4,934
Views
5
CrossRef citations to date
0
Altmetric
Research Paper

Abnormal triaging of misfolded proteins by adult neuronal ceroid lipofuscinosis-associated DNAJC5/CSPα mutants causes lipofuscin accumulation

ORCID Icon, ORCID Icon, , , ORCID Icon & ORCID Icon
Pages 204-223 | Received 25 Jan 2022, Accepted 08 Apr 2022, Published online: 04 May 2022

References

  • Anderson GW, Goebel HH, Simonati A. Human pathology in NCL. Biochim Biophys Acta. 2013 Nov;1832(11):1807–1826.
  • Naseri N, Sharma M, Velinov M. Autosomal dominant neuronal ceroid lipofuscinosis: clinical features and molecular basis. Clin Genet. 2021 Jan;99(1):111–118.
  • Haltia M. The neuronal ceroid-lipofuscinoses: from past to present. Biochim Biophys Acta. 2006 Oct;1762(10):850–856.
  • Cotman SL, Karaa A, Staropoli JF, et al. Neuronal ceroid lipofuscinosis: impact of recent genetic advances and expansion of the clinicopathologic spectrum. Curr Neurol Neurosci Rep. 2013 Aug;13(8):366. DOI:10.1007/s11910-013-0366-z.
  • Specchio N, Ferretti A, Trivisano M, et al. Neuronal ceroid lipofuscinosis: potential for targeted therapy. Drugs. 2021 Jan 26;81(1):101–123. DOI:10.1007/s40265-020-01440-7; PMID: 33242182. .
  • Mole SE, Cotman SL. Genetics of the neuronal ceroid lipofuscinoses (Batten disease). Biochim Biophys Acta. 2015 Oct;1852(10 Pt B):2237–2241.
  • Bajaj L, Sharma J, Di Ronza A, et al. A CLN6-CLN8 complex recruits lysosomal enzymes at the ER for Golgi transfer. J Clin Invest. 2020 Aug 3;130(8):4118–4132.
  • Di Ronza A, Bajaj L, Sharma J, et al. CLN8 is an endoplasmic reticulum cargo receptor that regulates lysosome biogenesis. Nat Cell Biol. 2018 Dec;20(12):1370–1377. DOI:10.1038/s41556-018-0228-7.
  • Chamberlain LH, Burgoyne RD. Cysteine-string protein: the chaperone at the synapse. J Neurochem. 2000 May;74(5):1781–1789.
  • Greaves J, Salaun C, Fukata Y, et al. Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J Biol Chem. 2008 Sep 5;283(36):25014–25026.
  • Greaves J, Chamberlain LH. Dual role of the cysteine-string domain in membrane binding and palmitoylation-dependent sorting of the molecular chaperone cysteine-string protein. Mol Biol Cell. 2006 Nov;17(11):4748–4759.
  • Zinsmaier KE, Hofbauer A, Heimbeck G, et al. A cysteine-string protein is expressed in retina and brain of Drosophila. J Neurogenet. 1990 Nov;7(1):15–29. DOI:10.3109/01677069009084150.
  • Ohyama T, Verstreken P, Ly CV, et al. Huntingtin-interacting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles. J Cell Biol. 2007 Dec 31;179(7):1481–1496.
  • Tobaben S, Thakur P, Fernandez-Chacon R, et al. A trimeric protein complex functions as a synaptic chaperone machine. Neuron. 2001 Sep 27;31(6):987–999.
  • Benitez BA, Sands MS. Primary fibroblasts from CSPalpha mutation carriers recapitulate hallmarks of the adult onset neuronal ceroid lipofuscinosis. Sci Rep. 2017 Jul 24;7(1):6332.
  • Schroder B, Elsasser HP, Schmidt B, et al. Characterisation of lipofuscin-like lysosomal inclusion bodies from human placenta. FEBS Lett. 2007 Jan 9;581(1):102–108.
  • Nylandsted J, Becker AC, Bunkenborg J, et al. ErbB2-associated changes in the lysosomal proteome. Proteomics. 2011 Jul;11(14):2830–2838. DOI:10.1002/pmic.201000734.
  • Chapel A, Kieffer-Jaquinod S, Sagne C, et al. An extended proteome map of the lysosomal membrane reveals novel potential transporters. Mol Cell Proteomics. 2013 Jun;12(6):1572–1588. DOI:10.1074/mcp.M112.021980.
  • Xu Y, Cui L, Dibello A, et al. DNAJC5 facilitates USP19-dependent unconventional secretion of misfolded cytosolic proteins. Cell Discov. 2018;4(1):11. DOI:10.1038/s41421-018-0012-7.
  • Braun JE, Wilbanks SM, Scheller RH. The cysteine string secretory vesicle protein activates Hsc70 ATPase. J Biol Chem. 1996 Oct 18;271(42):25989–25993.
  • Chamberlain LH, Burgoyne RD. Activation of the ATPase activity of heat-shock proteins Hsc70/Hsp70 by cysteine-string protein. Biochem J. 1997 Mar 15;322(Pt 3):853–858.
  • Sharma M, Burre J, Bronk P, et al. CSPalpha knockout causes neurodegeneration by impairing SNAP-25 function. EMBO J. 2012 Feb 15;31(4):829–841.
  • Sharma M, Burre J, Sudhof TC. CSPalpha promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nat Cell Biol. 2011 Jan;13(1):30–39.
  • Ranjan R, Bronk P, Zinsmaier KE. Cysteine string protein is required for calcium secretion coupling of evoked neurotransmission in drosophila but not for vesicle recycling. J Neurosci. 1998 Feb 1;18(3):956–964.
  • Miller LC, Swayne LA, Chen L, et al. Cysteine string protein (CSP) inhibition of N-type calcium channels is blocked by mutant huntingtin. J Biol Chem. 2003 Dec 26;278(52):53072–53081.
  • Weng N, Baumler MD, Thomas DD, et al. Functional role of J domain of cysteine string protein in Ca2+-dependent secretion from acinar cells. Am J Physiol Gastrointest Liver Physiol. 2009 May;296(5):G1030–9. DOI:10.1152/ajpgi.90592.2008.
  • Bronk P, Nie Z, Klose MK, et al. The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J Neurosci. 2005 Mar 2;25(9):2204–2214.
  • Bronk P, Wenniger JJ, Dawson-Scully K, et al. Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron. 2001 May;30(2):475–488. DOI:10.1016/S0896-6273(01)00292-6.
  • Nie Z, Ranjan R, Wenniger JJ, et al. Overexpression of cysteine-string proteins in Drosophila reveals interactions with syntaxin. J Neurosci. 1999 Dec 1;19(23):10270–10279.
  • Evans GJ, Morgan A. Phosphorylation-dependent interaction of the synaptic vesicle proteins cysteine string protein and synaptotagmin I. Biochem J. 2002 Jun 1;364(Pt 2):343–347.
  • Wu MN, Fergestad T, Lloyd TE, et al. Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron. 1999 Jul;23(3):593–605. DOI:10.1016/S0896-6273(00)80811-9.
  • Fernandez-Chacon R, Wolfel M, Nishimune H, et al. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron. 2004 Apr 22;42(2):237–251.
  • Gorenberg EL, Chandra SS. The role of co-chaperones in synaptic proteostasis and neurodegenerative disease. Front Neurosci. 2017;11:248.
  • Donnelier J, Braun JE. CSPalpha-chaperoning presynaptic proteins. Front Cell Neurosci. 2014;8:116.
  • Lee JG, Takahama S, Zhang G, et al. Unconventional secretion of misfolded proteins promotes adaptation to proteasome dysfunction in mammalian cells. Nat Cell Biol. 2016 Jul;18(7):765–776. DOI:10.1038/ncb3372.
  • Fontaine SN, Zheng D, Sabbagh JJ, et al. DnaJ/Hsc70 chaperone complexes control the extracellular release of neurodegenerative-associated proteins. EMBO J. 2016 Jul 15;35(14):1537–1549.
  • Noskova L, Stranecky V, Hartmannova H, et al. Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am J Hum Genet. 2011 Aug 12;89(2):241–252.
  • Benitez BA, Alvarado D, Cai Y, et al. Exome-sequencing confirms DNAJC5 mutations as cause of adult neuronal ceroid-lipofuscinosis. PLoS One. 2011;6(11):e26741. DOI:10.1371/journal.pone.0026741.
  • Cadieux-Dion M, Andermann E, Lachance-Touchette P, et al. Recurrent mutations in DNAJC5 cause autosomal dominant Kufs disease. Clin Genet. 2013 Jun;83(6):571–575. DOI:10.1111/cge.12020.
  • Diez-Ardanuy C, Greaves J, Munro KR, et al. A cluster of palmitoylated cysteines are essential for aggregation of cysteine-string protein mutants that cause neuronal ceroid lipofuscinosis. Sci Rep. 2017 Jan 31;7(1):10.
  • Imler E, Pyon JS, Kindelay S, et al. A Drosophila model of neuronal ceroid lipofuscinosis CLN4 reveals a hypermorphic gain of function mechanism. Elife. 2019 Oct ; 30(8):e46607. DOI:10.7554/eLife.46607. PMID: 31663851; PMCID: PMC6897512.
  • Naseri NN, Ergel B, Kharel P, et al. Aggregation of mutant cysteine string protein-alpha via Fe-S cluster binding is mitigated by iron chelators. Nat Struct Mol Biol. 2020 Feb;27(2):192–201. DOI:10.1038/s41594-020-0375-y.
  • Violot S, Carpentier P, Blanchoin L, et al. Reverse pH-dependence of chromophore protonation explains the large Stokes shift of the red fluorescent protein mKeima. J Am Chem Soc. 2009 Aug 5;131(30):10356–10357.
  • Katayama H, Kogure T, Mizushima N, et al. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol. 2011 Aug 26;18(8):1042–1052.
  • Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science. 1997 Jun 27;276(5321):2045–2047.
  • Sardana R, Emr SD. Membrane protein quality control mechanisms in the endo-lysosome system. Trends Cell Biol. 2021 Apr;31(4):269–283.
  • Sahu R, Kaushik S, Clement CC, et al. Microautophagy of cytosolic proteins by late endosomes. Dev Cell. 2011 Jan 18;20(1):131–139.
  • Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2014 Jan;24(1):24–41. DOI:10.1038/cr.2013.168.
  • Lee C, Lamech L, Johns E, et al. Selective lysosome membrane turnover is induced by nutrient starvation. Dev Cell. 2020 Nov 9;55(3):289–297 e4.
  • Mesquita A, Glenn J, Jenny A. Differential activation of eMI by distinct forms of cellular stress. Autophagy. 2020 Jul;9:1–13.
  • Wu S, Sirkis DW, Schekman RW. Unconventional secretion of α-synuclein mediated by palmitoylated DNAJC5 oligomers. BioRxiv. 2022. DOI:10.1101/2022.01.27.477991
  • Rosell A, Meury M, Alvarez-Marimon E, et al. Structural bases for the interaction and stabilization of the human amino acid transporter LAT2 with its ancillary protein 4F2hc. Proc Natl Acad Sci U S A. 2014 Feb 25;111(8):2966–2971.
  • Zhang M, Liu L, Lin X, et al. A translocation pathway for vesicle-mediated unconventional protein secretion. Cell. 2020 Apr 30;181(3):637–652 e15.
  • Tyynela J, Palmer DN, Baumann M, et al. Storage of saposins A and D in infantile neuronal ceroid-lipofuscinosis. FEBS Lett. 1993 Sep 6;330(1):8–12.
  • Lojewski X, Staropoli JF, Biswas-Legrand S, et al. Human iPSC models of neuronal ceroid lipofuscinosis capture distinct effects of TPP1 and CLN3 mutations on the endocytic pathway. Hum Mol Genet. 2014 Apr 15;23(8):2005–2022.
  • Greaves J, Lemonidis K, Gorleku OA, et al. Palmitoylation-induced aggregation of cysteine-string protein mutants that cause neuronal ceroid lipofuscinosis. J Biol Chem. 2012 Oct 26;287(44):37330–37339.
  • Milkereit R, Persaud A, Vanoaica L, et al. LAPTM4b recruits the LAT1-4F2hc Leu transporter to lysosomes and promotes mTORC1 activation. Nat Commun. 2015 May 22;6(1):7250.
  • Bruns C, McCaffery JM, Curwin AJ, et al. Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol. 2011 Dec 12;195(6):979–992.
  • Malhotra V. Unconventional protein secretion: an evolving mechanism. EMBO J. 2013 Jun 12;32(12):1660–1664.
  • Lee JG, Kim W, Gygi S, et al. Characterization of the deubiquitinating activity of USP19 and its role in endoplasmic reticulum-associated degradation. J Biol Chem. 2014 Feb 7;289(6):3510–3517.
  • Patel P, Prescott GR, Burgoyne RD, et al. Phosphorylation of cysteine string protein triggers a major conformational switch. Structure. 2016 Aug 2;24(8):1380–1386.
  • Henderson MX, Wirak GS, Zhang YQ, et al. Neuronal ceroid lipofuscinosis with DNAJC5/CSPalpha mutation has PPT1 pathology and exhibit aberrant protein palmitoylation. Acta Neuropathol. 2016 Apr;131(4):621–637. DOI:10.1007/s00401-015-1512-2.
  • Deng J, Koutras C, Donnelier J, et al. Neurons export extracellular vesicles enriched in cysteine string protein and misfolded protein cargo. Sci Rep. 2017 Apr 19;7(1):956.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013 Nov;8(11):2281–2308. DOI:10.1038/nprot.2013.143.
  • Shalem O, Sanjana NE, Hartenian E, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 2014 Jan 3;343(6166):84–87.
  • Fueller J, Herbst K, Meurer M, et al. CRISPR-Cas12a-assisted PCR tagging of mammalian genes. J Cell Biol. 2020 Jun 1;219(6). DOI:10.1083/jcb.201910210.