Low-intensity red and infrared lasers affect mRNA expression of DNA nucleotide excision repair in skin and muscle tissue

Abstract

Lasers emit light beams with specific characteristics, in which wavelength, frequency, power, fluence, and emission mode properties determine the photophysical, photochemical, and photobiological responses. Low-intensity lasers could induce free radical generation in biological tissues and cause alterations in macromolecules, such as DNA. Thus, the aim of this work was to evaluate excision repair cross-complementing group 1 (ERCC1) and excision repair cross-complementing group 2 (ERCC2) messenger RNA (mRNA) expression in biological tissues exposed to low-intensity lasers. Wistar rat (n = 28, 4 for each group) skin and muscle were exposed to low-intensity red (660 nm) and near-infrared (880 nm) lasers at different fluences (25, 50, and 100 J/cm2), and samples of these tissues were withdrawn for RNA extraction, cDNA synthesis, and gene expression evaluation by quantitative polymerase chain reaction. Laser exposure was in continuous wave and power of 100 mW. Data show that ERCC1 and ERCC2 mRNA expressions decrease in skin (p < 0.001) exposed to near-infrared laser, but increase in muscle tissue (p < 0.001). ERCC1 mRNA expression does not alter (p > 0.05), but ERCC2 mRNA expression decreases in skin (p < 0.001) and increases in muscle tissue (p < 0.001) exposed to red laser. Our results show that ERCC1 and ERCC2 mRNA expression is differently altered in skin and muscle tissue exposed to low-intensity lasers depending on wavelengths and fluences used in therapeutic protocols.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Svelto O, Hanna DC (1998) Principles of laser. Plenum Press, New York

    Book  Google Scholar 

  2. 2.

    O’Shea DC, Callen WR, Rhodes WT (1978) Introduction to lasers and their applications, edition 1. Addison-Wesley Publishing Company, Menlo Park, California

    Google Scholar 

  3. 3.

    Karu T (2003) Low power laser therapy. In: Biomedical Photonics Handbook. Vo-Dinh (ed.). CRC Press, Boca Raton: USA

  4. 4.

    Beckmann KH, Meyer-Hamme G, Schröder S (2014) Low level laser therapy for treatment of diabetic foot ulcers: a critical survey. Evid Base Complement Alternat Med 2014:626127. doi:10.1155/2014/626127

    Google Scholar 

  5. 5.

    Peplow PV, Chung TY, Baxter GD (2010) Laser photobiomodulation of wound healing: a review of experimental studies in mouse and rat animal models. Photomed Laser Surg 28:291–325. doi:10.1089/pho.2008.2446

    Article  PubMed  Google Scholar 

  6. 6.

    Doğan GE, Demir T, Orbak R (2014) Effect of low-level laser on guided tissue regeneration performed with equine bone and membrane in the treatment of intrabony defects: a clinical study. Photomed Laser Surg 32:226–231. doi:10.1089/pho.2013.3664

    Article  PubMed  Google Scholar 

  7. 7.

    Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49:1–17. doi:10.1016/S1011-1344(98)00219-X

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Migliario M, Pittarella P, Fanuli M, Rizzi M, Renò F (2014) Laser-induced osteoblast proliferation is mediated by ROS production. Lasers Med Sci 29:1463–1467. doi:10.1007/s10103-014-1556-x

    Article  PubMed  Google Scholar 

  9. 9.

    Barzilai A, Yamamoto K (2004) DNA damage responses to oxidative stress. DNA Repair (Amst) 3:1109–1115. doi:10.1016/j.dnarep.2004.03.002

    CAS  Article  Google Scholar 

  10. 10.

    Marnett LJ (2000) Oxyradicals and DNA damage. Carcinogenesis 21:361–370. doi:10.1093/carcin/21.3.361

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Kim YG (2002) Laser mediated production of reactive oxygen and nitrogen species; implications for therapy. Free Radic Res 36:1243–1250. doi:10.1080/1071576021000028389

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Slupphaug G, Kavli B, Kroka HE (2003) The interacting pathways for prevention and repair of oxidative DNA damage. Mutat Res 531:231–251. doi:10.1016/j.mrfmmm.2003.06.002

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Fonseca AS, Teixeira AF, Presta GA, Geller M, Valença SS, Paoli F (2012) Low intensity infrared laser effects on Escherichia coli cultures and plasmid DNA. Laser Phys 22:1635–1641. doi:10.1134/S1054660X12100076

    CAS  Article  Google Scholar 

  14. 14.

    Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberg T (2006) DNA repair and mutagenesis. ASM Press, Washington

    Google Scholar 

  15. 15.

    Klungland A, Bjelland S (2007) Oxidative damage to purines in DNA: role of mammalian Ogg1. DNA Repair (Amst) 6:481–488. doi:10.1016/j.dnarep.2006.10.012

    CAS  Article  Google Scholar 

  16. 16.

    Patrono C, Sterpone S, Testa A, Cozzi R (2014) Polymorphisms in base excision repair genes: breast cancer risk and individual radiosensitivity. World J Clin Oncol 5:874–882. doi:10.5306/wjco.v5.i5.874

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Mitra S, Hazra TK, Roy R, Ikeda S, Biswas T, Lock J, Boldogh I, Izumi T (1997) Complexities of DNA base excision repair in mammalian cells. Mol Cells 7:305–312

    CAS  PubMed  Google Scholar 

  18. 18.

    Trajano ET, Mencalha AL, Monte-Alto-Costa A, Pôrto LC, de Souza da Fonseca A (2014) Expression of DNA repair genes in burned skin exposed to low-level red laser. Lasers Med Sci 29:1953–1957. doi:10.1007/s10103-014-1612-6

    Article  PubMed  Google Scholar 

  19. 19.

    Fonseca AS, Mencalha AL, Campos VMA, Ferreira-Machado SC, Peregrino AAF, Magalhães LAG, Geller M, Paoli F (2013) Low-intensity infrared lasers alter actin gene expression in skin and muscle tissue. Laser Phys 23:025602. doi:10.1088/1054-660X/23/2/025602

    Article  Google Scholar 

  20. 20.

    Fonseca AS, Magalhães LAG, Mencalha AL, Geller M, Paoli F (2014) Low intensity infrared laser affects expression of oxidative DNA repair genes in mitochondria and nucleus. Laser Phys 24:115605. doi:10.1088/1054-660X/24/11/115605

    Article  Google Scholar 

  21. 21.

    Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JHJ (2014) Understanding nucleotide excision repair and its role in cancer and ageing. Nat Rev Mol Cell Biol 15:465–481. doi:10.1038/nrm3822

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Mellon I, Bohr VA, Smith CA, Hanawalt PC (1986) Preferential DNA repair of an active gene in human cells. Proc Natl Acad Sci U S A 83:8878–8882

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Costa RM, Chiganças V, Galhardo RDAS, Carvalho H, Menck CF (2003) The eukaryotic nucleotide excision repair pathway. Biochimie 85:1083–1099. doi:10.1016/j.biochi.2003.10.017

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Maillard O, Solyom S, Naegeli H (2007) An aromatic sensor with aversion to damaged strands confers versatility to DNA repair. PLoS Biol 5, e79. doi:10.1371/journal.pbio.0050079

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Shuck SC, Short EA, Turchi JJ (2008) Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 18:64–72. doi:10.1038/cr.2008.2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Bernard-Gallon D, Bosviel R, Delort L, Fontana L, Chamoux A, Rabiau N, Kwiatkowski F, Chalabi N, Satih S, Bignon YJ (2008) DNA repair gene ERCC2 polymorphisms and associations with breast and ovarian cancer risk. Mol Cancer 7:36. doi:10.1186/1476-4598-7-36

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Friedberg EC (2001) How nucleotide excision repair protects against cancer. Nat Rev Cancer 1:22–33. doi:10.1038/35094000

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Bowden NA (2014) Nucleotide excision repair: why is it not used to predict response to platinum-based chemotherapy? Cancer Lett 346:163–171. doi:10.1016/j.canlet.2014.01.005

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Mitchel JR, Hoeijmakers JH, Niedernhofer LJ (2003) Divide and conquer: nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol 15:232–240. doi:10.1016/j.canlet.2014.01.005

    Article  Google Scholar 

  30. 30.

    Sancar A, Reardon JT (2004) Nucleotide excision repair in E. coli and man. Adv Protein Chem 69:43–71. doi:10.1016/S0300-9084(99)80034-0

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Fousteri M, Mullenders LHF (2008) Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18:73–84. doi:10.1038/cr.2008.6

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Petruseva IO, Evdokimov AN, Lavrik OI (2014) Molecular mechanism of global genome nucleotide excision repair. Acta Nat 6:23–34

    CAS  Google Scholar 

  33. 33.

    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25:402–408. doi:10.1006/meth.2001.1262

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Postollec F, Falentin H, Pavan S, Combrisson J, Sohier D (2011) Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol 28:848–861. doi:10.1016/j.fm.2011.02.008

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Lobert S, Hiser L, Correia JJ (2010) Expression profiling of tubulin isotypes and microtubule-interacting proteins using real-time polymerase chain reaction. Methods Cell Biol 95:547–558. doi:10.1016/S0091-679X(10)95004-8

    Google Scholar 

  36. 36.

    Barber RD, Harmer DW, Coleman RA, Clark BJ (2005) GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol Genomics 21:389–395. doi:10.1152/physiolgenomics.00025.2005

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    da Silva Marciano R, da Silva Sergio LP, Polignano GA, Presta GA, Guimarães OR, Geller M, de Paoli S, de Paoli F, da Fonseca Ade S (2012) Laser for treatment of aphthous ulcers on bacteria cultures and DNA. Photochem Photobiol Sci 11:1476–1483. doi:10.1039/c2pp25027f

    Article  PubMed  Google Scholar 

  38. 38.

    Sergio LP, Marciano Rda S, Teixeira GR, Canuto Kda S, Polignano GA, Guimarães OR, Geller M, de Paoli F, da Fonseca Ade S (2013) Therapeutic low-intensity red laser for herpes labialis on plasmid survival and bacterial transformation. Photochem Photobiol Sci 12:930–935. doi:10.1039/c3pp25394e

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Fonseca AS, Mencalha AL, Campos VMA, Machado SCF, Peregrino AAF, Geller M, Paoli F (2013) DNA repair gene expression on biological tissues exposed to low-intensity infrared laser. Laser Med Sci 28:1077–1084. doi:10.1007/s10103-012-1191-3

    Article  Google Scholar 

  40. 40.

    Martignago CC, Oliveira RF, Pires-Oliveira DA, Oliveira PD, Pacheco Soares C, Monzani PS, Poli-Frederico RC (2014) Effect of low-level laser therapy on the gene expression of collagen and vascular endothelial growth factor in a culture of fibroblast cells in mice. Lasers Med Sci 30:203–208. doi:10.1007/s10103-014-1644-y

    Article  PubMed  Google Scholar 

  41. 41.

    Rodrigues NC, Brunelli R, de Araújo HS, Parizotto NA, Renno AC (2013) Low-level laser therapy (LLLT) (660nm) alters gene expression during muscle healing in rats. J Photochem Photobiol B 120:29–35. doi:10.1016/j.jphotobiol.2013.01.002

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Rodrigues NC, Brunelli R, Abreu DC, Fernandes K, Parizotto NA, Renno ACM (2014) Morphological aspects and Cox-2 expression after exposure to 780-nm laser therapy in injured skeletal muscle: an in vivo study. Braz J Phys Ther 18:395–401. doi:10.1590/bjpt-rbf.2014.0057

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Fonseca AS, Magalhães LAG, Mencalha AL, Ferreira-Machado SC, Geller M, Paoli F (2014) Low-intensity red and infrared lasers on XPA and XPC gene expression. Laser Phys Lett 11:095601. doi:10.1088/1612-2011/11/9/095601

    Article  Google Scholar 

  44. 44.

    Almeida-Lopes L, Rigau J, Zângaro RA, Guidugli-Neto J, Jaeger MM (2001) Comparison of the low level laser therapy effects on cultured human gingival fibroblasts proliferation using different irradiance and same fluence. Lasers Surg Med 29:179–184. doi:10.1002/lsm.1107

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Niemz MH (2007) Laser-tissue interactions: fundamentals and applications. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

This work was supported by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Conselho Nacional de Pesquisa (CNPq).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Adenilson S. Fonseca.

Ethics declarations

Experiments were conducted in accordance with the Institutional Committee of Animal Care (Comissão de Ética para o Cuidado e Uso de Animais Experimentais, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro), protocol CEUA/038/2012.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sergio, L.P.S., Campos, V.M.A., Vicentini, S.C. et al. Low-intensity red and infrared lasers affect mRNA expression of DNA nucleotide excision repair in skin and muscle tissue. Lasers Med Sci 31, 429–435 (2016). https://doi.org/10.1007/s10103-016-1870-6

Download citation

Keywords

  • Biostimulation
  • DNA repair
  • Oxidative lesion
  • Wistar rats