Skip to main content
Log in

Moderate adiposity levels counteract protein metabolism modifications associated with aging in rats

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Physiological parameters such as adiposity and age are likely to influence protein digestion and utilization. The aim of this study was to evaluate the combined effects of age and adiposity on casein protein and amino acid true digestibility and its postprandial utilization in rats.

Methods

Four groups were included (n = 7/8): 2 months/normal adiposity, 2 months/high adiposity, 11 months/normal adiposity and 11 months/high adiposity. Rats were given a calibrated meal containing 15N-labeled casein (Ingredia, Arras, France) and were euthanized 6 h later. Digestive contents were collected to assess protein and amino acid digestibilities. 15N enrichments were measured in plasma and urine to determine total body deamination. Fractional protein synthesis rate (FSR) was determined in different organs using a flooding dose of 13C valine.

Results

Nitrogen and amino acid true digestibility of casein was around 95–96% depending on the group and was increased by 1% in high adiposity rats (P = 0.04). Higher adiposity levels counteracted the increase in total body deamination (P = 0.03) that was associated with older age. Significant effects of age (P = 0.006) and adiposity (P = 0.002) were observed in the muscle FSR, with age decreasing it and adiposity increasing it.

Conclusion

This study revealed that a higher level of adiposity resulted in a slight increase in protein and individual amino acid true digestibility values and seemed to compensate for the metabolic postprandial protein alterations observed at older age.

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

Similar content being viewed by others

References

  1. Consultation JWFUE (2007) Protein and amino acid requirements in human nutrition. World Health Organ Tech Rep Ser. Switzerland

  2. Millward DJ, Layman DK, Tome D, Schaafsma G (2008) Protein quality assessment: impact of expanding understanding of protein and amino acid needs for optimal health. Am J Clin Nutr 87(5):1576S-1581S. https://doi.org/10.1093/ajcn/87.5.1576S

    Article  CAS  PubMed  Google Scholar 

  3. Bhutto A, Morley JE (2008) The clinical significance of gastrointestinal changes with aging. Curr Opin Clin Nutr Metab Care 11(5):651–660. https://doi.org/10.1097/MCO.0b013e32830b5d37

    Article  CAS  PubMed  Google Scholar 

  4. Salles N (2007) Basic mechanisms of the aging gastrointestinal tract. Dig Dis 25(2):112–117. https://doi.org/10.1159/000099474

    Article  CAS  PubMed  Google Scholar 

  5. Gorissen SHM, Trommelen J, Kouw IWK, Holwerda AM, Pennings B, Groen BBL, Wall BT, Churchward-Venne TA, Horstman AMH, Koopman R, Burd NA, Fuchs CJ, Dirks ML, Res PT, Senden JMG, Steijns J, de Groot L, Verdijk LB, van Loon LJC (2020) Protein type, protein dose, and age modulate dietary protein digestion and phenylalanine absorption kinetics and plasma phenylalanine availability in humans. J Nutr 150(8):2041–2050. https://doi.org/10.1093/jn/nxaa024

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gilani GS, Cockell KA, Sepehr E (2005) Effects of antinutritional factors on protein digestibility and amino acid availability in foods. J AOAC Int 88(3):967–987

    Article  CAS  Google Scholar 

  7. Dardevet D, Sornet C, Balage M, Grizard J (2000) Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age. J Nutr 130(11):2630–2635. https://doi.org/10.1093/jn/130.11.2630

    Article  CAS  PubMed  Google Scholar 

  8. Dardevet D, Sornet C, Bayle G, Prugnaud J, Pouyet C, Grizard J (2002) Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J Nutr 132(1):95–100. https://doi.org/10.1093/jn/132.1.95

    Article  CAS  PubMed  Google Scholar 

  9. Wall BT, Gorissen SH, Pennings B, Koopman R, Groen BB, Verdijk LB, van Loon LJ (2015) Aging is accompanied by a blunted muscle protein synthetic response to protein ingestion. PLoS One 10(11):e0140903. https://doi.org/10.1371/journal.pone.0140903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Markofski MM, Dickinson JM, Drummond MJ, Fry CS, Fujita S, Gundermann DM, Glynn EL, Jennings K, Paddon-Jones D, Reidy PT, Sheffield-Moore M, Timmerman KL, Rasmussen BB, Volpi E (2015) Effect of age on basal muscle protein synthesis and mTORC1 signaling in a large cohort of young and older men and women. Exp Gerontol 65:1–7. https://doi.org/10.1016/j.exger.2015.02.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Do TT, Hindlet P, Waligora-Dupriet AJ, Kapel N, Neveux N, Mignon V, Delomenie C, Farinotti R, Feve B, Buyse M (2014) Disturbed intestinal nitrogen homeostasis in a mouse model of high-fat diet-induced obesity and glucose intolerance. Am J Physiol Endocrinol Metab 306(6):E668-680. https://doi.org/10.1152/ajpendo.00437.2013

    Article  CAS  PubMed  Google Scholar 

  12. Anderson SR, Gilge DA, Steiber AL, Previs SF (2008) Diet-induced obesity alters protein synthesis: tissue-specific effects in fasted versus fed mice. Metab Clin Exp 57(3):347–354. https://doi.org/10.1016/j.metabol.2007.10.009

    Article  CAS  PubMed  Google Scholar 

  13. Beals JW, Sukiennik RA, Nallabelli J, Emmons RS, van Vliet S, Young JR, Ulanov AV, Li Z, Paluska SA, De Lisio M, Burd NA (2016) Anabolic sensitivity of postprandial muscle protein synthesis to the ingestion of a protein-dense food is reduced in overweight and obese young adults. Am J Clin Nutr 104(4):1014–1022. https://doi.org/10.3945/ajcn.116.130385

    Article  CAS  PubMed  Google Scholar 

  14. Zhu S, Tian Z, Torigoe D, Zhao J, Xie P, Sugizaki T, Sato M, Horiguchi H, Terada K, Kadomatsu T, Miyata K, Oike Y (2019) Aging- and obesity-related peri-muscular adipose tissue accelerates muscle atrophy. PLoS One 14(8):e0221366. https://doi.org/10.1371/journal.pone.0221366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tessier R, Khodorova N, Calvez J, Kapel R, Quinsac A, Piedcoq J, Tome D, Gaudichon C (2020) 15N and (2)H intrinsic labeling demonstrate that real digestibility in rats of proteins and amino acids from sunflower protein isolate is almost as high as that of goat whey. J Nutr 150(3):450–457. https://doi.org/10.1093/jn/nxz279

    Article  PubMed  Google Scholar 

  16. Chevalier L, Bos C, Azzout-Marniche D, Fromentin G, Mosoni L, Hafnaoui N, Piedcoq J, Tome D, Gaudichon C (2013) Energy restriction only slightly influences protein metabolism in obese rats, whatever the level of protein and its source in the diet. Int J Obes 37(2):263–271. https://doi.org/10.1038/ijo.2012.19

    Article  CAS  Google Scholar 

  17. Bos C, Stoll B, Fouillet H, Gaudichon C, Guan X, Grusak MA, Reeds PJ, Burrin DG, Tome D (2005) Postprandial intestinal and whole body nitrogen kinetics and distribution in piglets fed a single meal. Am J Physiol Endocrinol Metab 288(2):E436-446. https://doi.org/10.1152/ajpendo.00263.2004

    Article  CAS  PubMed  Google Scholar 

  18. Lacroix M, Leonil J, Bos C, Henry G, Airinei G, Fauquant J, Tome D, Gaudichon C (2006) Heat markers and quality indexes of industrially heat-treated [15N] milk protein measured in rats. J Agric Food Chem 54(4):1508–1517. https://doi.org/10.1021/jf051304d

    Article  CAS  PubMed  Google Scholar 

  19. Moro J, Chaumontet C, Even PC, Blais A, Piedcoq J, Gaudichon C, Tome D, Azzout-Marniche D (2021) Severe protein deficiency induces hepatic expression and systemic level of FGF21 but inhibits its hypothalamic expression in growing rats. Sci Rep 11(1):12436. https://doi.org/10.1038/s41598-021-91274-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Guillin FM, Gaudichon C, Guerin-Deremaux L, Lefranc-Millot C, Azzout-Marniche D, Khodorova N, Calvez J (2021) Multi-criteria assessment of pea protein quality in rats: a comparison between casein, gluten and pea protein alone or supplemented with methionine. Br J Nutr 125(4):389–397. https://doi.org/10.1017/S0007114520002883

    Article  CAS  PubMed  Google Scholar 

  21. Tessier R, Ribeiro-Parenti L, Bruneau O, Khodorova N, Cavin JB, Bado A, Azzout-Marniche D, Calvez J, Le Gall M, Gaudichon C (2019) Effect of different bariatric surgeries on dietary protein bioavailability in rats. Am J Physiol Gastrointest Liver Physiol 317(5):G592–G601. https://doi.org/10.1152/ajpgi.00142.2019

    Article  CAS  PubMed  Google Scholar 

  22. Waynforth HB, Flecknell PA (1992) Experimental and surgical technique in the rat. Academic Press, San Diego

    Google Scholar 

  23. Gilani GS, Sepehr E (2003) Protein digestibility and quality in products containing antinutritional factors are adversely affected by old age in rats. J Nutr 133(1):220–225. https://doi.org/10.1093/jn/133.1.220

    Article  CAS  PubMed  Google Scholar 

  24. Oberli M, Lan A, Khodorova N, Sante-Lhoutellier V, Walker F, Piedcoq J, Davila AM, Blachier F, Tome D, Fromentin G, Gaudichon C (2016) Compared with raw bovine meat, boiling but not grilling, barbecuing, or roasting decreases protein digestibility without any major consequences for intestinal mucosa in rats, although the daily ingestion of bovine meat induces histologic modifications in the colon. J Nutr 146(8):1506–1513. https://doi.org/10.3945/jn.116.230839

    Article  CAS  PubMed  Google Scholar 

  25. Ghasemi A, Zahediasl S (2012) Normality tests for statistical analysis: a guide for non-statisticians. Int J Endocrinol Metab 10(2):486–489. https://doi.org/10.5812/ijem.3505

    Article  PubMed  PubMed Central  Google Scholar 

  26. Whitley E, Ball J (2002) Statistics review 5: comparison of means. Crit Care 6(5):424–428. https://doi.org/10.1186/cc1548

    Article  PubMed  PubMed Central  Google Scholar 

  27. Mishra P, Singh U, Pandey CM, Mishra P, Pandey G (2019) Application of student’s t-test, analysis of variance, and covariance. Ann Card Anaesth 22(4):407–411. https://doi.org/10.4103/aca.ACA_94_19

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gałecki A, Burzykowski T (2013) Linear mixed-effects model. In: Linear mixed-effects models using R: a step-by-step approach. Springer New York, New York, NY, pp 245–273. https://doi.org/10.1007/978-1-4614-3900-4_13

  29. Chalvon-Demersay T, Blachier F, Tome D, Blais A (2017) Animal models for the study of the relationships between diet and obesity: a focus on dietary protein and estrogen deficiency. Front Nutr 4:5. https://doi.org/10.3389/fnut.2017.00005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. FAO (2013) Dietary protein quality evaluation in human nutrition. Report of an FAO expert consultation. Food and Nutrition Paper no. 92, Rome

  31. Deglaire A, Moughan PJ (2012) Animal models for determining amino acid digestibility in humans—a review. Br J Nutr 108(Suppl 2):S273–S281. https://doi.org/10.1017/S0007114512002346

    Article  CAS  PubMed  Google Scholar 

  32. Gaudichon C, Calvez J (2021) Determinants of amino acid bioavailability from ingested protein in relation to gut health. Curr Opin Clin Nutr Metab Care 24(1):55–61. https://doi.org/10.1097/MCO.0000000000000708

    Article  CAS  PubMed  Google Scholar 

  33. de Moura EDM, Dos Reis SA, da Conceicao LL, Sediyama C, Pereira SS, de Oliveira LL, Gouveia Peluzio MDC, Martinez JA, Milagro FI (2021) Diet-induced obesity in animal models: points to consider and influence on metabolic markers. Diabetol Metab Syndr 13(1):32. https://doi.org/10.1186/s13098-021-00647-2

    Article  CAS  Google Scholar 

  34. Hira T, Suto R, Kishimoto Y, Kanahori S, Hara H (2018) Resistant maltodextrin or fructooligosaccharides promotes GLP-1 production in male rats fed a high-fat and high-sucrose diet, and partially reduces energy intake and adiposity. Eur J Nutr 57(3):965–979. https://doi.org/10.1007/s00394-017-1381-7

    Article  CAS  PubMed  Google Scholar 

  35. Matias AM, Estevam WM, Coelho PM, Haese D, Kobi J, Lima-Leopoldo AP, Leopoldo AS (2018) Differential effects of high sugar, high lard or a combination of both on nutritional, hormonal and cardiovascular metabolic profiles of rodents. Nutrients 10 (8). https://doi.org/10.3390/nu10081071

  36. Miranda J, Eseberri I, Lasa A, Portillo MP (2018) Lipid metabolism in adipose tissue and liver from diet-induced obese rats: a comparison between Wistar and Sprague-Dawley strains. J Physiol Biochem 74(4):655–666. https://doi.org/10.1007/s13105-018-0654-9

    Article  CAS  PubMed  Google Scholar 

  37. Masgrau A, Mishellany-Dutour A, Murakami H, Beaufrere AM, Walrand S, Giraudet C, Migne C, Gerbaix M, Metz L, Courteix D, Guillet C, Boirie Y (2012) Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol 590(20):5199–5210. https://doi.org/10.1113/jphysiol.2012.238576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rutherfurd SM, Moughan PJ (1998) The digestible amino acid composition of several milk proteins: application of a new bioassay. J Dairy Sci 81(4):909–917. https://doi.org/10.3168/jds.S0022-0302(98)75650-4

    Article  CAS  PubMed  Google Scholar 

  39. Horiuchi A, Tanaka N, Sakai R, Kawamata Y (2014) Effect of age and elemental diets on gastric emptying in rats. J Gastroenterol Hepatol Res 3:1340–1343

    Article  CAS  Google Scholar 

  40. Smits GJ, Lefebvre RA (1996) Influence of aging on gastric emptying of liquids, small intestine transit, and fecal output in rats. Exp Gerontol 31(5):589–596. https://doi.org/10.1016/0531-5565(96)00029-0

    Article  CAS  PubMed  Google Scholar 

  41. Rehfeld JF (2017) Cholecystokinin-from local gut hormone to ubiquitous messenger. Front Endocrinol 8:47. https://doi.org/10.3389/fendo.2017.00047

    Article  Google Scholar 

  42. Miner-Williams WM, Stevens BR, Moughan PJ (2014) Are intact peptides absorbed from the healthy gut in the adult human? Nutr Res Rev 27(2):308–329. https://doi.org/10.1017/S0954422414000225

    Article  CAS  PubMed  Google Scholar 

  43. Rohr MW, Narasimhulu CA, Rudeski-Rohr TA, Parthasarathy S (2020) Negative effects of a high-fat diet on intestinal permeability: a review. Adv Nutr 11(1):77–91. https://doi.org/10.1093/advances/nmz061

    Article  PubMed  Google Scholar 

  44. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrere B (1997) Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA 94(26):14930–14935. https://doi.org/10.1073/pnas.94.26.14930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jourdan M, Deutz NE, Cynober L, Aussel C (2011) Features, causes and consequences of splanchnic sequestration of amino acid in old rats. PLoS ONE 6(11):e27002. https://doi.org/10.1371/journal.pone.0027002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mays PK, McAnulty RJ, Laurent GJ (1991) Age-related changes in rates of protein synthesis and degradation in rat tissues. Mech Ageing Dev 59(3):229–241. https://doi.org/10.1016/0047-6374(91)90134-l

    Article  CAS  PubMed  Google Scholar 

  47. Obled C, Arnal M (1992) Contribution of skin to whole-body protein synthesis in rats at different stages of maturity. J Nutr 122(11):2167–2173. https://doi.org/10.1093/jn/122.11.2167

    Article  CAS  PubMed  Google Scholar 

  48. Holloszy JO, Chen M, Cartee GD, Young JC (1991) Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech Ageing Dev 60(2):199–213. https://doi.org/10.1016/0047-6374(91)90131-i

    Article  CAS  PubMed  Google Scholar 

  49. Mosoni L, Patureau Mirand P, Houlier ML, Arnal M (1993) Age-related changes in protein synthesis measured in vivo in rat liver and gastrocnemius muscle. Mech Ageing Dev 68(1–3):209–220. https://doi.org/10.1016/0047-6374(93)90152-h

    Article  CAS  PubMed  Google Scholar 

  50. Mosoni L, Valluy MC, Serrurier B, Prugnaud J, Obled C, Guezennec CY, Mirand PP (1995) Altered response of protein synthesis to nutritional state and endurance training in old rats. Am J Physiol 268(2 Pt 1):E328-335. https://doi.org/10.1152/ajpendo.1995.268.2.E328

    Article  CAS  PubMed  Google Scholar 

  51. Rasmussen BB, Fujita S, Wolfe RR, Mittendorfer B, Roy M, Rowe VL, Volpi E (2006) Insulin resistance of muscle protein metabolism in aging. FASEB J 20(6):768–769. https://doi.org/10.1096/fj.05-4607fje

    Article  CAS  PubMed  Google Scholar 

  52. Wolfe RR (2000) Effects of insulin on muscle tissue. Curr Opin Clin Nutr Metab Care 3(1):67–71. https://doi.org/10.1097/00075197-200001000-00011

    Article  CAS  PubMed  Google Scholar 

  53. Gloy VL, Lutz TA, Langhans W, Geary N, Hillebrand JJ (2010) Basal plasma levels of insulin, leptin, ghrelin, and amylin do not signal adiposity in rats recovering from forced overweight. Endocrinology 151(9):4280–4288. https://doi.org/10.1210/en.2010-0439

    Article  CAS  PubMed  Google Scholar 

  54. Devi S, Varkey A, Sheshshayee MS, Preston T, Kurpad AV (2018) Measurement of protein digestibility in humans by a dual-tracer method. Am J Clin Nutr 107(6):984–991. https://doi.org/10.1093/ajcn/nqy062

    Article  PubMed  PubMed Central  Google Scholar 

  55. Pes GM, Licheri G, Soro S, Longo NP, Salis R, Tomassini G, Niolu C, Errigo A, Dore MP (2019) Overweight: a protective factor against comorbidity in the elderly. Int J Environ Res Public Health 16(19). https://doi.org/10.3390/ijerph16193656

Download references

Acknowledgements

We thank Antoine Verloin from GAEC des 3 chênes for labeling the cow milk and Aziz Smira for contributing to sample analysis.

Funding

This project was funded by Ingredia.

Author information

Authors and Affiliations

Authors

Contributions

The authors’ responsibilities were as follows: CG, JC, ABa and ABo contributed to the conception and design of the study; NA, JC conducted the research; NA, JC, NK, CC, JP, and MC contributed to data acquisition; NA and JC analyzed the data; NA wrote the original draft of the paper; JC, CG, DAM, ABa, and ABo reviewed and edited the manuscript; CG administered the project; and all authors read and approved the final manuscript.

Corresponding author

Correspondence to Juliane Calvez.

Ethics declarations

Conflict of interest

C.G., D.A.M., N.K., C.C., J.P., M.C. and J.C. declare that they have no conflict of interest. N.A., A.Ba., and A.Bo. are employed by Ingredia.

Ethics approval

All procedures involving animals were in compliance with the European Union directive 2010/63/EU for animal experiments and approved by the ethics committee in animal experiments of INRAE Jouy-en-Josas (Comethea, registration number: 18-14) and the French Ministry of Higher Education and Research (APAFIS no 15907-2018061823133762 v1).

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 55 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Atallah, N., Gaudichon, C., Boulier, A. et al. Moderate adiposity levels counteract protein metabolism modifications associated with aging in rats. Eur J Nutr 61, 3189–3200 (2022). https://doi.org/10.1007/s00394-022-02881-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-022-02881-4

Keywords

Navigation