Complement modulates the function of the ubiquitin-proteasome system and endoplasmic reticulum-associated degradation in glomerular epithelial cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 5, 2012, Pages 1007-1016

  Kitzler, Thomas M ^a   Papillon, Joan ^a   Guillemette, Julie ^a   Wing, Simon S ^a   Cybulsky, Andrey V ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Cell injury; Glomerulonephritis; Kidney; Protein kinase; Signal transduction

Indexed keywords

ANTIBODY; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; COMPLEMENT COMPONENT C8; COMPLEMENT MEMBRANE ATTACK COMPLEX; CYCLIN A; CYCLOHEXIMIDE; GREEN FLUORESCENT PROTEIN; PROTEASOME; STRESS ACTIVATED PROTEIN KINASE; UBIQUITIN; YELLOW FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; GLOMERULUS; MALE; MEMBRANOUS GLOMERULONEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; UBIQUITINATION;

ANIMALS; COMPLEMENT MEMBRANE ATTACK COMPLEX; COMPLEMENT SYSTEM PROTEINS; CYCLIN A; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; EPITHELIAL CELLS; GLOMERULONEPHRITIS, MEMBRANOUS; GREEN FLUORESCENT PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KIDNEY GLOMERULUS; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RATS; UBIQUITIN; UBIQUITINATION;

RATTUS;

EID: 84859181046     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.03.001     Document Type: Article

References (43)

1. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999, 13:1211-1233.
2. Caramelo J.J., Parodi A.J. Getting in and out from calnexin/calreticulin cycles. J. Biol. Chem. 2008, 283:10221-10225.
3. Ni M., Lee A.S. ER chaperones in mammalian development and human diseases. FEBS Lett. 2007, 581:3641-3651.
4. Dantuma N.P., Lindsten K. Stressing the ubiquitin-proteasome system. Cardiovasc. Res. 2010, 85:263-271.
5. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
6. Wilkinson K.D. Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin. Cell Dev. Biol. 2000, 11:141-148.
7. Zhu Q., Wani G., Wang Q.E., El-mahdy M., Snapka R.M., Wani A.A. Deubiquitination by proteasome is coordinated with substrate translocation for proteolysis in vivo. Exp. Cell Res. 2005, 307:436-451.
8. Bagola K., Mehnert M., Jarosch E., Sommer T. Protein dislocation from the ER. Biochim. Biophys. Acta 2011, 1808:925-936.
9. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 2008, 9:944-957.
10. Rutkowski D.T., Kaufman R.J. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem. Sci. 2007, 32:469-476.
11. Harding H.P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., Sabatini D.D., Ron D. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 2001, 7:1153-1163.
12. Kumar R., Azam S., Sullivan J.M., Owen C., Cavener D.R., Zhang P., Ron D., Harding H.P., Chen J.J., Han A., White B.C., Krause G.S., DeGracia D.J. Brain ischemia and reperfusion activates the eukaryotic initiation factor 2alpha kinase, PERK. J. Neurochem. 2001, 77:1418-1421.
13. Takahashi R., Imai Y., Hattori N., Mizuno Y. Parkin and endoplasmic reticulum stress. Ann. N. Y. Acad. Sci. 2003, 991:101-106.
14. Cybulsky A.V., Takano T., Papillon J., Khadir A., Liu J., Peng H. Complement C5b-9 membrane attack complex increases expression of endoplasmic reticulum stress proteins in glomerular epithelial cells. J. Biol. Chem. 2002, 277:41342-41351.
15. Cybulsky A.V., Takano T., Papillon J., Bijian K. Role of the endoplasmic reticulum unfolded protein response in glomerular epithelial cell injury. J. Biol. Chem. 2005, 280:24396-24403.
16. Inagi R., Nangaku M., Onogi H., Ueyama H., Kitao Y., Nakazato K., Ogawa S., Kurokawa K., Couser W.G., Miyata T. Involvement of endoplasmic reticulum (ER) stress in podocyte injury induced by excessive protein accumulation. Kidney Int. 2005, 68:2639-2650.
17. Inagi R., Kumagai T., Nishi H., Kawakami T., Miyata T., Fujita T., Nangaku M. Preconditioning with endoplasmic reticulum stress ameliorates mesangioproliferative glomerulonephritis. J. Am. Soc. Nephrol. 2008, 19:915-922.
18. Cybulsky A.V. Membranous nephropathy. Contrib. Nephrol. 2011, 169:107-125.
19. Cybulsky A.V., Quigg R.J., Salant D.J. Experimental membranous nephropathy redux. Am. J. Physiol. Renal Physiol. 2005, 289:F660-F671.
20. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001, 292:1552-1555.
21. Treier M., Staszewski L.M., Bohmann D. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 1994, 78:787-798.
22. Menendez-Benito V., Verhoef L.G., Masucci M.G., Dantuma N.P. Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Hum. Mol. Genet. 2005, 14:2787-2799.
23. Cybulsky A.V., Takano T., Guillemette J., Papillon J., Volpini R.A., Di Battista J.A. The Ste20-like kinase SLK promotes p53 transactivation and apoptosis. Am. J. Physiol. Renal Physiol. 2009, 297:F971-F980.
24. Coers W., Reivinen J., Miettinen A., Huitema S., Vos J.T., Salant D.J., Weening J.J. Characterization of a rat glomerular visceral epithelial cell line. Exp. Nephrol. 1996, 4:184-192.
25. Quigg R.J., Cybulsky A.V., Jacobs J.B., Salant D.J. Anti-Fx1A produces complement-dependent cytotoxicity of glomerular epithelial cells. Kidney Int. 1988, 34:43-52.
26. Cybulsky A.V., Papillon J., McTavish A.J. Complement activates phospholipases and protein kinases in glomerular epithelial cells. Kidney Int. 1998, 54:360-372.
27. Gilon T., Chomsky O., Kulka R.G. Degradation signals recognized by the Ubc6p-Ubc7p ubiquitin-conjugating enzyme pair. Mol. Cell. Biol. 2000, 20:7214-7219.
28. Peng H., Takano T., Papillon J., Bijian K., Khadir A., Cybulsky A.V. Complement activates the c-Jun N-terminal kinase/stress-activated protein kinase in glomerular epithelial cells. J. Immunol. 2002, 169:2594-2601.
29. Barrett A.J., Kembhavi A.A., Brown M.A., Kirschke H., Knight C.G., Tamai M., Hanada K. l-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem. J. 1982, 201:189-198.
30. Lee D.H., Goldberg A.L. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 1998, 8:397-403.
31. Yang M., Omura S., Bonifacino J.S., Weissman A.M. Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes. J. Exp. Med. 1998, 187:835-846.
32. Klausner R.D., Lippincott-Schwartz J., Bonifacino J.S. The T cell antigen receptor: insights into organelle biology. Annu. Rev. Cell Biol. 1990, 6:403-431.
33. Kuball J., Hauptrock B., Malina V., Antunes E., Voss R.H., Wolfl M., Strong R., Theobald M., Greenberg P.D. Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J. Exp. Med. 2009, 206:463-475.
34. Bennett E.J., Bence N.F., Jayakumar R., Kopito R.R. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell 2005, 17:351-365.
35. Kumarapeli A.R., Horak K.M., Glasford J.W., Li J., Chen Q., Liu J., Zheng H., Wang X. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J. 2005, 19:2051-2053.
36. Dantuma N.P., Lindsten K., Glas R., Jellne M., Masucci M.G. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 2000, 18:538-543.
37. Meyer-Schwesinger C., Meyer T.N., Sievert H., Hoxha E., Sachs M., Klupp E.M., Munster S., Balabanov S., Carrier L., Helmchen U., Thaiss F., Stahl R.A. Ubiquitin C-terminal hydrolase-l1 activity induces polyubiquitin accumulation in podocytes and increases proteinuria in rat membranous nephropathy. Am. J. Pathol. 2011, 178:2044-2057.
38. Liu J., Zheng H., Tang M., Ryu Y.C., Wang X. A therapeutic dose of doxorubicin activates ubiquitin-proteasome system-mediated proteolysis by acting on both the ubiquitination apparatus and proteasome. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H2541-H2550.
39. Kim S.J., Park K.M., Kim N., Yeom Y.I. Doxorubicin prevents endoplasmic reticulum stress-induced apoptosis. Biochem. Biophys. Res. Commun. 2006, 339:463-468.
40. Cohen P., Tcherpakov M. Will the ubiquitin system furnish as many drug targets as protein kinases?. Cell 2010, 143:686-693.
41. Gallagher E., Gao M., Liu Y.C., Karin M. Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1717-1722.
42. Meyer-Schwesinger C., Meyer T., Munster S., Klug P., Saleem M., Helmchen U., Stahl R. A new role for the neuronal ubiquitin C-terminal hydrolase-L1 (UCH-L1) in podocyte process formation and podocyte injury in human glomerulopathies. J. Pathol. 2009, 217:452-464.
43. Hauser P.V., Perco P., Muhlberger I., Pippin J., Blonski M., Mayer B., Alpers C.E., Oberbauer R., Shankland S.J. Microarray and bioinformatics analysis of gene expression in experimental membranous nephropathy. Nephron Exp. Nephrol. 2009, 112:e43-e58.