Immune and non-immune functions of the immunoproteasome

Frontiers in Bioscience

Volumn 17, Issue 5, 2012, Pages 1904-1916

  Angeles, Arkhjamil ^a   Fung, Gabriel ^a   Luo, Honglin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Autoimmune diseases; Cancer; Cytokine production; Immunoproteasome; MHC class I antigen presentation; Oxidative stress; Review; T cell differentiation survival

Indexed keywords

PROTEASOME;

DISEASES; HUMAN; IMMUNOLOGY; OXIDATIVE STRESS; PHYSIOLOGY; REVIEW;

DISEASE; HUMANS; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 84859164670     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4027     Document Type: Review

References (88)

1. A. Ciechanover and A. L. Schwartz: The ubiquitinproteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci U S A, 95(6), 2727-30 (1998). (Pubitemid 28135795)
2. M. Hochstrasser: Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol, 7(2), 215-23 (1995).
3. M. Aki, N. Shimbara, M. Takashina, K. Akiyama, S. Kagawa, T. Tamura, N. Tanahashi, T. Yoshimura, K. Tanaka and A. Ichihara: Interferon-gamma induces different subunit organizations and functional diversity of proteasomes. J Biochem, 115(2), 257-69 (1994).
4. K. Fruh, M. Gossen, K. Wang, H. Bujard, P. A. Peterson and Y. Yang: Displacement of housekeeping proteasome subunits by MHC-encoded LMPs: a newly discovered mechanism for modulating the multicatalytic proteinase complex. EMBO J, 13(14), 3236-44 (1994). (Pubitemid 24226938)
5. M. Eggers, B. Boes-Fabian, T. Ruppert, P. M. Kloetzel and U. H. Koszinowski: The cleavage preference of the proteasome governs the yield of antigenic peptides. J Exp Med, 182(6), 1865-70 (1995).
6. M. Gaczynska, K. L. Rock, T. Spies and A. L. Goldberg: Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proc Natl Acad Sci U S A, 91(20), 9213-7 (1994). (Pubitemid 24297884)
7. P. M. Kloetzel and F. Ossendorp: Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol, 16(1), 76-81 (2004). (Pubitemid 38198120)
8. M. Basler, M. Dajee, C. Moll, M. Groettrup and C. J. Kirk: Prevention of experimental colitis by a selective inhibitor of the immunoproteasome. J Immunol, 185(1), 634-41 (2010).
9. S. E. Hensley, D. Zanker, B. P. Dolan, A. David, H. D. Hickman, A. C. Embry, C. N. Skon, K. M. Grebe, T. A. Griffin, W. Chen, J. R. Bennink and J. W. Yewdell: Unexpected role for the immunoproteasome subunit LMP2 in antiviral humoral and innate immune responses. J Immunol, 184(8), 4115-22 (2010).
10. T. Muchamuel, M. Basler, M. A. Aujay, E. Suzuki, K. W. Kalim, C. Lauer, C. Sylvain, E. R. Ring, J. Shields, J. Jiang, P. Shwonek, F. Parlati, S. D. Demo, M. K. Bennett, C. J. Kirk and M. Groettrup: A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat Med, 15(7), 781-7 (2009).
11. C. M. Caudill, K. Jayarapu, L. Elenich, J. J. Monaco, R. A. Colbert and T. A. Griffin: T cells lacking immunoproteasome subunits MECL-1 and LMP7 hyperproliferate in response to polyclonal mitogens. J Immunol, 176(7), 4075-82 (2006). (Pubitemid 44264386)
12. D. M. Zaiss, N. de Graaf and A. J. Sijts: The proteasome immunosubunit multicatalytic endopeptidase complex-like 1 is a T-cell-intrinsic factor influencing homeostatic expansion. Infect Immun, 76(3), 1207-13 (2008). (Pubitemid 351428083)
13. D. A. Ferrington, S. A. Hussong, H. Roehrich, R. J. Kapphahn, S. M. Kavanaugh, N. D. Heuss and D. S. Gregerson: Immunoproteasome responds to injury in the retina and brain. J Neurochem, 106(1), 158-69 (2008). (Pubitemid 351840197)
14. A. M. Pickering, A. L. Koop, C. Y. Teoh, G. Ermak, T. Grune and K. J. Davies: The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J, 432(3), 585-94 (2010).
15. U. Seifert, L. P. Bialy, F. Ebstein, D. Bech-Otschir, A. Voigt, F. Schroter, T. Prozorovski, N. Lange, J. Steffen, M. Rieger, U. Kuckelkorn, O. Aktas, P. M. Kloetzel and E. Kruger: Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell, 142(4), 613- 24 (2010).
16. S. van Deventer and J. Neefjes: The Immunoproteasome Cleans up after Inflammation. Cell, 142(4), 517-8 (2010).
17. Y. K. Ho, P. Bargagna-Mohan, M. Wehenkel, R. Mohan and K. B. Kim: LMP2-specific inhibitors: chemical genetic tools for proteasome biology. Chem Biol, 14(4), 419-30 (2007). (Pubitemid 46617320)
18. D. J. Kuhn, S. A. Hunsucker, Q. Chen, P. M. Voorhees, M. Orlowski and R. Z. Orlowski: Targeted inhibition of the immunoproteasome is a potent strategy against models of multiple myeloma that overcomes resistance to conventional drugs and nonspecific proteasome inhibitors. Blood, 113(19), 4667-76 (2009).
19. A. V. Singh, M. Bandi, M. A. Aujay, C. J. Kirk, D. E. Hark, N. Raje, D. Chauhan and K. C. Anderson: PR- 924, a selective inhibitor of the immunoproteasome subunit LMP-7, blocks multiple myeloma cell growth both in vitro and in vivo. Br J Haematol, 152(2), 155-63 (2011).
20. Z. P. Cai, Z. Shen, L. Van Kaer and L. C. Becker: Ischemic preconditioning-induced cardioprotection is lost in mice with immunoproteasome subunit low molecular mass polypeptide-2 deficiency. FASEB J, 22(12), 4248-57 (2008).
21. L. Zu, D. Bedja, K. Fox-Talbot, K. L. Gabrielson, L. Van Kaer, L. C. Becker and Z. P. Cai: Evidence for a role of immunoproteasomes in regulating cardiac muscle mass in diabetic mice. J Mol Cell Cardiol, 49(1), 5-15 (2010).
22. J. Dannull, D. T. Lesher, R. Holzknecht, W. Qi, G. Hanna, H. Seigler, D. S. Tyler and S. K. Pruitt: Immunoproteasome down-modulation enhances the ability of dendritic cells to stimulate antitumor immunity. Blood, 110(13), 4341-50 (2007). (Pubitemid 351377799)
23. J. J. Driscoll and R. Dechowdhury: Therapeutically targeting the SUMOylation, Ubiquitination and Proteasome pathways as a novel anticancer strategy. Target Oncol, 5(4), 281-9 (2010).
24. M. Diaz-Hernandez, F. Hernandez, E. Martin-Aparicio, P. Gomez-Ramos, M. A. Moran, J. G. Castano, I. Ferrer, J. Avila and J. J. Lucas: Neuronal induction of the immunoproteasome in Huntington's disease. J Neurosci, 23(37), 11653-61 (2003). (Pubitemid 38021292)
25. M. Diaz-Hernandez, E. Martin-Aparicio, J. Avila, F. Hernandez and J. J. Lucas: Enhanced induction of the immunoproteasome by interferon gamma in neurons expressing mutant Huntingtin. Neurotox Res, 6(6), 463-8 (2004).
26. M. Mishto, E. Bellavista, A. Santoro, A. Stolzing, C. Ligorio, B. Nacmias, L. Spazzafumo, M. Chiappelli, F. Licastro, S. Sorbi, A. Pession, T. Ohm, T. Grune and C. Franceschi: Immunoproteasome and LMP2 polymorphism in aged and Alzheimer's disease brains. Neurobiol Aging, 27(1), 54-66 (2006). (Pubitemid 41627950)
27. K. Puttaparthi and J. L. Elliott: Non-neuronal induction of immunoproteasome subunits in an ALS model: possible mediation by cytokines. Exp Neurol, 196(2), 441-51 (2005). (Pubitemid 41607833)
28. Z. Yang, D. Gagarin, G. St Laurent ,3rd, N. Hammell, I. Toma, C. A. Hu, A. Iwasa and T. A. McCaffrey: Cardiovascular inflammation and lesion cell apoptosis: a novel connection via the interferoninducible immunoproteasome. Arterioscler Thromb Vasc Biol, 29(8), 1213-9 (2009).
29. M. Bochtler, L. Ditzel, M. Groll, C. Hartmann and R. Huber: The proteasome. Annu Rev Biophys Biomol Struct, 28, 295-317 (1999). (Pubitemid 29319261)
30. M. Groll, L. Ditzel, J. Lowe, D. Stock, M. Bochtler, H. D. Bartunik and R. Huber: Structure of 20S proteasome from yeast at 2.4 A resolution. Nature, 386(6624), 463-71 (1997). (Pubitemid 27164066)
31. T. A. Griffin, D. Nandi, M. Cruz, H. J. Fehling, L. V. Kaer, J. J. Monaco and R. A. Colbert: Immunoproteasome assembly: cooperative incorporation of interferon gamma (IFN-gamma)-inducible subunits. J Exp Med, 187(1), 97- 104 (1998). (Pubitemid 28044824)
32. M. Groettrup, S. Standera, R. Stohwasser and P. M. Kloetzel: The subunits MECL-1 and LMP2 are mutually required for incorporation into the 20S proteasome. Proc Natl Acad Sci U S A, 94(17), 8970-5 (1997). (Pubitemid 27357766)
33. D. J. Kingsbury, T. A. Griffin and R. A. Colbert: Novel propeptide function in 20 S proteasome assembly influences beta subunit composition. J Biol Chem, 275(31), 24156-62 (2000). (Pubitemid 30627463)
34. S. Heink, D. Ludwig, P. M. Kloetzel and E. Kruger: IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci U S A, 102(26), 9241-6 (2005). (Pubitemid 40923548)
35. P. C. Ramos, J. Hockendorff, E. S. Johnson, A. Varshavsky and R. J. Dohmen: Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell, 92(4), 489-99 (1998). (Pubitemid 28101112)
36. E. Witt, D. Zantopf, M. Schmidt, R. Kraft, P. M. Kloetzel and E. Kruger: Characterisation of the newly identified human Ump1 homologue POMP and analysis of LMP7(beta 5i) incorporation into 20 S proteasomes. J Mol Biol, 301(1), 1-9 (2000).
37. M. Orlowski and S. Wilk: Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch Biochem Biophys, 383(1), 1-16 (2000).
38. M. Gaczynska, A. L. Goldberg, K. Tanaka, K. B. Hendil and K. L. Rock: Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-gamma-induced subunits LMP2 and LMP7. J Biol Chem, 271(29), 17275-80 (1996). (Pubitemid 26244285)
39. S. Morel, F. Levy, O. Burlet-Schiltz, F. Brasseur, M. Probst-Kepper, A. L. Peitrequin, B. Monsarrat, R. Van Velthoven, J. C. Cerottini, T. Boon, J. E. Gairin and B. J. Van den Eynde: Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity, 12(1), 107-17 (2000). (Pubitemid 30069219)
40. O. Coux, K. Tanaka and A. L. Goldberg: Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem, 65, 801-47 (1996). (Pubitemid 26255262)
41. W. Dubiel, G. Pratt, K. Ferrell and M. Rechsteiner: Purification of an 11 S regulator of the multicatalytic protease. J Biol Chem, 267(31), 22369-77 (1992).
42. M. Chatterjee-Kishore, R. Kishore, D. J. Hicklin, F. M. Marincola and S. Ferrone: Different requirements for signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 in the regulation of low molecular mass polypeptide 2 and transporter associated with antigen processing 1 gene expression. J Biol Chem, 273(26), 16177-83 (1998). (Pubitemid 28311390)
43. S. Namiki, T. Nakamura, S. Oshima, M. Yamazaki, Y. Sekine, K. Tsuchiya, R. Okamoto, T. Kanai and M. Watanabe: IRF-1 mediates upregulation of LMP7 by IFNgamma and concerted expression of immunosubunits of the proteasome. FEBS Lett, 579(13), 2781-7 (2005). (Pubitemid 40725245)
44. S. Bose, P. Brooks, G. G. Mason and A. J. Rivett: gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation. Biochem J, 353(Pt 2), 291-7 (2001). (Pubitemid 32096938)
45. S. Jakel, U. Kuckelkorn, G. Szalay, M. Plotz, K. Textoris-Taube, E. Opitz, K. Klingel, S. Stevanovic, R. Kandolf, K. Kotsch, K. Stangl, P. M. Kloetzel and A. Voigt: Differential interferon responses enhance viral epitope generation by myocardial immunoproteasomes in murine enterovirus myocarditis. Am J Pathol, 175(2), 510-8 (2009).
46. E. C. Shin, U. Seifert, T. Kato, C. M. Rice, S. M. Feinstone, P. M. Kloetzel and B. Rehermann: Virusinduced type I IFN stimulates generation of immunoproteasomes at the site of infection. J Clin Invest, 116(11), 3006-14 (2006). (Pubitemid 44684485)
47. G. Szalay, S. Meiners, A. Voigt, J. Lauber, C. Spieth, N. Speer, M. Sauter, U. Kuckelkorn, A. Zell, K. Klingel, K. Stangl and R. Kandolf: Ongoing coxsackievirus myocarditis is associated with increased formation and activity of myocardial immunoproteasomes. Am J Pathol, 168(5), 1542-52 (2006).
48. M. P. Gavilan, A. Castano, M. Torres, M. Portavella, C. Caballero, S. Jimenez, A. Garcia-Martinez, J. Parrado, J. Vitorica and D. Ruano: Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J Neurochem, 108(1), 260-72 (2009).
49. G. S. Foss, F. Larsen, J. Solheim and H. Prydz: Constitutive and interferon-gamma-induced expression of the human proteasome subunit multicatalytic endopeptidase complex-like 1. Biochim Biophys Acta, 1402(1), 17-28 (1998). (Pubitemid 28122381)
50. S. Kotamraju, S. Matalon, T. Matsunaga, T. Shang, J. M. Hickman-Davis and B. Kalyanaraman: Upregulation of immunoproteasomes by nitric oxide: potential antioxidative mechanism in endothelial cells. Free Radic Biol Med, 40(6), 1034-44 (2006). (Pubitemid 43376013)
51. M. K. Callahan, E. A. Wohlfert, A. Menoret and P. K. Srivastava: Heat shock up-regulates lmp2 and lmp7 and enhances presentation of immunoproteasome-dependent epitopes. J Immunol, 177(12), 8393-9 (2006). (Pubitemid 44893801)
52. Q. Ding, K. Reinacker, E. Dimayuga, V. Nukala, J. Drake, D. A. Butterfield, J. C. Dunn, S. Martin, A. J. Bruce-Keller and J. N. Keller: Role of the proteasome in protein oxidation and neural viability following low-level oxidative stress. FEBS Lett, 546(2- 3), 228-32 (2003). (Pubitemid 36782416)
53. M. A. Khan, H. Oubrahim and E. R. Stadtman: Inhibition of apoptosis in acute promyelocytic leukemia cells leads to increases in levels of oxidized protein and LMP2 immunoproteasome. Proc Natl Acad Sci U S A, 101(32), 11560-5 (2004). (Pubitemid 39095335)
54. S. Singh, N. Awasthi, C. E. Egwuagu and B. J. Wagner: Immunoproteasome expression in a nonimmune tissue, the ocular lens. Arch Biochem Biophys, 405(2), 147-53 (2002) doi:S0003986102003417 [pii]. (Pubitemid 35191726)
55. L. F. Barton, M. Cruz, R. Rangwala, G. S.Jr. Deepe and J. J. Monaco: Regulation of immunoproteasome subunit expression in vivo following pathogenic fungal infection. J Immunol, 169(6), 3046-52 (2002). (Pubitemid 35013148)
56. L. Y. Hwang, P. T. Lieu, P. A. Peterson and Y. Yang: Functional regulation of immunoproteasomes and transporter associated with antigen processing. Immunol Res, 24(3), 245-72 (2001). (Pubitemid 33064385)
57. S. Hutchinson, S. Sims, G. O'Hara, J. Silk, U. Gileadi, V. Cerundolo and P. Klenerman: A dominant role for the immunoproteasome in CD8+ T cell responses to murine cytomegalovirus. PLoS One, 6(2), e14646 (2011).
58. W. Chen, C. C. Norbury, Y. Cho, J. W. Yewdell and J. R. Bennink: Immunoproteasomes shape immunodominance hierarchies of antiviral CD8(+) T cells at the levels of T cell repertoire and presentation of viral antigens. J Exp Med, 193(11), 1319-26 (2001). (Pubitemid 32524782)
59. M. Basler, J. Moebius, L. Elenich, M. Groettrup and J. J. Monaco: An altered T cell repertoire in MECL-1- deficient mice. J Immunol, 176(11), 6665-72 (2006). (Pubitemid 43787850)
60. H. J. Fehling, W. Swat, C. Laplace, R. Kuhn, K. Rajewsky, U. Muller and H. von Boehmer: MHC class I expression in mice lacking the proteasome subunit LMP-7. Science, 265(5176), 1234-7 (1994). (Pubitemid 24291982)
61. L. Van Kaer, P. G. Ashton-Rickardt, M. Eichelberger, M. Gaczynska, K. Nagashima, K. L. Rock, A. L. Goldberg, P. C. Doherty and S. Tonegawa: Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity, 1(7), 533-41 (1994).
62. A. K. Nussbaum, M. P. Rodriguez-Carreno, N. Benning, J. Botten and J. L. Whitton: Immunoproteasomedeficient mice mount largely normal CD8+ T cell responses to lymphocytic choriomeningitis virus infection and DNA vaccination. J Immunol, 175(2), 1153-60 (2005). (Pubitemid 41095002)
63. N. Schmidt, E. Gonzalez, A. Visekruna, A. A. Kuhl, C. Loddenkemper, H. Mollenkopf, S. H. Kaufmann, U. Steinhoff and T. Joeris: Targeting the proteasome: partial inhibition of the proteasome by bortezomib or deletion of the immunosubunit LMP7 attenuates experimental colitis. Gut, 59(7), 896-906 (2010).
64. Q. Ding, S. Martin, E. Dimayuga, A. J. Bruce-Keller and J. N. Keller: LMP2 knock-out mice have reduced Immunoproteasome and its functions 1915 proteasome activities and increased levels of oxidatively damaged proteins. Antioxid Redox Signal, 8(1- 2), 130-5 (2006). (Pubitemid 43324539)
65. A. Mani and E. P. Gelmann: The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol, 23(21), 4776- 89 (2005). (Pubitemid 46224082)
66. J. Adams: The development of proteasome inhibitors as anticancer drugs. Cancer Cell, 5(5), 417-21 (2004). (Pubitemid 38610244)
67. D. Chauhan, T. Hideshima and K. C. Anderson: Proteasome inhibition in multiple myeloma: therapeutic implication. Annu Rev Pharmacol Toxicol, 45, 465-76 (2005).
68. D. R. Fels, J. Ye, A. T. Segan, S. J. Kridel, M. Spiotto, M. Olson, A. C. Koong and C. Koumenis: Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways. Cancer Res, 68(22), 9323-30 (2008).
69. S. T. Nawrocki, J. S. Carew, K.Jr. Dunner, L. H. Boise, P. J. Chiao, P. Huang, J. L. Abbruzzese and D. J. McConkey: Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res, 65(24), 11510-9 (2005). (Pubitemid 41821709)
70. G. Cavaletti: Bortezomib-induced peripheral neuropathy: facts and genes. Lancet Oncol, 12(2), 120-1; author reply 121 (2011).
71. F. Parlati, S. J. Lee, M. Aujay, E. Suzuki, K. Levitsky, J. B. Lorens, D. R. Micklem, P. Ruurs, C. Sylvain, Y. Lu, K. D. Shenk and M. K. Bennett: Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood, 114(16), 3439-47 (2009).
72. C. P. Miller, K. Ban, M. E. Dujka, D. J. McConkey, M. Munsell, M. Palladino and J. Chandra: NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROSdependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood, 110(1), 267-77 (2007). (Pubitemid 47026844)
73. C. P. Miller, S. Rudra, M. J. Keating, W. G. Wierda, M. Palladino and J. Chandra: Caspase-8 dependent histone acetylation by a novel proteasome inhibitor, NPI-0052: a mechanism for synergy in leukemia cells. Blood, 113(18), 4289-99 (2009).
74. M. Altun, P. J. Galardy, R. Shringarpure, T. Hideshima, R. LeBlanc, K. C. Anderson, H. L. Ploegh and B. M. Kessler: Effects of PS-341 on the activity and composition of proteasomes in multiple myeloma cells. Cancer Res, 65(17), 7896-901 (2005). (Pubitemid 41297267)
75. A. Johnsen, J. France, M. S. Sy and C. V. Harding: Down-regulation of the transporter for antigen presentation, proteasome subunits, and class I major histocompatibility complex in tumor cell lines. Cancer Res, 58(16), 3660-7 (1998). (Pubitemid 28376566)
76. T. Kageshita, S. Hirai, T. Ono, D. J. Hicklin and S. Ferrone: Down-regulation of HLA class I antigenprocessing molecules in malignant melanoma: association with disease progression. Am J Pathol, 154(3), 745-54 (1999). (Pubitemid 29122593)
77. N. Meidenbauer, A. Zippelius, M. J. Pittet, M. Laumer, S. Vogl, J. Heymann, M. Rehli, B. Seliger, S. Schwarz, F. A. Le Gal, P. Y. Dietrich, R. Andreesen, P. Romero and A. Mackensen: High frequency of functionally active Melan-aspecific T cells in a patient with progressive immunoproteasome-deficient melanoma. Cancer Res, 64(17), 6319-26 (2004). (Pubitemid 39129437)
78. S. Heink, B. Fricke, D. Ludwig, P. M. Kloetzel and E. Kruger: Tumor cell lines expressing the proteasome subunit isoform LMP7E1 exhibit immunoproteasome deficiency. Cancer Res, 66(2), 649-52 (2006). (Pubitemid 43165925)
79. T. Egerer, L. Martinez-Gamboa, A. Dankof, B. Stuhlmuller, T. Dorner, V. Krenn, K. Egerer, P. E. Rudolph, G. R. Burmester and E. Feist: Tissue-specific up-regulation of the proteasome subunit beta5i (LMP7) in Sjogren's syndrome. Arthritis Rheum, 54(5), 1501-8 (2006).
80. L. R. Fitzpatrick, J. S. Small, L. S. Poritz, K. J. McKenna and W. A. Koltun: Enhanced intestinal expression of the proteasome subunit low molecular mass polypeptide 2 in patients with inflammatory bowel disease. Dis Colon Rectum, 50(3), 337-48; discussion 348-50 (2007).
81. A. Visekruna, T. Joeris, D. Seidel, A. Kroesen, C. Loddenkemper, M. Zeitz, S. H. Kaufmann, R. Schmidt- Ullrich and U. Steinhoff: Proteasome-mediated degradation of IkappaBalpha and processing of p105 in Crohn disease and ulcerative colitis. J Clin Invest, 116(12), 3195-203 (2006). (Pubitemid 44878633)
82. C. Noda, N. Tanahashi, N. Shimbara, K. B. Hendil and K. Tanaka: Tissue distribution of constitutive proteasomes, immunoproteasomes, and PA28 in rats. Biochem Biophys Res Commun, 277(2), 348-54 (2000).
83. D. A. Ferrington, A. D. Husom and L. V. Thompson: Altered proteasome structure, function, and oxidation in aged muscle. FASEB J, 19(6), 644-6 (2005). (Pubitemid 40471272)
84. A. D. Husom, E. A. Peters, E. A. Kolling, N. A. Fugere, L. V. Thompson and D. A. Ferrington: Altered proteasome function and subunit composition in aged muscle. Arch Biochem Biophys, 421(1), 67-76 (2004). (Pubitemid 37543497)
85. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell, 72(6), 971-83 (1993).
86. N. F. Bence, R. M. Sampat and R. R. Kopito: Impairment of the ubiquitin-proteasome system by protein aggregation. Science, 292(5521), 1552-5 (2001). (Pubitemid 32493425)
87. H. Otani: Ischemic preconditioning: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal, 10(2), 207-47 (2008).
88. P. Libby, Y. Okamoto, V. Z. Rocha and E. Folco: Inflammation in atherosclerosis: transition from theory to practice. Circ J, 74(2), 213-20 (2010).