The structure, stability and pheromone binding of the male mouse protein sex pheromone darcin

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Phelan, Marie M ^a   McLean, Lynn ^a   Armstrong, Stuart D ^a   Hurst, Jane L ^a   Beynon, Robert J ^a   Lian, Lu Yun ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DARCIN; MAJOR URINARY PROTEIN 11; PEPTIDES AND PROTEINS; SEX PHEROMONE; UNCLASSIFIED DRUG; DARCIN PROTEIN, MOUSE; LIGAND; PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HYDROPHOBICITY; MALE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CALORIMETRY; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN DENATURATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALORIMETRY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGANDS; MALE; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEX ATTRACTANTS; THERMODYNAMICS;

EID: 84911899355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108415     Document Type: Article

References (60)

1. Cavaggioni A, Mucignat-Caretta C (2000) Major urinary proteins, alpha2U-globulins and aphrodisin. Biochim Biophys Acta 1482: 218-228.
2. Parfentjev A, Perlzweig A (1932) Composition of Mouse Urine. J Biol Chem: 551-555.
3. Beynon R, Hurst J (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 32: 393-396.
4. Garratt M, Stockley P, Armstrong SD, Beynon RJ, Hurst JL (2011) The scent of senescence: sexual signalling and female preference in house mice. J Evol Biol 24: 2398-2409. doi:10.1111/j.1420-9101.2011.02367.x
5. Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, et al. (2011) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc Biol Sci 278: 1098-1106. doi:10.1098/rspb.2010.1818
6. Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26: 1288-1298. doi:10.1002/bies.20147
7. Stopková R, Stopka P, Janotová K, Jedelský PL (2007) Species-specific expression of major urinary proteins in the house mice (Mus musculus musculus and Mus musculus domesticus). J Chem Ecol 33: 861-869.
8. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, et al. (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450: 899-902. doi:10.1038/nature05997
9. Chamero P, Katsoulidou V, Hendrix P, Bufe B, Roberts R, et al. (2011) G protein G(alpha)o is essential for vomeronasal function and aggressive behavior in mice. Proc Natl Acad Sci U S A 108: 12898-12903. doi:10.1073/pnas.1107770108
10. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318: 1-14.
11. Robertson DHL, Beynon RJ, Evershed RP (1993) Extraction, characterization, and binding analysis of two pheromonally active ligands associated with major urinary protein of house mouse (Mus musculus). J Chem Ecol 19: 1405-1416. doi:10.1007/BF00984885
12. Bacchini A, Gaetani E, Cavaggioni A (1992) Pheromone binding proteins of the mouse, Mus musculus. Experientia 48: 419-421.
13. Novotny M V, Jemiolo B, Wiesler D, Ma W, Harvey S, et al. (1999) A unique urinary constituent, 6-hydroxy-6-methyl-3-heptanone, is a pheromone that accelerates puberty in female mice. Chem Biol 6: 377-383.
14. Kwak J, Grigsby CC, Rizki MM, Preti G, Köksal M, et al. (2012) Differential binding between volatile ligands and major urinary proteins due to genetic variation in mice. Physiol Behav 107: 112-120.
15. Vandenbergh JG (1967) Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 81: 345-349.
16. Bruce HM (1959) An exteroceptive block to pregnancy in the mouse. Nature 184: 105.
17. Hurst J, Robertson D, Tolladay U, Beynon R (1998) Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim Behav 55: 1289-1297.
18. Sharrow SD, Vaughn JL, Zídek L, Novotny MV, Stone MJ (2002) Pheromone binding by polymorphic mouse major urinary proteins. Protein Sci 11: 2247-2256. doi:10.1110/ps.0204202
19. Perez-Miller S, Zou Q, Novotny MV, Hurley TD (2010) High resolution X-ray structures of mouse major urinary protein nasal isoform in complex with pheromones. Protein Sci 19: 1469-1479. doi:10.1002/pro.426
20. Eppig JT, Blake JA, Bult CJ, Kadin JA, Richardson JE (2012) The Mouse Genome Database (MGD): comprehensive resource for genetics and genomics of the laboratory mouse. Nucleic Acids Res 40: D881-886. doi:10.1093/nar/gkr974
21. Mudge JM, Armstrong SD, McLaren K, Beynon RJ, Hurst JL, et al. (2008) Dynamic instability of the major urinary protein gene family revealed by genomic and phenotypic comparisons between C57 and 129 strain mice. Genome Biol 9: R91. doi:10.1186/gb-2008-9-5-r91
22. Logan DW, Marton TF, Stowers L (2008) Species specificity in major urinary proteins by parallel evolution. PLoS One 3: e3280. doi:10.1371/journal.pone.0003280
23. Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE, et al. (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414: 631-634. doi:10.1038/414631a
24. Beynon RJ, Veggerby C, Payne CE, Robertson DHL, Gaskell SJ, et al. (2002) Polymorphism in major urinary proteins: molecular heterogeneity in a wild mouse population. J Chem Ecol 28: 1429-1446.
25. Cheetham SA, Thom MD, Jury F, Ollier WER, Beynon RJ, et al. (2007) The genetic basis of individual-recognition signals in the mouse. Curr Biol 17: 1771-1777. doi:10.1016/j.cub.2007.10.007
26. Sherborne AL, Thom MD, Paterson S, Jury F, Ollier WER, et al. (2007) The genetic basis of inbreeding avoidance in house mice. Curr Biol 17: 2061-2066. doi:10.1016/j.cub.2007.10.041.
27. Marie AMRD, Veggerby C, Robertson DHL, Gaskell SJ, Hubbard SJ, et al. (2001) Effect of polymorphisms on ligand binding by mouse major urinary proteins. Protein Sci 10: 411-417. doi:10.1110/ps.31701
28. Armstrong SD, Robertson DHL, Cheetham SA, Hurst JL, Beynon RJ (2005) Structural and functional differences in isoforms of mouse major urinary proteins: a male-specific protein that preferentially binds a male pheromone. Biochem J 391: 343-350. doi:10.1042/BJ20050404
29. Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, et al. (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 8: 75. doi:10.1186/1741-7007-8-75
30. Roberts SA, Davidson AJ, McLean L, Beynon RJ, Hurst JL (2012) Pheromonal induction of spatial learning in mice. Science 338: 1462-1465. doi:10.1126/science.1225638
31. Shahan K, Denaro M, Gilmartin M, Shi Y, Derman E (1987) Expression of six mouse major urinary protein genes in the mammary, parotid, sublingual, submaxillary, and lachrymal glands and in the liver. Mol Cell Biol 7: 1947-1954.
32. Phelan MM, McLean L, Simpson DM, Hurst JL, Beynon RJ, et al. (2010) 1H, 15N and 13C resonance assignment of darcin, a mouse major urinary protein. Biomol NMR Assign 4: 239-241. doi:10.1007/s12104-010-9253-6
33. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, et al. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59: 687-696. doi:10.1002/prot.20449
34. Leopold MF, Urbauer JL, Wand AJ (1994) Resonance assignment strategies for the analysis of NMR spectra of proteins. Mol Biotechnol 2: 61-93. doi:10.1007/BF02789290
35. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR Structure Determination with Automated NOE Assignment Using the New Software CANDID and the Torsion Angle Dynamics Algorithm DYANA. J Mol Biol 319: 209-227. doi:10.1016/S0022-2836(02)00241-3
36. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302.
37. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
38. Doreleijers JF, Vranken WF, Schulte C, Markley JL, Ulrich EL, et al. (2012) NRG-CING: integrated validation reports of remediated experimental biomolecular NMR data and coordinates in wwPDB. Nucleic Acids Res 40: D519-524. doi:10.1093/nar/gkr1134
39. Frishman D, Argos P (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579. doi:10.1002/prot.340230412
40. Heinig M, Frishman D (2004) STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res 32: W500-502. doi:10.1093/nar/gkh429
41. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60: 2288-2294. doi:10.1107/S0907444904023716
42. Pei J, Grishin NV (2007) PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics 23: 802-808. doi:10.1093/bioinformatics/btm017
43. Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36: W30-34. doi:10.1093/nar/gkn322.
44. Shatsky M, Nussinov R, Wolfson HJ (2004) A method for simultaneous alignment of multiple protein structures. Proteins 56: 143-156. doi:10.1002/prot.10628
45. Berjanskii M V, Wishart DS (2005) A simple method to predict protein flexibility using secondary chemical shifts. J Am Chem Soc 127: 14970-14971. doi:10.1021/ja054842f
46. Binkowski TA, Naghibzadeh S, Liang J (2003) CASTp: Computed Atlas of Surface Topography of proteins. Nucleic Acids Res 31: 3352-3355.
47. Tina KG, Bhadra R, Srinivasan N (2007) PIC: Protein Interactions Calculator. Nucleic Acids Res 35: W473-476. doi:10.1093/nar/gkm423
48. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797. doi:10.1016/j.jmb.2007.05.022
49. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127-134.
50. Brechbühl J, Moine F, Klaey M, Nenniger-Tosato M, Hurni N, et al. (2013) Mouse alarm pheromone shares structural similarity with predator scents. Proc Natl Acad Sci U S A 110: 4762-4767. doi:10.1073/pnas.1214249110
51. Cheetham SA, Smith AL, Armstrong SD, Beynon RJ, Hurst JL (2009) Limited variation in the major urinary proteins of laboratory mice. Physiol Behav 96: 253-261. doi:10.1016/j.physbeh.2008.10.005
52. Bingham RJ, Findlay JBC, Hsieh S-Y, Kalverda AP, Kjellberg A, et al. (2004) Thermodynamics of binding of 2-methoxy-3-isopropylpyrazine and 2-methoxy-3-isobutylpyrazine to the major urinary protein. J Am Chem Soc 126: 1675-1681. doi:10.1021/ja038461i
53. Pertinhez TA, Ferrari E, Casali E, Patel JA, Spisni A, et al. (2009) The binding cavity of mouse major urinary protein is optimised for a variety of ligand binding modes. Biochem Biophys Res Commun 390: 1266-1271. doi:10.1016/j.bbrc.2009.10.133
54. Macek P, Novák P, Krízová H, Zídek L, Sklenár V (2006) Molecular dynamics study of major urinary protein-pheromone interactions: a structural model for ligand-induced flexibility increase. FEBS Lett 580: 682-684. doi:10.1016/j.febslet.2005.12.088
55. Barratt E, Bingham RJ, Warner DJ, Laughton CA, Phillips SEV, et al. (2005) Van der Waals interactions dominate ligand-protein association in a protein binding site occluded from solvent water. J Am Chem Soc 127: 11827-11834. doi:10.1021/ja0527525
56. Sharrow SD, Vaughn JL, Ídek LŠŽ, Novotny MV, Stone MJ (2002) Pheromone binding by polymorphic mouse major urinary proteins. Protein Sci 11: 2247-2256. doi:10.1110/ps.0204202.fects
57. Barratt E, Bronowska A, Vondrásek J, Cerný J, Bingham R, et al. (2006) Thermodynamic penalty arising from burial of a ligand polar group within a hydrophobic pocket of a protein receptor. J Mol Biol 362: 994-1003. doi:10.1016/j.jmb.2006.07.067
58. Syme NR, Dennis C, Phillips SEV, Homans SW (2007) Origin of heat capacity changes in a "nonclassical" hydrophobic interaction. Chembiochem 8: 1509-1511. doi:10.1002/cbic.200700281
59. Malham R, Johnstone S, Bingham RJ, Barratt E, Phillips SEV, et al. (2005) Strong solute-solute dispersive interactions in a protein-ligand complex. J Am Chem Soc 127: 17061-17067. doi:10.1021/ja055454g
60. Timm DE, Baker LJ, Mueller H, Zidek L, Novotny M V (2001) Structural basis of pheromone binding to mouse major urinary protein (MUP-I). Protein Sci 10: 997-1004. doi:10.1110/ps.52201