Ultra-weak photon emission as a dynamic tool for monitoring oxidative stress metabolism

. 2017 Apr 27 ; 7 (1) : 1229. [epub] 20170427

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28450732
Odkazy

PubMed 28450732
PubMed Central PMC5430737
DOI 10.1038/s41598-017-01229-x
PII: 10.1038/s41598-017-01229-x
Knihovny.cz E-zdroje

In recent years, excessive oxidative metabolism has been reported as a critical determinant of pathogenicity in many diseases. The advent of a simple tool that can provide a physiological readout of oxidative stress would be a major step towards monitoring this dynamic process in biological systems, while also improving our understanding of this process. Ultra-weak photon emission (UPE) has been proposed as a potential tool for measuring oxidative processes due to the association between UPE and reactive oxygen species. Here, we used HL-60 cells as an in vitro model to test the potential of using UPE as readout for dynamically monitoring oxidative stress after inducing respiratory burst. In addition, to probe for possible changes in oxidative metabolism, we performed targeted metabolomics on cell extracts and culture medium. Lastly, we tested the effects of treating cells with the NADPH oxidase inhibitor diphenyleneiodonium chloride (DPI). Our results show that UPE can be used as readout for measuring oxidative stress metabolism and related processes.

Zobrazit více v PubMed

Babior, B. M. The respiratory burst oxidase. In: Molecular Aspects of Inflammation (Sies, H., Flohe, L., Zimmer, G. Eds). Springer-Verlag Berlin Heidelberg. 41–47 (1991).

Dahlgren C, Karlsson A. Respiratory burst in human neutrophils. Journal of immunological methods. 1999;232:3–14. doi: 10.1016/S0022-1759(99)00146-5. PubMed DOI

Glass GA, et al. The respiratory burst oxidase of human neutrophils. Further studies of the purified enzyme. Journal of Biological Chemistry. 1986;261:13247–13251. PubMed

Bylund J, Björnsdottir H, Sundqvist M, Karlsson A, Dahlgren C. Measurement of respiratory burst products, released or retained, during activation of professional phagocytes. Neutrophil methods and protocols. 2014;1124:321–338. doi: 10.1007/978-1-62703-845-4_21. PubMed DOI

Bylund J, Brown KL, Movitz C, Dahlgren C, Karlsson A. Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic Biol and Med. 2010;49:1834–1845. doi: 10.1016/j.freeradbiomed.2010.09.016. PubMed DOI

Panday A, Sahoo MK, Osorio D, Batra S. NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell Mol Immunol. 2015;12:5–23. doi: 10.1038/cmi.2014.89. PubMed DOI PMC

Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464–1476. PubMed

Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245–313. doi: 10.1152/physrev.00044.2005. PubMed DOI

Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012;24:981–990. doi: 10.1016/j.cellsig.2012.01.008. PubMed DOI PMC

Bartsch H, Nair J. Chronic inflammation and oxidative stress in the genesis and perpetuation of cancer: role of lipid peroxidation, DNA damage, and repair. Langenbecks Arch Surg. 2006;391:499–510. doi: 10.1007/s00423-006-0073-1. PubMed DOI

Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 2008;68:1777–1785. doi: 10.1158/0008-5472.CAN-07-5259. PubMed DOI

Perry G, Castellani RJ, Hirai K, Smith MA. Reactive Oxygen Species Mediate Cellular Damage in Alzheimer Disease. J Alzheimers Dis. 1998;1:45–55. doi: 10.3233/JAD-1998-1103. PubMed DOI

Sugamura K, Keaney JF., Jr. Reactive oxygen species in cardiovascular disease. Free Radic Biol Med. 2011;51:978–992. doi: 10.1016/j.freeradbiomed.2011.05.004. PubMed DOI PMC

Altenhofer S, Radermacher KA, Kleikers PW, Wingler K, Schmidt HH. Evolution of NADPH Oxidase Inhibitors: Selectivity and Mechanisms for Target Engagement. Antioxid Redox Signal. 2015;23:406–427. doi: 10.1089/ars.2013.5814. PubMed DOI PMC

Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov. 2011;10:453–471. doi: 10.1038/nrd3403. PubMed DOI PMC

Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014;24:R453–462. doi: 10.1016/j.cub.2014.03.034. PubMed DOI PMC

Bylund J, Bjornsdottir H, Sundqvist M, Karlsson A, Dahlgren C. Measurement of respiratory burst products, released or retained, during activation of professional phagocytes. Methods Mol Biol. 2014;1124:321–338. doi: 10.1007/978-1-62703-845-4_21. PubMed DOI

Prasad A, Pospisil P. Linoleic acid-induced ultra-weak photon emission from Chlamydomonas reinhardtii as a tool for monitoring of lipid peroxidation in the cell membranes. PLoS One. 2011;6:e22345. doi: 10.1371/journal.pone.0022345. PubMed DOI PMC

Rastogi A, Pospisil P. Ultra-weak photon emission as a non-invasive tool for the measurement of oxidative stress induced by UVA radiation in Arabidopsis thaliana. J Photochem Photobiol B. 2013;123:59–64. doi: 10.1016/j.jphotobiol.2013.03.012. PubMed DOI

Ives JA, et al. Ultraweak photon emission as a non-invasive health assessment: a systematic review. PLoS One. 2014;9:e87401. doi: 10.1371/journal.pone.0087401. PubMed DOI PMC

Cifra M, Pospisil P. Ultra-weak photon emission from biological samples: definition, mechanisms, properties, detection and applications. J Photochem Photobiol B. 2014;139:2–10. doi: 10.1016/j.jphotobiol.2014.02.009. PubMed DOI

Devaraj, B., Usa, M. & Inaba, H. Biophotons: Ultraweak light emission from living systems. Curr Opin Solid St M2, 188–193, doi:10.1016/S1359-0286(97)80064-2 (1997).

Pospisil P, Prasad A, Rac M. Role of reactive oxygen species in ultra-weak photon emission in biological systems. J Photochem Photobiol B. 2014;139:11–23. doi: 10.1016/j.jphotobiol.2014.02.008. PubMed DOI

Van Wijk R, Van Wijk EP, Wiegant FA, Ives J. Free radicals and low-level photon emission in human pathogenesis: state of the art. Indian J Exp Biol. 2008;46:273–309. PubMed

Rastogi A, Pospisil P. Spontaneous ultraweak photon emission imaging of oxidative metabolic processes in human skin: effect of molecular oxygen and antioxidant defense system. J Biomed Opt. 2011;16:096005. doi: 10.1117/1.3616135. PubMed DOI

Burgos RC, van Wijk EP, van Wijk R, He M, van der Greef J. Crossing the Boundaries of Our Current Healthcare System by Integrating Ultra-Weak Photon Emissions with Metabolomics. Front Physiol. 2016;7:611. doi: 10.3389/fphys.2016.00611. PubMed DOI PMC

Burgos RC, et al. Tracking biochemical changes correlated with ultra-weak photon emission using metabolomics. J Photochem Photobiol B. 2016;163:237–245. doi: 10.1016/j.jphotobiol.2016.08.030. PubMed DOI

Galantsev VP, Kovalenko SG, Moltchanov AA, Prutskov VI. Lipid peroxidation, low-level chemiluminescence and regulation of secretion in the mammary gland. Experientia. 1993;49:870–875. doi: 10.1007/BF01952600. PubMed DOI

McCarthy MK, Weinberg JB. Eicosanoids and respiratory viral infection: coordinators of inflammation and potential therapeutic targets. Mediators Inflamm. 2012;2012:236345–13. doi: 10.1155/2012/236345. PubMed DOI PMC

Montuschi P, Barnes PJ, Roberts LJ. 2nd. Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004;18:1791–1800. doi: 10.1096/fj.04-2330rev. PubMed DOI

Cadenas, E., Boveris, A. & Chance, B. In Free Radicals in Biology 211–242 (Academic Press, 1984).

Cadenas E, Sies H. Formation of electronically excited states during the oxidation of arachidonic acid by prostaglandin endoperoxide synthase. Methods Enzymol. 2000;319:67–77. doi: 10.1016/S0076-6879(00)19009-3. PubMed DOI

Cadenas E, Sies H, Nastainczyk W, Ullrich V. Singlet oxygen formation detected by low-level chemiluminescence during enzymatic reduction of prostaglandin G2 to H2. Hoppe Seylers Z Physiol Chem. 1983;364:519–528. doi: 10.1515/bchm2.1983.364.1.519. PubMed DOI

Nakano M. Low-level chemiluminescence during lipid peroxidations and enzymatic reactions. J Biolumin Chemilumin. 1989;4:231–240. doi: 10.1002/bio.1170040133. PubMed DOI

Breitman TR, Selonick SE, Collins SJ. Induction of differentiation of the human promyelocytic leukemia cell line (HL-60) by retinoic acid. Proc Natl Acad Sci USA. 1980;77:2936–2940. doi: 10.1073/pnas.77.5.2936. PubMed DOI PMC

Levy R, Rotrosen D, Nagauker O, Leto TL, Malech HL. Induction of the respiratory burst in HL-60 cells. Correlation of function and protein expression. J Immunol. 1990;145:2595–2601. PubMed

Fu J, et al. Metabolomics profiling of the free and total oxidised lipids in urine by LC-MS/MS: application in patients with rheumatoid arthritis. Anal Bioanal Chem. 2016;408:6307–6319. doi: 10.1007/s00216-016-9742-2. PubMed DOI PMC

Collins SJ. The HL-60 promyelocytic leukemia cell line: proliferation, differentiation, and cellular oncogene expression. Blood. 1987;70:1233–1244. PubMed

Gallagher R, et al. Characterization of the continuous, differentiating myeloid cell line (HL-60) from a patient with acute promyelocytic leukemia. Blood. 1979;54:713–733. PubMed

Dang PM, Fontayne A, Hakim J, El Benna J, Perianin A. Protein kinase C zeta phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst. J Immunol. 2001;166:1206–1213. doi: 10.4049/jimmunol.166.2.1206. PubMed DOI

el Benna J, Faust LP, Babior BM. The phosphorylation of the respiratory burst oxidase component p47phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases. J Biol Chem. 1994;269:23431–23436. PubMed

Tardif M, Rabiet MJ, Christophe T, Milcent MD, Boulay F. Isolation and characterization of a variant HL60 cell line defective in the activation of the NADPH oxidase by phorbol myristate acetate. J Immunol. 1998;161:6885–6895. PubMed

Cross AR, Jones OT. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem J. 1986;237:111–116. doi: 10.1042/bj2370111. PubMed DOI PMC

Hancock JT, Jones OTG. The Inhibition by Diphenyleneiodonium and Its Analogs of Superoxide Generation by Macrophages. Biochemical Journal. 1987;242:103–107. doi: 10.1042/bj2420103. PubMed DOI PMC

Liu Y, Fiskum G, Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem. 2002;80:780–787. doi: 10.1046/j.0022-3042.2002.00744.x. PubMed DOI

Li Y, Trush MA. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Bioph Res Co. 1998;253:295–299. doi: 10.1006/bbrc.1998.9729. PubMed DOI

Buczynski MW, Dumlao DS, Dennis EA. Thematic Review Series: Proteomics. An integrated omics analysis of eicosanoid biology. J Lipid Res. 2009;50:1015–1038. doi: 10.1194/jlr.R900004-JLR200. PubMed DOI PMC

Fullerton JN, O’Brien AJ, Gilroy DW. Lipid mediators in immune dysfunction after severe inflammation. Trends Immunol. 2014;35:12–21. doi: 10.1016/j.it.2013.10.008. PubMed DOI PMC

Parchmann S, Mueller MJ. Evidence for the Formation of Dinor Isoprostanes E1from α-Linolenic Acid in Plants. J Biol Chem. 1998;273:32650–32655. doi: 10.1074/jbc.273.49.32650. PubMed DOI

Morrow JD, et al. Free radical-induced generation of isoprostanes in vivo. Evidence for the formation of D-ring and E-ring isoprostanes. J Biol Chem. 1994;269:4317–4326. PubMed

Longmire AW, Roberts LJ, Morrow JD. Actions of the E2-isoprostane, 8-ISO-PGE2, on the platelet thromboxane/endoperoxide receptor in humans and rats: additional evidence for the existence of a unique isoprostane receptor. Prostaglandins. 1994;48:247–256. doi: 10.1016/0090-6980(94)90011-6. PubMed DOI

Wilson JR, Kapoor SC. Contribution of prostaglandins to exercise-induced vasodilation in humans. Am J Physiol. 1993;265:H171–175. PubMed

Smith JB. Prostaglandins and platelet aggregation. Acta Med Scand Suppl. 1981;651:91–99. PubMed

Rieser C, Bock G, Klocker H, Bartsch G, Thurnher M. Prostaglandin E2 and tumor necrosis factor alpha cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J Exp Med. 1997;186:1603–1608. doi: 10.1084/jem.186.9.1603. PubMed DOI PMC

Van Brocklyn JR, Williams JB. The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 2012;163:26–36. doi: 10.1016/j.cbpb.2012.05.006. PubMed DOI

Lambeth J, Burnham D, Tyagi S. Sphinganine effects on chemoattractant-induced diacylglycerol generation, calcium fluxes, superoxide production, and on cell viability in the human neutrophil. Delivery of sphinganine with bovine serum albumin minimizes cytotoxicity without affecting inhibition of the respiratory burst. J Biol Chem. 1988;263:3818–3822. PubMed

Hannun YA, Loomis CR, Merrill AH, Jr., Bell RM. Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J Biol Chem. 1986;261:12604–12609. PubMed

Satoshi K, et al. Effect of sphingosine and its N-methyl derivatives on oxidative burst, phagokinetic activity, and trans-endothelial migration of human neutrophils. Biochemical pharmacology. 1992;44:1585–1595. doi: 10.1016/0006-2952(92)90476-Y. PubMed DOI

Shishikura K, et al. Prostaglandin E2 inhibits neutrophil extracellular trap formation through production of cyclic AMP. British Journal of Pharmacology. 2016;173:319–331. doi: 10.1111/bph.13373. PubMed DOI PMC

Mitsuyama T, Takeshige K, Minakami S. Cyclic AMP inhibits the respiratory burst of electropermeabilized human neutrophils at a downstream site of protein kinase C. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 1993;1177:167–173. doi: 10.1016/0167-4889(93)90036-O. PubMed DOI

Heinemann A, Schuligoi R, Sabroe I, Hartnell A, Peskar BA. Delta 12-prostaglandin J2, a plasma metabolite of prostaglandin D2, causes eosinophil mobilization from the bone marrow and primes eosinophils for chemotaxis. J Immunol. 2003;170:4752–4758. doi: 10.4049/jimmunol.170.9.4752. PubMed DOI

Saito S, Tsuda H, Michimata T. Prostaglandin D2 and reproduction. Am J Reprod Immunol. 2002;47:295–302. doi: 10.1034/j.1600-0897.2002.01113.x. PubMed DOI

Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012;40:W127–133. doi: 10.1093/nar/gks374. PubMed DOI PMC

Xia J, Sinelnikov IV, Han B, Wishart DS. MetaboAnalyst 3.0-making metabolomics more meaningful. Nucleic Acids Res. 2015;43:W251–257. doi: 10.1093/nar/gkv380. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...