Lactation Biology Symposium: Lactocrine signaling and developmental programming

Authors: BARTOL, FRANK - Auburn University; WILEY, ANNE - Auburn University; MILLER, DORI - Auburn University; SILVA, ALEJANDRO - Auburn University; ROBERTS, KIMBERLY - Auburn University; DAVOLT, MEGHAN - Auburn University; CHEN, JOSEPH - Rutgers University; FRANKSHUN, AMY-LYNN - Rutgers University; CAMP, MEREDITH - Rutgers University; RAHMAN, KATHLEEN - Rutgers University; Vallet, Jeff; BAGNELL, CAROL - Rutgers University

Submitted to: Journal of Animal Science
Publication Type: Review Article
Publication Acceptance Date: 9/7/2012
Publication Date: 2/1/2013
Citation: Bartol, F.F., Wiley, A.A., Miller, D.J., Silva, A.J., Roberts, K.E., Davolt, M.L.P., Chen, J.C., Frankshun, A.-L., Camp, M.E., Rahman, K.M., Vallet, J.L., Bagnell, C.A. 2013. Lactation Biology Symposium: Lactocrine signaling and developmental programming. Journal of Animal Science. 91(2):696-705.

Interpretive Summary: Parents pass more than just genes to their offspring. In livestock, mothers also cause permanent changes in the development of offspring during both pregnancy and milk production, and the physiological mechanisms that cause these effects is beginning to be revealed. This paper reviews our current understanding of the effect of factors in milk that alter development in the offspring, which is referred to as lactocrine signaling. This process may allow a way for the mother to continue to influence the development of the offspring in response to environmental changes. Several experiments have shown that the development of the uterus in female offspring is influenced by factors in the first milk produced by the sow, called colostrum. Specifically, lack of colostrum caused delayed uterine gland development. Uterine glands are components of the uterus that have been shown to be required for optimal fertility in pigs. Results also indicated that inadequate acquisition of colostrum is associated with reduced fertility in pigs. Collectively, these results reinforce the importance of sufficient colostrum and milk during the neonatal period on the optimal development of female pigs for improved fertility.

Technical Abstract: Lactocrine signaling is defined as transmission of bioactive factors from mother to offspring as a consequence of nursing. Lactocrine transmission of signaling molecules may be an evolutionarily conserved process through which bioactive factors necessary for support of neonatal development are delivered postnatally. Dependence on maternal resources for development in eutherian mammals extends into neonatal life for at least that period of time when nutrition is obtained solely from first milk (i.e., colostrum). Data for the pig (Sus scrofa domesticus) provide evidence of lactocrine mediated effects on development of the female reproductive tract and other somatic tissues. Porcine uterine gland development, an estrogen receptor-alpha (ESR1)-dependent process, begins within 2 d of birth [postnatal day (PND) 0]. A lactocrine-driven, ESR1-mediated process was proposed as a regulatory mechanism governing onset of uterine gland development and endometrial maturation in the neonatal pig. Gilts maintained in a lactocrine-null state for 2 d from birth by milk-replacer feeding displayed altered patterns of endometrial gene expression and retarded uterine gland development by PND 14. In lactocrine-null gilts, inhibition of endometrial and cervical ESR1 and vascular endothelial growth factor (VEGFA) expression observed on PND 2 persisted to PND 14, even after gilts were returned to nursing on PND 2. Collectively, data support a role for lactocrine signaling in regulation of critical neonatal developmental events. Maternal lactocrine programming of postnatal development may help to insure healthy developmental outcomes. A systems biology approach will be required to define and understand mechanistic dynamics of lactocrine signaling events that may ultimately connect genotype to phenotype and establish the parameters of reproductive potential.