Vulnerability of the Fetal Primate Brain to Moderate Reduction in Maternal Global Nutrient Availability

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2011 Jan 22

PMID 21252306

Citations 63

Authors

Iwa Antonow-Schlorke

Matthias Schwab

Laura A Cox

Cun Li

Kristina Stuchlik

Otto W Witte

Peter W Nathanielsz

Thomas J McDonald

Affiliations

Soon will be listed here.

Abstract

Moderate maternal nutrient restriction during pregnancy occurs in both developing and developed countries. In addition to poverty, maternal dieting, teenage pregnancy, and uterine vascular problems in older mothers are causes of decreased fetal nutrition. We evaluated the impact of global 30% maternal nutrient reduction (MNR) on early fetal baboon brain maturation. MNR induced major cerebral developmental disturbances without fetal growth restriction or marked maternal weight reduction. Mechanisms evaluated included neurotrophic factor suppression, cell proliferation and cell death imbalance, impaired glial maturation and neuronal process formation, down-regulation of gene ontological pathways and related gene products, and up-regulated transcription of cerebral catabolism. Contrary to the known benefits from this degree of dietary reduction on life span, MNR in pregnancy compromises structural fetal cerebral development, potentially having an impact on brain function throughout life.

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References

Colman R, Anderson R, Johnson S, Kastman E, Kosmatka K, Beasley T . Caloric restriction delays disease onset and mortality in rhesus monkeys. Science. 2009; 325(5937):201-4. PMC: 2812811. DOI: 10.1126/science.1173635. View

OKusky J, Ye P, DErcole A . Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J Neurosci. 2000; 20(22):8435-42. PMC: 6773150. View

Cohen S, Greenberg M . Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol. 2008; 24:183-209. PMC: 2709812. DOI: 10.1146/annurev.cellbio.24.110707.175235. View

Richards M, Hardy R, Kuh D, Wadsworth M . Birth weight and cognitive function in the British 1946 birth cohort: longitudinal population based study. BMJ. 2001; 322(7280):199-203. PMC: 26584. DOI: 10.1136/bmj.322.7280.199. View

Niblock M, Brunso-Bechtold J, Riddle D . Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci. 2000; 20(11):4165-76. PMC: 6772633. View

DErcole A, Ye P . Expanding the mind: insulin-like growth factor I and brain development. Endocrinology. 2008; 149(12):5958-62. PMC: 2613055. DOI: 10.1210/en.2008-0920. View

Gibbons A . Solving the brain's energy crisis. Science. 1998; 280(5368):1345-7. DOI: 10.1126/science.280.5368.1345. View

Matte T, Bresnahan M, Begg M, Susser E . Influence of variation in birth weight within normal range and within sibships on IQ at age 7 years: cohort study. BMJ. 2001; 323(7308):310-4. PMC: 37317. DOI: 10.1136/bmj.323.7308.310. View

Baker P, Wheeler S, Sanders T, Thomas J, Hutchinson C, Clarke K . A prospective study of micronutrient status in adolescent pregnancy. Am J Clin Nutr. 2009; 89(4):1114-24. DOI: 10.3945/ajcn.2008.27097. View

10.

Crozier S, Robinson S, Godfrey K, Cooper C, Inskip H . Women's dietary patterns change little from before to during pregnancy. J Nutr. 2009; 139(10):1956-63. PMC: 3113465. DOI: 10.3945/jn.109.109579. View

11.

Beard J, Lincoln D, Donoghue D, Taylor D, Summerhayes R, Dunn T . Socioeconomic and maternal determinants of small-for-gestational age births: patterns of increasing disparity. Acta Obstet Gynecol Scand. 2009; 88(5):575-83. DOI: 10.1080/00016340902818170. View

12.

Walker S, Wachs T, Meeks Gardner J, Lozoff B, Wasserman G, Pollitt E . Child development: risk factors for adverse outcomes in developing countries. Lancet. 2007; 369(9556):145-57. DOI: 10.1016/S0140-6736(07)60076-2. View

13.

Garcion E, Faissner A, Ffrench-Constant C . Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development. 2001; 128(13):2485-96. DOI: 10.1242/dev.128.13.2485. View

14.

Nielsen J, Kulahin N, Walmod P . Extracellular protein interactions mediated by the neural cell adhesion molecule, NCAM: heterophilic interactions between NCAM and cell adhesion molecules, extracellular matrix proteins, and viruses. Adv Exp Med Biol. 2009; 663:23-53. DOI: 10.1007/978-1-4419-1170-4_2. View

15.

Olness K . Effects on brain development leading to cognitive impairment: a worldwide epidemic. J Dev Behav Pediatr. 2003; 24(2):120-30. DOI: 10.1097/00004703-200304000-00009. View

16.

CHEEK D, Holt A, London W, Ellenberg J, Hill D, Sever J . Nutritional studies in the pregnant rhesus monkey--the effect of protein-calorie or protein deprivation on growth of the fetal brain. Am J Clin Nutr. 1976; 29(10):1149-57. DOI: 10.1093/ajcn/29.10.1149. View

17.

Van Eldik L, Wainwright M . The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci. 2003; 21(3-4):97-108. View

18.

Neugebauer R, Hoek H, Susser E . Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. JAMA. 1999; 282(5):455-62. DOI: 10.1001/jama.282.5.455. View

19.

Jones F, Jones P . The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn. 2000; 218(2):235-59. DOI: 10.1002/(SICI)1097-0177(200006)218:2<235::AID-DVDY2>3.0.CO;2-G. View

20.

Schlabritz-Loutsevitch N, Moore C, Lopez-Alvarenga J, Dunn B, Dudley D, Hubbard G . The baboon model (Papio hamadryas) of fetal loss: maternal weight, age, reproductive history and pregnancy outcome. J Med Primatol. 2008; 37(6):337-45. PMC: 3016714. DOI: 10.1111/j.1600-0684.2008.00297.x. View