The alpha-fetoprotein knock-out mouse model suggests that parental behavior is sexually differentiated under the influence of prenatal estradiol.

Keller, Matthieu; Pawluski, Jodi; Brock, Olivier; Douhard, Quentin; Bakker, Julie

doi:10.1016/j.yhbeh.2010.01.013

Article (Scientific journals)

The alpha-fetoprotein knock-out mouse model suggests that parental behavior is sexually differentiated under the influence of prenatal estradiol.

Keller, Matthieu; Pawluski, Jodi; Brock, Olivier et al.

2010 • In Hormones and Behavior

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/70007

DOI
10.1016/j.yhbeh.2010.01.013

PubMed
20109458

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

KellerHB2010.pdf

Publisher postprint (440.76 kB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

hormones; brain; behavior

Abstract :

[en] In rodent species, sexual differentiation of the brain for many reproductive processes depends largely on estradiol. This was recently confirmed again by using the α-fetoprotein knockout (AFP-KO) mouse model, which lacks the protective actions of α-fetoprotein against maternal estradiol and as a result represents a good model to determine the contribution of prenatal estradiol to the sexual differentiation of the brain and behavior. In the present study, we determined whether parental responses are differentiated prenatally under the influence of estradiol. It was found that AFP-KO females showed longer latencies to retrieve pups to the nest and also exhibited lower levels of crouching over the pups in the nest in comparison to WT females. Thus our results suggest that prenatal estradiol defeminizes the parental brain in mice.

Research Center/Unit :

Giga-Neurosciences - ULiège

Disciplines :

Neurology
Endocrinology, metabolism & nutrition

Author, co-author :

Keller, Matthieu; INRA > UMR85 Physiologie de la Reproduction et des Comportements

Pawluski, Jodi ; Maastricht University (The Netherlands) > Faculty of Health, Medicine and Life Science > Department of Psychiatry and Neuropsychology

Brock, Olivier ; Université de Liège - ULiège > Doct. sc. (biol. orga. & écol. - Bologne)

Douhard, Quentin ; Université de Liège - ULiège > Génétique

Bakker, Julie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Language :

English

Title :

The alpha-fetoprotein knock-out mouse model suggests that parental behavior is sexually differentiated under the influence of prenatal estradiol.

Publication date :

2010

Journal title :

Hormones and Behavior

ISSN :

0018-506X

eISSN :

1095-6867

Publisher :

Academic Press, San Diego, United States - California

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

NICHD - National Institutes of Health. Eunice Kennedy Shriver National Institute of Child Health and Human Development

Available on ORBi :

since 23 August 2010

Statistics

Number of views

98 (8 by ULiège)

Number of downloads

252 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Bakker J., Baum M.J. Role for estradiol in female-typical brain and behavior sexual differentiation. Front. Neuroendocrinol. 2008, 29:1-16.
Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat. Neurosci. 2006, 9:220-226.
Bakker J., De Mees C., Szpirer J., Szpirer C., Balthazart J. Exposure to oestrogen prenatally does not interfere with the normal female-typical development of odour preferences. J. Neuroendocrinol. 2007, 19:329-334.
Baum M.J. Sexual differentiation of pheromone processing: links to male-typical mating behavior and partner preference. Horm. Behav. 2009, 55:579-588.
Beilharz R.G. The aggressive response of male mice (Mus musculus L) to a variety of stimulus animals. Z. Tierpsychol. 1975, 39:141-149.
Bridges R.S., Zarrow M.X., Denenberg V.H. The role of neonatal androgen in the expression of hormonally induced maternal responsiveness in the adult rat. Horm. Behav. 1973, 4:315-322.
Brown J.R., Ye H., Bronson R.T., Dikkes P., Greenberg M.E. A defect in nurturing in mice lacking the immediate early gene FosB. Cell 1996, 86:297-309.
Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci. 2005, 21:513-521.
Dalla C., Antoniou K., Papadopoulou-Daifoti Z., Balthazart J., Bakker J. Male aromatase-knockout mice exhibit normal levels of activity, anxiety and "depressive-like" symptomatology. Behav. Brain Res. 2005, 163:186-193.
Davis P.G., Gandelman R. Pup-killing produced by administration of testosterone propionate to adult female mice. Horm. Behav. 1972, 3:169-173.
Dickinson C., Keverne E.B. Importance of noradrenergic mechanisms in the olfactory bulbs for the maternal behaviour of mice. Physiol. Behav. 1988, 43:313-316.
Elwood R. Ethical implications of studies on infanticide and maternal aggression in rodents. Anim. Behav. 1991, 42:841-849.
Ennaceur A., Meliani I. A new one-trial test for neurobiological studies of memory in rats: III. Spatial vs. non-spatial working memory. Behav. Brain Res. 1992, 51:83-92.
Fleming A.S., Rosenblatt J.S. Olfactory regulation of maternal behavior in rats: I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J. Comp. Physiol. Psychol. 1974, 86:221-232.
Fleming A.S., Rosenblatt J.S. Olfactory regulation of maternal behavior in rats: II. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. J. Comp. Physiol. Psychol. 1974, 86:233-246.
Fleming A.S., Vaccarino F., Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 1980, 25:731-743.
Gabant P., Forrester L., Nichols J., Van Reeth T., De Mees C., Pajack B., Watt A., Smitz J., Alexandre H., Szpirer C., Szpirer J. Alpha-fetoprotein, the major fetal serum protein, is not essential for embryonic development but is required for female fertility. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12865-12870.
Gandelman R. Induction of pup killing in female mice by androgenization. Physiol. Behav. 1972, 9:101-102.
Gandelman R. The development of cannibalism in male Rockland-Swiss mice and the influence of olfactory bulb removal. Dev. Psychobiol. 1973, 6:159-164.
Gandelman R. The ontogeny of maternal responsiveness in female Rockland-Swiss albino mice. Horm. Behav. 1973, 4:257-268.
Gandelman R., Vom Saal F.S. Pup-killing in mice: the effects of gonadectomy and testosterone administration. Physiol. Behav. 1975, 15:647-651.
Gandelman R., Zarrow M.X., Denenberg V.H. Maternal behavior: differences between mother and virgin mice as a function of the testing procedure. Dev. Psychobiol. 1970, 3:207-214.
Gandelman R., Zarrow M.X., Denenberg V.H. Stimulus control of cannibalism and maternal behavior in anosmic mice. Physiol. Behav. 1971, 7:583-586.
Gandelman R., Zarrow M.X., Denenberg V.H., Myers M. Olfactory bulb removal eliminates maternal behavior in the mouse. Science 1971, 171:210-211.
Hines M., Allen L.S., Gorski R.A. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res. 1992, 579:321-326.
Ichikawa S., Fujii Y. Effect of prenatal androgen treatment on maternal behavior in the female rat. Horm. Behav. 1982, 16:224-233.
Insel T.R., Gelhard R., Shapiro L.E. The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 1991, 43:623-630.
Juarez J., Del Rio-Portilla I., Corsi-Cabrera M. Effects of prenatal testosterone on sex and age differences in behavior elicited by stimulus pups in the rat. Dev. Psychobiol. 1998, 32:121-129.
Keller M., Baum M.J., Brock O., Brennan P.A., Bakker J. Both main and accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav. Brain Res. 2009, 200:268-276.
Keller M., Douhard Q., Baum M.J., Bakker J. Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses 2006, 31:315-323.
Keller M., Douhard Q., Baum M.J., Bakker J. Sexual experience does not compensate for the disruptive effects of zinc sulfate-lesioning of the main olfactory epithelium on sexual behavior in male mice. Chem. Senses 2006, 31:753-762.
Leboucher G. Maternal behavior in normal and androgenized female rats: effect of age and experience. Physiol. Behav. 1989, 45:313-319.
Lévy F., Keller M. Olfactory mediation of maternal behavior in selected mammalian species. Behav. Brain Res. 2009, 200:336-345.
Lévy F., Keller M., Poindron P. Olfactory regulation of maternal behavior in mammals. Horm. Behav. 2004, 46:284-302.
Lonstein J.S., De Vries G.J. Influence of gonadal hormones in the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behav. Brain Res. 2000, 114:79-87.
Lonstein J., De Vries G.J. Sex differences in the parental behavior of rodents. Neurosci. Biobehav. Rev. 2000, 24:669-686.
McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
Noirot E. Changes in responsiveness to young in the adult mouse: II. The effect of external stimuli. J. Comp. Physiol. Psychol. 1964, 57:97-99.
Palanza P., Howdeshell K.L., Parmigliani S., Vom Saal F. Exposure to bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect. 2002, 110:415-422.
Perrigo G., Bryant W.C., vom Saal F.S. Fetal, hormonal, and experiential factors influencing the mating-induced regulation of infanticide in male house mice. Physiol. Behav. 1989, 46:121-128.
Pierman S., Balthazart J., Douhard Q., Baum M.J., Bakker J. Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice. Horm. Behav. 2006, 49:96-104.
Pierman S., Douhard Q., Bakker J. Evidence for a role of early oestrogens in the central processing of sexually relevant olfactory cues in female mice. Eur. J. Neurosci. 2008, 27:423-431.
Quadagno J.M., McCullough J., Ho G.K.-H., Spevak A.M. Neonatal gonadal hormones: effect on maternal and sexual behavior in the female rat. Physiol. Behav. 1973, 11:251-254.
Quadagno J.M., DeBold J.F., Gorzalka B.B., Whalen R.E. Maternal behavior in the rat: aspects of concaveation and neonatal androgen treatment. Physiol. Behav. 1974, 12:1071-1074.
Rosenberg K.M., Denenberg V.H., Zarrow M.X., Frank B.L. Effects of neonatal castration and testosterone on the rat's pup-killing behavior and activity. Physiol. Behav. 1971, 7:363-368.
Rosenblatt J.S. Nonhormonal basis of maternal behavior in the rat. Science 1967, 156:1512-1514.
Rosenson L.M. Responses of virgin mice, and of maternal females, to normal and caesarian-section delivered pups. J. Comp. Physiol. Psychol. 1975, 88:670-677.
Seegal R.F., Denenberg V.H. Maternal experience prevents pup killing in mice induced by peripheral anosmia. Physiol. Behav. 1974, 13:339-341.
Segovia S., Guillamon A. Sexual dimorphisms in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev. 1993, 18:51-74.
Siegel S. Nonparametric Statistics for the Behavioral Sciences. Series in Psychology 1956, McGraw-Hill, New York, ISBN 07-057348-4.
Svare B. Steroidal influences on pup-killing behavior in mice. Horm. Behav. 1979, 13:153-164.
Svare B., Mann M. Infanticide: genetic, developmental and hormonal influences in mice. Physiol. Behav. 1981, 27:921-927.
Svare B., Bartke A., Gandelman R. Individual differences in the maternal behavior of male mice: no evidence for a relationship to circulating testosterone levels. Horm. Behav. 1977, 8:326-372.
Svare B., Bartke A., Macrides F. Juvenile male mice: an attempt to accelerate testis function by exposure to adult female stimuli. Physiol. Behav. 1978, 21:1009-1013.
Svare B., Broida J. Genotypic influences on infanticide in mice: environmental, situational and experiential determinants. Physiol. Behav. 1982, 28:171-175.
Svare B., Kinsley C.H., Mann M.A., Broida J. Infanticide: accounting for genetic variation in mice. Physiol. Behav. 1984, 33:137-152.
Swann J, Fiber J.M. Sex differences in function of a pheromonally stimulated pathway: role of steroids and the main olfactory system. Brain Res. Bull. 1997, 44:409-413.
Vom Saal F.S. Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol. Behav. 1985, 34:7-15.
Vom Saal F.S., Howard L.S. The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 1982, 215:1270-1272.
Weber E.M., Olsson A.S. Maternal behavior in Mus musculus sp.: an ethological review. Appl. Anim. Behav. Sci. 2008, 114:1-22.
Wesson D., Keller M., Douhard Q., Baum M.J., Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm. Behav. 2006, 49:580-586.