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Preeclampsia pp 113-124 | Cite as

Obesity, Adipokines, and Lipokines

  • Katsuhiko NaruseEmail author
Chapter
Part of the Comprehensive Gynecology and Obstetrics book series (CGO)

Abstract

Obesity during pregnancy is increasing in frequency worldwide. Similar to other complications, obesity is a strong risk factor for hypertensive disorders in pregnancy (HDP). The mechanisms of this vicious cycle, unclear up to the last century, have recently been elucidated in the field of internal medicine, where adipose tissue was found to be an important endocrine organ in the human body that releases several immunoactive molecules in high concentrations. In addition to circulating lipids and lipids subjected to oxidative stress, novel cytokines derived from adipocytes or other cells of the adipose tissue (adipokines and lipokines) enhance the pathological effects of HDP. Some adipokines behave in HDP in the same way as in hypertension or metabolic syndrome in nonpregnant subjects, but a few adipokines in pregnancy or HDP act differently from insulin-resistant syndromes. In addition, during normal pregnancy, insulin resistance is an important process for fetal growth, labor, and breastfeeding, and molecules produced by adipose tissue seem to act an immunologically critical role in HDP.

Keywords

Adipokine Adipose tissue Fatty acids Lipokine Obesity 

References

  1. 1.
    Denison FC, Roberts KA, Barr SM, Norman JE. Obesity, pregnancy, inflammation, and vascular function. Reproduction. 2010;140:373–85.  https://doi.org/10.1530/REP-10-0074.CrossRefPubMedGoogle Scholar
  2. 2.
    Takagi K, Yamasaki M, Nakamoto O, Saito S, Suzuki H. A review of best practice guide 2015 for care and treatment of hypertension in pregnancy. Hypertens Res Pregnancy. 2015;3:65–103.  10.14390/jsshp.3.105.CrossRefGoogle Scholar
  3. 3.
    Mitchell S, Shaw D. The worldwide epidemic of female obesity. Best Pract Res Clin Obstet Gynaecol. 2015;29:289–99.  https://doi.org/10.1016/j.bpobgyn.2014.10.002.CrossRefPubMedGoogle Scholar
  4. 4.
    Mission JF, Marshall NE, Caughey AB. Obesity in pregnancy: a big problem and getting bigger. Obstet Gynecol Surv. 2013;68:389–99.  https://doi.org/10.1097/OGX.0b013e31828738ce.CrossRefPubMedGoogle Scholar
  5. 5.
    Morikawa M, Yamada T, Yamada T, Sato S, Cho K, Minakami H. Prevalence of hyperglycemia during pregnancy according to maternal age and pre-pregnancy body mass index in Japan, 2007-2009. Int J Gynaecol Obstet. 2012;118:198–201.  https://doi.org/10.1016/j.ijgo.2012.04.019.CrossRefPubMedGoogle Scholar
  6. 6.
    Enomoto K, Aoki S, Toma R, Fujiwara K, Sakamaki K, Hirahara F. Pregnancy outcomes based on pre-pregnancy body mass index in Japanese women. PLoS One. 2016;11:e0157081.  https://doi.org/10.1371/journal.pone.0157081.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Santangeli L, Sattar N, Huda SS. Impact of maternal obesity on perinatal and childhood outcomes. Best Pract Res Clin Obstet Gynaecol. 2015;29:438–48.  https://doi.org/10.1016/j.bpobgyn.2014.10.009.CrossRefPubMedGoogle Scholar
  8. 8.
    Myatt L, Maloyan A. Obesity and placental function. Semin Reprod Med. 2016;34:42–9.  https://doi.org/10.1055/s-0035-1570027.CrossRefPubMedGoogle Scholar
  9. 9.
    Spradley FT, Palei AC, Granger JP. Immune mechanisms linking obesity and preeclampsia. Biomolecules. 2015;5:3142–76.  https://doi.org/10.3390/biom5043142.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Gallos ID, Sivakumar K, Kilby MD, Coomarasamy A, Thangaratinam S, Vatish M. Pre-eclampsia is associated with, and preceded by, hypertriglyceridaemia: a meta-analysis. BJOG. 2013;120:1321–32.  https://doi.org/10.1111/1471-0528.12375.CrossRefPubMedGoogle Scholar
  11. 11.
    Zavalza-Gómez AB. Obesity and oxidative stress: a direct link to preeclampsia? Arch Gynecol Obstet. 2011;283:415–22.  https://doi.org/10.1007/s00404-010-1753-1.CrossRefPubMedGoogle Scholar
  12. 12.
    Gupta S, Aziz N, Sekhon L, Agarwal R, Mansour G, Li J, et al. Lipid peroxidation and antioxidant status in preeclampsia: a systematic review. Obstet Gynecol Surv. 2009;64:750–9.  https://doi.org/10.1097/OGX.0b013e3181bea0ac.CrossRefPubMedGoogle Scholar
  13. 13.
    Morisaki N, Nagata C, Jwa SC, Sago H, Saito S, Oken E, et al. Pre-pregnancy BMI-specific optimal gestational weight gain for women in Japan. J Epidemiol. 2017;27:492–8.  https://doi.org/10.1016/j.je.2016.09.013.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Masuyama H, Segawa T, Sumida Y, Masumoto A, Inoue S, Akahori Y, et al. Different profiles of circulating angiogenic factors and adipocytokines between early- and late-onset pre-eclampsia. BJOG. 2010;117:314–20.  https://doi.org/10.1111/j.1471-0528.2009.02453.x.CrossRefPubMedGoogle Scholar
  15. 15.
    Ramsay JE, Jamieson N, Greer IA, Sattar N. Paradoxical elevation in adiponectin concentrations in women with preeclampsia. Hypertension. 2003;42:891–4.CrossRefPubMedGoogle Scholar
  16. 16.
    Otun HA, Lash GE, Innes BA, Bulmer JN, Naruse K, Hannon T, et al. Effect of tumour necrosis factor-α in combination with interferon-γ on first trimester extravillous trophoblast invasion. J Reprod Immunol. 2011;88:1–11.  https://doi.org/10.1016/j.jri.2010.10.003. CrossRefPubMedGoogle Scholar
  17. 17.
    Haider S, Knöfler M. Human tumour necrosis factor: physiological and pathological roles in placenta and endometrium. Placenta. 2009;30:111–23.  https://doi.org/10.1016/j.placenta.2008.10.012.CrossRefPubMedGoogle Scholar
  18. 18.
    Kupferminc MJ, Peaceman AM, Wigton TR, Rehnberg KA, Socol ML. Tumor necrosis factor-alpha is elevated in plasma and amniotic fluid of patients with severe preeclampsia. Am J Obstet Gynecol. 1994;170:1752–7.CrossRefPubMedGoogle Scholar
  19. 19.
    Pijnenborg R, McLaughlin PJ, Vercruysse L, Hanssens M, Johnson PM, Keith JC, et al. Immunolocalization of tumour necrosis factor-alpha (TNF-alpha) in the placental bed of normotensive and hypertensive human pregnancies. Placenta. 1998;19:231–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Opsjøn SL, Novick D, Wathen NC, Cope AP, Wallach D, Aderka D. Soluble tumor necrosis factor receptors and soluble interleukin-6 receptor in fetal and maternal sera, coelomic and amniotic fluids in normal and pre-eclamptic pregnancies. J Reprod Immunol. 1995;29:119–34.CrossRefPubMedGoogle Scholar
  21. 21.
    Kaneko K, Sugitani M, Goto M, Murashima A. Tocilizumab and pregnancy: four cases of pregnancy in young women with rheumatoid arthritis refractory to anti-TNF biologics with exposure to tocilizumab. Mod Rheumatol. 2016;26:672–5.  https://doi.org/10.3109/14397595.2016.1140256.CrossRefPubMedGoogle Scholar
  22. 22.
    LaMarca B, Speed J, Fournier L, Babcock SA, Berry H, Cockrell K, et al. Hypertension in response to chronic reductions in uterine perfusion in pregnant rats: effect of tumor necrosis factor-alpha blockade. Hypertension. 2008;52:1161–7.  https://doi.org/10.1161/HYPERTENSIONAHA.108.120881.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Weedon-Fekjær MS, Sheng Y, Sugulle M, Johnsen GM, Herse F, Redman CW, et al. Placental miR-1301 is dysregulated in early-onset preeclampsia and inversely correlated with maternal circulating leptin. Placenta. 2014;35:709–17.  https://doi.org/10.1016/j.placenta.2014.07.002.CrossRefPubMedGoogle Scholar
  24. 24.
    Molvarec A, Szarka A, Walentin S, Beko G, Karádi I, Prohászka Z, et al. Serum leptin levels in relation to circulating cytokines, chemokines, adhesion molecules and angiogenic factors in normal pregnancy and preeclampsia. Reprod Biol Endocrinol. 2011;9:124.  https://doi.org/10.1186/1477-7827-9-124.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Chrelias G, Makris GM, Papanota AM, Spathis A, Salamalekis G, Sergentanis TN, et al. Serum inhibin and leptin: risk factors for pre-eclampsia? Clin Chim Acta. 2016;463:84–7.  https://doi.org/10.1016/j.cca.2016.10.013.CrossRefPubMedGoogle Scholar
  26. 26.
    Naruse K, Yamasaki M, Umekage H, Sado T, Sakamoto Y, Morikawa H. Peripheral blood concentrations of adiponectin, an adipocyte-specific plasma protein, in normal pregnancy and preeclampsia. J Reprod Immunol. 2005;65:65–75.CrossRefPubMedGoogle Scholar
  27. 27.
    Khosrowbeygi A, Ahmadvand H. Positive correlation between serum levels of adiponectin and homocysteine in pre-eclampsia. J Obstet Gynaecol Res. 2013;39:641–6.  https://doi.org/10.1111/j.1447-0756.2012.02015.x.CrossRefPubMedGoogle Scholar
  28. 28.
    Masuyama H, Nobumoto E, Inoue S, Hiramatsu Y. Potential interaction of brain natriuretic peptide with hyperadiponectinemia in preeclampsia. Am J Physiol Endocrinol Metab. 2012;302:E687–93.  https://doi.org/10.1152/ajpendo.00548.2011.CrossRefPubMedGoogle Scholar
  29. 29.
    Naruse K, Yamasaki Y, Tsunemi T, Onogi A, Noguchi T, Sado T, et al. Increase of high molecular weight adiponectin in hypertensive pregnancy was correlated with brain-type natriuretic peptide stimulation on adipocyte. Pregnancy Hypertens. 2011;1:200–5.  https://doi.org/10.1016/j.preghy.2011.07.004.CrossRefPubMedGoogle Scholar
  30. 30.
    D’Anna R, Baviera G, Corrado F, Giordano D, De Vivo A, Nicocia G, et al. Adiponectin and insulin resistance in early- and late-onset pre-eclampsia. BJOG. 2006;113:1264–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Mori T, Shinohara K, Wakatsuki A, Watanabe K, Fujimaki A. Adipocytokines and endothelial function in preeclamptic women. Hypertens Res. 2010;33:250–4.  https://doi.org/10.1038/hr.2009.222.CrossRefPubMedGoogle Scholar
  32. 32.
    Utzschneider KM, Carr DB, Tong J, Wallace TM, Hull RL, Zraika S, et al. Resistin is not associated with insulin sensitivity or the metabolic syndrome in humans. Diabetologia. 2005;48:2330–3.CrossRefPubMedGoogle Scholar
  33. 33.
    Lappas M, Yee K, Permezel M, Rice GE. 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. 2005;186:457–65.CrossRefPubMedGoogle Scholar
  34. 34.
    Chen D, Dong M, Fang Q, He J, Wang Z, Yang X. Alterations of serum resistin in normal pregnancy and preeclampsia. Clin Sci. 2005;108:81–4.CrossRefPubMedGoogle Scholar
  35. 35.
    Yura S, Sagawa N, Itoh H, Kakui K, Nuamah MA, Korita D, et al. Resistin is expressed in the human placenta. J Clin Endocrinol Metab. 2003;88:1394–7.CrossRefPubMedGoogle Scholar
  36. 36.
    Dechend R, Müller DN, Wallukat G, Homuth V, Krause M, Dudenhausen J, et al. AT1 receptor agonistic antibodies, hypertension, and preeclampsia. Semin Nephrol. 2004;24:571–9.CrossRefPubMedGoogle Scholar
  37. 37.
    Zhao L, Bracken MB, Dewan AT, Chen S. Association between the SERPINE1 (PAI-1) 4G/5G insertion/deletion promoter polymorphism (rs1799889) and pre-eclampsia: a systematic review and meta-analysis. Mol Hum Reprod. 2013;19:136–43.  https://doi.org/10.1093/molehr/gas056.CrossRefPubMedGoogle Scholar
  38. 38.
    Ito A, Suganami T, Miyamoto Y, Yoshimasa Y, Takeya M, Kamei Y, et al. Role of MAPK phosphatase-1 in the induction of monocyte chemoattractant protein-1 during the course of adipocyte hypertrophy. J Biol Chem. 2007;282:25445–52.CrossRefPubMedGoogle Scholar
  39. 39.
    Madan JC, Davis JM, Craig WY, Collins M, Allan W, Quinn R, et al. Maternal obesity and markers of inflammation in pregnancy. Cytokine. 2009;47:61–4.  https://doi.org/10.1016/j.cyto.2009.05.004.CrossRefPubMedGoogle Scholar
  40. 40.
    Naruse K, Noguchi T, Sado T, Tsunemi T, Shigetomi H, Kanayama S, et al. Chemokine and free fatty acid levels in insulin-resistant state of successful pregnancy: a preliminary observation. Mediat Inflamm. 2012;2012:432575.  https://doi.org/10.1155/2012/432575.CrossRefGoogle Scholar
  41. 41.
    Fasshauer M, Waldeyer T, Seeger J, Schrey S, Ebert T, Kratzsch J, et al. Serum levels of the adipokine visfatin are increased in pre-eclampsia. Clin Endocrinol (Oxf). 2008;69:69–73.CrossRefPubMedGoogle Scholar
  42. 42.
    Demir BC, Atalay MA, Ozerkan K, Doster Y, Ocakoglu G, Kucukkomurcu S. Maternal adiponectin and visfatin concentrations in normal and complicated pregnancies. Clin Exp Obstet Gynecol. 2013;40:261–7.PubMedGoogle Scholar
  43. 43.
    Montagnana M, Lippi G, Albiero A, Salvagno GL, Franchi M, Guidi GC. Serum pro-inflammatory cytokines in physiological and pre-eclamptic pregnancies. Gynecol Endocrinol. 2008;24:113–6.  https://doi.org/10.1080/09513590801895575.CrossRefPubMedGoogle Scholar
  44. 44.
    Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol. 1997;37:240–9.CrossRefPubMedGoogle Scholar
  45. 45.
    De Falco M, De Luca L, Onori N, Cavallotti I, Artigiano F, Esposito V, et al. Apelin expression in normal human tissues. In Vivo. 2002;16:333–6.PubMedGoogle Scholar
  46. 46.
    Simsek Y, Celik O, Yilmaz E, Karaer A, Dogan C, Aydin S, et al. Serum levels of apelin, salusin-alpha and salusin-beta in normal pregnancy and preeclampsia. J Matern Fetal Neonatal Med. 2012;25:1705–8.  https://doi.org/10.3109/14767058.2011.660221.CrossRefPubMedGoogle Scholar
  47. 47.
    Cobellis L, De Falco M, Mastrogiacomo A, Giraldi D, Dattilo D, Scaffa C, et al. Modulation of apelin and APJ receptor in normal and preeclampsia complicated placentas. Histol Histopathol. 2007;22:1–8.  10.14670/HH-22.1.PubMedGoogle Scholar
  48. 48.
    Inuzuka H, Nishizawa H, Inagaki A, Suzuki M, Ota S, Miyamura H, et al. Decreased expression of apelin in placentas from severe pre-eclampsia patients. Hypertens Pregnancy. 2013;32:410–21.  https://doi.org/10.3109/10641955.2013.813535.CrossRefPubMedGoogle Scholar
  49. 49.
    Harris WS, Connor WE, Alam N, Illingworth DR. Reduction of postprandial triglyceridemia in humans by dietary n-3 fatty acids. J Lipid Res. 1988;29:1451–60.PubMedGoogle Scholar
  50. 50.
    Marnett LJ. Lipid peroxidation-DNA damage by malondialdehyde. Mutat Res. 1999;424:83–95.CrossRefPubMedGoogle Scholar
  51. 51.
    Murdolo G, Piroddi M, Luchetti F, Tortoioli C, Canonico B, Zerbinati C, et al. Oxidative stress and lipid peroxidation by-products at the crossroad between adipose organ dysregulation and obesity-linked insulin resistance. Biochimie. 2013;95:585–94.  https://doi.org/10.1016/j.biochi.2012.12.014.CrossRefPubMedGoogle Scholar
  52. 52.
    Nakakita B, Mogami H, Kondoh E, Tsukamoto T, Yanagita M, Konishi I. Case of soluble fms-like tyrosine kinase 1 apheresis in severe pre-eclampsia developed at 15 weeks’ gestation. J Obstet Gynaecol Res. 2015;41:1661–3.  https://doi.org/10.1111/jog.12760.CrossRefPubMedGoogle Scholar
  53. 53.
    Thadhani R, Hagmann H, Schaarschmidt W, Roth B, Cingoez T, Karumanchi SA, et al. Removal of soluble Fms-like tyrosine Kinase-1 by dextran sulfate apheresis in preeclampsia. J Am Soc Nephrol. 2016;27:903–13.  https://doi.org/10.1681/ASN.2015020157.CrossRefPubMedGoogle Scholar
  54. 54.
    Kumasawa K, Ikawa M, Kidoya H, Hasuwa H, Saito-Fujita T, Morioka Y, et al. Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc Natl Acad Sci U S A. 2011;108:1451–5.  https://doi.org/10.1073/pnas.1011293108.CrossRefPubMedGoogle Scholar
  55. 55.
    Schaeffler I, Gross P, Buettner R, Bollheimer C, Buechler C, Neumeier M, et al. Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology. 2009;126:233–45.  https://doi.org/10.1111/j.1365-2567.2008.02892.x.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Schaefer-Graf UM, Graf K, Kulbacka I, Kjos SL, Dudenhausen J, Vetter K, et al. Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care. 2008;31:1858–63.  https://doi.org/10.2337/dc08-0039.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Chen X, Scholl TO. Association of elevated free fatty acids during late pregnancy with preterm delivery. Obstet Gynecol. 2008;112:297–303.  https://doi.org/10.1097/AOG.0b013e3181802150.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Villa PM, Laivuori H, Kajantie E, Kaaja R. Free fatty acid profiles in preeclampsia. Prostaglandins Leukot Essent Fatty Acids. 2009;81:17–21.  https://doi.org/10.1016/j.plefa.2009.05.002.CrossRefPubMedGoogle Scholar
  59. 59.
    Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, Hotamisligil GS. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell. 2008;134:933–44.  https://doi.org/10.1016/j.cell.2008.07.048.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Frigolet ME, Gutiérrez-Aguilar R. The role of the novel lipokine palmitoleic acid in health and disease. Adv Nutr. 2017;8:173S–81S.  https://doi.org/10.3945/an.115.011130.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, et al. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature. 2005;436:356–62.CrossRefPubMedGoogle Scholar
  62. 62.
    Vaisbuch E, Romero R, Mazaki-Tovi S, Erez O, Kim SK, Chaiworapongsa T, et al. Retinol binding protein 4—a novel association with early-onset preeclampsia. J Perinat Med. 2010;38:129–39.  https://doi.org/10.1515/JPM.2009.140.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Masuyama H, Inoue S, Hiramatsu Y. Retinol-binding protein 4 and insulin resistance in preeclampsia. Endocr J. 2011;58:47–53.CrossRefPubMedGoogle Scholar
  64. 64.
    Xu A, Wang Y, Xu JY, Stejskal D, Tam S, Zhang J, et al. Adipocyte fatty acid-binding protein is a plasma biomarker closely associated with obesity and metabolic syndrome. Clin Chem. 2006;52:405–13.CrossRefPubMedGoogle Scholar
  65. 65.
    Fasshauer M, Seeger J, Waldeyer T, Schrey S, Ebert T, Kratzsch J, et al. Serum levels of the adipokine adipocyte fatty acid-binding protein are increased in preeclampsia. Am J Hypertens. 2008;21:582–6.  https://doi.org/10.1038/ajh.2008.23.CrossRefPubMedGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.St. Barnabas’ HospitalOsaka CityJapan

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