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Photobiomodulation enhances the Th1 immune response of human monocytes

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Abstract

This study aims to evaluate the effects of photobiomodulation (PBM) on human monocytes, assessing the oxidative burst and ultimate fungicidal potential of these cells, as well as the gene expression at the mRNA level of CD68, CD80, CD163, CD204, IL-6, TNF-α and IL-10 in derived macrophages. Primary cultures of human monocytes were irradiated with an InGaAlP (660 nm)/GaAlAs (780 nm) diode laser (parameters: 40 mW, 0.04 cm2, 1 W/cm2; doses: 200, 400 and 600 J/cm2). Cells were submitted to the chemiluminescence assay, and a microbicidal activity assay against Candida albicans was performed. Reactive oxygen species (ROS) and nitric oxide (NO) production were measured, and cell viability was assessed by the exclusion method using 0.2% Trypan blue reagent. Irradiated monocytes were cultured for 72 h towards differentiation into macrophages. Total RNA was extracted, submitted to reverse transcription and real-time PCR. The results were analysed by ANOVA and the Tukey test (α = 0.05). Irradiated monocytes revealed a significant increase in their intracellular and extracellular ROS (P < 0.001). The 660 nm wavelength and 400 J/cm2 dose were the most relevant parameters (P < 0.001). The fungicidal capacity of the monocytes was shown to be greatly increased after PBM (P < 0.001). PBM increased the expression of TNF-α (P = 0.0302) and the production of NO (P < 0.05) and did not impair monocyte viability. PBM induces a pro-inflammatory Th1-driven response in monocytes and macrophages.

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References

  1. Cerdeira CD, Brigagão MRL, Carli ML, Ferreira CS, Moraes GOI, Hadad H, Hanemann JAC, Hamblin MR, Sperandio FF (2016) Low-level laser therapy stimulates the oxidative burst in human neutrophils and increases their fungicidal capacity. J Biophotonics 9:1180–1188. https://doi.org/10.1002/jbio.201600035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Eslamipour F, Motamedian SR, Bagheri F (2017) Ibuprofen and low-level laser therapy for pain control during fixed orthodontic therapy: a systematic review of randomized controlled trials and meta-analysis. J Contemp Dent Pract 18:527–533

    Article  PubMed  Google Scholar 

  3. Heidari M, Paknejad M, Jamali R, Nokhbatolfoghahaei H, Fekrazad R, Moslemi N (2017) Effect of laser photobiomodulation on wound healing and postoperative pain following free gingival graft: a split-mouth triple-blind randomized controlled clinical trial. J Photochem Photobiol B 172:109–114. https://doi.org/10.1016/j.jphotobiol.2017.05.022

    Article  CAS  PubMed  Google Scholar 

  4. Karu T (1989) Photobiology of low-power laser effects. Health Phys 56:691–704

    Article  CAS  PubMed  Google Scholar 

  5. Hamblin MR (2017) Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys 4:337–361. https://doi.org/10.3934/biophy.2017.3.337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Burger E, Mendes AC, Bani GM, Brigagão MR, Santos GB, Malaquias LC, Chavasco JK, Verinaud LM, de Camargo ZP, Hamblin MR, Sperandio FF (2015) Low-level laser therapy to the mouse femur enhances the fungicidal response of neutrophils against Paracoccidioides brasiliensis. PLoS Negl Trop Dis 9:e0003541. https://doi.org/10.1371/journal.pntd.0003541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Hemvani N, Chitnis DS, Bhagwanani NS (2005) Helium-neon and nitrogen laser irradiation accelerates the phagocytic activity of human monocytes. Photomed Laser Surg 23:571–574. https://doi.org/10.1089/pho.2005.23.571

    Article  PubMed  Google Scholar 

  8. Nathan CF, Root RK (1977) Hydrogen peroxide release from mouse peritoneal macrophages: dependence on sequential activation and triggering. J Exp Med 146:1648–1662

    Article  CAS  PubMed  Google Scholar 

  9. Dale DC, Boxer L, Liles WC (2008) The phagocytes: neutrophils and monocytes. Blood 112:935–945. https://doi.org/10.1182/blood-2007

    Article  CAS  PubMed  Google Scholar 

  10. Rada B, Leto TL (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15:164–187. https://doi.org/10.1159/000136357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kalyanaraman B, Hardy M, Zielonka J (2016) A critical review of methodologies to detect reactive oxygen and nitrogen species stimulated by NADPH oxidase enzymes: implications in pesticide toxicity. Curr Pharmacol Rep 2:193–201. https://doi.org/10.1007/s40495-016-0063-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Liu H, Colavitti R, Rovira II, Finkel T (2005) Redox-dependent transcriptional regulation. Circ Res 97:967–974. https://doi.org/10.1161/01.RES.0000188210.72062.10

    Article  CAS  PubMed  Google Scholar 

  13. Callaghan GA, Riordan C, Gilmore WS, McIntyre IA, Allen JM, Hannigan BM (1996) Reactive oxygen species inducible by low-intensity laser irradiation alter DNA synthesis in the haemopoietic cell line U937. Lasers Surg Med 19:201–206. https://doi.org/10.1002/(SICI)1096-9101(1996)19:2<201::AID-LSM12>3.0.CO;2-9

    Article  CAS  PubMed  Google Scholar 

  14. Lindgård A, Hultén LM, Svensson L, Soussi B (2007) Irradiation at 634 nm releases nitric oxide from human monocytes. Lasers Med Sci 22:30–36. https://doi.org/10.1007/s10103-006-0419-5

    Article  PubMed  Google Scholar 

  15. Silva IH, de Andrade SC, de Faria AB, Fonsêca DD, Gueiros LA, Carvalho AA, da Silva WT, de Castro RM, Leão JC (2016) Increase in the nitric oxide release without changes in cell viability of macrophages after laser therapy with 660 and 808 nm lasers. Lasers Med Sci 31:1855–1862. https://doi.org/10.1007/s10103-016-2061-1

    Article  PubMed  Google Scholar 

  16. Chen CH, Wang CZ, Wang YH, Liao WT, Chen YJ, Kuo CH, Kuo HF, Hung CH (2014) Effects of low-level laser therapy on M1-related cytokine expression in monocytes via histone modification. Mediat Inflamm 2014:625048. https://doi.org/10.1155/2014/625048

    Article  CAS  Google Scholar 

  17. de Brito Sousa K, Rodrigues MFSD, de Souza Santos D, Mesquita-Ferrari RA, Nunes FD, da Silva DFTDifferential expression of inflammatory and anti-inflammatory mediators by M1 and M2 macrophages after photobiomodulation with red or infrared lasers, Bussadori SK, Fernandes KPS (2019) . Lasers Med Sci https://doi.org/10.1007/s10103-019-02817-1

  18. Yin M, Shen J, Yu S, Fei J, Zhu X, Zhao J, Zhai L, Sadhukhan A, Zhou J (2019) Tumor-associated macrophages (TAMs): a critical activator in ovarian cancer metastasis. Onco Targets Ther 12:8687–8699. https://doi.org/10.2147/OTT.S216355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tarique AA, Logan J, Thomas E, Holt PG, Sly PD, Fantino E (2015) Phenotypic, functional, and plasticity features of classical and alternatively activated human macrophages. Am J Respir Cell Mol Biol 53:676–688. https://doi.org/10.1165/rcmb.2015-0012OC

    Article  CAS  PubMed  Google Scholar 

  20. Yaniv E, Hadar T, Shvero J, Tamir R, Nageris B (2009) KTP/532 YAG laser treatment for allergic rhinitis. Am J Rhinol Allergy 23:527–530. https://doi.org/10.2500/ajra.2009.23.3346

    Article  PubMed  Google Scholar 

  21. Fairweathera D, Cihakovab D (2009) Alternatively activated macrophages in infection and autoimmunity. J Autoimmun 33:222–230. https://doi.org/10.1016/j.jaut.2009.09.012

    Article  CAS  Google Scholar 

  22. Hultén LM, Holmström M, Soussi B (1999) Harmful singlet oxygen can be helpful. Free Radic Biol Med 27:1203–1207

    Article  PubMed  Google Scholar 

  23. Babior BM (1984) The respiratory burst of phagocytes. J Clin Invest 73:599–601. https://doi.org/10.1172/JCI111249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dahlgren C, Karlsson A, Bylund J (2007) Measurement of respiratory burst products generated by professional phagocytes. Methods Mol Biol 412:349–363. https://doi.org/10.1007/978-1-59745-467-4_23

    Article  CAS  PubMed  Google Scholar 

  25. Silva DF, Mesquita-Ferrari RA, Fernandes KP, Raele MP, Wetter NU, Deana AM (2012) Effective transmission of light for media culture, plates and tubes. Photochem Photobiol 88:1211–1216. https://doi.org/10.1111/j.1751-1097.2012.01166.x

    Article  CAS  PubMed  Google Scholar 

  26. Green JN, Winterbourn CC, Hampton MB (2007) Analysis of neutrophil bactericidal activity. Methods Mol Biol 412:319–332. https://doi.org/10.1007/978-1-62703-845-4_19

    Article  CAS  PubMed  Google Scholar 

  27. Raggi F, Pelassa S, Pierobon D, Penco F, Gattorno M, Novelli F, Eva A, Varesio L, Giovarelli M, Bosco MC (2017) Regulation of human macrophage M1-M2 polarization balance by hypoxia and the triggering receptor expressed on myeloid cells-1. Front Immunol 8:1097. https://doi.org/10.3389/fimmu.2017.01097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Jaguin M, Houlbert N, Fardel O, Lecureur V (2013) Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol 281:51–61. https://doi.org/10.1016/j.cellimm.2013.01.010

    Article  CAS  PubMed  Google Scholar 

  29. Meirelles MN, Araujo TCJ, Souza W (1980) Interaction of epimastigote and trypomastigote forms of Trypanosoma cruzi with chicken macrophages in vitro. Parasitology 81:373–381

    Article  PubMed  Google Scholar 

  30. Ding J, Jin W, Chen C, Shao Z, Wu J (2012) Tumor associated macrophage × cancer cell hybrids may acquire cancer stem cell properties in breast cancer. PLoS One 7:e41942. https://doi.org/10.1371/journal.pone.0041942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Article  PubMed  PubMed Central  Google Scholar 

  32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Method Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  33. R Core Team (2016) R Foundation for Statistical Computing

  34. Ferreira EB, Cavalcanti PP, Nogueira DA (2013) R package version:1.1.2

  35. Pal G, Dutta A, Mitra K, Grace MS, Romanczyk TB, Wu X, Chakrabarti K, Anders J, Gorman E, Waynant RW, Tata DB (2007) Effect of low intensity laser interaction with human skin fibroblast cells using fiber-optic nano-probes. J Photochem Photobiol B 86:252–261. https://doi.org/10.1016/j.jphotobiol.2006.12.001

    Article  CAS  PubMed  Google Scholar 

  36. 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.Hamblin

    Article  PubMed  PubMed Central  Google Scholar 

  37. Huang YY, Sharma SK, Carroll J, Hamblin MR (2011) Biphasic dose response in low level light therapy - an update. Dose-Response 9:602–618. https://doi.org/10.2203/dose-response.11-009.Hamblin

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ellis JA, Mayer SJ, Jones OT (1988) The effect of the NADPH oxidase inhibitor diphenyleneiodonium on aerobic and anaerobic microbicidal activities of human neutrophils. Biochem J 251:887–891. https://doi.org/10.1042/bj2510887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tucureanu MM, Rebleanu D, Constantinescu CA, Deleanu M, Voicu G, Butoi E, Calin M, Manduteanu I (2017) Lipopolysaccharide-induced inflammation in monocytes/macrophages is blocked by liposomal delivery of Gi-protein inhibitor. Int J Nanomedicine 13:63–76. https://doi.org/10.2147/IJN.S150918

    Article  PubMed  PubMed Central  Google Scholar 

  40. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511. https://doi.org/10.1038/nri1391

    Article  CAS  PubMed  Google Scholar 

  41. Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700. https://doi.org/10.1146/annurev.biochem.71.110601.135414

    Article  CAS  PubMed  Google Scholar 

  42. Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, Hauschildt S (2011) LPS-induced cytokine production in human monocytes and macrophages. Crit Rev Immunol 31:379–446

    Article  CAS  PubMed  Google Scholar 

  43. Netea MG, Sutmuller R, Hermann C, Van der Graaf CA, Van der Meer JW, van Krieken JH, Hartung T, Adema G, Kullberg BJ (2004) Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 172:3712–3718

    Article  CAS  PubMed  Google Scholar 

  44. Netea MG, Van der Graaf C, Van der Meer JW, Kullberg BJ (2004) Recognition of fungal pathogens by toll-like receptors. Eur J Clin Microbiol Infect Dis 23:672–676. https://doi.org/10.1007/s10096-004-1192-7

    Article  CAS  PubMed  Google Scholar 

  45. Farah CS, Saunus JM, Hu Y, Kazoullis A, Ashman RB (2009) Gene targeting demonstrates that inducible nitric oxide synthase is not essential for resistance to oral candidiasis in mice, or for killing of Candida albicans by macrophages in vitro. Oral Microbiol Immunol 24:83–88. https://doi.org/10.1111/j.1399-302X.2008.00462.x

    Article  CAS  PubMed  Google Scholar 

  46. Avci P, Gupta A, Sadasivam M, Vecchio D, Pam Z, Pam N, Hamblin MR (2013) Low-level laser (light) therapy (LLLT) in skin: stimulating, healing, restoring. Semin Cutan Med Surg 32:41–52

    PubMed  PubMed Central  Google Scholar 

  47. Sperandio FF, Simoes A, Aranha AC, Correa L, Orsini Machado de Sousa SC (2010) Photodynamic therapy mediated by methylene blue dye in wound healing. Photomed Laser Surg 28:581–587. https://doi.org/10.1089/pho.2009.2601

    Article  CAS  PubMed  Google Scholar 

  48. Sperandio FF, Simoes A, Correa L, Aranha AC, Giudice FS, Hamblin MR, Sousa SC (2015) Low-level laser irradiation promotes the proliferation and maturation of keratinocytes during epithelial wound repair. J Biophotonics 8:795–803. https://doi.org/10.1002/jbio.201400064

    Article  CAS  PubMed  Google Scholar 

  49. Viegas VN, Abreu ME, Viezzer C, Machado DC, Filho MS, Silva DN, Pagnoncelli RM (2007) Effect of low-level laser therapy on inflammatory reactions during wound healing: comparison with meloxicam. Photomed Laser Surg 25:467–473. https://doi.org/10.1089/pho.2007.1098

    Article  CAS  PubMed  Google Scholar 

  50. Woodruff LD, Bounkeo JM, Brannon WM, Dawes KS, Barham CD, Waddell DL, Enwemeka CS (2004) The efficacy of laser therapy in wound repair: a meta-analysis of the literature. Photomed Laser Surg 22:241–247. https://doi.org/10.1089/1549541041438623

    Article  PubMed  Google Scholar 

  51. Moriyama Y, Nguyen J, Akens M, Moriyama EH, Lilge L (2009) In vivo effects of low level laser therapy on inducible nitric oxide synthase. Lasers Surg Med 41:227–231. https://doi.org/10.1002/lsm.20745

    Article  PubMed  Google Scholar 

  52. Labonte AC, Tosello-Trampont AC, Hahn YS (2014) The role of macrophage polarization in infectious and inflammatory diseases. Mol Cell 37:275–285. https://doi.org/10.14348/molcells.2014.2374

    Article  CAS  Google Scholar 

  53. Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787–795. https://doi.org/10.1172/JCI59643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–686. https://doi.org/10.1016/j.it.2004.09.015

    Article  CAS  PubMed  Google Scholar 

  55. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27:451–483. https://doi.org/10.1146/annurev.immunol.021908.132532

    Article  CAS  PubMed  Google Scholar 

  56. Colvin EK (2014) Tumor-associated macrophages contribute to tumor progression in ovarian cancer. Front Oncol 4:137. https://doi.org/10.3389/fonc.2014.00137

    Article  PubMed  PubMed Central  Google Scholar 

  57. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23:549–555. https://doi.org/10.1016/s1471-4906(02)02302-5

    Article  CAS  PubMed  Google Scholar 

  58. Homan JW, Steele AD, Martinand-Mari C, Rogers TJ, Henderson EE, Charubala R, Pfleiderer W, Reichenbach NL, Suhadolnik RJ (2002) Inhibition of morphine-potentiated HIV-1 replication in peripheral blood mononuclear cells with the nuclease-resistant 2-5A agonist analog, 2-5A(N6B). J Acquir Immune Defic Syndr 30:9–20. https://doi.org/10.1097/00042560-200205010-00002

    Article  CAS  PubMed  Google Scholar 

  59. Lagging M, Romero AI, Westin J, Norkrans G, Dhillon AP, Pawlotsky JM, Zeuzem S, von Wagner M, Negro F, Schalm SW, Haagmans BL, Ferrari C, Missale G, Neumann AU, Verheij-Hart E, Hellstrand K (2006) IP-10 predicts viral response and therapeutic outcome in difficult-to-treat patients with HCV genotype 1 infection. Hepatology 44:1617–1625. https://doi.org/10.1002/hep.21407

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors wish to thank Dr. Janete M. Cerutti for some reagents provided for the molecular study.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Master’s Scholarship).

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Correspondence to Mayara Santos de Castro.

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The present study was approved by the Human Research Ethics Committee of the University Federal of Alfenas, Brazil (Protocol # 1980248).

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Fig. S1

The process of differentiating monocytes into macrophages was followed for 72 h, observing the change in the morphological aspect of the cells. Monocytes (arrow) have a rounded morphology, whilst macrophages (star) cease to be rounded cells and become elongated, spindle shaped and often stellar. Image obtained by inverted microscopy in phase contrast (× 400). (PNG 772 kb)

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de Castro, M.S., Miyazawa, M., Nogueira, E.S.C. et al. Photobiomodulation enhances the Th1 immune response of human monocytes. Lasers Med Sci 37, 135–148 (2022). https://doi.org/10.1007/s10103-020-03179-9

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