Skip to main content

Advertisement

Log in

Voluntary exercise improves murine dermal connective tissue status in high-fat diet-induced obesity

  • Concise Communication
  • Published:
Archives of Dermatological Research Aims and scope Submit manuscript

Abstract

Obesity is a risk factor for several cardiovascular and metabolic diseases. Its influence on the skin is less obvious, yet certain negative effects of adipose tissue inflammation on the dermis have been suggested. Excess weight is closely associated with sedentary behavior, so any increase in physical activity is considered beneficial against obesity. To investigate the effects of obesity and physical exercise on the skin, we established a mouse model in which mice were kept either on a high-fat diet or received standard chow. After the two groups achieved a significant weight difference, physical exercise was introduced to both. Animals were given the opportunity to perform voluntary exercise for 40 min daily in a hamster wheel for a period of 8 weeks. We evaluated the status of the dermis at the beginning and at the end of the exercise period by in vivo nonlinear microscopy. Obese mice kept on high-fat diet lost weight steadily after they started to exercise. In the high-fat diet group, we could detect significantly larger adipocytes and a thicker layer of subcutaneous tissue; both changes started to normalize after exercise. Nonlinear microscopy revealed an impaired collagen structure in obese mice that improved considerably after physical activity was introduced. With the ability to detect damage on collagen structure, we set out to address the question whether this process is reversible. With the use of a novel imaging method, we were able to show the reversibility of connective tissue deterioration as a benefit of physical exercise.

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

References

  1. Alex A, Weingast J, Weinigel M, Kellner-Hofer M, Nemecek R, Binder M, Pehamberger H, Konig K, Drexler W (2013) Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology. J Biophoton 6:352–362. doi:10.1002/jbio.201200085

    Article  Google Scholar 

  2. Brianezi G, Grandi F, Bagatin E, Enokihara MM, Miot HA (2015) Dermal type I collagen assessment by digital image analysis. An Bras Dermatol 90:723–727. doi:10.1590/abd1806-4841.20153331

    Article  PubMed  PubMed Central  Google Scholar 

  3. Conney AH, Lou YR, Nghiem P, Bernard JJ, Wagner GC, Lu YP (2013) Inhibition of UVB-induced nonmelanoma skin cancer: a path from tea to caffeine to exercise to decreased tissue fat. Top Curr Chem 329:61–72. doi:10.1007/128_2012_336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Crane JD, MacNeil LG, Lally JS, Ford RJ, Bujak AL, Brar IK, Kemp BE, Raha S, Steinberg GR, Tarnopolsky MA (2015) Exercise-stimulated interleukin-15 is controlled by AMPK and regulates skin metabolism and aging. Aging cell 14:625–634. doi:10.1111/acel.12341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Distler JH, Jungel A, Huber LC, Schulze-Horsel U, Zwerina J, Gay RE, Michel BA, Hauser T, Schett G, Gay S, Distler O (2007) Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis Rheum 56:311–322. doi:10.1002/art.22314

    Article  CAS  PubMed  Google Scholar 

  6. Ezure T, Amano S (2010) Increased subcutaneous adipose tissue impairs dermal function in diet-induced obese mice. Exp Dermatol 19:878–882. doi:10.1111/j.1600-0625.2009.00970.x

    Article  CAS  PubMed  Google Scholar 

  7. Ezure T, Amano S (2015) Increment of subcutaneous adipose tissue is associated with decrease of elastic fibres in the dermal layer. Exp Dermatol 24:924–929. doi:10.1111/exd.12816

    Article  CAS  PubMed  Google Scholar 

  8. Firth J, Stubbs B, Rosenbaum S, Vancampfort D, Malchow B, Schuch F, Elliott R, Nuechterlein KH, Yung AR (2016) Aerobic exercise improves cognitive functioning in people with schizophrenia: a systematic review and meta-analysis. Schizophr Bull. doi:10.1093/schbul/sbw115

    Google Scholar 

  9. Gkogkolou P, Bohm M (2012) Advanced glycation end products: key players in skin aging? Dermatoendocrinol 4:259–270. doi:10.4161/derm.22028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Grundy SM (2016) Metabolic syndrome update. Trends Cardiovasc Med 26:364–373. doi:10.1016/j.tcm.2015.10.004

    Article  PubMed  Google Scholar 

  11. Haluszka D, Lorincz K, Molnar G, Tamas G, Kolonics A, Szipocs R, Karpati S, Wikonkal NM (2015) In vivo second-harmonic generation and ex vivo coherent anti-stokes raman scattering microscopy to study the effect of obesity to fibroblast cell function using an Yb-fiber laser-based CARS extension unit. Microsc Res Tech 78:823–830. doi:10.1002/jemt.22545

    Article  CAS  PubMed  Google Scholar 

  12. Haluszka D, Lőrincz K, Kiss N, Szipőcs R, Kuroli E, Gyöngyösi N, Wikonkál NM (2016) Diet-induced obesity skin changes monitored by in vivo SHG and ex vivo CARS microscopy. Biomed Opt Express 7:4480–4489. doi:10.1364/BOE.7.004480

    Article  PubMed  PubMed Central  Google Scholar 

  13. Head GA (2015) Cardiovascular and metabolic consequences of obesity. Front Physiol. doi:10.3389/fphys.2015.00032

    PubMed  PubMed Central  Google Scholar 

  14. Kawanishi N, Niihara H, Mizokami T, Yada K, Suzuki K (2015) Exercise training attenuates neutrophil infiltration and elastase expression in adipose tissue of high-fat-diet-induced obese mice. Physiol Rep. doi:10.14814/phy2.12534

    PubMed  PubMed Central  Google Scholar 

  15. Keylock KT, Vieira VJ, Wallig MA, DiPietro LA, Schrementi M, Woods JA (2008) Exercise accelerates cutaneous wound healing and decreases wound inflammation in aged mice. Am J Physiol Regul Integr Comp Physiol 294:R179–R184. doi:10.1152/ajpregu.00177.2007

    Article  CAS  PubMed  Google Scholar 

  16. Kim TW, Choi HH, Chung YR (2016) Treadmill exercise alleviates impairment of cognitive function by enhancing hippocampal neuroplasticity in the high-fat diet-induced obese mice. J Exerc Rehabil 12:156–162. doi:10.12965/jer.1632644.322

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lopes HF, Correa-Giannella ML, Consolim-Colombo FM, Egan BM (2016) Visceral adiposity syndrome. Diabetol Metab Syndr 8:40. doi:10.1186/s13098-016-0156-2

    Article  PubMed  PubMed Central  Google Scholar 

  18. Mirmirani P, Carpenter DM (2014) Skin disorders associated with obesity in children and adolescents: a population-based study. Pediatr Dermatol 31:183–190. doi:10.1111/pde.12271

    Article  PubMed  Google Scholar 

  19. Murphy EA, Enos RT, Velazquez KT (2015) Influence of exercise on inflammation in cancer: direct effect or innocent bystander? Exerc Sport Sci Rev 43:134–142. doi:10.1249/JES.0000000000000054

    Article  PubMed  Google Scholar 

  20. Mykkanen OT, Huotari A, Herzig KH, Dunlop TW, Mykkanen H, Kirjavainen PV (2014) Wild blueberries (Vaccinium myrtillus) alleviate inflammation and hypertension associated with developing obesity in mice fed with a high-fat diet. PLoS One 9:e114790. doi:10.1371/journal.pone.0114790

    Article  PubMed  PubMed Central  Google Scholar 

  21. Pence BD, DiPietro LA, Woods JA (2012) Exercise speeds cutaneous wound healing in high-fat diet-induced obese mice. Med Sci Sports Exerc 44:1846–1854. doi:10.1249/MSS.0b013e31825a5971

    Article  PubMed  Google Scholar 

  22. Pence BD, Woods JA (2014) Exercise, obesity, and cutaneous wound healing: evidence from rodent and human studies. Adv Wound Care (New Rochelle) 3:71–79. doi:10.1089/wound.2012.0377

    Article  Google Scholar 

  23. Rosen ED, Spiegelman BM (2014) What we talk about when we talk about fat. Cell 156:20–44. doi:10.1016/j.cell.2013.12.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Seitz O, Schurmann C, Hermes N, Muller E, Pfeilschifter J, Frank S, Goren I (2010) Wound healing in mice with high-fat diet- or ob gene-induced diabetes-obesity syndromes: a comparative study. Exp Diabetes Res 2010:476969. doi:10.1155/2010/476969

    Article  PubMed  Google Scholar 

  25. Shipman AR, Millington GW (2011) Obesity and the skin. Br J Dermatol 165:743–750. doi:10.1111/j.1365-2133.2011.10393.x

    Article  CAS  PubMed  Google Scholar 

  26. Yosipovitch G, DeVore A, Dawn A (2007) Obesity and the skin: skin physiology and skin manifestations of obesity. J Am Acad Dermatol 56:901–916. doi:10.1016/j.jaad.2006.12.004 (quiz 917–920)

    Article  PubMed  Google Scholar 

  27. Zhang Y, Li Q, Rao E, Sun Y, Grossmann ME, Morris RJ, Cleary MP, Li B (2015) Epidermal fatty acid binding protein promotes skin inflammation induced by high-fat diet. Immunity 42:953–964. doi:10.1016/j.immuni.2015.04.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zogaib FG, Monte-Alto-Costa A (2011) Moderate intensity physical training accelerates healing of full-thickness wounds in mice. Braz J Med Biol Res 44:1025–1035. doi:10.1590/s0100-879x2011007500115

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge the work of Prof. Sarolta Kárpáti, and the support and help of Drs. Enikő Kuroli and Dávid Szöllősi for reading the histopathological sections and for the statistical analyses. Funding: Hungarian Development Agency, Contract No.: TECH-09-A2-2009-0134.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Norbert M. Wikonkál.

Ethics declarations

All procedures were approved by the institutional Ethical Committee of Semmelweis University (PEI/001/800-6/2015).

Conflict of interest

The authors declare no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lőrincz, K., Haluszka, D., Kiss, N. et al. Voluntary exercise improves murine dermal connective tissue status in high-fat diet-induced obesity. Arch Dermatol Res 309, 209–215 (2017). https://doi.org/10.1007/s00403-017-1715-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00403-017-1715-6

Keywords

Navigation