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The Functional Interaction Between CDK11p58 and β-1,4-Galactosyltransferase I Involved in Astrocyte Activation Caused by Lipopolysaccharide

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Abstract

Glial cells are mediating the main activation of the central nervous system (CNS), being astrocytes the mayor glial cells in the brain. Glial activation may result beneficial since it could promote tissue repair and pathogen elimination. However, excessive glial activation mechanism can also have do harm to the tissue. β-1,4-Galactosyltransferase I (β-1,4-GalT-I) is a key inflammatory mediator that participates in the initiation and maintenance of inflammatory reaction in some diseases. Moreover, CDK11p58 has been reported to be associated with β-1,4-GalT-I. We have found that CDK11p58 and β-1,4-GalT-I are induced in lipopolysaccharide (LPS)-challenged rat primary astrocytes in a affinis dose- and time-dependent manner. CDK11p58 regulates the expression of β-1,4-GalT-I by interacting with it. After the knockdown of CDK11p58 expression, the expression of β-1,4-GalT-I decreases, and astrocyte activation downregulates. Inversely, the expression of β-1,4-GalT-I increases, and astrocyte activation enhances due to the overexpression of CDK11p58. Knockdown of β-1,4-GalT-I reduces the activation potentiation caused by the overexpression of CDK11p58, illustrating the function of CDK11p58 to promote astrocyte activation depends on β-1,4-GalT-I. The interaction between CDK11p58 and β-1,4-GalT-I to upregulate astrocyte activation is related to activating p38 and JNK pathways. These findings indicated that the functional interaction between CDK11p58 and β-1,4-GalT-I may play an important role during astrocyte activation after LPS administration.

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References

  1. Zhao, G., and M. Flavin. 2000. Differential sensitivity of rat hippocampal and cortical astrocytes to oxygen–glucose deprivation injury. Neuroscience Letters 285: 177–180.

    Article  PubMed  CAS  Google Scholar 

  2. Smith, S.J. 1992. Do astrocytes process neural information? Progress in Brain Research 94: 119–136.

    Article  PubMed  CAS  Google Scholar 

  3. Dong, Y., and E.N. Benveniste. 2001. Immune function of astrocytes. Glia 36: 180–190.

    Article  PubMed  CAS  Google Scholar 

  4. Liu, L., M. Rudin, and E.N. Kozlova. 2000. Glial cell proliferation in the spinal cord after dorsal rhizotomy or sciatic nerve transection in the adult rat. Experimental Brain Research 131: 64–73.

    Article  CAS  Google Scholar 

  5. Ridet, J.L., S.K. Malhotra, A. Privat, and F.H. Gage. 1997. Reactive astrocytes: cellular and molecular cues to biological function. Trends in Neurosciences 20: 570–577.

    Article  PubMed  CAS  Google Scholar 

  6. Hamill, C.E., A. Goldshmidt, O. Nicole, R.J. McKeon, D.J. Brat, and S.F. Traynelis. 2005. Glial reactivity following damage: implications for scar formation and neuronal recovery. Clinical Neurosurgery 52: 29–44.

    PubMed  Google Scholar 

  7. Liberto, C.M., P.J. Albrecht, L.M. Herx, V.W. Yong, and S.W. Levison. 2004. Proregenerative properties of cytokine-activated astrocytes. Journal of Neurochemistry 89: 1092–1100.

    Article  PubMed  CAS  Google Scholar 

  8. Menet, V., M. Prieto, A. Privat, and M. Gimenez y Ribotta. 2003. Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proceedings of the National Academy of Sciences of the United States of America 100: 8999–9004.

    Article  PubMed  CAS  Google Scholar 

  9. Silver, J., and J.H. Miller. 2004. Regeneration beyond the glial scar. Nature Reviews Neuroscience 5: 146–156.

    Article  PubMed  CAS  Google Scholar 

  10. Mrak, R.E., and W.S. Griffin. 2001. Interleukin-1, neuroinflammation, and Alzheimer’s disease. Neurobiology of Aging 22: 903–908.

    Article  PubMed  CAS  Google Scholar 

  11. Wyss-Coray, T., and L. Mucke. 2002. Inflammation in neurodegenerative disease-a double-edged sword. Neuron 35: 419–432.

    Article  PubMed  CAS  Google Scholar 

  12. Shur, B.D. 1991. Cell surface beta 1,4 galactosyltransferase: twenty years later. Glycobiology 1(6): 563–575.

    Article  PubMed  CAS  Google Scholar 

  13. Yang, H., L. Hu, J. Chen, J. Zhu, T. Tao, F. Zhang, X. Li, X. He, A. Shen, and C. Cheng. 2009. Lipopolysaccharide induced upregulation of beta-1,4-galactosyltransferase-I in Schwann cell. Inflammation 32(5): 279–286.

    Article  PubMed  CAS  Google Scholar 

  14. Asano, M., S. Nakae, N. Kotani, N. Shirafuji, A. Nambu, and N. Hashimoto. 2003. Impaired selectin-ligand biosynthesis and reduced inflammatory responses in beta-1,4-galactosyltransferase-I-deficient mice. Blood 102: 1678–1685.

    Article  PubMed  CAS  Google Scholar 

  15. Mori, R., T. Kondo, T. Nishima, and M. Asano. 2004. Impairment of skin wound healing in β-1,4-galactosyltransferase-deficient mice with reduced leukocyte recruitment. American Journal of Pathology 164: 1303–1314.

    Article  PubMed  CAS  Google Scholar 

  16. Bunnellt, B.A., D.E. Adams, and V.J. Kiddt. 1990. Transient expression of a CDK11p58 protein kinase cDNA enhances mammalian glycosyltransferase activity. Biochemical and Biophysical Research Communications 171(1): 196–203.

    Article  Google Scholar 

  17. Bunnell, B.A., L.S. Heath, D.E. Adams, J.M. Lahti, and V.J. Kidd. 1990. Increased expression of a 58-kDa protein kinase leads to changes in the CHO cell cycle. Proceedings of the National Academy of Sciences 87: 7467–7471.

    Article  CAS  Google Scholar 

  18. Trembley, J.H., D. Hu, L.C. Hsu, C.Y. Yeung, C. Slaughter, J.M. Lahti, and V.J. Kidd. 2002. PITSLRE p110 protein kinases associate with transcription complexes and affect their activity. Journal of Biological Chemistry 277: 2589–2596.

    Article  PubMed  CAS  Google Scholar 

  19. Lahti, J.M., J. **ang, L.S. Heath, D. Campana, and V.J. Kidd. 1995. PITSLRE protein kinase activity is associated with apoptosis. Molecular and Cellular Biology 15: 1–11.

    PubMed  CAS  Google Scholar 

  20. Hu, D., A. Mayeda, J.H. Trembley, J.M. Lahti, and V.J. Kidd. 2003. CDK11 complexes promote pre-mRNA splicing. Journal of Biological Chemistry 278: 8623–8629.

    Article  PubMed  CAS  Google Scholar 

  21. Ariza, M.E., M. Broome-Powell, J.M. Lahti, V.J. Kidd, and M.A. Nelson. 1999. Fas-induced apoptosis in human malignant melanoma cell lines is associated with the activation of the p34(cdc2)-related PITSLRE protein kinases. Journal of Biological Chemistry 274: 28505–28513.

    Article  PubMed  CAS  Google Scholar 

  22. Li, T., A. Inoue, J.M. Lahti, and V.J. Kidd. 2004. Failure to proliferate and mitotic arrest of CDK11(p110/p58)-null mutant mice at the blastocyst stage of embryonic cell development. Molecular and Cellular Biology 24(8): 3188–3197.

    Article  PubMed  CAS  Google Scholar 

  23. Ji, Y., F. **ao, and L. Sun. 2008. Increased expression of CDK11p58 and cyclin D3 following spinal cord injury in rats. Molecular and Cellular Biochemistry 309: 49–60.

    Article  PubMed  CAS  Google Scholar 

  24. Zhang, S.W., S.L. Xu, M.M. Cai, J. Yan, X.Y. Zhu, Y. Hu, and J.X. Gu. 2001. Effect of p58GTA on beta-1,4-galactosyltransferase 1 activity and cell-cycle in human hepatocarcinoma cells. Molecular and Cellular Biochemistry 221(1–2): 161–168.

    Article  PubMed  CAS  Google Scholar 

  25. Kong, X., H. Gan, and Y. Hao. 2009. CDK11p58 phosphorylation of PAK1 Ser174 promotes DLC2 binding and roles on cell cycle progression. Journal of Biochemistry 146(3): 417–427.

    Article  PubMed  CAS  Google Scholar 

  26. Glasgow, L.R., J.C. Paulson, and R.L. Hill. 1977. Systematic purification of five glycosidases from Streptococcus (Diplococcus) pneumoniae. Journal of Biological Chemistry 252: 8615–8623.

    PubMed  CAS  Google Scholar 

  27. Nakamura, N., N. Yamakawa, T. Sato, H. Tojo, C. Tachi, and K. Furukawa. 2001. Differential gene expression of beta-1,4-galactosyltransferases I, II and V during mouse brain development. Journal of Neurochemistry 76: 29–38.

    Article  PubMed  CAS  Google Scholar 

  28. Baenziger, J.U., and D. Fiete. 1979. Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. Journal of Biological Chemistry 254: 9795–9799.

    PubMed  CAS  Google Scholar 

  29. Eckstein, D.J., and B.D. Shur. 1992. Cell surface beta-1,4-galactosyltransferase is associated with the detergent-insoluble cytoskeleton on migrating mesenchymal cells. Journal Experimental Cell Research 201: 83–90.

    Article  CAS  Google Scholar 

  30. Evans, S.C., L.C. Lopez, and B.D. Shur. 1993. Dominant negative mutation in cell surface beta-1,4-Galactosyltransferase inhibits cell–cell and cell–matrix interactions. Journal of Biological Chemistry 120: 1045–1057.

    CAS  Google Scholar 

  31. Hathaway, H.J., and B.D. Shur. 1992. Cell surface beta-l,4-galactosyltransferase functions during neural crest cell migration and neurulation in vivo. The Journal of Cell Biology 117: 369–382.

    Article  PubMed  CAS  Google Scholar 

  32. Huang, Q.L., B.D. Shur, and P.C. Begovac. 1995. Overexpression cell surface β-1,4-galactosyltransferase-I in PC12 cells increases neurite outgrowth on laminin. Journal of Cell Science 108: 839–847.

    PubMed  CAS  Google Scholar 

  33. Maillet, C.M., and B.D. Shur. 1994. Perturbing cell surface β-1,4-galactosyltransferase on F9 embryonal carcinoma cells arrests cell growth and induces laminin synthesis. Journal of Cell Science 107: 1713–1724.

    PubMed  CAS  Google Scholar 

  34. Miller, D.J., M.B. Macek, and B.D. Shur. 1992. Complementarity between sperm surface beta-l,4-galactosyltransferase and egg-coat ZP3 mediates sperm–egg binding. Journal of Natural 357: 589–593.

    CAS  Google Scholar 

  35. Ridet, J.L., S.K. Malhotra, A. Privat, and F.H. Gage. 1997. Reactive astrocytes: cellular and molecular cues to biological function. Trends in Neurosciences 20: 570–577.

    Article  PubMed  CAS  Google Scholar 

  36. Kidd, V.J., D. Hu, M. Valentine, and J.M. Lahti. 2007. CDK11(p58) is required for the maintenance of sister chromatid cohesion. Journal of Cell Science 120(14): 2424–2434.

    Article  PubMed  Google Scholar 

  37. Niu, Z., A. Shen, H. Shen, J. Jiang, H. Zong, and J. Gu. 2005. Protein expression pattern of CDK11(p58) during testicular development in the mouse. Molecular and Cellular Biochemistry 70(1–2): 99–106.

    Article  Google Scholar 

  38. Cornelis, S., Y. Bruynooghe, G. Denecker, S. Van Huffel, S. Tinton, and R. Beyaert. 2000. Identification and characterization of a novel cell cycle-regulated internal ribosome entry site. Molecular Cell 5(4): 597–605.

    Article  PubMed  CAS  Google Scholar 

  39. Ariza, M.E., M. Broome-Powell, J.M. Lahti, V.J. Kidd, and M.A. Nelson. 1999. Fas-induced apoptosis in human malignant melanoma cell lines is associated with the activation of the p34(cdc2)-related PITSLRE protein kinases. Journal of Biological Chemistry 274: 28505–28513.

    Article  PubMed  CAS  Google Scholar 

  40. Hensley, K., R.A. Floyd, N.Y. Zheng, R. Nael, K.A. Robinson, X. Nguyen, Q.N. Pye, C.A. Stewart, J. Geddes, W.R. Markesbery, et al. 1999. p38 kinase is activated in the Alzheimer’s disease brain. Journal of Neurochemistry 72: 2053–2058.

    Article  PubMed  CAS  Google Scholar 

  41. Ferrer, I., R. Blanco, M. Carmona, B. Puig, M. Barrachina, C. Gomez, and S. Ambrosio. 2001. Active, phosphorylation-dependent mitogen-activated protein kinase (MAPK/ERK), stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK), and p38 kinase expression in Parkinson’s disease and dementia with Lewy bodies. Journal of Neural Transmission 108: 1383–1396.

    Article  PubMed  CAS  Google Scholar 

  42. Piao, C.S., Y. Che, P.L. Han, and J.K. Lee. 2002. Delayed and differential induction of p38 MAPK isoforms in microglia and astrocytes in the brain after transient global ischemia. Brain Research. Molecular Brain Research 107: 137–144.

    Article  PubMed  CAS  Google Scholar 

  43. Ferrer, I., P. Pastor, M.J. Rey, E. Munoz, B. Puig, E. Pastor, R. Oliva, and E. Tolosa. 2003. Phosphorylation and kinase activation in familial tauopathy linked to deln296 mutation. Neuropathology and Applied Neurobiology 29: 23–34.

    Article  PubMed  CAS  Google Scholar 

  44. Ferrer, I., M. Barrachina, M. Tolnay, M.J. Rey, N. Vidal, M. Carmona, R. Blanco, and B. Puig. 2003. Phosphorylated protein kinases associated with neuronal and glial-deposits in argyrophilic grain disease. Brain Pathology 13: 62–78.

    Article  PubMed  CAS  Google Scholar 

  45. Shin, T., M. Ahn, K. Jung, S. Heo, D. Kim, Y. Jee, Y.K. Lim, and E.J. Yeo. 2003. Activation of mitogen-activated protein kinases in experimental autoimmune encephalomyelitis. Journal of Neuroimmunology 140: 118–125.

    Article  PubMed  CAS  Google Scholar 

  46. Migheli, A., R. Piva, C. Atzori, D. Troost, and D. Schiffer. 1997. c-Jun, JNK/SAPK kinases and transcription factor NF-_B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. Journal of Neuropathology and Experimental Neurology 56: 1314–1322.

    Article  PubMed  CAS  Google Scholar 

  47. Hua, L.L., M.L. Zhao, M. Cosenza, M.O. Kim, H. Huang, H.B. Tanowitz, C.F. Brosnan, and S.C. Lee. 2002. Role of mitogen-activated protein kinases in inducible nitric oxide synthase and TNFalpha expression in human fetal astrocytes. Journal of Neuroimmunology 126: 180–189.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Basic Research Program of China (973 Program, No.2011CB910604, and No.2012BC822104); the National Natural Science Foundation of China (No.31070723, No.81070275 and No. 81172879); Natural Science Foundation of Jiangsu province (No.BK2009157, and No.BK2010169); Key Project Natural Science Foundation of Jiangsu University and College (No.11KJA310002); A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Correspondence to **ang Lu or Aiguo Shen.

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Liu, X., Cheng, C., Shao, B. et al. The Functional Interaction Between CDK11p58 and β-1,4-Galactosyltransferase I Involved in Astrocyte Activation Caused by Lipopolysaccharide. Inflammation 35, 1365–1377 (2012). https://doi.org/10.1007/s10753-012-9450-9

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