Skip to main content
Erschienen in: Lasers in Medical Science 3/2013

01.05.2013 | Original Article

Laser irradiation affects enzymatic antioxidant system of streptozotocin-induced diabetic rats

verfasst von: Flavia Kazue Ibuki, Alyne Simões, José Nicolau, Fernando Neves Nogueira

Erschienen in: Lasers in Medical Science | Ausgabe 3/2013

Einloggen, um Zugang zu erhalten

Abstract

The aim of the present study was to analyze the effect of low-power laser irradiation in the antioxidant enzymatic system of submandibular (SMG) and parotid (PG) salivary glands of streptozotocin-induced diabetic rats. The animals were randomly divided into six groups: three diabetic groups (D0, D5, and D20) and three non-diabetic groups (C0, C5, and C20), according to laser dose received (0, 5, and 20 J/cm2, respectively). Areas of approximately 1 cm2 were demarcated in the salivary glands (each parotid and both submandibular glands) and after irradiated according to Simões et.al. (Lasers Med Sci 24:202–208, 2009). A diode laser (660 nm/100 mW) was used, with laser beam spot of 0.0177 cm2. The group treated with 5 J/cm2 laser dose was subjected to irradiation for 1 min and 4 s (total irradiation time) and the group treated with 20 J/cm2 laser dose was subjected to irradiation for 4 min and 16 s. Twenty-four hours after irradiation the animals were euthanized and the salivary glands were removed for biochemical analysis. The total antioxidant values (TA), the activity of superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase enzymes were determined. SOD and CAT activities, as well as TA were higher in SMG of irradiated diabetic rats. However, in SMG of non-diabetic rats, laser irradiation decreased TA values and led to an increase in the CAT activity. In addition, there was a decrease in the activity of CAT in PG of diabetic and non-diabetic animals after laser irradiation. According to the results of the present study, low-power laser irradiation can affect the enzymatic antioxidant system of salivary glands of streptozotocin-induced diabetic rats.
Literatur
1.
Zurück zum Zitat Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 2003 26 Suppl 1:S5–20 Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 2003 26 Suppl 1:S5–20
2.
Zurück zum Zitat Darnell JA, Saunders MJ (1990) Oral manifestations of the diabetic patient. Tex Dent J 107(2):23–27PubMed Darnell JA, Saunders MJ (1990) Oral manifestations of the diabetic patient. Tex Dent J 107(2):23–27PubMed
3.
Zurück zum Zitat Loe H (1993) Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 16(1):329–334PubMed Loe H (1993) Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 16(1):329–334PubMed
4.
Zurück zum Zitat Ship JA (2003) Diabetes and oral health: an overview. J Am Dent Assoc 134 Spec No:4 S–10S Ship JA (2003) Diabetes and oral health: an overview. J Am Dent Assoc 134 Spec No:4 S–10S
5.
Zurück zum Zitat Mata AD, Marques D, Rocha S, Francisco H, Santos C, Mesquita MF et al (2004) Effects of diabetes mellitus on salivary secretion and its composition in the human. Mol Cell Biochem 261(1–2):137–142PubMedCrossRef Mata AD, Marques D, Rocha S, Francisco H, Santos C, Mesquita MF et al (2004) Effects of diabetes mellitus on salivary secretion and its composition in the human. Mol Cell Biochem 261(1–2):137–142PubMedCrossRef
6.
Zurück zum Zitat Moore PA, Guggenheimer J, Etzel KR, Weyant RJ, Orchard T (2001) Type 1 diabetes mellitus, xerostomia, and salivary flow rates. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92(3):281–291PubMedCrossRef Moore PA, Guggenheimer J, Etzel KR, Weyant RJ, Orchard T (2001) Type 1 diabetes mellitus, xerostomia, and salivary flow rates. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92(3):281–291PubMedCrossRef
7.
Zurück zum Zitat Dodds MW, Yeh CK, Johnson DA (2000) Salivary alterations in type 2 (non-insulin-dependent) diabetes mellitus and hypertension. Community Dent Oral Epidemiol 28(5):373–381PubMedCrossRef Dodds MW, Yeh CK, Johnson DA (2000) Salivary alterations in type 2 (non-insulin-dependent) diabetes mellitus and hypertension. Community Dent Oral Epidemiol 28(5):373–381PubMedCrossRef
8.
Zurück zum Zitat Yoon MS, Jankowski V, Montag S, Zidek W, Henning L, Schluter H et al (2004) Characterisation of advanced glycation endproducts in saliva from patients with diabetes mellitus. Biochem Biophys Res Commun 323(2):377–381PubMedCrossRef Yoon MS, Jankowski V, Montag S, Zidek W, Henning L, Schluter H et al (2004) Characterisation of advanced glycation endproducts in saliva from patients with diabetes mellitus. Biochem Biophys Res Commun 323(2):377–381PubMedCrossRef
9.
Zurück zum Zitat Sandberg GE, Sundberg HE, Fjellstrom CA, Wikblad KF (2000) Type 2 diabetes and oral health: a comparison between diabetic and non-diabetic subjects. Diabetes Res Clin Pract 50(1):27–34PubMedCrossRef Sandberg GE, Sundberg HE, Fjellstrom CA, Wikblad KF (2000) Type 2 diabetes and oral health: a comparison between diabetic and non-diabetic subjects. Diabetes Res Clin Pract 50(1):27–34PubMedCrossRef
10.
Zurück zum Zitat Ben-Aryeh H, Serouya R, Kanter Y, Szargel R, Laufer D (1993) Oral health and salivary composition in diabetic patients. J Diabetes Complications 7(1):57–62PubMedCrossRef Ben-Aryeh H, Serouya R, Kanter Y, Szargel R, Laufer D (1993) Oral health and salivary composition in diabetic patients. J Diabetes Complications 7(1):57–62PubMedCrossRef
12.
Zurück zum Zitat Nogueira FN, Carvalho AM, Yamaguti PM, Nicolau J (2005) Antioxidant parameters and lipid peroxidation in salivary glands of streptozotocin-induced diabetic rats. Clin Chim Acta 353(1–2):133–139PubMedCrossRef Nogueira FN, Carvalho AM, Yamaguti PM, Nicolau J (2005) Antioxidant parameters and lipid peroxidation in salivary glands of streptozotocin-induced diabetic rats. Clin Chim Acta 353(1–2):133–139PubMedCrossRef
13.
Zurück zum Zitat Turner S, Zettler G, Arcos ML, Cremaschi G, Davicino R, Anesini C (2011) Effect of streptozotocin on reactive oxygen species and antioxidant enzyme secretion in rat submandibulary glands: a direct and an indirect relationship between enzyme activation and expression. Eur J Pharmacol 659(2–3):281–288PubMedCrossRef Turner S, Zettler G, Arcos ML, Cremaschi G, Davicino R, Anesini C (2011) Effect of streptozotocin on reactive oxygen species and antioxidant enzyme secretion in rat submandibulary glands: a direct and an indirect relationship between enzyme activation and expression. Eur J Pharmacol 659(2–3):281–288PubMedCrossRef
14.
Zurück zum Zitat Halliwell B, Gutteridge, JMC, editor. Free radicals in biology and medicine. 4th edition ed. Oxford, New York: Oxford University Press 2007 Halliwell B, Gutteridge, JMC, editor. Free radicals in biology and medicine. 4th edition ed. Oxford, New York: Oxford University Press 2007
15.
Zurück zum Zitat Ibuki FK, Simoes A, Nogueira FN (2010) Antioxidant enzymatic defense in salivary glands of streptozotocin-induced diabetic rats: a temporal study. Cell Biochem Funct 28(6):503–508PubMedCrossRef Ibuki FK, Simoes A, Nogueira FN (2010) Antioxidant enzymatic defense in salivary glands of streptozotocin-induced diabetic rats: a temporal study. Cell Biochem Funct 28(6):503–508PubMedCrossRef
16.
Zurück zum Zitat Nicolau J, de Matos JA, de Souza DN, Neves LB, Lopes AC (2005) Altered glycogen metabolism in the submandibular and parotid salivary glands of rats with streptozotocin-induced diabetes. J Oral Sci 47(2):111–116PubMedCrossRef Nicolau J, de Matos JA, de Souza DN, Neves LB, Lopes AC (2005) Altered glycogen metabolism in the submandibular and parotid salivary glands of rats with streptozotocin-induced diabetes. J Oral Sci 47(2):111–116PubMedCrossRef
17.
Zurück zum Zitat Nicolau J, de Souza DN, Carrilho M (2009) Increased glycated calmodulin in the submandibular salivary glands of streptozotocin-induced diabetic rats. Cell Biochem Funct 27(4):193–198PubMedCrossRef Nicolau J, de Souza DN, Carrilho M (2009) Increased glycated calmodulin in the submandibular salivary glands of streptozotocin-induced diabetic rats. Cell Biochem Funct 27(4):193–198PubMedCrossRef
18.
Zurück zum Zitat Nicolau J, De Souza DN, Simoes A (2009) Alteration of Ca(2+)-ATPase activity in the homogenate, plasma membrane and microsomes of the salivary glands of streptozotocin-induced diabetic rats. Cell Biochem Funct 27(3):128–134PubMedCrossRef Nicolau J, De Souza DN, Simoes A (2009) Alteration of Ca(2+)-ATPase activity in the homogenate, plasma membrane and microsomes of the salivary glands of streptozotocin-induced diabetic rats. Cell Biochem Funct 27(3):128–134PubMedCrossRef
19.
Zurück zum Zitat Simoes A, Ganzerla E, Yamaguti PM, de Paula Eduardo C, Nicolau J (2009) Effect of diode laser on enzymatic activity of parotid glands of diabetic rats. Lasers Med Sci 24(4):591–596PubMedCrossRef Simoes A, Ganzerla E, Yamaguti PM, de Paula Eduardo C, Nicolau J (2009) Effect of diode laser on enzymatic activity of parotid glands of diabetic rats. Lasers Med Sci 24(4):591–596PubMedCrossRef
20.
Zurück zum Zitat Simoes A, Nicolau J, de Souza DN, Ferreira LS, de Paula Eduardo C, Apel C et al (2008) Effect of defocused infrared diode laser on salivary flow rate and some salivary parameters of rats. Clin Oral Investig 12(1):25–30PubMedCrossRef Simoes A, Nicolau J, de Souza DN, Ferreira LS, de Paula Eduardo C, Apel C et al (2008) Effect of defocused infrared diode laser on salivary flow rate and some salivary parameters of rats. Clin Oral Investig 12(1):25–30PubMedCrossRef
21.
Zurück zum Zitat Simoes A (2010) Nogueira FN, de Paula Eduardo C. Nicolau J Diode laser decreases the activity of catalase on submandibular glands of diabetic rats Photomed Laser Surg 28(1):91–95CrossRef Simoes A (2010) Nogueira FN, de Paula Eduardo C. Nicolau J Diode laser decreases the activity of catalase on submandibular glands of diabetic rats Photomed Laser Surg 28(1):91–95CrossRef
22.
Zurück zum Zitat Simoes A, Platero MD, Campos L, Aranha AC, Eduardo Cde P, Nicolau J (2009) Laser as a therapy for dry mouth symptoms in a patient with Sjogren's syndrome: a case report. Spec Care Dent 29(3):134–137CrossRef Simoes A, Platero MD, Campos L, Aranha AC, Eduardo Cde P, Nicolau J (2009) Laser as a therapy for dry mouth symptoms in a patient with Sjogren's syndrome: a case report. Spec Care Dent 29(3):134–137CrossRef
23.
Zurück zum Zitat Simoes A, Siqueira WL, Lamers ML, Santos MF, Eduardo Cde P, Nicolau J (2009) Laser phototherapy effect on protein metabolism parameters of rat salivary glands. Lasers Med Sci 24(2):202–208PubMedCrossRef Simoes A, Siqueira WL, Lamers ML, Santos MF, Eduardo Cde P, Nicolau J (2009) Laser phototherapy effect on protein metabolism parameters of rat salivary glands. Lasers Med Sci 24(2):202–208PubMedCrossRef
24.
Zurück zum Zitat Fahimipour F, Mahdian M, Houshmand B, Asnaashari M, Sadrabadi AN, Farashah SE, et al (2012) The effect of He–Ne and Ga–Al–As laser light on the healing of hard palate mucosa of mice. Lasers Med Sci Fahimipour F, Mahdian M, Houshmand B, Asnaashari M, Sadrabadi AN, Farashah SE, et al (2012) The effect of He–Ne and Ga–Al–As laser light on the healing of hard palate mucosa of mice. Lasers Med Sci
25.
Zurück zum Zitat Nouruzian M, Alidoust M, Bayat M, Akbari M (2012) Effect of low-level laser therapy on healing of tenotomized Achilles tendon in streptozotocin-induced diabetic rats. Lasers Med Sci Nouruzian M, Alidoust M, Bayat M, Akbari M (2012) Effect of low-level laser therapy on healing of tenotomized Achilles tendon in streptozotocin-induced diabetic rats. Lasers Med Sci
26.
Zurück zum Zitat Tunér J, Hode L, editor. Low level laser therapy—clinical practice and scientific background. Prima Book. Grängesberg, Sweden 1999 Tunér J, Hode L, editor. Low level laser therapy—clinical practice and scientific background. Prima Book. Grängesberg, Sweden 1999
27.
Zurück zum Zitat Kats AG, Belostotskaia IM, Malomud ZP, Makarova LG (1985) Remote results of the complex treatment of chronic sialadenitis using the helium–neon laser. Vestn Khir Im I I Grek 135(10):39–42PubMed Kats AG, Belostotskaia IM, Malomud ZP, Makarova LG (1985) Remote results of the complex treatment of chronic sialadenitis using the helium–neon laser. Vestn Khir Im I I Grek 135(10):39–42PubMed
28.
Zurück zum Zitat Jung KaH W (1996) Developmental changes of antioxidants enzymes in kidney and liver from rats. Free Radic Biol Med 20(4):613–617CrossRef Jung KaH W (1996) Developmental changes of antioxidants enzymes in kidney and liver from rats. Free Radic Biol Med 20(4):613–617CrossRef
29.
Zurück zum Zitat Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci (Lond) 84(4):407–412 Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci (Lond) 84(4):407–412
30.
Zurück zum Zitat Suttle NF, McMurray CH (1983) Use of erythrocyte copper:zinc superoxide dismutase activity and hair or fleece copper concentrations in the diagnosis of hypocuprosis in ruminants. Res Vet Sci 35(1):47–52PubMed Suttle NF, McMurray CH (1983) Use of erythrocyte copper:zinc superoxide dismutase activity and hair or fleece copper concentrations in the diagnosis of hypocuprosis in ruminants. Res Vet Sci 35(1):47–52PubMed
31.
Zurück zum Zitat Woolliams JA, Wiener G, Anderson PH, McMurray CH (1983) Variation in the activities of glutathione peroxidase and superoxide dismutase and in the concentration of copper in the blood in various breed crosses of sheep. Res Vet Sci 34(3):253–256PubMed Woolliams JA, Wiener G, Anderson PH, McMurray CH (1983) Variation in the activities of glutathione peroxidase and superoxide dismutase and in the concentration of copper in the blood in various breed crosses of sheep. Res Vet Sci 34(3):253–256PubMed
32.
Zurück zum Zitat Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169PubMed Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169PubMed
33.
Zurück zum Zitat Aebi H, editor. Catalase in vitro 1984 Aebi H, editor. Catalase in vitro 1984
34.
Zurück zum Zitat Simoes A, de Oliveira E, Campos L, Nicolau J (2009) Ionic and histological studies of salivary glands in rats with diabetes and their glycemic state after laser irradiation. Photomed Laser Surg 27(6):877–883PubMedCrossRef Simoes A, de Oliveira E, Campos L, Nicolau J (2009) Ionic and histological studies of salivary glands in rats with diabetes and their glycemic state after laser irradiation. Photomed Laser Surg 27(6):877–883PubMedCrossRef
35.
Zurück zum Zitat Patel DG, Begum N, Smith PH (1986) Insulin-like material in parotid and submaxillary salivary glands of normal and diabetic adult male mice. Diabetes 35(7):753–758PubMedCrossRef Patel DG, Begum N, Smith PH (1986) Insulin-like material in parotid and submaxillary salivary glands of normal and diabetic adult male mice. Diabetes 35(7):753–758PubMedCrossRef
36.
Zurück zum Zitat Kerr M, Lee A, Wang PL, Purushotham KR, Chegini N, Yamamoto H et al (1995) Detection of insulin and insulin-like growth factors I and II in saliva and potential synthesis in the salivary glands of mice. Effects of type 1 diabetes mellitus. Biochem Pharmacol 49(10):1521–1531PubMedCrossRef Kerr M, Lee A, Wang PL, Purushotham KR, Chegini N, Yamamoto H et al (1995) Detection of insulin and insulin-like growth factors I and II in saliva and potential synthesis in the salivary glands of mice. Effects of type 1 diabetes mellitus. Biochem Pharmacol 49(10):1521–1531PubMedCrossRef
37.
Zurück zum Zitat Anderson LC (1983) Effects of alloxan diabetes and insulin in vivo on rat parotid gland. Am J Physiol 245(3):G431–G437PubMed Anderson LC (1983) Effects of alloxan diabetes and insulin in vivo on rat parotid gland. Am J Physiol 245(3):G431–G437PubMed
38.
Zurück zum Zitat Wang D, Yuan Z, Inoue N, Cho G, Shono M, Ishikawa Y (2011) Abnormal subcellular localization of AQP5 and downregulated AQP5 protein in parotid glands of streptozotocin-induced diabetic rats. Biochim Biophys Acta 1810(5):543–554PubMedCrossRef Wang D, Yuan Z, Inoue N, Cho G, Shono M, Ishikawa Y (2011) Abnormal subcellular localization of AQP5 and downregulated AQP5 protein in parotid glands of streptozotocin-induced diabetic rats. Biochim Biophys Acta 1810(5):543–554PubMedCrossRef
39.
Zurück zum Zitat Mahay S, Adeghate E, Lindley MZ, Rolph CE, Singh J (2004) Streptozotocin-induced type 1 diabetes mellitus alters the morphology, secretory function and acyl lipid contents in the isolated rat parotid salivary gland. Mol Cell Biochem 261(1–2):175–181PubMedCrossRef Mahay S, Adeghate E, Lindley MZ, Rolph CE, Singh J (2004) Streptozotocin-induced type 1 diabetes mellitus alters the morphology, secretory function and acyl lipid contents in the isolated rat parotid salivary gland. Mol Cell Biochem 261(1–2):175–181PubMedCrossRef
40.
Zurück zum Zitat Watanabe M, Yamagishi-Wang H, Kawaguchi M (2001) Lowered susceptibility of muscarinic receptor involved in salivary secretion of streptozotocin-induced diabetic rats. Jpn J Pharmacol 87(2):117–124PubMedCrossRef Watanabe M, Yamagishi-Wang H, Kawaguchi M (2001) Lowered susceptibility of muscarinic receptor involved in salivary secretion of streptozotocin-induced diabetic rats. Jpn J Pharmacol 87(2):117–124PubMedCrossRef
41.
Zurück zum Zitat Kakkar R, Kalra J, Mantha SV, Prasad K (1995) Lipid peroxidation and activity of antioxidant enzymes in diabetic rats. Mol Cell Biochem 151(2):113–119PubMedCrossRef Kakkar R, Kalra J, Mantha SV, Prasad K (1995) Lipid peroxidation and activity of antioxidant enzymes in diabetic rats. Mol Cell Biochem 151(2):113–119PubMedCrossRef
42.
Zurück zum Zitat Gumieniczek A, Hopkala H, Wojtowicz Z, Nieradko M (2001) Differences in antioxidant status in skeletal muscle tissue in experimental diabetes. Clin Chim Acta 314(1–2):39–45PubMedCrossRef Gumieniczek A, Hopkala H, Wojtowicz Z, Nieradko M (2001) Differences in antioxidant status in skeletal muscle tissue in experimental diabetes. Clin Chim Acta 314(1–2):39–45PubMedCrossRef
43.
Zurück zum Zitat Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112PubMedCrossRef Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112PubMedCrossRef
44.
Zurück zum Zitat Onizawa K, Muramatsu T, Matsuki M, Ohta K, Matsuzaka K, Oda Y et al (2009) Low-level (gallium–aluminum–arsenide) laser irradiation of Par-C10 cells and acinar cells of rat parotid gland. Laser Med Sci 24(2):155–161CrossRef Onizawa K, Muramatsu T, Matsuki M, Ohta K, Matsuzaka K, Oda Y et al (2009) Low-level (gallium–aluminum–arsenide) laser irradiation of Par-C10 cells and acinar cells of rat parotid gland. Laser Med Sci 24(2):155–161CrossRef
45.
Zurück zum Zitat Tuner J, Hode L (1998) It's all in the parameters: a critical analysis of some well-known negative studies on low-level laser therapy. J Clin Laser Med Surg 16(5):245–248PubMed Tuner J, Hode L (1998) It's all in the parameters: a critical analysis of some well-known negative studies on low-level laser therapy. J Clin Laser Med Surg 16(5):245–248PubMed
46.
47.
Zurück zum Zitat Nicolau J, Sassaki KT (1976) Metabolism of carbohydrate in the major salivary glands of rats. Arch Oral Biol 21(11):659–661PubMedCrossRef Nicolau J, Sassaki KT (1976) Metabolism of carbohydrate in the major salivary glands of rats. Arch Oral Biol 21(11):659–661PubMedCrossRef
48.
Zurück zum Zitat Schenkels LC, Veerman EC, Nieuw Amerongen AV (1995) Biochemical composition of human saliva in relation to other mucosal fluids. Crit Rev Oral Biol Med 6(2):161–175PubMedCrossRef Schenkels LC, Veerman EC, Nieuw Amerongen AV (1995) Biochemical composition of human saliva in relation to other mucosal fluids. Crit Rev Oral Biol Med 6(2):161–175PubMedCrossRef
49.
Zurück zum Zitat Kirkman HN, Gaetani GF (2007) Mammalian catalase: a venerable enzyme with new mysteries. Trends Biochem Sci 32(1):44–50PubMedCrossRef Kirkman HN, Gaetani GF (2007) Mammalian catalase: a venerable enzyme with new mysteries. Trends Biochem Sci 32(1):44–50PubMedCrossRef
50.
Zurück zum Zitat Artyukhov VG, Basharina OV, Pantak AA, Sveklo LS (2000) Effect of helium–neon laser on activity and optical properties of catalase. Bull Exp Biol Med 129(6):537–540PubMedCrossRef Artyukhov VG, Basharina OV, Pantak AA, Sveklo LS (2000) Effect of helium–neon laser on activity and optical properties of catalase. Bull Exp Biol Med 129(6):537–540PubMedCrossRef
Metadaten
Titel
Laser irradiation affects enzymatic antioxidant system of streptozotocin-induced diabetic rats
verfasst von
Flavia Kazue Ibuki
Alyne Simões
José Nicolau
Fernando Neves Nogueira
Publikationsdatum
01.05.2013
Verlag
Springer-Verlag
Erschienen in
Lasers in Medical Science / Ausgabe 3/2013
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-012-1173-5

Weitere Artikel der Ausgabe 3/2013

Lasers in Medical Science 3/2013 Zur Ausgabe