Can ‘calpain-cathepsin hypothesis’ explain Alzheimer neuronal death?

Ageing Research Reviews

Volumn 32, Issue , 2016, Pages 169-179

  Yamashima, Tetsumori ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

Autophagy; Carbonylation; Hsp70.1; Hydroxynonenal; Lysosome; Neuronal death

Indexed keywords

CALPAIN; CATHEPSIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK COGNATE PROTEIN 70;

ALZHEIMER DISEASE; AUTOPHAGY; CELL DEATH; CELL VACUOLE; HOUSEKEEPING GENE; HUMAN; HYPOTHESIS; ISCHEMIA; NERVE CELL; NERVE DEGENERATION; PROTEIN CARBONYLATION; PROTEIN FUNCTION; REVIEW; AGING; ANIMAL; BRAIN ISCHEMIA; LYSOSOME; METABOLISM; PHYSIOLOGY;

AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN ISCHEMIA; CALPAIN; CATHEPSINS; CELL DEATH; HSC70 HEAT-SHOCK PROTEINS; HUMANS; LYSOSOMES; NERVE DEGENERATION;

EID: 84997610307     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2016.05.008     Document Type: Review

References (99)

1. Aits, S., Jäättelä, M., Lysosomal cell death at a glance. J. Cell Sci. 126 (2013), 1905–1912.
2. Ando, Y., Brännström, T., Uchida, K., Nyhlin, N., Näsman, B., Suhr, O., Yamashita, T., Olsson, T., El Salhy, M., Uchino, M., Ando, M., Histochemical detection of 4-hydroxynonenal protein in Alzheimer amyloid. J. Neurol. Sci. 156 (1998), 172–176.
3. Baixauli, F., López-Otín, C., Mittelbrunn, M., Exosomes and autophagy: coordinated mechanisms for the maintenance of cellular fitness. Front. Immunol., 2014, 10.3389/fimmu.2014.00403.
4. Bartus, R.T., Baker, K.L., Heiser, A.D., Sawyer, S.D., Dean, R.L., Elliott, P.J., Straub, J.A., Postischemic administration of AK275, a calpain inhibitor, provides substantial protection against focal ischemic brain damage. J. Cereb. Blood Flow Metab. 14 (1994), 537–544.
5. Bartus, R.T., Hayward, N.J., Elliott, P.J., Sawyer, S.D., Baker, K.L., Dean, R.L., Akiyama, A., Straub, J.A., Harbeson, S.L., Li, Z., Calpain inhibitor AK295 protects neurons from focal brain ischemia: effects of postocclusion intra-arterial administration. Stroke 25 (1994), 2265–2270.
6. Bartus, R.T., Dean, R.L., Mennerick, S., Eveleth, D., Lynch, G., Temporal ordering of pathogenic events following transient global ischemia. Brain Res. 790 (1998), 1–13.
7. Bevers, M.B., Neumar, R.W., Mechanistic role of calpains in postischemic neurodegeneration. J. Cereb. Blood Flow Metab. 28 (2008), 655–673.
8. Boiocchi, C., Maggioli, E., Monti, M.C., Zorzetto, M., Sinforiani, E., Cereda, C., Ricevuti, G., Cuccia, M., The possible involvement of HLA Class III haplotype (RAGE, HSP70 and TNF Genes) in Alzheimer's disease. Curr. Alzheimer Res 12 (2015), 997–1005.
9. Brunk, U.T., Ericsson, J.L., Cytochemical evidence for the leakage of acid phosphatase through ultrastructurally intact lysosomal membranes. Histochem. J. 4 (1972), 479–491.
10. Castegna, A., Aksenov, M., Thongboonkerd, V., Klein, J.B., Pierce, W.M., Booze, R., Markesbery, W.R., Butterfield, D.A., Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, α-enolase and heat shock cognate 71. J. Neurochem 82 (2002), 1524–1532.
11. Chong, Z.Z., Li, F., Maiese, K., Oxidative stress in the brain. Novel cellular targets that govern survival during neurodegenerative disease. Prog. Neurobiol. 75 (2005), 207–246.
12. Coffey, E.E., Beckel, J.M., Laties, A.M., Mitchell, C.H., Lysosomal alkalization and dysfunction in human fibroblasts with the Alzheimer's disease-linked presenilin 1 A246E mutation can be reversed with cAMP. Neuroscience 263 (2014), 111–124.
13. Cuerrier, D., Moldoveanu, T., Davies, P.L., Determination of peptide substrate specificity for μ-calpain by a peptide library-based approach: the importance of primed side interactions. J. Biol. Chem. 280 (2005), 40632–40641.
14. Cuervo, A.M., Dice, J., A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273 (1996), 501–503.
15. Cuervo, A.M., Chaperone-mediated autophagy: selectivity pays off. Trends Endocrinol. Metab. 21 (2010), 142–150.
16. de Duve, C., Lysosomes revisited. Eur. J. Biochem. 137 (1983), 391–397.
17. de Duve, C., de Barsy, T., Poole, B., Trouet, A., Tulkens, P., Van Hoof, F., Commentary. Lysosomotropic agents. Biochem. Pharmacol. 23 (1974), 2495–2531.
18. Dou, F., Netzer, W.J., Tanemura, K., Li, F., Hartl, F.U., Takashima, A., Gouras, G.K., Greengard, P., Xu, H., Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 721–726.
19. Fader, C.M., Colombo, M.I., Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 16 (2009), 70–78.
20. Firestone, R.A., Pisano, J.M., Bonney, R.J., Lysosomotropic agents. 1. Synthesis and cytotoxic action of lysosomotropic detergents. J. Med. Chem. 22 (1979), 1130–1133.
21. Gao, L., Tian, S., Gao, H., Xu, Y., Hypoxia increases Aβ-induced tau phosphorylation by calpain and promotes behavioral consequences in AD transgenic mice. J. Mol. Neurosci. 51 (2013), 138–147 2013.
22. Granato, M., Lacconi, V., Peddis, M., Lotti, L.V., Di Renzo, L., Gonnella, R., Santarelli, R., Trivedi, P., Frati, L., D'Orazi, G., Faggioni, A., Cirone, M., HSP70 inhibition by 2-phenylethynesulfonamide induces lysosomal cathepsin D release and immunogenic cell death in primary effusion lymphoma. Cell. Death. Dis., 4, 2013, e730, 10.1038/cddis.2013.263.
23. Guroff, G., A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239 (1964), 149–155.
24. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., Mizushima, N., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889.
25. Heinrich, M., Wickel, M., Winoto-Morbach, S., Schneider-Brachert, W., Weber, T., Brunner, J., Saftig, P., Peters, C., Krönke, M., Schütze, S., Ceramide as an activator lipid of cathepsin D. Adv. Exp. Med. Biol. 477 (2000), 305–315.
26. Hong, S.C., Lanzino, G., Goto, Y., Kang, S.K., Schottler, F., Kassell, N.F., Lee, K.S., Calcium-activated proteolysis in rat neocortex induced by transient focal ischemia. Brain Res. 661 (1994), 43–50.
27. Iqbal, K., Liu, F., Gong, C.X., Alonso, A.C., Grundke-Iqbal, I., Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 118 (2009), 53–69.
28. Katunuma, N., Kominami, E., Structures and functions of lysosomal thiol proteinases and their endogenous inhibitor. Curr. Top Cell Regul. 22 (1983), 71–101.
29. Kirkegaard, T., Jäättelä, M., Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta 1793 (2009), 746–754.
30. Kirkegaard, T., Roth, A.G., Petersen, N.H., Mahalka, A.K., Olsen, O.D., Moilanen, I., Zylicz, A., Knudsen, J., Sandhoff, K., Arenz, C., Kinnunen, P.K.J., Nylandsted, J., Jäättelä, M., Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463 (2010), 549–553.
31. Kolter, T., Sandhoff, K., Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell Dev. Biol. 21 (2005), 81–103.
32. Kolter, T., Sandhoff, K., Lysosomal degradation of membrane lipids. FEBS Lett. 584 (2010), 1700–1712.
33. Komatsu, M., Ueno, T., Waguri, S., Uchiyama, Y., Kominami, E., Tanaka, K., Constitutive autophagy: vital role in clearance of unfavorable proteins in neurons. Cell Death Differ. 14 (2007), 887–894.
34. Koriyama, Y., Sugitani, K., Ogai, K., Kato, S., Heat shock protein 70 induction by valproic acid delays photoreceptor cell death by N-methyl-N-nitrosourea in mice. J. Neurochem. 130 (2014), 707–719.
35. Lee, K.S., Frank, S., Vanderklish, P., Arai, A., Lynch, G., Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 7233–7237.
36. Leu, J.I., Pimkina, J., Frank, A., Murphy, M.E., George, D.L., A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell 36 (2009), 15–27.
37. Levine, B., Kroemer, G., Autophagy in the pathogenesis of disease. Cell 132 (2008), 27–42.
38. Li, P.A., Howlett, W., He, Q.P., Miyashita, H., Siddiqui, M., Shuaib, A., Postischemic treatment with calpain inhibitor MDL 28170 ameliorates brain damage in a gerbil model of global ischemia. Neurosci. Lett. 247 (1998), 17–20.
39. Linke, T., Wilkening, G., Lansmann, S., Moczall, H., Bartelsen, O., Weisgerber, J., Sandhoff, K., Stimulation of acid sphingomyelinase activity by lysosomal lipids and sphingolipid activator proteins. Biol. Chem. 382 (2001), 283–290.
40. Linke, T., Wilkening, G., Sadeghlar, F., Mozcall, H., Bernardo, K., Schuchman, E., Sandhoff, K., Interfacial regulation of acid ceramidase activity. Stimulation of ceramide degradation by lysosomal lipids and sphingolipid activator proteins. J. Biol. Chem. 276 (2001), 5760–5768.
41. Lovell, M.A., Ehmann, W.D., Mattson, M.P., Markesbery, W.R., Elevated 4-hydroxynonenal in ventricular fluid in Alzheimer's disease. Neurobiol. Aging 18 (1997), 457–461.
42. Lv, L., Sun, Y., Han, X., Xu, C.C., Tang, Y.P., Dong, Q., Valproic acid improves outcome after rodent spinal cord injury: potential roles of histone deacetylase inhibition. Brain Res. 1396 (2011), 60–68.
43. Marinova, Z., Ren, M., Wendland, J.R., Leng, Y., Liang, M.H., Yasuda, S., Leeds, P., Chuang, D.M., Valproic acid induces functional heat-shock protein 70 via Class I histone deacetylase inhibition in cortical neurons: a potential role of Sp1 acetylation. J. Neurochem. 111 (2009), 976–987.
44. Markesbery, W.R., Lovell, M.A., Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19 (1998), 33–36.
45. Markgraf, C.G., Velayo, N.L., Johnson, M.P., McCarty, D.R., Medhi, S., Koehl, J.R., Chmielewski, P.A., Linnik, M.D., Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 29 (1998), 152–158.
46. Martinez-Vicente, M., Talloczy, Z., Kaushik, S., Massey, A.C., Mazzulli, J., Mosharov, E.V., Hodara, R., Fredenburg, R., Wu, D.C., Follenzi, A., Dauer, W., Przedborski, S., Ischiropoulos, H., Lansbury, P.T., Sulzer, D., Cuervo, A.M., Dopamine-modified α-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest. 118 (2008), 777–788.
47. Massey, J.B., Interaction of ceramides with phosphatidylcholine, sphingomyelin and sphingomyelin/cholesterol bilayers. Biochim. Biophys. Acta 1510 (2001), 167–184.
48. McGrath, L.T., McGleenon, B.M., Brennan, S., McColl, D., McI. Lroy, S., Passmore, A.P., Increased oxidative stress in Alzheimer's disease as assessed with 4-hydroxynonenal but not malondialdehyde. QJM 94 (2001), 485–490.
49. Mjahed, H., Girodon, F., Fontenay, M., Garrido, C., Heat shock proteins in hematopoietic malignancies. Exp. Cell Res. 318 (2012), 1946–1958.
50. Neumar, R.W., Hagle, S.M., DeGracia, D.J., Krause, G.S., White, B.C., Brain μ-calpain autolysis during global cerebral ischemia. J. Neurochem. 66 (1996), 421–424.
51. Nikoletopoulou, V., Papandreou, M.E., Tavernarakis, N., Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ. 22 (2015), 398–407.
52. Nixon, R.A., Wegiel, J., Kumar, A., Yu, W.H., Peterhoff, C., Cataldo, A., Cuervo, A.M., Extensive involvement of autophagy in Alzheimer disease: an immunoelectron microscopy study. J. Neuropathol. Exp. Neurol. 64 (2005), 113–122.
53. Nixon, R.A., Autophagy, amyloidogenesis and Alzheimer disease. J. Cell Sci. 120 (2007), 4081–4091.
54. Nylandsted, J., Wick, W., Hirt, U.A., Brand, K., Rohde, M., Leist, M., Weller, M., Jäättelä, M., Eradication of glioblastoma, and breast and colon carcinoma xenografts by Hsp70 depletion. Cancer Res. 62 (2002), 7139–7142.
55. Oikawa, S., Yamada, T., Minohata, T., Kobayashi, H., Furukawa, A., Tada-Oikawa, S., Hiraku, Y., Murata, M., Kikuchi, M., Yamashima, T., Proteomic identification of carbonylated proteins in the monkey hippocampus after ischemia-reperfusion. Free Radic. Biol. Med. 46 (2009), 1472–1477.
56. Pan, T., Li, X., Xie, W., Jankovic, J., Le, W., Valproic acid-mediated Hsp70 induction and anti-apoptotic neuroprotection in SH-SY5Y cells. FEBS Lett. 579 (2005), 6716–6720.
57. Patterson, K.R., Remmers, C., Fu, Y., Brooker, S., Kanaan, N.M., Vana, L., Ward, S., Reyes, J.F., Philibert, K., Glucksman, M.J., Binder, L.I., Characterization of prefibrillar tau oligomers in vitro and in Alzheimers disease. J. Biol. Chem. 286 (2011), 23063–23076.
58. Patterson, K.R., Ward, S.M., Combs, B., Voss, K., Kanaan, N.M., Morfini, G., Brady, S.T., Gamblin, T.C., Binder, L.I., Heat shock protein 70 prevents both tau aggregation and the inhibitory effects of preexisting tau aggregates on fast axonal transport. Biochemistry 50 (2011), 10300–10310.
59. Periyasamy-Thandavan, S., Jiang, M., Schoenlein, P., Dong, Z., Autophagy: molecular machinery, regulation, and implications for renal pathophysiology. Am. J. Physiol. Renal Physiol. 297 (2009), F244–256.
60. Petersen, N.H., Kirkegaard, T., HSP70 and lysosomal storage disorders: novel therapeutic opportunities. Biochem. Soc. Trans. 38 (2010), 1479–1483.
61. Petersen, N.H., Kirkegaard, T., Olsen, O.D., Jäättelä, M., Connecting Hsp70, sphingolipid metabolism and lysosomal stability. Cell Cycle 9 (2010), 2305–2309.
62. Petrucelli, L., Dickson, D., Kehoe, K., Taylor, J., Snyder, H., Grover, A., De Lucia, M., McGowan, E., Lewis, J., Prihar, G., Kim, J., Dillmann, W.H., Browne, S.E., Hall, A., Voellmy, R., Tsuboi, Y., Dawson, T.M., Wolozin, B., Hardy, J., Hutton, M., CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum. Mol. Genet. 13 (2004), 703–714.
63. Pickford, F., Masliah, E., Britschgi, M., Lucin, K., Narasimhan, R., Jaeger, P.A., Small, S., Spencer, B., Rockenstein, E., Levine, B., Wyss-Coray, T., The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. J. Clin. Invest. 118 (2008), 2190–2199.
64. Rami, A., Krieglstein, J., Protective effects of calpain inhibitors against neuronal damage caused by cytotoxic hypoxia in vitro and ischemia in vivo. Brain Res. 609 (1993), 67–70.
65. Ren, M., Leng, Y., Jeong, M., Leeds, P.R., Chuang, D.M., Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: potential roles of histone deacetylase inhibition and heat shock protein induction. J. Neurochem. 89 (2004), 1358–1367.
66. Rerole, A.L., Jego, G., Garrido, C., Hsp70: anti-apoptotic and tumorigenic protein. Methods Mol. Biol. 787 (2011), 205–230.
67. Roberts-Lewis, J.M., Savage, M.J., Marcy, V.R., Pinsker, L.R., Siman, R., Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 14 (1994), 3934–3944.
68. Rubinsztein, D.C., DiFiglia, M., Heintz, N., Nixon, R.A., Qin, Z.H., Ravikumar, B., Stefanis, L., Tolkovsky, A., Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1 (2005), 11–22.
69. Sahara, S., Yamashima, T., Calpain-mediated Hsp70.1 cleavage in hippocampal CA1 neuronal death. Biochem. Biophys. Res. Commun. 393 (2010), 806–811.
70. Sahu, R., Kaushik, S., Clement, C.C., Cannizzo, E.S., Scharf, B., Follenzi, A., Potolicchio, I., Nieves, E., Cuervo, A.M., Santambrogio, L., Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20 (2011), 131–139.
71. Saido, T.C., Yokota, M., Nagao, S., Yamaura, I., Tani, E., Tsuchiya, T., Suzuki, K., Kawashima, S., Spatial resolution of fodrin proteolysis in postischemic brain. J. Biol. Chem. 268 (1993), 25239–25243.
72. Saito, K., Elce, J.S., Hamos, J.E., Nixon, R.A., Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 2628–2632.
73. Schulze, H., Kolter, T., Sandhoff, K., Principles of lysosomal membrane degradation: cellular topology and biochemistry of lysosomal lipid degradation. Biochim. Biophys. Acta 1793 (2009), 674–683.
74. Stadtman, E.R., Berlett, B.S., Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab. Rev. 30 (1998), 225–243.
75. Sultana, R., Perluigi, M., Newman, S.F., Pierce, W.M., Cini, C., Coccia, R., Butterfield, D.A., Redox proteomic analysis of carbonylated brain proteins in mild cognitive impairment and early Alzheimer's disease. Antioxid. Redox Signal. 12 (2010), 327–336.
76. Syntichaki, P., Xu, K., Driscoll, M., Tavernarakis, N., Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419 (2002), 939–944.
77. Taniguchi, S., Fujita, Y., Hayashi, S., Kakita, A., Takahashi, H., Murayama, S., Saido, T.C., Hisanaga, S., Iwatsubo, T., Hasegawa, M., Calpain-mediated degradation of p35 to p25 in postmortem human and rat brains. FEBS Lett. 489 (2001), 46–50.
78. Terman, A., Kurz, T., Gustafsson, B., Brunk, U.T., Lysosomal labilization. IUBMB Life 58 (2006), 531–539.
79. Tompa, P., Buzder-Lantos, P., Tantos, A., Farkas, A., Szilágyi, A., Bánóczi, Z., Hudecz, F., Friedrich, P., On the sequential determinants of calpain cleavage. J. Biol. Chem. 279 (2004), 20775–20785.
80. Wang, K.K., Calpain and caspase. Can you tell the difference?. Trends Neurosci. 23 (2000), 20–26.
81. Wen, Y., Yang, S.-H., Liu, R., Perez, E.J., Brun-Zinkernagel, A.M., Koulen, P., James, W., Simpkins, J.W., Cdk5 is involved in NFT-like tauopathy induced by transient cerebral ischemia in female rats. Biochim. Biophys. Acta 1772 (2007), 473–483.
82. Williams, T.I., Lynn, B.C., Markesbery, W.R., Mark, A., Love, M.A., Increased levels of 4-hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in Mild Cognitive Impairment and early Alzheimer's disease. Neurobiol. Ageing 27 (2006), 1094–1099.
83. Wolfe, D.M., Lee, J.H., Kumar, A., Lee, S., Orenstein, S.J., Nixon, R.A., Autophagy failure in Alzheimer's disease and the role of defective lysosomal acidification. Eur. J. Neurosci. 37 (2013), 1949–1961.
84. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C., London, E., Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 276 (2001), 33540–33546.
85. Xuan, A., Long, D., Li, J., Ji, W., Hong, L., Zhang, M., Zhang, W., Neuroprotective effects of valproic acid following transient global ischemia in rats. Life Sci. 90 (2012), 463–468.
86. Yamada, K.H., Kozlowski, D.A., Seidl, S.E., Lance, S., Wieschhaus, A.J., Sundivakkam, P., Tiruppathi, C., Chishti, I., Herman, I.M., Kuchay, S.M., Chisht, A.H., Targeted gene inactivation of calpain-1 suppresses cortical degeneration due to traumatic brain injury and neuronal apoptosis induced by oxidative stress. J. Biol. Chem. 287 (2012), 13182–13193.
87. Yamashima, T., Oikawa, S., The role of lysosomal rupture in neuronal death. Prog. Neurobiol. 89 (2009), 343–358.
88. 2 and calpain responses prior to delayed neuronal death in monkeys. Eur. J. Neurosci. 8 (1996), 1932–1944.
89. Yamashima, T., Kohda, Y., Tsuchiya, K., Ueno, T., Yamashita, J., Yoshioka, T., Komi-nami, E., Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on ‘calpain–cathepsin hypothesis’. Eur. J. Neurosci. 10 (1998), 1723–1733.
90. Yamashima, T., Tonchev, A.B., Tsukada, T., Saido, T.C., Imajoh-Ohmi, S., Momoi, T., Kominami, E., Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 13 (2003), 791–800.
91. Yamashima, T., Mathivanan, A., Dazortsava, M.Y., Sakai, S., Kurimoto, S., Zhu, H., Funaki, N., Liang, H., Hullin-Matsuda, F., Kobayashi, T., Akatsu, H., Takahashi, H., Minabe, Y., Calpain-mediated Hsp70.1 cleavage in monkey CA1 after ischemia induces similar ‘lysosomal vesiculosis’ to Alzheimer neurons. J. Alzheimers Dis. Parkinsonism, 4(2), 2014, 10.4172/2161-0460.1000139.
92. Yamashima, T., Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol. 62 (2000), 273–295.
93. 2+-dependent proteases in ischemic neuronal death: a conserved ‘calpain–cathepsin cascade’ from nematodes to primates. Cell Calcium 36 (2004), 285–293.
94. Yamashima, T., Hsp70.1 and related lysosomal factors for necrotic neuronal death. J. Neurochem. 120 (2012), 477–494.
95. Yamashima, T., Reconsider Alzheimer's disease by the ‘calpain-cathepsin hypothesis’ - a perspective review. Prog. Neurobiol. 105 (2013), 1–23.
96. Yang, D.S., Stavrides, P., Mohan, P.S., Kaushik, S., Kumar, A., Ohno, M., Schmidt, S.D., Wesson, D.W., Bandyopadhyay, U., Jiang, Y., Pawlik, M., Peterhoff, C.M., Yang, A.J., Wilson, D.A., St. George-Hyslop, P., Westaway, D., Mathews, P.M., Levy, E., Cuervo, A.M., Nixon, R.A., Therapeutic effects of remediating autophagy failure in a mouse model of Alzheimer disease by enhancing lysosomal proteolysis. Autophagy 7 (2011), 788–789.
97. Yokota, M., Tani, E., Tsubuki, S., Yamaura, I., Nakagaki, I., Hori, S., Saido, T.C., Calpain inhibitor entrapped in liposome rescues ischemic neuronal damage. Brain Res. 819 (1999), 8–14.
98. Yoshimori, T., Autophagy: paying Charon's toll. Cell 128 (2007), 833–836.
99. Zhu, H., Yoshimoto, T., Yamashima, T., Heat Shock protein 70.1 (Hsp70.1) affects neuronal cell fate by regulating lysosomal acid sphingomyelinase. J. Biol. Chem. 289 (2014), 27432–27443.