Rett syndrome and other autism spectrum disordersbrain diseases of immune malfunction

Molecular Psychiatry

Volumn 15, Issue 4, 2010, Pages 355-363

  Derecki, N C ^a,b   Privman, E ^a,b   Kipnis, J ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Immune system; Neurodevelopment; Neuroimmunology; Protective immunity; Rett syndrome; T cells

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOKINE; CYTOKINE; METHYL CPG BINDING PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA;

AUTISM; BRAIN DISEASE; COMPLEMENT FACTOR; GENE EXPRESSION; HUMAN; IMMUNE DYSREGULATION; IMMUNE SYSTEM; MAJOR HISTOCOMPATIBILITY COMPLEX; NERVE CELL DIFFERENTIATION; NEUROIMMUNOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; RETT SYNDROME; REVIEW; T LYMPHOCYTE;

ANIMALS; AUTISTIC DISORDER; BRAIN DISEASES; HUMANS; IMMUNE SYSTEM DISEASES; RETT SYNDROME;

EID: 77950019870     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2010.21     Document Type: Review

References (105)

1. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M. Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 1999; 5: 49-55.
2. Cohen IR, Schwartz M. Autoimmune maintenance and neuro-protection of the central nervous system. J Neuroimmunol 1999; 100: 111-114.
3. Schwartz M, Moalem G, Leibowitz-Amit R, Cohen IR. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 1999; 22: 295-299.
4. Serpe CJ, Tetzlaff JE, Coers S, Sanders VM, Jones KJ. Functional recovery after facial nerve crush is delayed in severe combined immunodeficient mice. Brain Behav Immun 2002; 16: 808-812.
5. Serpe CJ, Coers S, Sanders VM, Jones KJ. CD4 \+ T, but not CD8 \+ or B, lymphocytes mediate facial motoneuron survival after facial nerve transection. Brain Behav Immun 2003; 17: 393-402.
6. Byram SC, Carson MJ, DeBoy CA, Serpe CJ, Sanders VM, Jones KJ. CD4-positive T cell-mediated neuroprotection requires dual compartment antigen presentation. J Neurosci 2004; 24: 4333-4339.
7. Hofstetter HH, Sewell DL, Liu F, Sandor M, Forsthuber T, Lehmann PV et al. Autoreactive T cells promote post-traumatic healing in the central nervous system. J Neuroimmunol 2003; 134: 25-34.
8. Kipnis J, Schwartz M. Dual action of glatiramer acetate (Cop-1) in the treatment of CNS autoimmune and neurodegenerative disorders. Trends Mol Med 2002; 8: 319-323.
9. Karman J, Chu HH, Co DO, Seroogy CM, Sandor M, Fabry Z. Dendritic cells amplify T cell-mediated immune responses in the central nervous system. J Immunol 2006; 177: 7750-7760.
10. Frenkel D, Huang Z, Maron R, Koldzic DN, Moskowitz MA, Weiner HL. Neuroprotection by IL-10-producing MOG CD4 \+ T cells following ischemic stroke. J Neurol Sci 2005; 233: 125-132.
11. Butovsky O, Landa G, Kunis G, Ziv Y, Avidan H, Greenberg N et al. Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 2006; 116: 905-915.
12. Persson M, Brantefjord M, Hansson E, Ronnback L. Lipopoly-saccharide increases microglial GLT-1 expression and glutamate uptake capacity in vitro by a mechanism dependent on TNF-alpha. Glia 2005; 51: 111-120.
13. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009; 6: e1000113.
14. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10: 1387-1394.
15. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity 2005; 23: 344-346.
16. Michelucci A, Heurtaux T, Grandbarbe L, Morga E, Heuschling P. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: effects of oligomeric and fibrillar amyloid-beta. J Neuroimmunol 2009; 210: 3-12.
17. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 2009; 27: 119-145.
18. Kipnis J, Mizrahi T, Hauben E, Shaked I, Shevach E, Schwartz M. Neuroprotective autoimmunity: naturally occurring CD4 \+ CD25 \+ regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci USA 2002; 99: 15620-15625.
19. Schwartz M, Kipnis J. Protective autoimmunity and neuroprotec-tion in inflammatory and noninflammatory neurodegenerative diseases. J Neurol Sci 2005; 233: 163-166.
20. Yoles E, Hauben E, Palgi O, Agranov E, Gothilf A, Cohen A et al. Protective autoimmunity is a physiological response to CNS trauma. J Neurosci 2001; 21: 3740-3748.
21. Kipnis J, Cohen H, Cardon M, Ziv Y, Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc Natl Acad Sci USA 2004; 101: 8180-8185.
22. Brynskikh A, Warren T, Zhu J, Kipnis J. Adaptive immunity affects learning behavior in mice. Brain Behav Immun 2008; 22: 861-869.
23. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006; 9: 268-275.
24. Ransohoff RM, Kivisakk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003; 3: 569-581.
25. Cserr HF, Knopf PM. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol Today 1992; 13: 507-512.
26. Widner H, Moller G, Johansson BB. Immune response in deep cervical lymph nodes and spleen in the mouse after antigen deposition in different intracerebral sites. Scand J Immunol 1988; 28: 563-571.
27. McMenamin PG, Wealthall RJ, Deverall M, Cooper SJ, Griffin B. Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy. Cell Tissue Res 2003; 313: 259-269.
28. McMenamin PG. Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 1999; 405: 553-562.
29. Kivisakk P, Mahad DJ, Callahan MK, Trebst C, Tucky B, Wei T et al. Human cerebrospinal fluid central memory CD4 \+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc Natl Acad Sci USA 2003; 100: 8389-8394.
30. Qing Z, Sewell D, Sandor M, Fabry Z. Antigen-specific T cell trafficking into the central nervous system. J Neuroimmunol 2000; 105: 169-178.
31. Tran PB, Miller RJ. Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 2003; 4: 444-455.
32. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007; 131: 1164-1178.
33. Boulanger LM. Immune proteins in brain development and synaptic plasticity. Neuron 2009; 64: 93-109.
34. Corriveau RA, Huh GS, Shatz CJ. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 1998; 21: 505-520.
35. Hawley SH, Wunnenberg-Stapleton K, Hashimoto C, Laurent MN, Watabe T, Blumberg BW et al. Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev 1995; 9: 2923-2935.
36. Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR et al. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 2000; 403: 658-661.
37. Deverman BE, Patterson PH. Cytokines and CNS development. Neuron 2009; 64: 61-78.
38. Ohtani T, Ishihara K, Atsumi T, Nishida K, Kaneko Y, Miyata T et al. Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3-and SHP2-mediated signals in immune responses. Immunity 2000; 12: 95-105.
39. Mehler MF, Kessler JA. Hematolymphopoietic and inflammatory cytokines in neural development. Trends Neurosci 1997; 20: 357-365.
40. Lovett-Racke AE, Smith ME, Arredondo LR, Bittner PS, Ratts RB, Shive CL et al. Developmentally regulated gene expression of Th2 cytokines in the brain. Brain Res 2000; 870: 27-35.
41. Dziegielewska KM, Moller JE, Potter AM, Ek J, Lane MA, Saunders NR. Acute-phase cytokines IL-1beta and TNF-alpha in brain development. Cell Tissue Res 2000; 299: 335-345.
42. Gillard SE, Lu M, Mastracci RM, Miller RJ. Expression of functional chemokine receptors by rat cerebellar neurons. J Neuroimmunol 2002; 124: 16-28.
43. Oberlin E, Amara A, Bachelerie F, Bessia C, Virelizier JL, Arenzana-Seisdedos F et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996; 382: 833-835.
44. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4-and SDF-1-deficient mice. Proc Natl Acad Sci USA 1998; 95: 9448-9453.
45. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M et al. The chemokine SDF1 regulates migration of dentate granule cells. Development 2002; 129: 4249-4260.
46. Borrell V, Marin O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat Neurosci 2006; 9: 1284-1293.
47. Zhu Y, Yu T, Zhang XC, Nagasawa T, Wu JY, Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci 2002; 5: 719-720.
48. Reiss K, Mentlein R, Sievers J, Hartmann D. Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 2002; 115: 295-305.
49. Chalasani SH, Sabol A, Xu H, Gyda MA, Rasband K, Granato M et al. Stromal cell-derived factor-1 antagonizes slit/robo signaling in vivo. J Neurosci 2007; 27: 973-980.
50. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA. A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 2003; 23: 1360-1371.
51. Lieberam I, Agalliu D, Nagasawa T, Ericson J, Jessell TM. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 2005; 47: 667-679.
52. Pettigrew HD, Teuber SS, Gershwin ME. Clinical significance of complement deficiencies. Ann N Y Acad Sci 2009; 1173: 108-123.
53. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ. Functional requirement for class I MHC in CNS development and plasticity. Science 2000; 290: 2155-2159.
54. McConnell MJ, Huang YH, Datwani A, Shatz CJ. H2-K(b) and H2-D(b) regulate cerebellar long-term depression and limit motor learning. Proc Natl Acad Sci USA 2009; 106: 6784-6789.
55. Laurvick CL, Msall ME, Silburn S, Bower C, de Klerk N, Leonard H. Physical and mental health of mothers caring for a child with Rett syndrome. Pediatrics 2006; 118: e1152-e1164.
56. Moog U, Smeets EE, van Roozendaal KE, Schoenmakers S, Herbergs J, Schoonbrood-Lenssen AM et al. Neurodevelopmental disorders in males related to the gene causing Rett syndrome in females (MECP2). Eur J Paediatr Neurol 2003; 7: 5-12.
57. Shetty AK, Chatters R, Tilton AH, Lacassie Y. Syndrome of microcephaly, mental retardation, and tracheoesophageal fistula associated with features of Rett syndrome. J Child Neurol 2000; 15: 61-63.
58. Armstrong DD. Neuropathology of Rett syndrome. J Child Neurol 2005; 20: 747-753.
59. Horska A, Farage L, Bibat G, Nagae LM, Kaufmann WE, Barker PB et al. Brain metabolism in Rett syndrome: age, clinical, and genotype correlations. Ann Neurol 2009; 65: 90-97.
60. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 1999; 23: 185-188.
61. Bao X, Jiang S, Song F, Pan H, Li M, Wu X. X chromosome inactivation in Rett syndrome and its correlations with MECP2 mutations and phenotype. J Child Neurol 2008; 23: 22-25.
62. Tong Y, Aune T, Boothby M. T-bet antagonizes mSin3a recruitment and transactivates a fully methylated IFN-gamma promoter via a conserved T-box half-site. Proc Natl Acad Sci USA 2005; 102: 2034-2039.
63. Lal G, Zhang N, van der Touw W, Ding Y, Ju W, Bottinger EP et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009; 182: 259-273.
64. Balmer D, Arredondo J, Samaco RC, LaSalle JM. MECP2 mutations in Rett syndrome adversely affect lymphocyte growth, but do not affect imprinted gene expression in blood or brain. Hum Genet 2002; 110: 545-552.
65. Webb R, Wren JD, Jeffries M, Kelly JA, Kaufman KM, Tang Y et al. Variants within MECP2, a key transcription regulator, are associated with increased susceptibility to lupus and differential gene expression in patients with systemic lupus erythematosus. Arthritis Rheum 2009; 60: 1076-1084.
66. Delgado IJ, Kim DS, Thatcher KN, LaSalle JM, Van den Veyver IB. Expression profiling of clonal lymphocyte cell cultures from Rett syndrome patients. BMC Med Genet 2006; 7: 61.
67. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000; 100: 655-669.
68. Tanioka T, Hattori A, Mizutani S, Tsujimoto M. Regulation of the human leukocyte-derived arginine aminopeptidase/endoplasmic reticulum-aminopeptidase 2 gene by interferon-gamma. FEBS J 2005; 272: 916-928.
69. Plioplys AV, Greaves A, Kazemi K, Silverman E. Lymphocyte function in autism and Rett syndrome. Neuropsychobiology 1994; 29: 12-16.
70. Fiumara A, Sciotto A, Barone R, D'Asero G, Munda S, Parano E et al. Peripheral lymphocyte subsets and other immune aspects in Rett syndrome. Pediatr Neurol 1999; 21: 619-621.
71. Arman M, Aguilera-Montilla N, Mas V, Puig-Kroger A, Pignatelli M, Guigo R et al. The human CD6 gene is transcriptionally regulated by RUNX and Ets transcription factors in T cells. Mol Immunol 2009; 46: 2226-2235.
72. Komine O, Hayashi K, Natsume W, Watanabe T, Seki Y, Seki N et al. The Runx1 transcription factor inhibits the differentiation of naive CD4 \+ T cells into the Th2 lineage by repressing GATA3 expression. J Exp Med 2003; 198: 51-61.
73. Cayrol R, Wosik K, Berard JL, Dodelet-Devillers A, Ifergan I, Kebir H et al. Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system. Nat Immunol 2008; 9: 137-145.
74. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener 2009; 4: 47.
75. Holling TM, van der Stoep N, Quinten E, van den Elsen PJ. Activated human T cells accomplish MHC class II expression through T cell-specific occupation of class II transactivator promoter III. J Immunol 2002; 168: 763-770.
76. Latham KA, Whittington KB, Zhou R, Qian Z, Rosloniec EF. Ex vivo characterization of the autoimmune T cell response in the HLA-DR1 mouse model of collagen-induced arthritis reveals long-term activation of type II collagen-specific cells and their presence in arthritic joints. J Immunol 2005; 174: 3978-3985.
77. Maezawa I, Swanberg S, Harvey D, LaSalle JM, Jin LW. Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions. J Neurosci 2009; 29: 5051-5061.
78. Ballas N, Lioy DT, Grunseich C, Mandel G. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 2009; 12: 311-317.
79. Alvarez-Saavedra M, Saez MA, Kang D, Zoghbi HY, Young JI. Cell-specific expression of wild-type MeCP2 in mouse models of Rett syndrome yields insight about pathogenesis. Hum Mol Genet 2007; 16: 2315-2325.
80. Guy J, Gan J, Selfridge J, Cobb S, Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 2007; 315: 1143-1147.
81. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 2003; 302: 885-889.
82. 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.
83. Engelhardt B, Ransohoff RM. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 2005; 26: 485-495.
84. Allen NJ, Barres BA. Neuroscience: Glia\more than just brain glue. Nature 2009; 457: 675-677.
85. Ullian EM, Christopherson KS, Barres BA. Role for glia in synaptogenesis. Glia 2004; 47: 209-216.
86. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A et al. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005; 120: 421-433.
87. Chung IY, Benveniste EN. Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta. J Immunol 1990; 144: 2999-3007.
88. Chao CC, Hu S, Sheng WS, Bu D, Bukrinsky MI, Peterson PK. Cytokine-stimulated astrocytes damage human neurons via a nitric oxide mechanism. Glia 1996; 16: 276-284.
89. Garg SK, Banerjee R, Kipnis J. Neuroprotective immunity: T cell-derived glutamate endows astrocytes with a neuroprotective phenotype. J Immunol 2008; 180: 3866-3873.
90. Garg SK, Kipnis J, Banerjee R. IFN-gamma and IL-4 differentially shape metabolic responses and neuroprotective phenotype of astrocytes*. J Neurochem 2009; 108: 1155-1166.
91. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/ progenitor cells. Mol Cell Neurosci 2006; 31: 149-160.
92. Schwartz M, Butovsky O, Bruck W, Hanisch UK. Microglial phenotype: is the commitment reversible? Trends Neurosci 2006; 29: 68-74.
93. Zhao W, Xie W, Xiao Q, Beers DR, Appel SH. Protective effects of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J Neurochem 2006; 99: 1176-1187.
94. Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. CD4 \+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci USA 2008; 105: 15558-15563.
95. Baracskay KL, Kidd GJ, Miller RH, Trapp BD. NG2-positive cells generate A2B5-positive oligodendrocyte precursor cells. Glia 2007; 55: 1001-1010.
96. Pan JW, Lane JB, Hetherington H, Percy AK. Rett syndrome: 1H spectroscopic imaging at 4.1 Tesla. J Child Neurol 1999; 14: 524-528.
97. Teitelbaum D, Arnon R, Sela M. Copolymer 1: from basic research to clinical application. Cell Mol Life Sci 1997; 53: 24-28.
98. Teitelbaum D, Fridkis-Hareli M, Arnon R, Sela M. Copolymer 1 inhibits chronic relapsing experimental allergic encephalomye-litis induced by proteolipid protein (PLP) peptides in mice and interferes with PLP-specific T cell responses. J Neuroimmunol 1996; 64: 209-217.
99. Weber MS, Hohlfeld R, Zamvil SS. Mechanism of action of glatiramer acetate in treatment of multiple sclerosis. Neurother-apeutics 2007; 4: 647-653.
100. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L et al. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med 2007; 13: 935-943.
101. Frenkel D, Maron R, Burt DS, Weiner HL. Nasal vaccination with a proteosome-based adjuvant and glatiramer acetate clears beta-amyloid in a mouse model of Alzheimer disease. J Clin Invest 2005; 115: 2423-2433.
102. Benner EJ, Mosley RL, Destache CJ, Lewis TB, Jackson-Lewis V, Gorantla S et al. Therapeutic immunization protects dopaminer-gic neurons in a mouse model of Parkinson's disease. Proc Natl Acad Sci USA 2004; 101: 9435-9440.
103. Kipnis J, Yoles E, Porat Z, Cohen A, Mor F, Sela M et al. T cell immunity to copolymer 1 confers neuroprotection on the damaged optic nerve: possible therapy for optic neuropathies. Proc Natl Acad Sci USA 2000; 97: 7446-7451.
104. Liu J, Johnson TV, Lin J, Ramirez SH, Bronich TK, Caplan S et al. T cell independent mechanism for copolymer-1-induced neuro-protection. Eur J Immunol 2007; 37: 3143-3154.
105. Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C, Braun A et al. CD4-positive T lymphocytes provide a neuroim-munological link in the control of adult hippocampal neuro-genesis. J Immunol 2009; 182: 3979-3984.