The scaffold protein JSAP1 regulates proliferation and differentiation of cerebellar granule cell precursors by modulating JNK signaling

Molecular and Cellular Neuroscience

Volumn 39, Issue 4, 2008, Pages 569-578

  Sato, Tokiharu ^a   Torashima, Takashi ^b   Sugihara, Kazushi ^a   Hirai, Hirokazu ^b   Asano, Masahide ^a   Yoshioka, Katsuji ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Granule cell precursor; MAP kinase; Scaffold protein; Signal transduction; Sonic hedgehog

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; JSAP1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NEURON SPECIFIC NUCLEAR PROTEIN; SCAFFOLD PROTEIN; SONIC HEDGEHOG PROTEIN; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CEREBELLUM; ENZYME ACTIVITY; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MITOGENESIS; MITOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLUM; CYCLIN-DEPENDENT KINASE INHIBITOR P27; HEDGEHOG PROTEINS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KI-67 ANTIGEN; MICE; NERVE TISSUE PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

ERINACEIDAE;

EID: 56249140019     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.08.003     Document Type: Article

References (43)

1. KCTD11 regulates proliferation and apoptosis of developing granule cell progenitors. J. Neurosci. 25 (2005) 8338-8346
2. Bayarsaikhan M., Shiratsuchi A., Gantulga D., Nakanishi Y., and Yoshioka K. Selective expression of the scaffold protein JSAP1 in spermatogonia and spermatocytes. Reproduction 131 (2006) 711-719
3. Bayarsaikhan M., Takino T., Gantulga D., Sato H., Ito T., and Yoshioka K. Regulation of N-cadherin-based cell-cell interaction by JSAP1 scaffold in PC12h cells. Biochem. Biophys. Res. Commun. 353 (2007) 357-362
4. Blaess S., Graus-Porta D., Belvindrah R., Radakovits R., Pons S., Littlewood-Evans A., Senften M., Guo H., Li Y., Miner J.H., Reichardt L.F., and Müller U. β1-integrins are critical for cerebellar granule cell precursor proliferation. J. Neurosci. 24 (2004) 3402-3412
5. Byrd D.T., Kawasaki M., Walcoff M., Hisamoto N., Matsumoto K., and Jin Y. UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32 (2001) 787-800
6. Casaccia-Bonnefil P., Hardy R.J., Teng K.K., Levine J.M., Koff A., and Chao M.V. Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Development 126 (1999) 4027-4037
7. Cavalli V., Kujala P., Klumperman J., and Goldstein L.S. Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 168 (2005) 775-787
8. Chang L., and Karin M. Mammalian MAP kinase signaling cascades. Nature 410 (2001) 37-40
9. Dahmane N., and Ruiz i Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126 (1999) 3089-3100
10. Dhanasekaran D.N., Kashef K., Lee C.M., Xu H., and Reddy E.P. Scaffold proteins of MAP-kinase modules. Oncogene 26 (2007) 3185-3202
11. KCTD11 is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 10833-10838
12. Fogarty M.P., Emmenegger B.A., Grasfeder L.L., Oliver T.G., and Wechsler-Reya R.J. Fibroblast growth factor blocks Sonic hedgehog signaling in neuronal precursors and tumor cells. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 2973-2978
13. Goto T., Mitsuhashi T., and Takahashi T. Altered patterns of neuron production in the p27 knockout mouse. Dev. Neurosci. 26 (2004) 208-217
14. Hanawa H., Hematti P., Keyvanfar K., Metzger M.E., Krouse A., Donahue R.E., Kepes S., Gray J., Dunbar C.E., Persons D.A., and Nienhuis A.W. Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system. Blood 103 (2004) 4062-4069
15. Hatten M.E., Gao W.Q., Morrison M.E., and Mason C.A. The cerebellum: purification and co-culture of identified cell populations. In: Banker G., and Goslin K. (Eds). Culturing Nerve Cells (1998), MIT Press, Cambridge, MA 419-459
16. Hatten M.E. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22 (1999) 511-539
17. Hirai S., Kawaguchi A., Hirasawa R., Baba M., Ohnishi T., and Ohno S. MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo. Development 129 (2002) 4483-4495
18. Hirai S., Cui d.F., Miyata T., Ogawa M., Kiyonari H., Suda Y., Aizawa S., Banba Y., and Ohno S. The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J. Neurosci. 26 (2006) 11992-12002
19. Inoue C., Dhillon N., and Thorner J. Ste5 RING-H2 domain: role in Ste4-promoted oligomerization for yeast pheromone signaling. Science 278 (1997) 103-106
20. Ito M., Yoshioka K., Akechi M., Yamashita S., Takamatsu N., Sugiyama K., Hibi M., Nakabeppu Y., Shiba T., and Yamamoto K. JSAP1, a novel Jun N-terminal protein kinase (JNK) that functions as scaffold factor in the JNK signaling pathway. Mol. Cell. Biol. 19 (1999) 7539-7548
21. Ito M., Akechi M., Hirose R., Ichimura M., Takamatsu N., Xu P., Nakabeppu Y., Shiba T., Yamamoto K., and Yoshioka K. Isoforms of JSAP1 protein generated through alternative splicing. Gene 255 (2000) 229-234
22. kip1 contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8 (2006) 17-26
23. Kelkar N., Gupta S., Dickens M., and Davis R.J. Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein. JIP3. Mol. Cell. Biol. 20 (2000) 1030-1043
24. Kyriakis J.K., and Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81 (2001) 807-869
25. Millen K.J., Hui C.-C., and Joyner A.L. A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development 121 (1995) 3935-3945
26. Miura E., Fukaya M., Sato T., Sugiyama K., Asano M., Yoshioka K., and Watanabe M. Expression and distribution of JNK/SAPK-associated scaffold protein in developing and adult mouse brain. J. Neurochem. 97 (2006) 1431-1446
27. Miyazawa K., Himi T., Garcia V., Yamagishi H., Sato S., and Ishizaki Y. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J. Neurosci. 20 (2000) 5756-5763
28. Morales D., and Hatten M.E. Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J. Neurosci. 26 (2006) 12226-12236
29. Morrison D.K., and Davis R.J. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu. Rev. Cell Dev. Biol. 19 (2003) 91-118
30. Pons S., Trejo J.L., Martínez-Morales J.R., and Marti E. Vitronectin regulates sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128 (2001) 1481-1492
31. Rubin J.B., Choi Y., and Segal R.A. Cerebellar proteoglycans regulate sonic hedgehog responses during development. Development 129 (2002) 2223-2232
32. Sato S., Ito M., Ito T., and Yoshioka K. Scaffold protein JSAP1 is transported to growth cones of neurites independent of JNK signaling pathways in PC12h cells. Gene 329 (2004) 51-60
33. Sato T., Hidaka K., Iwanaga A., Ito M., Asano M., Nakabeppu Y., Morisaki T., and Yoshioka K. Impairment of cardiomyogenesis in embryonic stem cells lacking scaffold protein JSAP1. Biochem. Biophys. Res. Commun. 338 (2005) 1152-1157
34. Schüller U., Kho A.T., Zhao Q., Ma Q., and Rowitch D.H. Cerebellar 'transcriptome' reveals cell-type and stage-specific expression during postnatal development and tumorigenesis. Mol. Cell. Neurosci. 33 (2006) 247-259
35. Suenaga J., Cui d.F., Yamamoto I., Ohno S., and Hirai S. Developmental changes in the expression pattern of the JNK activator kinase MUK/DLK/ZPK and active JNK in the mouse cerebellum. Cell Tissue Res. 325 (2006) 189-195
36. Takino T., Yoshioka K., Miyamori H., Yamada K.M., and Sato H. A scaffold protein in the c-Jun N-terminal kinase signaling pathway is associated with focal adhesion kinase and tyrosine-phosphorylated. Oncogene 21 (2002) 6488-6497
37. Takino T., Nakada M., Miyamori H., Watanabe Y., Sato T., Gantulga D., Yoshioka K., Yamada K.M., and Sato H. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J. Biol. Chem. 280 (2005) 37772-37781
38. Torashima T., Okoyama S., Nishizaki T., and Hirai H. In vivo transduction of murine cerebellar Purkinje cells by HIV-derived lentiviral vectors. Brain Res. 1082 (2006) 11-22
39. Torashima T., Yamada N., Itoh M., Yamamoto A., and Hirai H. Exposure of lentiviral vectors to subneutral pH shifts the tropism from Purkinje cell to Bergmann glia. Eur. J. Neurosci. 24 (2006) 371-380
40. Wallace V.A. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9 (1999) 445-448
41. Wang W., Mullikin-Kilpatrick D., Crandall J.E., Gronostajski R.M., Litwack E.D., and Kilpatrick D.L. Nuclear factor I coordinates multiple phases of cerebellar granule cell development via regulation of cell adhesion molecules. J. Neurosci. 27 (2007) 6115-6127
42. Wechsler-Reya R.J., and Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22 (1999) 103-114
43. Yoshioka K. Scaffold proteins in mammalian MAP kinase cascades. J. Biochem. 135 (2004) 657-661