Proteasomal and autophagic degradative activities in spinal and bulbar muscular atrophy

Neurobiology of Disease

Volumn 40, Issue 2, 2010, Pages 361-369

  Rusmini, Paola ^a,b   Bolzoni, Elena ^a,b   Crippa, Valeria ^a,b   Onesto, Elisa ^a,b   Sau, Daniela ^a,b   Galbiati, Mariarita ^a,b   Piccolella, Margherita ^a   Poletti, Angelo ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ANDROGEN RECEPTOR; CYTOSINE; GUANINE; POLYGLUTAMINE; PROTEASOME; TESTOSTERONE;

AMINO TERMINAL SEQUENCE; AUTOPHAGY; BRAIN REGION; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; EXON; GENE MUTATION; HUMAN; KENNEDY DISEASE; MOTONEURON; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; REVIEW; SPINAL CORD VENTRAL HORN; TRINUCLEOTIDE REPEAT; UBIQUITINATION;

ANIMALS; AUTOPHAGY; BULBO-SPINAL ATROPHY, X-LINKED; HUMANS; MUTATION; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 78349310900     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.06.016     Document Type: Review

References (115)

1. Abel A., et al. Expression of expanded repeat androgen receptor produces neurologic disease in transgenic mice. Hum. Mol. Genet. 2001, 10:107-116.
2. Adachi H., et al. Transgenic mice with an expanded CAG repeat controlled by the human AR promoter show polyglutamine nuclear inclusions and neuronal dysfunction without neuronal cell death. Hum. Mol. Genet. 2001, 10:1039-1048.
3. Adachi H., et al. Heat shock protein 70 chaperone overexpression ameliorates phenotypes of the spinal and bulbar muscular atrophy transgenic mouse model by reducing nuclear-localized mutant androgen receptor protein. J. Neurosci. 2003, 23:2203-2211.
4. Adachi H., et al. Widespread nuclear and cytoplasmic accumulation of mutant androgen receptor in SBMA patients. Brain Res. 2005, 128:659-670.
5. Adachi H., et al. Pathogenesis and molecular targeted therapy of spinal and bulbar muscular atrophy. Neuropathol. Appl. Neurobiol. 2007, 33:135-151.
6. Adachi H., et al. CHIP overexpression reduces mutant androgen receptor protein and ameliorates phenotypes of the spinal and bulbar muscular atrophy transgenic mouse model. J. Neurosci. 2007, 27:5115-5126.
7. Anglade P., et al. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 1997, 12:25-31.
8. Arndt V., et al. Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr. Biol. 2010, 20:143-148.
9. Bailey C.K., et al. Molecular chaperones enhance the degradation of expanded polyglutamine repeat androgen receptor in a cellular model of spinal and bulbar muscular atrophy. Hum. Mol. Genet. 2002, 11:515-523.
10. Batlevi Y., et al. Dynein light chain 1 is required for autophagy, protein clearance, and cell death in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:742-747.
11. Bence N.F., et al. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001, 292:1552-1555.
12. Breedlove S.M., Arnold A.P. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 1980, 210:564-566.
13. Brooks B.P., Fischbeck K.H. Spinal and bulbar muscular atrophy: a trinucleotide-repeat expansion neurodegenerative disease. Trends Neurosci. 1995, 18:459-461.
14. Brooks B.P., et al. A cell culture model for androgen effects in motor neurons. J. Neurochem. 1998, 70:1054-1060.
15. Cappelletti G., et al. Neuritin (cpg15) enhances the differentiating effect of NGF on neuronal PC12 cells. J. Neurosci. Res. 2007, 85:2702-2713.
16. Carra S., et al. HspB8, a small heat shock protein mutated in human neuromuscular disorders, has in vivo chaperone activity in cultured cells. Hum. Mol. Genet. 2005, 14:1659-1669.
17. Carra S., et al. HspB8 chaperone activity toward poly(Q)-containing proteins depends on its association with Bag3, a stimulator of macroautophagy. J. Biol. Chem. 2008, 283:1437-1444.
18. Carra S., et al. HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 2008, 4:237-239.
19. Chevalier-Larsen E.S., et al. Castration restores function and neurofilament alterations of aged symptomatic males in a transgenic mouse model of spinal and bulbar muscular atrophy. J. Neurosci. 2004, 24:4778-4786.
20. Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell 1994, 79:13-21.
21. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
22. Crippa V., et al. The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS). Hum. Mol. Genet. 2010, 19:3440-3456.
23. Dondi D. Estrogen receptor beta and the progression of prostate cancer: role of 5{alpha}-androstane-3{beta}, 17{beta}-diol (3{beta}-Adiol). Endocrine-related cancer. Endocr. Relat. Cancer 2010, 17:731-742.
24. Drengler S.M., et al. Regulation of androgen receptor mRNA expression in hamster facial motoneurons: differential effects of non-aromatizable and aromatizable androgens. Brain Res. Mol. Brain Res. 1996, 41:8-15.
25. Fischbeck K.H. Kennedy disease. J. Inher. Metab. Dis. 1997, 20:152-158.
26. Fischbeck K.H. Polyglutamine expansion neurodegenerative disease. Brain Res. Bull. 2001, 56:161-163.
27. Fontanella B., et al. The co-chaperone BAG3 interacts with the cytosolic chaperonin CCT: new hints for actin folding. Int. J. Biochem. Cell Biol. 2010, 42:641-650.
28. Forger N.G., et al. Regulation of motoneuron death in the spinal nucleus of the bulbocavernosus. J. Neurobiol. 1992, 23:1192-1203.
29. Freeman L.M., et al. Distribution of androgen receptor immunoreactivity in the spinal cord of wild-type, androgen-insensitive and gonadectomized male rats. J. Neurobiol. 1995, 27:51-59.
30. Fuchs M., et al. Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochem. J. 2010, 425:245-255.
31. Garcia-Arencibia M., et al. Autophagy, a guardian against neurodegeneration. Semin. Cell Dev. Biol. 2010.
32. Guerini V., et al. The androgen derivative 5alpha-androstane-3beta, 17beta-diol inhibits prostate cancer cell migration through activation of the estrogen receptor beta subtype. Cancer Res. 2005, 65:5445-5453.
33. Hafezparast M., et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 2003, 300:808-812.
34. Hamson D.K., et al. Time course of adult castration-induced changes in soma size of motoneurons in the rat spinal nucleus of the bulbocavernosus. Neurosci. Lett. 2009, 454:148-151.
35. Hamson D.K., et al. The testosterone two-step is really a minuet. Neuron 2010, 66:167-169.
36. Holmberg C.I., et al. Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO J. 2004, 23:4307-4318.
37. Johnston J.A., et al. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskeleton 2002, 53:26-38.
38. Jordan C.L., et al. Androgen receptor messenger RNA and protein in adult rat sciatic nerve: implications for site of androgen action. J. Neurosci. Res. 2002, 69:509-518.
39. Katsuno M., et al. Testosterone reduction prevents phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Neuron 2002, 35:843-854.
40. Katsuno M., et al. Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat. Med. 2003, 9:768-773.
41. Katsuno M., et al. Reversible disruption of dynactin 1-mediated retrograde axonal transport in polyglutamine-induced motor neuron degeneration. J. Neurosci. 2006, 26:12106-12117.
42. Kennedy W.R., et al. Progressive proximal spinal and bulbar muscular atrophy of late onset. A sex-linked recessive trait. Neurol. 1968, 18:671-680.
43. Kobayashi Y., et al. Chaperones Hsp70 and Hsp40 suppress aggregate formation and apoptosis in cultured neuronal cells expressing truncated androgen receptor protein with expanded polyglutamine tract. J. Biol. Chem. 2000, 275:8772-8778.
44. Kujawa K.A., et al. Testosterone regulation of the regenerative properties of injured rat sciatic motor neurons. J. Neurosci. Res. 1993, 35:268-273.
45. Kurz E.M., et al. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 1986, 232:395-398.
46. La Spada A.R., et al. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 1991, 352:77-79.
47. Lamb D.J., et al. Androgen receptors and their biology. Vitam. Horm. 2001, 62:199-230.
48. Larkowski T.D., et al. Androgen receptor mRNA regulation in adult male and female hamster facial motoneurons: effects of axotomy and exogenous androgens. J. Neurobiol. 2000, 45:207-214.
49. Lazarov O., et al. Impairments in fast axonal transport and motor neuron deficits in transgenic mice expressing familial Alzheimer's disease-linked mutant presenilin 1. J. Neurosci. 2007, 27:7011-7020.
50. Lee J.Y., et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29:969-980.
51. Li M., et al. Nonneural nuclear inclusions of androgen receptor protein in spinal and bulbar muscular atrophy. Am. J. Pathol. 1998, 153:695-701.
52. Li M., et al. Soluble androgen receptor oligomers underlie pathology in a mouse model of SBMA. J. Biol. Chem. 2007, 282:3157-3164.
53. Li X., et al. Intracellular degradation of misfolded proteins in polyglutamine neurodegenerative diseases. Brain Res. Rev. 2008, 59:245-252.
54. Lieberman A.P., et al. Altered transcriptional regulation in cells expressing the expanded polyglutamine androgen receptor. Hum. Mol. Genet. 2002, 11:1967-1976.
55. Marron T.U., et al. Androgen-induced neurite outgrowth is mediated by neuritin in motor neurones. J. Neurochem. 2005, 92:10-20.
56. Matsumoto A. Hormonally induced neuronal plasticity in the adult motoneurons. Brain Res. Bull. 1997, 44:539-547.
57. Matsumoto A., et al. Androgen regulates synaptic input to motoneurones of the adult rat spinal cord. J. Neurosci. 1988, 8:4168-4176.
58. Merry D.E., et al. Cleavage, aggregation and toxicity of the expanded androgen receptor in spinal and bulbar muscular atrophy. Hum. Mol. Genet. 1998, 7:693-701.
59. Mizushima N., et al. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
60. Mizushima N., et al. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
61. Montie H.L., Merry D.E. Autophagy and access: understanding the role of androgen receptor subcellular localization in SBMA. Autophagy 2009, 5:1194-1197.
62. Montie H.L., et al. Cytoplasmic retention of polyglutamine-expanded androgen receptor ameliorates disease via autophagy in a mouse model of spinal and bulbar muscular atrophy. Hum. Mol. Genet. 2009, 18:1937-1950.
63. Morfini G., et al. JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat. Neurosci. 2006, 9:907-916.
64. Morishima Y., et al. CHIP deletion reveals functional redundancy of E3 ligases in promoting degradation of both signaling proteins and expanded glutamine proteins. Hum. Mol. Genet. 2008, 17:3942-3952.
65. Nedelsky N.B., et al. Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim. Biophys. Acta 2008, 1782:691-699.
66. Nixon R.A., et al. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 2005, 64:113-122.
67. Nordeen E.J., et al. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 1985, 229:671-673.
68. Ozanne D.M., et al. Androgen receptor nuclear translocation is facilitated by the f-actin cross-linking protein filamin. Mol. Endocrinol. 2000, 14:1618-1626.
69. Palazzolo I., et al. Overexpression of IGF-1 in muscle attenuates disease in a mouse model of spinal and bulbar muscular atrophy. Neuron 2009, 63:316-328.
70. Pandey U.B., et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
71. Pennuto M., et al. Post-translational modifications of expanded polyglutamine proteins: impact on neurotoxicity. Hum. Mol. Genet. 2009, 18:R40-R47.
72. Perutz M.F., et al. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S.A. 1994, 91:5355-5358.
73. Perutz M.F., et al. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. U. S.A. 2002, 99:5591-5595.
74. Piccioni F., et al. Androgen receptor with elongated polyglutamine tract forms aggregates that alter axonal trafficking and mitochondrial distribution in motor neuronal processes. FASEB J. 2002, 160:1418-1420.
75. Piccioni F., et al. Polyglutamine tract expansion of the androgen receptor in a motoneuronal model of spinal and bulbar muscular atrophy. Brain Res. Bull. 2001, 56:215-220.
76. Poletti A. The polyglutamine tract of androgen receptor: from functions to dysfunctions in motor neurons. Front. Neuroendocrinol. 2004, 25:1-26.
77. Poletti A., Martini L. Androgen-activating enzymes in the central nervous system. J. Steroid Biochem. Mol. Biol. 1999, 69:117-122.
78. Poletti A., et al. Steroid binding and metabolism in the luteinizing hormone-releasing hormone-producing neuronal cell line GT1-1. Endocrinology 1994, 135:2623-2638.
79. Poletti A., et al. Expression of androgen-activating enzymes in cultured cells of developing rat brain. J. Neurochem. 1997, 68:1298-1303.
80. Poletti A., et al. The 5alpha-reductase isozymes in the central nervous system. Steroids 1998, 63:246-251.
81. Poletti A., et al. 5alpha-reductase type 2 and androgen receptor expression in gonadotropin releasing hormone GT1-1 cells. J. Neuroendocrinol. 2001, 13:353-357.
82. Poletti A., et al. Reflections on the diseases linked to mutations of the androgen receptor. Endocr. 2005, 28:243-262.
83. Pozzi P., et al. Androgen 5-alpha-reductase type 2 is highly expressed and active in rat spinal cord motor neurones. J. Neuroendocrinol. 2003, 15:882-887.
84. Ranganathan S., et al. Mitochondrial abnormalities in spinal and bulbar muscular atrophy. Hum. Mol. Genet. 2009, 18:27-42.
85. Ravikumar B., et al. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 2002, 11:1107-1117.
86. Ravikumar B., et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 2004, 36:585-595.
87. Ravikumar B., et al. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet. 2005, 37:771-776.
88. Ross C.A. Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 2002, 35:819-822.
89. Ross C.A., Poirier M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 2004, 10(Suppl):S10-S17.
90. Rubinsztein D.C., et al. In search of an "autophagomometer". Autophagy 2009, 5:585-589.
91. Rusmini P., et al. Aggregation and proteasome: the case of elongated polyglutamine aggregation in spinal and bulbar muscular atrophy. Neurobiol. Aging 2007, 28:1099-1111.
92. Sakamoto H., et al. Androgen regulates the sexually dimorphic gastrin-releasing peptide system in the lumbar spinal cord that mediates male sexual function. Endocrinology 2009, 150:3672-3679.
93. Sau D., et al. Mutation of SOD1 in ALS: a gain of a loss of function. Hum. Mol. Genet. 2007, 16:1604-1618.
94. Schmidt B.J., et al. Expression of X-linked bulbospinal muscular atrophy (Kennedy disease) in two homozygous women. Neurology 2002, 59:770-772.
95. Simeoni S., et al. Motoneuronal cell death is not correlated with aggregate formation of androgen receptors containing an elongated polyglutamine tract. Hum. Mol. Genet. 2000, 9:133-144.
96. Sobue G., et al. X-linked recessive bulbospinal neuronopathy. A clinicopathological study. Brain 1989, 112:209-232.
97. Stenoien D.L., et al. Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum. Mol. Genet. 1999, 8:731-741.
98. Szebenyi G., et al. Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport. Neuron 2003, 40:41-52.
99. Takeyama K., et al. Androgen-dependent neurodegeneration by polyglutamine-expanded human androgen receptor in Drosophila. Neuron 2002, 35:855-864.
100. Taylor J.P., et al. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 2003, 12:749-757.
101. Taylor J.P., et al. Aberrant histone acetylation, altered transcription, and retinal degeneration in a Drosophila model of polyglutamine disease are rescued by CREB-binding protein. Genes Dev. 2003, 17:1463-1468.
102. Thomas M., et al. Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction. Hum. Mol. Genet. 2006, 15:1876-1883.
103. Tokui K., et al. 17-DMAG ameliorates polyglutamine-mediated motor neuron degeneration through well-preserved proteasome function in an SBMA model mouse. Hum. Mol. Genet. 2009, 18:898-910.
104. Vismara G., et al. Androgens inhibit androgen receptor promoter activation in motor neurons. Neurobiol. Dis. 2009, 33:395-404.
105. von Mikecz A. PolyQ fibrillation in the cell nucleus: who's bad?. Trends Cell Biol. 2009, 19:685-691.
106. Walcott J.L., Merry D.E. Ligand promotes intranuclear inclusions in a novel cell model of spinal and bulbar muscular atrophy. J. Biol. Chem. 2002, 277:50855-50859.
107. Watson N.V., et al. Neuronal size in the spinal nucleus of the bulbocavernosus: direct modulation by androgen in rats with mosaic androgen insensitivity. J. Neurosci. 2001, 21:1062-1066.
108. Waza M., et al. 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat. Med. 2005, 11:1088-1095.
109. Waza M., et al. Modulation of Hsp90 function in neurodegenerative disorders: a molecular-targeted therapy against disease-causing protein. J. Mol. Med. 2006, 84:635-646.
110. Webb J.L., et al. alpha-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 2003, 278:25009-25013.
111. Williams A.J., Paulson H.L. Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci. 2008, 31:521-528.
112. Xie Z., Klionsky D.J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 2007, 9:1102-1109.
113. Yu W.A. Administration of testosterone attenuates neuronal loss following axotomy in the brain-stem nuclei of female rats. J. Neurosci. 1989, 9:3908-3914.
114. Yu Z., et al. Abnormalities of germ cell maturation and Sertoli cell cytoskeleton in androgen receptor 113 CAG knock-in mice reveal toxic effects of the mutant protein. Am. J. Pathol. 2006, 168:195-204.
115. Zuloaga D.G., et al. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm. Behav. 2008, 53:613-626.