Regulation of Cellular Ribonucleoprotein Granules: From Assembly to Degradation Via Post-translational Modification

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2022 Jul 9

PMID 35805146

Authors

Pureum Jeon

Hyun-Ji Ham

Semin Park

Jin-A Lee

Affiliations

Soon will be listed here.

Abstract

Cells possess membraneless ribonucleoprotein (RNP) granules, including stress granules, processing bodies, Cajal bodies, or paraspeckles, that play physiological or pathological roles. RNP granules contain RNA and numerous RNA-binding proteins, transiently formed through the liquid-liquid phase separation. The assembly or disassembly of numerous RNP granules is strongly controlled to maintain their homeostasis and perform their cellular functions properly. Normal RNA granules are reversibly assembled, whereas abnormal RNP granules accumulate and associate with various neurodegenerative diseases. This review summarizes current studies on the physiological or pathological roles of post-translational modifications of various cellular RNP granules and discusses the therapeutic methods in curing diseases related to abnormal RNP granules by autophagy.

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References

Naganuma T, Nakagawa S, Tanigawa A, Sasaki Y, Goshima N, Hirose T . Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 2012; 31(20):4020-34. PMC: 3474925. DOI: 10.1038/emboj.2012.251. View

Trcek T, Grosch M, York A, Shroff H, Lionnet T, Lehmann R . Drosophila germ granules are structured and contain homotypic mRNA clusters. Nat Commun. 2015; 6:7962. PMC: 4918342. DOI: 10.1038/ncomms8962. View

Patel A, Lee H, Jawerth L, Maharana S, Jahnel M, Hein M . A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation. Cell. 2015; 162(5):1066-77. DOI: 10.1016/j.cell.2015.07.047. View

Fox A, Lam Y, Leung A, Lyon C, Andersen J, Mann M . Paraspeckles: a novel nuclear domain. Curr Biol. 2002; 12(1):13-25. DOI: 10.1016/s0960-9822(01)00632-7. View

Zhang Y, Gendron T, Ebbert M, ORaw A, Yue M, Jansen-West K . Poly(GR) impairs protein translation and stress granule dynamics in C9orf72-associated frontotemporal dementia and amyotrophic lateral sclerosis. Nat Med. 2018; 24(8):1136-1142. PMC: 6520050. DOI: 10.1038/s41591-018-0071-1. View

Clemson C, Hutchinson J, Sara S, Ensminger A, Fox A, Chess A . An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell. 2009; 33(6):717-26. PMC: 2696186. DOI: 10.1016/j.molcel.2009.01.026. View

Gao M, Arkov A . Next generation organelles: structure and role of germ granules in the germline. Mol Reprod Dev. 2012; 80(8):610-23. PMC: 3584238. DOI: 10.1002/mrd.22115. View

Fox A, Nakagawa S, Hirose T, Bond C . Paraspeckles: Where Long Noncoding RNA Meets Phase Separation. Trends Biochem Sci. 2018; 43(2):124-135. DOI: 10.1016/j.tibs.2017.12.001. View

Li H, Yeh P, Chiu H, Tang C, Tu B . Hyperphosphorylation as a defense mechanism to reduce TDP-43 aggregation. PLoS One. 2011; 6(8):e23075. PMC: 3151276. DOI: 10.1371/journal.pone.0023075. View

10.

Rouhana L, Vieira A, Roberts-Galbraith R, Newmark P . PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development. 2012; 139(6):1083-94. PMC: 3283120. DOI: 10.1242/dev.076182. View

11.

Madhusudan S, Middleton M . The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer. Cancer Treat Rev. 2005; 31(8):603-17. DOI: 10.1016/j.ctrv.2005.09.006. View

12.

Tenekeci U, Poppe M, Beuerlein K, Buro C, Muller H, Weiser H . K63-Ubiquitylation and TRAF6 Pathways Regulate Mammalian P-Body Formation and mRNA Decapping. Mol Cell. 2016; 62(6):943-957. DOI: 10.1016/j.molcel.2016.05.017. View

13.

Saito M, Hess D, Eglinger J, Fritsch A, Kreysing M, Weinert B . Acetylation of intrinsically disordered regions regulates phase separation. Nat Chem Biol. 2018; 15(1):51-61. DOI: 10.1038/s41589-018-0180-7. View

14.

Ayache J, Benard M, Ernoult-Lange M, Minshall N, Standart N, Kress M . P-body assembly requires DDX6 repression complexes rather than decay or Ataxin2/2L complexes. Mol Biol Cell. 2015; 26(14):2579-95. PMC: 4501357. DOI: 10.1091/mbc.E15-03-0136. View

15.

Xie X, Matsumoto S, Endo A, Fukushima T, Kawahara H, Saeki Y . Deubiquitylases USP5 and USP13 are recruited to and regulate heat-induced stress granules through their deubiquitylating activities. J Cell Sci. 2018; 131(8). DOI: 10.1242/jcs.210856. View

16.

Yang S, Jeong J, Brown A, Lee C, Pandolfi P, Chung J . Promyelocytic leukemia activates Chk2 by mediating Chk2 autophosphorylation. J Biol Chem. 2006; 281(36):26645-54. DOI: 10.1074/jbc.M604391200. View

17.

Kim J, Huang W, Stromhaug P, Klionsky D . Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J Biol Chem. 2001; 277(1):763-73. PMC: 2754695. DOI: 10.1074/jbc.M109134200. View

18.

Gwon Y, Maxwell B, Kolaitis R, Zhang P, Kim H, Taylor J . Ubiquitination of G3BP1 mediates stress granule disassembly in a context-specific manner. Science. 2021; 372(6549):eabf6548. PMC: 8574224. DOI: 10.1126/science.abf6548. View

19.

Ding Q, Chaplin J, Morris M, Hilliard M, Wolvetang E, Ng D . TDP-43 Mutation Affects Stress Granule Dynamics in Differentiated NSC-34 Motoneuron-Like Cells. Front Cell Dev Biol. 2021; 9:611601. PMC: 8217991. DOI: 10.3389/fcell.2021.611601. View

20.

Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P . A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol. 2008; 10(10):1224-31. PMC: 4318256. DOI: 10.1038/ncb1783. View