Abstract
The ability of animals to recognise and discriminate individual conspecifics is a vital feature of mammalian social systems. Genes of the major histocompatibility complex (MHC) have long been recognised to play an important role in influencing chemosensory cues of individual identity. In particular, the profile of urinary volatiles of mice has been related to MHC type, although a mechanism to explain this link has remained obscure. This article aims to review recent developments, which have revealed a new class of MHC-associated chemosignals. These are nine-amino acid peptide ligands bound by MHC class I molecules, which are presented at the cell surface for immune surveillance. In addition to this immune function, these peptides have been found to elicit highly sensitive and specific responses in sensory neurons of both the main olfactory and vomeronasal systems. They have also been shown to convey information about strain identity in biologically relevant contexts. Hence it now appears that there are multiple systems for signalling MHC identity, with distinct features that are likely to be adapted for use in different behavioural contexts.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Bellringer, J.F., Pratt, H.P.M. and Keverne, E.B. (1980) Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice. J. Reprod. Fert. 59, 223–228.
Boehm, T. (2006) Co-evolution of a primordial peptide-presentation system and cellular immunity. Nature Rev. Immunol. 6, 79–84.
Boehm, T. and Zufall, F. (2006) MHC peptides and the sensory evaluation of genotype. Trends Neurosci. 29, 100–107.
Boyse, E.A., Beauchamp, G.K. and Yamazaki, K. (1987) The genetics of body scent. Trends Genet. 3, 97–102.
Brennan, P., Kaba, H. and Keverne, E.B. (1990) Olfactory Recognition: a simple memory system. Science 250, 1223–1226.
Brennan, P. and Zufall, F. (2006) Pheromonal communication in vertebrates. Nature, in press.
Bruce, H. (1959) An exteroceptive block to pregnancy in the mouse. Nature 184, 105.
Carroll, L.S., Penn, D.J. and Potts, W.K. (2002) Discrimination of MHC-derived odors by untrained mice is consistent with divergence in peptide-binding region residues. Proc. Natl. Acad. Sci. USA 99, 2187–2192.
Hurst, J. and Beynon, R. (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26, 1288–1298.
Ishii, T., Hirota, J. and Mombaerts, P. (2003) Combinational coexpression of neural and immune multigene families in mouse vomeronasal sensory systems. Curr. Biol. 13, 394–400.
Jacob, S., McClintock, M.K., Zelano, B. and Ober, C. (2002) Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat. Genet. 30, 175–179.
Jordan, W.C. and Bruford, M.W. (1998) New perspectives on mate choice and the MHC. Heredity 81, 127–133.
Kelliher, K., Spehr, M., Li, X.-H., Zufall, F. and Leinders-Zufall, T. (2006) Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur. J. Neurosci. 23, 3385–3390.
Leinders-Zufall, T., Brennan, P., Widmayer, P., Chandramani, P.S., Maul-Pavicic, A., Jäger, M., Li, X.-H., Breer, H., Zufall, F. and Boehm, T. (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033–1037.
Lloyd-Thomas, A. and Keverne, E.B. (1982) Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience 7, 907–913.
Loconto, J., Papes, F., Chang, E., Stowers, L., Jones, E.P., Takada, T., Kumanovics, A., Fischer-Lindahl, K. and Dulac, C. (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class 1b molecules. Cell 112, 607–618.
Luo, M.M., Fee, M.S. and Katz, L.C. (2003) Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299, 1196–1201.
Ma, D., Allen, N.D., Van Bergen, Y.C.H., Jones, C.M.E., Baum, M.J., Keverne, E.B. and Brennan, P.A. (2002) Selective ablation of olfactory receptor neurons without functional impairment of vomeronasal receptor neurons in OMP-ntr transgenic mice. Eur. J. Neurosci. 16, 2317–2323.
Manning, C.J., Wakeland, E.K. and Potts, W.K. (1992) Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360, 581–583.
Martini, S., Silvotti, L., Shirazi, A., Ryba, J.P. and Tirindelli, R. (2001) Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. J. Neurosci. 21, 843–848.
Milinski, M., Griffiths, S., Wegner, K., Reusch, T., Haas-Assenbaum, A. and Boehm, T. (2005) Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc. Natl. Acad. Sci. USA 102, 4414–4418.
Olson, R., Huey-Tubman, K., Dulac, C. and Bjorkman, P. (2005) Structure of a pheromone receptor-associated MHC molecule with an open and empty groove. PLOS 3, e257.
Paulsson, K. (2004) Evolutionary and functional perspectives of the major histocompatibility complex class I antigen-processing machinery. Cell. Mol. Life Sci. 61, 2446–2460.
Penn, D. and Potts, W.K. (1998a) MHC-disassortative mating preferences reversed by cross-fostering. Proc. R. Soc. Lond. B 265, 1299–1306.
Penn, D. and Potts, W.K. (1998b) Untrained mice discriminate MHC-determined odors. Physiol. Behav. 63, 235–243.
Penn, D. and Potts, W.K.. (1998c) How do major histocompatibility complex genes influence odor and mating preferences? Adv. Immunol. 69, 411–436.
Porter, R.H., Balogh, R.D., Cernoch, J.M. and Franchi, C. (1986) Recognition of kin through characteristic body odors. Chem. Sens. 11, 389–395.
Potts, W.K., Manning, C.J. and Wakeland, E.K. (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352, 619–621.
Reusch, T., Häberli, M., Aeschlimann, P. and Milinski, M. (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414, 300–302.
Schaefer, M.L., Yamazaki, K., Osada, K., Restrepo, D. and Beauchamp, G.K. (2002) Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition, and behavior. J. Neurosci. 22, 9513–9521.
Singer, A.G., Beauchamp, G.K. and Yamazaki, K. (1997) Volatile signals of the major histocompatibility complex in male mouse urine. Proc. Natl. Acad. Sci. USA 94, 2210–2214.
Singh, P.B. (2001) Chemosensation and genetic individuality. Reproduction 121, 529–539.
Singh, P.B., Brown, R.E. and Roser, B. (1987) MHC antigens in urine as olfactory recognition cues. Nature 327, 161–164.
Spehr, M., Kelliher, K., Li, X.-H., Boehm, T., Leinders-Zufall, T. and Zufall, F. (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci 26, 1961–1970.
Wedekind, C. and Furi, S. (1997) Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc. R. Soc. Lond. B 264, 1471–1479.
Yamazaki, K., Beauchamp, G.K., Curran, M. and Boyse, E.A. (2000) Parent-progeny recognition as a function of MHC odotype identity. Proc. R. Soc. Lond. B 97, 10500–10502.
Yamazaki, K., Beauchamp, G.K., Kupniewski, D., Bard, J., Thomas, L. and Boyse E.A. (1988) Familial imprinting determines H-2 selective mating preferences. Science 240, 1331–1332.
Yamazaki, K., Beauchamp, G.K., Imai, Y., Bard, J., Phelan, S.P., Thomas, L. and Boyse, E.A. (1990) Odortypes determined by the major histocompatibility complex in germfree mice. Proc. Natl. Acad. Sci. 87, 8413–8416.
Yamazaki, K., Beauchamp, G.K., Wysocki, C.J., Bard, J., Thomas, L. and Boyse, E.A. (1983) Recognition of H-2 Types in relation to the blocking of pregnancy in mice. Science 221, 186–188.
Yamazaki, K., Yamaguchi, M., Baranoski, L., Bard, J., Boyse, E.A. and Thomas, L. (1979) Recognition among mice: Evidence from the use of a Y maze differentially scented by congenic mice of different major histocompatibility types. J. Exp. Med. 150, 755–760.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer Science+Business Media,LLC
About this paper
Cite this paper
Brennan, P.A. (2008). MHC-Associated Chemosignals and Individual Identity. In: Hurst, J.L., Beynon, R.J., Roberts, S.C., Wyatt, T.D. (eds) Chemical Signals in Vertebrates 11. Springer, New York, NY. https://doi.org/10.1007/978-0-387-73945-8_12
Download citation
DOI: https://doi.org/10.1007/978-0-387-73945-8_12
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-73944-1
Online ISBN: 978-0-387-73945-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)