J protein mutations and resulting proteostasis collapse

Frontiers in Cellular Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Koutras, Carolina ^a   Braun, Janice E A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Auxilin; CSP ; HSJ1; Hsp40; Mrj; Rme 8; Sacsin; Tim14

Indexed keywords

AUXILIN; CHAPERONE; CSP ALPHA PROTEIN; DNAJC29 PROTEIN; HEAT SHOCK COGNATE PROTEIN 70; PROTEIN DNAJ; PROTEIN DNAJB2; PROTEIN DNAJC13; PROTEIN DNAJC19; PROTEIN J; SACSIN; UNCLASSIFIED DRUG;

AGING; ARTICLE; ATAXIA; DNAJB2 GENE; DNAJB6 GENE; DNAJC13 GENE; DNAJC19 GENE; DNAJC29 GENE; DNAJC5 GENE; DNAJC6 GENE; GENE; GENE MUTATION; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; MENTAL DEFICIENCY; MOTOR NEUROPATHY; MUTATION; NERVE DEGENERATION; NEURONAL CEROID LIPOFUSCINOSIS; NEUROTRANSMISSION; NONHUMAN; PARKINSONISM; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN MISFOLDING; SYNAPSE VESICLE;

EID: 84904040867     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00191     Document Type: Article

References (82)

1. Ahrendt, E., Kyle, B., Braun, A. P., and Braun, J. E. (2014). Cysteine string protein limits expression of the large conductance, calcium-activated K(+) (BK) channel. PLoS One 9:e86586. doi: 10.1371/journal.pone.0086586
2. Anderson, G. W., Goebel, H. H., and Simonati, A. (2013). Human pathology in NCL. Biochim. Biophys. Acta 1832, 1807-1826. doi: 10.1016/j.bbadis.2012.11. 014
3. Andrews, J. F., Sykora, L. J., Letostak, T. B., Menezes, M. E., Mitra, A., Barik, S., et al. (2012). Cellular stress stimulates nuclear localization signal (NLS) independent nuclear transport of MRJ. Exp. Cell Res. 318, 1086-1093. doi: 10.1016/j.yexcr. 2012.03.024
4. Baets, J., Deconinck, T., Smets, K., Goossens, D., Van den Bergh, P., Dahan, K., et al. (2010). Mutations in SACS cause atypical and late-onset forms ofARSACS. Neurology 75, 1181-1188. doi: 10.1212/wnl.0b013e3181f4d86c
5. Benitez, B. A., Alvarado, D., Cai, Y., Mayo, K., Chakraverty, S., Norton, J., et al. (2011). Exome-sequencing confirms DNAJC5 mutations as cause of adult neuronal ceroid-lipofuscinosis. PLoS One 6:e26741. doi: 10.1371/journal.pone. 0026741
6. Blumen, S. C., Astord, S., Robin, V., Vignaud, L., Toumi, N., Cieslik, A., et al. (2012). A rare recessive distal hereditary motor neuropathy with HSJ1 chaperone mutation. Ann. Neurol. 71, 509-519. doi: 10.1002/ana.22684
7. Boillee, S., Berruti, G., Meccariello, R., Grannec, G., Razan, F., Pierantoni, R., et al. (2002). Early defect in the expression of mouse sperm DNAJ 1, a member of the DNAJ/heat shock protein 40 chaperone protein family, in the spinal cord of the wobbler mouse, a murine model of motoneuronal degeneration. Neuroscience 113, 825-835. doi: 10.1016/s0306-4522(02)00235-x
8. Bouchard, J. P., Barbeau, A., Bouchard, R., and Bouchard, R. W. (1978). Autosomal recessive spastic ataxia of Charlevoix-Saguenay. Can. J. Neurol. Sci. 5, 61-69.
9. Braun, J. E., and Scheller, R. H. (1995). Cysteine string protein, a DnaJ family member, is present on diverse secretory vesicles. Neuropharmacology 34, 1361-1369. doi: 10.1016/0028-3908(95)00114-l
10. Brown, H., Larsson, O., Bränström, R., Yang, S., Leibiger, B., Leibiger, I., et al. (1998). Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating beta-cell exocytosis. EMBO J. 17, 5048-5058. doi: 10. 1093/emboj/17.17.5048
11. Chamberlain, L. H., Henry, J., and Burgoyne, R. D. (1996). Cysteine string proteins are associated with chromaffin granules. J. Biol. Chem. 271, 19514-19517. doi: 10.1074/jbc.271.32.19514
12. Chandra, S., Gallardo, G., Fernândez-Chacön, R., Schlüter, O. M., and Südhof, T. C. (2005).Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123, 383-396. doi: 10.1016/j.cell.2005.09.028
13. Chang, H. C., Hull, M., and Mellman, I. (2004). The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. J. Cell. Biol. 164, 1055-1064. doi: 10.1083/jcb.200311084
14. Chapple, J. P., and Cheetham, M. E. (2003). The chaperone environment at the cytoplasmic face of the endoplasmic reticulum can modulate rhodopsin processing and inclusion formation. J. Biol. Chem. 278, 19087-19094. doi: 10. 1074/jbc.m212349200
15. Chapple, J. P., van der, S. J., Poopalasundaram, S., and Cheetham, M. E. (2004). Neuronal DnaJ proteins HSJ1aand HSJ1b: a role in linking the Hsp70 chaperone machine to the ubiquitin-proteasome system? Biochem. Soc. Trans. 32, 640-642. doi: 10.1042/bst0320640
16. Cheetham, M. E., Brion, J. P., and Anderton, B. H. (1992). Human homologues of the bacterial heat-shock protein DnaJ are preferentially expressed in neurons. Biochem. J. 284, 469-476.
17. Chuang, J. Z., Zhou, H., Zhu, M., Li, S. H., Li, X. J., and Sung, C. H. (2002). Characterization of a brain-enriched chaperone, MRJ, that inhibits huntingtin aggregation and toxicity independently. J. Biol. Chem. 277, 19831-19838. doi: 10.1074/jbc.m109613200
18. Dai, Y. S., Xu, J., and Molkentin, J. D. (2005). The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol. Cell. Biol. 25, 9936-9948. doi: 10.1128/mcb.25.22.9936-9948.2005
19. Davey, K. M., Parboosingh, J. S., McLeod, D. R., Chan, A., Casey, R., Ferreira, P., et al. (2006). Mutation of DNAJC19, a human homologue of yeast inner mitochondrial membrane co-chaperones, causes DCMA syndrome, a novel autosomal recessive Barth syndrome-like condition. J. Med. Genet. 43, 385-393. doi: 10.1136/jmg.2005.036657
20. Donnelier, J., and Braun, J. E. (2014). CSPalpha-chaperoning presynaptic proteins. Front. Cell Neurosci. 8:116. doi: 10.3389/fncel.2014.00116
21. Durrenberger, P. F., Filiou, M. D., Moran, L. B., Michael, G. J., Novoselov, S., Cheetham, M. E., et al. (2009). DnaJB6 is present in the core of Lewy bodies and is highly up-regulated in parkinsonian astrocytes. J. Neurosci. Res. 87, 238-245. doi: 10.1002/jnr.21819
22. Edvardson, S., Cinnamon, Y., Ta-Shma, A., Shaag, A., Yim, Y. I., Zenvirt, S., et al. (2012). A deleterious mutation in DNAJC6 encoding the neuronal- specific clathrin-uncoating co-chaperone auxilin, is associated with juvenile parkinsonism. PLoS One 7:e36458. doi: 10.1371/journal.pone.0036458
23. Eisenberg, E., and Greene, L. E. (2007). Multiple roles of auxilin and hsc70 in clathrin-mediated endocytosis. Traffic 8, 640-646. doi: 10.1111/j.1600-0854. 2007.00568.x
24. Engert, J. C., Berube, P., Mercier, J., Dore, C., Lepage, P., Ge, B., et al. (2000). ARSACS, a spastic ataxia common in northeastern Quebec, is caused by mutations in anewgene encoding an 11.5-kb ORF. Nat. Genet. 24, 120-125. doi: 10. 1038/72769
25. Fernândez-Chacon, R., Wolfel, M., Nishimune, H., Tabares, L., Schmitz, F., Castellano-Munoz, M., et al. (2004). The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42, 237-251. doi: 10.1016/s0896- 6273(04)00190-4
26. Freeman, C. L., Hesketh, G., and Seaman, M. N. (2014). RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J. Cell Sci. 127, 2053-2070. doi: 10.1242/jcs. 144659
27. Gao, X. C., Zhou, C. J., Zhou, Z. R., Zhang, Y. H., Zheng, X. M., Song, A. X., et al. (2011). Co-chaperone HSJ1a dually regulates the proteasomal degradation of ataxin-3. PLoS One 6:e19763. doi: 10.1371/journal.pone.001 9763
28. Garcia-Junco-Clemente, P., Cantero, G., Gomez-Sanchez, L., Linares-Clemente, P., Martinez-Lopez, J. A., Lujan, R., et al. (2010). Cysteine string protein-alpha prevents activity-dependent degeneration in GABAergic synapses. J. Neurosci. 30, 7377-7391. doi: 10.1523/jneurosci.0924-10.2010
29. Georgopoulos, C. P., Lundquist-Heil, A., Yochem, J., and Feiss, M. (1980). Identification of the E. coli. DnaJ gene product. Mol. Gen. Genet. 178, 583-588. doi: 10. 1007/BF00337864
30. Girard, M., Lariviere, R., Parfitt, D. A., Deane, E. C., Gaudet, R., Nossova, N., et al. (2012). Mitochondrial dysfunction and Purkinje cell loss in autosomal recessive spastic ataxia of Charlevoix-Saguenay (ARSACS). Proc. Natl. Acad. Sci. USA 109, 1661-1666. doi: 10.1073/pnas.1113166109
31. Girard, M., and McPherson, P. S. (2008). RME-8 regulates trafficking of the epidermal growth factor receptor. FEBS Lett. 582, 961-966. doi: 10.1016/j. febslet.2008.02.042
32. Girard, M., Poupon, V., Blondeau, F., and McPherson, P. S. (2005). The DnaJ- domain protein RME-8 functions in endosomal trafficking. J. Biol. Chem. 280, 40135-40143. doi: 10.1074/jbc.m505036200
33. Hageman, J., Rujano, M. A., van Waarde, M. A., Kakkar, V., Dirks, R. P., Govorukhina, N., et al. (2010). A DNAJB chaperone subfamily with HDAC- dependent activities suppresses toxic protein aggregation. Mol. Cell 37, 355-369. doi: 10.1016/j.molcel.2010.01.001
34. Hanai, R., and Mashima, K. (2003). Characterization of two isoforms of a human DnaJ homologue, HSJ2. Mol. Biol. Rep. 30, 149-153. doi: 10.1379/1466- 1268(2003)8<8:cotama>2.0.co;2
35. Harms, M. B., Sommerville, R. B., Allred, P., Bell, S., Ma, D., Cooper, P., et al. (2012). Exome sequencing reveals DNAJB6 mutations in dominantly-inherited myopathy. Ann. Neurol. 71, 407-416. doi: 10.1002/ana.22683
36. Howarth, J. L., Kelly, S., Keasey, M. P., Glover, C. P., Lee, Y. B., Mitrophanous, K., et al. (2007). Hsp40 molecules that target to the ubiquitin-proteasome system decrease inclusion formation in models ofpolyglutamine disease. Mol. Ther. 15, 1100-1105. doi: 10.1038/sj.mt.6300163
37. Hunter, P. J., Swanson, B. J., Haendel, M. A., Lyons, G. E., and Cross, J. C. (1999). Mrj encodes a DnaJ-related co-chaperone that is essential for murine placental development. Development 126, 1247-1258.
38. Kakkar, V., Prins, L. C., and Kampinga, H. H. (2012). DNAJ proteins and protein aggregation diseases. Curr. Top. Med. Chem. 12, 2479-2490. doi: 10. 2174/1568026611212220004
39. Kampinga, H. H., and Craig, E. A. (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. CellBiol. 11, 579-592. doi: 10.1038/nrm2941
40. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., and Hartl, F. U. (2013). Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355. doi: 10.1146/annurev-biochem-060208-092442
41. Köroglu, C., Baysal, L., Cetinkaya, M., Karasoy, H., andTolun, A. (2013). DNAJC6is responsible for juvenile parkinsonism with phenotypic variability. Parkinsonism Relat. Disord. 19, 320-324. doi: 10.1016/j.parkreldis.2012.11.006
42. Kozlov, G., Denisov, A. Y., Girard, M., Dicaire, M. J., Hamlin, J., McPherson, P. S., et al. (2011). Structural basis of defects in the sacsin HEPN domain responsible for autosomal recessive spastic ataxia ofCharlevoix-Saguenay(ARSACS). J. Biol. Chem. 286, 20407-20412. doi: 10.1074/jbc.M111.232884
43. Kyle, B. D., Ahrendt, E., Braun, A. P., and Braun, J. E. (2013). The large conductance, calcium-activated K(+) (BK) channel is regulated by cysteine string protein. Sci. Rep. 3:2447. doi: 10.1038/srep02447
44. Labbadia, J., and Morimoto, R. I. (2014). Proteostasis and longevity: when does aging really begin? F1000Prime. F1000Prime Rep. 6:7. doi: 10.12703/ p6-07
45. Labbadia, J., Novoselov, S. S., Bett, J. S., Weiss, A., Paganetti, P., Bates, G. P., et al. (2012). Suppression of protein aggregation by chaperone modification of high molecular weight complexes. Brain 135, 1180-1196. doi: 10.1093/brain/aws022
46. Li, N. N., Chang, X. L., Mao, X. Y., Zhang, J. H., Zhao, D. M., Tan, E. K., et al. (2012). GWAS-linked GAK locus in Parkinson's disease in Han Chinese and meta-analysis. Hum. Genet. 131, 1089-1093. doi: 10.1007/s00439-011- 1133-3
47. Mastrogiacomo, A., Parsons, S. M., Zampighi, G. A., Jenden, D. J., Umbach, J. A., and Gundersen, C. B. (1994). Cysteine string proteins: a potential link between synaptic vesicles and presynaptic Ca2+ channels. Science 263, 981-982. doi: 10. 1126/science.7906056
48. Mitsuhashi, S., and Kang, P. B. (2012). Update on the genetics of limb girdle muscular dystrophy. Semin. Pediatr. Neurol. 19, 211-218. doi: 10.1016/j.spen. 2012.09.008
49. Morgan, J. R., Jiang, J., Oliphint, P. A., Jin, S., Gimenez, L. E., Busch, D. J., et al. (2013). A role for an Hsp70 nucleotide exchange factor in the regulation of synaptic vesicle endocytosis. J. Neurosci. 33, 8009-8021. doi: 10.1523/jneurosci. 4505-12.2013
50. Morgan, J. R., Prasad, K., Jin, S., Augustine, G. J., and Lafer, E. M. (2001). Uncoating of clathrin-coated vesicles in presynaptic terminals: roles for Hsc70 and auxilin. Neuron 32, 289-300. doi: 10.1016/s0896-6273(01)00467-6
51. Muchowski, P. J., and Wacker, J. L. (2005). Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11-22. doi: 10.1038/nrn1587
52. Noskovâ, L., Stranecky, V., Hartmannova, H., Pristoupilova, A., Baresova, V., Ivanek, R., et al. (2011). Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am.J. Hum. Genet. 89, 241-252. doi: 10.1016/j.ajhg.2011.07.003
53. Novoselov, S. S., Mustill, W. J., Gray, A. L., Dick, J. R., Kanuga, N., Kalmar, B., et al. (2013). Molecular chaperone mediated late-stage neuroprotection in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. PLoS One 8:e73944. doi: 10.1371/journal.pone.0073944
54. Ohtsuka, K., Masuda, A., Nakai, A., and Nagata, K. (1990). A novel 40-kDa protein induced by heat shock and other stresses in mammalian and avian cells. Biochem. Biophys. Res. Commun. 166, 642-647. doi: 10.1016/0006- 291x(90)90857-j
55. Ojala, T., Polinati, P., Manninen, T., Hiippala, A., Rajantie, J., Karikoski, R., et al. (2012). New mutation of mitochondrial DNAJC19 causing dilated and noncompaction cardiomyopathy, anemia, ataxia and male genital anomalies. Pediatr. Res. 72, 432-437. doi: 10.1038/pr.2012.92
56. Parfitt, D. A., Michael, G. J., Vermeulen, E. G., Prodromou, N. V., Webb, T. R., Gallo, J. M., et al. (2009). The ataxia protein sacsin is afunctional co-chaperone that protects against polyglutamine-expanded ataxin-1. Hum. Mol. Genet. 18, 1556-1565. doi: 10.1093/hmg/ddp067
57. Popoff, V., Mardones, G. A., Bai, S. K., Chambon, V., Tenza, D., Burgos, P. V., et al. (2009). Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic 10, 1868-1880. doi: 10.1111/j.1600-0854. 2009.00993.x
58. Rose, J. M., Novoselov, S. S., Robinson, P. A., and Cheetham, M. E. (2011). Molecular chaperone-mediated rescue of mitophagyby aParkin RING1 domain mutant. Hum. Mol. Genet. 20, 16-27. doi: 10.1093/hmg/ddQ528
59. Rozas, J. L., Gomez-Sanchez, L., Mircheski, J., Linares-Clemente, P., Nieto- Gonzalez, J. L., Vazquez, M. E., et al. (2012). Motorneurons require cysteine string protein-alpha to maintain the readily releasable vesicular pool and synaptic vesicle recycling. Neuron 74, 151-165. doi: 10.1016/j.neuron.2012.02.019
60. Sarparanta, J., Jonson, P. H., Golzio, C., Sandell, S., Luque, H., Screen, M., et al. (2012). Mutations affecting the cytoplasmic functions of the co-chaperone DNAJB6 cause limb-girdle muscular dystrophy. Nat. Genet. 44, 450-452. doi: 10. 1038/ng.1103
61. Sato, T., Hayashi, Y. K., Oya, Y., Kondo, T., Sugie, K., Kaneda, D., et al. (2013). DNAJB6 myopathy in an Asian cohort and cytoplasmic/nuclear inclusions. Neuromuscul. Disord. 23, 269-276. doi: 10.1016/j.nmd.2012.12.010
62. Schmitz, F., Tabares, L., Khimich, D., Strenzke, N., de la Villa-Polo, P., Castellano- Munoz, M., et al. (2006). CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proc. Natl. Acad. Sci. USA 103, 2926-2931. doi: 10. 1073/pnas.0510060103
63. Sharma, M., Burre, J., and Sudhof, T. C. (2011). CSPalpha promotes SNARE- complex assembly by chaperoning SNAP-25 during synaptic activity. Nat. Cell Biol. 13, 30-39. doi: 10.1038/ncb2131
64. Sharma, M., Burre, J., Bronk, P., Zhang, Y., Xu, W., and Sudhof, T. C. (2012). CSPalpha knockout causes neurodegeneration by impairing SNAP-25 function. EMBO J. 31, 829-841. doi: 10.1038/emboj.2011.467
65. Sinha, D., Srivastava, S., Krishna, L., and D'Silva, P. (2014). Unraveling the intricate organization of Mammalian mitochondrial presequence translocases: existence of multiple translocases for maintenance of mitochondrial function. Mol. Cell. Biol. 34, 1757-1775. doi: 10.1128/MCB.01527-13
66. Soti, C., and Csermely, P. (2002). Chaperones come of age. Cell Stress Chaperones 7, 186-190. doi: 10.1379/1466-1268(2002)007%3C0186:CCOA%3E2.0.CO;2
67. Sparkes, R., Patton, D., and Bernier, F. (2007). Cardiac features of a novel autosomal recessive dilated cardiomyopathic syndrome due to defective importation of mitochondrial protein. Cardiol. Young 17, 215-217. doi: 10. 1017/s1047951107000042
68. Stevens, J. C., Murphy, S. M., Davagnanam, I., Phadke, R., Anderson, G., Nethisinghe, S., et al. (2013). The ARSACS phenotype can include supranuclear gaze palsy and skin lipofuscin deposits. J. Neurol. Neurosurg. Psychiatry 84, 114116. doi: 10.1136/jnnp-2012-303634
69. Suarez-Cedeno, G., Winder, T., and Milone, M. (2014). DNAJB6 myopathy: a vacuolar myopathy with childhood onset. Muscle Nerve 49, 607-610. doi: 10. 1002/mus.24106
70. Sundaram, S. K., Huq, A. M., Sun, Z., Yu, W., Bennett, L., Wilson, B. J., et al. (2011). Exome sequencing of a pedigree with Tourette syndrome or chronic tic disorder. Ann. Neurol. 69, 901-904. doi: 10.1002/ana.22398
71. Thiffault, I., Dicaire, M. J., Tetreault, M., Huang, K. N., Demers-Lamarche, J., Bernard, G., et al. (2013). Diversity of ARSACS mutations in French-Canadians. Can. J. Neurol. Sci. 40, 61-66.
72. Ungewickell, E., Ungewickell, H., Holstein, S. E. H., Linder, R., Prasad, K., Barouch, W., et al. (1995). Role of auxilin in uncoating clathrin-coated vesicles. Nature 378, 632-635. doi: 10.1038/378632a0
73. Vauthier, V., Jaillard, S., Journel, H., Dubourg, C., Jockers, R., and Dam, J. (2012). Homozygous deletion of an 80 kb region comprising part of DNAJC6 and LEPR genes on chromosome 1P31.3 is associated with early onset obesity, mental retardation and epilepsy. Mol. Genet. Metab. 106, 345-350. doi: 10. 1016/j.ymgme.2012.04.026
74. Velinov, M., Dolzhanskaya, N., Gonzalez, M., Powell, E., Konidari, I., Hulme, W., et al. (2012). Mutations in the gene DNAJC5 cause autosomal dominant kufs disease in a proportion of cases: study of the parry family and 8 other families. PLoS One 7:e29729. doi: 10.1371/journal.pone.0029729
75. Vilarino-Güell, C., Rajput, A., Milnerwood, A. J., Shah, B., Szu-Tu, C., Trinh, J., et al. (2014). DNAJC13 mutations in Parkinson disease. Hum. Mol. Genet. 23, 1794-1801. doi: 10.1093/hmg/ddt570
76. Watson, E. D., Geary-Joo, C., Hughes, M., and Cross, J. C. (2007). The Mrj co-chaperone mediates keratin turnover and prevents the formation of toxic inclusion bodies in trophoblast cells of the placenta. Development 134, 1809-1817. doi: 10.1242/dev.02843
77. Westhoff, B., Chapple, J. P., van der, S. J., Hohfeld, J., and Cheetham, M. E. (2005). HSJ1 is a neuronal shuttling factor for the sorting of chaperone clients to the proteasome. Curr. Biol. 15, 1058-1064. doi: 10.1016/j.cub.2005.04.058
78. Yim, Y. I., Sun, T., Wu, L. G., Raimondi, A., De, C. P., Eisenberg, E., et al. (2010). Endocytosis and clathrin-uncoating defects at synapses of auxilin knockout mice. Proc. Natl. Acad. Sci. USA 107, 4412-4417. doi: 10.1073/pnas.10007 38107
79. Zhang, Y., Grant, B., and Hirsh, D. (2001). RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell 12, 2011-2021. doi: 10.1091/mbc.12.7.2011
80. Zhang, Y. Q., Henderson, M. X., Colangelo, C. M., Ginsberg, S. D., Bruce, C., Wu, T., et al. (2012). Identification of CSPalpha clients reveals a role in dynamin 1 regulation. Neuron 74, 136-150. doi: 10.1016/j.neuron.2012. 01.029
81. Zhao, X., Braun, A. P., and Braun, J. E. (2008). Biological roles of neural J proteins. Cell. Mol. Life. Sci. 65, 2385-2396. doi: 10.1007/s00018-008-8089-z
82. Zinsmaier, K. E., Eberle, K. K., Buchner, E., Walter, N., and Benzer, S. (1994). Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263, 977-980. doi: 10.1126/science.8310297