The laforin-malin complex, involved in Lafora disease, promotes the incorporation of K63-linked ubiquitin chains into AMP-activated protein kinase β subunits

Molecular Biology of the Cell

Volumn 21, Issue 15, 2010, Pages 2578-2588

  Moreno, Daniel ^a   Towler, Mhairi C ^b   Hardie, D Grahame ^b   Knecht, Erwin ^a   Sanz, Pascual ^a  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; DUAL SPECIFICITY PHOSPHATASE LAFORIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; OLIGONUCLEOTIDE; PROTEASOME; PROTEIN SUBUNIT; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 MALIN; UNCLASSIFIED DRUG;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CELL ENERGY; CELL INCLUSION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MYOCLONUS EPILEPSY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; STEADY STATE; UBIQUITINATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARRIER PROTEINS; CELL LINE; HUMANS; LAFORA DISEASE; LEUPEPTINS; LYSINE; MICE; MULTIPROTEIN COMPLEXES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITINATION;

EID: 77955098709     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-03-0227     Document Type: Article

References (46)

1. Bateman, A. (1997). The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22, 12-13.
2. Brady, M., Vlatkovic, N., and Boyd, M. T. (2005). Regulation of p53 and MDM2 activity by MTBP. Mol. Cell. Biol. 25, 545-553.
3. Crute, B. E., Seefeld, K., Gamble, J., Kemp, B. E., and Witters, L. A. (1998). Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. J. Biol. Chem. 273, 35347-35354.
4. Chan, E. M., Omer, S., Ahmed, M., Bridges, L. R., Bennett, C., Scherer, S. W., and Minassian, B. A. (2004). Progressive myoclonus epilepsy with polyglucosans (Lafora disease): evidence for a third locus. Neurology 63, 565-567. (Pubitemid 39031396)
5. Chan, E. M., et al. (2003). Mutations in NHLRC1 cause progressive myoclonus epilepsy. Nat. Genet. 35, 125-127.
6. Delgado-Escueta, A. V. (2007). Advances in lafora progressive myoclonus epilepsy. Curr. Neurol. Neurosci. Rep. 7, 428-433.
7. Deshaies, R. J., and Joazeiro, C. A. (2009). RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
8. Ganesh, S., et al. (2002). Targeted disruption of the Epm2a gene causes formation of Lafora inclusion bodies, neurodegeneration, ataxia, myoclonus epilepsy and impaired behavioral response in mice. Hum. Mol. Genet. 11, 1251-1262.
9. Ganesh, S., Puri, R., Singh, S., Mittal, S., and Dubey, D. (2006). Recent advances in the molecular basis of Lafora's progressive myoclonus epilepsy. J. Hum. Genet. 51, 1-8.
10. Gentry, M. S., Dixon, J. E., and Worby, C. A. (2009). Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem. Sci. 34, 628-639.
11. Gentry, M. S., Dowen, R. H., 3rd, Worby, C. A., Mattoo, S., Ecker, J. R., and Dixon, J. E. (2007). The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J. Cell Biol. 178, 477-488.
12. Gentry, M. S., Worby, C. A., and Dixon, J. E. (2005). Insights into Lafora disease: malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin. Proc. Natl. Acad. Sci. USA 102, 8501-8506.
13. Gimeno-Alcaniz, J. V., and Sanz, P. (2003). Glucose and type 2A protein phosphatase regulate the interaction between catalytic and regulatory sub-units of AMP-activated protein kinase. J. Mol. Biol. 333, 201-209.
14. Ikeda, F., and Dikic, I. (2008). Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep. 9, 536-542.
15. Kaiser, P., and Tagwerker, C. (2005). Is this protein ubiquitinated? Methods Enzymol. 399, 243-248.
16. Kostova, Z., Tsai, Y. C., and Weissman, A. M. (2007). Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin. Cell Dev. Biol. 18, 770-779.
17. Lim, K. L., et al. (2005). Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1, implications for Lewy body formation. J. Neurosci. 25, 2002-2009.
18. Lim, K. L., Dawson, V. L., and Dawson, T. M. (2006). Parkin-mediated lysine 63-linked polyubiquitination: a link to protein inclusions formation in Parkinson's and other conformational diseases? Neurobiol. Aging 27, 524-529.
19. Liu, C., Fei, E., Jia, N., Wang, H., Tao, R., Iwata, A., Nukina, N., Zhou, J., and Wang, G. (2007). Assembly of lysine 63-linked ubiquitin conjugates by phosphorylated alpha-synuclein implies Lewy body biogenesis. J. Biol. Chem. 282, 14558-14566.
20. Liu, Y., Wang, Y., Wu, C., Liu, Y., and Zheng, P. (2009). Deletions and missense mutations of EPM2A exacerbate unfolded protein response and apoptosis of neuronal cells induced by endoplasm reticulum stress. Hum. Mol. Genet. 18, 2622-2631.
21. Lohi, H., Ianzano, L., Zhao, X. C., Chan, E. M., Turnbull, J., Scherer, S. W., Ackerley, C. A., and Minassian, B. A. (2005). Novel glycogen synthase kinase 3 and ubiquitination pathways in progressive myoclonus epilepsy. Hum. Mol. Genet. 14, 2727-2736.
22. Minassian, B. A., Ianzano, L., Meloche, M., Andermann, E., Rouleau, G. A., Delgado-Escueta, A. V., and Scherer, S. W. (2000). Mutation spectrum and predicted function of laforin in Lafora's progressive myoclonus epilepsy. Neurology 55, 341-346.
23. Minassian, B. A., et al. (1998). Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat. Genet. 20, 171-174.
24. Mittal, S., Dubey, D., Yamakawa, K., and Ganesh, S. (2007). Lafora disease proteins malin and laforin are recruited to aggresomes in response to proteasomal impairment. Hum. Mol. Genet. 16, 753-762.
25. Newton, K., et al. (2008). Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678.
26. Olzmann, J. A., Li, L., Chudaev, M. V., Chen, J., Perez, F. A., Palmiter, R. D., and Chin, L. S. (2007). Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J. Cell Biol. 178, 1025-1038.
27. Pang, T., Xiong, B., Li, J. Y., Qiu, B. Y., Jin, G. Z., Shen, J. K., and Li, J. (2007). Conserved alpha-helix acts as autoinhibitory sequence in AMP-activated protein kinase alpha subunits. J. Biol. Chem. 282, 495-506.
28. Qi, J., Gong, J., Zhao, T., Zhao, J., Lam, P., Ye, J., Li, J. Z., Wu, J., Zhou, H. M., and Li, P. (2008). Downregulation of AMP-activated protein kinase by Cidea-mediated ubiquitination and degradation in brown adipose tissue. EMBO J. 27, 1537-1548.
29. Rao, S. N., Sharma, J., Maity, R., and Jana, N. R. (2010). Co-chaperone CHIP stabilizes aggregate-prone malin, a ubiquitin ligase mutated in Lafora disease. J. Biol. Chem. 285, 1404-1413.
30. Sanz, P. (2008). AMP-activated protein kinase: structure and regulation. Curr. Protein Peptide Sci. 9, 478-492.
31. Scott, J. W., Hawley, S. A., Green, K. A., Anis, M., Stewart, G., Scullion, G. A., Norman, D. G., and Hardie, D. G. (2004). CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J. Clin. Invest. 113, 274-284.
32. Serratosa, J. M., et al. (1999). A novel protein tyrosine phosphatase gene is mutated in progressive myoclonus epilepsy of the Lafora type (EPM2). Hum. Mol. Genet 8, 345-352.
33. Solaz-Fuster, M. C., Gimeno-Alcaniz, J. V., Casado, M., and Sanz, P. (2006). TRIP6 transcriptional co-activator is a novel substrate of AMP-activated protein kinase. Cell Signal. 18, 1702-1712. (Pubitemid 44216134)
34. Solaz-Fuster, M. C., et al. (2008). Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMP-activated protein kinase pathway. Hum. Mol. Genet. 17, 667-678.
35. Tagliabracci, V. S., Girard, J. M., Segvich, D., Meyer, C., Turnbull, J., Zhao, X., Minassian, B. A., Depaoli-Roach, A. A., and Roach, P. J. (2008). Abnormal metabolism of glycogen phosphate as a cause for Lafora disease. J. Biol. Chem. 283, 33816-33825.
36. Tagliabracci, V. S., et al. (2007). Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc. Natl. Acad. Sci. USA 104, 19262-19266.
37. Tan, J. M., et al. (2008). Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 17, 431-439.
38. Thornton, C., Snowden, M. A., and Carling, D. (1998). Identification of a novel AMP-activated protein kinase beta subunit isoform that is highly expressed in skeletal muscle. J. Biol. Chem. 273, 12443-12450.
39. Vernia, S., Rubio, T., Heredia, M., Rodriguez de Cordoba, S., and Sanz, P. (2009). Increased endoplasmic reticulum stress and decreased proteasomal function in lafora disease models lacking the phosphatase laforin. PloS One 4, e5907.
40. Wang, J., Stuckey, J. A., Wishart, M. J., and Dixon, J. E. (2002). A unique carbohydrate binding domain targets the lafora disease phosphatase to glycogen. J. Biol. Chem. 277, 2377-2380.
41. Windheim, M., Peggie, M., and Cohen, P. (2008). Two different classes of E2 ubiquitin-conjugating enzymes are required for the mono-ubiquitination of proteins and elongation by polyubiquitin chains with a specific topology. Biochem. J. 409, 723-729.
42. Worby, C. A., Gentry, M. S., and Dixon, J. E. (2006). Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J. Biol. Chem. 281, 30412-30418.
43. Worby, C. A., Gentry, M. S., and Dixon, J. E. (2008). Malin decreases glycogen accumulation by promoting the degradation of protein targeting to glycogen (PTG). J. Biol. Chem. 283, 4069-4076.
44. Xiao, B., et al. (2007). Structural basis for AMP binding to mammalian AMPactivated protein kinase. Nature 449, 496-500.
45. Xu, Z., Kohli, E., Devlin, K. I., Bold, M., Nix, J. C., and Misra, S. (2008). Interactions between the quality control ubiquitin ligase CHIP and ubiquitin conjugating enzymes. BMC Struct. Biol. 8, 26.
46. Yoshida, H. (2007). ER stress and diseases. FEBS J. 274, 630-658.