Down-Regulation of Growth Signaling Pathways Linked to a Reduced Cotyledonary Vascularity in Placentomes of Over-Nourished, Obese Pregnant Ewes

Placenta

Volumn 30, Issue 5, 2009, Pages 405-410

  Zhu, M J ^a   Du, M ^a   Nijland, M J ^b   Nathanielsz, P W ^b   Hess, B W ^a   Moss, G E ^a   Ford, S P ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

IGF 1; Insulin; Maternal obesity; Placentome; Sheep; Vascularity

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE PHOSPHATE; FIBRINOGEN; GLUCOSE; GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE; PROTEIN KINASE B; SERINE; SOMATOMEDIN C; THREONINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY; ARTICLE; AUTOPSY; BIRTH WEIGHT; BLOOD LEVEL; CHORION VILLUS; CONCENTRATION (PARAMETERS); CONCEPTION; DIET; ENZYME PHOSPHORYLATION; EWE; FEMALE; FETOMATERNAL TRANSFUSION; FETUS; FETUS WEIGHT; GESTATIONAL AGE; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; LAMB; MALE; NONHUMAN; OBESITY; PLACENTOMA; PREGNANCY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASCULARIZATION;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DOWN-REGULATION; FEMALE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; OBESITY; PHOSPHORYLATION; PLACENTA; PREGNANCY; SHEEP; SIGNAL TRANSDUCTION;

EID: 65049086375     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2009.02.001     Document Type: Article

References (48)

1. Ford S.P. Cotyledonary placenta. In: Knobil E., and Neil J.D. (Eds). Encyclopedia of reproduction vol. 1 (2000), Academic Press, San Diego, CA R730-738
2. Zhu M.J., Du M., Hess B.W., Nathanielsz P.W., and Ford S.P. Periconceptional nutrient restriction in the ewe alters MAPK/ERK1/2 and PI3K/Akt growth signaling pathways and vascularity in the placentome. Placenta 28 (2007) R1192-1199
3. Zhu M.J., Du M., Hess B.W., Means W.J., Nathanielsz P.W., and Ford S.P. Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes. Placenta 28 (2007) R361-368
4. Reynolds L.P., and Redmer D.A. Angiogenesis in the placenta. Biol Reprod 64 (2001) 1033-1040
5. Subramaniam S., Shahani N., Strelau J., Laliberte C., Brandt R., Kaplan D., et al. Insulin-like growth factor 1 inhibits extracellular signal-regulated kinase to promote neuronal survival via the phosphatidylinositol 3-kinase/protein kinase A/c-Raf pathway. J Neurosci 25 (2005) 2838-2852
6. Bush J.A., Kimball S.R., O'Connor P.M., Suryawan A., Orellana R.A., Nguyen H.V., et al. Translational control of protein synthesis in muscle and liver of growth hormone-treated pigs. Endocrinology 144 (2003) 1273-1283
7. Vary T.C. IGF-I stimulates protein synthesis in skeletal muscle through multiple signaling pathways during sepsis. Am J Physiol Regul Integr Comp Physiol 290 (2006) R313-R321
8. Park I.H., Erbay E., Nuzzi P., and Chen J. Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp Cell Res 309 (2005) 211-219
9. Song Y.H., Godard M., Li Y., Richmond S.R., Rosenthal N., and Delafontaine P. Insulin-like growth factor I-mediated skeletal muscle hypertrophy is characterized by increased mTOR-p70S6K signaling without increased Akt phosphorylation. J Investig Med 53 (2005) 135-142
10. Latres E., Amini A.R., Amini A.A., Griffiths J., Martin F.J., Wei Y., et al. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280 (2005) 2737-2744
11. Anthony J.C., Anthony T.G., Kimball S.R., and Jefferson L.S. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr 131 (2001) 856S-860S
12. Chiang G.G., and Abraham R.T. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem 280 (2005) 25485-25490
13. Hwang J.J., and Hur K.C. Insulin cannot activate extracellular-signal-related kinase due to inability to generate reactive oxygen species in SK-N-BE(2) human neuroblastoma cells. Mol Cells 20 (2005) 280-287
14. Choi W.S., and Sung C.K. Inhibition of phosphatidylinositol-3-kinase enhances insulin stimulation of insulin receptor substrate 1 tyrosine phosphorylation and extracellular signal-regulated kinases in mouse R- fibroblasts. J Recept Signal Transduct Res 24 (2004) 67-83
15. Jakobsen S.N., Hardie D.G., Morrice N., and Tornqvist H.E. 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J Biol Chem 276 (2001) 46912-46916
16. Ford S.P., Hess B.W., Schwope M.M., Nijland M.J., Gilbert J.S., Vonnahme K.A., et al. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci 85 (2007) 1285-1294
17. Vonnahme K.A., Hess B.W., Nijland M.J., Nathanielsz P.W., and Ford S.P. Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. J Anim Sci 84 (2006) 3451-3459
18. Vonnahme K.A., Hess B.W., Hansen T.R., McCormick R.J., Rule D.C., Moss G.E., et al. Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep. Biol Reprod 69 (2003) 133-140
19. Zhu M.J., Ford S.P., Nathanielsz P.W., and Du M. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol Reprod 71 (2004) 1968-1973
20. SAS. SAS user's guide. Version 8 (2000), SAS Institute Inc, Cary, NC
21. Reynolds L.P., Borowicz P.P., Vonnahme K.A., Johnson M.L., Grazul-Bilska A.T., Redmer D.A., et al. Placental angiogenesis in sheep models of compromised pregnancy. J Physiol 565 (2005) 43-58
22. Reynolds L.P., and Redmer D.A. Utero-placental vascular development and placental function. J Anim Sci 73 (1995) 1839-1851
23. Ford S.P., Christenson L.K., Rosazza J.P., and Short R.E. Effects of Ponderosa pine needle ingestion of uterine vascular function in late-gestation beef cows. J Anim Sci 70 (1992) 1609-1614
24. Reynolds L.P., Ferrell C.L., and Ford S.P. Transplacental diffusion and blood flow of gravid bovine uterus. Am J Physiol 249 (1985) R539-R543
25. Regnault T.R., and Hay Jr. W.W. In vivo techniques for studying fetoplacental nutrient uptake, metabolism, and transport. Methods Mol Med 122 (2006) 207-224
26. Gerber H.P., McMurtrey A., Kowalski J., Yan M., Keyt B.A., Dixit V., et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273 (1998) 30336-30343
27. Fujio Y., and Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 274 (1999) 16349-16354
28. Shiojima I., and Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90 (2002) 1243-1250
29. Yang Z.Z., Tschopp O., Hemmings-Mieszczak M., Feng J., Brodbeck D., Perentes E., et al. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem 278 (2003) 32124-32131
30. Ma L., Chen Z., Erdjument-Bromage H., Tempst P., and Pandolfi P.P. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121 (2005) 179-193
31. Zheng J., Wen Y., Austin J.L., and Chen D.B. Exogenous nitric oxide stimulates cell proliferation via activation of a mitogen-activated protein kinase pathway in ovine fetoplacental artery endothelial cells. Biol Reprod 74 (2006) 375-382
32. Boileau P., Cauzac M., Pereira M.A., Girard J., and Hauguel-De Mouzon S. Dissociation between insulin-mediated signaling pathways and biological effects in placental cells: role of protein kinase B and MAPK phosphorylation. Endocrinology 142 (2001) 3974-3979
33. Shao J., Yamashita H., Qiao L., Draznin B., and Friedman J.E. Phosphatidylinositol 3-kinase redistribution is associated with skeletal muscle insulin resistance in gestational diabetes mellitus. Diabetes 51 (2002) 19-29
34. Kim J., Solis R.S., Arias E.B., and Cartee G.D. Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5′ AMP-activated protein kinase phosphorylation. J Appl Physiol 96 (2004) 575-583
35. Hardie D.G. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc 36 (2004) 28-34
36. Hawley S.A., Pan D.A., Mustard K.J., Ross L., Bain J., Edelman A.M., et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2 (2005) 9-19
37. Woods A., Dickerson K., Heath R., Hong S.P., Momcilovic M., Johnstone S.R., et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2 (2005) 21-33
38. Hardie D.G., and Hawley S.A. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23 (2001) 1112-1119
39. Fujii N., Jessen N., and Goodyear L.J. AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab 291 (2006) E867-877
40. Musi N., and Goodyear L.J. Targeting the AMP-activated protein kinase for the treatment of type 2 diabetes. Curr Drug Targets Immune Endocr Metabol Disord 2 (2002) 119-127
41. Zang M., Zuccollo A., Hou X., Nagata D., Walsh K., Herscovitz H., et al. AMP-activated protein kinase is required for the lipid-lowering effect of metformin in insulin-resistant human HepG2 cells. J Biol Chem 279 (2004) R47898-47905
42. Musi N., Hirshman M.F., Nygren J., Svanfeldt M., Bavenholm P., Rooyackers O., et al. Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 51 (2002) R2074-2081
43. Steinberg G.R., Michell B.J., van Denderen B.J., Watt M.J., Carey A.L., Fam B.C., et al. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 4 (2006) 465-474
44. Lee Y.S., Kim W.S., Kim K.H., Yoon M.J., Cho H.J., Shen Y., et al. Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55 (2006) 2256-2264
45. Watt M.J., Dzamko N., Thomas W.G., Rose-John S., Ernst M., Carling D., et al. CNTF reverses obesity-induced insulin resistance by activating skeletal muscle AMPK. Nat Med 12 (2006) 541-548
46. Babischkin J.S., Suresch D.L., Pepe G.J., and Albrecht E.D. Differential expression of placental villous angiopoietin-1 and -2 during early, mid and late baboon pregnancy. Placenta 28 (2007) 212-218
47. Pfarrer C.D., Ruziwa S.D., Winther H., Callesen H., Leiser R., Schams D., et al. Localization of vascular endothelial growth factor (VEGF) and its receptors VEGFR-1 and VEGFR-2 in bovine placentomes from implantation until term. Placenta 27 (2006) 889-898
48. Reynolds L.P., Borowicz P.P., Vonnahme K.A., Johnson M.L., Grazul-Bilska A.T., Wallace J.M., et al. Animal models of placental angiogenesis. Placenta 26 (2005) 689-708