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Bariatric Surgery

One-anastomosis gastric bypass modulates the serum levels of pro- and anti-inflammatory oxylipins, which may contribute to the resolution of inflammation

Abstract

Background/objectives

Oxylipins are polyunsaturated fatty acid derivatives involved in the regulation of various processes, including chronic inflammation, insulin resistance and hepatic steatosis. They can be synthesized in various tissues, including adipose tissue. There is some evidence that obesity is associated with the deregulation of serum oxylipin levels. The aim of this study was to evaluate the effect of bariatric surgery (one-anastomosis gastric bypass) on the serum levels of selected oxylipins and their fatty acid precursors and to verify the hypothesis that their changes after surgery can contribute to the resolution of inflammation. Moreover, we compared the oxylipin levels (prostaglandin E2, 13-HODE, maresin 1 and resolvin E1), fatty acids and the expression of enzymes that synthesize oxylipins in adipose tissue of lean controls and subjects with severe obesity.

Subjects/methods

The study included 50 patients with severe obesity that underwent bariatric surgery and 41 subjects in lean, control group. Fatty acid content was analyzed by GC-MS, oxylipin concentrations were measured with immunoenzymatic assay kits and real-time PCR analysis was used to assess mRNA levels in adipose tissue.

Results

Our results show increased expression of some enzymes that synthesize oxylipins in adipose tissue and alterations in the levels of oxylipins in both adipose tissue and serum of subjects with obesity. After bariatric surgery, the levels of anti-inflammatory oxylipins increased, whereas pro-inflammatory oxylipins decreased.

Conclusions

In patients with obesity, the metabolism of oxylipins is deregulated in adipose tissue, and their concentrations in serum are altered. Bariatric surgery modulates the serum levels of pro- and anti-inflammatory oxylipins, which may contribute to the resolution of inflammation.

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Fig. 1: Comparison of oxylipins (ELISA) and their PUFA precursors (GC-MS analysis) in visceral adipose tissue of patients with obesity and lean subjects.
Fig. 2: Serum oxylipin concentrations (ELISA) and selected PUFA levels (GC-MS analysis) in patients with severe obesity compared with lean controls.
Fig. 3: Serum oxylipin concentrations (ELISA) and selected PUFA levels (GC-MS analysis) in patients with severe obesity before and 6-9 months after bariatric surgery.

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References

  1. Boini KM, Xia M, Koka S, Gehr TWB, Li PL. Sphingolipids in obesity and related complications. Front Biosci—Landmark. 2017;22:96–116.

    Article  CAS  Google Scholar 

  2. Mika A, Sledzinski T. Alterations of specific lipid groups in serum of obese humans: a review. Obes Rev. 2017;18:247–72.

    Article  CAS  PubMed  Google Scholar 

  3. Al-Sulaiti H, Diboun I, Banu S, Al-Emadi M, Amani P, Harvey TM, et al. Triglyceride profiling in adipose tissues from obese insulin sensitive, insulin resistant and type 2 diabetes mellitus individuals. J Transl Med. 2018;16:1–13.

    Article  Google Scholar 

  4. Wang Y, Huang F. N-3 polyunsaturated fatty acids and inflammation in obesity: local effect and systemic benefit. Biomed Res Int. 2015;2015:581469.

  5. Castagneto-Gissey L, Casella-Mariolo J, Casella G, Mingrone G. Obesity surgery and cancer: what are the unanswered questions? Front Endocrinol (Lausanne). 2020;11:213.

    Article  Google Scholar 

  6. Yamashita AS, Belchior T, Lira FS, Bishop NC, Wessner B, Rosa JC, et al. Regulation of metabolic disease-associated inflammation by nutrient sensors. Mediators Inflamm. 2018;2018:8261432.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444:860–7.

    Article  CAS  PubMed  Google Scholar 

  8. Hsieh P-S, Jin J-S, Chiang C-F, Chan P-C, Chen C-H, Shih K-C. COX-2-mediated inflammation in fat is crucial for obesity-linked insulin resistance and fatty liver. Obesity. 2009;17:1150–7.

    Article  CAS  PubMed  Google Scholar 

  9. Martínez-Fernández L, Laiglesia LM, Huerta AE, Martínez JA, Moreno-Aliaga MJ. Omega-3 fatty acids and adipose tissue function in obesity and metabolic syndrome. Prostaglandins Other Lipid Mediat. 2015;121:24–41.

    Article  PubMed  Google Scholar 

  10. Ahima R, Flier J. Adipose tissue as an endocrine organ. Trends Endocrinol Metab. 2000;11:327–32.

    Article  CAS  PubMed  Google Scholar 

  11. Liakh I, Pakiet A, Sledzinski T, Mika A. Methods of the analysis of oxylipins in biological samples. Molecules. 2020;25:349.

    Article  CAS  PubMed Central  Google Scholar 

  12. Jacobi D, Stanya K, Lee C-H. Adipose tissue signaling by nuclear receptors in metabolic complications of obesity. Adipocyte. 2012;1:4–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Pauls SD, Du Y, Clair L, Winter T, Aukema HM, Taylor CG, et al. Impact of age, menopause, and obesity on oxylipins linked to vascular health. Arterioscler Thromb Vasc Biol. 2021;41:883–97.

    Article  CAS  PubMed  Google Scholar 

  14. Dieckmann S, Maurer S, Fromme T, Colson C, Virtanen KA, Amri EZ, et al. Fatty acid metabolite profiling reveals oxylipins as markers of brown but not brite adipose tissue. Front Endocrinol (Lausanne). 2020;11. https://doi.org/10.3389/fendo.2020.00073.

  15. Schulte F, Asbeutah AA, Benotti PN, Wood GC, Still C, Bistrian BR, et al. The relationship between specialized pro-resolving lipid mediators, morbid obesity and weight loss after bariatric surgery. Sci Rep. 2020;10:1–11.

    Article  Google Scholar 

  16. Liakh Pakiet, Sledzinski Mika. Modern methods of sample preparation for the analysis of oxylipins in biological samples. Molecules. 2019;24:1639.

    Article  CAS  PubMed Central  Google Scholar 

  17. Melissa Gabbs, Leng S, Devassy JG, Monirujjaman M, Aukema HM. Advances in our understanding of oxylipins derived from dietary PUFAs 1,2. Adv. Nutr. 2015;6:513–40.

    Article  Google Scholar 

  18. Liakh I, Pakiet A, Sledzinski T, Mika A. Methods of the analysis of oxylipins in biological samples. Molecules. 2020;25. https://doi.org/10.3390/molecules25020349.

  19. Pal A, Al-Shaer AE, Guesdon W, Torres MJ, Armstrong M, Quinn K, et al. Eicosapentaenoic acid prevents obesity‐induced metabolic impairments through the host‐genetic dependent effects of resolvin E1. FASEB J. 2020;34:1–1.

    Google Scholar 

  20. Kutzner L, Rund KM, Ostermann AI, Hartung NM, Galano J-M, Balas L, et al. Development of an optimized LC-MS method for the detection of specialized pro-resolving mediators in biological samples. Front Pharmacol. 2019;10. https://doi.org/10.3389/fphar.2019.00169.

  21. González-Périz A, Horrillo R, Ferré N, Gronert K, Dong B, Morán-Salvador E, et al. Obesity‐induced insulin resistance and hepatic steatosis are alleviated by ω‐3 fatty acids: a role for resolvins and protectins. FASEB J. 2009;23:1946–57.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Spector AA, Kim H-Y. Cytochrome P450 epoxygenase pathway of polyunsaturated fatty acid metabolism. Biochim Biophys Acta—Mol Cell Biol Lipids. 2015;1851:356–65.

    Article  CAS  Google Scholar 

  23. Pickens CA, Sordillo LM, Comstock SS, Harris WS, Hortos K, Kovan B, et al. Plasma phospholipids, non-esterified plasma polyunsaturated fatty acids and oxylipids are associated with BMI. Prostaglandins Leukot Essent Fat Acids. 2015;95:31–40.

    Article  CAS  Google Scholar 

  24. Keenan AH, Pedersen TL, Fillaus K, Larson MK, Shearer GC, Newman JW. Basal omega-3 fatty acid status affects fatty acid and oxylipin responses to high-dose n3-HUFA in healthy volunteers. J Lipid Res. 2012;53:1662–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Naoe S, Tsugawa H, Takahashi M, Ikeda K, Arita M. Characterization of lipid profiles after dietary intake of polyunsaturated fatty acids using integrated untargeted and targeted lipidomics. Metabolites. 2019;9:241.

    Article  CAS  PubMed Central  Google Scholar 

  26. Pickens CA, Sordillo LM, Zhang C, Fenton JI. Obesity is positively associated with arachidonic acid-derived 5- and 11-hydroxyeicosatetraenoic acid (HETE). Metabolism. 2017;70:177–91.

    Article  CAS  PubMed  Google Scholar 

  27. Möller K, Ostermann AI, Rund K, Thoms S, Blume C, Stahl F, et al. Influence of weight reduction on blood levels of C-reactive protein, tumor necrosis factor-α, interleukin-6, and oxylipins in obese subjects. Prostaglandins, Leukot Essent Fat Acids. 2016;106:39–49.

    Article  Google Scholar 

  28. Hernandez-Carretero A, Weber N, La Frano MR, Ying W, Lantero Rodriguez J, Sears DD, et al. Obesity-induced changes in lipid mediators persist after weight loss. Int J Obes. 2018;42:728–36.

    Article  CAS  Google Scholar 

  29. Laiglesia LM, Lorente-Cebrián S, Martínez-Fernández L, Sáinz N, Prieto-Hontoria PL, Burrell MA, et al. Maresin 1 mitigates liver steatosis in ob/ob and diet-induced obese mice. Int J Obes. 2018;42:572–9.

    Article  CAS  Google Scholar 

  30. Chakrabarti SK, Wen Y, Dobrian AD, Cole BK, Ma Q, Pei H, et al. Evidence for activation of inflammatory lipoxygenase pathways in visceral adipose tissue of obese Zucker rats. Am J Physiol—Endocrinol Metab. 2011;300. https://doi.org/10.1152/ajpendo.00203.2010.

  31. Clŕria J, Dalli J, Yacoubian S, Gao F, Serhan CN. Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J Immunol. 2012;189:2597–605.

    Article  Google Scholar 

  32. Mika A, Sledzinski T, Proczko-Stepaniak M, Magkos F. One anastomosis gastric bypass in the treatment of obesity: effects on body weight and the metabolome. In: Faintuch J, Faintuch S, editors. Obesity and diabetes. Springer International Publishing; 2020. p. 777–790.

  33. Pakiet A, Wilczynski M, Rostkowska O, Korczynska J, Jabłonska P, Kaska L, et al. The effect of one anastomosis gastric bypass on branched-chain fatty acid and branched-chain amino acid metabolism in subjects with morbid obesity. Obes Surg. 2020;30:304–12.

    Article  PubMed  Google Scholar 

  34. Mika A, Wilczynski M, Pakiet A, Kaska L, Proczko-stepaniak M, Stankiewicz M, et al. Short-term effect of one-anastomosis gastric bypass on essential fatty acids in the Serum of obese patients. Nutrients 2020;12. https://doi.org/10.3390/nu12010187.

  35. Halinski LP, Pakiet A, Jablonska P, Kaska L, Proczko-Stepaniak M, Slominska E, et al. One Anastomosis Gastric Bypass Reconstitutes the Appropriate Profile of Serum Amino Acids in Patients with Morbid Obesity. J Clin Med. 2019;9:100.

    Article  PubMed Central  Google Scholar 

  36. Mika A, Kaska L, Proczko-Stepaniak M, Chomiczewska A, Swierczynski J, Smolenski RT, et al. Evidence that the length of bile loop determines serum bile acid concentration and glycemic control after bariatric surgery. Obes Surg. 2018;28:3405–14.

    Article  PubMed  Google Scholar 

  37. Das U. Bioactive lipids in age-related disorders. Adv Exp Med Biol. 2020;1260:33–83.

    Article  CAS  PubMed  Google Scholar 

  38. García-Alonso V, Titos E, Alcaraz-Quiles J, Rius B, Lopategi A, López-Vicario C, et al. Prostaglandin E2 exerts multiple regulatory actions on human obese adipose tissue remodeling, inflammation, adaptive thermogenesis and lipolysis. PLoS ONE. 2016;11:e0153751.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wolfer AM, Scott AJ, Rueb C, Gaudin M, Darzi A, Nicholson JK, et al. Longitudinal analysis of serum oxylipin profile as a novel descriptor of the inflammatory response to surgery. J Transl Med. 2017;15:83.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Neels JG. A role for 5-lipoxygenase products in obesity-associated inflammation and insulin resistance. Adipocyte. 2013;2:262–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Miyauchi E, Tachikawa M, Declčves X, Uchida Y, Bouillot J-L, Poitou C, et al. Quantitative atlas of cytochrome P450, UDP-glucuronosyltransferase, and transporter proteins in jejunum of morbidly obese subjects. Mol Pharm. 2016;13:2631–40.

    Article  CAS  PubMed  Google Scholar 

  42. Chan P-C, Liao M-T, Hsieh P-S. The dualistic effect of COX-2-mediated signaling in obesity and insulin resistance. Int J Mol Sci. 2019;20:3115.

    Article  CAS  PubMed Central  Google Scholar 

  43. Fried M, Yumuk V, Oppert J-M, Scopinaro N, Torres AJ, Weiner R, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Obes Facts. 2013;6:449–68.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497–509.

    Article  CAS  PubMed  Google Scholar 

  45. Pakiet A, Jakubiak A, Mierzejewska P, Zwara A, Liakh I, Sledzinski T, et al. The effect of a high-fat diet on the fatty acid composition in the hearts of mice. Nutrients. 2020;12:1–20.

    Article  Google Scholar 

  46. Piehler AP, Grimholt RM, Ovstebo R, Berg JP. Gene expression results in lipopolysaccharide-stimulated monocytes depend significantly on the choice of reference genes. BMC Immunol. 2010;11:21.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Tang S, Wan M, Huang W, Stanton RC, Xu Y. Maresins: specialized proresolving lipid mediators and their potential role in inflammatory-related diseases. Mediators Inflamm. 2018;2018. https://doi.org/10.1155/2018/2380319.

  48. Ota T Obesity-induced inflammation and insulin resistance. Front Endocrinol (Lausanne). 2014;5. https://doi.org/10.3389/fendo.2014.00204.

  49. Shearer GC, Walker RE. An overview of the biologic effects of omega-6 oxylipins in humans. Prostaglandins Leukot Essent Fat Acids. 2018;137:26–38.

    Article  CAS  Google Scholar 

  50. Aslan M, Aslan I, Özcan F, Erylmaz R, Ensari CO, Bilecik T. A pilot study investigating early postoperative changes of plasma polyunsaturated fatty acids after laparoscopic sleeve gastrectomy. Lipids Health Dis. 2014;13:1–7.

    Article  Google Scholar 

  51. Colson C, Ghandour RA, Dufies O, Rekima S, Loubat A, Munro P, et al. Diet supplementation in ω3 polyunsaturated fatty acid favors an anti-inflammatory basal environment in mouse adipose tissue. Nutrients. 2019;11:1–17.

    Article  Google Scholar 

  52. Culp BR, Titus BG, Lands WEM. Inhibition of prostaglandin biosynthesis by eicosapentaenoic acid. Prostaglandines Med. 1979;3:269–78.

    Article  CAS  Google Scholar 

  53. Sima C, Paster B, Van, Dyke TE. Function of pro-resolving lipid mediator resolvin E1 in type 2 diabetes. Crit Rev Immunol. 2018;38:343–65.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Gustafson B, Hammarstedt A, Andersson CX, Smith U. Inflamed adipose tissue: a culprit underlying the metabolic syndrome and atherosclerosis. Arterioscler Thromb Vasc Biol. 2007;27:2276–83.

    Article  CAS  PubMed  Google Scholar 

  55. Martínez-Fernández L, González-Muniesa P, Sáinz N, Escoté X, Martínez JA, Arbones-Mainar JM, et al. Maresin 1 regulates insulin signaling in human adipocytes as well as in adipose tissue and muscle of lean and obese mice. J Physiol Biochem. 2020. https://doi.org/10.1007/s13105-020-00775-9.

  56. Masoodi M, Kuda O, Rossmeisl M, Flachs P, Kopecky J. Lipid signaling in adipose tissue: connecting inflammation & metabolism. Biochim Biophys Acta—Mol Cell Biol Lipids. 2015;1851:503–18.

    Article  CAS  Google Scholar 

  57. Pakiet A, Jakubiak A, Czumaj A, Sledzinski T, Mika A. The effect of western diet on mice brain lipid composition. Nutr Metab. 2019;16:81.

    Article  Google Scholar 

  58. Hishikawa D, Valentine WJ, Iizuka-Hishikawa Y, Shindou H, Shimizu T. Metabolism and functions of docosahexaenoic acid-containing membrane glycerophospholipids. FEBS Lett. 2017;591:2730–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Irún P, Lanas A, Piazuelo E. Omega-3 polyunsaturated fatty acids and their bioactive metabolites in gastrointestinal malignancies related to unresolved inflammation. a review. Front Pharmacol. 2019;10. https://doi.org/10.3389/FPHAR.2019.00852.

  60. Serhan C, Lu Y, Hong S, Yang R. Mediator lipidomics: search algorithms for eicosanoids, resolvins, and protectins. Methods Enzymol. 2007;432:275–317.

    Article  CAS  PubMed  Google Scholar 

  61. Swierczynski J, Sledzinski T, Slominska E, Smolenski R, Sledzinski Z. Serum phenylalanine concentration as a marker of liver function in obese patients before and after bariatric surgery. Obes Surg. 2009;19:883–9.

    Article  PubMed  Google Scholar 

  62. Colas R, Sassolas A, Guichardant M, Cugnet-Anceau C, Moret M, Moulin P, et al. LDL from obese patients with the metabolic syndrome show increased lipid peroxidation and activate platelets. Diabetologia. 2011;54:2931–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Vangaveti V, Baune BT, Kennedy RL. Hydroxyoctadecadienoic acids: novel regulators of macrophage differentiation and atherogenesis. Ther Adv Endocrinol Metab. 2010;1:51–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Ávila-Román J, Arreaza-Gil V, Cortés-Espinar AJ, Soliz-Rueda JR, Mulero M, Muguerza B, et al. Impact of gut microbiota on plasma oxylipins profile under healthy and obesogenic conditions. Clin Nutr. 2021;40:1475–86.

    Article  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the National Science Centre of Poland, grant number NCN 2016/21/D/NZ5/00219; to AM, and by Medical University of Gdansk, grants ST40; to TS.

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A.M. and T.S. conceived and designed the study; M.P.S. and L.K. were responsible for resources and clinical data; I.L., J.K. and A.M. were responsible for methodology; I.L., A.J., A.P., J.K. and A.M. conducted the investigations; A.M. and T.S. interpreted the data; A.P. produced the figures; A.M. produced the tables; A.M., A.P. and T.S. searched the literature and wrote the first draft. All authors contributed to the revision of the first draft, reviewed and approved the final version of the paper.

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Correspondence to Adriana Mika.

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Liakh, I., Janczy, A., Pakiet, A. et al. One-anastomosis gastric bypass modulates the serum levels of pro- and anti-inflammatory oxylipins, which may contribute to the resolution of inflammation. Int J Obes 46, 408–416 (2022). https://doi.org/10.1038/s41366-021-01013-y

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