Skip to main content
SpringerLink
Log in

Effect of Photomodulation Therapy on Development of Oxidative Stress in Blood Leukocytes of Rats with Streptozocin-Induced Diabetes Mellitus

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract—Oxidative stress is among the main causes of developing severe complications in diabetes mellitus (DM). Existing pharmaceuticals, although efficient in reducing the blood glucose level, infrequently demonstrate antioxidant properties. On the other hand, there are many reliable reports about a broad range of biological activity exhibited by photobiomodulation therapy (PBMT). Its potential sugar-lowering and antioxidant action makes this type of therapy a promising option for the treatment of DM and its complications. The effect of PBMT on the state of the antioxidant defense system in blood leukocytes was investigated in rats with streprozocin-induced DM. This study has shown that the PBMT increased superoxide dismutase (SOD) activity in rats with DM and normalized the content of oxidative stress markers (thiobarbituric acid (TBA)-active products, oxidatively modified proteins, and protein glycation end products).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Elbe, H., Vardi, N., Esrefoglu, M., Ates, B., Yologlu, S., and Taskapan, C., Amelioration of strep-tozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats, Hum. Exp. Toxicol., 2015, vol. 34, no. 1, pp. 1–14.https://doi.org/10.1177/0960327114531995

  2. Evan, D.H., Abrahamse, H., Efficacy of three laser wavelengths for in vitro wound healing, Photodermat. Photoimm. Photomed., 2008, vol. 24 no. 4, pp. 199–210. https://doi.org/10.1111/j.1600-0781.2008.00362.x

  3. Chung, H., Dai, T., Sharma, S.K., Huang, Y.Y., Carroll, J.D., and Hamblin, M.R., The nuts and bolts of low-level laser (light) therapy, Ann. Biomed. Eng., 2012, vol. 40, no. 2, pp. 516–533. https://doi.org/10.1007/s10439-011-0454-7

    Article  PubMed  Google Scholar 

  4. Karmash, O.I., Liuta, M.Y., Yefimenko, N.V., Korobov, A.M., and Sybirna, N.O., The influence of low-level light radiation of red spectrum diapason on glycemic profile and physicochemical characteristics of rat’s erythrocytes in diabetes mellitus, Fiziol. Zh., 2018, vol. 64, no. 6, pp. 68– 76. https://doi.org/10.15407/fz64.06.068

    Article  Google Scholar 

  5. Denadai, A.S., Aydos, R.D., Silva, I.S., Olmedo, L., de Senna Cardoso, B.M., da Silva, B.A.K., and de Carvalho, P.T.C., Acute effects of low-level laser therapy (660 nm) on oxidative stress levels in diabetic rats with skin wounds, Exp. Ther. Oncol., 2017, vol. 11, no. 2, pp. 85–89.

    Google Scholar 

  6. Korolyuk, M.A., Ivanova, I.H., and Maiorova, I.H., Method for the determination of catalase activity, Lab. Delo, 1988, no. 1, pp. 16–19.

  7. Hnatush, A.R., Drel, V.R., Yalaneckyy, A.Ya., Mizin, V.I., Zagoruyko, V.A., Gerzhykova, V.G., and Sybirna, N.O., The antioxidant effect of natural polyphenolic complexes of grape wine in the rat retina under streptozotocin-induced diabetes mellitus., Biol. Stud., 2011, vol. 5, no. 2, pp. 61–72. https://doi.org/10.30970/sbi.0502.156

    Article  Google Scholar 

  8. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J., Protein measurement with the Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, no. 1, pp. 265–275.

    CAS  PubMed  Google Scholar 

  9. Meshchyshyn, I.F., Method for the determination of proteins oxidative modification, Bukov. Med. Visn., 1999, no. 1, pp. 196–205.

  10. Witko-Sarsat, V., Friedlander, M., Capeillere-Blandin, C., Nguyen-Khoa, T., Nguyen, A.T., Zingraff, J., Jungers, P., and Descamps-Latscha, B., Advanced oxidation protein products as a novel marker of oxidative stress in uremia, Kidney Int., 1996, vol. 49, no. 5, pp. 1304–1313. https://doi.org/10.1038/ki.1996.186

    Article  CAS  PubMed  Google Scholar 

  11. Kalousová, M., Skrha, J., and Zima, T., Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus, Physiol. Res., 2002, vol. 51, no. 6, pp. 597–604.

  12. Swathi, P. and Kilari, E., A review on methods of estimation of advanced glycation end products, World J. Pharm. Res., 2015, vol. 4, no. 1, pp. 689–699.

    Google Scholar 

  13. Timirbulatov, R.A. and Selesnev, E.I., Method for increasing the free-radical oxidation of lipid-containing blood components and its diagnostical meaning, Lab. Delo, 1981, no. 4, pp. 209–211.

  14. De Marchi, T., Leal Junior, E.C., Bortoli, C, Tomazoni, S.S., Lopes-Martins, R.A., and Salvador, M., Low-level laser therapy (LLLT) in human progressive-intensity running: effects on exercise performance, skeletal muscle status, and oxidative stress, Lasers Med. Sci., 2012, vol. 27, no. 1, pp. 231–236. https://doi.org/10.1007/s10103-011-0955-5

    Article  PubMed  Google Scholar 

  15. Guaraldo, S.A., Serra, A.J., Amadio, E.M., Antonio, E.L., Silva, F., Portes, LA., Tucci, P.J.F., Leal-Junior, E.C.P., and de Tarso Camillo de Carvalho, P., The effect of low-level laser therapy on oxidative stress and functional fitness in aged rats subjected to swimming: an aerobic exercise, Lasers Med. Sci., 2016, vol. 31, no. 5, pp. 833–840. https://doi.org/10.1007/s10103-016-1882-2

    Article  PubMed  Google Scholar 

  16. Dos Santos, S.A., Dos Santos Vieira, M.A., Simxes, M.C.B., Serra, A.J., Leal-Junior, E.C., and de Carvalho, P.T.C., Photobiomodulation therapy associated with treadmill training in the oxidative stress in a collagen-induced arthritis model, Lasers Med. Sci., 2017, vol. 32, no. 5, pp. 1071–1079. https://doi.org/10.1007/s10103-017-2209-7

    Article  PubMed  Google Scholar 

  17. Ibuki, F.K., Simxes, A., Nicolau, J., and Nogueira, F.N., Laser irradiation affects enzymatic antioxidant system of streptozotocin-induced diabetic rats, Lasers Med. Sci., 2013, vol. 28, no. 3, pp. 911–918. https://doi.org/10.1007/s10103-012-1173-5

    Article  PubMed  Google Scholar 

  18. Lim, J., Ali, Z.M., Sanders, R.A., Snyder, A.C., Eells, J.T., Henshel, D.S., Watkins, J.B., Effects of low-level light therapy on hepatic antioxidant defense in acute and chronic diabetic rats, Biochem. Mol. Toxicol., 2009, vol. 23, no. 1, pp. 1–8. https://doi.org/10.1002/jbt.20257

    Article  CAS  Google Scholar 

  19. Lim, J., Sanders, R.A., Snyder, A.C., Eells, J.T., Henshel, D.S., and Watkins, J.B., Effects of low-level light therapy on streptozotocin-induced diabetic kidney, J. Photochem. Photobiol. B., 2010, vol. 99, no. 2, pp. 105–110. https://doi.org/10.1016/j.jphoto-biol.2010.03.00

    Article  CAS  PubMed  Google Scholar 

  20. Hamblin, M.R. and Demidova, T.N., Mechanisms of low-level light therapy, Proc. SPIE, 2006, vol. 6140, no. 1, pp. 1–12. https://doi.org/10.1117/12.646294

    Article  Google Scholar 

  21. Karu, T., Is it time to consider photobiomodulation as a drug equivalent?, Photomed. Laser Surg., 2013, vol. 31, no. 5, pp. 189–191. https://doi.org/10.1089/pho.2013.3510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chen, C.H., Wang, C.Z., Wang, Y.H., Liao, W.T., Chen, Y.J., Kuo, C.H., Kuo, H.F., and Hung, C.H., Effects of low-level laser therapy on M1-related cytokine expression in monocytes via histone modification, Mediat. Inflamm., 2014, vol. 2014, pp. 1– 13. https://doi.org/10.1155/2014/625048

    Article  CAS  Google Scholar 

  23. Drel, V.R. and Sybirna, N., Protective effects of polyphenolics in red wine on diabetes associated oxidative/nitrative stress in streptozotocin-diabetic rats, Cell Biol. Int., 2010, vol. 34, no. 12, pp. 1147–1153. https://doi.org/10.1042/CBI20100201

    Article  CAS  PubMed  Google Scholar 

  24. Lima, P.L.V., Pereira, C.V., Nissanka, N., Arguello, T., Gavini, G., Maranduba, C.M.D.C., Diaz, F., and Moraes, C.T., Photobiomodulation enhancement of cell proliferation at 660 nm does not require cytochrome c oxidase, J. Photochem. Photobiol. B, 2019, vol. 194, pp. 71–75. https://doi.org/10.1016/j.jphoto-biol.2019.03.015

    Article  CAS  PubMed  Google Scholar 

  25. Amaroli, A., Ferrando, S., and Benedicenti, S., Photobiomodulation affects key cellular pathways of all life-forms: considerations on old and new laser light targets and the calcium issue, Photochem. Photobiol., 2019, vol. 95, no. 1, pp. 455–459. https://doi.org/10.1111/php.13032

    Article  CAS  PubMed  Google Scholar 

  26. Martin, K.R. and Barrett, J.C., Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity, Hum. Exp. Toxicol., 2002, vol. 21, no. 2, pp. 71–75. https://doi.org/10.1191/0960327102ht213oa

    Article  CAS  PubMed  Google Scholar 

  27. Sperandio, F.F., Giudice, F.S., Corria, L., Pinto, D.S. Jr., Hamblin, M.R., and de Sousa, S.C, Low-level laser therapy can produce increased aggressiveness of dysplastic and oral cancer cell lines by modulation of Akt/mTOR signaling pathway, J. Biophotonics, 2013, vol. 6, no. 10, pp. 839–847. https://doi.org/10.1002/jbio.201300015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Batinic-Haberle, I., Tovmasyan, A., Roberts, E.R., Vujaskovic, Z., Leong, K.W., and Spasojevic, I., SOD therapeutics: latest insights into their structure–activity relationships and impact on the cellular redox-based signaling pathways, Antioxid. Red. Signal., 2014, vol. 20, no. 15, pp. 2372–415. https://doi.org/10.1089/ars.2012.5147

    Article  CAS  Google Scholar 

  29. Ellis, E.M., Reactive carbonyls and oxidative stress: potential for therapeutic intervention, Pharmacol. Ther., 2007, vol. 115, no. 1, pp. 13–24. https://doi.org/10.1016/j.pharmthera.2007.03.015

    Article  CAS  PubMed  Google Scholar 

  30. Qian, W., Zhao-Ming, Z., Ying, P., Ji-Huan, Z., Shuai, Z., Si-Yuan, Z., and Jian-Ting, C., Advanced oxidation protein products as a novel marker of oxidative stress in postmenopausal osteoporosis, Med. Sci. Monit., 2015, vol. 21, pp. 2428– 2432. https://doi.org/10.12659/MSM.894347

    Article  Google Scholar 

  31. Bochi, G.V., Torbitz, V.D., de Campos, L.P., Sangoi, M.B., Fernandes, N.F., Gomes, P., Moretto, M.B., Barbisan, F., da Cruz, I.B., and Moresco, R.N., In vitro oxidation of collagen promotes the formation of advanced oxidation protein products and the activation of human neutrophils, Inflammation, 2016, vol. 39, no. 2, pp. 916–927. https://doi.org/10.1007/s10753-016-0325-3

    Article  CAS  PubMed  Google Scholar 

  32. Merhi, Z., Kandaraki, E.A., and Diamanti-Kandarakis, E., Implications and future perspectives of AGEs in PCOS pathophysiology, Trends Endocrinol. Metab., 2019, vol. 30, no. 3, pp. 150–162. https://doi.org/10.1016/j.tem.2019.01.005

    Article  CAS  PubMed  Google Scholar 

  33. Deluyker, D., Evens, L., and Bito, V., Advanced glycation end products (AGEs) and cardiovascular dysfunction: focus on high molecular weight AGEs, Amino Acids, 2017, vol. 49, no. 9, pp. 1535–1541. https://doi.org/10.1007/s00726-017-2464-8

    Article  CAS  PubMed  Google Scholar 

  34. Huang, L., Jiang, X., Gong, L., Xing, D., Photoactivation of Akt1/GSK3β isoform-specific signaling axis promotes pancreatic β-cell regeneration, J. Cell Biochem., 2015, vol. 116, no. 8, pp. 1741–1754. https://doi.org/10.1002/jcb.25133

    Article  CAS  PubMed  Google Scholar 

  35. Vrhovac, I., Breljak, D., and Sabolic, I., Glucose transporters in the mammalian blood cells, Periodic. Biologor., 2014, vol. 116, no. 2, pp. 131–138.

    Google Scholar 

  36. Kipmen-Korgun, D., Bilmen-Sarikcioglu, S., Altunbas, H., Demir, R., and Korgun, E.T., Type-2 diabetes down-regulates glucose transporter proteins and genes of the human blood leukocytes, Scand. J. Clin. Lab. Invest., 2009, vol. 69, no. 3, pp. 350–358. https://doi.org/10.1080/00365510802632163

    Article  CAS  PubMed  Google Scholar 

  37. Simpson, I.A., Dwyer, D., Malide, D., Moley, K.H., Travis, A., and Vannucci, S.J., The facilitative glucose transporter GLUT3: 20 years of distinction, Am. J. Physiol. Endocrinol. Metab., 2008, vol. 295, no. 2, pp. 242–253. https://doi.org/10.1152/ajpendo. 90388.2008

  38. Ueda-Wakagi, M., Hayashibara, K., Nagano, T., Ikeda, M., Yuan, S., Ueda, S., Shirai, Y., Yoshida, K.I., and Ashida, H., Epigallocatechin gallate induces GLUT4 translocation in skeletal muscle through both PI3K- and AMPK-dependent pathways, Food Funct., 2018, vol. 9, no. 8, pp. 4223–4233. https://doi.org/10.1039/C8FO00807H

    Article  CAS  PubMed  Google Scholar 

  39. Krook, A., Wallberg-Henriksson, H., and Zierath, J.R., Sending the signal: molecular mechanisms regulating glucose uptake, Med. Sci. Sports Exerc., 2004, vol. 36, no. 7, pp. 1212–1217. https://doi.org/10.1249/01.MSS.0000132387.25853.3B

    Article  CAS  PubMed  Google Scholar 

  40. Thomas, M.C., Forbes, J.M., and Cooper, M.E., Advanced glycation end products and diabetic nephropathy, Am. J. Ther., 2005, vol. 12, no. 6, pp. 562–572. https://doi.org/10.1097/01.ASN.00000-77413.41276.17

    Article  PubMed  Google Scholar 

  41. Dzydzan, O., Bila, I., Kucharska, A.Z., Brodyak, I., and Sybirna, N., Antidiabetic effects of extracts of red and yellow fruits of cornelian cherries (Cornus mas L.) on rats with streptozotocin-induced diabetes mellitus, Food Funct., 2019, pp. 1–14. https://doi.org/10.1039/C9FO00515C

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Ivan Franko Lviv National University, Lviv, Ukraine

    O. I. Karmash, M. Ya. Liuta & N. O. Sybirna

  2. Laboratory of Quantum Biology and Quantum Medicine, Karazin Kharkiv National University, Kharkiv, Ukraine

    A. M. Korobov

Authors
  1. O. I. Karmash
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Ya. Liuta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Korobov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. O. Sybirna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. I. Karmash.

Ethics declarations

FUNDING

This study did not receive any particular grant from any financial organizations in the state, commercial, or noncommercial sectors.

COMPLIANCE WITH ETHICAL STANDARDS

Conflict of interest. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All our studies involving the use of animals were performed with the observation of the recommendations of the General Ethical Principles of Animal Experiments approved by the First National Congress for Bioethics (Kyiv, 2001), which corresponds to the provisions of the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (Strasbourg, 1986).

Additional information

Translated by N. Tarasyuk

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karmash, O.I., Liuta, M.Y., Korobov, A.M. et al. Effect of Photomodulation Therapy on Development of Oxidative Stress in Blood Leukocytes of Rats with Streptozocin-Induced Diabetes Mellitus. Cytol. Genet. 54, 456–464 (2020). https://doi.org/10.3103/S0095452720050114

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452720050114

Search

Navigation