The Cdk5/p35 kinases modulate leptin-induced STAT3 signaling

Journal of Molecular Neuroscience

Volumn 39, Issue 1-2, 2009, Pages 49-58

  He, Yi ^a   Kastin, Abba J ^a   Hsuchou, Hung ^a   Pan, Weihong ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Cdk5; Leptin; Neuron; P25; P35; Signal transduction; STAT3

Indexed keywords

CYCLIN DEPENDENT KINASE 5; LEPTIN; LEPTIN RECEPTOR; PROTEIN KINASE; PROTEIN OBR; PROTEIN P25; PROTEIN P35; RETINOIC ACID; ROSCOVITINE; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HYPOTHALAMUS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYCLIN-DEPENDENT KINASE 5; HUMANS; HYPOTHALAMUS; LEPTIN; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; NEURONS; PHOSPHOTRANSFERASES; PURINES; RANDOM ALLOCATION; RECEPTORS, LEPTIN; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 74149086504     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-008-9174-3     Document Type: Article

References (48)

1. Banks, W. A., Kastin, A. J., Huang, W., Jaspan, J. B., & Maness, L. M. (1996). Leptin enters the brain by a saturable system independent of insulin. Peptides, 17, 305-311. doi:10.1016/0196-9781 (96) 00025-3.
2. Baumann, K., Mandelkow, E. M., Biernat, J., Piwnica-Worms, H., & Mandelkow, E. (1993). Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Letters, 336, 417-424. doi:10.1016/0014-5793 (93) 80849-P.
3. Benomar, Y., Roy, A. F., Aubourg, A., Djiane, J., & Taouis, M. (2005). Cross down-regulation of leptin and insulin receptor expression and signalling in a human neuronal cell line. The Biochemical Journal, 388, 929-939. doi:10.1042/BJ20041621.
4. Bjorbak, C., Lavery, H. J., Bates, S. H., Olson, R. K., Davis, S. M., Flier, J. S., et al. (2000). SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985. The Journal of Biological Chemistry, 275, 40649-40657. doi:10.1074/jbc. M007577200.
5. Cheung, Z. H., Fu, A. K., & Ip, N. Y. (2006). Synaptic roles of Cdk5: Implications in higher cognitive functions and neurodegenerative diseases. Neuron, 50, 13-18. doi:10.1016/j.neuron. 2006.02.024.
6. Fu, A. K., Fu, W. Y., Ng, A. K., Chien, W. W., Ng, Y. P., Wang, J. H., et al. (2004). Cyclin-dependent kinase 5 phosphorylates signal transducer and activator of transcription 3 and regulates its transcriptional activity. Proceedings of the National Academy of Sciences of the United States of America, 101, 6728-6733. doi:10.1073/pnas.0307606100.
7. Garris, D. R. (1989). Morphometric analysis of obesity (ob/ob) - and diabetes (db/db)-associated hypothalamic neuronal degeneration in C57BL/KsJ mice. Brain Research, 501, 162-170. doi:10.1016/0006-8993 (89) 91037-8.
8. Guo, Z., Jiang, H., Xu, X., Duan, W., & Mattson, M. P. (2008). Leptin-mediated cell survival signaling in hippocampal neurons mediated by JAK STAT3 and mitochondrial stabilization. The Journal of Biological Chemistry, 283, 1754-1763. doi:10.1074/jbc. M703753200.
9. Harvey, J. (2007). Leptin: A diverse regulator of neuronal function. Journal of Neurochemistry, 100, 307-313. doi:10.1111/j.1471-4159.2006. 04205.x.
10. He, Y., Li, H. L., Xie, W. Y., Yang, C. Z., Yu, A. C., & Wang, Y. (2007). The presence of active Cdk5 associated with p35 in astrocytes and its important role in process elongation of scratched astrocyte. Glia, 55, 573-583. doi:10.1002/glia.20485.
11. Hellmich, M. R., Pant, H. C., Wada, E., & Battey, J. F. (1992). Neuronal cdc2-like kinase: A cdc2-related protein kinase with predominantly neuronal expression. Proceedings of the National Academy of Sciences of the United States of America, 89, 10867-10871. doi:10.1073/pnas.89.22.10867.
12. Jang, E. H., Park, C. S., Lee, S. K., Pie, J. E., & Kang, J. H. (2007). Excessive nitric oxide attenuates leptin-mediated signal transducer and activator of transcription 3 activation. Life Sciences, 80, 609-617. doi:10.1016/j.lfs.2006.10.007.
13. Kastin, A. J., Banks, W. A., Zadina, J. E., & Graf, M. V. (1983). Brain peptides: The dangers of constricted nomenclatures. Life Sciences, 32, 295-301. doi:10.1016/0024-3205 (3) 90073-5.
14. Kastin, A. J., & Pan, W. (2006). Intranasal leptin: Blood-brain barrier bypass (BBBB) for obesity? Endocrinology, 147, 2086-2087. doi:10.1210/en. 2006-0208.
15. Larsen, L., & Ropke, C. (2002). Suppressors of cytokine signalling: SOCS. APMIS, 110, 833-844. doi:10.1034/j.1600-0463.2002.1101201.x.
16. Levin, B. E., Dunn-Meynell, A. A., & Banks, W. A. (2004). Obesityprone rats have normal blood-brain barrier transport but defective central leptin signaling before obesity onset. The American Journal of Physiology, 286, R143-R150.
17. Lew, J., Huang, Q. Q., Qi, Z., Winkfein, R. J., Aebersold, R., Hunt, T., et al. (1994). A brain-specific activator of cyclin-dependent kinase 5. Nature, 371, 423-426. doi:10.1038/371423a0.
18. Lew, J., Qi, Z., Huang, Q. Q., Paudel, H., Matsuura, I., Matsushita, M., et al. (1995). Structure, function, and regulation of neuronal Cdc2-like protein kinase. Neurobiology of Aging, 16, 263-268. doi:10.1016/0197-4580 (95) 00014-6.
19. Lin, H., Chen, M. C., Chiu, C. Y., Song, Y. M., & Lin, S. Y. (2007). Cdk5 regulates STAT3 activation and cell proliferation in medullary thyroid carcinoma cells. The Journal of Biological Chemistry, 282, 2776-2784. doi:10.1074/jbc. M607234200.
20. Meijer, L., Borgne, A., Mulner, O., Chong, J. P., Blow, J. J., Inagaki, N., et al. (1997). Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. European Journal of Biochemistry, 243, 527-536. doi:10.1111/j.1432-1033. 1997.t01-2-00527.x.
21. Meyerson, M., Enders, G. H., Wu, C. L., Su, L. K., Gorka, C., Nelson, C., et al. (1992). A family of human cdc2-related protein kinases. The EMBO Journal, 11, 2909-2917.
22. O'Rourke, L., & Shepherd, P. R. (2002). Biphasic regulation of extracellular-signal-regulated protein kinase by leptin in macrophages: Role in regulating STAT3 Ser727 phosphorylation and DNA binding. The Biochemical Journal, 364, 875-879. doi:10.1042/BJ20020295.
23. Ohshima, T., Gilmore, E. C., Longenecker, G., Jacobowitz, D. M., Brady, R. O., Herrup, K., et al. (1999). Migration defects of cdk5 (-/-) neurons in the developing cerebellum is cell autonomous. The Journal of Neuroscience, 19, 6017-6026.
24. Pan, W., Hsuchou, H., He, Y., Sakharkar, A., Cain, C., Yu, C., et al. (2008a). Astrocyte leptin receptor (ObR) and leptin transport in adult-onset obese mice. Endocrinology, 149, 2798-2806. doi:10.1210/en. 2007-1673.
25. Pan, W., Hsuchou, H., Tu, H., & Kastin, A. J. (2008b). Developmental changes of leptin receptors in cerebral microvessels: Unexpected relation to leptin transport. Endocrinology, 149, 877-885. doi:10.1210/en. 2007-0893.
26. Pan, W., & Kastin, A. J. (2007a). Adipokines and the blood-brain barrier. Peptides, 28, 1317-1330. doi:10.1016/j.peptides.2007. 04.023.
27. Pan, W., & Kastin, A. J. (2007b). Mahogany, blood-brain barrier, and fat mass surge in A (VY) mice. International Journal of Obesity, 31, 1030-1032. doi:10.1038/sj.ijo.0803536.
28. Pan, W., Tu, H., Hsuchou, H., Daniel, J., & Kastin, A. J. (2007). Unexpected amplification of leptin-induced Stat3 signaling by urocortin: Implications for obesity. Journal of Molecular Neuroscience, 33, 232-238. doi:10.1007/s12031-007-0071-y.
29. Patrick, G. N., Zukerberg, L., Nikolic, M., de la Monte, S., Dikkes, P., & Tsai, L. H. (1999). Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature, 402, 615-622. doi:10.1038/45159.
30. Rosenblum, C. I., Tota, M., Cully, D., Smith, T., Collum, R., Qureshi, S., et al. (1996). Functional STAT 1 and 3 signaling by the leptin receptor (OB-R); reduced expression of the rat fatty leptin receptor in transfected cells. Endocrinology, 137, 5178-5181. doi:10.1210/en. 137.11.5178.
31. Russo, V. C., Metaxas, S., Kobayashi, K., Harris, M., & Werther, G. A. (2004). Antiapoptotic effects of leptin in human neuroblastoma cells. Endocrinology, 145, 4103-4112. doi:10.1210/en. 2003-1767.
32. Schwartz, M. W., Woods, S. C., Porte Jr, D., Seeley, R. J., & Baskin, D. G. (2000). Central nervous system control of food intake. Nature, 404, 661-671.
33. Sitko, J. C., Yeh, B., Kim, M., Zhou, H., Takaesu, G., Yoshimura, A., et al. (2008). SOCS3 regulates p21 expression and cell cycle arrest in response to DNA damage. Cell Signal, 20, 2221-2230.
34. Tang, D., Lee, K. Y., Qi, Z., Matsuura, I., & Wang, J. H. (1996). Neuronal Cdc2-like kinase: From cell cycle to neuronal function. Biochemistry and Cell Biology, 74, 419-429.
35. Tsai, L. H., Delalle, I., Caviness Jr, V. S., Chae, T., & Harlow, E. (1994). p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature, 371, 419-423. doi:10.1038/371419a0.
36. Tsai, L. H., Takahashi, T., Caviness Jr, V. S., & Harlow, E. (1993). Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development, 119, 1029-1040.
37. Tseng, H. C., Zhou, Y., Shen, Y., & Tsai, L. H. (2002). A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Letters, 523, 58-62. doi:10.1016/S0014-5793 (02) 02934-4.
38. Tu, H., Kastin, A. J., Hsuchou, H., & Pan, W. (2008). Soluble receptor inhibits leptin transport. Journal of Cellular Physiology, 214, 301-305. doi:10.1002/jcp. 21195.
39. Tu, H., Pan, W., Feucht, L., & Kastin, A. J. (2007). Convergent trafficking pattern of leptin after endocytosis mediated by ObRa-ObRd. Journal of Cellular Physiology, 212, 215-222. doi:10.1002/jcp. 21020.
40. Vaisse, C., Halaas, J. L., Horvath, C. M., Darnell Jr, J. E., Stoffel, M., & Friedman, J. M. (1996). Leptin activation of Stat3 in the hypothalamus of wild-type and ob/ob mice but not db/db mice. Nature Genetics, 14, 95-97. doi:10.1038/ng0996-95.
41. Veeranna, S. K. T., Takahashi, M., Grant, P., & Pant, H. C. (2000). Cdk5 and MAPK are associated with complexes of cytoskeletal proteins in rat brain. Brain Research. Molecular Brain Research, 76, 229-236. doi:10.1016/S0169-328X (00) 00003-6.
42. Waelput, W., Verhee, A., Broekaert, D., Eyckerman, S., Vandekerckhove, J., Beattie, J. H., et al. (2000). Identification and expression analysis of leptin-regulated immediate early response and late target genes. The Biochemical Journal, 348 (Pt 1), 55-61. doi:10.1042/0264-6021:3480055.
43. Wang, Y., Xie, W. Y., He, Y., Wang, M., Yang, Y. R., Zhang, Y., et al. (2006). Role of CDK5 in neuroprotection from serum deprivation by mu-opioid receptor agonist. Experimental Neurology, 202, 313-323. doi:10.1016/j.expneurol.2006.06.005.
44. Xu, L., Rensing, N., Yang, X. F., Zhang, H. X., Thio, L. L., Rothman, S. M., et al. (2008). Leptin inhibits 4-aminopyridine-and pentylenetetrazole- induced seizures and AMPAR-mediated synaptic transmission in rodents. The Journal of Clinical Investigation, 118, 272-280. doi:10.1172/JCI33009.
45. Yan, Z., Chi, P., Bibb, J. A., Ryan, T. A., & Greengard, P. (2002). Roscovitine: A novel regulator of P/Q-type calcium channels and transmitter release in central neurons. The Journal of Physiology, 540, 761-770. doi:10.1113/jphysiol.2001.013376.
46. Zabolotny, J. M., Bence-Hanulec, K. K., Stricker-Krongrad, A., Haj, F., Wang, Y., Minokoshi, Y., et al. (2002). PTP1B regulates leptin signal transduction in vivo. Developmental Cell, 2, 489-495. doi:10.1016/S1534-5807 (02) 00148-X.
47. Zheng, M., Leung, C. L., & Liem, R. K. (1998). Region-specific expression of cyclin-dependent kinase 5 (cdk5) and its activators, p35 and p39, in the developing and adult rat central nervous system. Journal of Neurobiology, 35, 141-159. doi:10.1002/(SICI) 1097-4695 (199805) 35:2<141::AID-NEU2>3.0.CO;2-4.
48. Zlokovic, B. V., Jovanovic, S., Miao, W., Samara, S., Verma, S., & Farrell, C. L. (2000). Differential regulation of leptin transport by the choroid plexus and blood-brain barrier and high affinity transport systems for entry into hypothalamus and across the blood-cerebrospinal fluid barrier. Endocrinology, 141, 1434-1441. doi:10.1210/en. 141.4.1434.