Photobiomodulation Therapy Decreases Oxidative Stress in the Lung Tissue after Formaldehyde Exposure: Role of Oxidant/Antioxidant Enzymes

Silva Macedo, Rodrigo; Peres Leal, Mayara; Braga, Tarcio Teodoro; Barioni, Éric Diego; de Oliveira Duro, Stephanie; Ratto Tempestini Horliana, Anna Carolina; Câmara, Niels Olsen Saraiva; Marcourakis, Tânia; Farsky, Sandra Helena Poliselli; Lino-dos-Santos-Franco, Adriana

doi:https://doi.org/10.1155/2016/9303126

Mediators of Inflammation

On this page

Abstract Introduction Materials and Methods Results Discussion Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2016 | Article ID 9303126 | https://doi.org/10.1155/2016/9303126

Photobiomodulation Therapy Decreases Oxidative Stress in the Lung Tissue after Formaldehyde Exposure: Role of Oxidant/Antioxidant Enzymes

Rodrigo Silva Macedo,¹Mayara Peres Leal,¹Tarcio Teodoro Braga,²Éric Diego Barioni,³Stephanie de Oliveira Duro,³Anna Carolina Ratto Tempestini Horliana,¹Niels Olsen Saraiva Câmara,²Tânia Marcourakis,³Sandra Helena Poliselli Farsky,³and Adriana Lino-dos-Santos-Franco¹

Academic Editor: Helen C. Steel

Received18 Feb 2016

Revised28 Apr 2016

Accepted04 May 2016

Published17 May 2016

Abstract

Formaldehyde is ubiquitous pollutant that induces oxidative stress in the lung. Several lung diseases have been associated with oxidative stress and their control is necessary. Photobiomodulation therapy (PBMT) has been highlighted as a promissory treatment, but its mechanisms need to be better investigated. Our objective was to evaluate the effects of PBMT on the oxidative stress generated by FA exposure. Male Wistar rats were submitted to FA exposure of 1% or vehicle (3 days) and treated or not with PBMT (1 and 5 h after each FA exposure). Rats treated only with laser were used as control. Twenty-four hours after the last FA exposure, we analyzed the effects of PBMT on the generation of nitrites and hydrogen peroxide, oxidative burst, glutathione reductase, peroxidase, S-transferase enzyme activities, the gene expression of nitric oxide, cyclooxygenase, superoxide dismutase, the catalase enzyme, and heme oxygenase-1. PBMT reduced the generation of nitrites and hydrogen peroxide and increased oxidative burst in the lung cells. A decreased level of oxidant enzymes was observed which were concomitantly related to an increased level of antioxidants. This study provides new information about the antioxidant mechanisms of PBMT in the lung and might constitute an important tool for lung disease treatment.

1. Introduction

Oxidative stress is characterized by the imbalance between an increased generation of reactive oxygen and nitrogen species (RONS) and a reduced antioxidant capacity. RONS are produced in high quantities by endogenous metabolisms which are represented primarily by the activation of neutrophils, the products of cyclooxygenase (COX), lipoxygenase (LOX), and nitric oxide synthases (NOS) [1–3]. At the same time, RONS are also produced in the body through exogenous factors including formaldehyde (FA), particulate matter (PM), metals, and quinones [4–9].

We have identified oxidative stress as an important pathway in which FA exerts its toxic effects, with a disruption of the lung physiological balance between the oxidant and antioxidant systems, modulating positively with a neutrophilic lung inflammation [9, 10]. FA is ubiquitous pollutant found in many industries, offices, and laboratories, and it is also emitted in the domestic ambient of homes, in things such as furniture, building materials, and chipboards, and in heating and cooking fumes [11].

Neutrophils that are activated by different biochemical mechanisms produce high quantities of RONS and inflammatory cytokines, leading to a severe destruction of the lung tissues [12, 13]. However, the deleterious effects of RONS are neutralized naturally by the lung through the defensive antioxidant system. Among the main antioxidant sources in the lung are glutathione reductase, peroxidase, s-transferase enzymes, superoxide dismutase, the catalase enzyme, and heme oxygenase-1 [14–16].

Several lung diseases such as asthma, chronic obstructive pulmonary diseases, and lung fibrosis have been associated with oxidative stress [17–19]. Lung diseases constitute an important public health problem and the control of oxidative stress into the lung is necessary. In this context, photobiomodulation has been highlighted as a promissory treatment, because of the absence of side effects, displaying low costs, and a noninvasiveness. However, its mechanisms need to be better investigated and understood.

Some studies have evaluated the antioxidant effects of laser therapy by using different models in vivo and in vitro [20–23]. When considering the antioxidant effects of PBMT in the lung tissues, studies have reported that, in an animal experimental model, laser treatment restored the balance between the oxidant and the antioxidant mediators, raising the PPAR expression and consequently the production of HSP70 [22].

Based upon the oxidative stress that is induced by FA exposure in the lung tissues and the antioxidant effects of PBMT, we evaluated the generation of nitrites and hydrogen peroxide, oxidative burst, glutathione reductase, peroxidase, s-transferase enzyme activities, the gene expression of nitric oxide, cyclooxygenase, superoxide dismutase, the catalase enzyme, and heme oxygenase-1. Thus, this study may provide information about the antioxidant mechanisms of PBMT in lung diseases.

2. Materials and Methods

The experiments were approved by the Committee on the Ethics of Animal Experiments of the University of Nove de Julho (CoEP-UNINOVE, Permit Number: AN0029.2014).

2.1. Animals

Male 2-month-old Wistar rats (40) were obtained from the University Nove de Julho and maintained in a light and temperature-controlled room (12/12-hour light-dark cycle, ), with free access to food and water.

2.2. Formaldehyde (FA) Exposure

Group of rats (5/chamber) were exposed to FA inhalation (1%, 90 min/day) or vehicle (distilled water) for 3 consecutive days. Thus, we utilized a standard glass chamber (20 L) coupled to an ultrasonic nebuliser device (Icel®, Brazil) which produces an aerosol with particles between 0.5 and 1 micron to generate a constant airstream in an aqueous solution of formalin [9, 10, 24].

2.3. Photobiomodulation Therapy

According to Miranda da Silva et al. [25], rats received infrared laser (CW Diode Laser-MMOptics, São Paulo, Brazil) 1 and 5 h after each FA or vehicle inhalation. The irradiation was performed directly in the skin in nine points of respiratory tract (3 points in the trachea and 3 points in the right and left lung lobes). After 24 h of last FA exposure the analyses were performed. We used the following parameters: output power of 30 mW, 660 nm wavelength, 60 s/point, and spot size of 0.14 cm², resulting in an irradiance of 210 mW/cm² and radiant exposure of 12.86 J/cm². The optical power was calibrated using a Newport 1835 C multifunction optical power meter (Equipland, Oklahoma Road, Sao Jose, CA, USA). The laser power was monitored during laser irradiation by collecting laser light with a partial reflection (4%) mirror. The laser irradiation dose was set at 1.8 J for 1 min [24–28].

2.4. Experimental Groups

The rats were assigned into 4 experimental groups: N, nonmanipulated rats; FA, identified as rats submitted to FA inhalation; L, identified as rats treated only with laser; and FA + L, identified as rats subjected to FA inhalation and treated with laser. The rats were killed by sectioning the abdominal aorta under deep anaesthesia with ketamine-xylazine by intraperitoneal route (100 mg/kg and 20 mg/kg, resp.) 24 h after the last FA inhalation.

2.5. Quantification of Nitrites in the Supernatant of Bronchoalveolar Lavage (BAL)

The concentration of nitrites (NO₂) was determined in the BAL supernatants samples. Nitrites levels were quantified according to the Griess method. The optical density (540 nm) was recorded using a microplate reader (Bio-Tek Instr., USA) and the nitrites levels were obtained using a standard curve of NaNO₂ (5–60 μM).

2.6. Quantification of Hydrogen Peroxide in the Bronchoalveolar Lavage (BAL) Cell Suspension

The hydrogen peroxide levels were quantified in sample of BAL cells. The BAL cell suspension (1 × 10⁵ cells/mL in phenol red solution) was stimulate with PMA (10 ng/well) and incubated at 37°C, 5% CO₂ for 1 hour. After this time, the reaction was stopped by the addition of 10 μL of NaOH 1 N. The optical density (620 nm) was recorded using a microplate reader (Bio-Tek Instr., USA) and the hydrogen peroxide levels were obtained using a standard curve of H₂O₂ (0–200 nM) and expressed in % H₂O₂/1 × 10⁴ cells.

2.7. Determination of Gene Expression of Oxidants and Antioxidants Enzymes in the Lung Tissue

Lung samples were snap-frozen in liquid nitrogen. The total RNA was isolated from lung tissue using Trizol Reagent (Invitrogen, Carlsbad, CA) according to Invitrogen. RNA concentrations were determined by spectrophotometer absorbance readings at 260 nm. First-strand cDNAs were synthesized using the MML-V reverse transcriptase (Promega, Madison, WI). RT-PCR was performed using the SYBR Green real-time PCR assay (Applied Biosystem, USA) for the following molecules: hypoxanthine guanine phosphoribosyl transferase (HPRT) (sense) 5′-CTC ATG GAC TGA TTA TGG ACA GGA C-3′ and (antisense) 5′-GCA GGT CAG CAA AGA ACT TAT AGC C-3′; iNOS (sense) 5′-AGT GAG GAG CAG GTT GAG GA-3′ and (antisense) 5′-GCT GTA ACT CTT CTG GGT GT-3′. RT-PCR was performed using the TaqMan real-time PCR assay (Applied Biosystem, USA) for the following molecules: COX-1 (Rn00566881_m), COX-2 (Rn01483828_m), SOD-1 (Rn00566938_m), SOD-2 (Rn00690587_g), and catalase (Rn00560930_m). Cycling conditions were as follows: 10 min at 95°C followed by 45 cycles at 20 s each at 95°C, 20 s at 58°C, and 20 s at 72°C. Analysis was performed using Sequence Detection Software 1.9 (SDS), and mRNA expression was normalized to HPRT expression.

2.8. Quantification of Enzymatic Activities of Glutathione Peroxidase, Reductase, and S-Transferase

Glutathione peroxidase (GPx) activity was determined using tert-butylhydroperoxide as the substrate, and the formation of oxidized glutathione (GSSG) was indirectly monitored through NAPDH consumption (5 min, wavelength of 340 nm). Glutathione reductase (GR) activity was determined by the reduction of GSSG to GSH measured through NADPH consumption, which was monitored spectrophotometrically (10 min, wavelength of 340 nm, 37°C). Glutathione S-transferase (GST) activity was determined by measuring the conjugation of 1-chloro-2,4-dinitrobenzene (CDNB) with reduced glutathione. The formation of the complex was monitored spectrophotometrically (5 min, wavelength of 340 nm, 25°C). The GPx, GR, and GST assays were performed in a Power Wave ×340 spectrophotometer (Bio-Tek Instruments INC, software KC4 v3.0).

2.9. Evaluation of Oxidative Burst in the Bronchoalveolar Lavage (BAL) Cells

Quantification of oxidative burst was performed using BAL total cells (2 × 10⁵ cells/well) estimated by means of 2′,7′-dichlorofluorescin diacetate (DCFH-DA) fluorescence cells. Direct measurement of the mean fluorescence recorded on green channel was recorded as oxidative burst. A flow cytometer (FACS Calibur, Becton Dickinson Immunocytometry Systems, San Jose, CA, USA) interfaced with a Macintosh G4 computer was used. Data from 10,000 events were collected in list mode and analyzed in Cell Quest (Becton Dickinson Immunocytometry Systems). Fluorescence data were plotted on log scale. Green fluorescence from DCFH was measured at nm (FL1 detector).

2.10. Statistical Analysis

The statistical analysis was performed using the GraphPad Prism software (GraphPad Software, Inc.). The normality test was performed using Kolmogorov-Smirnov test. Since the data were parametric, we used one-way ANOVA followed by Student’s Newman-Keuls. Differences were considered significant when .

3. Results

3.1. Photobiomodulation Therapy Reduced the Generation of Hydrogen Peroxide (H₂O₂) and Nitrites (NO₂) Induced by FA Exposure in the Lung

To investigate the effects of PBMT on generation of RONS in the lung tissue, we quantified the H₂O₂ and NO₂ in the bronchoalveolar lavage. Data of Figure 1 showed that treatment with laser reduced the levels of H₂O₂ (a) as well as NO₂ (b) when compared to nontreated group (FA group) and did not differ from nonmanipulated and laser groups (N and L groups). We can also observe that FA exposure increased the generation of NO₂ and H₂O₂ in relation to basal N and L groups.

(a)

(b)

Figure 1

Photobiomodulation therapy reduces generation of H₂O₂ and NO₂ after FA exposure in the lung. Group of rats was exposed or not to FA inhalation (1%, 90 min/day, 3 days) and treated or not with laser (30 mW, 1.8 J, 60 s/point, total 540 s, 1 and 5 h after each FA inhalation). In parallel, group of rats were treated only with laser and nonmanipulated rats were used to obtain basal parameters. The quantification of H₂O₂ and NO₂ (a, b) was determined 24 h after the last FA inhalation. Data mean ± SEM of 6 animals per group. in relation to N and L groups; in relation to FA group.

3.2. Photobiomodulation Therapy Increased the Oxidative Burst in the Lung

In order to investigate the effects of PBMT on the functional state of BAL cells, we evaluated the oxidative burst. Figures 2(a) and 2(b) showed that the treatment with laser increased the oxidative burst in BAL cells when compared to the FA, N, and L groups.

(a)

(b)

Figure 2

Photobiomodulation therapy increases oxidative burst in the lung. Group of rats was exposed to FA inhalation (1%, 90 min/day, 3 days) and treated or not with LLLT (30 mW, 1.8 J, 60 s/point, total 540 s, 1 and 5 h after each FA inhalation). In parallel, group of rats were treated only with laser and nonmanipulated rats were used to obtain basal parameters. The oxidative burst was determined 24 h after the last FA inhalation. Data mean ± SEM of 6 animals per group. in relation to N and L groups; in relation to FA group.

3.3. Photobiomodulation Therapy Reduced the Gene Expression of Nitric Oxide Synthase (iNOS and cNOS) and Cyclooxygenase (COX-2) Induced by FA Exposure in the Lung

In order to understand the possible mechanism involved in reactive oxygen and nitrogen species (RONS) after PBMT, we investigated important enzymes that generate RONS. Figure 3(a) showed that PBMT reduced the gene expression of COX-2 when compared to the N, L, and FA groups. No differences were observed between FA, L, and N groups.

(a)

(b)

(c)

Figure 3

Photobiomodulation therapy decreases oxidant enzymes after FA exposure in the lung. Group of rats was exposed to FA inhalation (1%, 90 min/day, 3 days) and treated or not with LLLT (30 mW, 1.8 J, 60 s/point, total 540 s, 1 and 5 h after each FA inhalation). In parallel, group of rats were treated only with laser and nonmanipulated rats were used to obtain basal parameters. The oxidant enzymes were determined 24 h after the last FA inhalation. Data mean ± SEM of 6 animals per group. in relation to N and L groups; in relation to FA group.

In Figures 3(b) and 3(c), we can observe that PBMT decreased the gene expression of cNOS and iNOS, respectively, when compared to the FA group and did not differ from L and N groups. We also showed that FA exposure increased the gene expression of both enzymes (cNOS and iNOS) in relation to nonmanipulated rats (N group) and rats treated only with laser (L group).

3.4. Photobiomodulation Therapy Increased the Gene Expression of Superoxide Dismutase (SOD-1 and SOD-2) and Heme Oxygenase-1 (HO-1) without Changing Catalase after FA Exposure in the Lung

We investigated the involvement of PBMT in the gene expression of antioxidant enzymes. Figure 4(a) showed that PBMT increased the gene expression of SOD-1 when compared to the FA, L, and N groups. On the other hand, in Figure 4(b) we showed that no differences were observed in the gene expression of catalase when rats were treated with laser (FA + L group). We also showed that FA exposure increased the gene expression of catalase in relation to control groups (N and L).

(a)

(b)

(c)

Figure 4

Photobiomodulation therapy increases antioxidant enzymes after FA exposure in the lung. Group of rats was exposed to FA inhalation (1%, 90 min/day, 3 days) and treated or not with LLLT (30 mW, 1.8 J, 60 s/point, total 540 s, 1 and 5 h after each FA inhalation). In parallel, group of rats were treated only with laser and nonmanipulated rats were used to obtain basal parameters. The antioxidant enzymes were determined 24 h after the last FA inhalation. Data mean ± SEM of 6 animals per group. in relation to N and L groups; in relation to FA group.

In Figure 4(c) we can observe that PBMT increased the gene expression of HO-1 when compared to the FA, L, and N groups. We also observed that FA exposure did not induce alteration in the expression of HO-1 in relation to control groups (N and L).

3.5. Photobiomodulation Therapy Increased the Activity of Glutathione S-Transferase (GST) and Peroxidase (GPX) without Changing Glutathione Reductase (GR) after FA Exposure in the Lung

We also investigated the involvement of PBMT in the activity of glutathione enzymes that exert an important protection of oxidant species in the lung tissue. Figures 5(a) and 5(c) showed that PBMT increased the activity of GST and GPX, respectively, when compared to the FA, L, and N groups. On the other hand, PBMT did not interfere in the GR activity (Figure 5(b)).

(a)

(b)

(c)

Figure 5

Photobiomodulation therapy increases activity of glutathione s-transferase and peroxidase enzymes after FA exposure in the lung. Group of rats was exposed to FA inhalation (1%, 90 min/day, 3 days) and treated or not with LLLT (30 mW, 1.8 J, 60 s/point, total 540 s, 1 and 5 h after each FA inhalation). In parallel, group of rats were treated only with laser and nonmanipulated rats were used to obtain basal parameters. The activities of glutathione s-transferase, reductase, and peroxidase were determined 24 h after the last FA inhalation. Data mean ± SEM of 6 animals per group. in relation to N, and L groups; in relation to FA group.

4. Discussion

Photobiomodulation therapy was an effective treatment for oxidative stress that was induced by an FA exposure in the lung tissue, as it reduced the generation of H₂O₂, NO₂, and the gene expression of oxidant enzymes that were concomitantly related to the increased gene expression of antioxidant enzymes. Photobiomodulation therapy also increased the activity of glutathione enzymes (GST and GPX) which are highly important for the protection of the lung against oxygen and nitrogen reactive species (RONS).

When considering the fact that oxidative stress is an important pathway by which FA induces a lung inflammation, we have shown here the protective effects of PBMT. As we expected, FA exposure evoked an increased generation of RONS in the cells recruited into the lung with respect to H₂O₂ and NO₂, which was reversed by PBMT. These results can explain the previous results published by our group that showed a reduced lung inflammation after PBMT [25]. This is since RONS has been implicated in initiating inflammatory responses in the lungs, through the activation of transcription factors, such as the nuclear factor NF-κB, leading to an enhanced gene expression of proinflammatory mediators.

The beneficial effects of PBMT were corroborated by a determination of the oxidative burst in the BAL cells that were predominantly neutrophils. The oxidative burst exerts an important role in the killing activity by the generation of oxygen reactive species by neutrophils. An elevated oxidative burst was found after PBMT, showing that this treatment improves the capacity of neutrophils to defend the body against microorganisms, although this process generates reactive species. Thus, we must consider that reactive species exert a dual role in the organism, protecting and/or prejudicing.

PBMT reduced the generation of NO₂ and H₂O₂ and simultaneously increased the oxidative burst. These data could be considered controversial if it is not taking into account that several pathways on phagocytes can generate reactive species, which are simultaneously inactivated by antioxidant enzymes. In this context, phagocytes, such as macrophages and neutrophils, generate reactive species via oxidative burst, regulated by NADPH-oxidase. This latter enzyme generates superoxide radical that is subsequently converted into hypochlorous acid, a potent bactericidal agent. Thus, increased oxidative burst may be observed in reduced levels of H₂O₂. In addition, different mechanisms of defense against H₂O₂ production are available, such as glutathione peroxidase that was increased by PBMT, which contribute to reduced levels of H₂O₂. It is important to mention that our results corroborate those obtained by Dolgushin et al. [29], which showed that PBMT increased killing activity by neutrophils.

Since, in previous studies, we have shown that FA exposure causes a disruption of the physiological balance between the oxidant and antioxidant enzymes in the lung tissue, most likely by favoring the oxidant pathways and thus positively modulating the lung’s inflammation [11, 20], we have investigated the effects of PBMT on the gene expression of these oxidant and antioxidant enzymes in the lung tissue.

Based on previous studies, we suppose that RONS produced during FA inhalation, generated by oxidant/antioxidant enzymes imbalance in the lung tissue, might alter the metabolism of lung phagocytes, which in turn could increase the release of inflammatory mediators, as well as reactive species, amplifying the lung inflammatory response [30]. In addition, it is reasonable to admit that we analyzed enzymes in the whole lung tissue, including parenchyma, muscle cells, structural cells, and phagocytes.

Our data has shown that PBMT reversed the increased gene expression of cNOS and iNOS in the lung tissue after FA exposure. These results corroborate with the reduced NO₂ released by the BAL cells. Similarly, PBMT also reduced the gene expression of COX-2 that is an important oxidant enzyme and one that generates potent inflammatory mediators including eicosanoids. We can infer this reduction in the COX, as well as in the NOS, and where this is caused by a PBMT, these results might be responsible, at least in part, for the decreased generation of oxidative species released during an FA exposure and culminating in a reduced lung inflammation, as noted previously [25].

In the literature few studies showed the PBMT effects in model of lung diseases [22, 25–28]. Almost the works showed the anti-inflammatory and antioxidants effects of PBMT in experimental models of arthritis. Thus, studies that investigate the effects of PBMT in lung diseases are important, showing the alternative therapy without side effects.

As mentioned above, we also evaluated the antioxidant enzymes including SOD, CAT, HO-1, GPX, GR, and GST. The increased gene expression of SOD and HO-1 demonstrated the protective antioxidant mechanisms that are induced by PBMT. Thus, we can infer that the SOD and HO-1 gene expressions were augmented after PBMT as a compensatory mechanism that prevented a pulmonary tissue disease from the oxidative damage induced by FA. It is known that HO-1 is a rate-limiting enzyme in heme catabolism, degrading heme to free iron, biliverdin, and carbon monoxide. SOD in turn promotes the degradation of the superoxide anion in hydrogen peroxide and it is less reactive. These products exert a cytoprotective mechanism against oxidative stress [31]. On the other hand, no differences were observed in CAT levels.

Another important antioxidant source in the lung is glutathione, which is essential for a defensive response to oxidants and inflammatory agents, by repairing the oxidized and damaged molecules and helping to regulate a variety of cellular functions [32]. Our study has found that the activities of GST and GPX were increased by PBMT. As previously mentioned, these data can explain the reduced levels of H₂O₂, since GPX is a potent antioxidant against H₂O₂.

Here we have utilized an interesting model of lung disease induced by pollution. Moreover, several lung diseases, such as asthma, a chronic obstructive pulmonary disease, and lung fibrosis, have all been associated with oxidative stress [18, 19, 33] and in addition the pollution might aggravate these diseases. In this context, taking everything into account, our data has shown that PBMT might be as a promissory treatment for lung diseases mediated by oxidative stress. Additionally, this treatment is without side effects, it presents low costs, and it demonstrates a noninvasive therapy.

Competing Interests

The authors declare that there are no competing interests regarding the publication of this paper.

Acknowledgments

This study was sponsored by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). Adriana Lino-dos-Santos-Franco is a Research Fellow from FAPESP (2015/00830-9).

References

A. Manda-Handzlik and U. Demkow, “Neutrophils: the role of oxidative and nitrosative stress in health and disease,” Advances in Experimental Medicine and Biology, vol. 857, pp. 51–60, 2015.
View at: Publisher Site | Google Scholar
H. R. Griffiths, I. H. K. Dias, R. S. Willetts, and A. Devitt, “Redox regulation of protein damage in plasma,” Redox Biology, vol. 2, no. 1, pp. 430–435, 2014.
View at: Publisher Site | Google Scholar
H. L. Hsieh and C. M. Yang, “Role of redox signaling in neuroinflammation and neurodegenerative diseases,” BioMed Research International, vol. 2013, Article ID 484613, 18 pages, 2013.
View at: Publisher Site | Google Scholar
N. D. Betancourt-Martínez, J. Jiménez-Villarreal, P. Carranza-Rosales et al., “Sperm chromatin dispersion by formaldehyde in wistar rats,” Genetics and Molecular Research, vol. 14, no. 3, pp. 10816–10826, 2015.
View at: Publisher Site | Google Scholar
B. Silva Ibrahim, C. Miranda da Silva, É. D. Barioni et al., “Formaldehyde inhalation during pregnancy abolishes the development of acute innate inflammation in offspring,” Toxicology Letters, vol. 235, no. 2, pp. 147–154, 2015.
View at: Publisher Site | Google Scholar
H. Fukui, S. Endoh, M. Shichiri et al., “The induction of lipid peroxidation during the acute oxidative stress response induced by intratracheal instillation of fine crystalline silica particles in rats,” Toxicology and Industrial Health, 2014.
View at: Publisher Site | Google Scholar
M. Maiellaro, M. Correa-Costa, L. B. Vitoretti et al., “Exposure to low doses of formaldehyde during pregnancy suppresses the development of allergic lung inflammation in offspring,” Toxicology and Applied Pharmacology, vol. 278, no. 3, pp. 266–274, 2014.
View at: Publisher Site | Google Scholar
L. Forchhammer, S. Loft, M. Roursgaard et al., “Expression of adhesion molecules, monocyte interactions and oxidative stress in human endothelial cells exposed to wood smoke and diesel exhaust particulate matter,” Toxicology Letters, vol. 209, no. 2, pp. 121–128, 2012.
View at: Publisher Site | Google Scholar
A. Lino-dos-Santos-Franco, M. Correa-Costa, A. C. C. Dos Santos Durão et al., “Formaldehyde induces lung inflammation by an oxidant and antioxidant enzymes mediated mechanism in the lung tissue,” Toxicology Letters, vol. 207, no. 3, pp. 278–285, 2011.
View at: Publisher Site | Google Scholar
A. Lino-dos-Santos-Franco, H. V. Domingos, A. P. L. D. Oliveira et al., “Differential effects of formaldehyde exposure on the cell influx and vascular permeability in a rat model of allergic lung inflammation,” Toxicology Letters, vol. 197, no. 3, pp. 211–218, 2010.
View at: Publisher Site | Google Scholar
T. Salthammer, “Formaldehyde in the ambient atmosphere: from an indoor pollutant to an outdoor pollutant?” Angewandte Chemie—International Edition, vol. 52, no. 12, pp. 3320–3327, 2013.
View at: Publisher Site | Google Scholar
B. Amulic, C. Cazalet, G. L. Hayes, K. D. Metzler, and A. Zychlinsky, “Neutrophil function: from mechanisms to disease,” Annual Review of Immunology, vol. 30, pp. 459–489, 2012.
View at: Publisher Site | Google Scholar
J. A. Marwick, D. A. Dorward, C. D. Lucas et al., “Oxygen levels determine the ability of glucocorticoids to influence neutrophil survival in inflammatory environments,” Journal of Leukocyte Biology, vol. 94, no. 6, pp. 1285–1292, 2013.
View at: Publisher Site | Google Scholar
S. K. Biswas and I. Rahman, “Environmental toxicity, redox signaling and lung inflammation: the role of glutathione,” Molecular Aspects of Medicine, vol. 30, no. 1-2, pp. 60–76, 2009.
View at: Publisher Site | Google Scholar
V. L. Kinnula and J. D. Crapo, “Superoxide dismutases in the lung and human lung diseases,” American Journal of Respiratory and Critical Care Medicine, vol. 167, no. 12, pp. 1600–1619, 2003.
View at: Publisher Site | Google Scholar
R. Stocker, Y. Yamamoto, A. F. McDonagh, A. N. Glazer, and B. N. Ames, “Bilirubin is an antioxidant of possible physiological importance,” Science, vol. 235, no. 4792, pp. 1043–1046, 1987.
View at: Publisher Site | Google Scholar
H. Lee, J. R. Park, E. J. Kim et al., “Cigarette smoke-mediated oxidative stress induces apoptosis via the MAPKs/STAT1 pathway in mouse lung fibroblasts,” Toxicology letters, vol. 240, no. 1, pp. 140–148, 2016.
View at: Publisher Site | Google Scholar
T. A. Moore, K. K. Schmid, A. Anderson-Berry, and A. M. Berger, “Lung disease, oxidative stress, and oxygen requirements in preterm infants,” Biological Research For Nursing, 2015.
View at: Publisher Site | Google Scholar
R.-M. Liu and L. P. Desai, “Reciprocal regulation of TGF-β and reactive oxygen species: a perverse cycle for fibrosis,” Redox Biology, vol. 6, pp. 565–577, 2015.
View at: Publisher Site | Google Scholar
A. C.-H. Chen, P. R. Arany, Y.-Y. Huang et al., “Low-Level laser therapy activates NF-κB via generation of reactive oxygen species in mouse embryonic fibroblasts,” PLoS ONE, vol. 6, no. 7, Article ID e22453, 2011.
View at: Publisher Site | Google Scholar
F. K. Ibuki, A. Simões, J. Nicolau, and F. N. Nogueira, “Laser irradiation affects enzymatic antioxidant system of streptozotocin-induced diabetic rats,” Lasers in Medical Science, vol. 28, no. 3, pp. 911–918, 2013.
View at: Publisher Site | Google Scholar
F. M. de Lima, R. Albertini, Y. Dantas et al., “Low-level laser therapy restores the oxidative stress balance in acute lung injury induced by gut ischemia and reperfusion,” Photochemistry and Photobiology, vol. 89, no. 1, pp. 179–188, 2013.
View at: Publisher Site | Google Scholar
M. Migliario, P. Pittarella, M. Fanuli, M. Rizzi, and F. Renò, “Laser-induced osteoblast proliferation is mediated by ROS production,” Lasers in Medical Science, vol. 29, no. 4, pp. 1463–1467, 2014.
View at: Publisher Site | Google Scholar
A. Lino dos Santos Franco, H. V. Domingos, A. S. Damazo et al., “Reduced allergic lung inflammation in rats following formaldehyde exposure: long-term effects on multiple effector systems,” Toxicology, vol. 256, no. 3, pp. 157–163, 2009.
View at: Publisher Site | Google Scholar
C. Miranda da Silva, M. Peres Leal, R. A. Brochetti et al., “Low level laser therapy reduces the development of lung inflammation induced by formaldehyde exposure,” PLoS ONE, vol. 10, no. 11, Article ID e0142816, 2015.
View at: Publisher Site | Google Scholar
J. P. S. Peron, A. A. de Brito, M. Pelatti et al., “Human tubal-derived mesenchymal stromal cells associated with low level laser therapy significantly reduces cigarette smoke-induced COPD in C57BL/6 mice,” PLoS ONE, vol. 10, no. 8, Article ID e0136942, 2015.
View at: Publisher Site | Google Scholar
V. R. Silva, P. Marcondes, M. Silva et al., “Low-level laser therapy inhibits bronchoconstriction, Th2 inflammation and airway remodeling in allergic asthma,” Respiratory Physiology and Neurobiology, vol. 194, no. 1, pp. 37–48, 2014.
View at: Publisher Site | Google Scholar
F. M. de Lima, F. Aimbire, H. Miranda, R. D. P. Vieira, A. P. de Oliveira, and R. Albertini, “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,” Journal of Lasers in Medical Sciences, vol. 5, pp. 63–70, 2014.
View at: Google Scholar
I. I. Dolgushin, V. A. Markova, and O. A. Gizinger, “Monitoring of the effect of low-intensity laser radiation with constant pulse generation on neutrophil granulocytes in vitro,” Bulletin of Experimental Biology and Medicine, vol. 150, no. 2, pp. 222–224, 2010.
View at: Publisher Site | Google Scholar
A. Lino-dos-Santos-Franco, H. V. Domingos, A. P. Oliveira et al., “Differential effects of formaldehyde exposure on the cell influx and vascular permeability in a rat model of allergic lung inflammation,” Toxicology Letters, vol. 197, no. 3, pp. 211–218, 2010.
View at: Publisher Site | Google Scholar
N. G. Abraham and A. Kappas, “Pharmacological and clinical aspects of heme oxygenase,” Pharmacological Reviews, vol. 60, no. 1, pp. 79–127, 2008.
View at: Publisher Site | Google Scholar
K. Doreswamy, B. Shrilatha, T. Rajeshkumar, and Muralidhara, “Nickel-induced oxidative stress in testis of mice: evidence of DNA damage and genotoxic effects,” Journal of Andrology, vol. 25, no. 6, pp. 996–1003, 2004.
View at: Publisher Site | Google Scholar
H. Lee, J. R. Park Kim, E. J. Kim et al., “Cigarette smoke-mediated oxidative stress induces apoptosis via the MAPKs/STAT1 pathway in mouse lung fibroblasts,” Toxicology Letters, vol. 240, no. 1, pp. 140–148, 2015.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2016 Rodrigo Silva Macedo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

1461

Downloads

1074

Citations

Mediators of Inflammation

Photobiomodulation Therapy Decreases Oxidative Stress in the Lung Tissue after Formaldehyde Exposure: Role of Oxidant/Antioxidant Enzymes

Abstract

1. Introduction

2. Materials and Methods

2.1. Animals

2.2. Formaldehyde (FA) Exposure

2.3. Photobiomodulation Therapy

2.4. Experimental Groups

2.5. Quantification of Nitrites in the Supernatant of Bronchoalveolar Lavage (BAL)

2.6. Quantification of Hydrogen Peroxide in the Bronchoalveolar Lavage (BAL) Cell Suspension

2.7. Determination of Gene Expression of Oxidants and Antioxidants Enzymes in the Lung Tissue

2.8. Quantification of Enzymatic Activities of Glutathione Peroxidase, Reductase, and S-Transferase

2.9. Evaluation of Oxidative Burst in the Bronchoalveolar Lavage (BAL) Cells

2.10. Statistical Analysis

3. Results

3.1. Photobiomodulation Therapy Reduced the Generation of Hydrogen Peroxide (H2O2) and Nitrites (NO2) Induced by FA Exposure in the Lung

3.2. Photobiomodulation Therapy Increased the Oxidative Burst in the Lung

3.3. Photobiomodulation Therapy Reduced the Gene Expression of Nitric Oxide Synthase (iNOS and cNOS) and Cyclooxygenase (COX-2) Induced by FA Exposure in the Lung

3.4. Photobiomodulation Therapy Increased the Gene Expression of Superoxide Dismutase (SOD-1 and SOD-2) and Heme Oxygenase-1 (HO-1) without Changing Catalase after FA Exposure in the Lung

3.5. Photobiomodulation Therapy Increased the Activity of Glutathione S-Transferase (GST) and Peroxidase (GPX) without Changing Glutathione Reductase (GR) after FA Exposure in the Lung

4. Discussion

Competing Interests

Acknowledgments

References

Copyright

3.1. Photobiomodulation Therapy Reduced the Generation of Hydrogen Peroxide (H₂O₂) and Nitrites (NO₂) Induced by FA Exposure in the Lung