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Indole derivatives in vegetables of the cruciferae family

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Abstract

The chemical background of the biological activities of vegetables of the Cruciferae family is considered. These vegetables contain alkaloids of the glucobrassicin group that are decomposed by the enzyme myrosinase (thioglucosidase, EC 3.2.3.1) released upon damage to the plant cells. This results in several indole derivatives, with ascorbigen and indole-3-carbinol predominating. In the gastrointestinal tract, these compounds form 5H,11H-indolo[3,2-b]carbazole, a natural ligand of the aromatic hydrocarbon receptor (Ah receptor) and a functional analogue of 2,3,7,8-tetrachlorodibenzo-p-dioxin, a dangerous xenobiotic. The indolocarbazole—Ah receptor complex activates the gene of CYP1A1, an isoenzyme of cytochrome P450-dependent monoamine oxidase, which enhances the 2-hydroxylation (inactivation) of estrogens. In its turn, the resulting lowered level of estrogens inhibits the growth of hormone-dependent tumors or prevents their appearance. The mechanism of xenobiotic inactivation, underlying the anticarcinogenic action of food products including vegetables of the Cruciferae family and some homogeneous indole compounds, is similar. Some other effects of nutrient indole compounds, e.g., the inhibition of expression of the cyclin-dependent kinase 6 (CDK6) by indole-3-carbinol that leads to the cell cycle arrest in G1 phase, are also considered. Analysis of the biological effects of the Cruciferae diet has helped start clinical studies of indole-3-carbinol as an antitumor and anticarcinogenic remedy for patients with a high risk of tumor diseases.

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Abbreviations

AA:

L-ascorbic acid

AFB1 :

aflatoxin B1

Ah receptor:

receptor of aromatic hydrocarbons

ASG:

ascorbigen (i.e., 2-(3-indolyl)methyl-α-L-threo-L-glycero-3-hexulosofuranosono-γ-lactone)

CDK:

cyclin-dependent kinase 6

CTr:

cyclic trimer of methyleneindolenine

CYP1A1:

cytochrome P4501A1-dependent monoamine oxidase

diFICZ:

6,12-diformylindolo[3,2-b]carbazole

DIM:

3,3′-diindolylmethane

diMeICZ:

5,11-dimethylindolo[3,2-b]carbazole

DMBA:

dimethylbenzanthracene

EROD:

ethoxyresorufinO-deethylase

FICZ:

6-formylindolo[3,2-b]carbazole

FMO1:

flavin-dependent monoamine oxidase

GB:

alkaloid glucobrassicin

13C:

indole-3-carbinol

ICZ:

5H,11H-indolo[3,2-b]carbazole

Ind-sorbose:

1-deoxy-1-(3-indolyl)-α-L-sorbopyranose

Ind-tagatose:

1-deoxy-1-(3-indolyl)-α-L-tagatopyranose

LTr:

linear trimer of methyleneindolenine

MDR:

multiple drug resistance

neo-ASG:

neoascorbigen

neo-DIM:

3,3′-di-N-methoxyindolylmethane

neo-GB:

neoglucobrassicin

TCDD:

2,3,7,8-tetrachlorodibenzo-p-dioxin

References

  1. Graham, S., Dayal, H., Swanson, M., Mittelman, A., and Wilkinson G.,J. Natl. Cancer Inst., 1978, vol. 61, pp. 709–714.

    PubMed  CAS  Google Scholar 

  2. Wattenberg, L.W., Loub, W.D., Lam, L.K., and Speier, J.,Fed. Proc., 1975, vol. 35, pp. 1327–1331.

    Google Scholar 

  3. Stoewsand, G.S., Babish, J.B., and Wimberly, H.C.,J. Environ. Pathol. Toxicol., 1978, vol. 2, pp. 399–406.

    PubMed  CAS  Google Scholar 

  4. Wattenberg, L.W.,Cancer Res., 1983 (Suppl.), vol. 43, pp. 2448–2453.

    CAS  Google Scholar 

  5. Boyd, J.N., Babish, J.G., and Stoewsand, G.S.,Food Chem. Toxicol., 1982, vol. 2, pp. 47–50.

    Article  Google Scholar 

  6. McDanell, R., McLean, A.E., Hanley, A.B., Heaney, R.K., and Fenwick, G.R.,Food Chem. Toxicol., 1987, vol. 25, pp. 363–368.

    Article  PubMed  CAS  Google Scholar 

  7. McDanell, R., McLean, A.E., Hanley, A.B., Heaney, R.K., and Fenwick, G.R.,Food Chem. Toxicol., 1989, vol. 27, pp. 289–293.

    Article  PubMed  CAS  Google Scholar 

  8. Bradfield, C.A. and Bjeldanes, L.F.,Food Chem. Toxicol., 1984, vol. 22, pp. 977–982.

    Article  PubMed  CAS  Google Scholar 

  9. Loub, W.D., Wattenberg, L.W., and Davis, D.W.,J. Natl. Cancer Inst., 1975, vol. 54, pp. 985–988.

    PubMed  CAS  Google Scholar 

  10. Pantuck, E.J., Pantuck, C.D., Anderson, K.E., Wattenberg, L.W., Conney, A.H., and Kappas, A.,Clin. Pharmacol. Ther., 1984, vol. 35, pp. 161–169.

    Article  PubMed  CAS  Google Scholar 

  11. Kali, M.A., Vang, O., and Clausen, J.,Cancer Lett. (Shannon, Ireland), 1997, vol. 114, pp. 169–170.

    Article  Google Scholar 

  12. Gmelin, R. and Virtanen, A.I.,Ann. Acad. Sci. Fenn., Ser. A II: Chem., 1961, vol. 107, pp. 1–25.

    Google Scholar 

  13. McDanell, R., McLean, A.E., Hanley, A.B., Heaney, R.K., and Fenwick, G.R.,Food Chem. Toxicol., 1988, vol. 26, pp. 59–70.

    Article  PubMed  CAS  Google Scholar 

  14. Verhoeven, D.T.H., Verhagen, H., Goldbohm, R.A., van den Brandt, P.A., and van Poffel, G.,Chem. Biol. Interactions, 1997, vol. 103, pp. 79–129.

    Article  CAS  Google Scholar 

  15. Naturally Occurring Antitumourigens: III. Indoles. TemaNord 1996:535, Copenhagen: Nordic Council of Ministers, 1996, pp. 107–108, 120.

  16. McMillan, M., Spinks, E.A., and Fenwick, G.R.,Hum. Toxicol., 1986, vol. 5, pp. 15–19.

    Article  PubMed  CAS  Google Scholar 

  17. Bradfield, C.A. and Bjeldanes, L.F.,J. Agric. Food Chem., 1987, vol. 35, pp. 46–49.

    Article  CAS  Google Scholar 

  18. West, L., Badenhop, A., and McLaughlin, J.,J. Agric. Food Chem., 1977, vol. 25, pp. 1234–1248.

    Article  PubMed  CAS  Google Scholar 

  19. Piironen, E., Rtturi, A., and Virtanen, A.I.,Acta Chem. Scand., 1962, vol. 16, pp. 14–15.

    Google Scholar 

  20. Ettlinger, M.G., Dateo, G.P., Harrison, B.W., Mabry, T.J., and Thompson, C.P.,Proc. Natl. Acad. Sci. USA, 1961, vol. 47, pp. 1875–1880.

    Article  PubMed  CAS  Google Scholar 

  21. Bjorkman, R. and Lonnerdal, B.,Biochim. Biophys. Acta, 1973, vol. 327, pp. 121–131.

    PubMed  CAS  Google Scholar 

  22. Preobrazhenskaya, M.N., Bukhman, V.M., Korolev, A.M., and Efimov, S.A.,Pharmacol. Ther., 1994, vol. 60, pp. 301–313.

    Article  Google Scholar 

  23. Ahmad, B.,Nature, 1935, no. 136, p. 797.

  24. McHenry, E.W. and Graham, M.L.,Nature, 1935, no. 135, pp. 871–872.

  25. Pal, J.C. and Guha, B.C.,J. Indian Chem. Soc., 1939, vol. 16, pp. 871–872.

    Google Scholar 

  26. Sen Gupta, P.N. and Guha, B.C.,J. Indian Chem. Soc., 1937, vol. 14, pp. 95–102.

    Google Scholar 

  27. Prochaska, Z., Sanda, V., and Sorm, F.,Collect. Czech. Chem. Commun., 1957, vol. 22, pp. 333–334.

    Google Scholar 

  28. Kiss, G. and Neukom, H.,Helv. Chim. Acta, 1966, vol. 49, pp. 989–992.

    Article  CAS  Google Scholar 

  29. Mukhanov, V.I., Yartseva, I.V., Kikot’, B.C., Volodin, Yu.Yu., Kustova, I.L., Lesnaya, N.A., Sof’ina, Z.P., Ermakova, N.P., and Preobrazhenskaya, M.N.,Bioorg. Khim., 1984, vol. 10, pp. 544–559.

    CAS  Google Scholar 

  30. Mukhanov, V.I., Kaganskii, M.M., Sorokin, A.A., Antonyan, S.G., Tananova, G.V., Mikhailevskaya, L.L., Kinzirskii, A.S., and Preobrazhenskaya, M.N.,Khim.-Farm. Zh., 1994, vol. 28, pp. 6–10.

    CAS  Google Scholar 

  31. Preobrazhenskaya, M.N. and Plikhtyak, I.L.,Khim.-Farm. Zh., 1993, vol. 27, pp. 22–34.

    CAS  Google Scholar 

  32. Aleksandrova, L.G., Korolev, A.M., and Preobrazhenskaya, M.N.,Food Chem., 1992, vol. 45, pp. 61–69.

    Article  CAS  Google Scholar 

  33. Preobrazhenskaya, M.N., Korolev, A.M., Rozhkov, I.I., Yudina, L.N., Lazhko, E.I., Aiello, E., Almerico, A.-M., and Mingoia, F.,Il Farmaco, 1999, vol. 54, pp. 265–274.

    Article  CAS  Google Scholar 

  34. Agerbirk, N., Olsen, C.E., and Sorensen, H.,J. Agric. Food Chem., 1998, vol. 46, pp. 1563–1571.

    Article  CAS  Google Scholar 

  35. Bailey, G.S., Hendricks, J.D., Shelton, D.W., Nixon, J.E., and Pawlowski, N.E.,J. Natl. Cancer Inst., 1987, vol. 78, pp. 931–934.

    PubMed  CAS  Google Scholar 

  36. Wall, M., Taylor, H., Perera, P., and Want, M.,J. Nat. Prod., 1988, vol. 51, pp. 129–135.

    Article  PubMed  CAS  Google Scholar 

  37. Preobrazhenskaya, M.N. and Korolev, A.M.,J. Natl. Cancer Inst., 1992, vol. 84, pp. 1210–1211.

    Article  PubMed  CAS  Google Scholar 

  38. Asmawi, M.Z. and Kankaanranta, H.,J. Pharm. Pharmacol., 1993, vol. 45, pp. 581–584.

    PubMed  CAS  Google Scholar 

  39. Nebert, D.W., Nelson, D.R., Coon, J.J., Estabrook, R.W., Feyreisen, R., Fujii-Kuriyama, Y., Gonzales, F.J., Guengerich, F.P., Gunsalus, I.C., Johnson, E.F., Loper, J.C., Sato, R., Waterman, M.R., and Waxman, D.J.,DNA, 1991, vol. 10, p. 1.

    CAS  Google Scholar 

  40. Liu, H., Wormke, M., Safe, S.H., and Bjeldanes, L.F.,J. Natl. Cancer Inst., 1994, vol. 86, pp. 1758–1765.

    Article  PubMed  CAS  Google Scholar 

  41. Dashwood., R.H.,Chem. Biol. Interact., 1998, vol. 110, pp. 211–215.

    Google Scholar 

  42. Grose, K.R. and Bjeldanes, L.F.,Chem. Res. Toxicol., 1992, vol. 5, pp. 188–193.

    Article  PubMed  CAS  Google Scholar 

  43. De Kruif, C.A., Marsman, J.W., Venekamp, J.C., Falke, H.E., Noordhoek, J., Blauboer, B.J., and Wortelboer, H.M.,Chem. Biol. Interact., 1991, vol. 80, pp. 303–315.

    Article  PubMed  Google Scholar 

  44. Agerbirk, N., Bjergegaard, C., Olsen, C.E., and Sörensen, H.,J. Chromatogr., 1996, vol. 745, pp. 239–248.

    Article  CAS  Google Scholar 

  45. Korolev, A.M., Lazhko, E.I., Yartseva, I.V., Plikhtyak, I.L., Aleksandrova, L.G., Rozynov, B.V., and Preobrazhenskaya, M.N.,Bioorg. Khim., 1991, vol. 17, pp. 981–987.

    CAS  Google Scholar 

  46. Plikhtyak, I.L., Yartseva, M.V., Aleksandrova, L.G., Podkhalyuzina, N.Ya., and Preobrazhenskaya, M.N.,Khim.-Farm. Zh., 1991, vol. 25, pp. 57–59.

    CAS  Google Scholar 

  47. Lazhko, E.I., Korolev, A.M., and Preobrazhenskaya, M.N.,Khim. Geterotsikl. Soedin., 1993, no. 3, pp. 353–359.

  48. Preobrazhenskaya, M.N., Korolev, A.M., Lazhko, E.I., Aleksandrova, L.G., Bergman, J., and Lindström, J.-O.,Food Chem., 1993, vol. 48, pp. 57–62.

    Article  CAS  Google Scholar 

  49. Matano, K. and Kato, N.,Acta Chem. Scand., 1967, vol. 21, pp. 2886–2887.

    PubMed  CAS  Google Scholar 

  50. Virtanen, A.I. and Kiesvaara, M.,Acta Chem. Scand., 1963, vol. 17, pp. 848–853.

    CAS  Google Scholar 

  51. Bjeldanes, L.F., Kim, J.-Y., Grose, K.R., Bartholomew, J., and Bradfield, C.,Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 9543–9547.

    Article  PubMed  CAS  Google Scholar 

  52. Ghent, Y.-H., Riby, J., Srivastava, P., Bartholomew, J., Denison, M., and Bjeldanes, L.,J. Biol. Chem., 1996, vol. 270, pp. 22 548–22 555.

    Google Scholar 

  53. Cover, C.M., Hsieh, S.J., Tran, S.H., Hallden, G., Kim, G.S., Bjeldanes, L.F., and Firestone, G.L.,J. Biol. Chem., 1998, vol. 273, pp. 3838–3847.

    Article  PubMed  CAS  Google Scholar 

  54. Perdew, G.H. and Babbs, C.F.,Nutrition and Cancer, 1991, vol. 16, pp. 209–218.

    Article  PubMed  CAS  Google Scholar 

  55. Rannung, U., Rannung, A., Sjöberg, U., Li, H., Westerholm, R., and Bergman, J.,Chem. Biol., 1995, vol. 2, pp. 841–845.

    Article  Google Scholar 

  56. Wei, Y.D., Hellenberg, H., Rannug, U., and Rannug, A.,Chem. Biol. Interact., 1998, vol. 110, pp. 39–55.

    Article  PubMed  CAS  Google Scholar 

  57. Tholander, J. and Bergman, J.,Tetrahedron Lett., 1998, vol. 39, pp. 1619–1622.

    Article  CAS  Google Scholar 

  58. Chen, L., Safe, S., and Bjeldanes, L.,Biochem. Pharmacol., 1996, vol. 51, pp. 1069–1076.

    Article  PubMed  CAS  Google Scholar 

  59. Gillner, M., Bergman, J., Cambillau, C., Alexandersson, M., Fernstrom, B., and Gustafsson, J.-A.,Mol. Pharmacol., 1993, vol. 44, pp. 336–345.

    PubMed  CAS  Google Scholar 

  60. Christensen, J.G. and LeBlanc, G.A.,Cancer Res., 1996, vol. 56, pp. 574–581.

    PubMed  CAS  Google Scholar 

  61. Baker, T.K., Kwiatkowski, A.P., Madhukar, B.V., and Klauning, J.E.,Carcinogenesis, 1995, vol. 16, pp. 2321–2326.

    Article  PubMed  CAS  Google Scholar 

  62. Wattenberg, L.W. and Laub, W.D.,Cancer Res., 1978, vol. 38, pp. 1410–1413.

    PubMed  CAS  Google Scholar 

  63. Michnovicz, J.J. and Bradlow, H.L.,J. Natl. Cancer Inst., 1990, vol. 82, pp. 947–949.

    Article  PubMed  CAS  Google Scholar 

  64. Lemon, H.M.,Cancer Medicine: Estrogens, Holland, J.F. and Frei, E., III, Eds., Philadelphia: Lea and Febiger, 1973.

    Google Scholar 

  65. Tiwari, K., Guo, Li., Bradlow, L.H., Telang, N.T., and Osborne, M.P.,J. Natl. Cancer Inst., 1994, vol. 86, pp. 126–131.

    Article  PubMed  CAS  Google Scholar 

  66. Michnovicz, J.J. and Bredlow, H.L.,J. Natl. Cancer Inst., 1990, vol. 82, pp. 947–949.

    Article  PubMed  CAS  Google Scholar 

  67. Michnovicz, J.J., Adlercreutz, H., and Bredlow, H.L.,J. Natl. Cancer Inst., 1997, vol. 89, pp. 718–723.

    Article  PubMed  CAS  Google Scholar 

  68. Michnovicz, J.J.,Int. J. Obes., 1998, vol. 22, pp. 227–229.

    Article  CAS  Google Scholar 

  69. Rosen, C.A., Woodson, G.E., Thompson, J.W., Hengesteg, A.P., and Bradlow, H.L.,Otolaryngol. Head Neck Surg., 1998, vol. 118, pp. 810–815.

    Article  PubMed  CAS  Google Scholar 

  70. Newfield, L., Goldsmith, A., Bradlow, H.L., and Auburn, K.,Anticancer Res., 1993, vol. 13, pp. 337–341.

    PubMed  CAS  Google Scholar 

  71. Ge, X.K., Yannai, S., Rennert, G., Gruener, N., and Fares, F.A.,Biochem. Biophys. Res. Commun., 1996, vol. 228, pp. 153–158.

    Article  PubMed  CAS  Google Scholar 

  72. Telang, N.T., Katdare, M., Bradlow, H.L., Osborne, M.P., and Fishman, J.,Proc. Soc. Exp. Biol. Med., 1997, vol. 216, pp. 246–252.

    PubMed  CAS  Google Scholar 

  73. Plikhtyak, I.L., Yartseva, I.V., Klyuev, N.A., and Preobrazhenskaya, M.N.,Khim. Geterotsikl. Soedin., 1989, no. 5, pp. 607–610.

  74. Preobrazhenskaya, M., Lazhko, E., Korolev, A., Reznikova, M., and Rozhkov, I.,Tetrahedron: Asymmetry, 1996, vol. 7, pp. 461–467.

    Article  Google Scholar 

  75. Preobrazhenskaya, M., Abstracts of Papers,17th Int. Congr. of Heterocyclic Chemistry, Vienna, 1999, PO-286.

  76. Plikhtyak, I.L., Yartseva, I.V., Khan, Z.E., and Preobrazhenskaya, M.N.,Bioorg. Khim., 1988, vol. 14, pp. 1437–1443.

    CAS  Google Scholar 

  77. Preobrazhenskaya, M., Rozhkov, I., Lazhko, E., and Korolev, A.,Tetrahedron Lett., 1998, vol. 39, pp. 109–112.

    Article  CAS  Google Scholar 

  78. Taioli, E., Garbers, S., Bradlow, H.L., Carmella, S.G., Akerkar, S., and Hecht, S.S.,Cancer Epidemiol. Biomarkers Prev., 1997, vol. 6, pp. 517–522.

    PubMed  CAS  Google Scholar 

  79. Schut, H.A.J. and Dashwood, R.H.,Ann. N. Y. Acad. Sci., 1995, vol. 768, pp. 210–214.

    Article  PubMed  CAS  Google Scholar 

  80. He, Y.H., Smale, M.H.E., and Schut, H.A.,Cell. Biochem., 1997, vol. 64, pp. 42–51.

    Article  Google Scholar 

  81. Oganesian, A., Hendricks, J.D., and Williams, D.E.,Cancer Lett. (Shannon, Ireland), 1997, vol. 118, pp. 87–94.

    Article  CAS  Google Scholar 

  82. Srivastava, B.H. and Shukla, Y.,Cancer Lett. (Shannon, Ireland), 1998, vol. 134, pp. 91–95.

    Article  CAS  Google Scholar 

  83. Stresser, D.M., Williams, D.E., McLellan, L.I., Harris, T.M., and Bailey, G.S.,Drug Metab. Dispos., 1994, vol. 22, pp. 392–399.

    PubMed  CAS  Google Scholar 

  84. Larsen, S.S. and Williams, D.E.,Drug Metab. Dispos., 1996, vol. 24, pp. 927–931.

    Google Scholar 

  85. Park, J.Y.K., Shigenaga, M.K., and Ames, B.N.,Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 2322–2327.

    Article  PubMed  CAS  Google Scholar 

  86. National Research Council Diet, Nutrition and Cancer, Washington, DC: Natl. Acad., 1982.

  87. Musk, S.R., Preobrazhenskaya, M.N., Belitsky, G.A., Korolev, A.M., Lytcheva, T.A., Khitrovo, I.A., and Johnson, I.T.,Mutation Res., 1994, vol. 323, pp. 69–74.

    Article  PubMed  CAS  Google Scholar 

  88. Efimov, S.A.,Antibiot. Khimioter., 1989, vol. 34, pp. 125–129.

    PubMed  CAS  Google Scholar 

  89. Efimov, S.A., Shevchenko, V.E., Shchukin, I.A., and Preobrazhenskaya, M.N.,Biochem. Biophys. Res. Commun., 1993, vol. 190, pp. 895–900.

    Article  PubMed  CAS  Google Scholar 

  90. Berezina, L.K., Posevaya, T.A., Barinskii, M.F., Korolev, A.M., Zakharov, V.E., and Preobrazhenskaya, M.N.,Khim.-Farm. Zh., 1993, vol. 27, pp. 55–59.

    CAS  Google Scholar 

  91. Malkova, I.V., Bukhman, V.M., Vinogradova, I.V., Fomina, T.V., Korolev, A.M., and Preobrazhenskaya, M.N.,J. Antimicrob. Chemother., 1991, vol. 28, pp. 935–936.

    Article  PubMed  CAS  Google Scholar 

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  1. Institute of New Antibiotics, Russian Academy of Medical Sciences, ul. Bol’shaya Pirogovskaya 11, 119867, Moscow, Russia

    M. N. Preobrazhenskaya & A. M. Korolev

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Preobrazhenskaya, M.N., Korolev, A.M. Indole derivatives in vegetables of the cruciferae family. Russ J Bioorg Chem 26, 85–97 (2000). https://doi.org/10.1007/BF02759153

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