Cln6 mutants associated with neuronal ceroid lipofuscinosis are degraded in a proteasome-dependent manner

Bioscience Reports

Volumn 29, Issue 3, 2009, Pages 173-181

  Oresic, Kristina ^a   Mueller, Britta ^b   Tortorella, Domenico ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Derlin 1; Endoplasmic reticulum quality control; Endoplasmic reticulum associated degradation (ERAD); Genetic disease; Misfolded membrane protein; sel 1 suppressor of lin 12 like (Caenorhabditis elegans) (SEL1L)

Indexed keywords

DERLIN 1; MUTANT PROTEIN; PROTEASOME; PROTEIN; PROTEIN CLN6; PROTEIN P97; PROTEIN SEL1L; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NEURONAL CEROID LIPOFUSCINOSIS; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; QUALITY CONTROL;

AMINO ACID SUBSTITUTION; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE PROTEINS; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; UBIQUITIN-PROTEIN LIGASES;

CAENORHABDITIS ELEGANS;

EID: 67249116116     PISSN: 01448463     EISSN: None     Source Type: Journal    
DOI: 10.1042/BSR20080143     Document Type: Article

References (54)

1. Rider, J. A. and Rider, D. L. (1997) Batten disease, a twenty-eight-year struggle: past, present and future. Neuropediatrics 28, 4-5 (Pubitemid 27283145)
2. Goebel, H. H. and Wisniewski, K. E. (2004) Current state of clinical and morphological features in human NCL. Brain Pathol. 14, 61-69 (Pubitemid 38200591)
3. Kohlschutter, A., Gardiner, R. M. and Goebel, H. H. (1993) Human forms of neuronal ceroid-lipofuscinosis (Batten disease): consensus on diagnostic criteria, Hamburg 1992. J. Inherit. Metab. Dis. 16, 241-244 (Pubitemid 23213638)
4. Wisniewski, K. E., Rapin, I. and Heaney-Kieras, J. (1988) Clinico-pathological variability in the childhood neuronal ceroid-lipofuscinoses and new observations on glycoprotein abnormalities. Am. J. Med. Genet. Suppl. 5, 27-46
5. Prasad, V. V. and Pullarkat, R. K. (1996) Brain lysosomal hydrolases in neuronal ceroid-lipofuscinoses. Mol. Chem. Neuropathol. 29, 169-179
6. Palmer, D. N., Tyynela, J., van Mil, H. C., Westlake, V. J. and Jolly, R. D. (1997) Accumulation of sphingolipid activator proteins (SAPs) A and D in granular osmiophilic deposits in miniature Schnauzer dogs with ceroid-lipofuscinosis. J. Inherit. Metab. Dis. 20, 74-84
7. Kyttala, A., Lahtinen, U., Braulke, T. and Hofmann, S. L. (2006) Functional biology of the neuronal ceroid lipofuscinoses (NCL) proteins. Biochim. Biophys. Acta 1762, 920-933
8. Qu, D., Teckman, J. H., Omura, S. and Perlmutter, D. H. (1996) Degradation of a mutant secretory protein, α1-antitrypsin Z, in the endoplasmic reticulum requires proteasome activity. J. Biol. Chem. 271, 22791-22795
9. Hirano, K., Zuber, C., Roth, J. and Ziak, M. (2003) The proteasome is involved in the degradation of different aquaporin-2 mutants causing nephrogenic diabetes insipidus. Am. J. Pathol. 163, 111-120
10. Halaban, R., Svedine, S., Cheng, E., Smicun, Y., Aran, R. and Hebert, D. N. (2000) Endoplasmic reticulum retention is a common defect associated with tyrosinase-negative albinism. Proc. Natl. Acad. Sci. U.S.A. 97, 5889-5894
11. Kida, E., Golabek, A. A. and Wisniewski, K. E. (2001) Cellular pathology and pathogenic aspects of neuronal ceroid lipofuscinoses. Adv. Genet. 45, 35-68
12. Wheeler, R. B., Sharp, J. D., Schultz, R. A., Joslin, J. M., Williams, R. E. and Mole, S. E. (2002) The gene mutated in variant late-infantile neuronal ceroid lipofuscinosis (CLN6) and in nclf mutant mice encodes a novel predicted transmembrane protein. Am. J. Hum. Genet. 70, 537-542
13. Gao, H., Boustany, R. M., Espinola, J. A., Cotman, S. L., Srinidhi, L., Antonellis, K. A., Gillis, T., Qin, X., Liu, S., Donahue, L. R. et al. (2002) Mutations in a novel CLN6-encoded transmembrane protein cause variant neuronal ceroid lipofuscinosis in man and mouse. Am. J. Hum. Genet. 70, 324-335
14. Heine, C., Quitsch, A., Storch, S., Martin, Y., Lonka, L., Lehesjoki, A. E., Mole, S. E. and Braulke, T. (2007) Topology and endoplasmic reticulum retention signals of the lysosomal storage disease-related membrane protein CLN6. Mol. Membr. Biol. 24, 74-87
15. Oresic, K., Noriega, V., Andrews, L. and Tortorella, D. (2006) A structural determinant of human cytomegalovirus US2 dictates the down-regulation of class I major histocompatibility molecules. J. Biol. Chem. 281, 19395-19406
16. Tortorella, D., Story, C. M., Huppa, J. B., Wiertz, E. J., Jones, T. R., Bacik, I., Bennink, J. R., Yewdell, J. W. and Ploegh, H. L. (1998) Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J. Cell Biol. 142, 365-376 (Pubitemid 28361545)
17. Mueller, B., Lilley, B. N. and Ploegh, H. L. (2006) SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J. Cell Biol. 175, 261-270 (Pubitemid 44631420)
18. Hochstenbach, F., David, V., Watkins, S. and Brenner, M. B. (1992) Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly. Proc. Natl. Acad. Sci. U.S.A. 89, 4734-4738
19. Teixeira, C. A., Espinola, J., Huo, L., Kohlschutter, J., Persaud Sawin, D. A., Minassian, B., Bessa, C. J., Guimaraes, A., Stephan, D. A., Sa Miranda, M. C. et al. (2003) Novel mutations in the CLN6 gene causing a variant late infantile neuronal ceroid lipofuscinosis. Hum. Mutat. 21, 502-508
20. Scott, D. C. and Schekman, R. (2008) Role of Sec61p in the ER-associated degradation of short-lived transmembrane proteins. J. Cell Biol. 181, 1095-1105 (Pubitemid 351915485)
21. Wang, Q., Li, L. and Ye, Y. (2006) Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J. Cell Biol. 174, 963-971 (Pubitemid 44455185)
22. Wiertz, E. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A. and Ploegh, H. L. (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438 (Pubitemid 26414653)
23. Fiebiger, E., Hirsch, C., Vyas, J. M., Gordon, E., Ploegh, H. L. and Tortorella, D. (2004) Dissection of the dislocation pathway for type I membrane proteins with a new small molecule inhibitor, eeyarestatin. Mol. Biol. Cell 15, 1635-1646
24. Omura, S., Fujimoto, T., Otoguro, K., Matsuzaki, K., Moriguchi, R., Tanaka, H. and Sasaki, Y. (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot. (Tokyo) 44, 113-116
25. Baker, B. M. and Tortorella, D. (2007) Dislocation of an endoplasmic reticulum membrane glycoprotein involves the formation of partially dislocated ubiquitinated polypeptides. J. Biol. Chem. 282, 26845-26856
26. Lilley, B. N. and Ploegh, H. L. (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840 (Pubitemid 38843291)
27. 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
28. Lilley, B. N. and Ploegh, H. L. (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 14296-14301
29. Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E. and Rapoport, T. A. (2005) Inaugural article: recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 14132-14138
30. Kopito, R. R. (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530 (Pubitemid 30831451)
31. Haltia, M. (2006) The neuronal ceroid-lipofuscinoses: from past to present. Biochim. Biophys. Acta 1762, 850-856
32. Hebert, D. N. and Molinari, M. (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87, 1377-1408
33. Aridor, M. (2007) Visiting the ER: the endoplasmic reticulum as a target for therapeutics in traffic related diseases. Adv. Drug Deliv. Rev. 59, 759-781
34. Brodsky, J. L. (2007) The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic- reticulum-associated degradation). Biochem. J. 404, 353-363 (Pubitemid 46953909)
35. Nakatsukasa, K. and Brodsky, J. L. (2008) The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9, 861-870 (Pubitemid 351639492)
36. Ye, Y., Meyer, H. H. and Rapoport, T. A. (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656 (Pubitemid 33151262)
37. Cheng, S. H., Gregory, R. J., Marshall, J., Paul, S., Souza, D. W., White, G. A., O'Riordan, C. R. and Smith, A. E. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834 (Pubitemid 120035055)
38. Yam, G. H., Zuber, C. and Roth, J. (2005) A synthetic chaperone corrects the trafficking defect and disease phenotype in a protein misfolding disorder. FASEB J. 19, 12-18 (Pubitemid 40069915)
39. Beck, M. (2007) New therapeutic options for lysosomal storage disorders: enzyme replacement, small molecules and gene therapy. Hum. Genet. 121, 1-22
40. Brady, R. O. (2006) Emerging strategies for the treatment of hereditary metabolic storage disorders. Rejuvenation Res. 9, 237-244 (Pubitemid 43856816)
41. Sakuraba, H., Sawada, M., Matsuzawa, F., Aikawa, S., Chiba, Y., Jigami, Y. and Itoh, K. (2006) Molecular pathologies of and enzyme replacement therapies for lysosomal diseases. CNS Neurol. Disord. Drug Targets 5, 401-413
42. Ahmad-Annuar, A., Tabrizi, S. J. and Fisher, E. M. (2003) Mouse models as a tool for understanding neurodegenerative diseases. Curr. Opin. Neurol. 16, 451-458
43. Cooper, J. D., Russell, C. and Mitchison, H. M. (2006) Progress towards understanding disease mechanisms in small vertebrate models of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 1762, 873-889
44. Hafezparast, M., Ahmad-Annuar, A., Wood, N. W., Tabrizi, S. J. and Fisher, E. M. (2002) Mouse models for neurological disease. Lancet Neurol. 1, 215-224 (Pubitemid 37159183)
45. Gupta, P., Soyombo, A. A., Atashband, A., Wisniewski, K. E., Shelton, J. M., Richardson, J. A., Hammer, R. E. and Hofmann, S. L. (2001) Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc. Natl. Acad. Sci. U.S.A. 98, 13566-13571
46. Jalanko, A., Vesa, J., Manninen, T., von Schantz, C., Minye, H., Fabritius, A. L., Salonen, T., Rapola, J., Gentile, M., Kopra, O. and Peltonen, L. (2005) Mice with Ppt1Deltaex4 mutation replicate the INCL phenotype and show an inflammation-associated loss of interneurons. Neurobiol. Dis. 18, 226-241
47. Sleat, D. E., Wiseman, J. A., El-Banna, M., Kim, K. H., Mao, Q., Price, S., Macauley, S. L., Sidman, R. L., Shen, M. M., Zhao, Q. et al. (2004) A mouse model of classical late-infantile neuronal ceroid lipofuscinosis based on targeted disruption of the CLN2 gene results in a loss of tripeptidyl-peptidase I activity and progressive neurodegeneration. J. Neurosoi. 24, 9117-9126 (Pubitemid 39372255)
48. Kopra, O., Vesa, J., von Schantz, C., Manninen, T., Minye, H., Fabritius, A. L., Rapola, J., van Diggelen, O. P., Saarela, J., Jalanko, A. and Peltonen, L. (2004) A mouse model for Finnish variant late infantile neuronal ceroid lipofuscinosis, CLN5, reveals neuropathology associated with early aging. Hum. Mol. Genet. 13, 2893-2906
49. Branson, R. T., Donahue, L. R., Johnson, K. R., Tanner, A., Lane, P. W. and Faust, J. R. (1998) Neuronal ceroid lipofuscinosis (nclf), a new disorder of the mouse linked to chromosome 9. Am. J. Med. Genet. 77, 289-297
50. Cooper, J. D., Messer, A., Feng, A. K., Chua-Couzens, J. and Mobley, W. C. (1999) Apparent loss and hypertrophy of interneurons in a mouse model of neuronal ceroid lipofuscinosis: evidence for partial response to insulin-like growth factor-1 treatment. J. Neurosci. 19, 2556-2567 (Pubitemid 29162404)
51. Mitchison, H. M., Bernard, D. J., Greene, N. D., Cooper, J. D., Junaid, M. A., Pullarkat, R. K., de Vos, N., Breuning, M. H., Owens, J. W., Mobley, W. C. et al. (1999) Targeted disruption of the Cln3 gene provides a mouse model for Batten disease. The Batten Mouse Model Consortium. Neurobiol Dis. 6, 321-334
52. Cotman, S. L., Vrbanac, V., Lebel, L. A., Lee, R. L., Johnson, K. A., Donahue, L. R., Teed, A. M., Antonellis, K., Branson, R. T., Lerner, T. J. and MacDonald, M. E. (2002) Cln3(Deltaex7/8) knock-in mice with the common JNCL mutation exhibit progressive neurologic disease that begins before birth. Hum. Mol. Genet. 11, 2709-2721
53. Katz, M. L., Shibuya, H., Liu, P. C., Kaur, S., Gao, C. L. and Johnson, G. S. (1999) A mouse gene knockout model for juvenile ceroid-lipofuscinosis (Batten disease). J. Neurosci. Res. 57, 551-556 (Pubitemid 29372930)
54. Wendt, K. D., Lei, B., Schachtman, T. R., Tullis, G. E., Ibe, M. E. and Katz, M. L. (2005) Behavioral assessment in mouse models of neuronal ceroid lipofuscinosis using a light-cued T-maze. Behav. Brain Res. 161, 175-182