User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Intrauterine programming of the endocrine pancreas.

Primary tabs

Remacle, Claude [UCL] Dumortier, O Bol, Vanesa [UCL] Goosse, K Romanus, Pierre [UCL] Theys, Nicolas [UCL] Reusens, Brigitte [UCL]

Epidemiological studies have revealed strong relationships between poor foetal growth and subsequent development of the metabolic syndrome. Persisting effects of early malnutrition become translated into pathology, thereby determine chronic risk for developing glucose intolerance and diabetes. These epidemiological observations identify the phenomena of foetal programming without explaining the underlying mechanisms that establish the causal link. Animal models have been established and studies have demonstrated that reduction in the availability of nutrients during foetal development programs the endocrine pancreas and insulin-sensitive tissues. Whatever the type of foetal malnutrition, whether there are not enough calories or protein in food or after placental deficiency, malnourished pups are born with a defect in their beta-cell population that will never completely recover, and insulin-sensitive tissues will be definitively altered. Despite the similar endpoint, different cellular and physiological mechanisms are proposed. Hormones operative during foetal life like insulin itself, insulin-like growth factors and glucocorticoids, as well as specific molecules like taurine, or islet vascularization were implicated as possible factors amplifying the defect. The molecular mechanisms responsible for intrauterine programming of the beta cells are still elusive, but two hypotheses recently emerged: the first one implies programming of mitochondria and the second, epigenetic regulation.

Document type Article de périodique (Journal article) – Journal Article, Research Support, Non-U.S. Gov't, Review
Publication date 2007
Journal information "Diabetes, obesity & metabolism" - Vol. 9 Suppl 2, p. 196-209 (2007)
Peer reviewed yes
issn 1462-8902
Publication status Publié
Affiliation UCL - SC/BIOL - Département de biologie
MESH Subject Animals ; Caloric Restriction ; Cell Proliferation ; Diabetes Mellitus - embryology ; Diet, Protein-Restricted ; Female ; Fetal Development ; Humans ; Insulin-Secreting Cells - cytology ; Ligation ; Malnutrition - complications ; Mitochondria - physiology ; Models, Animal ; Pancreas - embryology ; Pancreatic Diseases - embryology ; Pregnancy ; Pregnancy Complications - etiology ; Rats ; Uterus - blood supply
Links
  1. Edlund H, Diabetes, 50, S5 (2001)
  2. El Khattabi Ilham, Grégoire Francine, Remacle Claude, Reusens Brigitte, Isocaloric maternal low-protein diet alters IGF-I, IGFBPs, and hepatocyte proliferation in the fetal rat, 10.1152/ajpendo.00037.2003
  3. Thamotharan M, Am J Physiol Endocrinol Metab, 292, E1270 (2007)
  4. McLean M., Chipps D., Cheung N. Wah, Mother to child transmission of diabetes mellitus: does gestational diabetes program Type 2 diabetes in the next generation?, 10.1111/j.1464-5491.2006.01979.x
  5. Waterland RA, J Nutr, 132, 357 (2002)
  6. Barker DJ, J Epidemiol Community Health, 43, 237 (1989)
  7. Hales CN, BMJ, 303, 1019 (1991)
  8. Hales C Nicholas, Barker David J P, The thrifty phenotype hypothesis, 10.1093/bmb/60.1.5
  9. Fernandez-Twinn DS, Physiol Behav, 88, 234 (2006)
  10. Poulsen P., Vaag A., The Intrauterine Environment as Reflected by Birth Size and Twin and Zygosity Status Influences Insulin Action and Intracellular Glucose Metabolism in an Age- or Time-Dependent Manner, 10.2337/db05-1462
  11. Lucas A, Am J Clin Nutr, 71, 602 (2000)
  12. Gluckman P.D., Hanson M.A., The Consequences of Being Born Small – An Adaptive Perspective, 10.1159/000091500
  13. Palmer A. J., Weiss C., Sendi P. P., Neeser K., Brandt A., Singh G., Wenzel H., Spinas G. A., The cost-effectiveness of different management strategies for Type I diabetes: a Swiss perspective, 10.1007/s001250050003
  14. Yajnik CS, J Nutr, 134, 205 (2004)
  15. Mericq V., Ong K. K., Bazaes R., Peña V., Avila A., Salazar T., Soto N., Iñiguez G., Dunger D. B., Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children, 10.1007/s00125-005-0036-z
  16. Aerts L, Diabetes Metab Rev, 6, 147 (1990)
  17. Plagemann A, Harder T, Kohlhoff R, Rohde W, Dörner G, Overweight and obesity in infants of mothers with long-term insulin-dependent diabetes or gestational diabetes, 10.1038/sj.ijo.0800429
  18. Dabelea D, J Pediatr Endocrinol Metab, 14, 1085 (2001)
  19. Van Assche F. A, Long-term consequences for offspring of diabetes during pregnancy, 10.1093/bmb/60.1.173
  20. Van Assche FA, J Perinat Med, 26, 337 (1998)
  21. Silverman B. L., Metzger B. E., Cho N. H., Loeb C. A., Impaired Glucose Tolerance in Adolescent Offspring of Diabetic Mothers: Relationship to fetal hyperinsulinism, 10.2337/diacare.18.5.611
  22. Singh R., Pearson E., Avery P. J., McCarthy M. I., Levy J. C., Hitman G. A., Sampson M., Walker M., Hattersley A. T., Reduced beta cell function in offspring of mothers with young-onset type 2 diabetes, 10.1007/s00125-006-0285-5
  23. Han J., Xu J., Epstein P. N., Liu Y. Qi, Long-term effect of maternal obesity on pancreatic beta cells of offspring: reduced beta cell adaptation to high glucose and high-fat diet challenges in adult female mouse offspring, 10.1007/s00125-005-1854-8
  24. Boney C. M., Metabolic Syndrome in Childhood: Association With Birth Weight, Maternal Obesity, and Gestational Diabetes Mellitus, 10.1542/peds.2004-1808
  25. Laitinen J, Eur J Clin Nutr, 58, 180 (2004)
  26. Lake JK, Arch Dis Child, 77, 376 (1997)
  27. Rogers I, The influence of birthweight and intrauterine environment on adiposity and fat distribution in later life, 10.1038/sj.ijo.0802316
  28. Catalano PM, Ehrenberg HM, Review article: The short- and long-term implications of maternal obesity on the mother and her offspring, 10.1111/j.1471-0528.2006.00989.x
  29. Mcmillen I. C., Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming, 10.1152/physrev.00053.2003
  30. Armitage JA, J Physiol, 561, 355 (2004)
  31. Prentki M., Islet   cell failure in type 2 diabetes, 10.1172/jci29103
  32. Hebrok M, Genes Dev, 12, 1705 (1998)
  33. Lammert Eckhard, Cleaver Ondine, Melton Douglas, Role of endothelial cells in early pancreas and liver development, 10.1016/s0925-4773(02)00332-5
  34. Deutsch G, Development, 128, 871 (2001)
  35. Kim SK, Curr Opin Genet Dev, 12, 540 (2002)
  36. Habener JF, Endocrinology, 146, 1025 (2005)
  37. Murtaugh LC, Development, 134, 427 (2007)
  38. Jacquemin Patrick, Yoshitomi Hideyuki, Kashima Yasushige, Rousseau Guy G., Lemaigre Frederic P., Zaret Kenneth S., An endothelial–mesenchymal relay pathway regulates early phases of pancreas development, 10.1016/j.ydbio.2005.11.023
  39. Scharfmann R., Control of early development of the pancreas in rodents and humans: implications of signals from the mesenchyme, 10.1007/s001250051498
  40. Murtaugh L. Charles, Melton Douglas A., Genes, Signals, and Lineages in Pancreas Development, 10.1146/annurev.cellbio.19.111301.144752
  41. Lammert E., Induction of Pancreatic Differentiation by Signals from Blood Vessels, 10.1126/science.1064344
  42. Herrera PL, Development, 127, 2317 (2000)
  43. Cerf ME, Eur J Endocrinol, 155, 671 (2006)
  44. Kaung Hue-lee Cheng, Growth dynamics of pancreatic islet cell populations during fetal and neonatal development of the rat, 10.1002/aja.1002000208
  45. Nikolova Ganka, Jabs Normund, Konstantinova Irena, Domogatskaya Anna, Tryggvason Karl, Sorokin Lydia, Fässler Reinhard, Gu Guoqiang, Gerber Hans-Peter, Ferrara Napoleone, Melton Douglas A., Lammert Eckhard, The Vascular Basement Membrane: A Niche for Insulin Gene Expression and β Cell Proliferation, 10.1016/j.devcel.2006.01.015
  46. Petrik J., Apoptosis in the Pancreatic Islet Cells of the Neonatal Rat Is Associated with a Reduced Expression of Insulin-Like Growth Factor II that May Act as a Survival Factor, 10.1210/en.139.6.2994
  47. Scaglia L., Apoptosis Participates in the Remodeling of the Endocrine Pancreas in the Neonatal Rat, 10.1210/en.138.4.1736
  48. Dor Yuval, Brown Juliana, Martinez Olga I., Melton Douglas A., Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation, 10.1038/nature02520
  49. Lardon Jessy, Bouwens Luc, Metaplasia in the pancreas, 10.1111/j.1432-0436.2005.00030.x
  50. Stanger BZ, Nature, 445, 886 (2007)
  51. Robinson JS, Fetal Origins of Cardiovascular and Lung Disease, 273 (2001)
  52. Piper K, Beta cell differentiation during early human pancreas development, 10.1677/joe.0.1810011
  53. Snoeck A, Biol Neonate, 57, 107 (1990)
  54. Petrik J., A Low Protein Diet Alters the Balance of Islet Cell Replication and Apoptosis in the Fetal and Neonatal Rat and Is Associated with a Reduced Pancreatic Expression of Insulin-Like Growth Factor-II, 10.1210/en.140.10.4861
  55. Boujendar S., Reusens B., Merezak S., Ahn M.-T., Arany E., Hill D., Remacle C., Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets, 10.1007/s00125-002-0833-6
  56. Joanette EA, Endocrinology, 145, 3004 (2004)
  57. Dahri S., Reusens B., Remacle C., Hoet J. J., Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes, 10.1079/pns19950003
  58. Cherif H, J Nutr, 131, 1555 (2001)
  59. Cherif H, Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet, 10.1677/joe.0.1590341
  60. Sparre T, Diabetologia, 46, 1497 (2003)
  61. Garofano A., Czernichow P., Bréant B., In utero undernutrition impairs rat beta-cell development, 10.1007/s001250050812
  62. Blondeau B, Am J Physiol Endocrinol Metab, 281, E592 (2001)
  63. Bernstein I, Obstetrics: Normal and Problem Pregnancies, 863 (1996)
  64. Boloker J., Gertz S. J., Simmons R. A., Gestational Diabetes Leads to the Development of Diabetes in Adulthood in the Rat, 10.2337/diabetes.51.5.1499
  65. Stoffers D. A., Desai B. M., DeLeon D. D., Simmons R. A., Neonatal Exendin-4 Prevents the Development of Diabetes in the Intrauterine Growth Retarded Rat, 10.2337/diabetes.52.3.734
  66. Holness MJ, Br J Nutr, 81, 481 (1999)
  67. Ozanne SE, Am J Physiol, 273, E46 (1997)
  68. Shepherd Peter R., Navé Barbara T., Rincon Jorge, Nolte Lorraine A., Bevan A. Paul, Siddle Kenneth, Zierath Juleen R., Wallberg-Henriksson Harriet, Differential Regulation of Phosphoinositide 3-Kinase Adapter Subunit Variants by Insulin in Human Skeletal Muscle, 10.1074/jbc.272.30.19000
  69. OZANNE S, HALES C, Early programming of glucose–insulin metabolism, 10.1016/s1043-2760(02)00666-5
  70. Hales C. N., Desai M., Ozanne S. E., Crowther N. J., Fishing in the Stream of Diabetes: From Measuring Insulin to the Control of Fetal Organogenesis, 10.1042/bst0240341
  71. Petry Clive J., Dorling Matthew W., Pawlak Dorota B., Ozanne Susan E., Hales C. Nicholas, Diabetes in Old Male Offspring of Rat Dams Fed a Reduced Protein Diet, 10.1155/edr.2001.139
  72. Reusens B., Goosse K., Kalbe L., Ahn M. T., Tamarit-Rodriguez J., Remacle C., Merezak S., Renard A., Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines, 10.1007/s00125-004-1357-z
  73. Wilson MR, J Endocrinol, 154, 177 (1997)
  74. Bieswal F, Obesity, 14, 1330 (2006)
  75. Garofano A., Czernichow P., Bréant B., Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat, 10.1007/s001250051038
  76. Garofano A., Czernichow P., Bréant B., Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period, 10.1007/s001250051219
  77. Blondeau B., Age-Dependent Inability of the Endocrine Pancreas to Adapt to Pregnancy: A Long-Term Consequence of Perinatal Malnutrition in the Rat, 10.1210/en.140.9.4208
  78. Avril I, J Endocrinol, 174, 215 (2002)
  79. Aerts L, Vercruysse L, Van Assche F.A, The endocrine pancreas in virgin and pregnant offspring of diabetic pregnant rats, 10.1016/s0168-8227(97)00080-6
  80. Sorenson RL, Horm Metab Res, 29, 301 (1997)
  81. Blondeau B., Avril I., Duchene B., Bréant B., Endocrine pancreas development is altered in foetuses from rats previously showing intra-uterine growth retardation in response to malnutrition, 10.1007/s00125-001-0767-4
  82. H. Hyöty, K. Taylor, The role of viruses in human diabetes, 10.1007/s00125-002-0852-3
  83. Dahlquist G., Can we slow the rising incidence of childhood-onset autoimmune diabetes? The overload hypothesis, 10.1007/s00125-005-0076-4
  84. Merezak S, J Endocrinol, 171, 299 (2001)
  85. Goosse KJR, Diabetologia, 49, 266 (2006)
  86. Heasman L., Clarke L., Stephenson T. J., Symonds M. E., The influence of maternal nutrient restriction in early to mid-pregnancy on placental and fetal development in sheep, 10.1017/s0029665199000397
  87. Fowden A L, Forhead A J, Endocrine mechanisms of intrauterine programming, 10.1530/rep.1.00033
  88. SECKL JONATHAN R., MEANEY MICHAEL J., Glucocorticoid Programming, 10.1196/annals.1314.006
  89. Fowden A. L., Ward J. W., Wooding F. P. B., Forhead A. J., Constancia M., Programming placental nutrient transport capacity : Placental transport capacity, 10.1113/jphysiol.2005.104141
  90. de Gasparo M, J Endocrinol, 77, 241 (1978)
  91. Bertin Eric, Gangnerau Marie-Noëlle, Bellon Georges, Bailbé Danièle, Arbelot De Vacqueur Annick, Portha Bernard, Development of β-cell mass in fetuses of rats deprived of protein and/or energy in last trimester of pregnancy, 10.1152/ajpregu.00037.2002
  92. Sturman JA, Physiol Rev, 73, 119 (1993)
  93. Kulkarni Rohit N., New Insights into the Roles of Insulin/IGF-I in the Development and Maintenance of β-Cell Mass, 10.1007/s11154-005-3051-y
  94. Vasavada Rupangi C., Gonzalez-Pertusa Jose A., Fujinaka Yuichi, Fiaschi-Taesch Nathalie, Cozar-Castellano Irene, Garcia-Ocaña Adolfo, Growth factors and beta cell replication, 10.1016/j.biocel.2005.08.003
  95. Hyatt MA, Proc Nutr Soc, 63, 127 (2004)
  96. El Khattabi I, Am J Physiol Endocrinol Metab, 291, E835 (2006)
  97. Fernandez-Twinn D. S., Ozanne S. E., Ekizoglou S., Doherty C., James L., Gusterson B., Hales C. N., The maternal endocrine environment in the low-protein model of intra-uterine growth restriction, 10.1079/bjn2003967
  98. Lesage J., Maternal Undernutrition during Late Gestation Induces Fetal Overexposure to Glucocorticoids and Intrauterine Growth Retardation, and Disturbs the Hypothalamo-Pituitary Adrenal Axis in the Newborn Rat, 10.1210/en.142.5.1692
  99. Langley-Evans S.C., Phillips G.J., Benediktsson R., Gardner D.S., Edwards C.R.W., Jackson A.A., Seckl J.R., Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat, 10.1016/s0143-4004(96)80010-5
  100. Gesina E., Blondeau B., Milet A., Le Nin I., Duchene B., Czernichow P., Scharfmann R., Tronche F., Breant B., Glucocorticoid signalling affects pancreatic development through both direct and indirect effects, 10.1007/s00125-006-0449-3
  101. Gesina E, Diabetes, 53, 2322 (2004)
  102. Dumortier O, Diabetologia, 48, A152 (2005)
  103. Simmons Rebecca A., Suponitsky-Kroyter Irena, Selak Mary A., Progressive Accumulation of Mitochondrial DNA Mutations and Decline in Mitochondrial Function Lead to β-Cell Failure, 10.1074/jbc.m505695200
  104. Puigserver Pere, Spiegelman Bruce M., Peroxisome Proliferator-Activated Receptor-γ Coactivator 1α (PGC-1α): Transcriptional Coactivator and Metabolic Regulator, 10.1210/er.2002-0012
  105. Lee YY, J Nutr Biochem, 16, 195 (2005)
  106. Patti M. E., Butte A. J., Crunkhorn S., Cusi K., Berria R., Kashyap S., Miyazaki Y., Kohane I., Costello M., Saccone R., Landaker E. J., Goldfine A. B., Mun E., DeFronzo R., Finlayson J., Kahn C. R., Mandarino L. J., Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1, 10.1073/pnas.1032913100
  107. Larsson Nils-Göran, Silva José P., Köhler Martin, Graff Caroline, Oldfors Anders, Magnuson Mark A., Berggren Per-Olof, 10.1038/81649
  108. Serradas P., Mitochondrial deoxyribonucleic acid content is specifically decreased in adult, but not fetal, pancreatic islets of the Goto-Kakizaki rat, a genetic model of noninsulin-dependent diabetes, 10.1210/en.136.12.5623
  109. Selak Mary A., Storey Bayard T., Peterside Iyalla, Simmons Rebecca A., Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats, 10.1152/ajpendo.00322.2002
  110. Taylor P. D., Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy, 10.1152/ajpregu.00355.2004
  111. PARK HYEONG KYU, JIN CHENG JI, CHO YOUNG MIN, PARK DO JOON, SHIN CHAN SOO, PARK KYONG SOO, KIM SEONG YEON, CHO BO YOUN, LEE HONG KYU, Changes of Mitochondrial DNA Content in the Male Offspring of Protein-Malnourished Rats, 10.1196/annals.1293.021
  112. Suzuki T., Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases, 10.1093/emboj/cdf656
  113. Tiedge M., Lortz S., Drinkgern J., Lenzen S., Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells, 10.2337/diabetes.46.11.1733
  114. Robertson R. Paul, Chronic Oxidative Stress as a Central Mechanism for Glucose Toxicity in Pancreatic Islet Beta Cells in Diabetes, 10.1074/jbc.r400019200
  115. Luedi P. P., Genome-wide prediction of imprinted murine genes, 10.1101/gr.3303505
  116. D?Alessio AC, Biochem Cell Biol, 84, 463 (2006)
  117. Waterland Robert A., Lin Juan-Ru, Smith Charlotte A., Jirtle Randy L., Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus, 10.1093/hmg/ddi484
Bibliographic reference Remacle, Claude ; Dumortier, O ; Bol, Vanesa ; Goosse, K ; Romanus, Pierre ; et. al. Intrauterine programming of the endocrine pancreas.. In: Diabetes, obesity & metabolism, Vol. 9 Suppl 2, p. 196-209 (2007)
Permanent URL http://hdl.handle.net/2078.1/23100