Autoimmunity contributes to nociceptive sensitization in a mouse model of complex regional pain syndrome

Pain

Volumn 155, Issue 11, 2014, Pages 2377-2389

  Li, Wen Wu ^a,b   Guo, Tian Zhi ^a   Shi, Xiaoyou ^a,b   Czirr, Eva ^a,b   Stan, Trisha ^a,b   Sahbaie, Peyman ^a,b   Wyss Coray, Tony ^a,b   Kingery, Wade S ^a   Clark, J David ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; B cell; Complex regional pain syndrome; Fracture; Pain

Indexed keywords

CD20 ANTIBODY; CD20 ANTIGEN; COMPLEMENT MEMBRANE ATTACK COMPLEX; IMMUNOGLOBULIN M;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CAST APPLICATION; CELL AGGREGATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM SENSITIZATION; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; COMPLEX REGIONAL PAIN SYNDROME; CONTROLLED STUDY; FRACTURE HEALING; HUMORAL IMMUNE DEFICIENCY; IMMUNE COMPLEX DEPOSITION; IMMUNOGLOBULIN PRODUCTION; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; MALE; MOUSE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SCIATIC NERVE; SKIN; TIBIA FRACTURE; ANIMAL; C57BL MOUSE; COMPLEX REGIONAL PAIN SYNDROMES; COMPLICATION; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FRACTURE; GENETICS; HINDLIMB; HYPERALGESIA; IMMUNOLOGY; METABOLISM; MUTANT MOUSE STRAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME;

ANIMALS; ANTIGENS, CD20; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; COMPLEX REGIONAL PAIN SYNDROMES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FRACTURES, BONE; HINDLIMB; HYPERALGESIA; IMMUNOGLOBULIN M; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NOCICEPTION; PAIN MEASUREMENT; PAIN THRESHOLD; TIME FACTORS;

EID: 84923579511     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.09.007     Document Type: Article

References (69)

1. Bean DJ, Johnson MH, Kydd RR. The outcome of complex regional pain syndrome type 1: A systematic review. J Pain 2014;15:677-90.
2. Brekke OH, Sandlie I. Therapeutic antibodies for human diseases at the dawn of the twenty-first century. Nat Rev Drug Discov 2003;2:52-62.
3. Buskila D, Sarzi-Puttini P. Fibromyalgia and autoimmune diseases: the pain behind autoimmunity. Isr Med Assoc J 2008;10:77-8.
4. Calder JS, Holten I, McAllister RM. Evidence for immune system involvement in reflex sympathetic dystrophy. J Hand Surg Br 1998;23:147-50.
5. Caudie C, Quittard Pinon A, Taravel D, Sivadon-Tardy V, Orlikowski D, Rozenberg F, Sharshar T, Raphael JC, Gaillard JL. Preceding infections and anti-ganglioside antibody profiles assessed by a dot immunoassay in 306 French Guillain-Barre syndrome patients. J Neurol 2011;258:1958-64.
6. Chen WH, Chen YT, Lin CS, Li TH, Lee LH, Chen CJ. A high prevalence of autoimmune indices and disorders in primary nummular headache. J Neurol Sci 2012;320:127-30.
7. Cossins L, Okell RW, Cameron H, Simpson B, Poole HM, Goebel A. Treatment of complex regional pain syndrome in adults: A systematic review of randomized controlled trials published from June 2000 to February 2012. Eur J Pain 2013;17:158-73.
8. Curtis J, Bourne FJ. Half-lives of immunoglobulins IgG, IgA and IgM in the serum of new-born pigs. Immunology 1973;24:147-55.
9. de Rooij AM, Florencia Gosso M, Haasnoot GW, Marinus J, Verduijn W, Claas FH, van den Maagdenberg AM, van Hilten JJ. HLA-B62 and HLA-DQ8 are associated with Complex Regional Pain Syndrome with fixed dystonia. PAIN- 2009;145:82-5.
10. Devaux JJ, Odaka M, Yuki N. Nodal proteins are target antigens in Guillain-Barre syndrome. J Peripher Nerv Syst 2012;17:62-71.
11. Dirckx M, Stronks DL, Groeneweg G, Huygen FJ. Effect of immunomodulating medications in complex regional pain syndrome: A systematic review. Clin J Pain 2012;28:355-63.
12. Forster M, Umnus A, Siebrecht D, Baron R, Wasner G. A case of pain, motor impairment, and swelling of the arm after acute herpes zoster infection. PAIN- 2012;153:2478-81.
13. Fosbrink M, Niculescu F, Rus H. The role of c5b-9 terminal complement complex in activation of the cell cycle and transcription. Immunol Res 2005;31:37-46.
14. Goebel A, Baranowski A, Maurer K, Ghiai A, McCabe C, Ambler G. Intravenous immunoglobulin treatment of the complex regional pain syndrome: A randomized trial. Ann Intern Med 2010;152:152-8.
15. Goebel A, Blaes F. Complex regional pain syndrome, prototype of a novel kind of autoimmune disease. Autoimmun Rev 2013;12:682-6.
16. Goebel A, Netal S, Schedel R, Sprotte G. Human pooled immunoglobulin in the treatment of chronic pain syndromes. Pain Med 2002;3:119-27.
17. 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.
18. Guo TZ, Offley SC, Boyd EA, Jacobs CR, Kingery WS. Substance P signaling contributes to the vascular and nociceptive abnormalities observed in a tibial fracture rat model of complex regional pain syndrome type I. PAIN- 2004;108:95-107.
19. Guo TZ, Wei T, Kingery WS. Glucocorticoid inhibition of vascular abnormalities in a tibia fracture rat model of complex regional pain syndrome type I. PAIN- 2006;121:158-67.
20. Guo TZ, Wei T, Shi X, Li WW, Hou S, Wang L, Tsujikawa K, Rice KC, Cheng K, Clark DJ, Kingery WS. Neuropeptide deficient mice have attenuated nociceptive, vascular, and inflammatory changes in a tibia fracture model of complex regional pain syndrome. Mol Pain 2012;8:85.
21. Gurcan HM, Keskin DB, Stern JN, Nitzberg MA, Shekhani H, Ahmed AR. A review of the current use of rituximab in autoimmune diseases. Int Immunopharmacol 2009;9:10-25.
22. Huang H, Benoist C, Mathis D. Rituximab specifically depletes short-lived autoreactive plasma cells in a mouse model of inflammatory arthritis. Proc Natl Acad Sci USA 2010;107:4658-63.
23. Jang JH, Clark JD, Li X, Yorek MS, Usachev YM, Brennan TJ. Nociceptive sensitization by complement C5a and C3a in mouse. PAIN- 2010;148: 343-52.
24. Joseph SA, Tsao CY. Guillain-Barre syndrome. Adolesc Med 2002;13:487-94.
25. Kaida K. Guillain-Barre and Fisher syndromes: update on the pathophysiological role of antiganglioside antibodies. Rinsho Shinkeigaku 2012;52:914-6.
26. Kaufmann I, Eisner C, Richter P, Huge V, Beyer A, Chouker A, Schelling G, Thiel M. Lymphocyte subsets and the role of TH1/TH2 balance in stressed chronic pain patients. Neuroimmunomodulation 2007;14:272-80.
27. Kingery WS, Davies MF, Clark JD. A substance P receptor (NK1) antagonist can reverse vascular and nociceptive abnormalities in a rat model of complex regional pain syndrome type II. PAIN- 2003;104:75-84.
28. Klein CJ, Lennon VA, Aston PA, McKeon A, Pittock SJ. Chronic pain as a manifestation of potassium channel-complex autoimmunity. Neurology 2012;79:1136-44.
29. 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 beta2 adrenergic receptor and muscarinic-2 receptor in complex regional pain syndrome. PAIN- 2011;152:2690-700.
30. 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.
31. Koike H, Tanaka F, Sobue G. Paraneoplastic neuropathy: wide-ranging clinicopathological manifestations. Curr Opin Neurol 2011;24:504-10.
32. Kurtuncu M, Kaya D, Zuliani L, Erdag E, Icoz S, Ugurel E, Cavus F, Aysit N, Birisik O, Vincent A, Eraksoy M, Vural B, Akman-Demir G, Tuzun E. CACNA1H antibodies associated with headache with neurological deficits and cerebrospinal fluid lymphocytosis (HaNDL). Cephalalgia 2013;33:123-9.
33. Leandro MJ, de la Torre I. Translational mini-review series on B cell-directed therapies: the pathogenic role of B cells in autoantibody-associated autoimmune diseases-lessons from B cell-depletion therapy. Clin Exp Immunol 2009;157:191-7.
34. Lee YC. Effect and treatment of chronic pain in inflammatory arthritis. Curr Rheumatol Rep 2013;15:300.
35. Li W, Shi X, Wang L, Guo T, Wei T, Cheng K, Rice KC, Kingery WS, Clark JD. Epidermal adrenergic signaling contributes to inflammation and pain sensitization in a rat model of complex regional pain syndrome. PAIN- 2013;154:1224-36.
36. Li WW, Guo TZ, Li XQ, Kingery WS, Clark JD. Fracture induces keratinocyte activation, proliferation, and expression of pro-nociceptive inflammatory mediators. PAIN- 2010;151:843-52.
37. Li WW, Guo TZ, Liang D, Shi X, Wei T, Kingery WS, Clark JD. The NALP1 inflammasome controls cytokine production and nociception in a rat fracture model of complex regional pain syndrome. PAIN- 2009;147:277-86.
38. Li WW, Sabsovich I, Guo TZ, Zhao R, Kingery WS, Clark JD. The role of enhanced cutaneous IL-1beta signaling in a rat tibia fracture model of complex regional pain syndrome. PAIN- 2009;144:303-13.
39. Mannoor K, Xu Y, Chen C. Natural autoantibodies and associated B cells in immunity and autoimmunity. Autoimmunity 2013;46:138-47.
40. Marinus J, Moseley GL, Birklein F, Baron R, Maihofner C, Kingery WS, van Hilten JJ. Clinical features and pathophysiology of complex regional pain syndrome. Lancet Neurol 2011;10:637-48.
41. Nandakumar KS, Andren M, Martinsson P, Bajtner E, Hellstrom S, Holmdahl R, Kleinau S. Induction of arthritis by single monoclonal IgG anti-collagen type II antibodies and enhancement of arthritis in mice lacking inhibitory FcgammaRIIB. Eur J Immunol 2003;33:2269-77.
42. O'Neill SK, Glant TT, Finnegan A. The role of B cells in animal models of rheumatoid arthritis. Front Biosci 2007;12:1722-36.
43. Orlikowski D, Porcher R, Sivadon-Tardy V, Quincampoix JC, Raphael JC, Durand MC, Sharshar T, Roussi J, Caudie C, Annane D, Rozenberg F, Leruez-Ville M, Gaillard JL, Gault E. Guillain-Barre syndrome following primary cytomegalovirus infection: A prospective cohort study. Clin Infect Dis 2011;52:837-44.
44. Petkova SB, Konstantinov KN, Sproule TJ, Lyons BL, Awwami MA, Roopenian DC. Human antibodies induce arthritis in mice deficient in the low-affinity inhibitory IgG receptor Fc gamma RIIB. J Exp Med 2006;203:275-80.
45. Pogatzki EM, Raja SN. A mouse model of incisional pain. Anesthesiology 2003;99:1023-7.
46. Poree LR, Guo TZ, Kingery WS, Maze M. The analgesic potency of dexmedetomidine is enhanced after nerve injury: A possible role for peripheral alpha2-adrenoceptors. Anesth Analg 1998;87:941-8.
47. Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, Newman RA, Hanna N, Anderson DR. Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood 1994;83:435-45.
48. Ribbers GM, Oosterhuis WP, van Limbeek J, De metz M. Reflex sympathetic dystrophy: is the immune system involved? Arch Phys Med Rehabil 1998;79:1549-52.
49. Richards S, Chalkiadis G, Lakshman R, Buttery JP, Crawford NW. Complex regional pain syndrome following immunisation. Arch Dis Child 2012;97:913-5.
50. Ritz BW, Alexander GM, Nogusa S, Perreault MJ, Peterlin BL, Grothusen JR, Schwartzman RJ. Elevated blood levels of inflammatory monocytes (CD14+ CD16+) in patients with complex regional pain syndrome. Clin Exp Immunol 2011;164:108-17.
51. Romero V, Fert-Bober J, Nigrovic PA, Darrah E, Haque UJ, Lee DM, van Eyk J, Rosen A, Andrade F. Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci Transl Med 2013;5:209ra150.
52. Sabsovich I, Clark JD, Liao G, Peltz G, Lindsey DP, Jacobs CR, Yao W, Guo TZ, Kingery WS. Bone microstructure and its associated genetic variability in 12 inbred mouse strains: microCT study and in silico genome scan. Bone 2008;42:439-51.
53. Sabsovich I, Guo TZ, Wei T, Zhao R, Li X, Clark DJ, Geis C, Sommer C, Kingery WS. TNF signaling contributes to the development of nociceptive sensitization in a tibia fracture model of complex regional pain syndrome type I. PAIN- 2008;137:507-19.
54. Sabsovich I, Wei T, Guo TZ, Zhao R, Shi X, Li X, Yeomans DC, Klyukinov M, Kingery WS, Clark JD. Effect of anti-NGF antibodies in a rat tibia fracture model of complex regional pain syndrome type I. PAIN- 2008;138:47-60.
55. Schwartzman RJ, Erwin KL, Alexander GM. The natural history of complex regional pain syndrome. Clin J Pain 2009;25:273-80.
56. Shulman MJ, Pennell N, Collins C, Hozumi N. Activation of complement by immunoglobulin-M is impaired by the substitution serine-406-asparagine in the immunoglobulin-mu heavy chain. Proc Natl Acad Sci USA 1986;83:7678-82.
57. Sibanc B, Lesnicar G. Complex regional pain syndrome and lyme borreliosis: two different diseases? Infection 2002;30:396-9.
58. Sorkin LS, Otto M, Baldwin III WM, Vail E, Gillies SD, Handgretinger R, Barfield RC, Ming Yu H, Yu AL. Anti-GD(2) with an FC point mutation reduces complement fixation and decreases antibody-induced allodynia. PAIN- 2010;149:135-42.
59. Subbarao J, Stillwell GK. Reflex sympathetic dystrophy syndrome of the upper extremity: Analysis of total outcome of management of 125 cases. Arch Phys Med Rehabil 1981;62:549-54.
60. Svensson L, Jirholt J, Holmdahl R, Jansson L. B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol 1998;111:521-6.
61. 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.
62. van de Beek WJ, Roep BO, van der Slik AR, Giphart MJ, van Hilten BJ. Susceptibility loci for complex regional pain syndrome. PAIN- 2003;103:93-7.
63. van de Vusse AC, Goossens VJ, Kemler MA, Weber WE. Screening of patients with complex regional pain syndrome for antecedent infections. Clin J Pain 2001;17:110-4.
64. van Rooijen DE, Roelen DL, Verduijn W, Haasnoot GW, Huygen FJ, Perez RS, Claas FH, Marinus J, van Hilten JJ, van den Maagdenberg AM. Genetic HLA associations in complex regional pain syndrome with and without dystonia. J Pain 2012;13:784-9.
65. Vaneker M, Wilder-Smith OH, Schrombges P, Oerlemans HM. Impairments as measured by ISS do not greatly change between one and eight years after CRPS 1 diagnosis. Eur J Pain 2006;10:639-44.
66. Vargas ME, Watanabe J, Singh SJ, Robinson WH, Barres BA. Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury. Proc Natl Acad Sci USA 2010;107:11993-8.
67. Vieira P, Rajewsky K. The half-lives of serum immunoglobulins in adult mice. Eur J Immunol 1988;18:313-6.
68. Yuki N. Guillain-Barre syndrome and anti-ganglioside antibodies: A clinicianscientist's journey. Proc Jpn Acad Ser B Phys Biol Sci 2012;88:299-326.
69. Zwart B, Ciurana C, Rensink I, Manoe R, Hack CE, Aarden LA. Complement activation by apoptotic cells occurs predominantly via IgM and is limited to late apoptotic (secondary necrotic) cells. Autoimmunity 2004;37:95-102