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.

doi:10.1152/ajpregu.00494.2004

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

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

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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.

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A growth-restricted fetus has fewer insulin-producing beta cells and reduced vascularization in the pancreas, and compromised structure and maturation of the brain, lungs, and liver.
“In addition, the pancreas has fewer insulin-producing beta cells and reduced vascularization (159, 340, 473), and the structure and maturation of the brain (142), lungs (358, 359, 424, 460) and liver (209, 474) are compromised.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [340]

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 · see citing works
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 · see citing works
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 · see citing works
Intrauterine growth restriction
Resnik, R. (2002) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(01)01780-x · Cited by 1,022 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
β-cells in type II diabetes mellitus
Porte, D. (1991) · Diabetes · doi:10.2337/diab.40.2.166 · Cited by 585 · see citing works
Adaptation of Islets of Langerhans to Pregnancy: β-Cell Growth, Enhanced Insulin Secretion and the Role of Lactogenic Hormones
Sorenson, R., & Brelje, T. (1997) · Hormone and Metabolic Research · doi:10.1055/s-2007-979040 · Cited by 531 · see citing works
Maternal-Fetal Medicine
(2020) · American Academy of Pediatrics eBooks · doi:10.1542/9781610023993-2-ch27 · Cited by 482 · see citing works
Is birth weight related to later glucose and insulin metabolism?—a systematic review
Newsome, C., Shiell, A. W., Fall, C. H. D., Phillips, D. I. W., Shier, R., & Law, C. (2003) · Diabetic Medicine · doi:10.1046/j.1464-5491.2003.00871.x · Cited by 455 · see citing works
Islet Function in Offspring of Mothers on Low-Protein Diet During Gestation
Dahri, S., Snoeck, A., Reusens-Billen, B., Remacle, C., & Hote, J. J. (1991) · Diabetes · doi:10.2337/diab.40.2.s115 · Cited by 445 · see citing works
Maternal Undernutrition during Late Gestation Induces Fetal Overexposure to Glucocorticoids and Intrauterine Growth Retardation, and Disturbs the Hypothalamo-Pituitary Adrenal Axis in the Newborn Rat1
Lésage, J., Blondeau, B., Grino, M., Bréant, B., & Dupouy, J. (2001) · Endocrinology · doi:10.1210/endo.142.5.8139 · Cited by 380 · see citing works
Regulation of insulin gene transcription
Melloul, D., Marshak, S., & Cerasi, E. (2002) · Diabetologia · doi:10.1007/s00125-001-0728-y · Cited by 357 · see citing works
Diagnostic Value of Blood Sampling in Fetuses with Growth Retardation
Pardi, G., Cetin, I., Marconi, A. M., Lanfranchi, A., Bozzetti, P., Farrazzi, E., Buscaglia, M., & Battaglia, F. C. (1993) · New England Journal of Medicine · doi:10.1056/nejm199303113281004 · Cited by 345 · see citing works
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-II1
Petrik, J., Reusens, B., Arany, E. J., Remacle, C., Coelho, C., Hoet, J., & Hill, D. J. (1999) · Endocrinology · doi:10.1210/endo.140.10.7042 · Cited by 337 · see citing works
In utero undernutrition impairs rat beta-cell development
Garofano, A., Czernichow, P., & Bréant, B. (1997) · Diabetologia · doi:10.1007/s001250050812 · Cited by 320 · see citing works
A MORPHOLOGICAL STUDY OF THE ENDOCRINE PANCREAS IN HUMAN PREGNANCY
Van Assche, F. A., Aerts, L., & Prins, F. D. (1978) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1978.tb15835.x · Cited by 267 · see citing works
Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat
Garofano, A., Czernichow, P., & Bréant, B. (1998) · Diabetologia · doi:10.1007/s001250051038 · Cited by 226 · see citing works
Placental Transport of Leucine, Phenylalanine, Glycine, and Proline in Intrauterine Growth-Restricted Pregnancies
Paolini, C. L., Marconi, A. M., Ronzoni, S., Noio, M. D., Fennessey, P. V., Pardi, G., & Battaglia, F. C. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.11.8036 · Cited by 210 · see citing works
Intra-uterine programming of the endocrine pancreas
Fowden, A. L., & Hill, D. J. (2001) · British Medical Bulletin · doi:10.1093/bmb/60.1.123 · Cited by 189 · see citing works
Weights of Placentae From Small-for-Gestational Age Infants Revisited
Heinonen, S. T., Taipale, P., & Saarikoski, S. (2001) · Placenta · doi:10.1053/plac.2001.0630 · Cited by 185 · see citing works
Early and persistent reduction in umbilical vein blood flow in the growth-restricted fetus: A longitudinal study
Rigano, S., Bozzo, M., Ferrazzi, E. M., Bellotti, M., Battaglia, F. C., & Galan, H. L. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.117356 · Cited by 179 · see citing works
Umbilical vein blood flow in growth‐restricted fetuses
Ferrazzi, E. M., Rigano, S., Bozzo, M., Bellotti, M., Giovannini, N., Galan, H. L., & Battaglia, F. C. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00208.x · Cited by 176 · see citing works
Placental glucose transport in heat-induced fetal growth retardation
Thureen, P. J., Trembler, K. A., Meschia, G., Makowski, E. L., & Wilkening, R. B. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.3.r578 · Cited by 173 · see citing works
THE ENDOCRINE PANCREAS IN SMALL‐FOR‐DATES INFANTS
Assche, F. A. V., Prins, F. D., Aerts, L., & Verjans, M. (1977) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1977.tb12486.x · Cited by 171 · see citing works
Some aspects of placental function in chronically heat-stressed ewes.
Aw, B., Rb, W., & Meschia, G. (1987) · PubMed · Cited by 169 · see citing works
Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet
Cherif, H., Reusens, B., Ahn, M., Hoet, J., & Remacle, C. (1998) · Journal of Endocrinology · doi:10.1677/joe.0.1590341 · Cited by 156 · see citing works
Endocrine pancreas plasticity under physiological and pathological conditions.
Kargar, C., & Ktorza, A. (2001) · Diabetes · doi:10.2337/diabetes.50.2007.s30 · Cited by 151 · see citing works
Placental transport and fetal utilization of leucine in a model of fetal growth retardation
J. C. Ross, Fennessey, P. V., Wilkening, R. B., Battaglia, F. C., & Meschia, G. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.3.e491 · Cited by 146 · see citing works
Requirement for proliferating cell nuclear antigen expression during stages of the Chinese hamster ovary cell cycle
Liu, Y. C., Marraccino, R. L., Keng, P. C., Bambara, R. A., Lord, E. M., Chou, W. G., & Zain, S. B. (1989) · Biochemistry · doi:10.1021/bi00433a034 · Cited by 141 · see citing works
Nutrient regulation of insulin gene expression
Docherty, K., & Clark, A. R. (1994) · The FASEB Journal · doi:10.1096/fasebj.8.1.8299887 · Cited by 140 · see citing works
The relationship between transplacental O2 diffusion and placental expression of PlGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction
Regnault, T. R. H., de Vrijer, B., Galan, H. L., Davidsen, M. L., Trembler, K. A., Battaglia, F. C., Wilkening, R. B., & Anthony, R. V. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.039511 · Cited by 136 · see citing works
Dissecting the role of glucocorticoids on pancreas development.
Gésina, E., Tronche, F., Herrera, P., Duchêne, B., Tales, W., Czernichow, P., & Bréant, B. (2004) · Diabetes · doi:10.2337/diabetes.53.9.2322 · Cited by 124 · see citing works
Glucocorticoids impair fetal β-cell development in rats
Blondeau, B., Lésage, J., Czernichow, P., Dupouy, J., & Bréant, B. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.3.e592 · Cited by 124 · see citing works
Steady State Maternal-Fetal Leucine Enrichments in Normal and Intrauterine Growth-Restricted Pregnancies
Marconi, A. M., Paolini, C. L., Stramare, L., Cetin, I., Fennessey, P. V., Pardi, G., & Battaglia, F. C. (1999) · Pediatric Research · doi:10.1203/00006450-199907000-00019 · Cited by 121 · see citing works
Venous drainage of the human uterus: Respiratory gas studiesin normal and fetal growth-retarded pregnancies
Pardi, G., Cetin, I., Marconi, A. M., Bozzetti, P., Buscaglia, M., Makowski, E. L., & Battaglia, F. C. (1992) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(92)91700-k · Cited by 119 · see citing works
Placental Expression of VEGF, PlGF and their Receptors in a Model of Placental Insufficiency—Intrauterine Growth Restriction (PI-IUGR)
Regnault, T. R. H., Orbus, R. J., de Vrijer, B., Davidsen, M. L., Galan, H. L., Wilkening, R. B., & Anthony, R. V. (2002) · Placenta · doi:10.1053/plac.2001.0757 · Cited by 119 · see citing works
Regulation of insulin gene transcription
Ohneda, K., Ee, H. C., & German, M. S. (2000) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0171 · Cited by 116 · see citing works
Effects of Fetal Intravenous Glucose Challenge in Normal and Growth Retarded Fetuses
Nicolini, U., Hubinont, C., Santolaya, J. L., Fisk, N. M., & Rodeck, C. H. (1990) · Hormone and Metabolic Research · doi:10.1055/s-2007-1004939 · Cited by 107 · see citing works
Relationship of fetal growth to duration of heat stress in an ovine model of placental insufficiency
Galan, H. L., Hussey, M. J., Barbera, A., Ferrazzi, E. M., Chung, M., Hobbins, J. C., & Battaglia, F. C. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70629-0 · Cited by 99 · see citing works
Intrauterine Growth Retardation and Development of Endocrine Pancreas in the Experimental Rat
Prins, F. A. D., & Assche, F. A. V. (2009) · Biology of the Neonate · doi:10.1159/000241511 · Cited by 98 · see citing works
Ruminant models of prenatal growth restriction
Anthony, R., Scheaffer, A., Wright, C., & Regnault, T. R. H. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.5.014 · Cited by 98 · see citing works
Endocrine Pancreas Development in Growth-Retarded Human Fetuses
Beringue, F., Blondeau, B., Castellotti, M. C., Bréant, B., Czernichow, P., & Polak, M. (2002) · Diabetes · doi:10.2337/diabetes.51.2.385 · Cited by 95 · see citing works
Placental transport of threonine and its utilization in the normal and growth-restricted fetus
Anderson, A., Fennessey, P. V., Meschia, G., Wilkening, R. B., & Battaglia, F. C. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.272.5.e892 · Cited by 80 · see citing works
Characterization of Glucose Transporter 8 (GLUT8) in the Ovine Placenta of Normal and Growth Restricted Fetuses
Limesand, S. W., Regnault, T. R. H., & Hay, W. W. (2003) · Placenta · doi:10.1016/j.placenta.2003.08.012 · Cited by 79 · see citing works
Self-citation
Adaptation of ovine fetal pancreatic insulin secretion to chronic hypoglycaemia and euglycaemic correction
Limesand, S. W., & Hay, W. W. (2002) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00095.x · Cited by 62 · see citing works
Self-citation
Relation of cord plasma concentrations of proinsulin, 32–33 split proinsulin, insulin and C-peptide to placental weight and the baby's size and proportions at birth
Godfrey, K. M., Hales, C. N., Osmond, C., Barker, D. J. P., & Taylor, K. (1996) · Early Human Development · doi:10.1016/0378-3782(96)01752-5 · Cited by 56 · see citing works
Adaptation of ovine fetal pancreatic insulin secretion to chronic hypoglycaemia and euglycaemic correction
Limesand, S. W., & Hay, W. W. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.026831 · Cited by 51 · see citing works
Self-citation
A dual population of islets of Langerhans in bovine pancreas
Bonner‐Weir, S., & Like, A. A. (1980) · Cell and Tissue Research · doi:10.1007/bf00233616 · Cited by 50 · see citing works
Effects of hypoglycemia and prolonged fasting on insulin and glucagon gene expression. Studies with in situ hybridization.
Chen, L., Komiya, I., Inman, L. R., O’Neil, J. J., APPEL, M. C., Alam, T., & Unger, R. H. (1989) · Journal of Clinical Investigation · doi:10.1172/jci114219 · Cited by 46 · see citing works
Fetal growth and long-term consequences in animal models of growth retardation
Holemans, K., Aerts, L., & Assche, F. A. V. (1998) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(98)00180-8 · Cited by 44 · see citing works
Endocrine pancreatic function in growth-retarded fetuses.
Hubinont, C., Nicolini, U., Fisk, N. M., Tannirandorn, Y., & Rodeck, C. H. (1991) · PubMed · Cited by 39 · see citing works
Flow cytometric characterisation of proliferating cell nuclear antigen using the monoclonal antibody PC10
Wilson, G. D., Camplejohn, R. S., Martindale, C. A., Brock, A., Lane, D. P., & Barnes, D. M. (1992) · European Journal of Cancer · doi:10.1016/0959-8049(92)90250-6 · Cited by 26 · see citing works
AN IMMUNOFLUORESCENT STUDY OF INSULIN‐, GLUCAGON‐, PANCREATIC POLYPEPTIDE‐ AND SOMATOSTATIN‐CONTAINING CELLS IN THE EARLY OVINE FETAL PANCREAS
Reddy, S., Bibby, N. J., & Elliott, R. B. (1988) · Quarterly Journal of Experimental Physiology · doi:10.1113/expphysiol.1988.sp003135 · Cited by 25 · see citing works
Novel activator protein‐2α splice‐variants function as transactivators of the ovine placental lactogen gene
Limesand, S. W., & Anthony, R. V. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02124.x · Cited by 22 · see citing works
Self-citation
Postnatal maturation of the islets of Langerhans in sheep. Light microscopic, immunohistochemical, morphometric, and ultrastructural investigations with particular reference to the transient appearance of argyrophil insulin immunoreactive cells.
Titlbach, M., Fält, K., & Falkmer, S. (1985) · PubMed · Cited by 21 · see citing works
Dissecting the Role of Glucocorticoids on Pancreas
Herrera, P. L., Duchêne, B., Czernichow, P., & Bréant, B. (2004) · Cited by 19 · see citing works
A Defective Beta-Cell Glucose Sensor as a Cause of Diabetes
Weir, G. C. (1993) · New England Journal of Medicine · doi:10.1056/nejm199303113281012 · Cited by 15 · see citing works
Defective insulin secretion in niddm: Integral part of a multiplier hypothesis
Robertson, R. P. (1992) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240480302 · Cited by 15 · see citing works
Cytological Localization of Insulin and Insulin Concentration in the Fetal Ovine Pancreas1
WlLLES, R. F., Boda, J. M., & STOKES, H. (1969) · Endocrinology · doi:10.1210/endo-84-3-671 · Cited by 14 · see citing works

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Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
The fetal brain sparing response to hypoxia: physiological mechanisms
Giussani, D. A. (2015) · The Journal of Physiology · doi:10.1113/jp271099 · Cited by 393 · see citing works
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 · see citing works
Placental-fetal glucose exchange and fetal glucose metabolism.
(2006) · Europe PMC (PubMed Central) · Cited by 226 · see citing works
Self-citation
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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 206 · see citing works
Self-citation
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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 · see citing works
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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 181 · see citing works
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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 · see citing works
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Thorn, S., Rozance, P., Brown, L., & Hay, W. (2011) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1275516 · Cited by 153 · see citing works
Self-citation
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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 · see citing works
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Rozance, P. J., & Hay, W. W. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2010.05.002 · Cited by 118 · see citing works
Self-citation
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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 · see citing works
Self-citation
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Self-citation
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Rashid, C. S., Bansal, A., & Simmons, R. A. (2018) · Physiology · doi:10.1152/physiol.00023.2018 · Cited by 84 · see citing works
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 84 · see citing works
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 82 · see citing works
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 · see citing works
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 69 · see citing works
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 · see citing works
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 · see citing works
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 65 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citation
Restriction of placental growth in sheep impairs insulin secretion but not sensitivity before birth
Owens, J. A., Gatford, K. L., Blasio, M. J. D., Edwards, L. J., McMillen, I. C., & Fowden, A. L. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.142141 · Cited by 59 · see citing works
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 · see citing works
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 · see citing works
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 55 · see citing works
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 · see citing works
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 · see citing works
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 50 · see citing works
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 50 · see citing works
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 · see citing works
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 48 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 44 · see citing works
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 · see citing works
Chronic anemic hypoxemia attenuates glucose-stimulated insulin secretion in fetal sheep
Benjamin, J. S., Culpepper, C., Brown, L. D., Wesolowski, S. R., Jonker, S. S., Davis, M. A., Limesand, S. W., Wilkening, R. B., Hay, W. W., & Rozance, P. J. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00484.2016 · Cited by 42 · see citing works
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 · see citing works
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 41 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 29 · see citing works
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 29 · see citing works
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 · see citing works
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 28 · see citing works
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 · see citing works
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 · see citing works
Glucose metabolic adaptations in the intrauterine growth-restricted adult female rat offspring
Garg, M., Thamotharan, M., Rogers, L., Bassilian, S., Lee, W. N. P., & Devaskar, S. U. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00474.2005 · Cited by 25 · see citing works
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 25 · see citing works
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 · see citing works
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 24 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 21 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 16 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 13 · see citing works
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 13 · see citing works
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 · see citing works
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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 69 · see citing works
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 82 · see citing works
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In utero undernutrition impairs rat beta-cell development
Garofano, A., Czernichow, P., & Bréant, B. (1997) · Diabetologia · doi:10.1007/s001250050812 · Cited by 320 · see citing works
The levels of Pdx1/insulin, Cacna1c and Cacna1d, and β-cell mass in a rat model of intrauterine undernutrition
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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 › Surgery › 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

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

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