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Offspring’s hydromineral adaptive responses to maternal undernutrition during lactation

Published online by Cambridge University Press:  03 August 2015

P. Nuñez*
Affiliation:
Departamento de Biologia Funcional (Area de Fisiologia), Facultad de Medicina, Universidad de Oviedo, Oviedo, Spain
J. Arguelles
Affiliation:
Departamento de Biologia Funcional (Area de Fisiologia), Facultad de Medicina, Universidad de Oviedo, Oviedo, Spain
C. Perillan
Affiliation:
Departamento de Biologia Funcional (Area de Fisiologia), Facultad de Medicina, Universidad de Oviedo, Oviedo, Spain
*
*Address for correspondence: P. Nuñez, Departamento de Biologia Funcional (Area de Fisiologia), Facultad de Medicina, Universidad de Oviedo, C/Julian Claveria 6, E-33006 Oviedo, Spain. (Email nunezpaula@uniovi.es)

Abstract

Early development, throughout gestation and lactation, represents a period of extreme vulnerability during which susceptibility to later metabolic and cardiovascular injuries increases. Maternal diet is a major determinant of the foetal and newborn developmental environment; maternal undernutrition may result in adaptive responses leading to structural and molecular alterations in various organs and tissues, such as the brain and kidney. New nephron anlages appear in the renal cortex up to postnatal day 4 and the last anlages to be formed develop into functional nephrons by postnatal day 10 in rodents. We used a model of undernutrition in rat dams that were food-restricted during the first half of the lactation period in order to study the long-term effects of maternal diet on renal development, behaviour and neural hydromineral control mechanisms. The study showed that after 40% food restriction in maternal dietary intake, the dipsogenic responses for both water and salt intake were not altered; Fos expression in brain areas investigated involved in hydromineral homeostasis control was always higher in the offspring in response to isoproterenol. This was accompanied by normal plasma osmolality changes and typical renal histology. These results suggest that the mechanisms for the control of hydromineral balance were unaffected in the offspring of these 40% food-restricted mothers. Undernutrition of the pups may not be as drastic as suggested by dams’ restriction.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. Barker, DJ, Eriksson, JG, Forsén, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 12351239.Google Scholar
2. Barker, DJ, Osmond, C, Golding, J, Kuh, D, Wadsworth, ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br Med J. 1989; 298, 564567.Google Scholar
3. Langley-Evans, SC, McMullen, S. Developmental origins of adult disease. Med Princip Pract. 2010; 19, 8798.Google Scholar
4. Ravussin, E, Burnand, B, Schutz, Y, Jéquier, E. Energy expenditure before and during energy restriction in obese. Am J Clinic Nutr. 1985; 41, 753759.Google Scholar
5. Rosenbaum, M, Murphy, EM, Heymsfield, SB, Matthews, DE, Leibel, RL. Low dose leptin administration reverses effects of sustained weight reduction on energy expenditure and circulating concentrations of thyroid hormones. J Clinic Endocrinol Metab. 2002; 87, 23912394.Google Scholar
6. Araujo, RL, de Andrade, BM, de Figueiredo, AS, et al. Low replacement doses of thyroxine during food restriction restores type 1 deiodinase activity in rats and promotes body protein loss. J Endocrinol. 2008; 198, 119125.Google Scholar
7. Hao, S, Avraham, Y, Mechoulam, R, Berry, EM. Low dose anandamide affects food intake, cognitive function, neurotransmitter and corticosterone levels in diet-restricted mice. Eur J Pharmacol. 2000; 392, 147156.Google Scholar
8. Langley-Evans, SC. Fetal programming of CVD and renal disease: animal models and mechanistic considerations. Proc Nutr Soc. 2013; 72, 317325.Google Scholar
9. Thompson, NM, Norman, AM, Donkin, SS, et al. Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes. Endocrinology. 2007; 148, 23452354.Google Scholar
10. Lucas, A, Baker, BA, Desai, M, Hales, CN. Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutr. 1996; 76, 605612.Google Scholar
11. Luzardo, R, Silva, PA, Einicker-Lamas, M, et al. Metabolic programming during lactation stimulates renal Na+ transport in the adult offspring due to an early impact on local angiotensin II pathways. PLoS One. 2011; 6, e21232.Google Scholar
12. Langley-Evans, SC. Fetal origins of adult disease. Br J Nutr. 1999; 81, 56.Google Scholar
13. Lucas, A. Programming by early nutrition in man. Ciba Found Symp. 1991; 156, 3850.Google Scholar
14. Paixão, AD, Maciel, CR, Teles, MB, Figueiredo-Silva, J. Regional Brazilian diet-induced low birth weight is correlated with changes in renal hemodynamics and glomerular morphometry in adult age. Biol Neonat. 2001; 80, 239246.Google Scholar
15. Wlodek, ME, Westcott, K, Siebel, AL, Owens, JA, Moritz, KM. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008; 74, 187195.Google Scholar
16. Woods, LL, Rasch, R. Perinatal ANG II programs adult blood pressure, glomerular number, and renal function in rats. Am J Physiol. 1998; 275, 15931599.Google Scholar
17. Moritz, KM, Dodic, M, Wintour, EM. Kidney development and the fetal programming of adult disease. Bioessays. 2003; 25, 212220.Google Scholar
18. Neiss, WF, Klehn, KL. The postnatal development of the rat kidney, with special reference to the chemodifferentiation of the proximal tubule. Histochemical. 1981; 73, 251268.Google Scholar
19. Schreuder, MF, Nyengaard, JR, Remmers, F, van Wijk, JA, Delemarre-van de Waal, HA. Postnatal food restriction in the rat as a model for a low nephron endowment. Am J Physiol Renal Physiol. 2006; 291, 11041107.Google Scholar
20. Langley-Evans, SC, Welham, SJ, Jackson, AA. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999; 64, 965974.Google Scholar
21. Mao, C, Shi, L, Xu, F, Zhang, L, Xu, Z. Development of fetal brain renin-angiotensin system and hypertension programmed in fetal origins. Prog Neurobiol. 2009; 87, 252263.Google Scholar
22. Woods, LL, Ingelfinger, JR, Nyengaard, JR, Rasch, R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res. 2001; 49, 460467.Google Scholar
23. Mahon, JM, Allen, M, Herbert, J, Fitzsimons, JT. The association of thirst, sodium appetite and vasopressin release with c-fos expression in the forebrain of the rat after intracerebroventricular injection of angiotensin II, angiotensin-(1-7) or carbachol. Neuroscience. 1995; 69, 199208.Google Scholar
24. Mecawi, AS, Macchione, AF, Nuñez, P, et al. Developmental programing of thirst and sodium appetite. Neurosci Biobehav Rev. 2015; 51, 114.Google Scholar
25. Herbert, J, Forsling, ML, Howes, SR, Stacey, PM, Shiers, HM. Regional expression of c-fos antigen in the basal forebrain following intraventricular infusions of angiotensin and its modulation by drinking either water or saline. Neuroscience. 1992; 51, 867882.Google Scholar
26. Hoffman, GE, Smith, MS, Verbalis, JG. c-Fos and related immediateimmediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol. 1993; 14, 173213.Google Scholar
27. McKinley, MJ, Johnson, AK. The physiological regulation of thirst and fluid intake. News Physiol Sci. 2004; 19, 16.Google Scholar
28. Rowland, NE. Brain mechanisms of mammalian fluid homeostasis: insights from use of immediate early gene mapping. Neurosci Biobehav Rev. 1998; 23, 4963.Google Scholar
29. Fitzsimons, JT. Angiotensin, thirst, and sodium appetite. Physiol Rev. 1998; 78, 583586.Google Scholar
30. Alwasel, SH, Barker, DJ, Ashton, N. Prenatal programming of renal salt wasting resets postnatal salt appetite, which drives food intake in the rat. Clin Sci. 2012; 122, 281288.Google Scholar
31. Argüelles, J, Brime, JI, López-Sela, P, Perillán, C, Vijande, M. Adult offspring long-term effects of high salt and water intake during pregnancy. Hormon Behav. 2000; 37, 156162.Google Scholar
32. Contreras, RJ. High NaCl intake of rat dams alters maternal behavior and elevates blood pressure of adult offspring. Am J Physiol. 1993; 264, 296304.Google Scholar
33. Contreras, RJ, Wong, DL, Henderson, R, Curtis, KS, Smith, JC. High dietary NaCl early in development enhances mean arterial pressure of adult rats. Physiol Behav. 2000; 71, 173181.Google Scholar
34. Galaverna, O, Nicolaïdis, S, Yao, SZ, Sakai, RR, Epstein, AN. Endocrine consequences of prenatal sodium depletion prepare rats for high need-free NaCl intake in adulthood. Am J Physiol. 1995; 269, 578583.Google Scholar
35. Nicolaïdis, S, Galaverna, O, Metzler, CH. Extracellular dehydratation during pregnancy increases salt appetite of offspring. Am J Physiol. 1990; 258, 281283.Google Scholar
36. Hsu, SM, Raine, L, Fanger, H. A comparative study of the peroxidase-antiperoxidase method and an avidin-biotin complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clinic Pathol. 1981; 75, 734738.Google Scholar
37. Paxinos, G, Watson, C. The Rat Nervous System. 2nd edn, 1998. Academic Press: San Diego.Google Scholar
38. Thunhorst, RL, Xu, Z, Cicha, MZ, Zardetto-Smith, AM, Johnson, AK. Fos expression in rat brain during depletion-induced thirst and salt appetite. Am J Physiol. 1998; 274, 18071814.Google Scholar
39. Brigham, HE, Sakanashi, TM, Rasmussen, KM. The effect of food restriction during the reproductive cycle on organ growth and milk yield and composition in rats. Nutr Res. 1992; 12, 845856.Google Scholar
40. Kliewer, RL, Rasmussen, KM. Malnutrition during the reproductive cycle: effects on galactopoietic hormones and lactational performance in the rat. Am J Clin Nutr. 1987; 46, 926935.Google Scholar
41. Harris, RB, Kasser, TR, Martin, RJ. Dynamics of recovery of body composition after overfeeding, food restriction or starvation of mature female rats. J Nutr. 1986; 116, 25362546.Google Scholar
42. Garg, M, Thamotharan, M, Dai, Y, et al. Early postnatal caloric restriction protects adult male intrauterine growth-restricted offspring from obesity. Diabetes. 2012; 61, 13911398.Google Scholar
43. Perillan, C, Costales, M, Vijande, M, Arguelles, J. Maternal RAS influence on the ontogeny of thirst. Physiol Behav. 2007; 92, 554559.Google Scholar
44. Perillán, C, Núñez, P, Costales, M, Vijande, M, Argüelles, J. Ingestive behavior in rat pups is modified by maternal sodium depletion. Psicothema. 2012; 24, 422426.Google Scholar
45. Ross, GM, Nijland, MJ. Development of ingestive behavior. Am J Physiol. 1998; 274, 879893.Google Scholar
46. Wirth, JB, Epstein, AN. Ontogeny of thirst in the infant rat. Am J Physiol. 1976; 230, 188198.Google Scholar
47. Macchione, AF, Caeiro, XE, Godino, A, et al. Availability of a rich source of sodium during the perinatal period programs the fluid balance restoration pattern in adult offspring. Physiol Behav. 2012; 105, 10351044.Google Scholar
48. Leshem, M, Levin, T, Schulkin, J. Intake and hedonics of calcium and sodium during pregnancy and lactation in the rat. Physiol Behav. 2002; 75, 313322.Google Scholar
49. Johnson, AK, Mann, JF, Rascher, W, Johnson, JK, Ganten, D. Plasma angiotensin II concentrations and experimentally induced thirst. Am J Physiol. 1981; 240, 229334.Google Scholar
50. Moosavi, SM, Johns, EJ. The effect of isoprenaline infusion on renal renin and angiotensinogen gene expression in the anaesthetised rat. Exp Physiol. 2003; 88, 221227.Google Scholar
51. Robinson, MM, Evered, MD. Pressor action of intravenous angiotensin II reduces drinking response in rats. Am J Physiol. 1987; 252, 754759.Google Scholar
52. Joles, JA, Sculley, DV, Langley-Evans, SC. Proteinuria in aging rats due to low-protein diet during mid-gestation. J Dev Org Health Dis. 2010; 1, 7583.Google Scholar
53. Wlodek, ME, Mibus, A, Tan, A, et al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007; 18, 16881696.Google Scholar
54. Chen, CM, Chou, HC. Effects of maternal undernutrition on glomerular ultrastructure in rat offspring. Pediatr Neonat. 2009; 50, 5053.Google Scholar
55. Sly, JD, Colvill, L, McKinley, JM, Oldfield, JB. Identification of neural projections from the forebrain to the kidney, using the virus pseudorabies. J Auton Nerv Syst. 1999; 77, 7382.Google Scholar
56. Sagar, SM, Sharp, FR, Curran, T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science. 1988; 240, 13281331.Google Scholar
57. Antunes-Rodrigues, J, Ruginsk, SG, Mecawi, AS, et al. Mapping and signaling of neural pathways involved in the regulation of hydromineral homeostasis. Braz J Med Biol Res. 2013; 46, 327338.Google Scholar
58. Krause, EG, Curtis, KS, Stincic, TL, Markle, JP, Contreras, RJ. Oestrogen and weight loss decrease isoproterenol-induced Fos immunoreactivity and angiotensin type 1 mRNA in the subfornical organ of female rats. J Physiol. 2006; 573, 251262.Google Scholar
59. Landgraf, R, Malkinson, T, Horn, T, et al. Release of vasopressin and oxytocin by paraventricular nucleus stimulation in rats. Am J Physiol. 1990; 258, 155159.Google Scholar