Intracellular clusterin causes juxtanuclear aggregate formation and mitochondrial alteration

Journal of Cell Science

Volumn 116, Issue 15, 2003, Pages 3109-3121

  Debure, Laure ^a   Vayssière, Jean Luc ^b   Rincheval, Vincent ^b   Loison, Fabien ^a   Le Drŕean, Yves ^a   Michel, Denis ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

m; Aggresome; Apoptosis; Clusterin; Heart shock protein; Mitochondria

Indexed keywords

CASPASE; CLUSTERIN; PROTEIN BCL 2;

ALPHA CHAIN; ANIMAL CELL; APOPTOSIS; CELL COMPARTMENTALIZATION; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MITOCHONDRION; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; STRESS; UPREGULATION;

ANIMALS; APOPTOSIS; CASPASES; CELL NUCLEUS; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CLUSTERIN; COS CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; GLYCOPROTEINS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MITOCHONDRIA; MOLECULAR CHAPERONES; PROTEIN ISOFORMS; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-BCL-2; UBIQUITIN;

ANIMALIA;

EID: 0042887445     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00619     Document Type: Review

References (73)

1. Bailey, R. W., Dunker, A. K., Brown, C. J., Garner, E. C. and Griswold, M. D. (2001). Clusterin, a binding protein with a molten globule-like region. Biochemistry 40, 11828-11840.
2. Buttyan, R., Olsson, C. A., Pintar, J., Chang, C., Bandyk, M., Ng, P.-Y. and Sawczuk, I. S. (1989). Induction of the TRPM-2 gene in cells undergoing programmed death. Mol. Cell. Biol. 9, 3473-3481.
3. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K. and Varshavsky, A. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583.
4. Chung, K. K. K., Dawson, V. L. and Dawson, T. M. (2001). The role of the ubiquitin-proteasomal pathway in Parkinson's disease and other neurodegenerative disorders. Trends Neurosci. 24, S7-S14.
5. Cyr, D. M., Hohfeld, J. and Patterson, C. (2002). Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27, 368-375.
6. Danik, M., Chabot, J.-G., Hassan-Gonzalez, D., Suh, M. and Quirion, R. (1993). Localization of sulfated glycoprotein-2/clusterin mRNA in the rat brain by in situ hybridization. J. Comp. Neurol. 334, 209-227.
7. DeMattos, R. B., O'dell, M. A., Parsadanian, M., Taylor, J. W., Harmony, J. A., Bales, K. R., Paul, S. M., Aronow, B. J. and Holtzman, D. M. (2002). Clusterin promotes amyloid plaque formation and is critical for neuritic toxicity in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 99, 10843-10848.
8. Desagher, S. and Martinou, J. C. (2000). Mitochondria as the central control point of apoptosis. Trends Cell. Biol. 10, 369-377.
9. Dragunow, M., Preston, K., Dodd, J., Young, D., Lawlor, P. and Christie, D. (1995). Clusterin accumulates in dying neurons following status epilepticus. Mol. Brain Res. 32, 279-290.
10. Duguid, J. R., Bohmont, C. W., Liu, C. W. and Tourtelotte, W. W. (1989). Changes in brain gene expression shared by scrapie and Alzheimer disease. Proc. Natl. Acad. Sci. USA 86, 7260-7264.
11. Dul, J. L., Davis, D. P., Williamson, E. K., Stevens, F. J. and Argon, Y. (2001). Hsp70 and antifibrillogenic peptides promote degradation and inhibit intracellular aggregation of amyloidogenic light chains. J. Cell Biol. 152, 705-716.
12. Fabunmi, R. P., Wigley, W. C., Thomas, P. J. and DeMartino, G. N. (2000). Activity and regulation of the centrosome-associated proteasome. J. Biol. Chem. 275, 409-413.
13. Falnes, P. O. and Sandvig, K. (2000). Penetration of protein toxins into cells. Curr. Opin. Cell. Biol. 12, 407-413.
14. Fujihara, S. M. and Nadler, S. G. (1999). Intranuclear targeted delivery of functional NF-κB by 70 kDa heat shock protein. EMBO J. 18, 411-419.
15. Garcia-Mata, R., Bebok, Z., Sorscher, E. J. and Sztul, E. S. (1999). Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146, 1239-1254.
16. Graves, T. K., Patel, S., Dannies, P. S. and Hinkle, P. M. (2001). Misfolded growth hormone causes fragmentation of the Golgi apparatus and disrupts endoplasmic reticulum-to-Golgi traffic. J. Cell. Sci. 114, 3685-3694.
17. Gray, D. A. (2001). Damage control - a possible non-proteolytic role for ubiquitin in limiting neurodegeneration. Neuropathol. Appl. Neurobiol. 27, 89-94.
18. Grewal, R. P., Morgan, T. E. and Finch, C. E. (1999). C1qB and clusterin mRNA increase in association with neurodegeneration in sporadic amyotrophic lateral sclerosis. Neurosci. Lett. 271, 65-67.
19. Guenette, R. S., Corbeil, H. B., Léger, J., Wong, K., Mézl, V., Mooibroek, M. and Tenniswod, M. (1994). Induction of gene expression during involution of the lactating mammary gland of the rat. J. Mol. Endocrinol. 12, 47-60.
20. Han, B. H., DeMattos, R. B., Dugan, L. L., Kim-Han, J. S., Brendza, R. P., Fryer, J. D., Kierson, M., Cirrito, J., Quick, K., Harmony, J. A. et al. (2001). Clusterin contributes to caspase-3-independent brain injury following neonatal hypoxia-ischemia. Nat. Med. 7, 338-343.
21. Hu, B. R., Martone, M. E., Jones, Y. Z. and Liu, C. L. (2000). Protein aggregation after transient cerebral ischemia. J. Neurosci. 20, 3191-3199.
22. Humphreys, D. T., Carver, J. A., Easterbrook-Smith, S. B. and Wilson, M. R. (1999). Clusterin has chaperone-like activity similar to that of small heat shock proteins. J. Biol. Chem. 274, 6875-6881.
23. Iwaki, T., Kume-Iwaki, A., Liem, R. K. and Goldman, J. E. (1989). α B-Crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57, 71-78.
24. Johnston, J. A., Ward, C. L. and Kopito, R. R. (1998). Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898.
25. Jomary, C., Chatelain, G., Michel, D., Weston, A., Neal, M. J. and Jones, S. E. (1999). Effect of targeted expression of clusterin in photoreceptor cells on retinal development and differentiation. J. Cell. Sci. 112, 1455-1464.
26. Jones, S. E. and Jomary, C. (2002). Clusterin. Int. J. Biochem. Cell. Biol. 34, 427-431.
27. Kakizuka, A. (1998). Protein precipitation: a common etiology in neurodegenerative disorders? Trends Genet. 14, 396-402.
28. Kaufmann, S. H. and Hengartner, M. O. (2001). Programmed cell death: alive and well in the new millennium. Trends Cell Biol. 11, 526-534.
29. Kopito, R. R. (2000). Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530.
30. Kounnas, M. Z., Loukinova, E. B., Stefansson, S., Harmony, J. A., Brewer, B. H., Strickland, D. K. and Argraves, W. S. (1995). Identification of glycoprotein 330 as an endocytic receptor for apolipoprotein J/clusterin. J. Biol. Chem. 270, 13070-13075.
31. Kroemer, G., Petit, P., Zamzami, N., Vayssière, J. L. and Mignotte, B. (1995). The biochemistry of programmed cell death. FASEB J. 9, 1277-1287.
32. LaFerla, F. M., Troncoso, J. C., Strickland, D. K., Kawas, C. H. and Jay, G. (1997). Neuronal cell death in Alzheimer's disease correlates with apoE uptake and intracellular Abeta stabilization. J. Clin. Invest. 100, 310-320.
33. Lakins, J., Bennett, S. A., Chen, J. H., Arnold, J. M., Morrissey, C., Wong, P., O'Sullivan, J. and Tenniswood, M. (1998). Clusterin biogenesis is altered during apoptosis in the regressing rat ventral prostate. J. Biol. Chem. 273, 27887-27895.
34. Li, H., Zhu, H., Xu, C. J. and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
35. Macho, A., Decaudin, D., Castedo, M., Hirsch, T., Susin, S. A., Zamzami, N. and Kroemer, G. (1996). Chloromethyl-X-Rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 25, 333-340.
36. Mahon, M. G., Lindstedt, K. A., Hermann, M., Nimpf, J. and Schneider, W. J. (1999). Multiple involvement of clusterin chicken ovarian follicle development. Binding to two oocyte-specific members of the low density lipoprotein receptor gene family. J. Biol. Chem. 274, 4036-4044.
37. Matsubara, E., Soto, C., Governale, S., Frangione, B. and Ghiso, J. (1996). Apolipoprotein J and Alzheimer's amyloid beta solubility. Biochem. J. 316, 671-679.
38. May, P. C. and Finch, C. E. (1992). Sulfated glycoprotein 2: new relationships of this multifunctional protein to neurodegeneration. Trends Neurosci. 15, 391-396,
39. McCarthy, N. J., Whyte, M. K. B., Gilbert, C. S. and Evan, G. I. (1997). Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or Bc1-2 homologue Bak. J. Cell Biol. 136, 215-227.
40. McGeer, P. L., Kawamata, T. and Walker, D. G. (1992). Distribution of clusterin in Alzheimer brain tissue. Brain Res. 579, 337-341.
41. McHattie, S. and Edington, N. (1999). Clusterin prevents aggregation of neuropeptide 106-126 in vitro. Biochem. Biophys. Res. Commun. 259, 336-340.
42. Michel, D., Chabot, J.-G., Moyse, E., Danik, M. and Quirion, R. (1992). Possible functions of a new genetic marker in central nervous system: the sulfated glycoprotein-2 (SGP-2). Synapse 11, 105-111.
43. Michel, D., Moyse, E., Brun, G. and Jourdan, F. (1994). Induction of apoptosis in mouse olfactory neuroepithelium by synaptic target ablation. Neuroreport 5, 1329-1332.
44. Michel, D., Chatelain, G., North, S. and Brun, G. (1997a). Stress-induced transcription of the clusterin/apoJ gene. Biochem. J. 328, 45-50.
45. Michel, D., Moyse, E., Trembleau, A., Jourdan, F. and Brun, G. (1997b). Clusterin/ApoJ expression is associated with neuronal apoptosis in the olfactory mucosa of the adult mouse. J. Cell. Sci. 110, 1635-1645.
46. Multhoff, G. and Hightower, L. E. (1996). Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones 1, 167-176.
47. Newnam, G. P., Wegrzyn, R. D., Lindquist, S. L. and Chernoff, Y. O. (1999). Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol. Cell. Biol. 19, 1325-1333.
48. Norman, D. J., Feng, L., Cheng, S. S., Gubbay, J., Chan, E. and Heintz, N. (1995). The lurcher gene induces apoptotic death in cerebellar Purkinje cells. Development 121, 1183-1193.
49. Pasinetti, G. M., Johnson, S. A., Oda, T., Rozovsky, I. and Finch, C. E. (1994). Clusterin (SGP-2): a multifunctional glycoprotein with regional expression in astrocytes and neurons of the adult rat brain. J. Comp. Neurol. 339, 387-400.
50. Poon, S., Easterbrook-Smith, S. B., Rybchyn, M. S., Carver, J. A. and Wilson, M. R. (2000). Clusterin is an ATP-independent chaperone with very broad substrate specificity that stabilizes stressed proteins in a folding-competent state. Biochemistry 39, 15953-15960.
51. Poon, S., Treweek, T. M., Wilson, M. R., Easterbrook-Smith, S. B. and Carver, J. A. (2002a). Clusterin is an extracellular chaperone that specifically interacts with slowly aggregating proteins on their off-folding pathway. FEBS Lett. 513, 259-266.
52. Poon, S., Rybchyn, M. S., Easterbrook-Smith, S. B., Carver, J. A., Pankhurst, G. J. and Wilson, M. R. (2002b). Mildly acidic pH activates the extracellular molecular chaperone clusterin. J. Biol. Chem. 277, 39532-39540.
53. Poot, M., Zhang, Y. Z., Kramer, J. A., Wells, K. S., Jones, L. J., Hanzel, D. K., Lugade, A. G., Singer, V. L. and Haugland, R. P. (1996). Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 44, 1363-1372.
54. Rakhit, R., Cunningham, P., Furtos-Matei, A., Dahan, S., Qi, X. F., Crow, J., Cashman, N. R., Kondejewski, L. H. and Chakrabartty, A. (2002). Oxidation-induced misfolding and aggregation of superoxide dismutase and Its implications for amyotrophic lateral sclerosis. J. Biol. Chem. 277, 47551-47556.
55. Reddy, K. B., Jin, G., Karode, M. C., Harmony, J. A. K. and Howe, P. H. (1996). Transforming growth factor β (TGFβ -induced nuclear localization of Apolipoprotein J/Clusterin in epithelial cells. Biochemistry 35, 6157-6163.
56. Sakahira, H., Breuer, P., Hayer-Hartl, M. K. and Hartl, F. U. (2002). Molecular chaperones as modulators of polyglutamine protein aggregation and toxicity. Proc. Natl. Acad. Sci. USA 99 Suppl. 4, 16412-16418.
57. Saliba, R. S., Munro, P. M., Luthert, P. J. and Cheetham, M. E. (2002). The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J. Cell Sci. 115, 2907-2918.
58. Sasaki, K., Doh-Ura, K., Ironside, J. W. and Iwaki, T. (2002a). Increased clusterin (apolipoprotein J) expression in human and mouse brains infected with transmissible spongiform encephalopathies. Acta Neuropathol. 103, 199-208.
59. Sasaki, K., Doh-Ura, K., Wakisaka, Y. and Iwaki, T. (2002b). Clusterin/apolipoprotein J is associated with cortical Lewy bodies: immunohistochemical study in cases with alpha-synucleinopathies. Acta Neuropathol. 104, 225-230.
60. Sensibar, J. A., Sutkowski, D. M., Raffo, A., Buttyan, R., Griswold, M. D., Sylvester, S. R., Kozlowski, J. M. and Lee, C. (1995). Prevention of cell death induced by tumor necrosis factor alpha in LNCaP cells by overexpression of sulfated glycoprotein-2 (clusterin). Cancer Res. 55, 2431-2437.
61. Senut, M. C., Jazat, F., Choi, N. H. and Lamour, Y. (1992). Protein SP40,40-like imunoreactivity in the rat brain - progressive increase with age. Eur. J. Neurosci. 4, 917-928.
62. Simpson, J. C., Roberts, L. M., Romisch, K., Davey, J., Wolf, D. H. and Lord, J. M. (1999). Ricin A chain utilises the endoplasmic reticulum-associated protein degradation pathway to enter the cytosol of yeast. FEBS Lett. 459, 80-84.
63. Sourisseau, T., Desbois, C., Debure, L., Bowtell, D. D., Cato, A. C., Schneikert, J., Moyse, E. and Michel, D. (2001). Alteration of the stability of Bag-1 protein in the control of olfactory neuronal apoptosis. J. Cell Sci. 114, 1409-1416.
64. Stieber, A., Gonatas, J. O. and Gonatas, N. K. (2000). Aggregates of mutant protein appear progressively in dendrites, in periaxonal processes of oligodendrocytes, and in neuronal and astrocytic perikarya of mice expressing the SOD1(G93A) mutation of familial amyotrophic lateral sclerosis. J. Neurol. Sci. 177, 114-123.
65. Tamaoka, A., Mizusawa, H., Mori, H. and Shoji, S. (1995). Ubiquitinated α B-crystallin in glial cytoplasmic inclusions from the brain of a patient with multiple system atrophy. J. Neurol. Sci. 129, 192-198.
66. Tytell, M., Greenberg, S. G. and Lasek, R. J. (1986). Heat shock-like protein is transferred from glia to axon. Brain Res. 363, 161-164.
67. Vayssière, J. L., Petit, P. X., Risler, Y. and Mignotte, B. (1994). Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with Simian Virus 40. Proc. Natl. Acad. Sci. USA 91, 11752-11756.
68. Waelter, S., Boeddrich, A., Lurz, R., Scherzinger, E., Lueder, G., Lehrach, H. and Wanker, E. E. (2001). Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol. Biol. Cell 12, 1393-1407.
69. Walton, M., Young, D., Sirimanne, E., Dodd, J., Christie, D., Williams, C., Gluckman, P. and Dragunow, M. (1996). Induction of clusterin in the immature brain following a hypoxic-ischemic injury. Mol. Brain Res. 39, 137-152.
70. Wehrli, P., Charnay, Y., Vallet, P., Zhu, G., Harmony, J., Aronow, B., Tschopp, J., Bouras, C., Viard-Leveugle, I., French, L. E. et al. (2001). Inhibition of post-ischemic brain injury by clusterin overexpression. Nat. Med. 7, 977-978.
71. Wilson, M. R. and Easterbrook-Smith, S. B. (2000). Clusterin is a secreted mammalian chaperone. Trends Biochem. Sci. 25, 95-98.
72. Wyttenbach, A., Carmichael, J., Swartz, J., Furlong, R. A., Narain, Y., Rankin, J. and Rubinsztein, D. C. (2000). Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease. Proc. Natl. Acad. Sci. USA 97, 2898-2903.
73. Yang, C. R., Leskov, K., Hosley-Eberlein, K., Criswell, T., Pink, J. J., Kinsella, T. J. and Boothman, D. A. (2000). Nuclear clusterin/XIP8, an X-ray-induced Ku70-binding protein that signals cell death. Proc. Natl. Acad. Sci. USA 97, 5907-5912.