Postnatal growth velocity modulates alterations of proteins involved in metabolism and neuronal plasticity in neonatal hypothalamus in rats born with intrauterine growth restriction

Journal of Nutritional Biochemistry

Volumn 23, Issue 2, 2012, Pages 140-152

  Alexandre Gouabau, Marie Cécile F ^a   Bailly, Emilie ^a   Moyon, Thomas L ^a   Grit, Isabelle C ^a   Coupé, Bérengère ^a   Le Drean, Gwenola ^a   Rogniaux, Hélène J ^b   Parnet, Patricia ^a  

^a HÔTEL DIEU   (France)

^b INRA   (France)

Author keywords

Hypothalamus; Intrauterine growth restriction; Metabolism; Proteomics

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 3; ACYL COENZYME A THIOESTERASE I; ACYLTRANSFERASE; ALPHA SYNUCLEIN; AMINOACYLASE; APOLIPOPROTEIN A1; BRAIN PROTEIN; CHAPERONIN CONTAINING TCP1; CHLORIDE CHANNEL; CHLORIDE INTRACELLULAR CHANNEL 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; DIHYDROPYRIMIDINASE RELATED PROTEIN 5; EPIDERMAL FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN; INSULIN; KETONE BODY; LEPTIN; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PEROXIREDOXIN 3; PROTEIN 14 3 3; PROTEIN 14 3 3 EPSILON; PROTEIN 14 3 3 ZETA; PROTEOME; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; ENERGY METABOLISM; FEMALE; HORMONE BLOOD LEVEL; HYPOTHALAMUS; INSULIN BLOOD LEVEL; INTRACELLULAR SIGNALING; INTRAUTERINE GROWTH RETARDATION; KETOGENESIS; LIPID OXIDATION; LIPOGENESIS; MALE; MALNUTRITION; MATERNAL NUTRITION; NERVE CELL PLASTICITY; NONHUMAN; POSTNATAL DEVELOPMENT; POSTNATAL GROWTH; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN RESTRICTION; PROTEOMICS; RAT;

ANIMALS; ANIMALS, NEWBORN; BIRTH WEIGHT; DIET, PROTEIN-RESTRICTED; FEMALE; FETAL GROWTH RETARDATION; HYPOTHALAMUS; LACTATION; NEURONAL PLASTICITY; PREGNANCY; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; RATTUS;

EID: 84855479415     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.11.008     Document Type: Article

References (69)

1. Jones R.H., Ozanne S.E. Fetal programming of glucose-insulin metabolism. Mol Cell Endocrinol 2009, 297(1-2):4-9.
2. Hales C.N., Barker D.J. The thrifty phenotype hypothesis. Br Med Bull 2001, 60:5-20.
3. Tashima L., Nakata M., Anno K., Sugino N., Kato H. Prenatal influence of ischemia-hypoxia-induced intrauterine growth retardation on brain development and behavioral activity in rats. Biol Neonate 2001, 80(1):81-87.
4. Rolland-Cachera M.F. Rate of growth in early life: a predictor of later health?. Adv Exp Med Biol 2005, 569:35-39.
5. Stettler N., Stallings V.A., Troxel A.B., Zhao J., Schinnar R., Nelson S.E., et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation 2005, 111(15):1897-1903.
6. Cripps R.L., Archer Z.A., Mercer J.G., Ozanne S.E. Early life programming of energy balance. Biochem Soc Trans 2007, 35(Pt 5):1203-1204.
7. Ozanne S.E., Hales C.N. Lifespan: catch-up growth and obesity in male mice. Nature 2004, 427(6973):411-412.
8. Plagemann A., Harder T., Rake A., Melchior K., Rohde W., Dorner G. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 2000, 130(10):2582-2589.
9. Langley-Evans S.C., Sculley D.V. The association between birthweight and longevity in the rat is complex and modulated by maternal protein intake during fetal life. FEBS Lett 2006, 580(17):4150-4153.
10. Fountoulakis M., Hardmaier R., Schuller E., Lubec G. Differences in protein level between neonatal and adult brain. Electrophoresis 2000, 21(3):673-678.
11. Lubec G., Krapfenbauer K., Fountoulakis M. Proteomics in brain research: potentials and limitations. Prog Neurobiol 2003, 69(3):193-211.
12. Seefeldt I., Nebrich G., Romer I., Mao L., Klose J. Evaluation of 2-DE protein patterns from pre- and postnatal stages of the mouse brain. Proteomics 2006, 6(18):4932-4939.
13. Cheon M.S., Kim S.H., Fountoulakis M., Lubec G. Heart type fatty acid binding protein (H-FABP) is decreased in brains of patients with Down syndrome and Alzheimer's disease. J Neural Transm Suppl 2003, (67):225-234.
14. Butterfield D.A. Proteomics: a new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res 2004, 1000(1-2):1-7.
15. De Iuliis A., Grigoletto J., Recchia A., Giusti P., Arslan P. A proteomic approach in the study of an animal model of Parkinson's disease. Clin Chim Acta 2005, 357(2):202-209.
16. Deshane J., Chaves L., Sarikonda K.V., Isbell S., Wilson L., Kirk M., et al. Proteomics analysis of rat brain protein modulations by grape seed extract. J Agric Food Chem 2004, 52(26):7872-7883.
17. Bouret S.G., Simerly R.B. Developmental programming of hypothalamic feeding circuits. Clin Genet 2006, 70(4):295-301.
18. Morgane P.J., Mokler D.J., Galler J.R. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002, 26(4):471-483.
19. Fanca-Berthon P., Michel C., Pagniez A., Rival M., Van Seuningen I., Darmaun D., et al. Intrauterine growth restriction alters postnatal colonic barrier maturation in rats. Pediatr Res 2009, 66(1):47-52.
20. Coupe B., Amarger V., Grit I., Benani A., Parnet P. Nutritional programming affects hypothalamic organization and early response to leptin. Endocrinology 2010, 151(2):702-713.
21. Westermeier R., Marouga R. Protein detection methods in proteomics research. Biosci Rep 2005, 25(1-2):19-32.
22. Berth M., Moser F.M., Kolbe M., Bernhardt J. The state of the art in the analysis of two-dimensional gel electrophoresis images. Appl Microbiol Biotechnol 2007, 76(6):1223-1243.
23. Coupe B., Grit I., Darmaun D., Parnet P. The timing of ' catch-up growth' affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 2009, 297(3):R813-R824.
24. Coupe B., Dutriez-Casteloot I., Breton C., Lefevre F., Mairesse J., Dickes-Coopman A., et al. Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J Neuroendocrinol 2009, 21(1):40-48.
25. Grigor M.R., Allan J.E., Carrington J.M., Carne A., Geursen A., Young D., et al. Effect of dietary protein and food restriction on milk production and composition, maternal tissues and enzymes in lactating rats. J Nutr 1987, 117(7):1247-1258.
26. Shen Q., Xu H., Wei L.M., Chen J., Liu H.M., Guo W. A comparative proteomic study of nephrogenesis in intrauterine growth restriction. Pediatr Nephrol 2010, 25(6):1063-1072.
27. Wang J., Chen L., Li D., Yin Y., Wang X., Li P., et al. Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr 2008, 138(1):60-66.
28. Campostrini N., Areces L.B., Rappsilber J., Pietrogrande M.C., Dondi F., Pastorino F., et al. Spot overlapping in two-dimensional maps: a serious problem ignored for much too long. Proteomics 2005, 5(9):2385-2395.
29. Pawlyk A.C., Ferber M., Shah A., Pack A.I., Naidoo N. Proteomic analysis of the effects and interactions of sleep deprivation and aging in mouse cerebral cortex. J Neurochem 2007, 103(6):2301-2313.
30. Becker M., Nothwang H.G., Friauf E. Different protein profiles in inferior colliculus and cerebellum: a comparative proteomic study. Neuroscience 2008, 154(1):233-244.
31. Gupta P., Narang M., Banerjee B.D., Basu S. Oxidative stress in term small for gestational age neonates born to undernourished mothers: a case control study. BMC Pediatr 2004, 4:14.
32. Simmons R.A. Developmental origins of diabetes: the role of oxidative stress. Free Radic Biol Med 2006, 40(6):917-922.
33. Peterside I.E., Selak M.A., Simmons R.A. Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats. Am J Physiol Endocrinol Metab 2003, 285(6):E1258-E1266.
34. Selak M.A., Storey B.T., Peterside I., Simmons R.A. Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am J Physiol Endocrinol Metab 2003, 285(1):E130-E137.
35. Gallagher E.A., Newman J.P., Green L.R., Hanson M.A. The effect of low protein diet in pregnancy on the development of brain metabolism in rat offspring. J Physiol 2005, 568(Pt 2):553-558.
36. Wallace D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005, 39:359-407.
37. Schapira A.H. Mitochondrial disease. Lancet 2006, 368(9529):70-82.
38. Benani A., Troy S., Carmona M.C., Fioramonti X., Lorsignol A., Leloup C., et al. Role for mitochondrial reactive oxygen species in brain lipid sensing: redox regulation of food intake. Diabetes 2007, 56(1):152-160.
39. Sandoval D., Cota D., Seeley R.J. The integrative role of CNS fuel-sensing mechanisms in energy balance and glucose regulation. Annu Rev Physiol 2008, 70:513-535.
40. Kjarland E., Keen T.J., Kleppe R. Does isoform diversity explain functional differences in the 14-3-3 protein family?. Curr Pharm Biotechnol 2006, 7(3):217-223.
41. Kobayashi-Miura M., Shioji K., Hoshino Y., Masutani H., Nakamura H., Yodoi J. Oxygen sensing and redox signaling: the role of thioredoxin in embryonic development and cardiac diseases. Am J Physiol Heart Circ Physiol 2007, 292(5):H2040-50.
42. Das K.C. Thioredoxin system in premature and newborn biology. Antioxid Redox Signal 2004, 6(1):177-184.
43. Sarr O., Louveau I., Kalbe C., Metges C.C., Rehfeldt C., Gondret F. Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets. J Anim Sci 2010, 88(5):1626-1641.
44. Armstrong C.L., Hawkes R. Pattern formation in the cerebellar cortex. Biochem Cell Biol 2000, 78(5):551-562.
45. Balaban N., Goldman R. The association of glycosomal enzymes and microtubules: a physiological phenomenon or an experimental artifact?. Exp Cell Res 1990, 191(2):219-226.
46. Pellerin L., Bergersen L.H., Halestrap A.P., Pierre K. Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J Neurosci Res 2005, 79(1-2):55-64.
47. Wolfgang M.J., Lane M.D. The role of hypothalamic malonyl-CoA in energy homeostasis. J Biol Chem 2006, 281(49):37265-37269.
48. Nehlig A. Brain uptake and metabolism of ketone bodies in animal models. Prostaglandins Leukot Essent Fatty Acids 2004, 70(3):265-275.
49. Dierks-Ventling C., Cone A.L. Acetoacetyl-coenzyme A thiolase in brain, liver, and kidney during maturation of the rat. Science 1971, 172(981):380-382.
50. Morris A.A. Cerebral ketone body metabolism. J Inherit Metab Dis 2005, 28(2):109-121.
51. Alonso de la Torre S.R., Serrano M.A., Medina J.M. Carrier-mediated beta-D-hydroxybutyrate transport in brush-border membrane vesicles from rat placenta. Pediatr Res 1992, 32(3):317-323.
52. Guzman M., Blazquez C. Is there an astrocyte-neuron ketone body shuttle?. Trends Endocrinol Metab 2001, 12(4):169-173.
53. Tabernero A., Velasco A., Granda B., Lavado E.M., Medina J.M. Transcytosis of albumin in astrocytes activates the sterol regulatory element-binding protein-1, which promotes the synthesis of the neurotrophic factor oleic acid. J Biol Chem 2002, 277(6):4240-4246.
54. Bennett E., Stenvers K.L., Lund P.K., Popko B. Cloning and characterization of a cDNA encoding a novel fatty acid binding protein from rat brain. J Neurochem 1994, 63(5):1616-1624.
55. Owada Y. Fatty acid binding protein: localization and functional significance in the brain. Tohoku J Exp Med 2008, 214(3):213-220.
56. Maeda K., Uysal K.T., Makowski L., Gorgun C.Z., Atsumi G., Parker R.A., et al. Role of the fatty acid binding protein mal1 in obesity and insulin resistance. Diabetes 2003, 52(2):300-307.
57. Liu M., Shen L., Doi T., Woods S.C., Seeley R.J., Tso P. Neuropeptide Y and lipid increase apolipoprotein AIV gene expression in rat hypothalamus. Brain Res 2003, 971(2):232-238.
58. Narishima R., Yamasaki M., Hasegawa S., Fukui T. Genetic obesity affects neural ketone body utilization in the rat brain. Obesity (Silver Spring) 2009, 17(3):611-615.
59. Parimi P.S., Cripe-Mamie C., Kalhan S.C. Metabolic responses to protein restriction during pregnancy in rat and translation initiation factors in the mother and fetus. Pediatr Res 2004, 56(3):423-431.
60. Sadasivudu B., Swamy M. Possible occurrence of ornithine-omega-aminotransferase in GABAergic neurons. Neurochem Res 1984, 9(11):1593-1598.
61. Yu H., Iyer R.K., Kern R.M., Rodriguez W.I., Grody W.W., Cederbaum S.D. Expression of arginase isozymes in mouse brain. J Neurosci Res 2001, 66(3):406-422.
62. Shin J.H., Weitzdoerfer R., Fountoulakis M., Lubec G. Expression of cystathionine beta-synthase, pyridoxal kinase, and ES1 protein homolog (mitochondrial precursor) in fetal Down syndrome brain. Neurochem Int 2004, 45(1):73-79.
63. Ding Q., Vaynman S., Souda P., Whitelegge J.P., Gomez-Pinilla F. Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 2006, 24(5):1265-1276.
64. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327(5968):1000-1004.
65. Lavedan C. The synuclein family. Genome Res 1998, 8(9):871-880.
66. Yoo B.C., Fountoulakis M., Dierssen M., Lubec G. Expression patterns of chaperone proteins in cerebral cortex of the fetus with Down syndrome: dysregulation of T-complex protein 1. J Neural Transm Suppl 2001, (61):321-334.
67. Byk T., Ozon S., Sobel A. The Ulip family phosphoproteins-common and specific properties. Eur J Biochem 1998, 254(1):14-24.
68. Hotta A., Inatome R., Yuasa-Kawada J., Qin Q., Yamamura H., Yanagi S. Critical role of collapsin response mediator protein-associated molecule CRAM for filopodia and growth cone development in neurons. Mol Biol Cell 2005, 16(1):32-39.
69. Yanagi S. Role of CRAM (CRMP5) in growth cone development and semaphorin-mediated signaling. Seikagaku 2006, 78(4):291-300.