Iron-dependent degradation of apo-IRP1 by the ubiquitin-proteasome pathway

Molecular and Cellular Biology

Volumn 27, Issue 7, 2007, Pages 2423-2430

  Wang, Jian ^a,d   Fillebeen, Carine ^a   Chen, Guohua ^a,d   Biederbick, Annette ^b   Lill, Roland ^b   Pantopoulos, Kostas ^a,c  

^a MCGILL UNIVERSITY   (Canada)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYSTATHIONINE GAMMA LYASE; CYSTEINE; FERRIC AMMONIUM CITRATE; IRON; IRON REGULATORY PROTEIN 1; IRON SULFUR PROTEIN; LACTACYSTIN; MESSENGER RNA; MUTANT PROTEIN; PROTEASOME; SERINE; SMALL INTERFERING RNA; UBIQUITIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL STRAIN; CONTROLLED STUDY; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IRON RESPONSIVE ELEMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STABILITY; REGULATORY MECHANISM; RNA INTERFERENCE; RNA STABILITY; TRANSLATION REGULATION; UBIQUITINATION;

ACETYLCYSTEINE; CARBON-SULFUR LYASES; CELL LINE, TUMOR; CYSTEINE PROTEINASE INHIBITORS; HUMANS; IRON; IRON REGULATORY PROTEIN 1; LEUPEPTINS; METABOLIC NETWORKS AND PATHWAYS; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; TRANS-ACTIVATION (GENETICS); UBIQUITIN;

EID: 34147195143     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01111-06     Document Type: Article

References (43)

1. Biederbick, A., O. Stehling, R. Rösser, B. Niggemeyer, Y. Nakai, H. P. Elsässer, and R. Lill. 2006. Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol. 26:5675-5687.
2. Brazzolotto, X., P. Timmins, Y. Dupont, and J. M. Moulis. 2002. Structural changes associated with switching activities of the human iron regulatory protein 1. J. Biol. Chem. 277:11995-12000.
3. Brown, N. M., S. A. Anderson, D. W. Steffen, T. B. Carpenter, M. C. Kennedy, W. E. Walden, and R. S. Eisenstein. 1998. Novel role of phosphorylation in Fe-S cluster stability revealed by phosphomimetic mutations at Ser-138 of iron regulatory protein 1. Proc. Natl. Acad. Sci. USA 95:15235-15240.
4. Clarke, S. L., A. Vasanthakumar, S. A. Anderson, C. Pondarre, C. M. Koh, K. M. Deck, J. S. Pitula, C. J. Epstein, M. D. Fleming, and R. S. Eisenstein. 2006. Iron-responsive degradation of iron-regulatory protein 1 does not require the Fe-S cluster. EMBO J. 25:544-553.
5. Cooperman, S. S., E. G. Meyron-Holtz, H. Olivierre-Wilson, M. C. Ghosh, J. P. McConnell, and T. A. Rouault. 2005. Microcytic anemia, erythropoietic protoporphyria and neurodegeneration in mice with targeted deletion of iron regulatory protein 2. Blood 106:1084-1091.
6. Dupuy, J., A. Volbeda, P. Carpentier, C. Darnault, J. M. Moulis, and J. C. Fontecilla-Camps. 2006. Crystal structure of human iron regulatory protein 1 as cytosolic aconitase. Structure 14:129-139.
7. Fillebeen, C., A. Caltagirone, A. Martelli, J. M. Moulis, and K. Pantopoulos. 2005. IRP1 Ser-711 is a phosphorylation site, critical for regulation of RNA-binding and aconitase activities. Biochem. J. 388:143-150.
8. Fillebeen, C., D. Chahine, A. Caltagirone, P. Segal, and K. Pantopoulos. 2003. A phosphomimetic mutation at Ser-138 renders iron regulatory protein 1 sensitive to iron-dependent degradation. Mol. Cell. Biol. 23:6973-6981.
9. Fosset, C., M. J. Chauveau, B. Guillon, F. Canal, J. C. Drapier, and C. Bouton. 2006. RNA silencing of mitochondrial m-Nfs1 reduces Fe-S enzyme activity both in mitochondria and cytosol of mammalian cells. J. Biol. Chem. 281:25398-25406.
10. Frishman, D., and M. W. Hentze. 1996. Conservation of aconitase residues revealed by multiple sequence analysis. Implications for structure/function relationships. Eur. J. Biochem. 239:197-200.
11. Galy, B., D. Ferring, and M. W. Hentze. 2005. Generation of conditional alleles of the murine iron regulatory protein (IRP)-1 and -2 genes. Genesis 43:181-188.
12. Galy, B., D. Ferring, B. Minana, O. Bell, H. G. Janser, M. Muckenthaler, K. Schumann, and M. W. Hentze. 2005. Altered body iron distribution and microcytosis in mice deficient for iron regulatory protein 2 (IRP2). Blood 106:2580-2589.
13. Galy, B., S. M. Hölter, T. Klopstock, D. Ferring, L. Becker, S. Kaden, W. Wurst, H.-J. Gröne, and M. W. Hentze. 2006. Iron homeostasis in the brain: complete iron regulatory protein 2 deficiency without symptomatic neurodegeneration in the mouse. Nat. Genet. 38:967-969.
14. Gehring, N., M. W. Hentze, and K. Pantopoulos. 1999. Menadione-induced oxidative stress leads to inactivation of both RNA-binding and aconitase activities of iron regulatory protein-1. J. Biol. Chem. 274:6219-6225.
15. Guo, B., J. D. Phillips, Y. Yu, and E. A. Leibold. 1995. Iron regulates the intracellular degradation of iron regulatory protein 2 by the proteasome. J. Biol. Chem. 270:21645-21651.
16. Henderson, B. R., and L. C. Kühn. 1995. Differential modulation of the RNA-binding proteins IRP1 and IRP2 in response to iron. IRP2 inactivation requires translation of another protein. J. Biol. Chem. 270:20509-20515.
17. Hirling, H., B. R. Henderson, and L. C. Kühn. 1994. Mutational analysis of the [4Fe-4S]-cluster converting iron regulatory factor from its RNA-binding form to cytoplasmic aconitase. EMBO J. 13:453-461.
18. Kaptain, S., W. E. Downey, C. Tang, C. Philpott, D. Haile, D. G. Orloff, J. B. Harford, T. A. Rouault, and R. D. Klausner. 1991. A regulated RNA binding protein also possesses aconitase activity. Proc. Natl. Acad. Sci. USA 88:10109-10113.
19. LaVaute, T., S. Smith, S. Cooperman, K. Iwai, W. Land, E. Meyron-Holtz, S. K. Drake, G. Miller, M. Abu-Asab, M. Tsokos, R. Switzer III, A. Grinberg, P. Love, N. Tresser, and T. A. Rouault. 2001. Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat. Genet. 27:209-214.
20. Lill, R., and U. Muhlenhoff. 2005. Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30:133-141.
21. Lobmayr, L., D. G. Brooks, and R. B. Wilson. 2005. Increased IRP1 activity in Friedreich ataxia. Gene 354:157-161.
22. Meyron-Holtz, E. G., M. C. Ghosh, K. Iwai, T. LaVaute, X. Brazzolotto, U. V. Berger, W. Land, H. Ollivierre-Wilson, A. Grinberg, P. Love, and T. A. Rouault. 2004. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J. 23:386-395.
23. Mueller, S., and K. Pantopoulos. 2002. Activation of iron regulatory protein-1 (IRP1) by oxidative stress. Methods Enzymol. 348:324-337.
24. Müllner, E. W., B. Neupert, and L. C. Kühn. 1989. A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell 58:373-382.
25. Ory, D. S., B. A. Neugeboren, and R. C. Mulligan. 1996. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc. Natl. Acad. Sci. USA 93:11400-11406.
26. Pantopoulos, K. 2004. Iron metabolism and the IRE/IRP regulatory system: an update. Ann. N. Y. Acad. Sci. 1012:1-13.
27. B. RNA 1:155-163.
28. Pantopoulos, K., and M. W. Hentze. 1995. Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J. 14:2917-2924.
29. Philpott, C. C., D. Haile, T. A. Rouault, and R. D. Klausner. 1993. Modification of a free Fe-S cluster cysteine residue in the active iron-responsive element-binding protein prevents RNA binding. J. Biol. Chem. 268:17655-17658.
30. Pondarre, C., B. B. Antiochos, D. R. Campagna, S. L. Clarke, E. L. Greer, K. M. Deck, A. McDonald, A. P. Han, A. Medlock, J. L. Kutok, S. A. Anderson, R. S. Eisenstein, and M. D. Fleming. 2006. The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis. Hum. Mol. Genet. 15:953-964.
31. Rouault, T. A. 2006. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2:406-414.
32. Roy, A., N. Solodovnikova, T. Nicholson, W. Antholine, and W. E. Walden. 2003. A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J. 22:4826-4835.
33. Seznec, H., D. Simon, C. Bouton, L. Reutenauer, A. Hertzog, P. Golik, V. Procaccio, M. Patel, J. C. Drapier, M. Koenig, and H. Puccio. 2005. Friedreich ataxia: the oxidative stress paradox. Hum. Mol. Genet. 14:463-474.
34. Smith, S. R., S. Cooperman, T. Lavaute, N. Tresser, M. Ghosh, E. Meyron-Holtz, W. Land, H. Ollivierre, B. Jortner, R. Switzer III, A. Messing, and T. A. Rouault. 2004. Severity of neurodegeneration correlates with compromise of iron metabolism in mice with iron regulatory protein deficiencies. Ann. N. Y. Acad. Sci. 1012:65-83.
35. Smith, S. R., M. C. Ghosh, H. Ollivierre-Wilson, W. Hang Tong, and T. A. Rouault. 2006. Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development. Blood Cells Mol. Dis. 36:283-287.
36. Stehling, O., H. P. Elsasser, B. Bruckel, U. Muhlenhoff, and R. Lill. 2004. Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum. Mol. Genet. 13:3007-3015.
37. Tang, C. K., J. Chin, J. B. Harford, R. D. Klausner, and T. A. Rouault. 1992. Iron regulates the activity of the iron-responsive element binding protein without changing its rate of synthesis or degradation. J. Biol. Chem. 267: 24466-24470.
38. Tong, W. H., and T. A. Rouault. 2006. Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell Metab. 3:199-210.
39. Wang, J., G. Chen, M. Muckenthaler, B. Galy, M. W. Hentze, and K. Pantopoulos. 2004. Iron-mediated degradation of IRP2: an unexpected pathway involving a 2-oxoglutarate-dependent oxygenase activity. Mol. Cell. Biol. 24:954-965.
40. Wang, J., C. Fillebeen, G. Chen, B. Andriopoulos, and K. Pantopoulos. 2006. Sodium nitroprusside promotes IRP2 degradation via an increase in intracellular iron and in the absence of S nitrosylation at C178. Mol. Cell. Biol. 26:1948-1954.
41. Wang, J., and K. Pantopoulos. 2002. Conditional derepression of ferritin synthesis in cells expressing a constitutive IRP1 mutant. Mol. Cell. Biol. 22:4638-4651.
42. Wingert, R. A., J. L. Galloway, B. Barut, H. Foott, P. Fraenkel, J. L. Axe, G. J. Weber, K. Dooley, A. J. Davidson, B. Schmidt, B. H. Paw, G. C. Shaw, P. Kingsley, J. Palis, H. Schubert, O. Chen, J. Kaplan, and L. I. Zon. 2005. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436:1035-1039.
43. Yikilmaz, E., T. A. Rouault, and P. Schuck. 2005. Self-association and ligand-induced conformational changes of iron regulatory proteins 1 and 2. Biochemistry 44:8470-8478.