Impairment of mitochondrial calcium handling in a mtSOD1 cell culture model of motoneuron disease

BMC Neuroscience

Volumn 10, Issue , 2009, Pages

  Jaiswal, Manoj ^a   Zech, Wolf Dieter ^a   Goos, Miriam ^a   Leutbecher, Christine ^a   Ferri, Alberto ^b   Zippelius, Annette ^a   Carrì, Maria Teresa ^b,c   Nau, Roland ^a,d   Keller, Bernhard U ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d Department of Geriatrics Evangelisches Krakenhaus ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CALCIUM ION; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; COPPER ZINC SUPEROXIDE DISMUTASE; GUANINE; CALCIUM; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; FURA 2; FUSED HETEROCYCLIC RINGS; RHOD 2; RHOD-2; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; CYTOSOL; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOLECULAR IMAGING; NEUROPATHOLOGY; WILD TYPE; CALCIUM SIGNALING; ENZYMOLOGY; GENE TRANSFER; METABOLISM; MOTONEURON; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

AMYOTROPHIC LATERAL SCLEROSIS; CALCIUM; CALCIUM SIGNALING; CELL LINE, TUMOR; FURA-2; GENE TRANSFER TECHNIQUES; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; INDICATORS AND REAGENTS; MITOCHONDRIA; MOTOR NEURONS; NERVE DEGENERATION; SUPEROXIDE DISMUTASE;

EID: 68049094212     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-10-64     Document Type: Article

References (78)

1. Bruijn LI Houseweart MK Kato S Anderson KL Anderson SD Ohama E Reaume AG Scott RW Cleveland DW Aggregation and motorneuron toxicity of an ALS-linked SOD1 mutant independent from wildtype SOD1 Science 1998, 281:1851-1854 10.1126/science.281.5384.1851 9743498
2. Rowland LP Shneider NA Amyotrophic Lateral Sclerosis N Engl J Med 2001, 344:1688-1700 10.1056/NEJM200105313442207 11386269
3. Rosen DR Siddique T Patterson D Figlewicz DA Sapp P Hentati A Donaldson D Goto J O'Regan JP Deng HX et al Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 1993, 362:59-62 10.1038/362059a0 8446170
4. Rosen DR Bowling AC Patterson D Usdin TB Sapp P Mezey E McKenna-Yasek D O'Regan J Rahmani Z Ferrante RJ et al A frequent ala 4 to val superoxide dismutase-1 mutation is associated with a rapidly progressive familial amyotrophic lateral sclerosis Hum Mol Genet 1994, 3:981-7 10.1093/hmg/ 3.6.981 7951249
5. Gurney ME Pu H Chiu AY Dal Canto MC Polchow CY Alexander DD Caliendo J Hentati A Kwon YW Deng H-X Chen W Zhai P Sufit RL Siddique T Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase Science 1994, 264:1772-1775 10.1126/science.8209258 8209258
6. Carri MT Ferri A Battistoni A Famhy L Gabbianelli R Poccia F Rotilio G Expression of a Cu, Zn superoxide dismutase typical of familial amyotrophic lateral sclerosis induces mitochondrial alteration and increase of cytosolic Ca2+ concentration in transfected neuroblastoma SH-SY5Y cells FEBS Lett 1997, 414:365-8 10.1016/S0014-5793(97)01051-X 9315720
7. Andersen PM Sims KB Xin WW Kiely R O'Neill G Ravits J Pioro E Harati Y Brower RD Levine JS Heinicke HU Seltzer W Boss M Brown RH Jr Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: A decade of discoveries defects and disputes Amyotroph Lateral. Scler Other Motor Neuron Disord 2003, 4:62-73 10.1080/ 14660820310011700 14506936
8. Bowling AC Schulz JB Brown RH Jr Beal MF Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis J Neurochem 1993, 61:2322-5 10.1111/j.1471-4159.1993.tb07478.x 8245985
9. Wong PC Pardo CA Borchelt DR Lee MK Copeland NG Jenkins NA Sisodia SS Cleveland DW Price DL An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria Neuron 1995, 14:1105-16 10.1016/ 0896-6273(95)90259-7 7605627
10. Sasaki S Iwata M Ultrastructural study of synapses in the anterior horn neurons of patients with amyotrophic lateral sclerosis Neurosci Lett 1996, 204:53-6 10.1016/0304-3940(96)12314-4 8929976
11. Sasaki S Iwata M Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis Neurology 1996, 47:535-540 8757033
12. Kong J Xu Z Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1 J Neurosci 1998, 18:3241-50 9547233
13. Jaarsma D Rognoni F Duijn WV Verspaget HW Haasdijk ED Holstege JC Cu-Zn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations Acta Neuropath 2001, 102:293-305 11603803
14. Menzies FM Cookson MR Taylor RW Turnbull DM Chrzanowska-Lightowlers ZM Dong L Figlewicz DA Shaw PJ Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis Brain 2002, 125:1522-1533 10.1093/brain/awf167 12077002
15. Menzies FM Ince PG Shaw PJ Mitochondrial involvement in amyotrophic lateral sclerosis Neurochem Inter 2002, 40:543-551 10.1016/ S0197-0186(01)00125-5
16. Wiedemann FR Winkler K Kuznetsov AV Bartels C Vielhaber S Feistner H Kunz WS Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis J Neurol Sci 1998, 156:65-72 10.1016/S0022-510X(98)00008-2 9559989
17. Wiedemann FR Manfredi G Mawrin C Beal MF Schon EA Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients J Neurochem 2002, 80:616-625 10.1046/j.0022-3042.2001.00731.x 11841569
18. Vielhaber S Kunz D Winkler K Wiedemann FR Kirches E Feistner H Heinze HJ Elger CE Schubert W Kunz WS Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis Brain 2000, 123(Pt 7):1339-48 10.1093/brain/123.7.1339 10869047
19. Bergmann F Keller BU Impact of mitochondrial inhibition on excitability and cytosolic Ca2+ levels in brainstem motoneurons from mouse J Physiol 2004, 555:45-59 1664822 14660707 10.1113/jphysiol.2003.053900
20. Ferri A Gabbianelli R Casciati A Paolucci E Rotilio G Carrì MT Calcineurin activity is regulated both by redox compounds and by mutant familial amyotrophic lateral sclerosis-superoxide dismutase J Neurochem 2000, 75:606-13 10.1046/j.1471-4159.2000.0750606.x 10899935
21. Rao SD Weiss JH Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis Trends Neurosci 2004, 27:17-23 10.1016/j.tins.2003.11.001 14698606
22. Rothstein JD Martin LJ Kuncl RW Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis N Engl J Med 1992, 326:1464-8 1349424
23. Rothstein JD Van Kammen M Levey AI Martin LJ Kuncl RW Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis Ann Neurol 1995, 38:73-84 10.1002/ana.410380114 7611729
24. Trotti D Rolfs A Danbolt NC Brown RH Hediger MA SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter Nat Neurosci 1999, 2:427-433 10.1038/8091 10321246
25. Carriedo SG Sensi SL Yin HZ Weiss JH AMPA exposures induce mitochondrial Ca2+ overload and ROS generation in spinal motor neurons in vitro J Neurosci 2000, 20:240-50 10627601
26. Maragakis NJ Rothstein JD Glutamate transporters in neurologic disease Arch Neurol 2001, 58:365-70 10.1001/archneur.58.3.365 11255439
27. Heath PR Shaw PJ Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis Muscle Nerve 2002, 26:438-58 10.1002/mus.10186 12362409
28. Guo H Lai L Butchbach ME Stockinger MP Shan X Bishop GA Lin CL Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice Hum Mol Genet 2003, 12:2519-32 10.1093/hmg/ddg267 12915461
29. Rao SD Yin HZ Weiss JH Disruption of glial glutamate transport by reactive oxygen species produced in motor neurons J Neurosci 2003, 23:2627-2633 12684448
30. Llinas R Sugimori M Cherksey BD Smith RG Delbono O Stefani E Appel SH IgG from amyotrophic lateral sclerosis patients increases current through P-type calcium channels in mammalian cerebellar Purkinje cells and in isolated channel protein in lipid bilayer Proc Natl Acad Sci USA 1993, 90:11743-7 48060 8265620 10.1073/pnas.90.24.11743
31. Appel SH Smith RG Engelhardt JI Stefani E Evidence for autoimmunity in amyotrophic lateral sclerosis J Neurol Sci 1994, 124(Suppl):14-9 10.1016/ 0022-510X(94)90171-6 7807136
32. Appel SH Smith RG Alexianu M Siklos L Engelhardt J Colom LV Stefani E Increased intracellular calcium triggered by immune mechanisms in amyotrophic lateral sclerosis Clin Neurosci 1996, 3(6):368-374
33. Mattson MP LaFerla FM Chan SL Leissring MA Shepel PN Geiger JD Calcium signaling in the ER: Its role in neuronal plasticity and neurodegenerative disorders Trends Neurosci 2000, 23:222-229 10.1016/ S0166-2236(00)01548-4 10782128
34. Beal MF Oxidatively modified proteins in aging and disease Free Radical Biology and Medicine 2002, 32:797-803 10.1016/S0891-5849(02)00780-3
35. Bosch Van Den L Schwaller B Vleminckx V Meijers B Stork S Ruehlicke T Van Houtte E Klaassen H Celio MR Missiaen L Protective effect of parvalbumin on excitotoxic motor neuron death Exp Neurol 2002, 174:150-161 10.1006/exnr.2001.7858 11922657
36. Simpson EP Yen AA Appel SH Oxidative Stress: A common denominator in the pathogenesis of amyotrophic lateral sclerosis Curr Opin Rheumatol 2003, 15:730-736 10.1097/00002281-200311000-00008 14569202
37. Tateno M Sadakata H Tanaka M Itohara S Shin RM Miura M Masuda M Aosaki T Urushitani M Misawa H Takahashi R Calcium-permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model Hum Mol Genet 2004, 13:2183-2196 10.1093/hmg/ddh246 15294873
38. Von Lewinski F Keller BU Ca2+, mitochondria and selective motoneuron vulnerability: Implications for ALS Trends Neurosci 2005, 28:494-500 10.1016/j.tins.2005.07.001 16026864
39. Goodall EF Morrison KE Amyotrophic lateral sclerosis (motor neuron disease): Proposed mechanisms and pathways to treatment Expert Rev Mol Med 2006, 8:1-22 10.1017/S1462399406010854 16723044
40. Goos M Zech WD Jaiswal MK Balakrishnan S Ebert S Mitchell T Carrì MT Keller BU Nau R Expression of a Cu, Zn superoxide dismutase typical for familial amyotrophic lateral sclerosis increases the vulnerability of neuroblastoma cells to infectious injury BMC Infect Dis 2007, 12(7):131 10.1186/1471-2334-7-131
41. Herrington J Park YB Babcock DF Hille B Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells Neuron 1996, 16:219-228 10.1016/S0896-6273(00)80038-0 8562086
42. Schinder AF Olson EC Spitzer NC Montal M Mitochondrial dysfunction is a primary event in glutamate neurotoxicity J Neurosci 1996, 16:6125-33 8815895
43. Bar PR Motor neuron disease in vitro: The use of cultured motor neurons to study amyotrophic lateral sclerosis Eur J Pharmacol 2000, 405:285-295 10.1016/S0014-2999(00)00560-4 11033335
44. Sachiko T Seiji K Kazuyoshi S Jun T Riichiro K Ichiro Y Shoichi Y Masayoshi T Hidenao S Proteasome inhibition induces selective motor neuron death in organotypic slice cultures J Neurosci Res 2005, 82:443-451 10.1002/jnr.20665 16235246
45. Avossa D Grandolfo M Mazzarol F Zatta M Ballerini L Early signs of motoneuron vulnerability in a disease model system: Characterization of transverse slice cultures of spinal cord isolated from embryonic ALS mice Neuroscience 2006, 138:1179-1194 10.1016/j.neuroscience.2005.12.009 16442737
46. Carri MT Ferri A Cozzolino M Calabrese L Rotilio G Neurodegeneration in amyotrophic lateral sclerosis: The role of oxidative stress and altered homeostasis of metals Brain Res Bull 2003, 61:365-374 10.1016/ S0361-9230(03)00179-5 12909279
47. Ciriolo MR De Martino A Lafavia E Rossi L Carrì MT Rotilio G Cu, Zn superoxide dismutase-dependent apoptosis induced by nitric oxide in neuronal cells J Biol Chem 2000, 275:5065-5072 10.1074/jbc.275.7.5065 10671549
48. Gabbianelli R Ferri A Rotilio G Carrì MT Aberrant copper chemistry as a major mediator of oxidative stress in a human cellular model of amyotrophic lateral sclerosis J Neurochem 1999, 73:1175-80 10.1046/j.1471-4159.1999.0731175.x 10461909
49. Ferri A Nencini M Casciati A Cozzolino M Angelini DF Longone P Spalloni A Rotilio G Carrì MT Cell death in amyotrophic lateral sclerosis: interplay between neuronal and glial cells FASEB J 2004, 18:1261-3 15208263
50. Di Poto C Iadarola P Bardoni AM Passadore I Giorgetti S Cereda C Carrì MT Ceroni M Salvini R 2-DE and MALDI-TOF-MS for a comparative analysis of proteins expressed in different cellular models of amyotrophic lateral sclerosis Electrophoresis 2007, 28:4320-9 10.1002/ elps.200700455 17979159
51. Ladewig T Keller BU Simultaneous patch-clamp recording and calcium imaging in a rhythmically active neuronal network in the brainstem slice preparation from mouse Pflugers Arch 2000, 440:322-332 10898534
52. Ladewig T Kloppenburg P Lalley PM Zipfel WR Webb WW Keller BU Spatial profiles of store-dependent calcium release in motoneurones of the nucleus hypoglossus from newborn mouse J Physiol 2003, 547:775-787 2342737 12562905 10.1113/jphysiol.2002.033605
53. Duchen MR Mitochondria and Ca2+ in cell physiology and pathophysiology Cell Calcium 2000, 28:339-348 10.1054/ceca.2000.0170 11115373
54. Duchen MR Mitochondria and calcium: From cell signalling to cell death J Physiol 2000, 15:57-68 10.1111/j.1469-7793.2000.00057.x
55. Nicholls DG Budd SL Mitochondria and neuronal survival Physiol Rev 2000, 80:315-360 10617771
56. Billups B Forsythe ID Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses J Neurosci 2002, 22:5840-5847 12122046
57. Sagara Y Inesi G Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations J Biol Chem 1991, 266:13503-6 1830305
58. Svichar N Shmigol A Verkhratsky A Kostyuk P ATP induces Ca2+ release from IP3-sensitive Ca2+ stores exclusively in large DRG neurones Neuroreport 1997, 8:1555-1559 9189891
59. Solovyova N Veselovsky N Toescu EC Verkhratsky A Ca (2+) dynamics in the lumen of the endoplasmic reticulum in sensory neurons: Direct visualization of Ca (2+)-induced Ca (2+) release triggered by physiological Ca (2+) entry EMBO J 2002, 21:622-30 125857 11847110 10.1093/emboj/21.4.622
60. Kirichok Y Krapivinsky G Clapham DE The mitochondrial calcium uniporter is a highly selective ion channel Nature 2004, 22:360-4 10.1038/ nature02246
61. Lytton J Westlin M Hanley MR Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps J Biol Chem 1991, 266:17067-71 1832668
62. Jaiswal MK Keller BU Cu/Zn superoxide dismutase typical for familial amyotrophic lateral sclerosis increases the vulnerability of mitochondria and perturbs Ca2+ homeostasis in SOD1G93A mice Mol Pharmacol 2009, 75:478-489 10.1124/mol.108.050831 19060114
63. Wei H Perry DC Dantrolene is cytoprotective in two models of neuronal cell death J Neurochem 1996, 67:2390-2398 8931471
64. Friel DD Tsien RW An FCCP-sensitive Ca2+ store in bullfrog sympathetic neurons and its participation in stimulus-evoked changes in [Ca2+]i J Neurosci 1994, 14:4007-4024 8027759
65. Budd SL Nicholls DG A reevaluation of the role of mitochondria in neuronal Ca2+ homeostasis J Neurochem 1996, 66:403-411 8522981
66. David G Barrett JN Barrett EF Evidence that mitochondria buffer physiological Ca2+ loads in lizard motor nerve terminals J Physiol 1998, 509:59-65 2230953 9547381 10.1111/j.1469-7793.1998.059bo.x
67. Alexianu ME Ho BK Mohamed AH La Bella V Smith RG Appel SH The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis Ann Neurol 1994, 36:846-858 10.1002/ ana.410360608 7998770
68. Siklós L Engelhardt JI Alexianu ME Gurney ME Siddique T Appel SH Intracellular calcium parallels motoneuron degeneration in SOD-1 mutant mice J Neuropathol Exp Neurol 1998, 57:571-87 10.1097/ 00005072-199806000-00005 9630237
69. Beers DR Ho BK Siklos L Alexianu ME Mosier DR Habib Mohamed A Otsuka Y Kozovska ME Smith RE McAlhany RG Appel SH Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis J Neurochem 2001, 79:499-509 10.1046/j.1471-4159.2001.00582.x 11701753
70. Balakrishnan S Bergmann F Keller BU Mitochondria differentially regulate [Ca]i in brainstem motoneurons from mouse: Implications for selective motoneuron vulnerability [abstract] Program No. 340.16, Abstract Viewer and Itinerary Planner, Society for Neuroscience 2004 http://www.sfn.org/ index.aspx?pagename=abstracts_ampublications
71. Jaiswal MK Stefan H Balakrishnan S Schomburg ED Keller BU Disruptions of [Ca]i and mitochondria in the adult SOD1G93A mouse model of ALS: evidence from recordings in vitro and in vivo Program No. 508.8, 2006, In 2006 Abstract Viewer and Itinerary Planner, Society for Neuroscience http://www.sfn.org/index.aspx?pagename=abstracts_ampublications
72. David G Barrett EF Stimulation-evoked increases in cytosolic [Ca2+] in mouse motor nerve terminals are limited by mitochondrial uptake and are temperature-dependent J Neurosci 2000, 20:7290-7296 11007886
73. Fill M Copello JA Ryanodine receptor calcium release channels Physiol Rev 2002, 82:893-922 12270947
74. Sher AA Hinch R Noble PJ Gavaghan DJ Noble D Functional significance of Na+/Ca2+ exchangers co-localization with ryanodine receptors Ann N Y Acad Sci 2007, 1099:215-220 10.1196/annals.1387.047 17446461
75. Leoty C Huchet-Cadiou C Talon S Choisy S Hleihel W Caffeine stimulates the reverse mode of Na+/Ca2+ exchanger in ferret ventricular muscled Acta Physiologica Scandinavica 2001, 172:27-37 10.1046/ j.1365-201X.2001.00819.x 11437737
76. Sasaki S Warita H Murakami T Abe K Iwata M Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene Acta Neuropathol 2004, 107:461-74 10.1007/s00401-004-0837-z 15029445
77. Sasaki S Warita H Abe K Iwata M Impairment of axonal transport in the axon hillock and the initial segment of anterior horn neurons in transgenic mice with a G93A mutant SOD1 gene Acta Neuropathol 2005, 110:48-56 10.1007/s00401-005-1021-9 15920660
78. Sen I Nalini A Joshi NB Joshi PG Cerebrospinal fluid from amyotrophic lateral sclerosis patients preferentially elevates intracellular calcium and toxicity in motor neurons via AMPA/kainate receptor J Neurol Sci 2005, 235:45-54 10.1016/j.jns.2005.03.049 15936037