MHC homologs in the nervous system - they haven't lost their groove

Current Opinion in Neurobiology

Volumn 16, Issue 3, 2006, Pages 351-357

  Olson, Rich ^a   Dulac, Catherine ^b   Bjorkman, Pamela J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GUANINE NUCLEOTIDE BINDING PROTEIN; M10 PROTEIN; PHEROMONE; UNCLASSIFIED DRUG;

BINDING SITE; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; NERVOUS SYSTEM; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; REVIEW;

ANIMALS; BRAIN; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PHEROMONES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PHEROMONE; SIGNAL TRANSDUCTION; VOMERONASAL ORGAN;

EID: 33745190019     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2006.05.007     Document Type: Review

References (61)

1. Boulanger L.M., and Shatz C.J. Immune signalling in neural development, synaptic plasticity and disease. Nat Rev Neurosci 5 (2004) 521-531
2. Loconto J., Papes F., Chang E., Stowers L., Jones E.P., Takada T., Kumanovics A., Fischer Lindahl K., and Dulac C. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112 (2003) 607-618
3. Ishii T., Hirota J., and Mombaerts P. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr Biol 13 (2003) 394-400
4. Keverne E.B. The vomeronasal organ. Science 286 (1999) 716-720
5. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., and Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405 (2000) 792-796
6. Dulac C., and Torello A.T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4 (2003) 551-562
7. Yoon H., Enquist L.W., and Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123 (2005) 669-682
8. Boehm U., Zou Z., and Buck L.B. Feedback loops link odor and pheromone signaling with reproduction. Cell 123 (2005) 683-695
9. Lin Da Y., Zhang S.Z., Block E., and Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 434 (2005) 470-477. The authors identify a male-specific volatile compound in mouse urine that increases the attractiveness of male urine to female mice and is detected by the main olfactory system.
10. Trinh K., and Storm D.R. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6 (2003) 519-525
11. Matsunami H., and Buck L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90 (1997) 775-784
12. Herrada G., and Dulac C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90 (1997) 763-773
13. Ryba N.J., and Tirindelli R. A new multigene family of putative pheromone receptors. Neuron 19 (1997) 371-379
14. Yang H., Shi P., Zhang Y.P., and Zhang J. Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86 (2005) 306-315
15. Jones E.P., Kumanovics A., Yoshino M., and Fischer Lindahl K. Mhc class I and non-class I gene organization in the proximal H2-M region of the mouse. Immunogenetics 49 (1999) 183-195
16. Pin J.P., Kniazeff J., Goudet C., Bessis A.S., Liu J., Galvez T., Acher F., Rondard P., and Prezeau L. The activation mechanism of class-C G-protein coupled receptors. Biol Cell 96 (2004) 335-342
17. Olson R., Huey-Tubman K.E., Dulac C., and Bjorkman P.J. Structure of a pheromone receptor-associated MHC molecule with an open and empty groove. PLoS Biol 3 (2005) e257. These authors show that the structure of M10.5 demonstrates that the traditional peptide-binding groove is in an open and empty conformation. Peptides that traditionally bind to classical MHC molecules do not bind to the M10.5 groove.
18. Bjorkman P.J., Saper M.A., Samraoui B., Bennett W.S., Strominger J.L., and Wiley D.C. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329 (1987) 506-512
19. Braud V.M., Allan D.S., and McMichael A.J. Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol 11 (1999) 100-108
20. Fahnestock M.L., Tamir I., Narhi L., and Bjorkman P.J. Thermal stability comparison of purified empty and peptide-filled forms of a class I MHC molecule. Science 258 (1992) 1658-1662
21. Burmeister W.P., Gastinel L.N., Simister N.E., Blum M.L., and Bjorkman P.J. Crystal structure at 2.2 Å resolution of the MHC-related neonatal Fc receptor. Nature 372 (1994) 336-343
22. Lebrón J.A., Bennett M.J., Vaughn D.E., Chirino A.J., Snow P.M., Mintier G.A., Feder J.N., and Bjorkman P.J. Crystal structure of the hemochromatosis protein HFE and characterization of its interaction with transferrin receptor. Cell 93 (1998) 111-123
23. Raghavan M., Gastinel L.N., and Bjorkman P.J. The class I major histocompatibility complex related Fc receptor shows pH-dependent stability differences correlating with immunoglobulin binding and release. Biochemistry 32 (1993) 8654-8660
24. McLatchie L.M., Fraser N.J., Main M.J., Wise A., Brown J., Thompson N., Solari R., Lee M.G., and Foord S.M. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393 (1998) 333-339
25. Bomberger J.M., Parameswaran N., Hall C.S., Aiyar N., and Spielman W.S. Novel function for receptor activity-modifying proteins (RAMPs) in post-endocytic receptor trafficking. J Biol Chem 280 (2005) 9297-9307
26. Bouschet T., Martin S., and Henley J.M. Receptor-activity-modifying proteins are required for forward trafficking of the calcium-sensing receptor to the plasma membrane. J Cell Sci 118 (2005) 4709-4720
27. Saito H., Kubota M., Roberts R.W., Chi Q., and Matsunami H. RTP family members induce functional expression of mammalian odorant receptors. Cell 119 (2004) 679-691
28. Teasdale R.D., and Jackson M.R. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu Rev Cell Dev Biol 12 (1996) 27-54
29. Shikano S., and Li M. Membrane receptor trafficking: evidence of proximal and distal zones conferred by two independent endoplasmic reticulum localization signals. Proc Natl Acad Sci USA 100 (2003) 5783-5788
30. Baker E.K., Colley N.J., and Zuker C.S. The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J 13 (1994) 4886-4895
31. Ferreira P.A., Nakayama T.A., Pak W.L., and Travis G.H. Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 383 (1996) 637-640
32. Kikuyama S., Yamamoto K., Iwata T., and Toyoda F. Peptide and protein pheromones in amphibians. Comp Biochem Physiol B Biochem Mol Biol 132 (2002) 69-74
33. Milinski M., Griffiths S., Wegner K.M., Reusch T.B., Haas-Assenbaum A., and Boehm T. Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc Natl Acad Sci USA 102 (2005) 4414-4418
34. Pearse-Pratt R., Schellinck H., Brown R., Singh P.B., and Roser B. Soluble MHC antigens and olfactory recognition of genetic individuality: the mechanism. Genetica 104 (1998) 223-230
35. Singer A.G., Beauchamp G.K., and Yamazaki K. Volatile signals of the major histocompatibility complex in male mouse urine. Proc Natl Acad Sci USA 94 (1997) 2210-2214
36. Singh P.B., Brown R.E., and Roser B. MHC antigens in urine as olfactory recognition cues. Nature 327 (1987) 161-164
37. Yamazaki K., Boyse E.A., Mike V., Thaler H.T., Mathieson B.J., Abbott J., Boyse J., Zayas Z.A., and Thomas L. Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144 (1976) 1324-1335
38. Potts W.K., Manning C.J., and Wakeland E.K. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352 (1991) 619-621
39. Hurst J.L., Robertson D.H.L., Tolladay U., and Beynon R.J. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim Behav 55 (1998) 1289-1297
40. Bruce H.M. An exteroceptive block to pregnancy in the mouse. Nature 184 (1959) 105
41. Leinders-Zufall T, Brennan P, Widmayer P, S PC, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T: MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306:1033-1037. The authors show that peptides that bind to classical MHC class I proteins activate V2R-expressing VNO neurons. Replacing residues necessary for binding to MHC molecules abolishes the activation. These peptides are also reported to elicit pregnancy block behavior in mice.
42. Rammensee H.G., Falk K., and Rötzschke O. Peptides naturally presented by MHC class I molecules. Annu Rev Immunol 11 (1993) 213-244
43. Matsumura M., Fremont D.H., Peterson P.A., and Wilson I.A. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257 (1992) 927-934
44. Cresswell P. Assembly, transport, and function of MHC class II molecules. Annu Rev Immunol 12 (1994) 259-293
45. Hurst J.L., and Beynon R.J. Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26 (2004) 1288-1298
46. Hurst J.L., Payne C.E., Nevison C.M., Marie A.D., Humphries R.E., Robertson D.H., Cavaggioni A., and Beynon R.J. Individual recognition in mice mediated by major urinary proteins. Nature 414 (2001) 631-634
47. Kimoto H., Haga S., Sato K., and Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437 (2005) 898-901. The authors demonstrate that a family of 7-kDa peptides secreted from the extraorbital lactimal gland activates V2R-expressing VNO neurons. The gene family is located downstream from the MHC on chromosome 17.
48. Corriveau R.A., Huh G.S., and Shatz C.J. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21 (1998) 505-520
49. Huh G.S., Boulanger L.M., Du H., Riquelme P.A., Brotz T.M., and Shatz C.J. Functional requirement for class I MHC in CNS development and plasticity. Science 290 (2000) 2155-2159
50. Syken J., and Shatz C.J. Expression of T cell receptor beta locus in central nervous system neurons. Proc Natl Acad Sci USA 100 (2003) 13048-13053
51. Oliveira A.L., Thams S., Lidman O., Piehl F., Hokfelt T., Karre K., Linda H., and Cullheim S. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci USA 101 (2004) 17843-17848
52. Ressler K.J., Sullivan S.L., and Buck L.B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79 (1994) 1245-1255
53. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., and Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell 79 (1994) 981-991
54. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., and Axel R. Visualizing an olfactory sensory map. Cell 87 (1996) 675-686
55. Feinstein P., and Mombaerts P. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117 (2004) 817-831
56. Belluscio L., Koentges G., Axel R., and Dulac C. A map of pheromone receptor activation in the mammalian brain. Cell 97 (1999) 209-220
57. Rodriguez I., Feinstein P., and Mombaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97 (1999) 199-208
58. He X., Tabaczewski P., Ho J., Stroynowski I., and Garcia K.C. Promiscuous antigen presentation by the nonclassical MHC Ib Qa-2 is enabled by a shallow, hydrophobic groove and self-stabilized peptide conformation. Structure 9 (2001) 1213-1224
59. Gadola S.D., Zaccai N.R., Harlos K., Shepherd D., Castro-Palomino J.C., Ritter G., Schmidt R.R., Jones E.Y., and Cerundolo V. Structure of human CD1b with bound ligands at 2.3 Å, a maze for alkyl chains. Nat Immunol 3 (2002) 721-726
60. Nicholls A., Sharp K.A., and Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11 (1991) 281-296
61. Spehr M., Kelliher K.R., Li X.H., Boehm T., Leinders-Zufall T., and Zufall F. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26 (2006) 1961-1970