Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-15T11:19:45.855Z Has data issue: false hasContentIssue false

Prolactin, prolactin receptor and uncoupling proteins during fetal and neonatal development

Published online by Cambridge University Press:  05 March 2007

S. Pearce*
Affiliation:
Academic Division of Child Health, School of Human Development, University Hospital, Nottingham, NG7 2UH, UK
A. Mostyn
Affiliation:
Academic Division of Child Health, School of Human Development, University Hospital, Nottingham, NG7 2UH, UK
M. C. Alves-Guerra
Affiliation:
CEREMOD, 9 rue Jules Hetzel, 92190, Meudon, France
C. Pecqueur
Affiliation:
CEREMOD, 9 rue Jules Hetzel, 92190, Meudon, France
B. Miroux
Affiliation:
CEREMOD, 9 rue Jules Hetzel, 92190, Meudon, France
R. Webb
Affiliation:
Division of Agriculture and Horticulture, School ofBiosciences, University of Nottingham, Sutton Bonington Campus, Loughbrough, LEI2 5RD, UK
T. Stephenson
Affiliation:
Academic Division of Child Health, School of Human Development, University Hospital, Nottingham, NG7 2UH, UK
M. E. Symonds
Affiliation:
Academic Division of Child Health, School of Human Development, University Hospital, Nottingham, NG7 2UH, UK
*
*Corresponding author: Miss Sarah Pearce, fax +44 115 970 9382, [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Uncoupling proteins (UCP) 1 and 2 are members of the subfamily of inner mitochondrial membrane carriers. UCP1 is specific to brown adipose tissue (BAT), where it is responsible for the rapid production of heat at birth. In fetal sheep UCP1 is first detectable at approximately 900d of gestation; its abundance increases with gestational age and peaks at the time of birth. The mRNA and protein for both the long and short form of the prolactin (PRL) receptor (PRLR) are also highly abundant in BAT. Enhanced PRLR abundance in late gestation is associated with an increase in the abundance of UCP1. This relationship between PRLR and UCP is not only present in BAT. Similar findings are now reported in the pregnant ovine uterus, where PRLR abundance reaches a maximum just before that of UCP2. However, the role of PRLR in BAT remains undetermined. Rat studies have shown that PRL administration throughout pregnancy results in offspring with increased UCP1 at birth. Studies in newborn lambs have shown that administration of PRL (20mg/d) causes an acute response, increasing colonic temperature in the first hour by 1°. This increased colonic temperature is maintained for the first 240h of life, in conjunction with enhanced lipolysis. After 70d of treatment there is no difference in the abundance of UCP1 but an increase in UCP1 activity; this effect may be mediated by an increase in lipolysis. Taken together these findings suggest that PRL could be an important endocrine factor during pregnancy and early postnatal life.

Type
Micronutrient Group Symposium on ‘Micronutrient supplementation: when and why?’
Copyright
Copyright © The Nutrition Society 2003

References

Alexander, G (1978) Quantitative development of adipose tissue in foetal sheep. Australian Journal of Biological Science 31, 489503CrossRefGoogle ScholarPubMed
Arsenijevic, D, Onuma, H, Pecqueur, C, Raimbault, S, Manning, BS, Miroux, B, Couplan, E, Alves-Guerra, M-C, Goubern, M, Surwit, R, Bouillaud, F, Richard, D, Collins, S & Ricquier, D (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nature Genetics 26, 435439CrossRefGoogle ScholarPubMed
Bassett, JM, Curtis, N, Hanson, C & Weeding, CM (1989) Effects of altered photoperiod or maternal melatonin administration on plasma prolactin concentrations in fetal lambs. Journal of Endocrinology 122, 633643CrossRefGoogle ScholarPubMed
Ben-Jonathan, N, Mershon, JL, Allen, DL & Steinmetz, RW (1996) Extra pituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocrine Reviews 17, 639669Google Scholar
Bispham, J, Budge, H, Mostyn, A, Dandrea, J, Clarke, L, Keisler, D, Symonds, ME & Stephenson, T (2002) Ambient temperature, maternal dexamethasone, and postnatal ontogeny of leptin in the neonatal lamb. Pediatric Research 52, 8590CrossRefGoogle ScholarPubMed
Bispham, J, Heasman, L, Clarke, L, Ingleton, PM, Stephenson, T & Symonds, ME (1999) Effect of maternal dexamethasone treatment and ambient temperature on prolactin receptor abundance in brown adipose and hepatic tissue in the foetal and new-born lamb. Journal of Neuroendocrinology 11, 849856CrossRefGoogle Scholar
Bole-Feysot, C, Goffin, V, Edery, M, Binart, N & Kelly, PA (1998) Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in prolactin receptor knockout mice. Endocrine Reviews 19, 225268CrossRefGoogle Scholar
Budge, H, Bispham, J, Dandrea, J, Evans, E, Heasman, L, Ingleton, PM, Sullivan, C, Wilson, V, Stephenson, T & Symonds, ME (2000) Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781786CrossRefGoogle ScholarPubMed
Budge, H, Bryce, A, Owens, JA, Stephenson, T, Symonds, ME & McMillen, IC (2002a) Differential effects of nutrient restriction in late gestation and placental restriction throughout gestation on uncoupling protein 1 expression in fetal perinatal adipose tissue. Early Human Development 66, 43Google Scholar
Budge, H, Dandrea, J, Mostyn, A, Evens, Y, Watkins, R, Sullivan, C, Ingleton, P, Stephenson, T & Symonds, ME (2003) Differential effects of fetal number and maternal nutrition in late gestation on prolactin receptor abundance and adipose tissue development in the neonatal lamb. Pediatric Research 53, 302308CrossRefGoogle ScholarPubMed
Budge, H, Mostyn, A, Wilson, V, Khong, A, Walker, AM, Symonds, ME & Stephenson, T (2002b) The effect of maternal prolactin infusion during pregnancy on fetal adipose tissue development. Journal of Endocrinology 174, 427433CrossRefGoogle ScholarPubMed
Cannon, B, Connoley, E, Obregon, M-J & Nedergaard, J (1988) Perinatal activation of brown adipose tissue The Endocrine Control of the Fetus 306320 Kunzel W Jesen A Berlin Springer VerlagCrossRefGoogle Scholar
Cannon, B & Nedergaard, J (1985) The biochemistry of an inefficient tissue: brown adipose tissue. Essays in Biochemistry 20, 110164Google ScholarPubMed
Cassy, S, Charlier, M, Guillemot, M, Pessemesse, L & Dijane, J (1999) Cellular localization and evolution of prolactin receptor mRNA in ovine endometrium during pregnancy. FEES Letters 445, 207211CrossRefGoogle ScholarPubMed
Casteilla, L, Forest, C, Robelin, J, Ricquier, D, Lombet, A & Ailhaud, G (1987) Characterization of mitochondrial-uncoupling protein in bovine fetus and newborn calf. American Journal of Physiology 15, E627 – E636Google Scholar
Chan, E & Swaminathan, R (1990) Role of prolactin in lactation-induced changes in brown adipose tissue. American Journal of Physiology 27, R51 – R56Google Scholar
Clarke, L, Bryant, MJ, Lomax, MA & Symonds, ME (1997a) Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. British Journal of Nutrition 77, 871883CrossRefGoogle ScholarPubMed
Clarke, L, Buss, DS, Juniper, DT, Lomax, MA & Symonds, ME (1997b) Adipose tissue development during early postnatal life in ewe-reared lambs. Experimental Physiology 82, 10151027Google ScholarPubMed
Clarke, L, Heasman, L, Firth, K & Symonds, ME (1997c) Influence of route of delivery and ambient temperature on thermo-regulation in newborn lambs. American Journal of Physiology 272, R1931R1939Google Scholar
Ellacott, KLJ, Lawrence, CB, Rothwell, NJ & Luckman, SM (2002) PRL-releasing peptide interacts with leptin to reduce food intake and body weight. Endocrinology 143, 368374CrossRefGoogle ScholarPubMed
Fleury, C, Neverova, M, Collins, S, Raimbault, S, Champigny, O, Levi-Meyrueis, C, Bouillaud, F, Seldin, M, Surwit, R, Ricquier, D & Warden, C (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nature Genetics 15, 269272CrossRefGoogle ScholarPubMed
Fleury, C & Sanchis, D (1999) The mitochondrial uncoupling protein-2: current status. International Journal of Biochemistry and Cell Biology 31, 12611278CrossRefGoogle ScholarPubMed
Freemark, M (2001) Ontogenesis of prolactin receptors in the human fetus: roles in fetal development. Biochemical Society Transactions 29, 3841CrossRefGoogle ScholarPubMed
Gellersen, B, Bonhoff, A, Hunt, N & Bohnet, H (1991) Decidual-type prolactin expression by the human myometrium. Endocrinology 129, 158168CrossRefGoogle ScholarPubMed
Gemmel, RT, Bell, AW & Alexander, G (1972) Morphology of adipose cells in lambs at birth and during subsequent transition of brown to white adipose tissue in cold and warm conditions. American Journal of Anatomy 133, 143164CrossRefGoogle Scholar
Genever, E, Ingleton, PM, Mostyn, A, Pearce, S, Stephenson, T, Symonds, ME & Webb, R (2001) Effect of administration of prolactin on thermoregulation in neonatal lambs. Proceedings of the Physiological Society of New Zealand 20, P932Google Scholar
Gimeo, R, Dembski, M, Weng, X, Deng, N, Shyjan, A, Gimeno, C, Iris, F, Ellis, S, Woolf, E & Tartaglia, L (1997) Cloning and characterization of an uncoupling protein homolog: a potential molecular mediator of human thermogenesis. Diabetes 46, 900906CrossRefGoogle Scholar
Gluckman, PD, Grumbach, MM & Kaplan, SL (1981) The neuro-endocrine regulation and function of growth hormone and prolactin in the mammalian fetus. Endocrine Reviews 2, 363395CrossRefGoogle Scholar
Goffin, V, Binart, N, Clement-Lacroix, P, Bouchard, B, Bole-Feysot, C, Edery, M, Lucas, BK, Touraine, P, Pezet, A, Maaskant, R, Pichard, C, Helloco, C, Baran, N, Favre, H, Bernichtein, S, Allamando, A, Ormandy, C & Kelly, PA (1999) From the molecular biology of prolactin and its receptor to the lessons learned from knockout mice models. Genetic Analysis: Biomolecular Engineering 15, 189201CrossRefGoogle Scholar
Goffin, V, Binart, N, Touraine, P & Kelly, P (2002) Prolactin: The new biology of an old hormone. Annual Review of Physiology 64, 4767CrossRefGoogle ScholarPubMed
Gualillo, O, Lago, F, Garcia, M, Menendez, C, Senaris, R, Casanueva, FF & Dieguez, C (1999) Prolactin stimulates leptin secretion by rat white adipose tissue. Endocrinology 140, 51495153CrossRefGoogle ScholarPubMed
Heasman, L, Spencer, JAD & Symonds, ME (1997) Plasma prolactin concentrations after Caesarean section or vaginal delivery. Archives of Diseases in Childhood 77, 237238CrossRefGoogle ScholarPubMed
Klaus, S, Casteilla, L, Bouillaud, F & Ricquier, D (1991) The uncoupling protein UCP: a membraneous mitochondrial ion carrier exclusively expressed in brown adipose tissue. International Journal of Biochemistry 23, 791801CrossRefGoogle ScholarPubMed
Koritnik, DR, Humphrey, WD, Kaltenbach, CC & Dunn, TG (1981) Effects of maternal undernutrition on the development of the ovine fetus and the associated changes in growth hormone and prolactin. Biology of Reproduction 24, 125137CrossRefGoogle Scholar
Lean, M (1989) Brown adipose tissue in humans. Proceedings of the Nutrition Society 48, 243256CrossRefGoogle ScholarPubMed
Lowell, BB (1998) Adaptive thermogenesis: Turning on the heat. Current Biology 8, R517 – R520CrossRefGoogle ScholarPubMed
Lucas, A, Baker, BA & Cole, TJ (1990) Plasma prolactin and clinical outcome in preterm infants. Archives of Diseases in Childhood 65, 977983CrossRefGoogle ScholarPubMed
McMillen, IC, Jenkin, G, Thorburn, G & Robinson, J (1983) Concentrations of prolactin in the plasma of the fetal sheep and in amniotic fluid in late gestation and during dexamethasone induced parturition. Journal of Endocrinology 99, 107114CrossRefGoogle ScholarPubMed
Masaki, T, Yoshimata, H, Chiba, S, Kurokawa, M & Sakata, T (1999) Up-regulation of uterine UCP2 and UCP3 in pregnant rats. Biochimica et Biophysica Acta 1440, 8188CrossRefGoogle ScholarPubMed
Merei, J, Rao, A, Clarke, I & McMillen, I (1993) Proopiomelanocortin, prolactin and growth hormone messenger ribonucleic acid levels in the fetal sheep pituitary during late gestation. Acta Endocrinologica 129, 263267Google ScholarPubMed
Mostyn, A (2001) Endocrine regulation of adipose tissue thermogenesis in the fetal and neonatal sheep. PhD Thesis, Nottingham University.Google Scholar
Nedergaard, J & Cannon, B (1992) The uncoupling protein thermogenin and mitochondrial thermogenesis. New Comprehensive Biochemistry 23, 385419CrossRefGoogle Scholar
Nicholls, DG & Locke, RM (1983) Cellular mechanisms of heat dissipation In Mammalian Thermogenesis, 849 [Girardier, L and Stock, M. editors], New York: Chapman and HallCrossRefGoogle Scholar
Noble, RC, Steele, W & Moore, JH (1971) Diet and the fatty acids in the plasma of lambs during the first eight days after birth. Lipids 1, 2634CrossRefGoogle Scholar
Pearce, S, Alves-Guerra, M-C, Pecqueur, C, Miroux, B, Symonds, ME & Stephenson, T (2003) Ontogeny of prolactin receptor and uncoupling protein 2 in the pregnant uterus during mid to late gestation in sheep Early Human DevelopmentGoogle Scholar
Pearce, S, Dieguez, C, Symonds, ME & Stephenson, T (2001) The effect of chronic prolactin administration to growing rats on uncoupling protein (UCP)-1 abundance in intrascapular brown adipose tissue (BAT). Endocrine Abstracts 2, P54Google Scholar
Pearce, S, Genever, E, Mostyn, A, Webb, R, Ingleton, PM, Symonds, ME & Stephenson, T (2000) Effect of administration of prolactin on thermoregulation in neonatal lambs. Early Human Development 60, 4950Google Scholar
Phillips, ID, Anthony, RV, Houghton, DC & McMillen, IC (1999) The regulation of prolactin receptor messenger ribonucleic acid levels in the sheep liver before birth: relative roles of the fetal hypothalamus, cortisol, and external photoperiod. Endocrinology 140, 19661971CrossRefGoogle ScholarPubMed
Phillips, ID, Fielke, SI, Young, IR & McMillen, IC (1996) The relative roles of the hypothalamus and cortisol in the control of prolactin gene expression in the anterior pituitary of the sheep fetus. Journal of Neuroendocrinology 8, 929933CrossRefGoogle ScholarPubMed
Power, G (1989) Biology of temperature: the mammalian fetus. Journal of Developmental Physiology 12, 295304Google ScholarPubMed
Reese, J, Binart, N, Brown, N, Ma, W-G, Paria, BC, Das, SK, Kelly, PA & Dey, SK (2000) Implication and decidualization defects in prolactin receptor (PRLR)-deficient mice are mediated by ovarian but not uterine PRLR. Endocrinology 141, 18721881CrossRefGoogle Scholar
Ricquier, D & Bouillaud, F (2000a) Mitochondrial uncoupling proteins: from mitochondria to the regulation of energy balance. Journal of Physiology 529, 310CrossRefGoogle Scholar
Ricquier, D & Bouillaud, F (2000b) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochemical Journal 345, 161179CrossRefGoogle ScholarPubMed
Scarpace, P, Matheny, M, Pollock, B & Turner, N (1997) Leptin increases uncoupling protein expression and energy expenditure. American Journal of Physiology 273, E226E230Google ScholarPubMed
Schermer, S, Bird, JA, Lomax, MA, Shepherd, D & Symonds, ME (1996) Effect of fetal thyroidectomy on brown adipose tissue thermoregulation in newborn lambs. Reproduction, Fertility and Development 8, 9951002CrossRefGoogle ScholarPubMed
Sinha, YN (1995) Structural variants of prolactin: occurrence and physiological significance. Endocrine Reviews 16, 354369CrossRefGoogle ScholarPubMed
Stephenson, T, Budge, H, Mostyn, A, Pearce, S, Webb, R & Symonds, ME (2001) Fetal and neonatal adipose maturation: a primary site of cytokine and cytokine-receptor action. Biochemical Society Transactions 29, 8085CrossRefGoogle ScholarPubMed
Symonds, ME, Budge, H & Stephenson, T (2000) Limitations of models used to examine the influence of nutrition during pregnancy and adult disease. Archives of Diseases in Childhood 83, 215219CrossRefGoogle ScholarPubMed
Symonds, ME, Mostyn, A & Stephenson, T (2001) Cytokines and cytokine receptors in fetal growth and development. Biochemical Society Transactions 29, 3337CrossRefGoogle ScholarPubMed
Symonds, ME, Phillips, ID, Anthony, RV, Owens, JA & McMillen, IC (1998) Prolactin receptor gene expression and foetal adipose tissue. Journal of Neuroendocrinology 10, 885890CrossRefGoogle ScholarPubMed
Yang, L, Kuo, CB, Liu, Y, Coss, D, Xu, X, Chen, C, Oster-Granite, ML & Walker, AM (2001) Administration of unmodified prolactin (U-PRL) and a molecular mimic of phosphorylated prolactin (PP-PRL) during rat pregnancy provides evidence that the U-PRL:PP-PRL ratio is crucial to the normal development of pup tissue. Journal of Endocrinology 168, 227238CrossRefGoogle Scholar
Yang, L, Lii, S, Kuo, B, Buckley, A, Buckley, D, Chen, C, Xu, X, Coss, D & Walker, AM (2002) Maternal prolactin composition can permanently affect epidermal γδT cell function in the offspring. Developmental and Comparative Immunology 26, 849860CrossRefGoogle ScholarPubMed