Maternal prolactin during late pregnancy is important in generating nurturing behavior in the offspring

被引:22
|
作者
Sairenji, Taku James [1 ]
Ikezawa, Jun [1 ,8 ]
Kaneko, Ryosuke [2 ]
Masuda, Shinnosuke [1 ]
Uchida, Kaoru [3 ]
Takanashi, Yurie [1 ]
Masuda, Hiroko [1 ]
Sairenji, Tomoko [4 ]
Amano, Izuki [1 ]
Takatsuru, Yusuke [1 ]
Sayama, Kazutoshi [5 ]
Haglund, Kaisa [6 ]
Dikic, Ivan [7 ]
Koibuchi, Noriyuki [1 ]
Shimokawa, Noriaki [1 ,3 ]
机构
[1] Gunma Univ, Grad Sch Med, Dept Integrat Physiol, Gunma 3718511, Japan
[2] Gunma Univ, Grad Sch Med, Bioresource Ctr, Gunma 3718511, Japan
[3] Takasaki Univ Hlth & Welf, Dept Nutr, Gunma 3700033, Japan
[4] Univ Washington, Sch Med, Dept Family Med, Seattle, WA 98195 USA
[5] Shizuoka Univ, Grad Sch Agr, Lab Anim Physiol & Biochem, Shizuoka 4228529, Japan
[6] Univ Oslo, Fac Med, Dept Biochem, N-0379 Oslo, Norway
[7] Goethe Univ, Sch Med, Inst Biochem 2, D-60590 Frankfurt, Germany
[8] Yokohama City Univ, Grad Sch Med, Dept Neurol & Stroke Med, Yokohama, Kanagawa 2360004, Japan
关键词
nurturing behavior; neglect; prenatal environment; prolactin; fetal brain; PRENATAL STRESS; RECEPTOR GENE; MOUSE-BRAIN; DOPAMINE; MICE; EXPRESSION; RATS; NEUROGENESIS; STIMULATION; ANXIETY;
D O I
10.1073/pnas.1621196114
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Although maternal nurturing behavior is extremely important for the preservation of a species, our knowledge of the biological underpinnings of these behaviors is insufficient. Here we show that the degree of a mother's nurturing behavior is regulated by factors present during her own fetal development. We found that Cin85-deficient (Cin85(-/-)) mother mice had reduced pituitary hormone prolactin (PRL) secretion as a result of excessive dopamine signaling in the brain. Their offspring matured normally and produced their own pups; however, nurturing behaviors such as pup retrieval and nursing were strongly inhibited. Surprisingly, when WT embryos were transplanted into the fallopian tubes of Cin85(-/-) mice, they also exhibited inhibited nurturing behavior as adults. Conversely, when Cin85(-/-) embryos were transplanted into the fallopian tubes of WT mice, the resultant pups exhibited normal nurturing behaviors as adults. When PRL was administered to Cin85(-/-) mice during late pregnancy, a higher proportion of the resultant pups exhibited nurturing behaviors as adults. This correlates with our findings that neural circuitry associated with nurturing behaviors was less active in pups born to Cin85(-/-) mothers, but PRL administration to mothers restored neural activity to normal levels. These results suggest that the prenatal period is extremely important in determining the expression of nurturing behaviors in the subsequent generation, and that maternal PRL is one of the critical factors for expression. In conclusion, perinatally secreted maternal PRL affects the expression of nurturing behaviors not only in a mother, but also in her pups when they have reached adulthood.
引用
收藏
页码:13042 / 13047
页数:6
相关论文
共 50 条
  • [1] Maternal prolactin levels during late pregnancy and nurturing behavior of offspring in mice
    Masuda, Shinnosuke
    Ee, Oh Kwan
    Sairenji, Taku James
    Sato, Seika
    Yajima, Hiroyuki
    Amano, Izuki
    Koibuchi, Noriyuki
    Shimokawa, Noriaki
    [J]. DEVELOPMENTAL PSYCHOBIOLOGY, 2022, 64 (03)
  • [2] Maternal smoking during late pregnancy and offspring smoking behaviour
    Munafo, M. R.
    Wileyto, E. P.
    Murphy, M. F. G.
    Collins, B. N.
    [J]. ADDICTIVE BEHAVIORS, 2006, 31 (09) : 1670 - 1682
  • [4] Maternal smoking during pregnancy and severe antisocial behavior in offspring: A review
    Wakschlag, LS
    Pickett, KE
    Cook, E
    Benowitz, NL
    Leventhal, BL
    [J]. AMERICAN JOURNAL OF PUBLIC HEALTH, 2002, 92 (06) : 966 - 974
  • [5] Effects of maternal smoking during pregnancy on offspring blood pressure in late adolescence
    Hogberg, Lovisa
    Cnattingius, Sven
    Lundholm, Cecilia
    D'Onofrio, Brian M.
    Langstrom, Niklas
    Iliadou, Anastasia N.
    [J]. JOURNAL OF HYPERTENSION, 2012, 30 (04) : 693 - 699
  • [6] Maternal folate levels during pregnancy and offspring brain development in late childhood
    Zou, Runyu
    El Marroun, Hanan
    Cecil, Charlotte
    Jaddoe, Vincent W. V.
    Hillegers, Manon
    Tiemeier, Henning
    White, Tonya
    [J]. CLINICAL NUTRITION, 2021, 40 (05) : 3391 - 3400
  • [7] Maternal immune suppression during pregnancy does not prevent abnormal behavior in offspring
    Griffin, Ashley
    Bowles, Teylor
    Solis, Lucia
    Railey, Teryn
    Beauti, Samer
    Robinson, Reanna
    Spencer, Shauna-Kay
    Shaffery, James P.
    Wallace, Kedra
    [J]. BIOLOGY OF SEX DIFFERENCES, 2024, 15 (01)
  • [8] Maternal immune suppression during pregnancy does not prevent abnormal behavior in offspring
    Ashley Griffin
    Teylor Bowles
    Lucia Solis
    Teryn Railey
    Samer Beauti
    Reanna Robinson
    Shauna-Kay Spencer
    James P Shaffery
    Kedra Wallace
    [J]. Biology of Sex Differences, 15
  • [9] EFFECTS OF MATERNAL STRESS DURING PREGNANCY ON FORCED SWIMMING TEST BEHAVIOR OF THE OFFSPRING
    ALONSO, SJ
    AREVALO, R
    AFONSO, D
    RODRIGUEZ, M
    [J]. PHYSIOLOGY & BEHAVIOR, 1991, 50 (03) : 511 - 517
  • [10] Maternal smoking during pregnancy and offspring behavior II: a propensity score approach
    Knopik, Valerie
    Bidwell, Cinnamon
    Palmer, Rohan
    Brick, Leslie
    Madden, Pamela
    Heath, Andrew
    [J]. BEHAVIOR GENETICS, 2016, 46 (06) : 790 - 791