Table of Contents
Journal of Signal Transduction
Volume 2012 (2012), Article ID 459265, 9 pages
http://dx.doi.org/10.1155/2012/459265
Review Article

Diverse Roles of JNK and MKK Pathways in the Brain

1Department of Developmental and Regenerative Biology, Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan
2Department of Molecular and Systems Neurobiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
3Global COE Program “Comprehensive Center of Education and Research for Chemical Biology of the Diseases”, University of Tokyo, Tokyo 113-0033, Japan

Received 11 August 2011; Accepted 1 November 2011

Academic Editor: M. Gaestel

Copyright © 2012 Tokiwa Yamasaki 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. J. Davis, “Signal transduction by the JNK group of MAP kinases,” Cell, vol. 103, no. 2, pp. 239–252, 2000. View at Google Scholar · View at Scopus
  2. L. Chang and M. Karin, “Mammalian MAP kinase signalling cascades,” Nature, vol. 410, no. 6824, pp. 37–40, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. M. Hibi, A. Lin, T. Smeal, A. Minden, and M. Karin, “Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain,” Genes and Development, vol. 7, no. 11, pp. 2135–2148, 1993. View at Google Scholar · View at Scopus
  4. A. Gdalyahu, I. Ghosh, T. Levy et al., “DCX, a new mediator of the JNK pathway,” EMBO Journal, vol. 23, no. 4, pp. 823–832, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. T. Kawauchi, K. Chihama, Y. I. Nabeshima, and M. Hoshino, “The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration,” EMBO Journal, vol. 22, no. 16, pp. 4190–4201, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. T. Tararuk, N. Östman, W. Li et al., “JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length,” Journal of Cell Biology, vol. 173, no. 2, pp. 265–277, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. M. A. Bogoyevitch and B. Kobe, “Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases,” Microbiology and Molecular Biology Reviews, vol. 70, no. 4, pp. 1061–1095, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. X. Wang, A. Destrument, and C. Tournier, “Physiological roles of MKK4 and MKK7: insights from animal models,” Biochimica et Biophysica Acta, vol. 1773, no. 8, pp. 1349–1357, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. Y. Asaoka and H. Nishina, “Diverse physiological functions of MKK4 and MKK7 during early embryogenesis,” Journal of Biochemistry, vol. 148, no. 4, pp. 393–401, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. W. Haeusgen, T. Herdegen, and V. Waetzig, “The bottleneck of JNK signaling: molecular and functional characteristics of MKK4 and MKK7,” European Journal of Cell Biology, vol. 90, no. 6-7, pp. 536–544, 2011. View at Publisher · View at Google Scholar · View at PubMed
  11. S. Lawler, Y. Fleming, M. Goedert, and P. Cohen, “Synergistic activation of SAPK1/JNK1 by two MAP kinase kinases in vitro,” Current Biology, vol. 8, no. 25, pp. 1387–1390, 1998. View at Google Scholar · View at Scopus
  12. H. Kishimoto, K. Nakagawa, T. Watanabe et al., “Different properties of SEK1 and MKK7 in dual phosphorylation of stress-induced activated protein kinase SAPK/JNK in embryonic stem cells,” Journal of Biological Chemistry, vol. 278, no. 19, pp. 16595–16601, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. B. D. Cuevas, A. N. Abell, and G. L. Johnson, “Role of mitogen-activated protein kinase kinase kinases in signal integration,” Oncogene, vol. 26, no. 22, pp. 3159–3171, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. M. Dickens, J. S. Rogers, J. Cavanagh et al., “A cytoplasmic inhibitor of the JNK signal transduction pathway,” Science, vol. 277, no. 5326, pp. 693–696, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Yasuda, A. J. Whitmarsh, J. Cavanagh, M. Sharma, and R. J. Davis, “The JIP group of mitogen-activated protein kinase scaffold proteins,” Molecular and Cellular Biology, vol. 19, no. 10, pp. 7245–7254, 1999. View at Google Scholar · View at Scopus
  16. M. Ito, K. Yoshioka, M. Akechi et al., “JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a scaffold factor in the JNK signaling pathway,” Molecular and Cellular Biology, vol. 19, no. 11, pp. 7539–7548, 1999. View at Google Scholar · View at Scopus
  17. N. Kelkar, S. Gupta, M. Dickens, and R. J. Davis, “Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3,” Molecular and Cellular Biology, vol. 20, no. 3, pp. 1030–1043, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Y. Kuan, D. D. Yang, D. R. Samanta Roy, R. J. Davis, P. Rakic, and R. A. Flavell, “The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development,” Neuron, vol. 22, no. 4, pp. 667–676, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Sabapathy, W. Jochum, K. Hochedlinger, L. Chang, M. Karin, and E. F. Wagner, “Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2,” Mechanisms of Development, vol. 89, no. 1-2, pp. 115–124, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Westerlund, J. Zdrojewska, A. Padzik et al., “Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate,” Nature Neuroscience, vol. 14, no. 3, pp. 305–313, 2011. View at Publisher · View at Google Scholar · View at PubMed
  21. B. Björkblom, N. Östman, V. Hongisto et al., “Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector,” Journal of Neuroscience, vol. 25, no. 27, pp. 6350–6361, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. L. Chang, Y. Jones, M. H. Ellisman, L. S. B. Goldstein, and M. Karin, “JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins,” Developmental Cell, vol. 4, no. 4, pp. 521–533, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Dauer and S. Przedborski, “Parkinson's disease: mechanisms and models,” Neuron, vol. 39, no. 6, pp. 889–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Hunot, M. Vila, P. Teismann et al., “JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 2, pp. 665–670, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. D. D. Yang, C. Y. Kuan, A. J. Whitmarsh et al., “Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene,” Nature, vol. 389, no. 6653, pp. 865–870, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. C. Y. Kuan, A. J. Whitmarsh, D. D. Yang et al., “A critical role of neural-specific JNK3 for ischemic apoptosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 15184–15189, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. G. Pirianov, K. G. Brywe, C. Mallard et al., “Deletion of the c-Jun N-terminal kinase 3 gene protects neonatal mice against cerebral hypoxic-ischaemic injury,” Journal of Cerebral Blood Flow and Metabolism, vol. 27, no. 5, pp. 1022–1032, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. Y. Morishima, Y. Gotoh, J. Zieg et al., “β-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of fas ligand,” Journal of Neuroscience, vol. 21, no. 19, pp. 7551–7560, 2001. View at Google Scholar · View at Scopus
  29. S. Brecht, R. Kirchhof, A. Chromik et al., “Specific pathophysiological functions of JNK isoforms in the brain,” European Journal of Neuroscience, vol. 21, no. 2, pp. 363–377, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. B. F. Belgardt, J. Mauer, F. T. Wunderlich et al., “Hypothalamic and pituitary c-Jun N-terminal kinase 1 signaling coordinately regulates glucose metabolism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 13, pp. 6028–6033, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. E. K. Unger, M. L. Piper, L. E. Olofsson, and A. W. Xu, “Functional role of c-Jun-N-terminal kinase in feeding regulation,” Endocrinology, vol. 151, no. 2, pp. 671–682, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. G. Tuncman, J. Hirosumi, G. Solinas, L. Chang, M. Karin, and G. S. Hotamisligil, “Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 28, pp. 10741–10746, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. J. Hirosumi, G. Tuncman, L. Chang et al., “A central, role for JNK in obesity and insulin resistance,” Nature, vol. 420, no. 6913, pp. 333–336, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. H. Nishina, C. Vaz, P. Billia et al., “Defective liver formation and liver cell apoptosis in mice lacking the stress signaling kinase SEK1/MKK4,” Development, vol. 126, no. 3, pp. 505–516, 1999. View at Google Scholar · View at Scopus
  35. T. Watanabe, K. Nakagawa, S. Ohata et al., “SEK1/MKK4-mediated SAPK/JNK signaling participates in embryonic hepatoblast proliferation via a pathway different from NF-κB-induced anti-apoptosis,” Developmental Biology, vol. 250, no. 2, pp. 332–347, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Wada, N. Joza, H. M. Cheng et al., “MKK7 couples stress signalling to G2/M cell-cycle progression and cellular senescence,” Nature Cell Biology, vol. 6, no. 3, pp. 215–226, 2004. View at Google Scholar · View at Scopus
  37. X. Wang, B. Nadarajah, A. C. Robinson et al., “Targeted deletion of the mitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death,” Molecular and Cellular Biology, vol. 27, no. 22, pp. 7935–7946, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. T. Yamasaki et al., “Stress-activated protein kinase MKK7 regulates axon elongation in the developing cerebral cortex,” The Journal of Neuroscience, vol. 31, no. 46, pp. 16872–16883, 2011. View at Publisher · View at Google Scholar · View at PubMed
  39. D. Horiuchi, C. A. Collins, P. Bhat, R. V. Barkus, A. DiAntonio, and W. M. Saxton, “Control of a kinesin-cargo linkage mechanism by JNK pathway kinases,” Current Biology, vol. 17, no. 15, pp. 1313–1317, 2007. View at Publisher · View at Google Scholar · View at PubMed
  40. S. I. Hirai, F. C. De, T. Miyata et al., “The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex,” Journal of Neuroscience, vol. 26, no. 46, pp. 11992–12002, 2006. View at Publisher · View at Google Scholar · View at PubMed
  41. S.-I. Hirai, Y. Banba, T. Satake, and S. Ohno, “Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-jun N-terminal kinase pathway,” Journal of Neuroscience, vol. 31, no. 17, pp. 6468–6480, 2011. View at Publisher · View at Google Scholar · View at PubMed
  42. H. Ichijo, E. Nishida, K. Irie et al., “Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways,” Science, vol. 275, no. 5296, pp. 90–94, 1997. View at Publisher · View at Google Scholar
  43. K. Tobiume, A. Matsuzawa, T. Takahashi et al., “ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis,” EMBO Reports, vol. 2, no. 3, pp. 222–228, 2001. View at Publisher · View at Google Scholar · View at PubMed
  44. C. Harada, K. Nakamura, K. Namekata et al., “Role of apoptosis signal-regulating kinase 1 in stress-induced neural cell apoptosis in vivo,” American Journal of Pathology, vol. 168, no. 1, pp. 261–269, 2006. View at Publisher · View at Google Scholar · View at PubMed
  45. H. Nishitoh, A. Matsuzawa, K. Tobiume et al., “ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats,” Genes and Development, vol. 16, no. 11, pp. 1345–1355, 2002. View at Publisher · View at Google Scholar · View at PubMed
  46. H. Nishitoh, H. Kadowaki, A. Nagai et al., “ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1,” Genes and Development, vol. 22, no. 11, pp. 1451–1464, 2008. View at Publisher · View at Google Scholar · View at PubMed
  47. K. Kumakura, H. Nomura, T. Toyoda et al., “Hyperactivity in novel environment with increased dopamine and impaired novelty preference in apoptosis signal-regulating kinase 1 (ASK1)-deficient mice,” Neuroscience Research, vol. 66, no. 3, pp. 313–320, 2010. View at Publisher · View at Google Scholar · View at PubMed
  48. B. Glise, H. Bourbon, and S. Noselli, “hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement,” Cell, vol. 83, no. 3, pp. 451–461, 1995. View at Google Scholar
  49. J. R. Riesgo-Escovar, M. Jenni, A. Fritz, and E. Hafen, “The Drosophila jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye,” Genes and Development, vol. 10, no. 21, pp. 2759–2768, 1996. View at Google Scholar
  50. H. K. Sluss, Z. Han, T. Barrett, R. J. Davis, and Y. T. Ip, “A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila,” Genes and Development, vol. 10, no. 21, pp. 2745–2758, 1996. View at Google Scholar
  51. H. Taru, K. I. Iijima, M. Hase, Y. Kirino, Y. Yagi, and T. Suzuki, “Interaction of Alzheimer's β-amyloid precursor family proteins with scaffold proteins of the JNK signaling cascade,” Journal of Biological Chemistry, vol. 277, no. 22, pp. 20070–20078, 2002. View at Publisher · View at Google Scholar · View at PubMed
  52. G. A. Morfini, Y. M. You, S. L. Pollema et al., “Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin,” Nature Neuroscience, vol. 12, no. 7, pp. 864–871, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. P. Xu, M. Das, J. Reilly, and R. J. Davis, “JNK regulates FoxO-dependent autophagy in neurons,” Genes and Development, vol. 25, no. 4, pp. 310–322, 2011. View at Publisher · View at Google Scholar · View at PubMed
  54. L. Yu, A. Alva, H. Su et al., “Regulation of an ATG7-beclin 1 program of autophaglic cell death by caspase-8,” Science, vol. 304, no. 5676, pp. 1500–1502, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. S. Shimizu, A. Konishi, Y. Nishida et al., “Involvement of JNK in the regulation of autophagic cell death,” Oncogene, vol. 29, no. 14, pp. 2070–2082, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus