Protein quality control during erythropoiesis and hemoglobin synthesis

Hematology/Oncology Clinics of North America

Volumn 24, Issue 6, 2010, Pages 1071-1088

  Khandros, Eugene ^a   Weiss, Mitchell J ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Hemoglobin; Protein quality control; Thalassemia

Indexed keywords

ALPHA GLOBIN; BETA GLOBIN; CHAPERONE; HEMOGLOBIN; UBIQUITIN;

AGGRESOME; AUTOPHAGY; ERYTHROPOIESIS; HEMOGLOBIN SYNTHESIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN QUALITY CONTROL; REGULATORY MECHANISM; REVIEW;

ALPHA-GLOBINS; BETA-GLOBINS; BETA-THALASSEMIA; ERYTHROCYTES; ERYTHROPOIESIS; HEMOGLOBIN A; HUMANS; MODELS, BIOLOGICAL; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITINATION;

EID: 78249279351     PISSN: 08898588     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hoc.2010.08.013     Document Type: Review

References (127)

1. Weatherall D.J., Clegg J.B. The thalassaemia syndromes 2001, Blackwell Science, Oxford, Malden (MA). 4th edition.
2. Aigelsreiter A., Janig E., Stumptner C., et al. How a cell deals with abnormal proteins. Pathogenetic mechanisms in protein aggregation diseases. Pathobiology 2007, 74(3):145-158.
3. Garcia-Mata R., Gao Y.S., Sztul E. Hassles with taking out the garbage: aggravating aggresomes. Traffic 2002, 3(6):388-396.
4. Ding W.X., Yin X.M. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 2008, 4(2):141-150.
5. Angastiniotis M., Modell B. Global epidemiology of hemoglobin disorders. Ann N Y Acad Sci 1998, 850:251-269.
6. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 2009, 16(6):574-581.
7. McClellan A.J., Tam S., Kaganovich D., et al. Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 2005, 7(8):736-741.
8. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426(6968):895-899.
9. Dantuma N., Lindsten K. Stressing the ubiquitin/proteasome system. Cardiovasc Res 2010, 85(2):263-271.
10. Barral J.M., Broadley S.A., Schaffar G., et al. Roles of molecular chaperones in protein misfolding diseases. Semin Cell Dev Biol 2004, 15(1):17-29.
11. Broadley S.A., Hartl F.U. The role of molecular chaperones in human misfolding diseases. FEBS Lett 2009, 583(16):2647-2653.
12. Thulasiraman V., Yang C.F., Frydman J. In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J 1999, 18(1):85-95.
13. Pickart C.M. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001, 70:503-533.
14. Jaakkola P., Mole D.R., Tian Y.M., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292(5516):468-472.
15. Jaeger P.A., Wyss-Coray T. All-you-can-eat: autophagy in neurodegeneration and neuroprotection. Mol Neurodegeneration 2009, 4:16.
16. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140(3):313-326.
17. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000, 10(12):524-530.
18. Olzmann J.A., Li L., Chin L.S. Aggresome formation and neurodegenerative diseases: therapeutic implications. Curr Med Chem 2008, 15(1):47-60.
19. Johnston J.A., Ward C.L., Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J Cell Biol 1998, 143(7):1883-1898.
20. Johnston J.A., Dalton M.J., Gurney M.E., et al. Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 2000, 97(23):12571-12576.
21. García-Mata R., Bebök Z., Sorscher E.J., et al. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 1999, 146(6):1239-1254.
22. Junn E., Lee S.S., Suhr U.T., et al. Parkin accumulation in aggresomes due to proteasome impairment. J Biol Chem 2002, 277(49):47870-47877.
23. Ma J., Lindquist S. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc Natl Acad Sci U S A 2001, 98(26):14955-14960.
24. McNaught K.S., Shashidharan P., Perl D.P., et al. Aggresome-related biogenesis of Lewy bodies. Eur J Neurosci 2002, 16(11):2136-2148.
25. Mukai H., Isagawa T., Goyama E., et al. Formation of morphologically similar globular aggregates from diverse aggregation-prone proteins in mammalian cells. Proc Natl Acad Sci U S A 2005, 102(31):10887-10892.
26. Salomons F.A., Menéndez-Benito V., Böttcher C., et al. Selective accumulation of aggregation-prone proteasome substrates in response to proteotoxic stress. Mol Cell Biol 2009, 29(7):1774-1785.
27. Tanaka M., Kim Y.M., Lee G., et al. Aggresomes formed by alpha-synuclein and synphilin-1 are cytoprotective. J Biol Chem 2004, 279(6):4625-4631.
28. Waelter S., Boeddrich A., Lurz R., et al. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol Biol Cell 2001, 12(5):1393-1407.
29. Wigley W.C., Fabunmi R.P., Lee M.G., et al. Dynamic association of proteasomal machinery with the centrosome. J Cell Biol 1999, 145(3):481-490.
30. Wojcik C., Schroeter D., Wilk S., et al. Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome. Eur J Cell Biol 1996, 71(3):311-318.
31. Kaganovich D., Kopito R., Frydman J. Misfolded proteins partition between two distinct quality control compartments. Nature 2008, 454(7208):1088-1095.
32. Bjørkøy G., Lamark T., Brech A., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171(4):603-614.
33. Komatsu M., Waguri S., Koike M., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131(6):1149-1163.
34. Pankiv S., Clausen T.H., Lamark T., et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007, 282(33):24131-24145.
35. Zatloukal K., Stumptner C., Fuchsbichler A., et al. p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol 2002, 160(1):255-263.
36. Riley N.E., Li J., Worrall S., et al. The Mallory body as an aggresome: in vitro studies. Exp Mol Pathol 2002, 72(1):17-23.
37. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001, 292(5521):1552-1555.
38. Bennett E.J., Shaler T.A., Woodman B., et al. Global changes to the ubiquitin system in Huntington's disease. Nature 2007, 448(7154):704-708.
39. Bennett E.J., Bence N.F., Jayakumar R., et al. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell 2005, 17(3):351-365.
40. Rosen D.R., Siddique T., Patterson D., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362(6415):59-62.
41. Cleveland D.W., Liu J. Oxidation versus aggregation - how do SOD1 mutants cause ALS?. Nat Med 2000, 6(12):1320-1321.
42. Cheroni C., Marino M., Tortarolo M., et al. Functional alterations of the ubiquitin-proteasome system in motor neurons of a mouse model of familial amyotrophic lateral sclerosis. Hum Mol Genet 2009, 18(1):82-96.
43. Urushitani M., Kurisu J., Tsukita K., et al. Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J Neurochem 2002, 83(5):1030-1042.
44. Niwa J.I., Ishigaki S., Hishikawa N., et al. Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J Biol Chem 2002, 277(39):36793-36798.
45. Bruening W., Roy J., Giasson B., et al. Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J Neurochem 1999, 72(2):693-699.
46. Weiss M.J., Dos Santos C.O. Chaperoning erythropoiesis. Blood 2009, 113(10):2136-2144.
47. Banerji S.S., Theodorakis N.G., Morimoto R.I. Heat shock-induced translational control of HSP70 and globin synthesis in chicken reticulocytes. Mol Cell Biol 1984, 4(11):2437-2448.
48. Ribeil J.A., Zermati Y., Vandekerckhove J., et al. Hsp70 regulates erythropoiesis by preventing caspase-3-mediated cleavage of GATA-1. Nature 2007, 445(7123):102-105.
49. Kihm A.J., Kong Y., Hong W., et al. An abundant erythroid protein that stabilizes free alpha-haemoglobin. Nature 2002, 417(6890):758-763.
50. Yu X., Kong Y., Dore L.C., et al. An erythroid chaperone that facilitates folding of alpha-globin subunits for hemoglobin synthesis. J Clin Invest 2007, 117(7):1856-1865.
51. Kong Y., Zhou S., Kihm A.J., et al. Loss of alpha-hemoglobin-stabilizing protein impairs erythropoiesis and exacerbates beta-thalassemia. J Clin Invest 2004, 114(10):1457-1466.
52. Ciehanover A., Hod Y., Hershko A. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun 1978, 81(4):1100-1105.
53. Etlinger J.D., Goldberg A.L. A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes. Proc Natl Acad Sci U S A 1977, 74(1):54-58.
54. Hershko A., Heller H., Elias S., et al. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J Biol Chem 1983, 258(13):8206-8214.
55. Liu J., Guo X., Mohandas N., et al. Membrane remodeling during reticulocyte maturation. Blood 2010, 115(10):2021-2027.
56. Chen C.Y., Pajak L., Tamburlin J., et al. The effect of proteasome inhibitors on mammalian erythroid terminal differentiation. Exp Hematol 2002, 30(7):634-639.
57. Walrafen P., Verdier F., Kadri Z., et al. Both proteasomes and lysosomes degrade the activated erythropoietin receptor. Blood 2005, 105(2):600-608.
58. Gronowicz G., Swift H., Steck T.L. Maturation of the reticulocyte in vitro. J Cell Sci 1984, 71:177-197.
59. Heynen M.J., Tricot G., Verwilghen R.L. Autophagy of mitochondria in rat bone marrow erythroid cells. Relation to nuclear extrusion. Cell Tissue Res 1985, 239(1):235-239.
60. Kent G., Minick O.T., Volini F.I., et al. Autophagic vacuoles in human red cells. Am J Pathol 1966, 48(5):831-857.
61. Takano-Ohmuro H., Mukaida M., Kominami E., et al. Autophagy in embryonic erythroid cells: its role in maturation. Eur J Cell Biol 2000, 79(10):759-764.
62. Sandoval H., Thiagarajan P., Dasgupta S.K., et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454(7201):232-235.
63. Schweers R.L., Zhang J., Randall M.S., et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A 2007, 104(49):19500-19505.
64. Kundu M., Lindsten T., Yang C.Y., et al. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 2008, 112(4):1493-1502.
65. Zhang J., Randall M.S., Loyd M.R., et al. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 2009, 114(1):157-164.
66. Bank A., O'Donnell J.V. Intracellular loss of free alpha chains in beta thalassemia. Nature 1969, 222(5190):295-296.
67. Bargellesi A., Pontremoli S., Menini C., et al. Excess of alpha-globin synthesis in homozygous beta-thalassemia and its removal from the red blood cell cytoplasm. Eur J Biochem 1968, 3(3):364-368.
68. Chalevelakis G., Clegg J.B., Weatherall D.J. Imbalanced globin chain synthesis in heterozygous beta-thalassemic bone marrow. Proc Natl Acad Sci U S A 1975, 72(10):3853-3857.
69. Clegg J.B., Weatherall D.J. Haemoglobin synthesis during erythroid maturation in β-thalassaemia. Nature New Biol 1972, 240(101):190-192.
70. Kan Y.W., Nathan D.G., Lodish H.F. Equal synthesis of α- and β-globin chains in erythroid precursors in heterozygous β-thalassemia. J Clin Invest 1972, 51(7):1906-1909.
71. Wood W.G., Stamatoyannopoulos G. Globin synthesis in fractionated normoblasts of beta-thalassemia heterozygotes. J Clin Invest 1975, 55(3):567-578.
72. Shaeffer J.R. Evidence for soluble alpha-chains as intermediates in hemoglobin synthesis in the rabbit reticulocyte. Biochem Biophys Res Commun 1967, 28(4):647-652.
73. Gill F.M., Schwartz E. Free alpha-globin pool in human bone marrow. J Clin Invest 1973, 52(12):3057-3063.
74. Borsook H., Lingrel J.B., Scaro J.L., et al. Synthesis of haemoglobin in relation to the maturation of erythroid cells. Nature 1962, 196:347-350.
75. Casale G.P., Khairallah E.A., Grasso J.A. An analysis of hemoglobin synthesis in erythropoietic cells. Dev Biol 1980, 80(1):107-119.
76. Nathan D.G., Piomelli S., Gardner F.H. The synthesis of heme and globin in the maturing human erythroid cell. J Clin Invest 1961, 40:940-946.
77. Skadberg O., Brun A., Sandberg S. Human reticulocytes isolated from peripheral blood: maturation time and hemoglobin synthesis. Lab Hematol 2003, 9(4):198-206.
78. Bank A. Hemoglobin synthesis in beta-thalassemia: the properties of the free alpha-chains. J Clin Invest 1968, 47(4):860-866.
79. Bargellesi A., Pontremoli S., Menini C., et al. Kinetic evidence for the existence of alpha-globin pool in beta-thalassemic reticulocytes. Eur J Biochem 1968, 7(1):73-77.
80. Conconi F., Bargellesi A., Pontremoli S. Excess of alpha-globin synthesis in homozygous beta-thalassemia. Its cytoplasmic molecular forms. Eur J Biochem 1968, 5(3):409-414.
81. Nathan D.G., Stossel T.B., Gunn R.B., et al. Influence of hemoglobin precipitation on erythrocyte metabolism in alpha and beta thalassemia. J Clin Invest 1969, 48(1):33-41.
82. Rachmilewitz E.A., Peisach J., Blumberg W.E. Studies on the stability of oxyhemoglobin A and its constituent chains and their derivatives. J Biol Chem 1971, 246(10):3356-3366.
83. Bank A., Braverman A.S., O'Donnell J.V., et al. Absolute rates of globin chain synthesis in thalassemia. Blood 1968, 31(2):226-233.
84. Hanash S.M., Rucknagel D.L. Proteolytic activity in erythrocyte precursors. Proc Natl Acad Sci U S A 1978, 75(7):3427-3431.
85. Braverman A.S., Lester D. Evidence for increased proteolysis in intact beta thalassemia erythroid cells. Hemoglobin 1981, 5(6):549-564.
86. Loukopoulos D., Karoulias A., Fessas P. Proteolysis in thalassemia: studies with protease inhibitors. Ann N Y Acad Sci 1980, 344:323-335.
87. Vettore L., De Matteis M.C., Di Iorio E.E., et al. Erythrocytic proteases: preferential degradation of alpha hemoglobin chains. Acta Haematol 1983, 70(1):35-42.
88. Klemes Y., Etlinger J.D., Goldberg A.L. Properties of abnormal proteins degraded rapidly in reticulocytes. Intracellular aggregation of the globin molecules prior to hydrolysis. J Biol Chem 1981, 256(16):8436-8444.
89. Shaeffer J.R. Turnover of excess hemoglobin alpha chains in beta-thalassemic cells is ATP-dependent. J Biol Chem 1983, 258(21):13172-13177.
90. Shaeffer J.R. ATP-dependent proteolysis of hemoglobin alpha chains in beta-thalassemic hemolysates is ubiquitin-dependent. J Biol Chem 1988, 263(27):13663-13669.
91. Shaeffer J.R. Monoubiquitinated alpha globin is an intermediate in the ATP-dependent proteolysis of alpha globin. J Biol Chem 1994, 269(35):22205-22210.
92. Shaeffer J.R. Heterogeneity in the structure of the ubiquitin conjugates of human alpha globin. J Biol Chem 1994, 269(47):29530-29536.
93. Shaeffer J.R., Cohen R.E. Ubiquitin aldehyde increases adenosine triphosphate-dependent proteolysis of hemoglobin alpha-subunits in beta-thalassemic hemolysates. Blood 1997, 90(3):1300-1308.
94. Shaeffer J.R., Kania M.A. Degradation of monoubiquitinated alpha-globin by 26S proteasomes. Biochemistry 1995, 34(12):4015-4021.
95. Adachi K., Lakka V., Zhao Y., et al. Ubiquitylation of nascent globin chains in a cell-free system. J Biol Chem 2004, 279(40):41767-41774.
96. Ciavatta D.J., Ryan T.M., Farmer S.C., et al. Mouse model of human beta zero thalassemia: targeted deletion of the mouse beta maj- and beta min-globin genes in embryonic stem cells. Proc Natl Acad Sci U S A 1995, 92(20):9259-9263.
97. Yang B., Kirby S., Lewis J., et al. A mouse model for beta 0-thalassemia. Proc Natl Acad Sci U S A 1995, 92(25):11608-11612.
98. Rouyer-Fessard P., Leroy-Viard K., Domenget C., et al. Mouse beta thalassemia, a model for the membrane defects of erythrocytes in the human disease. J Biol Chem 1990, 265(33):20247-20251.
99. Rouyer-Fessard P., Scott M.D., Leroy-Viard K., et al. Fate of alpha-hemoglobin chains and erythrocyte defects in beta-thalassemia. Ann N Y Acad Sci 1990, 612:106-117.
100. Sancar G.B., Cedeno M.M., Rieder R.F. Rapid destruction of newly synthesized excess beta-globin chains in HbH disease. Blood 1981, 57(5):967-971.
101. Fagan J.M., Waxman L. The ATP-independent pathway in red blood cells that degrades oxidant-damaged hemoglobin. J Biol Chem 1992, 267(32):23015-23022.
102. Fagan J.M., Waxman L., Goldberg A.L. Red blood cells contain a pathway for the degradation of oxidant-damaged hemoglobin that does not require ATP or ubiquitin. J Biol Chem 1986, 261(13):5705-5713.
103. Fessas P. Inclusions of hemoglobin erythroblasts and erythrocytes of thalassemia. Blood 1963, 21:21-32.
104. Yataganas X., Fessas P. The pattern of hemoglobin precipitation in thalassemia and its significance. Ann N Y Acad Sci 1969, 165(1):270-287.
105. Braverman A.S., Schwartzberg L., Berkowitz R. Soluble and stroma-bound globin chains in mild and severe beta thalassemia. Hemoglobin 1982, 6(4):347-367.
106. Fessas P., Loukopoulos D., Kaltsoya A. Peptide analysis of the inclusions of erythroid cells in beta-thalassemia. Biochim Biophys Acta 1966, 124(2):430-432.
107. Fessas P., Loukopoulos D., Thorell B. Absorption spectra of inclusion bodies in beta-thalassemia. Blood 1965, 25:105-109.
108. Ballas S.K., Burka E.R., Gill F.M. Abnormal red cell membrane proteolytic activity in severe heterozygous beta-thalassemia. J Lab Clin Med 1982, 99(2):263-274.
109. Wickramasinghe S.N., Bush V. Observations on the ultrastructure of erythropoietic cells and reticulum cells in the bone marrow of patients with homozygous beta-thalassaemia. Br J Haematol 1975, 30(4):395-399.
110. Polliack A., Rachmilewitz E.A. Ultrastructural studies in beta-thalassaemia major. Br J Haematol 1973, 24(3):319-326.
111. Wickramasinghe S.N., Hughes M. Ultrastructural studies of erythropoiesis in beta-thalassaemia trait. Br J Haematol 1980, 46(3):401-407.
112. Wickramasinghe S.N., Hughes M. Precipitation of alpha-chains on the centrioles of erythroblasts in beta-thalassaemia. Br J Haematol 1982, 52(4):681-682.
113. Wickramasinghe S.N., Lee M.J. Evidence that the ubiquitin proteolytic pathway is involved in the degradation of precipitated globin chains in thalassaemia. Br J Haematol 1998, 101(2):245-250.
114. Wickramasinghe S.N., Lee M.J., Furukawa T., et al. Composition of the intra-erythroblastic precipitates in thalassaemia and congenital dyserythropoietic anaemia (CDA): identification of a new type of CDA with intra-erythroblastic precipitates not reacting with monoclonal antibodies to alpha- and beta-globin chains. Br J Haematol 1996, 93(3):576-585.
115. Ho P.J., Wickramasinghe S.N., Rees D.C., et al. Erythroblastic inclusions in dominantly inherited beta thalassemias. Blood 1997, 89(1):322-328.
116. Beris P., Miescher P.A., Diaz-Chico J.C., et al. Inclusion body beta-thalassemia trait in a Swiss family is caused by an abnormal hemoglobin (Geneva) with an altered and extended beta chain carboxy-terminus due to a modification in codon beta 114. Blood 1988, 72(2):801-805.
117. Wickramasinghe S.N., Hughes M., Fucharoen S., et al. The fate of excess beta-globin chains within erythropoietic cells in alpha-thalassaemia 2 trait, alpha-thalassaemia 1 trait, haemoglobin H disease and haemoglobin Q-H disease: an electron microscope study. Br J Haematol 1984, 56(3):473-482.
118. Wickramasinghe S.N., Hughes M., Hollan S.R., et al. Electron microscope and high resolution autoradiographic studies of the erythroblasts in haemoglobin H disease. Br J Haematol 1980, 45(3):401-404.
119. Antonelou M.H., Papassideri I.S., Karababa F.J., et al. Ultrastructural characterization of the erythroid cells in a novel case of congenital anemia. Blood Cells Mol Dis 2003, 30(1):30-42.
120. Iolascon A., Martire B., Lee M.J., et al. Transfusion-dependent congenital dyserythropoietic anaemia with intraerythroblastic inclusions of a non-globin protein. Eur J Haematol 2000, 65(2):140-143.
121. Salvatori F., Breveglieri G., Zuccato C., et al. Production of beta-globin and adult hemoglobin following G418 treatment of erythroid precursor cells from homozygous beta(0)39 thalassemia patients. Am J Hematol 2009, 84(11):720-728.
122. Zhang Y., Kwon S., Yamaguchi T., et al. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 2008, 28(5):1688-1701.
123. Hideshima T., Bradner J.E., Wong J., et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci U S A 2005, 102(24):8567-8572.
124. Colland F. The therapeutic potential of deubiquitinating enzyme inhibitors. Biochem Soc Trans 2010, 38(Pt 1):137-143.
125. Testa U. Proteasome inhibitors in cancer therapy. Curr Drug Targets 2009, 10(10):968-981.
126. Schessl J., Zou Y., McGrath M.J., et al. Proteomic identification of FHL1 as the protein mutated in human reducing body myopathy. J Clin Invest 2008, 118(3):904-912.
127. Lindsten K., Menéndez-Benito V., Masucci M.G., et al. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol 2003, 21(8):897-902.