Dysregulation of stathmin, a microtubule-destabilizing protein, and up-regulation of Hsp25, Hsp27, and the antioxidant peroxiredoxin 6 in a mouse model of familial amyotrophic lateral sclerosis

American Journal of Pathology

Volumn 165, Issue 5, 2004, Pages 1701-1718

  Strey, Christoph W ^a   Spellman, Daniel ^a   Stieber, Anna ^a   Gonatas, Jacqueline O ^a   Wang, Xiaosong ^b   Lambris, John D ^a   Gonatas, Nicholas K ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; APOLIPOPROTEIN E; FERRITIN; HEAT SHOCK PROTEIN 25; HEAT SHOCK PROTEIN 27; ISOPROTEIN; MUTANT PROTEIN; PEROXIREDOXIN; PEROXIREDOXIN 6; PHOSPHATIDYLINOSITOL; STATHMIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ACIDITY; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; ASTROCYTE; CELL LINE; CONTROLLED STUDY; CYTOPLASM; GOLGI COMPLEX; HUMAN; MICROTUBULE ASSEMBLY; MOTONEURON; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PARALYSIS; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SPINAL CORD; UPREGULATION;

EID: 7244239105     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63426-8     Document Type: Article

References (68)

1. Hirano A: Cytopathology of amyotrophic lateral sclerosis: a personal perspective of recent developments. Neuropathology 1995, 15:1-6
2. Kondo K: Epidemiological aspects of motor neuron disease. Amyotrophic Lateral Sclerosis: Progress and Perspectives in Basic Research and Clinical Alication. Edited by P Nakano, A Hirano. Amsterdam, Elsevier Excerpta Medica, International Congress Series 1996, 1104, pp 133-141
3. Okumura H, Chen K-M, Kurland LT: Recent epidemiological study of ALS and PDC in Guam Island. Amyotrophic Lateral Sclerosis: Progress and Perspectives in Basic Research and Clinical Alication. Edited by P Nakano, A Hirano. Amsterdam, Elsevier Excerpta Medica, International Congress Series 1996, 1104, pp 154-157
4. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, Getzof ED, Hu P, Herzfeld B, Roos RP, Warner C, Deng G, Soriano E, Smyth C, Parge HE, Ahmed A, Roses AD, Hallewell RA, Pericak-Vance MA, Siddique T: Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 1993, 261:1047-1051
5. Rosen DR, Siddique T, Patterson S, Figlewicz DA, Sa P, Hentati A, Donaldson D, Goto J, O'Reagan JP, Deng HX, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung WY, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella GS, Horvitz HR, Brown Jr RH: Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62
6. 1 Zn superoxide mutation. Science 1994, 264:1772-1775
7. Julien, J-P: Review. Amyotrophic lateral sclerosis: unfolding the toxicity of the misfolded. Cell 2001, 104:581-591
8. Sobel A, Butterin M-C, Beretta L, Chneiweis H, Doye V, Peyro-Saint-Paul H: Intracellular substrates for extracellular signaling. Characterization of a ubiquitous, neuron enriched phosphoprotein (Stathmin). J Biol Chem 1989, 264:3765-3772
9. Gavet O, Messari SE, Ozon S, Sobel A: Regulation and subcellular localization of the microtubule-destabilizing Stathmin family phosphoproteins in cortical neurons. J Neurosci Res 2002, 68:535-550
10. Gavet O, Ozon S, Manceau V, Lawler S, Curmi P, Sobel A: The Stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J Cell Sci 1998, 111:3333-3346
11. Robbins E, Gonatas NK: Histochemical and ultrastructural studies on HeLa cell cultures exposed to spindle inhibitors with special reference to the interphase cell. J Histochem Cytochem 1964, 1:704-711
12. Kreis TE, Goodson HV, Perez F, Roonnholm R: Golgi apparatus-cytoskeleton interactions. The Golgi Apparatus. Edited by EG Berger, J Roth. Basel, Birkhauser, 1997:179-193
13. Gonatas NK: Contributions to the physiology and pathology of the Golgi apparatus. Am J Pathol 1994, 145:751-761
14. Fujita Y, Okamoto K, Sakurai A, Gonatas NK, Hirano A: Fragmentation of the Golgi apparatus of the anterior horn cells in patients with familial amyotrophic lateral sclerosis with SOD1 mutations and posterior column involvement. J Neurol Sci 2000, 174:137-140
15. Mourelatos Z, Gonatas NK, Stieber A, Gurney ME, Dal Canto MC: The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc Natl Acad Sci USA 1996, 93:5472-5477
16. Tu PH, Gurney MC, Julien J-P, Lee M-Y V, Trojanowski JQ: Oxidative stress, human SOD1, and neurofilament pathology in transgenic mouse models of human motor neuron disease. Lab Invest 1997, 76:441-456
17. Okado-Matsumoto A, Fridovich I: Amyotrophic lateral sclerosis: a proposed mechanism. Proc Natl Acad Sci USA 2002, 99:9010-9014
18. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins JA, Copeland NG, Sisodia SS, Rothstein JD, Borchelt DR, Price DL, Cleveland DW: ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1977, 18:327-338
19. Kato S, Shimoda M, Watanabe Y, Nakashima K, Takahashi K, Ohama E: Familial amyotrophic lateral sclerosis with a two base pair deletion in superoxide dismutase 1 gene: multisystem degeneration with intracytoplasmic inclusions in astrocytes. J Neuropathol Exp Neurol 1996, 55:1089-1101
20. Gonatas JO, Mezitis SGE, Stieber A, Fleischer B, Gonatas NK: MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi apparatus. J Biol Chem 1989, 264:646-653
21. Croul S, Mezitis SGE, Stieber A, Chen Y, Gonatas JO, Goud B, Gonatas NK: lmmunocytochemical visualization of the Golgi apparatus in several species, including human, and tissues with an antiserum against MG-160, a sialoglycoprotein of rat Golgi apparatus. J Histochem Cytochem 1990, 38:957-963
22. Lowe M, Gonatas NK, Warren G: The mitotic phosphorylation cycle of the cis-Golgi matrix protein GM130. J Cell Biol 2000, 149:341-355
23. Stuhlmeier KM, Kao J, Wallbrandt P, Lindberg M, Hammarstrom B, Broell H, Paigen B: Antioxidant protein 2 prevents methemoglobin formation in erythrocyte hemolysates. Eur J Biochem 2003, 270:334-341
24. Koppel JJ, Boutterin M-C, Doye V, Peyro-Saint-Paul H, Sobel A: Developmental tissue expression and phylogenetic conservation of Stathmin, a phosphoprotein associated with cell regulations. J Biol Chem 1990, 265:3703-3707
25. Collins J, Schandl CA, Young KK, Vessely J, Willingham MC: Major DNA fragmentation is a late event in apoptosis. J Histochem Cytochem 1997, 45:923-934
26. Stieber A, Gonatas JO, Collard J-F, Meier J, Julien J-P, Schweitzer P, Gonatas NK: The neuronal Golgi apparatus is fragmented in transgenic mice expressing a human SOD1, but not in mice expressing the human NF-H gene. J Neurol Sci 2000, 173:63-67
27. Johnston PA, Stieber A, Gonatas NK: A hypothesis on the traffic of MG160, a medial Golgi sialoglycoprotein, from the trans-Golgi network to the Golgi cisternae. J Neurol Sci 1994, 107:529-537
28. Ahn J, Murphy M, Kratowicz S, Wang A, Levine AJ, George D: Down-regulation of the Stathmin/Op28 and FKBR genes following p53 induction. Oncogene 1999, 18:5954-5958
29. Gonatas JO, Chen Y-J, Stieber A, Mourelatos Z, Gonatas NK: Truncations of the C-terminal cytoplasmic domain of MG160, a medial Golgi sialoglycoprotein, result in its partial transport to the plasma membrane and filopodia. J Cell Sci 1998, 111:249-260
30. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254
31. Langen H, Roder D, Juranville JF, Fountoulakis M: Effect of protein application mode and acrylamide concentration on the resolution of protein spots separated by two-dimensional gel electrophoresis. Electrophoresis 1997, 18:2085-2090
32. Alb Jr JG, Cortese JD, Phillips SE, Albin RL, Nagy TR, Hamilton BA, Bankaitis VA: Mice lacking phosphatidylinositol transfer protein-alpha exhibit spinocerebellar degeneration, intestinal and hepatic steatosis, and hypoglycemia. J Biol Chem 2003, 278:33501-33518
33. Haasdijk ED, Vlug A, Mulder MT, Jaarsma D: Increased apolipoprotein E expression correlates with the onset of neuronal degeneration in the spinal cord of G93A-SOD1 mice. Neurosci Lett 2002, 335:29-33
34. Wang X, Phelan SA, Forsman-Semb K, Taylor EF, Petros C, Brown A, Lerner CP, Paigen B: Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J Biol Chem 2003, 278:25179-25190
35. Double KL, Gerlach M, Youdim MB, Biederer P: Impaired iron homeostasis in Parkinson's disease. J Neural Transm 2000, 60:S37-S58
36. Senior K: New genes reveal major role for iron in neurodegeneration. Lancet 2001, 358:302
37. Helfand SL: Neurobiology. Chaperones take flight. Science 2002, 295:809-810
38. Bonini NM: Chaperoning brain degeneration. Proc Natl Acad Sci USA 2002, 99(Suppl 4): 16407-16411
39. Farah CA, Nguyen MD, Julien JP, Leclerc N: Altered levels and distribution of microtubule-associated proteins before disease onset in a mouse model of amyotrophic lateral sclerosis. J Neurochem 2003, 84:77-86
40. Liedtke W, Leman EE, Fyffe REW, Raine CS, Schubart UK: Stathmin-deficient mice develop an age dependent axonopathy of the central and peripheral nervous systems. Am J Pathol 2002, 160:469-480
41. Jin LW, Masliah E, Iimoto D, Deteresa R, Mallory M, Sundsmo M, Mori N, Sobel A, Saitoh T: Neurofibrillary tangle-associated alteration of Stathmin in Alzheimer's disease. Neurobiol Aging 1996, 17:331-341
42. Stieber A, Mourelatos Z, Gonatas NK: In Alzheimer's disease the Golgi apparatus of a population of neurons without neurofibrillary tangles is fragmented and atrophic. Am J Pathol 1996, 148:415-426
43. Cheon MS, Foundoulakis M, Caims NJ: Decreased protein levels of Stathmin in adult brains with Down's syndrome and Aizheimer's disease. J Neurol Transm 2001, 61:S281-S286
44. Stieber A, Gonatas JO, Gonatas NK: Aggregates of ubiquitin and a mutant ALS-linked SOD1 protein correlate with disease progression and fragmentation of the Golgi apparatus. J Neurol Sci 2000, 173:53-62
45. Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reume AG, Scott RW, Cleveland DW: Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 1998, 281:1851-1854
46. Brown JR RH: SOD1 aggregates in ALS: cause, correlate or consequence? Nat Med 1998, 4:1362-1364
47. Stieber A, Gonatas JO, Moore JS, Bantly A, Yim H-S, Yim MB, Gonatas NK: Disruption of the structure of the Golgi apparatus and the function of the secretory pathway by mutants G93A and G85R of Cu,Zn superoxide dismutase (SOD1) of familial amyotrophic lateral sclerosis. J Neurol Sci 2004, 219:45-53
48. Gosavi N, Lee H-J, Lee JS, Patel S, Lee S-J: Golgi fragmentation occurs in the cells with prefibrillar α-synuclein aggregates and precedes the formation of fibrillar inclusion. J Biol Chem 2002, 277:48984-48992
49. Graves TK, Patel S, Dannies PS, Hinkle PM: Misfolded growth hormone causes fragmentation of the Golgi apparatus and disrupts endoplasmic reticulum-to-Golgi traffic. J Cell Sci 2001, 114:3685-3694
50. Yoshiyama Y, Zhang B, Bruce J, Trojanowski JQ, Lee M-Y V: Reduction of detyrosinated microtubules and Golgi fragmentation are linked to Tau-induced degeneration in astrocytes. J Neurosci 2003, 23:10662-10671
51. Stromer T, Ernsperger M, Gaestel M, Buchner J: Analysis of the interaction of small heat shock proteins with unfolding proteins. J Biol Chem 2003, 278:18015-18021
52. Pieri I, Cifuentes-Diaz C, Oudinet JP, Blondet B, Rieger F, Gonin S, Arrigo AP, Thomas Y: Modulation of HSP25 expression in the paralysed mouse mutant. J Neurosci Res 2001, 65:247-253
53. Dabir DV, Trojanowski JQ, Richter-Landsberg C, Lee VM-Y, Forman MS: Expression of the small heat-shock protein αB crystallin in tauopathies and glial pathology. Am J Pathol 2004, 164:155-166
54. Takeushi H, Niwa J-I, Hishikawa N, Ishigaki S, Tanaka F, Doyu M, Sobue G: Dorfin prevents cell death by reducing mitochondrial localizing mutant superoxide dismutase 1 in a neuronal cell model of familial amyotrophic lateral sclerosis J Neurochem 2004, 89:64-72
55. Krapfenbauer K, Engidawork E, Cairns N, Foundoulakis M, Lubec G: Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Res 2003, 967:152-160
56. Pałacino JJ, Sagi D, Goldberg SM, Krauss S, Motz C, Wacker M, Klose JJ, Shen J: Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J Biol Chem 2004, 279:18614-18622
57. Valentine JS, Hart PJ: Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2003, 100:3617-3622
58. Chen G, Gharib TG, Huang CC, Taylor JM, Misek DE, Kardia SL, Giordano TJ, Iannettoni MD, Orringer MB, Hanash SM, Beer DG: Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics 2002, 1:304-313
59. Olsen M, Roberts SL, Ellenbrook BR: Disease mechanisms revealed by transcription profiling in SOD1-G93A transgenic mouse spinal cord. Ann Neurol 2001, 50:730-740
60. Yoshihara T, Ishigaki S, Yamamoto M, Liang Y, Niwa J-I, Takeuchi H, Doyo M, Sobue G: Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 2002, 80:158-167
61. Kirby J, Menzies FM, Cookson MR, Busby K, Shaw PJ: Differential gene expression in a cell culture model of SOD1-related familial motor neuron disease. Hum Mol Genet 2002, 11:2061-2075
62. Allen S, Heath PR, Kirby J, Wharton SB, Cookson MR, Menzies FM, Banks RE, Shaw PJ: Analysis of the cytosolic proteome in a cell culture model of familial amyotrophic lateral sclerosis reveals alterations to the proteasome, antioxidant defenses and nitric oxide synthetic pathways. J Biol Chem 2003, 278:6371-6383
63. Malaspina A, Kaushik N, Belleroche DJ: Differential expression of 14 genes in amyotrophic lateral sclerosis spinal cord detected using gridded cDNA arrays. J Neurochem 2001, 77:132-145
64. Stieber A, Gonatas JO, Gonatas NK: Aggregates of mutant protein appear progressively in dendrites, in periaxonal processes of oligodendrocytes, and in neuronal and astrocytic perikarya of mice expressing the SOD1G93A mutation of familial amyotrophic lateral sclerosis. J Neurol Sci 2000, 177:114-123
65. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA: Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 2001, 21:3369-3374
66. Lino MM, Schneider C, Caroni P: Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 2002, 22:4825-4832
67. Gong YH, Parsadanian AS, Andreeva A, Snider WD, Elliott JL: Restricted expression of G86R superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J Neurosci 2000, 20:660-665
68. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillé S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown Jr RH, Julien J-P, Goldstein LSB, Cleveland DW: Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003, 302:113-117