Lysosome size, motility and stress response regulated by fronto-temporal dementia modifier TMEM106B

Molecular and Cellular Neuroscience

Volumn 61, Issue , 2014, Pages 226-240

  Stagi, Massimiliano ^a,b   Klein, Zoe A ^a   Gould, Travis J ^a   Bewersdorf, Joerg ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Fronto temporal dementia; Lysosome; Neurodegeneration; Progranulin; TDP 43; TFEB

Indexed keywords

MEMBRANE PROTEIN; TMEM106B PROTEIN; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, MOUSE; NERVE PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN; SMALL INTERFERING RNA; TFEB PROTEIN, HUMAN; TMEM106B PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; AUTOREGULATION; CELL MOTILITY; CELL SIZE; CELL STRESS; CELLULAR DISTRIBUTION; EXPRESSION VECTOR; FRONTOTEMPORAL DEMENTIA; GENE SILENCING; GENETIC VARIABILITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LOSS OF FUNCTION MUTATION; LYSOSOME; MODIFIER GENE; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL CULTURE; CHLOROCEBUS AETHIOPS; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PROTEIN TRANSPORT;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; EMBRYO, MAMMALIAN; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; RNA, MESSENGER; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL; TRANSFECTION;

EID: 84905373368     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.07.006     Document Type: Article

References (41)

1. Avrova A.O., Stewart H.E., De Jong W.D., Heilbronn J., Lyon G.D., Birch P.R. A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol. Plant Microbe Interact. 1999, 12:1114-1119.
2. Bankaitis V.A., Johnson L.M., Emr S.D. Isolation of yeast mutants defective in protein targeting to the vacuole. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:9075-9079.
3. Banta L.M., Robinson J.S., Klionsky D.J., Emr S.D. Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol. 1988, 107:1369-1383.
4. Brady O.A., Zheng Y., Murphy K., Huang M., Hu F. The frontotemporal lobar degeneration risk factor, TMEM106B, regulates lysosomal morphology and function. Hum. Mol. Genet. 2013, 22:685-695.
5. Chen H.J., Huang D.J., Hou W.C., Liu J.S., Lin Y.H. Molecular cloning and characterization of a granulin-containing cysteine protease SPCP3 from sweet potato (Ipomoea batatas) senescent leaves. J. Plant Physiol. 2006, 163:863-876.
6. Chen-Plotkin A.S., Unger T.L., Gallagher M.D., Bill E., Kwong L.K., Volpicelli-Daley L., Busch J.I., Akle S., Grossman M., Van Deerlin V., Trojanowski J.Q., Lee V.M. TMEM106B, the risk gene for frontotemporal dementia, is regulated by the microRNA-132/212 cluster and affects progranulin pathways. J. Neurosci. 2012, 32:11213-11227.
7. Cruchaga C., Graff C., Chiang H.H., Wang J., Hinrichs A.L., Spiegel N., Bertelsen S., Mayo K., Norton J.B., Morris J.C., Goate A. Association of TMEM106B gene polymorphism with age at onset in granulin mutation carriers and plasma granulin protein levels. Arch. Neurol. 2011, 68:581-586.
8. Finch N., et al. TMEM106B regulates progranulin levels and the penetrance of FTLD in GRN mutation carriers. Neurology 2011, 76:467-474.
9. Gu C., Shabab M., Strasser R., Wolters P.J., Shindo T., Niemer M., Kaschani F., Mach L., van der Hoorn R.A. Post-translational regulation and trafficking of the granulin-containing protease RD21 of Arabidopsis thaliana. PLoS One 2012, 7:e32422.
10. Herskowitz J.H., Gozal Y.M., Duong D.M., Dammer E.B., Gearing M., Ye K., Lah J.J., Peng J., Levey A.I., Seyfried N.T. Asparaginyl endopeptidase cleaves TDP-43 in brain. Proteomics 2012, 12:2455-2463.
11. Hu F., Padukkavidana T., Vaegter C.B., Brady O.A., Zheng Y., Mackenzie I.R., Feldman H.H., Nykjaer A., Strittmatter S.M. Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron 2010, 68:654-667.
12. Ju J.S., Fuentealba R.A., Miller S.E., Jackson E., Piwnica-Worms D., Baloh R.H., Weihl C.C. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J. Cell Biol. 2009, 187:875-888.
13. Kirkegaard T., Roth A.G., Petersen N.H., Mahalka A.K., Olsen O.D., Moilanen I., Zylicz A., Knudsen J., Sandhoff K., Arenz C., Kinnunen P.K., Nylandsted J., Jaattela M. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010, 463:549-553.
14. Lang C.M., Fellerer K., Schwenk B.M., Kuhn P.H., Kremmer E., Edbauer D., Capell A., Haass C. Membrane orientation and subcellular localization of transmembrane protein 106B (TMEM106B), a major risk factor for frontotemporal lobar degeneration. J. Biol. Chem. 2012, 287:19355-19365.
15. Mackenzie I.R., et al. Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update. Acta Neuropathol. 2010, 119:1-4.
16. Nicholson A.M., Finch N.A., Wojtas A., Baker M.C., Perkerson R.B., Castanedes-Casey M., Rousseau L., Benussi L., Binetti G., Ghidoni R., Hsiung G.Y., Mackenzie I.R., Finger E., Boeve B.F., Ertekin-Taner N., Graff-Radford N.R., Dickson D.W., Rademakers R. TMEM106B p.T185S regulates TMEM106B protein levels: implications for frontotemporal dementia. J. Neurochem. 2013, 126:781-791.
17. Park J.S., Neiman A.M. VPS13 regulates membrane morphogenesis during sporulation in Saccharomyces cerevisiae. J. Cell Sci. 2012, 125:3004-3011.
18. Pellett P.A., Sun X., Gould T.J., Rothman J.E., Xu M.Q., Correa I.R., Bewersdorf J. Two-color STED microscopy in living cells. Biomed. Opt. Express 2011, 2:2364-2371.
19. Rampoldi L., Dobson-Stone C., Rubio J.P., Danek A., Chalmers R.M., Wood N.W., Verellen C., Ferrer X., Malandrini A., Fabrizi G.M., Brown R., Vance J., Pericak-Vance M., Rudolf G., Carre S., Alonso E., Manfredi M., Nemeth A.H., Monaco A.P. A conserved sorting-associated protein is mutant in chorea-acanthocytosis. Nat. Genet. 2001, 28:119-120.
20. Rieder S.E., Emr S.D. A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol. Biol. Cell 1997, 8:2307-2327.
21. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., Ferguson S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 2012, 5:ra42.
22. Rutherford N.J., Carrasquillo M.M., Li M., Bisceglio G., Menke J., Josephs K.A., Parisi J.E., Petersen R.C., Graff-Radford N.R., Younkin S.G., Dickson D.W., Rademakers R. TMEM106B risk variant is implicated in the pathologic presentation of Alzheimer disease. Neurology 2012, 79:717-718.
23. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Di Malta C., Donaudy F., Embrione V., Polishchuk R.S., Banfi S., Parenti G., Cattaneo E., Ballabio A. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.
24. Sato T.K., Rehling P., Peterson M.R., Emr S.D. Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol. Cell 2000, 6:661-671.
25. Schwenk B.M., Lang C.M., Hogl S., Tahirovic S., Orozco D., Rentzsch K., Lichtenthaler S.F., Hoogenraad C.C., Capell A., Haass C., Edbauer D. The FTLD risk factor TMEM106B and MAP6 control dendritic trafficking of lysosomes. EMBO J. 2014, 33:450-467.
26. Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., Erdin S.U., Huynh T., Medina D., Colella P., Sardiello M., Rubinsztein D.C., Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
27. Settembre C., Zoncu R., Medina D.L., Vetrini F., Erdin S., Erdin S., Huynh T., Ferron M., Karsenty G., Vellard M.C., Facchinetti V., Sabatini D.M., Ballabio A. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 2012, 31:1095-1108.
28. Settembre C., De Cegli R., Mansueto G., Saha P.K., Vetrini F., Visvikis O., Huynh T., Carissimo A., Palmer D., Klisch T.J., Wollenberg A.C., Di Bernardo D., Chan L., Irazoqui J.E., Ballabio A. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat. Cell Biol. 2013, 15:647-658.
29. Sherer N.M., Lehmann M.J., Jimenez-Soto L.F., Ingmundson A., Horner S.M., Cicchetti G., Allen P.G., Pypaert M., Cunningham J.M., Mothes W. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 2003, 4:785-801.
30. Smith K.R., Damiano J., Franceschetti S., Carpenter S., Canafoglia L., Morbin M., Rossi G., Pareyson D., Mole S.E., Staropoli J.F., Sims K.B., Lewis J., Lin W.L., Dickson D.W., Dahl H.H., Bahlo M., Berkovic S.F. Strikingly different clinicopathological phenotypes determined by progranulin-mutation dosage. Am. J. Hum. Genet. 2012, 90:1102-1107.
31. Thoreen C.C., Kang S.A., Chang J.W., Liu Q., Zhang J., Gao Y., Reichling L.J., Sim T., Sabatini D.M., Gray N.S. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 2009, 284:8023-8032.
32. Um J.W., Nygaard H.B., Heiss J.K., Kostylev M.A., Stagi M., Vortmeyer A., Wisniewski T., Gunther E.C., Strittmatter S.M. Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 2012, 15:1227-1235.
33. Um J.W., Kaufman A.C., Kostylev M., Heiss J.K., Stagi M., Takahashi H., Kerrisk M.E., Vortmeyer A., Wisniewski T., Koleske A.J., Gunther E.C., Nygaard H.B., Strittmatter S.M. Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer abeta oligomer bound to cellular prion protein. Neuron 2013, 79:887-902.
34. Urwin H., Authier A., Nielsen J.E., Metcalf D., Powell C., Froud K., Malcolm D.S., Holm I., Johannsen P., Brown J., Fisher E.M., van der Zee J., Bruyland M., Consortium F.R., Van Broeckhoven C., Collinge J., Brandner S., Futter C., Isaacs A.M. Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations. Hum. Mol. Genet. 2010, 19:2228-2238.
35. Van Deerlin V.M., et al. Common variants at 7p21 are associated with frontotemporal lobar degeneration with TDP-43 inclusions. Nat. Genet. 2010, 42:234-239.
36. van der Zee J., Van Langenhove T., Kleinberger G., Sleegers K., Engelborghs S., Vandenberghe R., Santens P., Van den Broeck M., Joris G., Brys J., Mattheijssens M., Peeters K., Cras P., De Deyn P.P., Cruts M., Van Broeckhoven C. TMEM106B is associated with frontotemporal lobar degeneration in a clinically diagnosed patient cohort. Brain 2011, 134:808-815.
37. Vass R., Ashbridge E., Geser F., Hu W.T., Grossman M., Clay-Falcone D., Elman L., McCluskey L., Lee V.M., Van Deerlin V.M., Trojanowski J.Q., Chen-Plotkin A.S. Risk genotypes at TMEM106B are associated with cognitive impairment in amyotrophic lateral sclerosis. Acta Neuropathol. 2011, 121:373-380.
38. Wang I.F., Guo B.S., Liu Y.C., Wu C.C., Yang C.H., Tsai K.J., Shen C.K. Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15024-15029.
39. Westphal V., Rizzoli S.O., Lauterbach M.A., Kamin D., Jahn R., Hell S.W. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 2008, 320:246-249.
40. Yamada K., Matsushima R., Nishimura M., Hara-Nishimura I. A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves. Plant Physiol. 2001, 127:1626-1634.
41. Zdolsek J.M., Olsson G.M., Brunk U.T. Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem. Photobiol. 1990, 51:67-76.