Advertisement

Endocrine

, Volume 27, Issue 2, pp 119–130 | Cite as

Atioxidative protection by melatonin

Multiplicity of mechanisms from radical detoxification to radical avoidance
Article

Abstract

Melatonin has been shown to protect against oxidative stress in various, highly divergent experimental systems. There are many reasons for its remarkable protective potential. Signaling effects comprise the upregulation of antioxidant enzymes, such as superoxide dismutases, peroxidases, and enzymes of glutathione supply, downregulation of prooxidant enzymes, such as nitric oxide synthases and lipoxygenases, and presumably also the control of quinone reductase 2. Other mechanisms are based on direct interactions with several reactive oxygen and nitrogen species. Among these reactions, the capacity of easily undergoing single-electron transfer reactions is of particular importance. Electron donation by melatonin is not only an aspect of direct radical scavenging, but additionally represents the basis for formation of the protective metabolites AMK (N 1-acetyl-N 2-formyl-5methoxykynuramine) and AMK (N 1-acetyl-5methoxykynuramine). Recent investigations on mitochondrial metabolism indicate that melatonin as well as AMK are capable of supporting the electron flux through the respiratory chain, of preventing the breakdown of the mitochondrial membrane potential, and of decreasing electron leakage, thereby reducing the formation of superoxide anions. Radical avoidance is a new line of investigation, which exceeds mitochondrial actions and also comprises antiexcitatory effects and contributions to the maintenance of internal circadian phase relationships.

Key Words

Antioxidants free radicals kynuramines melatonin mitochondria 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Reiter, R. J., Melchiorri, D., Sewerynek, E., et al. (1995). J. Pineal Res. 18, 1–11.PubMedGoogle Scholar
  2. 2.
    Hardeland, R. and Rodríguez, C. (1995). Chronobiol. Int. 12, 157–165.Google Scholar
  3. 3.
    Reiter, R. J. (1995). FASEB J. 9, 526–533.PubMedGoogle Scholar
  4. 4.
    Hardeland, R. (1997). In: Skin cancer and UV radiation. Altmeyer, P., Hoffmann, K., and Stücker, M. (eds.). Springer: Berlin, Heidelberg, pp. 186–198.Google Scholar
  5. 5.
    Reiter, R. J. (1997). Adv. Pharmacol. 38, 103–117.PubMedGoogle Scholar
  6. 6.
    Hardeland, R. (1997). Int. J. Biometeorol. 41, 47–57.PubMedGoogle Scholar
  7. 7.
    Reiter, R. J. (1998). Drug News Perspect. 11, 291–296.PubMedGoogle Scholar
  8. 8.
    Reiter, R. J. (1998). Prog. Neurobiol. 56, 359–384.PubMedGoogle Scholar
  9. 9.
    Reiter, R. J., Garcia, J. J., and Pie, J. (1998). Restor. Neurol. Neurosci. 12, 135–142.PubMedGoogle Scholar
  10. 10.
    Reiter, R. J. (1999). Neuroendocrinol. Lett. 20, 145–150.PubMedGoogle Scholar
  11. 11.
    Karbownik, M. and Reiter, R. J. (2000). Proc. Soc. Exp. Biol. Med. 225, 9–22.PubMedGoogle Scholar
  12. 12.
    Reiter, R. J., Tan, D.-X., Osuna, C., and Gitto, E. (2000). J. Biomed. Sci. 7, 444–458.PubMedGoogle Scholar
  13. 13.
    Reiter, R. J., Acuña-Castroviejo, D., Tan, D.-X., and Burkhardt, S. (2001). Ann. NY Acad. Sci. 939, 200–215.PubMedGoogle Scholar
  14. 14.
    Reiter, R. J., Tan, D.-X., and Burkhardt, S. (2002). Mech. Ageing Dev. 123, 1007–1019.PubMedGoogle Scholar
  15. 15.
    Srinivasan, V. (2002). Indian J. Exp. Biol. 40, 668–679.PubMedGoogle Scholar
  16. 16.
    Cuzzocrea, S. and Reiter, R.J. (2002). Curr. Top. Med. Chem. 2, 153–165.PubMedGoogle Scholar
  17. 17.
    Anisimov, V. N. (2003). Toxicol. Pathol. 31, 589–603.PubMedGoogle Scholar
  18. 18.
    Reiter, R. J., Sainz, R. M., Lopez-Burillo, S., Mayo, J. C., Manchester, L. C., and Tan, D.-X. (2003). Ann. NY Acad. Sci. 993, 35–47.PubMedGoogle Scholar
  19. 19.
    Reiter, R. J., Tan, D.-X., Mayo, J. C., Sainz, R. M., Leon, J., and Czarnocki, Z. (2003). Acta Biochim. Pol. 50, 1129–1146.PubMedGoogle Scholar
  20. 20.
    Reiter, R. J., Tan, D.-X., Manchester, L. C., Lopez-Burillo, S., Sainz, R. M., and Mayo, J. C. (2003). Adv. Exp. Med. Biol. 527, 539–548.PubMedGoogle Scholar
  21. 21.
    Reiter, R. J., Tan, D.-X., Gitto, E., et al. (2004). Pol. J. Pharmacol. 56, 159–170.PubMedGoogle Scholar
  22. 22.
    Vijayalaxmi, Reiter, R. J., Tan, D.-X., Herman, T. S., and Thomas C. R. Jr. (2004). Int. J. Radiat. Oncol. Biol. Phys. 59, 639–653.PubMedGoogle Scholar
  23. 23.
    Behrmann, G. (1989). Die Rolle des Metabolismus der aromatischen Aminosäure Tryptophan bei Gonyaulax polyedra. Diploma Thesis, University of Göttingen.Google Scholar
  24. 24.
    Hardeland, R., Poeggeler, B., Balzer, I., and Behrmann, G. (1991). J. Interdiscipl. Cycle Res. 22, 87–88.Google Scholar
  25. 25.
    Hardeland, R., Fuhrberg, B., Behrmann, G., and Balzer, I. (1993). Sleep Res. 22, 621.Google Scholar
  26. 26.
    Hardeland, R., Poeggeler, B., Balzer, I., and Behrmann, G. (1993). In: Chronobiology & chronomedicine. Gutenbrunner, C., Hildebrandt, G., and Moog, R. (eds.). Lang, Frankfurt, pp. 113–120.Google Scholar
  27. 27.
    Tan, D.-X., Chen, L.-D., Poeggeler, B., Manchester, L.C., and Reiter, R. J. (1993). Endocr. J. 1, 57–60.Google Scholar
  28. 28.
    Hardeland, R., Reiter, R. J., Poeggeler, B., and Tan, D.-X. (1993). Neurosci. Biobehav. Rev. 17, 347–357.PubMedGoogle Scholar
  29. 29.
    Reiter, R. J., Poeggeler, B., Tan, D.-X., Chen, L.-D., Manchester, L. C., and Guerrero, J. M. (1993). Neuroendocrinol. Lett. 15, 103–116.Google Scholar
  30. 30.
    Hardeland, R., Balzer, I., Poeggeler, B., et al. (1995). J. Pineal Res. 18, 104–111.PubMedGoogle Scholar
  31. 31.
    Poeggeler, B., Reiter, R. J., Hardeland, R., Sewerynek, E., Melchiorri, D., and Barlow-Walden, L. R. (1995). Neuroendocrinol. Lett. 17, 87–92.Google Scholar
  32. 32.
    Hardeland, R. and Fuhrberg, B. (1996). Trends Comp. Biochem. Physiol. 2, 25–45.Google Scholar
  33. 33.
    Poeggeler, B., Reiter, R. J., Hardeland, R., Tan, D.-X., and Barlow-Walden, L. R. (1996). Redox Rep. 2, 179–184.Google Scholar
  34. 34.
    Tan, D.-X., Poeggeler, B., Reiter, R. J., et al. (1993). Cancer Lett. 70, 65–71.PubMedGoogle Scholar
  35. 35.
    Tan, D.-X., Reiter, R. J., Chen, L.-D., Poeggeler, B., Manchester, L. C., and Barlow-Walden, L. R. (1994). Carcinogenesis 15, 615–618.Google Scholar
  36. 36.
    Manev, H., Uz, T., Kharlamov, A., and Joo, J.-Y. (1996). FASEB J. 10, 1546–1551.PubMedGoogle Scholar
  37. 37.
    Martín, M., Macías, M., León, J., Escames, G., Khaldy, H., and Acuña-Castroviejo, D. (2002). Int. J. Biochem. Cell Biol. 34, 348–357.PubMedGoogle Scholar
  38. 38.
    Hardeland, R., Coto-Montes, A., and Poeggeler, B. (2003). Chronobiol. Int. 20, 921–962.PubMedGoogle Scholar
  39. 39.
    Antolín, I., Obst, B., Burkhardt, S., and Hardeland, R., (1997). J. Pineal Res. 23, 182–190.PubMedGoogle Scholar
  40. 40.
    Antolín, I. and Hardeland, R. (1997). In: Biological rhythms and antioxidative protection. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 86–97.Google Scholar
  41. 41.
    Hardeland, R. and Coto-Montes, A. (2000). In: Recent research developments in comparative biochemistry and physiology, vol. 1. Pandalai, S. G. (ed.). Transworld Research Network, Trivandrum, pp. 123–137.Google Scholar
  42. 42.
    Poeggeler, B., Thuermann, S., Dose, A., Schoenke, M., Burkhardt, S., and Hardeland, R. (2002). J. Pineal Res. 33, 20–30.PubMedGoogle Scholar
  43. 43.
    Poeggeler, B., Saarela, S., Reiter, R. J., et al. (1994). Ann. NY Acad. Sci. 738, 419–420.PubMedGoogle Scholar
  44. 44.
    Matuszak, Z., Reszka, K. J., and Chignell, C. F. (1997). Free Radic. Biol. Med. 23, 367–372.PubMedGoogle Scholar
  45. 45.
    Stasica, P., Ulanski, P., and Rosiak, J. M. (1998). J. Radioanal. Nucl. Chem. 232, 107–113.Google Scholar
  46. 46.
    Chyan, Y.-J., Poeggeler, B., Omar, R. A., et al. (1999). J. Biol. Chem. 274, 21937–21942.PubMedGoogle Scholar
  47. 47.
    Mahal, H. S., Sharma, H. S., and Mukherjee, T. (1999). Free Radic. Biol. Med. 26, 557–565.PubMedGoogle Scholar
  48. 48.
    Tan, D.-X., Reiter, R. J., Manchester, L. C., et al. (2002). Curr. Top. Med. Chem. 2, 181–197.PubMedGoogle Scholar
  49. 49.
    Hardeland, R., Niebergall, R., Schoenke, M., and Poeggeler, B. (2001). In: Actions and redox properties of melatonin and other aromatic amino acid metabolites. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 49–55.Google Scholar
  50. 50.
    Hardeland, R., Poeggeler, B., Niebergall, R., and Zelosko, V. (2003). J. Pineal Res. 34, 17–25.PubMedGoogle Scholar
  51. 51.
    Uría, H., Fuhrberg, B., Poeggeler, B., and Hardeland, R. (1994). In: Cell biological problems in chronobiology. Hardeland, R. (ed.). University of Göttingen, Göttingen, pp. 89–99.Google Scholar
  52. 52.
    Burkhardt, S., Poeggeler, B., Tan, D.-X., et al. (2001). In: Actions and redox properties of melatonin and other aromatic amino acid metabolites. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 9–22.Google Scholar
  53. 53.
    Tomás-Zapico, C., Hardeland, R., Poeggeler, B., and Coto-Montes, A. (2001). In: Actions and redox properties of melatonin and other aromatic amino acid metabolites. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 136–141.Google Scholar
  54. 54.
    Hardeland, R., Poeggeler, B., Burkhardt, S., et al. (2003). In: Neuroendocrine system and pineal gland with special reference to lifestock. Haldar, C. and Singh S. S. (eds.). Banaras Hindu University, Varanasi, pp. 27–35.Google Scholar
  55. 55.
    Tan, D.-X., Manchester, L. C., Reiter, R. J., et al. (1998). Biochem. Biophys. Res. Commun. 253, 614–620.PubMedGoogle Scholar
  56. 56.
    Stasica, P., Paneth, P., and Rosiak, J. M. (2000). J. Pineal Res. 29, 125–127.PubMedGoogle Scholar
  57. 57.
    Agozzino, P., Avellone, G., Bongiorno, D., et al. (2003). J. Pineal Res. 35, 269–275.PubMedGoogle Scholar
  58. 58.
    Turjanski, A. G., Chaia, Z., Rosenstein, R. E., Estrin, D. A., Doctorovich, F., and Piro, O. (2000). Acta Crystallogr. C56, 682–683.Google Scholar
  59. 59.
    Turjanski, A. G., Leonik, F., Rosenstein, R. E., Estrin, D. A., and Doctorovich, F. (2000). J. Am. Chem. Soc. 122, 10468–10469.Google Scholar
  60. 60.
    Turjanski, A. G., Saenz, D. A., Doctorovich, F., Estrin, D. A., and Rosenstein, R. E. (2001). J. Pineal Res. 31, 97–101.PubMedGoogle Scholar
  61. 61.
    Tesoriere, L., Avellone, G., Ceraulo, L., D’Arpa, D., Allegra, M., and Livrea, M. A. (2001). Free Radic. Res. 35, 633–642.PubMedGoogle Scholar
  62. 62.
    Dose, A., Poeggeler, B., Krimphove, K., Schleicher, I., and Hardeland, R. (2001). In: Actions and redox properties of melatonin and other aromatic amino acid metabolites. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 23–31.Google Scholar
  63. 63.
    Tan, D.-X., Hardeland, R., Manchester, L. C., et al. (2003). J. Pineal Res. 34, 249–259.PubMedGoogle Scholar
  64. 64.
    Roberts, J. E., Hu, D. N., and Wishart, J. F. (1997). J. Photochem. Photobiol. B 42, 125–132.Google Scholar
  65. 65.
    Mueller, U., Hardeland, R., Poeggeler, B., Fuhrberg, B., and Burkhardt, S. (2001). Biol. Rhythm Res. 32, 465.Google Scholar
  66. 66.
    Hardeland, R., Ressmeyer, A.-R., Zelosko, V., Burkhardt, S., and Poeggeler, B. (2004). In: Recent advances in endocrinology and reproduction: evolutionary, biotechnological and clinical implications. Haldar, C. and Singh, S. S. (eds.). Banaras Hindu University, Varanasi, pp. 21–38.Google Scholar
  67. 67.
    Hardeland, R. and Poeggeler, B. (2002). In: Treatise on pineal gland and melatonin. Haldar, C., Singaravel, M., and Maitra, S. K. (eds.). Science Publishers, Enfield, pp. 407–422.Google Scholar
  68. 68.
    Ressmeyer, A.-R., Mayo, J. C., Zelosko, V., et al. (2003). Redox Rep. 8, 205–213.PubMedGoogle Scholar
  69. 69.
    Tan, D.-X., Manchester, L. C., Burkhardt, S., et al. (2001). FASEB J. 15, 2294–2296.PubMedGoogle Scholar
  70. 70.
    Zhang, H., Squadrito, G. L., and Pryor, W. A. (1998). Biochem. Biophys. Res. Commun. 251, 83–87.PubMedGoogle Scholar
  71. 71.
    Zhang, H., Squadrito, G. L., Uppu, R., and Pryor, W. A. (1999). Chem. Res. Toxicol. 12, 526–534.PubMedGoogle Scholar
  72. 72.
    Coto-Montes, A., Boga, J. A., Tomás-Zapico, C., et al. (2001). Free Radic. Biol. Med. 30, 785–792.PubMedGoogle Scholar
  73. 73.
    Coto-Montes, A., Boga, J. A., Tomás-Zapico, C., et al. (2001). Chem.-Biol. Interact. 134, 135–149.PubMedGoogle Scholar
  74. 74.
    Tomás-Zapico, C., Martínez-Fraga, J., Rodríguez-Colunga, M. J., Tolivia, D., Hardeland, R., and Coto-Montes, A. (2002). Int. J. Biochem. Cell Biol. 34, 544–553.PubMedGoogle Scholar
  75. 75.
    Menendez-Pelaez, A., Poeggeler, B., Reiter, R. J., Barlow-Walden, L. R., Pablos, M. I., and Tan, D.-X. (1993). J. Cell. Biochem. 53, 373–382.PubMedGoogle Scholar
  76. 76.
    Menendez-Pelaez, A. and Reiter, R. J. (1993). J. Pineal Res. 15, 59–69.PubMedGoogle Scholar
  77. 77.
    Messner, M., Hardeland, R., Rodenbeck, A., and Huether, G. (1998). J. Pineal Res. 25, 251–259.PubMedGoogle Scholar
  78. 78.
    Messner, M., Hardeland, R., Rodenbeck, A., and Huether, G. (1999). Adv. Exp. Med. Biol. 467, 303–313.PubMedGoogle Scholar
  79. 79.
    Fuhrberg, B., Hardeland, R., Poeggeler, B., and Behrmann, G. (1997). Biol. Rhythm Res. 28, 144–150.Google Scholar
  80. 80.
    Hardeland, R. (1999). Reprod. Nutr. Dev. 39, 399–408.PubMedGoogle Scholar
  81. 81.
    Sprenger, J., Hardeland, R., Fuhrberg, B., and Han, S.-Z. (1999). Cytologia 64, 209–213.Google Scholar
  82. 82.
    Hardeland, R. and Poeggeler, B. (2003). J. Pineal Res. 34, 233–241.PubMedGoogle Scholar
  83. 83.
    Costa, E. J. X., Lopes, R. H., and Lamy-Freund, M. T. (1994). J. Pineal Res. 16, 123–126.Google Scholar
  84. 84.
    Shida, C. S., Castrucci, A. L., and Lamy-Freund, M. T. (1994). J. Pineal Res. 16, 198–201.PubMedGoogle Scholar
  85. 85.
    Barlow-Walden, L. R., Reiter, R. J., Abe, M., et al. (1995). Neurochem. Int. 26, 497–502.PubMedGoogle Scholar
  86. 86.
    Pablos, M. I., Agapito, M. T., Gutierrez, R., et al. (1995). J. Pineal Res. 19, 111–115.PubMedGoogle Scholar
  87. 87.
    Pablos, M. I., Chuang, J., Reiter, R. J., et al. (1995). Biol. Signals 4, 325–330.PubMedGoogle Scholar
  88. 88.
    Kotler, M., Rodriguez, C., Sainz, R. M., Antolin, I., and Menendez-Pelaez, A. (1998). J. Pineal Res. 24, 83–89.PubMedGoogle Scholar
  89. 89.
    Okatani, Y., Wakatsuki, A., and Kaneda, C. (2000). J. Pineal Res. 28, 89–96.PubMedGoogle Scholar
  90. 90.
    Ustundag, B., Kazeze, A., Demirbag, M., Canatan, H., Halifeoglu I., and Ozercan, I. H. (2000). Cell. Physiol. Biochem. 10, 229–236.PubMedGoogle Scholar
  91. 91.
    Wakatsuki, A., Okatani, Y., Shinohara, K., Ikenoue, N., Kaneda, C., and Fukaya, T. (2001). J. Pineal Res. 30, 22–28.PubMedGoogle Scholar
  92. 92.
    Okatani, Y., Wakatsuki, A., Shinohara, K., Kaneda, C., and Fukaya, T. (2001). J. Pineal Res. 30, 199–205.PubMedGoogle Scholar
  93. 93.
    Gultekin, F., Delibas, N., Yasar, S., and Kilinc, I. (2001). Arch. Toxicol. 75, 88–96.PubMedGoogle Scholar
  94. 94.
    Gürdöl, F., Genç, S., Öner-İyidogan, Y., and Süzme, R. (2001). Horm. Metab. Res. 33, 608–611.PubMedGoogle Scholar
  95. 95.
    Okatani, Y., Wakatsuki, A., Reiter, R. J., and Miyahara, Y. (2002). Neurobiol. Aging 23, 639–644.PubMedGoogle Scholar
  96. 96.
    Mayo, J. C., Sainz, R. M., Antolin, I., Herrera, F., Martin, V. and Rodriguez, C. (2002). Cell. Mol. Life Sci. 59, 1706–1713.PubMedGoogle Scholar
  97. 97.
    Gurlek, A., Aydogan, H., Parlakpinar, H., et al. (2004). J. Pineal Res. 36, 58–63.PubMedGoogle Scholar
  98. 98.
    Balkan, J., Sener, G., Cevikbas, U., Keyser-Uysal, M., and Uysal, M. (2004). Int. J. Vitam. Nutr. Res. 74, 349–354.PubMedGoogle Scholar
  99. 99.
    Gómez, M., Esparza, J. L., Nogués, M. R., Giralt, M., Cabré, M. and Domingo, J. L. (2005). Free Radic. Biol. Med. 38, 104–111.PubMedGoogle Scholar
  100. 100.
    Liu, F. and Ng, T. B. (2000). Biochem. Cell Biol. 78, 447–453.PubMedGoogle Scholar
  101. 101.
    Antolín, I., Rodríguez, C., Sáinz, R. M., et al. (1996). FASEB J. 10, 882–890.PubMedGoogle Scholar
  102. 102.
    Öztürk, G., Coskun, S., Erbas, D., and Hasanoglu, E. (2000). Jpn. J. Physiol. 50, 149–153.PubMedGoogle Scholar
  103. 103.
    Taskiran, D., Tanyalcin, T., Sozmen, E. Y., et al. (2000). Int. J. Neurosci. 104, 63–73.PubMedGoogle Scholar
  104. 104.
    Wang, H., Wei, W., Shen, Y. X., et al. (2004). World J. Gastroenterol. 10, 2690–2696.PubMedGoogle Scholar
  105. 105.
    Rodriguez, C., Mayo, J. C., Sainz, R. M., Herrera, F., Martin, V., and Reiter, R. J. (2004). J. Pineal Res. 36, 1–9.PubMedGoogle Scholar
  106. 106.
    Tomás-Zapico, C., Coto-Montes, A., Martínez-Fraga, J., Rodríguez-Colunga, M. J., Hardeland, R., and Tolivia, D. (2002). Free Radic. Biol. Med. 32, 1197–1204.PubMedGoogle Scholar
  107. 107.
    Yerer, M. B., Aydogan, S., Yapislar, H., Yalcin, O., Kuru, O., and Baskurt, O. K. (2003). J. Pineal Res. 35, 138–139.PubMedGoogle Scholar
  108. 108.
    Pablos, M. I., Reiter, R. J., Ortiz, G. G., et al. (1998). Neurochem. Int. 32, 69–75.PubMedGoogle Scholar
  109. 109.
    Agapito, M. T., Redondo, I., Plaza, R., Lopez-Burillo, S., Recio, J. M., and Pablos, M. I. (1999). Adv. Exp. Med. Biol. 460, 377–381.PubMedGoogle Scholar
  110. 110.
    Dziegiel, P., Murawska-Cialowicz, E., Jethon, Z., et al. (2003). J. Pineal Res. 35, 183–187.PubMedGoogle Scholar
  111. 111.
    Ohta, Y., Kongo-Nishimura, M., Matsura, T., Yamada, K., Kitagawa, A., and Kishikawa, T. (2004). J. Pineal Res. 36, 10–17.PubMedGoogle Scholar
  112. 112.
    Erten, S. F., Kocak, A., Ozdemir, I., Aydemir, S., Colak, A., and Reeder, B. S. (2003). Spinal Cord 41, 533–538.PubMedGoogle Scholar
  113. 113.
    Halici, M., Narin, F., Turk, C. Y., Saraymen, R., Baykan, A., and Kabak, S. (2004). J. Int. Med. Res. 32, 500–506.PubMedGoogle Scholar
  114. 114.
    Uz, T. and Manev, H. (1998). Neuroreport 9, 783–786.PubMedGoogle Scholar
  115. 115.
    Manev, H., Uz, T., and Qu, T. (1998). Restor. Neurol. Neurosci. 12, 81–85.PubMedGoogle Scholar
  116. 116.
    Zhang, H., Akbar, M., and Kim, H. Y. (1999). Biochem. J. 344 (Pt. 2), 487–493.PubMedGoogle Scholar
  117. 117.
    Pozo, D., Reiter, R. J., Calvo, J. R., and Guerrero, J. M. (1994). Life Sci. 55, PL455–460.PubMedGoogle Scholar
  118. 118.
    Bettahi, I., Pozo, D., Osuna, C., Reiter, R. J., Acuña-Castroviejo, D., and Guerrero, J. M. (1996). J. Pineal Res. 20, 205–210.PubMedGoogle Scholar
  119. 119.
    Gilad, E., Wong, H. R., Zingarelli, B., et al. (1998). FASEB J. 12, 685–693.PubMedGoogle Scholar
  120. 120.
    Chang, H.-M., Ling, E.-A., Chen, C.-F., Lue, J.-H., Wen, C.-Y., and Shieh, J.-Y. (2002). J. Pineal Res. 32, 65–73.PubMedGoogle Scholar
  121. 121.
    Rogério, F., de Souza Queiroz, L., Teixeira, S. A., Oliveira, A. L., de Nucci, G., and Langone, F. (2002). Brain Res. 926, 33–41.PubMedGoogle Scholar
  122. 122.
    Storr, M., Koppitz, P., Sibaev, A., et al. (2002). J. Pineal Res. 33, 101–108.PubMedGoogle Scholar
  123. 123.
    Nosjean, O., Ferro, M., Cogé, F., et al. (2000). J. Biol. Chem. 275, 31311–31317.PubMedGoogle Scholar
  124. 124.
    Nosjean, O., Nicolas, J. P., Klupsch, F., Delagrange, P., Canet, E., and Boutin, J. A. (2001). Biochem. Pharmacol. 61, 1369–1379.PubMedGoogle Scholar
  125. 125.
    Witt-Enderby, P. A., Bennett, J., Jarzynka, M. M., Firestine, S., and Melan, M. A. (2003). Life Sci. 72, 2183–2198.PubMedGoogle Scholar
  126. 126.
    Gitto, E., Tan, D.-X., Reiter, R. J., et al. (2001). J. Pharm. Pharmacol. 53, 1393–1401.PubMedGoogle Scholar
  127. 127.
    Lapin, I. P., Mirzaev, S. M., Ryzow, I. V., and Oxenkrug, G. F. (1998). J. Pineal Res. 24, 215–218.PubMedGoogle Scholar
  128. 128.
    Espinar, A., García-Oliva, A., Isorna, E. M., Quesada, A., Prada, F. A., and Guerrero, J. M. (2000). J. Pineal Res. 28, 81–88.PubMedGoogle Scholar
  129. 129.
    Husson, I., Mesples, B., Bac, P., Vamecq, J., Evrard, P., and Gressens, P. (2002). Ann. Neurol. 51, 82–92.PubMedGoogle Scholar
  130. 130.
    Chung, S. Y. and Han S. H. (2003). J. Pineal Res. 34, 95–102.PubMedGoogle Scholar
  131. 131.
    Annanth, C., Gopalakrishnakone, P., and Kaur, C. (2003). Hippocampus 13, 375–387.Google Scholar
  132. 132.
    Southgate, G. S., Daya, S., and Potgieter, B. (1998). J. Chem. Neuroanat. 14, 151–156.PubMedGoogle Scholar
  133. 133.
    Behan, W. M., McDonald, M., Darlington, L. G., and Stone, T. W. (1999). Br. J. Pharmacol. 128, 1754–1760.PubMedGoogle Scholar
  134. 134.
    Cabrera, J., Reiter, R. J., Tan, D.-X., et al. (2000). Neuropharmacology 39, 507–514.PubMedGoogle Scholar
  135. 135.
    Coto-Montes, A. and Hardeland R. (1999). Biol. Rhythm Res. 30, 383–391.Google Scholar
  136. 136.
    Coto-Montes, A., Tomás-Zapico, C., Rodríguez-Colunga, M. J., et al. (2001). J. Cell. Biochem. 83, 426–434.PubMedGoogle Scholar
  137. 137.
    Tunçtan, B., Weigl, Y., Dotan, A., et al. (2002). Chronobiol. Int. 19, 393–404.PubMedGoogle Scholar
  138. 138.
    Clément, P., Gharib, A., Cespuglio, R., and Sarda, N. (2003). Neuroscience 116, 863–870.PubMedGoogle Scholar
  139. 139.
    Albarrán, M. T., López-Burillo, S., Pablos, M. I., Reiter, R. J., and Agapito, M. T. (2001). J. Pineal Res. 30, 227–233.PubMedGoogle Scholar
  140. 140.
    Bubenik, G. A. (2001). Biol. Signals Recept. 10, 350–366.PubMedGoogle Scholar
  141. 141.
    Bubenik, G. A. (2002). Dig. Dis. Sci. 47, 2336–2348.PubMedGoogle Scholar
  142. 142.
    Balzer, I. and Hardeland, R. (1989). Comp. Biochem. Physiol. 94C, 129–132.Google Scholar
  143. 143.
    Burkhardt, S., Reiter, R. J., Tan, D.-X., Hardeland, R., Cabrera, J., and Karbownik, M. (2001). Int. J. Biochem. Cell Biol. 33, 775–783.PubMedGoogle Scholar
  144. 144.
    Behrends, A., Hardeland, R., Ness, H., Grube, S., Poeggeler, B., and Haldar, C. (2004). Redox Rep. 9, 279–288.PubMedGoogle Scholar
  145. 145.
    Kelly, R. W., Amato, F., and Seamark, R. F. (1984). Biochem. Biophys. Res. Commun. 121, 372–379.PubMedGoogle Scholar
  146. 146.
    Ferry, G., Ubeaud, C., Lambert, P. H., et al. (2005). Biochem. J. 388(Pt. 1), 205–215.PubMedGoogle Scholar
  147. 147.
    Hirata, F., Hayaishi, O., Tokuyama, T., and Senoh, S. (1974). J. Biol. Chem. 249, 1311–1313.PubMedGoogle Scholar
  148. 148.
    Tricoire, H., Locatelli, A., Chemineau, P., and Malpaux, B. (2002). Endocrinology 143, 84–90.PubMedGoogle Scholar
  149. 149.
    Alberati-Giani, D., Ricciardi-Castagnoli, P., Köhler, C., and Cesura, A. M. (1996). Adv. Exp. Med. Biol. 398, 171–175.PubMedGoogle Scholar
  150. 150.
    Lestage, J., Verrier, D., Palin, K., and Dantzer, R. (2002). Brain Behav. Immun. 16, 596–601.PubMedGoogle Scholar
  151. 151.
    Kwidzinski, E., Bunse, J., Kovac, A. D., et al. (2003). Adv. Exp. Med. Biol. 527, 113–118.PubMedGoogle Scholar
  152. 152.
    Schoenke, M., Poeggeler, B., Burkhardt, S., Hardeland, R., and Zsizsik, B. K. (2001). In: Actions and redox properties of melatonin and other aromatic amino acid metabolites. Hardeland, R. (ed.). Cuvillier, Göttingen, pp. 32–38.Google Scholar
  153. 153.
    Tan, D.-X., Manchester, L. C., Reiter, R. J., Qi, W.-B., Karbownik, M., and Calvo, J. R. (2000). Biol. Signals Recept. 9, 137–159.PubMedGoogle Scholar
  154. 154.
    Silva, S. O., Rodrigues, M. R., Carvalho, S. R. Q., Catalani, L. H., Campa, A., and Ximenes, V. F. (2004). J. Pineal Res. 37, 171–175.PubMedGoogle Scholar
  155. 155.
    Acuña-Castroviejo, D., Martín, M., Macías, M., et al. (2001). J. Pineal Res. 30, 65–74.PubMedGoogle Scholar
  156. 156.
    Okatani, Y., Wakatsuki, A., Reiter, R. J., Enzan, H., and Miyahara, Y. (2003). Eur. J. Pharmacol. 469, 145–152.PubMedGoogle Scholar
  157. 157.
    Watanabe, K., Wakatsuki, A., Shinohara, K., Ikenoue, N., Yokota, K., and Fukaya, T. (2004). J. Pineal Res. 37, 276–280.PubMedGoogle Scholar
  158. 158.
    León, J., Acuña-Castroviejo, D., Escames, G., Tan, D.-X., and Reiter, R. J. (2005). J. Pineal Res. 38, 1–9.PubMedGoogle Scholar
  159. 159.
    Escames, G., León, J., Macías, M., Khaldy, H., and Acuña-Castroviejo, D. (2003). FASEB J. 17, 932–934.PubMedGoogle Scholar
  160. 160.
    Acuña-Castroviejo, D., Escames, G., León, J., Carazo, A., and Khaldy, H. (2003). Adv. Exp. Med. Biol. 527, 549–557.PubMedGoogle Scholar
  161. 161.
    Yalcin, A., Kilinc, E., Kocturk, S., Resmi, H., and Sozmen, E. Y. (2004). Int. J. Neurosci. 114, 1085–1097.PubMedGoogle Scholar
  162. 162.
    Martín, M., Macías, M., Escames, G., et al. (2000). J. Pineal Res. 28, 242–248.PubMedGoogle Scholar
  163. 163.
    Reiter, R. J., Tan, D.-X., Manchester, L. C., and El-Sawi, M. R. (2002). Ann. NY Acad. Sci. 959, 238–250.PubMedGoogle Scholar
  164. 164.
    León, J., Acuña-Castroviejo, D., Sáinz, R. M., Mayo, J. C., Tan, D.-X., and Reiter, R. J. (2004). Life Sci. 75, 765–790.PubMedGoogle Scholar
  165. 165.
    Sharman, E. H. and Bondy, S. C. (2001). Neurobiol. Aging 22, 629–634.PubMedGoogle Scholar
  166. 166.
    Reyes-Toso, C. F., Ricci, C. R., de Mignone, I. R., et al. (2003). Neurendocrinol. Lett. 24, 341–344.Google Scholar
  167. 167.
    Okatani, Y., Wakatsuki, A., and Reiter, R. J. (2002). J. Pineal Res. 32, 143–148.PubMedGoogle Scholar
  168. 168.
    Okatani, Y., Wakatsuki, A., Reiter, R. J., and Miyahara, Y. (2002). J. Pineal Res. 33, 127–133.PubMedGoogle Scholar
  169. 169.
    Okatani, Y., Wakatsuki, A., Reiter, R. J., and Miyahara, Y. (2003). Int. J. Biochem. Cell Biol. 35, 367–375.PubMedGoogle Scholar
  170. 170.
    Jou, M.-J., Peng, T.-I., Reiter, R. J., Jou, S.-B., Wu, H.-Y., and Wen, S.-T. (2004). J. Pineal Res. 37, 5–70.Google Scholar
  171. 171.
    Andrabi, S. A., Sayeed, I., Siemen, D., Wolf, G., and Horn, T. F. (2004). FASEB J. 18, 869–871.PubMedGoogle Scholar
  172. 172.
    Xu, M. and Ashraf, M. (2002). J. Mol. Cell. Cardiol. 34, 75–79.PubMedGoogle Scholar
  173. 173.
    Poeggeler, B. (2004). 9th Int. Conf. on Alzheimer’s Disease and Related Disorders, Philadelphia, abstract P4-398.Google Scholar
  174. 174.
    Genova, M. L., Merlo Pich, M., Bernacchia, A., et al. (2004). Ann. NY Acad. Sci. 1011, 86–100.PubMedGoogle Scholar
  175. 175.
    Xu, J.-X. (2004). Ann. NY Acad. Sci. 1011, 57–60.PubMedGoogle Scholar
  176. 176.
    Jacob, S., Poeggeler, B., Weishaupt, J. H., et al. (2002). J. Pineal Res. 33, 186–187.PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 2005

Authors and Affiliations

  1. 1.Institute of Zoology, Anthropology and Developmental BiologyUniversity of GöttingenGöttingenGermany

Personalised recommendations