Early Human Development
Volume 86, Issue 3 , Pages 179-185 , March 2010

Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPARγ2 expression in male rat offspring prior to the onset of obesity

  • Lisa A. Joss-Moore

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • Corresponding Author InformationCorresponding author. Division of Neonatology, University of Utah, 295 Chepeta Way 2N141, Salt Lake City, UT, 84108, United States. Tel.: +1 801 587 7486; fax: +1 801 585 7395.
    • ,
  • Yan Wang

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Michael S. Campbell

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Barry Moore

      Affiliations

    • Department of Human Genetics, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Xing Yu

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Christopher W. Callaway

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Robert A. McKnight

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Mina Desai

      Affiliations

    • Department of Obstetrics and Gynecology, David Geffen School of Medicine at UCLA and LABioMed at Harbor—UCLA, United States
    • ,
  • Laurie J. Moyer-Mileur

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States
    • ,
  • Robert H. Lane

      Affiliations

    • Division of Neonatology, University of Utah, Salt Lake City, Utah, United States

Received 4 December 2009 ,Revised 16 February 2010 ,Accepted 17 February 2010.

References 

  1. Kinzler WL, Vintzileos AM. Fetal growth restriction: a modern approach. Curr Opin Obstet Gynecol. Apr 2008;20(2):125–131
  2. Cetin I, Alvino G. Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta. Mar 2009;30(Suppl A):S77–S82
  3. Rosenberg A. The IUGR newborn. Semin Perinatol. Jun 2008;32(3):219–224
  4. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. Oct 26 1991;303(6809):1019–1022
  5. Barker DJ. The developmental origins of insulin resistance. Horm Res. 2005;64(Suppl 3):2–7
  6. Gastaldelli A, Miyazaki Y, Pettiti M, Matsuda M, Mahankali S, Santini E, et al. Metabolic effects of visceral fat accumulation in type 2 diabetes. J Clin Endocrinol Metab. Nov 2002;87(11):5098–5103
  7. Muhlhausler B, Smith SR. Early-life origins of metabolic dysfunction: role of the adipocyte. Trends Endocrinol Metab. Mar 2009;20(2):51–57
  8. Chakraborty S, Joseph DV, Bankart MJ, Petersen SA, Wailoo MP. Fetal growth restriction: relation to growth and obesity at the age of 9years. Arch Dis Child Fetal Neonatal Ed. Nov 2007;92(6):F479–F483
  9. Jaquet D, Deghmoun S, Chevenne D, Collin D, Czernichow P, Levy-Marchal C. Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth. Diabetologia. May 2005;48(5):849–855
  10. Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, et al. Altered fat tissue distribution in young adult men who had low birth weight. Diab Care. Jan 2005;28(1):151–153
  11. Ibanez L, Lopez-Bermejo A, Suarez L, Marcos MV, Diaz M, de Zegher F. Visceral adiposity without overweight in children born small-for-gestational-age. J Clin Endocrinol Metab. 2008;93(6):2079–2083
  12. Yajnik CS, Lubree HG, Rege SS, Naik SS, Deshpande JA, Deshpande SS, et al. Adiposity and hyperinsulinemia in Indians are present at birth. J Clin Endocrinol Metab. Dec 2002;87(12):5575–5580
  13. Medina-Gomez G, Gray SL, Yetukuri L, Shimomura K, Virtue S, Campbell M, et al. PPAR gamma 2 prevents lipotoxicity by controlling adipose tissue expandability and peripheral lipid metabolism. PLoS Genet. Apr 27 2007;3(4):e64
  14. Kim JY, van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM, et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Investig. Sep 2007;117(9):2621–2637
  15. Tran TT, Yamamoto Y, Gesta S, Kahn CR. Beneficial effects of subcutaneous fat transplantation on metabolism. Cell Metab. May 2008;7(5):410–420
  16. Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM, Saladin R, et al. The organization, promoter analysis, and expression of the human PPARgamma gene. J Biol Chem. Jul 25 1997;272(30):18779–18789
  17. Zhu Y, Qi C, Korenberg JR, Chen XN, Noya D, Rao MS, et al. Structural organization of mouse peroxisome proliferator-activated receptor gamma (mPPAR gamma) gene: alternative promoter use and different splicing yield two mPPAR gamma isoforms. Proc Natl Acad Sci USA. Aug 15 1995;92(17):7921–7925
  18. Ershov AV, Bazan NG. Photoreceptor phagocytosis selectively activates PPARgamma expression in retinal pigment epithelial cells. J Neurosci Res. May 1 2000;60(3):328–337
  19. Magee TR, Han G, Cherian B, Khorram O, Ross MG, Desai M. Down-regulation of transcription factor peroxisome proliferator-activated receptor in programmed hepatic lipid dysregulation and inflammation in intrauterine growth-restricted offspring. Am J Obstet Gynecol. Sep 2008;199(3):271;e1-5
  20. Anghel SI, Bedu E, Vivier CD, Descombes P, Desvergne B, Wahli W. Adipose tissue integrity as a prerequisite for systemic energy balance: a critical role for peroxisome proliferator-activated receptor gamma. J Biol Chem. Oct 12 2007;282(41):29946–29957
  21. Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. Dec 14 2006;444(7121):847–853
  22. Schoonjans K, Peinado-Onsurbe J, Lefebvre AM, Heyman RA, Briggs M, Deeb S, et al. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. Embo J. Oct 1 1996;15(19):5336–5348
  23. Tontonoz P, Hu E, Devine J, Beale EG, Spiegelman BM. PPAR gamma 2 regulates adipose expression of the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol. Jan 1995;15(1):351–357
  24. Targett-Adams P, McElwee MJ, Ehrenborg E, Gustafsson MC, Palmer CN, McLauchlan J. A PPAR response element regulates transcription of the gene for human adipose differentiation-related protein. Biochim Biophys Acta. Apr 5 2005;1728(1–2):95–104
  25. Heikkinen S, Auwerx J, Argmann CA. PPARgamma in human and mouse physiology. Biochim Biophys Acta. Aug 2007;1771(8):999–1013
  26. Larsen LN, Granlund L, Holmeide AK, Skattebol L, Nebb HI, Bremer J. Sulfur-substituted and alpha-methylated fatty acids as peroxisome proliferator-activated receptor activators. Lipids. Jan 2005;40(1):49–57
  27. Devchand PR, Ijpenberg A, Devesvergne B, Wahli W. PPARs: nuclear receptors for fatty acids, eicosanoids, and xenobiotics. Adv Exp Med Biol. 1999;469:231–236
  28. Krey G, Braissant O, L'Horset F, Kalkhoven E, Perroud M, Parker MG, et al. Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol Endocrinol. Jun 1997;11(6):779–791
  29. Armoni M, Kritz N, Harel C, Bar-Yoseph F, Chen H, Quon MJ, et al. Peroxisome proliferator-activated receptor-gamma represses GLUT4 promoter activity in primary adipocytes, and rosiglitazone alleviates this effect. J Biol Chem. Aug 15 2003;278(33):30614–30623
  30. Bispham J, Gardner DS, Gnanalingham MG, Stephenson T, Symonds ME, Budge H. Maternal nutritional programming of fetal adipose tissue development: differential effects on messenger ribonucleic acid abundance for uncoupling proteins and peroxisome proliferator-activated and prolactin receptors. Endocrinology. Sep 2005;146(9):3943–3949
  31. Muhlhausler BS, Duffield JA, McMillen IC. Increased maternal nutrition stimulates peroxisome proliferator activated receptor-gamma, adiponectin, and leptin messenger ribonucleic acid expression in adipose tissue before birth. Endocrinology. Feb 2007;148(2):878–885
  32. Bortolotto JW, Margis R, Ferreira AC, Padoin AV, Mottin CC, Guaragna RM. Adipose tissue distribution and quantification of PPARbeta/delta and PPARgamma1–3 mRNAs: discordant gene expression in subcutaneous, retroperitoneal and visceral adipose tissue of morbidly obese patients. Obes Surg. Jul 2007;17(7):934–940
  33. Perrini S, Laviola L, Cignarelli A, Melchiorre M, De Stefano F, Caccioppoli C, et al. Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells. Diabetologia. Jan 2008;51(1):155–164
  34. Rodriguez E, Ribot J, Rodriguez AM, Palou A. PPAR-gamma2 expression in response to cafeteria diet: gender- and depot-specific effects. Obes Res. Sep 2004;12(9):1455–1463
  35. Desai M, Guang H, Ferelli M, Kallichanda N, Lane RH. Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring. Reprod Sci. Oct 2008;15(8):785–796
  36. Lane RH, Dvorak B, MacLennan NK, Dvorakova K, Halpern MD, Pham TD, et al. IGF alters jejunal glucose transporter expression and serum glucose levels in immature rats. Am J Physiol Regul Integr Comp Physiol. Dec 2002;283(6):R1450–R1460
  37. Lane RH, Chandorkar AK, Flozak AS, Simmons RA. Intrauterine growth retardation alters mitochondrial gene expression and function in fetal and juvenile rat skeletal muscle. Pediatr Res. May 1998;43(5):563–570
  38. Unterman TG, Simmons RA, Glick RP, Ogata ES. Circulating levels of insulin, insulin-like growth factor-I (IGF-I), IGF-II, and IGF-binding proteins in the small for gestational age fetal rat. Endocrinology. Jan 1993;132(1):327–336
  39. Guiding principles for research involving animals and human beings. Am J Physiol Regul Integr Comp Physiol. Aug 2002;283(2):R281–R283
  40. Kloesz JL, Serdikoff CM, Maclennan NK, Adibi SA, Lane RH. Uteroplacental insufficiency alters liver and skeletal muscle branched-chain amino acid metabolism in intrauterine growth-restricted fetal rats. Pediatr Res. Nov 2001;50(5):604–610
  41. Pham TD, MacLennan NK, Chiu CT, Laksana GS, Hsu JL, Lane RH. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. Nov 2003;285(5):R962–R970
  42. Hubscher CH, Brooks DL, Johnson JR. A quantitative method for assessing stages of the rat estrous cycle. Biotech Histochem. Mar–Apr 2005;80(2):79–87
  43. Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with image. J Biophotonics Int. 2004;11(7):36–42
  44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. Dec 2001;25(4):402–408
  45. Baserga M, Hale MA, Ke X, Wang ZM, Yu X, Callaway CW, et al. Uteroplacental insufficiency increases p53 phosphorylation without triggering the p53-MDM2 functional circuit response in the IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. Aug 2006;291(2):R412–R418
  46. Baserga M, Hale MA, Wang ZM, Yu X, Callaway CW, McKnight RA, et al. Uteroplacental insufficiency alters nephrogenesis and downregulates cyclooxygenase-2 expression in a model of IUGR with adult-onset hypertension. Am J Physiol Regul Integr Comp Physiol. May 2007;292(5):R1943–R1955
  47. Ke X, Lei Q, James SJ, Kelleher SL, Melnyk S, Jernigan S, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics. Mar 13 2006;25(1):16–28
  48. Choi GY, Tosh DN, Garg A, Mansano R, Ross MG, Desai M. Gender-specific programmed hepatic lipid dysregulation in intrauterine growth-restricted offspring. Am J Obstet Gynecol. May 2007;196(5):477;e1-7
  49. De Blasio MJ, Gatford KL, McMillen IC, Robinson JS, Owens JA. Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb. Endocrinology. Mar 2007;148(3):1350–1358
  50. Louey S, Cock ML, Harding R. Long term consequences of low birthweight on postnatal growth, adiposity and brain weight at maturity in sheep. J Reprod Dev. Feb 2005;51(1):59–68
  51. Yu C, Markan K, Temple KA, Deplewski D, Brady MJ, Cohen RN. The nuclear receptor corepressors NCoR and SMRT decrease peroxisome proliferator-activated receptor gamma transcriptional activity and repress 3T3-L1 adipogenesis. J Biol Chem. Apr 8 2005;280(14):13600–13605
  52. Mattevi VS, Zembrzuski VM, Hutz MH. Effects of a PPARG gene variant on obesity characteristics in Brazil. Braz J Med Biol Res. Jul 2007;40(7):927–932
  53. Morini E, Tassi V, Capponi D, Ludovico O, Dallapiccola B, Trischitta V, et al. Interaction between PPARgamma2 variants and gender on the modulation of body weight. Obesity (Silver Spring). Jun 2008;16(6):1467–1470
  54. Lane RH, Kelley DE, Ritov VH, Tsirka AE, Gruetzmacher EM. Altered expression and function of mitochondrial beta-oxidation enzymes in juvenile intrauterine-growth-retarded rat skeletal muscle. Pediatr Res. Jul 2001;50(1):83–90
  55. Campbell M, Joss-Moore LA, Wang Y, Callaway C, Yu X, McKnight R, et al. IUGR alters TNFα and NFκB mRNA levels in rat adipose tissue in gender specific manner. J Investig Med. 2009;57(1):214
  56. Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J Clin Endocrinol Metab. Apr 2000;85(4):1401–1406

PII: S0378-3782(10)00050-2

doi: 10.1016/j.earlhumdev.2010.02.006

Early Human Development
Volume 86, Issue 3 , Pages 179-185 , March 2010

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