Pre- and/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats

Behavioural Brain Research

Volumn 227, Issue 2, 2012, Pages 324-329

  Reyes Castro, L A ^a   Rodriguez, J S ^b   Rodriguez Gonzalez G L ^a   Chavira, R ^a   Bautista, C J ^a   McDonald, T J ^b   Nathanielsz, P W ^b   Zambrano, E ^a  

^a INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Anxiety; Emotional reactivity; Locomotion; Protein restriction; Stress

Indexed keywords

CASEIN; CORTICOSTERONE;

AFFECT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR; CONTROLLED STUDY; FEMALE; IMMOBILIZATION; LACTATION; MALE; MATERNAL NUTRITION; MAZE TEST; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; RAT; RISK ASSESSMENT;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; BEHAVIOR, ANIMAL; DIET, PROTEIN-RESTRICTED; EXPLORATORY BEHAVIOR; FEMALE; MALE; MOTOR ACTIVITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

EID: 84855964576     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.06.008     Document Type: Article

References (64)

1. Warner M.J., Ozanne S.E. Mechanisms involved in the developmental programming of adulthood disease. Biochem J 2010, 427(3):333-347.
2. Morgane P.J., Austin-LaFrance R., Bronzino J., Tonkiss J., Díaz-Cintra S., Cintra L., et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev 1993, 17(1):91-128.
3. Morgane P., Galler J., Mokler D. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol 2005, 75(2):143-160.
4. Lister J., Blatt G., DeBassio W., Kemper T., Tonkiss J., Galler J., et al. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus 2005, 15(3):393-403.
5. Morgane P., Mokler D., Galler J. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002, 26(4):471-483.
6. Rosene D., Lister J., Schwagerl A., Tonkiss J., McCormick C., Galler J. Prenatal protein malnutrition in rats alters the c-Fos response of neurons in the anterior cingulate and medial prefrontal region to behavioral stress. Nutr Neurosci 2004, 7(5-6):281-289.
7. Lister J., Tonkiss J., Blatt G., Kemper T., DeBassio W., Galler J., et al. Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus 2006, 16(11):946-958.
8. Bedi K. Nutritional effects on neuron numbers. Nutr Neurosci 2003, 6(3):141-152.
9. Galler J.R., Ramsey F., Solimano G., Lowell W.E., Mason E. The influence of early malnutrition on subsequent behavioral development. I. Degree of impairment in intellectual performance. J Am Acad Child Psychiatry 1983, 22(1):8-15.
10. Galler J.R., Ramsey F., Solimano G. The influence of early malnutrition on subsequent behavioral development III. Learning disabilities as a sequel to malnutrition. Pediatr Res 1984, 18(4):309-313.
11. Galler J.R., Ramsey F., Solimano G., Kucharski L.T., Harrison R. The influence of early malnutrition on subsequent behavioral development. IV. Soft neurologic signs. Pediatr Res 1984, 18(9):826-832.
12. Galler J.R., Ramsey F., Solimano G. A follow-up study of the effects of early malnutrition on subsequent development. II. Fine motor skills in adolescence. Pediatr Res 1985, 19(6):524-527.
13. Galler J.R., Ramsey F.C., Forde V., Salt P., Archer E. Long-term effects of early kwashiorkor compared with marasmus. II. Intellectual performance. J Pediatr Gastroenterol Nutr 1987, 6(6):847-854.
14. Galler J.R., Ramsey F.C., Salt P., Archer E. Long-term effects of early kwashiorkor compared with marasmus. III. Fine motor skills. J Pediatr Gastroenterol Nutr 1987, 6(6):855-859.
15. Galler J.R., Ramsey F.C., Morley D.S., Archer E., Salt P. The long-term effects of early kwashiorkor compared with marasmus. IV. Performance on the national high school entrance examination. Pediatr Res 1990, 28(3):235-239.
16. Stein A.D., Pierik F.H., Verrips G.H.W., Susser E.S., Lumey L.H. Maternal exposure to the Dutch famine before conception and during pregnancy: quality of life and depressive symptoms in adult offspring. Epidemiology 2009, 20(6):909-915.
17. Coupe B., Dutriez-Casteloot I., Breton C., Lefevre F., Mairesse J., Vickes-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.
18. da Silva Hernandes A., Françolin-Silva A.L., Valadares C.T., Fukuda M.T.H., Almeida S.S. Effects of different malnutrition techniques on the behavior of rats tested in the elevated T-maze. Behav Brain Res 2005, 162(2):240-245.
19. Almeida S.S., de Oliveira L.M., Graeff F.G. Early life protein malnutrition changes exploration of the elevated plus-maze and reactivity to anxiolytics. Psychopharmacology (Berl) 1991, 103(4):513-518.
20. Almeida S.S., Garcia R.A., de Oliveira L.M. Effects of early protein malnutrition and repeated testing upon locomotor and exploratory behaviors in the elevated plus-maze. Physiol Behav 1993, 54(4):749-752.
21. Almeida S., Tonkiss J., Galler J. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav 1996, 60(2):675-680.
22. Watkins A., Wilkins A., Cunningham C., Perry V., Seet M., Osmond C., et al. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol 2008, 586(8):2231-2244.
23. Trzctnska M., Tonkiss J., Galler J. Influence of prenatal protein malnutrition on behavioral reactivity to stress in adult rats. Stress 1999, 3(1):71-83.
24. Gallo P.V. Physiological and behavioral consequences of maternal and post-weaning protein restriction. Physiol Behav 1981, 26(1):77-84.
25. Wiener S.G., Robinson L., Levine S. Influence of perinatal malnutrition on adult physiological and behavioral reactivity in rats. Physiol Behav 1983, 30(1):41-50.
26. Nolan L.A., Hart E.J., Windle R.J., Wood S.A., Hu X.W., Levi A.J., et al. Lack of effect of protein deprivation-induced intrauterine growth retardation on behavior and corticosterone and growth hormone secretion in adult male rats: a long-term follow-up study. Endocrinology 2001, 142(7):2996-3005.
27. Levay E., Paolini A., Govic A., Hazi A., Penman J., Kent S. Anxiety-like behaviour in adult rats perinatally exposed to maternal calorie restriction. Behav Brain Res 2008, 191(2):164-172.
28. Kursmark M., Weitzman M. Recent findings concerning childhood food insecurity. Curr Opin Clin Nutr Metab Care 2009, 12(3):310-316.
29. Zambrano E., Rodriguez-Gonzalez G., Guzman C., Garcia-Becerra R., Boeck L., Diaz L., et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol 2005, 563(Pt 1):275-284.
30. Zambrano E., Martinez-Samayoa P., Bautista C., Deas M., Guillen L., Rodriguez-Gonzalez G., et al. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol 2005, 566(Pt 1):225-236.
31. Zambrano E., Bautista C., Deas M., Martinez-Samayoa P., Gonzalez-Zamorano M., Ledesma H., et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol 2006, 571(Pt 1):221-230.
32. Graham S., Gandelman R. The expression of ano-genital distance data in the mouse. Physiol Behav 1986, 36(1):103-104.
33. Guzman C., Cabrera R., Cardenas M., Larrea F., Nathanielsz P., Zambrano E. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol 2006, 572(Pt 1):97-108.
34. Reyes-Castro L.A., Rodriguez J.S., Rodríguez-González G.L., Wimmer R.D., McDonald T.J., Larrea F., et al. Pre- and/or postnatal protein restriction in rats impairs learning and motivation in male offspring. Int J Dev Neurosci 2010, 29(2):177-182.
35. Bautista C., Boeck L., Larrea F., Nathanielsz P., Zambrano E. Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res 2008, 63(4):358-363.
36. Langley-Evans S. Critical differences between two low protein diet protocols in the programming of hypertension in the rat. Int J Food Sci Nutr 2000, 51(1):11-17.
37. Langley S.C., Jackson A.A. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci 1994, 86(2):217-222. [discussion 121].
38. Vickers M.H., Reddy S., Ikenasio B.A., Breier B.H. Dysregulation of the adipoinsular axis-a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming. J Endocrinol 2001, 170(2):323-332.
39. Holemans K., Gerber R., Meurrens K., De C.F., Poston L., Van Assche F. Maternal food restriction in the second half of pregnancy affects vascular function but not blood pressure of rat female offspring. Br J Nutr 1999, 81(1):73-79.
40. Galler J., Tonkiss J. Prenatal protein malnutrition and maternal behavior in Sprague-Dawley rats. J Nutr 1991, 121(5):762-769.
41. Langley S.C., Browne R.F., Jackson A.A. Altered glucose tolerance in rats exposed to maternal low protein diets in utero. Comp Biochem Physiol Physiol 1994, 109(2):223-229.
42. Langley-Evans S., Gardner D., Jackson A. Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J Reprod Fertil 1996, 106(2):307-312.
43. Vuguin P.M. Animal models for small for gestational age and fetal programming of adult disease. Horm Res 2007, 68(3):113-123.
44. Hotchkiss A.K., Lambright C.S., Ostby J.S., Parks-Saldutti L., Vandenbergh J.G., Gray L.E. Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague-Dawley rats. Toxicol Sci 2007, 96(2):335-345.
45. Meyer-Bahlburg H.F.L. Brain development and cognitive, psychosocial, and psychiatric functioning in classical 21-hydroxylase deficiency. Endocr Dev 2011, 20:88-95.
46. Puts D.A., McDaniel M.A., Jordan C.L., Breedlove S.M. Spatial ability and prenatal androgens: meta-analyses of congenital adrenal hyperplasia and digit ratio (2D:4D) studies. Arch Sex Behav 2008, 37(1):100-111.
47. Ramos A. Animal models of anxiety: do I need multiple tests?. Trends Pharmacol Sci 2008, 29(10):493-498.
48. Ramos A., Mormède P. Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav Rev 1998, 22(1):33-57.
49. Trullas R., Skolnick P. Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology (Berl) 1993, 111(3):323-331.
50. Vendruscolo L.F., Takahashi R.N., Brüske G.R., Ramos A. Evaluation of the anxiolytic-like effect of NKP608, a NK1-receptor antagonist, in two rat strains that differ in anxiety-related behaviors. Psychopharmacology (Berl) 2003, 170(3):287-293.
51. Atallah M., Barbeau I., Pellett P. Metabolic and development changes in growing rats born to dams restricted in protein and/or energy intake. J Nutr 1977, 107(4):650-655.
52. Forbes W., Tracy C., Resnick O., Morgane P. Effects of maternal dietary protein restriction on growth of the brain and body in the rat. Brain Res Bull 1977, 2(2):131-135.
53. Pond W., Yen J., Yen L. Body weight deficit in the absence of reduction in cerebrum weight and nucleic acid content in progeny of swine restricted in protein intake during pregnancy. Proc Soc Exp Biol Med 1988, 188(2):117-121.
54. Siassi F., Siassi B. Differential effects of protein-calorie restriction and subsequent repletion on neuronal and nonneuronal components of cerebral cortex in newborn rats. J Nutr 1973, 103(11):1625-1633.
55. Desai M., Crowther N., Lucas A., Hales C. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 1996, 76(4):591-603.
56. Torres N., Bautista C.J., Tovar A.R., Ordaz G., Rodriguez-Cruz M., Ortiz V., et al. Protein restriction during pregnancy affects maternal liver lipid metabolism and fetal brain lipid composition in the rat. Am J Physiol Endocrinol Metab 2009, 298(2):E270-277.
57. Lesage J., Sebaai N., Leonhardt M., Dutriez-Casteloot I., Breton C., Deloof S., et al. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress 2006, 9(4):183-198.
58. Schäffer L., Müller-Vizentini D., Burkhardt T., Rauh M., Ehlert U., Beinder E. Blunted stress response in small for gestational age neonates. Pediatr Res 2009, 65(2):231-235.
59. Sebaai N., Lesage J., Breton C., Vieau D., Deloof S. Perinatal food deprivation induces marked alterations of the hypothalamo-pituitary-adrenal axis in 8-month-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology 2004, 79(4):163-173.
60. Vieau D., Sebaai N., Leonhardt M., Dutriez-Casteloot I., Molendi-Coste O., Laborie C., et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 2007, 32(Suppl. (1)):S16-S20.
61. Sebaai N., Lesage J., Vieau D., Alaoui A., Dupouy J., Deloof S. Altered control of the hypothalamo-pituitary-adrenal axis in adult male rats exposed perinatally to food deprivation and/or dehydration. Neuroendocrinology 2002, 76(4):243-253.
62. Leonhardt M., Lesage J., Dufourny L., Dickes-Coopman A., Montel V., Dupouy J. Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology 2002, 75(1):45-54.
63. Chisari A., Giovambattista A., Perello M., Spinedi E. Impact of maternal undernutrition on hypothalamo-pituitary-adrenal axis and adipocyte functions in male rat offspring. Endocrine 2001, 14(3):375-382.
64. Galler J.R., Bryce C.P., Waber D., Hock R.S., Exner N., Eaglesfield D., et al. Early childhood malnutrition predicts depressive symptoms at ages 11-17. J Child Psychol Psychiatry 2010, 51(7):789-798.