SARS-CoV-2 impairs the disassembly of stress granules and promotes ALS-associated amyloid aggregation

Amraei R, Yin W, Napoleon MA, Suder EL, Berrigan J, Zhao Q, Olejnik J, Chandler K, Xia C, Feldman J, et al (2021) CD209L/L-SIGN and CD209/DC-SIGN act as receptors for SARS-CoV-2. bioRxiv

Bellmann J, Monette A, Tripathy V, Sojka A, Abo-Rady M, Janosh A, Bhatnagar R, Bickle M, Mouland AJ, Sterneckert J (2019) Viral infections exacerbate FUS-ALS phenotypes in iPSC-derived spinal neurons in a virus species-specific manner. Front Cell Neurosci 13:480

CAS  PubMed  PubMed Central  Google Scholar 

Bostanciklioglu M (2020) Severe acute respiratory syndrome coronavirus 2 is penetrating to dementia research. Curr Neurovasc Res.

Buchan JR, Kolaitis RM, Taylor JP, Parker R (2013) Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153:1461–1474

CAS  PubMed  PubMed Central  Google Scholar 

Burke KA, Janke AM, Rhine CL, Fawzi NL (2015) Residue-by-residue view of in vitro FUS granules that bind the C-terminal domain of RNA polymerase II. Mol Cell 60:231–241

CAS  PubMed  PubMed Central  Google Scholar 

Carlson CR, Asfaha JB, Ghent CM, Howard CJ, Hartooni N, Safari M, Frankel AD, Morgan DO (2020) Phosphoregulation of phase separation by the SARS-CoV-2 N protein suggests a biophysical basis for its dual functions. Mol Cell 80:1092–1103

CAS  PubMed  PubMed Central  Google Scholar 

Chan JF, Kok KH, Zhu Z, Chu H, To KK, Yuan S, Yuen KY (2020) Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect 9:221–236

CAS  PubMed  PubMed Central  Google Scholar 

Chen H, Cui Y, Han X, Hu W, Sun M, Zhang Y, Wang PH, Song G, Chen W, Lou J (2020) Liquid-liquid phase separation by SARS-CoV-2 nucleocapsid protein and RNA. Cell Res 30:1143–1145

CAS  PubMed  Google Scholar 

Chen J, Fan J, Chen Z, Zhang M, Peng H, Liu J, Ding L, Liu M, Zhao C, Zhao P et al (2021) Nonmuscle myosin heavy chain IIA facilitates SARS-CoV-2 infection in human pulmonary cells. Proc Natl Acad Sci USA 118:e2111011118

PubMed  PubMed Central  Google Scholar 

Cohen ME, Eichel R, Steiner-Birmanns B, Janah A, Ioshpa M, Bar-Shalom R, Paul JJ, Gaber H, Skrahina V, Bornstein NM et al (2020) A case of probable Parkinson’s disease after SARS-CoV-2 infection. Lancet Neurol 19:804–805

CAS  PubMed  PubMed Central  Google Scholar 

Conicella AE, Zerze GH, Mittal J, Fawzi NL (2016) ALS mutations disrupt phase separation mediated by alpha-helical structure in the TDP-43 low-complexity C-terminal domain. Structure 24:1537–1549

CAS  PubMed  PubMed Central  Google Scholar 

Crunfli F, Carregari VC, Veras FP, Vendramini PH, Fragnani Valença AG, Marcelo Antunes ASL, Brandão-Teles C, da Silva Zuccoli G, Reis-de-Oliveira G, Silva-Costa LC, et al (2021) SARS-CoV-2 infects brain astrocytes of COVID-19 patients and impairs neuronal viability. medRxiv

Cubuk J, Alston JJ, Incicco JJ, Singh S, Stuchell-Brereton MD, Ward MD, Zimmerman MI, Vithani N, Griffith D, Wagoner JA, et al (2020) The SARS-CoV-2 nucleocapsid protein is dynamic, disordered, and phase separates with RNA. bioRxiv

De Santis R, Alfano V, de Turris V, Colantoni A, Santini L, Garone MG, Antonacci G, Peruzzi G, Sudria-Lopez E, Wyler E et al (2019) Mutant FUS and ELAVL4 (HuD) aberrant crosstalk in amyotrophic lateral sclerosis. Cell Rep 27:3818–3831

PubMed  PubMed Central  Google Scholar 

Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, Than ME, Mackenzie IR, Capell A, Schmid B et al (2010) ALS-associated fused in sarcoma (FUS) mutations disrupt transportin-mediated nuclear import. EMBO J 29:2841–2857

CAS  PubMed  PubMed Central  Google Scholar 

Duan Y, Du A, Gu J, Duan G, Wang C, Gui X, Ma Z, Qian B, Deng X, Zhang K et al (2019) PARylation regulates stress granule dynamics, phase separation, and neurotoxicity of disease-related RNA-binding proteins. Cell Res 29:233–247

CAS  PubMed  PubMed Central  Google Scholar 

Eimer WA, Vijaya Kumar DK, Navalpur Shanmugam NK, Rodriguez AS, Mitchell T, Washicosky KJ, Gyorgy B, Breakefield XO, Tanzi RE, Moir RD (2018) Alzheimer’s disease-associated beta-amyloid is rapidly seeded by herpesviridae to protect against brain infection. Neuron 99:56–63

CAS  PubMed  PubMed Central  Google Scholar 

Gao C, Zeng J, Jia N, Stavenhagen K, Matsumoto Y, Zhang H, Li J, Hume AJ, Muhlberger E, van Die I, et al (2020) SARS-CoV-2 spike protein interacts with multiple innate immune receptors. bioRxiv

Gatto EM, Fernandez Boccazzi J (2020) COVID-19 and neurodegeneration: what can we learn from the past? Eur J Neurol. https://doi.org/10.1111/ene.14311

Article  PubMed  PubMed Central  Google Scholar 

Gordon DE, Jang GM, Bouhaddou M, Xu J, Obernier K, White KM, O’Meara MJ, Rezelj VV, Guo JZ, Swaney DL et al (2020) A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature 583:459–468

CAS  PubMed  PubMed Central  Google Scholar 

Gu J, Wang C, Hu R, Li Y, Zhang S, Sun Y, Wang Q, Li D, Fang Y, Liu C (2021a) Hsp70 chaperones TDP-43 in dynamic, liquid-like phase and prevents it from amyloid aggregation. Cell Res 31:1024–1027

CAS  PubMed  Google Scholar 

Gu Y, Cao J, Zhang X, Gao H, Wang Y, Wang J, He J, Jiang X, Zhang J, Shen G, et al (2021b) Receptome profiling identifies KREMEN1 and ASGR1 as alternative functional receptors of SARS-CoV-2. Cell Res

Guseva S, Milles S, Jensen MR, Salvi N, Kleman JP, Maurin D, Ruigrok RWH, Blackledge M (2020) Measles virus nucleo- and phosphoproteins form liquid-like phase-separated compartments that promote nucleocapsid assembly. Sci Adv 6:eaaz7095

CAS  PubMed  PubMed Central  Google Scholar 

Gwon Y, Maxwell BA, Kolaitis RM, Zhang P, Kim HJ, Taylor JP (2021) Ubiquitination of G3BP1 mediates stress granule disassembly in a context-specific manner. Science 372:eabf6548

CAS  PubMed  PubMed Central  Google Scholar 

Hascup ER, Hascup KN (2020) Does SARS-CoV-2 infection cause chronic neurological complications? Geroscience 42:1083–1087

CAS  PubMed  PubMed Central  Google Scholar 

Heneka MT, Golenbock D, Latz E, Morgan D, Brown R (2020) Immediate and long-term consequences of COVID-19 infections for the development of neurological disease. Alzheimers Res Ther 12:69

CAS  PubMed  PubMed Central  Google Scholar 

Iserman C, Roden CA, Boerneke MA, Sealfon RSG, McLaughlin GA, Jungreis I, Fritch EJ, Hou YJ, Ekena J, Weidmann CA et al (2020) Genomic RNA elements drive phase separation of the SARS-CoV-2 nucleocapsid. Mol Cell 80:1078–1091

CAS  PubMed  PubMed Central  Google Scholar 

Jain S, Wheeler JR, Walters RW, Agrawal A, Barsic A, Parker R (2016) ATPase-modulated stress granules contain a diverse proteome and substructure. Cell 164:487–498

CAS  PubMed  PubMed Central  Google Scholar 

Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ (2009) Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci USA 106:14063–14068

CAS  PubMed  PubMed Central  Google Scholar 

Johnson BS, Snead D, Lee JJ, McCaffery JM, Shorter J, Gitler AD (2009) TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. J Biol Chem 284:20329–20339

CAS  PubMed  PubMed Central  Google Scholar 

Kato M, Han TW, Xie S, Shi K, Du X, Wu LC, Mirzaei H, Goldsmith EJ, Longgood J, Pei J et al (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–767

CAS  PubMed  PubMed Central  Google Scholar 

Kaur R, Lal SK (2020) The multifarious roles of heterogeneous ribonucleoprotein A1 in viral infections. Rev Med Virol 30:e2097

PubMed  PubMed Central  Google Scholar 

Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, Diaz Z, MacLea KS, Freibaum B, Li S, Molliex A et al (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495:467–473

CAS  PubMed  PubMed Central  Google Scholar 

Klingstedt T, Shirani H, Aslund KO, Cairns NJ, Sigurdson CJ, Goedert M, Nilsson KP (2013) The structural basis for optimal performance of oligothiophene-based fluorescent amyloid ligands: conformational flexibility is essential for spectral assignment of a diversity of protein aggregates. Chemistry 19:10179–10192

CAS  PubMed  PubMed Central  Google Scholar 

Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T et al (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323:1205–1208

CAS  PubMed  Google Scholar 

Lai MM, Cavanagh D (1997) The molecular biology of coronaviruses. Adv Virus Res 48:1–100

CAS  PubMed  PubMed Central  Google Scholar 

Lee IC, Huo TI, Huang YH (2020) Gastrointestinal and liver manifestations in patients with COVID-19. J Chin Med Assoc 83:521–523

CAS  PubMed  Google Scholar 

Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC et al (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450–454

CAS  PubMed  PubMed Central  Google Scholar 

Li H, Xue Q, Xu X (2020) Involvement of the nervous system in SARS-CoV-2 infection. Neurotox Res 38:1–7

PubMed  PubMed Central  Google Scholar 

Liu Z, Zhang S, Gu J, Tong Y, Li Y, Gui X, Long H, Wang C, Zhao C, Lu J et al (2020) Hsp27 chaperones FUS phase separation under the modulation of stress-induced phosphorylation. Nat Struct Mol Biol 27:363–372

CAS  PubMed  Google Scholar 

Luo L, Li Z, Ma P, Zou Y, Li P, Liang A, Jin Z, Chi T, Huang C, Zhang Y, et al (2020). SARS-CoV-2 Nucleocapsid protein impairs SG assembly by partitioning into G3BP condensate. SSRN Electron J

Luo L, Li Z, Zhao T, Ju X, Ma P, Jin B, Zhou Y, He S, Huang J, Xu X et al (2021a) SARS-CoV-2 nucleocapsid protein phase separates with G3BPs to disassemble stress granules and facilitate viral production. Sci Bull 66:1194–1204

CAS  Google Scholar 

Luo L, Li Z, Zhao T, Ju X, Ma P, Jin B, Zhou Y, He S, Huang J, Xu X et al (2021b) SARS-CoV-2 nucleocapsid protein phase separates with G3BPs to disassemble stress granules and facilitate viral production. Sci Bull 66(12):1194–1204

CAS  Google Scholar 

Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, Chang J, Hong C, Zhou Y, Wang D et al (2020) Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan. China. JAMA Neurol 77(6):683–690

PubMed  Google Scholar 

Marreiros R, Muller-Schiffmann A, Trossbach SV, Prikulis I, Hansch S, Weidtkamp-Peters S, Moreira AR, Sahu S, Soloviev I, Selvarajah S et al (2020) Disruption of cellular proteostasis by H1N1 influenza A virus causes alpha-synuclein aggregation. Proc Natl Acad Sci USA 117:6741–6751

CAS  PubMed  PubMed Central 

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