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Photobiomodulation therapy protects skeletal muscle and improves muscular function of mdx mice in a dose-dependent manner through modulation of dystrophin

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Abstract

This study aimed to analyze the protective effects of photobiomodulation therapy (PBMT) with combination of low-level laser therapy (LLLT) and light emitting diode therapy (LEDT) on skeletal muscle tissue to delay dystrophy progression in mdx mice (DMDmdx). To this aim, mice were randomly divided into five different experimental groups: wild type (WT), placebo-control (DMDmdx), PBMT with doses of 1 J (DMDmdx), 3 J (DMDmdx), and 10 J (DMDmdx). PBMT was performed employing a cluster probe with 9 diodes (1 x 905nm super-pulsed laser diode; 4 x 875nm infrared LEDs; and 4 x 640nm red LEDs, manufactured by Multi Radiance Medical®, Solon - OH, USA), 3 times a week for 14 weeks. PBMT was applied on a single point (tibialis anterior muscle—bilaterally). We analyzed functional performance, muscle morphology, and gene and protein expression of dystrophin. PBMT with a 10 J dose significantly improved (p < 0.001) functional performance compared to all other experimental groups. Muscle morphology was improved by all PBMT doses, with better outcomes with the 3 and 10 J doses. Gene expression of dystrophin was significantly increased with 3 J (p < 0.01) and 10 J (p < 0.01) doses when compared to placebo-control group. Regarding protein expression of dystrophin, 3 J (p < 0.001) and 10 J (p < 0.05) doses also significantly showed increase compared to placebo-control group. We conclude that PBMT can mainly preserve muscle morphology and improve muscular function of mdx mice through modulation of gene and protein expression of dystrophin. Furthermore, since PBMT is a non-pharmacological treatment which does not present side effects and is easy to handle, it can be seen as a promising tool for treating Duchenne’s muscular dystrophy.

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Acknowledgements

This study received support from São Paulo Research Foundation (FAPESP) for Professor Ernesto Cesar Pinto Leal-Junior (grant number 2010/52404-0) and a PhD scholarship for Gianna Móes Albuquerque-Pontes (grant number 2014/05203-0).

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Authors and Affiliations

  1. Laboratory of Phototherapy in Sports and Exercise, Universidade Nove de Julho (UNINOVE), São Paulo, Brazil

    Gianna Móes Albuquerque-Pontes, Heliodora Leão Casalechi, Cheila de Sousa Bacelar Ferreira, Adriane Aver Vanin, Kadma Karênina Damasceno Soares Monteiro & Ernesto Cesar Pinto Leal-Junior

  2. Postgraduate Program in Biophotonics Applied to Health Sciences, Universidade Nove de Julho (UNINOVE), São Paulo, Brazil

    Gianna Móes Albuquerque-Pontes, Andrey Jorge Serra, Rodrigo Labat Marcos & Paulo de Tarso Camillo de Carvalho

  3. Postgraduate Program in Rehabilitation Sciences, Universidade Nove de Julho (UNINOVE), São Paulo, Brazil

    Heliodora Leão Casalechi, Adriane Aver Vanin, Kadma Karênina Damasceno Soares Monteiro, Paulo de Tarso Camillo de Carvalho & Ernesto Cesar Pinto Leal-Junior

  4. Masters and Doctoral Programs in Physical Therapy, Universidade Cidade de São Paulo, São Paulo, Brazil

    Shaiane Silva Tomazoni

  5. Postgraduate Program in Medicine, Universidade Nove de Julho (UNINOVE), São Paulo, Brazil

    Rodrigo Barbosa de Oliveira Brito & Humberto Dellê

  6. Postgraduate Program in Medicine, Universidade Federal de São Paulo (UNIFESP), São Paulo, Brazil

    Brunno Lemes de Melo

  7. Biological Sciences and Health Center, Cruzeiro do Sul University, São Paulo, Brazil

    Lucio Frigo

Authors
  1. Gianna Móes Albuquerque-Pontes
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  2. Heliodora Leão Casalechi
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  3. Shaiane Silva Tomazoni
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  4. Andrey Jorge Serra
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  8. Adriane Aver Vanin
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  9. Kadma Karênina Damasceno Soares Monteiro
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  11. Lucio Frigo
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  12. Rodrigo Labat Marcos
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  13. Paulo de Tarso Camillo de Carvalho
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  14. Ernesto Cesar Pinto Leal-Junior
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Corresponding author

Correspondence to Ernesto Cesar Pinto Leal-Junior.

Ethics declarations

All experimental procedures were performed in accordance with the standards of the Brazilian College of Animal Experimentation (COBEA). All experimental protocols were submitted and approved by the Animal Experimentation Ethics Committee of our institution.

The study was conducted in accordance with policies and procedures of Brazilian laws and the Department of Health and Human Services in the USA.

Conflict of interests

Professor Ernesto Cesar Pinto Leal-Junior receives research support from Multi Radiance Medical (Solon, OH, USA), a PBMT device manufacturer. The remaining authors declare that they have no conflict of interests.

Ethical aspects

All experimental protocols were submitted and approved by the Animal Experimentation Ethics Committee of the University of Nove de Julho (UNINOVE) (Protocol AN0008.2014).

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Albuquerque-Pontes, G.M., Casalechi, H.L., Tomazoni, S.S. et al. Photobiomodulation therapy protects skeletal muscle and improves muscular function of mdx mice in a dose-dependent manner through modulation of dystrophin. Lasers Med Sci 33, 755–764 (2018). https://doi.org/10.1007/s10103-017-2405-5

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  • DOI: https://doi.org/10.1007/s10103-017-2405-5

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