Accumulation of misfolded SOD1 in dorsal root ganglion degenerating proprioceptive sensory neurons of transgenic mice with amyotrophic lateral sclerosis

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Sábado, Javier ^a   Casanovas, Anna ^a   Tarabal, Olga ^a   Hereu, Marta ^a   Piedrafita, Lídia ^a   Calderó, Jordi ^a   Esquerda, Josep E ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MYELIN; NEUROTROPHIN RECEPTOR P75; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; INFLAMMATION; MACROPHAGE; MICROGLIA; MITOCHONDRION; MOTONEURON; MOUSE; NERVE DEGENERATION; NERVE FIBER; NEUROTOXICITY; NONHUMAN; PHAGOCYTOSIS; PROPRIOCEPTIVE SENSORY NEURON; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN MISFOLDING; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL CORD VENTRAL HORN; SPINAL GANGLION; SYNAPTIC TRANSMISSION; UPREGULATION; AMINO ACID SUBSTITUTION; ANIMAL; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PATHOLOGY; PROTEIN FOLDING; TRANSGENIC MOUSE;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; GANGLIA, SPINAL; HUMANS; MICE; MICE, TRANSGENIC; MUTATION, MISSENSE; PROTEIN FOLDING; SENSORY RECEPTOR CELLS; SUPEROXIDE DISMUTASE;

EID: 84901272326     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/852163     Document Type: Article

References (44)

1. Cleveland D. W., Rothstein J. D., From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nature Reviews Neuroscience 2001 2 11 806 819 2-s2.0-0035516124 10.1038/35097565 (Pubitemid 33674062)
2. Mitchell J., Borasio G., Amyotrophic lateral sclerosis. The Lancet 2007 369 9578 2031 2041 2-s2.0-34250209501 10.1016/S0140-6736(07)60944-1 (Pubitemid 46899183)
3. Gaudette M., Hirano M., Siddique T., Current status of SOD1 mutations in familial amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders 2000 1 2 83 89 2-s2.0-0034158520
4. Gurney M. E., The use of transgenic mouse models of amyotrophic lateral sclerosis in preclinical drug studies. Journal of the Neurological Sciences 1997 152 supplement 1 S67 S73 2-s2.0-0030690490 10.1016/S0022-510X(97)00247-5 (Pubitemid 27505293)
5. Bosco D. A., Morfini G., Karabacak N. M., Song Y., Gros-Louis F., Pasinelli P., Goolsby H., Fontaine B. A., Lemay N., McKenna-Yasek D., Frosch M. P., Agar J. N., Julien J.-P., Brady S. T., Brown R. H., Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nature Neuroscience 2010 13 11 1396 1403 2-s2.0-77958519939 10.1038/nn.2660
6. Mochizuki Y., Mizutani T., Shimizu T., Kawata A., Proportional neuronal loss between the primary motor and sensory cortex in amyotrophic lateral sclerosis. Neuroscience Letters 2011 503 1 73 75 2-s2.0-80052651800 10.1016/j.neulet.2011.08.014
7. Merico A., Cavinato M., Autonomic dysfunction in the early stage of ALS with bulbar involvement. Amyotrophic Lateral Sclerosis 2011 12 5 363 367 2-s2.0-80053999738 10.3109/17482968.2011.584628
8. Williams C., Kozlowski M. A., Hinton D. R., Miller C. A., Degeneration of spinocerebellar neurons in amyotrophic lateral sclerosis. Annals of Neurology 1990 27 3 215 225 2-s2.0-0025271783 (Pubitemid 20122372)
9. Dentel C., Palamiuc L., Henriques A., Lannes B., Spreux-Varoquaux O., Gutknecht L., René F., Echaniz-Laguna A., Gonzalez de Aguilar J. L., Lesch K. P., Meininger V., Loeffler J. P., Dupuis L., Degeneration of serotonergic neurons in amyotrophic lateral sclerosis: a link to spasticity. Brain 2013 136 2 483 493 10.1093/brain/aws274
10. Theys P. A., Peeters E., Robberecht W., Evolution of motor and sensory deficits in amyotrophic lateral sclerosis estimated by neurophysiological techniques. Journal of Neurology 1999 246 6 438 442 2-s2.0-0032808124 10.1007/s004150050379 (Pubitemid 29326836)
11. Guo Y.-S., Wu D.-X., Wu H.-R., Wu S.-Y., Yang C., Li B., Bu H., Zhang Y.-S., Li C.-Y., Sensory involvement in the SOD1-G93A mouse model of amyotrophic lateral sclerosis. Experimental and Molecular Medicine 2009 41 3 140 150 2-s2.0-65949109907 10.3858/emm.2009.41.3.017
12. Casanovas A., Hernández S., Tarabal O., Rosselló J., Esquerda J. E., Strong P2X4 purinergic receptor-like immunoreactivity is selectively associated with degenerating neurons in transgenic rodent models of amyotrophic lateral sclerosis. Journal of Comparative Neurology 2008 506 1 75 92 2-s2.0-37349068139 10.1002/cne.21527 (Pubitemid 350293491)
13. Hernández S., Casanovas A., Piedrafita L., Tarabal O., Esquerda J. E., Neurotoxic species of misfolded SOD1G93A recognized by antibodies against the P2X4 subunit of the ATP receptor accumulate in damaged neurons of transgenic animal models of amyotrophic lateral sclerosis. Journal of Neuropathology and Experimental Neurology 2010 69 2 176 187 2-s2.0-75949096699 10.1097/NEN. 0b013e3181cd3e33
14. Sábado J., Casanovas A., Hernández S., Piedrafita L., Hereu M., Esquerda J. E., Immunodetection of disease-associated conformers of mutant SOD1 selectively expressed in degenerating neurons in amyotrophic lateral sclerosis. Journal of Neuropathology & Experimental Neurology 2013 72 646 661
15. Gurney M. E., Pu H., Chiu A. Y., Dal Canto M. C., Polchow C. Y., Alexander D. D., Caliendo J., Hentati A., Kwon Y. W., Deng H.-X., Chen W., Zhai P., Sufit R. L., Siddique T., Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994 264 5166 1772 1775 2-s2.0-0028284779 (Pubitemid 24227760)
16. Chiu A. Y., Zhai P., Dal Canto M. C., Peters T. M., Kwon Y. W., Prattis S. M., Gurney M. E., Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Molecular and Cellular Neurosciences 1995 6 4 349 362 2-s2.0-0029096114 10.1006/mcne.1995.1027
17. Reichert F., Saada A., Rotshenker S., Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2. Journal of Neuroscience 1994 14 5 3231 3245 2-s2.0-0028334842 (Pubitemid 24139006)
18. Taniuchi M., Clark H. B., Schweitzer J. B., Johnson E. M. Jr., Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. Journal of Neuroscience 1988 8 2 664 681 2-s2.0-0023856172 (Pubitemid 18078090)
19. Ferri C. C., Bisby M. A., Improved survival of injured sciatic nerve Schwann cells in mice lacking the p75 receptor. Neuroscience Letters 1999 272 3 191 194 2-s2.0-0032831279 10.1016/S0304-3940(99)00618-7 (Pubitemid 29412975)
20. Midroni G., Bilbao J. M., Midroni G., Bilbao J. M., The axon: normal structure and pathological reactions. Biopsy Diagnosis of Peripheral Neuropathy 1995 Boston, Mass, USA Butterworth-Heinemann 45 74
21. Saxena S., Roselli F., Singh K., Leptien K., Julien J. P., Gros-Louis F., Caroni P., Neuroprotection through excitability and mTOR required in ALS motoneurons to delay disease and extend survival. Neuron 2013 80 80 96
22. Ernfors P., Lee K.-F., Kucera J., Jaenisch R., Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 1994 77 4 503 512 2-s2.0-0028291238 10.1016/0092-8674(94)90213-5 (Pubitemid 24153991)
23. Basbaum A. I., Bautista D. M., Scherrer G., Julius D., Cellular and molecular mechanisms of pain. Cell 2009 139 2 267 284 2-s2.0-70349845440 10.1016/j.cell.2009.09.028
24. Marmigère F., Ernfors P., Specification and connectivity of neuronal subtypes in the sensory lineage. Nature Reviews Neuroscience 2007 8 2 114 127 2-s2.0-33846447430 10.1038/nrn2057 (Pubitemid 46146950)
25. Kawamura Y., Dyck P. J., Shimono M., Okazaki H., Tateishi J., Doi H., Morphometric comparison of the vulnerability of peripheral motor and sensory neurons in amyotrophic lateral sclerosis. Journal of Neuropathology and Experimental Neurology 1981 40 6 667 675 2-s2.0-0019784990 (Pubitemid 12248680)
26. Dyck P. J., Stevens J. C., Mulder D. W., Espinosa R. E., Frequency of nerve fiber degeneration of peripheral motor and sensory neurons in amyotrophic lateral sclerosis. Morphometry of deep and superficial peroneal nerves. Neurology 1975 25 8 781 785 2-s2.0-0016788436
27. Bradley W. G., Good P., Rasool C. G., Adelman L. S., Morphometric and biochemical studies of peripheral nerves in amyotrophic lateral sclerosis. Annals of Neurology 1983 14 3 267 277 2-s2.0-0020507869 (Pubitemid 13051229)
28. Heads T., Pollock M., Robertson A., Sutherland W. H. F., Allpress S., Sensory nerve pathology in amyotrophic lateral sclerosis. Acta Neuropathologica 1991 82 4 316 320 2-s2.0-0025833494
29. Pugdahl K., Fuglsang-Frederiksen A., de Carvalho M., Johnsen B., Fawcett P. R. W., Labarre-Vila A., Liguori R., Nix W. A., Schofield I. S., Generalised sensory system abnormalities in amyotrophic lateral sclerosis: a European multicentre study. Journal of Neurology, Neurosurgery and Psychiatry 2007 78 7 746 749 2-s2.0-34347247316 10.1136/jnnp.2006.098533 (Pubitemid 46998851)
30. Sun W., Funakoshi H., Nakamura T., Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. Journal of Neuroscience 2002 22 15 6537 6548 2-s2.0-0036703771 (Pubitemid 35386410)
31. Fischer L. R., Culver D. G., Davis A. A., Tennant P., Wang M., Coleman M., Asress S., Adalbert R., Alexander G. M., Glass J. D., The WldS gene modestly prolongs survival in the SOD1 G93A fALS mouse. Neurobiology of Disease 2005 19 1-2 293 300 2-s2.0-20244390181 10.1016/j.nbd.2005.01.008 (Pubitemid 40544747)
32. Wong P. C., Pardo C. A., Borchelt D. R., Lee M. K., Copeland N. G., Jenkins N. A., Sisodia S. S., Cleveland D. W., Price D. L., An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995 14 6 1105 1116 2-s2.0-0029053881
33. Bendotti C., Calvaresi N., Chiveri L., Prelle A., Moggio M., Braga M., Silani V., De Biasi S., Early vacuolization and mitochondrial damage in motor neurons of FALS mice are not associated with apoptosis or with changes in cytochrome oxidase histochemical reactivity. Journal of the Neurological Sciences 2001 191 1-2 25 33 2-s2.0-0035886428 10.1016/S0022-510X(01)00627-X (Pubitemid 33035892)
34. Sasaki S., Warita H., Murakami T., Abe K., Iwata M., Ultrastructural study mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathologica 2004 107 5 461 474 2-s2.0-2342442179 10.1007/s00401-004-0837-z (Pubitemid 38559256)
35. Higgins C. M. J., Jung C., Xu Z., ALS-associated mutant SODIG93A causes mitochondrial vacuolation by expansion of the intermembrane space by involvement of SODI aggregation and peroxisomes. BMC Neuroscience 2003 4, article 16 2-s2.0-0344240348 10.1186/1471-2202-4-16 (Pubitemid 38729163)
36. Deng H.-X., Shi Y., Furukawa Y., Zhai H., Fu R., Liu E., Gorrie G. H., Khan M. S., Hung W.-Y., Bigio E. H., Lukas T., Dal Canto M. C., O'Halloran T. V., Siddique T., Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proceedings of the National Academy of Sciences of the United States of America 2006 103 18 7142 7147 2-s2.0-33646466296 10.1073/pnas. 0602046103
37. Kamiya H., Zhang W., Sima A. A., Degeneration of the Golgi and neuronal loss in dorsal root ganglia in diabetic BioBreeding/Worcester rats. Diabetologia 2006 49 11 2763 2774 2-s2.0-34250330253 10.1007/s00125-006-0379-0
38. Katona I., Zhang X., Bai Y., Shy M. E., Guo J., Yan Q., Hatfield J., Kupsky W. J., Li J., Distinct pathogenic processes between Fig4-deficient motor and sensory neurons. European Journal of Neuroscience 2011 33 8 1401 1410 2-s2.0-79954471977 10.1111/j.1460-9568.2011.07651.x
39. Cavaletti G., Gilardini A., Canta A., Rigamonti L., Rodriguez-Menendez V., Ceresa C., Marmiroli P., Bossi M., Oggioni N., D'Incalci M., De Coster R., Bortezomib-induced peripheral neurotoxicity: a neurophysiological and pathological study in the rat. Experimental Neurology 2007 204 1 317 325 2-s2.0-33847293709 10.1016/j.expneurol.2006.11.010 (Pubitemid 46330280)
40. Saxena S., Cabuy E., Caroni P., A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nature Neuroscience 2009 12 5 627 636 2-s2.0-67349164383 10.1038/nn.2297
41. Prell T., Lautenschläger J., Witte O. W., Carri M. T., Grosskreutz J., The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. European Journal of Neuroscience 2012 35 5 652 660 2-s2.0-84857953079 10.1111/j.1460-9568.2012.08008.x
42. Grad L. I., Guest W. C., Yanai A., Pokrishevsky E., O'Neill M. A., Gibbs E., Semenchenko V., Yousefi M., Wishart D. S., Plotkin S. S., Cashman N. R., Intermolecular transmission of superoxide dismutase 1 misfolding in living cells. Proceedings of the National Academy of Sciences of the United States of America 2011 108 39 16398 16403 2-s2.0-80053652133 10.1073/pnas.1102645108
43. Münch C., O'Brien J., Bertolotti A., Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proceedings of the National Academy of Sciences of the United States of America 2011 108 9 3548 3553 2-s2.0-79952743365 10.1073/pnas.1017275108
44. Polymenidou M., Cleveland D. W., The seeds of neurodegeneration: prion-like spreading in ALS. Cell 2011 147 3 498 508 2-s2.0-80155157847 10.1016/j.cell.2011.10.011