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Published in: Lasers in Medical Science 2/2020

01-03-2020 | Cytokines | Original Article

Differential expression of inflammatory and anti-inflammatory mediators by M1 and M2 macrophages after photobiomodulation with red or infrared lasers

Authors: Kaline de Brito Sousa, Maria Fernanda Setúbal Destro Rodrigues, Debora de Souza Santos, Raquel Agnelli Mesquita-Ferrari, Fabio Daumas Nunes, Daniela de Fátima Teixeira da Silva, Sandra Kalil Bussadori, Kristianne Porta Santos Fernandes

Published in: Lasers in Medical Science | Issue 2/2020

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Abstract

In response to stimuli in the microenvironment, macrophages adopt either the M1 or M2 phenotype to coordinate the tissue repair process. Photobiomodulation (PBM) plays an important role in the modulation of acute inflammation, including cellular influx, macrophage polarization, and the release of inflammatory mediators. The aim of the present study was to evaluate the effects of red and infrared PBM on the mRNA expression of cytokines and chemokines in macrophages polarized to the M1 and M2 phenotypes. J774 macrophages activated to induce M1 (lipopolysaccharide + interferon gamma) or M2 (interleukin-4) phenotypes were irradiated with red or infrared PBM (1 J). After 4 and 24 h, gene expression was analyzed by qPCR. PBM at 660 nm decreased the mRNA expression of CCL3, CXCL2, and TNF-α in M1 macrophages and CXCL2 in M2 macrophages 4 h after irradiation. Similarly, PBM at 780 nm decreased mRNA expression levels of CCL3 and IL-6 by M1 macrophages 24 h after irradiation. Moreover, PBM at 780 nm increased the mRNA expression of TGFβ1 4 h after irradiation and decreased the expression of this gene after 24 h in M2 macrophages. Although red and infrared PBM were able to modulate and reduce M1/M2a-related markers, infrared laser irradiation promoted a temporal increase in the expression of TGFβ1 in M2 macrophages. Thus, depending on the time PBM is used on injured tissue, different parameters can promote optimal results by modulating specific macrophage phenotypes.
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Literature
2.
go back to reference Mehrsai A, Afsharpad M, Afsharpad M, Mohydin M, Ansari B, Pourmand G, Nikbin B (2009) The effect of low-level helium-neon (HeNe) laser radiation on the secretion of cytokines that promote chronic graft rejection – an in vitro study. Med Laser Appl 24:194–200CrossRef Mehrsai A, Afsharpad M, Afsharpad M, Mohydin M, Ansari B, Pourmand G, Nikbin B (2009) The effect of low-level helium-neon (HeNe) laser radiation on the secretion of cytokines that promote chronic graft rejection – an in vitro study. Med Laser Appl 24:194–200CrossRef
3.
go back to reference Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000 Prime Rep 6:13CrossRef Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000 Prime Rep 6:13CrossRef
4.
go back to reference 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 25:677–686CrossRef 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 25:677–686CrossRef
5.
go back to reference 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 281:51–61CrossRef 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 281:51–61CrossRef
6.
go back to reference Xuan W, Qu Q, Zheng B, Xiong S, Fan G (2015) The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J Leukoc Biol 97:61–69CrossRef Xuan W, Qu Q, Zheng B, Xiong S, Fan G (2015) The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J Leukoc Biol 97:61–69CrossRef
7.
go back to reference Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M (2013) Macrophage plasticity and polarization in tissue repair and remodeling. J Pathol 229:176–185CrossRef Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M (2013) Macrophage plasticity and polarization in tissue repair and remodeling. J Pathol 229:176–185CrossRef
8.
go back to reference Novak ML, Koh TJ (2013) Macrophage phenotypes during tissue repair. J Leukoc Biol 93:875–881CrossRef Novak ML, Koh TJ (2013) Macrophage phenotypes during tissue repair. J Leukoc Biol 93:875–881CrossRef
9.
go back to reference Duque AG, Descoteaux A (2014) Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol 5:491 Duque AG, Descoteaux A (2014) Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol 5:491
10.
go back to reference Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16:585–601CrossRef Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16:585–601CrossRef
11.
go back to reference Souza TO, Mesquita DA, Ferrari RA, Pinto D, Júnior S, Correa L, Bussadori SK, Fernandes KPS, Martins MD (2011) Phototherapy with low-level laser affects the remodeling of types I and III collagen in skeletal muscle repair. Lasers Med Sci 26:803–814CrossRef Souza TO, Mesquita DA, Ferrari RA, Pinto D, Júnior S, Correa L, Bussadori SK, Fernandes KPS, Martins MD (2011) Phototherapy with low-level laser affects the remodeling of types I and III collagen in skeletal muscle repair. Lasers Med Sci 26:803–814CrossRef
12.
go back to reference Fernandes KP, Alves AN, Nunes FD, Souza NH, Silva JA Jr, Bussadori SK, Ferrari RA (2013) Effect of photobiomodulation on expression of IL-1beta in skeletal muscle following acute injury. Lasers Med Sci 28:1043–1046CrossRef Fernandes KP, Alves AN, Nunes FD, Souza NH, Silva JA Jr, Bussadori SK, Ferrari RA (2013) Effect of photobiomodulation on expression of IL-1beta in skeletal muscle following acute injury. Lasers Med Sci 28:1043–1046CrossRef
13.
go back to reference de Lima FM, Aimbire F, Miranda H, Vieira RP, Oliveira AP, Albertini R (2014) Low-level laser therapy attenuates the myeloperoxidase activity and inflammatory mediator generation in lung inflammation induced by gut ischemia and reperfusion: a dose-response study. J Lasers Med Sci Spring 5:63–70 de Lima FM, Aimbire F, Miranda H, Vieira RP, Oliveira AP, Albertini R (2014) Low-level laser therapy attenuates the myeloperoxidase activity and inflammatory mediator generation in lung inflammation induced by gut ischemia and reperfusion: a dose-response study. J Lasers Med Sci Spring 5:63–70
14.
go back to reference Fernandes KPS, Souza NHC, Mesquita-Ferrari RA, Silva DF, Rocha LA, Alves AN, Sousa KB, Bussadori SK, Hamblin MR, Nunes FD (2015) Photobiomodulation with 660-nm and 780-nm laser on activated J774 macrophage-like cells: effect on M1 inflammatory markers. J Photochem Photobiol B 153:344–351CrossRef Fernandes KPS, Souza NHC, Mesquita-Ferrari RA, Silva DF, Rocha LA, Alves AN, Sousa KB, Bussadori SK, Hamblin MR, Nunes FD (2015) Photobiomodulation with 660-nm and 780-nm laser on activated J774 macrophage-like cells: effect on M1 inflammatory markers. J Photochem Photobiol B 153:344–351CrossRef
15.
go back to reference Souza NHC, Mesquita-Ferrari RA, Rodrigues MFSD, da Silva DFT, Ribeiro BG, Alves AN, Garcia MP, Nunes FD, da Silva Junior EM, França CM, Bussadori SK, Fernandes KPS (2018) Photobiomodulation and different macrophages phenotypes during muscle tissue repair. J Cell Mol Med 22:4922–4934CrossRef Souza NHC, Mesquita-Ferrari RA, Rodrigues MFSD, da Silva DFT, Ribeiro BG, Alves AN, Garcia MP, Nunes FD, da Silva Junior EM, França CM, Bussadori SK, Fernandes KPS (2018) Photobiomodulation and different macrophages phenotypes during muscle tissue repair. J Cell Mol Med 22:4922–4934CrossRef
16.
go back to reference Gavish L, Perez LS, Reissman P, Gertz SD (2008) Irradiation with 780 nm diode laser attenuates inflammatory cytokines but upregulates nitric oxide in lipopolysaccharide-stimulated macrophages: implications for the prevention of aneurysm progression. Lasers Surg Med 40:371–378CrossRef Gavish L, Perez LS, Reissman P, Gertz SD (2008) Irradiation with 780 nm diode laser attenuates inflammatory cytokines but upregulates nitric oxide in lipopolysaccharide-stimulated macrophages: implications for the prevention of aneurysm progression. Lasers Surg Med 40:371–378CrossRef
17.
go back to reference Sousa LR, Cavalcanti BN, Marques MM (2009) Effect of laser phototherapy on the release of TNF-alpha and MMP-1 by endodontic sealer-stimulated macrophages. Photomed Laser Surg 27:37–42CrossRef Sousa LR, Cavalcanti BN, Marques MM (2009) Effect of laser phototherapy on the release of TNF-alpha and MMP-1 by endodontic sealer-stimulated macrophages. Photomed Laser Surg 27:37–42CrossRef
18.
go back to reference de Lima FM, Villaverde AB, Albertini R, de Oliveira AP, Faria Neto HC, Aimbire F (2010) Low-level laser therapy associated to N-acetylcysteine lowers macrophage inflammatory protein-2 (MIP-2) mRNA expression and generation of intracellular reactive oxygen species in alveolar macrophages. Photomed Laser Surg 28:763–771CrossRef de Lima FM, Villaverde AB, Albertini R, de Oliveira AP, Faria Neto HC, Aimbire F (2010) Low-level laser therapy associated to N-acetylcysteine lowers macrophage inflammatory protein-2 (MIP-2) mRNA expression and generation of intracellular reactive oxygen species in alveolar macrophages. Photomed Laser Surg 28:763–771CrossRef
19.
go back to reference Souza NH, Marcondes PT, Albertini R, Mesquita-Ferrari RA, Fernandes KP, Aimbire F (2014) Low-level laser therapy supresses the oxidative stress-induced glucocorticoids resistance in U937 cells: relevance to cytokine secretion and histone deacetylase in alveolar macrophages. J Photochem Photobiol B Biol 130:327–336CrossRef Souza NH, Marcondes PT, Albertini R, Mesquita-Ferrari RA, Fernandes KP, Aimbire F (2014) Low-level laser therapy supresses the oxidative stress-induced glucocorticoids resistance in U937 cells: relevance to cytokine secretion and histone deacetylase in alveolar macrophages. J Photochem Photobiol B Biol 130:327–336CrossRef
20.
go back to reference 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. Hindawi Publishing Corporation 2014:625048 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. Hindawi Publishing Corporation 2014:625048
21.
go back to reference Silva DF, Mesquita-Ferrari RA, Fernandes KPS, Raele MP, Wetter NU, Deana AM (2012) Effective transmission of light for media culture, plates and tubes. Photochem Photobiol 88:1211–1216CrossRef Silva DF, Mesquita-Ferrari RA, Fernandes KPS, Raele MP, Wetter NU, Deana AM (2012) Effective transmission of light for media culture, plates and tubes. Photochem Photobiol 88:1211–1216CrossRef
22.
go back to reference Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969CrossRef Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969CrossRef
23.
go back to reference Filardy AA, Pires DR, Nunes MP, Takiya CM, Freire-de-Lima CG, Ribeiro-Gomes FL, Reis GA (2010) Proinflammatory clearance of apoptotic neutrophils induces an IL-12 (low) IL-10 (high) regulatory phenotype in macrophages. J Immunol 185:2044–2050CrossRef Filardy AA, Pires DR, Nunes MP, Takiya CM, Freire-de-Lima CG, Ribeiro-Gomes FL, Reis GA (2010) Proinflammatory clearance of apoptotic neutrophils induces an IL-12 (low) IL-10 (high) regulatory phenotype in macrophages. J Immunol 185:2044–2050CrossRef
24.
go back to reference Lindell DM, Standiford TJ, Mancuso P, Leshen ZJ, Huffnagle GB (2001) Macrophage inflammatory protein 1alpha/CCL3 is required for clearance of an acute Klebsiella pneumoniae pulmonary infection. Infect Immun 69:6364–6369CrossRef Lindell DM, Standiford TJ, Mancuso P, Leshen ZJ, Huffnagle GB (2001) Macrophage inflammatory protein 1alpha/CCL3 is required for clearance of an acute Klebsiella pneumoniae pulmonary infection. Infect Immun 69:6364–6369CrossRef
25.
go back to reference Fahey TJ 3rd, Tracey KJ, Tekamp-Olson P, Cousens LS, Jones WG, Shires GT, Cerami A, Sherry B (1992) Macrophage inflammatory protein 1 modulates macrophage function. J Immunol 148:2764–2769PubMed Fahey TJ 3rd, Tracey KJ, Tekamp-Olson P, Cousens LS, Jones WG, Shires GT, Cerami A, Sherry B (1992) Macrophage inflammatory protein 1 modulates macrophage function. J Immunol 148:2764–2769PubMed
26.
go back to reference Raman D, Sobolik-Delmaire T, Richmond A (2011) Chemokines in health and disease. Exp Cell Res 317:575–589CrossRef Raman D, Sobolik-Delmaire T, Richmond A (2011) Chemokines in health and disease. Exp Cell Res 317:575–589CrossRef
27.
go back to reference Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP (2011) Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 26:335–340CrossRef Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP (2011) Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 26:335–340CrossRef
28.
go back to reference Albertini R, Villaverde AB, Aimbire F, Bjordal J, Brugnera A, Mittmann J, Silva JA Jr, Costa M (2008) Cytokine mRNA expression is decreased in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation after low-level laser therapy. Photomed Laser Surg 26:19–24CrossRef Albertini R, Villaverde AB, Aimbire F, Bjordal J, Brugnera A, Mittmann J, Silva JA Jr, Costa M (2008) Cytokine mRNA expression is decreased in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation after low-level laser therapy. Photomed Laser Surg 26:19–24CrossRef
29.
go back to reference Almeida PD, Tomazoni SS, Frigo L, de Carvalho PT, Vanin AA, Santos LA, Albuquerque-Pontes GM, De Marchi T, Tairova O, Marcos RL, Lopes-Martins RA, Leal-Junior EC (2014) What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy? Lasers Med Sci 29:653–658CrossRef Almeida PD, Tomazoni SS, Frigo L, de Carvalho PT, Vanin AA, Santos LA, Albuquerque-Pontes GM, De Marchi T, Tairova O, Marcos RL, Lopes-Martins RA, Leal-Junior EC (2014) What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy? Lasers Med Sci 29:653–658CrossRef
30.
go back to reference Arany PR (2016) Photobiomodulation therapy: communicating with stem cells for regeneration? Photomed Laser Surg 34:497–499CrossRef Arany PR (2016) Photobiomodulation therapy: communicating with stem cells for regeneration? Photomed Laser Surg 34:497–499CrossRef
32.
go back to reference Karin M, Clevers H (2016) Reparative inflammation takes charge of tissue regeneration. Nature 529:307–315CrossRef Karin M, Clevers H (2016) Reparative inflammation takes charge of tissue regeneration. Nature 529:307–315CrossRef
33.
go back to reference Pallotta RC, Bjordal JM, Frigo L, Leal Junior EC, Teixeira S, Marcos RL, Ramos L, Messias FM, Lopes-Martins RA (2012) Infrared (810-nm) low-level laser therapy on rat experimental knee inflammation. Lasers Med Sci 27:71–78CrossRef Pallotta RC, Bjordal JM, Frigo L, Leal Junior EC, Teixeira S, Marcos RL, Ramos L, Messias FM, Lopes-Martins RA (2012) Infrared (810-nm) low-level laser therapy on rat experimental knee inflammation. Lasers Med Sci 27:71–78CrossRef
34.
go back to reference Silva IH, de Andrade SC, de Faria AB (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 31:1855–1862CrossRef Silva IH, de Andrade SC, de Faria AB (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 31:1855–1862CrossRef
35.
go back to reference Alves AN, Fernandes KPS, Deana AM, Bussadori SK, Mesquita-Ferrari RA (2014) Effects of low-level laser therapy on skeletal muscle repair: a systematic review. Am J Phys Med Rehabil 93:1073–1085CrossRef Alves AN, Fernandes KPS, Deana AM, Bussadori SK, Mesquita-Ferrari RA (2014) Effects of low-level laser therapy on skeletal muscle repair: a systematic review. Am J Phys Med Rehabil 93:1073–1085CrossRef
36.
go back to reference Karu TI, Afanas'eva NI (1995) Cytochrome c oxidase as the primary photoacceptor upon laser exposure of cultured cells to visible and near IR-range light. Dokl Akad Nauk 342:693–695PubMed Karu TI, Afanas'eva NI (1995) Cytochrome c oxidase as the primary photoacceptor upon laser exposure of cultured cells to visible and near IR-range light. Dokl Akad Nauk 342:693–695PubMed
37.
go back to reference Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 22:7000417CrossRef Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 22:7000417CrossRef
Metadata
Title
Differential expression of inflammatory and anti-inflammatory mediators by M1 and M2 macrophages after photobiomodulation with red or infrared lasers
Authors
Kaline de Brito Sousa
Maria Fernanda Setúbal Destro Rodrigues
Debora de Souza Santos
Raquel Agnelli Mesquita-Ferrari
Fabio Daumas Nunes
Daniela de Fátima Teixeira da Silva
Sandra Kalil Bussadori
Kristianne Porta Santos Fernandes
Publication date
01-03-2020
Publisher
Springer London
Keywords
Cytokines
Laser
Published in
Lasers in Medical Science / Issue 2/2020
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-019-02817-1

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