Effect of pre-existing maternal obesity, gestational diabetes and adipokines on the expression of genes involved in lipid metabolism in adipose tissue

Metabolism: Clinical and Experimental

Volumn 63, Issue 2, 2014, Pages 250-262

  Lappas, Martha ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

Cytokines; Fatty acid transport; Fatty acid uptake; Pregnancy; Transcription factors

Indexed keywords

ADIPOCYTOKINE; CARRIER PROTEIN; FATTY ACID TRANSPORTER; INTERLEUKIN 1BETA; LEPTIN; LIPOPROTEIN LIPASE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN FATP2; PROTEIN FATP6; PROTEIN PNPLA2; RETINOID X RECEPTOR ALPHA; TRANSCRIPTION FACTOR MASH1; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ADULT; ARTICLE; BIOSYNTHESIS; CLINICAL ARTICLE; CONTROLLED STUDY; FATTY ACID SYNTHESIS; FATTY ACID TRANSPORT; FEMALE; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN TISSUE; INTRAABDOMINAL FAT; LEAN BODY WEIGHT; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; MATERNAL OBESITY; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS TISSUE;

ACYL-COA SYNTHETASE LONG-CHAIN FAMILY MEMBER 1; ADIPOSE TRIGLYCERIDE LIPASE; ASCL1; CYTOKINES; DAG; DGAT; DIACYLGLYCEROL; DIACYLGLYCEROL ACYLTRANSFERASES; FABP; FABPPM; FASN; FATP; FATTY ACID BINDING PROTEIN; FATTY ACID SYNTHASE; FATTY ACID TRANSPORT; FATTY ACID TRANSPORT PROTEIN; FATTY ACID UPTAKE; FFA; FREE FATTY ACID; GDM; GESTATIONAL DIABETES MELLITUS; HORMONE-SENSITIVE LIPASE; HSL; LIPOPROTEIN LIPASE; LIVER X RECEPTOR; LPL; LXR; MAG; MGAT; MGLL; MONOACYGLYCEROL ACYLTRANSFERASES; MONOACYLGLYCEROL.; MONOGLYCERIDE LIPASE; NGT; NORMAL GLUCOSE TOLERANT; PLASMA MEMBRANE FATTY ACID BINDING PROTEIN; PNPLA2; PPAR; PREGNANCY; PROLIFERATOR ACTIVATED RECEPTOR; QRT-PCR; QUANTITATIVE RT-PCR; RETINOID X RECEPTOR; RXR; SREBP1C; STEROL REGULATORY ELEMENT BINDING PROTEIN; TAG; TRANSCRIPTION FACTORS; TRIACYLGLYCERIDE;

ADIPOKINES; ADIPOSE TISSUE; ADULT; BODY MASS INDEX; DIABETES, GESTATIONAL; DOWN-REGULATION; FATTY ACIDS; FEMALE; HUMANS; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; MALE; MOTHERS; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 84892675992     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.10.001     Document Type: Article

References (85)

1. P. Trayhurn, and J.H. Beattie Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ Proc Nutr Soc 60 3 2001 329 339 (Pubitemid 32772448)
2. B.E. Metzger, R.L. Phelps, and N. Freinkel et al. Effects of gestational diabetes on diurnal profiles of plasma glucose, lipids, and individual amino acids Diabetes Care 3 3 1980 402 409 (Pubitemid 10000683)
3. K.Y. Lain, and P.M. Catalano Metabolic changes in pregnancy Clin Obstet Gynecol 50 4 2007 938 948 (Pubitemid 350059291)
4. P.M. Catalano, S.E. Nizielski, and J.H. Shao et al. Downregulated IRS-1 and PPAR gamma in obese women with gestational diabetes: relationship to FFA during pregnancy Am J Physiol Endocrinol Metab 282 3 2002 E522 E533
5. M. Colomiere, M. Permezel, and M. Lappas Diabetes and obesity during pregnancy alter insulin signalling and glucose transporter expression in maternal skeletal muscle and subcutaneous adipose tissue J Mol Endocrinol 44 4 2010 213 223
6. A. Kautzky-Willer, M. Krssak, and C. Winzer et al. Increased intramyocellular lipid concentration identifies impaired glucose metabolism in women with previous gestational diabetes Diabetes 52 2 2003 244 251 (Pubitemid 36173175)
7. N.C. Okereke, L. Huston-Presley, and S.B. Amini et al. Longitudinal changes in energy expenditure and body composition in obese women with normal and impaired glucose tolerance Am J Physiol Endocrinol Metab 287 3 2004 E472 E479
8. P.M. Catalano, J.P. Kirwan, and S. Haugel-de Mouzon et al. Gestational diabetes and insulin resistance: role in short- and long-term implications for mother and fetus J Nutr 133 5 Suppl 2 2003 1674S 1683S (Pubitemid 36548675)
9. G. Darios, N. Carl, and V.A. Cande et al. Gestational diabetes in the United States: temporal trends 1989 through 2004 Am J Obstet Gynecol 198 5 2008 525.e1 525.e5
10. P. Laws, and E.A. Sullivan Australia's mothers and babies 2007 Perinatal statistics series no 23 cat no PER 48 Sydney: AIHW National Perinatal Statistics Unit 2009
11. A.J. Lee, R.J. Hiscock, and P. Wein et al. Gestational diabetes mellitus: clinical predictors and long-term risk of developing type 2 diabetes: a retrospective cohort study using survival analysis Diabetes Care 30 4 2007 878 883 (Pubitemid 46556581)
12. P.E. Scherer Adipose tissue - from lipid storage compartment to endocrine organ Diabetes 55 6 2006 1537 1545 (Pubitemid 44324105)
13. D.B. Savage, K.F. Petersen, and G.I. Shulman Disordered lipid metabolism and the pathogenesis of insulin resistance Physiol Rev 87 2 2007 507 520 (Pubitemid 47084679)
14. T. Ronti, G. Lupattelli, and E. Mannarino The endocrine function of adipose tissue: an update Clin Endocrinol 64 4 2006 355 365
15. A. Stahl A current review of fatty acid transport proteins (SLC27) Pflugers Arch 447 5 2004 722 727 (Pubitemid 38241457)
16. C.H. Lee, P. Olson, and R.M. Evans Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors Endocrinology 144 6 2003 2201 2207 (Pubitemid 36629867)
17. K. Schoonjans, B. Staels, and J. Auwerx The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocyte differentiation Biochim Biophys Acta 1302 2 1996 93 109 (Pubitemid 26247079)
18. G. Chinetti, J.C. Fruchart, and B. Staels Peroxisome proliferator- activated receptors (PPARs): nuclear receptors at the crossroads between lipid metabolism and inflammation Inflamm Res 49 10 2000 497 505
19. N. Zelcer, and P. Tontonoz Liver X receptors as integrators of metabolic and inflammatory signaling J Clin Investig 116 3 2006 607 614 (Pubitemid 43326865)
20. S.W. Beaven, and P. Tontonoz Nuclear receptors in lipid metabolism: targeting the heart of dyslipidemia 2006 313 329
21. P. Ferre, and F. Foufelle SREBP-1c transcription factor and lipid homeostasis: clinical perspective Horm Res 68 2 2007 72 82 (Pubitemid 47026704)
22. G.F. Lewis, A. Carpentier, and K. Adeli et al. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes Endocr Rev 23 2 2002 201 229 (Pubitemid 34299024)
23. H.N. Ginsberg, Y.L. Zhang, and A. Hernandez-Ono Regulation of plasma triglycerides in insulin resistance and diabetes Arch Med Res 36 3 2005 232 240 (Pubitemid 40755136)
24. J.P. Bastard, M. Maachi, and C. Lagathu et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance Eur Cytokine Netw 17 1 2006 4 12
25. C. Koutsari, and M.D. Jensen Thematic review series: patient-oriented research. Free fatty acid metabolism in human obesity J Lipid Res 47 8 2006 1643 1650
26. D. Langin Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome Pharmacol Res 53 6 2006 482 491 (Pubitemid 43767551)
27. C. Holm Molecular mechanisms regulating hormone-sensitive lipase and lipolysis Biochem Soc Trans 31 Pt 6 2003 1120 1124 (Pubitemid 38030921)
28. R.A. Memon, K.R. Feingold, and A.H. Moser et al. Regulation of fatty acid transport protein and fatty acid translocase mRNA levels by endotoxin and cytokines Am J Physiol 274 2 Pt 1 1998 E210 E217
29. G.R. Steinberg, D.J. Dyck, and J. Calles-Escandon et al. Chronic leptin administration decreases fatty acid uptake and fatty acid transporters in rat skeletal muscle J Biol Chem 277 11 2002 8854 8860 (Pubitemid 34952953)
30. M. Lappas, U. Hiden, and G. Desoye et al. The role of oxidative stress in the pathophysiology of gestational diabetes mellitus Antioxid Redox Signal 15 12 2011 3061 3100
31. M. Kuzmicki, B. Telejko, and J. Szamatowicz et al. High resistin and interleukin-6 levels are associated with gestational diabetes mellitus Gynecol Endocrinol 25 4 2009 258 263
32. C. Lopez-Tinoco, M. Roca, and A. Fernandez-Deudero et al. Cytokine profile, metabolic syndrome and cardiovascular disease risk in women with late-onset gestational diabetes mellitus Cytokine 58 1 2012 14 19
33. C. Winzer, O. Wagner, and A. Festa et al. Plasma adiponectin, insulin sensitivity, and subclinical inflammation in women with prior gestational diabetes mellitus Diabetes Care 27 7 2004 1721 1727 (Pubitemid 38857450)
34. M. Wolf, J. Sauk, and A. Shah et al. Inflammation and glucose intolerance - a prospective study of gestational diabetes mellitus Diabetes Care 27 1 2004 21 27 (Pubitemid 38196704)
35. F.C. Denison, K.A. Roberts, and S.M. Barr et al. Obesity, pregnancy, inflammation, and vascular function Reproduction 140 3 2010 373 385
36. J.C. Madan, J.M. Davis, and W.Y. Craig et al. Maternal obesity and markers of inflammation in pregnancy Cytokine 47 1 2009 61 64
37. G. Barker, R. Lim, and H.M. Georgiou et al. Omentin-1 is decreased in maternal plasma, placenta and adipose tissue of women with pre-existing obesity PLoS One 7 8 2012 e42943
38. M. Lappas, A. Mitton, and M. Permezel In response to oxidative stress, the expression of inflammatory cytokines and antioxidant enzymes are impaired in placenta, but not adipose tissue, of women with gestational diabetes J Endocrinol 204 1 2010 75 84
39. M. Lappas, M. Permezel, and G.E. Rice Leptin and adiponectin stimulate the release of proinflammatory cytokines and prostaglandins from human placenta and maternal adipose tissue via nuclear factor-kappaB, peroxisomal proliferator-activated receptor-gamma and extracellularly regulated kinase 1/2 Endocrinology 146 8 2005 3334 3342 (Pubitemid 41058105)
40. M. Lappas, M. Permezel, and G.E. Rice Release of proinflammatory cytokines and 8-isoprostane from placenta, adipose tissue, and skeletal muscle from normal pregnant women and women with gestational diabetes mellitus J Clin Endocrinol Metab 89 11 2004 5627 5633 (Pubitemid 39518451)
41. R.B. Simsolo, J.M. Ong, and B. Saffari et al. Effect of improved diabetes control on the expression of lipoprotein lipase in human adipose tissue J Lipid Res 33 1 1992 89 95
42. T.A. Buchanan, and A.H. Xiang Gestational diabetes mellitus J Clin Invest 115 3 2005 485 491 (Pubitemid 40322217)
43. A. Martin-Hidalgo, C. Holm, and P. Belfrage et al. Lipoprotein lipase and hormone-sensitive lipase activity and mRNA in rat adipose tissue during pregnancy Am J Physiol 266 6 Pt 1 1994 E930 E935
44. J. Soronen, P.P. Laurila, and J. Naukkarinen et al. Adipose tissue gene expression analysis reveals changes in inflammatory, mitochondrial respiratory and lipid metabolic pathways in obese insulin-resistant subjects BMC Med Genomics 5 2012 9
45. D.G. Mashek, and R.A. Coleman Cellular fatty acid uptake: the contribution of metabolism Curr Opin Lipidol 17 3 2006 274 278 (Pubitemid 43786061)
46. J.E. Schaffer, and H.F. Lodish Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein Cell 79 3 1994 427 436 (Pubitemid 24346058)
47. R. Mukherjee, and J.W. Yun Long chain acyl CoA synthetase 1 and gelsolin are oppositely regulated in adipogenesis and lipogenesis Biochem Biophys Res Commun 420 3 2012 588 593
48. J.I. Joo, T.S. Oh, and D.H. Kim et al. Differential expression of adipose tissue proteins between obesity-susceptible and -resistant rats fed a high-fat diet Proteomics 11 8 2011 1429 1448
49. J.E. Ramsay, W.R. Ferrell, and L. Crawford et al. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways J Clin Endocrinol Metab 87 9 2002 4231 4237
50. M. Dolinkova, I. Dostalova, and Z. Lacinova et al. The endocrine profile of subcutaneous and visceral adipose tissue of obese patients Mol Cell Endocrinol 291 1-2 2008 63 70
51. F. Diraison, E. Dusserre, and H. Vidal et al. Increased hepatic lipogenesis but decreased expression of lipogenic gene in adipose tissue in human obesity Am J Physiol Endocrinol Metab 282 1 2002 E46 E51
52. L.C. Hudgins, A. Baday, and M.K. Hellerstein et al. The effect of dietary carbohydrate on genes for fatty acid synthase and inflammatory cytokines in adipose tissues from lean and obese subjects J Nutr Biochem 19 4 2008 237 245 (Pubitemid 351312274)
53. M.D. Mayas, F.J. Ortega, and M. Macias-Gonzalez et al. Inverse relation between FASN expression in human adipose tissue and the insulin resistance level Nutr Metab 7 2010 http://dx.doi.org/10.1186/1743-7075-7-3
54. R. Roberts, L. Hodson, and A.L. Dennis et al. Markers of de novo lipogenesis in adipose tissue: associations with small adipocytes and insulin sensitivity in humans Diabetologia 52 5 2009 882 890
55. G. Ranganathan, R. Unal, and I. Pokrovskaya et al. The lipogenic enzymes DGAT1, FAS, and LPL in adipose tissue: effects of obesity, insulin resistance, and TZD treatment J Lipid Res 47 11 2006 2444 2450 (Pubitemid 44936106)
56. F.B. Hillgartner, L.M. Salati, and A.G. Goodridge Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis Physiol Rev 75 1 1995 47 76
57. J. Hoffstedt, D. Förster, and P. Löfgren Impaired subcutaneous adipocyte lipogenesis is associated with systemic insulin resistance and increased apolipoprotein B/AI ratio in men and women J Intern Med 262 1 2007 131 139 (Pubitemid 47000629)
58. M. Schweiger, R. Schreiber, and G. Haemmerle et al. Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism J Biol Chem 281 52 2006 40236 40241 (Pubitemid 46041828)
59. R. Zimmermann, J.G. Strauss, and G. Haemmerle et al. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase Science 306 5700 2004 1383 1386 (Pubitemid 39532517)
60. D. Langin, A. Dicker, and G. Tavernier et al. Adipocyte lipases and defect of lipolysis in human obesity Diabetes 54 11 2005 3190 3197 (Pubitemid 43334374)
61. V. Large, S. Reynisdottir, and D. Langin et al. Decreased expression and function of adipocyte hormone-sensitive lipase in subcutaneous fat cells of obese subjects J Lipid Res 40 11 1999 2059 2066
62. Y. Schutz Concept of fat balance in human obesity revisited with particular reference to de novo lipogenesis Int J Obes Relat Metab Disord 28 Suppl 4 2004 S3 S11
63. M.J. Watt, A.L. Carey, and E. Wolsk-Petersen et al. Hormone-sensitive lipase is reduced in the adipose tissue of patients with type 2 diabetes mellitus: influence of IL-6 infusion Diabetologia 48 1 2005 105 112 (Pubitemid 40174662)
64. G.R. Steinberg, B.E. Kemp, and M.J. Watt Adipocyte triglyceride lipase expression in human obesity Am J Physiol Endocrinol Metab 293 4 2007 E958 E964
65. J.W.E. Jocken, D. Langin, and E. Smit et al. Adipose triglyceride lipase and hormone-sensitive lipase protein expression is decreased in the obese insulin-resistant state J Clin Endocrinol Metab 92 6 2007 2292 2299 (Pubitemid 46997136)
66. U.A. White, and J.M. Stephens Transcriptional factors that promote formation of white adipose tissue Mol Cell Endocrinol 318 1-2 2010 10 14
67. D. Eberle, B. Hegarty, and P. Bossard et al. SREBP transcription factors: master regulators of lipid homeostasis Biochimie 86 11 2004 839 848 (Pubitemid 39602764)
68. N.Y. Kalaany, K.C. Gauthier, and A.M. Zavacki et al. LXRs regulate the balance between fat storage and oxidation Cell Metab 1 4 2005 231 244 (Pubitemid 43960607)
69. J.M. Way, W.W. Harrington, and K.K. Brown et al. Comprehensive messenger ribonucleic acid profiling reveals that peroxisome proliferator-activated receptor gamma activation has coordinate effects on gene expression in multiple insulin-sensitive tissues Endocrinology 142 3 2001 1269 1277 (Pubitemid 32202838)
70. G. Martin, K. Schoonjans, and A.M. Lefebvre et al. Coordinate regulation of the expression of the fatty acid transport protein and acyl-CoA synthetase genes by PPARalpha and PPARgamma activators J Biol Chem 272 45 1997 28210 28217 (Pubitemid 27517759)
71. K. Motojima, P. Passilly, and J.M. Peters et al. Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor alpha and gamma activators in a tissue- and inducer-specific manner J Biol Chem 273 27 1998 16710 16714 (Pubitemid 28311694)
72. H. Masuzaki, Y. Ogawa, and N. Sagawa et al. Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans Nat Med 3 9 1997 1029 1033 (Pubitemid 27391961)
73. J. Bodner, C.F. Ebenbichler, and H.J. Wolf et al. Leptin receptor in human term placenta: in situ hybridization and immunohistochemical localization Placenta 20 8 1999 677 682 (Pubitemid 29479013)
74. R.G. Lea, D. Howe, and L.T. Hannah et al. Placental leptin in normal, diabetic and fetal growth-retarded pregnancies Mol Hum Reprod 6 8 2000 763 769 (Pubitemid 30625867)
75. J.A. Engelman, A.H. Berg, and R.Y. Lewis et al. Tumor necrosis factor alpha-mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3 T3-L1 adipocytes Mol Endocrinol 14 10 2000 1557 1569
76. A.G. Pittas, N.A. Joseph, and A.S. Greenberg Adipocytokines and insulin resistance J Clin Endocrinol Metab 89 2 2004 447 452 (Pubitemid 38269842)
77. C. Lagathu, L. Yvan-Charvet, and J.P. Bastard et al. Long-term treatment with interleukin-1beta induces insulin resistance in murine and human adipocytes Diabetologia 49 9 2006 2162 2173 (Pubitemid 44168485)
78. W. Khovidhunkit, M.-S. Kim, and R.A. Memon et al. Thematic review series: the pathogenesis of atherosclerosis. Effects of infection and inflammation on lipid and lipoprotein metabolism mechanisms and consequences to the host J Lipid Res 45 7 2004 1169 1196 (Pubitemid 38802622)
79. F. Lago, R. Gomez, and J.J. Gomez-Reino et al. Adipokines as novel modulators of lipid metabolism Trends Biochem Sci 34 10 2009 500 510
80. W.P. Cawthorn, and J.K. Sethi TNF-alpha and adipocyte biology Febs Lett 582 1 2008 117 131
81. M. Ho, S. Foxall, and M. Higginbottom et al. Leptin-mediated inhibition of the insulin-stimulated increase in fatty acid uptake in differentiated 3 T3-L1 adipocytes Metabolism 55 1 2006 8 12 (Pubitemid 41736240)
82. J. Berndt, P. Kovacs, and K. Ruschke et al. Fatty acid synthase gene expression in human adipose tissue: association with obesity and type 2 diabetes Diabetologia 50 7 2007 1472 1480 (Pubitemid 46879018)
83. C. Sztalryd, and F.B. Kraemer Regulation of hormone-sensitive lipase during fasting Am J Physiol 266 2 Pt 1 1994 E179 E185
84. E.E. Kershaw, J.K. Hamm, and L.A. Verhagen et al. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin Diabetes 55 1 2006 148 157 (Pubitemid 43343310)
85. M.D. Mayas, M.I. Queipo-Ortuno, and M. Clemente-Postigo et al. Influence of a fat overload on lipogenic regulators in metabolic syndrome patients Br J Nutr 105 6 2011 895 901