Major histocompatibility complex class I proteins in brain development and plasticity

Trends in Neurosciences

Volumn 35, Issue 11, 2012, Pages 660-670

  Elmer, Bradford M ^a   McAllister, A Kimberley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Neuroimmunology; Synapse formation

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

BRAIN DEVELOPMENT; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; PRIORITY JOURNAL; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL SYSTEM;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM DISEASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, MHC CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOMEOSTASIS; HUMANS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURITES; NEUROGENESIS; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; ORGAN SPECIFICITY; RECEPTORS, IMMUNOLOGIC; REGENERATION; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84867916817     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.08.001     Document Type: Review

References (106)

1. Murphy J.B., Sturm E. conditions determining the transplantability of tissues in the brain. J. Exp. Med. 1923, 38:183-197.
2. Joly E., et al. Viral persistence in neurons explained by lack of major histocompatibility class I expression. Science 1991, 253:1283-1285.
3. Garay P.A., McAllister A.K. Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front. Synaptic Neurosci. 2010, 2:136.
4. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 2009, 64:93-109.
5. Shatz C.J. MHC class I: an unexpected role in neuronal plasticity. Neuron 2009, 64:40-45.
6. Stephan A.H., et al. The complement system: an unexpected role in synaptic pruning during development and disease. Annu. Rev. Neurosci. 2012, 35:369-389.
7. Schafer D.P., Stevens B. Synapse elimination during development and disease: immune molecules take centre stage. Biochem. Soc. Trans. 2010, 38:476-481.
8. Cullheim S., Thams S. Classic major histocompatibility complex class I molecules: new actors at the neuromuscular junction. Neuroscientist 2010, 16:600-607.
9. Shiina T., et al. The HLA genomic loci map: expression, interaction, diversity and disease. J. Hum. Genet. 2009, 54:15-39.
10. Thorsby E. Invited anniversary review: HLA associated diseases. Hum. Immunol. 1997, 53:1-11.
11. Murphy K.P., et al. Janeway's Immunobiology 2008, Garland Science.
12. Chao Y.L., et al. Association study of HLA-A gene and schizophrenia in Han Chinese from Taiwan. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:1834-1837.
13. Peaper D.R., Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 2008, 24:343-368.
14. Abbas A.K., et al. Cellular and Molecular Immunology 2010, Saunders/Elsevier.
15. Krzewski K., Strominger J.L. The killer's kiss: the many functions of NK cell immunological synapses. Curr. Opin. Cell Biol. 2008, 20:597-605.
16. Long E.O. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 2008, 224:70-84.
17. Corriveau R., et al. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 1998, 21:505-520.
18. Belgard T.G., et al. A transcriptomic atlas of mouse neocortical layers. Neuron 2011, 71:605-616.
19. McConnell M.J., et al. H2-Kb and H2-Db regulate cerebellar long-term depression and limit motor learning. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6784-6789.
20. Letellier M., et al. Normal adult climbing fiber monoinnervation of cerebellar Purkinje cells in mice lacking MHC class I molecules. Dev. Neurobiol. 2008, 68:997-1006.
21. Loconto J., et al. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 2003, 112:607-618.
22. Ribic A., et al. Activity-dependent regulation of MHC class I expression in the developing primary visual cortex of the common marmoset monkey. Behav. Brain Funct. 2011, 7:1.
23. Cahoy J.D., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
24. Neumann H., et al. Major histocompatibility complex (MHC) class I gene expression in single neurons of the central nervous system: differential regulation by interferon (IFN)-gamma and tumor necrosis factor (TNF)-alpha. J. Exp. Med. 1997, 185:305-316.
25. Ishii T., Mombaerts P. Expression of nonclassical class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system. J. Neurosci. 2008, 28:2332-2341.
26. Miralves J., et al. High levels of MeCP2 depress MHC class I expression in neuronal cells. PLoS ONE 2007, 2:e1354.
27. Thams S., et al. MHC class I expression and synaptic plasticity after nerve lesion. Brain Res. Rev. 2008, 57:265-269.
28. Linda H., et al. Expression of MHC class I and beta2-microglobulin in rat spinal motoneurons: regulatory influences by IFN-gamma and axotomy. Exp. Neurol. 1998, 150:282-295.
29. Needleman L.A., et al. MHC class I molecules are present both pre- and postsynaptically in the visual cortex during postnatal development and in adulthood. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16999-17004.
30. Neumann H., et al. Induction of MHC class I genes in neurons. Science 1995, 269:549-552.
31. Rall G., et al. Consequences of cytotoxic T lymphocyte interaction with major histocompatibility complex class I-expressing neurons in vivo. J. Exp. Med. 1995, 182:1201-1212.
32. Glynn M.W., et al. MHCI negatively regulates synapse density during the establishment of cortical connections. Nat. Neurosci. 2011, 14:442-451.
33. Zhong J., et al. Dendritic mRNAs encode diversified functionalities in hippocampal pyramidal neurons. BMC Neurosci. 2006, 7:17.
34. Brown V., et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 2001, 107:477-487.
35. Adelson J.D., et al. Neuroprotection from stroke in the absence of MHCI or PirB. Neuron 2012, 73:1100-1107.
36. Massa P.T., et al. Cell type-specific regulation of major histocompatibility complex (MHC) class I gene expression in astrocytes, oligodendrocytes, and neurons. Glia 1993, 8:201-207.
37. Ling E.A., et al. Expression of major histocompatibility complex antigens and CR3 complement receptors in activated microglia following an injection of ricin into the sciatic nerve in rats. Histol. Histopathol. 1992, 7:93-100.
38. VanGuilder Starkey H.D., et al. Neuroglial expression of the MHCI pathway and PirB receptor is upregulated in the hippocampus with advanced aging. J. Mol. Neurosci. 2012, 48:111-126.
39. Goddard C., et al. Regulation of CNS synapses by neuronal MHC class I. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:6828-6833.
40. Huh G., et al. Functional requirement for class I MHC in CNS development and plasticity. Science 2000, 290:2155-2159.
41. Baudouin S.J., et al. The signaling adaptor protein CD3zeta is a negative regulator of dendrite development in young neurons. Mol. Biol. Cell 2008, 19:2444-2456.
42. Nakamura K., et al. CD3 and immunoglobulin G Fc receptor regulate cerebellar functions. Mol. Cell. Biol. 2007, 27:5128-5134.
43. Syken J., Shatz C.J. Expression of T cell receptor beta locus in central nervous system neurons. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13048-13053.
44. Syken J., et al. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006, 313:1795-1800.
45. Zohar O., et al. Cutting edge: MHC class I-Ly49 interaction regulates neuronal function. J. Immunol. 2008, 180:6447-6451.
46. Bryceson Y.T., et al. Expression of a killer cell receptor-like gene in plastic regions of the central nervous system. J. Neuroimmunol. 2005, 161:177-182.
47. Datwani A., et al. Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron 2009, 64:463-470.
48. Xu H.P., et al. The immune protein CD3zeta is required for normal development of neural circuits in the retina. Neuron 2010, 65:503-515.
49. Schafer D.P., et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012, 74:691-705.
50. Rall G.F., et al. Consequences of cytotoxic T lymphocyte interaction with major histocompatibility complex class I-expressing neurons in vivo. J. Exp. Med. 1995, 182:1201-1212.
51. Wu Z.P., et al. Enhanced neuronal expression of major histocompatibility complex class I leads to aberrations in neurodevelopment and neurorepair. J. Neuroimmunol. 2011, 232:8-16.
52. Bilousova T., et al. Major histocompatibility complex class I molecules modulate embryonic neuritogenesis and neuronal polarization. J. Neuroimmunol. 2012, 247:1-8.
53. Washburn L.R., et al. A potential role for shed soluble major histocompatibility class I molecules as modulators of neurite outgrowth. PLoS ONE 2011, 6:e18439.
54. Escande-Beillard N., et al. Neurons preferentially respond to self-MHC class I allele products regardless of peptide presented. J. Immunol. 2010, 184:816-823.
55. Fourgeaud L., et al. MHC class I modulates NMDA receptor function and AMPA receptor trafficking. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:22278-22283.
56. Raiker S.J., et al. Oligodendrocyte-myelin glycoprotein and Nogo negatively regulate activity-dependent synaptic plasticity. J. Neurosci. 2010, 30:12432-12445.
57. Barco A., et al. Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 2005, 48:123-137.
58. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
59. Boulanger L., Shatz C. Immune signalling in neural development, synaptic plasticity and disease. Nat. Rev. Neurosci. 2004, 5:521-531.
60. Doucey M.A., et al. Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 2004, 5:328-336.
61. Fishman D., et al. Non-immune functions of MHC class I glycoproteins in normal and malignant cells. Folia Biol. (Praha) 2004, 50:35-42.
62. Hsu D., Olefsky J. Effect of a major histocompatibility complex class I peptide on insulin-like growth factor-I receptor internalization and biological signaling. Endocrinology 1993, 133:1247-1251.
63. Olsson L., et al. Regulation of receptor internalization by the major histocompatibility complex class I molecule. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:9086-9090.
64. Stagsted J., et al. Regulation of insulin receptor functions by a peptide derived from a major histocompatibility complex class I antigen. Cell 1990, 62:297-307.
65. Bennett M.J., et al. Crystal structure of the hereditary haemochromatosis protein HFE complexed with transferrin receptor. Nature 2000, 403:46-53.
66. Stagsted J., et al. Inhibition of internalization of glucose transporters and IGF-II receptors. Mechanism of action of MHC class I-derived peptides which augment the insulin response in rat adipose cells. J. Biol. Chem. 1993, 268:22809-22813.
67. Chvatchko Y., et al. Immunoprecipitation of insulin receptors by antibodies against class 1 antigens of the murine H-2 major histocompatibility complex. FEBS Lett. 1983, 163:207-211.
68. Demaria S., et al. Soluble beta 2-microglobulin-free class I heavy chains are released from the surface of activated and leukemia cells by a metalloprotease. J. Biol. Chem. 1994, 269:6689-6694.
69. Stevens B., et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
70. Fujita Y., et al. Myelin suppresses axon regeneration by PIR-B/SHP-mediated inhibition of Trk activity. EMBO J. 2011, 30:1389-1401.
71. Atwal J.K., et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
72. Nakamura Y., et al. Paired immunoglobulin-like receptor B knockout does not enhance axonal regeneration or locomotor recovery after spinal cord injury. J. Biol. Chem. 2011, 286:1876-1883.
73. Joseph M.S., et al. Transgenic mice with enhanced neuronal major histocompatibility complex class I expression recover locomotor function better after spinal cord injury. J. Neurosci. Res. 2011, 89:365-372.
74. Oliveira A.L., et al. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17843-17848.
75. Zanon R.G., Oliveira A.L. MHC I upregulation influences astroglial reaction and synaptic plasticity in the spinal cord after sciatic nerve transection. Exp. Neurol. 2006, 200:521-531.
76. Torres A.R., et al. The association and linkage of the HLA-A2 class I allele with autism. Hum. Immunol. 2006, 67:346-351.
77. Stubbs E.G., et al. Autism and shared parental HLA antigens. J. Am. Acad. Child Psychiatry 1985, 24:182-185.
78. Stubbs G. Shared parental HLA antigens and autism. Lancet 1981, 2:534.
79. Shi J., et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009, 460:753-757.
80. Stefansson H., et al. Common variants conferring risk of schizophrenia. Nature 2009, 460:744-747.
81. Purcell S.M., et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009, 460:748-752.
82. Jia P., et al. A bias-reducing pathway enrichment analysis of genome-wide association data confirmed association of the MHC region with schizophrenia. J. Med. Genet. 2012, 49:96-103.
83. Kano S., et al. Altered MHC class I expression in dorsolateral prefrontal cortex of nonsmoker patients with schizophrenia. Neurosci. Res. 2011, 71:289-293.
84. Drew P.D., et al. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J. Immunol. 1993, 150:3300-3310.
85. Fujimaki H., et al. IFN-gamma induces expression of MHC class I molecules in adult mouse dorsal root ganglion neurones. Neuroreport 1996, 7:2951-2955.
86. Chevalier G., et al. Neurons are MHC class I-dependent targets for CD8 T cells upon neurotropic viral infection. PLoS Pathog. 2011, 7:e1002393.
87. Vargas D.L., et al. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 2005, 57:67-81.
88. Chez M.G., et al. Elevation of tumor necrosis factor-alpha in cerebrospinal fluid of autistic children. Pediatr. Neurol. 2007, 36:361-365.
89. Ashwood P., et al. Associations of impaired behaviors with elevated plasma chemokines in autism spectrum disorders. J. Neuroimmunol. 2011, 232:196-199.
90. Ashwood P., et al. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav. Immun. 2011, 25:40-45.
91. Ashwood P., et al. Decreased transforming growth factor beta1 in autism: a potential link between immune dysregulation and impairment in clinical behavioral outcomes. J. Neuroimmunol. 2008, 204:149-153.
92. Nawa H., et al. Cytokine and growth factor involvement in schizophrenia--support for the developmental model. Mol. Psychiatry 2000, 5:594-603.
93. Deverman B.E., Patterson P.H. Cytokines and CNS development. Neuron 2009, 64:61-78.
94. Brown A.S., Patterson P.H. Maternal infection and schizophrenia: implications for prevention. Schizophr. Bull. 2011, 37:284-290.
95. Bauer S., et al. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat. Rev. 2007, 8:221-232.
96. Patterson P.H. Neuroscience. Maternal effects on schizophrenia risk. Science 2007, 318:576-577.
97. Molloy C.A., et al. Elevated cytokine levels in children with autism spectrum disorder. J. Neuroimmunol. 2006, 172:198-205.
98. Careaga M., et al. Immune dysfunction in autism: a pathway to treatment. Neurotherapeutics 2010, 7:283-292.
99. Miller B.J., et al. Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol. Psychiatry 2011, 70:663-671.
100. McAllister A.K., van de Water J. Breaking boundaries in neural-immune interactions. Neuron 2009, 64:9-12.
101. Held W., Mariuzza R.A. Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat. Rev. Immunol. 2008, 8:269-278.
102. Scarpellino L., et al. Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J. Immunol. 2007, 178:1277-1284.
103. Stagsted J. Journey beyond immunology. Regulation of receptor internalization by major histocompatibility complex class I (MHC-I) and effect of peptides derived from MHC-I. APMIS Suppl. 1998, 85:1-40.
104. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5:97-107.
105. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
106. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.