Skip to main content
Erschienen in: European Journal of Nutrition 4/2016

14.07.2015 | Original Contribution

Methylating micronutrient supplementation during pregnancy influences foetal hepatic gene expression and IGF signalling and increases foetal weight

verfasst von: M. Oster, W. Nuchchanart, N. Trakooljul, E. Muráni, A. Zeyner, E. Wirthgen, A. Hoeflich, S. Ponsuksili, K. Wimmers

Erschienen in: European Journal of Nutrition | Ausgabe 4/2016

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Maternal diet during pregnancy impacts foetal growth and development. In particular, dietary levels of methylating micronutrients (methionine, folate, choline, vitamins B6, and B12) interfere with the availability and allocation of methyl groups for methylation reactions, thereby influencing normal transcription. However, the currently recommended methylating micronutrient supplementation regimen is haphazard and arbitrary at best.

Methods

To investigate the effects of a methylating micronutrient-rich maternal diet, pregnant Pietrain sows were fed either a standard diet (CON) or a diet supplemented with methionine, folate, choline, B6, B12, and zinc (MET). Foetal liver and muscle (M. longissimus dorsi) tissues were collected at 35, 63, and 91 days post-conception. Transcriptional responses to diet were assessed in foetal liver. Altered insulin-like growth factor (IGF) signalling in transcriptome analyses prompted investigation of IGF-2 and insulin-like growth factor binding proteins (IGFBPs) levels in muscle and liver.

Results

Maternal diet enriched with methylating micronutrients was associated with increased foetal weight in late gestation. Hepatic transcriptional patterns also revealed differences in vitamin B6 and folate metabolism between the two diets, suggesting that supplementation was effective. Additionally, shifts in growth-supporting metabolic routes of the lipid and energy metabolism, including IGF signalling, and of cell cycle-related pathways were found to occur in liver tissue in supplemented individuals. Weight differences and modulated IGF pathways were also reflected in the muscle content of IGF-2 (increased in MET) and IGFBP-2 (decreased in MET).

Conclusions

Maternal dietary challenges provoke stage-dependent and tissue-specific transcriptomic modulations in the liver pointing to molecular routes contributing to the organismal adaptation. Subtle effects on late foetal growth are associated with changes in the IGF signalling mainly in skeletal muscle tissue that is less resilient to dietary stimuli than liver.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Snoeck A, Remacle C, Reusens B, Hoet J (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57:107–118CrossRef Snoeck A, Remacle C, Reusens B, Hoet J (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57:107–118CrossRef
2.
Zurück zum Zitat Bertin E, Gangnerau M, Bellon G, Bailb D, Arbelot De Vacqueur A, Portha B (2002) Development of beta-cell mass in fetuses of rats deprived of protein and/or energy in last trimester of pregnancy. Am J Physiol Regul Integr Comp Physiol 283:R623–R630CrossRef Bertin E, Gangnerau M, Bellon G, Bailb D, Arbelot De Vacqueur A, Portha B (2002) Development of beta-cell mass in fetuses of rats deprived of protein and/or energy in last trimester of pregnancy. Am J Physiol Regul Integr Comp Physiol 283:R623–R630CrossRef
3.
Zurück zum Zitat Du M, Zhu M, Means W, Hess B, Ford S (2005) Nutrient restriction differentially modulates the mammalian target of rapamycin signalling and the ubiquitin-proteasome system in skeletal muscle of cows and their fetuses. J Anim Sci 83:117–123 Du M, Zhu M, Means W, Hess B, Ford S (2005) Nutrient restriction differentially modulates the mammalian target of rapamycin signalling and the ubiquitin-proteasome system in skeletal muscle of cows and their fetuses. J Anim Sci 83:117–123
4.
Zurück zum Zitat Hyatt M, Gardner D, Sebert S, Wilson V, Davidson N, Nigmatullina Y, Chan L, Budge H, Symonds M (2011) Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring. Reproduction 141:119–126CrossRef Hyatt M, Gardner D, Sebert S, Wilson V, Davidson N, Nigmatullina Y, Chan L, Budge H, Symonds M (2011) Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring. Reproduction 141:119–126CrossRef
5.
Zurück zum Zitat McMillen I, Robinson J (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633CrossRef McMillen I, Robinson J (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633CrossRef
6.
Zurück zum Zitat McMullen S, Langley-Evans S, Gambling L, Lang C, Swali A, McArdle H (2012) A common cause for a common phenotype: the gatekeeper hypothesis in fetal programming. Med Hypotheses 78:88–94CrossRef McMullen S, Langley-Evans S, Gambling L, Lang C, Swali A, McArdle H (2012) A common cause for a common phenotype: the gatekeeper hypothesis in fetal programming. Med Hypotheses 78:88–94CrossRef
7.
Zurück zum Zitat Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2014) High and low protein gestation diets do not provoke common transcriptional responses representing universal target-pathways in muscle and liver of porcine progeny. Acta Physiol (Oxf) 210:202–214CrossRef Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2014) High and low protein gestation diets do not provoke common transcriptional responses representing universal target-pathways in muscle and liver of porcine progeny. Acta Physiol (Oxf) 210:202–214CrossRef
8.
Zurück zum Zitat Burdge G, Lillycrop K, Phillips E, Slater-Jefferies J, Jackson A, Hanson M (2009) Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J Nutr 139:1054–1060CrossRef Burdge G, Lillycrop K, Phillips E, Slater-Jefferies J, Jackson A, Hanson M (2009) Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J Nutr 139:1054–1060CrossRef
9.
Zurück zum Zitat Sebert S, Sharkey D, Budge H, Symonds M (2011) The early programming of metabolic health: is epigenetic setting the missing link? Am J Clin Nutr 94:1953S–1958SCrossRef Sebert S, Sharkey D, Budge H, Symonds M (2011) The early programming of metabolic health: is epigenetic setting the missing link? Am J Clin Nutr 94:1953S–1958SCrossRef
10.
Zurück zum Zitat Maloney C, Hay S, Rees W (2007) Folate deficiency during pregnancy impacts on methyl metabolism without affecting global DNA methylation in the rat fetus. Br J Nutr 97:1090–1098CrossRef Maloney C, Hay S, Rees W (2007) Folate deficiency during pregnancy impacts on methyl metabolism without affecting global DNA methylation in the rat fetus. Br J Nutr 97:1090–1098CrossRef
11.
Zurück zum Zitat Lillycrop K, Phillips E, Jackson A, Hanson M, Burdge G (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382–1386 Lillycrop K, Phillips E, Jackson A, Hanson M, Burdge G (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382–1386
12.
Zurück zum Zitat Sie K, Li J, Ly A, Sohn KJ, Croxford R, Kim YI (2013) Effect of maternal and postweaning folic acid supplementation on global and gene-specific dna methylation in the liver of the rat offspring. Mol Nutr Food Res 57:677685CrossRef Sie K, Li J, Ly A, Sohn KJ, Croxford R, Kim YI (2013) Effect of maternal and postweaning folic acid supplementation on global and gene-specific dna methylation in the liver of the rat offspring. Mol Nutr Food Res 57:677685CrossRef
13.
Zurück zum Zitat Waterland R, Dolinoy D, Lin J, Smith C, Shi X et al (2006) Maternal methyl supplements increase offspring dna methylation at axin fused. Genesis 44:401–406CrossRef Waterland R, Dolinoy D, Lin J, Smith C, Shi X et al (2006) Maternal methyl supplements increase offspring dna methylation at axin fused. Genesis 44:401–406CrossRef
14.
Zurück zum Zitat Wolff G, Kodell R, Moore S, Cooney C (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in avy/a mice. FASEB J 12:949–957 Wolff G, Kodell R, Moore S, Cooney C (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in avy/a mice. FASEB J 12:949–957
15.
Zurück zum Zitat Varela-Moreiras G, Selhub J, da Costa K, Zeisel S (1992) Effect of chronic choline deficiency in rats on liver folate content and distribution. J Nutr Biochem 3:519–522CrossRef Varela-Moreiras G, Selhub J, da Costa K, Zeisel S (1992) Effect of chronic choline deficiency in rats on liver folate content and distribution. J Nutr Biochem 3:519–522CrossRef
16.
Zurück zum Zitat Jacob R, Jenden D, Allman-Farinelli M, Swendseid M (1999) Folate nutriture alters choline status of women and men fed low choline diets. J Nutr 129:712–717 Jacob R, Jenden D, Allman-Farinelli M, Swendseid M (1999) Folate nutriture alters choline status of women and men fed low choline diets. J Nutr 129:712–717
17.
Zurück zum Zitat Niculescu M, Zeisel S (2002) Diet, methyl donors and dna methylation: interactions between dietary folate, methionine and choline. J Nutr 132:2333S–2335S Niculescu M, Zeisel S (2002) Diet, methyl donors and dna methylation: interactions between dietary folate, methionine and choline. J Nutr 132:2333S–2335S
18.
Zurück zum Zitat Shaw G, Lammer E, Wasserman C, O’Malley C, Tolarova M (1995) Risks of orofacial clefts in children born to women using multivitamins containing folic acid periconceptionally. Lancet 346(8972):393–396CrossRef Shaw G, Lammer E, Wasserman C, O’Malley C, Tolarova M (1995) Risks of orofacial clefts in children born to women using multivitamins containing folic acid periconceptionally. Lancet 346(8972):393–396CrossRef
19.
Zurück zum Zitat Hoile S, Lillycrop K, Grenfell L, Hanson M, Burdge G (2012) Increasing the folic acid content of maternal or post-weaning diets induces differential changes in phosphoenolpyruvate carboxykinase mRNA expression and promoter methylation in rats. Br J Nutr 108:852–857CrossRef Hoile S, Lillycrop K, Grenfell L, Hanson M, Burdge G (2012) Increasing the folic acid content of maternal or post-weaning diets induces differential changes in phosphoenolpyruvate carboxykinase mRNA expression and promoter methylation in rats. Br J Nutr 108:852–857CrossRef
20.
Zurück zum Zitat Schaible T, Harris R, Dowd S, Smith C, Kellermayer R (2011) Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 20:1687–1696CrossRef Schaible T, Harris R, Dowd S, Smith C, Kellermayer R (2011) Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 20:1687–1696CrossRef
21.
Zurück zum Zitat Mikael L, Deng L, Paul L, Selhub J, Rozen R (2013) Moderately high intake of folic acid has a negative impact on mouse embryonic development. Birth Defects Res A Clin Mol Teratol 97:47–52CrossRef Mikael L, Deng L, Paul L, Selhub J, Rozen R (2013) Moderately high intake of folic acid has a negative impact on mouse embryonic development. Birth Defects Res A Clin Mol Teratol 97:47–52CrossRef
22.
Zurück zum Zitat Pickell L, Brown K, Li D, Wang X, Deng L, Wu Q, Selhub J, Luo L, Jerome-Majewska L, Rozen R (2011) High intake of folic acid disrupts embryonic development in mice. Birth Defects Res A Clin Mol Teratol 91:8–19CrossRef Pickell L, Brown K, Li D, Wang X, Deng L, Wu Q, Selhub J, Luo L, Jerome-Majewska L, Rozen R (2011) High intake of folic acid disrupts embryonic development in mice. Birth Defects Res A Clin Mol Teratol 91:8–19CrossRef
23.
Zurück zum Zitat Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R, Grenyer R, Price S, Vos R, Gittleman J, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512CrossRef Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R, Grenyer R, Price S, Vos R, Gittleman J, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512CrossRef
24.
Zurück zum Zitat Lunney J (2007) Advances in swine biomedical model genomics. Int J Biol Sci 3:179–184CrossRef Lunney J (2007) Advances in swine biomedical model genomics. Int J Biol Sci 3:179–184CrossRef
25.
Zurück zum Zitat Guilloteau P, Zabielski R, Hammon H, Metges C (2010) Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev 23:4–22CrossRef Guilloteau P, Zabielski R, Hammon H, Metges C (2010) Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev 23:4–22CrossRef
26.
Zurück zum Zitat Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2011) A high protein diet during pregnancy affects hepatic gene expression of energy sensing pathways along ontogenesis in a porcine model. PLoS One 6:e21691CrossRef Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2011) A high protein diet during pregnancy affects hepatic gene expression of energy sensing pathways along ontogenesis in a porcine model. PLoS One 6:e21691CrossRef
27.
Zurück zum Zitat Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2012) A low protein diet during pregnancy provokes a lasting shift of hepatic expression of genes related to cell cycle throughout ontogenesis in a porcine model. BMC Genomics 13:93CrossRef Oster M, Muráni E, Metges C, Ponsuksili S, Wimmers K (2012) A low protein diet during pregnancy provokes a lasting shift of hepatic expression of genes related to cell cycle throughout ontogenesis in a porcine model. BMC Genomics 13:93CrossRef
28.
Zurück zum Zitat Valle M, Guay F, Beaudry D, Matte J, Blouin R et al (2002) Effects of breed, parity, and folic acid supplement on the expression of folate metabolism genes in endometrial and embryonic tissues from sows in early pregnancy. Biol Reprod 67:1259–1267CrossRef Valle M, Guay F, Beaudry D, Matte J, Blouin R et al (2002) Effects of breed, parity, and folic acid supplement on the expression of folate metabolism genes in endometrial and embryonic tissues from sows in early pregnancy. Biol Reprod 67:1259–1267CrossRef
29.
Zurück zum Zitat Liu J, Chen D, Yu B, Mao X (2011) Effect of maternal folic acid supplementation on hepatic one-carbon unit associated gene expressions in newborn piglets. Mol Biol Rep 38:3849–3856CrossRef Liu J, Chen D, Yu B, Mao X (2011) Effect of maternal folic acid supplementation on hepatic one-carbon unit associated gene expressions in newborn piglets. Mol Biol Rep 38:3849–3856CrossRef
30.
Zurück zum Zitat Rucker RB (2007) Allometric scaling, metabolic body size and interspecies comparison of basal nutritional requirements. J Anim Physiol Anim Nutr 91:148–156CrossRef Rucker RB (2007) Allometric scaling, metabolic body size and interspecies comparison of basal nutritional requirements. J Anim Physiol Anim Nutr 91:148–156CrossRef
31.
Zurück zum Zitat Zeyner A, Harris P (2013) Vitamins. In: Geor R, Harris P, Coenen M (eds) Equine applied and clinical nutrition. Saunders Elsevier, Philadelphia, pp 168–189CrossRef Zeyner A, Harris P (2013) Vitamins. In: Geor R, Harris P, Coenen M (eds) Equine applied and clinical nutrition. Saunders Elsevier, Philadelphia, pp 168–189CrossRef
32.
Zurück zum Zitat AfBN (2014) Empfehlungen zur Energie- und Nährstoffversorgung von Pferden. DLG-Verlag, Frankfurt (Main) AfBN (2014) Empfehlungen zur Energie- und Nährstoffversorgung von Pferden. DLG-Verlag, Frankfurt (Main)
33.
Zurück zum Zitat AfBN (2005) Communications of the Committee for Requirement Standards of the Society of Nutrition Physiology: standardised precaecal digestibility of amino acids in feedstuffs for pigs—methods and concepts. Proc Soc Nutr Physiol 14:185–205 AfBN (2005) Communications of the Committee for Requirement Standards of the Society of Nutrition Physiology: standardised precaecal digestibility of amino acids in feedstuffs for pigs—methods and concepts. Proc Soc Nutr Physiol 14:185–205
34.
Zurück zum Zitat Deutsche Gesellschaft für Ernährung e.V. (DGE) (2013) Referenzwerte für die Nährstoffzufuhr. Umschau Braus GmbH Verlagsgesellschaft, Frankfurt (Main) Deutsche Gesellschaft für Ernährung e.V. (DGE) (2013) Referenzwerte für die Nährstoffzufuhr. Umschau Braus GmbH Verlagsgesellschaft, Frankfurt (Main)
35.
Zurück zum Zitat Reeves P, Nielsen F, Fahey G (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951 Reeves P, Nielsen F, Fahey G (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951
36.
Zurück zum Zitat AfBN (2006) Energie- und Nährstoffbedarf landwirtschaftlicher Nutztiere. 10: Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen. Ausschuss für Bedarfsnormen der Gesellschaft für Ernährungsphysiologie. DLG-Verlag, Frankfurt (Main) AfBN (2006) Energie- und Nährstoffbedarf landwirtschaftlicher Nutztiere. 10: Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen. Ausschuss für Bedarfsnormen der Gesellschaft für Ernährungsphysiologie. DLG-Verlag, Frankfurt (Main)
37.
Zurück zum Zitat Braunschweig M, Jagannathan V, Gutzwiller A, Bee G (2012) Investigations on transgenerational epigenetic response down the male line in f2 pigs. PLoS One 7:e30583CrossRef Braunschweig M, Jagannathan V, Gutzwiller A, Bee G (2012) Investigations on transgenerational epigenetic response down the male line in f2 pigs. PLoS One 7:e30583CrossRef
38.
Zurück zum Zitat Bruggmann R, Jagannathan V, Braunschweig M (2013) In search of epigenetic marks in testes and sperm cells of differentially fed boars. PLoS One 8:e78691CrossRef Bruggmann R, Jagannathan V, Braunschweig M (2013) In search of epigenetic marks in testes and sperm cells of differentially fed boars. PLoS One 8:e78691CrossRef
39.
Zurück zum Zitat Bielanska-Osuchowska Z, Krzynwek-Wojciechowska J (1990) Morphometric investigations of the pig developing liver during the prenatal period. Pol Arch Weter 30:7–16 Bielanska-Osuchowska Z, Krzynwek-Wojciechowska J (1990) Morphometric investigations of the pig developing liver during the prenatal period. Pol Arch Weter 30:7–16
40.
Zurück zum Zitat Bielanska-Osuchowska Z (1996) Ultrastructural and stereological studies of hepatocytes in prenatal development of swine. Folia Morphol (Warsz) 55:1–19 Bielanska-Osuchowska Z (1996) Ultrastructural and stereological studies of hepatocytes in prenatal development of swine. Folia Morphol (Warsz) 55:1–19
41.
Zurück zum Zitat Ponsuksili S, Muráni E, Walz C, Schwerin M, Wimmers K (2007) Pre- and postnatal hepatic gene expression profiles of two pig breeds differing in body composition: insight into pathways of metabolic regulation. Physiol Genomics 29:267–279CrossRef Ponsuksili S, Muráni E, Walz C, Schwerin M, Wimmers K (2007) Pre- and postnatal hepatic gene expression profiles of two pig breeds differing in body composition: insight into pathways of metabolic regulation. Physiol Genomics 29:267–279CrossRef
42.
Zurück zum Zitat Kauffmann A, Gentleman R, Huber W (2009) arrayqualitymetrics—a bioconductor package for quality assessment of microarray data. Bioinformatics 25:415–416CrossRef Kauffmann A, Gentleman R, Huber W (2009) arrayqualitymetrics—a bioconductor package for quality assessment of microarray data. Bioinformatics 25:415–416CrossRef
43.
Zurück zum Zitat Storey J, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445CrossRef Storey J, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445CrossRef
44.
Zurück zum Zitat Edgar R, Domrachev M, Lash A (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210CrossRef Edgar R, Domrachev M, Lash A (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210CrossRef
45.
Zurück zum Zitat Naraballobh W, Chomdej S, Muráni E, Wimmers K, Ponsuksili S (2010) Annotation and in silico localization of the affymetrix genechip porcine genome array. Arch Anim Breed 53:230–238 Naraballobh W, Chomdej S, Muráni E, Wimmers K, Ponsuksili S (2010) Annotation and in silico localization of the affymetrix genechip porcine genome array. Arch Anim Breed 53:230–238
46.
Zurück zum Zitat Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M (1986) Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 154:138–143CrossRef Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M (1986) Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 154:138–143CrossRef
47.
Zurück zum Zitat Laeger T, Wirthgen E, Piechotta M, Metzger F, Metges C, Kuhla B, Hoeflich A (2014) Effects of parturition and feed restriction on concentrations and distribution of the insulin-like growth factor-binding proteins in plasma and cerebrospinal fluid of dairy cows. J Dairy Sci 97:2876–2885CrossRef Laeger T, Wirthgen E, Piechotta M, Metzger F, Metges C, Kuhla B, Hoeflich A (2014) Effects of parturition and feed restriction on concentrations and distribution of the insulin-like growth factor-binding proteins in plasma and cerebrospinal fluid of dairy cows. J Dairy Sci 97:2876–2885CrossRef
48.
Zurück zum Zitat Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRef Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRef
49.
Zurück zum Zitat Ullrey D, Sprague J, Becker D, Miller E (1965) Growth of the swine fetus. J Anim Sci 24:711–717 Ullrey D, Sprague J, Becker D, Miller E (1965) Growth of the swine fetus. J Anim Sci 24:711–717
50.
Zurück zum Zitat Rehfeldt C, Lang I, Goers S, Hennig U, Kalbe C, Stabenow B, Bruessow K, Pfuhl R, Bellmann O, Nuernberg G, Otten W, Metges C (2011) Low and excess dietary protein levels during gestation affect growth and compositional traits in gilts and impair offspring fetal growth. J Anim Sci 89:329–341CrossRef Rehfeldt C, Lang I, Goers S, Hennig U, Kalbe C, Stabenow B, Bruessow K, Pfuhl R, Bellmann O, Nuernberg G, Otten W, Metges C (2011) Low and excess dietary protein levels during gestation affect growth and compositional traits in gilts and impair offspring fetal growth. J Anim Sci 89:329–341CrossRef
51.
Zurück zum Zitat Osgerby J, Wathes D, Howard D, Gadd T (2002) The effect of maternal undernutrition on ovine fetal growth. J Endocrinol 173:131–141CrossRef Osgerby J, Wathes D, Howard D, Gadd T (2002) The effect of maternal undernutrition on ovine fetal growth. J Endocrinol 173:131–141CrossRef
52.
Zurück zum Zitat Rees W, Hay S, Brown D, Antipatis C, Palmer R (2000) Maternal protein deficiency causes hypermethylation of dna in the livers of rat fetuses. J Nutr 130:1821–1826 Rees W, Hay S, Brown D, Antipatis C, Palmer R (2000) Maternal protein deficiency causes hypermethylation of dna in the livers of rat fetuses. J Nutr 130:1821–1826
53.
Zurück zum Zitat Rees W, Hay S, Cruickshank M (2006) An imbalance in the methionine content of the maternal diet reduces postnatal growth in the rat. Metabolism 55:763–770CrossRef Rees W, Hay S, Cruickshank M (2006) An imbalance in the methionine content of the maternal diet reduces postnatal growth in the rat. Metabolism 55:763–770CrossRef
54.
Zurück zum Zitat Maloney C, Hay S, Rees W (2009) The effects of feeding rats diets deficient in folic acid and related methyl donors on the blood pressure and glucose tolerance of the offspring. Br J Nutr 101:1333–1340CrossRef Maloney C, Hay S, Rees W (2009) The effects of feeding rats diets deficient in folic acid and related methyl donors on the blood pressure and glucose tolerance of the offspring. Br J Nutr 101:1333–1340CrossRef
55.
Zurück zum Zitat Roberfroid D, Huybregts L, Lanou H, Habicht J, Henry M, Meda N, Kolsteren P (2012) Prenatal micronutrient supplements cumulatively increase fetal growth. J Nutr 142:548–554CrossRef Roberfroid D, Huybregts L, Lanou H, Habicht J, Henry M, Meda N, Kolsteren P (2012) Prenatal micronutrient supplements cumulatively increase fetal growth. J Nutr 142:548–554CrossRef
56.
Zurück zum Zitat Fekete K, Berti C, Trovato M, Lohner S, Dullemeijer C, Souverein O, Cetin I, Decsi T (2012) Effect of folate intake on health outcomes in pregnancy: a systematic review and meta-analysis on birth weight, placental weight and length of gestation. Nutr J 11:75CrossRef Fekete K, Berti C, Trovato M, Lohner S, Dullemeijer C, Souverein O, Cetin I, Decsi T (2012) Effect of folate intake on health outcomes in pregnancy: a systematic review and meta-analysis on birth weight, placental weight and length of gestation. Nutr J 11:75CrossRef
57.
Zurück zum Zitat Hoeflich A, Bünger L, Nedbal S, Renne U, Elmlinger M, Blum W, Bruley C, Kolb H, Wolf E (2004) Growth selection in mice reveals conserved and redundant expression patterns of the insulin-like growth factor system. Gen Comp Endocrinol 136:248–259CrossRef Hoeflich A, Bünger L, Nedbal S, Renne U, Elmlinger M, Blum W, Bruley C, Kolb H, Wolf E (2004) Growth selection in mice reveals conserved and redundant expression patterns of the insulin-like growth factor system. Gen Comp Endocrinol 136:248–259CrossRef
58.
Zurück zum Zitat Kampman K, Ramsay T, White M (1993) Developmental changes in hepatic IGF-2 and IGFBP-2 mRNA levels in intrauterine growth-retarded and control swine. Comp Biochem Physiol B 104:415–421 Kampman K, Ramsay T, White M (1993) Developmental changes in hepatic IGF-2 and IGFBP-2 mRNA levels in intrauterine growth-retarded and control swine. Comp Biochem Physiol B 104:415–421
59.
Zurück zum Zitat Tilley R, McNeil C, Ashworth C, Page K, McArdle H (2007) Altered muscle development and expression of the insulin-like growth factor system in growth retarded fetal pigs. Domest Anim Endocrinol 32:167–177CrossRef Tilley R, McNeil C, Ashworth C, Page K, McArdle H (2007) Altered muscle development and expression of the insulin-like growth factor system in growth retarded fetal pigs. Domest Anim Endocrinol 32:167–177CrossRef
60.
Zurück zum Zitat Gay E, Seurin D, Babajko S, Doublier S, Cazillis M, Binoux M (1997) Liver-specific expression of human insulin-like growth factor binding protein-1 in transgenic mice: repercussions on reproduction, ante- and perinatal mortality and postnatal growth. Endocrinology 138:2937–2947 Gay E, Seurin D, Babajko S, Doublier S, Cazillis M, Binoux M (1997) Liver-specific expression of human insulin-like growth factor binding protein-1 in transgenic mice: repercussions on reproduction, ante- and perinatal mortality and postnatal growth. Endocrinology 138:2937–2947
61.
Zurück zum Zitat Hoeflich A, Wu M, Mohan S, Föll J, Wanke R, Froehlich T, Arnold G, Lahm H, Kolb H, Wolf E (1999) Overexpression of insulin-like growth factor-binding protein-2 in transgenic mice reduces postnatal body weight gain. Endocrinology 140:5488–5496CrossRef Hoeflich A, Wu M, Mohan S, Föll J, Wanke R, Froehlich T, Arnold G, Lahm H, Kolb H, Wolf E (1999) Overexpression of insulin-like growth factor-binding protein-2 in transgenic mice reduces postnatal body weight gain. Endocrinology 140:5488–5496CrossRef
62.
Zurück zum Zitat D’Ercole A, Dai Z, Xing Y, Boney C, Wilkie M, Lauder J, Han V, Clemmons D (1994) Brain growth retardation due to the expression of human insulin like growth factor binding protein-1 in transgenic mice: an in vivo model for the analysis of igf function in the brain. Brain Res Dev Brain Res 82:213–222CrossRef D’Ercole A, Dai Z, Xing Y, Boney C, Wilkie M, Lauder J, Han V, Clemmons D (1994) Brain growth retardation due to the expression of human insulin like growth factor binding protein-1 in transgenic mice: an in vivo model for the analysis of igf function in the brain. Brain Res Dev Brain Res 82:213–222CrossRef
63.
Zurück zum Zitat Hausman G, Campion D, Buonomo F (1991) Concentration of insulin-like growth factors (IGF-I and IGF-II) in tissues of developing lean and obese pig fetuses. Growth Dev Aging 55:43–52 Hausman G, Campion D, Buonomo F (1991) Concentration of insulin-like growth factors (IGF-I and IGF-II) in tissues of developing lean and obese pig fetuses. Growth Dev Aging 55:43–52
64.
Zurück zum Zitat Sohlström A, Katsman A, Kind K, Roberts C, Owens P, Robinson J, Owens J (1998) Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am J Physiol 274:E410–E416 Sohlström A, Katsman A, Kind K, Roberts C, Owens P, Robinson J, Owens J (1998) Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am J Physiol 274:E410–E416
65.
Zurück zum Zitat Donovan S, McNeil L, Jiménez-Flores R, Odle J (1994) Insulin-like growth factors and insulin-like growth factor binding proteins in porcine serum and milk throughout lactation. Pediatr Res 36:159–168CrossRef Donovan S, McNeil L, Jiménez-Flores R, Odle J (1994) Insulin-like growth factors and insulin-like growth factor binding proteins in porcine serum and milk throughout lactation. Pediatr Res 36:159–168CrossRef
66.
Zurück zum Zitat Peng M, Abribat T, Calvo E, LeBel D, Palin M, Bernatchez G, Morisset J, Pelletier G (1998) Ontogeny of insulin-like growth factors (IGF), IGF binding proteins, IGF receptors, and growth hormone receptor mRNA levels in porcine pancreas. J Anim Sci 76:1178–1188 Peng M, Abribat T, Calvo E, LeBel D, Palin M, Bernatchez G, Morisset J, Pelletier G (1998) Ontogeny of insulin-like growth factors (IGF), IGF binding proteins, IGF receptors, and growth hormone receptor mRNA levels in porcine pancreas. J Anim Sci 76:1178–1188
67.
Zurück zum Zitat Wyrwoll C, Kerrigan D, Holmes M, Seckl J, Drake A (2012) Altered placental methyl donor transport in the dexamethasone programmed rat. Placenta 33:220–223CrossRef Wyrwoll C, Kerrigan D, Holmes M, Seckl J, Drake A (2012) Altered placental methyl donor transport in the dexamethasone programmed rat. Placenta 33:220–223CrossRef
68.
Zurück zum Zitat Nijhout H, Reed M, Budu P, Ulrich C (2004) A mathematical model of the folate cycle: new insights into folate homeostasis. J Biol Chem 279:55008–55016CrossRef Nijhout H, Reed M, Budu P, Ulrich C (2004) A mathematical model of the folate cycle: new insights into folate homeostasis. J Biol Chem 279:55008–55016CrossRef
69.
Zurück zum Zitat McNeil C, Hay S, Rucklidge G, Reid M, Duncan G, Rees W (2009) Maternal diets deficient in folic acid and related methyl donors modify mechanisms associated with lipid metabolism in the fetal liver of the rat. Br J Nutr 102:1445–1452CrossRef McNeil C, Hay S, Rucklidge G, Reid M, Duncan G, Rees W (2009) Maternal diets deficient in folic acid and related methyl donors modify mechanisms associated with lipid metabolism in the fetal liver of the rat. Br J Nutr 102:1445–1452CrossRef
70.
Zurück zum Zitat Pooya S, Blaise S, Moreno Garcia M, Giudicelli J, Alberto J, Guéant-Rodriguez R, Jeannesson E, Gueguen N, Bressenot A, Nicolas B, Malthiery Y, Daval J, Peyrin-Biroulet L, Bronowicki J, Guéant J (2012) Methyl donor deficiency impairs fatty acid oxidation through pgc-1alpha hypomethylation and decreased er-alpha, err-alpha, and hnf-4alpha in the rat liver. J Hepatol 57:344–351CrossRef Pooya S, Blaise S, Moreno Garcia M, Giudicelli J, Alberto J, Guéant-Rodriguez R, Jeannesson E, Gueguen N, Bressenot A, Nicolas B, Malthiery Y, Daval J, Peyrin-Biroulet L, Bronowicki J, Guéant J (2012) Methyl donor deficiency impairs fatty acid oxidation through pgc-1alpha hypomethylation and decreased er-alpha, err-alpha, and hnf-4alpha in the rat liver. J Hepatol 57:344–351CrossRef
71.
Zurück zum Zitat Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K (2004) Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol 279:19–30CrossRef Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K (2004) Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol 279:19–30CrossRef
72.
Zurück zum Zitat Lillycrop K, Rodford J, Garratt E, Slater-Jefferies J, Godfrey K et al (2010) Maternal protein restriction with or without folic acid supplementation during pregnancy alters the hepatic transcriptome in adult male rats. Br J Nutr 103:1711–1719CrossRef Lillycrop K, Rodford J, Garratt E, Slater-Jefferies J, Godfrey K et al (2010) Maternal protein restriction with or without folic acid supplementation during pregnancy alters the hepatic transcriptome in adult male rats. Br J Nutr 103:1711–1719CrossRef
73.
Zurück zum Zitat Burdge G, Hoile S, Lillycrop K (2012) Epigenetics: are there implications for personalised nutrition? Curr Opin Clin Nutr Metab Care 15:442–447CrossRef Burdge G, Hoile S, Lillycrop K (2012) Epigenetics: are there implications for personalised nutrition? Curr Opin Clin Nutr Metab Care 15:442–447CrossRef
74.
Zurück zum Zitat Rees W, Wilson F, Maloney C (2006) Sulfur amino acid metabolism in pregnancy: the impact of methionine in the maternal diet. J Nutr 136:1701S–1705S Rees W, Wilson F, Maloney C (2006) Sulfur amino acid metabolism in pregnancy: the impact of methionine in the maternal diet. J Nutr 136:1701S–1705S
75.
Zurück zum Zitat Ciappio E, Mason J, Crott J (2011) Maternal one-carbon nutrient intake and cancer risk in offspring. Nutr Rev 69:561–571CrossRef Ciappio E, Mason J, Crott J (2011) Maternal one-carbon nutrient intake and cancer risk in offspring. Nutr Rev 69:561–571CrossRef
76.
Zurück zum Zitat Parker M, Rifas-Shiman SL, Oken E, Belfort MB, Jaddoe VW, Gillman MW (2012) Second trimester estimated fetal weight and fetal weight gain predict childhood obesity. J Pediatr 161:864–870CrossRef Parker M, Rifas-Shiman SL, Oken E, Belfort MB, Jaddoe VW, Gillman MW (2012) Second trimester estimated fetal weight and fetal weight gain predict childhood obesity. J Pediatr 161:864–870CrossRef
Metadaten
Titel
Methylating micronutrient supplementation during pregnancy influences foetal hepatic gene expression and IGF signalling and increases foetal weight
verfasst von
M. Oster
W. Nuchchanart
N. Trakooljul
E. Muráni
A. Zeyner
E. Wirthgen
A. Hoeflich
S. Ponsuksili
K. Wimmers
Publikationsdatum
14.07.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 4/2016
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0990-2

Weitere Artikel der Ausgabe 4/2016

European Journal of Nutrition 4/2016 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.