Skip to main content
Log in

The effects of exercise training associated with low-level laser therapy on biomarkers of adipose tissue transdifferentiation in obese women

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

Investigations suggest the benefits of low-level laser therapy (LLLT) to improve noninvasive body contouring treatments, inflammation, insulin resistance and to reduce body fat. However, the mechanism for such potential effects in association with exercise training (ET) and possible implications in browning adiposity processes remains unclear. Forty-nine obese women were involved, aged between 20 and 40 years with a body mass index (BMI) of 30–40 kg/m2. The volunteers were divided into Phototherapy (808 nm) and SHAM groups. Interventions consisted of exercise training and phototherapy applications post exercise for 4 months, with three sessions/week. Body composition, lipid profile, insulin resistance, atrial natriuretic peptide (ANP), WNT5 signaling, interleukin-6 (IL-6), and fibroblast growth factor-21 (FGF-21) were measured. Improvements in body mass, BMI, body fat mass, lean mass, visceral fat, waist circumference, insulin, HOMA-IR, total cholesterol, LDL-cholesterol, triglycerides, and ANP in both groups were demonstrated. Only the Phototherapy group showed a reduction in interleukin-6 and an increase in WNT5 signaling. In addition, it was possible to observe a higher magnitude change for the fat mass, insulin, HOMA-IR, and FGF-21 variables in the Phototherapy group. In the present investigation, it was demonstrated that exercise training associated with LLLT promotes an improvement in body composition and inflammatory processes as previously demonstrated. The Phototherapy group especially presented positive modifications of WNT5 signaling, FGF-21, and ANP, possible biomarkers associated with browning adiposity processes. This suggests that this kind of intervention promotes results applicable in clinical practice to control obesity and related comorbidities.

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

Similar content being viewed by others

References

  1. Gold MH, Khatri KA, Hails K, Weiss RA, Fournier N (2011) Reduction in thigh circumference and improvement in the appearance of cellulite with dual-wavelength, low-level laser energy and massage. J Cosmet Laser Ther 13:13–20. https://doi.org/10.3109/14764172.2011.552608

    Article  PubMed  Google Scholar 

  2. Jackson RF, Dedo DD, Roche GC, Turok DI, Maloney RJ (2009) Low-level laser therapy as a non-invasive approach for body contouring: a randomized, controlled study. Lasers Surg Med 41:799–809. https://doi.org/10.1002/lsm.20855

    Article  PubMed  Google Scholar 

  3. da Silveira Campos RM, Dâmaso AR, Masquio DC et al (2015) Low-level laser therapy (LLLT) associated with aerobic plus resistance training to improve inflammatory biomarkers in obese adults. Lasers Med Sci 30:1553–1563. https://doi.org/10.1007/s10103-015-1759-9

    Article  PubMed  Google Scholar 

  4. Duarte FO, Sene-Fiorese M, de Aquino Junior AE et al (2015) Can low-level laser therapy (LLLT) associated with an aerobic plus resistance training change the cardiometabolic risk in obese women? A placebo-controlled clinical trial. J Photochem Photobiol B 153:103–110. https://doi.org/10.1016/j.jphotobiol.2015.08.026

    Article  PubMed  CAS  Google Scholar 

  5. Sene-Fiorese M, Duarte FO, de Aquino Junior AE et al (2015) The potential of phototherapy to reduce body fat, insulin resistance and “metabolic inflexibility” related to obesity in women undergoing weight loss treatment. Lasers Surg Med 47:634–642. https://doi.org/10.1002/lsm.22395

    Article  PubMed  Google Scholar 

  6. Elsen M, Raschke S, Tennagels N et al (2014) BMP4 and BMP7 induce the white-to-brown transition of primary human adipose stem cells. Am J Physiol Cell Physiol 306:C431–C440. https://doi.org/10.1152/ajpcell.00290.2013

    Article  PubMed  CAS  Google Scholar 

  7. Ouellet V, Labbé SM, Blondin DP et al (2012) Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 122:545–552. https://doi.org/10.1172/JCI60433

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Stephens M, Ludgate M, Rees DA (2011) Brown fat and obesity: the next big thing? Clin Endocrinol 74:661–670. https://doi.org/10.1111/j.1365-2265.2011.04018.x

    Article  CAS  Google Scholar 

  9. Cypess AM, Lehman S, Williams G et al (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509–1517. https://doi.org/10.1056/NEJMoa0810780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM et al (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508. https://doi.org/10.1056/NEJMoa0808718

    Article  PubMed  Google Scholar 

  11. Saito M, Okamatsu-Ogura Y, Matsushita M et al (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531. https://doi.org/10.2337/db09-0530

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Virtanen KA, Lidell ME, Orava J et al (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525. https://doi.org/10.1056/NEJMoa0808949

    Article  PubMed  CAS  Google Scholar 

  13. Zingaretti MC, Crosta F, Vitali A et al (2009) The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J 23:3113–3120. https://doi.org/10.1096/fj.09-133546

    Article  PubMed  CAS  Google Scholar 

  14. Nishida C, Ko GT, Kumanyika S (2010) Body fat distribution and noncommunicable diseases in populations: overview of the 2008 WHO expert consultation on waist circumference and waist-hip ratio. Eur J Clin Nutr 64:2–5. https://doi.org/10.1038/ejcn.2009.139

    Article  PubMed  CAS  Google Scholar 

  15. Geloneze B, Repetto EM, Geloneze SR, Tambascia MA, Ermetice MN (2006) The threshold value for insulin resistance (HOMA-IR) in an admixtured population IR in the Brazilian Metabolic Syndrome Study. Diabetes Res Clin Pract 72:219–220

    Article  PubMed  CAS  Google Scholar 

  16. Kraemer WJ, Ratamess NA, French DN (2002) Resistance training for health and performance. Curr Sports Med Rep 1:165–171

    Article  PubMed  Google Scholar 

  17. Donnelly JE, Blair SN, Jakicic JM et al (2009) American College of Sports Medicine position stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc 41:459–471. https://doi.org/10.1249/MSS.0b013e3181949333

    Article  PubMed  Google Scholar 

  18. Min KH, Byun JH, Heo CY, Kim EH, Choi HY, Pak CS (2015) Effect of low-level laser therapy on human adipose-derived stem cells: in vitro and in vivo studies. Aesthet Plast Surg 39:778–782. https://doi.org/10.1007/s00266-015-0524-6

    Article  Google Scholar 

  19. Huang YY, Chen AC, Carroll JD, Hamblin MR (2009) Biphasic dose response in low level light therapy. Dose-Response 7:358–383. https://doi.org/10.2203/dose-response.09-027

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yu HS, Chang KL, Yu CL, Chen JW, Chen GS (1996) Low-energy helium-neon laser irradiation stimulates interleukin-1 alpha and interleukin-8 release from cultured human keratinocytes. J Invest Dermatol 107:593–596

    Article  PubMed  CAS  Google Scholar 

  21. Conlan MJ, Rapley JW, Cobb CM (1996) Biostimulation of wound healing by low-energy laser irradiation. A review. J Clin Periodontol 23:492–496

    Article  PubMed  CAS  Google Scholar 

  22. Lo KA, Ng PY, Kabiri Z, Virshup D, Sun L (2016) Wnt inhibition enhances browning of mouse primary white adipocytes. Adipocyte 5:224–231. https://doi.org/10.1080/21623945.2016.1148834

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Jeon M, Rahman N, Kim YS (2016) Wnt/β-catenin signaling plays a distinct role in methyl gallate-mediated inhibition of adipogenesis. Biochem Biophys Res Commun 479:22–27. https://doi.org/10.1016/j.bbrc.2016.08.178

    Article  PubMed  CAS  Google Scholar 

  24. Chung SS, Lee JS, Kim M (2012) Regulation of Wnt/β-catenin signaling by CCAAT/enhancer binding protein β during adipogenesis. Obesity (Silver Spring) 20:482–487. https://doi.org/10.1038/oby.2011.212

    Article  CAS  Google Scholar 

  25. Prestwich TC, Macdougald OA (2007) Wnt/beta-catenin signaling in adipogenesis and metabolism. Curr Opin Cell Biol 19:612–617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM (2000) Transcriptional regulation of adipogenesis. Genes Dev 14:1293–1307

    PubMed  CAS  Google Scholar 

  27. Wu Z, Rosen ED, Brun R et al (1999) Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 3:151–158

    Article  PubMed  CAS  Google Scholar 

  28. He X, Semenov M, Tamai K, Zeng X (2004) LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 131:1663–1677

    Article  PubMed  CAS  Google Scholar 

  29. Kawai M, Mushiake S, Bessho K et al (2007) Wnt/Lrp/beta-catenin signaling suppresses adipogenesis by inhibiting mutual activation of PPARgamma and C/EBPalpha. Biochem Biophys Res Commun 363:276–282

    Article  PubMed  CAS  Google Scholar 

  30. Kimelman D, Xu W (2006) Beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25:7482–7491

    Article  PubMed  CAS  Google Scholar 

  31. Herencia C, Martínez-Moreno JM, Herrera C (2012) Nuclear translocation of β-catenin during mesenchymal stem cells differentiation into hepatocytes is associated with a tumoral phenotype. PLoS One 7:e34656. https://doi.org/10.1371/journal.pone.0034656

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Liu C, Li Y, Semenov M et al (2002) Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837–847

    Article  PubMed  CAS  Google Scholar 

  33. Gruden G, Landi A, Bruno G (2014) Natriuretic peptides, heart, and adipose tissue: new findings and future developments for diabetes research. Diabetes Care 37:2899–2908. https://doi.org/10.2337/dc14-0669

    Article  PubMed  CAS  Google Scholar 

  34. Nishikimi T, Kuwahara K, Nakao K (2011) Current biochemistry, molecular biology, and clinical relevance of natriuretic peptides. J Cardiol 57:131–140. https://doi.org/10.1016/j.jjcc.2011.01.002

    Article  PubMed  Google Scholar 

  35. Potter LR (2011) Natriuretic peptide metabolism, clearance and degradation. FEBS J 278:1808–1817. https://doi.org/10.1111/j.1742-4658.2011.08082.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Sellitti DF, Koles N, Mendonça MC (2011) Regulation of C-type natriuretic peptide expression. Peptides 32:1964–1971. https://doi.org/10.1016/j.peptides.2011.07.013

    Article  PubMed  CAS  Google Scholar 

  37. Chen-Tournoux A, Khan AM, Baggish AL (2010) Effect of weight loss after weight loss surgery on plasma N-terminal pro-B-type natriuretic peptide levels. Am J Cardiol 106:1450–1455. https://doi.org/10.1016/j.amjcard.2010.06.076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Bordicchia M, Liu D, Amri EZ et al (2012) Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest 122:1022–1036. https://doi.org/10.1172/JCI59701

    Article  PubMed  PubMed Central  Google Scholar 

  39. Miyashita K, Itoh H, Tsujimoto H et al (2009) Natriuretic peptides/cGMP/cGMP-dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes 58:2880–2892. https://doi.org/10.2337/db09-0393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Tsukamoto O, Fujita M, Kato M et al (2009) Natriuretic peptides enhance the production of adiponectin in human adipocytes and in patients with chronic heart failure. J Am Coll Cardiol 53(22):2070–2077. https://doi.org/10.1016/j.jacc.2009.02.038

    Article  PubMed  CAS  Google Scholar 

  41. Osborn O, Olefsky JM (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18:363–374. https://doi.org/10.1038/nm.2627

    Article  PubMed  CAS  Google Scholar 

  42. El-Kadre LJ, Tinoco AC (2013) Interleukin-6 and obesity: the crosstalk between intestine, pancreas and liver. Curr Opin Clin Nutr Metab Care 16:564–568. https://doi.org/10.1097/MCO.0b013e32836410e6

    Article  PubMed  CAS  Google Scholar 

  43. Böttcher RT, Niehrs C (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26:63–77

    Article  PubMed  CAS  Google Scholar 

  44. Cuevas-Ramos D, Almeda-Valdes P, Aguilar-Salinas CA, Cuevas-Ramos G, Cuevas-Sosa AA, Gomez-Perez FJ (2009) The role of fibroblast growth factor 21 (FGF21) on energy balance, glucose and lipid metabolism. Curr Diabetes Rev 5:216–220

    Article  PubMed  CAS  Google Scholar 

  45. Inagaki T, Dutchak P, Zhao G et al (2007) Endocrine regulation of the fasting response by PPARα-mediated induction of fibroblast growth factor 21. Cell Metab 5:415–425

    Article  PubMed  CAS  Google Scholar 

  46. Fisher FM, Kleiner S, Douris N et al (2012) FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 26:271–281. https://doi.org/10.1101/gad.177857.111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M, Mampel T, Villarroya F (2011) Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J Biol Chem 286:12983–12990. https://doi.org/10.1074/jbc.M110.215889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Kim KH, Kim SH, Min YK, Yang HM, Lee JB, Lee MS (2013) Acute exercise induces FGF21 expression in mice and in healthy humans. PLoS One 8:e63517. https://doi.org/10.1371/journal.pone.0063517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Roca-Rivada A, Castelao C, Senin LL et al (2013) FNDC5/irisin is not only a myokine but also an adipokine. PLoS One 8:e60563. https://doi.org/10.1371/journal.pone.0060563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Boström P, Wu J, Jedrychowski MP et al (2012) PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–468. https://doi.org/10.1038/nature10777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Cuevas-Ramos D, Almeda-Valdés P, Meza-Arana CE et al (2012) Exercise increases serum fibroblast growth factor 21 (FGF21) levels. PLoS One 7:e38022. https://doi.org/10.1371/journal.pone.0038022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Campos RMS, Masquio DCL, Aquino AE Jr (2016) The role of FGF-21/NPY pathway on weight loss therapy in obese women. In: 13th International Congress on Obesity, 2016, Vancouver. Abstracts of the 13th International Congress on Obesity 1–4 May 2016 Vancouver, Canada, 2016. v. 17. pp 1–213

  53. Tilg H, Moschen AR (2008) Inflammatory mechanisms in the regulation of insulin resistance. Mol Med 14:222–231. https://doi.org/10.2119/2007-00119.Tilg

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Tangvarasittichai S, Pongthaisong S, Tangvarasittichai O (2016) Tumor necrosis factor-Α, Interleukin-6, C-reactive protein levels and insulin resistance associated with type 2 diabetes in abdominal obesity women. Indian J Clin Biochem 31:68–74. https://doi.org/10.1007/s12291-015-0514-0

    Article  PubMed  CAS  Google Scholar 

  55. Moreno-Navarrete JM, Ortega F, Serrano M (2013) Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J Clin Endocrinol Metab 98:E769–E778. https://doi.org/10.1210/jc.2012-2749

    Article  PubMed  CAS  Google Scholar 

  56. Houreld NN (2014) Shedding light on a new treatment for diabetic wound healing: a review on phototherapy. Sci World J 2014:398412. https://doi.org/10.1155/2014/398412

    Article  CAS  Google Scholar 

  57. Masha RT, Houreld NN, Abrahamse H (2013) Low-intensity laser irradiation at 660 nm stimulates transcription of genes involved in the electron transport chain. Photomed Laser Surg 31:47–53. https://doi.org/10.1089/pho.2012.3369

    Article  PubMed  CAS  Google Scholar 

  58. Silveira PC, Silva LA, Fraga DB, Freitas TP, Streck EL, Pinho R (2009) Evaluation of mitochondrial respiratory chain activity in muscle healing by low-level laser therapy. J Photochem Photobiol B 95:89–92. https://doi.org/10.1016/j.jphotobiol.2009.01.004

    Article  PubMed  CAS  Google Scholar 

  59. Aquino AE Jr, Sene-Fiorese M, Castro CA (2015) Can low-level laser therapy when associated to exercise decrease adipocyte area? J Photochem Photobiol B 149:21–26. https://doi.org/10.1016/j.jphotobiol.2015.04.033

    Article  PubMed  CAS  Google Scholar 

  60. Nurković J, Zaletel I, Nurković S et al (2017) Combined effects of electromagnetic field and low-level laser increase proliferation and alter the morphology of human adipose tissue-derived mesenchymal stem cells. Lasers Med Sci 32:151–160. https://doi.org/10.1007/s10103-016-2097-2

    Article  PubMed  Google Scholar 

  61. Karu TI (2008) Mitochondrial signaling in mammalian cells activated by red and near-IR radiation. Photochem Photobiol 84:1091–1099. https://doi.org/10.1111/j.1751-1097.2008.00394.x

    Article  PubMed  CAS  Google Scholar 

  62. Lavi R, Shainberg A, Friedmann H et al (2003) Low energy visible light induces reactive oxygen species generation and stimulates an increase of intracellular calcium concentration in cardiac cells. J Biol Chem 278:40917–40922

    Article  PubMed  CAS  Google Scholar 

  63. Hu WP, Wang JJ, Yu CL, Lan CC, Chen GS, Yu HS (2007) Helium-neon laser irradiation stimulates cell proliferation through photostimulatory effects in mitochondria. J Invest Dermatol 127:2048–2057

    Article  PubMed  CAS  Google Scholar 

  64. AlGhamdi KM, Kumar A, Moussa NA (2012) Low-level laser therapy: a useful technique for enhancing the proliferation of various cultured cells. Lasers Med Sci 27:237–249. https://doi.org/10.1007/s10103-011-0885-2

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the patients that participated of the study.

Funding

We thank the financial support for all research agencies Support Foundation of São Paulo Research—FAPESP (2013/041364; 2013/19046-0; 2013/08522-6; 2015/14309-9) and National Council for Scientific and Technological Development—CNPq (573587/2008-6; 300654/2013-8; 150177/2014-3) and Coordination of Higher Education Personnel Training—CAPES.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Raquel Munhoz da Silveira Campos, Ana Raimunda Dâmaso or Nivaldo Antonio Parizotto.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silveira Campos, R.M., Dâmaso, A.R., Masquio, D.C.L. et al. The effects of exercise training associated with low-level laser therapy on biomarkers of adipose tissue transdifferentiation in obese women. Lasers Med Sci 33, 1245–1254 (2018). https://doi.org/10.1007/s10103-018-2465-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-018-2465-1

Keywords

Navigation