Advertisement

Biogerontology

, Volume 20, Issue 1, pp 71–82 | Cite as

Carbohydrate-restricted diet promotes skin senescence in senescence-accelerated prone mice

  • Qiming Wu
  • Shuang E
  • Kazushi Yamamoto
  • Tsuyoshi TsudukiEmail author
Research Article

Abstract

This study used senescence-accelerated prone mice (SAMP8) to examine the effects of a carbohydrate-restricted diet on aging and skin senescence, to determine how long-term carbohydrate restriction affects the aging process. Three-week-old male SAMP8 mice were divided into three groups after 1 week of preliminary feeding: one was given a controlled diet, the other was given a high-fat diet, and the third was given a carbohydrate-restricted diet. Ad libitum feeding was administered until the mice reached 50 weeks of age. Before the end of the test period, a grading test was used to evaluate visible aging in the mice. After the test period, serum and skin samples in mice were obtained and submitted for analysis. As a result, the grading test demonstrated that there was significant progression of visible aging in the carbohydrate-restricted group, as well as a decreased survival rate. Histological examination of the skin revealed that the epidermis and dermis in the carbohydrate-restricted group had become thinner. Analysis of the mechanisms involved demonstrated an increase in serum interleukin-6, aggravated skin senescence, inhibition of skin autophagy and activation of skin mTOR. Therefore, this study proved that a carbohydrate-restricted diet promoted skin senescence in senescence-accelerated mice.

Keywords

Aging Autophagy Carbohydrate-restricted diet IL-6 mTOR Senescence-accelerated mice 

Notes

Acknowledgements

This research was supported by grants from the Project of the NARO Bio-oriented Technology Research Advancement Institution (Advanced integration research for agriculture and interdisciplinary fields).

Compliance with ethical standards

Conflict of interest

There are no conflicts of interest.

References

  1. Asano M, Iwagaki Y, Sugawara S, Kushida M, Okouchi R, Yamamoto K, Tsuduki T (2018) Effects of the Japanese diet in combination with exercise on visceral fat accumulation. Nutrition 57:173–182.  https://doi.org/10.1016/j.nut.2018.05.023 CrossRefGoogle Scholar
  2. Bedarida T, Baron S, Vessieres E, Vibert F, Ayer A, Marchiol-Fournigault C, Henrion D, Paul JL, Noble F, Golmard JL, Beaudeux JL, Cottart CH, Nivet-Antoine V (2014) High-protein-low-carbohydrate diet: deleterious metabolic and cardiovascular effects depend on age. Am J Physiol Heart Circ Physiol 307:H649–H657.  https://doi.org/10.1152/ajpheart.00291.2014 CrossRefGoogle Scholar
  3. Bhawan J, Oh CH, Lew R, Nehal KS, Labadie RR, Tsay A, Gilchrest BA (1992) Histopathologic differences in the photoaging process in facial versus arm skin. Am J Dermatopathol 14:224–230CrossRefGoogle Scholar
  4. Bringhenti I, Schultz A, Rachid T, Bomfim MA, Mandarim-de-Lacerda CA, Aguila MB (2011) An early fish oil-enriched diet reverses biochemical, liver and adipose tissue alterations in male offspring from maternal protein restriction in mice. J Nutr Biochem 22:1009–1014CrossRefGoogle Scholar
  5. Butterfield DA, Poon HF (2005) The senescence-accelerated prone mouse (SAMP8): a model of age-related cognitive decline with relevance to alterations of the gene expression and protein abnormalities in Alzheimer’s disease. Exp Gerontol 40:774–783CrossRefGoogle Scholar
  6. Dehghan M, Mente A, Zhang X, Swaminathan S, Li W, Mohan V, Iqbal R, Kumar R, Wentzel-Viljoen E, Rosengren A, Amma LI, Avezum A, Chifamba J, Diaz R, Khatib R, Lear S, Lopez-Jaramillo P, Liu X, Gupta R, Mohammadifard N, Gao N, Oguz A, Ramli AS, Seron P, Sun Y, Szuba A, Tsolekile L, Wielgosz A, Yusuf R, Hussein Yusufali A, Teo KK, Rangarajan S, Dagenais G, Bangdiwala SI, Islam S, Anand SS, Yusuf S, Prospective Urban Rural Epidemiology (PURE) study investigators (2017) Associations of fats and carbohydrate intake with cardiovascular disease and mortality in 18 countries from five continents (PURE): a prospective cohort study. Lancet 390:2050–2062.  https://doi.org/10.1016/S0140-6736(17)32252-3 CrossRefGoogle Scholar
  7. Donati A, Cavallini G, Paradiso C, Vittorini S, Pollera M, Gori Z, Bergamini E (2001) Age-related changes in the autophagic proteolysis of rat isolated liver cells: effects of antiaging dietary restrictions. J Gerontol A 56:B375–B383CrossRefGoogle Scholar
  8. Everitt AV, Rattan SI, Le Couteur DG, de Cabo R (eds) (2010) Calorie restriction, aging and longevity. Springer, New YorkGoogle Scholar
  9. Fromentin G, Darcel N, Chaumontet C, Marsset-Baglieri A, Nadkarni N, Tomé D (2012) Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins. Nutr Res Rev 25:29–39CrossRefGoogle Scholar
  10. Gilchrest BA, Blog FB, Szabo G (1979) Effects of aging and chronic sun exposure on melanocytes in human skin. J Invest Dermatol 73:141–143CrossRefGoogle Scholar
  11. Gilchrest BA, Murphy GF, Soter NA (1982) Effect of chronologic aging and ultraviolet irradiation on Langerhans cells in human epidermis. J Invest Dermatol 79:85–88CrossRefGoogle Scholar
  12. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885–889CrossRefGoogle Scholar
  13. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392–395CrossRefGoogle Scholar
  14. Honma T, Kitano Y, Kijima R, Jibu Y, Kawakami Y, Tsuduki T, Nakagawa K, Miyazawa T (2013) Comparison of the health benefits of different eras of japanese foods: lipid and carbohydrate metabolism focused research. Nippon Shokuhin Kagaku Kogaku Kaishi 60:541–553CrossRefGoogle Scholar
  15. Hosokawa M, Sakura M, Chiba Y (2013) The grading score system: a method for evaluating the degree of senescence in SAM strains of mice. In: Takeda T (ed) The senescence-accelerated mouse (SAM): achievements and future directions. Elsevier, Amsterdam, pp 561–567Google Scholar
  16. Inami Y, Waguri S, Sakamoto A, Kouno T, Nakada K, Hino O, Watanabe S, Ando J, Iwadate M, Yamamoto M, Lee MS, Tanaka K, Komatsu M (2011) Persistent activation of Nrf2 through p62 in hepatocellular carcinoma cells. J Cell Biol 193:275–284CrossRefGoogle Scholar
  17. Ishikawa H, Guo X, Sugawara S, Iwagaki Y, Yamamoto K, Tsuduki T (2018a) Effect of the Japanese diet during pregnancy and lactation or post-weaning on the risk of metabolic syndrome in offspring. Biosci Biotechnol Biochem 82:515–524.  https://doi.org/10.1080/09168451.2018.1428788 CrossRefGoogle Scholar
  18. Ishikawa H, Guo X, Sugawara S, Iwagaki Y, Yamamoto K, Konno A, Nishiuchi M, Tsuduki T (2018b) Influence of Japanese diet consumption during pregnancy and lactation on lipid metabolism in offspring. Nutrition.  https://doi.org/10.1016/j.nut.2018.06.006 Google Scholar
  19. Iwagaki Y, Sakamoto Y, Sugawara S, Mizowaki Y, Yamamoto K, Sugawara T, Kimura K, Tsuduki T (2017) Identification of characteristic components and foodstuffs in healthy Japanese diet and the health effects of a diet with increased use frequency of these foodstuffs. Mol Nutr Food Res 61:1700430.  https://doi.org/10.1002/mnfr.201700430 CrossRefGoogle Scholar
  20. Iwagaki Y, Sugawara S, Huruya Y, Sato M, Wu Q, E S, Yamamoto K, Tsuduki T (2018) The 1975 Japanese diet has a stress reduction effect in mice: search for physiological effects using metabolome analysis. Biosci Biotechnol Biochem 82:709–715CrossRefGoogle Scholar
  21. Jacobsen E, Billings JK, Frantz RA, Kinney CK, Stewart ME, Downing DT (1985) Age-related changes in sebaceous wax ester secretion rates in men and women. J Invest Dermatol 85:483–485CrossRefGoogle Scholar
  22. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150:1507–1513CrossRefGoogle Scholar
  23. Kamada Y, Yoshino K, Kondo C, Kawamata T, Oshiro N, Yonezawa K, Ohsumi Y (2010) Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 30:1049–1058CrossRefGoogle Scholar
  24. Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW, Thomas EL, Kockel L (2010) With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453–465CrossRefGoogle Scholar
  25. Kitano Y, Honma T, Hatakeyama Y, Jibu Y, Kawakami Y, Tsuduki T, Nakagawa K, Miyazawa T (2014) The effect of Japanese foods which changed with the age on the risk of obesity in mice. J Jpn Soc Nutr Food Sci 67:73–85CrossRefGoogle Scholar
  26. Kligman AM (1979) Perspectives and problems in cutaneous gerontology. J Invest Dermatol 73:39–46CrossRefGoogle Scholar
  27. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880–884CrossRefGoogle Scholar
  28. Kurban RS, Kurban AK (1993) Common skin disorders of aging: diagnosis and treatment. Geriatrics 48: 30–1, 35–6, 39–42Google Scholar
  29. Kushida M, Okouchi R, Iwagaki Y, Asano M, Du MX, Yamamoto K, Tsuduki T (2018) Fermented soybean suppresses visceral fat accumulation in mice. Mol Nutr Food Res 17:54.  https://doi.org/10.1002/mnfr.201701054 Google Scholar
  30. Longas MO, Russell CS, He XY (1987) Evidence for structural changes in dermatan sulfate and hyaluronic acid with aging. Carbohydr Res 159:127–136CrossRefGoogle Scholar
  31. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, Sinclair D, Starnes JW, Wilkinson JE, Nadon NL, Strong R (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A 66:191–201CrossRefGoogle Scholar
  32. Ministry of Agriculture, Forestry and Fisheries (2011) Food supply and demand figures (2010 fiscal year version). Ministry of Agriculture, Forestry and Fisherie, TokyoGoogle Scholar
  33. Ministry of Health, Labour and Welfare (2011) Patients survey. Ministry of Health, Labour and Welfare, TokyoGoogle Scholar
  34. Mizowaki Y, Sugawara S, Yamamoto K, Sakamoto Y, Iwagaki Y, Kawakami Y, Igarashi M, Tsuduki T (2017) Comparison of the effects of the 1975 Japanese diet and the modern Mediterranean diet on lipid metabolism in mice. J Oleo Sci 66:507–519.  https://doi.org/10.5650/jos.ess16241 CrossRefGoogle Scholar
  35. Montagna W, Carlisle K (1979) Structural changes in aging human skin. J Invest Dermatol 73:47–53CrossRefGoogle Scholar
  36. Procacci P, Bozza G, Buzzelli G, Della Corte M (1970) The cutaneous pricking pain threshold in old age. Gerontol Clin (Basel) 12:213–218CrossRefGoogle Scholar
  37. Rebrin I, Zicker S, Wedekind KJ, Paetau-Robinson I, Packer L, Sohal RS (2005) Effect of antioxidant-enriched diets on glutathione redox status in tissue homogenates and mitochondria of the senescence-accelerated mouse. Free Radic Biol Med 39:549–557CrossRefGoogle Scholar
  38. Shai I, Schwarzfuchs D, Henkin Y, Shahar DR, Witkow S, Greenberg I, Golan R, Fraser D, Bolotin A, Vardi H, Tangi-Rozental O, Zuk-Ramot R, Sarusi B, Brickner D, Schwartz Z, Sheiner E, Marko R, Katorza E, Thiery J, Fiedler GM, Blüher M, Stumvoll M, Stampfer MJ (2008) Dietary Intervention Randomized Controlled Trial (DIRECT) group, weight loss with a low-carbohydrate, mediterranean, or low-fat diet. N Engl J Med 359:229–241.  https://doi.org/10.1056/NEJMoa0708681 CrossRefGoogle Scholar
  39. Shimizu T, Mori K, Ouchi K, Kushida M, Tsuduki T (2018) Effects of dietary intake of japanese mushrooms on visceral fat accumulation and gut microbiota in mice. Nutrients 10:610.  https://doi.org/10.3390/nu10050610 CrossRefGoogle Scholar
  40. Shuster S, Black MM, McVitie E (1975) The influence of age and sex on skin thickness, skin collagen and density. Br J Dermatol 93:639–643CrossRefGoogle Scholar
  41. Solon-Biet SM, McMahon AC, Ballard JW, Ruohonen K, Wu LE, Cogger VC, Warren A, Huang X, Pichaud N, Melvin RG, Gokarn R, Khalil M, Turner N, Cooney GJ, Sinclair DA, Raubenheimer D, Le Couteur DG, Simpson SJ (2014) The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab 19:418–430.  https://doi.org/10.1016/j.cmet.2014.02.009 CrossRefGoogle Scholar
  42. Srividhya R, Jyothilakshmi V, Arulmathi K, Senthilkumaran V, Kalaiselvi P (2008) Attenuation of senescence-induced oxidative exacerbations in aged rat brain by (-)-epigallocatechin-3-gallate. Int J Dev Neurosci 26:217–223CrossRefGoogle Scholar
  43. Sugawara S, Kushida M, Iwagaki Y, Asano M, Yamamoto K, Tomata Y, Tsuji I, Tsuduki T (2018) The 1975 type Japanese diet improves lipid metabolic parameters in younger adults: a randomized controlled trial. J Oleo Sci 67:599–607.  https://doi.org/10.5650/jos.ess17259 CrossRefGoogle Scholar
  44. Takamura A, Komatsu M, Hara T, Sakamoto A, Kishi C, Waguri S, Eishi Y, Hino O, Tanaka K, Mizushima N (2011) Autophagy-deficient mice develop multiple liver tumors. Genes Dev 25:795–800CrossRefGoogle Scholar
  45. Takeda T, Hosokawa M, Takeshita S, Irino M, Higuchi K, Matsushita T, Tomita Y, Yasuhira K, Hamamoto H, Shimizu K, Ishii M, Yamamuro T (1981) A new murine model of accelerated senescence. Mech Ageing Dev 17:183–194CrossRefGoogle Scholar
  46. Takeda T, Hosokawa M, Higuchi K (1991) Senescence-accelerated mouse (SAM): a novel murine model of accelerated senescence. J Am Geriatr Soc 39:911–919CrossRefGoogle Scholar
  47. Takeda T, Matsushita T, Kurozumi M, Takemura K, Higuchi K, Hosokawa M (1997) Pathobiology of the senescence-accelerated mouse (SAM). Exp Gerontol 32:117–127CrossRefGoogle Scholar
  48. Terman A (1995) The effect of age on formation and elimination of autophagic vacuoles in mouse hepatocytes. Gerontology 41(Suppl 2):319–326CrossRefGoogle Scholar
  49. Tsuduki T, Takeshika N, Nakamura Y, Nakagawa K, Igarashi M, Miyazawa T (2008) DNA microarray analysis of rat liver after ingestion of Japanese and American food. J Jpn Soc Nutr Food Sci 61:255–264CrossRefGoogle Scholar
  50. Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T (2011) Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 27:334–337CrossRefGoogle Scholar
  51. Tsuduki T, Kuriyama K, Nakagawa K, Miyazawa T (2013) Tocotrienol (unsaturated vitamin E) suppresses degranulation of mast cells and reduces allergic dermatitis in mice. J Oleo Sci 62:825–834CrossRefGoogle Scholar
  52. Tsuzuki T, Tokuyama Y, Igarashi M, Miyazawa T (2004) Tumor growth suppression by alpha-eleostearic acid, a linolenic acid isomer with a conjugated triene system, via lipid peroxidation. Carcinogenesis 25:1417–1425CrossRefGoogle Scholar
  53. Uddin MN, Nishio N, Ito S, Suzuki H, Isobe K (2012) Autophagic activity in thymus and liver during aging. Age (Dordr) 34:75–85.  https://doi.org/10.1007/s11357-011-9221-9 CrossRefGoogle Scholar
  54. Yamamoto K, E S, Hatakeyama Y, Sakamoto Y, Tsuduki T (2015) High-fat diet intake from senescence inhibits the attenuation of cell functions and the degeneration of villi with aging in the small intestine, and inhibits the attenuation of lipid absorption ability in SAMP8 mice. J Clin Biochem Nutr 57:204–211CrossRefGoogle Scholar
  55. Yamamoto K, E S, Hatakeyama Y, Sakamoto Y, Honma T, Jibu Y, Kawakami Y, Tsuduki T (2016) The Japanese diet from 1975 delays senescence and prolongs life span in SAMP8 mice. Nutrition 32:122–128CrossRefGoogle Scholar
  56. Yamamoto K, Iwagaki Y, Watanabe K, Nochi T, Aso H, Tsuduki T (2018) Effects of a moderate-fat diet enriched with fish oil on intestinal lipid absorption in a senescence-accelerated prone mouse model. Nutrition 50:26–35.  https://doi.org/10.1016/j.nut.2017.10.015 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Qiming Wu
    • 1
  • Shuang E
    • 1
  • Kazushi Yamamoto
    • 1
  • Tsuyoshi Tsuduki
    • 1
    Email author
  1. 1.Laboratory of Food and Biomolecular Science, Graduate School of AgricultureTohoku UniversitySendaiJapan

Personalised recommendations