Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 9, 2006 - Issue 4
1,117
Views
65
CrossRef citations to date
0
Altmetric
Original

Perinatal maternal undernutrition programs the offspring hypothalamo–pituitary–adrenal (HPA) axis

, , , , , & show all
Pages 183-198 | Received 14 May 2006, Accepted 10 Oct 2006, Published online: 07 Jul 2009

Keep up to date with the latest research on this topic with citation updates for this article.

Read on this site (3)

Kit-Yi Yam, Eva F. G. Naninck, Mathias V. Schmidt, Paul J. Lucassen & Aniko Korosi. (2015) Early-life adversity programs emotional functions and the neuroendocrine stress system: the contribution of nutrition, metabolic hormones and epigenetic mechanisms. Stress 18:3, pages 328-342.
Read now
Jane E Harding, José GB Derraik & Frank H Bloomfield. (2010) Maternal undernutrition and endocrine development. Expert Review of Endocrinology & Metabolism 5:2, pages 297-312.
Read now
. (2007) Stress milestones. Stress 10:1, pages 1-2.
Read now

Articles from other publishers (62)

Shuai Liu, Huizhen Lu, Shengyong Mao, Zijun Zhang, Wen Zhu, Jianbo Cheng & Yanfeng Xue. (2023) Undernutrition-induced substance metabolism and energy production disorders affected the structure and function of the pituitary gland in a pregnant sheep model. Frontiers in Nutrition 10.
Crossref
Chika Ando, Sihui Ma, Moe Miyoshi, Kyohei Furukawa, Xuguang Li, Huijuan Jia & Hisanori Kato. (2023) Postnatal nutrition environment reprograms renal DNA methylation patterns in offspring of maternal protein-restricted stroke-prone spontaneously hypertensive rats. Frontiers in Nutrition 10.
Crossref
Isabela Peixoto Martins, Rodrigo Vargas, Lucas Paulo Jacinto Saavedra, Sarah Rickli, Camila Cristina Ianoni Matiusso, Audrei Pavanello, Lucas Casagrande, Maria José Pastre, Júlia Berno Oliveira, Ariadny Martins de Almeida, Anna Carolina Huppes de Souza, Júlio Cezar de Oliveira, Ananda Malta & Paulo Cezar de Freitas Mathias. (2023) Protein-caloric restriction induced HPA axis activation and altered the milk composition imprint metabolism of weaned rat offspring. Nutrition 108, pages 111945.
Crossref
Ana Luiza Machado Wunderlich, Andressa Busetti Martins, Camila Franciele de Souza, Larissa Rugila S. Stopa, Érica Cristina A.M. Monteiro, Danielly D. Aguiar, Rhauany P. Guergolette, Cássia Thaïs B.V. Zaia & Ernane Torres Uchôa. (2023) Neonatal overnutrition, but not neonatal undernutrition, disrupts CCK-induced hypophagia and neuron activation of the nucleus of the solitary tract and paraventricular nucleus of hypothalamus of male Wistar rats. Brain Research Bulletin 195, pages 109-119.
Crossref
Zoe West, Iryna Demchenko, Lee Clark, Marina White, Amanda J. MacFarlane, William D. Fraser, Tye E. Arbuckle & Kristin L. Connor. (2022) Relationships between maternal body mass index and child cognitive outcomes at 3 years of age are buffered by specific early environments in a prospective Canadian birth cohort. Journal of Developmental Origins of Health and Disease, pages 1-11.
Crossref
Tiago J. Costa, Júlio Cezar De Oliveira, Fernanda Regina Giachini, Victor Vitorino Lima, Rita C. Tostes & Gisele Facholi Bomfim. (2022) Programming of Vascular Dysfunction by Maternal Stress: Immune System Implications. Frontiers in Physiology 13.
Crossref
Gabriel Boer Grigoletti-Lima, Marcelo Gustavo Lopes, Ana Tereza Barufi Franco, Aparecida Marcela Damico, Patrìcia Aline Boer & José Antonio Rocha Gontijo. (2022) Severe Gestational Low-Protein Intake Impacts Hippocampal Cellularity, Tau, and Amyloid-β Levels, and Memory Performance in Male Adult Offspring: An Alzheimer-Simile Disease Model?. Journal of Alzheimer's Disease Reports 6:1, pages 17-30.
Crossref
Yinxian Wen, Siyuan Cheng, Juan Lu, Xia He, Zhexiao Jiao, Dan Xu & Hui Wang. (2021) Dysfunction of the hypothalamic‑pituitary‑adrenal axis in male rat offspring with prenatal food restriction: Fetal programming of hypothalamic hyperexcitability and poor hippocampal feedback. Molecular Medicine Reports 25:1.
Crossref
Henrique Rodrigues Vieira, Gessica Dutra Gonçalves, Vander Silva Alves, Milene Aparecida Bobato de Melo, Stephanie Carvalho Borges, Josana Klagenberg, Camila Quaglio Neves, Carina Previate, Lucas Paulo Jacinto Saavedra, Gláucia Eloisa Munhoz de Lion Siervo, Ananda Malta, Marialba Avezum Alves de Castro Prado, Kesia Palma-Rigo, Nilza Cristina Buttow, Glaura Scantamburlo Alves Fernandes & Paulo Cezar de Freitas Mathias. (2021) Neonatal metformin short exposure inhibits male reproductive dysfunction caused by a high-fat diet in adult rats. Toxicology and Applied Pharmacology 429, pages 115712.
Crossref
Phoebe D. Edwards, Sophia G. Lavergne, Laura K. McCaw, Sanoji Wijenayake, Rudy Boonstra, Patrick O. McGowan & Melissa M. Holmes. (2021) Maternal effects in mammals: Broadening our understanding of offspring programming. Frontiers in Neuroendocrinology 62, pages 100924.
Crossref
György Csaba. (2020) Reprogramming of the Immune System by Stress and Faulty Hormonal Imprinting. Clinical Therapeutics 42:6, pages 983-992.
Crossref
Declan Wayne, T’ng Chang Kwok, Shalini Ojha, Helen Budge & Michael E. Symonds. 2020. Maternal-Fetal and Neonatal Endocrinology. Maternal-Fetal and Neonatal Endocrinology 663 672 .
Bernard P. Chang. (2019) Can hospitalization be hazardous to your health? A nosocomial based stress model for hospitalization. General Hospital Psychiatry 60, pages 83-89.
Crossref
Heather C. Brenhouse & Kevin G. Bath. (2019) Bundling the haystack to find the needle: Challenges and opportunities in modeling risk and resilience following early life stress. Frontiers in Neuroendocrinology 54, pages 100768.
Crossref
John A. Russell & Paula J. Brunton. (2019) Giving a good start to a new life via maternal brain allostatic adaptations in pregnancy. Frontiers in Neuroendocrinology 53, pages 100739.
Crossref
Y. Diz-Chaves, L. Toba, J. Fandiño, L. C. González-Matías, L. M. Garcia-Segura & F. Mallo. (2018) The GLP-1 analog, liraglutide prevents the increase of proinflammatory mediators in the hippocampus of male rat pups submitted to maternal perinatal food restriction. Journal of Neuroinflammation 15:1.
Crossref
D. B. Torres, A. Lopes, A. J. Rodrigues, J. J Cerqueira, N. Sousa, J. A. R. Gontijo & P. A. Boer. (2018) Anxiety-like behavior and structural changes of the bed nucleus of the stria terminalis (BNST) in gestational protein-restricted male offspring. Journal of Developmental Origins of Health and Disease 9:5, pages 536-543.
Crossref
Nancy Rodriguez, Ana C Liaudat, Nora I Mayer, Adriana Vivas, María C Romanini & Pablo Bosch. (2018) Attenuation effects of prenatal stress by early postnatal stimulation in different research models. MOJ Anatomy & Physiology 5:5.
Crossref
Luba Sominsky, Lin Kooi Ong, Ilvana Ziko, Phillip W. Dickson & Sarah J. Spencer. (2018) Neonatal overfeeding increases capacity for catecholamine biosynthesis from the adrenal gland acutely and long-term in the male rat. Molecular and Cellular Endocrinology 470, pages 295-303.
Crossref
Isabela Peixoto Martins, Júlio Cezar de Oliveira, Audrei Pavanello, Camila Cristina Ianoni Matiusso, Carina Previate, Laize Peron Tófolo, Tatiane Aparecida Ribeiro, Claudinéia Conationi da Silva Franco, Rosiane Aparecida Miranda, Kelly Valério Prates, Vander Silva Alves, Flávio Andrade Francisco, Ana Maria Praxedes de Moraes, Paulo Cezar de Freitas Mathias & Ananda Malta. (2018) Protein-restriction diet during the suckling phase programs rat metabolism against obesity and insulin resistance exacerbation induced by a high-fat diet in adulthood. The Journal of Nutritional Biochemistry 57, pages 153-161.
Crossref
Flávio Andrade Francisco, Luiz Felipe Barella, Sandra da Silva Silveira, Lucas Paulo Jacinto Saavedra, Kelly Valério Prates, Vander Silva Alves, Claudinéia Conationi da Silva Franco, Rosiane Aparecida Miranda, Tatiane Aparecida Ribeiro, Laize Peron Tófolo, Ananda Malta, Elaine Vieira, Kesia Palma-Rigo, Audrei Pavanello, Isabela Peixoto Martins, Veridiana Mota Moreira, Júlio Cezar de Oliveira, Paulo Cezar de Freitas Mathias & Rodrigo Mello Gomes. (2016) Methylglyoxal treatment in lactating mothers leads to type 2 diabetes phenotype in male rat offspring at adulthood. European Journal of Nutrition 57:2, pages 477-486.
Crossref
K.E. Waldie, C.M. Cornforth, R.E. Webb, J.M.D. Thompson, R. Murphy, D. Moreau, R. Slykerman, A.R. Morgan, L.R. Ferguson & E.A. Mitchell. (2017) Dopamine transporter (DAT1/SLC6A3) polymorphism and the association between being born small for gestational age and symptoms of ADHD. Behavioural Brain Research 333, pages 90-97.
Crossref
Xiang Li, Mengshu Zhang, Xinghua Pan, Zhice Xu & Miao Sun. (2017) “Three Hits” Hypothesis for Developmental Origins of Health and Diseases in View of Cardiovascular Abnormalities. Birth Defects Research 109:10, pages 744-757.
Crossref
Qian Zhang, Xiaofang Sun, Xinhua Xiao, Jia Zheng, Ming Li, Miao Yu, Fan Ping, Zhixin Wang, Cuijuan Qi, Tong Wang & Xiaojing Wang. (2016) Maternal Chromium Restriction Leads to Glucose Metabolism Imbalance in Mice Offspring through Insulin Signaling and Wnt Signaling Pathways. International Journal of Molecular Sciences 17:10, pages 1767.
Crossref
Ananda Malta, Aline Amenencia de Souza, Tatiane Aparecida Ribeiro, Flávio Andrade Francisco, Audrei Pavanello, Kelly Valério Prates, Laize Peron Tófolo, Rosiane Aparecida Miranda, Júlio Cezar de Oliveira, Isabela Peixoto Martins, Carina Previate, Rodrigo Mello Gomes, Claudinéia Conationi da Silva Franco, Maria Raquel Marçal Natali, Kesia Palma-Rigo & Paulo Cezar de Freitas Mathias. (2016) Neonatal treatment with scopolamine butylbromide prevents metabolic dysfunction in male rats. Scientific Reports 6:1.
Crossref
Annika Thorsell & Daniel Nätt. (2016) Maternal stress and diet may influence affective behavior and stress-response in offspring via epigenetic regulation of central peptidergic function. Environmental Epigenetics 2:3, pages dvw012.
Crossref
Rajendra K. Shukla, Richa Gupta, Pranay Srivastava, Yogesh K. Dhuriya, Anshuman Singh, Lalit P. Chandravanshi, Ajay Kumar, M. Haris Siddiqui, Devendra Parmar, Aditya B. Pant & Vinay K. Khanna. (2016) Brain cholinergic alterations in rats subjected to repeated immobilization or forced swim stress on lambda-cyhalothrin exposure. Neurochemistry International 93, pages 51-63.
Crossref
F. I. Milagro, J. I. Riezu-Boj & J. A. Martinez. (2015) Epigenetic Determinants of Weight Management: Methylation Signatures. Current Nutrition Reports 4:4, pages 330-339.
Crossref
P Nguyen, S Khurana, H Peltsch, J Grandbois, J Eibl, J Crispo, D Ansell & T C Tai. (2015) Prenatal glucocorticoid exposure programs adrenal PNMT expression and adult hypertension. Journal of Endocrinology 227:2, pages 117-127.
Crossref
Vinita Khot, Preeti Chavan-Gautam & Sadhana Joshi. (2015) Proposing interactions between maternal phospholipids and the one carbon cycle: A novel mechanism influencing the risk for cardiovascular diseases in the offspring in later life. Life Sciences 129, pages 16-21.
Crossref
Barbara T. Alexander, John Henry Dasinger & Suttira Intapad. 2011. Comprehensive Physiology. Comprehensive Physiology 997 1025 .
L.A. Reyes-Castro, G.L. Rodríguez-González, R. Chavira, C. Ibáñez, C. Lomas-Soria, J.S. Rodriguez, P.W. Nathanielsz & E. Zambrano. (2015) Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet. Physiology & Behavior 140, pages 89-95.
Crossref
Jennifer E. Khoury, Andrea Gonzalez, Robert D. Levitan, Jens C. Pruessner, Kevin Chopra, Vincenzo Santo Basile, Mario Masellis, Alasdair Goodwill & Leslie Atkinson. (2015) Summary cortisol reactivity indicators: Interrelations and meaning. Neurobiology of Stress 2, pages 34-43.
Crossref
C. Shilton, G. P. Brown, L. Chambers, S. Benedict, S. Davis, S. Aumann & S. R. Isberg. (2014) Pathology of Runting in Farmed Saltwater Crocodiles ( Crocodylus porosus ) in Australia . Veterinary Pathology 51:5, pages 1022-1034.
Crossref
A. Malta, J. C. de Oliveira, T. A. d. S. Ribeiro, L. P. Tofolo, L. F. Barella, K. V. Prates, R. A. Miranda, G. Elmhiri, C. C. d. S. Franco, A. R. Agostinho, A. B. Trombini, A. Pavanello, C. Gravena, L. Abdennebi-Najar & P. C. d. F. Mathias. (2014) Low-protein diet in adult male rats has long-term effects on metabolism. Journal of Endocrinology 221:2, pages 285-295.
Crossref
Marie-Amélie Lukaszewski, Delphine EberléDidier VieauChristophe Breton. (2013) Nutritional manipulations in the perinatal period program adipose tissue in offspring. American Journal of Physiology-Endocrinology and Metabolism 305:10, pages E1195-E1207.
Crossref
W. Otten, E. Kanitz, M. Tuchscherer, M. Gräbner, G. Nürnberg, O. Bellmann, U. Hennig, C. Rehfeldt & C. C. Metges. (2013) Effects of low and high protein:carbohydrate ratios in the diet of pregnant gilts on maternal cortisol concentrations and the adrenocortical and sympathoadrenal reactivity in their offspring1,2. Journal of Animal Science 91:6, pages 2680-2692.
Crossref
Marie-Amélie Lukaszewski, Laura Butruille, Emmanuelle Moitrot, Valérie Montel, Anne Dickes-Coopman, Jean Lesage, Christine Laborie, Didier Vieau & Christophe Breton. (2013) The hypothalamic POMC mRNA expression is upregulated in prenatally undernourished male rat offspring under high-fat diet. Peptides 43, pages 146-154.
Crossref
A. Lopes, D.B. Torres, A.J. Rodrigues, J.J. Cerqueira, J.M. Pêgo, N. Sousa, J.A.R. Gontijo & P.A. Boer. (2012) Gestational protein restriction induces CA3 dendritic atrophy in dorsal hippocampal neurons but does not alter learning and memory performance in adult offspring. International Journal of Developmental Neuroscience 31:3, pages 151-156.
Crossref
J. C. de Oliveira, P. C. Lisboa, E. G. de Moura, L. F. Barella, R. A. Miranda, A. Malta, C. C. d. S. Franco, T. A. d. S. Ribeiro, R. Torrezan, C. Gravena & P. C. d. F. Mathias. (2012) Poor pubertal protein nutrition disturbs glucose-induced insulin secretion process in pancreatic islets and programs rats in adulthood to increase fat accumulation. Journal of Endocrinology 216:2, pages 195-206.
Crossref
Christophe Breton. (2013) Role of maternal nutrition in programming adiposity in the offspring: potential implications of glucocorticoids. Hormone Molecular Biology and Clinical Investigation 14:1.
Crossref
Ellen Kanitz, Winfried Otten, Margret Tuchscherer, Maria Gräbner, Klaus-Peter Brüssow, Charlotte Rehfeldt & Cornelia C. Metges. (2012) High and Low Protein∶ Carbohydrate Dietary Ratios during Gestation Alter Maternal-Fetal Cortisol Regulation in Pigs. PLoS ONE 7:12, pages e52748.
Crossref
Júlio Cezar de Oliveira, Sabrina Grassiolli, Clarice Gravena & Paulo Cezar Freitas de Mathias. (2012) Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life. Nutrition & Metabolism 9:1.
Crossref
Michelle M. Kett. (2012) Arterial pressure in animal models of fetal programming. Journal of Hypertension 30:12, pages 2268-2270.
Crossref
Ganga Gokulakrishnan, Irma J. Estrada, Horacio A. Sosa & Marta L. Fiorotto. (2012) In utero glucocorticoid exposure reduces fetal skeletal muscle mass in rats independent of effects on maternal nutrition. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 302:10, pages R1143-R1152.
Crossref
Xingqi Zhang, Ni Lan, Paxton Bach, David Nordstokke, Wayne Yu, Linda Ellis, Gary G. Meadows & Joanne Weinberg. (2012) Prenatal alcohol exposure alters the course and severity of adjuvant-induced arthritis in female rats. Brain, Behavior, and Immunity 26:3, pages 439-450.
Crossref
Renato Chaves Souto Branco, Júlio Cezar de Oliveira, Sabrina Grassiolli, Rosiane Aparecida Miranda, Luiz Felipe Barella, Rodrigo Mello Gomes, Luiz Augusto Bataglini, Rosana Torrezan, Clarice Gravena & Paulo Cezar de Freitas Mathias. (2012) Maternal Protein Malnutrition Does Not Impair Insulin Secretion from Pancreatic Islets of Offspring after Transplantation into Diabetic Rats. PLoS ONE 7:2, pages e30685.
Crossref
L.A. Reyes-Castro, J.S. Rodriguez, G.L. Rodríguez-González, R. Chavira, C.J. Bautista, T.J. McDonald, P.W. Nathanielsz & E. Zambrano. (2012) Pre- and/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats. Behavioural Brain Research 227:2, pages 324-329.
Crossref
Marie-Amélie Lukaszewski, Sylvain Mayeur, Isabelle Fajardy, Fabien Delahaye, Isabelle Dutriez-Casteloot, Valérie Montel, Anne Dickes-Coopman, Christine Laborie, Jean Lesage, Didier Vieau & Christophe Breton. (2011) Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. American Journal of Physiology-Endocrinology and Metabolism 301:3, pages E548-E559.
Crossref
Johann Guillemot, Marie-Amélie Lukaszewski, Valérie Montel, Fabien Delahaye, Sylvain Mayeur, Christine Laborie, Anne Dickes-Coopman, Isabelle Dutriez-Casteloot, Jean Lesage, Christophe Breton & Didier Vieau. (2011) Influence of prenatal undernutrition on the effects of clozapine and aripiprazole in the adult male rats: Relevance to a neurodevelopmental origin of schizophrenia?. European Journal of Pharmacology 667:1-3, pages 402-409.
Crossref
Paula J. Brunton & John A. Russell. (2011) Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35:5, pages 1178-1191.
Crossref
Lynette C. Daws & Georgianna G. Gould. (2011) Ontogeny and regulation of the serotonin transporter: Providing insights into human disorders. Pharmacology & Therapeutics 131:1, pages 61-79.
Crossref
Cathy M. Dwyer, Christine Moinard, Kirstin M. McIlvaney, Colin A. Morgan & Lutz Bünger. (2011) The effect of gestational undernutrition on maternal weight change and fetal weight in lines of mice selected for different growth characteristics. British Journal of Nutrition 105:4, pages 539-548.
Crossref
J. C. de Oliveira, D. X. Scomparin, A. E. Andreazzi, R. C. S. Branco, A. G. Martins, C. Gravena, S. Grassiolli, W. Rinaldi, F. B. Barbosa & P. C. F. Mathias. (2011) Metabolic Imprinting by Maternal Protein Malnourishment Impairs Vagal Activity in Adult Rats. Journal of Neuroendocrinology 23:2, pages 148-157.
Crossref
Didier Vieau, Sylvain Mayeur, Marie-Amélie Lukaszewski, Fabien Delahave, Isabelle Dutriez-Casteloot, Christine Laborie, Sylvie Deloof, Jean Lesage & Christophe Breton. 2011. Handbook of Behavior, Food and Nutrition. Handbook of Behavior, Food and Nutrition 2055 2068 .
Miriam Schneider. (2009) Cannabis use in pregnancy and early life and its consequences: animal models. European Archives of Psychiatry and Clinical Neuroscience 259:7, pages 383-393.
Crossref
Kaiqing Rao, Jingjing Xie, Xiaojing Yang, Lei Chen, Roland Grossmann & Ruqian Zhao. (2009) Maternal low-protein diet programmes offspring growth in association with alterations in yolk leptin deposition and gene expression in yolk-sac membrane, hypothalamus and muscle of developing Langshan chicken embryos. British Journal of Nutrition 102:6, pages 848-857.
Crossref
Christophe Breton, Marie-Amélie Lukaszewski, Pierre-Yves Risold, Mihaela Enache, Johann Guillemot, Guillaume Rivière, Fabien Delahaye, Jean Lesage, Isabelle Dutriez-Casteloot, Christine Laborie & Didier Vieau. (2009) Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. American Journal of Physiology-Endocrinology and Metabolism 296:3, pages E462-E472.
Crossref
Margaret Semrud-Clikeman & Phyllis Anne Teeter EllisonMargaret Semrud-Clikeman & Phyllis Anne Teeter Ellison. 2009. Child Neuropsychology. Child Neuropsychology 47 64 .
Peter D Eckersall, Fraser P Lawson, Carol E Kyle, Mary Waterston, Laura Bence, Michael J Stear & Stewart M Rhind. (2008) Maternal undernutrition and the ovine acute phase response to vaccination. BMC Veterinary Research 4:1.
Crossref
Fabien Delahaye, Christophe Breton, Pierre-Yves Risold, Mihaela Enache, Isabelle Dutriez-Casteloot, Christine Laborie, Jean Lesage & Didier Vieau. (2008) Maternal Perinatal Undernutrition Drastically Reduces Postnatal Leptin Surge and Affects the Development of Arcuate Nucleus Proopiomelanocortin Neurons in Neonatal Male Rat Pups. Endocrinology 149:2, pages 470-475.
Crossref
Paula J. Brunton & John A. Russell. (2008) The expectant brain: adapting for motherhood. Nature Reviews Neuroscience 9:1, pages 11-25.
Crossref

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.