Advertisement

Biochemistry (Moscow)

, Volume 75, Issue 9, pp 1088–1097 | Cite as

Lysophosphatidic acid is a lipid mediator with wide range of biological activities. Biosynthetic pathways and mechanism of action

  • I. N. BerdichevetsEmail author
  • T. V. Tyazhelova
  • Kh. R. Shimshilashvili
  • E. I. Rogaev
Review

Abstract

Lysophosphatidic acid (LPA) is a lipid mediator required for maintaining homeostasis of numerous physiological functions and also involved in development of some pathological processes through interactions with G protein-coupled receptors. Recently many data have appeared about the role of this phospholipid in humans, but pathways of LPA biosynthesis and mechanisms of its action remain unclear. This review presents modern concepts about biosynthesis, reception, and biological activity of LPA in humans. Natural and synthetic LPA analogs are considered in the view of their possible use in pharmacology as agonists and/or antagonists of G protein-coupled receptors of LPA.

Key words

lysophosphatidic acid LPA analogs autotaxin G protein-coupled receptors expression of human phospholipase genes 

Abbreviations

ATX

autotaxin

DAG

diacylglycerol

GPC-receptors (GPCR)

G protein-coupled receptors

LPA

lysophosphatidic acid

lysoPLD

lysophospholipase D

MAPK

mitogen-activated protein kinase

NPP

nucleotide phosphatase/phosphodiesterase

PA

phosphatidic acid

PLA1

phospholipase A1

PLA2

phospholipase A2

PLC

phospholipase C

VEGF

vascular endothelial growth factor

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sano, T., Baker, D., Virag, T., Wada, A., Yatomi, Y., Kobayashi, T., Igarashi, Y., and Tigyi, G. (2002) J. Biol. Chem., 277, 21197–21206.PubMedCrossRefGoogle Scholar
  2. 2.
    Baker, D. L., Umstot, E. S., Desiderio, D. M., and Tigyi, G. J. (2000) Ann. N. Y. Acad. Sci., 905, 267–269.PubMedCrossRefGoogle Scholar
  3. 3.
    Tokumura, A., Harada, K., Fukuzawa, K., and Tsukatani, H. (1986) Biochim. Biophys. Acta, 875, 31–38.PubMedGoogle Scholar
  4. 4.
    Gerrard, J. M., and Robinson, P. (1989) Biochim. Biophys. Acta, 1001, 282–285.PubMedGoogle Scholar
  5. 5.
    Eichholtz, T., Jalink, K., Fahrenfort, I., and Moolenaar, W. H. (1993) Biochem. J., 291, 677–680.PubMedGoogle Scholar
  6. 6.
    Sugiura, T., Nakane, S., Kishimoto, S., Waku, K., Yoshioka, Y., and Tokumura, A. (2002) J. Lipid Res., 43, 2049–2055.PubMedCrossRefGoogle Scholar
  7. 7.
    Sugiura, T., Tokumura, A., Gregory, L., Nouchi, T., Weintraub, S. T., and Hanahan, D. J. (1994) Arch. Biochem. Biophys., 311, 358–368.PubMedCrossRefGoogle Scholar
  8. 8.
    Gueguen, G., Gaige, B., Grevy, J. M., Rogalle, P., Bellan, J., Wilson, M., Klaebe, A., Pont, F., Simon, M. F., and Chap, H. (1999) Biochemistry, 38, 8440–8450.PubMedCrossRefGoogle Scholar
  9. 9.
    Van Corven, E. J., van Rijswijk, A., Jalink, K., van der Bend, R. L., van Blitterswijk, W. J., and Moolenaar, W. H. (1992) Biochem. J., 281, 163–169.PubMedGoogle Scholar
  10. 10.
    Tokumura, A., Iimori, M., Nishioka, Y., Kitahara, M., Sakashita, M., and Tanaka, S. (1994) Am. J. Physiol., 267, C204–C210.PubMedGoogle Scholar
  11. 11.
    Perkins, L. M., Ramirez, F. E., Kumar, C. C., Thomson, F. J., and Clark, M. A. (1994) Nucleic Acids Res., 22, 450–452.PubMedCrossRefGoogle Scholar
  12. 12.
    Moolenaar, W. H., van Meeteren, M. L., and Giepmans, B. N. (2004) Bioessays, 26, 870–881.PubMedCrossRefGoogle Scholar
  13. 13.
    Jalink, K., Hengeveld, T., Mulder, S., Postma, F. R., Simon, M. F., Chap, H., van der Marel, G. A., van Boom, J. H., van Blitterswijk, W. J., and Moolenaar, W. H. (1995) Biochem. J., 307, 609–616.PubMedGoogle Scholar
  14. 14.
    Hayashi, K., Takahashi, M., Nishida, W., Yoshida, K., Ohkawa, Y., Kitabatake, A., Aoki, J., Arai, H., and Sobue, K. (2001) Circ. Res., 89, 251–258.PubMedCrossRefGoogle Scholar
  15. 15.
    Yoshida, K., Nishida, W., Hayashi, K., Ohkawa, Y., Ogawa, A., Aoki, J., Arai, H., and Sobue, K. (2003) Circulation, 108, 1746–1752.PubMedCrossRefGoogle Scholar
  16. 16.
    Aoki, J. (2004) Semin. Cell Dev. Biol., 15, 477–489.PubMedCrossRefGoogle Scholar
  17. 17.
    Tokumura, A., Fujimoto, H., Yoshimoto, O., Nishioka, Y., Miyake, M., and Fukuzawa, K. (1999) Life Sci., 65, 245–253.PubMedCrossRefGoogle Scholar
  18. 18.
    Gesta, S., Simon, M. F., Rey, A., Sibrac, D., Girard, A., Lafontan, M., Valet, P., and Saulnier-Blache, J. S. (2002) J. Lipid Res., 43, 904–910.PubMedGoogle Scholar
  19. 19.
    Tokumura, A., Majima, E., Kariya, Y., Tominaga, K., Kogure, K., Yasuda, K., and Fukuzawa, K. (2002) J. Biol. Chem., 277, 39436–39442.PubMedCrossRefGoogle Scholar
  20. 20.
    Stefan, C., Jansen, S., and Bollen, M. (2005) Trends. Biochem. Sci., 30, 542–550.PubMedCrossRefGoogle Scholar
  21. 21.
    Van Meeteren, L. A., and Moolenaar, W. H. (2007) Progress Lipid Res., 46, 145–160.CrossRefGoogle Scholar
  22. 22.
    Kishi, Y., Okudaira, S., Tanaka, M., Hama, K., Shida, D., Kitayama, J., Yamori, T., Aoki, J., Fujimaki, T., and Arai, H. (2006) J. Biol. Chem., 281, 17492–17500.PubMedCrossRefGoogle Scholar
  23. 23.
    Stassar, M. J., Devitt, G., Brosius, M., Rinnab, L., Prang, J., Schradin, T., Simon, J., Petersen, S., Kopp-Schneider, A., and Zoller, M. (2001) Br. J. Cancer, 85, 1372–1382.PubMedCrossRefGoogle Scholar
  24. 24.
    Mills, G. B., and Moolenaar, W. H. (2003) Nat. Rev. Cancer, 3, 582–591.PubMedCrossRefGoogle Scholar
  25. 25.
    Kehlen, A., Lauterbach, R., Santos, A. N., Thiele, K., Kabisch, U., Weber, E., Reimann, D., and Langner, J. (2001) Clin. Exp. Immunol., 123, 147–154.PubMedCrossRefGoogle Scholar
  26. 26.
    Umemura, K., Yamashita, N., Yu, X., Arima, K., Asada, T., Makifuchi, T., Murayamae, T., Saitoe, Y., Kanamarue, K., Gotoa, Y., Kohsakaa, S., Kanazawaa, I., and Kimura, H. (2006) Neurosci. Lett., 400, 97–100.PubMedCrossRefGoogle Scholar
  27. 27.
    Hammack, B. N., Fung, K. Y., Hunsucker, S. W., Duncan, M. W., Burgoon, M. P., Owens, G. P., and Gilden, D. H. (2004) Mult. Scler., 10, 245–260.PubMedCrossRefGoogle Scholar
  28. 28.
    Inoue, K., Arai, H., and Aoki, J. (2004) in Lipases and Phospholipases in Drug Development (Muller, G., and Petry, S., eds.) Wiley-VCH Verlag GmbH & Co. KGaA, Wiley, pp. 23–39.Google Scholar
  29. 29.
    Aoki, J., Inoue, A., Makide, K., Saiki, N., and Arai, H. (2007) Biochimie, 89, 197–204.PubMedCrossRefGoogle Scholar
  30. 30.
    Winkler, F. K., D’Arcy, A., and Hunziker, W. (1990) Nature, 343, 771–774.PubMedCrossRefGoogle Scholar
  31. 31.
    Carriere, F., Thirstrup, K., Hjorth, S., Ferrato, F., Nielsen, P. F., Withers-Martinez, C., Cambillau, C., Boel, E., Thim, L., and Verger, R. (1997) Biochemistry, 36, 239–248.PubMedCrossRefGoogle Scholar
  32. 32.
    Hill, J. S., Davis, R. C., Yang, D., Wen, J., Philo, J. S., Poon, P. H., Phillips, M. L., Kempner, E. S., and Wong, H. (1996) J. Biol. Chem., 271, 22931–22936.PubMedCrossRefGoogle Scholar
  33. 33.
    Wong, H., Yang, D., Hill, J. S., Davis, R. C., Nikazy, J., and Schotz, M. C. (1997) Proc. Natl. Acad. Sci. USA, 94, 5594–5598.PubMedCrossRefGoogle Scholar
  34. 34.
    Kazantseva, A., Goltsov, A., Zinchenko, R., Grigorenko, A. P., Abrukova, A. V., Moliaka, Y. K., Kirillov, A. G., Guo, Z., Lyle, S., Ginter, E. K., and Rogaev, E. I. (2006) Science, 314, 982–985.PubMedCrossRefGoogle Scholar
  35. 35.
    Sonoda, H., Aoki, J., Hiramatsu, T., Ishida, M., Bandoh, K., Nagai, Y., Taguchi, R., Inoue, K., and Arai, H. (2002) J. Biol. Chem., 277, 34254–34263.PubMedCrossRefGoogle Scholar
  36. 36.
    Jin, W., Broedl, U. C., Monajemi, H., Glick, J. M., and Rader, D. J. (2002) Genomics, 80, 268–273.PubMedCrossRefGoogle Scholar
  37. 37.
    Hiramatsu, T., Sonoda, H., Takanezawa, Y., Morikawa, R., Ishida, M., Kasahara, K., Sanai, Y., Taguchi, R., Aoki, J., and Arai, H. (2003) J. Biol. Chem., 278, 49438–49447.PubMedCrossRefGoogle Scholar
  38. 38.
    Hecht, J. H., Weiner, J. A., Post, S. R., and Chun, J. (1996) J. Cell Biol., 135, 1071–1083.PubMedCrossRefGoogle Scholar
  39. 39.
    An, S., Bleu, T., Hallmark, O. G., and Goetzl, E. J. (1998) J. Biol. Chem., 273, 7906–7910.PubMedCrossRefGoogle Scholar
  40. 40.
    Bandoh, K., Aoki, J., Hosono, H., Kobayashi, S., Kobayashi, T., Murakami-Murofushi, K., Tsujimoto, M., Arai, H., and Inoue, K. (1999) J. Biol. Chem., 274, 27776–27785.PubMedCrossRefGoogle Scholar
  41. 41.
    Ishii, I., Fukushima, N., Ye, X., and Chun, J. (2004) Annu. Rev. Biochem., 73, 321–354.PubMedCrossRefGoogle Scholar
  42. 42.
    Noguchi, K., Ishii, S., and Shimizu, T. (2003) J. Biol. Chem., 278, 25600–25606.PubMedCrossRefGoogle Scholar
  43. 43.
    Kotarsky, K., Boketoft, A., Bristulf, J., Nilsson, N. E., Norberg, A., Hansson, S., Sillard, R., Owman, C., Leeb-Lundberg, F. L. M., and Olde, B. (2006) J. Pharmacol. Exp. Ther., 318, 619–628.PubMedCrossRefGoogle Scholar
  44. 44.
    Tabata, K., Baba, K., Shiraishi, A., Ito, M., and Fujita, N. (2007) Biochem. Biophys. Res. Commun., 363, 861–866.PubMedCrossRefGoogle Scholar
  45. 45.
    Pasternack, S. M., von Kugelgen, I., Aboud, K. A., Lee, Y. A., Ruschendorf, F., Voss, K., Hillmer, A. M., Molderings, G. J., Franz, T., Ramirez, A., Nurnberg, P., Nothen, M. M., and Betz, R. C. (2008) Nat. Genet., 40, 329–334.PubMedCrossRefGoogle Scholar
  46. 46.
    Anliker, B., and Chun, J. (2004) J. Biol. Chem., 279, 20555–20558.PubMedCrossRefGoogle Scholar
  47. 47.
    Lee, C. W., Rivera, R., Gardell, S., Dubin, A. E., and Chun, J. (2006) J. Biol. Chem., 281, 23589–23597.PubMedCrossRefGoogle Scholar
  48. 48.
    Gugger, M., White, R., Song, S., Waser, B., Cescato, R., Riviere, P., and Reubi, J. C. (2008) Dis. Markers, 24, 41–50.PubMedGoogle Scholar
  49. 49.
    Glatt, S., Halbauer, D., Heindl, S., Wernitznig, A., Kozina, D., Su, K. C., Puri, C., Garin-Chesa, P., and Sommergruber, W. (2008) Int. J. Cancer, 122, 2008–2016.PubMedCrossRefGoogle Scholar
  50. 50.
    Lee, M., Choi, S., Hallden, G., Yo, S. J., Schichnes, D., and Aponte, G. W. (2009) Am. J. Physiol. Gastrointest. Liver Physiol., 297, G641–G654.PubMedCrossRefGoogle Scholar
  51. 51.
    Radeff-Huang, J., Seasholtz, T. M., Matteo, R. G., and Brown, J. H. (2004) J. Cell. Biochem., 92, 949–966.PubMedCrossRefGoogle Scholar
  52. 52.
    Tigyi, G. (2001) Mol. Pharmacol., 60, 1161–1164.PubMedGoogle Scholar
  53. 53.
    Gardell, S. E., Dubin, A. E., and Chun, J. (2006) Trends Mol. Med., 12, 65–75.PubMedCrossRefGoogle Scholar
  54. 54.
    Torkhovskaya, T. N., Ipatova, O. M., Zakharova, T. S., Kochetova, M. M., and Khalilov, E. M. (2007) Biochemistry (Moscow), 72, 125–131.CrossRefGoogle Scholar
  55. 55.
    McIntyre, T. M., Pontsler, A. V., Silva, A. R., St Hilaire, A., Xu, Y., Hinshaw, J. C., Zimmerman, G. A., Hama, K., Aoki, J., Arai, H., and Prestwich, G. D. (2003) Proc. Natl. Acad. Sci. USA, 100, 131–136.PubMedCrossRefGoogle Scholar
  56. 56.
    Murakami, M., Shiraishi, A., Tabata, K., and Fujita, N. (2008) Biochem. Biophys. Res. Commun., 371, 707–712.PubMedCrossRefGoogle Scholar
  57. 57.
    Contos, J. J., Fukushima, N., Weiner, J. A., Kaushal, D., and Chun, J. (2000) Proc. Natl. Acad. Sci. USA, 97, 13384–13389.PubMedCrossRefGoogle Scholar
  58. 58.
    Inoue, M., Rashid, M. H., Fujita, R., Contos, J. J., Chun, J., and Ueda, H. (2004) Nat. Med., 10, 712–718.PubMedCrossRefGoogle Scholar
  59. 59.
    Pradere, J. P., Klein, J., Gres, S., Guigne, C., Neau, E., Valet, P., Calise, D., Chun, J., Bascands, J. L., Saulnier-Blache, J. S., and Schanstra, J. P. (2007) J. Am. Soc. Nephrol., 18, 3110–3118.PubMedCrossRefGoogle Scholar
  60. 60.
    Tager, A. M., Camera, P. L., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Poorvu, E. C., Brooks, S. F., Bercury, C. D., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., and Luster, A. D. (2008) Nat. Med., 14, 45–54.PubMedCrossRefGoogle Scholar
  61. 61.
    Hama, K., Aoki, J., Fukaya, M., Kishi, Y., Sakai, T., Suzuki, R., Ohta, H., Yamori, T., Watanabe, M., Chun, J., and Arai, H. (2004) J. Biol. Chem., 279, 17634–17639.PubMedCrossRefGoogle Scholar
  62. 62.
    Deng, W., Balazs, L., Wang, D. A., van Middlesworth, L., Tigyi, G., and Johnson, L. R. (2002) Gastroenterology, 123, 206–216.PubMedCrossRefGoogle Scholar
  63. 63.
    Deng, W., Shuyu, E., Tsukahara, R., Valentine, W. J., Durgam, G., Gududuru, V., Balazs, L., Manickam, V., Arsura, M., van Middlesworth, L., Johnson, L. R., Parrill, A. L., Miller, D. D., and Tigyi, G. (2007) Gastroenterology, 132, 1834–1851.PubMedCrossRefGoogle Scholar
  64. 64.
    Hama, K., Aoki, J., Inoue, A., Endo, T., Amano, T., Motoki, R., Kanai, M., Ye, X., Chun, J., Matsuki, N., Suzuki, H., Shibasaki, M., and Arai, H. (2007) Biol. Reprod., 77, 954–959.PubMedCrossRefGoogle Scholar
  65. 65.
    Zhang, Y., Qian, Y., Lu, W., and Chen, X. (2009) Cancer Res., 69, 6049–6056.PubMedCrossRefGoogle Scholar
  66. 66.
    Ali, G., Chishti, M. S., Raza, S. I., John, P., and Ahmad, W. (2007) Hum. Genet., 121, 319–325.PubMedCrossRefGoogle Scholar
  67. 67.
    Galaria, I., Fegley, A. J., Nicholl, S. M., Roatocil, E., and Davies, M. G. (2004) J. Surg. Res., 122, 173–179.PubMedCrossRefGoogle Scholar
  68. 68.
    Murakami-Murofushi, K., Shioda, M., Kaji, K., Yoshida, S., and Murofushi, H. (1992) J. Biol. Chem., 267, 21512–21517.PubMedGoogle Scholar
  69. 69.
    Murakami-Murofushi, K., Kaji, K., Kano, K., Fukuda, M., Shioda, M., and Murofushi, H. (1993) Cell Struct. Funct., 18, 363–370.PubMedCrossRefGoogle Scholar
  70. 70.
    Kobayashi, T., Tanaka-Ishii, R., Taguchi, R., Ikezawa, H., and Murakami-Murofushi, K. (1999) Life Sci., 65, 2185–2191.PubMedCrossRefGoogle Scholar
  71. 71.
    Tsuda, S., Okudaira, S., Moriya-Ito, K., Shimamoto, C., Tanaka, M., Aoki, J., Arai, H., Murakami-Murofushi, K., and Kobayashi, T. (2006) J. Biol. Chem., 281, 26081–26088.PubMedCrossRefGoogle Scholar
  72. 72.
    Ishihara, R., Tatsuta, M., Iishi, H., Baba, M., Uedo, N., Higashino, K., Mukai, M., Ishiguro, S., Kobayashi, S., and Murakami-Murofushi, K. (2004) Int. J. Cancer, 110, 188–193.PubMedCrossRefGoogle Scholar
  73. 73.
    Baker, D. L., Fujiwara, Y., Pigg, K. R., Tsukahara, R., Kobayashi, S., Murofushi, H., Uchiyama, A., Murakami-Murofushi, K., Koh, E., Bandle, R. W., Byun, H.-S., Bittman, R., Fan, D., Murph, M., Mills, G. B., and Tigyi, G. (2006) J. Biol. Chem., 281, 22786–22793.PubMedCrossRefGoogle Scholar
  74. 74.
    Uchiyama, A., Mukai, M., Fujiwara, Y., Kobayashi, S., Kawai, N., Murofushi, H., Inoue, M., Enoki, S., Tanaka, Y., Niki, T., Kobayashi, T., Tigyi, G., and Murakami-Murofushi, K. (2007) Biochim. Biophys. Acta, 1771, 103–112.PubMedGoogle Scholar
  75. 75.
    Xu, Y., Jiang, G., Tsukahara, R., Fujiwara, Y., Tigyi, G., and Prestwich, G. D. (2006) J. Med. Chem., 49, 5309–5315.PubMedCrossRefGoogle Scholar
  76. 76.
    Prestwich, G. D., Gajewiak, J., Zhang, X., Xu, X., Yang, G., and Serban, M. (2008) Biochim. Biophys. Acta, 1781, 588–594.PubMedGoogle Scholar
  77. 77.
    Moolenaar, W. H. (2000) Ann. N. Y. Acad. Sci., 905, 1–10.PubMedCrossRefGoogle Scholar
  78. 78.
    Mills, G. B., Eder, A., Fang, X., Hasegawa, Y., Mao, M., Lu, M., Tanyi, J., Tabassam, F. H., Wiener, J., Lapushin, R., Yu, S., Parrott, J. A., Compton, T., Tribley, W., Fishman, D., Stack, M. S., Gaudette, D., Jaffe, R., Furui, T., Aoki, J., and Erickson, J. R. (2002) Cancer Treat. Res., 107, 259–283.PubMedGoogle Scholar
  79. 79.
    Aoki, J., Taira, A., Takanezawa, Y., Kishi, Y., Hama, K., Kishimoto, T., Mizuno, K., Saku, K., Taguchi, R., and Arai, H. (2002) J. Biol. Chem., 277, 48737–48744.PubMedCrossRefGoogle Scholar
  80. 80.
    Chen, X., Yang, X. Y., Wang, N. D., Ding, C., Yang, Y. J., You, Z. J., Su, Q., and Chen, J. H. (2003) Scand. J. Clin. Lab. Invest., 63, 497–503.PubMedCrossRefGoogle Scholar
  81. 81.
    Hu, Y. L., Tee, M. K., Goetzl, E. J., Auersperg, N., Mills, G. B., Ferrara, N., and Jaffe, R. B. (2001) J. Natl. Cancer Inst., 93, 762–768.PubMedCrossRefGoogle Scholar
  82. 82.
    So, J., Navari, J., Wang, F. Q., and Fishman, D. A. (2004) Gynecol. Oncol., 95, 314–322.PubMedCrossRefGoogle Scholar
  83. 83.
    Rivera-Lopez, C. M., Tucker, A. L., and Lynch, K. R. (2008) Angiogenesis, 11, 301–310.PubMedCrossRefGoogle Scholar
  84. 84.
    Nam, S. W., Clair, T., Kim, Y. S., McMarlin, A., Schiffmann, E., Liotta, L. A., and Stracke, M. L. (2001) Cancer Res., 61, 6938–6944.PubMedGoogle Scholar
  85. 85.
    Van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., Pradere, J. P., Pettit, T. R., Wakelam, M. J. O., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., and Jonkers, J. (2006) Mol. Cell. Biol., 26, 5015–5022.PubMedCrossRefGoogle Scholar
  86. 86.
    Lee, H., Geotzl, E. J., and An, S. (2000) Am. J. Physiol., 47, C612–C617.Google Scholar
  87. 87.
    Siess, W. (2002) Biochim. Biophys. Acta, 1582, 204–215.PubMedGoogle Scholar
  88. 88.
    Pilquil, C., Dewald, J., Cherney, A., Gorshkova, I., Tigyi, G., English, D., Natarajan, V., and Brindley, D. N. (2006) J. Biol. Chem., 281, 38418–38429.PubMedCrossRefGoogle Scholar
  89. 89.
    Wu, W. T., Chen, C.-N., Lin, C. I., Chen, J. H., and Lee, H. (2005) Endocrinology, 146, 3387–3400.PubMedCrossRefGoogle Scholar
  90. 90.
    Balazs, L., Okolicany, J., Ferrebee, M., Tolley, B., and Tigyi, G. (2001) Am. J. Physiol., 280, R466–R472.Google Scholar
  91. 91.
    Sturm, A., and Dignass, A. U. (2002) Biochim. Biophys. Acta, 1582, 282–288.PubMedGoogle Scholar
  92. 92.
    Fukushima, N. (2004) J. Cell. Biochem., 92, 993–1003.PubMedCrossRefGoogle Scholar
  93. 93.
    Ye, X., Fukushima, N., Kingsbury, M. A., and Chun, J. (2002) Neuroreport, 13, 2169–2175.PubMedCrossRefGoogle Scholar
  94. 94.
    Goetzl, E. J., and Rosen, H. (2004) J. Clin. Invest., 114, 1531–1537.PubMedGoogle Scholar
  95. 95.
    Rubenfeld, J., Guo, J., Sookrung, N., Chen, R., Chaicumpa, W., Casolaro, V., Zhao, Y., Natarajan, V., and Georas, S. (2006) Am. J. Physiol. Lung Cell Mol. Physiol., 290, L66–L74.PubMedCrossRefGoogle Scholar
  96. 96.
    Rieken, S., Herroeder, S., Sassmann, A., Wallenwein, B., Moers, A., Offermanns, S., and Wettschureck, N. (2006) J. Biol. Chem., 281, 36985–36992.PubMedCrossRefGoogle Scholar
  97. 97.
    Gustin, C., van Steenbrugge, M., and Raes, M. (2008) Am. J. Physiol. Cell Physiol., 295, C905–C914.PubMedCrossRefGoogle Scholar
  98. 98.
    Lin, D. A., and Boyce, J. A. (2005) J. Immunol., 175, 5430–5438.PubMedGoogle Scholar
  99. 99.
    Bagga, S., Price, K. S., Lin, D. A., Friend, D. S., Austen, K. F., and Boyce, J. A. (2004) Blood, 104, 4080–4087.PubMedCrossRefGoogle Scholar
  100. 100.
    Fishman, D. A., Liu, Y., Ellerbroek, S. M., and Stack, M. S. (2001) Cancer Res., 61, 3194–3199.PubMedGoogle Scholar
  101. 101.
    Van Leeuwen, F. N., Giepmans, B. N., van Meeteren, L. A., and Moolenaar, W. H. (2003) Biochem. Soc. Trans., 31, 1209–1212.PubMedCrossRefGoogle Scholar
  102. 102.
    Fang, X., Gaudette, D., Furui, T., Mao, M., Estrella, V., Eder, A., Pustilnik, T., Sasagawa, A., Lapushin, R., Yu, S., Jaffe, R. B., Wiener, J. R., Erickson, J. R., and Mills, G. B. (2000) Ann. N. Y. Acad. Sci., 905, 188–208.PubMedCrossRefGoogle Scholar
  103. 103.
    Fang, X., Yu, S., Bast, R. C., Liu, S., Xu, H. J., Hu, S. X., Lapushin, R., Claret, F. X., Aggarwal, B. B., Lu, Y., and Mills, G. B. (2004) J. Biol. Chem., 279, 9653–9661.PubMedCrossRefGoogle Scholar
  104. 104.
    Li, H., Ye, X., Mahanivong, C., Bian, D., Chun, J., and Huang, S. (2005) J. Biol. Chem., 280, 10564–10571.PubMedCrossRefGoogle Scholar
  105. 105.
    Hu, Y., Albanese, C., Pestell, R., and Jaffe, R. (2003) J. Natl. Cancer Inst., 95, 733–740.PubMedCrossRefGoogle Scholar
  106. 106.
    Kang, Y. C., Kim, K. M., Lee, K. S., Namkoong, S., Lee, S. J., Han, J. A., Jeoung, D., Ha, K. S., Kwon, Y. G., and Kim, M. (2004) Cell Death Differ., 11, 1287–1298.PubMedCrossRefGoogle Scholar
  107. 107.
    Boucharaba, A., Serre, C. M., Gres, S., Saulnier-Blache, J. S., Bordet, J. C., Guglielmi, J., Clezardin, P., and Peyruchaud, O. (2004) J. Clin. Invest., 114, 1714–1725.PubMedGoogle Scholar
  108. 108.
    Wang, P., Wu, X., Chen, W., Liu, J., and Wang, X. (2007) Gynecol. Oncol., 104, 714–720.PubMedCrossRefGoogle Scholar
  109. 109.
    Shida, D., Kitayama, J., Yamaguchi, H., Okaji, Y., Tsuno, N. H., Watanabe, T., Takuwa, Y., and Nagawa, H. (2003) Cancer Res., 63, 1706–1711.PubMedGoogle Scholar
  110. 110.
    Schulte, K. M., Beyer, A., Kohrer, K., Oberhauser, S., and Roher, H. D. (2001) Int. J. Cancer, 92, 249–256.PubMedCrossRefGoogle Scholar
  111. 111.
    Kitayama, J., Shida, D., Sako, A., Ishikawa, M., Hama, K., Aoki, J., Arai, H., and Nagawa, H. (2004) Breast Cancer Res., 6, R640–646.PubMedCrossRefGoogle Scholar
  112. 112.
    Guo, R., Kasbohm, E. A., Arora, P., Sample, C. J., Baban, B., Sud, N., Sivashanmugam, P., Moniri, N. H., and Daaka, Y. (2006) Endocrinology, 147, 4883–4892.PubMedCrossRefGoogle Scholar
  113. 113.
    Peyruchaud, O., and Karin, N. J. (2009) in Bone and Cancer, Topics in Bone Biology 5 (Bronner, F., and Farach-Carson, M. C., eds.) Springer-Verlag London Limited, London, pp. 73–88.Google Scholar
  114. 114.
    Yang, S. Y., Lee, J., Park, C. G., Kim, S., Hong, S., Chung, H. C., Min, S. K., Han, J. W., Lee, H. W., and Lee, H. Y. (2002) Clin. Exp. Metastasis, 19, 603–608.PubMedCrossRefGoogle Scholar
  115. 115.
    Baumforth, K. R., Flavell, J. R., Reynolds, G. M., Davies, G., Pettit, T. R., Wei, W., Morgan, S., Stankovic, T., Kishi, Y., Arai, H., Nowakova, M., Pratt, G., Aoki, J., Wakelam, M. J., Young, L. S., and Murray, P. G. (2005) Blood, 106, 2138–2146.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • I. N. Berdichevets
    • 1
    Email author
  • T. V. Tyazhelova
    • 1
  • Kh. R. Shimshilashvili
    • 1
  • E. I. Rogaev
    • 1
    • 2
    • 3
  1. 1.Vavilov Institute of General GeneticsRussian Academy of SciencesMoscowRussia
  2. 2.Mental Health Research CenterRussian Academy of Medical SciencesMoscowRussia
  3. 3.Brudnick Neuropsychiatric Research Institute, Department of PsychiatryUniversity of Massachusetts Medical SchoolWorcesterUSA

Personalised recommendations