Table of Contents
Journal of Signal Transduction
Volume 2011, Article ID 636951, 15 pages
http://dx.doi.org/10.1155/2011/636951
Research Article

Repetitive Peroxide Exposure Reveals Pleiotropic Mitogen-Activated Protein Kinase Signaling Mechanisms

1Receptor Pharmacology Unit, Laboratory of Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, MD 21224, USA
2Miller School of Medicine, University of Miami, Miami, FL 33136, USA
3Metabolism Unit, Laboratory of Clinical Investigation, National Institute on Aging, National Institutes of Health, Baltimore, MD 21224, USA

Received 14 August 2010; Accepted 28 September 2010

Academic Editor: Wan-Wan Lin

Copyright © 2011 Wayne Chadwick et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. E. Bumgarner and K. Y. Yeung, “Methods for the inference of biological pathways and networks,” Methods in Molecular Biology, vol. 541, pp. 225–245, 2009. View at Google Scholar · View at Scopus
  2. S. Maudsley, B. Martin, and L. M. Luttrell, “G protein-coupled receptor signaling complexity in neuronal tissue: implications for novel therapeutics,” Current Alzheimer Research, vol. 4, no. 1, pp. 3–19, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Martin, R. Brenneman, E. Golden et al., “Growth factor signals in neural cells: coherent patterns of interaction control multiple levels of molecular and phenotypic responses,” The Journal of Biological Chemistry, vol. 284, no. 4, pp. 2493–2511, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Maudsley, B. Martin, and L. M. Luttrell, “The origins of diversity and specificity in G protein-coupled receptor signaling,” Journal of Pharmacology and Experimental Therapeutics, vol. 314, no. 2, pp. 485–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. J. T. Hancock, “The role of redox mechanisms in cell signalling,” Molecular Biotechnology, vol. 43, no. 2, pp. 162–166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Ullrich and R. Kissner, “Redox signaling: bioinorganic chemistry at its best,” Journal of Inorganic Biochemistry, vol. 100, no. 12, pp. 2079–2086, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Moncada, R. M. J. Palmer, and E. A. Higgs, “Nitric oxide: physiology, pathophysiology, and pharmacology,” Pharmacological Reviews, vol. 43, no. 2, pp. 109–142, 1991. View at Google Scholar · View at Scopus
  8. L. J. Ignarro, “Nitric oxide: a unique endogenous signaling molecule in vascular biology,” Bioscience Reports, vol. 19, no. 2, pp. 51–71, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Garthwaite, “Concepts of neural nitric oxide-mediated transmission,” European Journal of Neuroscience, vol. 27, no. 11, pp. 2783–2802, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. M. J. Rand and C. G. Li, “Nitric oxide as a neurotransmitter in peripheral nerves: nature of transmitter and mechanism of transmission,” Annual Review of Physiology, vol. 57, pp. 659–682, 1995. View at Google Scholar · View at Scopus
  11. R. M. Golub and B. Descamps-Latscha, “Role of oxygen-dependent mechanisms in monoclonal antibody-induced lysis of normal T cells by phagocytes. I. Human phagocytes,” Annales de l'Institut Pasteur Immunology, vol. 136, no. 1, pp. 3–18, 1985. View at Google Scholar · View at Scopus
  12. A. L. Harris, “Hypoxia—a key regulatory factor in tumour growth,” Nature Reviews Cancer, vol. 2, no. 1, pp. 38–47, 2002. View at Google Scholar · View at Scopus
  13. T. Finkel, “Oxygen radicals and signaling,” Current Opinion in Cell Biology, vol. 10, no. 2, pp. 248–253, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. S. G. Rhee, Y. S. Bae, S. R. Lee, and J. Kwon, “Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation,” Science's STKE, vol. 2000, no. 53, p. pe1, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. V. J. Thannickal and B. L. Fanburg, “Reactive oxygen species in cell signaling,” American Journal of Physiology, vol. 279, no. 6, pp. L1005–L1028, 2000. View at Google Scholar · View at Scopus
  16. J. L. Martindale and N. J. Holbrook, “Cellular response to oxidative stress: signaling for suicide and survival,” Journal of Cellular Physiology, vol. 192, no. 1, pp. 1–15, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. R. H. Burdon, “Superoxide and hydrogen peroxide in relation to mammalian cell proliferation,” Free Radical Biology and Medicine, vol. 18, no. 4, pp. 775–794, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Sundaresan, Z.-X. Yu, V. J. Ferrans, K. Irani, and T. Finkel, “Requirement for generation of H2O2 for platelet-derived growth factor signal transduction,” Science, vol. 270, no. 5234, pp. 296–299, 1995. View at Google Scholar · View at Scopus
  19. Y. S. Bae, S. W. Kang, M. S. Seo et al., “Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation,” The Journal of Biological Chemistry, vol. 272, no. 1, pp. 217–221, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Ushio-Fukai, R. W. Alexander, M. Akers et al., “Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells,” The Journal of Biological Chemistry, vol. 274, no. 32, pp. 22699–22704, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. S. G. Sullivan, D. T.-Y. Chiu, M. Errasfa, J. M. Wang, J.-S. Qi, and A. Stern, “Effects of H2O2 on protein tyrosine phosphatase activity in HER14 cells,” Free Radical Biology and Medicine, vol. 16, no. 3, pp. 399–403, 1994. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Kwon, S.-R. Lee, K.-S. Yang et al., “Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 47, pp. 16419–16424, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. H.-L. Chan, H.-C. Chou, M. Duran et al., “Major role of epidermal growth factor receptor and Src kinases in promoting oxidative stress-dependent loss of adhesion and apoptosis in epithelial cells,” The Journal of Biological Chemistry, vol. 285, no. 7, pp. 4307–4318, 2010. View at Publisher · View at Google Scholar
  24. G. D. Frank, E. D. Motley, T. Inagami, and S. Eguchi, “PYK2/CAKβ represents a redox-sensitive tyrosine kinase in vascular smooth muscle cells,” Biochemical and Biophysical Research Communications, vol. 270, no. 3, pp. 761–765, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Maudsley, K. L. Pierce, A. M. Zamah et al., “The β2-adrenergic receptor mediates extracellular signal-regulated kinase activation via assembly of a multi-receptor complex with the epidermal growth factor receptor,” The Journal of Biological Chemistry, vol. 275, no. 13, pp. 9572–9580, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. B. P. Yu and H. Y. Chung, “Adaptive mechanisms to oxidative stress during aging,” Mechanisms of Ageing and Development, vol. 127, no. 5, pp. 436–443, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Martin, M. P. Mattson, and S. Maudsley, “Caloric restriction and intermittent fasting: two potential diets for successful brain aging,” Ageing Research Reviews, vol. 5, no. 3, pp. 332–353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Maudsley, Z. Naor, D. Bonfil et al., “Proline-rich tyrosine kinase 2 mediates gonadotropin-releasing hormone signaling to a specific extracellularly regulated kinase-sensitive transcriptional locus in the luteinizing hormone β-subunit gene,” Molecular Endocrinology, vol. 21, no. 5, pp. 1216–1233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. A. J. Pawson, S. R. Maudsley, J. Lopes et al., “Multiple determinants for rapid agonist-induced internalization of a nonmammalian gonadotropin-releasing hormone receptor: a putative palmitoylation site and threonine doublet within the carboxyl-terminal tail are critical,” Endocrinology, vol. 144, no. 9, pp. 3860–3871, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Finkel, “Reactive oxygen species and signal transduction,” IUBMB Life, vol. 52, no. 1-2, pp. 3–6, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. J. L. Martindale and N. J. Holbrook, “Cellular response to oxidative stress: signaling for suicide and survival,” Journal of Cellular Physiology, vol. 192, no. 1, pp. 1–15, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Z. Guyton, Y. Liu, M. Gorospe, Q. Xu, and N. J. Holbrook, “Activation of mitogen-activated protein kinase by H2O2: role in cell survival following oxidant injury,” The Journal of Biological Chemistry, vol. 271, no. 8, pp. 4138–4142, 1996. View at Google Scholar · View at Scopus
  33. K. Irani, Y. Xia, J. L. Zweier et al., “Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts,” Science, vol. 275, no. 5306, pp. 1649–1652, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Maudsley, L. Davidson, A. J. Pawson et al., “Gonadotropin-releasing hormone functionally antagonizes testosterone activation of the human androgen receptor in prostate cells through focal adhesion complexes involving Hic-5,” Neuroendocrinology, vol. 84, no. 5, pp. 285–300, 2007. View at Publisher · View at Google Scholar
  35. L. Davidson, A. J. Pawson, R. P. Millar, and S. Maudsley, “Cytoskeletal Reorganization Dependence of Signaling by the Gonadotropin-releasing Hormone Receptor,” The Journal of Biological Chemistry, vol. 279, no. 3, pp. 1980–1993, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. Q.-F. Li, A. M. Spinelli, and D. D. Tang, “Cdc42GAP, reactive oxygen species, and the vimentin network,” American Journal of Physiology, vol. 297, no. 2, pp. C299–C309, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. G. J. Della Rocca, S. Maudsley, Y. Daaka, R. J. Lefkowitz, and L. M. Luttrell, “Pleiotropic coupling of G protein-coupled receptors to the mitogen- activated protein kinase cascade: role of focal adhesions and receptor tyrosine kinases,” The Journal of Biological Chemistry, vol. 274, no. 20, pp. 13978–13984, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. L. M. Luttrell, S. S.G. Ferguson, Y. Daaka et al., “β-arrestin-dependent formation of β2 adrenergic receptor-src protein kinase complexes,” Science, vol. 283, no. 5402, pp. 655–661, 1999. View at Publisher · View at Google Scholar
  39. S.-Y. Park, K. A. Schinkmann, and S. Avraham, “RAFTK/Pyk2 mediates LPA-induced PC12 cell migration,” Cellular Signalling, vol. 18, no. 7, pp. 1063–1071, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. L. M. Luttrell, “'Location, location, location': activation and targeting of MAP kinases by G protein-coupled receptors,” Journal of Molecular Endocrinology, vol. 30, no. 2, pp. 117–126, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Sorkin, “Internalization of the epidermal growth factor receptor: role in signalling,” Biochemical Society Transactions, vol. 29, no. 4, pp. 480–484, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. K. L. Pierce, S. Maudsley, Y. Daaka, L. M. Luttrell, and R. J. Lefkowitz, “Role of endocytosis in the activation of the extracellular signal- regulated kinase cascade by sequestering and nonsequestering G protein- coupled receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 4, pp. 1489–1494, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. F. L. Roudabush, K. L. Pierce, S. Maudsley, K. D. Khan, and L. M. Luttrell, “Transactivation of the EGF receptor mediates IGF-1-stimulated Shc phosphorylation and ERK1/2 activation in COS-7 cells,” The Journal of Biological Chemistry, vol. 275, no. 29, pp. 22583–22589, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Avraham, S.-Y. Park, K. Schinkmann, and S. Avraham, “RAFTK/Pyk2-mediated cellular signalling,” Cellular Signalling, vol. 12, no. 3, pp. 123–133, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Zwick, C. Wallasch, H. Daub, and A. Ullrich, “Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and PYK2 tyrosine phosphorylation in PC12 cells,” The Journal of Biological Chemistry, vol. 274, no. 30, pp. 20989–20996, 1999. View at Publisher · View at Google Scholar · View at Scopus
  46. C. von Montfort, N. S. Fernau, J. I. Beier, H. Sies, and L.-O. Klotz, “Extracellular generation of hydrogen peroxide is responsible for activation of EGF receptor by ultraviolet A radiation,” Free Radical Biology and Medicine, vol. 41, no. 9, pp. 1478–1487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Davidson, A. J. Pawson, R. L. De Maturana et al., “Gonadotropin-releasing Hormone-induced Activation of Diacylglycerol Kinase-ζ and Its Association with Active c-Src,” The Journal of Biological Chemistry, vol. 279, no. 12, pp. 11906–11916, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. I. Dikic, G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger, “A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation,” Nature, vol. 383, no. 6600, pp. 547–550, 1996. View at Publisher · View at Google Scholar · View at Scopus
  49. O. Kranenburg and W. H. Moolenaar, “Ras-MAP kinase signaling by lysophosphatidic acid and other G protein-coupled receptor agonists,” Oncogene, vol. 20, no. 13, pp. 1540–1546, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Kodama, K. Fukuda, E. Takahashi et al., “Selective involvement of p130Cas/Crk/Pyk2/c-Src in endothelin-1-induced JNK activation,” Hypertension, vol. 41, no. 6, pp. 1372–1379, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. P. H. Fishman and J. P. Perkins, “Receptor desensitization,” Advances in Second Messenger and Phosphoprotein Research, vol. 21, pp. 25–32, 1988. View at Google Scholar · View at Scopus
  52. S. Collins, M. Bouvier, M. J. Lohse, J. L. Benovic, M. G. Caron, and R. J. Lefkowitz, “Glycoprotein receptors and cell triggering. Mechanisms involved in adrenergic receptor desensitization,” Biochemical Society Transactions, vol. 18, no. 4, pp. 541–544, 1990. View at Google Scholar · View at Scopus
  53. L. M. Luttrell and D. Gesty-Palmer, “Beyond desensitization: physiological relevance of arrestin-dependent signaling,” Pharmacological Reviews, vol. 62, no. 2, pp. 305–330, 2010. View at Publisher · View at Google Scholar
  54. S. Maudsley, J. P. Gent, J. B. C. Findlay, and D. Donnelly, “The relationship between the agonist-induced activation and desensitization of the human tachykinin NK2 receptor expressed in Xenopus oocytes,” British Journal of Pharmacology, vol. 124, no. 4, pp. 675–684, 1998. View at Publisher · View at Google Scholar · View at Scopus
  55. S. J. Charlton, “Agonist efficacy and receptor desensitization: from partial truths to a fuller picture,” British Journal of Pharmacology, vol. 158, no. 1, pp. 165–168, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Gesty-Palmer, M. Chen, E. Reiter et al., “Distinct β-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation,” The Journal of Biological Chemistry, vol. 281, no. 16, pp. 10856–10864, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. T. A. Kohout, S. L. Nicholas, S. J. Perry, G. Reinhart, S. Junger, and R. S. Struthers, “Differential desensitization, receptor phosphorylation, β-arrestin recruitment, and ERK1/2 activation by the two endogenous ligands for the CC chemokine receptor 7,” The Journal of Biological Chemistry, vol. 279, no. 22, pp. 23214–23222, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. E. J. Melief, M. Miyatake, M. R. Bruchas, and C. Chavkin, “Ligand-directed c-Jun N-terminal kinase activation disrupts opioid receptor signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11608–11613, 2010. View at Publisher · View at Google Scholar
  59. G. S. Wu, “Role of mitogen-activated protein kinase phosphatases (MKPs) in cancer,” Cancer and Metastasis Reviews, vol. 26, no. 3-4, pp. 579–585, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. S. M. Keyse, “Dual-specificity MAP kinase phosphatases (MKPs) and cancer,” Cancer and Metastasis Reviews, vol. 27, no. 2, pp. 253–261, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Sun, C. H. Charles, L. F. Lau, and N. K. Tonks, “MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo,” Cell, vol. 75, no. 3, pp. 487–493, 1993. View at Publisher · View at Google Scholar · View at Scopus
  62. Y.-X. Liu, J. Wang, J. Guo, J. Wu, H. B. Lieberman, and Y. Yin, “DUSP1 is controlled by p53 during the cellular response to oxidative stress,” Molecular Cancer Research, vol. 6, no. 4, pp. 624–633, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Kuwano, H. K. Hyeon, K. Abdelmohsen et al., “MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90,” Molecular and Cellular Biology, vol. 28, no. 14, pp. 4562–4575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Dasgupta, S. Kar, R. Liu et al., “Reactive oxygen species control senescence-associated matrix metalloproteinase-1 through c-Jun-N-terminal kinase,” Journal of Cellular Physiology, vol. 225, no. 1, pp. 52–62, 2010. View at Publisher · View at Google Scholar
  65. S. H. Ross, Y. Lindsay, S. T. Safrany et al., “Differential redox regulation within the PTP superfamily,” Cellular Signalling, vol. 19, no. 7, pp. 1521–1530, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. S. J. Park, H. Y. Kim, H. Kim et al., “Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes,” Free Radical Biology and Medicine, vol. 46, no. 12, pp. 1694–1702, 2009. View at Publisher · View at Google Scholar · View at Scopus