Increased presence of nuclear DNAJA3 and upregulation of cytosolic STAT1 and of nucleic acid sensors trigger innate immunity in the ClpP-null mouse
Tóm tắt
Từ khóa
Tài liệu tham khảo
Jenkinson EM, Rehman AU, Walsh T, Clayton-Smith J, Lee K, Morell RJ, Drummond MC, Khan SN, Naeem MA, Rauf B, Billington N, Schultz JM, Urquhart JE, Lee MK, Berry A, Hanley NA, Mehta S, Cilliers D, Clayton PE, Kingston H, Smith MJ, Warner TT, University of Washington Center for Mendelian Genomics, Black GC, Trump D, Davis JR, Ahmad W, Leal SM, Riazuddin S, King MC, Friedman TB, Newman WG (2013) Perrault syndrome is caused by recessive mutations in CLPP, encoding a mitochondrial ATP-dependent chambered protease. Am J Hum Genet 92(4):605–613
Newman WG et al (1993) GeneReviews®: Perrault syndrome. Seattle (WA), 1993–2021
Bhaskaran S et al (2018) Loss of mitochondrial protease ClpP protects mice from diet-induced obesity and insulin resistance. EMBO Rep 19(3): e45009
Nishi Y, Hamamoto K, Kajiyama M, Kawamura I, Opitz JM, Reynolds JF (1988) The Perrault syndrome: clinical report and review. Am J Med Genet 31(3):623–629
Theunissen TEJ et al (2016) Specific MRI abnormalities reveal severe Perrault syndrome due to CLPP defects. Front Neurol 7:203
Sherman MY, Goldberg AL (1996) Involvement of molecular chaperones in intracellular protein breakdown. EXS 77:57–78
Haynes CM, Petrova K, Benedetti C, Yang Y, Ron D (2007) ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 13(4):467–480
Szczepanowska K, Maiti P, Kukat A, Hofsetz E, Nolte H, Senft K, Becker C, Ruzzenente B, Hornig-Do HT, Wibom R, Wiesner RJ, Krüger M, Trifunovic A (2016) CLPP coordinates mitoribosomal assembly through the regulation of ERAL1 levels. EMBO J 35(23):2566–2583
Torres-Odio S et al (2021) Loss of mitochondrial protease CLPP activates type I IFN responses through the mitochondrial DNA-cGAS-STING signaling axis. Journal of Immunology (Baltimore, MD: 1950) 206(8):1890–1900
Gispert S, Parganlija D, Klinkenberg M, Drose S, Wittig I, Mittelbronn M, Grzmil P, Koob S, Hamann A, Walter M, Buchel F, Adler T, Hrabe de Angelis M, Busch DH, Zell A, Reichert AS, Brandt U, Osiewacz HD, Jendrach M, Auburger G (2013) Loss of mitochondrial peptidase Clpp leads to infertility, hearing loss plus growth retardation via accumulation of CLPX, mtDNA and inflammatory factors. Hum Mol Genet 22(24):4871–4887
Key J, Maletzko A, Kohli A, Gispert S, Torres-Odio S, Wittig I, Heidler J, Bárcena C, López-Otín C, Lei Y, West AP, Münch C, Auburger G (2020) Loss of mitochondrial ClpP, Lonp1, and Tfam triggers transcriptional induction of Rnf213, a susceptibility factor for moyamoya disease. Neurogenetics 21(3):187–203
Tigano M, Vargas DC, Tremblay-Belzile S, Fu Y, Sfeir A (2021) Nuclear sensing of breaks in mitochondrial DNA enhances immune surveillance. Nature 591(7850):477–481
Oziębło D et al (2020) Two novel pathogenic variants confirm RMND1 causative role in Perrault syndrome with renal involvement. Genes 11(9):1060
Tucker EJ, Rius R, Jaillard S, Bell K, Lamont PJ, Travessa A, Dupont J, Sampaio L, Dulon J, Vuillaumier-Barrot S, Whalen S, Isapof A, Stojkovic T, Quijano-Roy S, Robevska G, van den Bergen J, Hanna C, Simpson A, Ayers K, Thorburn DR, Christodoulou J, Touraine P, Sinclair AH (2020) Genomic sequencing highlights the diverse molecular causes of Perrault syndrome: a peroxisomal disorder (PEX6), metabolic disorders (CLPP, GGPS1), and mtDNA maintenance/translation disorders (LARS2, TFAM). Hum Genet 139(10):1325–1343
Rauthan M, Ranji P, Aguilera Pradenas N, Pitot C, Pilon M (2013) The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proc Natl Acad Sci U S A 110(15):5981–5986
Raimundo N, Song L, Shutt TE, McKay SE, Cotney J, Guan MX, Gilliland TC, Hohuan D, Santos-Sacchi J, Shadel GS (2012) Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell 148(4):716–726
Hutchin TP, Cortopassi GA (2000) Mitochondrial defects and hearing loss. Cellular and Molecular Life Sciences: CMLS 57(13-14):1927–1937
Greber BJ et al (2015) Ribosome. The complete structure of the 55S mammalian mitochondrial ribosome. Science (New York, NY) 348(6232):303–308
West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11(6):389–402
West AP, Khoury-Hanold W, Staron M, Tal MC, Pineda CM, Lang SM, Bestwick M, Duguay BA, Raimundo N, MacDuff DA, Kaech SM, Smiley JR, Means RE, Iwasaki A, Shadel GS (2015) Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520(7548):553–557
Andreeva L, Hiller B, Kostrewa D, Lässig C, de Oliveira Mann CC, Jan Drexler D, Maiser A, Gaidt M, Leonhardt H, Hornung V, Hopfner KP (2017) cGAS senses long and HMGB/TFAM-bound U-turn DNA by forming protein-DNA ladders. Nature 549(7672):394–398
Wu Z, Oeck S, West AP, Mangalhara KC, Sainz AG, Newman LE, Zhang XO, Wu L, Yan Q, Bosenberg M, Liu Y, Sulkowski PL, Tripple V, Kaech SM, Glazer PM, Shadel GS (2019) Mitochondrial DNA stress signalling protects the nuclear genome. Nature Metabolism 1(12):1209–1218
Zhang W et al (2019) Cellular DNAJA3, a novel VP1-interacting protein, inhibits foot-and-mouth disease virus replication by inducing lysosomal degradation of VP1 and attenuating its antagonistic role in the beta interferon signaling pathway. Virol J 93(13):e00588–19
West AP, Shadel GS (2017) Mitochondrial DNA in innate immune responses and inflammatory pathology. Nat Rev Immunol 17(6):363–375
Dhir A, Dhir S, Borowski LS, Jimenez L, Teitell M, Rötig A, Crow YJ, Rice GI, Duffy D, Tamby C, Nojima T, Munnich A, Schiff M, de Almeida CR, Rehwinkel J, Dziembowski A, Szczesny RJ, Proudfoot NJ (2018) Mitochondrial double-stranded RNA triggers antiviral signalling in humans. Nature 560(7717):238–242
Corti O, Lesage S, Brice A (2011) What genetics tells us about the causes and mechanisms of Parkinson’s disease. Physiol Rev 91(4):1161–1218
Pickrell AM, Youle RJ (2015) The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron 85(2):257–273
Manzanillo PS, Ayres JS, Watson RO, Collins AC, Souza G, Rae CS, Schneider DS, Nakamura K, Shiloh MU, Cox JS (2013) The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501(7468):512–516
Torres-Odio S, Key J, Hoepken HH, Canet-Pons J, Valek L, Roller B, Walter M, Morales-Gordo B, Meierhofer D, Harter PN, Mittelbronn M, Tegeder I, Gispert S, Auburger G (2017) Progression of pathology in PINK1-deficient mouse brain from splicing via ubiquitination, ER stress, and mitophagy changes to neuroinflammation. J Neuroinflammation 14(1):154
Sliter DA, Martinez J, Hao L, Chen X, Sun N, Fischer TD, Burman JL, Li Y, Zhang Z, Narendra DP, Cai H, Borsche M, Klein C, Youle RJ (2018) Parkin and PINK1 mitigate STING-induced inflammation. Nature 561(7722):258–262
Crooks DR et al (2021) Mitochondrial DNA alterations underlie an irreversible shift to aerobic glycolysis in fumarate hydratase-deficient renal cancer. Science Signaling 14(664):eabc4436
Ryan DG, Murphy MP, Frezza C, Prag HA, Chouchani ET, O’Neill LA, Mills EL (2019) Coupling Krebs cycle metabolites to signalling in immunity and cancer. Nature Metabolism 1:16–33
Krysko DV, Agostinis P, Krysko O, Garg AD, Bachert C, Lambrecht BN, Vandenabeele P (2011) Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol 32(4):157–164
Larsson NG, Oldfors A, David Garman J, Barsh GS, Clayton DA (1997) Down-regulation of mitochondrial transcription factor A during spermatogenesis in humans. Hum Mol Genet 6(2):185–191
Lee EJ, Kang YC, Park WH, Jeong JH, Pak YK (2014) Negative transcriptional regulation of mitochondrial transcription factor A (TFAM) by nuclear TFAM. Biochem Biophys Res Commun 450(1):166–171
Meier JA, Larner AC (2014) Toward a new STATe: the role of STATs in mitochondrial function. Semin Immunol 26(1):20–28
Wittig I, Karas M, Schagger H (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 6(7):1215–1225
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108
Sen N-E, Canet-Pons J, Halbach MV, Arsovic A, Pilatus U, Chae WH, Kaya ZE, Seidel K, Rollmann E, Mittelbronn M, Meierhofer D, de Zeeuw CI, Bosman LWJ, Gispert S, Auburger G (2019) Generation of an Atxn2-CAG100 knock-in mouse reveals N-acetylaspartate production deficit due to early Nat8l dysregulation. Neurobiol Dis 132:104559
Yochem J, Uchida H, Sunshine M, Saito H, Georgopoulos CP, Feiss M (1978) Genetic analysis of two genes, dnaJ and dnaK, necessary for Escherichia coli and bacteriophage lambda DNA replication. Mol Gen Genet 164(1):9–14
Szczepanowska K, Senft K, Heidler J, Herholz M, Kukat A, Höhne MN, Hofsetz E, Becker C, Kaspar S, Giese H, Zwicker K, Guerrero-Castillo S, Baumann L, Kauppila J, Rumyantseva A, Müller S, Frese CK, Brandt U, Riemer J, Wittig I, Trifunovic A (2020) A salvage pathway maintains highly functional respiratory complex I. Nat Commun 11(1):1643
Beck JS, Mufson EJ, Counts SE (2016) Evidence for mitochondrial UPR gene activation in familial and sporadic Alzheimer’s disease. Curr Alzheimer Res 13(6):610–614
Copeland E, Balgobin S, Lee CM, Rozakis-Adcock M (2011) hTID-1 defines a novel regulator of c-Met receptor signaling in renal cell carcinomas. Oncogene 30(19):2252–2263
Sehgal PB (2003) Plasma membrane rafts and chaperones in cytokine/STAT signaling. Acta Biochim Pol 50(3):583–594
Lu B, Garrido N, Spelbrink JN, Suzuki CK (2006) Tid1 isoforms are mitochondrial DnaJ-like chaperones with unique carboxyl termini that determine cytosolic fate. J Biol Chem 281(19):13150–13158
Cheng H, Cenciarelli C, Nelkin G, Tsan R, Fan D, Cheng-Mayer C, Fidler IJ (2005) Molecular mechanism of hTid-1, the human homolog of Drosophila tumor suppressor l(2)Tid, in the regulation of NF-kappaB activity and suppression of tumor growth. Mol Cell Biol 25(1):44–59
Kim SW, Hayashi M, Lo JF, Fearns C, Xiang R, Lazennec G, Yang Y, Lee JD (2005) Tid1 negatively regulates the migratory potential of cancer cells by inhibiting the production of interleukin-8. Cancer Res 65(19):8784–8791
Kumada K, Fuse N, Tamura T, Okamori C, Kurata S (2019) HSP70/DNAJA3 chaperone/cochaperone regulates NF-kappaB activity in immune responses. Biochem Biophys Res Commun 513(4):947–951
Konieczny I, Zylicz M (1999) Role of bacterial chaperones in DNA replication. Genet Eng (N Y) 21:95–111
Choudhury NR, Heikel G, Michlewski G (2020) TRIM25 and its emerging RNA-binding roles in antiviral defense. Wiley Interdiscip Rev RNA 11(4):e1588
Zhu J, Zhang Y, Ghosh A, Cuevas RA, Forero A, Dhar J, Ibsen MS, Schmid-Burgk JL, Schmidt T, Ganapathiraju MK, Fujita T, Hartmann R, Barik S, Hornung V, Coyne CB, Sarkar SN (2014) Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity 40(6):936–948
Diamond MS (2014) IFIT1: a dual sensor and effector molecule that detects non-2'-O methylated viral RNA and inhibits its translation. Cytokine Growth Factor Rev 25(5):543–550
Pichlmair A, Lassnig C, Eberle CA, Górna MW, Baumann CL, Burkard TR, Bürckstümmer T, Stefanovic A, Krieger S, Bennett KL, Rülicke T, Weber F, Colinge J, Müller M, Superti-Furga G (2011) IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol 12(7):624–630
Seo GJ, Kim C, Shin WJ, Sklan EH, Eoh H, Jung JU (2018) TRIM56-mediated monoubiquitination of cGAS for cytosolic DNA sensing. Nat Commun 9(1):613
Wan L, Juszkiewicz S, Blears D, Bajpe PK, Han Z, Faull P, Mitter R, Stewart A, Snijders AP, Hegde RS, Svejstrup JQ (2021) Translation stress and collided ribosomes are co-activators of cGAS. Mol Cell 81:2808–2822.e10
McArthur K et al (2018) BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science 359(6378):eaao6047
Fredriksson A, Ballesteros M, Peterson CN, Persson O, Silhavy TJ, Nystrom T (2007) Decline in ribosomal fidelity contributes to the accumulation and stabilization of the master stress response regulator sigmaS upon carbon starvation. Genes Dev 21(7):862–874
Becker LA, Huang B, Bieri G, Ma R, Knowles DA, Jafar-Nejad P, Messing J, Kim HJ, Soriano A, Auburger G, Pulst SM, Taylor JP, Rigo F, Gitler AD (2017) Therapeutic reduction of ataxin-2 extends lifespan and reduces pathology in TDP-43 mice. Nature 544(7650):367–371
Mercuri E, Darras BT, Chiriboga CA, Day JW, Campbell C, Connolly AM, Iannaccone ST, Kirschner J, Kuntz NL, Saito K, Shieh PB, Tulinius M, Mazzone ES, Montes J, Bishop KM, Yang Q, Foster R, Gheuens S, Bennett CF, Farwell W, Schneider E, de Vivo DC, Finkel RS (2018) Nusinersen versus sham control in later-onset spinal muscular atrophy. N Engl J Med 378(7):625–635
Antonellis A, Green ED (2008) The role of aminoacyl-tRNA synthetases in genetic diseases. Annu Rev Genomics Hum Genet 9:87–107
Demain LA, Conway GS, Newman WG (2017) Genetics of mitochondrial dysfunction and infertility. Clin Genet 91(2):199–207
Ognjenovic J, Simonovic M (2018) Human aminoacyl-tRNA synthetases in diseases of the nervous system. RNA Biol 15(4-5):623–634
Opinc AH, Makowska JS (2021) Antisynthetase syndrome - much more than just a myopathy. Semin Arthritis Rheum 51(1):72–83
Adang L, Gavazzi F, de Simone M, Fazzi E, Galli J, Koh J, Kramer-Golinkoff J, de Giorgis V, Orcesi S, Peer K, Ulrick N, Woidill S, Shults J, Vanderver A (2020) Developmental outcomes of Aicardi Goutieres syndrome. J Child Neurol 35(1):7–16
Bamborschke D, Kreutzer M, Koy A, Koerber F, Lucas N, Huenseler C, Herkenrath P, Lee-Kirsch MA, Cirak S (2021) PNPT1 mutations may cause Aicardi-Goutieres-syndrome. Brain and Development 43(2):320–324