Extracts from salivary glands stimulate aggression and inositol-1, 4, 5-triphosphate (IP3) production in the vomeronasal organ of mice

Physiology and Behavior

Volumn 98, Issue 1-2, 2009, Pages 147-155

  Taha, Murtada ^a   McMillon, Ronald ^a   Napier, Audrey ^a   Wekesa, Kennedy S ^a  

^a ALABAMA STATE UNIVERSITY   (United States)

Author keywords

Aggression; Exocrine glands; IP3; Salivary glands; VNO

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE; PHEROMONE; PHOSPHOLIPASE C BETA;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONGENIC STRAIN; CONTROLLED STUDY; EXOCRINE GLAND; FEMALE; MALE; MOUSE; NONHUMAN; PAROTID GLAND; PRIORITY JOURNAL; SALIVARY GLAND; SEX DIFFERENCE; SUBMANDIBULAR GLAND; VOMERONASAL ORGAN;

AGGRESSION; ANIMALS; FEMALE; INOSITOL 1,4,5-TRISPHOSPHATE; LACTATION; MALE; MATERNAL BEHAVIOR; MEMBRANES; MICE; OVARIECTOMY; PAROTID GLAND; SALIVA; SALIVARY GLANDS; SECOND MESSENGER SYSTEMS; SUBMANDIBULAR GLAND; TISSUE EXTRACTS; VOMERONASAL ORGAN;

EID: 67649470410     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2009.05.006     Document Type: Article

References (57)

1. Rodriguez I. Remarkable diversity of mammalian pheromone receptor repertoires. Proc Natl Acad Sci U S A 102 19 (2005) 6639-6640
2. Castañeda M.L.A., Gomez M.M., Guzmán R.G., and Hudson R. Chemical communication in domestic animals. Vet Mex 38 1 (2007) 105-123
3. Brennan P.A., and Zufall F. Pheromonal communication in vertebrates. Nature 444 (2006) 308-315
4. Keverne K.B. The VNO organ. Science 286 5440 (1999) 716-720
5. Brennan P.A., and Keverne E.B. Something in the air? New insights into mammalian pheromones. Curr Biol 14 2 (2004) R81-R89
6. Thompson R.N., Napier A., and Wekesa K.S. Chemosensory cues from the lacrimal and preputial glands stimulate production of IP3 in the VNO organ and aggression in male mice. Physiol Behav 90 5 (2007) 797-802
7. Luo M., Fee M.S., and Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of Brann J.H. and D.A. Fadool, 2006 behaving mice. Science 299 5610 (2003) 1196-1201
8. Laukaitis C.M., Dlouhy S.R., Emes R.D., Ponting C.P., and Karn R.C. Diverse spatial, temporal, and sexual expression of recently duplicated androgen-binding protein genes in Mus musculus. BMC Evol Biol 5 (2005) 40
9. Wickliffe J.K., Lee V.H., Smith E., Tandler B., and Phillips C.J. Gene expression, cell localization, and evolution of rodent submandibular gland androgen-binding protein. Eur J Morphol 40 4 (2002) 257-260
10. Marchese S., Pes D., Scaloni A., Carbone V., and Pelosi P. Lipocalins of boar salivary glands binding odours and pheromones. Eur J Biochem 252 (1998) 563-568
11. Pelosi P. Odorant-binding proteins: structural aspects. Ann N Y Acad Sci 855 (1998) 281-293
12. Shahan K., Gilmartin M., and Derman E. Nucleotide sequences of liver, lachrymal, and submaxillary gland mouse major urinary protein mRNAs: mosaic structure and construction of panels of gene-specific synthetic oligonucleotide probes. Mol Cell Biol 7 5 (1987) 1938-1946
13. Brennan P.A., and Kendrick P.M. Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 361 1476 (2006) 2061-2078
14. Spinelli S., Vincent F., Pelosi P., Tegoni M., and Cambillau C. Boar salivary lipocalin. Three-dimensional X-ray structure and androstenol/androstenone docking simulations. Eur J Biochem 269 10 (2002) 2449-2456
15. Chemero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., et al. Identification of protein pheromones that promote aggressive behaviour. Nature 450 (2007) 899-902
16. Mucignat-Caretta C., Caretta A., and Cavaggioni A. Acceleration of puberty onset in female mice by male urinary proteins. J Physiol 15 486 (1995) 517-522
17. Morè L. Mouse MUPs trigger ovulation via the VNO organ. Chem Senses 31 5 (2006) 393-401
18. Denny P.C., Denny P.A., Chai Y., and Klauser D.K. DNA synthesis and development strategies with possible consequences on sexual dimorphism in adult mouse submandibular glands. Crit Rev Oral Biol Med 4 (1993) 511-516
19. Pinkstaff C.A. Salivary gland sexual dimorphism: a brief review. Eur J Morphol 36 (Suppl) (1998) 31-34
20. Campbell P.S., Ben-Aryeh H., and Swanson K.A. Differential distribution of an estrogen receptor in the submandibular and parotid salivary glands of female rats. Endocr Res 16 (1990) 333-345
21. Murai S., Saito H., Masuda Y., Itoh T., and Kawaguchi T. Sex-dependent differences in the concentrations of the principal neurotransmitters, noradrenaline and acetylcholine, in the three major salivary glands of mice. Arch Oral Biol 43 (1998) 9-14
22. Pellegrini A., Grieco M., Materazzi G., Gesi M., and Ricciardi M.P. Stress-induced morphohistochemical and functional changes in rat adrenal cortex, testis and major salivary glands. Histochem J 30 (1998) 695-701
23. Martel C., Rheaume E., Takahashi M., Trudel C., Couet J., Luu-The V., et al. Distribution of 17 beta-hydroxysteroid dehydrogenase gene expression and activity in rat and human tissues. J Steroid Biochem Mol Biol 41 (1992) 597-603
24. Treister N.S., Richards S.M., Lombardi M.J., Rowley P., Jensen R.V., and Sullivan D.A. Sex-related differences in gene expression in salivary glands of BALB/c mice. J Dent Res 84 2 (2005) 160-165
25. McKinney T.D., and Christian J.J. Effect of preputialectomy on fighting behavior in mice. Proc Soc Exp Biol Med 134 (1970) 291-293
26. Caldwell H.K., and Lepri J.J. Disruption of the fifth melanocortin receptor alters the urinary excretion of aggression-modifying pheromones in male house mice. Chem Senses 27 (2002) 91-94
27. Kimoto H., Haga S., Sato K., and Touhara K. Sex-specific peptides from exocrine glands stimulate mouse VNO sensory neurons. Nature 437 (2005) 898-901
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-275
29. Svare B., Betteridge C., Katz D., and Samuels O. Some situational and experiential determinants of maternal aggression in mice. Physiol Behav 26 (1981) 253-258
30. Maestripieri D. Maternal aggression and litter size in the female house mouse. Ethology 84 (1990) 27-34
31. Segovia S., and Guillamon A. Effects of sex steroids on the development of the VNO organ in the rat. Dev Brain Res 5 (1982) 209-212
32. Thompson R.N., Robertson B.K., Napier A., and Wekesa K.S. Sex-specific responses to urinary chemicals by the mouse VNO organ. Chem Senses 29 9 (2004) 749-754
33. Zufall F., Kelliher K.R., and Leinders-Zufall T. Pheromone detection by mammalian VNO neurons. Microsc Res Tech 58 (2002) 251-260
34. Holy T.E., Dulac D., and Mesiter M. Responses of VNO neurons to natural stimuli. Science 289 (2000) 1569-1572
35. Halem A.H., Baum M.J., and Cherry J.A. Sex differences and steroid modulation of pheromone-induced immediate early genes in the two zones of the mouse accessory olfactory system. J Neurosci 21 (2001) 2474-2480
36. Wickliffe J.K., Lee V.H., Smith E., Tandler B., and Philips C.J. Gene expression, cell localization, and evolution of rodent submandibular gland androgen-binding protein. Eur J Morphol 86 (2002) 8555-8559
37. Yamashita J., Hirata Y., and Hayashi S. Low intermale aggression associated with small submandibular and preputial glands in goldthioglucose-obese mice. Physiol Behav 52 1 (1992) 91-95
38. Talley H.M., Laukaitis C.M., and Karn R.C. Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies. Evolution Int J Org Evolution 55 3 (2001) 631-634
39. Bronson F.H., and Desjardins C. Aggressive behavior and seminal vesicle function in mice: differential sensitivity to androgen given neonatally. Endocrinology 85 (1969) 971-974
40. Edwards D.A. Neonatal administration of androstenedione, testosterone or testosterone propionate: effects on ovulation, sexual receptivity and aggressive behavior in female mice. Physiol Behav 4 (1969) 233-238
41. Lincoln G.A., Guiness F., and Short R.V. The reproductive cycle of the female red deer, Cervus elaphus L. J Reprod Fertil 27 3 (1971) 427-438
42. Gandelman R. Mice: postpartum aggression elicited by the presence of an intruder. Horm Behav 3 1 (1972) 23-28
43. Wolff J.O. Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus. Anim Behav 33 (1985) 117-123
44. Parmigiani S., Ferrari P.F., and Palanza P. An evolutionary approach to behavioral pharmacology: using drugs to understand proximate and ultimate mechanisms of different forms of aggression in mice. Neurosci Biobehav Rev 23 (1998) 143-153
45. Bradley G., Leypold C., Yu R., Leinders-Zufall T., Kim M.M., Zufall F., et al. Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci U S A 99 9 (2002) 6376-6381
46. Gammie S.C., and Nelson R.J. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J Neurosci 19 18 (1999) 8027-8035
47. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., et al. Deficient pheromone responses in mice lacking a cluster of VNO receptor genes. Nature 419 (2002) 70-74
48. Ogawa S., Nomura M., Choleris E., and Pfaff D.W. The role of estrogen receptors in the regulation of aggressive behaviors. In: Nelson R.J. (Ed). Biology of aggression (2005), Oxford University Press, New York 231-249
49. Mann M.A., Konen C., and Svare B. The role of progesterone in pregnancy-induced aggression in mice. Horm Behav 18 (1984) 140-160
50. Stern J.M., and McDonald C. Ovarian hormone-induced short-latency maternal behavior in OVX virgin Long-Evans rats. Horm Behav 23 (1989) 157-172
51. Bridges R.S. Biochemical basis of parental behavior in the rat. In: Rosenblatt J.S., and Snowden C.T. (Eds). Parental care: evolution, mechanisms, and adaptive significance (1996), Academic Press, San Diego 215-237
52. Bakker J., Baum M.J., and Slob A.K. Neonatal inhibition of brain estrogen synthesis alters adult neural fos response to mating and pheromonal stimulation in the male rat. Neuroscience 74 (1996) 251-260
53. Kelliher K.R., Chang Y.M., Wersinger S.R., and Baum M.J. Sex difference and testosterone modulation of pheromone-induced neuronal Fos in the ferret's main olfactory bulb and hypothalamus. Biol Reprod 59 (1998) 1454-1463
54. Halem H.D., Cherry J.A., and Baum M.J. VNO neuroepithelium and forebrain fos responses to male pheromones in male and female mice. J Neurobiol 39 (1999) 249-263
55. Kimoto H., Sato K., Nodari F., Haga S., Holy T.E., and Touhara K. Sex- and strain-specific expression and VNO activity of mouse ESP family peptides. Curr Biol 17 21 (2007) 1879-1884
56. Leinders-Zufall T., Brennan P., Widmayer P.S., Maul-Pavicic A., Jäger M., Li X.H., et al. MHC class I peptides as chemosensory signals in the VNO organ. Science 306 5698 (2004) 1033-1037
57. Brann J.H., and Fadool D.A. VNO sensory neurons from Sternotherus odoratus (stinkpot/musk turtle) respond to chemosignals via the phospholipase C system. J Exp Biol 209 (2006) 1914-1927