Placenta
Volume 30, Issue 5 , Pages 405-410 , May 2009

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

  • M.J. Zhu

      Affiliations

    • Center for the Study of Fetal Programming, Department of Animal Science, University of Wyoming, 1000E University Avenue, Laramie, WY 82071, USA
  • ,
  • M. Du

      Affiliations

    • Center for the Study of Fetal Programming, Department of Animal Science, University of Wyoming, 1000E University Avenue, Laramie, WY 82071, USA
  • ,
  • M.J. Nijland

      Affiliations

    • Center for Pregnancy and Newborn Research, University of Texas, Health Sciences Center, San Antonio, TX 78229, USA
  • ,
  • P.W. Nathanielsz

      Affiliations

    • Center for Pregnancy and Newborn Research, University of Texas, Health Sciences Center, San Antonio, TX 78229, USA
  • ,
  • B.W. Hess

      Affiliations

    • Center for the Study of Fetal Programming, Department of Animal Science, University of Wyoming, 1000E University Avenue, Laramie, WY 82071, USA
  • ,
  • G.E. Moss

      Affiliations

    • Center for the Study of Fetal Programming, Department of Animal Science, University of Wyoming, 1000E University Avenue, Laramie, WY 82071, USA
  • ,
  • S.P. Ford

      Affiliations

    • Center for the Study of Fetal Programming, Department of Animal Science, University of Wyoming, 1000E University Avenue, Laramie, WY 82071, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 307 766 2709; fax: +1 307 766 2355.

,Accepted 7 February 2009.

References 

  1. Ford SP. Cotyledonary placenta. In:  Knobil E,  Neil JD editor. Encyclopedia of reproduction. vol. 1:San Diego, CA: Academic Press; 2000;p. R730–738
  2. Zhu MJ, Du M, Hess BW, Nathanielsz PW, Ford SP. Periconceptional nutrient restriction in the ewe alters MAPK/ERK1/2 and PI3K/Akt growth signaling pathways and vascularity in the placentome. Placenta. 2007;28:R1192–1199
  3. Zhu MJ, Du M, Hess BW, Means WJ, Nathanielsz PW, Ford SP. Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes. Placenta. 2007;28:R361–368
  4. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod. 2001;64:1033–1040
  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. 2005;25:2838–2852
  6. Bush JA, Kimball SR, O'Connor PM, Suryawan A, Orellana RA, Nguyen HV, et al. Translational control of protein synthesis in muscle and liver of growth hormone-treated pigs. Endocrinology. 2003;144:1273–1283
  7. Vary TC. IGF-I stimulates protein synthesis in skeletal muscle through multiple signaling pathways during sepsis. Am J Physiol Regul Integr Comp Physiol. 2006;290:R313–R321
  8. Park IH, Erbay E, Nuzzi P, Chen J. Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp Cell Res. 2005;309:211–219
  9. Song YH, Godard M, Li Y, Richmond SR, Rosenthal N, 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. 2005;53:135–142
  10. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, 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. 2005;280:2737–2744
  11. Anthony JC, Anthony TG, Kimball SR, Jefferson LS. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr. 2001;131:856S–860S
  12. Chiang GG, Abraham RT. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem. 2005;280:25485–25490
  13. Hwang JJ, Hur KC. 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. 2005;20:280–287
  14. Choi WS, Sung CK. 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. 2004;24:67–83
  15. Jakobsen SN, Hardie DG, Morrice N, Tornqvist HE. 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. 2001;276:46912–46916
  16. Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, 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. 2007;85:1285–1294
  17. Vonnahme KA, Hess BW, Nijland MJ, Nathanielsz PW, Ford SP. Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. J Anim Sci. 2006;84:3451–3459
  18. Vonnahme KA, Hess BW, Hansen TR, McCormick RJ, Rule DC, Moss GE, 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. 2003;69:133–140
  19. Zhu MJ, Ford SP, Nathanielsz PW, Du M. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol Reprod. 2004;71:1968–1973
  20. SAS . SAS user's guide. Version 8 Cary, NC: SAS Institute Inc; 2000;
  21. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Redmer DA, et al. Placental angiogenesis in sheep models of compromised pregnancy. J Physiol. 2005;565:43–58
  22. Reynolds LP, Redmer DA. Utero-placental vascular development and placental function. J Anim Sci. 1995;73:1839–1851
  23. Ford SP, Christenson LK, Rosazza JP, Short RE. Effects of Ponderosa pine needle ingestion of uterine vascular function in late-gestation beef cows. J Anim Sci. 1992;70:1609–1614
  24. Reynolds LP, Ferrell CL, Ford SP. Transplacental diffusion and blood flow of gravid bovine uterus. Am J Physiol. 1985;249:R539–R543
  25. Regnault TR, Hay WW. In vivo techniques for studying fetoplacental nutrient uptake, metabolism, and transport. Methods Mol Med. 2006;122:207–224
  26. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, 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. 1998;273:30336–30343
  27. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem. 1999;274:16349–16354
  28. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res. 2002;90:1243–1250
  29. Yang ZZ, 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. 2003;278:32124–32131
  30. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, Pandolfi PP. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell. 2005;121:179–193
  31. Zheng J, Wen Y, Austin JL, Chen DB. Exogenous nitric oxide stimulates cell proliferation via activation of a mitogen-activated protein kinase pathway in ovine fetoplacental artery endothelial cells. Biol Reprod. 2006;74:375–382
  32. Boileau P, Cauzac M, Pereira MA, Girard J, 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. 2001;142:3974–3979
  33. Shao J, Yamashita H, Qiao L, Draznin B, Friedman JE. Phosphatidylinositol 3-kinase redistribution is associated with skeletal muscle insulin resistance in gestational diabetes mellitus. Diabetes. 2002;51:19–29
  34. Kim J, Solis RS, Arias EB, Cartee GD. Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5′ AMP-activated protein kinase phosphorylation. J Appl Physiol. 2004;96:575–583
  35. Hardie DG. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc. 2004;36:28–34
  36. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005;2:9–19
  37. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005;2:21–33
  38. Hardie DG, Hawley SA. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays. 2001;23:1112–1119
  39. Fujii N, Jessen N, Goodyear LJ. AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab. 2006;291:E867–877
  40. Musi N, Goodyear LJ. Targeting the AMP-activated protein kinase for the treatment of type 2 diabetes. Curr Drug Targets Immune Endocr Metabol Disord. 2002;2:119–127
  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. 2004;279:R47898–47905
  42. Musi N, Hirshman MF, 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. 2002;51:R2074–2081
  43. Steinberg GR, Michell BJ, van Denderen BJ, Watt MJ, Carey AL, Fam BC, et al. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab. 2006;4:465–474
  44. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, 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. 2006;55:2256–2264
  45. Watt MJ, Dzamko N, Thomas WG, Rose-John S, Ernst M, Carling D, et al. CNTF reverses obesity-induced insulin resistance by activating skeletal muscle AMPK. Nat Med. 2006;12:541–548
  46. Babischkin JS, Suresch DL, Pepe GJ, Albrecht ED. Differential expression of placental villous angiopoietin-1 and -2 during early, mid and late baboon pregnancy. Placenta. 2007;28:212–218
  47. Pfarrer CD, Ruziwa SD, 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. 2006;27:889–898
  48. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Wallace JM, et al. Animal models of placental angiogenesis. Placenta. 2005;26:689–708

PII: S0143-4004(09)00057-5

doi: 10.1016/j.placenta.2009.02.001

Placenta
Volume 30, Issue 5 , Pages 405-410 , May 2009