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Published in: Lasers in Medical Science 6/2013

01-11-2013 | Original Article

Low-level laser reduces the production of TNF-α, IFN-γ, and IL-10 induced by OVA

Authors: Rodrigo G. Oliveira, Ana P. Ferreira, Andréa J. Côrtes, Beatriz J. Vieira Aarestrup, Luis C. Andrade, Fernando M. Aarestrup

Published in: Lasers in Medical Science | Issue 6/2013

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Abstract

Delayed, or type IV, hypersensitivity reactions are a useful model to study the effects of new substances on the immune system. In this study, the experimental model of the delayed type hypersensitivity (DTH) reaction to ovalbumin (OVA) was used to evaluate the immunomodulating effects of low-level laser therapy (LLLT), which is used as an adjuvant therapy in medicine, dentistry, and physical therapy because of its potential anti-inflammatory and analgesic effects observed in several studies. The effects of LLLT (λ 780 nm, 0.06 W/cm2 of radiation, and fluency of 3.8 J/cm2) in reaction to ovalbumin in Balb/C mice were examined after the induction phase of the hypersensitivity reaction. The animals treated with azathioprine (AZA), the animals that received a vehicle instead of ovalbumin, and those not immunized served as controls (n = 6 for each group). Footpad thickness measurements and hematoxylin–eosin histopathological exams were performed. Proliferation tests were also performed (spontaneous, in the presence of concanavalin A and ovalbumin) to determine the production in mononuclear cells cultures of tumor necrosis factor-alpha (TNF-α), INF-γ, and IL-10. In the group of animals irradiated with lasers and in the group treated with AZA, footpad thickness measurements were significantly reduced in comparison to the control group (p < 0.05). This reduction was accompanied by a very significant reduction in the density of the inflammatory infiltrate and by a significant reduction in the levels of TNF-α, INF-γ, and IL-10. LLLT radiation was shown to have an immunomodulating effect on DTH to OVA in Balb/C mice.
Literature
1.
go back to reference Albertini R, Aimbire FS, Correa FI, Ribeiro W, Cogo JC, Antunes E et al (2004) Effects of different protocol doses of low power gallium-aluminum-arsenate (Ga-Al-As) laser radiation (650 nm) on carrageenan induced rat paw ooedema. J Photochem Photobiol B 74(2–3):101–107CrossRefPubMed Albertini R, Aimbire FS, Correa FI, Ribeiro W, Cogo JC, Antunes E et al (2004) Effects of different protocol doses of low power gallium-aluminum-arsenate (Ga-Al-As) laser radiation (650 nm) on carrageenan induced rat paw ooedema. J Photochem Photobiol B 74(2–3):101–107CrossRefPubMed
2.
go back to reference Albertini R, Villaverde AB, Aimbire F, Salgado MA, Bjordal JM, Alves LP et al (2007) Anti-inflammatory effects of low-level laser therapy (LLLT) with two different red wavelengths (660 and 684 nm) in carrageenan-induced rat paw edema. J Photochem Photobiol B 89(1):50–55CrossRefPubMed Albertini R, Villaverde AB, Aimbire F, Salgado MA, Bjordal JM, Alves LP et al (2007) Anti-inflammatory effects of low-level laser therapy (LLLT) with two different red wavelengths (660 and 684 nm) in carrageenan-induced rat paw edema. J Photochem Photobiol B 89(1):50–55CrossRefPubMed
3.
go back to reference Bjordal JM, Johnson MI, Iversen V, Aimbire F, Lopes-Martins RA (2006) Photoradiation in acute pain: a systematic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomed Laser Surg 24(2):158–168CrossRefPubMed Bjordal JM, Johnson MI, Iversen V, Aimbire F, Lopes-Martins RA (2006) Photoradiation in acute pain: a systematic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomed Laser Surg 24(2):158–168CrossRefPubMed
4.
go back to reference Mozzati M, Martinasso G, Cocero N et al (2011) Influence of superpulsed laser therapy on healing process following tooth extraction. Photomed Laser Surg 29(8):565–571CrossRefPubMed Mozzati M, Martinasso G, Cocero N et al (2011) Influence of superpulsed laser therapy on healing process following tooth extraction. Photomed Laser Surg 29(8):565–571CrossRefPubMed
5.
go back to reference Brill GE, Budnik IA, Gasparian LV, Shenkman B, Savion N, Varon D (2008) Influence of laser radiation of the whole blood in vitro on adhesion and aggregation of blood platelets. Vopr Kurortol Fizioter Lech Fiz Kult 1:15–18PubMed Brill GE, Budnik IA, Gasparian LV, Shenkman B, Savion N, Varon D (2008) Influence of laser radiation of the whole blood in vitro on adhesion and aggregation of blood platelets. Vopr Kurortol Fizioter Lech Fiz Kult 1:15–18PubMed
6.
go back to reference Enwemeka CS (2004) Therapeutic light. Rehab Manag 17(1):20–25, 56-7PubMed Enwemeka CS (2004) Therapeutic light. Rehab Manag 17(1):20–25, 56-7PubMed
7.
go back to reference Fujimaki Y, Shimoyama T, Liu Q, Umeda T, Nakaji S, Sugawara K (2003) Low-level laser irradiation attenuates production of reactive oxygen species by human neutrophils. J Clin Laser Med Surg 21(3):165–170CrossRefPubMed Fujimaki Y, Shimoyama T, Liu Q, Umeda T, Nakaji S, Sugawara K (2003) Low-level laser irradiation attenuates production of reactive oxygen species by human neutrophils. J Clin Laser Med Surg 21(3):165–170CrossRefPubMed
8.
go back to reference Beeton C, Chandy KG (2007) Induction and monitoring of active delayed type hypersensitivity (DTH) in rats. J Vis Exp 6:237PubMed Beeton C, Chandy KG (2007) Induction and monitoring of active delayed type hypersensitivity (DTH) in rats. J Vis Exp 6:237PubMed
9.
go back to reference Jacysyn JF, Abrahamsohn IA, Macedo MS (2001) Modulation of delayed-type hypersensitivity during the time course of immune response to a protein antigen. Immunology 102(3):373–379CrossRefPubMed Jacysyn JF, Abrahamsohn IA, Macedo MS (2001) Modulation of delayed-type hypersensitivity during the time course of immune response to a protein antigen. Immunology 102(3):373–379CrossRefPubMed
10.
go back to reference Pelletier RP, Bickerstaff AA, Adams PW, Orosz CG (2007) Evaluation of immune regulation in transplant patients using the trans vivo delayed type hypersensitivity assay. Hum Immunol 68(6):514–522CrossRefPubMed Pelletier RP, Bickerstaff AA, Adams PW, Orosz CG (2007) Evaluation of immune regulation in transplant patients using the trans vivo delayed type hypersensitivity assay. Hum Immunol 68(6):514–522CrossRefPubMed
11.
go back to reference Kobayashi K, Kaneda K, Kasama T (2001) Immunopathogenesis of delayed-type hypersensitivity. Microsc Res Tech 53(4):241–245CrossRefPubMed Kobayashi K, Kaneda K, Kasama T (2001) Immunopathogenesis of delayed-type hypersensitivity. Microsc Res Tech 53(4):241–245CrossRefPubMed
12.
go back to reference Phadke K, Carroll J, Nanda S (1982) Effects of various anti-inflammatory drugs on type II collagen-induced arthritis in rats. Clin Exp Immunol 47(3):579–586PubMed Phadke K, Carroll J, Nanda S (1982) Effects of various anti-inflammatory drugs on type II collagen-induced arthritis in rats. Clin Exp Immunol 47(3):579–586PubMed
13.
go back to reference Yamashita K, Sakai M, Takemoto N, Tsukimoto M, Uchida K, Yajima H et al (2009) Attenuation of delayed-type hypersensitivity by fullerene treatment. Toxicology 261(1–2):19–24CrossRefPubMed Yamashita K, Sakai M, Takemoto N, Tsukimoto M, Uchida K, Yajima H et al (2009) Attenuation of delayed-type hypersensitivity by fullerene treatment. Toxicology 261(1–2):19–24CrossRefPubMed
14.
15.
go back to reference Morris RE (1995) Mechanisms of action of new immunosuppressive drugs. Ther Drug Monit 17(6):564–569CrossRefPubMed Morris RE (1995) Mechanisms of action of new immunosuppressive drugs. Ther Drug Monit 17(6):564–569CrossRefPubMed
16.
go back to reference Craig JC, Webster AC, McDonald SP (2009) The case of azathioprine versus mycophenolate. Do different drugs really cause different transplant outcomes? Transplantation 87(6):803–804CrossRefPubMed Craig JC, Webster AC, McDonald SP (2009) The case of azathioprine versus mycophenolate. Do different drugs really cause different transplant outcomes? Transplantation 87(6):803–804CrossRefPubMed
17.
go back to reference Sakihama H (1995) Effect of a helium-neon laser on cutaneous inflammation. Kurume Med J 42(4):299–305CrossRefPubMed Sakihama H (1995) Effect of a helium-neon laser on cutaneous inflammation. Kurume Med J 42(4):299–305CrossRefPubMed
18.
go back to reference Persina IS, Rakcheev AP (1984) Effect of helium-neon laser radiation on the morphology of experimental allergic contact dermatitis. Biull Eksp Biol Med 97(5):603–605CrossRefPubMed Persina IS, Rakcheev AP (1984) Effect of helium-neon laser radiation on the morphology of experimental allergic contact dermatitis. Biull Eksp Biol Med 97(5):603–605CrossRefPubMed
19.
go back to reference Tsvetkova GM, Rakcheev AP, Persina IS (1984) Morphological changes in the normal skin of guinea pigs exposed to a helium-neon laser. Vestn Dermatol Venerol 3:14–17PubMed Tsvetkova GM, Rakcheev AP, Persina IS (1984) Morphological changes in the normal skin of guinea pigs exposed to a helium-neon laser. Vestn Dermatol Venerol 3:14–17PubMed
20.
go back to reference Rochkind S, Rousso M, Nissan M, Villarreal M, Barr-Nea L, Rees DG (1989) Systemic effects of low-power laser irradiation on the peripheral and central nervous system, cutaneous wounds, and burns. Lasers Surg Med 9(2):174–182CrossRefPubMed Rochkind S, Rousso M, Nissan M, Villarreal M, Barr-Nea L, Rees DG (1989) Systemic effects of low-power laser irradiation on the peripheral and central nervous system, cutaneous wounds, and burns. Lasers Surg Med 9(2):174–182CrossRefPubMed
21.
go back to reference Inoue K, Nishioka J, Hukuda S (1989) Suppressed tuberculin reaction in guinea pigs following laser irradiation. Lasers Surg Med 9(3):271–275CrossRefPubMed Inoue K, Nishioka J, Hukuda S (1989) Suppressed tuberculin reaction in guinea pigs following laser irradiation. Lasers Surg Med 9(3):271–275CrossRefPubMed
22.
go back to reference Basford JR (1995) Low intensity laser therapy: still not an established clinical tool. Lasers Surg Med 16(4):331–342CrossRefPubMed Basford JR (1995) Low intensity laser therapy: still not an established clinical tool. Lasers Surg Med 16(4):331–342CrossRefPubMed
23.
go back to reference Basford JR (1990) The clinical status of low energy laser therapy in 1989. J Laser Appl 2(1):57–63CrossRefPubMed Basford JR (1990) The clinical status of low energy laser therapy in 1989. J Laser Appl 2(1):57–63CrossRefPubMed
25.
go back to reference Nevins TE, Thomas W (2009) Quantitative patterns of azathioprine adherence after renal transplantation. Transplantation 87(5):711–718CrossRefPubMed Nevins TE, Thomas W (2009) Quantitative patterns of azathioprine adherence after renal transplantation. Transplantation 87(5):711–718CrossRefPubMed
26.
go back to reference Goldsmith P, Lennox G, Bhalla N (2008) Azathioprine prescribing in neurology. J Neurol 255(6):791–795CrossRefPubMed Goldsmith P, Lennox G, Bhalla N (2008) Azathioprine prescribing in neurology. J Neurol 255(6):791–795CrossRefPubMed
27.
go back to reference Sroka R, Schaffer M, Fuchs C, Pongratz T, Schrader-Reichard U, Busch M et al (1999) Effects on the mitosis of normal and tumor cells induced by light treatment of different wavelengths. Lasers Surg Med 25(3):263–271CrossRefPubMed Sroka R, Schaffer M, Fuchs C, Pongratz T, Schrader-Reichard U, Busch M et al (1999) Effects on the mitosis of normal and tumor cells induced by light treatment of different wavelengths. Lasers Surg Med 25(3):263–271CrossRefPubMed
28.
go back to reference Schindl A, Schindl M, Pernerstorfer-Schon H, Schindl L (2000) Low-intensity laser therapy: a review. J Investig Med 48(5):312–326PubMed Schindl A, Schindl M, Pernerstorfer-Schon H, Schindl L (2000) Low-intensity laser therapy: a review. J Investig Med 48(5):312–326PubMed
29.
30.
31.
go back to reference Enwemeka CS (2009) Intricacies of dose in laser phototherapy for tissue repair and pain relief. Photomed Laser Surg 27(3):387–393CrossRefPubMed Enwemeka CS (2009) Intricacies of dose in laser phototherapy for tissue repair and pain relief. Photomed Laser Surg 27(3):387–393CrossRefPubMed
32.
go back to reference de Oliveira RG, Aarestrup FM, Miranda C et al (2010) Lowl-level laser therapy reduces delayed hypersensitivy reaction to ovalbumin in Balb/C mice. Photomed Laser Surg 28(6):773–777CrossRefPubMed de Oliveira RG, Aarestrup FM, Miranda C et al (2010) Lowl-level laser therapy reduces delayed hypersensitivy reaction to ovalbumin in Balb/C mice. Photomed Laser Surg 28(6):773–777CrossRefPubMed
33.
go back to reference Brosseau L, Robinson V, Wells G, Debie R, Gam A, Harman K et al (2005) Low level laser therapy (Classes I, II and III) for treating rheumatoid arthritis. Cochrane Database Syst Rev 4:CD002049PubMed Brosseau L, Robinson V, Wells G, Debie R, Gam A, Harman K et al (2005) Low level laser therapy (Classes I, II and III) for treating rheumatoid arthritis. Cochrane Database Syst Rev 4:CD002049PubMed
34.
go back to reference Sandoval MC, Mattiello-Rosa SM, Soares EG, Parizotto NA (2009) Effects of Laser on the synovial fluid in the inflammatory process of the knee joint of the rabbit. Photomed Laser Surg Sandoval MC, Mattiello-Rosa SM, Soares EG, Parizotto NA (2009) Effects of Laser on the synovial fluid in the inflammatory process of the knee joint of the rabbit. Photomed Laser Surg
35.
go back to reference Ishigame H, Nakajima A, Saijo S, Komiyama Y, Nambu A, Matsuki T et al (2006) The role of TNFalpha and IL-17 in the development of excess IL-1 signaling-induced inflammatory diseases in IL-1 receptor antagonist-deficient mice. Ernst Schering Res Found Workshop 56:129–153CrossRefPubMed Ishigame H, Nakajima A, Saijo S, Komiyama Y, Nambu A, Matsuki T et al (2006) The role of TNFalpha and IL-17 in the development of excess IL-1 signaling-induced inflammatory diseases in IL-1 receptor antagonist-deficient mice. Ernst Schering Res Found Workshop 56:129–153CrossRefPubMed
36.
go back to reference Tanaka S, Sakaguchi S (2005) Regulatory T cell and autoimmune diseases. Nihon Rinsho Meneki Gakkai Kaishi 28(5):291–299CrossRefPubMed Tanaka S, Sakaguchi S (2005) Regulatory T cell and autoimmune diseases. Nihon Rinsho Meneki Gakkai Kaishi 28(5):291–299CrossRefPubMed
37.
go back to reference Wonderlich J, Shearer G, Livingstone A, Brooks A (2006) Induction and measurement of cytotoxic T lymphocyte activity. Curr Protoc Immunol 3(3):11PubMed Wonderlich J, Shearer G, Livingstone A, Brooks A (2006) Induction and measurement of cytotoxic T lymphocyte activity. Curr Protoc Immunol 3(3):11PubMed
38.
go back to reference Aimbire F, Albertini R, Pacheco MT, Castro-Faria-Neto HC, Leonardo PS, Iversen VV et al (2006) Low-level laser therapy induces dose-dependent reduction of TNFalpha levels in acute inflammation. Photomed Laser Surg 24(1):33–37CrossRefPubMed Aimbire F, Albertini R, Pacheco MT, Castro-Faria-Neto HC, Leonardo PS, Iversen VV et al (2006) Low-level laser therapy induces dose-dependent reduction of TNFalpha levels in acute inflammation. Photomed Laser Surg 24(1):33–37CrossRefPubMed
39.
go back to reference Srinivas TR, Meier-Kriesche HU, Kaplan B (2005) Pharmacokinetic principles of immunosuppressive drugs. Am J Transplant 5(2):207–217CrossRefPubMed Srinivas TR, Meier-Kriesche HU, Kaplan B (2005) Pharmacokinetic principles of immunosuppressive drugs. Am J Transplant 5(2):207–217CrossRefPubMed
40.
go back to reference Zhang J, Xiao X, Liu W, Demirci G, Li XC (2009) Inhibitory receptors of the immune system: functions and therapeutic implications. Cell Mol Immunol 6(6):407–414CrossRefPubMed Zhang J, Xiao X, Liu W, Demirci G, Li XC (2009) Inhibitory receptors of the immune system: functions and therapeutic implications. Cell Mol Immunol 6(6):407–414CrossRefPubMed
41.
go back to reference Bettini M, Vignali DA (2009) Regulatory T cells and inhibitory cytokines in autoimmunity. Curr Opin Immunol 21(6):612–618CrossRefPubMed Bettini M, Vignali DA (2009) Regulatory T cells and inhibitory cytokines in autoimmunity. Curr Opin Immunol 21(6):612–618CrossRefPubMed
42.
go back to reference Brook MO, Wood KJ, Jones ND (2006) The impact of memory T cells on rejection and the induction of tolerance. Transplantation 82(1):1–9CrossRefPubMed Brook MO, Wood KJ, Jones ND (2006) The impact of memory T cells on rejection and the induction of tolerance. Transplantation 82(1):1–9CrossRefPubMed
43.
go back to reference Cone RE, Li X, Sharafieh R, O'Rourke J, Vella AT (2007) The suppression of delayed-type hypersensitivity by CD8+ regulatory T cells requires interferon-gamma. Immunology 120(1):112–119CrossRefPubMed Cone RE, Li X, Sharafieh R, O'Rourke J, Vella AT (2007) The suppression of delayed-type hypersensitivity by CD8+ regulatory T cells requires interferon-gamma. Immunology 120(1):112–119CrossRefPubMed
44.
go back to reference Hernandez-Pando R, Rook GA (1994) The role of TNF-alpha in T-cell-mediated inflammation depends on the Th1/Th2 cytokine balance. Immunology 82(4):591–595PubMed Hernandez-Pando R, Rook GA (1994) The role of TNF-alpha in T-cell-mediated inflammation depends on the Th1/Th2 cytokine balance. Immunology 82(4):591–595PubMed
45.
go back to reference Kimber I, Pichowski JS, Basketter DA, Dearman RJ (1999) Immune responses to contact allergens: novel approaches to hazard evaluation. Toxicol Lett 106(2–3):237–246CrossRefPubMed Kimber I, Pichowski JS, Basketter DA, Dearman RJ (1999) Immune responses to contact allergens: novel approaches to hazard evaluation. Toxicol Lett 106(2–3):237–246CrossRefPubMed
46.
go back to reference Ohta A, Abergel RP, Uitto J (1987) Laser modulation of human immune system: inhibition of lymphocyte proliferation by a gallium-arsenide laser at low energy. Lasers Surg Med 7(2):199–201CrossRefPubMed Ohta A, Abergel RP, Uitto J (1987) Laser modulation of human immune system: inhibition of lymphocyte proliferation by a gallium-arsenide laser at low energy. Lasers Surg Med 7(2):199–201CrossRefPubMed
47.
go back to reference Hope JC, Campbell F, Hopkins SJ (2000) Deficiency of IL-2 or IL-6 reduces lymphocyte proliferation, but only IL-6 deficiency decreases the contact hypersensitivity response. Eur J Immunol 30(1):197–203CrossRefPubMed Hope JC, Campbell F, Hopkins SJ (2000) Deficiency of IL-2 or IL-6 reduces lymphocyte proliferation, but only IL-6 deficiency decreases the contact hypersensitivity response. Eur J Immunol 30(1):197–203CrossRefPubMed
48.
go back to reference Funk JO, Kruse A, Neustock P, Kirchner H (1993) Helium-neon laser irradiation induces effects on cytokine production at the protein and the mRNA level. Exp Dermatol 2(2):75–83CrossRefPubMed Funk JO, Kruse A, Neustock P, Kirchner H (1993) Helium-neon laser irradiation induces effects on cytokine production at the protein and the mRNA level. Exp Dermatol 2(2):75–83CrossRefPubMed
49.
go back to reference Funk JO, Kruse A, Kirchner H (1992) Cytokine production after helium-neon laser irradiation in cultures of human peripheral blood mononuclear cells. J Photochem Photobiol B 16(3–4):347–355CrossRefPubMed Funk JO, Kruse A, Kirchner H (1992) Cytokine production after helium-neon laser irradiation in cultures of human peripheral blood mononuclear cells. J Photochem Photobiol B 16(3–4):347–355CrossRefPubMed
50.
go back to reference Fulop AM, Dhimmer S, Deluca JR, Johanson DD, Lenz RV, Patel KB et al (2009) A meta-analysis of the efficacy of phototherapy in tissue repair. Photomed Laser Surg 27(5):695–702CrossRefPubMed Fulop AM, Dhimmer S, Deluca JR, Johanson DD, Lenz RV, Patel KB et al (2009) A meta-analysis of the efficacy of phototherapy in tissue repair. Photomed Laser Surg 27(5):695–702CrossRefPubMed
51.
go back to reference Kataranovski M, Draskovic-Pavlovic B, Jovcic G, Milojevic G, Todorovic V, Colic M et al (2001) Peripheral blood granulocyte activity following contact sensitization of rats with dinitrochlorobenzene. Toxicology 162(2):121–136CrossRefPubMed Kataranovski M, Draskovic-Pavlovic B, Jovcic G, Milojevic G, Todorovic V, Colic M et al (2001) Peripheral blood granulocyte activity following contact sensitization of rats with dinitrochlorobenzene. Toxicology 162(2):121–136CrossRefPubMed
Metadata
Title
Low-level laser reduces the production of TNF-α, IFN-γ, and IL-10 induced by OVA
Authors
Rodrigo G. Oliveira
Ana P. Ferreira
Andréa J. Côrtes
Beatriz J. Vieira Aarestrup
Luis C. Andrade
Fernando M. Aarestrup
Publication date
01-11-2013
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 6/2013
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-012-1262-5

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