Development and optimization of high-throughput methods to measure Plasmodium falciparum-specific growth inhibitory antibodies. J Clin Microbiol 2006; 44:1665-1673.
32. Bacman S, Berra A, Sterin-Borda L, Borda E. Muscarinic acetylcholine receptor antibodies as a new marker of dry eye Sjogren syndrome. Invest Ophthalmol Vis Sci 2001; 42:321-327.
33. Cavill D, Waterman SA, Gordon TP. Failure to detect antibodies to extracellular loop peptides of the muscarinic M3 receptor in primary Sjogren's syndrome. J Rheumatol 2002; 29:1342-1344.
34. He J, Guo JP, Ding Y etal. Diagnostic significance of measuring antibodies to cyclic type 3 muscarinic acetylcholine receptor peptides in primary Sjogren's syndrome. Rheumatology 2011; 50:879-884.
35. Kawaguchi Y, Nakamura Y, Matsumoto I etal. Muscarinic-3 acetylcholine receptor autoantibody in patients with systemic sclerosis: contribution to severe gastrointestinal tract dysmotility. Ann Rheum Dis 2009; 68:710-714.
36. Kovacs L, Marczinovits I, Gyorgy A etal. Clinical associations of autoantibodies to human muscarinic acetylcholine receptor 3(213-228) in primary Sjogren's syndrome. Rheumatology 2005; 44:1021-1025.
37. Li YN, Guo JP, He J etal. Serum IgA against type 3 muscarinic acetylcholine receptor is a novel marker in diagnosis of Sjogren's syndrome. Chin Med J 2011; 124:2490-2495.
38. Marczinovits I, Kovacs L, Gyorgy A etal. A peptide of human muscarinic acetylcholine receptor 3 is antigenic in primary Sjogren's syndrome. J Autoimmun 2005; 24:47-54.
39. Naito Y, Matsumoto I, Wakamatsu E etal. Muscarinic acetylcholine receptor autoantibodies in patients with Sjogren's syndrome. Ann Rheum Dis 2005; 64:510-511.
40. Roescher N, Kingman A, Shirota Y, Chiorini JA, Illei GG. Peptide-based ELISAs are not sensitive and specific enough to detect muscarinic receptor type 3 autoantibodies in serum from patients with Sjogren's syndrome. Ann Rheum Dis 2011; 70:235-236.
41. Baubet V, Le Mouellic H, Campbell AK, Lucas-Meunier E, Fossier P, Brulet P. Chimeric green fluorescent protein-aequorin as bioluminescent Ca2+ reporters at the single-cell level. Proc Natl Acad Sci USA 2000; 97:7260-7265.
42. Waud JP, Bermudez Fajardo A, Sudhaharan T etal. Measurement of proteases using chemiluminescence-resonance-energy-transfer chimaeras between green fluorescent protein and aequorin. Biochem J 2001; 357:687-697.
43. Bakayan A, Vaquero CF, Picazo F, Llopis J. Red fluorescent protein-aequorin fusions as improved bioluminescent Ca2+ reporters in single cells and mice. PLOS ONE 2011; 6:e19520.
44. Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 1962; 59:223-239.
45. Morise H, Shimomura O, Johnson FH, Winant J. Intermolecular energy transfer in the bioluminescent system of Aequorea. Biochemistry 1974; 13:2656-2662.
46. Shiboski SC, Shiboski CH, Criswell L etal., Sjogren's International Collaborative Clinical Alliance Research Group. American College of Rheumatology classification criteria for Sjogren's syndrome: a data-driven, expert consensus approach in the Sjogren's International Collaborative Clinical Alliance cohort. Arthritis Care Res 2012; 64:475-487.
47. van den Hoogen F, Khanna D, Fransen J etal. 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Arthritis Rheum 2013; 65:2737-2747.
48. Klein R, Marx A, Strobel P, Schalke B, Nix W, Willcox N. Autoimmune associations and autoantibody screening show focused recognition in patient subgroups with generalized myasthenia gravis. Hum Immunol 2013; 74:1184-1193.
49. Mussig K, Leyhe T, Holzmuller S etal. Increased prevalence of antibodies to central nervous system tissue and gangliosides in Hashimoto's thyroiditis compared to other thyroid illnesses. Psychoneuroendocrinology 2009; 34:1252-1256.
50. Wallukat G, Homuth V, Fischer T etal. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest 1999; 103:945-952.
51. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
52. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979; 76:4350-4354.
53. Cembala TM, Sherwin JD, Tidmarsh MD, Appadu BL, Lambert DG. Interaction of neuromuscular blocking drugs with recombinant human m1-m5 muscarinic receptors expressed in Chinese hamster ovary cells. Br J Pharmacol 1998; 125:1088-1094.
54. Chang ZL, Puhl HL, May LG, Williams CL, Aronstam RS. Influence of acute and chronic ethanol treatment on muscarinic responses and receptor expression in Chinese hamster ovary cells. Biochem Pharmacol 1997; 54:833-839.
55. Geisse S, Voedisch B. Transient expression technologies: past, present, and future. Methods Mol Biol 2012; 899:203-219.
56. Kekwick RA. The serum proteins in multiple myelomatosis. Biochem J 1940; 34:1248-1257.
57. Daha NA, Banda NK, Roos A etal. Complement activation by (auto-) antibodies. Mol Immunol 2011; 48:1656-1665.
58. Klein R, Lindenborn-Fotinos J, Berg PA. Use of ATPase-associated antigen (M2) for detection of antimitochondrial antibodies in primary biliary cirrhosis by fluorometric immunoassay. J Immunol Methods 1983; 64:227-238.
59. Leffler DA, Schuppan D. Update on serologic testing in celiac disease. Am J Gastroenterol 2010; 105:2520-2524.
60. Meijide H, Sciascia S, Sanna G, Khamashta MA, Bertolaccini ML. The clinical relevance of IgA anticardiolipin and IgA anti-beta2 glycoprotein I antiphospholipid antibodies: a systematic review. Autoimmun Rev 2013; 12:421-425.
61. Nann D, Berg CP, Preuss BE, Klein R. Analysis of the clinical relevance of antimitochondrial antibodies to the beta- and gamma-subunits of the F1F0-ATPase in patients with primary biliary cirrhosis. BMC Gastroenterol 2012; 12:152-162.
62. Roggenbuck D, Reinhold D, Werner L, Schierack P, Bogdanos DP, Conrad K. Glycoprotein 2 antibodies in Crohn's disease. Adv Clin Chem 2013; 60:187-208.
63. Hausdorf G, Roggenbuck D, Feist E etal. Autoantibodies to asialoglycoprotein receptor (ASGPR) measured by a novel ELISA - revival of a disease-activity marker in autoimmune hepatitis. Clin Chim Acta 2009; 408:19-24.
64. Herda LR, Felix SB, Boege F. Drug-like actions of autoantibodies against receptors of the autonomous nervous system and their impact on human heart function. Br J Pharmacol 2012; 166:847-857.
65. Michalek K, Morshed SA, Latif R, Davies TF. TSH receptor autoantibodies. Autoimmun Rev 2009; 9:113-116.
66. Berg CP, Blume K, Lauber K etal. Autoantibodies to muscarinic acetylcholine receptors found in patients with primary biliary cirrhosis. BMC Gastroenterol 2010; 10:120-127.
67. Preuss B, Berg CP, Tunaru S, Offermanns S, Klein R. Demonstration of functional antibodies inhibiting the human muscarinic acetylcholine receptor of the M3 type (hm3AchR) in sera from patients with autoimmune liver disorders. Hepatology 2013; 58:567A.