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Research Article

Deficiency of lipopolysaccharide binding protein facilitates adipose browning, glucose uptake and oxygen consumption in mouse embryonic fibroblasts via activating PI3K/Akt/mTOR pathway and inhibiting autophagy

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Pages 967-985 | Received 21 Jun 2021, Accepted 04 Jan 2023, Published online: 29 Jan 2023

References

  • Coronado-Cáceres LJ, Rabadán-Chávez G, Mojica L, et al. Cocoa (Theobroma cacao L.) seed proteins’ anti-obesity potential through lipase inhibition using in silico, in vitro and in vivo models. Vitro and in vivo Models Foods (Basel, Switzerland). 2020 Sep 25;9(10):1359. PubMed PMID: 32992701; PubMed Central PMCID: PMCPMC7599879. eng.
  • Flegal KM, Kit BK, Orpana H, et al. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA. 309(1). PubMed PMID: 23280227; PubMed Central PMCID: PMCPMC4855514. eng. 71–82. 2013 Jan 2.
  • Moon Y, Tong T, Kang W, et al. Filbertone ameliorates adiposity in mice fed a high-fat diet via activation of CAMP signaling. Nutrients. 2019 Jul 30;11(8):1749. PubMed PMID: 31366045; eng.
  • Engin A. Adiponectin-resistance in obesity. Adv Exp Med Biol. 2017;960:415–441. PubMed PMID: 28585210; eng.
  • Barazzoni R, Gortan Cappellari G, Ragni M, et al. Insulin resistance in obesity: an overview of fundamental alterations. Eat Weight Disord. 2018 Apr;23(2):149–157. PubMed PMID: 29397563; eng.
  • Smith GI, Mittendorfer B, Klein S. Metabolically healthy obesity: facts and fantasies. J Clin Investig. 129(10): PubMed PMID: 31524630; PubMed Central PMCID: PMCPMC6763224 funding from Merck Sharp & Dohme Corp. and Janssen Pharmaceuticals, and has served as a consultant for Pfizer, Novo Nordisk, and Merck Sharp & Dohme Corp. eng:3978–3989. 2019 Oct 1.
  • Merlin J, Sato M, Nowell C, et al. The PPARγ agonist rosiglitazone promotes the induction of brite adipocytes, increasing β-adrenoceptor-mediated mitochondrial function and glucose uptake. Cell Signal 2018 Jan;42:54–66. PubMed PMID: 28970184; eng
  • Ronti T, Lupattelli G, Mannarino E. The endocrine function of adipose tissue: an update. Clinical endocrinol. 2006 Apr;64(4):355–365. PubMed PMID: 16584505; eng.
  • Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 444(7121): PubMed PMID: 17167472; PubMed Central PMCID: PMCPMC3212857. eng:847–853. 2006 Dec 14.
  • Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 360(15). PubMed PMID: 19357407; eng. 1518–1525. 2009 Apr 9.
  • Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 360(15). PubMed PMID: 19357406; PubMed Central PMCID: PMCPMC2859951. eng. 1509–1517. 2009 Apr 9.
  • Miao Y, Qin H, Zhong Y, et al. Novel adipokine asprosin modulates browning and adipogenesis in white adipose tissue. J Endocrinol. 2021 May;249(2):83–93. PubMed PMID: 33705351.
  • Lucchini FC, Wueest S, Challa TD, et al. ASK1 inhibits browning of white adipose tissue in obesity. Nat Commun. 11(1). PubMed PMID: 32242025. 1642. 2020 Apr 2.
  • Guo F, Zhu Y, Han Y, et al. DEPP deficiency contributes to browning of white adipose tissue. Int J Mol Sci. 2022 Jun 12:23(12): DOI:10.3390/ijms23126563 PubMed PMID: 35743009.
  • Ikeda K, Yamada T. UCP1 Dependent and Independent Thermogenesis in Brown and Beige Adipocytes. Front Endocrinol (Lausanne). 2020;11:498. PubMed PMID: 32849287; PubMed Central PMCID: PMCPMC7399049. eng.
  • Stanford KI, Middelbeek RJ, Townsend KL, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Investig. 2013 Jan;123(1):215–223. PubMed PMID: 23221344; PubMed Central PMCID: PMCPMC3533266. eng.
  • Hansen JB, Kristiansen K. Regulatory circuits controlling white versus brown adipocyte differentiation. Biochem J. 398(2): PubMed PMID: 16898874; PubMed Central PMCID: PMCPMC1550312. eng:153–168. 2006 Sep 1.
  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009 Apr 9;360(15):1500–1508. PubMed PMID: 19357405; eng.
  • Qian SW, Tang Y, Li X, et al. BMP4-mediated brown fat-like changes in white adipose tissue alter glucose and energy homeostasis. Proc Natl Acad Sci USA. 2013 Feb 26 110(9):E798–807. PubMed PMID: 23388637; PubMed Central PMCID: PMCPMC3587258. eng
  • Chondronikola M, Volpi E, Børsheim E, et al. Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes. 2014 Dec;63(12):4089–4099. PubMed PMID: 25056438; PubMed Central PMCID: PMCPMC4238005. eng.
  • Seale P, Conroe HM, Estall J, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Investig. 2011 Jan;121(1):96–105. PubMed PMID: 21123942; PubMed Central PMCID: PMCPMC3007155. eng.
  • Lee P, Smith S, Linderman J, et al. Temperature-acclimated brown adipose tissue modulates insulin sensitivity in humans. Diabetes. 2014 Nov;63(11):3686–3698. PubMed PMID: 24954193; PubMed Central PMCID: PMCPMC4207391. eng.
  • Carobbio S, Rosen B, Vidal-Puig A. Adipogenesis: new insights into brown adipose tissue differentiation. J Mol Endocrinol. 2013 Dec;51(3):T75–85. PubMed PMID: 24041933; eng.
  • De Matteis R, Lucertini F, Guescini M, et al. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr Metab Cardiovasc Dis. 2013 Jun;23(6):582–590. PubMed PMID: 22633794; eng.
  • Ghorbani M, Claus TH, Himms-Hagen J. Hypertrophy of brown adipocytes in brown and white adipose tissues and reversal of diet-induced obesity in rats treated with a beta3-adrenoceptor agonist. Biochem Pharmacol. 1997 Jul 1;54(1):121–131. PubMed PMID: 9296358; eng.
  • Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol. 2014 Jan;10(1):24–36. PubMed PMID: 24146030; eng.
  • Kaisanlahti A, Glumoff T. Browning of white fat: agents and implications for beige adipose tissue to type 2 diabetes. J Physiol Biochem. 2019 Feb;75(1):1–10. PubMed PMID: 30506389; PubMed Central PMCID: PMCPMC6513802. eng.
  • Rodrigues AR, Salazar MJ, Rocha-Rodrigues S, et al. Peripherally administered melanocortins induce mice fat browning and prevent obesity. Int J Obes (Lond). 2019 May;43(5):1058–1069. PubMed PMID: 30018312.
  • Kang J, Park J, Park WY, et al. A phytoestrogen secoisolariciresinol diglucoside induces browning of white adipose tissue and activates non-shivering thermogenesis through AMPK pathway. Pharmacol Res 2020 Aug;158:104852. PubMed PMID: 32438038; eng
  • Saghafi-Asl M, Mirmajidi S, Asghari Jafarabadi M, et al. The association of dietary patterns with dietary inflammatory index, systemic inflammation, and insulin resistance, in apparently healthy individuals with obesity. Sci Rep. 11(1). PubMed PMID: 33824355; PubMed Central PMCID: PMCPMC8024341. eng. 7515. 2021 Apr 6.
  • Sun L, Yu Z, Ye X, et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care. 2010 Sep;33(9):1925–1932. PubMed PMID: 20530747; PubMed Central PMCID: PMCPMC2928335. eng.
  • Gonzalez-Quintela A, Alonso M, Campos J, et al. Determinants of serum concentrations of lipopolysaccharide-binding protein (LBP) in the adult population: the role of obesity. PLoS ONE. 2013;8(1):e54600. PubMed PMID: 23349936; PubMed Central PMCID: PMCPMC3551812. eng.
  • Jialal I, Devaraj S, Bettaieb A, et al. Increased adipose tissue secretion of Fetuin-A, lipopolysaccharide-binding protein and high-mobility group box protein 1 in metabolic syndrome. Atherosclerosis. 2015 Jul;241(1):130–137. PubMed PMID: 25978344; eng.
  • Liu X, Lu L, Yao P, et al. Lipopolysaccharide binding protein, obesity status and incidence of metabolic syndrome: a prospective study among middle-aged and older Chinese. Diabetologia. 2014 Sep;57(9):1834–1841. PubMed PMID: 24906952; eng.
  • Zhou H, Hu J, Zhu Q, et al. Lipopolysaccharide-binding protein cannot independently predict type 2 diabetes mellitus: a nested case-control study. J Diabetes. 2016 Mar;8(2):214–219. PubMed PMID: 25753130; eng.
  • Ruiz AG, Casafont F, Crespo J, et al. Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients: evidence for the potential role of endotoxin in the pathogenesis of non-alcoholic steatohepatitis. Obes Surg. 2007 Oct;17(10):1374–1380. PubMed PMID: 18000721; eng.
  • van Dielen FM, Buurman WA, Hadfoune M, et al. Macrophage inhibitory factor, plasminogen activator inhibitor-1, other acute phase proteins, and inflammatory mediators normalize as a result of weight loss in morbidly obese subjects treated with gastric restrictive surgery. J Clin Endocrinol Metab. 2004 Aug;89(8):4062–4068. PubMed PMID: 15292349; eng.
  • Moreno-Navarrete JM, Ortega F, Serino M, et al. Circulating lipopolysaccharide-binding protein (LBP) as a marker of obesity-related insulin resistance. Int J Obes (Lond). 2012 Nov;36(11):1442–1449. PubMed PMID: 22184060; eng.
  • Moreno-Navarrete JM, Escoté X, Ortega F, et al. A role for adipocyte-derived lipopolysaccharide-binding protein in inflammation- and obesity-associated adipose tissue dysfunction. Diabetologia. 2013 Nov;56(11):2524–2537. PubMed PMID: 23963324; eng.
  • Gavaldà-Navarro A, Moreno-Navarrete JM, Quesada-López T, et al. Lipopolysaccharide-binding protein is a negative regulator of adipose tissue browning in mice and humans. Diabetologia. 2016 Oct;59(10):2208–2218. PubMed PMID: 27344313; eng.
  • Sallam T, Ito A, Rong X, et al. The macrophage LBP gene is an LXR target that promotes macrophage survival and atherosclerosis. J Lipid Res. 2014 Jun;55(6):1120–1130. PubMed PMID: 24671012; PubMed Central PMCID: PMCPMC4031943. eng.
  • Moreno-Navarrete JM, Jové M, Padró T, et al. Adipocyte lipopolysaccharide binding protein (LBP) is linked to a specific lipidomic signature. Obesity (Silver Spring. Md). 2017 Feb;25(2):391–400. PubMed PMID: 28001010; eng.
  • Moreno-Navarrete JM, Escoté X, Ortega F, et al. Lipopolysaccharide binding protein is an adipokine involved in the resilience of the mouse adipocyte to inflammation. Diabetologia. 2015 Oct;58(10):2424–2434. PubMed PMID: 26201685; eng.
  • Tu WZ, Fu YB, Xie X. RepSox, a small molecule inhibitor of the TGFβ receptor, induces brown adipogenesis and browning of white adipocytes. Acta Pharmacol Sin. 2019 Dec;40(12):1523–1531. PubMed PMID: 31235818; PubMed Central PMCID: PMCPMC7471457. eng.
  • Gatticchi L, Petricciuolo M, Scarpelli P, et al. Tm7sf2 gene promotes adipocyte differentiation of mouse embryonic fibroblasts and improves insulin sensitivity. Biochim Biophys Acta Mol Cell Res. 2021 Jan;1868(1):118897. PubMed PMID: 33121932; eng.
  • Wang Q, Jin F, Zhang J, et al. Lipoxin A4 promotes adipogenic differentiation and browning of mouse embryonic fibroblasts. vitro cellular & developmental biology Animal. 2021 Dec;57(10):953–961. PubMed PMID: 34811702; eng.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego. Calif). 2001 Dec;25(4):402–408. PubMed PMID: 11846609; eng.
  • Bhurosy T, Jeewon R. Overweight and obesity epidemic in developing countries: a problem with diet, physical activity, or socioeconomic status? ScientificWorldjournal. 2014;2014:964236. PubMed PMID: 25379554; PubMed Central PMCID: PMCPMC4212551. eng.
  • Junker D, Syväri J, Weidlich D, et al. Investigation of the Relationship between MR-Based Supraclavicular Fat Fraction and Thyroid Hormones. Obes Facts. 2020;13(3):331–343. PubMed PMID: 32564012; PubMed Central PMCID: PMCPMC7445585. eng.
  • Torriani M, Fitch K, Stavrou E, et al. Deiodinase 2 expression is increased in dorsocervical fat of patients with HIV-associated lipohypertrophy syndrome. J Clin Endocrinol Metab. 2012 Apr;97(4):E602–7. PubMed PMID: 22259052; PubMed Central PMCID: PMCPMC3319185. eng.
  • Davis RAH, Deemer SE, Bergeron JM, et al. Dietary R, S-1,3-butanediol diacetoacetate reduces body weight and adiposity in obese mice fed a high-fat diet. FASEB J. 2019 Feb;33(2):2409–2421. PubMed PMID: 30303740; PubMed Central PMCID: PMCPMC6338649. eng.
  • Zhu Q, Ghoshal S, Tyagi R, et al. Global IP6K1 deletion enhances temperature modulated energy expenditure which reduces carbohydrate and fat induced weight gain. Mol Metabol. 2017 Jan;6(1):73–85. PubMed PMID: 28123939; PubMed Central PMCID: PMCPMC5220553. eng.
  • Ye Q, Chen C, Si E, et al. Mitochondrial Effects of PGC-1alpha Silencing in MPP(+) Treated Human SH-SY5Y Neuroblastoma Cells. Front Mol Neurosci. 2017;10:164. PubMed PMID: 28611589; PubMed Central PMCID: PMCPMC5447087. eng.
  • Liesa M, Borda-D’Agua B, Medina-Gómez G, et al. Mitochondrial fusion is increased by the nuclear coactivator PGC-1beta. PLoS ONE. 2008;3(10):e3613. PubMed PMID: 18974884; PubMed Central PMCID: PMCPMC2570954 Astra Zeneca R&D. eng.
  • Huang CJ, Stewart JK, Shibata Y, et al. Lipopolysaccharide-binding protein and leptin are associated with stress-induced interleukin-6 cytokine expression ex vivo in obesity. Psychophysiology. 2015 May;52(5):687–694. PubMed PMID: 25424507; eng.
  • Wang K, Lv Q, Miao YM, et al. Cardamonin, a natural flavone, alleviates inflammatory bowel disease by the inhibition of NLRP3 inflammasome activation via an AhR/Nrf2/NQO1 pathway. Biochem Pharmacol. 2018 Sep;155:494–509. PubMed PMID: 30071202; eng.
  • Luan Y, Zhang F, Cheng Y, et al. Hemin Improves Insulin Sensitivity and Lipid Metabolism in Cultured Hepatocytes and Mice Fed a High-Fat Diet. Nutrients. 2017 Jul 26:9(8): DOI:10.3390/nu9080805 PubMed PMID: 28933767; PubMed Central PMCID: PMCPMC5579599. eng.
  • Arribas M, Valverde AM, Benito M. Role of IRS-3 in the insulin signaling of IRS-1-deficient brown adipocytes. J Biol Chem. 278(46): PubMed PMID: 12944402; eng:45189–45199. 2003 Nov 14.
  • Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 132(1): PubMed PMID: 18191218; PubMed Central PMCID: PMCPMC2696814. eng:27–42. 2008 Jan 11.
  • Jansen HJ, van Essen P, Koenen T, et al. Autophagy activity is up-regulated in adipose tissue of obese individuals and modulates proinflammatory cytokine expression. Endocrinology. 2012 Dec;153(12):5866–5874. PubMed PMID: 23117929; eng.
  • Kosacka J, Kern M, Klöting N, et al. Autophagy in adipose tissue of patients with obesity and type 2 diabetes. Mol Cell Endocrinol PubMed PMID: 25818883; eng 2015 Jul 5;409:21–32.
  • Unuma K, Aki T, Funakoshi T, et al. Extrusion of mitochondrial contents from lipopolysaccharide-stimulated cells: involvement of autophagy. Autophagy. 2015;11(9):1520–1536. PubMed PMID: 26102061; PubMed Central PMCID: PMCPMC4590602. eng.
  • Zhang Y, Goldman S, Baerga R, et al. Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci USA. 106(47). PubMed PMID: 19910529; PubMed Central PMCID: PMCPMC2785257. eng. 19860–19865. 2009 Nov 24.
  • Singh R, Xiang Y, Wang Y, et al. Autophagy regulates adipose mass and differentiation in mice. J Clin Investig. 2009 Nov;119(11):3329–3339. PubMed PMID: 19855132; PubMed Central PMCID: PMCPMC2769174. eng.
  • Rosenwald M, Perdikari A, Rülicke T, et al. Bi-directional interconversion of brite and white adipocytes. Nat Cell Biol. 2013 Jun;15(6):659–667. PubMed PMID: 23624403; eng.
  • Gospodarska E, Nowialis P, Kozak LP. Mitochondrial turnover: a phenotype distinguishing brown adipocytes from interscapular brown adipose tissue and white adipose tissue. J Biol Chem. 290(13): PubMed PMID: 25645913; PubMed Central PMCID: PMCPMC4375480. eng:8243–8255. 2015 Mar 27.
  • Altshuler-Keylin S, Shinoda K, Hasegawa Y, et al. Beige Adipocyte Maintenance is Regulated by Autophagy-Induced Mitochondrial Clearance. Cell Metab. 24(3). PubMed PMID: 27568548; PubMed Central PMCID: PMCPMC5023491. eng. 402–419. 2016 Sep 13.
  • Pang Y, Pan L, Zhang Y, et al. TP53BP2 decreases cell proliferation and induces autophagy in neuroblastoma cell lines. Oncol Lett. 2019 Jun;17(6):4976–4984. PubMed PMID: 31186708; PubMed Central PMCID: PMCPMC6507348. eng.
  • Qin Y, Sun W, Wang Z, et al. ATF2-Induced lncRNA GAS8-AS1 Promotes Autophagy of Thyroid Cancer Cells by Targeting the miR-187-3p/atg5 and miR-1343-3p/atg7 Axes. Mol Ther Nucl Acids. 2020 Dec 4:22:584–600. PubMed PMID: 33230459; PubMed Central PMCID: PMCPMC7562962. eng.
  • Ost A, Svensson K, Ruishalme I, et al. Attenuated mTOR signaling and enhanced autophagy in adipocytes from obese patients with type 2 diabetes. Mol Med (Cambridge, MA). 2010 Jul-Aug;16(7–8):235–246. PubMed PMID: 20386866; PubMed Central PMCID: PMCPMC2896460. eng.
  • Meng J, Chen Y, Wang J, et al. EGCG protects vascular endothelial cells from oxidative stress-induced damage by targeting the autophagy-dependent PI3K-AKT-mTOR pathway. Ann translat Med. 2020 Mar;8(5):200. PubMed PMID: 32309347; PubMed Central PMCID: PMCPMC7154459. eng.
  • Wang Y, Zhang H. Regulation of Autophagy by mTOR Signaling Pathway. Adv Exp Med Biol. 2019;1206:67–83. PubMed PMID: 31776980; eng.
  • Zhang M, Liu S, Chua MS, et al. SOCS5 inhibition induces autophagy to impair metastasis in hepatocellular carcinoma cells via the PI3K/Akt/mTOR pathway. Sun, C. 2019 Aug 13 10(8):612. PubMed PMID: 31406106
  • Yau WW, Singh BK, Lesmana R, et al. Thyroid hormone (T(3)) stimulates brown adipose tissue activation via mitochondrial biogenesis and MTOR-mediated mitophagy. Autophagy. 2019 Jan;15(1):131–150. PubMed PMID: 30209975; PubMed Central PMCID: PMCPMC6287687. eng.
  • Takahashi N, Kobayashi M, Takaki T, et al. Actinobacillus actinomycetemcomitans lipopolysaccharide stimulates collagen phagocytosis by human gingival fibroblasts. Oral Microbiol Immunol. 2008 Jun;23(3):259–264. PubMed PMID: 18402614; eng.