Calpain-cleaved type 1 inositol 1,4,5-trisphosphate receptor impairs ER Ca2+ buffering and causes neurodegeneration in primary cortical neurons

Journal of Neurochemistry

Volumn 123, Issue 1, 2012, Pages 147-158

  Kopil, Catherine M ^a   Siebert, Adam P ^a   Kevin Foskett, J ^a   Neumar, Robert W ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

calcium; calpain; endoplasmic reticulum; excitotoxicity; inositol 1,4,5 trisphosphate receptor; neuron

Indexed keywords

CALPAIN; GLUTAMIC ACID; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; EXCITOTOXICITY; GENE MUTATION; INVERTED TERMINAL REPEAT; NERVE CELL DEGENERATION; NONHUMAN; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; SITE DIRECTED MUTAGENESIS; STIMULUS RESPONSE; TRANSGENE;

ANALYSIS OF VARIANCE; ANIMALS; CALCIUM; CALCIUM SIGNALING; CELL LINE, TRANSFORMED; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; METHOXYHYDROXYPHENYLGLYCOL; MICROTUBULE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; NERVE DEGENERATION; NEURONS; POINT MUTATION; PREGNANCY; RATS; THAPSIGARGIN; TRANSFECTION;

ADENO-ASSOCIATED VIRUS; RATTUS;

EID: 84866235786     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07859.x     Document Type: Article

References (43)

1. 2+ in triggering inositol 1,4,5-trisphosphate receptor ubiquitination. Biochem. J. 392, 601-606. (Pubitemid 43022740)
2. Assefa Z., Bultynck G., Szlufcik K., Nadif Kasri N., Vermassen E., Goris J., Missiaen L., Callewaert G., Parys J. B., and, De Smedt H., (2004) Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J. Biol. Chem. 279, 43227-43236. (Pubitemid 39372218)
3. 2+ store in the plasticity of central neurons. Trends Pharmacol. Sci. 27, 78-84. (Pubitemid 43184028)
4. Berridge M. J., Lipp P., and, Bootman M. D, (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21.
5. Berridge M. J., Bootman M. D., and, Roderick H. L., (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529. (Pubitemid 36773404)
6. Bevers M. B., Lawrence E., Maronski M., Starr N., Amesquita M., and, Neumar R. W, (2009) Knockdown of m-calpain increases survival of primary hippocampal neurons following NMDA excitotoxicity. J. Neurochem. 108, 1237-1250.
7. Bhanumathy C. D., Nakao S. K., and, Joseph S. K., (2006) Mechanism of proteasomal degradation of inositol trisphosphate receptors in CHO-K1 cells. J. Biol. Chem. 281, 3722-3730. (Pubitemid 43845990)
8. Boehning D., and, Joseph S. K, (2000) Functional properties of recombinant type I and type III inositol 1, 4,5-trisphosphate receptor isoforms expressed in COS-7 cells. J. Biol. Chem. 275, 21492-21499. (Pubitemid 30481853)
9. 2+ channels. J. Biol. Chem. 276, 13509-13512.
10. 2+ transfer to mitochondria. Cell 142, 270-283.
11. 2+ disruption in Alzheimer's disease by presenilin regulation of InsP3 receptor channel gating. Neuron 58, 871-883. (Pubitemid 351842747)
12. Conn P. J., and, Pin J. P, (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237. (Pubitemid 27238875)
13. Cummings D. D., Wilcox K. S., and, Dichter M. A, (1996) Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapses in culture. J. Neurosci. 16, 5312-5323. (Pubitemid 26277860)
14. Dong J. Y., Fan P. D., and, Frizzell R. A, (1996) Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7, 2101-2112. (Pubitemid 26400735)
15. 2+ stores and ion channels in neurons. Trends Neurosci. 23, 80-88. (Pubitemid 30084765)
16. Fisher K. J., Jooss K., Alston J., Yang Y., Haecker S. E., High K., Pathak R., Raper S. E., and, Wilson J. M, (1997) Recombinant adeno-associated virus for muscle directed gene therapy. Nat. Med. 3, 306-312. (Pubitemid 27112928)
17. 2+ release channels in neurological diseases. Pflugers Arch. 460, 481-494.
18. 2+ release channels. Physiol. Rev. 87, 593-658. (Pubitemid 47084681)
19. Gao L., Balshaw D., Xu L., Tripathy A., Xin C., and, Meissner G., (2000) Evidence for a role of the lumenal M3-M4 loop in skeletal muscle Ca(2+) release channel (ryanodine receptor) activity and conductance. Biophys. J. 79, 828-840. (Pubitemid 30626177)
20. Goll D. E., Thompson V. F., Li H., Wei W., and, Cong J., (2003) The calpain system. Physiol. Rev. 83, 731-801. (Pubitemid 36828925)
21. Hirota J., Furuichi T., and, Mikoshiba K., (1999) Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J. Biol. Chem. 274, 34433-34437. (Pubitemid 129511789)
22. Ikegaya Y., Le Bon-Jego M., and, Yuste R, (2005) Large-scale imaging of cortical network activity with calcium indicators. Neurosci. Res. 52, 132-138. (Pubitemid 40704595)
23. Joseph S. K., and, Samanta S., (1993) Detergent solubility of the inositol trisphosphate receptor in rat brain membranes. Evidence for association of the receptor with ankyrin. J. Biol. Chem. 268, 6477-6486. (Pubitemid 23099346)
24. Kopil C. M., Vais H., Cheung K. H., Siebert A. P., Mak D. O., Foskett J. K., and, Neumar R. W, (2011) Calpain-cleaved type 1 inositol 1,4,5-trisphosphate receptor (InsP(3)R1) has InsP(3)-independent gating and disrupts intracellular Ca(2+) homeostasis. J. Biol. Chem. 286, 35998-36010.
25. Maeda E., Robinson H. P., and, Kawana A., (1995) The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. J. Neurosci. 15, 6834-6845.
26. Mak D. O., McBride S. M., and, Foskett J. K, (2003) Spontaneous channel activity of the inositol 1,4,5-trisphosphate (InsP3) receptor (InsP3R). Application of allosteric modeling to calcium and InsP3 regulation of InsP3R single-channel gating. J. Gen. Physiol. 122, 583-603. (Pubitemid 37420852)
27. 2+ release channels. EMBO Rep. 8, 1044-1051. (Pubitemid 350042340)
28. Mattson M. P, (2007) Calcium and neurodegeneration. Aging Cell 6, 337-350.
29. Mattson M. P., LaFerla F. M., Chan S. L., Leissring M. A., Shepel P. N., and, Geiger J. D., (2000) Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23, 222-229. (Pubitemid 30236182)
30. Michaelis E. K, (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54, 369-415. (Pubitemid 28085741)
31. Murphy T. H., Blatter L. A., Wier W. G., and, Baraban J. M., (1992) Spontaneous synchronous synaptic calcium transients in cultured cortical neurons. J. Neurosci. 12, 4834-4845.
32. Nakayama T., Hattori M., Uchida K., Nakamura T., Tateishi Y., Bannai H., Iwai M., Michikawa T., Inoue T., and, Mikoshiba K., (2004) The regulatory domain of the inositol 1,4,5-trisphosphate receptor is necessary to keep the channel domain closed: possible physiological significance of specific cleavage by caspase 3. Biochem. J. 377, 299-307. (Pubitemid 38142185)
33. O'Donnell L. A., Agrawal A., Jordan-Sciutto K. L., Dichter M. A, Lynch D. R., and, Kolson D. L, (2006) Human immunodeficiency virus (HIV)-induced neurotoxicity: roles for the NMDA receptor subtypes. J. Neurosci. 26, 981-990.
34. Orrenius S., Zhivotovsky B., and, Nicotera P., (2003) Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4, 552-565. (Pubitemid 36773407)
35. Royo N. C., Vandenberghe L. H., Ma J. Y., Hauspurg A., Yu L., Maronski M., Johnston J., Dichter M. A., Wilson J. M., and, Watson D. J., (2008) Specific AAV serotypes stably transduce primary hippocampal and cortical cultures with high efficiency and low toxicity. Brain Res. 1190, 15-22.
36. 2+ release channels in rat brain. J. Neurosci. 13, 3051-3063. (Pubitemid 23199230)
37. Sliter D. A., Kubota K., Kirkpatrick D. S., Alzayady K. J, Gygi S. P., and, Wojcikiewicz R. J., (2008) Mass spectrometric analysis of type 1 inositol 1,4,5-trisphosphate receptor ubiquitination. J. Biol. Chem. 283, 35319-35328.
38. Stutzmann G. E., and, Mattson M. P., (2011) Endoplasmic reticulum Ca(2+) handling in excitable cells in health and disease. Pharmacol. Rev. 63, 700-727.
39. Taylor R. C., Cullen S. P., and, Martin S. J., (2008) Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9, 231-241. (Pubitemid 351301823)
40. 2+ signalling. Biol. Cell 100, 39-49. (Pubitemid 351201432)
41. Verkhratsky A., and, Toescu E. C., (2003) Endoplasmic reticulum Ca(2+) homeostasis and neuronal death. J. Cell Mol. Med. 7, 351-361. (Pubitemid 44151686)
42. Wang Y., Xu L., Pasek D. A., Gillespie D., and, Meissner G., (2005) Probing the role of negatively charged amino acid residues in ion permeation of skeletal muscle ryanodine receptor. Biophys. J. 89, 256-265. (Pubitemid 41098280)
43. White C., Li C., Yang J., Petrenko N. B., Madesh M., Thompson C. B., and, Foskett J. K., (2005) The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat. Cell Biol. 7, 1021-1028. (Pubitemid 41486277)