Maternal perinatal undernutrition alters postnatal development of chromaffin cells in the male rat adrenal medulla.
Numerous data suggest that the development of the sympathoadrenal system is highly sensitive to the perinatal environment. We previously reported that maternal perinatal food restriction by 50% (FR50) altered chromaffin cell (CC) organization and activity in offspring at weaning. This study investigated the effects of FR50 on the postnatal time course of CC functional and structural adaptations. FR50 pups exhibited smaller and more abundant scattered clusters of noradrenergic CCs as early as postnatal day 7 (P7), indicating that morphological changes took place earlier during development. At birth, the adrenaline release was defective in FR50 pups, suggesting that maternal FR50 impaired the non-neurogenic control of catecholamine release. At P4, the catecholamine release in response to insulin-induced hypoglycaemia was also absent in FR50 pups. This was associated with the reduction of adrenal catecholamine contents, indicating that the failure to synthesize catecholamine might lead to impaired secretion. We hypothesized that maternal FR50 accelerated the functional connections between CCs and splanchnic nerve endings, leading to the premature loss of the non-neurogenic response. Acetylcholine-containing synaptic endings seemed more precociously functional in FR50 pups, as suggested by increased levels of acetylcholine esterase activity at P14. At P7, insulin-induced hypoglycaemia caused preferential adrenaline release associated with increased catecholamine contents in both groups. However, the response was accentuated in FR50 pups. At P14, the insulin challenge increased plasma levels of adrenaline in control rats, whereas it markedly enhanced the circulating level of both catecholamines in FR50 pups. We demonstrated that maternal FR50 leads to developmentally impaired noradrenergic CC aggregation and advanced splanchnic neurotransmission maturation associated with altered medulla activity in response to metabolic stress. This might contribute to the long-lasting malprogramming of the adrenal medulla and to the development of chronic adult diseases.
Molendi-Coste
Olivier
O
Unité de Neurosciences et Physiologie Adaptatives, UPRES EA 4052, Equipe Dénutritions Maternelles Périnatales, SN4, Université de Lille I, Villeneuve d'Ascq, France.
Laborie
Christine
C
Scarpa
Maria Cristina
MC
Montel
Valérie
V
Vieau
Didier
D
Breton
Christophe
C
D000110:Acetylcholinesterase / Q000378:metabolism; D000313:Adrenal Medulla / Q000254:growth & development* / Q000502:physiology / Q000503:physiopathology; D000818:Animals; D000831:Animals, Newborn; D002395:Catecholamines / Q000097:blood / Q000378:metabolism; D019439:Chromaffin Cells / Q000502:physiology*; D004837:Epinephrine / Q000097:blood / Q000378:metabolism; D005260:Female; D007003:Hypoglycemia / Q000139:chemically induced / Q000503:physiopathology; D007328:Insulin; D008297:Male; D044342:Malnutrition; D009035:Mothers; D009638:Norepinephrine / Q000378:metabolism; D011247:Pregnancy; D011297:Prenatal Exposure Delayed Effects; D011897:Random Allocation; D051381:Rats; D017208:Rats, Wistar; D013312:Stress, Physiological / Q000502:physiology; D013569:Synapses / Q000502:physiology
D002395:Catecholamines; D007328:Insulin; D000110:Acetylcholinesterase; D009638:Norepinephrine; D004837:Epinephrine