Longstanding complex regional pain syndrome is associated with activating autoantibodies against alpha-1a adrenoceptors

Pain

Volumn 155, Issue 11, 2014, Pages 2408-2417

  Dubuis, Eric ^a   Thompson, Victoria ^a   Leite, Maria Isabella ^b   Blaes, Franz ^c   Maihöfner, Christian ^d   Greensmith, David ^e   Vincent, Angela ^b   Shenker, Nicolas ^f   Kuttikat, Anoop ^f   Leuwer, Martin ^a   Goebel, Andreas ^a,g  

^a UNIVERSITY HOSPITAL AINTREE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f ADDENBROOKE S HOSPITAL   (United Kingdom)

^g THE WALTON CENTRE NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Adrenergic; Autoantibodies; Complex regional pain syndrome; CRPS; Pain

Indexed keywords

3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; ALPHA 1A ADRENERGIC RECEPTOR; ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; ATROPINE; AUTOANTIBODY; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; N [5 (4,5 DIHYDRO 1H IMIDAZOL 2 YL) 5,6,7,8 TETRAHYDRO 2 HYDROXY 1 NAPHTHYL]METHANESULFONAMIDE; (2-(2',6'-DIMETHOXY)PHENOXYETHYLAMINO)METHYLBENZO-1,4-DIOXANE; ALPHA 1 ADRENERGIC RECEPTOR; CALCIUM; DIOXANE DERIVATIVE; MUSCARINIC RECEPTOR BLOCKING AGENT; PROTEIN BINDING;

ADULT; ANALGESIA; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CELL CONTRACTION ASSAY; CLINICAL ARTICLE; COMPLEX REGIONAL PAIN SYNDROME; CONTROLLED STUDY; DISEASE DURATION; ELECTRIC FIELD; FEMALE; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; HEART MUSCLE CELL; HUMAN; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; LOW DRUG DOSE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TREATMENT RESPONSE; ANIMAL; BLOOD; CELL CULTURE; COMPLEX REGIONAL PAIN SYNDROMES; CROSSOVER PROCEDURE; DRUG EFFECTS; GENETIC TRANSFECTION; IMMUNOLOGY; MEMBRANE POTENTIAL; METABOLISM; MIDDLE AGED; PATCH CLAMP TECHNIQUE; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADULT; ANIMALS; ATROPINE; AUTOANTIBODIES; CALCIUM; CELLS, CULTURED; COMPLEX REGIONAL PAIN SYNDROMES; CROSS-OVER STUDIES; DIOXANES; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULINS, INTRAVENOUS; MALE; MEMBRANE POTENTIALS; MIDDLE AGED; MUSCARINIC ANTAGONISTS; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; RATS; RECEPTORS, ADRENERGIC, ALPHA-1; TRANSFECTION; YOUNG ADULT;

EID: 84921516596     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.09.022     Document Type: Article

References (54)

1. Ali Z, Raja SN, Wesselmann U, Fuchs PN, Meyer RA, Campbell JN. Intradermal injection of norepinephrine evokes pain in patients with sympathetically maintained pain. PAIN- 2000;88:161-8.
2. Arnold JM, Teasell RW, MacLeod AP, Brown JE, Carruthers SG. Increased venous alpha-adrenoceptor responsiveness in patients with reflex sympathetic dystrophy. Ann Intern Med 1993;118:619-21.
3. Baker JG. The selectivity of beta-adrenoceptor antagonists at the human beta1, beta2 and beta3 adrenoceptors. Br J Pharmacol 2005;144:317-22.
4. Bartur G, Vatine JJ, Raphaely-Beer N, Peleg S, Katz-Leurer M. Heart rate autonomic regulation system at rest and during paced breathing among patients with crps as compared to age-matched healthy controls. Pain Med 2014;15:1569-74.
5. Birklein F, Drummond PD, Li W, Schlereth T, Albrecht N, Finch PM, Dawson LF, Clark JD, Kingery WS. Activation of cutaneous immune responses in complex regional pain syndrome. J Pain 2014;15:485-95.
6. Blaes F, Schmitz K, Tschernatsch M, Kaps M, Krasenbrink I, Hempelmann G, Brau ME. Autoimmune etiology of complex regional pain syndrome (M. Sudeck). Neurology 2004;63:1734-6.
7. Campbell JN, Raja SN. Reflex sympathetic dystrophy. Neurology 1995;45:1235-7.
8. Cheng JT, Liu IM, Yen ST, Chen PC. Role of alpha1A-adrenoceptor in the regulation of glucose uptake into white adipocyte of rats in vitro. Auton Neurosci 2000;84:140-6.
9. Cotecchia S. The alpha1-adrenergic receptors: diversity of signaling networks and regulation. J Recept Signal Transduct Res 2010;30:410-9.
10. Davis KD, Treede RD, Raja SN, Meyer RA, Campbell JN. Topical application of clonidine relieves hyperalgesia in patients with sympathetically maintained pain. PAIN- 1991;47:309-17.
11. de Mos M, Huygen FJ, Hoeven-Borgman M, Dieleman JP, Ch Stricker BH, Sturkenboom MC. Outcome of the complex regional pain syndrome. Clin J Pain 2009;25:590-7.
12. Drummond PD. Inflammation contributes to axon reflex vasodilatation evoked by iontophoresis of an alpha-1 adrenoceptor agonist. Auton Neurosci 2011;159:90-7.
13. Drummond PD, Drummond ES, Dawson LF, Mitchell V, Finch PM, Vaughan CW, Phillips JK. Upregulation of alpha1-adrenoceptors on cutaneous nerve fibres after partial sciatic nerve ligation and in complex regional pain syndrome type II. PAIN- 2014;155:606-16.
14. Drummond PD, Finch PM, Smythe GA. Reflex sympathetic dystrophy: the significance of differing plasma catecholamine concentrations in affected and unaffected limbs. Brain 1991;114:2025-36.
15. Drummond PD, Skipworth S, Finch PM. Alpha 1-adrenoceptors in normal and hyperalgesic human skin. Clin Sci (Lond) 1996;91:73-7.
16. Dubuis E, Rockliffe N, Hussain M, Boyett M, Wray D, Gawler D. Evidence for multiple Src binding sites on the alpha1c L-type Ca2+ channel and their roles in activity regulation. Cardiovasc Res 2006;69:391-401.
17. Farrar JT, Young Jr JP, LaMoreaux L, Werth JL, Poole RM. Clinical importance of changes in chronic pain intensity measured on an 11-point numerical pain rating scale. PAIN- 2001;94:149-58.
18. Frampton JE, Orchard CH, Boyett MR. Diastolic, systolic and sarcoplasmic reticulum [Ca2+] during inotropic interventions in isolated rat myocytes. J Physiol 1991;437:351-75.
19. Goebel A, Baranowski AP, Maurer K, Ghiai A, McCabe C, Ambler G. Intravenous immunoglobulin treatment of complex regional pain syndrome: A randomized trial. Ann Intern Med 2010;152:152-8.
20. Goebel A, Leite MI, Yang L, Deacon R, Cendan CM, Fox-Lewis A, Vincent A. The passive transfer of immunoglobulin G serum antibodies from patients with longstanding Complex Regional Pain Syndrome. Eur J Pain 2011;15. 504.e1-6.
21. Goebel A, Misbah S, Maciver K, Haynes L, Burton J, Philips C, Frank B, Poole H. Immunoglobulin maintenance therapy in long-standing complex regional pain syndrome, an open study. Rheumatology (Oxford) 2013;52:2091-3.
22. Goebel A, Netal S, Schedel R, Sprotte G. Human pooled immunoglobulin in the treatment of chronic pain syndromes. Pain Med 2002;3:119-27.
23. Goebel A, Stock M, Deacon R, Sprotte G, Vincent A. Intravenous immunoglobulin response and evidence for pathogenic antibodies in a case of complex regional pain syndrome 1. Ann Neurol 2005;57:463-4.
24. Goebel A, Vogel H, Caneris O, Bajwa Z, Clover L, Roewer N, Schedel R, Karch H, Sprotte G, Vincent A. Immune responses to Campylobacter and serum autoantibodies in patients with complex regional pain syndrome. J Neuroimmunol 2005;162:184-9.
25. Goebel A, Blaes F. Complex regional pain syndrome, prototype of a novel kind of autoimmune disease. Autoimmun Rev 2013;12:682-6.
26. Greensmith DJ, Eisner DA, Nirmalan M. The effects of hydrogen peroxide on intracellular calcium handling and contractility in the rat ventricular myocyte. Cell Calcium 2010;48:341-51.
27. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 1981;391:85-100.
28. Kang M, Walker JW. Protein kinase C delta and epsilon mediate positive inotropy in adult ventricular myocytes. J Mol Cell Cardiol 2005;38:753-64.
29. Kashihara K, Varga EV, Waite SL, Roeske WR, Yamamura HI. Cloning of the rat M3, M4 and M5 muscarinic acetylcholine receptor genes by the polymerase chain reaction (PCR) and the pharmacological characterization of the expressed genes. Life Sci 1992;51:955-71.
30. Kemler MA, Furnee CA. Economic evaluation of spinal cord stimulation for chronic reflex sympathetic dystrophy. Neurology 2002;59:1203-9.
31. Kilts JD, Grocott HP, Kwatra MM. G alpha(q)-coupled receptors in human atrium function through protein kinase C epsilon and delta. J Mol Cell Cardiol 2005;38:267-76.
32. Knepper SM, Buckner SA, Brune ME, DeBernardis JF, Meyer MD, Hancock AA. A-61603, a potent alpha 1-adrenergic receptor agonist, selective for the alpha 1A receptor subtype. J Pharmacol Exp Ther 1995;274:97-103.
33. Kohr D, Singh P, Tschernatsch M, Kaps M, Pouokam E, Diener M, Kummer W, Birklein F, Vincent A, Goebel A, Wallukat G, Blaes F. Autoimmunity against the beta(2) adrenergic receptor and muscarinic-2 receptor in complex regional pain syndrome. PAIN- 2011;152:2690-700.
34. Kohr D, Tschernatsch M, Schmitz K, Singh P, Kaps M, Schafer KH, Diener M, Mathies J, Matz O, Kummer W, Maihofner C, Fritz T, Birklein F, Blaes F. Autoantibodies in complex regional pain syndrome bind to a differentiationdependent neuronal surface autoantigen. PAIN- 2009;143:246-51.
35. Millan MJ, Newman-Tancredi A, Audinot V, Cussac D, Lejeune F, Nicolas JP, Coge F, Galizzi JP, Boutin JA, Rivet JM, Dekeyne A, Gobert A. Agonist and antagonist actions of yohimbine as compared to fluparoxan at alpha(2)-adrenergic receptors (AR)s, serotonin (5-HT)(1A), 5-HT(1B), 5-HT(1D) and dopamine D(2) and D(3) receptors. Significance for the modulation of frontocortical monoaminergic transmission and depressive states. Synapse 2000;35:79-95.
36. Patane MA, Scott AL, Broten TP, Chang RS, Ransom RW, DiSalvo J, Forray C, Bock MG. 4-Amino-2-[4-[1-(benzyloxycarbonyl)-2(S)-[[(1,1-dimethylethyl) amino]carbonyl]-piperazinyl]-6,7-dimethoxyquinazoline (L-765,314): A potent and selective alpha1b adrenergic receptor antagonist. J Med Chem 1998;41:1205-8.
37. Price DD, Long S, Wilsey B, Rafii A. Analysis of peak magnitude and duration of analgesia produced by local anesthetics injected into sympathetic ganglia of complex regional pain syndrome patients. Clin J Pain 1998;14:216-26.
38. Raja SN, Treede RD, Davis KD, Campbell JN. Systemic alpha-adrenergic blockade with phentolamine: A diagnostic test for sympathetically maintained pain. Anesthesiology 1991;74:691-8.
39. Raja SN, Turnquist JL, Meleka S, Campbell JN. Monitoring adequacy of alphaadrenoceptor blockade following systemic phentolamine administration. PAIN- 1996;64:197-204.
40. Ramos-Mondragon R, Galindo CA, Garcia-Castaneda M, Sanchez-Vargas JL, Vega AV, Gomez-Viquez NL, Avila G. Chronic potentiation of cardiac L-type Ca(2+) channels by pirfenidone. Cardiovasc Res 2012;96:244-54.
41. Rose NR, Bona C. Defining criteria for autoimmune diseases (Witebsky's postulates revisited). Immunol Today 1993;14:426-30.
42. Taneyama C, Yokota S, Goto H. Patients with complex regional pain syndrome type 1: fractal dynamics of heart rate variability and baroreflex evaluations. Clin J Pain 2013;29:962-6.
43. Tekus V, Hajna Z, Borbely E, Markovics A, Bagoly T, Szolcsanyi J, Thompson V, Kemeny A, Helyes Z, Goebel A. A CRPS-IgG-transfer-trauma model reproducing inflammatory and positive sensory signs associated with complex regional pain syndrome. PAIN- 2014;155:299-308.
44. Terkelsen AJ, Molgaard H, Hansen J, Finnerup NB, Kroner K, Jensen TS. Heart rate variability in complex regional pain syndrome during rest and mental and orthostatic stress. Anesthesiology 2012;116:133-46.
45. Torebjork E, Wahren L, Wallin G, Hallin R, Koltzenburg M. Noradrenalineevoked pain in neuralgia. PAIN- 1995;63:11-20.
46. van Vliet P, Smits AM, de Boer TP, Korfage TH, Metz CH, Roccio M, van der Heyden MA, van Veen TA, Sluijter JP, Doevendans PA, Goumans MJ. Foetal and adult cardiomyocyte progenitor cells have different developmental potential. J Cell Mol Med 2010;14:861-70.
47. Verdugo RJ, Ochoa JL. 'Sympathetically maintained pain'. I. Phentolamine block questions the concept. Neurology 1994;44:1003-10.
48. Volders PG. Novel insights into the role of the sympathetic nervous system in cardiac arrhythmogenesis. Heart Rhythm 2010;7:1900-6.
49. Waugh DJ, Gaivin RJ, Zuscik MJ, Gonzalez-Cabrera P, Ross SA, Yun J, Perez DM. Phe-308 and Phe-312 in transmembrane domain 7 are major sites of alpha 1-adrenergic receptor antagonist binding. Imidazoline agonists bind like antagonists. J Biol Chem 2001;276:25366-71.
50. Wenzel K, Haase H, Wallukat G, Derer W, Bartel S, Homuth V, Herse F, Hubner N, Schulz H, Janczikowski M, Lindschau C, Schroeder C, Verlohren S, Morano I, Muller DN, Luft FC, Dietz R, Dechend R, Karczewski P. Potential relevance of alpha(1)-adrenergic receptor autoantibodies in refractory hypertension. PLoS One 2008;3:e3742.
51. Wilkinson SE, Parker PJ, Nixon JS. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem J 1993;294:335-7.
52. Wise A, Lee TW, MacEwan DJ, Milligan G. Degradation of G11 alpha/Gq alpha is accelerated by agonist occupancy of alpha 1A/D, alpha 1B, and alpha 1C adrenergic receptors. J Biol Chem 1995;270:17196-203.
53. Wolfe F, Clauw DJ, Fitzcharles MA, Goldenberg DL, Hauser W, Katz RS, Mease P, Russell AS, Russell IJ, Winfield JB. Fibromyalgia criteria and severity scales for clinical and epidemiological studies: A modification of the ACR Preliminary Diagnostic Criteria for Fibromyalgia. J Rheumatol 2011;38:1113-22.
54. Zhang YH, Hinde AK, Hancox JC. Anti-adrenergic effect of adenosine on Na(+)-Ca(2+) exchange current recorded from guinea-pig ventricular myocytes. Cell Calcium 2001;29:347-58.