Cathepsin D deficiency induces persistent neurodegeneration in the absence of bax-dependent apoptosis

Journal of Neuroscience

Volumn 27, Issue 8, 2007, Pages 2081-2090

  Shacka, John J ^a   Klocke, Barbara J ^a   Young, Chainllie ^b   Shibata, Masahiro ^c   Olney, John W ^b   Uchiyama, Yasuo ^c   Saftig, Paul ^d   Roth, Kevin A ^a  

^a University of Alabama at Birmingham   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

Apoptosis; Autophagic stress; Autophagy; Bax; Cathepsin D; Neurodegeneration

Indexed keywords

CASPASE 3; CATHEPSIN D; CELL NUCLEUS ANTIGEN; LIPOFUSCIN; MARKER; PROTEIN BAX; SILVER;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOFLUORESCENCE; AUTOPHAGY; BRAIN; CELL DEATH; CELL FUNCTION; CELL LOSS; CELL STRESS; CELL SWELLING; CYTOPLASM; ENZYME ACTIVATION; ENZYME DEFICIENCY; GENE DISRUPTION; HIPPOCAMPUS; LYSOSOME; MORPHOLOGY; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPATHOLOGY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PYKNOTIC NEURON; STATISTICAL SIGNIFICANCE;

ANIMALS; APOPTOSIS; AUTOPHAGY; BCL-2-ASSOCIATED X PROTEIN; BRAIN; CASPASE 3; CATHEPSIN D; CELL DEATH; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HIPPOCAMPUS; IN SITU NICK-END LABELING; LIPOFUSCIN; LYSOSOMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONAL CEROID-LIPOFUSCINOSES; NEURONS; NUCLEAR PROTEINS;

EID: 33847215777     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5577-06.2007     Document Type: Article

References (49)

1. Anglade P, Vyas S, Javoy-Agid F, Herrero MT, Michel PP, Marquez J, Mouatt-Prigent A, Ruberg M, Hirsch EC, Agid Y (1997) Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histopathol 12:25-31.
2. Awano T, Katz ML, O'Brien DP, Taylor JF, Evans J, Khan S, Sohar I, Lobel P, Johnson GS (2006) A mutation in the cathepsin D gene (CTSD) in American Bulldogs with neuronal ceroid lipofuscinosis. Mol Genet Metab 87:341-348.
3. Bahr BA, Bendiske J (2002) The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 83:481-489.
4. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620-1624.
5. Boya P, Gonzalez-Polo RA, Poncet D, Andreau K, Vieira HL, Roumier T, Perfettini JL, Kroemer G (2003) Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene 22:3927-3936.
6. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25:1025-1040.
7. Chu CT (2006) Autophagic stress in neuronal injury and disease. J Neuropathol Exp Neurol 65:423-432.
8. Deckwerth TL, Elliott JL, Knudson CM, Johnson Jr EM, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
9. DeOlmos JS, Ingram WR (1971) An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res 33:523-529.
10. Fernandes-Alnemri T, Armstrong RC, Krebs J, Srinivasula SM, Wang L, Bullrich F, Fritz LC, Trapani JA, Tomaselli KJ, Litwack G, Alnemri ES (1996) In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc Natl Acad Sci USA 93:7464-7469.
11. Ghatan S, Larner S, Kinoshita Y, Hetman M, Patel L, Xia Z, Youle RJ, Morrison RS (2000) p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol 150:335-347.
12. Goebel HH, Wisniewski KE (2004) Current state of clinical and morphological features in human NCL. Brain Pathol 14:61-69.
13. Haltia M (2003) The neuronal ceroid-lipofuscinoses. J Neuropathol Exp Neurol 62:1-13.
14. Ischiropoulos H, Beckman JS (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 111:163-169.
15. Jellinger KA, Stadelmann CH (2000) The enigma of cell death in neurodegenerative disorders. J Neural Transm Suppl l21-36.
16. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95:4997-5002.
17. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728.
18. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
19. Koike M, Nakanishi H, Saftig P, Ezaki J, Isahara K, Ohsawa Y, Schulz-Schaeffer W, Watanabe T, Waguri S, Kametaka S, Shibata M, Yamamoto K, Kominami E, Peters C, von Figura K, Uchiyama Y (2000) Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J Neurosci 20:6898-6906.
20. Koike M, Shibata M, Ohsawa Y, Nakanishi H, Koga T, Kametaka S, Waguri S, Momoi T, Kominami E, Peters C, Figura K, Saftig P, Uchiyama Y (2003) Involvement of two different cell death pathways in retinal atrophy of cathepsin D-deficient mice. Mol Cell Neurosci 22:146-161.
21. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, Kominami E, Gotow T, Peters C, von Figura K, Mizushima N, Saftig P, Uchiyama Y (2005) Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease). Am J Pathol 167:1713-1728.
22. Lu Z, Dono K, Gotoh K, Shibata M, Koike M, Marubashi S, Miyamoto A, Takeda Y, Nagano H, Umeshita K, Uchiyama Y, Monden M (2005) Participation of autophagy in the degeneration process of rat hepatocytes after transplantation following prolonged cold preservation. Arch Histol Cytol 68:71-80.
23. Nakanishi H, Zhang J, Koike M, Nishioku T, Okamoto Y, Kominami E, von Figura K, Peters C, Yamamoto K, Saftig P, Uchiyama Y (2001) Involvement of nitric oxide released from microglia-macrophages in pathological changes of cathepsin D-deficient mice. J Neurosci 21:7526-7533.
24. Nixon RA, Cataldo AM (1995) The endosomal-lysosomal system of neurons: new roles. Trends Neurosci 18:489-496.
25. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64:113-122.
26. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939.
27. Pervin S, Singh R, Chaudhuri G (2003) Nitric-oxide-induced Bax integration into the mitochondrial membrane commits MDA-MB-468 cells to apoptosis: essential role of Akt. Cancer Res 63:5470-5479.
28. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36:585-595.
29. Reid WA, Valler MJ, Kay J (1986) Immunolocalization of cathepsin D in normal and neoplastic human tissues. J Clin Pathol 39:1323-1330.
30. Roth KA (2001) Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion. J Neuropathol Exp Neurol 60:829-838.
31. Saftig P, Hetman M, Schmahl W, Weber K, Heine L, Mossmann H, Koster A, Hess B, Evers M, von Figura K, (1995) Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J 14:3599-3608.
32. Shacka JJ, Roth KA (2005) Cathepsin deficiency as a model for neuronal ceroid lipofuscinoses. Am J Pathol 167:1473-1476.
33. Shacka JJ, Roth KA (2006) Bcl-2 family and the central nervous system: from rheostat to real complex. Cell Death Differ 13:1299-1304.
34. Shacka JJ, Klocke BJ, Shibata M, Uchiyama Y, Datta G, Schmidt RE, Roth KA (2006a) Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons. Mol Pharmacol 69:1125-1136.
35. Shacka JJ, Sahawneh MA, Gonzalez JD, Ye YZ, D'alessandro TL, Estevez AG (2006b) Two distinct signaling pathways regulate peroxynitrite-induced apoptosis in PC12 cells. Cell Death Differ 13:1506-1514.
36. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Tsujimoto Y (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6:1221-1228.
37. Shindler KS, Latham CB, Roth KA (1997) Bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J Neurosci 17:3112-3119.
38. Shindler KS, Yunker AM, Cahn R, Zha J, Korsmeyer SJ, Roth KA (1998) Trophic support promotes survival of bcl-x-deficient telencephalic cells in vitro. Cell Death Differ 5:901-910.
39. Siintola E, Partanen S, Stromme P, Haapanen A, Haltia M, Maehlen J, Lehesjoki AE, Tyynela J (2006) Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis. Brain 129:1438-1445.
40. Steinfeld R, Reinhardt K, Schreiber K, Hillebrand M, Kraetzner R, Bruck W, Saftig P, Gartner J (2006) Cathepsin D deficiency is associated with a human neurodegenerative disorder. Am J Hum Genet 78:988-998.
41. Tamatani M, Ogawa S, Nunez G, Tohyama M (1998) Growth factors prevent changes in Bcl-2 and Bax expression and neuronal apoptosis induced by nitric oxide. Cell Death Differ 5:911-919.
42. Tornusciolo DR, Schmidt RE, Roth KA (1995) Simultaneous detection of TDT-mediated dUTP-biotin nick end-labeling (TUNEL)-positive cells and multiple immunohistochemical markers in single tissue sections. Biotechniques 19:800-805.
43. Tyynela J, Sohar I, Sleat DE, Gin RM, Donnelly RJ, Baumann M, Haltia M, Lobel P (2000) A mutation in the ovine cathepsin D gene causes a congenital lysosomal storage disease with profound neurodegeneration. EMBO J 19:2786-2792.
44. van Lookeren CM, Lucassen PJ, Vermeulen JP, Balazs R (1995) NMDA and kainate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. Eur J Neurosci 7:1627-1640.
45. Walls KC, Klocke BJ, Saftig P, Shibata M, Uchiyama Y, Roth KA, Shacka JJ (2007) Altered regulation of phosphatidylinositol 3-kinase signaling in cathepsin D-deficient brain. Autophagy, in press.
46. Whitaker JN, Rhodes RH (1983) The distribution of cathepsin D in rat tissues determined by immunocytochemistry. Am J Anat 166:417-428.
47. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18:1428-1439.
48. Zaidi AU, McDonough JS, Klocke BJ, Latham CB, Korsmeyer SJ, Flavell RA, Schmidt RE, Roth KA (2001) Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J Neuropathol Exp Neurol 60:937-945.
49. Zhu JH, Guo F, Shelburne J, Watkins S, Chu CT (2003) Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases. Brain Pathol 13:473-481.