Requirement of apoptotic protease-activating factor-1 for bortezomib-induced apoptosis but not for Fas-mediated apoptosis in human leukemic cells

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 245-255

  Ottosson Wadlund, Astrid ^a   Ceder, Rebecca ^a   Preta, Giulio ^a   Pokrovskaja, Katja ^c   Grafström, Roland C ^a,b   Heyman, Mats ^c   Sod̈erhäll, Stefan ^c   Grandeŕ, Dan ^c   Hedenfalk, Ingrid ^d   Robertson, John D ^e   Fadeel, Bengt ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d LUND UNIVERSITY   (Sweden)

^e UNIVERSITY OF KANSAS CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BORTEZOMIB; CASPASE 3; CYTOCHROME C; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLSERINE; PROTEIN NOXA; UBIQUITINATED PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA CONTENT; ENZYME ACTIVITY; ENZYME RELEASE; GENE SILENCING; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMIA CELL LINE; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

ADOLESCENT; ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BORONIC ACIDS; CASPASE 3; CHILD; CHILD, PRESCHOOL; CYTOCHROMES C; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GENE SILENCING; HUMANS; JURKAT CELLS; LEUKEMIA, MYELOID; MEMBRANE POTENTIAL, MITOCHONDRIAL; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZINES; RNA, SMALL INTERFERING; TRANSCRIPTOME;

EID: 84871593969     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.080788     Document Type: Article

References (51)

1. Almond JB, Snowden RT, Hunter A, Dinsdale D, Cain K, and Cohen GM (2001) Proteasome inhibitor-induced apoptosis of B-chronic lymphocytic leukaemia cells involves cytochrome c release and caspase activation, accompanied by formation of an approximately 700 kDa Apaf-1 containing apoptosome complex. Leukemia 15:1388-1397.
2. Baou M, Kohlhaas SL, Butterworth M, Vogler M, Dinsdale D, Walewska R, Majid A, Eldering E, Dyer MJ, and Cohen GM (2010) Role of NOXA and its ubiquitination in proteasome inhibitor-induced apoptosis in chronic lymphocytic leukemia cells. Haematologica 95:1510-1518.
3. Calvaruso G, Giuliano M, Portanova P, De Blasio A, Vento R, and Tesoriere G (2006) Bortezomib induces in HepG2 cells IkappaBalpha degradation mediated by caspase-8. Mol Cell Biochem 287:13-19.
4. Chauhan D, Singh A, Brahmandam M, Podar K, Hideshima T, Richardson P, Munshi N, Palladino MA, and Anderson KC (2008) Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. Blood 111:1654-1664.
5. Chen S, Blank JL, and Peters T et al. (2010) Genome-wide siRNA screen for modulators of cell death induced by proteasome inhibitor bortezomib. Cancer Res 70:4318-4326.
6. Cortes J, Thomas D, and Koller C et al. (2004) Phase I study of bortezomib in refractory or relapsed acute leukemias. Clin Cancer Res 10:3371-3376.
7. Cusack JC, Jr, Liu R, Houston M, Abendroth K, Elliott PJ, Adams J, and Baldwin AS, Jr (2001) Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res 61:3535-3540.
8. Danial NN and Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205-219.
9. Fadeel B, Ottosson A, and Pervaiz S (2008) Big wheel keeps on turning: apoptosome regulation and its role in chemoresistance. Cell Death Differ 15:443-452.
10. Fang HT, Zhang B, and Pan XF et al. (2012) Bortezomib interferes with C-KIT processing and transforms the t(8;21)-generated fusion proteins into tumor-suppressing fragments in leukemia cells. Proc Natl Acad Sci USA 109:2521-2526.
11. Franklin EE and Robertson JD (2007) Requirement of Apaf-1 for mitochondrial events and the cleavage or activation of all procaspases during genotoxic stress-induced apoptosis. Biochem J 405:115-122.
12. Fu WN, Bertoni F, Kelsey SM, McElwaine SM, Cotter FE, Newland AC, and Jia L (2003) Role of DNA methylation in the suppression of Apaf-1 protein in human leukaemia. Oncogene 22:451-455.
13. Gomez-Bougie P, Wuillème-Toumi S, Ménoret E, Trichet V, Robillard N, Philippe M, Bataille R, and Amiot M (2007) Noxa up-regulation and Mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res 67:5418-5424.
14. Guzman ML, Swiderski CF, Howard DS, Grimes BA, Rossi RM, Szilvassy SJ, and Jordan CT (2002) Preferential induction of apoptosis for primary human leukemic stem cells. Proc Natl Acad Sci USA 99:16220-16225.
15. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, Adams J, and Anderson KC (2001) The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 61:3071-3076.
16. Jia L, Srinivasula SM, Liu FT, Newland AC, Fernandes-Alnemri T, Alnemri ES, and Kelsey SM (2001) Apaf-1 protein deficiency confers resistance to cytochrome c-dependent apoptosis in human leukemic cells. Blood 98:414-421.
17. Jia L, Patwari Y, Kelsey SM, Srinivasula SM, Agrawal SG, Alnemri ES, and Newland AC (2003) Role of Smac in human leukaemic cell apoptosis and proliferation. Oncogene 22:1589-1599.
18. α)-tosyl-L-phenylalanine chloromethyl ketone induces caspase-dependent apoptosis in transformed human B cell lines with transcriptional down-regulation of anti-apoptotic HS1-associated protein X-1. J Biol Chem 284:27827-27837.
19. Juo P, Woo MS-A, Kuo CJ, Signorelli P, Biemann HP, Hannun YA, and Blenis J (1999) FADD is required for multiple signaling events downstream of the receptor Fas. Cell Growth Differ 10:797-804.
20. Karpinich NO, Tafani M, Schneider T, Russo MA, and Farber JL (2006) The course of etoposide-induced apoptosis in Jurkat cells lacking p53 and Bax. J Cell Physiol 208:55-63.
21. Karpova MB, Sanmun D, Henter JI, Smirnov AF, and Fadeel B (2006) Betulinic acid, a natural cytotoxic agent, fails to trigger apoptosis in human Burkitt's lymphoma-derived B-cell lines. Int J Cancer 118:246-252.
22. Kumatori A, Tanaka K, Inamura N, Sone S, Ogura T, Matsumoto T, Tachikawa T, Shin S, and Ichihara A (1990) Abnormally high expression of proteasomes in human leukemic cells. Proc Natl Acad Sci USA 87:7071-7075.
23. Kwiecinska A, Ottosson-Wadlund A, Ceder R, Grafström RC, Björck E, Nordenskjöld M, Porwit A, and Fadeel B (2011) HAX-1 expression in human B lymphoma. Leukemia 25:868-872.
24. Laane E, Panaretakis T, and Pokrovskaja K et al. (2007) Dexamethasone-induced apoptosis in acute lymphoblastic leukemia involves differential regulation of Bcl-2 family members. Haematologica 92:1460-1469.
25. Liu X, Yue P, Chen S, Hu L, Lonial S, Khuri FR, and Sun SY (2007) The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res 67:4981-4988.
26. Lukk M, Kapushesky M, Nikkilä J, Parkinson H, Goncalves A, Huber W, Ukkonen E, and Brazma A (2010) A global map of human gene expression. Nat Biotechnol 28:322-324.
27. Masdehors P, Omura S, Merle-Béral H, Mentz F, Cosset JM, Dumont J, Magdelénat H, and Delic J (1999) Increased sensitivity of CLL-derived lymphocytes to apoptotic death activation by the proteasome-specific inhibitor lactacystin. Br J Haematol 105:752-757.
28. Matondo M, Bousquet-Dubouch MP, Gallay N, Uttenweiler-Joseph S, Recher C, Payrastre B, Manenti S, Monsarrat B, and Burlet-Schiltz O (2010) Proteasome inhibitor-induced apoptosis in acute myeloid leukemia: a correlation with the proteasome status. Leuk Res 34:498-506.
29. Messinger Y, Gaynon P, Raetz E, Hutchinson R, Dubois S, Glade-Bender J, Sposto R, van der Giessen J, Eckroth E, and Bostrom BC (2010) Phase I study of bortezomib combined with chemotherapy in children with relapsed childhood acute lymphoblastic leukemia (ALL): a report from the therapeutic advances in childhood leukemia (TACL) consortium. Pediatr Blood Cancer 55:254-259.
30. Mitsiades N, Mitsiades CS, and Richardson PG et al. (2003) The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 101:2377-2380.
31. Nikrad M, Johnson T, Puthalalath H, Coultas L, Adams J, and Kraft AS (2005) The proteasome inhibitor bortezomib sensitizes cells to killing by death receptor ligand TRAIL via BH3-only proteins Bik and Bim. Mol Cancer Ther 4:443-449.
32. Orlowski RZ, Stinchcombe TE, and Mitchell BS et al. (2002) Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol 20:4420-4427.
33. Orlowski RZ and Kuhn DJ (2008) Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin Cancer Res 14:1649-1657.
34. Pérez-Galán P, Roué G, Villamor N, Montserrat E, Campo E, and Colomer D (2006) The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 107:257-264.
35. Qin JZ, Ziffra J, and Stennett L et al. (2005) Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res 65:6282-6293.
36. Ragusa M, Avola G, and Angelica R et al. (2010) Expression profile and specific network features of the apoptotic machinery explain relapse of acute myeloid leukemia after chemotherapy. BMC Cancer 10:377.
37. Russo SM, Tepper JE, Baldwin AS, Jr, Liu R, Adams J, Elliott P, and Cusack JC, Jr (2001) Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-kappaB. Int J Radiat Oncol Biol Phys 50:183-193.
38. Sandberg R and Ernberg I (2005) The molecular portrait of in vitro growth by meta-analysis of gene-expression profiles. Genome Biol 6:R65.1-R65.15.
39. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, and Peter ME (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17:1675-1687.
40. Schneider U, Schwenk HU, and Bornkamm G (1977) Characterization of EBV-genome negative "null" and "T" cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int J Cancer 19:621-626.
41. Shawgo ME, Shelton SN, and Robertson JD (2009) Caspase-9 activation by the apoptosome is not required for fas-mediated apoptosis in type II Jurkat cells. J Biol Chem 284:33447-33455.
42. Shelton SN, Dillard CD, and Robertson JD (2010) Activation of caspase-9, but not caspase-2 or caspase-8, is essential for heat-induced apoptosis in Jurkat cells. J Biol Chem 285:40525-40533.
43. Smith AJ, Dai H, Correia C, Takahashi R, Lee SH, Schmitz I, and Kaufmann SH (2011) Noxa/Bcl-2 protein interactions contribute to bortezomib resistance in human lymphoid cells. J Biol Chem 286:17682-17692.
44. Soengas MS, Capodieci P, and Polsky D et al. (2001) Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 409:207-211.
45. Soligo D, Servida F, Delia D, Fontanella E, Lamorte G, Caneva L, Fumiatti R, and Lambertenghi Deliliers G (2001) The apoptogenic response of human myeloid leukaemia cell lines and of normal and malignant haematopoietic progenitor cells to the proteasome inhibitor PSI. Br J Haematol 113:126-135.
46. Sturm I, Bosanquet AG, Radetzki S, Hummel M, Dörken B, and Daniel PT (2006) Silencing of APAF-1 in B-CLL results in poor prognosis in the case of concomitant p53 mutation. Int J Cancer 118:2329-2336.
47. Sun Y, Orrenius S, Pervaiz S, and Fadeel B (2005) Plasma membrane sequestration of apoptotic protease-activating factor-1 in human B-lymphoma cells: a novel mechanism of chemoresistance. Blood 105:4070-4077.
48. Sun Y, Ottosson A, Pervaiz S, and Fadeel B (2007) Smac-mediated sensitization of human B-lymphoma cells to staurosporine- and lactacystin-triggered apoptosis is apoptosome-dependent. Leukemia 21:1035-1043.
49. Uthaisang W, Nutt LK, Orrenius S, and Fadeel B (2003) Phosphatidylserine exposure in Fas type I cells is mitochondria-dependent. FEBS Lett 545:110-114.
50. Vink J, Cloos J, and Kaspers GJ (2006) Proteasome inhibition as novel treatment strategy in leukaemia. Br J Haematol 134:253-262.
51. Zhao X, Qiu W, Kung J, Zhao X, Peng X, Yegappan M, Yen-Lieberman B, and Hsi ED (2008) Bortezomib induces caspase-dependent apoptosis in Hodgkin lymphoma cell lines and is associated with reduced c-FLIP expression: a gene expression profiling study with implications for potential combination therapies. Leuk Res 32:275-285.