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Published in: Nutrition & Metabolism 1/2018

Open Access 01-12-2018 | Research

Curcumin and piperine supplementation of obese mice under caloric restriction modulates body fat and interleukin-1β

Authors: Taiki Miyazawa, Kiyotaka Nakagawa, Sharon H. Kim, Michael J. Thomas, Ligi Paul, Jean-Marc Zingg, Gregory G. Dolnikowski, Susan B. Roberts, Fumiko Kimura, Teruo Miyazawa, Angelo Azzi, Mohsen Meydani

Published in: Nutrition & Metabolism | Issue 1/2018

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Abstract

Background

Dietary bioactive compounds capable of improving metabolic profiles would be of great value, especially for overweight individuals undergoing a caloric restriction (CR) regimen. Curcumin (Cur), a possible anti-obesity compound, and piperine (Pip), a plausible enhancer of Cur’s bioavailability and efficacy, may be candidate agents for controlling body fat, metabolism and low grade inflammation.

Methods

47 eight-week-old male C57BL/6 mice were fed a high fat diet (HFD) for 23 weeks to induce obesity. Then, mice were divided into 5 groups. Group 1 continued on HFD ad libitum. The other 4 groups underwent CR (reduced 10% HFD intake for 10 weeks, 20% for 20 weeks) with Cur, Pip, Cur + Pip or none of these. Percent body fat, plasma inflammatory markers associated with obesity (interferon (IFN)-γ, interleukin (IL)-10, IL-12 p70, IL-1β, IL-6 and KC/GRO), plasma Cur metabolites and liver telomere length were measured.

Results

Compared to the other groups, obese mice who underwent CR and received Cur + Pip in their diet lost more fat and had significantly lower IL-1β and KC/GRO. Tandem mass spectrometry analysis of plasma from obese mice under CR showed no difference in Cur metabolite levels between groups supplemented with Cur alone or combined with Pip. However, plasma IL-1β levels were inversely correlated with curcumin glucuronide. Minor modulation of telomere length were observed.

Conclusions

It is plausible that supplementing the high fat diet of CR mice with Cur + Pip may increase loss of body fat and suppresses HFD induced inflammation. Combination of Cur and Pip has potential to enhance CR effects for the prevention of metabolic syndrome.
Literature
1.
go back to reference Bartke A, Wright JC, Mattison JA, Ingram DK, Miller RA, Roth GS. Longevity : extending the lifespan of long-lived mice. Nature. 2001;414:412.CrossRefPubMed Bartke A, Wright JC, Mattison JA, Ingram DK, Miller RA, Roth GS. Longevity : extending the lifespan of long-lived mice. Nature. 2001;414:412.CrossRefPubMed
2.
go back to reference Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AH, Herbert RL, et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature. 2012;489:318–21.CrossRefPubMed Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AH, Herbert RL, et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature. 2012;489:318–21.CrossRefPubMed
3.
go back to reference Vera E, Bernardes de Jesus B, Foronda M, Flores JM, Blasco MA. Telomerase reverse transcriptase synergizes with calorie restriction to increase health span and extend mouse longevity. PLoS One. 2013;8:e53760.CrossRefPubMedPubMedCentral Vera E, Bernardes de Jesus B, Foronda M, Flores JM, Blasco MA. Telomerase reverse transcriptase synergizes with calorie restriction to increase health span and extend mouse longevity. PLoS One. 2013;8:e53760.CrossRefPubMedPubMedCentral
4.
go back to reference He Y, Yue Y, Zheng X, Zhang K, Chen S, Du Z. Curcumin, inflammation, and chronic diseases: how are they linked? Molecules. 2015;20:9183–213.CrossRefPubMed He Y, Yue Y, Zheng X, Zhang K, Chen S, Du Z. Curcumin, inflammation, and chronic diseases: how are they linked? Molecules. 2015;20:9183–213.CrossRefPubMed
5.
go back to reference Ejaz A, Wu D, Kwan P, Meydani M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr. 2009;139:919–25.CrossRefPubMed Ejaz A, Wu D, Kwan P, Meydani M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr. 2009;139:919–25.CrossRefPubMed
6.
go back to reference Shao W, Yu Z, Chiang Y, Yang Y, Chai T, Foltz W, et al. Curcumin prevents high fat diet induced insulin resistance and obesity via attenuating lipogenesis in liver and inflammatory pathway in adipocytes. PLoS One. 2012;7:e28784.CrossRefPubMedPubMedCentral Shao W, Yu Z, Chiang Y, Yang Y, Chai T, Foltz W, et al. Curcumin prevents high fat diet induced insulin resistance and obesity via attenuating lipogenesis in liver and inflammatory pathway in adipocytes. PLoS One. 2012;7:e28784.CrossRefPubMedPubMedCentral
7.
go back to reference Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med. 1998;64:353–6.CrossRefPubMed Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med. 1998;64:353–6.CrossRefPubMed
8.
go back to reference Neyrinck AM, Alligier M, Memvanga PB, Névraumont E, Larondelle Y, Préat V, et al. Curcuma Longa extract associated with white pepper lessens high fat diet-induced inflammation in subcutaneous adipose tissue. PLoS One. 2013;8:e81252.CrossRefPubMedPubMedCentral Neyrinck AM, Alligier M, Memvanga PB, Névraumont E, Larondelle Y, Préat V, et al. Curcuma Longa extract associated with white pepper lessens high fat diet-induced inflammation in subcutaneous adipose tissue. PLoS One. 2013;8:e81252.CrossRefPubMedPubMedCentral
9.
go back to reference Panahi Y, Hosseini MS, Khalili N, Naimi E, Majeed M, Sahebkar A. Antioxidant and anti-inflammatory effects of curcuminoid-piperine combination in subjects with metabolic syndrome: a randomized controlled trial and an updated meta-analysis. Clin Nutr. 2015;34:1101–8.CrossRefPubMed Panahi Y, Hosseini MS, Khalili N, Naimi E, Majeed M, Sahebkar A. Antioxidant and anti-inflammatory effects of curcuminoid-piperine combination in subjects with metabolic syndrome: a randomized controlled trial and an updated meta-analysis. Clin Nutr. 2015;34:1101–8.CrossRefPubMed
10.
go back to reference Wang J, Vanegas SM, Du X, Noble T, Zingg JM, Meydani M, et al. Caloric restriction favorably impacts metabolic and immune/inflammatory profiles in obese mice but curcumin/piperine consumption adds no further benefit. Nutr Metab. 2013;10:29.CrossRef Wang J, Vanegas SM, Du X, Noble T, Zingg JM, Meydani M, et al. Caloric restriction favorably impacts metabolic and immune/inflammatory profiles in obese mice but curcumin/piperine consumption adds no further benefit. Nutr Metab. 2013;10:29.CrossRef
11.
go back to reference Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458–60.CrossRefPubMed Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458–60.CrossRefPubMed
12.
go back to reference Van der Harst P, Van der Steege G, De Boer RA, Voors AA, Hall AS, Mulder MJ, et al. Telomere length of circulating leukocytes is decreased in patients with chronic heart failure. J Am Coll Cardiol. 2017;49:1459–64.CrossRef Van der Harst P, Van der Steege G, De Boer RA, Voors AA, Hall AS, Mulder MJ, et al. Telomere length of circulating leukocytes is decreased in patients with chronic heart failure. J Am Coll Cardiol. 2017;49:1459–64.CrossRef
13.
go back to reference Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366:662–4.CrossRefPubMed Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366:662–4.CrossRefPubMed
14.
go back to reference Garcia-Calzon S, Gea A, Razquin C, Corella D, Lamuela-Raventós RM, Martínez JA, et al. Longitudinal association of telomere length and obesity indices in an intervention study with a Mediterranean diet: the PREDIMED-NAVARRA trial. Int J Obes. 2013;38:177–82.CrossRef Garcia-Calzon S, Gea A, Razquin C, Corella D, Lamuela-Raventós RM, Martínez JA, et al. Longitudinal association of telomere length and obesity indices in an intervention study with a Mediterranean diet: the PREDIMED-NAVARRA trial. Int J Obes. 2013;38:177–82.CrossRef
15.
go back to reference O’Callaghan NJ, Clifton PM, Noakes M, Fenech M. Weight loss in obese men is associated with increased telomere length and decreased abasic sites in rectal mucosa. Rejuvenation Res. 2009;12:169–76.CrossRefPubMed O’Callaghan NJ, Clifton PM, Noakes M, Fenech M. Weight loss in obese men is associated with increased telomere length and decreased abasic sites in rectal mucosa. Rejuvenation Res. 2009;12:169–76.CrossRefPubMed
16.
go back to reference Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K, et al. Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr. 2011;106:S5–78.CrossRefPubMed Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K, et al. Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr. 2011;106:S5–78.CrossRefPubMed
17.
go back to reference Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141–50.CrossRefPubMed Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141–50.CrossRefPubMed
18.
go back to reference Takahiro H, Nakagawa K, Miyazawa T, Inoue N, Kimura F, Ikeda I, et al. Metabolic fate of poly-(lactic-co-glycolic acid)-based curcumin nanoparticles following oral administration. Int J Nanomedicine. 2016;11:3009–22. Takahiro H, Nakagawa K, Miyazawa T, Inoue N, Kimura F, Ikeda I, et al. Metabolic fate of poly-(lactic-co-glycolic acid)-based curcumin nanoparticles following oral administration. Int J Nanomedicine. 2016;11:3009–22.
19.
go back to reference Nakagawa K, Zingg JM, Kim SH, Thomas MJ, Dolnikowski GG, Azzi A. Differential cellular uptake and metabolism of curcuminoids in monocytes/macrophages: regulatory effects on lipid accumulation. Br J Nutr. 2014;112:8–14.CrossRefPubMed Nakagawa K, Zingg JM, Kim SH, Thomas MJ, Dolnikowski GG, Azzi A. Differential cellular uptake and metabolism of curcuminoids in monocytes/macrophages: regulatory effects on lipid accumulation. Br J Nutr. 2014;112:8–14.CrossRefPubMed
20.
go back to reference Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361:393–5.CrossRefPubMed Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361:393–5.CrossRefPubMed
22.
go back to reference Baldwin AG, Brough D, Freeman S. Inhibiting the inflammasome: a chemical perspective. J Med Chem. 2016;59:1691–710.CrossRefPubMed Baldwin AG, Brough D, Freeman S. Inhibiting the inflammasome: a chemical perspective. J Med Chem. 2016;59:1691–710.CrossRefPubMed
23.
go back to reference Shea-Donohue T, Thomas K, Cody MJ, Zhao A, Detolla LJ, Kopydlowski KM. Mice deficient in the CXCR2 ligand, CXCL1 (KC/GRO-alpha), exhibit increased susceptibility to dextran sodium sulfate (DSS)-induced colitis. Innate Immun. 2008;14:117–24.CrossRefPubMedPubMedCentral Shea-Donohue T, Thomas K, Cody MJ, Zhao A, Detolla LJ, Kopydlowski KM. Mice deficient in the CXCR2 ligand, CXCL1 (KC/GRO-alpha), exhibit increased susceptibility to dextran sodium sulfate (DSS)-induced colitis. Innate Immun. 2008;14:117–24.CrossRefPubMedPubMedCentral
25.
go back to reference Park S, Park NY, Valacchi G, Lim Y. Calorie restriction with a high-fat diet effectively attenuated inflammatory response and oxidative stress-related markers in obese tissues of the high diet fed rats. Mediat Inflamm. 2012;984643 Park S, Park NY, Valacchi G, Lim Y. Calorie restriction with a high-fat diet effectively attenuated inflammatory response and oxidative stress-related markers in obese tissues of the high diet fed rats. Mediat Inflamm. 2012;984643
26.
go back to reference Asai A, Miyazawa T. Occurrence of orally administered curcuminoid as glucuronide and glucuronide/sulfate conjugates in rat plasma. Life Sci. 2000;67:2785–93.CrossRefPubMed Asai A, Miyazawa T. Occurrence of orally administered curcuminoid as glucuronide and glucuronide/sulfate conjugates in rat plasma. Life Sci. 2000;67:2785–93.CrossRefPubMed
27.
go back to reference Ireson CR, Jones DJ, Orr S, Coughtrie MW, Boocock DJ, Williams ML, et al. Metabolism of the cancer chemopreventive agent curcumin in human and rat intestine. Cancer Epidemiol Biomark Prev. 2002;11:105–11. Ireson CR, Jones DJ, Orr S, Coughtrie MW, Boocock DJ, Williams ML, et al. Metabolism of the cancer chemopreventive agent curcumin in human and rat intestine. Cancer Epidemiol Biomark Prev. 2002;11:105–11.
28.
go back to reference Reen RK, Jamwal DS, Taneja SC, Koul JL, Dubey RK, Wiebel FJ, et al. Impairment of UDP-glucose dehydrogenase and glucuronidation activities in liver and small intestine of rat and guinea pig in vitro by piperine. Biochem Pharmacol. 1993;46:229–38.CrossRefPubMed Reen RK, Jamwal DS, Taneja SC, Koul JL, Dubey RK, Wiebel FJ, et al. Impairment of UDP-glucose dehydrogenase and glucuronidation activities in liver and small intestine of rat and guinea pig in vitro by piperine. Biochem Pharmacol. 1993;46:229–38.CrossRefPubMed
29.
go back to reference Hlavačková L, Janegová A, Uličná O, Janega P, Cerná A, Babál P. Spice up the hypertension diet - curcumin and piperine prevent remodeling of aorta in experimental L-NAME induced hypertension. Nutr Metab (Lond). 2011;8:72.CrossRef Hlavačková L, Janegová A, Uličná O, Janega P, Cerná A, Babál P. Spice up the hypertension diet - curcumin and piperine prevent remodeling of aorta in experimental L-NAME induced hypertension. Nutr Metab (Lond). 2011;8:72.CrossRef
30.
go back to reference Bachmanov AA, Reed DR, Beauchamp GK, Food TMG. Intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32:435–43.CrossRefPubMedPubMedCentral Bachmanov AA, Reed DR, Beauchamp GK, Food TMG. Intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32:435–43.CrossRefPubMedPubMedCentral
31.
go back to reference Kumar S, Singhal V, Roshan R, Sharma A, Rembhotkar GW, Piperine GB. Inhibits cur/pip -alpha induced adhesion of neutrophils to endothelial monolayer through suppression of NF-kappaB and IkappaB kinase activation. Eur J Pharmacol. 2007;575:177–86.CrossRefPubMed Kumar S, Singhal V, Roshan R, Sharma A, Rembhotkar GW, Piperine GB. Inhibits cur/pip -alpha induced adhesion of neutrophils to endothelial monolayer through suppression of NF-kappaB and IkappaB kinase activation. Eur J Pharmacol. 2007;575:177–86.CrossRefPubMed
32.
go back to reference Kanitkar M, Gokhale K, Galande S, Novel BRR. Role of curcumin in the prevention of cytokine-induced islet death in vitro and diabetogenesis in vivo. Br J Pharmacol. 2008;155:702–13.CrossRefPubMedPubMedCentral Kanitkar M, Gokhale K, Galande S, Novel BRR. Role of curcumin in the prevention of cytokine-induced islet death in vitro and diabetogenesis in vivo. Br J Pharmacol. 2008;155:702–13.CrossRefPubMedPubMedCentral
33.
go back to reference Thomas P, Wang YJ, Zhong JH Kosaraju S, O'Callaghan NJ, Zhou XF. Grape seed polyphenols and curcumin reduce genomic instability events in a transgenic mouse model for Alzheimer's disease. Mutat Res. 2009;661:25–34.CrossRefPubMed Thomas P, Wang YJ, Zhong JH Kosaraju S, O'Callaghan NJ, Zhou XF. Grape seed polyphenols and curcumin reduce genomic instability events in a transgenic mouse model for Alzheimer's disease. Mutat Res. 2009;661:25–34.CrossRefPubMed
34.
go back to reference Rippe C, Lesniewski L, Connell M, LaRocca T, Donato A, Seals D. Short-term calorie restriction reverses vascular endothelial dysfunction in old mice by increasing nitric oxide and reducing oxidative stress. Aging Cell. 2010;9:304–12.CrossRefPubMedPubMedCentral Rippe C, Lesniewski L, Connell M, LaRocca T, Donato A, Seals D. Short-term calorie restriction reverses vascular endothelial dysfunction in old mice by increasing nitric oxide and reducing oxidative stress. Aging Cell. 2010;9:304–12.CrossRefPubMedPubMedCentral
35.
go back to reference Houtkooper RH, Argmann C, Houten SM, Cantó C, Jeninga EH, Andreux PA, Thomas C, Doenlen R, Schoonjans K, Auwerx J. The metabolic footprint of aging in mice. Sci Rep. 2011;1:134.CrossRefPubMedPubMedCentral Houtkooper RH, Argmann C, Houten SM, Cantó C, Jeninga EH, Andreux PA, Thomas C, Doenlen R, Schoonjans K, Auwerx J. The metabolic footprint of aging in mice. Sci Rep. 2011;1:134.CrossRefPubMedPubMedCentral
Metadata
Title
Curcumin and piperine supplementation of obese mice under caloric restriction modulates body fat and interleukin-1β
Authors
Taiki Miyazawa
Kiyotaka Nakagawa
Sharon H. Kim
Michael J. Thomas
Ligi Paul
Jean-Marc Zingg
Gregory G. Dolnikowski
Susan B. Roberts
Fumiko Kimura
Teruo Miyazawa
Angelo Azzi
Mohsen Meydani
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Nutrition & Metabolism / Issue 1/2018
Electronic ISSN: 1743-7075
DOI
https://doi.org/10.1186/s12986-018-0250-6

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