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Research Article

Laser Mediated Production of Reactive Oxygen and Nitrogen Species; Implications for Therapy

Y.G. Kim Biological Science, Natural Sciences, Chosun University, Kwangju 501-759, South Korea
Pages 1243-1250 | Published online: 07 Jul 2009

  • Tope, W.D. and Kageyama, N. (2001) "Hot KTP-laser treatment of facial angiofibromata", Lasers Surg. Med. 29, 78-81.
  • Trelles, M.A., Mordon, S., Benitez, V. and Levy, J.L. (1999) "Er:yag laser resurfacing using combined ablation and coagulation modes'", Dermatol. Surg. 27, 727-734.
  • Forney, R. and Mauro, T. (1999) "Using lasers in diabetic would healing", Diabetes Technol. Ther. 1, 189-192.
  • Ratkay-Traub, L, Hopp, B., Bor, Z., Dux, L., Becker, D.L., and Krenacs, T. (2001) "Regeneration of rabbit cornea following excimer laser photorefractive keratectomy: a study on gap junctions, epithelial junctions and epidermal growth factor receptor expression in correlation with cell proliferation", Exp. Eye Res. 73, 291-302.
  • Greeley, A. (2000) "Cosmetic laser surgery. A high-tech weapon in the fight against aging", FDA Consum. 34, 34-37.
  • Korenfield, MS. (2001) "Maximizing surgeon safety during excimer laser photorefractive procedures", Am. J. Ophthalmol. 132, 209-291.
  • Chichuk, T.V., Strashkevich, LA. and Klebanov, G.L (1999) "Free radical mechanisms of low-intensive laser radiation", Vestn. Ross. Akad. Med. Nauk. 2, 27-32.
  • Cabiscol, E., Tamarit, E.J. and Ros, J. (2000) "Oxidative stress in bacteria and protein damage by reactive oxygen species", Int. Microbiol. 3, 3-8.
  • Brozmanova, J., Dudas, A. and Henriques, J. A. (2001) "Repair of exudative DNA damage--an important factor reducing cancer risk", Néoplasme 48, 85-93.
  • Halliwell, B. and Gutteridge, J.M.C. (1999) Free Radicals in Biology and Medicine, 3rd Ed. (Oxford University Press, Oxford), pp 1-936.
  • Klebanov, G.I., Strashkevich, LA., Chichuk, T.V., Modestova, T.M. and Vladimirov, Y.A. (1998) "Effects of endogenous photosensitizers on the laser-induced priming of leucocytes", Membr. Cell Biol. 12, 339-354
  • Brocdo, M, Delia Rovere, R, Granata, A., Wanderlingh, U., Zirilli, A., Tanzariello, A., Pirrone, G. and Brocdo, G. (1998) "Free radical erythrocyte damage in tumoral disease assessed by He-Ne laser and optical microscope through "Heinz Bodies" method", Anticancer Res. 18, 1075-1078.
  • Grossman, N., Schneid, N., Reuveni, H., Halevy, S. and Lubart, R. (1998) "780nm low power diode laser irradiation stimulates proliferation of keratinocyte cultures: involvement of reactive oxygen species", Lasers Surg. Med. 22, 212-218.
  • Jackson, S.N and Murray, K.K. (2001) "Infrared matrix-assisted laser desorption/ionization of polycyclic aromatic hydrocarbons with a sulfolane matrix", Rapid Commun. Mass Spectrom. 15, 1448-1452.
  • Shimmura, S., Masumizu, T., Nakai, Y., Urayama, K., Shimazalti, J., Bissen-Miyajima, H., Kohno, M. and Tsubota, K. (1999) "Excimer laser-induced hydroxyl radical formation and keratocyte death in vitro. Invest", Ophthalmol. Vis. Sci. 40, 1245-1249.
  • Hayashi, S., bhimoto, S., Wu, G.S., Wee, W.R., Rao, N.A. and McDonnell, P.J. (1997) "Oxygen free radical damage in the cornea after excimer laser therapy", Br. J. Opthalmol. 81, 141-144.
  • Procacdni, E.M, Ricao, G., Bellocci, M., Di Martino, C. and Monfrecola, G. (2001) "The effects of a diode laser (810 nm) on pigmented guinea-pig skin", Lasers Med. Sci. 16, 171-175.
  • Belougne-Malfatti, E., Aguejouf, O., Doutremepuich, F. and Doutremepuich, C. (1997) "Action of neurotransmitters: acetylcholine, serotonin, and adrenaline in an experimental arterial thrombosis induced by oxygen free radicals", Thromb. Res. 88, 435-439.
  • Sasaki, Y., Noguchi, T., Seki, J., Giddings, J.C. and Yamamoto, J. (2000) "Protective effects of imidapril on He-Ne laser-induced thrombosis in cerebral blood vessels of stroke-prone spontaneously hypertensive rats", Thromb. Haemostasis 83, 722-727.
  • Nakagiri, K., Okada, M., Tsuji, Y., Yoshida, M. and Yamashita, T. (1999) "Evaluation of local platelet deposition during laser thermal angioplasty", Kobe J. Med. Sci. 45, 137-148.
  • Rosen, E.D., Raymond, S., Tollman, A., Noria, F., Sandoval-Cooper, M., Shulman, A., Merz, J.L. and Castellino, F.J. (2001) "Laser-induced noninvasive vascular injury models in mice generate platelet- and coagulation-dependent thrombi", Am. J. PathoI 158, 1613-1622.
  • Kim, Y.G., Pak, S.C and Lee, R.L. (2000) "Hairless mouse epidermal antioxidants and lipid peroxidation assessed by He-Ne laser", Lasen Surg. Med. 27, 420-426.
  • Sharov, VS., Briviba, K. and Sies, R (1996) "Assessment of the C-525 laser dye as a chemiluminescence sensitizer for lipid peroxidation in biological membranes: a comparison with chlorophyll-a", Free Radie. Biol. Med. 21, 833-843.
  • Ediger, M., Pettit, G.R and Matehette, L.S. (1997) "In vitro measurements of cytotoxic effects of 193 and 213 nm laser pulses at subablative fluences", Lasers Surg. Med. 21, 88-93.
  • Haywood, R.-M., Wardman, P., Gault, D.T. and Linge, C. (1999) "Ruby laser irradiation (694 nm) of human skin biopsies: assessment by electron spin resonance spectroscopy of free radical production and oxidative stress during laser depilation", Photochem. Photobiol. 70, 348-352.
  • Pettit, G.H., Ediger, M.N., Hahn, D.W., Landry, R.J., Weiblinger, R.P. and Morehouse, K.M. (1996) "Electron paramagnetic resonance spectroscopy of free radicals in comeal tissue following excimer laser irradiation", Lasers Surg. Med. 18, 367-372.
  • Benedetto, A.V. (1999) "Carbon dioxide laser resurfacing of the aged face", Adv. Exp. Med. Biol. 455, 483-490.
  • Harashima, T., Hossain, M., Walverde, D.A., Yamada, Y. and Matsumoto, K. (2001) 'Treatment of lymphangioma with Nd:YAG laser irradiation: a case report", J. Clin. Laser Med. Surg. 19, 189-191.
  • Vakhliaev, V.D., Smirnova, I.E., Uchaikina, L.V., Barsel, V.A., Aksiutina, M.S., Matveeva, S.A., Paramonova, M.A., Shchedrina, J.S. and Syrkin, A.L. (1992) "The effect of transvenous laser therapy on lipid peroxidation function in patients with ischemic heart disease", Kardiologiia 32, 43-45.
  • Ralulin, C. (2001) "Ethical considerations concerning lasermedicine", Lasers Surg. Med. 28, 100-101.
  • Anderson, R.R. (2001) "Response to letter to letter" Lasers Surg. Med. 28, 102.
  • Martin, L.D., Krunkosky, T.M., Dye, J.A., Fischer, B.M., Jiang, N.F., Rochelle, L.G., Aklev, N.J., Dreher, K.L. and Adler, K.B. (1997) "The role of reactive oxygen and nitrogen species in the response of airway epithelium to particulates", Environ. Health. Perspect. 105(Suppl 5), 1301-1307, Review.
  • Espey, M.G., Miranda, K.M., Thomas, D.D., Xavier, S., Citrin, D., Vitek, M.P. and Wink, D.A. (2002) "A chemical perspectives on the interplay between NO, reactive oxygen species, and reactive nitrogen oxide species", Ann. N.Y. Acad. Sci. 962, 195-200, Review.
  • Reid, M.B. and Durham, W.J. (2002) "Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging", Ann. N.Y. Acad. Sci. 959, 108-116, Review.
  • Spikes, J.D. (1999) "Photosensitization", In: Smith, K.C., eds, The Science of Photobiology (Plenum Press, New York), pp 79-110.
  • Schulz, I., Mahler, H.C., Boiteux, S. and Epe, B. (2000) "Oxidative DNA base damage induced by singlet oxygen and photosensitization: recognition by repair endonucleases and mutageniaty", Mutat. Res. 461, 145-156.
  • Michaeli, A. and Feitelson, J. (1994) "Reactivity of singlet oxygen toward amino acids and peptides", J. Photochem. Photobiol. 59, 284-289.
  • Polo, L., Presti, R, Schindl, A., Schindl, L, Jori, G. and Bertoloni, G. (1999) "Role of ground and excited singlet state oxygen in the red light-induced stimulation of Escherichia coli cell growth", Biochem. Biophys. Res. Commun. 257, 753-758.
  • Galankma, E., Volkov, S.V., Permiakov, N.K., Sinev, I.V. and Luzhnikov, E.A. (1996) "Healing of extensive acute gastric ulcer after chemical burn by helium-neon laser (endoscopic and morphologic investigation)", Klin. Med. (Mosc.) 74, 56-58.
  • Baxter, G.D. (1994) "Therapeutic lasers", Theory and Practice (Churchill Livingstone, Edinburgh, UK).
  • Kohli, R., Bose, B. and Gupta, P.K. (2001) "Induction of phr gene expression in E. coli strain KY706/pPL-1 by He-Ne laser (632.8 nm) irradiation", J. Photochem. Photobiol. B. 60, 136-142.
  • Timberlake, G.T., Gemperli, A.W., Larive, C.K., Warren, K.A. and Mainster, MA. (1997) "Free radical production by Nd:YAG laser photodisruption", Ophthalmic Surg. Lasers 28, 582-589.
  • Mulcahy, M., McInerney, J.G., Nikogosyan, D.N. and Gorner, R (2000) "193 nm photolysis of aromatic and aliphatic dipeptides in aqueous solution; dependence of decomposition quantum yield on the amino acid sequence", Biol. Chem. 381, 1259-1262.
  • Osipov, A.N., Borisenko, G.G., Kazarinov, K.D. and Valdimirov, IuA. (2000) "Nitric oxide, hemoglobin and laser irradiation", Vestn. Ross. Akad. Med. Nauk. 4, 48-52.
  • Vladimirov, Y., Borisenko, G., Boriskina, N., Kazarinov, K. and Osipov, A. (2000) "NO-hemoglobin may be a light-sensitive source of nitric oxide both in solution and in red blood cells", J. Photochem. Photobiol. B 59, 115-122.
  • Oelckers, S., Ziegler, T., Michler, T. and Roder, B. (1999) "Time-resolved detection of singlet oxygen luminescence in red-cell ghost suspensions: concerning a signal component mat can be attributed to 1O2 luminescence from the inside of `a native membrane", J. Photochem. Photobiol. B 53, 121-127.
  • Rochkind, S. and Ouaknine, G.E. (1992) "New trend in neuroscience: low-power laser effect on peripheral and central nervous system (basic science, preclinical and clinical studies)", Neurol. Res. 4, 2-11.
  • Possam, L.D., Banerjee, R., Balny, C and Douzou, F. (1970) "Oxidation of haemoglobin by oxygen in light possible role of singlet oxygen", Nature 226, 861-862.
  • Foots, C.S. (1991) "Definition of Type 1 and Type II photosensitized oxidation", J. Photochem. Photobiol. 54, 659.
  • Timberlake, G.T., Gemperli, A.W., Larive, C.K., Warren, K.A. and Mainster, M.A. (1997) "Free radical production by Nd: YAG laser photodisruption", Free Radic. Biol. Med. 26, 482-490.
  • Berki, T., Nemem, P., Poto, L and Nemeth, A. (1991) "Effects of photosensitization and low-power helium-neon laser irradiation", Vastn. Ross. Akad. Med. Nauk. 4, 48-52.
  • Belougne-Malfatti, E., Aguejouf, O., Doutremepuich, F., Belon, P. and Doutremepuich, C. (1998) "Combination of two doses of acetyl salicylic acid: experimental study of arterial thrombosis", Thromb. Res. 90, 215-221.
  • Tuikangas, G., Smith, T., Falcone, T., Boparai, N. and Walters, M.D. (2001) "Gross and histologic characteristics of laparoscopic injuries with four different energy sources", Fertil. Steril. 75, 806-810.
  • Cai, Y.S., Xu, D. and Mo, X (1989) "Clinical, pathological and photochemical studies of laser injury of the retina", Health Phys. 56, 643-646.
  • Jenings, P.E., MacEwen, C.J., Fallen, T.J., Scott, N., Haining, W.M. and Belch, J.J. (1991) "Oxidative effects of laser photocoagulation", Free Radie. Biol. Med. 11, 327-330.
  • Shimmura, S., Masumizu, T., Nakai, Y., Urayama, K., Shimazaki, J., Bissen-Miyajima, H., Kohno, M. and Tsubota, K. (1999) "Excimer laser-induced hydroxyl radical formation and keratocyte death in vitro", Imestig. Ophthalmol. Vis. Sci. 40, 1245-1249.
  • Mileva, M., Zlateva, G., Karabasheva, S., Hadjimitova, V. and Antonov, L (2000) "Effect of He-Ne laser treatment on the level lipid peroxidation products in experimental cataract of rabbit eyes", Methods Find. Exp. Clin. Pharmacol. 22, 676-681.
  • Katel'nitskaia, L.I., Khodareva, N.K. and Glushko, A.B. (1989) "Lipid peroxidation as an indicator of the effectiveness of treating patients with chronic ischemic heart disease using a helium-neon laser", Klin. Med. (Max.) 67, 37-39.
  • Zyrianova, T.N., Lavrova, V.M., Kanapatskaia, I.A. and Kanapatskaia, A.T. (1994) "Effect of tow-energy laser radiation on lipid peroxidation intensity", Vopr. Med. Khim. 40, 31-33.
  • Schulte-Frohlinde, D., Opitz, J., Corner, R and Bothe, E. (1985) "Model studies for the direct effect of high-energy irradiation on DNA. Mechanism of strand break formation induced by laser photoionization of poly U in aqueous solution", Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 48, 397-408.
  • Folkard, M., Prise, K.M., Vojnovic, B., Davies, S., Roper, M.J. and Michael, B.D. (1993) "Measurement of DNA damage by electrons with energies between 25 and 4000eV", Int. J. Radiat. Biol. 64, 651-658.
  • Prise, K.M., Folkard, M., Michael, B.D., Vojnovic, B., Brocklehurst, B., Hopkirk, A. and Munro, I.H. (2000) "Critical energies for SSB and DSB induction in plasmid DNA by low-energy photons: action spectra for strandbreak induction in plasmid DNA irradiated in vacuum", Int. J. Radiat. Biol. 76, 881-890.
  • Nikjoo, H., O'Neill, P., Goodhead, D.T. and Terrissol, M. (1997) "Computational modelling of low-energy electron-induced DNA damage by early physical and chemical events", Int. J. Radiat. Biol. 71, 467-483.
  • Burilkoy, V.K., Kovarskii, E.V. and Krochik, G.M. (1988) "Induction of DNA strand breaks by laser irradiation in a visible range", Biofizika 33, 242-246.
  • Song, Q.H., Yao, S.D. and Lin, N.Y. (1997) "Laser-induced modification of DNA and Poly[A,G] at guanine moiety using acetone as photosensitizer", J. Photochem. Photobiol. B. 40, 199-203.
  • Gorner, H., WaIa, M. and Schulte-Frohlinde, D. (1992) "Strand breakage in poly(C), poly(A), single- and double-stranded DNA induced by nanosecond laser excitation at 193 nm", Photochem. Photobiol. 55, 173-184.
  • Gurzadyan, G.G. and Gorner, R (1992) "Base release from DNA and polynucleotides upon 193 nm laser excitation", Photochem. Photobiol. 56, 371-378.
  • Cao, H., Ling, Y., Xu, J.Y., Cao, C.Q. and Kumar, P. (2001) "Photon statistics of random lasers with resonant feedback", Phys. Rev. Lett. 86, 4524-4527.
  • de With, A. and Greulich, K.O. (1995) "Wavelength dependence of laser-induced DNA damage in lymphocytes observed by single-cell gel electrophoresis", J. Photochem. Photobiol. B. 30, 71-76.
  • Schulte-Frohlinde, D. (1986) "Mechanism of radiation-induced strand break formation in DNA and polynucleotides", Adv. Space Res. 6, 89-96.
  • Gurzadyan, G.G. and Corner, R (1993) "Photolesions in DNA upon 193 nm excitation", Photochem. Photobiol. 58, 71-80.
  • Muhlberger, F., Zimmermann, R. and Kettrup, A. (2001) "A mobile mass spectrometer for comprehensive on-line analysis of trace and bulk components of complex gas mixtures: parallel application of the laser-based ionization methods VUV single-photon ionization, resonant multiphoton ionization, and laser-induced electron impact ionization", Anal. Chem. 73, 3590-3604.
  • Jackson, S.N. and Murray, K.K. (2001) "Infrared matrix-assisted laser desorption/ionization of polycyclic aromatic hydrocarbons with a sulfolane matrix", Rapid Commun. Mass Spectrom. 15, 1448-1452.
  • Plappert, U.C., Stocker, B., Heibig, R., Fliedner, T.M. and Seidel, H.J. (1999) "Laser pyrolysis products-genotoxic, elastogemc and mutagenic effects of the particulate aerosol fractions", Mutat. Res. 441, 29-41.
  • Stocker, B., Meier, T., Fliedner, T.M. and Plappert U. (1998) "Laser pyrolysis products: ampling procedures, cytotoxic and genotoxic effects", Mutat. Res. 412, 145-154.
  • Tomita, Y., Mihashi, S., Nagata, K., Ueda, S., Fujiki, M., Hirano, M. and Hirohata, T. (1981) "Mutagenicity of smoke condensates induced by CO2-laser irradiation and electro-cauterization", Mutat. Res. 89, 145-149.
  • Sonden, A., Svensson, B., Roman, N., Ostmark, H., Brismar, B., Pahnblad, J. and Kjellstrom, B.T. (2000) "Laser-induced shock wave endothelial cell injury", Lasers Surg. Med. 26, 364-375.
  • Moran, L.K., Gutteridge, J.M. and Quinlan, G.J. (2001) "Thiols in cellular redox signalling and control", Curr. Med. Chem. 8, 763-772.
  • Madison, R.D. and Macklis, J.D. (1993) "Noninvasively induced degeneration of neocortical pyramidal neurons in vivo: selective targeting by laser activation of retrogradely transported photolytic chromophore", Exp. Neural. 121, 153-159.
  • Lubart, R., Wollman, Y., Friedmann, H., Rochkind, S. and Laulicht, L (1992) "Effects of visible and near-infrared lasers on cell cultures", J. Photochem. Photobiol. B 12, 305-310.
  • Horton, J.C and Hocking, D.R. (1998) "Monocular core zones and binocular border strips in primate striate cortex revealed by the contrasting effects of enucleation, eyelid suture, and retinal laser lesions on cytochrome oxidase activity", J. Neurosci. 18, 5433-5455.
  • Cempel, L, Piot, J.M., Aubry, J.M., Patrice, T., Foultier, M.T. and Guillochon, D. (1994) "Photophysical and photobiological activities of a porphyrin peptide fraction derived from haemoglobin", J. Photochem. Photobiol. B 26, 141-146.
  • Michaeli, A. and Feitelson, J. (1994) "Reactivity of singlet oxygen toward amino acids and peptides", J. Photochem. Photobiol. 59, 284-289.
  • Kim, Y.G. (2001) "Thrombosis may be caused by low-intensity laser irradiation", Lasers Surg. Med. 29, A106.
  • Schindl, A. (2001) "Does low intensity laser irradiation really cause cell damage", Lasers Surg. Med. 29, A105.
  • Schindl, A. (1999) "Misleading terminology regarding the possible induction of apoptosis by laser", Lasers Surg. Med. 24, A177.
  • Schindl, A., Schindl, M., Pernerstorfer-Schon, H. and Schindl, L. (2000) "Low-intensity laser therapy: a review", J. Investig. Med. 48, 312-326.
  • Abeia, GA, Hage-Korban, E., Tomaru, T., Barbeau, G.R., Friedl, S.E., Kaelin, L.D. and Seeger, J.M. (2001) "A model for evaluation of arterial thrombosis following interventional procedures", Lasers Med. Sci. 16, 141-147.
  • Yamshita, T., Kitamori, K., Hashimoto, M., Watanabe, S., Giddings, J.C. and Yamamoto, J. (2000) "Conjunctive effects of the 5HT(2) receptor antagonist sarpogrelate, on thrombolysis with modified tissue plasminogen activator in different laser-induced thrombosis models", Haemostasis 30, 321-332.
  • Ogawa, T., Fujii, S., Urasawa, K. and Kitabatake, A. (2001) "Effects of nonionic contrast media on platelet aggregation: assessment by particle counting with laser-light scattering", Jpn Heart J. 42, 115-124.
  • Bonn, D. (2000) "Laser thrombolysis: safe and rapid removal of clots?", Lancet 355, A1976.
  • Aguejouf, O., Malfatti, E., Doutremepuich, F. and Doutremepuich, C. (2000) "Thrombogenic potential of contrast media in an experimental model of laser-induced thrombosis", Thromb. Res. 100, 167-177.
  • Zvereva, K.V. and Grunina, E.A. (1996) "The negative effects of low-intensity laser therapy in rheumatoid arthritis", Ter. Arkh. 68, 22-24.
  • Landau, Z. and Schattner, A. (2001) "Topical hyperbaric oxygen and low energy laser therapy for chronic diabetic foot ulcers resistant to conventional treatment", Yale J. Biol. Med. 74, 95-100.
  • Konstantinovic, L., Cernak, I. and Prokic, V. (1997) "Influence of low level laser irradiation on biochemical processes in brainstem and cortex of intact rabbits", Vojnosanit. Pregl. 54, 533-540.
  • Procaccini, E.M., Riccio, G., Bellocci, M., Di Martino, C. and Monfrecola, G. (2001) "The effects of a diode laser (810 nm) on pigmented guinea-pig skin", Lasers Med. Sci. 16, 171-175.
  • Vasil'ev, A.P., Strel'tsoya, N.N. and Kiianiuk, N.S. (1997) The stress-limiting action of low intensity laser radiation in patients with ischemic heart disease", Vopr. Kurortol. Fizioter. Lech. Fiz. Kul't. 6, 3-5.
  • Vakhliaev, V.D., Smirnova, I.E., Uchaikina, L.V., Barsel, V.A., Aksiutina, M.S., Matveeva, S.A., Paramonova, M.A., Shchedrina, I.S. and Syrkin, A.L. (1992) 'The effect of transvenous laser therapy on lipid peroxidation function in patients with ischemic heart disease", Kardiologiia 32, 43-45.
  • Jourdan, A., Aguejouf, O., Imbault, P., Doutremepuich, F., Inamo, J. and Doutremepuich, C. (1995) "Experimental thrombosis model induced by free radicals. Application to aspirin and other different substances", Thromb. Res. 79, 109-123.
  • Kasetsuwan, N., Wu, F.M., Hsieh, R, Sanchez, D. and McDonnell, P.J. (1994) "Effect of topical ascorbic acid on free radical tissue damage and inflammatory cell influx in the cornea after excimer laser corneal surgery", Arch. Ophthalmol. 117, 649-652.
  • Shimmura, S., Masumizu, T., Nakai, Y., Urayama, K., Shimazaki, J., Bissen-Miyajima, H., Kohno, M. and Tsubota, K. (1999) "Excimer laser-induced hydroxyl radical formation and keratocyte death in vitro", Investig. Ophthalmol. Vis. Sci. 40, 1245-1249.

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