The Ubiquitinated Axon: Local Control of Axon Development and Function by Ubiquitin

Overview

Journal J Neurosci

Specialty Neurology

Date 2021 Apr 1

PMID 33789876

Citations 7

Authors

Maria J Pinto

Diogo Tome

Ramiro D Almeida

Affiliations

Soon will be listed here.

Abstract

Ubiquitin tagging sets protein fate. With a wide range of possible patterns and reversibility, ubiquitination can assume many shapes to meet specific demands of a particular cell across time and space. In neurons, unique cells with functionally distinct axons and dendrites harboring dynamic synapses, the ubiquitin code is exploited at the height of its power. Indeed, wide expression of ubiquitination and proteasome machinery at synapses, a diverse brain ubiquitome, and the existence of ubiquitin-related neurodevelopmental diseases support a fundamental role of ubiquitin signaling in the developing and mature brain. While special attention has been given to dendritic ubiquitin-dependent control, how axonal biology is governed by this small but versatile molecule has been considerably less discussed. Herein, we set out to explore the ubiquitin-mediated spatiotemporal control of an axon's lifetime: from its differentiation and growth through presynaptic formation, function, and pruning.

Citing Articles

Ubiquitination contributes to the regulation of GDP-mannose pyrophosphorylase B activity.

Franzka P, Mittag S, Chakraborty A, Huber O, Hubner C Front Mol Neurosci. 2024; 17:1375297.

PMID: 38979475 PMC: 11228364. DOI: 10.3389/fnmol.2024.1375297.

Ubiquitin system mutations in neurological diseases.

Zenge C, Ordureau A Trends Biochem Sci. 2024; 49(10):875-887.

PMID: 38972780 PMC: 11455613. DOI: 10.1016/j.tibs.2024.06.011.

E3 Ubiquitin Ligase Knockout Reveals a Critical Role in Social Behavior and Synaptic Plasticity in the Hippocampus.

Zhuang Y, Li C, Zhao F, Yan Y, Pan H, Zhan J Int J Mol Sci. 2024; 25(3).

PMID: 38338822 PMC: 10855348. DOI: 10.3390/ijms25031543.

Ubiquitin-specific peptidases: Players in bone metabolism.

Shen J, Lin X, Dai F, Chen G, Lin H, Fang B Cell Prolif. 2023; 56(8):e13444.

PMID: 36883930 PMC: 10392067. DOI: 10.1111/cpr.13444.

Immune Evasion and Drug Resistance Mediated by USP22 in Cancer: Novel Targets and Mechanisms.

Guo J, Zhao J, Fu W, Xu Q, Huang D Front Immunol. 2022; 13:918314.

PMID: 35935969 PMC: 9347222. DOI: 10.3389/fimmu.2022.918314.

References

Hall A, LUCAS F, Salinas P . Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell. 2000; 100(5):525-35. DOI: 10.1016/s0092-8674(00)80689-3. View

Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E . The ubiquitin pathway in Parkinson's disease. Nature. 1998; 395(6701):451-2. DOI: 10.1038/26652. View

Wilson S, Bhattacharyya B, Rachel R, Coppola V, Tessarollo L, Householder D . Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat Genet. 2002; 32(3):420-5. DOI: 10.1038/ng1006. View

Yan D, Guo L, Wang Y . Requirement of dendritic Akt degradation by the ubiquitin-proteasome system for neuronal polarity. J Cell Biol. 2006; 174(3):415-24. PMC: 2064237. DOI: 10.1083/jcb.200511028. View

Opperman K, Grill B . RPM-1 is localized to distinct subcellular compartments and regulates axon length in GABAergic motor neurons. Neural Dev. 2014; 9:10. PMC: 4077836. DOI: 10.1186/1749-8104-9-10. View

Koo B, Spit M, Jordens I, Low T, Stange D, van de Wetering M . Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature. 2012; 488(7413):665-9. DOI: 10.1038/nature11308. View

Kimura Y, Yashiroda H, Kudo T, Koitabashi S, Murata S, Kakizuka A . An inhibitor of a deubiquitinating enzyme regulates ubiquitin homeostasis. Cell. 2009; 137(3):549-59. DOI: 10.1016/j.cell.2009.02.028. View

Tai H, Schuman E . Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat Rev Neurosci. 2008; 9(11):826-38. DOI: 10.1038/nrn2499. View

Dupraz S, Grassi D, Karnas D, Nieto Guil A, Hicks D, Quiroga S . The insulin-like growth factor 1 receptor is essential for axonal regeneration in adult central nervous system neurons. PLoS One. 2013; 8(1):e54462. PMC: 3548777. DOI: 10.1371/journal.pone.0054462. View

10.

Yuasa-Kawada J, Kinoshita-Kawada M, Wu G, Rao Y, Wu J . Midline crossing and Slit responsiveness of commissural axons require USP33. Nat Neurosci. 2009; 12(9):1087-9. PMC: 3893063. DOI: 10.1038/nn.2382. View

11.

Zhu Q, Dong H, Bukhari A, Zhao A, Li M, Sun Y . HUWE1 promotes EGFR ubiquitination and degradation to protect against renal tubulointerstitial fibrosis. FASEB J. 2020; 34(3):4591-4601. DOI: 10.1096/fj.201902751R. View

12.

Powis R, Karyka E, Boyd P, Come J, Jones R, Zheng Y . Systemic restoration of UBA1 ameliorates disease in spinal muscular atrophy. JCI Insight. 2016; 1(11):e87908. PMC: 5033939. DOI: 10.1172/jci.insight.87908. View

13.

Lowe J, Blanchard A, Morrell K, Lennox G, Reynolds L, Billett M . Ubiquitin is a common factor in intermediate filament inclusion bodies of diverse type in man, including those of Parkinson's disease, Pick's disease, and Alzheimer's disease, as well as Rosenthal fibres in cerebellar astrocytomas, cytoplasmic.... J Pathol. 1988; 155(1):9-15. DOI: 10.1002/path.1711550105. View

14.

Kowalski J, Dube H, Touroutine D, Rush K, Goodwin P, Carozza M . The Anaphase-Promoting Complex (APC) ubiquitin ligase regulates GABA transmission at the C. elegans neuromuscular junction. Mol Cell Neurosci. 2013; 58:62-75. PMC: 4036811. DOI: 10.1016/j.mcn.2013.12.001. View

15.

Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M . FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell. 2009; 136(1):123-35. DOI: 10.1016/j.cell.2008.10.051. View

16.

Liani E, Eyal A, Avraham E, Shemer R, Szargel R, Berg D . Ubiquitylation of synphilin-1 and alpha-synuclein by SIAH and its presence in cellular inclusions and Lewy bodies imply a role in Parkinson's disease. Proc Natl Acad Sci U S A. 2004; 101(15):5500-5. PMC: 397412. DOI: 10.1073/pnas.0401081101. View

17.

Bao H, Reist N, Zhang B . The Drosophila epsin 1 is required for ubiquitin-dependent synaptic growth and function but not for synaptic vesicle recycling. Traffic. 2008; 9(12):2190-205. DOI: 10.1111/j.1600-0854.2008.00832.x. View

18.

Saigoh K, Wang Y, Suh J, Yamanishi T, Sakai Y, Kiyosawa H . Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet. 1999; 23(1):47-51. DOI: 10.1038/12647. View

19.

Artinian J, McGauran A, De Jaeger X, Mouledous L, Frances B, Roullet P . Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur J Neurosci. 2008; 27(11):3009-19. DOI: 10.1111/j.1460-9568.2008.06262.x. View

20.

Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore P, Dikic I . Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol. 2003; 5(5):461-6. DOI: 10.1038/ncb983. View