Skip to main content
Log in

Effect of Resveratrol, l-Carnitine, and Aromatic Amino Acid Supplements on the Trace Element Content in the Organs of Mice with Dietary-Induced Obesity

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Given environmental contamination with toxic metals, diets that promote the elimination of these metals from the body of individuals, including those suffering from obesity, are urgently needed. The aim of this study was to determine the effects of supplementation with resveratrol (Res), l-carnitine (l-Car), tyrosine (Tyr), and tryptophan (Trp) on the content of trace elements in the organs of mice. DBA/2J mice and DBCB tetrahybrid mice received diets high in carbohydrate and fat supplemented with Res, l-Car, Tyr, or Trp for 65 days. In the liver, kidneys, and brain, the contents of 18 elements, including Al, As, Cu, Fe, Mn, Pb, Se, and Zn, were determined by inductively coupled plasma mass spectrometry. Res, l-Car, Tyr, and Trp had minimal or no effect on the essential elements (Fe, Mg, Cu, Zn, Se) in all organs studied. The Mn content notably increased in the organs of mice consuming l-Car and Trp. Mn accumulation was stimulated by Res in organs exclusively in DBCB mice and by Tyr exclusively in livers and brains of DBA/2J mice. Al levels were significantly reduced by l-Car and Trp in all organs of the mice, by Res in only DBCB mice, and by Tyr in only kidneys and livers of DBA/2J mice. In addition, l-Car and Trp decreased Pb accumulation in most organs of mice. Res and Tyr also inhibited Pb accumulation in some cases. Thus, the studied supplements affected the metabolism of trace elements, which may contribute to dietary treatments for obese individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

The datasets generated during the current study are available from the corresponding author on reasonable request by email.

References

  1. Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019:6730305–6730314. https://doi.org/10.1155/2019/6730305

    Article  CAS  Google Scholar 

  2. Masindi V, Muedi KL (2018) Environmental contamination by heavy metals. In: Saleh HM, Aglan RF (eds) Heavy metals. IntechOpen. https://www.intechopen.com/books/heavy-metals/environmental-contamination-by-heavy-metals. Accessed 26 Nov 2020

  3. Rahman Z, Singh VP (2019) The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environ Monit Assess 191:419. https://doi.org/10.1007/s10661-019-7528-7

    Article  CAS  PubMed  Google Scholar 

  4. Gmoshinski IV, Bagryantseva OV, Arnautov OV, Khotimchenko SA (2020) Nanoclays in food products: benefits and possible risks (literature review). Health Risk Anal 1:142–164. https://doi.org/10.21668/health.risk/2020.1.16

    Article  Google Scholar 

  5. Stahl T, Taschan H, Brunn H (2011) Aluminium content of selected foods and food products. Environ Sci Eur 23:37. https://doi.org/10.1186/2190-4715-23-37

    Article  Google Scholar 

  6. Lavrishchev A, Litvinovich A, Bure V, Pavlova O, Saljnikov E (2018) Strontium dynamics in soil and assimilation by plants during dissolution of conversion chalk. Biol Commun 63:163–173. https://doi.org/10.21638/spbu03.2018.302

    Article  Google Scholar 

  7. Das KK, Reddy RC, Bagoji IB, Das S, Bagali S, Mullur L, Khodnapur JP, Biradar MS (2018) Primary concept of nickel toxicity - an overview. J Basic Clin Physiol Pharmacol 30:141–152. https://doi.org/10.1515/jbcpp-2017-0171

    Article  CAS  PubMed  Google Scholar 

  8. Skalny AV, Tinkov AA, Bohan TG, Shabalovskaya MB, Terekhina O, Leshchinskaia SB, Agarkova LA, Notova SV, Skalnaya MG, Kovas Y (2019) The impact of maternal overweight on hair essential trace element and mineral content in pregnant women and their children. Biol Trace Elem Res 193:64–72. https://doi.org/10.1007/s12011-019-01693-8

    Article  CAS  PubMed  Google Scholar 

  9. Zohal M, Jam-Ashkezari S, Namiranian N, Moosavi A, Ghadiri-Anari A (2019) Association between selected trace elements and body mass index and waist circumference: a cross sectional study. Diabetes Metab Syndr 13:1293–1297. https://doi.org/10.1016/j.dsx.2019.01.019

    Article  PubMed  Google Scholar 

  10. Adnan MT, Amin MN, Uddin MG, Hussain MS, Sarwar MS, Hossain MK, Uddin SMN, Islam MS (2019) Increased concentration of serum MDA, decreased antioxidants and altered trace elements and macro-minerals are linked to obesity among Bangladeshi population. Diabetes Metab Syndr 13:933–938. https://doi.org/10.1016/j.dsx.2018.12.022

    Article  PubMed  Google Scholar 

  11. Skalnaya MG, Skalny AV, Grabeklis AR, Serebryansky EP, Demidov VA, Tinkov AA (2018) Hair trace elements in overweight and obese adults in association with metabolic parameters. Biol Trace Elem Res 186:12–20. https://doi.org/10.1007/s12011-018-1282-5

    Article  CAS  PubMed  Google Scholar 

  12. Poznyakovskiy VM, Sukhanov BP (2009) Food supplements in modern nutritional science. Tekhnika i tekhnologiya pishchevykh proizvodstv. https://docplayer.ru/45992786-Biologicheski-aktivnye-dobavki-v-sovremennoy-nutriciologii.html. Accessed 23 Feb 2021 (in Russian)

  13. Tutelyan VA, Kiseleva TL, Kochetkova AA, Smirnova EA, Kiseleva MA, Sarkisyan VA (2016) Promising sources of phytonutrients for specialized foods with a modified carbohydrate profile: the experience of traditional medicine. Vopr Pitan 84(4):46–60 (in Russian)

    Google Scholar 

  14. Sun N-N, Wu T-Y, Chau C-F (2016) Natural dietary and herbal products in anti-obesity treatment. Molecules 21:1351. https://doi.org/10.3390/molecules21101351

    Article  CAS  PubMed Central  Google Scholar 

  15. Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15(1):37–46. https://doi.org/10.1016/j.tics.2010.11.001

    Article  CAS  PubMed  Google Scholar 

  16. Herrera CP, Smith K, Atkinson F, Ruell P, Chow CM, O’Connor H, Brand-Miller J (2011) High-glycaemic index and -glycaemic load meals increase the availability of tryptophan in healthy volunteers. Br J Nutr 105:1601–1606. https://doi.org/10.1017/S0007114510005192

    Article  CAS  PubMed  Google Scholar 

  17. Flora SJ, Shrivastava R, Mittal M (2013) Chemistry and pharmacological properties of some natural and synthetic antioxidants for heavy metal toxicity. Curr Med Chem 20:4540–4574. https://doi.org/10.2174/09298673113209990146

    Article  CAS  PubMed  Google Scholar 

  18. Muselin F, Gârban Z, Cristina RT, Doma AO, Dumitrescu E, Vițălaru AB, Bănățean-Dunea I (2019) Homeostatic changes of some trace elements in geriatric rats in the condition of oxidative stress induced by aluminum and the beneficial role of resveratrol. J Trace Elem Med Biol 55:136–142. https://doi.org/10.1016/j.jtemb.2019.06.013

    Article  CAS  PubMed  Google Scholar 

  19. Hassan MH, Desoky T, Sakhr HM, Gabra RH, Bakri AH (2019) Possible metabolic alterations among autistic male children: clinical and biochemical approaches. J Mol Neurosci 67:204–216. https://doi.org/10.1007/s12031-018-1225-9

    Article  CAS  PubMed  Google Scholar 

  20. Knerr I, Blessing H, Seyferth S, Watling RJ, Chaudhri MA (2013) Evaluation of plasma trace element and mineral status in children and adolescents with phenylketonuria using data from inductively-coupled-plasma atomic emission and mass spectrometric analysis. Ann Nutr Metab 63:168–173. https://doi.org/10.1159/000354869

    Article  CAS  PubMed  Google Scholar 

  21. Apryatin SA, Mzhel’skaya KV, Trusov NV, Balakina AS, Soto KS, Beketova NA et al (2018) Biochemical and morphological parameters of inbred/outbred lines and DBCB tetrahybrid mouse in high-sugar in vivo model of metabolic syndrome. Bull Exp Biol Med 166:96–101. https://doi.org/10.1007/s10517-018-4296-2

    Article  CAS  PubMed  Google Scholar 

  22. Reeves PC (2000) AIN-93 purified diets for the study of trace elements metabolism in rodents. In: Watson RR (ed) Trace elements in laboratory rodents. CRC Press, New York, pp 3–39

    Google Scholar 

  23. Shumakova AA, Shipelin VA, Trusov NV, Gmoshinski IV (2020) Content of essential and toxic trace elements in organs of obese Wistar and Zucker leprfa rats receiving quercetin. J Trace Elem Med Biol 64:126687. https://doi.org/10.1016/j.jtemb.2020.126687

    Article  CAS  PubMed  Google Scholar 

  24. ISO 17294-1:2004. Water quality — application of inductively coupled plasma mass spectrometry (ICP-MS) — part 1: general guidelines. https://www.iso.org/standard/32957.html. Accessed 23 Feb 2021 

  25. Trusov NV, Mzhelskaya KV, Shipelin VA, Shumakova AA, Timonin AN, Riger NA et al (2019) The influence of l-carnitine on the immunological, integral and biochemical parameters of mice receiving a diet with excess of fat and fructose. Russ J Physiol 105:619–633. https://doi.org/10.1134/S086981391905012

    Article  CAS  Google Scholar 

  26. Trusov NV, Shipelin VA, Mzhelskaya KV, Shumakova AA, Timonin AN, Riger NA, Apryatin SA, Gmoshinski IV (2020) Effect of resveratrol on behavioral, biochemical and immunological parameters of DBA/2J and tetrahybrid DBCB mice receiving diet with excess fat and fructose. J Nutr Biochem 8:108527. https://doi.org/10.1016/j.jnutbio.2020.108527

    Article  CAS  Google Scholar 

  27. Tinkov AA, Popova EV, Polyakova VS, Kwan OV, Skalny AV, Nikonorov AA (2019) Adipose tissue chromium and vanadium disbalance in high-fatfed Wistar rats. J Trace Elem Med Biol 29:176–181. https://doi.org/10.1016/j.jtemb.2014.07.006

    Article  CAS  Google Scholar 

  28. Ortega-Pacheco D, Jiménez-Pérez MM, Serafín-López J, Juárez-Rojas JG, Ruiz-García A, Pacheco-García U (2011) Vanadyl sulfate effects on systemic profiles of metabolic syndrome in old rats with fructose-induced obesity. Int J Endocrinol 2018:5257216–5257212. https://doi.org/10.1155/2018/5257216

    Article  CAS  Google Scholar 

  29. Lemire J, Mailloux R, Darwich R, Auger C, Appanna VD (2011) The disruption of l-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells. Toxicol Lett 203:219–226. https://doi.org/10.1016/j.toxlet.2011.03.019

    Article  CAS  PubMed  Google Scholar 

  30. Li X, Zhang C, Zhang X, Wang S, Meng Q, Wu S, Yang H, Xia Y, Chen R (2016) An acetyl-L-carnitine switch on mitochondrial dysfunction and rescue in the metabolomics study on aluminum oxide nanoparticles. Part Fibre Toxicol 13:4. https://doi.org/10.1186/s12989-016-0115-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Thomas SC, Alhasawi A, Appanna VP, Auger C, Appanna VD (2015) Brain metabolism and Alzheimer’s disease: the prospect of a metabolite-based therapy. J Nutr Health Aging 19:58–63. https://doi.org/10.1007/s12603-014-0511-7

    Article  CAS  PubMed  Google Scholar 

  32. Mailloux RJ, Lemire J, Appanna VD (2011) Hepatic response to aluminum toxicity: dyslipidemia and liver diseases. Exp Cell Res 317:2231–2238. https://doi.org/10.1016/j.yexcr.2011.07.009

    Article  CAS  PubMed  Google Scholar 

  33. El-Sherbini ES, El-Sayed G, El Shotory R, Gheith N, Abou-Alsoud M, Harakeh SM et al (2017) Ameliorative effects of l-carnitine on rats raised on a diet supplemented with lead acetate. Saudi J Biol Sci 24:1410–1417. https://doi.org/10.1016/j.sjbs.2016.08.010

    Article  CAS  PubMed  Google Scholar 

  34. Cao X, Tian S, Fu M, Li Y, Sun Y, Liu J, Liu Y (2020) Resveratrol protects human bronchial epithelial cells against nickel-induced toxicity via suppressing p38 MAPK, NF-κB signaling, and NLRP3 inflammasome activation. Environ Toxicol 35:609–618. https://doi.org/10.1002/tox.22896

    Article  CAS  PubMed  Google Scholar 

  35. Zaky A, Bassiouny A, Farghaly M, El-Sabaa BM (2017) A combination of resveratrol and curcumin is effective against aluminum chloride-induced neuroinflammation in rats. J Alzheimers Dis 60:S221–S235. https://doi.org/10.3233/JAD-161115

    Article  CAS  PubMed  Google Scholar 

  36. Al Dera HS (2016) Protective effect of resveratrol against aluminum chloride induced nephrotoxicity in rats. Saudi Med J 37:369–378. https://doi.org/10.15537/smj.2016.4.13611

    Article  PubMed  PubMed Central  Google Scholar 

  37. Liu F, Xue Z, Zhang N, Wang W, Chen C, Li W (2012) Antagonizing effect of resveratrol on the lipid peroxidative damage induced by lead in mice. Wei Sheng Yan Jiu 416:920–924 (in Chinese)

    Google Scholar 

  38. Ma C, Wang Y, Dong L, Li M, Cai W (2015) Anti-inflammatory effect of resveratrol through the suppression of NF-κB and JAK/STAT signaling pathways. Acta Biochim Biophys Sin Shanghai 47:207–213. https://doi.org/10.1093/abbs/gmu135

    Article  CAS  PubMed  Google Scholar 

  39. Kim S, Nam J, Kim K (2007) Aluminum exposure decreases dopamine D1 and D2 receptor expression in mouse brain. Hum Exp Toxicol 26:741–746

    Article  CAS  Google Scholar 

  40. VanDuyn N, Settivari R, LeVora J, Zhou S, Unrine J, Nass R (2013) The metal transporter SMF-3/DMT-1 mediates aluminum-induced dopamine neuron degeneration. J Neurochem 124:147–157. https://doi.org/10.1111/jnc.12072

    Article  CAS  PubMed  Google Scholar 

  41. Dalla Torre G, Mujika JI, Lachowicz JI, Ramos MJ, Lopez X (2019) The interaction of aluminum with catecholamine-based neurotransmitters: can the formation of these species be considered a potential risk factor for neurodegenerative diseases? Dalton Trans 48:6003–6018. https://doi.org/10.1039/c8dt04216k

    Article  CAS  PubMed  Google Scholar 

  42. Roth JA, Li Z, Sridhar S, Khoshbouei H (2013) The effect of manganese on dopamine toxicity and dopamine transporter (DAT) in control and DAT transfected HEK cells. Neurotoxicology. 35:121–128. https://doi.org/10.1016/j.neuro.2013.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lack B, Daya S, Nyokong T (2001) Interaction of serotonin and melatonin with sodium, potassium, calcium, lithium and aluminium. J Pineal Res 31:102–108. https://doi.org/10.1034/j.1600-079x.2001.310202.x

    Article  CAS  PubMed  Google Scholar 

  44. Limson J, Nyokong T, Daya S (1998) The interaction of melatonin and its precursors with aluminium, cadmium, copper, iron, lead, and zinc: an adsorptive voltammetric study. J Pineal Res 24:15–21. https://doi.org/10.1111/j.1600-079x.1998.tb00361.x

    Article  CAS  PubMed  Google Scholar 

  45. Kumar S (2002) Aluminium-induced changes in the rat brain serotonin system. Food Chem Toxicol 40:1875–1880. https://doi.org/10.1016/s0278-6915(02)00180-1

    Article  CAS  PubMed  Google Scholar 

  46. Shumakova AA, Apryatin SA, Shipelin VA, Efimova EV, Fesenko ZS, Gmoshinski IV (2020) Influence of the DAT gene knockout on exchange of essential and toxic trace elements in rats. Vopr Pitan 89(5). https://doi.org/10.24411/0042-8833-2020 (in Russian)

  47. O’Neal SL, Zheng W (2015) Manganese toxicity upon overexposure: a decade in review. Curr Environ Health Rep 2:315–328. https://doi.org/10.1007/s40572-015-0056-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Macconi D, Perico L, Longaretti L, Morigi M, Cassis P, Buelli S, Perico N, Remuzzi G, Benigni A (2015) Sirtuin3 dysfunction is the key determinant of skeletal muscle insulin resistance by angiotensin II. PLoS One 10:e0127172. https://doi.org/10.1371/journal.pone.0127172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Gertz M, Nguyen GTT, Fischer F, Suenkel B, Schlicker C, Fränzel B, Tomaschewski J, Aladini F, Becker C, Wolters D, Steegborn C (2012) A molecular mechanism for direct sirtuin activation by resveratrol. PLoS ONE 7:e49761. https://doi.org/10.1371/journal.pone.0049761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Singh CK, Chhabra G, Ndiaye MA, Garcia-Peterson LM, Mack NJ, Ahmad N (2018) The role of sirtuins in antioxidant and redox signaling. Antioxid Redox Signal 28:643–661. https://doi.org/10.1089/ars.2017.7290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ozgür S, Sümer H, Koçoğlu G (1996) Rickets and soil strontium. Arch Dis Child 75:524–526. https://doi.org/10.1136/adc.75.6.524

    Article  PubMed  PubMed Central  Google Scholar 

  52. Li XT, Yu PF, Gao Y, Guo WH, Wang J, Liu X, Gu AH, Ji GX, Dong Q, Wang BS, Cao Y, Zhu BL, Xiao H (2017) Association between plasma metal levels and diabetes risk:a case-control study in China. Biomed Environ Sci 30:482–491. https://doi.org/10.3967/bes2017.064

    Article  PubMed  Google Scholar 

  53. Wang X, Ning Y, Zhang P, Li C, Zhou R, Guo X (2019) Hair multi-bioelement profile of Kashin-Beck disease in the endemic regions of China. J Trace Elem Med Biol 54:79–97. https://doi.org/10.1016/j.jtemb.2019.04.002

    Article  CAS  PubMed  Google Scholar 

  54. Budis H, Kalisinska E, Lanocha N, Kosik-Bogacka DI (2013) The concentration of manganese, iron and strontium in bone of red fox Vulpes vulpes (L. 1758). Biol Trace Elem Res 155:361–369. https://doi.org/10.1007/s12011-013-9809-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kravchenko J, Darrah TH, Miller RK, Lyerly HK, Vengosh A (2014) A review of the health impacts of barium from natural and anthropogenic exposure. Environ Geochem Health 36:797–814

    Article  CAS  Google Scholar 

  56. Chitambar CR (2010) Medical applications and toxicities of gallium compounds. Int J Environ Res Public Health 7:2337–2361. https://doi.org/10.3390/ijerph7052337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Yang M, Chitambar CR (2008) Role of oxidative stress in the induction of metallothionein-2A and heme oxygenase-1 gene expression by the antineoplastic agent gallium nitrate in human lymphoma cells. Free Radic Biol Med 45:763–772. https://doi.org/10.1016/j.freeradbiomed.2008.05.031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The work was supported by a grant from the Russian Scientific Foundation: No. 17-16-01043, “Search for effector units of metabolism regulated by alimentary factors in obesity or the development of innovative specialized food.”

Author information

Authors and Affiliations

Authors

Contributions

A.A. Shumakova: methodology, data curation, visualization, supervision, validation.

V.A. Shipelin: writing—original draft, supervision, project administration.

E.V. Leontyeva: investigation, resources.

I.V. Gmoshinski: conceptualization, formal analysis, writing—review and editing, supervision, funding acquisition.

Corresponding author

Correspondence to Ivan V. Gmoshinski.

Ethics declarations

Ethics Approval

The design of the experiment was approved by the Ethics Committee of the Federal Research Centre of Nutrition and Biotechnology (protocol no. 4 of 04/20/2017).

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shumakova, A.A., Shipelin, V.A., Leontyeva, E.V. et al. Effect of Resveratrol, l-Carnitine, and Aromatic Amino Acid Supplements on the Trace Element Content in the Organs of Mice with Dietary-Induced Obesity. Biol Trace Elem Res 200, 281–297 (2022). https://doi.org/10.1007/s12011-021-02642-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02642-0

Keywords

Navigation