Singlet oxygen: a primary effector in the ultraviolet A/near-visible light induction of the human heme oxygenase gene.

Both singlet oxygen and the hydroxyl radical are generated in mammalian cells by UVA (320-380 nm) and possibly near-visible (380-420 nm) radiation. We have modulated the cellular levels of these two reactive oxygen species in order to compare their involvement in the induction of the human heme oxygenase (HO) gene by broad spectrum UVA/near-visible light (UVA/NVL). Irradiation in deuterium oxide (in which singlet oxygen has a longer half-life) enhances the broad spectrum UVA/NVL induction of this gene. Sodium azide and L-histidine which are scavengers of both singlet oxygen and the hydroxyl radical reduce the fluence-dependent accumulation of HO mRNA, while compounds which are only hydroxyl radical scavengers, namely, mannitol and dimethyl sulfoxide do not. Rose Bengal, a known generator of singlet oxygen, also increases the HO mRNA levels, and this induction is enhanced in deuterium oxide. We conclude that the observed effects of deuterium oxide and singlet oxygen scavengers on HO mRNA levels are not due to a nonspecific effect on transcription but that singlet oxygen is a primary effector in the UVA/NVL induction of the human heme oxygenase gene.

[1]  M. Maines.  Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications , 1988, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[2]  R. Tyrrell,et al.  New trends in photobiology. The interaction of UVA radiation with cultured cells. , 1990, Journal of photochemistry and photobiology. B, Biology.

[3]  F. Wilkinson,et al.  Rate constants for the decay and reactions of the lowest electronically excited singlet state of molecular oxygen in solution , 1981 .

[4]  Sirshendu Chatterjee,et al.  Membrane lipid peroxidation by UV‐A: mechanism and implications , 1990, Biotechnology and applied biochemistry.

[5]  J. A. Badwey,et al.  Active oxygen species and the functions of phagocytic leukocytes. , 1980, Annual review of biochemistry.

[6]  A. Cederbaum,et al.  Production of formaldehyde during metabolism of dimethyl sulfoxide by hydroxyl radical generating systems. , 1981, Biochemistry.

[7]  R. Tyrrell,et al.  SINGLET OXYGEN INVOLVEMENT IN THE INACTIVATION OF CULTURED HUMAN FIBROBLASTS BY UVA (334 nm, 365 nm) AND NEAR‐VISIBLE (405 nm) RADIATIONS , 1989, Photochemistry and photobiology.

[8]  R. Tyrrell,et al.  Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Tyrrell,et al.  Cellular Defense Against UVA (320–380 nm) and UVB (290–320 nm) Radiations , 1991 .

[10]  Farhataziz,et al.  Selected specific rates of reactions of transients from water in aqueous solution. III. Hydroxyl radical and perhydroxyl radical and their radical ions , 1977 .

[11]  M. Rodgers,et al.  Determination of the lifetime of singlet oxygen in water-d2 using 9,10-anthracenedipropionic acid, a water-soluble probe , 1980 .

[12]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[13]  S. Shibahara,et al.  Human heme oxygenase cDNA and induction of its mRNA by hemin. , 1988, European journal of biochemistry.

[14]  R. Tyrrell,et al.  Both near ultraviolet radiation and the oxidizing agent hydrogen peroxide induce a 32-kDa stress protein in normal human skin fibroblasts. , 1987, The Journal of biological chemistry.

[15]  S. Chatterjee,et al.  UV-A induced lipid peroxidation in liposomal membrane , 1989, Radiation and environmental biophysics.

[16]  C. Harris,et al.  Differential control by platelet factors of squamous differentiation in normal and malignant human bronchial epithelial cells. , 1983, Cancer research.

[17]  R. Tyrrell,et al.  Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts , 1990, Molecular and cellular biology.

[18]  A. Singh.  Chemical and biochemical aspects of superoxide radicals and related species of activated oxygen. , 1982, Canadian journal of physiology and pharmacology.

[19]  H. Kohno,et al.  The human 32‐kDa stress protein induced by exposure to arsenite and cadmium ions is heme oxygenase , 1989, FEBS letters.

[20]  J. McCord,et al.  Superoxide‐dependent production of hydroxyl radical catalyzed by iron—EDTA complex , 1978, FEBS letters.

[21]  T. Dahl,et al.  COMPARISON OF PHOTODYNAMIC ACTION BY ROSE BENGAL IN GRAM‐POSITIVE AND GRAM‐NEGATIVE BACTERIA , 1988, Photochemistry and photobiology.

[22]  L. Dubertret,et al.  UVA-induced lipid peroxidation in cultured human fibroblasts. , 1991, Biochimica et biophysica acta.

[23]  R. Tyrrell,et al.  Quantitative differences in host cell reactivation of ultraviolet-damaged virus in human skin fibroblasts and epidermal keratinocytes cultured from the same foreskin biopsy. , 1986, Cancer research.

[24]  石澤 志信.  Induction of heme oxygenase in rat liver , 1983 .

[25]  T. Dahl,et al.  Partition of rose bengal anion from aqueous medium into a lipophilic environment in the cell envelope of Salmonella typhimurium: implications for cell-type targeting in photodynamic therapy. , 1989, Journal of photochemistry and photobiology. B, Biology.

[26]  I. Fridovich,et al.  A mechanism for the production of ethylene from methional. The generation of the hydroxyl radical by xanthine oxidase. , 1970, The Journal of biological chemistry.

[27]  A. Johnsson,et al.  AN ACTION SPECTRUM FOR BLUE AND NEAR ULTRAVIOLET IN ACTIVATION OF Propionibacterium acnes; WITH EMPHASIS ON A POSSIBLE PORPHYRIN PHOTOSENSITIZATION , 1986, Photochemistry and photobiology.

[28]  W. R. Midden,et al.  Singlet oxygen generation for solution kinetics: clean and simple , 1983 .

[29]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[30]  L. G. Davis,et al.  Basic methods in molecular biology , 1986 .

[31]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[32]  R. Tyrrell,et al.  Induction of the heme oxygenase gene in human skin fibroblasts by hydrogen peroxide and UVA (365 nm) radiation: evidence for the involvement of the hydroxyl radical. , 1990, Carcinogenesis.

[33]  R. W. Tuveson,et al.  SENSITIVITY OF HemA MUTANT Escherichia coli CELLS TO INACTIVATION BY NEAR‐UV LIGHT DEPENDS ON THE LEVEL OF SUPPLEMENTATION WITH δ‐AMINOLEVULINIC ACID , 1986, Photochemistry and photobiology.

[34]  S. Koga,et al.  Mechanism for the generation of superoxide anion and singlet oxygen during heme compound-catalyzed linoleic acid hydroperoxide decomposition. , 1991, Archives of biochemistry and biophysics.