Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides

Nature Neuroscience

Volumn 12, Issue 12, 2009, Pages 1551-1558

  Leinders Zufall, Trese ^a   Ishii, Tomohiro ^b,c,e   Mombaerts, Peter ^b,c   Zufall, Frank ^a   Boehm, Thomas ^d  

^a SAARLAND UNIVERSITY   (Germany)

^b ROCKEFELLER UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID;

ANALYTICAL PARAMETERS; ARTICLE; CELL ACTIVATION; CELL STRUCTURE; GENE; GENE IDENTIFICATION; GENE LOCUS; GENE TARGETING; GENETIC TRANSCRIPTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SENSORY RECEPTOR; T LYMPHOCYTE; VOMERONASAL ORGAN; VOMERONASAL RECEPTOR;

AMINO ACIDS; ANIMALS; CALCIUM; GREEN FLUORESCENT PROTEINS; LIGANDS; MICE; MUTAGENESIS; PEPTIDE FRAGMENTS; PROTEIN BINDING; RECEPTORS, PHEROMONE; SENSORY RECEPTOR CELLS; SMELL; VOMERONASAL ORGAN;

EID: 70549099965     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2452     Document Type: Article

References (43)

1. Davis, M.M. et al. T cells as a self-referential, sensory organ. Annu. Rev. Immunol. 25, 681-695 (2007).
2. Cooper, M.D. & Alder, M.N. The evolution of adaptive immune systems. Cell 124, 815-822 (2006).
3. Davis, M.M. & Bjorkman, P.J. T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402 (1988).
4. Eason, D.D. et al. Mechanisms of antigen receptor evolution. Semin. Immunol. 16, 215-226 (2004).
5. Huh, G.S. et al. Functional requirement for class I MHC in CNS development and plasticity. Science 290, 2155-2159 (2000).
6. McConnell, M.J., Huang, Y.H., Datwani, A. & Shatz, C.J. H2-Kb and H2-Db regulate cerebellar long-term depression and limit motor learning. Proc. Natl. Acad. Sci. USA 106, 6784-6789 (2009).
7. Leinders-Zufall, T. et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033-1037 (2004).
8. He, J., Ma, L., Kim, S., Nakai, J. & Yu, C.R. Encoding gender and individual information in the mouse vomeronasal organ. Science 320, 535-538 (2008).
9. Spehr, M. et al. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 26, 1961-1970 (2006).
10. Boehm, T. Quality control in self/nonself discrimination. Cell 125, 845-858 (2006).
11. Brennan, P.A. & Zufall, F. Pheromonal communication in vertebrates. Nature 444, 308-315 (2006).
12. Rammensee, H.G., Bachmann, J. & Stefanovic, S. MHC Ligands and Peptide Motifs, (Landes Bioscience, Georgetown, TX, 1997).
13. Herrada, G. & Dulac, C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763-773 (1997).
14. Matsunami, H. & Buck, L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90, 775-784 (1997).
15. Ryba, N.J. & Tirindelli, R. A new multigene family of putative pheromone receptors. Neuron 19, 371-379 (1997).
16. Young, J.M. & Trask, B.J. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet. 23, 212-215 (2007).
17. Silvotti, L., Moiani, A., Gatti, R. & Tirindelli, R. Combinatorial co-expression of pheromone receptors, V2Rs. J. Neurochem. 103, 1753-1763 (2007).
18. Grus, W.E. & Zhang, J. Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates. Mol. Biol. Evol. 26, 407-419 (2009).
19. Del Punta, K., Puche, A., Adams, N.C., Rodriguez, I. & Mombaerts, P. A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35, 1057-1066 (2002).
20. Leinders-Zufall, T. et al. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405, 792-796 (2000).
21. Spehr, J. et al. Ca2+-calmodulin feedback mediates sensory adaptation and inhibits pheromone-sensitive ion channels in the vomeronasal organ. J. Neurosci. 29, 2125-2135 (2009).
22. Ukhanov, K., Leinders-Zufall, T. & Zufall, F. Patch-clamp analysis of gene-targeted vomeronasal neurons expressing a defned V1r or V2r receptor: ionic mechanisms underlying persistent fring. J. Neurophysiol. 98, 2357-2369 (2007).
23. Ishii, T. & Mombaerts, P. Expression of nonclassical class I major histocompatibility genes defnes a tripartite organization of the mouse vomeronasal system. J. Neurosci. 28, 2332-2341 (2008).
24. Lucas, P., Ukhanov, K., Leinders-Zufall, T. & Zufall, F. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: Mechanism of pheromone transduction. Neuron 40, 551-561 (2003).
25. Boehm, T. & Zufall, F. MHC peptides and the sensory evaluation of genotype. Trends Neurosci. 29, 100-107 (2006).
26. Bozza, T., Feinstein, P., Zheng, C. & Mombaerts, P. Odorant receptor expression defnes functional units in the mouse olfactory system. J. Neurosci. 22, 3033-3043 (2002).
27. Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A. & Mombaerts, P. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117, 833-846 (2004). (Pubitemid 38748897)
28. Grosmaitre, X., Vassalli, A., Mombaerts, P., Shepherd, G.M. & Ma, M. Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc. Natl. Acad. Sci. USA 103, 1970-1975 (2006).
29. Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263-278 (2004). (Pubitemid 38478654)
30. Boschat, C. et al. Pheromone detection mediated by a V1r vomeronasal receptor. Nat. Neurosci. 5, 1261-1262 (2002).
31. Malnic, B., Hirono, J., Sato, T. & Buck, L.B. Combinatorial receptor codes for odors. Cell 96, 713-723 (1999).
32. Firestein, S. How the olfactory system makes sense of scents. Nature 413, 211-218 (2001).
33. Luo, M. & Katz, L.C. Encoding pheromonal signals in the mammalian vomeronasal system. Curr. Opin. Neurobiol. 14, 428-434 (2004).
34. Chandrashekar, J., Hoon, M.A., Ryba, N.J. & Zuker, C.S. The receptors and cells for mammalian taste. Nature 444, 288-294 (2006).
35. Slev, P.R., Nelson, A.C. & Potts, W.K. Sensory neurons with MHC-like peptide binding properties: disease consequences. Curr. Opin. Immunol. 18, 608-616 (2006).
36. Mouritsen, S., Meldal, M., Werdelin, O., Hansen, A.S. & Buus, S. MHC molecules protect T cell epitopes against proteolytic destruction. J. Immunol. 149, 1987-1993 (1992).
37. Milinski, M. The major histocompatibility complex, sexual selection, and mate choice. Annu. Rev. Ecol. Evol. Syst. 37, 159-186 (2006).
38. Marrack, P., Scott-Browne, J.P., Dai, S., Gapin, L. & Kappler, J.W. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu. Rev. Immunol. 26, 171-203 (2008).
39. Garcia, K.C., Adams, J.J., Feng, D. & Ely, L.K. The molecular basis of TCR germline bias for MHC is surprisingly simple. Nat. Immunol. 10, 143-147 (2009).
40. Krogsgaard, M., Juang, J. & Davis, M.M. A role for "self" in T-cell activation. Semin. Immunol. 19, 236-244 (2007).
41. Wucherpfennig, K.W. The structural interactions between T cell receptors and MHC-peptide complexes place physical limits on self-nonself discrimination. Curr. Top. Microbiol. Immunol. 296, 19-37 (2005).
42. Padovan, E. et al. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 262, 422-424 (1993).
43. Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675-686 (1996).