Behavioral, pharmacological, and immunological abnormalities after streptococcal exposure: A novel rat model of sydenham chorea and related neuropsychiatric disorders

Neuropsychopharmacology

Volumn 37, Issue 9, 2012, Pages 2076-2087

  Brimberg, Lior ^a   Benhar, Itai ^a   Mascaro Blanco, Adita ^b   Alvarez, Kathy ^b   Lotan, Dafna ^a   Winter, Christine ^c,d   Klein, Julia ^d   Moses, Allon E ^e   Somnier, Finn E ^f   Leckman, James F ^g   Swedo, Susan E ^h   Cunningham, Madeleine W ^b   Joel, Daphna ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^f STATENS SERUM INSTITUT   (Denmark)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

animal model; autoimmunity; dopamine; PANDAS; streptococcus group A (GAS); Sydenham chorea (SC)

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DOPAMINE; GLUTAMIC ACID; HALOPERIDOL; IMMUNOGLOBULIN G; PAROXETINE; TUBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BEHAVIOR DISORDER; CHOREA MINOR; CONTROLLED STUDY; CORPUS STRIATUM; FRONTAL CORTEX; GROUP A STREPTOCOCCAL INFECTION; MALE; MENTAL DISEASE; MOTOR DYSFUNCTION; NEUROPSYCHIATRIC DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; THALAMUS;

ADOLESCENT; ANIMALS; AUTOANTIBODIES; CHILD; CHILD, PRESCHOOL; CHOREA; DISEASE MODELS, ANIMAL; FEMALE; GROOMING; HUMANS; MALE; MENTAL DISORDERS; MOTOR ACTIVITY; RATS; RATS, INBRED LEW; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES;

EID: 84863988844     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.56     Document Type: Article

References (61)

1. Albelda N, Joel D (2012). Animal models of obsessive-compulsive disorder: exploring pharmacology and neural substrates. Neurosci Biobehav Rev 36: 47-63.
2. Ayalon L, Doron R, Weiner I, Joel D (2004). Amelioration of behavioral deficits in a rat model of Huntington's disease by an excitotoxic lesion to the globus pallidus. Exp Neurol 186: 46-58.
3. Bhattacharyya S, Chakraborty K (2007). Glutamatergic dysfunction-newer targets for anti-obsessional drugs. Recent Pat CNS Drug Discov 2: 47-55.
4. Bhattacharyya S, Khanna S, Chakrabarty K, Mahadevan A, Christopher R, Shankar SK (2009). Anti-brain autoantibodies and altered excitatory neurotransmitters in obsessive-compulsive disorder. Neuropsychopharmacology 34: 2489-2496.
5. Brimberg L, Flaisher-Grinberg S, Schilman EA, Joel D (2007). Strain differences in 'compulsive' lever-pressing. Behav Brain Res 179: 141-151.
6. Bronze MS, Dale JB (1993). Epitopes of streptococcal M proteins that evoke antibodies that cross-react with human brain. J Immunol 151: 2820-2828.
7. Church AJ, Cardoso F, Dale RC, Lees AJ, Thompson EJ, Giovannoni G (2002). Anti-basal ganglia antibodies in acute and persistent Sydenham's chorea. Neurology 59: 227-231.
8. Church AJ, Dale RC, Cardoso F, Candler PM, Chapman MD, Allen ML et al (2003). CSF and serum immune parameters in Sydenham's chorea: evidence of an autoimmune syndrome? J Neuroimmunol 136: 149-153.
9. Colony HS, Malamud N (1956). Sydenham's chorea; a clinicopathologic study. Neurology 6: 672-676.
10. Conners CK, Sitarenios G, Parker JD, Epstein JN (1998). The revised Conners' Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 26: 257-268.
11. Dale RC, Candler PM, Church AJ, Wait R, Pocock JM, Giovannoni G (2006). Neuronal surface glycolytic enzymes are autoantigen targets in post-streptococcal autoimmune CNS disease. J Neuroimmunol 172: 187-197.
12. Demiroren K, Yavuz H, Cam L, Oran B, Karaaslan S, Demiroren S (2007). Sydenham's chorea: a clinical follow-up of 65 patients. J Child Neurol 22: 550-554.
13. Dilenge ME, Shevell MI, Dinh L (1999). Restricted unilateral Sydenham's chorea: reversible contralateral striatal hypermetabolism demonstrated on single photon emission computed tomographic scanning. J Child Neurol 14: 509-513.
14. Fenderson PG, Fischetti VA, Cunningham MW (1989). Tropomyosin shares immunologic epitopes with group A streptococcal M proteins. J Immunol 142: 2475-2481.
15. Gause C, Morris C, Vernekar S, Pardo-Villamizar C, Grados MA, Singer HS (2009). Antineuronal antibodies in OCD: comparisons in children with OCD-only, OCD+chronic tics and OCD+PANDAS. J Neuroimmunol 214: 118-124.
16. Giedd JN, Rapoport JL, Garvey MA, Perlmutter S, Swedo SE (2000). MRI assessment of children with obsessive-compulsive disorder or tics associated with streptococcal infection. Am J Psychiatry 157: 281-283.
17. Giedd JN, Rapoport JL, Kruesi MJ, Parker C, Schapiro MB, Allen AJ et al (1995). Sydenham's chorea: magnetic resonance imaging of the basal ganglia. Neurology 45: 2199-2202.
18. Giedd JN, Rapoport JL, Leonard HL, Richter D, Swedo SE (1996). Case study: acute basal ganglia enlargement and obsessivecompulsive symptoms in an adolescent boy. J Am Acad Child Adolesc Psychiatry 35: 913-915.
19. Gordon N (2009). Sydenham's chorea, and its complications affecting the nervous system. Brain Dev 31: 11-14.
20. Greer JM, Capecchi MR (2002). Hoxb8 is required for normal grooming behavior in mice. Neuron 33: 23-34.
21. Hallett JJ, Harling-Berg CJ, Knopf PM, Stopa EG, Kiessling LS (2000). Anti-striatal antibodies in Tourette syndrome cause neuronal dysfunction. J Neuroimmunol 111: 195-202.
22. Hoffman KL, Hornig M, Yaddanapudi K, Jabado O, Lipkin WI (2004). A murine model for neuropsychiatric disorders associated with group A beta-hemolytic streptococcal infection. J Neurosci 24: 1780-1791.
23. Hogg S (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 54: 21-30.
24. Homberg JR, van den Akker M, Raaso HS, Wardeh G, Binnekade R, Schoffelmeer AN et al (2002). Enhanced motivation to selfadminister cocaine is predicted by self-grooming behaviour and relates to dopamine release in the rat medial prefrontal cortex and amygdala. Eur J Neurosci 15: 1542-1550.
25. Husby G, van de Rijn I, Zabriskie JB, Abdin ZH, Williams Jr RC (1976). Antibodies reacting with cytoplasm of subthalamic and caudate nuclei neurons in chorea and acute rheumatic fever. J Exp Med 144: 1094-1110.
26. Huyser C, Veltman DJ, de Haan E, Boer F (2009). Paediatric obsessive-compulsive disorder, a neurodevelopmental disorder? Evidence from neuroimaging. Neurosci Biobehav Rev 33: 818-830.
27. Joel D, Doljansky J (2003). Selective alleviation of compulsive lever-pressing in rats by D1, but not D2, blockade: possible implications for the involvement of D1 receptors in obsessivecompulsive disorder. Neuropsychopharmacology 28: 77-85.
28. Kirvan CA, Cox CJ, Swedo SE, Cunningham MW (2007). Tubulin is a neuronal target of autoantibodies in Sydenham's chorea. J Immunol 178: 7412-7421.
29. Kirvan CA, Swedo SE, Heuser JS, Cunningham MW (2003). Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea. Nat Med 9: 914-920.
30. Kirvan CA, Swedo SE, Kurahara D, Cunningham MW (2006a). Streptococcal mimicry and antibody-mediated cell signaling in the pathogenesis of Sydenham's chorea. Autoimmunity 39: 21-29.
31. Kirvan CA, Swedo SE, Snider LA, Cunningham MW (2006b). Antibody-mediated neuronal cell signaling in behavior and movement disorders. J Neuroimmunol 179: 173-179.
32. Klavir O, Flash S, Winter C, Joel D (2009). High frequency stimulation and pharmacological inactivation of the subthalamic nucleus reduces 'compulsive' lever-pressing in rats. Exp Neurol 215: 101-109.
33. Kurlan R, Kaplan EL (2004). The pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection (PANDAS) etiology for tics and obsessive-compulsive symptoms: hypothesis or entity? Practical considerations for the clinician. Pediatrics 113: 883-886.
34. Kushner MG, Kim SW, Donahue C, Thuras P, Adson D, Kotlyar M et al (2007). D-cycloserine augmented exposure therapy for obsessive-compulsive disorder. Biol Psychiatry 62: 835-838.
35. Linthicum DS, Munoz JJ, Blaskett A (1982). Acute experimental autoimmune encephalomyelitis in mice. I. Adjuvant action of Bordetella pertussis is due to vasoactive amine sensitization and increased vascular permeability of the central nervous system. Cell Immunol 73: 299-310.
36. Loiselle CR, Lee O, Moran TH, Singer HS (2004). Striatal microinfusion of Tourette syndrome and PANDAS sera: failure to induce behavioral changes. Mov Disord 19: 390-396.
37. Marques-Dias MJ, Mercadante MT, Tucker D, Lombroso P (1997). Sydenham's chorea. Psychiatr Clin North Am 20: 809-820.
38. Morshed SA, Parveen S, Leckman JF, Mercadante MT, Bittencourt Kiss MH, Miguel EC et al (2001). Antibodies against neural, nuclear, cytoskeletal, and streptococcal epitopes in children and adults with Tourette's syndrome, Sydenham's chorea, and autoimmune disorders. Biol Psychiatry 50: 566-577.
39. Murphy TK, Husted DS, Edge PJ (2006a). Preclinical/Clinical evidence of central nervous system infectious etiology in PANDAS. Adv Neurol 99: 148-158.
40. Murphy TK, Sajid MW, Goodman WK (2006b). Immunology of obsessive-compulsive disorder. Psychiatr Clin North Am 29: 445-469.
41. Pavone P, Bianchini R, Parano E, Incorpora G, Rizzo R, Mazzone L et al (2004). Anti-brain antibodies in PANDAS versus uncomplicated streptococcal infection. Pediatr Neurol 30: 107-110.
42. Peterson BS, Leckman JF, Tucker D, Scahill L, Staib L, Zhang H et al (2000). Preliminary findings of antistreptococcal antibody titers and basal ganglia volumes in tic, obsessive-compulsive, and attention deficit/ hyperactivity disorders. Arch Gen Psychiatry 57: 364-372.
43. Piontkewitz Y, Arad M, Weiner I (2010). Risperidone administered during asymptomatic period of adolescence prevents the emergence of brain structural pathology and behavioral abnormalities in an animal model of schizophrenia. Schizophr Bull 37: 1257-1269.
44. Quinn A, Kosanke S, Fischetti VA, Factor SM, Cunningham MW (2001). Induction of autoimmune valvular heart disease by recombinant streptococcal m protein. Infect Immun 69: 4072-4078.
45. Rosenberg DR, Mirza Y, Russell A, Tang J, Smith JM, Banerjee SP et al (2004). Reduced anterior cingulate glutamatergic concentrations in childhood OCD and major depression versus healthy controls. J Am Acad Child Adolesc Psychiatry 43: 1146-1153.
46. Shannon KM, Fenichel GM (1990). Pimozide treatment of Sydenham's chorea. Neurology 40: 186.
47. Singer HS, Loiselle C (2003). PANDAS: a commentary. J Psychosom Res 55: 31-39.
48. Singer HS, Mink JW, Loiselle CR, Burke KA, Ruchkina I, Morshed S et al (2005). Microinfusion of antineuronal antibodies into rodent striatum: failure to differentiate between elevated and low titers. J Neuroimmunol 163: 8-14.
49. Singer HS, Minzer K (2003). Neurobiology of Tourette's syndrome: concepts of neuroanatomic localization and neurochemical abnormalities. Brain Dev 25(Suppl 1): S70-S84.
50. Singer HS, Morris C, Grados M (2009). Glutamatergic modulatory therapy for Tourette syndrome. Med Hypotheses 74: 862-867.
51. Snider LA, Swedo SE (2004). PANDAS: current status and directions for research. Mol Psychiatry 9: 900-907.
52. Stein DJ (2002). Obsessive-compulsive disorder. Lancet 360: 397-405.
53. Stollerman GH (1997). Rheumatic fever. Lancet 349: 935-942.
54. Swedo SE, Leonard HL, Garvey M, Mittleman B, Allen AJ, Perlmutter S et al (1998). Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases. Am J Psychiatry 155: 264-271.
55. Swedo SE, Leonard HL, Rapoport JL (2004). The pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection (PANDAS) subgroup: separating fact from fiction. Pediatrics 113: 907-911.
56. Swedo SE, Rapoport JL, Cheslow DL, Leonard HL, Ayoub EM, Hosier DM et al (1989). High prevalence of obsessivecompulsive symptoms in patients with Sydenham's chorea. Am J Psychiatry 146: 246-249.
57. Taylor JR, Morshed SA, Parveen S, Mercadante MT, Scahill L, Peterson BS et al (2002). An animal model of Tourette's syndrome. Am J Psychiatry 159: 657-660.
58. Umene W, Yoshimura R, Hori H, Nakano H, Sugita A, Shimono M et al (2007). Blood levels of catecholamine metabolites and brain-derived neurotrophic factor in a case of Sydenham's chorea. World J Biol Psychiatry 10: 248-251.
59. Urakawa S, Hida H, Masuda T, Misumi S, Kim TS, Nishino H (2007). Environmental enrichment brings a beneficial effect on beam walking and enhances the migration of doublecortinpositive cells following striatal lesions in rats. Neuroscience 144: 920-933.
60. Weindl A, Kuwert T, Leenders KL, Poremba M, Grafin von Einsiedel H, Antonini A et al (1993). Increased striatal glucose consumption in Sydenham's chorea. Mov Disord 8: 437-444.
61. Yaddanapudi K, Hornig M, Serge R, De Miranda J, Baghban A, Villar G et al (2009). Passive transfer of streptococcus-induced antibodies reproduces behavioral disturbances in a mouse model of pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection. Mol Psychiatry 15: 712-726.