Skip to main content

Advertisement

SpringerLink
Log in

Irradiation at 634 nm releases nitric oxide from human monocytes

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

Previous studies have shown that irradiation at 634 nm decreases the release of extracellular reactive oxygen species (ROS) without affecting viability in human monocytes. Here, we examined the effect of irradiation at 634 nm on the release of nitric oxide (NO), activation of inducible nitric oxide synthase (iNOS) and endothelial NOS (eNOS), and release of intracellular ROS. Chemiluminescence assays were used to measure NO release, intracellular ROS, and adenosine triphosphate levels (to assess cell viability). Levels of iNOS and eNOS mRNA were analyzed using PCR. Irradiation resulted in elevated levels of NO but had no effect on iNOS or eNOS. Irradiation also caused a decrease in levels of intracellular ROS and had no effect on cell viability. Our studies indicate that irradiation at 634 nm releases NO, possibly from a preformed store, and reduces the production of intracellular ROS without affecting cell viability. Irradiation at 634 nm may have a wide range of clinical applications, including a reduction in oxidative stress-mediated injury in the vasculature.

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

Similar content being viewed by others

References

  1. Daniell MD, Hill JS (1991) A history of photodynamic therapy. Aust NZ J Surg 61(5):340–348

    CAS  Google Scholar 

  2. Alora MB, Anderson RR (2000) Recent developments in cutaneous lasers. Lasers Surg Med 26(2):108–118

    Article  PubMed  CAS  Google Scholar 

  3. Whelan HT, Smits RL Jr, Buchman EV, Whelan NT, Turner SG, Margolis DA, Cevenini V, Stinson H, Ignatius R, Martin T, Cwiklinski J, Philippi AF, Graf WR, Hodgson B, Gould L, Kane M, Chen G, Caviness J (2001) Effect of NASA light-emitting diode irradiation on wound healing. J Clin Laser Med Surg 19(6):305–314

    Article  PubMed  CAS  Google Scholar 

  4. Lane N (2003) New light on medicine. Sci Am 288(1):38–45

    Article  PubMed  CAS  Google Scholar 

  5. Santana-Blank LA, Rodriguez-Santana E, Santana-Rodriguez KE (2005) Photo-infrared pulsed bio-modulation (PIPBM): a novel mechanism for the enhancement of physiologically reparative responses. Photomed Laser Surg 23(4):416–424

    Article  PubMed  Google Scholar 

  6. Wright A, Hawkins CL, Davies MJ (2003) Photo-oxidation of cells generates long-lived intracellular protein peroxides. Free Radic Biol Med 34(6):637–647

    Article  PubMed  CAS  Google Scholar 

  7. Boelens R, Wever R, Van Gelder BF, Rademaker H (1983) An EPR study of the photodissociation reactions of oxidised cytochrome c oxidase-nitric oxide complexes. Biochim Biophys Acta 724(2):176–183

    Article  PubMed  CAS  Google Scholar 

  8. Ferezin CZ, Oliveira FS, da Silva RS, Simioni AR, Tedesco AC, Bendhack LM (2005) The complex trans-[RuCl([15]aneN4NO]2+ induces rat aorta relaxation by ultraviolet light irradiation. Nitric Oxide 13(3):170–175

    Article  PubMed  CAS  Google Scholar 

  9. Ergun Y, Ogulener N (2005) Selective modifiers of glutathione prevent restoration of photorelaxations in mouse gastric fundus. Fundam Clin Pharmacol 19(4):503–509

    Article  PubMed  CAS  Google Scholar 

  10. Pagliaro P (2003) Differential biological effects of products of nitric oxide (NO) synthase: it is not enough to say NO. Life Sci 73(17):2137–2149

    Article  PubMed  CAS  Google Scholar 

  11. Brown GC (2003) Cell biology. NO says yes to mitochondria. Science 299(5608):838–839

    Article  PubMed  Google Scholar 

  12. Vladimirov Y, Borisenko G, Boriskina N, Kazarinov K, 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(1–3):115–122

    Article  PubMed  CAS  Google Scholar 

  13. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357(3):593–615

    Article  PubMed  CAS  Google Scholar 

  14. Schneemann M, Schoedon G, Hofer S, Blau N, Guerrero L, Schaffner A (1993) Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis 167(6):1358–1363

    PubMed  CAS  Google Scholar 

  15. Denis M (1994) Human monocytes/macrophages: NO or no NO? J Leukoc Biol 55(5):682–684

    PubMed  CAS  Google Scholar 

  16. Wang CH, Lin HC, Liu CY, Huang KH, Huang TT, Yu CT, Kuo HP (2001) Upregulation of inducible nitric oxide synthase and cytokine secretion in peripheral blood monocytes from pulmonary tuberculosis patients. Int J Tuberc Lung Dis 5(3):283–291

    PubMed  CAS  Google Scholar 

  17. Schena M, Mulatero P, Schiavone D, Mengozzi G, Tesio L, Chiandussi L, Veglio F (1999) Vasoactive hormones induce nitric oxide synthase mRNA expression and nitric oxide production in human endothelial cells and monocytes. Am J Hypertens 12(4 Pt 1):388–397

    PubMed  CAS  Google Scholar 

  18. Fang FC (1997) Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99(12):2818–2825

    PubMed  CAS  Google Scholar 

  19. MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323–350

    Article  PubMed  CAS  Google Scholar 

  20. Hulten LM, Holmstrom M, Soussi B (1999) Harmful singlet oxygen can be helpful. Free Radic Biol Med 27(11–12):1203–1207

    Article  PubMed  CAS  Google Scholar 

  21. Lindgård A, Lundberg J, Rakotonirainy O, Elander A, Soussi B (2003) Preservation of rat skeletal muscle energy metabolism by illumination. Life Sci 72(23):2649–2658

    Article  PubMed  CAS  Google Scholar 

  22. Lundberg J, Lindgård A, Elander A, Soussi B (2002) Improved energetic recovery of skeletal muscle in response to ischemia and reperfusion injury followed by in vivo 31P-magnetic resonance spectroscopy. Microsurgery 22(4):158–164

    Article  PubMed  Google Scholar 

  23. Lukes D, Lundgren A, Wilton J, Lindgård A, Omerovic E, Rakotonirainy O, Karlsson-Parra A, Olausson M, Soussi B (2003) Singlet oxygen energy illumination during ischemia preserves high-energy phosphates in a concordant heart xenotransplantation model. Laser Physics 13(1):84–90

    CAS  Google Scholar 

  24. Boyum A (1976) Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol Suppl 5:9–15

    Article  Google Scholar 

  25. Wilkinson F, Helman WP, Ross AB (1993) Quantum yields for the photosensitized formation of the lowest electronically excited singlet state of molecular oxygen in solution. J Phys Chem Ref Data 22:113–262

    Article  CAS  Google Scholar 

  26. Frimer A (2000) Physical–chemical aspects. In: Rayton B (ed) Singlet O2. CRC Press, Florida, pp 8–18

    Google Scholar 

  27. Ewing JF, Janero DR (1998) Specific S-nitrosothiol (thionitrite) quantification as solution nitrite after vanadium(III) reduction and ozone-chemiluminescent detection. Free Radic Biol Med 25(4–5):621–628

    Article  PubMed  CAS  Google Scholar 

  28. Kharitonov S, Alving K, Barnes PJ (1997) Exhaled and nasal nitric oxide measurements: recommendations. The European Respiratory Society Task Force. Eur Respir J 10(7):1683–1693

    Article  PubMed  CAS  Google Scholar 

  29. Archer S (1993) Measurement of nitric oxide in biological models. FASEB J 7(2):349–360

    PubMed  CAS  Google Scholar 

  30. Kopprasch S, Pietzsch J, Graessler J (2003) Validation of different chemilumigenic substrates for detecting extracellular generation of reactive oxygen species by phagocytes and endothelial cells. Luminescence 18(5):268–273

    Article  PubMed  CAS  Google Scholar 

  31. Lundqvist H, Dahlgren C (1996) Isoluminol-enhanced chemiluminescence: a sensitive method to study the release of superoxide anion from human neutrophils. Free Radic Biol Med 20(6):785–792

    Article  PubMed  CAS  Google Scholar 

  32. Lundin A (2000) Use of firefly luciferase in ATP-related assays of biomass, enzymes, and metabolites. Methods Enzymol 305:346–370

    Article  PubMed  CAS  Google Scholar 

  33. Ruetten H, Thiemermann C (1996) Prevention of the expression of inducible nitric oxide synthase by aminoguanidine or aminoethyl-isothiourea in macrophages and in the rat. Biochem Biophys Res Commun 225(2):525–530

    Article  PubMed  CAS  Google Scholar 

  34. Corbett JA, Tilton RG, Chang K, Hasan KS, Ido Y, Wang JL, Sweetland MA, Lancaster JR Jr, Williamson JR, McDaniel ML (1992) Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes 41(4):552–556

    PubMed  CAS  Google Scholar 

  35. Lubart R, Eichler M, Lavi R, Friedman H, Shainberg A (2005) Low-energy laser irradiation promotes cellular redox activity. Photomed Laser Surg 23(1):3–9

    Article  PubMed  CAS  Google Scholar 

  36. Matsunaga K, Furchgott RF (1989) Interactions of light and sodium nitrite in producing relaxation of rabbit aorta. J Pharmacol Exp Ther 248(2):687–695

    PubMed  CAS  Google Scholar 

  37. Singh RJ, Hogg N, Joseph J, Kalyanaraman B (1996) Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem 271(31):18596–18603

    Article  PubMed  CAS  Google Scholar 

  38. Lovren F, Triggle CR (1998) Involvement of nitrosothiols, nitric oxide and voltage-gated K+ channels in photorelaxation of vascular smooth muscle. Eur J Pharmacol 347(2–3):215–221

    Article  PubMed  CAS  Google Scholar 

  39. Cathcart MK (2004) Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler Thromb Vasc Biol 24(1):23–28

    Article  PubMed  CAS  Google Scholar 

  40. Yagisawa M, Yuo A, Yonemaru M, Imajoh-Ohmi S, Kanegasaki S, Yazaki Y, Takaku F (1996) Superoxide release and NADPH oxidase components in mature human phagocytes: correlation between functional capacity and amount of functional proteins. Biochem Biophys Res Commun 228(2):510–516

    Article  PubMed  CAS  Google Scholar 

  41. Lagerwall K, Daneryd P, Schersten T, Soussi B (1995) In vivo 31P nuclear magnetic resonance evidence of the salvage effect of ascorbate on the postischemic reperfused rat skeletal muscle. Life Sci 56(6):389–397

    Article  PubMed  CAS  Google Scholar 

  42. Jonsson O, Lindgard A, Fae A, Gondalia J, Aneman A, Soussi B (2003) Enhanced post-ischaemic recovery in rabbit kidney after pretreatment with an indeno–indole compound and ascorbate monitored in vivo by 31P magnetic resonance spectroscopy. Scand J Urol Nephrol 37(6):450–455

    Article  PubMed  CAS  Google Scholar 

  43. Jiang F, Drummond GR, Dusting GJ (2004) Suppression of oxidative stress in the endothelium and vascular wall. Endothelium 11(2):79–88

    Article  PubMed  CAS  Google Scholar 

  44. Vinck EM, Cagnie BJ, Cornelissen MJ, Declercq HA, Cambier DC (2003) Increased fibroblast proliferation induced by light emitting diode and low power laser irradiation. Lasers Med Sci 18(2):95–99

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from HM Sultan Qaboos Research Trust Funds (project no. SR/AGR/FOOD/05/01), the Swedish Research Council (grant no. K2005-73X-00536-41A), Sahlgrenska Academy at Göteborg University, the Inga Britta & Arne Lundberg Foundation, the Foundation for Scientific Research at the Department of Surgery, and by the Wallenberg Foundation. We thank Gaia Care AS, Norway, for providing the Oxylight equipment.

Author information

Authors and Affiliations

  1. Wallenberg Laboratory, Sahlgrenska University Hospital, Göteborg University, Gothenburg, 413 45, Sweden

    Ann Lindgård, Lillemor Mattsson Hultén & Bassam Soussi

  2. Sultan Qaboos University, Al Khod, PC 123, Oman

    Bassam Soussi

  3. AstraZeneca, R&D, Mölndal, 431 83, Sweden

    Lennart Svensson

Authors
  1. Ann Lindgård
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lillemor Mattsson Hultén
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lennart Svensson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bassam Soussi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bassam Soussi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lindgård, A., Hultén, L.M., Svensson, L. et al. Irradiation at 634 nm releases nitric oxide from human monocytes. Lasers Med Sci 22, 30–36 (2007). https://doi.org/10.1007/s10103-006-0419-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-006-0419-5

Keywords

Search

Navigation