Cited by 154Pancreatic function and diabetesBirth, Development, and HealthDiabetes and associated disorders

The DOI matches its Crossref record; 63 of the 63 references it cites were found in a registry or an index.

Diminished β-cell replication contributes to reduced β-cell mass in fetal sheep with intrauterine growth restriction

Limesand, Sean W., Jensen, Jan, Hutton, John C., Hay, William W.·2005·American Journal of Physiology-Regulatory, Integrative and Comparative Physiology

DOI 10.1152/ajpregu.00494.2004

Open this paper in CoChat — free account

Abstract

Human fetuses with severe intrauterine growth restriction (IUGR) have less pancreatic endocrine tissue and exhibit β-cell dysfunction, which may limit β-cell function in later life and contribute to their increased incidence of noninsulin-dependent diabetes mellitus. Three factors, replication, apoptosis, and neoformation, contribute to fetal β-cell mass. We studied an ovine model of IUGR to understand whether nutrient deficits lead to decreased rates of fetal pancreatic β-cell replication, increased rates of apoptosis, or lower rates of differentiation. At 90% of term gestation, IUGR fetal and pancreatic weights were 58% and 59% less than pair-fed control, respectively. We identified a selective impairment of β-cell mass compared with other pancreatic cell types in IUGR fetuses. Insulin and insulin mRNA contents were less than other pancreatic endocrine hormones in IUGR fetuses, as were pancreatic insulin positive area (42%) and β-cell mass (76%). Pancreatic β-cell apoptosis was not different between treatments. β-cell capacity for cell cycling, determined by proliferating cell nuclear antigen (PCNA) immunostaining, was not different between treatment groups. However, the percentage of β-cells actually undergoing mitosis was 72% lower in IUGR fetuses. These results indicate that in utero nutrient deficits decrease the population of pancreatic β-cells by lengthening G1, S, and G2 stages of interphase and decreasing mitosis near term. Diminished β-cell mass in IUGR infants at birth, if not adequately compensated for after birth, may contribute to insufficient insulin production in later life and, thus, a predisposition to noninsulin-dependent diabetes.

Integrity signals

Registry

Crossref · 10.1152/ajpregu.00494.2004

Cites

63 of 63 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Fetal and infant growth and impaired glucose tolerance at age 64
Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., & Winter, P. D. (1991) · BMJ · doi:10.1136/bmj.303.6809.1019 · Cited by 2,708
Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation
Hendzel, M. J., Wei, Y., Mancini, M. A., Hooser, A. A. V., Ranalli, T. A., Brinkley, B. R., Bazett‐Jones, D. P., & Allis, C. D. (1997) · Chromosoma · doi:10.1007/s004120050256 · Cited by 1,860
Cyclin/PCNA is the auxiliary protein of DNA polymerase-δ
Bravo, R., Frank, R. W., Blundell, P. A., & Macdonald-Bravo, H. (1987) · Nature · doi:10.1038/326515a0 · Cited by 1,740
Intrauterine growth restriction
Resnik, R. (2002) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(01)01780-x · Cited by 1,022
β-Cell-specific inactivation of the mouseIpf1/Pdx1 gene results in loss of the β-cell phenotype and maturity onset diabetesPreprint
Ahlgren, U., Jönsson, J., Jönsson, L., Simu, K., & Edlund, H. (1998) · Genes & Development · doi:10.1101/gad.12.12.1763 · Cited by 918
Early-onset type-ll diabetes mellitus (MODY4) linked to IPF1
Staffers, D. A., Ferrer, J. P., Clarke, W. L., & Habener, J. F. (1997) · Nature Genetics · doi:10.1038/ng1097-138 · Cited by 880
Phosphorylation of Histone H3 Is Required for Proper Chromosome Condensation and Segregation
Wei, Y., Yu, L., Bowen, J. K., Gorovsky, M. A., & Allis, C. D. (1999) · Cell · doi:10.1016/s0092-8674(00)80718-7 · Cited by 719
Effect of a Low Protein Diet during Pregnancy on the Fetal Rat Endocrine Pancreas
Snoeck, A., Remacle, C., Reusens, B., & Hoet, J. J. (2009) · Biology of the Neonate · doi:10.1159/000243170 · Cited by 652
Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat
Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2279 · Cited by 638 · cited 1×
“In rat models of fetal growth restriction, deficits in insulin secretion capacity, as well as decreased -cell mass, have been observed in the adult animal (14, 52), although such long-term consequences also were dependent on early postnatal nutritional experiences (18).”
Background
Banting lecture 1990. Beta-cells in type II diabetes mellitus
Porte, D. (1991) · Diabetes · doi:10.2337/diab.40.2.166 · Cited by 599

Show all 62 references

Research works printed but not linked: 1

SAS Institute. SAS/STAT User's Guide (8th ed.). Cary, NC: SAS Institute, 1999.

Sorted by citations

Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717
The fetal brain sparing response to hypoxia: physiological mechanisms
Giussani, D. A. (2015) · The Journal of Physiology · doi:10.1113/jp271099 · Cited by 402
Invited review: Heat stress effects during late gestation on dry cows and their calves
Tao, S., & Dahl, G. E. (2013) · Journal of Dairy Science · doi:10.3168/jds.2012-6278 · Cited by 342
Placental-fetal glucose exchange and fetal glucose metabolism.
(2006) · Europe PMC (PubMed Central) · Cited by 226
Self-citation
Attenuated Insulin Release and Storage in Fetal Sheep Pancreatic Islets with Intrauterine Growth Restriction
Limesand, S. W., Rozance, P. J., Zerbe, G. O., Hutton, J. C., & Hay, W. W. (2005) · Endocrinology · doi:10.1210/en.2005-0900 · Cited by 214
Self-citation
Intrauterine growth restriction decreases pulmonary alveolar and vessel growth and causes pulmonary artery endothelial cell dysfunction in vitro in fetal sheep
Rozance, P. J., Seedorf, G., Brown, A., Roe, G. B., O'Meara, M. C., Gien, J., Tang, J., & Abman, S. H. (2011) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00197.2011 · Cited by 200
Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction
Limesand, S. W., Rozance, P. J., Smith, D. M., & Hay, W. W. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00459.2007 · Cited by 190
Self-citation
Maternal obesity accelerates fetal pancreatic β-cell but not α-cell development in sheep: prenatal consequences
Ford, S. P., Zhang, L., Zhu, M. J., Miller, M. M., Smith, D. T., Hess, B. W., Moss, G. E., Nathanielsz, P. W., & Nijland, M. J. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00072.2009 · Cited by 179
The Intrauterine Growth Restriction Phenotype: Fetal Adaptations and Potential Implications for Later Life Insulin Resistance and Diabetes
Thorn, S., Rozance, P., Brown, L., & Hay, W. (2011) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1275516 · Cited by 153
Self-citation
Hypoglycemia and the Origin of Hypoxia-Induced Reduction in Human Fetal Growth
Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008551 · Cited by 141
Developmental Origins of Adult Disease
Simmons, R. A. (2009) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2009.03.004 · Cited by 121
Describing hypoglycemia — Definition or operational threshold?
Rozance, P. J., & Hay, W. W. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2010.05.002 · Cited by 118
Self-citation
Recent observations on the regulation of fetal metabolism by glucose
Hay, W. W. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.105072 · Cited by 116
Self-citation
Intrauterine Growth Restriction: Hungry for an Answer
Devaskar, S. U., & Chu, A. (2016) · Physiology · doi:10.1152/physiol.00033.2015 · Cited by 117
Global gene expression profiling and histochemical analysis of the developing human fetal pancreas
Sarkar, S. A., Kobberup, S., Wong, R., Lopez, A. D., Quayum, N., Still, T., Kutchma, A. J., Jensen, J. N., Gianani, R., Beattie, G. M., et al. (2007) · Diabetologia · doi:10.1007/s00125-007-0880-0 · Cited by 103
Self-citation
Epigenetics and maternal nutrition: nature v. nurture
Simmons, R. A. (2010) · Proceedings of The Nutrition Society · doi:10.1017/s0029665110003988 · Cited by 109
Consequences of a compromised intrauterine environment on islet function
Green, A. S., Rozance, P. J., & Limesand, S. W. (2010) · Journal of Endocrinology · doi:10.1677/joe-09-0399 · Cited by 103
Self-citation
Chronic exposure to elevated norepinephrine suppresses insulin secretion in fetal sheep with placental insufficiency and intrauterine growth restriction
Leos, R. A., Anderson, M. J., Chen, X., Pugmire, J., Anderson, K. A., & Limesand, S. W. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00494.2009 · Cited by 99
Self-citation
One process for pancreatic β-cell coalescence into islets involves an epithelial–mesenchymal transition
Cole, L., Anderson, M. J., Antin, P. B., & Limesand, S. W. (2009) · Journal of Endocrinology · doi:10.1677/joe-09-0072 · Cited by 96
Self-citation
An Animal Model of Placental Insufficiency-Induced Intrauterine Growth Restriction
Barry, J. S., Rozance, P. J., & Anthony, R. V. (2008) · Seminars in Perinatology · doi:10.1053/j.semperi.2007.11.004 · Cited by 90
Oxidative Stress, Intrauterine Growth Restriction, and Developmental Programming of Type 2 Diabetes
Rashid, C. S., Bansal, A., & Simmons, R. A. (2018) · Physiology · doi:10.1152/physiol.00023.2018 · Cited by 84
Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring
Thamotharan, M., Garg, M., Oak, S. A., Rogers, L. M., Pan, G., Sangiorgi, F. O., Lee, P. W. N., & Devaskar, S. U. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00462.2006 · Cited by 86
The impact of IUGR on pancreatic islet development and β-cell function
Boehmer, B. H., Limesand, S. W., & Rozance, P. J. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0076 · Cited by 86
Self-citation
Perinatal Circulating Visfatin Levels in Intrauterine Growth Restriction
Malamitsi‐Puchner, A., Briana, D. D., Boutsikou, M., Kouskouni, E. E., Hassiakos, D., & Gourgiotis, D. (2007) · PEDIATRICS · doi:10.1542/peds.2006-2589 · Cited by 78
Impaired β-Cell Function and Inadequate Compensatory Increases in β-Cell Mass after Intrauterine Growth Restriction in Sheep
Gatford, K. L., Mohammad, S. N. B., Harland, M. L., Blasio, M. J. D., Fowden, A. L., Robinson, J. S., & Owens, J. A. (2008) · Endocrinology · doi:10.1210/en.2008-0233 · Cited by 72
Gα i/o -coupled receptor signaling restricts pancreatic β-cell expansion
Berger, M., Scheel, D. W., Macias, H., Miyatsuka, T., Kim, H., Hoang, P. T., Ku, G. M., Honig, G., Liou, A., Tang, Y., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319378112 · Cited by 68
Impact of thermal stress on placental function and fetal physiology
Limesand, S. W., Camacho, L. E., Kelly, A. C., & Antolic, A. T. (2018) · Animal Reproduction · doi:10.21451/1984-3143-ar2018-0056 · Cited by 66
Self-citation
Review: Placental Programming of Postnatal Diabetes and Impaired Insulin Action after IUGR
Gatford, K. L., Simmons, R. A., Blasio, M. J. D., Robinson, J. S., & Owens, J. A. (2010) · Placenta · doi:10.1016/j.placenta.2009.12.015 · Cited by 70
The bovine mammary gland expresses multiple functional isoforms of serotonin receptors
Hernandez, L. L., Limesand, S. W., Collier, J. L., Horseman, N. D., & Collier, R. J. (2009) · Journal of Endocrinology · doi:10.1677/joe-09-0187 · Cited by 64
Self-citation
Reductions in insulin concentrations and β-cell mass precede growth restriction in sheep fetuses with placental insufficiency
Limesand, S. W., Rozance, P. J., Macko, A. R., Anderson, M. J., Kelly, A. C., & Hay, W. W. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00435.2012 · Cited by 63
Self-citation
Catecholamines Mediate Multiple Fetal Adaptations during Placental Insufficiency That Contribute to Intrauterine Growth Restriction: Lessons from Hyperthermic Sheep
Yates, D. T., Green, A. S., & Limesand, S. W. (2011) · Journal of Pregnancy · doi:10.1155/2011/740408 · Cited by 62
Self-citation
New approaches to management of neonatal hypoglycemia
Rozance, P. J., & Hay, W. W. (2016) · Maternal Health Neonatology and Perinatology · doi:10.1186/s40748-016-0031-z · Cited by 61
Self-citation
Restriction of placental growth in sheep impairs insulin secretion but not sensitivity before birth
Owens, J., Gatford, K. L., Blasio, M. D., Edwards, L., McMillen, I., & Fowden, A. L. (2007) · Journal of Physiology · doi:10.1113/jphysiol.2007.142141 · Cited by 64
Short-term exercise training early in life restores deficits in pancreatic β-cell mass associated with growth restriction in adult male rats
Laker, R. C., Gallo, L. A., Wlodek, M. E., Siebel, A. L., Wadley, G. D., & McConell, G. K. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00114.2011 · Cited by 57
ALPHARMA BEEF CATTLE NUTRITION SYMPOSIUM: Implications of nutritional management for beef cow-calf systems1
Funston, R. N., Summers, A. F., & Roberts, A. J. (2011) · Journal of Animal Science · doi:10.2527/jas.2011-4568 · Cited by 55
Maternal exposure to Δ9-tetrahydrocannabinol impairs female offspring glucose homeostasis and endocrine pancreatic development in the rat
Gillies, R., Lee, K., Vanin, S., Laviolette, S. R., Holloway, A. C., Arany, E. J., & Hardy, D. B. (2020) · Reproductive Toxicology · doi:10.1016/j.reprotox.2020.04.070 · Cited by 58
Nutrition During Pregnancy and the Effect of Carbohydrates on the Offspring’s Metabolic Profile: In Search of the “Perfect Maternal Diet”
Tzanetakou, I. P., Mikhailidis, D. P., & Perrea, D. N. (2011) · The Open Cardiovascular Medicine Journal · doi:10.2174/1874192401105010103 · Cited by 54
Enhanced insulin secretion and insulin sensitivity in young lambs with placental insufficiency-induced intrauterine growth restriction
Camacho, L. E., Chen, X., Hay, W. W., & Limesand, S. W. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00068.2017 · Cited by 51
Self-citation
SGA Children with Moderate Catch-Up Growth Are Showing the Impaired Insulin Secretion at the Age of 4
Milovanovic, I., Njuieyon, F., Deghmoun, S., Chevenne, D., Lévy‐Marchal, C., & Beltrand, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100337 · Cited by 54
Fetal growth factors and fetal nutrition
Bloomfield, F. H., Spiroski, A., & Harding, J. E. (2013) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2013.03.003 · Cited by 53
Elevated plasma norepinephrine inhibits insulin secretion, but adrenergic blockade reveals enhanced β-cell responsiveness in an ovine model of placental insufficiency at 0.7 of gestation
Macko, A. R., Yates, D. T., Chen, X., Green, A. S., Kelly, A. C., Brown, L. D., & Limesand, S. W. (2013) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174413000093 · Cited by 49
Self-citation
Fetal undernutrition, placental insufficiency, and pancreatic β-cell development programming in utero
Mohan, R., Baumann, D. C., & Alejandro, E. U. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00072.2018 · Cited by 49
Hypoxaemia‐induced catecholamine secretion from adrenal chromaffin cells inhibits glucose‐stimulated hyperinsulinaemia in fetal sheep
Yates, D. T., Macko, A. R., Chen, X., Green, A. S., Kelly, A. C., Anderson, M. J., Fowden, A. L., & Limesand, S. W. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.237347 · Cited by 47
Self-citation
Placenta-specific Slc38a2 /SNAT2 knockdown causes fetal growth restriction in mice
Vaughan, O. R., Maksym, K., Silva, E., Barentsen, K., Anthony, R. V., Brown, T. L., Hillman, S. L., Spencer, R. N., David, A. L., Rosario, F. J., et al. (2021) · Clinical Science · doi:10.1042/cs20210575 · Cited by 48
Enhanced insulin secretion responsiveness and islet adrenergic desensitization after chronic norepinephrine suppression is discontinued in fetal sheep
Chen, X., Green, A. S., Macko, A. R., Yates, D. T., Kelly, A. C., & Limesand, S. W. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00517.2013 · Cited by 46
Self-citation
Late gestation undernutrition can predispose for visceral adiposity by altering fat distribution patterns and increasing the preference for a high-fat diet in early postnatal life
Nielsen, M. O., Kongsted, A. H., Thygesen, M. P., Strathe, A. B., Caddy, S., Quistorff, B., Jørgensen, W., Christensen, V. G., Husted, S., Chwalibog, A., et al. (2013) · British Journal of Nutrition · doi:10.1017/s0007114512004199 · Cited by 46
Placental Insufficiency Decreases Pancreatic Vascularity and Disrupts Hepatocyte Growth Factor Signaling in the Pancreatic Islet Endothelial Cell in Fetal Sheep
Rozance, P. J., Anderson, M., Martinez, M., Fahy, A., Macko, A. R., Kailey, J., Seedorf, G. J., Abman, S. H., Hay, W. W., & Limesand, S. W. (2015) · Diabetes · doi:10.2337/db14-0462 · Cited by 45
Self-citation
Prenatal programming of postnatal productivity and health of livestock: a brief review
Bell, A. W. (2006) · Australian Journal of Experimental Agriculture · doi:10.1071/ea06006 · Cited by 45
Prenatal Programming of Insulin Secretion in Intrauterine Growth Restriction
Gatford, K. L., & Simmons, R. A. (2013) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e31829e5b29 · Cited by 47
ASAS-SSR Triennnial Reproduction Symposium: Looking Back and Moving Forward—How Reproductive Physiology has Evolved: Fetal origins of impaired muscle growth and metabolic dysfunction: Lessons from the heat-stressed pregnant ewe1
Yates, D. T., Petersen, J. L., Schmidt, T. B., Cadaret, C. N., Barnes, T. L., Posont, R. J., & Beede, K. A. (2018) · Journal of Animal Science · doi:10.1093/jas/sky164 · Cited by 43
Chronic anemic hypoxemia attenuates glucose-stimulated insulin secretion in fetal sheep.
Benjamin, J. S., Culpepper, C., Brown, L., Wesolowski, S. R., Jonker, S., Davis, M. A., Limesand, S., Wilkening, R., Hay, W., & Rozance, P. (2017) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00484.2016 · Cited by 36
Self-citation
Glucose Replacement to Euglycemia Causes Hypoxia, Acidosis, and Decreased Insulin Secretion in Fetal Sheep With Intrauterine Growth Restriction
Rozance, P. J., Limesand, S. W., Barry, J. S., Brown, L. D., & Hay, W. W. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e318189358c · Cited by 41
Self-citation
Role of metabolic programming in the pathogenesis of β-cell failure in postnatal life
Simmons, R. A. (2007) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-007-9045-1 · Cited by 43
AMPK as Target for Intervention in Childhood and Adolescent Obesity
Rojas, J., Arráiz, N., Aguirre, M., Velasco, M., & Bermúdez, V. (2010) · Journal of Obesity · doi:10.1155/2011/252817 · Cited by 40
Characterization of glucose-insulin responsiveness and impact of fetal number and sex difference on insulin response in the sheep fetus
Green, A. S., Macko, A. R., Rozance, P. J., Yates, D. T., Chen, X., Hay, W. W., & Limesand, S. W. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00572.2010 · Cited by 38
Self-citation
Chronically Increased Amino Acids Improve Insulin Secretion, Pancreatic Vascularity, and Islet Size in Growth-Restricted Fetal Sheep
Brown, L. D., Davis, M. A., Wai, S., Wesolowski, S. R., Hay, W. W., Limesand, S. W., & Rozance, P. J. (2016) · Endocrinology · doi:10.1210/en.2016-1328 · Cited by 38
Self-citation
Early postnatal nutritional requirements of the very preterm infant based on a presentation at the NICHD-AAP workshop on research in neonatology
Hay, W. W. (2006) · Journal of Perinatology · doi:10.1038/sj.jp.7211426 · Cited by 37
Self-citation
RNA Sequencing Exposes Adaptive and Immune Responses to Intrauterine Growth Restriction in Fetal Sheep Islets
Kelly, A. C., Bidwell, C. A., McCarthy, F., Taska, D. J., Anderson, M. J., Camacho, L. E., & Limesand, S. W. (2017) · Endocrinology · doi:10.1210/en.2016-1901 · Cited by 36
Self-citation
Sensitivity to metabolic signals in late-gestation growth-restricted fetuses from rapidly growing adolescent sheep
Wallace, J. M., Milne, J. S., Aitken, R. P., & Hay, W. W. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00294.2007 · Cited by 36
Self-citation
Insulin and carbohydrate metabolism
Beardsall, K., Diderholm, B., & Dunger, D. B. (2008) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2007.10.001 · Cited by 35
Chronic fetal hypoglycemia inhibits the later steps of stimulus-secretion coupling in pancreatic β-cells
Rozance, P. J., Limesand, S. W., Zerbe, G. O., & Hay, W. W. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00265.2006 · Cited by 34
Self-citation
Increased amino acid supply potentiates glucose-stimulated insulin secretion but does not increase β-cell mass in fetal sheep
Gadhia, M. M., Maliszewski, A. M., O'Meara, M. C., Wesolowski, S. R., Lavezzi, J. R., Limesand, S. W., Hay, W. W., Brown, L. D., & Rozance, P. J. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00377.2012 · Cited by 33
Self-citation
The tissue and plasma concentration of polyols and sugars in sheep intrauterine growth retardation
Regnault, T. R. H., Teng, C. C., de Vrijer, B., Galan, H. L., Wilkening, R. B., & Battaglia, F. C. (2010) · Experimental Biology and Medicine · doi:10.1258/ebm.2010.009360 · Cited by 31
Programming of glucose–insulin homoeostasis: long‐term consequences of pre‐natal versus early post‐natal nutrition insults. Evidence from a sheep model
Kongsted, A. H., Tygesen, M. P., Husted, S., Oliver, M. H., Tolver, A., Christensen, V. G., Nielsen, J. H., & Nielsen, M. O. (2013) · Acta Physiologica · doi:10.1111/apha.12080 · Cited by 31
Fetal Adrenal Demedullation Lowers Circulating Norepinephrine and Attenuates Growth Restriction but not Reduction of Endocrine Cell Mass in an Ovine Model of Intrauterine Growth Restriction
Davis, M. A., Macko, A. R., Steyn, L. V., Anderson, M. J., & Limesand, S. W. (2015) · Nutrients · doi:10.3390/nu7010500 · Cited by 30
Self-citation
Hypothyroidism in utero stimulates pancreatic beta cell proliferation and hyperinsulinaemia in the ovine fetus during late gestation
Harris, S., Blasio, M. J. D., Davis, M. A., Kelly, A. C., Davenport, H. M., Wooding, F. B. P., Blache, D., Meredith, D., Anderson, M. J., Fowden, A. L., et al. (2017) · The Journal of Physiology · doi:10.1113/jp273555 · Cited by 30
Self-citation
Global Liver Proteome Analysis Using iTRAQ Reveals AMPK–mTOR–Autophagy Signaling Is Altered by Intrauterine Growth Restriction in Newborn Piglets
Long, B., Yin, C., Fan, Q., Yan, G., Wang, Z., Li, X., Chen, C., Yang, X., Liu, L., Zheng, Z., et al. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00001 · Cited by 29
Maternal nutritional status modifies heat-associated growth restriction in women with chronic malnutrition
Shankar, K., Ali, S. A., Ruebel, M. L., Jessani, S., Borengasser, S. J., Gilley, S. P., Jambal, P., Yazza, D. N., Weaver, N. E., Kemp, J. F., et al. (2023) · PNAS Nexus · doi:10.1093/pnasnexus/pgac309 · Cited by 32
Glucocorticoid-Induced Preterm Birth and Neonatal Hyperglycemia Alter Ovine β-Cell Development
Bansal, A., Bloomfield, F. H., Connor, K. L., Dragunow, M., Thorstensen, E. B., Oliver, M. H., Sloboda, D. M., Harding, J. E., & Alsweiler, J. M. (2015) · Endocrinology · doi:10.1210/en.2015-1095 · Cited by 30
Insulin-like growth factor and fibroblast growth factor expression profiles in growth-restricted fetal sheep pancreas
Chen, X., Rozance, P. J., Hay, W. W., & Limesand, S. W. (2012) · Experimental Biology and Medicine · doi:10.1258/ebm.2012.011375 · Cited by 28
Self-citation
Challenges in nourishing the intrauterine growth‐restricted foetus – Lessons learned from studies in the intrauterine growth‐restricted foetal sheep
Hay, W. W., Brown, L. D., Rozance, P. J., Wesolowski, S. R., & Limesand, S. W. (2016) · Acta Paediatrica · doi:10.1111/apa.13413 · Cited by 29
Self-citation
Increased Adrenergic Signaling Is Responsible for Decreased Glucose-Stimulated Insulin Secretion in the Chronically Hyperinsulinemic Ovine Fetus
Andrews, S. E., Brown, L. D., Wesolowski, S. R., Limesand, S. W., Davis, M. A., Hay, W. W., & Rozance, P. J. (2014) · Endocrinology · doi:10.1210/en.2014-1393 · Cited by 26
Self-citation
Gender-specific modulation of tumorigenesis by folic acid supply in theApc+/Minmouse during early neonatal life
McKay, J. A., Williams, E. A., & Mathers, J. C. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507819131 · Cited by 25
Glucose metabolic adaptations in the intrauterine growth-restricted adult female rat offspring.
Garg, M., Thamotharan, M., Rogers, L., Bassilian, S., Lee, W. P., & Devaskar, S. (2006) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00474.2005 · Cited by 22
Genes Involved in the Thermal Tolerance of Livestock
Collier, R. J., Gebremedhin, K. G., Macko, A. R., & Roy, K. S. (2012) · Springer eBooks · doi:10.1007/978-3-642-29205-7_14 · Cited by 27
American Pediatric Society Presidential Address 2008: Research in Early Life - Benefit and Promise
Hay, W. W. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e31818c7feb · Cited by 25
Self-citation
The Hexosamine Biosynthesis Pathway Is Essential for Pancreatic Beta Cell Development
Filhoulaud, G., Guillemain, G., & Scharfmann, R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.025288 · Cited by 27
Early exposure of the pregestational intrauterine and postnatal growth-restricted female offspring to a peroxisome proliferator-activated receptor-γ agonist
Garg, M., Thamotharan, M., Pan, G., Lee, P. W. N., & Devaskar, S. U. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00361.2009 · Cited by 22
The Ontogeny of the Endocrine Pancreas in the Fetal/Newborn Baboon
Quinn, A. R., Blanco, C., Perego, C., Finzi, G., Rosa, S. L., Capella, C., Guardado-Mendoza, R., Casiraghi, F., Gastaldelli, A., Johnson, M. C., et al. (2012) · Journal of Endocrinology · doi:10.1530/joe-12-0070 · Cited by 23
Exercise as an intervention to improve metabolic outcomes after intrauterine growth restriction
Gatford, K. L., Kaur, G., Falcão‐Tebas, F., Wadley, G. D., Wlodek, M. E., Laker, R. C., Ebeling, P. R., & McConell, G. K. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00456.2013 · Cited by 22
Neonatal Exendin-4 Reduces Growth, Fat Deposition and Glucose Tolerance during Treatment in the Intrauterine Growth-Restricted Lamb
Gatford, K. L., Sulaiman, S. A., Mohammad, S. N. B., Blasio, M. J. D., Harland, M. L., Simmons, R. A., & Owens, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056553 · Cited by 22
Effects of realimentation after nutrient restriction during mid‐ to late gestation on pancreatic digestive enzymes, serum insulin and glucose levels, and insulin‐containing cell cluster morphology
Keomanivong, F. E., Camacho, L. E., Lemley, C. O., Kuemper, E. A., Yunusova, R. D., Borowicz, P. P., Kirsch, J. D. D., Vonnahme, K. A., Caton, J. S., & Swanson, K. C. (2016) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.12480 · Cited by 22
Increased IRS-2 content and activation of IGF-I pathway contribute to enhance β-cell mass in fetuses from undernourished pregnant rats
Fernández‐Millán, E., Martín, M. Á., Fajardo, S., Escrivá, F., & Álvarez, C. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00283.2006 · Cited by 22
Reduced uterine perfusion pressure causes loss of pancreatic β-cell area but normal function in fetal rat offspring
Akhaphong, B., Lockridge, A. D., Jo, S., Mohan, R., Wilcox, J. A., Wing, C. R., Regal, J. F., & Alejandro, E. U. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00458.2017 · Cited by 21
Validation of different replication markers for the detection of beta-cell proliferation in human pancreatic tissue
Köhler, C. U., Kreuter, A., Rozynkowski, M., Rahmel, T., Uhl, W. H., Tannapfel, A., Schmidt, W. E., & Meier, J. J. (2010) · Regulatory Peptides · doi:10.1016/j.regpep.2009.12.021 · Cited by 22
Transcriptomic Analysis Reveals Novel Mechanisms Mediating Islet Dysfunction in the Intrauterine Growth–Restricted Rat
Rashid, C. S., Lien, Y., Bansal, A., Santos, L. J. J., Li, C., Won, K., & Simmons, R. A. (2018) · Endocrinology · doi:10.1210/en.2017-00888 · Cited by 20
The role of ghrelin, leptin and insulin in foetal development
Warchoł, M., Krauss, H., Wojciechowska, M., Opala, T., Pięta, B., Żukiewicz-Sobczak, W. A., Kupsz, J., & Grochowalska, A. (2014) · Annals of Agricultural and Environmental Medicine · doi:10.5604/1232-1966.1108603 · Cited by 18
Effects of a direct-fed microbial on digestive-tract morphology of Holstein bull calves and performance and carcass characteristics of Holstein steers
Dick, K. J., Duff, G. C., Limesand, S. W., Cuneo, S. P., Knudson, D. K., McMurphy, C. P., Hall, L. W., Bernal-Rigoli, J. C., & Marchello, J. A. (2013) · The Professional Animal Scientist · doi:10.15232/s1080-7446(15)30208-4 · Cited by 18
Self-citation
Liver transcriptome profiling and functional analysis of intrauterine growth restriction (IUGR) piglets reveals a genetic correction and sexual-dimorphic gene expression during postnatal development
Gao, H., Zhang, L., Wang, L., Liu, X., Hou, X., Zhao, F., Yan, H., & Wang, L. (2020) · BMC Genomics · doi:10.1186/s12864-020-07094-9 · Cited by 18
Nutrient Supplies for Optimal Health in Preterm Infants
Hay, W. W. (2007) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.mpg.0000302965.93546.b8 · Cited by 18
Self-citation
Evaluation of cord blood irisin levels in term newborns with small gestational age and appropriate gestational age
Keleş, E., & Turan, F. (2016) · SpringerPlus · doi:10.1186/s40064-016-2869-y · Cited by 17
Long-Term Metabolic Consequences of Intrauterine Growth Restriction
Joung, K. E., Lee, J., & Kim, J. H. (2020) · Current Pediatrics Reports · doi:10.1007/s40124-020-00212-x · Cited by 18
Fetal Requirements and Placental Transfer of Nitrogenous Compounds
Brown, L. D., Regnault, T. R. H., & Hay, W. W. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-35214-7.00045-7 · Cited by 16
Self-citation
Differential Effects of Chronic Pulsatile versus Chronic Constant Maternal Hyperglycemia on Fetal Pancreaticβ-Cells
Frost, M. S., Zehri, A. H., Limesand, S. W., Hay, W. W., & Rozance, P. J. (2012) · Journal of Pregnancy · doi:10.1155/2012/812094 · Cited by 14
Self-citation
Pancreatic islet hepatocyte growth factor and vascular endothelial growth factor A signaling in growth restricted fetuses
Rozance, P. J., & Hay, W. W. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.01.025 · Cited by 14
Self-citation
Increased fetal myocardial sensitivity to insulin-stimulated glucose metabolism during ovine fetal growth restriction
Barry, J. S., Rozance, P. J., Brown, L. D., Anthony, R. V., Thornburg, K. L. R., & Hay, W. W. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216632621 · Cited by 14
Self-citation
Fetal programming under maternal heat stress: a focus on skeletal muscle growth and nutrition in livestock
Zhao, W., Luna-Ramirez, R. I., Rhoads, R. P., Brown, L. D., & Limesand, S. W. (2025) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174425100111 · Cited by 13
Self-citation
Integrative Analysis of Liver Metabolomics and Transcriptomics Reveals Oxidative Stress in Piglets with Intrauterine Growth Restriction
Gao, H., Chen, X., Zhao, J., Xue, Z., Zhang, L., Zhao, F., Wang, B., & Wang, L. (2022) · Biology · doi:10.3390/biology11101430 · Cited by 14
Dousing the flame: reviewing the mechanisms of inflammatory programming during stress-induced intrauterine growth restriction and the potential for ω-3 polyunsaturated fatty acid intervention
White, M. R., & Yates, D. T. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1250134 · Cited by 15
A Chronic Fetal Leucine Infusion Potentiates Fetal Insulin Secretion and Increases Pancreatic Islet Size, Vascularity, and β Cells in Late-Gestation Sheep
Boehmer, B. H., Brown, L. D., Wesolowski, S. R., Hay, W. W., & Rozance, P. J. (2020) · Journal of Nutrition · doi:10.1093/jn/nxaa138 · Cited by 13
Self-citation

Authors: Limesand, S. W., Jensen, J., Hutton, J. C., & Hay, W. W.
Affiliations: University of Colorado Health (US)
University of Colorado Denver (US)
University of Colorado Anschutz (US)
ORCID: Limesand, Sean W.
Jensen, Jan
Hay, William W.
Venue: American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
Publisher: American Physiological Society
Published: 2005-05
Volume: 288
Issue: 5
Pages: R1297-R1305
ISSN: 0363-6119 (ISSN-L)
1522-1490
DOI: 10.1152/ajpregu.00494.2004
OpenAlex: W2105434442
Cited by: 153
References: 62
Citations by year: 2026: 4 · 2025: 5 · 2024: 4 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 6 · 2019: 3 · 2018: 9 · 2017: 7 · 2016: 13 · 2015: 6 · 2014: 6 · 2013: 10 · 2012: 11
FWCI: 7.00
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (DK-60300, F32DK060300, P30DK057516, P30 DK 57516, K01DK067393, DK-067393)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-42815, HD20761)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
Keywords: fetal growth restriction, beta-cell proliferation, beta-cell mass, fetal sheep, pancreatic beta cells, beta-cell apoptosis, cell cycle, mitosis, proliferating cell nuclear antigen, insulin, type 2 diabetes risk, nutritional deficiency, pancreatic development
MeSH terms: Animals, Cell Differentiation, Female, Fetal Growth Retardation, Fetus, Islets of Langerhans, Mitosis, Organ Size, Placental Insufficiency, Pregnancy, Sheep, Apoptosis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Diminished β-cell replication contributes to reduced β-cell mass in fetal sheep with intrauterine growth restriction

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks