NOD1 expression is increased in the adipose tissue of women with gestational diabetes

Journal of Endocrinology

Volumn 222, Issue 1, 2014, Pages 99-112

  Lappas, Martha ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

Adipose tissue; Gestational diabetes; Inflammation; Insulin resistance; NOD1

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CYCLOOXYGENASE 2; G DEXTRO GLUTAMYL MESO DIAMINOPIMELIC ACID; GELATINASE B; GLUCOSE TRANSPORTER 4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MURAMYL DIPEPTIDE; PROSTACYCLIN; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CLINICAL ARTICLE; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN TISSUE; INFLAMMATION; INSULIN RESISTANCE; MATERNAL OBESITY; OMENTUM; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROSTAGLANDIN SYNTHESIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT;

ADIPOSE TISSUE; GESTATIONAL DIABETES; INFLAMMATION; INSULIN RESISTANCE; NOD1;

ADIPOSE TISSUE; ADULT; CASE-CONTROL STUDIES; CYCLOOXYGENASE 2; DIABETES, GESTATIONAL; FEMALE; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTERCELLULAR ADHESION MOLECULE-1; MATRIX METALLOPROTEINASE 9; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; PREGNANCY; PREGNANCY COMPLICATIONS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84904411015     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0179     Document Type: Article

References (63)

1. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J & Karin M 2005 IKK-b links inflammation to obesity-induced insulin resistance. Nature Medicine 11 191-198
2. Bouloumie A, Sengenes C, Portolan G, Galitzky J & Lafontan M 2001 Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50 2080-2086
3. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. 2007 Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 1761-1772
4. Catalano PM, Nizielski SE, Shao JH, Preston L, Qiao LP & Friedman JE 2002 Downregulated IRS-1 and PPARg in obese women with gestational diabetes: relationship to FFA during pregnancy. American Journal of Physiology. Endocrinology and Metabolism 282 E522-E533
5. ChamaillardM, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, FukaseK, Kusumoto S,, et al. 2003Anessential role forNOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nature Immunology 4 702-707
6. Chang YC, Liu PH, Tsai YC, Chiu YF, Shih SR, Ho LT, Lee WJ, Lu CH, Quertermous T, Curb JD,, et al. 2012 Genetic variation in the carbonyl reductase 3 gene confers risk of type 2 diabetes and insulin resistance: a potential regulator of adipogenesis. Journal of Molecular Medicine 90 847-858
7. Colomiere M, Permezel M & Lappas M 2010 Diabetes and obesity during pregnancy alter insulin signalling and glucose transporter expression in maternal skeletal muscle and subcutaneous adipose tissue. Journal of Molecular Endocrinology 44 213-223
8. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, Roumain J, Bennett PH & Knowler WC 2000 Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 49 2208-2211
9. Ferrara A 2007 Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care 30(Suppl 2) S141-S146
10. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA,, et al. 2007 Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 116 39-48
11. Galis ZS & Khatri JJ 2002 Matrix metalloproteinases in vascular remodeling and atherogenesis - the good, the bad, and the ugly. Circulation Research 90 251-262
12. Garvey WT, Maianu L, Zhu JH, Hancock JA & Golichowski AM 1993 Multiple defects in the adipocyte glucose transport system cause cellular insulin resistance in gestational diabetes. Heterogeneity in the number and a novel abnormality in subcellular localization of GLUT4 glucose transporters. Diabetes 42 1773-1785
13. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ & Sansonetti PJ 2003 Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. Journal of Biological Chemistry 278 8869-8872
14. Goncalves FM, Jacob-Ferreira AL, Gomes VA, Casella-Filho A, Chagas AC, Marcaccini AM, Gerlach RF & Tanus-Santos JE 2009 Increased circulating levels of matrix metalloproteinase (MMP)-8, MMP-9, and pro-inflammatory markers in patients with metabolic syndrome. Clinica Chimica Acta 403 173-177
15. Gonzalez-Ortiz M, Martinez-Abundis E, Balcazar-Munoz BR & Robles-Cervantes JA 2001 Inhibition of cyclooxygenase-1 or -2 on insulin sensitivity in healthy subjects. Hormone and Metabolic Research 33 250-253
16. Guler S, Cakir B, Demirbas B, Yonem A, Odabasi E, Onde U, Aykut O & Gursoy G 2002 Plasma soluble intercellular adhesion molecule 1 levels are increased in type 2 diabetic patients with nephropathy. Hormone Research 58 67-70
17. Henkel J, Neuschafer-Rube F, Pathe-Neuschafer-Rube A & Puschel GP 2009 Aggravation by prostaglandin E2 of interleukin-6-dependent insulin resistance in hepatocytes. Hepatology 50 781-790
18. Henkel J, Frede K, Schanze N, Vogel H, Schurmann A, Spruss A, Bergheim I & Puschel GP 2012 Stimulation of fat accumulation in hepatocytes by PGE2-dependent repression of hepatic lipolysis, b-oxidation and VLDLsynthesis. Laboratory Investigation 92 1597-1606
19. Hsieh PS, Tsai HC, Kuo CH, Chan JY, Shyu JF, Cheng WT & Liu TT 2008 Selective COX2 inhibition improves whole body and muscular insulin resistance in fructose-fed rats. European Journal of Clinical Investigation 38 812-819
20. Inohara N & Nunez G 2003 NODs: intracellular proteins involved in inflammation and apoptosis. Nature Reviews. Immunology 3 371-382
21. Kautzky-Willer A, Fasching P, Jilma B, Waldhausl W & Wagner OF 1997 Persistent elevation and metabolic dependence of circulating E-selectin after delivery in women with gestational diabetes mellitus. Journal of Clinical Endocrinology and Metabolism 82 4117-4121
22. Kent JW, Comuzzie AG, Mahaney MC, Almasy L, Rainwater DL, VandeBerg JL, MacCluer JW & Blangero J 2004 Intercellular adhesion molecule-1 concentration is genetically correlated with insulin resistance, obesity, and HDL concentration in Mexican Americans. Diabetes 53 2691-2695
23. Kern PA, Ranganathan S, Li C, Wood L & Ranganathan G 2001 Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. American Journal of Physiology. Endocrinology and Metabolism 280 E745-E751.
24. Kim C, Berger DK & Chamany S 2007 Recurrence of gestational diabetes mellitus: a systematic review. Diabetes Care 30 1314-1319
25. Knock GA, McCarthy AL, Lowy C & Poston L 1997 Association of gestational diabetes with abnormal maternal vascular endothelial function. British Journal of Obstetrics and Gynaecology 104 229-234
26. Krauss T, Emons G, Kuhn W & Augustin HG 2002 Predictive value of routine circulating soluble endothelial cell adhesion molecule measurements during pregnancy. Clinical Chemistry 48 1418-1425
27. Kuzmicki M, Telejko B, Szamatowicz J, Zonenberg A, Nikolajuk A, Kretowski A & Gorska M 2009 High resistin and interleukin-6 levels are associated with gestational diabetes mellitus. Gynecological Endocrinology 25 258-263
28. Kuzmicki M, Telejko B, Wawrusiewicz-Kurylonek N, Citko A, Lipinska D, Pliszka J, Wilk J, Kalejta K, Lemancewicz A, Grabiec M,, et al. 2012 The expression of suppressor of cytokine signaling 1 and 3 in fat and placental tissue from women with gestational diabetes. Gynecological Endocrinology 28 841-844
29. Kvarnhammar AM, Tengroth L, Adner M & Cardell LO 2013 Innate immune receptors in human airway smooth muscle cells: activation by TLR1/2, TLR3, TLR4, TLR7 and NOD1 agonists. PLoS ONE 8 e68701
30. Laimer M, Kaser S, Kranebitter M, Sandhofer A, Muhlmann G, Schwelberger H, Weiss H, Patsch JR & Ebenbichler CF 2005 Effect of pronounced weight loss on the nontraditional cardiovascular risk marker matrix metalloproteinase-9 inmiddle-agedmorbidly obesewomen. International Journal of Obesity 29 498-501
31. Lain KY & Catalano PM 2007 Metabolic changes in pregnancy. Clinical Obstetrics and Gynecology 50 938-948
32. Laitinen K, Poussa T, Isolauri E, Nutrition AMI & Intestinal Microbiota G 2009 Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. British Journal of Nutrition 101 1679-1687
33. Lappas M 2013a NOD1 and NOD2 regulate proinflammatory and prolabor mediators in human fetal membranes and myometrium via nuclear factor-kB. Biology of Reproduction 89 14
34. Lappas M 2013b Activation of inflammasomes in adipose tissue of women with gestational diabetes. Molecular and Cellular Endocrinology 382 74-83
35. Lappas M 2014a Effect of pre-existing maternal obesity, gestational diabetes and adipokines on the expression of genes involved in lipid metabolism in adipose tissue. Metabolism 63 250-262
36. Lappas M 2014b Markers of endothelial cell dysfunction are increased in human omental adipose tissue from women with pre-existing maternal obesity and gestational diabetes. Metabolism 63 860-873
37. Lappas M, Permezel M & Rice GE 2005a Leptin and adiponectin stimulate the release of proinflammatory cytokines and prostaglandins fromhuman placenta and maternal adipose tissue via nuclear factor-kB, peroxisomal proliferator-activated receptor-g and extracellularly regulated kinase 1/2. Endocrinology 146 3334-3342
38. Lappas M, Yee K, Permezel M & Rice GE 2005b 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. Journal of Endocrinology 186 457-465
39. Lappas M, Yee K, Permezel M & Rice GE 2005c Sulfasalazine and BAY 11-7082 interfere with the nuclear factor-kB and IkB kinase pathway to regulate the release of proinflammatory cytokines from human adipose tissue and skeletal muscle in vitro. Endocrinology 146 1491-1497
40. Lappas M, Permezel M & Rice GE 2006 15-Deoxy-D12,14-prostaglandin J2 and troglitazone regulation of the release of phospholipid metabolites, inflammatory cytokines and proteases from human gestational tissues. Placenta 27 1060-1072
41. Lappas M, Andrikopoulos S & Permezel M 2012 Hypoxanthine-xanthine oxidase down-regulates GLUT1 transcription via SIRT1 resulting in decreased glucose uptake in human placenta. Journal of Endocrinology 213 49-57
42. Leinonen E, Hurt-Camejo E, Wiklund O, Hulten LM, Hiukka A & Taskinen MR 2003 Insulin resistance and adiposity correlate with acute-phase reaction and soluble cell adhesion molecules in type 2 diabetes. Atherosclerosis 166 387-394
43. Mordwinkin NM, Ouzounian JG, Yedigarova L, Montoro MN, Louie SG & Rodgers KE 2013 Alteration of endothelial function markers in women with gestational diabetes and their fetuses. Journal of Maternal-Fetal & Neonatal Medicine 26 507-512
44. Morisset AS, Dube MC, Cote JA, Robitaille J, Weisnagel SJ & Tchernof A 2011 Circulating interleukin-6 concentrations during and after gestational diabetes mellitus. Acta Obstetricia et Gynecologica Scandinavica 90 524-530
45. Nieto-Vazquez I, Fernandez-Veledo S, de Alvaro C & Lorenzo M 2008 Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle. Diabetes 57 3211-3221
46. Nishio H, Kanno S, Onoyama S, Ikeda K, Tanaka T, Kusuhara K, Fujimoto Y, Fukase K, Sueishi K & Hara T 2011 Nod1 ligands induce site-specific vascular inflammation. Arteriosclerosis, Thrombosis, and Vascular Biology 31 1093-1099
47. Oliva K, Barker G, Rice GE, Bailey MJ & Lappas M2013 2D-DIGE to identify proteins associated with gestational diabetes in omental adipose tissue. Journal of Endocrinology 218 165-178
48. Pleiner J, Mittermayer F, Langenberger H, Winzer C, Schaller G, Pacini G, Kautzky-Willer A, Tura A & Wolzt M 2007 Impaired vascular nitric oxide bioactivity in women with previous gestational diabetes. Wiener KlinischeWochenschrift 119 483-489
49. Pradhan AD, Manson JE, Rifai N, Buring JE & Ridker PM 2001 C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. Journal of the American Medical Association 286 327-334
50. Purohit JS, Hu P, Burke SJ, Collier JJ, Chen JG & Zhao L 2013 The effects of NOD activation on adipocyte differentiation. Obesity 21 737-747
51. Radaelli T, Uvena-Celebrezze J, Minium J, Huston-Presley L, Catalano P & Hauguel-de Mouzon S 2006 Maternal interleukin-6: marker of fetal growth and adiposity. Journal of the Society for Gynecologic Investigation 13 53-57
52. Schertzer JD, Tamrakar AK, Magalhaes JG, Pereira S, Bilan PJ, Fullerton MD, Liu Z, Steinberg GR, Giacca A, Philpott DJ, et al. 2011 NOD1 activators link innate immunity to insulin resistance. Diabetes 60 2206-2215
53. Senn JJ, Klover PJ, Nowak IA & Mooney RA 2002 Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 51 3391-3399
54. Sobngwi E, Boudou P, Mauvais-Jarvis F, Leblanc H, Velho G, Vexiau P, Porcher R, Hadjadj S, Pratley R, Tataranni PA, et al. 2003 Effect of a diabetic environment in utero on predisposition to type 2 diabetes. Lancet 361 1861-1865
55. Streuli C 1999 Extracellular matrix remodelling and cellular differentiation. Current Opinion in Cell Biology 11 634-640
56. Strober W, Murray PJ, Kitani A & Watanabe T 2006 Signalling pathways and molecular interactions of NOD1 and NOD2. Nature Reviews. Immunology 6 9-20
57. Tsai WH, Huang DY, Yu YH, Chen CY & LinWW2011 Dual roles of NOD2 in TLR4-mediated signal transduction and -induced inflammatory gene expression in macrophages. Cellular Microbiology 13 717-730
58. Winzer C, Wagner O, Festa A, Schneider B, Roden M, Bancher-Todesca D, Pacini G, Funahashi T & Kautzky-Willer A 2004 Plasma adiponectin, insulin sensitivity, and subclinical inflammation in women with prior gestational diabetes mellitus. Diabetes Care 27 1721-1727
59. Wong CK, Hu SQ, Leung KM, Dong J, He L, Chu YJ, Chu IM, Qiu HN, Liu KY & LamCW2013 NOD-like receptors mediated activation of eosinophils interacting with bronchial epithelial cells: a link between innate immunity and allergic asthma. Cellular & Molecular Immunology 10 317-329
60. Yi-Jun Z, Ai L, Yu-Ling S, Yan L & Hui Y 2012 Nucleotide-binding oligomerization domain-1 ligand induces inflammation and attenuates glucose uptake in human adipocytes. Chinese Medical Sciences Journal 27 147-152.
61. Yu F, Xue YM, Li CZ, Shen J, Gao F, Yu YH & Fu XJ 2007 Association of serum interleukin-6 and high-sensitivity C-reactive protein levels with insulin resistance in gestational diabetes mellitus. Nan Fang Yi Ke Da Xue Xue Bao 27 799-801
62. Zhao L, Hu P, Zhou Y, Purohit J & Hwang D 2011 NOD1 activation induces proinflammatory gene expression and insulin resistance in 3T3-L1 adipocytes. American Journal of Physiology. Endocrinology and Metabolism 301 E587-E598
63. Zhou YJ, Zhou H, Li Y & Song YL 2012 NOD1 activation induces innate immune responses and insulin resistance in human adipocytes. Diabetes & Metabolism 38 538-543