CELLULAR AND SUBCELLULAR MECHANISMS OF PHOTODYNAMIC ACTION: THE 1 O2 HYPOTHESIS AS A DRIVING FORCE IN RECENT RESEARCH

Abstract— Since 1972 the protective (quenching) effect of N3‐ and the enhancing effect of D2O have been used in combination to demonstrate 1O2 (1Δg) as the major reactive intermediate in the dye‐sensitized photooxygenation of biomolecules in in vitro systems. Extended application to in vivo systems has recently begun, producing some results which generally support the involvement of 1O2 pathways in the photosensitization processes. The use of other 1O2 quenchers and acceptors has also been increasing. In the application of these techniques as diagnostic tests for 1O2 participation in in vivo systems, careful examination of the experimental conditions should be made with respect to the quenching capability and accessibility of D2O in the specified cellular environment. Furthermore, the diffusive nature of 1O2, generation sites, generation efficiencies, the location and type of sensitizers, and the reactivity of 1O2 with presumed target structures in the cell should also be taken into account in the interpretation. Recent studies illustrating the importance of these factors are discussed. Finally, a tentative picture of the mode of in vivo photodynamic activity of common dye sensitizers is outlined.

[1]  E. Lochmann,et al.  CHAPTER 8 – Binding of Organic Dyes to Nucleic Acids and the Photodynamic Effect , 1973 .

[2]  S. Matsumoto PHOTODYNAMIC INACTIVATION OF ESCHERICHIA COLI CELLS AFTER STARVATION FOR REQUIRED AMINO ACID OR CHLORAMPHENICOL TREATMENT , 1974 .

[3]  L. Harber,et al.  PHOTOREACTIONS ASSOCIATED WITH IN VITRO HEMOLYSIS IN ERYTHROPOIETIC PROTOPORPHYRIA * , 1971, Photochemistry and photobiology.

[4]  J. Cooney,et al.  Action of light on Micrococcus roseus. , 1974, Canadian journal of microbiology.

[5]  H. Rosenkranz,et al.  Light-induced mutagenicity of neutral red (3-amino-7-dimethylamino-2-methylphenazine hydrochloride). , 1977, Cancer research.

[6]  B. Bagchi,et al.  LIQUID HOLDING RECOVERY OF PHOTODYNAMIC DAMAGE IN E. COLI , 1974, Photochemistry and photobiology.

[7]  C. Foote,et al.  Olefin Oxidations with Excited Singlet Molecular Oxygen , 1964 .

[8]  N. Krinsky MEMBRANE PHOTOCHEMISTRY AND PHOTOBIOLOGY , 1974, Photochemistry and photobiology.

[9]  S. Nishiyama-Watanabe Photodynamic action of thiopyronine on the respiration and fermentation in yeast. , 1976, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[10]  K. Kobayashi,et al.  IN VIVO EVIDENCE FOR THE PHOTODYNAMIC MEMBRANE DAMAGE AS A DETERMINING STEP OF THE INACTIVATION OF YEAST CELLS SENSITIZED BY TOLUIDINE BLUE , 1977, Photochemistry and photobiology.

[11]  M. Kasha,et al.  Red Chemiluminescence of Molecular Oxygen in Aqueous Solution , 1963 .

[12]  K. Hieda,et al.  Absence of apparent dark recovery from the photodynamically-induced mutational damages in yeast cells. , 1968, Mutation research.

[13]  N. Krinsky,et al.  PROTECTIVE ACTION OF CAROTENOID PIGMENTS AGAINST PHOTODYNAMIC DAMAGE TO LIPOSOMES* , 1973, Photochemistry and photobiology.

[14]  I. Matheson,et al.  Reaction rate of bilirubin with singlet oxygen (1delta g) and its strong enhancement by added base. , 1974, Journal of the American Chemical Society.

[15]  F. Hallett,et al.  Reactions between singlet oxygen and the constituents of nucleic acids. Importance of reactions in photodynamic processes. , 1970, Biophysical journal.

[16]  N. Krinsky,et al.  PHOTODYNAMIC KILLING OF ACHOLEPLASMA LAZDLAWII , 1972, Photochemistry and photobiology.

[17]  G. Geller,et al.  CHEMISTRY OF SINGLET OXYGEN—XVIII. RATES OF REACTION AND QUENCHING OF α‐TOCOPHEROL AND SINGLET OXYGEN * , 1974, Photochemistry and photobiology.

[18]  B. Stevens,et al.  THE PHOTOPEROXIDATION OF UNSATURATED ORGANIC MOLECULES‐XIII. O2 1 δg QUENCHING BY α‐TOCOPHEROL* , 1974, Photochemistry and photobiology.

[19]  H. Tseng,et al.  PHOTODYNAMIC INACTIVATION OF YEAST SENSITIZED BY EOSIN Y , 1977, Photochemistry and Photobiology.

[20]  Christopher S. Foote,et al.  Mechanisms of Photosensitized Oxidation , 1968 .

[21]  C. Foote CHAPTER 3 – Photosensitized Oxidation and Singlet Oxygen: Consequences in Biological Systems , 1976 .

[22]  M. Wolbarsht,et al.  Measurement of the absolute rate constants for singlet molecular oxygen (1.DELTA.g) reaction with 1,3-diphenylisobenzofuran and physical quenching by ground state molecular oxygen , 1974 .

[23]  C. Alving,et al.  LIGHT‐INDUCED LEAKAGE OF SPIN LABEL MARKER FROM LIPOSOMES IN THE PRESENCE OF PHOTOTOXIC PHENOTHIAZINES , 1976, Photochemistry and photobiology.

[24]  J. D. Macmillan,et al.  FUNCTION OF CAROTENOIDS IN PROTECTION OF RHODOTORULA GLUTINIS AGAINST IRRADIATION FROM A GAS LASER , 1966 .

[25]  J. Spikes Chapter 2 – PHOTODYNAMIC ACTION , 1968 .

[26]  T. Ito,et al.  TOLUIDINE BLUE: THE MODE OF PHOTODYNAMIC ACTION IN YEAST CELLS , 1977, Photochemistry and photobiology.

[27]  K. Kobayashi,et al.  FURTHER IN VIVO STUDIES ON THE PARTICIPATION OF SINGLET OXYGEN IN THE PHOTODYNAMIC INACTIVATION AND INDUCTION OF GENETIC CHANGES IN SACCHAROMYCES CEREVISIAE , 1976, Photochemistry and photobiology.

[28]  N. Krinsky,et al.  STUDIES ON THE PROTECTIVE FUNCTION OF THE CAROTENOID PIGMENTS OF SARCINA LUTEA , 1970, Photochemistry and photobiology.

[29]  E. Lochmann,et al.  Die Wirkung von Thiopyronin auf die Dunkelreaktivierung von UV-, Röntgen- und photodynamischen Schäden beiSaccharomyces , 1968 .

[30]  M. Kasai,et al.  PHOTODYNAMIC INACTIVATION OF SARCOPLASMIC RETICULUM VESICLE MEMBRANES BY XANTHENE DYES , 1974, Photochemistry and photobiology.

[31]  M. Vízdalová,et al.  On the nature of reparable and non-reparable lethal damage in E. coli and bacteriophage induced by the photodynamic action of acridine orange. , 1970, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[32]  F. L. Hill,et al.  Sterol metabolism. 23. Cholesterol oxidation by radiation-induced processes. , 1973, The Journal of organic chemistry.

[33]  E. Corey,et al.  A Study of the Peroxidation of Organic Compounds by Externally Generated Singlet Oxygen Molecules , 1964 .

[34]  L. Grossweiner,et al.  RESEARCH NOTE PHOTODYNAMIC SENSITIZATION BY 8‐METHOXYPSORALEN VIA THE SINGLET OXYGEN MECHANISM * , 1975, Photochemistry and photobiology.

[35]  L. Grossweiner APPLICATION OF DIFFUSION THEORY TO PHOTO‐DYNAMIC DAMAGE IN LARGE TARGETS* , 1977, Photochemistry and photobiology.

[36]  J. D. Macmillan,et al.  LETHAL PHOTOSENSITIZATION OF MICROORGANISMS WITH LIGHT FROM A CONTINUOUS‐WAVE GAS LASER , 1966, Photochemistry and photobiology.

[37]  D. Clayton,et al.  Strand breakage in solutions of DNA and ethidium bromide exposed to visible light. , 1977, Nucleic acids research.

[38]  H. Jacob DNA REPAIR AFTER PHOTODYNAMIC TREATMENT OF PROTEUS MIRABILIS , 1975 .

[39]  R. Haynes,et al.  DARK RECOVERY PHENOMENA IN YEAST. 1. COMPARATIVE EFFECTS WITH VARIOUS INACTIVATING AGENTS. , 1964, Radiation research.

[40]  N. Kratowich,et al.  THE QUENCHING OF SINGLET OXYGEN BY AMINO ACIDS AND PROTEINS , 1975, Photochemistry and photobiology.

[41]  A. Girotti BILIRUBIN‐SENSITIZED PHOTOINACTIVATION OF ENZYMES IN THE ISOLATED MEMBRANE OF THE HUMAN ERYTHROCYTE * , 1976, Photochemistry and photobiology.

[42]  B. Goldstein,et al.  Erythropoietic protoporphyria: lipid peroxidation and red cell membrane damage associated with photohemolysis. , 1972, The Journal of clinical investigation.

[43]  D. Macphee,et al.  Induction of frameshifts and base-pair substitutions by acridine orange plus visible light in bacteria. , 1973, Mutation research.

[44]  Takashi Ito,et al.  A SURVEY OF IN VIVO PHOTODYNAMIC ACTIVITY OF XANTHENES, THIAZINES, AND ACRIDINES IN YEAST CELLS , 1977 .

[45]  K. Kobayashi,et al.  WAVELENGTH DEPENDENCE OF SINGLET OXYGEN MECHANISM IN ACRIDINE ORANGE‐SENSITIZED PHOTODYNAMIC ACTION IN YEAST CELLS: EXPERIMENTS WITH 470 NM , 1977, Photochemistry and photobiology.

[46]  H. Rosenkranz,et al.  Further observations on the photooxidation of DNA in the presence of riboflavin. , 1976, Biochimica et biophysica acta.

[47]  H. Kautsky,et al.  Quenching of luminescence by oxygen , 1939 .

[48]  A. Allison,et al.  Chromosome Damage in Human Diploid Cells following Activation of Lysosomal Enzymes , 1965, Nature.

[49]  D. Kearns,et al.  Physical and chemical properties of singlet molecular oxygen , 1971 .

[50]  E. A. Ogryzlo,et al.  Some New Emission Bands of Molecular Oxygen , 1964 .

[51]  Katsumi Kobayashi EFFECT OF SODIUM AZIDE ON PHOTODYNAMIC INDUCTION OF GENETIC CHANGES IN YEAST , 1978, Photochemistry and photobiology.

[52]  N. Krinsky Chapter 5 – THE PROTECTIVE FUNCTION OF CAROTENOID PIGMENTS , 1968 .

[53]  J. Bourdon,et al.  PHOTOSENSITIZED OXIDATION THROUGH STEARATE MONOMOLECULAR FILMS * , 1968, Photochemistry and photobiology.

[54]  A. M. Michelson,et al.  HEMOLYSIS OF HUMAN ERYTHROCYTES BY ACTIVATED OXYGEN SPECIES , 1977, Photochemistry and photobiology.

[55]  N. Krinsky,et al.  EFFECT OF SINGLET OXYGEN QUENCHERS ON OXIDATIVE DAMAGE TO LIPOSOMES INITIATED BY PHOTOSENSITIZATION OR BY RADIOFREQUENCY DISCHARGE , 1974, Photochemistry and photobiology.

[56]  M. Rodgers,et al.  THE PHOTOSENSITIZED FORMATION AND REACTION OF SINGLET OXYGEN, O2*(1Δ), IN AQUEOUS MICELLAR SYSTEMS , 1976 .

[57]  J. Prebble,et al.  SENSITIVITY OF THE ELECTRON TRANSPORT CHAIN OF PIGMENTED AND NON‐PIGMENTED SARCINA MEMBRANES TO PHOTODYNAMIC ACTION , 1973, Photochemistry and photobiology.

[58]  Y. Usui,et al.  Kinetic Studies of Photosensitized Oxygenation by Singlet Oxygen in Aqueous Micellar Solutions , 1978 .

[59]  J. Spikes,et al.  THE EOSIN‐SENSITIZED PHOTOOXIDATION OF SUBSTITUTED PHENYLALANINES AND TYROSINES * , 1977, Photochemistry and photobiology.

[60]  J. Joussot-Dubien,et al.  pH DEPENDENCE OF SINGLET OXYGEN PRODUCTION IN AQUEOUS SOLUTIONS USING TOLUIDINE BLUE AS A PHOTOSENSITIZER , 1975, Photochemistry and photobiology.

[61]  H. Rosenkranz,et al.  A study of the photoinduced mutagenicity of methylene blue. , 1977, Mutation research.

[62]  J. Joussot-Dubien,et al.  pH DEPENDENCE OF SINGLET OXYGEN PRODUCTION IN AQUEOUS SOLUTIONS USING THIAZINE DYES AS PHOTOSENSITIZERS , 1975, Photochemistry and photobiology.

[63]  P. Merkel,et al.  Role of azide in singlet oxygen reactions: Reaction of azide with singlet oxygen. , 1972 .

[64]  T. Ito Some differences between 470 nm and 510 nm in the acridine-orange-sensitized photodynamic actions on yeast cells. , 1973, Mutation research.

[65]  C. Foote,et al.  QUENCHING OF SINGLET OXYGEN * , 1970 .

[66]  T. Wilson,et al.  Quenching of singlet oxygen by tertiary aliphatic amines. Effect of DABCO (1,4-diazabicyclo[2.2.2]octane) , 1968 .

[67]  L. Grossweiner,et al.  PHOTODYNAMIC INACTIVATION OF LYSOZYME BY EOSIN , 1973, Photochemistry and photobiology.

[68]  J. Litwin,et al.  The effect of photosensitizing dyes on the 3H-thymidine incorporation of cells grown in vitro. , 1973, Experimental cell research.

[69]  K. Kamogawa,et al.  A STANDARD SYSTEM TO DETERMINE THE QUANTUM YIELD OF SINGLET OXYGEN FORMATION IN AQUEOUS SOLUTION , 1974 .

[70]  N. Krinsky,et al.  FAILURE OF CONJUGATED OCTAENE CAROTENOIDS TO PROTECT A MUTANT OF SARCINA LUTEA AGAINST LETHAL PHOTOSENSITIZATION , 1970, Photochemistry and photobiology.

[71]  H. Jacob IN VIVO PRODUCTION OF DNA SINGLE‐STRAND BREAKS BY PHOTODYNAMIC ACTION , 1971, Photochemistry and photobiology.

[72]  A. P. Harrison,et al.  Ultraviolet-killing and photodynamic-killing in mutants of Escherichia coli. , 1972, Mutation research.

[73]  E. Lochmann,et al.  The effect of thiopyronine concentration and of temperature on the photodynamic inactivation of Saccharomyces cerevisiae. , 1974, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[74]  Michelinf M. Mathfws-Roth PHOTOSENSITIZATION IN SARCINA LUTE A: DIFFERENT MECHANISMS OF EXOGENOUS AND ENDOGENOUS PHOTOSENSITIZERS , 1977 .

[75]  D. Kearns,et al.  SENSITIZED PHOTOOXYGENATION REACTIONS AND THE ROLE OF SINGLET OXYGEN†,‡ , 1969, Photochemistry and photobiology.

[76]  A. Lamola,et al.  REACTIVITY OF CHOLESTEROL AND SOME FATTY ACIDS TOWARD SINGLET OXYGEN , 1974, Photochemistry and photobiology.

[77]  T. Yamane,et al.  Cholesterol Hydroperoxide Formation in Red Cell Membranes and Photohemolysis in Erythropoietic Protoporphyria , 1973, Science.

[78]  D. Kearns,et al.  A REMARKABLE DEUTERIUM EFFECT ON THE RATE OF PHOTOSENSITIZED OXIDATION OF ALCOHOL DEHYDROGENASE AND TRYPSIN , 1973, Photochemistry and photobiology.

[79]  N. I. Churakova,et al.  PHOTO‐OXIDATION OF LYSOZYME IN THE PRESENCE OF METHYLENE BLUE: A PROBABLE MECHANISM , 1973 .

[80]  T. Kimura,et al.  Reactivity of singlet molecular oxygen with cholesterol in a phospholipid membrane matrix. A model for oxidative damage of membranes. , 1977, Biochemical and biophysical research communications.

[81]  I. Pietsch,et al.  Über die RSN-Synthese bei Saccharomyces-Zellen nach photodynamischer Behandlung und nach Röntgenbestrahlung , 1973 .

[82]  P. Merkel,et al.  UNAMBIGUOUS EVIDENCE FOR THE PARTICIPATION OF SINGLET OXYGEN ( 1 δ) IN PHOTODYNAMIC OXIDATION OF AMINO ACIDS , 1972, Photochemistry and photobiology.

[83]  D. Freifelder,et al.  Mechanism of photoinactivation of coliphage T-7 sensitized by acridine orange. , 1966, Virology.

[84]  G Swanbeck,et al.  PRIMARY MECHANISMS OF ERYTHROCYTE PHOTOLYSIS INDUCED BY BIOLOGICAL SENSITIZERS AND PHOTOTOXIC DRUGS , 1975, Photochemistry and photobiology.

[85]  A. Lamola,et al.  ON THE QUENCHING OF SINGLET OXYGEN BY α‐TOCOPHEROL , 1974 .

[86]  N. Krinsky,et al.  A COMPARATIVE STUDY OF PHOTODYNAMIC OXIDATION AND RADIOFREQUENCY‐DISCHARGE‐GENERATED 1O2 OXIDATION OF GUANOSINE , 1973, Photochemistry and photobiology.

[87]  Y. Lion,et al.  New method of detecting singlet oxygen production , 1976, Nature.

[88]  G. Jori,et al.  THE EFFECT OF CHEMICAL STRUCTURE ON THE PHOTOSENSITIZING EFFICIENCIES OF PORPHYRINS , 1977, Photochemistry and photobiology.

[89]  W. Harm Dark repair of acridine dye-sensitized photoeffects in E. coli cells and bacteriophage. , 1968, Biochemical and biophysical research communications.

[90]  J. Howard,et al.  Autoxidation and Photooxidation of 1,3-Diphenylisobenzofuran: A Kinetic and Product Study , 1975 .

[91]  H. Jacob PHOTO‐OXIDATION SENSITIZED BY METHYLENE BLUE, THIOPYRONINE, AND PYRONINE‐IV. THE BEHAVIOUR OF THIOPYRONINE IN SUSPENSIONS OF BACTERIA * , 1974 .

[92]  D. Macphee,et al.  Induction of base-pair substitution and frameshift mutations in wild-type and repair-deficient strains of Salmonella typhimurium by the photodynamic action of methylene blue. , 1975, Mutation research.

[93]  W. G. Martin,et al.  DIFFERENTIAL EFFECTS OF NEAR‐UV AND VISIBLE LIGHT ON ACTIVE TRANSPORT AND OTHER MEMBRANE PROCESSES IN ESCHERICHIA COLI * , 1976, Photochemistry and photobiology.

[94]  N. Krinsky,et al.  CAROTENOID CHROMOPHORE LENGTH AND PROTECTION AGAINST PHOTOSENSITIZATION , 1974, Photochemistry and photobiology.

[95]  M. Hamann,et al.  PHOTODYNAMIC ALTERATIONS OF THE CELL ENVELOPE OF PROTEUS MIRABILIS AND THEIR REPAIR , 1975, Photochemistry and photobiology.

[96]  P. Merkel,et al.  Deuterium effects on singlet oxygen lifetimes in solutions. New test of singlet oxygen reactions , 1972 .

[97]  J. Regan,et al.  THE EFFECT OF PROFLAVINE PLUS VISIBLE LIGHT ON THE DNA OF HUMAN CELLS * , 1977, Photochemistry and photobiology.

[98]  I. Saito,et al.  OCCURRENCE OF THE SINGLET‐OXYGEN MECHANISM IN PHOTODYNAMIC OXIDATIONS OF GUANOSINE * , 1975, Photochemistry and photobiology.

[99]  R. Kaplan,et al.  [Photodynamic mutation induction and inactivation in Serratia phages kappa by methylene blue and light]. , 1967, Molecular & general genetics : MGG.