S. pombe btn1, the orthologue of the Batten disease gene CLN3, is required for vacuole protein sorting of Cpy1p and Golgi exit of Vps10p

Journal of Cell Science

Volumn 122, Issue 8, 2009, Pages 1163-1173

  Codlin, Sandra ^a   Mole, Sara E ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Batten; Btn1; Carboxypeptidase Y; CLN3; Golgi; Neurodegeneration; Neuronal ceroid lipofuscinosis; S. pombe; Vacuole; vps10

Indexed keywords

BREFELDIN A; BTN1 PROTEIN; CARBOXYPEPTIDASE C; FUNGAL PROTEIN; MEMBRANE PROTEIN; PROTEIN CLN3; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VPS10 PROTEIN; BTN1 PROTEIN, S POMBE; CHAPERONE; CLN3 PROTEIN, HUMAN; CPY1 PROTEIN, S POMBE; PHOSPHATIDYLINOSITOL 3 KINASE; SCHIZOSACCHAROMYCES POMBE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL MIGRATION; CELL STRUCTURE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE REPRESSION; GOLGI COMPLEX; HUMAN; NERVE DEGENERATION; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TARGETING; SCHIZOSACCHAROMYCES POMBE; TRANS GOLGI NETWORK; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; TIME;

MAMMALIA; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CARBOXYPEPTIDASE C; GOLGI APPARATUS; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TIME FACTORS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 66849138215     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.038323     Document Type: Article

References (85)

1. Andersen, O. M., Reiche, J., Schmidt, V., Gotthardt, M., Spoelgen, R., Behlke, J., von Arnim, C. A., Breiderhoff, T., Jansen, P., Wu, X. et al. (2005). Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. USA 102, 13461-13466.
2. Ayscough, K., Hajibagheri, N. M. A., Watson, R. and Warren, G. (1993). Stacking of Golgi cisternae in Schizosaccharomyces pombe requires intact mictrotubules. J. Cell Sci. 106, 1227-1237.
3. Baldwin, S. A., Beal, P. R., Yao, S. Y., King, A. E., Cass, C. E. and Young, J. D. (2004). The equilibrative nucleoside transporter family, SLC29. Pflugers Arch. 447, 735-743.
4. Bellemare, D. R., Shaner, L., Morano, K. A., Beaudoin, J., Langlois, R. and Labbe, S. (2002). Ctr6, a vacuolar membrane copper transporter in Schizosaccharomyces pombe. J. Biol. Chem. 277, 46676-46686.
5. Brass, A. L., Dykxhoorn, D. M., Benita, Y., Yan, N., Engelman, A., Xavier, R. J., Lieberman, J. and Elledge, S. J. (2008). Identification of host proteins required for HIV infection through a functional genomic screen. Science 319, 921-926.
6. Brazer, S. C., Williams, H. P., Chappell, T. G. and Cande, W. Z. (2000). A fission yeast kinesin affects Golgi membrane recycling. Yeast 16, 149-166.
7. Burda, P., Padilla, S. M., Sarkar, S. and Emr, S. D. (2002). Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3-kinase. J. Cell Sci. 115, 3889-3900.
8. Cao, Y., Espinola, J. A., Fossale, E., Massey, A. C., Cuervo, A. M., Macdonald, M. E. and Cotman, S. L. (2006). Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 281, 20483-20493.
9. Cereghino, J. L., Marcusson, E. G. and Emr, S. D. (1995). The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization. Mol. Biol. Cell 6, 1089-1102.
10. Chappell, T. G. and Warren, G. (1989). A galactosyltransferase from the fission yeast Schizosaccharomyces pombe. J. Cell Biol. 109, 2693-2702.
11. Chattopadhyay, S., Muzaffar, N. E., Sherman, F. and Pearce, D. A. (2000). The yeast model for Batten disease: mutations in BTN1, BTN2, and HSP30 alter pH homeostasis. J. Bacteriol. 182, 6418-6423.
12. Codlin, S., Haines, R. L., Burden, J. J. E. and Mole, S. E. (2008a). btn1 affects cytokinesis and cell wall deposition by independent mechanisms, one of which is linked to vacuole pH dysregulation. J. Cell Sci. 121, 2860-2870.
13. Codlin, S., Haines, R. L. and Mole, S. E. (2008b). btn1 affects endocytosis, polarisation of sterol-rich membrane domains and polarised growth in Schizosaccharomyces pombe. Traffic 9, 936-950.
14. The International Batten Disease Consortium (1995). Isolation of a novel gene underlying Batten disease, CLN3. Cell 82, 949-957.
15. Cooper, A. A. and Stevens, T. H. (1996). Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J. Cell Biol. 133, 529-541.
16. 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.
17. Dahms, N. M., Lobel, P. and Kornfeld, S. (1989). Mannose 6-phosphate receptors and lysosomal enzyme targeting. J. Biol. Chem. 264, 12115-12118.
18. De Matteis, M. A. and Luini, A. (2008). Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9, 273-284.
19. Deloche, O., Yeung, B. G., Payne, G. S. and Schekman, R. (2001). Vps10p transport from the trans-Golgi network to the endosome is mediated by clathrin-coated vesicles. Mol. Biol. Cell 12, 475-485.
20. Donaldson, J. G., Honda, A. and Weigert, R. (2005). Multiple activities for Arf1 at the Golgi complex. Biochim. Biophys. Acta 1744, 364-373.
21. Ezaki, J., Takeda-Ezaki, M., Koike, M., Ohsawa, Y., Taka, H., Mineki, R., Murayama, K., Uchiyama, Y., Ueno, T. and Kominami, E. (2003). Characterization of Cln3p, the gene product responsible for juvenile neuronal ceroid lipofuscinosis, as a lysosomal integral membrane glycoprotein. J. Neurochem. 87, 1296-1308.
22. Finn, R. D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A., Durbin, R. et al. (2006). Pfam: clans, web tools and services. Nucl. Acids Res. 34, D247-D251.
23. Fossale, E., Wolf, P., Espinola, J. A., Lubicz-Nawrocka, T., Teed, A. M., Gao, H., Rigamonti, D., Cattaneo, E., MacDonald, M. E. and Cotman, S. L. (2004). Membrane trafficking and mitochondrial abnormalities precede subunit c deposition in a cerebellar cell model of juvenile neuronal ceroid lipofuscinosis. BMC Neurosci. 5, 57.
24. Futter, C. E., Collinson, L. M., Backer, J. M. and Hopkins, C. R. (2001). Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155, 1251-1264.
25. Gachet, Y., Codlin, S., Hyams, J. S. and Mole, S. E. (2005). btn1, the fission yeast homologue of the human Batten disease gene, CLN3, regulates vacuole homeostasis. J. Cell Sci. 118, 5525-5536.
26. Gaits, F. and Russell, P. (1999). Vacuole fusion regulated by protein phosphatase 2C in fission yeast. Mol. Biol. Cell 10, 2647-2654.
27. Golabek, A. A., Kida, E., Walus, M., Kaczmarski, W., Michalewski, M. and Wisniewski, K. E. (2000). CLN3 protein regulates lysosomal pH and alters intracellular processing of Alzheimer's amyloid-beta protein precursor and cathepsin D in human cells. Mol. Genet. Metab. 70, 203-213.
28. Hall, B. S., Gabernet-Castello, C., Voak, A., Goulding, D., Natesan, S. K. and Field, M. C. (2006). TbVps34, the trypanosome orthologue of Vps34, is required for Golgi complex segregation. J. Biol. Chem. 281, 27600-27612.
29. Haskell, R. E., Derksen, T. A. and Davidson, B. L. (1999). Intracellular trafficking of the JNCL protein CLN3. Mol. Genet. Metab. 66, 253-260.
30. Haskell, R. E., Carr, C. J., Pearce, D. A., Bennett, M. J. and Davidson, B. L. (2000). Batten disease: evaluation of CLN3 mutations on protein localization and function. Hum. Mol. Genet. 9, 735-744.
31. Hobert, J. A. and Dawson, G. (2007). A novel role of the Batten disease gene CLN3: association with BMP synthesis. Biochem. Biophys. Res. Commun. 358, 111-116.
32. Holopainen, J. M., Saarikoski, J., Kinnunen, P. K. and Järvelä, I. (2001). Elevated lysosomal pH in neuronal ceroid lipofuscinoses (NCLs). Eur. J. Biochem. 268, 5851-5856.
33. Iwaki, T., Osawa, F., Onishi, M., Koga, T., Fujita, Y., Hosomi, A., Tanaka, N., Fukui, Y. and Takegawa, K. (2003). Characterization of vps33+, a gene required for vacuolar biogenesis and protein sorting in Schizosaccharomyces pombe. Yeast 20, 845-855.
34. Iwaki, T., Goa, T., Tanaka, N. and Takegawa, K. (2004). Characterization of Schizosaccharomyces pombe mutants defective in vacuolar acidification and protein sorting. Mol. Genet. Genomics 271, 197-207.
35. Iwaki, T., Hosomi, A., Tokudomi, S., Kusunoki, Y., Fujita, Y., Giga-Hama, Y., Tanaka, N. and Takegawa, K. (2006). Vacuolar protein sorting receptor in Schizosaccharomyces pombe. Microbiology 152, 1523-1532.
36. Järvelä, I., Sainio, M., Rantamaki, T., Olkkonen, V. M., Carpén, O., Peltonen, L. and Jalanko, A. (1998). Biosynthesis and intracellular targeting of the CLN3 protein defective in Batten disease. Hum. Mol. Genet. 7, 85-90.
37. Järvelä, I., Lehtovirta, M., Tikkanen, R., Kyttälä, A. and Jalanko, A. (1999). Defective intracellular transport of CLN3 is the molecular basis of Batten disease (JNCL). Hum. Mol. Genet. 8, 1091-1098.
38. Junaid, M. A. and Pullarkat, R. K. (1999). Increased brain lysosomal pepstatin-insensitive proteinase activity in patients with neurodegenerative diseases. Neurosci. Lett. 264, 157-160.
39. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152, 519-530.
40. Kim, Y., Ramirez-Montealegre, D. and Pearce, D. A. (2003). A role in vacuolar arginine transport for yeast Btn1p and for human CLN3, the protein defective in Batten disease. Proc. Natl. Acad. Sci. USA 100, 15458-15462.
41. Kitaguchi, T., Wisniewski, K. E., Maslinski, S., Maslinska, D., Wisniewski, T. M. and Kim, K. S. (1990). Beta-protein immunoreactivity in brains of patients with neuronal ceroid lipofuscinosis: ultrastructural and biochemical demonstration. Neurosci. Lett. 112, 155-160.
42. Kitzmüller, C., Haines, R., Codlin, S., Cutler, D. F. and Mole, S. E. (2008). A function retained by the common mutant CLN3 protein is responsible for the late onset of juvenile neuronal ceroid lipofuscinosis (JNCL). Hum. Mol. Genet. 17, 303-312.
43. Kremmidiotis, G., Lensink, I. L., Bilton, R. L., Woollatt, E., Chataway, T. K., Sutherland, G. R. and Callen, D. F. (1999). The Batten disease gene product (CLN3p) is a Golgi integral membrane protein. Hum. Mol. Genet. 8, 523-531.
44. Kyttälä, A., Ihrke, G., Vesa, J., Schell, M. J. and Luzio, J. P. (2004). Two motifs target Batten disease protein CLN3 to lysosomes in transfected non-neuronal and neuronal cells. Mol. Biol. Cell 15, 1313-1323.
45. Lawe, D. C., Patki, V., Heller-Harrison, R., Lambright, D. and Corvera, S. (2000). The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J. Biol. Chem. 275, 3699-3705.
46. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
47. Lobley, A., Swindells, M. B., Orengo, C. A. and Jones, D. T. (2007). Inferring function using patterns of native disorder in proteins. PLoS Comp. Biol. 3, e162.
48. Luiro, K., Kopra, O., Lehtovirta, M. and Jalanko, A. (2001). CLN3 protein is targeted to neuronal synapses but excluded from synaptic vesicles: new clues to Batten disease. Hum. Mol. Genet. 10, 2123-2131.
49. Luiro, K., Yliannala, K., Ahtiainen, L., Maunu, H., Järvelä, I., Kyttala, A. and Jalanko, A. (2004). Interconnections of CLN3, Hook1 and Rab proteins link Batten disease to defects in the endocytic pathway. Hum. Mol. Genet. 13, 3017-3027.
50. Metcalf, D. J., Calvi, A. A., Seaman, M. N. J., Mitchison, H. M. and Cutler, D. F. (2008). Loss of the Batten disease gene CLN3 prevents exit from the TGN of the mannose 6-phosphate receptor. Traffic 9, 1905-1914.
51. McNiven, M. A. and Thompson, H. M. (2006). Vesicle formation at the plasma membrane and trans-Golgi network: the same but different. Science 313, 1591-1594.
52. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
53. Narayan, S. B., Rakheja, D., Tan, L., Pastor, J. V. and Bennett, M. J. (2006). CLN3P, the Batten's disease protein, is a novel palmitoyl-protein Delta-9 desaturase. Ann. Neurol. 60, 570-577.
54. Nugent, T., Mole, S. E. and Jones, D. (2008). The transmembrane topology of Batten disease protein CLN3 determined by consensus computational prediction constrained by experimental data. FEBS Lett. 582, 1019-1024.
55. Osorio, N. S., Carvalho, A., Almeida, A. J., Padilla-Lopez, S., Leao, C., Laranjinha, J., Ludovico, P., Pearce, D. A. and Rodrigues, F. (2007). Nitric oxide signaling is disrupted in the yeast model for Batten disease. Mol. Biol. Cell 18, 2755-2767.
56. Padilla-Lopez, S. and Pearce, D. A. (2006). Saccharomyces cerevisiae lacking Btn1p modulate vacuolar ATPase activity in order to regulate pH imbalance in the vacuole. J. Biol. Chem. 281, 10273-10280.
57. Patterson, G. H., Hirschberg, K., Polishchuk, R. S., Gerlich, D., Phair, R. D. and Lippincott-Schwartz, J. (2008). Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133, 1055-1067.
58. Pearce, D. A. and Sherman, F. (1998). A yeast model for the study of Batten disease. Proc. Natl. Acad. Sci. USA 95, 6915-6918.
59. Pearce, D. A., Ferea, T., Nosel, S. A., Das, B. and Sherman, F. (1999). Action of BTN1, the yeast orthologue of the gene mutated in Batten disease. Nat. Genet. 22, 55-58.
60. Persaud-Sawin, D. A., VanDongen, A. and Boustany, R. M. (2002). Motifs within the CLN3 protein: modulation of cell growth rates and apoptosis. Hum. Mol. Genet. 11, 2129-2142.
61. Persaud-Sawin, D. A., Mousallem, T., Wang, C., Zucker, A., Kominami, E. and Boustany, R. M. (2007). Neuronal ceroid lipofuscinosis: a common pathway? Pediatr. Res. 61, 146-152.
62. Pidoux, A. L. and Armstrong, J. (1993). The BiP protein and the endoplasmic reticulum of Schizosaccharomyces pombe: fate of the nuclear envelope during cell division. J. Cell Sci. 105, 1115-1120.
63. Pohl, S., Mitchison, H. M., Kohlschutter, A., Diggelen, O. V., Braulke, T. and Storch, S. (2007). Increased expression of lysosomal acid phosphatase in CLN3-defective cells and mouse brain tissue. J. Neurochem. 103, 2177-2188.
64. Ramirez-Montealegre, D. and Pearce, D. A. (2005). Defective lysosomal arginine transport in juvenile Batten disease. Hum. Mol. Genet. 14, 3759-3773.
65. Ridley, S. H., Ktistakis, N., Davidson, K., Anderson, K. E., Manifava, M., Ellson, C. D., Lipp, P., Bootman, M., Coadwell, J., Nazarian, A. et al. (2001). FENS-1 and DFCP1 are FYVE domain-containing proteins with distinct functions in the endosomal and Golgi compartments. J. Cell Sci. 114, 3991-4000.
66. Robinson, J. S., Klionsky, D. J., Banta, L. M. and Emr, S. D. (1988). Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 8, 4936-4948.
67. Rothman, J. H. and Stevens, T. H. (1986). Protein sorting in yeast: mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway. Cell 47, 1041-1051.
68. Schaub, B. E., Berger, B., Berger, E. G. and Rohrer, J. (2006). Transition of galactosyltransferase 1 from trans-Golgi cisterna to the trans-Golgi network is signal mediated. Mol. Biol. Cell 17, 5153-5162.
69. Siintola, E., Lehesjoki, A. E. and Mole, S. E. (2006). Molecular genetics of the NCLs-status and perspectives. Biochim. Biophys. Acta 1762, 857-864.
70. Siintola, E., Topcu, M., Aula, N., Lohi, H., Minassian, B. A., Paterson, A. M., Liu, X.-Q., Wilson, C., Lahtinen, U., Anottonen, A.-K. et al. (2007). The novel neuronal ceroid lipofusinosis gene MFSD8 encodes a putative lysosomal transporter. Am. J. Hum. Genet. 81, 136-146.
71. Sleat, D. E., Sohar, I., Pullarkat, P. S., Lobel, P. and Pullarkat, R. K. (1998). Specific alterations in levels of mannose 6-phosphorylated glycoproteins in different neuronal ceroid lipofuscinoses. Biochem. J. 334, 547-551.
72. Stack, J. H., DeWald, D. B., Takegawa, K. and Emr, S. D. (1995). Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 129, 321-334.
73. Storch, S., Pohl, S., Quitsch, A., Falley, K. and Braulke, T. (2007). C-terminal prenylation of the CLN3 membrane glycoprotein is required for efficient endosomal sorting to lysosomes. Traffic 8, 431-444.
74. Tabuchi, M., Iwaihara, O., Ohtani, Y., Ohuchi, N., Sakurai, J., Morita, T., Iwahara, S. and Takegawa, K. (1997). Vacuolar protein sorting in fission yeast: cloning, biosynthesis, transport, and processing of carboxypeptidase Y from Schizosaccharomyces pombe. J. Bacteriol. 179, 4179-4189.
75. Takegawa, K., DeWald, D. B. and Emr, S. D. (1995). Schizosaccharomyces pombe Vps34p, a phosphatidylinositol-specific PI 3-kinase essential for normal cell growth and vacuole morphology. J. Cell Sci. 108, 3745-3756.
76. Tanaka, N. and Takegawa, K. (2001). Functional characterization of Gms1p/UDP-galactose transporter in Schizosaccharomyces pombe. Yeast 18, 745-757.
77. Valls, L. A., Winther, J. R. and Stevens, T. H. (1990). Yeast carboxypeptidase Y vacuolar targeting signal is defined by four propeptide amino acids. J. Cell Biol. 111, 361-368.
78. Villanova, M., Ceuterick, C., Dotti, M. T., Santorelli, F. M., Casali, C., Malandrini, A., De Stefano, N., Lubke, U., Martin, J. J., Guazzi, G. C. et al. (1999). Detection of beta-A4 amyloid and its precursor protein in the muscle of a patient with juvenile neuronal ceroid lipofuscinosis (Spielmeyer-Vogt-Sjogren). Acta Neuropathol. 98, 78-84.
79. Vjestica, A., Tang, X. Z. and Oliferenko, S. (2008). The actomyosin ring recruits early secretory compartments to the division site in fission yeast. Mol. Biol. Cell 19, 1125-1138.
80. Whyte, J. R. and Munro, S. (2001). A yeast homolog of the mammalian mannose 6-phosphate receptors contributes to the sorting of vacuolar hydrolases. Curr. Biol. 11, 1074-1078.
81. Wisniewski, K. E., Maslinska, D., Kitaguchi, T., Kim, K. S., Goebel, H. H. and Haltia, M. (1990). Topographic heterogeneity of amyloid B-protein epitopes in brains with various forms of neuronal ceroid lipofuscinoses suggesting defective processing of amyloid precursor protein. Acta Neuropathol. 80, 26-34.
82. Wisniewski, K. E., Gordon-Majszak, W., Maslinski, S. and Heaney-Kieras, J. (1992). Altered protein patterns in brains of children with neuronal ceroid lipofuscinosis. Am. J. Med. Genet. 42, 568-574.
83. Wurmser, A. E. and Emr, S. D. (2002). Novel PtdIns(3)P-binding protein Etf1 functions as an effector of the Vps34 PtdIns 3-kinase in autophagy. J. Cell Biol. 158, 761-772.
84. Yan, Y. and Backer, J. M. (2007). Regulation of class III (Vps34) PI3Ks. Biochem. Soc. Trans. 35, 239-241.
85. Zeng, X., Overmeyer, J. H. and Maltese, W. A. (2006). Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J. Cell Sci. 119, 259-270.