Biological Psychiatry
Volume 59, Issue 4 , Pages 354-363 , 15 February 2006

Brain-Derived Neurotrophic Factor and Autoantibodies to Neural Antigens in Sera of Children with Autistic Spectrum Disorders, Landau-Kleffner Syndrome, and Epilepsy

  • Anne M. Connolly

      Affiliations

    • Department of Neurology and Pediatrics, Washington University School of Medicine, St. Louis, Missouri
    • Corresponding Author InformationAddress reprint requests to Dr. Anne Connolly, Department of Neurology, Box 8111, Washington University School of Medicine, 660 S Euclid Ave, St. Louis, MO 63110
    • ,
  • Michael Chez

      Affiliations

    • Department of Neurology, Rosalind Franklin University, Chicago Medical School, Chicago, Illinois
    • ,
  • Elizabeth M. Streif

      Affiliations

    • Department of Neurology and Pediatrics, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Richard M. Keeling

      Affiliations

    • Department of Neurology and Pediatrics, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Paul T. Golumbek

      Affiliations

    • Department of Neurology and Pediatrics, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Jennifer M. Kwon

      Affiliations

    • University of Rochester, Rochester, New York
    • ,
  • James J. Riviello

      Affiliations

    • Harvard Medical School, Boston, Massachusetts
    • ,
  • Ricki G. Robinson

      Affiliations

    • Keck School of Medicine at USC, Los Angeles, California
    • ,
  • Rosalind J. Neuman

      Affiliations

    • Department of Psychiatry and Genetics, Washington University School of Medicine, St. Louis, Missouri
    • ,
  • Ruth Mary K. Deuel

      Affiliations

    • Saint Louis University, St. Louis, Missouri

Received 19 January 2005 ,Revised 10 June 2005 ,Accepted 1 July 2005.

References 

  1. Aarden LA , deGroot ER , Feltkamp TEW . Immunology of DNA. III. Crithidia luciliae, a simple substrate for the determination of anti-dsDNA with the immunofluorescence technique . Ann N Y Acad Sci . 1975;254:505–515
  2. American Psychiatric Association . Diagnostic and Statistical Manual-Text Revision (DSM-IV-TR TM) . Washington, DC: American Psychiatric Association; 2000;
  3. Appleton RE . The Landau-Kleffner syndrome . [review] Arch Dis Child . 1995;72:386–387
  4. Bailey A , Le Couteur A , Gottesman I , Bolton P , Simonoff E , Yuzda E , et al.   Autism as a strongly genetic disorder (Evidence from a British twin study) . Psychol Med . 1995;25:63–77
  5. Bailey A , Phillips W , Rutter M . Autism (Towards an integration of clinical, genetic, neuropsychological, and neurobiological perspectives) . J Child Psychol Psychiatry . 1996;37:89–126
  6. Baird G , Charman T , Baron-Cohen S , Cox A , Swettenham J , Wheelwright S , et al.   A screening instrument for autism at 18 months of age (A 6-year follow-up study) . J Am Acad Child Adolesc Psychiatry . 2000;39:694–702
  7. Binder DK , Croll SD , Gall CM , Scharfman HE . BDNF and epilepsy (Too much of a good thing?) . Trends Neurosci . 2001;24:47–53
  8. Chakrabarti S , Fombonne E . Pervasive developmental disorders in preschool children . JAMA . 2001;285:3093–3099
  9. Chavko M , Nadi NS , Keyser DO . Activation of BDNF mRNA and protein after seizures in hyperbaric oxygen (Implications for sensitization to seizures in re-exposures) . Neurochem Res . 2002;27:1649–1653
  10. Chez MG , Connolly AM , Nowinski C , Buchanan C . The presence of autoantibodies in idiopathic/acquired versus genetic variants of pediatric epilepsy . Epilepsia . 2000;41S:183
  11. Connolly AM , Chez MG , Pestronk A , Arnold S , Mehta S , Buchanon D , et al.   Serum autoantibodies to human temporal lobe cortex in children with epilepsyand language dysfunction . Ann Neurol . 1997;42:490
  12. Connolly AM , Chez MG , Pestronk A , Arnold ST , Mehta S , Deuel RK . Serum autoantibodies to brain in Landau-Kleffner variant, autism, and other neurologic disorders . J Pediatr . 1999;134:607–613
  13. Connolly AM , Pestronk A . Anti-tubulin autoantibodies in acquired demyelination polyneuropathies . J Infect Dis . 1997;176(suppl 2):S157–S159
  14. Connolly AM , Pestronk A , Mehta S , Pranzatelli MR , Noetzel MJ . Serum autoantibodies in childhood opsoclonus-myoclonus syndrome (An analysis of antigenic targets in neural tissues) . J Pediatr . 1997;130:878–884
  15. Connolly AM , Pestronk A , Trotter JL , Feldman EL , Cornblath DR , Olney RK . High titer selective serum anti-β-tubulin antibodies in chronic inflammatory demyelinating polyneuropathy . Neurology . 1993;43:557–562
  16. Cook EH . Genetics of autism . Child Adolesc Psychiatr Clin N Am . 2001;10:333–350
  17. Cross AH , Trotter JL , Lyons J . B cells and antibodies in CNS demyelinating disease . J Neuroimmunol . 2001;112:1–14
  18. DeLong G , Bear B , Brown F . Acquired reversible autistic syndrome in acute encephalopahtic illness in children . Arch Neurol . 1981;38:191–194
  19. Deuel RK . Autism (A cognitive developmental riddle) . Pediatr Neurol . 2002;26:349–357
  20. Echenne B , Cheminal R , Rivier F , Negre C , Touchon J , Billiard M . Epileptic electroencephalographic abnormalities and developmental dysphasias (A study of 32 patients) . Brain Dev . 1992;14:216–225
  21. Fayad MN , Choueiri R , Mikati M . Landau-Kleffner Syndrome – consistent response to repeated intravenous gamma-globulin doses – a case report . Epilepsia . 1997;38:489–494
  22. Fazio R , Nemni R , Quattrini A , Lorenzetti I , Canal N . IgG monoclonal proteins from patients with axonal peripheral neuropathies bind to different epitopes of the 68 kDa neurofilament protein . J Neuroimmunol . 1992;36:97–104
  23. Folstein D , Rutter M . Genetic influences and infantile autism . Nature . 1977;265:726–728
  24. Fujimura H , Altar CA , Chen R , Nakamura T , Nakahashi T , Kambayashi J , et al.   Brain-derived neurotrophic factor is stored in human platelets and released by agonist stimulation . Thromb Haemost . 2002;87:728–734
  25. Galvin KA , Oorschot DE . Continuous low-dose treatment with brain-derived neurotrophic factor or neurotrophin-3 protects striatal medium spiny neurons from mild neonatal hypoxia/ischemia (A stereological study) . Neuroscience . 2003;118:1023–1032
  26. Hurez V , Kaveri SV , Kazatchkine MD . Expression and control of the natural autoreactive IgG repertoire in normal human serum . Eur J Immunol . 1993;23:783–789
  27. Ilzecka J , Stelmasiak Z . Brain-derived neurotrophic factor is not altered in the serum and cerebrospinal fluid of amyotrophic lateral sclerosis patients . Neurol Sci . 2002;22:473–474
  28. Jankowsky JL , Patterson PH . Cytokine and growth factor involvement in long-term potentiation . Mol Cell Neurosci . 1999;14:273–286
  29. Kanemoto K , Kawasaki J , Tarao Y , Kumaki T , Oshima T , Kaji R , et al.   Association of partial epilepsy with brain-derived neurotrophic factor (BDNF) gene polymorphisms . Epilepsy Res . 2003;53:255–258
  30. Karege F , Perret G , Bondolfi G , Schwald M , Bertschy G , Aubry JM . Decreased serum brain-derived neurotrophic factor levels in major depressed patients . Psychiatry Res . 2002;109:143–148
  31. Kerschensteiner M , Gallmeier E , Behrens L , Leal VV , Misgeld T , Klinkert WE , et al.   Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions (A neuroprotective role of inflammation?) . J Exp Med . 1999;189:865–870
  32. Landau WM . Landau-Kleffner syndrome. An eponymic badge of ignorance . [editorial; comment] Arch Neurol . 1992;49:353
  33. Landau WM , Kleffner FR . Syndrome of acquired aphasia with convulsive disorder . Neurology . 1957;7:523–530
  34. Landau WM , Kleffner FR . Syndrome of acquired aphasia with convulsive disorder in children. 1956 . Neurology . 2001;57(11 suppl 4):S29–S36
  35. Lerman P , Lerman-Sagie T , Kivity S . Effect of early corticosteroid therapy for Landau-Kleffner syndrome . Dev Med Child Neurol . 1991;33:257–260
  36. Lindholm D , Hamner S , Zirrgiebel U . Neurotrophins and cerebellar development . Perspect Dev Neurobiol . 1997;5:83–94
  37. Mantovani JF , Landau WM . Acquired aphasia with convulsive disorder (Course and prognosis) . Neurology . 1980;30:524–529
  38. Marien P , Saerens J , Verslegers W , Borggreve F , De Deyn PP . Some controversies about type and nature of aphasic symptomatology in Landau-Kleffner’s syndrome (A case study) . Acta Neurol Belg . 1993;93:183–203
  39. Murphy CC , Trevathan E , Yeargin-Allsopp M . Prevalence of epilepsy and epileptic seizures in 10-year-old children (Results from the Metropolitan Atlanta Developmental Disabilities Study) . Epilepsia . 1995;36:866–872
  40. Naylor RL , Robertson AG , Allen SJ , Sessions RB , Clarke AR , Mason GG , et al.   A discrete domain of the human TrkB receptor defines the binding sites for BDNF and NT-4 . Biochem Biophys Res Commun . 2002;291:501–507
  41. Nelson KB , Grether JK , Croen LA , Dambrosia JM , Dickens BF , Jelliffe LL , et al.   Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation . Ann Neurol . 2001;49:597–606
  42. Nemni R , Feltri ML , Fazio R , Quattrini A , Lorenzetti I , Corbo M , et al.   Axonal neuropathy with monoclonal IgG kappa that binds to a neurofilament protein . Ann Neurol . 1990;28:361–364
  43. Nevsimalova S , Tauberova A , Doutlik S , Kucera V , Dlouha O . A role of autoimmunity in the etiopathogenesis of Landau-Kleffner syndrome? . Brain Dev . 1992;14:342–345
  44. Noetzel JJ , Agrawal HC . Immunoblot identification of glial fibrillary acidic protein in rat sciatic nerve, brain, and spinal cord during development . Neurochem Res . 1985;10:737–753
  45. Noetzel MJ , Cawley LP , James VL , Minard BJ , Agrawal HC . Anti-neurofilament protein antibodies in opsoclonus-myoclonus . J Neuroimmunol . 1987;15:137–145
  46. Paquier PF , Van Dongen HR , Loonen CB . The Landau-Kleffner syndrome or ’acquired aphasia with convulsive disorder’. Long-term follow-up of six children and a review of the recent literature . Arch Neurol . 1992;49:354–359
  47. Plioplys AV , Greaves A , Kazemi K , Silverman E . Immunoglobulin reactivity in autism and Rett’s syndrome . Dev Brain Dysfunct . 1994;7:12–16
  48. Rapin I . Acquired aphasia in children . J Child Neurol . 1995;10:267–270
  49. Shafrir Y , Prensky AL . Acquired epileptiform opercular syndrome (A second case report, review of the literature, and comparison to the Landau-Kleffner syndrome) . [review] Epilepsia . 1995;36:1050–1057
  50. Singh VK , Cheng JF . Immunoreactive S100 proteins of blood immunocytes and brain cells . J Neuroimmunol . 1996;64:135–139
  51. Singh VK , Fudenberg HH , Emerson D , Coleman M . Immunodiagnosis and immunotherapy in autistic children . Ann N Y Acad Sci . 1988;540:602–604
  52. Singh VK , Lin SX , Yang VC . Serological association of measles virus and human herpesvirus-6 with brain autoantibodies in autism . Clin Immunol Immunopathol . 1998;89:105–108
  53. Singh VK , Warren RP , Odell JD , Warren WL , Cole P . Antibodies to myelin basic protein in children with autistic behavior . Brain Behav Immun . 1993;7:97–103
  54. Soprano AM , Garcia EF , Caraballo R , Fejerman N . Acquired epileptic aphasia (Neuropsychologic follow-up of 12 patients) . Pediatr Neurol . 1994;11:230–235
  55. Tabakman R , Lecht S , Sephanova S , Arien-Zakay H , Lazarovici P . Interactions between the cells of the immune and nervous system (Neurotrophins as neuroprotection mediators in CNS injury) . Prog Brain Res . 2004;146:387–401
  56. Tanguay PE . Pervasive developmental disorders (A 10-year review) . J Am Acad Child Adolesc Psychiatry . 2000;39:1079–1095
  57. Todd RD , Hickok JM , Anderson GM , Cohen DJ . Antibrain antibodies in infantile autism . Biol Psychiatry . 1988;23:644–647
  58. Tuchman RF , Rapin I . Regression in pervasive developmental disorders (Seizures and epileptiform electroencephalogram correlates) . Pediatrics . 1997;99:560–566
  59. Warren RP , Foster A , Margaretten NC . Reduced natural killer cell activity in autism . J Am Acad Child Adolesc Psychiatry . 1987;26:333–335
  60. Warren RP , Yonk J , Burger RW , Odell D , Warren WL . DR-positive T cells in autism (Association with decreased plasma levels of the complement C4B protein) . Neuropsychobiology . 1995;31:53–57
  61. Warren RP , Yonk LJ , Burger RA , Cole P , Odell JD , Warren WL , et al.   Deficiency of suppressor-inducer (CD4+CD45RA+) T cells in autism . Immunol Invest . 1990;19:245–251
  62. Wu D , Pardridge WM . Neuroprotection with noninvasive neurotrophin delivery to the brain . Proc Natl Acad Sci U S A . 1999;96:254–259

PII: S0006-3223(05)00851-6

doi: 10.1016/j.biopsych.2005.07.004

Biological Psychiatry
Volume 59, Issue 4 , Pages 354-363 , 15 February 2006

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