Lithium rescues the impaired autophagy process in CbCln3 δex7/8/δex7/8 cerebellar cells and reduces neuronal vulnerability to cell death via IMPase inhibition

Journal of Neurochemistry

Volumn 116, Issue 4, 2011, Pages 659-668

  Chang, Jae Woong ^a   Choi, Hyunwoo ^a   Cotman, Susan L ^b   Jung, Yong Keun ^a  

^a Seoul National University   (South Korea)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

autophagy; Batten disease; IMPase; lithium

Indexed keywords

AMINO ACID; INOSITOL MONOPHOSPHATASE; LITHIUM; MEMBRANE PROTEIN; PHOSPHATASE; PROTEIN CLN3; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE SUBUNIT C; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN NERVE CELL; CELL VACUOLE; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; GENE TARGETING; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

5'-NUCLEOTIDASE; ANIMALS; AUTOPHAGY; CELL DEATH; CELLS, CULTURED; CEREBELLUM; ENZYME INHIBITORS; GENE KNOCK-IN TECHNIQUES; LITHIUM; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR CHAPERONES; NEURONS;

MUS;

EID: 79551626607     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07158.x     Document Type: Article

References (38)

1. Autti T., Raininko R, Vanhanen S. L., and, Santavuori P., (1996) MRI of neuronal ceroid lipofuscinosis. I. Cranial MRI of 30 patients with juvenile neuronal ceroid lipofuscinosis. Neuroradiology 38, 476-482.
2. Berridge M. J., Downes C. P., and, Hanley M. R., (1989) Neural and developmental actions of lithium: a unifying hypothesis. Cell 59, 411-419.
3. Busceti C. L., Biagioni F., Aronica E., Riozzi B., Storto M., Battaglia G., Giorgi F. S., Gradini R., Fornai F., and, Caricasole A., (2007) Induction of the Wnt inhibitor, Dickkopf-1, is associated with neurodegeneration related to temporal lobe epilepsy. Epilepsia 48, 694-705.
4. 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.
5. Cappuccio I., Calderone A., and, Busceti C. L., et al. (2005) Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is required for the development of ischemic neuronal death. J. Neurosci. 25, 2647-2657.
6. Chang J. W., Choi H., Kim H. J., Jo D. G., Jeon Y. J., Noh J. Y., Park W. J., and, Jung Y. K., (2007) Neuronal vulnerability of CLN3 deletion to calcium-induced cytotoxicity is mediated by calsenilin. Hum. Mol. Genet. 16, 317-326.
7. Chuang D. M., (2005) The antiapoptotic actions of mood stabilizers: molecular mechanisms and therapeutic potentials. Ann. N Y Acad. Sci. 1053, 195-204.
8. Cotman S. L., Vrbanac V., and, Lebel L. A., et al. (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.
9. Coyle J. T., and, Duman R. S., (2003) Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 24, 157-160.
10. Deranieh R.M., and, Greenberg M. L., (2009) Cellular consequences of inositol depletion. Biochem. Soc. Trans. 37, 1099-1103.
11. Fossale E., Wolf P., and, Espinola J. A., et al. (2004) Membrane trafficking and mitochondrial abnormalities precede subunit c deposition in a cerebellar cell model of juvenile neuronal ceroid lipofuscinosis. BMC Neurosci. 10, 57.
12. 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.
13. 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. 5, 735-744.
14. Heiseke A., Aguib Y., Riemer C., Baier M., and, Schätzl H. M., (2009) Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J. Neurochem. 109, 25-34.
15. HÃyer-Hansen M., Bastholm L., and, Szyniarowski P., et al. (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25, 193-205.
16. Jäger S., Bucci C., Tanida I., Ueno T., Kominami E., Saftig P., and, Eskelinen E. L., (2004) Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117, 4837-4848.
17. Jo D. G., Kim M. J., Choi Y. H., Kim I. K., Song Y. H., Woo H. N., Chung C. W., and, Jung Y. K., (2001) Pro-apoptotic function of calsenilin/DREAM/ KChIP3. FASEB J. 15, 589-591.
18. 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 23, 15458-15462.
19. Kimura S., Noda T., and, Yoshimori T., (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460.
20. Levine B., and, Yuan J., (2005) Autophagy in cell death: an innocent convict? J. Clin. Invest. 115, 2679-2688.
21. Manji H. K., and, Lenox R. H., (1998) Lithium: a molecular transducer of mood-stabilization in the treatment of bipolar disorder. Neuropsychopharmacology 19, 161-166.
22. Mizushima N., Ohsumi Y., and, Yoshimori T., (2002) Autophagosome formation in mammalian cells. Cell Struct. Funct. 27, 421-429.
23. Noh J. Y., Lee H., and, Song S., et al. (2009) SCAMP5 links endoplasmic reticulum stress to the accumulation of expanded polyglutamine protein aggregates via endocytosis inhibition. J. Biol. Chem. 284, 11318-11325.
24. Ohnishi T., Ohba H., Seo K. C., Im J., Sato Y., Iwayama Y., Furuichi T., Chung S. K., and, Yoshikawa T., (2007) Spatial expression patterns and biochemical properties distinguish a second myo-inositol monophosphatase IMPA2 from IMPA1. J. Biol. Chem. 282, 637-646.
25. Pearce D. A., Ferea T., Nosel S. A., Das B., and, Sherman F., (1999a) Action of BTN1, the yeast orthologue of the gene mutated in Batten disease. Nat. Genet. 22, 55-58.
26. Pearce D. A., Nosel S. A., and, Sherman F., (1999b) Studies of pH regulation by Btn1p, the yeast homolog of human Cln3p. Mol. Genet. Metab. 66, 320-323.
27. Persaud-Sawin D. A., and, Boustany R. M., (2005) Cell death pathways in juvenile Batten disease. Apoptosis 10, 973-985.
28. Phiel C. J., Wilson C. A., Lee V. M., and, Klein P. S., (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439.
29. Ramirez-Montealegre D., and, Pearce D. A., (2005) Defective lysosomal arginine transport in juvenile Batten disease. Hum. Mol. Genet. 14, 3759-3773.
30. Rubinsztein D. C., (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780-786.
31. Santavuori P., (1988) Neuronal ceroid-lipofuscinoses in childhood. Brain Dev. 10, 80-83.
32. Sarkar S., Floto R. A., Berger Z., Imarisio S., Cordenier A., Pasco M., Cook L. J., and, Rubinsztein D. C., (2005) Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 170, 1101-1111.
33. Sarkar S., Krishna G., Imarisio S., Saiki S., O'Kane CJ., and, Rubinsztein D. C., (2008) A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum. Mol. Genet. 17, 170-178.
34. Sourial-Bassillious N., Rydelius P. A., Aperia A., and, Aizman O., (2009) Glutamate-mediated calcium signaling: a potential target for lithium action. Neuroscience 161, 1126-1134.
35. Uusi-Rauva K., Luiro K., Tanhuanpää K., Kopra O., Martín-Vasallo P., Kyttälä A., and, Jalanko A., (2008) Novel interactions of CLN3 protein link Batten disease to dysregulation of fodrin-Na+, K+ ATPase complex. Exp. Cell Res. 314, 2895-2905.
36. Vicencio J. M., Ortiz C., Criollo A., et al. (2009) The inositol 1,4,5-trisphosphate receptor regulates autophagy through its interaction with Beclin 1. Cell Death Differ. 16, 1006-1017.
37. Weimer J. M., Benedict J. W., Getty A. L., Pontikis C. C., Lim M. J., Cooper J. D., and, Pearce D. A., (2009) Cerebellar defects in a mouse model of juvenile neuronal ceroid lipofuscinosis. Brain Res. 1266, 93-107.
38. Yogalingam G., and, Pendergast A. M., (2008) Abl kinases regulate autophagy by promoting the trafficking and function of lysosomal components. J. Biol. Chem. 283, 35941-35953.