CHIP as a therapeutic target for neurological diseases.


Journal

Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092

Informations de publication

Date de publication:
09 09 2020
Historique:
received: 10 05 2020
accepted: 27 08 2020
revised: 16 08 2020
entrez: 10 9 2020
pubmed: 11 9 2020
medline: 28 4 2021
Statut: epublish

Résumé

Carboxy-terminus of Hsc70-interacting protein (CHIP) functions both as a molecular co-chaperone and ubiquitin E3 ligase playing a critical role in modulating the degradation of numerous chaperone-bound proteins. To date, it has been implicated in the regulation of numerous biological functions, including misfolded-protein refolding, autophagy, immunity, and necroptosis. Moreover, the ubiquitous expression of CHIP in the central nervous system suggests that it may be implicated in a wide range of functions in neurological diseases. Several recent studies of our laboratory and other groups have highlighted the beneficial role of CHIP in the pathogenesis of several neurological diseases. The objective of this review is to discuss the possible molecular mechanisms that contribute to the pathogenesis of neurological diseases in which CHIP has a pivotal role, such as stroke, intracerebral hemorrhage, Alzheimer's disease, Parkinson's disease, and polyglutamine diseases; furthermore, CHIP mutations could also cause neurodegenerative diseases. Based on the available literature, CHIP overexpression could serve as a promising therapeutic target for several neurological diseases.

Identifiants

pubmed: 32908122
doi: 10.1038/s41419-020-02953-5
pii: 10.1038/s41419-020-02953-5
pmc: PMC7481199
doi:

Substances chimiques

STUB1 protein, human EC 2.3.2.27
Ubiquitin-Protein Ligases EC 2.3.2.27

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

727

Références

Amm, I., Sommer, T. & Wolf, D. H. Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim. Biophys. Acta 1843, 182–196 (2014).
pubmed: 23850760
Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M. & Hartl, F. U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323–355 (2013).
pubmed: 23746257
Ballinger, C. A. et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 19, 4535–4545 (1999).
pubmed: 10330192 pmcid: 104411
Connell, P. et al. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat. cell Biol. 3, 93–96 (2001).
pubmed: 11146632
Zhang, M. et al. Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. cell 20, 525–538 (2005).
pubmed: 16307917
McDonough, H. & Patterson, C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8, 303–308 (2003).
pubmed: 514901 pmcid: 514901
Cyr, D. M., Hohfeld, J. & Patterson, C. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27, 368–375 (2002).
pubmed: 12114026
Esser, C., Alberti, S. & Hohfeld, J. Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim. Biophys. Acta 1695, 171–188 (2004).
pubmed: 15571814
Tawo, R. et al. The Ubiquitin ligase CHIP integrates proteostasis and aging by regulation of insulin receptor turnover. Cell 169, 470–482.e413 (2017).
pubmed: 28431247 pmcid: 5406386
Seo, J. et al. CHIP controls necroptosis through ubiquitylation- and lysosome-dependent degradation of RIPK3. Nat. Cell Biol. 18, 291–302 (2016).
pubmed: 26900751
Sha, Y., Rao, L., Settembre, C., Ballabio, A. & Eissa, N. T. STUB1 regulates TFEB-induced autophagy-lysosome pathway. EMBO J. 36, 2544–2552 (2017).
pubmed: 28754656 pmcid: 5579343
Rinaldi, L. et al. Feedback inhibition of cAMP effector signaling by a chaperone-assisted ubiquitin system. Nat. Commun. 10, 2572 (2019).
pubmed: 31189917 pmcid: 6561907
Shi, C. H. et al. Disrupted structure and aberrant function of CHIP mediates the loss of motor and cognitive function in preclinical models of SCAR16. PloS Genet. 14, e1007664 (2018).
pubmed: 30222779 pmcid: 6160236
Pakdaman, Y. et al. In vitro characterization of six STUB1 variants in spinocerebellar ataxia 16 reveals altered structural properties for the encoded CHIP proteins. Biosci. Rep. 37, BSR20170251 (2017).
Kanack, A. J., Newsom, O. J. & Scaglione, K. M. Most mutations that cause spinocerebellar ataxia autosomal recessive type 16 (SCAR16) destabilize the protein quality-control E3 ligase CHIP. J. Biol. Chem. 293, 2735–2743 (2018).
pubmed: 29317501 pmcid: 5827432
Feigin, V. L., Lawes, C. M., Bennett, D. A., Barker-Collo, S. L. & Parag, V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. Lancet Neurol. 8, 355–369 (2009).
pubmed: 19233729
Sacco, S., Marini, C., Toni, D., Olivieri, L. & Carolei, A. Incidence and 10-year survival of intracerebral hemorrhage in a population-based registry. Stroke 40, 394–399 (2009).
pubmed: 19038914
Balami, J. S. & Buchan, A. M. Complications of intracerebral haemorrhage. Lancet Neurol. 11, 101–118 (2012).
pubmed: 22172625
Qureshi, A. I., Mendelow, A. D. & Hanley, D. F. Intracerebral haemorrhage. Lancet 373, 1632–1644 (2009).
pubmed: 19427958 pmcid: 3138486
Aronowski, J. & Zhao, X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke 42, 1781–1786 (2011).
pubmed: 21527759 pmcid: 3123894
Liang, X. et al. Necroptosis, a novel form of caspase-independent cell death, contributes to renal epithelial cell damage in an ATP-depleted renal ischemia model. Mol. Med. Rep. 10, 719–724 (2014).
pubmed: 24842629
Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112–119 (2005).
pubmed: 16408008
Grootjans, S., Vanden Berghe, T. & Vandenabeele, P. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ. 24, 1184–1195 (2017).
pubmed: 28498367 pmcid: 5520172
Su, X. et al. Necrostatin-1 ameliorates intracerebral hemorrhage-induced brain injury in mice through inhibiting RIP1/RIP3 pathway. Neurochem. Res. 40, 643–650 (2015).
pubmed: 25576092
Shen, H. et al. Role for RIP1 in mediating necroptosis in experimental intracerebral hemorrhage model both in vivo and in vitro. Cell Death Dis. 8, e2641 (2017).
pubmed: 28252651 pmcid: 5386555
Zhang, S. et al. AAV/BBB-mediated gene transfer of CHIP attenuates brain injury following experimental intracerebral hemorrhage. Transl. stroke Res. 11, 296–309 (2020).
pubmed: 31325153
Shinohara, Y. et al. Effects of neutralizing antibody production on AAV-PHP.B-mediated transduction of the mouse central nervous system. Mol. Neurobiol. 56, 4203–4214 (2019).
pubmed: 30291583
Cheng, X. et al. Exploring the potential value of miR-148b-3p, miR-151b and miR-27b-3p as biomarkers in acute ischemic stroke. Biosci. Rep. 38, BSR20181033 (2018).
Vieira, M. et al. Ischemic insults induce necroptotic cell death in hippocampal neurons through the up-regulation of endogenous RIP3. Neurobiol. Dis. 68, 26–36 (2014).
pubmed: 24746856
Tang, M. B. et al. Anisomycin prevents OGD-induced necroptosis by regulating the E3 ligase CHIP. Sci. Rep. 8, 6379 (2018).
pubmed: 29686306 pmcid: 5913227
Anderson, L. G., Meeker, R. B., Poulton, W. E. & Huang, D. Y. Brain distribution of carboxy terminus of Hsc70-interacting protein (CHIP) and its nuclear translocation in cultured cortical neurons following heat stress or oxygen-glucose deprivation. Cell Stress Chaperones 15, 487–495 (2010).
pubmed: 19953350
Palubinsky, A. M. et al. CHIP is an essential determinant of neuronal mitochondrial stress signaling. Antioxid. Redox Signal. 23, 535–549 (2015).
pubmed: 25602369 pmcid: 4544748
Stankowski, J. N. et al. C-terminus of heat shock cognate 70 interacting protein increases following stroke and impairs survival against acute oxidative stress. Antioxid. Redox Signal. 14, 1787–1801 (2011).
pubmed: 20677910 pmcid: 3078511
Cabral-Miranda, F. et al. rAAV8-733-mediated gene transfer of CHIP/Stub-1 prevents hippocampal neuronal death in experimental brain ischemia. Mol. Ther. 25, 392–400 (2017).
pubmed: 28153090
Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119–131 (2010).
pubmed: 20098416
Geisler, S. et al. The PINK1/Parkin-mediated mitophagy is compromised by PD-associated mutations. Autophagy 6, 871–878 (2010).
pubmed: 20798600
Narendra, D. P. & Youle, R. J. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid. Redox Signal. 14, 1929–1938 (2011).
pubmed: 21194381 pmcid: 3078490
Ghosh, D., Mehra, S., Sahay, S., Singh, P. K. & Maji, S. K. alpha-synuclein aggregation and its modulation. Int. J. Biol. Macromol. 100, 37–54 (2017).
pubmed: 27737778
Mehra, S., Sahay, S. & Maji, S. K. α-Synuclein misfolding and aggregation: Implications in Parkinson’s disease pathogenesis. Biochim. Biophys. Acta Proteins Proteom. 1867, 890–908 (2019).
pubmed: 30853581
Shin, Y., Klucken, J., Patterson, C., Hyman, B. T. & McLean, P. J. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J. Biol. Chem. 280, 23727–23734 (2005).
pubmed: 15845543
Tetzlaff, J. E. et al. CHIP targets toxic alpha-Synuclein oligomers for degradation. J. Biol. Chem. 283, 17962–17968 (2008).
pubmed: 18436529 pmcid: 2936239
Kalia, L. V. et al. Ubiquitinylation of alpha-synuclein by carboxyl terminus Hsp70-interacting protein (CHIP) is regulated by Bcl-2-associated athanogene 5 (BAG5). PloS ONE 6, e14695 (2011).
pubmed: 21358815 pmcid: 3040167
Zimprich, A. et al. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44, 601–607 (2004).
pubmed: 15541309
Valente, E. M. et al. Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304, 1158–1160 (2004).
pubmed: 15087508
Kitada, T. et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605–608 (1998).
pubmed: 9560156
Tolosa, E., Vila, M., Klein, C. & Rascol, O. LRRK2 in Parkinson disease: challenges of clinical trials. Nature reviews. Nat. Rev. Neurol. 16, 97–107 (2020).
pubmed: 31980808
Ko, H. S. et al. CHIP regulates leucine-rich repeat kinase-2 ubiquitination, degradation, and toxicity. Proc. Natl Acad. Sci. USA 106, 2897–2902 (2009).
pubmed: 19196961
Ding, X. & Goldberg, M. S. Regulation of LRRK2 stability by the E3 ubiquitin ligase CHIP. PloS ONE 4, e5949 (2009).
pubmed: 19536328 pmcid: 2694275
Funayama, M. et al. Leucine-rich repeat kinase 2 G2385R variant is a risk factor for Parkinson disease in Asian population. Neuroreport 18, 273–275 (2007).
pubmed: 17314670
Rudenko, I. N. et al. The G2385R variant of leucine-rich repeat kinase 2 associated with Parkinson’s disease is a partial loss-of-function mutation. Biochem. J. 446, 99–111 (2012).
pubmed: 22612223 pmcid: 4667980
Rudenko, I. N. et al. The G2385R risk factor for Parkinson’s disease enhances CHIP-dependent intracellular degradation of LRRK2. Biochem. J. 474, 1547–1558 (2017).
pubmed: 28320779 pmcid: 6178381
Morett, E. & Bork, P. A novel transactivation domain in parkin. Trends Biochem. Sci. 24, 229–231 (1999).
pubmed: 10366851
Imai, Y. et al. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105, 891–902 (2001).
pubmed: 11439185
Imai, Y. et al. CHIP is associated with Parkin, a gene responsible for familial Parkinson’s disease, and enhances its ubiquitin ligase activity. Mol. cell 10, 55–67 (2002).
pubmed: 12150907
Yoo, L. & Chung, K. C. The ubiquitin E3 ligase CHIP promotes proteasomal degradation of the serine/threonine protein kinase PINK1 during staurosporine-induced cell death. J. Biol. Chem. 293, 1286–1297 (2018).
pubmed: 29242192
Chen, J. et al. Drosophila CHIP protects against mitochondrial dysfunction by acting downstream of Pink1 in parallel with Parkin. FASEB J. 31, 5234–5245 (2017).
pubmed: 28778978
Oboudiyat, C., Glazer, H., Seifan, A., Greer, C. & Isaacson, R. S. Alzheimer’s disease. Semin. Neurol. 33, 313–329 (2013).
pubmed: 24234352
Harris, L. D., Jasem, S. & Licchesi, J. D. F. The Ubiquitin system in Alzheimer’s disease. Adv. Exp. Med. Biol. 1233, 195–221 (2020).
pubmed: 32274758
Spires-Jones, T. L., Stoothoff, W. H., de Calignon, A., Jones, P. B. & Hyman, B. T. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci. 32, 150–159 (2009).
pubmed: 19162340
Mandelkow, E. M. & Mandelkow, E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb. Perspect. Med. 2, a006247 (2012).
pubmed: 22762014 pmcid: 3385935
Dolan, P. J. & Johnson, G. V. A caspase cleaved form of tau is preferentially degraded through the autophagy pathway. J. Biol. Chem. 285, 21978–21987 (2010).
pubmed: 20466727 pmcid: 2903354
Dickey, C. A. et al. Akt and CHIP coregulate tau degradation through coordinated interactions. Proc. Natl Acad. Sci. USA 105, 3622–3627 (2008).
pubmed: 18292230
Saidi, L. J. et al. Carboxy terminus heat shock protein 70 interacting protein reduces tau-associated degenerative changes. J. Alzheimer’s Dis. 44, 937–947 (2015).
Shimura, H., Schwartz, D., Gygi, S. P. & Kosik, K. S. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J. Biol. Chem. 279, 4869–4876 (2004).
pubmed: 14612456
Goryunov, D. & Liem, R. K. CHIP-ping away at tau. J. Clin. Investig. 117, 590–592 (2007).
pubmed: 17332887
Dickey, C. A. et al. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J. Clin. Investig. 117, 648–658 (2007).
pubmed: 17304350
Sahara, N. et al. In vivo evidence of CHIP up-regulation attenuating tau aggregation. J. Neurochem. 94, 1254–1263 (2005).
pubmed: 16111477
Lee, S. et al. Sulforaphane upregulates the heat shock protein co-chaperone CHIP and clears amyloid-beta and Tau in a mouse model of Alzheimer’s Disease. Mol. Nutr. food Res. 62, e1800240 (2018).
pubmed: 29714053
Murphy, M. P. & LeVine, H. 3rd Alzheimer’s disease and the amyloid-beta peptide. J. Alzheimer’s Dis. 19, 311–323 (2010).
Li, Y., Zhou, W., Tong, Y., He, G. & Song, W. Control of APP processing and Abeta generation level by BACE1 enzymatic activity and transcription. FASEB J. 20, 285–292 (2006).
pubmed: 16449801
Cai, H. et al. BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat. Neurosci. 4, 233–234 (2001).
pubmed: 11224536
Del Prete, D., Rice, R. C., Rajadhyaksha, A. M. & D’Adamio, L. Amyloid Precursor Protein (APP) may act as a substrate and a recognition unit for CRL4CRBN and Stub1 E3 ligases facilitating ubiquitination of proteins involved in presynaptic functions and neurodegeneration. J. Biol. Chem. 291, 17209–17227 (2016).
pubmed: 27325702 pmcid: 5016122
Kumar, P. et al. CHIP and HSPs interact with beta-APP in a proteasome-dependent manner and influence Abeta metabolism. Hum. Mol. Genet. 16, 848–864 (2007).
pubmed: 17317785
Singh, A. K. & Pati, U. CHIP stabilizes amyloid precursor protein via proteasomal degradation and p53-mediated trans-repression of beta-secretase. Aging Cell 14, 595–604 (2015).
pubmed: 25773675 pmcid: 4531073
Keller, J. N., Hanni, K. B. & Markesbery, W. R. Impaired proteasome function in Alzheimer’s disease. J. Neurochem. 75, 436–439 (2000).
pubmed: 10854289
Bertram, L. et al. Family-based association between Alzheimer’s disease and variants in UBQLN1. N. Engl. J. Med. 352, 884–894 (2005).
pubmed: 15745979
Oddo, S. et al. Blocking Abeta42 accumulation delays the onset and progression of tau pathology via the C terminus of heat shock protein70-interacting protein: a mechanistic link between Abeta and tau pathology. J. Neurosci. 28, 12163–12175 (2008).
pubmed: 19020010 pmcid: 6671718
Meng, Y. et al. Toll-like receptor-2 ligand peptidoglycan upregulates expression and ubiquitin ligase activity of CHIP through JNK pathway. Cell. Physiol. Biochem. 32, 1097–1105 (2013).
pubmed: 24217650
Hiyoshi, H. et al. 2-(4-Hydroxy-3-methoxyphenyl)-benzothiazole suppresses tumor progression and metastatic potential of breast cancer cells by inducing ubiquitin ligase CHIP. Sci. Rep. 4, 7095 (2014).
pubmed: 25403352 pmcid: 4235287
Cheng, X. R. et al. A co-module regulated by therapeutic drugs in a molecular subnetwork of Alzheimer’s disease identified on the basis of traditional chinese medicine and SAMP8 mice. Curr. Alzheimer Res. 12, 870–885 (2015).
pubmed: 26159197
Zhang, G. R., Cheng, X. R., Zhou, W. X. & Zhang, Y. X. Age-related expression of STUB1 in senescence-accelerated mice and its response to anti-Alzheimer’s disease traditional Chinese medicine. Neurosci. Lett. 438, 371–375 (2008).
pubmed: 18495342
Pasinelli, P. & Brown, R. H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7, 710–723 (2006).
pubmed: 16924260
Renton, A. E., Chio, A. & Traynor, B. J. State of play in amyotrophic lateral sclerosis genetics. Nat. Neurosci. 17, 17–23 (2014).
pubmed: 24369373
Valentine, J. S. & Hart, P. J. Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 100, 3617–3622 (2003).
pubmed: 12655070
Urushitani, M. et al. CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J. Neurochem. 90, 231–244 (2004).
pubmed: 15198682
Niwa, J. et al. Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J. Biol. Chem. 277, 36793–36798 (2002).
pubmed: 12145308
Ishigaki, S. et al. Dorfin-CHIP chimeric proteins potently ubiquitylate and degrade familial ALS-related mutant SOD1 proteins and reduce their cellular toxicity. Neurobiol. Dis. 25, 331–341 (2007).
pubmed: 17157513
Niwa, J. et al. A novel centrosomal ring-finger protein, dorfin, mediates ubiquitin ligase activity. Biochem. Biophys. Res. Commun. 281, 706–713 (2001).
pubmed: 11237715
Sakamoto, K. M. et al. Protacs: chimeric molecules that target proteins to the Skp1-Cullin-F box complex for ubiquitination and degradation. Proc. Natl Acad. Sci. USA 98, 8554–8559 (2001).
pubmed: 11438690
Sakamoto, K. M. et al. Development of Protacs to target cancer-promoting proteins for ubiquitination and degradation. Mol. Cell. Proteom. 2, 1350–1358 (2003).
Oyake, D., Nishikawa, H., Koizuka, I., Fukuda, M. & Ohta, T. Targeted substrate degradation by an engineered double RING ubiquitin ligase. Biochem. Biophys. Res. Commun. 295, 370–375 (2002).
pubmed: 12150958
Gusella, J. F. & MacDonald, M. E. Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat. Rev. Neurosci. 1, 109–115 (2000).
pubmed: 11252773
Orr, H. T. & Zoghbi, H. Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575–621 (2007).
pubmed: 17417937
Nagai, Y. & Popiel, H. A. Conformational changes and aggregation of expanded polyglutamine proteins as therapeutic targets of the polyglutamine diseases: exposed beta-sheet hypothesis. Curr. Pharm. Des. 14, 3267–3279 (2008).
pubmed: 19075705
Takeuchi, T. & Nagai, Y. Protein misfolding and aggregation as a therapeutic target for polyglutamine diseases. Brain Res. 7, 128 (2017).
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. 17, 3942–3952 (2008).
pubmed: 18784277 pmcid: 2605787
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. 27, 5115–5126 (2007).
pubmed: 17494697 pmcid: 6672370
Al-Ramahi, I. et al. CHIP protects from the neurotoxicity of expanded and wild-type ataxin-1 and promotes their ubiquitination and degradation. J. Biol. Chem. 281, 26714–26724 (2006).
pubmed: 16831871
Miller, V. M. et al. CHIP suppresses polyglutamine aggregation and toxicity in vitro and in vivo. J. Neurosci. 25, 9152–9161 (2005).
pubmed: 16207874 pmcid: 6725774
Jana, N. R. et al. Co-chaperone CHIP associates with expanded polyglutamine protein and promotes their degradation by proteasomes. J. Biol. Chem. 280, 11635–11640 (2005).
pubmed: 15664989
Choi, J. Y. et al. Co-chaperone CHIP promotes aggregation of ataxin-1. Mol. Cell. Neurosci. 34, 69–79 (2007).
pubmed: 17127076
Williams, A. J., Knutson, T. M., Colomer Gould, V. F. & Paulson, H. L. In vivo suppression of polyglutamine neurotoxicity by C-terminus of Hsp70-interacting protein (CHIP) supports an aggregation model of pathogenesis. Neurobiol. Dis. 33, 342–353 (2009).
pubmed: 19084066
Holmes, G. A form of familial degeneration of the cerebellum. Brain 30, 466–489 (1908).
Shi, C. H. et al. Ataxia and hypogonadism caused by the loss of ubiquitin ligase activity of the U box protein CHIP. Hum. Mol. Genet. 23, 1013–1024 (2014).
pubmed: 24113144
Margolin, D. H. et al. Ataxia, dementia, and hypogonadotropism caused by disordered ubiquitination. N. Engl. J. Med. 368, 1992–2003 (2013).
pubmed: 23656588 pmcid: 3738065
Cordoba, M., Rodriguez-Quiroga, S., Gatto, E. M., Alurralde, A. & Kauffman, M. A. Ataxia plus myoclonus in a 23-year-old patient due to STUB1 mutations. Neurology 83, 287–288 (2014).
pubmed: 24928119
Depondt, C. et al. Autosomal recessive cerebellar ataxia of adult onset due to STUB1 mutations. Neurology 82, 1749–1750 (2014).
pubmed: 24719489
Chiu, H. H. et al. Clinical and genetic characterization of autosomal recessive spinocerebellar Ataxia Type 16 (SCAR16) in Taiwan. Cerebellum 19, 544–549 (2020).
pubmed: 32367277
Olszewska, D. A. & Kinsella, J. A. Extending the phenotypic spectrum associated with STUB1 mutations: a case of dystonia. Mov. Disord. Clin. Pract. 7, 318–324 (2020).
pubmed: 32258232
Shi, Y. et al. Identification of CHIP as a novel causative gene for autosomal recessive cerebellar ataxia. PloS ONE 8, e81884 (2013).
pubmed: 24312598 pmcid: 3846781
Gazulla, J., Izquierdo-Alvarez, S., Sierra-Martinez, E., Marta-Moreno, M. E. & Alvarez, S. Inaugural cognitive decline, late disease onset and novel STUB1 variants in SCAR16. Neurological Sci. 39, 2231–2233 (2018).
Synofzik, M. et al. Phenotype and frequency of STUB1 mutations: next-generation screenings in Caucasian ataxia and spastic paraplegia cohorts. Orphanet J. Rare Dis. 9, 57 (2014).
pubmed: 24742043 pmcid: 4021831
Turkgenc, B. et al. STUB1 polyadenylation signal variant AACAAA does not affect polyadenylation but decreases STUB1 translation causing SCAR16. Hum. Mutat. 39, 1344–1348 (2018).
pubmed: 30058754
Hayer, S. N. et al. STUB1/CHIP mutations cause Gordon Holmes syndrome as part of a widespread multisystemic neurodegeneration: evidence from four novel mutations. Orphanet J. Rare Dis. 12, 31 (2017).
pubmed: 28193273 pmcid: 5307643
Bettencourt, C. et al. Clinical and neuropathological features of spastic Ataxia in a Spanish family with novel compound heterozygous mutations in STUB1. Cerebellum 14, 378–381 (2015).
pubmed: 25592071
Heimdal, K. et al. STUB1 mutations in autosomal recessive ataxias - evidence for mutation-specific clinical heterogeneity. Orphanet J. Rare Dis. 9, 146 (2014).
pubmed: 25258038 pmcid: 4181732
Garcia, A. M. et al. The cerebellum and embodied semantics: evidence from a case of genetic ataxia due to STUB1 mutations. J. Med. Genet. 54, 114–124 (2017).
pubmed: 27811304
Madrigal, S. C. et al. Changes in protein function underlie the disease spectrum in patients with CHIP mutations. J. Biol. Chem. 294, 19236–19245 (2019).
pubmed: 31619515 pmcid: 6916485
Genis, D. et al. Heterozygous STUB1 mutation causes familial ataxia with cognitive affective syndrome (SCA48). Neurology 91, e1988–e1998 (2018).
pubmed: 30381368
Clarkson, Y. L., Gillespie, T., Perkins, E. M., Lyndon, A. R. & Jackson, M. Beta-III spectrin mutation L253P associated with spinocerebellar ataxia type 5 interferes with binding to Arp1 and protein trafficking from the Golgi. Hum. Mol. Genet. 19, 3634–3641 (2010).
pubmed: 20603325 pmcid: 2928133
Lise, S. et al. Recessive mutations in SPTBN2 implicate beta-III spectrin in both cognitive and motor development. PloS Genet. 8, e1003074 (2012).
pubmed: 23236289 pmcid: 3516553
Palvadeau, R. et al. Cerebellar cognitive-affective syndrome preceding ataxia associated with complex extrapyramidal features in a Turkish SCA48 family. Neurogenetics 21, 51–58 (2020).
pubmed: 31741143
Mol, M. O. et al. Clinical and pathologic phenotype of a large family with heterozygous STUB1 mutation. Neurol. Genet. 6, e417 (2020).
pubmed: 32337344 pmcid: 7164971
Chen, D. H. et al. Heterozygous STUB1 missense variants cause ataxia, cognitive decline, and STUB1 mislocalization. Neurol. Genet. 6, 1–13 (2020).
pubmed: 32211513 pmcid: 7073456
De Michele, G. et al. Spinocerebellar ataxia 48 presenting with ataxia associated with cognitive, psychiatric, and extrapyramidal features: a report of two Italian families. Parkinsonism Relat. Disord. 65, 91–96 (2019).
pubmed: 31126790
Lieto, M. et al. The complex phenotype of spinocerebellar ataxia type 48 in eight unrelated Italian families. Eur. J. Neurol. 27, 498–505 (2020).
pubmed: 31571321

Auteurs

Shuo Zhang (S)

Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.
Henan Key Laboratory of Cerebrovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.
Academy of Medical Sciences of Zhengzhou University Translational Medicine platform, 450052, Zhengzhou, Henan, China.

Zheng-Wei Hu (ZW)

Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.
Henan Key Laboratory of Cerebrovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.
Academy of Medical Sciences of Zhengzhou University Translational Medicine platform, 450052, Zhengzhou, Henan, China.

Cheng-Yuan Mao (CY)

Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.
Henan Key Laboratory of Cerebrovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China.

Chang-He Shi (CH)

Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China. shichanghe@gmail.com.
Henan Key Laboratory of Cerebrovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China. shichanghe@gmail.com.

Yu-Ming Xu (YM)

Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China. xuyuming@zzu.edu.cn.
Henan Key Laboratory of Cerebrovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou University, 450000, Zhengzhou, Henan, China. xuyuming@zzu.edu.cn.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH