Walnut supplementation increases levels of UCP1 and CD36 in brown adipose tissue independently of diet type.

Brown adipose tissue Fructose Metabolism Walnut

Journal

Molecular and cellular biochemistry
ISSN: 1573-4919
Titre abrégé: Mol Cell Biochem
Pays: Netherlands
ID NLM: 0364456

Informations de publication

Date de publication:
13 Mar 2024
Historique:
received: 14 12 2023
accepted: 28 02 2024
medline: 13 3 2024
pubmed: 13 3 2024
entrez: 13 3 2024
Statut: aheadofprint

Résumé

Dietary interventions that modulate the brown adipose tissue (BAT) thermogenic activity could represent a promising therapy for metabolic disorders. In order to examine if dietary walnuts intake regulates the expression of BAT thermogenic markers levels in healthy and metabolically challenged (fructose fed) animals, rats were initially divided into the control and fructose-fed groups. After nine weeks, these groups were subdivided into the one kept on the original regimens and the other supplemented with walnuts. High-fructose diet resulted in an increased relative BAT mass and no change in UCP1 content, while the walnut supplementation increased the amount of UCP1 in BAT, but did not affect 5-HT, NA, DHPG content and DHPG/NA ratio regardless of the diet. Moreover, the CD36 levels were increased following the walnut consumption, unlike FATP1, GLUT1, GLUT4, and glycogen content which remained unchanged. Additionally, the BAT levels of activated IR and Akt were not affected by walnut consumption, while ERK signaling was decreased. Overall, we found that walnut consumption increased UCP1 and CD36 content in the BAT of both control and metabolically challenged rats, suggesting that FFAs represent the BAT preferred substrate under the previously described circumstances. This further implies that incorporating walnuts into the everyday diet may help to alleviate some symptoms of the metabolic disorder.

Identifiants

pubmed: 38478220
doi: 10.1007/s11010-024-04981-7
pii: 10.1007/s11010-024-04981-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Bargut TCL, Silva-e-Silva ACAG, Souza-Mello V, Mandarim-de-Lacerda CA, Aguila MB (2016) Mice fed fish oil diet and upregulation of brown adipose tissue thermogenic markers. Eur J Nutr 55. https://doi.org/10.1007/s00394-015-0834-0
Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmüller A, Gordts PLSM, Rinninger F, Bruegelmann K, Freund B, Nielsen P, Merkel M, Heeren J (2011) Brown adipose tissue activity controls triglyceride clearance. Nat Med 17. https://doi.org/10.1038/nm.2297
doi: 10.1038/nm.2297
Betz MJ, Enerbäck S (2018) Targeting thermogenesis in brown fat and muscle to treat obesity and metabolic disease. Nat Rev Endocrinol 14:77–87. https://doi.org/10.1038/nrendo.2017.132
doi: 10.1038/nrendo.2017.132 pubmed: 29052591
Bolling BW, McKay DL, Blumberg JB (2010) The phytochemical composition and antioxidant actions of tree nuts. Asia Pac J Clin Nutr 19:117–123. https://doi.org/10.6133/apjcn.2010.19.1.16
doi: 10.6133/apjcn.2010.19.1.16 pubmed: 20199996 pmcid: 5012104
Brenna JT, Salem N, Sinclair AJ, Cunnane SC (2009) α-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fat Acids 80. https://doi.org/10.1016/j.plefa.2009.01.004
Calderon-Dominguez M, Mir JF, Fucho R, Weber M, Serra D, Herrero L (2016) Fatty acid metabolism and the basis of brown adipose tissue function. Adipocyte 5:98–118. https://doi.org/10.1080/21623945.2015.1122857
doi: 10.1080/21623945.2015.1122857 pubmed: 27386151
Castro-Barquero S, Ruiz-León AM, Sierra-Pérez M, Estruch R, Casas R (2020) Dietary strategies for metabolic syndrome: a comprehensive review. Nutrients 12:2983. https://doi.org/10.3390/nu12102983
doi: 10.3390/nu12102983 pubmed: 33003472 pmcid: 7600579
Chan AML, Ng AMH, Mohd Yunus MH, Idrus RBH, Law JX, Yazid MD, Chin KY, Shamsuddin SA, Lokanathan Y (2021) Recent developments in rodent models of high-fructose diet-induced metabolic syndrome: a systematic review. Nutrients 13:2497. https://doi.org/10.3390/nu13082497
doi: 10.3390/nu13082497 pubmed: 34444658 pmcid: 8401262
Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng Y-H, Doria A, Kolodny GM, Kahn CR (2009) Identification and importance of Brown Adipose tissue in adult humans. N Engl J Med 360:1509–1517. https://doi.org/10.1056/nejmoa0810780
doi: 10.1056/nejmoa0810780 pubmed: 19357406 pmcid: 2859951
Dong M, Lin J, Lim W, Jin W, Lee HJ (2018) Role of brown adipose tissue in metabolic syndrome, aging, and cancer cachexia. Front Med 12:130–138. https://doi.org/10.1007/s11684-017-0555-2
doi: 10.1007/s11684-017-0555-2 pubmed: 29119382
Farkas V, Kelenyi G, Sandor A (1999) A dramatic accumulation of glycogen in the brown adipose tissue of rats following recovery from cold exposure. Arch Biochem Biophys 365. https://doi.org/10.1006/abbi.1999.1157
Fedorenko A, Lishko PV, Kirichok Y (2012) Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151:400–413. https://doi.org/10.1016/j.cell.2012.09.010
doi: 10.1016/j.cell.2012.09.010 pubmed: 23063128 pmcid: 3782081
Greenberg AS, Shen WJ, Muliro K, Patel S, Souza SC, Roth RA, Kraemer FB (2001) Stimulation of Lipolysis and hormone-sensitive lipase via the Extracellular Signal-regulated kinase pathway. J Biol Chem 276. https://doi.org/10.1074/jbc.m104436200
Gunawan S, Aulia A, Soetikno V (2021) Development of rat metabolic syndrome models: a review. Vet World 14:1774–1783. https://doi.org/10.14202/vetworld.2021.1774-1783
doi: 10.14202/vetworld.2021.1774-1783 pubmed: 34475697 pmcid: 8404106
Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R (2006) Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312. https://doi.org/10.1126/science.1123965
Hao Q, Yadav R, Basse AL, Petersen S, Sonne SB, Rasmussen S, Zhu Q, Lu Z, Wang J, Audouze K, Gupta R, Madsen L, Kristiansen K, Hansen JB (2015) Transcriptome profiling of brown adipose tissue during cold exposure reveals extensive regulation of glucose metabolism. Am J Physiol - Endocrinol Metab 308. https://doi.org/10.1152/ajpendo.00277 . 2014
Herz CT, Kulterer OC, Prager M, Schmöltzer C, Langer FB, Prager G, Marculescu R, Kautzky-Willer A, Hacker M, Haug AR, Kiefer FW (2022) Active brown adipose tissue is Associated with a healthier metabolic phenotype in obesity. Diabetes 71. https://doi.org/10.2337/db21-0475
Huber KR, Wödl H, Robubi A, Hauser A, Schrattbauer K, Krugluger W (2016) In Vitro Culture of Human Brown adipocytes: effects of Fructose. Int J Life Sci Med Res 6:1–8. https://doi.org/10.5963/LSMR0601001
doi: 10.5963/LSMR0601001
Hwang HJ, Liu Y, Kim HS, Lee H, Lim Y, Park H (2019) Daily walnut intake improves metabolic syndrome status and increases circulating adiponectin levels: Randomized controlled crossover trial. Nutr Res Pract 13. https://doi.org/10.4162/nrp.2019.13.2.105
Jakus PB, Sandor A, Janaky T, Farkas V (2008) Cooperation between BAT and WAT of rats in thermogenesis in response to cold, and the mechanism of glycogen accumulation in BAT during reacclimation. J Lipid Res 49. https://doi.org/10.1194/jlr.m700316-jlr200
Jatkar A, Kurland IJ, Judex S (2017) Diets high in Fat or Fructose differentially modulate bone health and lipid metabolism. Calcif Tissue Int 100. https://doi.org/10.1007/s00223-016-0205-8
Jung SM, Doxsey WG, Le J, Haley JA, Mazuecos L, Luciano AK, Li H, Jang C, Guertin DA (2021) In vivo isotope tracing reveals the versatility of glucose as a brown adipose tissue substrate. Cell Rep 36:109459. https://doi.org/10.1016/j.celrep.2021.109459
doi: 10.1016/j.celrep.2021.109459 pubmed: 34320357 pmcid: 8369932
Kawada T, Kayahashi S, Hida Y, Koga KJ, Nadachi Y, Fushiki T (1998) Fish (Bonito) Oil Supplementation enhances the expression of uncoupling protein in Brown Adipose tissue of rat. J Agric Food Chem 46. https://doi.org/10.1021/jf9711000
Khedoe PPSJ, Hoeke G, Kooijman S, Dijk W, Buijs JT, Kersten S, Havekes LM, Hiemstra PS, Berbée JFP, Boon MR, Rensen PCN (2015) Brown adipose tissue takes up plasma triglycerides mostly after lipolysis. J Lipid Res 56. https://doi.org/10.1194/jlr.m052746
Khitan Z, Kim DH (2013) Fructose: a key factor in the development of metabolic syndrome and hypertension. J Nutr Metab 2013:1–12. https://doi.org/10.1155/2013/682673
doi: 10.1155/2013/682673
Kim SH, Plutzky J (2016) Brown fat and browning for the treatment of obesity and related metabolic disorders. Diabetes Metab J 40:12–21. https://doi.org/10.4093/dmj.2016.40.1.12
doi: 10.4093/dmj.2016.40.1.12 pubmed: 26912151 pmcid: 4768046
Kim M, Goto T, Yu R, Uchida K, Tominaga M, Kano Y, Takahashi N, Kawada T (2015) Fish oil intake induces UCP1 upregulation in brown and white adipose tissue via the sympathetic nervous system. Sci Rep 5. https://doi.org/10.1038/srep18013
Kuipers EN, Held NM, Panhuis W (2019) in het, Modder M, Ruppert PMM, Kersten S, Kooijman S, Guigas B, Houtkooper RH, Rensen PCN, Boon MR A single day of high-fat diet feeding induces lipid accumulation and insulin resistance in brown adipose tissue in mice. Am J Physiol - Endocrinol Metab 317. https://doi.org/10.1152/ajpendo.00123.2019
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin-Phenol Reagent. J Biol Cemistry 193:265–275. https://doi.org/10.1016/S0021-9258(19)52451-6
doi: 10.1016/S0021-9258(19)52451-6
Maguire LS, O’Sullivan SM, Galvin K, O’Connor TP, O’Brien NM (2004) Fatty acid profile, tocopherol, squalene and phytosterol content of walnuts, almonds, peanuts, hazelnuts and the macadamia nut. Int J Food Sci Nutr 55:171–178. https://doi.org/10.1080/09637480410001725175
doi: 10.1080/09637480410001725175 pubmed: 15223592
McNeill BT, Morton NM, Stimson RH (2020) Substrate utilization by Brown Adipose tissue: what’s Hot and what’s not? Front Endocrinol 11:1–8. https://doi.org/10.3389/fendo.2020.571659
doi: 10.3389/fendo.2020.571659
Oudart H, Groscolas R, Calgari C, Nibbelink M, Leray C, Le Maho Y, Malan A (1997) Brown fat thermogenesis in rats fed high-fat diets enriched with n-3 polyunsaturated fatty acids. Int J Obes 21. https://doi.org/10.1038/sj.ijo.0800500
Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin B, Haman F, Turcotte EE, Richard D, Carpentier AC (2012) Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 122. https://doi.org/10.117 2/jci60433
Pandareesh MD, Chauhan V, Chauhan A (2018) Walnut Supplementation in the Diet reduces oxidative damage and improves antioxidant status in transgenic mouse model of Alzheimer’s Disease. J Alzheimers Dis JAD 64:1295–1305. https://doi.org/10.3233/jad-180361
doi: 10.3233/jad-180361 pubmed: 30040727
Petrović-Oggiano G, Debeljak-Martačić J, Ranković S, Pokimica B, Mirić A, Glibetić M, Popović T (2020) The effect of walnut consumption on n-3 fatty acid profile of healthy people living in a non-mediterranean west balkan country, a small scale randomized study. Nutrients 12:192. https://doi.org/10.3390/nu12010192
doi: 10.3390/nu12010192 pubmed: 31936720 pmcid: 7019815
Postic C, Leturque A, Printz RL, Maulard P, Loizeau M, Granner DK, Girard J (1994) Development and regulation of glucose transporter and hexokinase expression in rat. Am J Physiol - Endocrinol Metab 266:E548–E559. https://doi.org/10.1152/ajpendo.1994.266.4.e548
doi: 10.1152/ajpendo.1994.266.4.e548
Putri M, Syamsunarno MRAA, Iso T, Yamaguchi A, Hanaoka H, Sunaga H, Koitabashi N, Matsui H, Yamazaki C, Kameo S, Tsushima Y, Yokoyama T, Koyama H, Abumrad NA, Kurabayashi M (2015) CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem Biophys Res Commun 457. https://doi.org/10.1016/j.bbrc.2014 12.124
Rasouli M, Ostovar-Ravari A, Shokri-Afra H (2014) Characterization and improvement of phenol-sulfuric acid microassay for glucose-based glycogen. Eur Rev Med Pharmacol Sci 18:2020–2024
pubmed: 25027341
Rasouli M, Shokri-Afra H, Ostovar-Ravari A (2015) A new protocol for separation of acid soluble and insoluble fractions from total glycogen and simultaneous measurements. Eur Rev Med Pharmacol Sci 19:1785–1789
pubmed: 26044221
Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659–661. https://doi.org/10.1096/fj.07-9574lsf
doi: 10.1096/fj.07-9574lsf pubmed: 17942826
Richard G, Blondin DP, Syed SA, Rossi L, Fontes ME, Fortin M, Phoenix S, Frisch F, Dubreuil S, Guérin B, Turcotte ÉE, Lepage M, Surette MG, Schertzer JD, Steinberg GR, Morrison KM, Carpentier AC (2022) High-fructose feeding suppresses cold-stimulated brown adipose tissue glucose uptake independently of changes in thermogenesis and the gut microbiome. Cell Rep Med 3:100742. https://doi.org/10.1016/j.xcrm.2022.100742
doi: 10.1016/j.xcrm.2022.100742 pubmed: 36130480 pmcid: 9512695
Roberts-Toler C, O’Neill BT, Cypess AM (2015) Diet-induced obesity causes insulin resistance in mouse brown adipose tissue. https://doi.org/10.1002/oby.21134 . Obesity 23
Ros E, Br (2015) J Nutr 113:S111–S120. https://doi.org/10.1017/s0007114514003924
doi: 10.1017/s0007114514003924
Rothwell NJ, Stock MJ (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281. https://doi.org/10.1038/281031a0
Saito M, Matsushita M, Yoneshiro T, Okamatsu-Ogura Y (2020) Brown Adipose tissue, Diet-Induced thermogenesis, and thermogenic food ingredients: from mice to men. Front Endocrinol 11:222. https://doi.org/10.3389/fendo.2020.00222
doi: 10.3389/fendo.2020.00222
Shin H, Ma Y, Chanturiya T, Cao Q, Wang Y, Kadegowda AKG, Jackson R, Rumore D, Xue B, Shi H, Gavrilova O, Yu L (2017) Lipolysis in Brown adipocytes is not essential for Cold-Induced thermogenesis in mice. Cell Metab 26. https://doi.org/10.1016/j.cmet.2017.09.002
Stanford KI, Middelbeek RJW, Townsend KL, An D, Nygaard EB, Hitchcox KM, Markan KR, Nakano K, Hirshman MF, Tseng YH, Goodyear LJ (2013) Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest 123. https://doi.org/10.1172/jci62308
Stanisic J, Ivkovic T, Romic S, Zec M, Culafic T, Stojiljkovic M, Koricanac G (2020) Beneficial effect of walnuts on vascular tone is associated with akt signalling, voltage-dependent calcium channel LTCC and ATP-sensitive potassium channel Kv1.2. Int J Food Sci Nutr 21:1–11. https://doi.org/10.1080/09637486.2020.1796931
doi: 10.1080/09637486.2020.1796931
Townsend K, Tseng Y-H (2014) Brown Fat fuel utilization and thermogenesis. Trends Endocrinol Metab 25:168–177. https://doi.org/10.1016/j.tem.2013.12.004
doi: 10.1016/j.tem.2013.12.004 pubmed: 24389130 pmcid: 3972344
Wade G, McGahee A, Ntambi JM, Simcox J (2021) Lipid Transport in brown adipocyte thermogenesis. Front Physiol 12:787535. https://doi.org/10.3389/fphys.2021.787535
doi: 10.3389/fphys.2021.787535 pubmed: 35002769 pmcid: 8733649
Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206:2049–2057. https://doi.org/10.1242/jeb.00241
doi: 10.1242/jeb.00241 pubmed: 12756287
Wu Q, Kazantzis M, Doege H, Ortegon AM, Tsang B, Falcon A, Stahl A (2006) Fatty acid transport protein 1 is required for nonshivering thermogenesis in brown adipose tissue. Diabetes 55. https://doi.org/10.2337/db06-0749
doi: 10.2337/db06-0749
Zambón D, Sabaté J, Muñoz S, Campero B, Casals E, Merlos M, Laguna JC, Ros E (2000) Substituting walnuts for monounsaturated fat improves the serum lipid profile of hypercholesterolemic men and women. A randomized crossover trial. Ann Intern Med 132:538–546. https://doi.org/10.7326/0003-4819-132-7-200004040-00005
doi: 10.7326/0003-4819-132-7-200004040-00005 pubmed: 10744590
Zec MM, Krga I, Takić M, Debeljak-Martačić J, Korićanac G, Ranković S, Popović T, Pantelić M, Glibetic M (2020) Walnut Consumption induces tissue-specific Omega-6/Omega-3 decrease in high-fructose-Fed Wistar rats. ACS Omega 5:28136–28145. https://doi.org/10.1021/acsomega.0c03784
doi: 10.1021/acsomega.0c03784 pubmed: 33163796 pmcid: 7643199

Auteurs

Tamara Dakic (T)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Dusan Jeremic (D)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Iva Lakic (I)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Nebojsa Jasnic (N)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Aleksandra Ruzicic (A)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Predrag Vujovic (P)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia.

Tanja Jevdjovic (T)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry "Ivan Djaja", Faculty of Biology, University of Belgrade, Belgrade, 11000, Serbia. tanja.jevdjovic@bio.bg.ac.rs.

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