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In vitro assessment of the toxicity of metal compounds

IV. Disposition of metals in cells: Interactions with membranes, glutathione, metallothionein, and DNA

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Abstract

This review has focused on several parameters related to the delivery of carcinogenic metal compounds to the cell nucleus as a basis for understanding the intermediates formed between metals and cellular components and the effect of these intermediates on DNA structure and function. Emphasis has been placed on metal interactions at the cellular membrane, including lipid peroxidation, metal interactions with glutathione and their relation to membrane injury, and metal effects on the membrane bound enzyme, Na+/K+ ATPase. Metal binding to metallothionein is also considered, particularly as related to transport and utilization of metal ions and to genetic defects in these processes exemplified in Menkes disease. The ability of cadmium to induce the synthesis of metallothionein more strongly than zinc is also discussed in relation to other toxic and carcinogenic metals. The effects of metal ions on purified DNA and RNA polymerase systems are presented with some of the recent studies using biological ligand-metal complexes. This review points out the importance of considering how metals affect in vitro systems when presented as ionic forms or complexed to relevant biological ligands.

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References

  1. J. D. Heck and M. Costa,Biol. Trace Elem. Res. 4, 71 (1982).

    CAS  Google Scholar 

  2. J. D. Heck and M. Costa,Biol. Trace Elem. Res. 4, 319 (1982).

    CAS  Google Scholar 

  3. N. T. Christie and M. Costa,Biol. Trace Elem. Res. 5, 55 (1983).

    CAS  Google Scholar 

  4. Y. Hiroshige,Tohoku J. Exp. Med. 130, 385 (1980).

    PubMed  CAS  Google Scholar 

  5. M. A. Amoruso, G. Witz, and B. D. Goldstein,Toxicol. Lett. 10, 133 (1982).

    PubMed  CAS  Google Scholar 

  6. B. L. Vallee and D. D. Ulmer,Ann. Rev. Biochem. 41, 91 (1972).

    PubMed  CAS  Google Scholar 

  7. A. Furst, inAdvances in Modern Toxicology, H. F. Kraybill and M. A. Mehlman, eds., Hemisphere, Washington, DC, 1977, Vol. 3, pp. 209–229.

    Google Scholar 

  8. O. Cantoni, R. M. Evans, and M. Costa,Biochem. Biophys. Res. Commun. 108, 614 (1982).

    PubMed  CAS  Google Scholar 

  9. N. T. Christie, O. Cantoni, and M. Costa,The Toxicologist, p. 26 (1983).

  10. M. Webb, inClinical Chemistry and Chemical Toxicology of Metals, S. S. Brown, ed., Elsevier, Amsterdam, 1977 pp. 51–64.

    Google Scholar 

  11. M. Chvapil,Life Sci. 13, 1041 (1973).

    PubMed  CAS  Google Scholar 

  12. J. Southard, P. Nitisewojo, and D. E. Green,Fed. Proc. 33, 2147 (1974).

    PubMed  CAS  Google Scholar 

  13. B. Chin, G. S. Lesowitz, and I. A. Bernstein,Environ. Res. 16, 432 (1976).

    Google Scholar 

  14. J. S. Bus, and J. E. Gibson,Reviews in Biochemical Toxicology, Hodgson, Bend, and Philpot, eds. 1979 pp. 125.

  15. T. K. Shires,Biochem. J. 205, 321 (1982).

    PubMed  CAS  Google Scholar 

  16. S. R. Ribarov, L. C. Benov, and J. C. Benchev,Biochim. Biophys. Acta 664, 453 (1981).

    PubMed  CAS  Google Scholar 

  17. V. F. Fairbanks,Arch Intern. Med. 120, 428 (1967).

    PubMed  CAS  Google Scholar 

  18. J. M. Salhary, J. C. Swanson, K. A. Cordes, S. B. Gaines, and K. C. Gaines,Biochem. Biophys. Res. Commun. 82, 1294 (1978).

    Google Scholar 

  19. Wills, E. D.,Biochim. Biophys. Acta 640, 721 (1965).

    Google Scholar 

  20. N. H. Stacey and C. D. Klassen,J. Toxicol. Environ. Health 7, 149 (1981).

    PubMed  CAS  Google Scholar 

  21. N. H. Stacey and H. Kappas,Toxicol. Appl. Pharmacol. 63, 29 (1982).

    PubMed  CAS  Google Scholar 

  22. S. Gabor, Z. Anca, and E. Bordas,Rev. Roum. Biochim. 15, 113 (1978).

    CAS  Google Scholar 

  23. N. H. Stacey, L. R. Cantilena, Jr., and C. D. Klassen,Tox. Appl. Pharmacol. 53, 470 (1980).

    CAS  Google Scholar 

  24. A. Azar, H. J. Trochiomowicz, and M. E. Maxfield, inEnvironmental Health Aspects of Lead, D. Berth, A. Berlin, R. Engel, P. Recht, and J. Smeets, eds., Amsterdam, The Netherlands, 1972, pp. 199–210.

  25. G. Kazantis,Environ. Health. Perspect. 40, 143 (1981).

    Google Scholar 

  26. M. Hasan and S. F. Ali,Toxicol. Appl. Pharmacol. 57, 8 (1981).

    PubMed  CAS  Google Scholar 

  27. F. W. Sunderman, Jr.,Fed. Proc. 37, 40 (1978).

    PubMed  CAS  Google Scholar 

  28. F. W. Sunderman, Jr.,Environ. Health Perspec. 40, 131 (1981).

    CAS  Google Scholar 

  29. R. L. Post, C. R. Merritt, C. R. Kinsolving, and C. D. Albright,J. Biol. Chem. 235, 1796 (1960).

    PubMed  CAS  Google Scholar 

  30. S. L. Bonting and L. L. Caravaggio,Arch. Biochem. Biophys. 101, 37 (1963).

    CAS  Google Scholar 

  31. P. D. Beck, D. P. Tirchudy, L. A. Shipley, J. G. Waggoner, and N. I. Berlin,Am. J. Med. 48, 137 (1970).

    Google Scholar 

  32. S. R. V. Raghavan, B. Culver, and H. C. Gonick,J. Toxicol. Environ. Health 7, 561 (1981).

    PubMed  CAS  Google Scholar 

  33. C. N. Ong and W. R. Lee,Brit. J. Indust. Med. 37, 78 (1980).

    CAS  Google Scholar 

  34. M. L. Caspers and G. J. Siegel,Biochim. Biophys. Acta 600, 27 (1980).

    PubMed  CAS  Google Scholar 

  35. G. J. Siegel, S. K. Fogt, and S. Iyengar,J. Biol. Chem. 253, 7207 (1978).

    PubMed  CAS  Google Scholar 

  36. A. Meister,Trends Biochem. Sci. 6, 1 (1981).

    Google Scholar 

  37. D. L. Rabenstein, R. Guevremont, and C. A. Evans, inMetal Ions in Biological Systems, H. Sigel, ed., 9, 104–138 (1979).

  38. C. C. Tseu and A. L. Tappel,J. Biol. Chem. 233, 1230 (1958).

    Google Scholar 

  39. B. J. Fahr and D. L. Rabenstein,J. Amer. Chem. Soc. 95, 6944 (1973).

    Google Scholar 

  40. N. Martin, R. B. Martin, and J. T. Edsall,J. Amer. Chem. Soc. 18, 4044 (1959).

    Google Scholar 

  41. G. K. Oster,Nature 234, 153 (1971).

    PubMed  CAS  Google Scholar 

  42. M. M. David, R. Sperling, and I. Z. Steinberg,Biochim. Biophys. Acta 359, 101 (1974).

    PubMed  CAS  Google Scholar 

  43. R. Cecil and J. R. McPhee,Biochem. J. 66, 538 (1957).

    PubMed  CAS  Google Scholar 

  44. A. McAuley and M. A. Olatunjii,Can. J. Chem. 55, 3328 (1977).

    CAS  Google Scholar 

  45. J. Aaseth, J. Alexander, and T. Norseth,Acta Pharmacol. Toxicol. 50, 310 (1982).

    CAS  Google Scholar 

  46. S. J. Gray and K. Sterling,J. Clin. Invest. 29, 1604 (1950).

    PubMed  CAS  Google Scholar 

  47. S. Kitagawa, H. Seki, F. Kametani, and H. Sakurai,Chem-Biol. Interactions 40, 265 (1982).

    CAS  Google Scholar 

  48. K. W. Jennette,Environ. Health Perspect. 40, 233 (1981).

    PubMed  CAS  Google Scholar 

  49. G. W. Rafter,Biol. Trace Element Res. 4, 191 (1982).

    CAS  Google Scholar 

  50. R. B. Martin, inMetal Ions in Biological Systems, H. Sigel, ed., Dekker, New York, Vol. I, 1974, p. 129.

    Google Scholar 

  51. R. B. Martin, M. Chamberlin, and J. T. Edsall,J. Amer. Chem. Soc. 82, 495 (1960).

    CAS  Google Scholar 

  52. B. Jezowska-Trzebiatowska, G. Formicha-Kozlowska, and H. Kozlowski,J. Inorg. Nucl. Chem. 39, 1265 (1977).

    CAS  Google Scholar 

  53. H. Rupp and U. Weser,FEBS Lett. 44, 293 (1974).

    PubMed  CAS  Google Scholar 

  54. T. L. Sayer, S. Backs, C. A. Evans, E. K. Millar, and D. L. Rabenstein,Can. J. Chem. 55, 3255 (1977).

    CAS  Google Scholar 

  55. K. D. Gibson, A. Neubergen, and J. J. Scott,Biochim. J. 61, 618 (1955).

    CAS  Google Scholar 

  56. J. M. Hsu,J. Nutr. 111, 26 (1981).

    PubMed  CAS  Google Scholar 

  57. W. Stricks and I. M. Kolthoff,J. Amer. Chem. Soc. 75, 5673 (1953).

    CAS  Google Scholar 

  58. N. Ballatori and T. W. Clarkson,Science 216, 61 (1982).

    PubMed  CAS  Google Scholar 

  59. T. Refsvik and T. Norseth,Acta Pharmacol. Toxicol. 36, 67 (1975).

    CAS  Google Scholar 

  60. R. Richardson and S. Murphy,Toxicol. Appl. Pharm. 31, 505 (1975).

    CAS  Google Scholar 

  61. J. R. Mitchell, D. J. Jollow, W. Z. Potter, J. R. Gillette, and B. B. Brodie,J. Pharmacol. Exp. Ther. 187, 211 (1973).

    PubMed  CAS  Google Scholar 

  62. J. M. Williams, B. Boettcher, and A. Meister,Proc. Natl. Acad. Sci. 79, 6246 (1982).

    Google Scholar 

  63. D. Pessayne, A. Dolder, J. Y. Artigou, J. C. Wandscheer, V. Descatoire, C. Degott, and J. D. Benhamon,Gastroenterology 77, 264 (1979).

    Google Scholar 

  64. D. L. Rabenstein and C. A. Evans,Bioinorg. Chem. 8, 107 (1978).

    PubMed  CAS  Google Scholar 

  65. S. T. Chow, C. A. McAuliffe, and B. J. Sayle,J. Inorg. Nucl. Chem. 37, 451 (1975).

    CAS  Google Scholar 

  66. M. Webb and K. Cain,Biochem. Pharmacol. 31, 137 (1982).

    PubMed  CAS  Google Scholar 

  67. D. Price and J. G. Joshi,Proc. Natl. Acad. Sci. 79, 3116 (1982).

    PubMed  CAS  Google Scholar 

  68. H. S. Jones and B. A. I. Fowler,Ann. NY Acad. Sci. 355, 309 (1980).

    PubMed  CAS  Google Scholar 

  69. T. Miyahara, M. Miyakoshi, Y. Saito, and T. Kosuka,Toxicol. Appl. Pharmacol. 55, 477 (1980).

    PubMed  CAS  Google Scholar 

  70. M. Lucassen and B. Sarkar,J. Toxicol. Environ. Health 5, 897 (1979).

    PubMed  CAS  Google Scholar 

  71. S. L. Guthans and W. T. Morgan,Arch. Biochem. Biophys. 218, 320 (1982).

    PubMed  CAS  Google Scholar 

  72. T. Terao and C. A. Owen, Jr.,Tohoku J. Exp. Med. 120, 209 (1976).

    PubMed  CAS  Google Scholar 

  73. C. A. Owen, Jr.,Am. J. Physiol. 209, 900 (1965).

    PubMed  CAS  Google Scholar 

  74. N. Marceau and N. Aspin,Am. J. Physiol. 222, 106 (1972).

    PubMed  CAS  Google Scholar 

  75. N. Marceau and N. Aspin,Biochim. Biophys. Acta 328 351 (1973).

    PubMed  CAS  Google Scholar 

  76. N. Marceau and N. Aspin,Biochim. Biophys. Acta 328, 338 (1973).

    PubMed  CAS  Google Scholar 

  77. H. S. Hsieh and E. Frieden,Biochem. Biophys. Res. Commun. 67, 1326 (1975).

    PubMed  CAS  Google Scholar 

  78. M. C. Linder and J. R. Moor,Biochim. Biophys. Acta 499, 329 (1977).

    PubMed  CAS  Google Scholar 

  79. A. O. Udom and F. O. Brady,Biochem. J. 187, 329 (1980).

    PubMed  CAS  Google Scholar 

  80. T. Y. Li, A. J. Kraker, C. F. Shaw, and D. H. Petering,Proc. Natl. Acad. Sci. 77, 6334 (1980).

    PubMed  CAS  Google Scholar 

  81. K. Lerch,Nature 284, 368 (1980).

    PubMed  CAS  Google Scholar 

  82. J. E. Balthrop, C. T. Dameron, and E. D. Harris,Biochem. J. 204, 541 (1982).

    PubMed  CAS  Google Scholar 

  83. T. Terao and C. A. Owen, Jr.,Mayo Clin. Proc. 49, 376 (1974).

    PubMed  CAS  Google Scholar 

  84. W. Levinson, J. Idriss, and J. Jackson,Biol. Trace Elem. Res. 1, 15 (1979).

    CAS  Google Scholar 

  85. J. H. Menkes, M. Alter, G. K. Steigleder, D. R. Weakley, and J. H. Sung,Pediatrics 29, 764 (1962).

    PubMed  CAS  Google Scholar 

  86. D. M. Danks, P. E. Campbell, B. J. Stevens, V. Mayne, and E. Cartwright,Pediatrics 50, 188 (1972).

    PubMed  CAS  Google Scholar 

  87. N. Horn, K. Keydorn, E. Damsgaard, J. Tygstrup, and S. Vestermark,Clin. Genet. 14, 186 (1978).

    PubMed  CAS  Google Scholar 

  88. D. M. Danks, B. J. Stevens, P. E. Campbell, E. C. Cartwright, J. M. Gillespie, R. R. W. Townley, J. A. Walker-Smith, J. Bloomfield, B. B. Turner, and V. Mayne,Birth Defects 10, 132–137 (1974).

    CAS  PubMed  Google Scholar 

  89. N. A. Holtzman,Fed. Proc. 35, 2276 (1976).

    PubMed  CAS  Google Scholar 

  90. A. D. Garnica, J. L. Frias, and O. M. Rennert,Clin. Genet. 11, 154 (1977).

    Article  PubMed  CAS  Google Scholar 

  91. G. U. LaBadie, N. G. Beratis, P. M. Price, and K. Hirschborn,J. Cell. Physiol. 106, 173 (1981).

    PubMed  CAS  Google Scholar 

  92. R. F. Bonewitz, Jr. and R. R. Howell,J. Cell Physiol. 106, 339 (1981).

    PubMed  CAS  Google Scholar 

  93. J. R. Riordan and L. Jolicoeur-Paquet,J. Biol. Chem. 257, 4639 (1982).

    PubMed  CAS  Google Scholar 

  94. J. Otvos and J. M. Armitage,Proc. Natl. Acad. Sci. 77 7094 (1980).

    PubMed  CAS  Google Scholar 

  95. M. Vašák and J. H. R. Kägi,Proc. Natl. Acad. Sci. 78, 6709 (1981).

    PubMed  Google Scholar 

  96. Y. Boulanger, C. M. Goodman, C. P. Forte, S. W. Fesik, and I. M. Armitage,Proc. Natl. Acad. Sci. 80, 1051 (1982).

    Google Scholar 

  97. R. W. Briggs and I. M. Armitage,J. Biol. Chem. 257, 1259 (1982).

    PubMed  CAS  Google Scholar 

  98. R. H. O. Bühler and J. H. R. Kägi,FEBS Lett. 39, 229 (1977).

    Google Scholar 

  99. K. T. Suzuki and S. Yamamura,Toxicol. Lett. 6, 301 (1980).

    PubMed  CAS  Google Scholar 

  100. I. Maiti, M. Mbikay, C. Margeno and J. Thirion,J. Cell. Physiol. 112, 35 (1982).

    PubMed  CAS  Google Scholar 

  101. K. G. Danielson, S. Ohi, and P. C. Huang,Proc. Natl. Acad. Sci. 79, 2301 (1982).

    PubMed  CAS  Google Scholar 

  102. C. D. Klaassen,Am. J. Physiol. 234, E47 (1978).

    PubMed  CAS  Google Scholar 

  103. D. Holt, L. Magos, and M. Webb,Chem.-Biol. Interact. 32, 125 (1980).

    PubMed  CAS  Google Scholar 

  104. M. Vašák, J. H. R. Kägi, B. Holmquist, and B. L. Vallee,Biochem. 20, 6659 (1981).

    Google Scholar 

  105. J. K. Piotrowski and J. A. Szymanska,J. Tox. Environ. Health 1, 991 (1976).

    CAS  Google Scholar 

  106. R. M. Evans, S. R. Patierno, D. Wang, O. Cantoni, and M. Costa,Mol. Pharmacol. 24, 77 (1983).

    PubMed  CAS  Google Scholar 

  107. S. Z. Cagen and C. D. Klaassen,Toxicol. Appl. Pharmacol. 51, 107 (1979).

    PubMed  CAS  Google Scholar 

  108. M. Margoshes and B. L. Vallee,J. Am. Chem. Soc. 79, 4813 (1957).

    CAS  Google Scholar 

  109. E. J. Underwood,Trace Elements in Human and Animal Nutrition, Academic Press, NY, 1977.

    Google Scholar 

  110. C. E. Hildebrand, R. A. Tobey, E. W. Campbell, and M. D. Enger,Exp. Cell. Res. 124, 237 (1979).

    PubMed  CAS  Google Scholar 

  111. S. A. Roberts and R. C. Schnell,Res. Comm. Chem. Path. Pharmacol. 35, 349 (1982).

    CAS  Google Scholar 

  112. K. Waku, F. Hayakawa, and Y. Nakazawa,Arch. Biochem. Biophys. 204, 288 (1980).

    PubMed  CAS  Google Scholar 

  113. M. G. Cherian and R. A. Goger,Life Sci. 23, 1 (1978).

    PubMed  CAS  Google Scholar 

  114. C. Tohyama, Z. A. Shaikh, K. J. Ellis, and S. H. Cohn,Toxicology 22, 181 (1981).

    PubMed  CAS  Google Scholar 

  115. C. Tohyama and Z. A. Shaikh,Fund. Appl. Toxicol. 1, 1 (1981).

    CAS  Google Scholar 

  116. C. Tohyama, Z. A. Shaikh, K. Nogawa, E. Kobayashi, and R. Honda,Toxicology 20, 289 (1981).

    PubMed  CAS  Google Scholar 

  117. J. H. R. Kägi and M. Nordberg, eds., inMetallothionein, Experimentia Suppl. 34, Birkhauser Verlag, Basel, 1979.

    Google Scholar 

  118. Y. Suzuki,J. Toxicol. Environ. Health 7, 251 (1981).

    Article  PubMed  CAS  Google Scholar 

  119. C. Tohyama, Z. A. Shaikh, K. Nogawa, E. Kobayashi, and R. Honda,Arch. Toxicol. 50, 159 (1982).

    PubMed  CAS  Google Scholar 

  120. M. A. Sirover and L. A. Loeb,Science 194, 1434 (1976).

    PubMed  CAS  Google Scholar 

  121. M. A. Sirover and L. A. Loeb,J. Biol. Chem. 252, 3605 (1977).

    PubMed  CAS  Google Scholar 

  122. J. McCann, E. Choi, E. Yamasaki, and B. E. Ames,Proc. Natl. Acad. Sci. 72, 5135 (1975).

    PubMed  CAS  Google Scholar 

  123. L. Haroun and B. E. Ames, inShort-term Tests for Chemical Carcinogens, H. F. Stach and R. H. C. San, eds., 1981, pp. 108–119.

  124. S. Venitt and L. S. Levy,Nature 250, 493 (1974).

    PubMed  CAS  Google Scholar 

  125. O. Cantoni and M. Costa,Mol. Pharmacol 24, 84 (1983).

    PubMed  CAS  Google Scholar 

  126. J. E. Lee, R. B. Cacarelli, and K. W. Jennette,Biochem. 21, 771 (1982).

    CAS  Google Scholar 

  127. S. K. Niyogi and R. P. Feldman, Nucleic Acids Res. 9, 2615 (1981).

    PubMed  CAS  Google Scholar 

  128. R. M. Izatt, J. J. Christensen, and J. Howard Rytting,Chem. Rev. 71, 439 (1971).

    PubMed  CAS  Google Scholar 

  129. D. Banerjee, S. Onosaka, and G. Cherian,Toxicology 24, 95 (1982).

    PubMed  CAS  Google Scholar 

  130. S. K. Niyogi, R. D. Feldman, and D. J. Hoffman,Toxicology 22, 9 (1981).

    PubMed  CAS  Google Scholar 

  131. F. W. Sunderman, Jr., inAdvances in Modern Toxicology, R. A. Goyer and M. A. Mehlman, eds., vol. 2, Hemisphere, Washington, DC, p. 257, 1977.

    Google Scholar 

  132. S. Ahrland, inStructure and Bonding, vol. 5, Springer-Verlag, New York, 1968, p. 118.

    Google Scholar 

  133. M. W. Williams, J. D. Hoeschele, J. E. Turner, K. Bruce Jacobson, N. T. Christie, C. L. Paton, L. H. Smith, H. R. Witschi, and E. H. Lee,Toxicol. Appl. Pharmacol. 63, 461 (1982).

    PubMed  CAS  Google Scholar 

  134. M. M. Jones and W. K. Vaughn,J. Inorg. Nucl. Chem. 40, 2081 (1978).

    CAS  Google Scholar 

  135. E. Nieboer and D. H. S. Richardson,Environ. Pollut. Ser. B 1, 3 (1980).

    CAS  Google Scholar 

  136. R. A. Zakour, T. A. Kunkel, and L. A. Loeb,Environ. Health Perspect. 40, 197 (1981).

    PubMed  CAS  Google Scholar 

  137. S. Okada, H. Ohba, and M. Taniyama,J. Inorg. Biochem. 15, 223 (1981).

    PubMed  CAS  Google Scholar 

  138. S. Okada, M. Taniyama, and H. Ohba,J. Inorg. Biochem. 17, 41 (1982).

    PubMed  CAS  Google Scholar 

  139. M. Costa and H. H. Mollenhauer,Science 209, 515 (1980).

    PubMed  CAS  Google Scholar 

  140. M. J. Tsapakos, T. H. Hampton, and K. W. Jennette,J. Biol. Chem. 256, 3623 (1981).

    PubMed  CAS  Google Scholar 

  141. R. B. Ciccarelli and K. E. Wetterhahn,Cancer Res. 42, 3544 (1982).

    PubMed  CAS  Google Scholar 

  142. C. M. Ireland, A. Eastman, and E. Bresnick,Biochem. Biophys. Res. Commun. 109, 1291 (1982).

    Article  PubMed  CAS  Google Scholar 

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  1. Nelwyn T. Christie

    Present address: Division of Pediatrics, Department of Experimental Pediatries, M. D. Anderson Hospital and Tumor Institute, 77033, Houston, TX

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  1. Department of Pharmacology, University of Texas Medical School at Houston, PO Box 20708, 77025, Houston, Texas

    Nelwyn T. Christie & Max Costa

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Christie, N.T., Costa, M. In vitro assessment of the toxicity of metal compounds. Biol Trace Elem Res 6, 139–158 (1984). https://doi.org/10.1007/BF02916931

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