Selective inhibition of caspases in skeletal muscle reverses the apoptotic synaptic degeneration in slow-channel myasthenic syndrome

Human Molecular Genetics

Volumn 23, Issue 1, 2014, Pages 69-77

  Zhu, Haipeng ^a   Pytel, Peter ^a   Gomez, Christopher M ^a  

^a UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CASPASE; CASPASE 3; CASPASE 7; CASPASE 9; CYCLIN DEPENDENT KINASE 5; INITIATOR CASPASE; PROTEINASE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONGENITAL MYASTHENIC SYNDROME; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; CALPAIN; CASPASE 3; CASPASE 7; CASPASE 9; CYCLIN-DEPENDENT KINASE 5; DISEASE MODELS, ANIMAL; DNA DAMAGE; EXTREMITIES; GENE EXPRESSION REGULATION; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MOTOR ENDPLATE; MUSCLE, SKELETAL; MYASTHENIC SYNDROMES, CONGENITAL;

EID: 84890380719     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt397     Document Type: Article

References (45)

1. Engel, A.G., Ohno, K., Milone, M. and Sine, S.M. (1998) Congenital myasthenic syndromes. New insights from molecular genetic and patch-clamp studies. Ann. N. Y. Acad. Sci., 841, 140-156.
2. Engel, A.G., Lambert, E.H., Mulder, D.M., Torres, C.F., Sahashi, K., Bertorini, T.E. and Whitaker, J.N. (1982) A newly recognized congenital myasthenic syndrome attributed to a prolonged open time of the acetylcholine-induced ion channel. Ann. Neurol., 11, 553-569.
3. Gomez, C.M., Maselli, R.A., Vohra, B.P., Navedo, M., Stiles, J.R., Charnet, P., Schott, K., Rojas, L., Keesey, J., Verity, A. et al. (2002) Novel delta subunit mutation in slow-channel syndrome causes severe weakness by novel mechanisms. Ann. Neurol., 51, 102-112.
4. Engel, A.G., Ohno, K., Milone, M., Wang, H.L., Nakano, S., Bouzat, C., Pruitt, J.N. 2nd, Hutchinson, D.O., Brengman, J.M., Bren, N. et al. (1996) New mutations in acetylcholine receptor subunit genes reveal heterogeneity in the slow-channel congenital myasthenic syndrome. Hum. Mol. Genet., 5, 1217-1227.
5. Gomez, C.M., Maselli, R., Gammack, J., Lasalde, J., Tamamizu, S., Cornblath, D.R., Lehar, M., McNamee, M. and Kuncl, R.W. (1996) A beta-subunit mutation in the acetylcholine receptor channel gate causes severe slow-channel syndrome. Ann. Neurol., 39, 712-723.
6. Vohra, B.P., Groshong, J.S., Maselli, R.A., Verity, M.A., Wollmann, R.L. and Gomez, C.M. (2004) Focal caspase activation underlies the endplate myopathy in slow-channel syndrome. Ann. Neurol., 55, 347-352.
7. Gomez, C.M., Maselli, R., Gundeck, J.E., Chao, M., Day, J.W., Tamamizu, S., Lasalde, J.A., McNamee, M. and Wollmann, R.L. (1997) Slow-channel transgenic mice: a model of postsynaptic organellar degeneration at the neuromuscular junction. J. Neurosci., 17, 4170-4179.
8. Gomez, C.M., Maselli, R.A., Groshong, J., Zayas, R.,Wollmann, R.L., Cens, T. and Charnet, P. (2002) Active calcium accumulation underlies severe weakness in a panel of mice with slow-channel syndrome. J. Neurosci., 22, 6447-6457.
9. Groshong, J.S., Spencer, M.J., Bhattacharyya, B.J., Kudryashova, E., Vohra, B.P., Zayas, R., Wollmann, R.L., Miller, R.J. and Gomez, C.M. (2007) Calpain activation impairs neuromuscular transmission in a mouse model of the slow-channel myasthenic syndrome. J. Clin. Invest., 117, 2903-2912.
10. Zhu, H., Bhattacharyya, B.J., Lin, H. and Gomez, C.M. (2011) Skeletal muscle IP3R1 receptors amplify physiological and pathological synaptic calcium signals. J. Neurosci., 31, 15269-15283.
11. Liu, X., Zou, H., Slaughter, C. and Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell, 89, 175-184.
12. D'Amelio, M., Cavallucci, V. and Cecconi, F. (2010) Neuronal caspase-3 signaling: not only cell death. Cell Death Differ., 17, 1104-1114.
13. McLaughlin, B. (2004)Thekinder side of killer proteases: caspase activation contributes to neuroprotection andCNSremodeling. Apoptosis, 9, 111-121.
14. Li, Z. and Sheng,M.(2012) Caspases in synaptic plasticity. Mol. Brain, 5, 15.
15. Colussi, P.A. and Kumar, S. (1999) Targeted disruption of caspase genes in mice: what they tell us about the functions of individual caspases in apoptosis. Immunol. Cell Biol., 77, 58-63.
16. Vandenabeele, P., Vanden Berghe, T. and Festjens, N. (2006) Caspase inhibitors promote alternative cell death pathways. Sci. STKE, 2006, pe44.
17. Hayashi, M., Saito, Y. and Kawashima, S. (1992) Calpain activation is essential for membrane fusion of erythrocytes in the presence of exogenous Ca2+. Biochem. Biophys. Res. Commun., 182, 939-946.
18. Kaczmarek, J.S., Riccio, A. and Clapham, D.E. (2012) Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc. Natl Acad. Sci.USA, 109, 7888-7892.
19. Smith, P.D., Mount, M.P., Shree, R., Callaghan, S., Slack, R.S., Anisman, H., Vincent, I., Wang, X., Mao, Z. and Park, D.S. (2006) Calpain-regulated p35/ cdk5 plays a central role in dopaminergic neuron death through modulation of the transcription factor myocyte enhancer factor 2. J. Neurosci., 26, 440- 447.
20. Takano, J., Tomioka, M., Tsubuki, S., Higuchi, M., Iwata, N., Itohara, S., Maki, M. and Saido, T.C. (2005) Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J. Biol. Chem., 280, 16175-16184.
21. Hung, K.S., Hwang, S.L., Liang, C.L., Chen, Y.J., Lee, T.H., Liu, J.K., Howng, S.L. and Wang, C.H. (2005) Calpain inhibitor inhibits p35-p25-Cdk5 activation, decreases tau hyperphosphorylation, and improves neurological function after spinal cord hemisection in rats. J. Neuropathol. Exp. Neurol., 64, 15-26.
22. Lee, M.S., Kwon, Y.T., Li, M., Peng, J., Friedlander, R.M. and Tsai, L.H. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature, 405, 360-364.
23. Vahidnia, A., van der Straaten, R.J., Romijn, F., van Pelt, J., van der Voet, G.B. and de Wolff, F.A. (2008) Mechanism of arsenic-induced neurotoxicity may be explained through cleavage of p35 to p25 by calpain. Toxicol. In Vitro, 22, 682-687.
24. Tian, B., Yang, Q. and Mao, Z. (2009) Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat. Cell. Biol., 11, 211-218.
25. Altieri, D.C. (2001) The molecular basis and potential role of survivin in cancer diagnosis and therapy. Trends Mol. Med., 7, 542-547.
26. Reed, J.C. (2001) The Survivin saga goes in vivo. J. Clin. Invest., 108, 965- 969.
27. Altieri, D.C. (2010) Survivin and IAP proteins in cell-death mechanisms. Biochem. J., 430, 199-205.
28. Chiou, S.K., Jones, M.K. and Tarnawski, A.S. (2003) Survivin - an anti-apoptosis protein: its biological roles and implications for cancer and beyond. Med. Sci. Monit., 9, PI25-PI29.
29. Johnson, M.E. and Howerth, E.W. (2004) Survivin: a bifunctional inhibitor of apoptosis protein. Vet. Pathol., 41, 599-607.
30. Patel, N., Chatterjee, S.K., Vrbanac, V., Chung, I., Mu, C.J., Olsen, R.R., Waghorne, C. and Zetter, B.R. (2010) Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc. Natl Acad. Sci. USA, 107, 2503-2508.
31. Koelle, G.B. and Friedenwald, J.A. (1949) A histochemical method for localizing cholinesterase activity. Proc. Soc. Exp. Biol. Med., 70, 617-622.
32. Kashiwa, H.K. and House, C.M. Jr. (1964) The glyoxal Bis(2-hydroxyanil) method modified for localizing insoluble calcium salts. Stain Technol., 39, 359-367.
33. Capalbo, G., Dittmann, K., Weiss, C., Reichert, S., Hausmann, E., Rodel, C. and Rodel, F. (2010) Radiation-induced survivin nuclear accumulation is linked to DNA damage repair. Int. J. Radiat. Oncol. Biol. Phys., 77, 226- 234.
34. Kanungo, J., Zheng, Y.L., Amin, N.D. and Pant, H.C. (2009) Targeting Cdk5 activity in neuronal degeneration and regeneration. Cell. Mol. Neurobiol., 29, 1073-1080.
35. Su, S.C. and Tsai, L.H. (2011) Cyclin-dependent kinases in brain development and disease. Annu. Rev. Cell Dev. Biol., 27, 465-491.
36. Zhu, H., Bhattacharyya, B.J., Lin, H. and Gomez, C.M. (2013) Skeletal muscle calpain acts through nitric oxide and neural miRNAs to regulate acetylcholine release in motor nerve terminals. J. Neurosci., 33, 7308-7324.
37. Uetsuki, T., Takemoto, K., Nishimura, I., Okamoto, M., Niinobe, M., Momoi, T., Miura, M. and Yoshikawa, K. (1999) Activation of neuronal caspase-3 by intracellular accumulation of wild-type Alzheimer amyloid precursor protein. J. Neurosci., 19, 6955-6964.
38. Srinivasan, A., Roth, K.A., Sayers, R.O., Shindler, K.S., Wong, A.M., Fritz, L.C. and Tomaselli, K.J. (1998) In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ., 5, 1004-1016.
39. Rideout,H.J. andStefanis,L. (2001)Caspase inhibition: a potential therapeutic strategy in neurological diseases. Histol. Histopathol., 16, 895-908.
40. Friedlander, R.M. (2003) Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med., 348, 1365-1375.
41. Schmitt, C.A. and Lowe, S.W. (2002) Apoptosis and chemoresistance in transgenic cancer models. J. Mol. Med., 80, 137-146.
42. Asada, A., Saito, T. and Hisanaga, S. (2012) Phosphorylation of p35 and p39 by Cdk5 determines the subcellular location of the holokinase in a phosphorylation-site-specific manner. J. Cell. Sci., 125, 3421-3429.
43. Mulder, K.J. and Mulder, J.B. (1979) Ketamine and xylazine anesthesia in the mouse. Vet. Med. Small Anim. Clin., 74, 569-570.
44. Lee, J.H., Jeong, M.W., Kim, W., Choi, Y.H. and Kim, K.T. (2008) Cooperative roles of c-Abl and Cdk5 in regulation of p53 in response to oxidative stress. J. Biol. Chem., 283, 19826-19835.
45. Schertzer, J.D. and Lynch, G.S. (2008) Plasmid-based gene transfer inmouse skeletal muscle by electroporation. Methods Mol. Biol., 433, 115-125.