Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 313 (5794): 1795-1800

Copyright © 2006 by the American Association for the Advancement of Science

PirB Restricts Ocular-Dominance Plasticity in Visual Cortex

Josh Syken, Tadzia GrandPre, Patrick O. Kanold, Carla J. Shatz*

Abstract: Experience can alter synaptic connectivity throughout life, but the degree of plasticity present at each age is regulated by mechanisms that remain largely unknown. Here, we demonstrate that Paired-immunoglobulin–like receptor B (PirB), a major histocompatibility complex class I (MHCI) receptor, is expressed in subsets of neurons throughout the brain. Neuronal PirB protein is associated with synapses and forms complexes with the phosphatases Shp-1 and Shp-2. Soluble PirB fusion protein binds to cortical neurons in an MHCI-dependent manner. In mutant mice lacking functional PirB, cortical ocular-dominance plasticity is more robust at all ages. Thus, an MHCI receptor is expressed in central nervous system neurons and functions to limit the extent of experience-dependent plasticity in the visual cortex throughout life. PirB is also expressed in many other regions of the central nervous system, suggesting that it may function broadly to stabilize neural circuits.

Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA.

* To whom correspondence should be addressed. E-mail: carla_shatz{at}hms.harvard.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
PirB regulates a structural substrate for cortical plasticity.
M. Djurisic, G. S. Vidal, M. Mann, A. Aharon, T. Kim, A. Ferrao Santos, Y. Zuo, M. Hubener, and C. J. Shatz (2013)
PNAS 110, 20771-20776
   Abstract »    Full Text »    PDF »
Promiscuous Alzheimer's Amyloid: Yet Another Partner.
I. Benilova and B. De Strooper (2013)
Science 341, 1354-1355
   Abstract »    Full Text »    PDF »
Human LilrB2 Is a {beta}-Amyloid Receptor and Its Murine Homolog PirB Regulates Synaptic Plasticity in an Alzheimer's Model.
T. Kim, G. S. Vidal, M. Djurisic, C. M. William, M. E. Birnbaum, K. C. Garcia, B. T. Hyman, and C. J. Shatz (2013)
Science 341, 1399-1404
   Abstract »    Full Text »    PDF »
Learning and memory ... and the immune system.
I. Marin and J. Kipnis (2013)
Learn. Mem. 20, 601-606
   Abstract »    Full Text »    PDF »
MHCI Requires MEF2 Transcription Factors to Negatively Regulate Synapse Density during Development and in Disease.
B. M. Elmer, M. L. Estes, S. L. Barrow, and A. K. McAllister (2013)
J. Neurosci. 33, 13791-13804
   Abstract »    Full Text »    PDF »
A TAP1 null mutation leads to an enlarged olfactory bulb and supernumerary, ectopic olfactory glomeruli.
E. Salcedo, N. M. Cruz, X. Ly, B. A. Welander, K. Hanson, E. Kronberg, and D. Restrepo (2013)
Open Bio 3, 130044
   Abstract »    Full Text »    PDF »
Nogo-A Represses Anatomical and Synaptic Plasticity in the Central Nervous System.
A. Kempf and M. E. Schwab (2013)
Physiology 28, 151-163
   Abstract »    Full Text »    PDF »
Synaptic Plasticity Defect Following Visual Deprivation in Alzheimer's Disease Model Transgenic Mice.
C. M. William, M. L. Andermann, G. J. Goldey, D. K. Roumis, R. C. Reid, C. J. Shatz, M. W. Albers, M. P. Frosch, and B. T. Hyman (2012)
J. Neurosci. 32, 8004-8011
   Abstract »    Full Text »    PDF »
Activation of Rho GTPases Triggers Structural Remodeling and Functional Plasticity in the Adult Rat Visual Cortex.
C. Cerri, A. Fabbri, E. Vannini, M. Spolidoro, M. Costa, L. Maffei, C. Fiorentini, and M. Caleo (2011)
J. Neurosci. 31, 15163-15172
   Abstract »    Full Text »    PDF »
Electrical synapses formed by connexin36 regulate inhibition- and experience-dependent plasticity.
F. Postma, C.-H. Liu, C. Dietsche, M. Khan, H.-K. Lee, D. Paul, and P. O. Kanold (2011)
PNAS 108, 13770-13775
   Abstract »    Full Text »    PDF »
Differential but Competitive Binding of Nogo Protein and Class I Major Histocompatibility Complex (MHCI) to the PIR-B Ectodomain Provides an Inhibition of Cells.
H. Matsushita, S. Endo, E. Kobayashi, Y. Sakamoto, K. Kobayashi, K. Kitaguchi, K. Kuroki, A. Soderhall, K. Maenaka, A. Nakamura, et al. (2011)
J. Biol. Chem. 286, 25739-25747
   Abstract »    Full Text »    PDF »
Transcriptional Activation of the Pirb Gene in B Cells by PU.1 and Runx3.
K. Arita, S. Endo, T. Kaifu, K. Kitaguchi, A. Nakamura, H. Ohmori, K. Kohu, M. Satake, and T. Takai (2011)
J. Immunol. 186, 7050-7059
   Abstract »    Full Text »    PDF »
Myelin suppresses axon regeneration by PIR-B/SHP-mediated inhibition of Trk activity.
Y. Fujita, S. Endo, T. Takai, and T. Yamashita (2011)
EMBO J. 30, 1389-1401
   Abstract »    Full Text »    PDF »
NogoA restricts synaptic plasticity in the adult hippocampus on a fast time scale.
A. Delekate, M. Zagrebelsky, S. Kramer, M. E. Schwab, and M. Korte (2011)
PNAS 108, 2569-2574
   Abstract »    Full Text »    PDF »
Emerging functions of myelin-associated proteins during development, neuronal plasticity, and neurodegeneration.
F. Llorens, V. Gil, and J. A. del Rio (2011)
FASEB J 25, 463-475
   Abstract »    Full Text »    PDF »
Paired Immunoglobulin-like Receptor B Knockout Does Not Enhance Axonal Regeneration or Locomotor Recovery after Spinal Cord Injury.
Y. Nakamura, Y. Fujita, M. Ueno, T. Takai, and T. Yamashita (2011)
J. Biol. Chem. 286, 1876-1883
   Abstract »    Full Text »    PDF »
MHC class I modulates NMDA receptor function and AMPA receptor trafficking.
L. Fourgeaud, C. M. Davenport, C. M. Tyler, T. T. Cheng, M. B. Spencer, and L. M. Boulanger (2010)
PNAS 107, 22278-22283
   Abstract »    Full Text »    PDF »
Classic Major Histocompatibility Complex Class I Molecules: New Actors at the Neuromuscular Junction.
S. Cullheim and S. Thams (2010)
Neuroscientist 16, 600-607
   Abstract »    PDF »
Lynx for Braking Plasticity.
M. J. Higley and S. M. Strittmatter (2010)
Science 330, 1189-1190
   Abstract »    Full Text »    PDF »
Lynx1, a Cholinergic Brake, Limits Plasticity in Adult Visual Cortex.
H. Morishita, J. M. Miwa, N. Heintz, and T. K. Hensch (2010)
Science 330, 1238-1240
   Abstract »    Full Text »    PDF »
Removing Brakes on Adult Brain Plasticity: From Molecular to Behavioral Interventions.
D. Bavelier, D. M. Levi, R. W. Li, Y. Dan, and T. K. Hensch (2010)
J. Neurosci. 30, 14964-14971
   Abstract »    Full Text »    PDF »
Nogo-A Stabilizes the Architecture of Hippocampal Neurons.
M. Zagrebelsky, R. Schweigreiter, C. E. Bandtlow, M. E. Schwab, and M. Korte (2010)
J. Neurosci. 30, 13220-13234
   Abstract »    Full Text »    PDF »
POSH is an Intracellular Signal Transducer for the Axon Outgrowth Inhibitor Nogo66.
H. M. Dickson, J. Zurawski, H. Zhang, D. L. Turner, and A. B. Vojtek (2010)
J. Neurosci. 30, 13319-13325
   Abstract »    Full Text »    PDF »
Genetic Deletion of Paired Immunoglobulin-Like Receptor B Does Not Promote Axonal Plasticity or Functional Recovery after Traumatic Brain Injury.
S. Omoto, M. Ueno, S. Mochio, T. Takai, and T. Yamashita (2010)
J. Neurosci. 30, 13045-13052
   Abstract »    Full Text »    PDF »
Oligodendrocyte-Myelin Glycoprotein and Nogo Negatively Regulate Activity-Dependent Synaptic Plasticity.
S. J. Raiker, H. Lee, K. T. Baldwin, Y. Duan, P. Shrager, and R. J. Giger (2010)
J. Neurosci. 30, 12432-12445
   Abstract »    Full Text »    PDF »
The Ig-Like V-Type Domain of Paired Ig-Like Type 2 Receptor Alpha Is Critical for Herpes Simplex Virus Type 1-Mediated Membrane Fusion.
Q. Fan and R. Longnecker (2010)
J. Virol. 84, 8664-8672
   Abstract »    Full Text »    PDF »
Guidance Molecules in Axon Regeneration.
R. J. Giger, E. R. Hollis II, and M. H. Tuszynski (2010)
Cold Spring Harb Perspect Biol 2, a001867
   Abstract »    Full Text »    PDF »
MAG and OMgp Synergize with Nogo-A to Restrict Axonal Growth and Neurological Recovery after Spinal Cord Trauma.
W. B. J. Cafferty, P. Duffy, E. Huebner, and S. M. Strittmatter (2010)
J. Neurosci. 30, 6825-6837
   Abstract »    Full Text »    PDF »
Neurons Preferentially Respond to Self-MHC Class I Allele Products Regardless of Peptide Presented.
N. Escande-Beillard, L. Washburn, D. Zekzer, Z.-P. Wu, S. Eitan, S. Ivkovic, Y. Lu, H. Dang, B. Middleton, T. V. Bilousova, et al. (2010)
J. Immunol. 184, 816-823
   Abstract »    Full Text »    PDF »
No Nogo66- and NgR-Mediated Inhibition of Regenerating Axons in the Zebrafish Optic Nerve.
H. Abdesselem, A. Shypitsyna, G. P. Solis, V. Bodrikov, and C. A. O. Stuermer (2009)
J. Neurosci. 29, 15489-15498
   Abstract »    Full Text »    PDF »
Nogo receptor 1 regulates formation of lasting memories.
A. Karlen, T. E. Karlsson, A. Mattsson, K. Lundstromer, S. Codeluppi, T. M. Pham, C. M. Backman, S. O. Ogren, E. Aberg, A. F. Hoffman, et al. (2009)
PNAS 106, 20476-20481
   Abstract »    Full Text »    PDF »
Classical Major Histocompatibility Complex Class I Molecules in Motoneurons: New Actors at the Neuromuscular Junction.
S. Thams, P. Brodin, S. Plantman, R. Saxelin, K. Karre, and S. Cullheim (2009)
J. Neurosci. 29, 13503-13515
   Abstract »    Full Text »    PDF »
The Development of Developmental Neuroscience.
C. Mason (2009)
J. Neurosci. 29, 12735-12747
   Full Text »    PDF »
Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice.
P. O. Kanold, Y. A. Kim, T. GrandPre, and C. J. Shatz (2009)
J. Physiol. 587, 2857-2867
   Abstract »    Full Text »    PDF »
Fragile Axons Forge the Path to Gene Discovery: A MAP Kinase Pathway Regulates Axon Regeneration.
G. S. O'Brien and A. Sagasti (2009)
Science Signaling 2, pe30
   Abstract »    Full Text »    PDF »
H2-Kb and H2-Db regulate cerebellar long-term depression and limit motor learning.
M. J. McConnell, Y. H. Huang, A. Datwani, and C. J. Shatz (2009)
PNAS 106, 6784-6789
   Abstract »    Full Text »    PDF »
How are neurons wired to form functional and plastic circuits?: Meeting on Axon Guidance, Synaptogenesis & Neural Plasticity.
E. Stoeckli and Y. Zou (2009)
EMBO Rep. 10, 326-330
   Full Text »    PDF »
Molecular mechanisms of experience-dependent plasticity in visual cortex.
D. Tropea, A. Van Wart, and M. Sur (2009)
Phil Trans R Soc B 364, 341-355
   Abstract »    Full Text »    PDF »
NEUROSCIENCE: Overcoming Inhibitions.
W.-Y. Kim and W. D. Snider (2008)
Science 322, 869-872
   Abstract »    Full Text »    PDF »
PirB is a Functional Receptor for Myelin Inhibitors of Axonal Regeneration.
J. K. Atwal, J. Pinkston-Gosse, J. Syken, S. Stawicki, Y. Wu, C. Shatz, and M. Tessier-Lavigne (2008)
Science 322, 967-970
   Abstract »    Full Text »    PDF »
Afferent Deprivation Elicits a Transcriptional Response Associated with Neuronal Survival after a Critical Period in the Mouse Cochlear Nucleus.
J. A. Harris, F. Iguchi, A. H. Seidl, D. I. Lurie, and E. W Rubel (2008)
J. Neurosci. 28, 10990-11002
   Abstract »    Full Text »    PDF »
PIR-B-Deficient Mice Are Susceptible to Salmonella Infection.
I. Torii, S. Oka, M. Hotomi, W. H. Benjamin Jr, T. Takai, J. F. Kearney, D. E. Briles, and H. Kubagawa (2008)
J. Immunol. 181, 4229-4239
   Abstract »    Full Text »    PDF »
Highly Selective Receptive Fields in Mouse Visual Cortex.
C. M. Niell and M. P. Stryker (2008)
J. Neurosci. 28, 7520-7536
   Abstract »    Full Text »    PDF »
Gene expression patterns in visual cortex during the critical period: Synaptic stabilization and reversal by visual deprivation.
A. W. Lyckman, S. Horng, C. A. Leamey, D. Tropea, A. Watakabe, A. Van Wart, C. McCurry, T. Yamamori, and M. Sur (2008)
PNAS 105, 9409-9414
   Abstract »    Full Text »    PDF »
Cutting Edge: MHC Class I-Ly49 Interaction Regulates Neuronal Function.
O. Zohar, Y. Reiter, J. R. Bennink, A. Lev, S. Cavallaro, S. Paratore, C. G. Pick, G. Brooker, and J. W. Yewdell (2008)
J. Immunol. 180, 6447-6451
   Abstract »    Full Text »    PDF »
Expression of Nonclassical Class I Major Histocompatibility Genes Defines a Tripartite Organization of the Mouse Vomeronasal System.
T. Ishii and P. Mombaerts (2008)
J. Neurosci. 28, 2332-2341
   Abstract »    Full Text »    PDF »
CD3 and Immunoglobulin G Fc Receptor Regulate Cerebellar Functions.
K. Nakamura, H. Hirai, T. Torashima, T. Miyazaki, H. Tsurui, Y. Xiu, M. Ohtsuji, Q. S. Lin, K. Tsukamoto, H. Nishimura, et al. (2007)
Mol. Cell. Biol. 27, 5128-5134
   Abstract »    Full Text »    PDF »
Regulation of CNS synapses by neuronal MHC class I.
C. A. Goddard, D. A. Butts, and C. J. Shatz (2007)
PNAS 104, 6828-6833
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882