Inhibition of proteasome by bortezomib causes intracellular aggregation of hepatic serpins and increases the latent circulating form of antithrombin

Laboratory Investigation

Volumn 88, Issue 3, 2008, Pages 306-317

  Hernández Espinosa, David ^a   Mĩano, Antonia ^a   Martínez, Constantino ^a   Ordõez, Adriana ^a   Pérez Ceballos, Elena ^a   De Arriba, Felipe ^a   Mota, Rubén A ^b   Ferrer, Francisca ^a   González, Marcos ^c   Vicente, Vicente ^a   Corral, Javier ^a  

^a HOSPITAL UNIVERSITARIO MORALES MESEGUER   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

^c HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

Aggregation; Bortezomib; Conformation; Heat shock proteins; Proteasome inhibitors; Serpin

Indexed keywords

ALPHA 1 ANTITRYPSIN; ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; BORTEZOMIB; FIBRINOGEN; PROTEASOME; PROTHROMBIN; SERINE PROTEINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSED IMMUNOELECTROPHORESIS; DRUG EFFECT; HEAT STRESS; HUMAN; HUMAN CELL; IMMUNOHISTOLOGY; LIVER TOXICITY; LUNG DISEASE; MALE; MALLORY BODY; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; RESPIRATORY FAILURE;

ALLELES; ALPHA 1-ANTITRYPSIN; ANIMALS; ANTINEOPLASTIC AGENTS; ANTITHROMBINS; BORONIC ACIDS; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG EVALUATION, PRECLINICAL; ENDOPLASMIC RETICULUM; FACTOR XA; FIBRINOGEN; HUMANS; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENOUS; LEUKOCYTE ELASTASE; LIVER; LIVER NEOPLASMS; MALE; MICE; MOLECULAR CHAPERONES; MULTIPLE MYELOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; PYRAZINES; SERPINS; UBIQUITIN;

EID: 39749085077     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.3700717     Document Type: Article

References (52)

1. Carrell RW, Huntington JA. How serpins change their fold for better and for worse. Biochem Soc Symp 2003;70:163-178.
2. Lomas DA, Carrell RW. Serpinopathies and the conformational dementias. Nat Rev Genet 2002;3:759-768.
3. Meusser B, Hirsch C, Jarosch E, et al. ERAD: the long road to destruction. Nat Cell Biol 2005;7:766-772.
4. Carrell RW. Cell toxicity and conformational disease. Trends Cell Biol 2005;15:574-580.
5. Tokunaga F, Shirotani H, Hara K, et al. Intracellular degradation of secretion defect-type mutants of antithrombin is inhibited by proteasomal inhibitors. FEBS Lett 1997;412:65-69.
6. Shirotani H, Tokunaga F, Koide T. Cellular and functional characterization of three recombinant antithrombin mutants that caused pleiotropic effect-type deficiency. J Biochem (Tokyo) 1999;125:253-262.
7. Wu Y, Swulius MT, Moremen KW, et al. Elucidation of the molecular logic by which misfolded alpha 1-antitrypsin is preferentially selected for degradation. Proc Natl Acad Sci USA 2003;100:8229-8234.
8. Teckman JH, Burrows J, Hidvegi T, et al. The proteasome participates in degradation of mutant alpha 1-antitrypsin Z in the endoplasmic reticulum of hepatoma-derived hepatocytes. J Biol Chem 2001;276:44865-44872.
9. Miranda E, Romisch K, Lomas DA. Mutants of neuroserpin that cause dementia accumulate as polymers within the endoplasmic reticulum. J Biol Chem 2004;279:28283-28291.
10. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 2005;12:1178-1190.
11. Richardson PG, Mitsiades C. Bortezomib: proteasome inhibition as an effective anticancer therapy. Future Oncol 2005;1:161-171.
12. Bruce D, Perry DJ, Borg J-Y, et al. Thromboembolic disease due to thermolabile conformational changes of antithrombin Rouen-VI (197 Asn-Asp). J Clin Invest 1994;94:2265-2274.
13. Zhou A, Huntington JA, Carrell RW. Formation of the antithrombin heterodimer in vivo and the onset of thrombosis. Blood 1999;94:3388-3396.
14. Mushunje A, Evans G, Brennan SO, et al. Latent antithrombin and its detection, formation and turnover in the circulation. J Thromb Haemost 2004;2:2170-2177.
15. Corral J, Rivera J, Martinez C, et al. Detection of conformational transformation of antithrombin in blood with crossed immunoelectrophoresis: new application for a classical method. J Lab Clin Med 2003;142:298-305.
16. Hernandez-Espinosa D, Minano A, Martinez C, et al. L-asparaginase-induced antithrombin type I deficiency: implications for conformational diseases. Am J Pathol 2006;169:142-153.
17. Braun A, Meyer P, Cleve H, et al. Rapid and simple diagnosis of the two common a1-proteinase inhibitor deficiency alleles P1*Z and Pi*S by DNA analysis. Eur J Clin Chem Clin Biochem 1996;34:761-764.
18. Corral J, Vicente V, Carrell RW. Thrombosis as a conformational disease. Haematologica 2005;90:238-246.
19. Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003;348:2609-2617.
20. Riley NE, Li J, McPhaul LW, et al. Heat shock proteins are present in Mallory bodies (cytokeratin aggresomes) in human liver biopsy specimens. Exp Mol Pathol 2003;74:168-172.
21. Swanson JC, Suttie JW. Prothrombin biosynthesis: characterization of processing events in rat liver microsomes. Biochemistry 1985;24:3890-3897.
22. Uehara S, Gotoh K, Handa H, et al. Process of carboxylation of glutamic acid residues in the gla domain of human des-gamma-carboxyprothrombin. Clin Chim Acta 1999;289:33-44.
23. The Human Gene Mutation Database at the Institute of Medical Genetics in Cardiff. http://www.hgmd.cf.ac.uk.
24. Vu D, Neerman-Arbez M. Molecular mechanism accounting for fibrinogen deficiency: from large deletions to intracellular retention of misfolded proteins. J Throm Hemost 2007;5(Suppl 1):125-131.
25. Obeng EA, Carlson LM, Gutman DM, et al. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006;107:4907-4916.
26. VanSlyke JK, Musil LS. Dislocation and degradation from the ER are regulated by cytosolic stress. J Cell Biol 2002;157:381-394.
27. Bush KT, Goldberg AL, Nigam SK. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J Biol Chem 1997;272:9086-9092.
28. Kim D, Kim SH, Li GC. Proteasome inhibitors MG132 and lactacystin hyperphosphorylate SF1 and induce hsp70 and hsp27 expression. Biochem Biophys Res Commun 1999;254:264-268.
29. Carrell RW, Lomas DA. Conformational disease. Lancet 1997;350:134-138.
30. Hernandez-Espinosa D, Ayala I, Castells MT, et al. Intracellular retention of hepatic serpins caused by severe hyperlipidemia. Liver Int 2006;26:708-715.
31. Hernández-Espinosa D, Mota R, Miñano A, et al. In vivo effects of hyperthermia on the functional and conformational characteristics of antithrombin. J Thromb Haemost 2007;5:963-970.
32. Lomas DA, Parfrey H. α1-antitrypsin deficiency 4: molecular pathophysiology. Thorax 2004;59:529-535.
33. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999;13:1211-1213.
34. Johnston JA, Ward CL, Kopito RR. Aggresomes: a cellular response to misfolded proteins. J Cell Biol 1998;143:1883-1898.
35. French BA, van Leeuwen F, Riley NE et al. Aggresome formation in liver cells in response to different toxic mechanisms: role of the ubiquitin-proteasome pathway and the frameshift mutant of ubiquitin. Exp Mol Pathol 2001;71:241-246.
36. Bardag-Gorce F, Riley NE, Nan L, et al. The proteasome inhibitor, PS-341, causes cytokeratin aggresome formation. Exp Mol Pathol 2004;76:9-16.
37. Moura Nunes JF, Soares J, Costa MC. Confronting cisternae in human hepatocellular carcinoma. J Submicrosc Cytol 1986;18:441-444.
38. Witzleben CL, Marshall GS, Wenner W, et al. HIV as a cause of giant cell hepatitis. Hum Pathol 1988;19:603-605.
39. Palisano JR. The origin and role of confronting cisternae in selected fetal mouse and rat tissues. Cell Biol Int Rep 1990;14:1025-1032.
40. Watanabe S, Ito T, Shirai M, et al. Electron microscopic studies of peripheral blood mononuclear cells in chronic type C hepatitis treated with interferon-alpha. Ultrastruct Pathol 1995;19:1-8.
41. Stumptner C, Fuchsbichler A, Heid H, et al. Mallory body - a disease-associated type of sequestosome. Hepatology 2002;35:1053-1062.
42. Mathew A, Mathur SK, Morimoto RI. Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol Cell Biol 1998;18:5091-5098.
43. Bruce D, Perry DJ, Borg JY, et al. Thromboembolic disease due to thermolabile conformational changes of antithrombin Rouen-VI (187 Asn→Asp). J Clin Invest 1994;94:2265-2274.
44. Picard V, Dautzenberg MD, Villoutreix BO, et al. Antithrombin Phe229Leu: a new homozygous variant leading to spontaneous antithrombin polymerization in vivo associated with severe childhood thrombosis. Blood 2003;102:919-925.
45. Beauchamp NJ, Pike RN, Daly M, et al. Antithrombins Wibble and Wobble (T85M/K): archetypal conformational diseases with in vivo latent-transition, thrombosis, and heparin activation. Blood 1998;92:2696-2706.
46. Corral J, Rivera J, Guerrero JA, et al. Latent and polymeric antithrombin: clearance and potential thrombotic risk. Exp Biol Med 2007;232:219-226.
47. Roemisch J, Gray E, Hoffmann JN, Wiedermann CJ. Antithrombin: a new look at the actions of a serine protease inhibitor. Blood Coagul Fibrinolysis 2002;13:657-670.
48. Davis NB, Taber DA, Ansari RH, et al. Phase II trial of PS-341 in patients with renal cell cancer: a University of Chicago phase II consortium study. J Clin Oncol 2004;22:115-119.
49. Rosinol L, Montoto S, Cibeira MT, et al. Bortezomib-induced severe hepatitis in multiple myeloma: a case report. Arch Intern Med 2005;165:464-465.
50. Miyakoshi S, Kami M, Yuji K, et al. Severe pulmonary complications in Japanese patients after bortezomib treatment for refractory multiple myeloma. Blood 2006;107:3492-3494.
51. Zappasodi P, Dore R, Castagnola C, et al. Rapid response to high-dose steroids of severe bortezomib-related pulmonary complication in multiple myeloma. J Clin Oncol 2007;25:3380-3381.
52. Harousseau JL. Thalidomide in multiple myeloma: past, present and future. Future Oncol 2006;2:577-589.