Maternal metformin treatment decreases fetal inflammation in a rat model of obesity and metabolic syndrome

American Journal of Obstetrics and Gynecology

Volumn 209, Issue 2, 2013, Pages 136.e1-136.e9

  Desai, Neeraj ^a   Roman, Amanda ^a   Rochelson, Burton ^a   Gupta, Madhu ^b   Xue, Xiangying ^b   Chatterjee, Prodyot K ^b   Tam Tam, Hima ^a   Metz, Christine N ^b  

^a DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

cytokine; inflammatory metabolic syndrome; metformin; obesity

Indexed keywords

INSULIN; INTERLEUKIN 6; LEPTIN; METFORMIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE DIET; CONTROLLED STUDY; DYSLIPIDEMIA; FEMALE; FETUS OUTCOME; INFERTILITY; INFLAMMATION; INSULIN BLOOD LEVEL; LIPID DIET; METABOLIC SYNDROME X; NONHUMAN; OBESITY; PLACENTA; PRIORITY JOURNAL;

EID: 84880922745     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2013.05.001     Document Type: Article

References (59)

1. R. Kahn, J. Buse, E. Ferrannini, and M. Stern The metabolic syndrome: time for a critical appraisal: joint statement from the American Diabetes Association and the European Association for the Study of Diabetes Diabetes Care 28 2005 2289 2304
2. S.M. Grundy, H.B. Brewer Jr., J.I. Cleeman, S.C. Smith Jr., and C. Lenfant Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition Circulation 109 2004 433 438
3. R.B. Ervin Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003-2006 Natl Health Stat Report 13 2009 1 7
4. J.C. King Maternal obesity, metabolism, and pregnancy outcomes Annu Rev Nutr 26 2006 271 291
5. N.J. Sebire, M. Jolly, and J.P. Harris Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London Int J Obes Relat Metab Disord 25 2001 1175 1182
6. R. Buettner, K.G. Parhofer, and M. Woenckhaus Defining high-fat-diet rat models: metabolic and molecular effects of different fat types J Mol Endocrinol 36 2006 485 501
7. T.Y. Reuter Diet-induced models for obesity and type 2 diabetes Drug Discov Today Dis Models 4 2007 3 8
8. M. Angela, M. Gadja, M.A. Pellizzon, M.R. Ricci, and E.A. Ulman Diet-induced metabolic syndrome in rodent models Animal Lab News 2007
9. H.N. Jones, L.A. Woollett, N. Barbour, P.D. Prasad, T.L. Powell, and T. Jansson High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice FASEB J 23 2009 271 278
10. Y.W. Park, S. Zhu, L. Palaniappan, S. Heshka, M.R. Carnethon, and S.B. Heymsfield The metabolic syndrome: prevalence and associated risk factor findings in the US population from the third national health and nutrition examination survey, 1988-1994 Arch Intern Med 163 2003 427 436
11. R. Dhingra, L. Sullivan, and P.F. Jacques Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community Circulation 116 2007 480 488
12. C. Zhang, M.B. Schulze, C.G. Solomon, and F.B. Hu A prospective study of dietary patterns, meat intake and the risk of gestational diabetes mellitus Diabetologia 49 2006 2604 2613
13. K. Holemans, S. Caluwaerts, L. Poston, and F.A. Van Assche Diet-induced obesity in the rat: a model for gestational diabetes mellitus Am J Obstet Gynecol 190 2004 858 865
14. A.E. Frias, T.K. Morgan, and A.E. Evans Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition Endocrinology 152 2011 2456 2464
15. D.S. Feig, and R.G. Moses Metformin therapy during pregnancy: good for the goose and good for the gosling too? Diabetes Care 34 2011 2329 2330
16. S.S. Thatcher, and E.M. Jackson Pregnancy outcome in infertile patients with polycystic ovary syndrome who were treated with metformin Fertil Steril 85 2006 1002 1009
17. C.J. Glueck, H. Phillips, D. Cameron, L. Sieve-Smith, and P. Wang Continuing metformin throughout pregnancy in women with polycystic ovary syndrome appears to safely reduce first-trimester spontaneous abortion: a pilot study Fertil Steril 75 2001 46 52
18. J.A. Rowan, W.M. Hague, W. Gao, M.R. Battin, and M.P. Moore Metformin versus insulin for the treatment of gestational diabetes N Engl J Med 358 2008 2003 2015
19. K. Isoda, J.L. Young, and A. Zirlik Metformin inhibits proinflammatory responses and nuclear factor-kappaB in human vascular wall cells Arterioscler Thromb Vasc Biol 26 2006 611 617
20. P. Dandona, A. Aljada, and H. Ghanim Increased plasma concentration of macrophage migration inhibitory factor (MIF) and MIF mRNA in mononuclear cells in the obese and the suppressive action of metformin J Clin Endocrinol Metab 89 2004 5043 5047
21. Y.P. Keepers, P.E. Pizao, G.J. Peters, J. van Ark-Otte, B. Winograd, and H.M. Pinedo Comparison of the sulforhodamine B protein and tetrazolium (MTT) assays for in vitro chemosensitivity testing Eur J Cancer 27 1991 897 900
22. P. Skehan, R. Storeng, and D. Scudiero New colorimetric cytotoxicity assay for anticancer-drug screening J Natl Cancer Inst 82 1990 1107 1112
23. J.E. Ramsay, W.R. Ferrell, L. Crawford, A.M. Wallace, I.A. Greer, and N. Sattar Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways J Clin Endocrinol Metab 87 2002 4231 4237
24. G.S. Hotamisligil, N.S. Shargill, and B.M. Spiegelman Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 259 1993 87 91
25. R. Feinstein, H. Kanety, M.Z. Papa, B. Lunenfeld, and A. Karasik Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates J Biol Chem 268 1993 26055 26058
26. S.K. Fried, D.A. Bunkin, and A.S. Greenberg Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid J Clin Endocrinol Metab 83 1998 847 850
27. P. Sartipy, and D.J. Loskutoff Monocyte chemoattractant protein 1 in obesity and insulin resistance Proc Natl Acad Sci U S A 100 2003 7265 7270
28. J.P. Bastard, M. Maachi, and C. Lagathu Recent advances in the relationship between obesity, inflammation, and insulin resistance Eur Cytokine Netw 17 2006 4 12
29. I. Nieto-Vazquez, S. Fernandez-Veledo, D.K. Kramer, R. Vila-Bedmar, L. Garcia-Guerra, and M. Lorenzo Insulin resistance associated to obesity: the link TNF-alpha Arch Physiol Biochem 114 2008 183 194
30. M. Schmatz, J. Madan, T. Marino, and J. Davis Maternal obesity: the interplay between inflammation, mother and fetus J Perinatol 30 2010 441 446
31. R.K. Creasy Creasy and Resnik's maternal-fetal medicine: principles and practice 6th ed. 2009 Saunders/Elsevier Philadelphia
32. J.P. Kirwan, S. Hauguel-De Mouzon, and J. Lepercq TNF-alpha is a predictor of insulin resistance in human pregnancy Diabetes 51 2002 2207 2213
33. T. Radaelli, A. Varastehpour, P. Catalano, and S. Hauguel-de Mouzon Gestational diabetes induces placental genes for chronic stress and inflammatory pathways Diabetes 52 2003 2951 2958
34. C.E. McCurdy, J.M. Bishop, and S.M. Williams Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates J Clin Invest 119 2009 323 335
35. G. Fantuzzi, and R. Faggioni Leptin in the regulation of immunity, inflammation, and hematopoiesis J Leuko Biol 68 2000 437 446
36. M. Lappas, K. Yee, M. Permezel, and G.E. Rice Release and regulation of leptin, resistin and adiponectin from human placenta, fetal membranes, and maternal adipose tissue and skeletal muscle from normal and gestational diabetes mellitus-complicated pregnancies J Endocrinol 186 2005 457 465
37. I. Shimomura, R.E. Hammer, S. Ikemoto, M.S. Brown, and J.L. Goldstein Leptin reverses insulin resistance and diabetes mellitus in mice with congenital lipodystrophy Nature 401 1999 73 76
38. O. Ogueh, S. Sooranna, K.H. Nicolaides, and M.R. Johnson The relationship between leptin concentration and bone metabolism in the human fetus J Clin Endocrinol Metab 85 2000 1997 1999
39. C.J. Ashworth, N. Hoggard, L. Thomas, J.G. Mercer, J.M. Wallace, and R.G. Lea Placental leptin Rev Reprod 5 2000 18 24
40. L. Morin-Papunen, K. Rautio, A. Ruokonen, P. Hedberg, M. Puukka, and J.S. Tapanainen Metformin reduces serum C-reactive protein levels in women with polycystic ovary syndrome J Clin Endocrinol Metab 88 2003 4649 4654
41. E. Diamanti-Kandarakis, T. Paterakis, and K. Alexandraki Indices of low-grade chronic inflammation in polycystic ovary syndrome and the beneficial effect of metformin Hum Reprod 21 2006 1426 1431
42. Y. Hattori, K. Suzuki, S. Hattori, and K. Kasai Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells Hypertension 47 2006 1183 1188
43. M.A. Suckow, S.H. Weisbroth, and C.L. Franklin The laboratory rat 2nd ed. 2006 Elsevier Boston
44. Glucophage (metformin hydrochloride tablets) Label Information. Available at: http://www.accessdata.fda.gov/drugsatfda-docs/label/2008/020357s031, 021202s016lbl.pdf. Accessed: March 15, 2010.
45. B. Charles, R. Norris, X. Xiao, and W. Hague Population pharmacokinetics of metformin in late pregnancy Ther Drug Monit 28 2006 67 72
46. E. Vanky, K. Zahlsen, O. Spigset, and S.M. Carlsen Placental passage of metformin in women with polycystic ovary syndrome Fertil Steril 83 2005 1575 1578
47. G.J. Howie, D.M. Sloboda, T. Kamal, and M.H. Vickers Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet J Physiol 587 2009 905 915
48. A.M. Samuelsson, P.A. Matthews, and M. Argenton Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming Hypertension 51 2008 383 392
49. E. Bytautiene, E. Tamayo, and T. Kechichian Prepregnancy obesity and sFlt1-induced preeclampsia in mice: developmental programming model of metabolic syndrome Am J Obstet Gynecol 204 2011 398.e1 398.e8
50. M.J. Zhu, M. Du, P.W. Nathanielsz, and S.P. Ford Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta Placenta 31 2010 387 391
51. S. Wang, J. Xu, P. Song, B. Viollet, and M.H. Zou In vivo activation of AMP-activated protein kinase attenuates diabetes-enhanced degradation of GTP cyclohydrolase I Diabetes 58 2009 1893 1901
52. R. Viana, C. Aguado, and I. Esteban Role of AMP-activated protein kinase in autophagy and proteasome function Biochem Biophys Res Comm 369 2008 964 968
53. Z. Chen, J. Hagler, and V.J. Palombella Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway Genes Dev 9 1995 1586 1597
54. S. Srividhya, M.K. Ravichandran, and C.V. Anuradha Metformin attenuates blood lipid peroxidation and potentiates antioxidant defense in high fructose-fed rats J Biochem Mol Biol Biophys 6 2002 379 385
55. A. Nerstedt, A. Johansson, C.X. Andersson, E. Cansby, U. Smith, and M. Mahlapuu AMP-activated protein kinase inhibits IL-6-stimulated inflammatory response in human liver cells by suppressing phosphorylation of signal transducer and activator of transcription 3 (STAT3) Diabetologia 53 2010 2406 2416
56. R. Mathur, C.J. Alexander, J. Yano, B. Trivax, and R. Azziz Use of metformin in polycystic ovary syndrome Am J Obstet Gynecol 199 2008 596 609
57. C. Gilbert, M. Valois, and G. Koren Pregnancy outcome after first-trimester exposure to metformin: a meta-analysis Fertil Steril 86 2006 658 663
58. C.J. Glueck, P. Wang, S. Kobayashi, H. Phillips, and L. Sieve-Smith Metformin therapy throughout pregnancy reduces the development of gestational diabetes in women with polycystic ovary syndrome Fertil Steril 77 2002 520 525
59. P.M. Catalano, and S. Hauguel-De Mouzon Is it time to revisit the Pedersen hypothesis in the face of the obesity epidemic? Am J Obstet Gynecol 204 2011 479 487