Prevalence of bortezomib-resistant constitutive NF-kappaB activity in mantle cell lymphoma

Molecular Cancer

Volumn 7, Issue , 2008, Pages

  Yang, David T ^a   Young, Ken H ^a,b   Kahl, Brad S ^a,b   Markovina, Stephanie ^a   Miyamoto, Shigeki ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CALCIUM CHANNEL L TYPE; CALCIUM CHELATING AGENT; CALMODULIN INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PERILLYL ALCOHOL; PROTEASOME; PROTEASOME INHIBITOR; TERPENE; ANTINEOPLASTIC AGENT; BORONIC ACID DERIVATIVE; PYRAZINE DERIVATIVE;

ADULT; AGED; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; B CELL LYMPHOMA; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; DRUG TARGETING; ENZYME INHIBITION; FEMALE; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; MALE; MANTLE CELL LYMPHOMA; MOUSE; NONHUMAN; PREVALENCE; ANIMAL; DRUG ANTAGONISM; DRUG RESISTANCE; METABOLISM; MIDDLE AGED; PATHOLOGY; TUMOR CELL LINE;

HUMAN HERPESVIRUS 4;

AGED; AGED, 80 AND OVER; ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FEMALE; HUMANS; LYMPHOMA, MANTLE-CELL; MALE; MIDDLE AGED; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES;

EID: 44849083877     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-7-40     Document Type: Article

References (82)

1. Swerdlow SH Nathwani BN Berger F Piris MA Isaacson PG Harris NL Muller-Hermelink HK Mantle cell lymphoma World Health Organization Classification of Tumours H. Lyon: IARC Press Jaffe V, Harris ES, Stein NL 2001, 160-170
2. Bosch F Lopez-Guillermo A Campo E Ribera JM Conde E Piris MA Vallespi T Woessner S Montserrat E Mantle cell lymphoma: Presenting features, response to therapy, and prognostic factors Cancer 1998, 82:567-75 10.1002/(SICI)1097-0142(19980201)82:3<567::AID-CNCR20>3.0.CO;2-Z 9452276
3. Argatoff LH Connors JM Klasa RJ Horsman DE Gascoyne RD Mantle cell lymphoma: A clinicopathologic study of 80 cases Blood 1997, 89:2067-78 9058729
4. Williams ME Densmore JJ Biology and therapy of mantle cell lymphoma Curr Opin Oncol 2005, 17:425-31 10.1097/01.cco.0000174039.69656.2b 16093790
5. Jemal A Siegel R Ward E Murray T Xu J Thun MJ Cancer statistics, 2007 CA Cancer J Clin 2007, 57:43-66 17237035
6. The Non-Hodgkin's Lymphoma Classification Project A clinical evaluation of the international lymphoma study group classification of non-hodgkin's lymphoma Blood 1997, 89:3909-3918 9166827
7. Dreyling M Forstpointner R Gramatzki M Bock H Hanel A Seymour JF Planker M Duhrsen U Wilms K Unterhalt M Hiddemann W Rituximab maintenance improves progression-free and overall survival rates after combined immun-chemotherapy (R-FCM) in patients with relapsed follicular and mantle cell lymphoma: Final results of a prospective randomized trial of the german low grade lymphoma study group (GLGLSG) J Clin Oncol 2006, 24:422s
8. Dreyling M Lenz G Hoster E Van Hoof A Gisselbrecht C Schmits R Metzner B Truemper L Reiser M Steinhauer H Boiron JM Boogaerts MA Aldaoud A Silingardi V Kluin-Nelemans HC Hasford J Parwaresch R Unterhalt M Hiddemann W Early consolidation by myeloablative radiochemotherapy followed by autologous stem cell transplantation in first remission significantly prolongs progression-free survival in mantle-cell lymphoma: Results of a prospective randomized trial of the european MCL network Blood 2005, 105:2677-2684 10.1182/blood-2004-10-3883 15591112
9. Kahl BS Longo WL Eickhoff JC Zehnder J Jones C Blank J McFarland T Bottner W Rezazedeh H Werndli J Bailey HH Wisconsin Oncology Network Maintenance rituximab following induction chemoimmunotherapy may prolong progression-free survival in mantle cell lymphoma: A pilot study from the wisconsin oncology network Ann Oncol 2006, 17:1418-1423 10.1093/ annonc/mdl127 16766582
10. Romaguera JE Fayad L Rodriguez MA Broglio KR Hagemeister FB Pro B McLaughlin P Younes A Samaniego F Goy A Sarris AH Dang NH Wang M V B Medeiros LJ Katz RL Gagneja H Samuels BI Smith TL Cabanillas FF High rate of durable remissions after treatment of newly diagnosed aggressive mantle-cell lymphoma with rituximab plus hyper-CVAD alternating with rituximab plus high-dose methotrexate and cytarabine J Clin Oncol 2005, 23:7013-23 10.1200/JCO.2005.01.1825 16145068
11. Lenz G Dreyling M Hoster E Wormann B Duhrsen U Metzner B Eimermacher H Neubauer A Wandt H Steinhauer H Martin S Heidemann E Aldaoud A Parwaresch R Hasford J Unterhalt M Hiddemann W Immunochemotherapy with rituximab and cyclophosphamide, doxorubicin, vincristine, and prednisone significantly improves response and time to treatment failure, but not long-term outcome in patients with previously untreated mantle cell lymphoma: Results of a prospective randomized trial of the german low grade lymphoma study group (GLSG) J Clin Oncol 2005, 23:1984-92 10.1200/ JCO.2005.08.133 15668467
12. Nickenig C Dreyling M Hoster E Pfreundschuh M Trumper L Reiser M Wandt H Lengfelder E Unterhalt M Hiddemann W Combined cyclophosphamide, vincristine, doxorubicin, and prednisone (CHOP) improves response rates but not survival and has lower hematologic toxicity compared with combined mitoxantrone, chlorambucil, and prednisone (MCP) in follicular and mantle cell lymphomas: Results of a prospective randomized trial of the german low-grade lymphoma study group Cancer 2006, 107:1014-22 10.1002/cncr.22093 16878325
13. Forstpointner R Unterhalt M Dreyling M Bock HP Repp R Wandt H Pott C Seymour JF Metzner B Hanel A Lehmann T Hartmann F Einsele H Hiddemann W Maintenance therapy with rituximab leads to a significant prolongation of response duration after salvage therapy with a combination of rituximab, fludarabine, cyclophosphamide, and mitoxantrone (R-FCM) in patients with recurring and refractory follicular and mantle cell lymphomas: Results of a prospective randomized study of the german low grade lymphoma study group (GLSG) Blood 2006, 108:4003-8 10.1182/ blood-2006-04-016725 16946304
14. Fisher RI Dahlberg S Nathwani BN Banks PM Miller TP Grogan TM A clinical analysis of two indolent lymphoma entities: Mantle cell lymphoma and marginal zone lymphoma (including the mucosa-associated lymphoid tissue and monocytoid B-cell subcategories): A southwest oncology group study Blood 1995, 85:1075-82 7849295
15. Howard OM Gribben JG Neuberg DS Grossbard M Poor C Janicek MJ Shipp MA Rituximab and CHOP induction therapy for newly diagnosed mantle-cell lymphoma: Molecular complete responses are not predictive of progression-free survival J Clin Oncol 2002, 20:1288-94 10.1200/ JCO.20.5.1288 11870171
16. Orlowski RZ Stinchcombe TE Mitchell BS Shea TC Baldwin AS Stahl S Adams J Esseltine DL Elliott PJ Pien CS Guerciolini R Anderson JK Depcik-Smith ND Bhagat R Lehman MJ Novick SC O'Connor OA Soignet SL Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies J Clin Oncol 2002, 20:4420-7 10.1200/JCO.2002.01.133 12431963
17. Jagannath S Barlogie B Berenson J Siegel D Irwin D Richardson PG Niesvizky R Alexanian R Limentani SA Alsina M Adams J Kauffman M Esseltine DL Schenkein DP Anderson KC A phase 2 study of two doses of bortezomib in relapsed or refractory myeloma Br J Haematol 2004, 127:165-72 10.1111/j.1365-2141.2004.05188.x 15461622
18. Richardson PG Barlogie B Berenson J Singhal S Jagannath S Irwin D Rajkumar SV Srkalovic G Alsina M Alexanian R Siegel D Orlowski RZ Kuter D Limentani SA Lee S Hideshima T Esseltine DL Kauffman M Adams J Schenkein DP Anderson KC A phase 2 study of bortezomib in relapsed, refractory myeloma N Engl J Med 2003, 348:2609-17 10.1056/NEJMoa030288 12826635
19. Bross PF Kane R Farrell AT Abraham S Benson K Brower ME Bradley S Gobburu JV Goheer A Lee SL Leighton J Liang CY Lostritto RT McGuinn WD Morse DE Rahman A Rosario LA Verbois SL Williams G Wang YC Pazdur R Approval summary for bortezomib for injection in the treatment of multiple myeloma Clin Cancer Res 2004 10 3954 64 10.1158/ 1078-0432.CCR-03-0781 15217925
20. Kane RC Bross PF Farrell AT Pazdur R Velcade: U.S. FDA approval for the treatment of multiple myeloma progressing on prior therapy Oncologist 2003, 8:508-13 10.1634/theoncologist.8-6-508 14657528
21. O'Connor OA Wright J Moskowitz C Muzzy J MacGregor-Cortelli B Stubblefield M Straus D Portlock C Hamlin P Choi E Dumetrescu O Esseltine D Trehu E Adams J Schenkein D Zelenetz AD Phase II clinical experience with the novel proteasome inhibitor bortezomib in patients with indolent non-hodgkin's lymphoma and mantle cell lymphoma J Clin Oncol 2005, 23:676-84 10.1200/JCO.2005.02.050 15613699
22. Goy A Younes A McLaughlin P Pro B Romaguera JE Hagemeister F Fayad L Dang NH Samaniego F Wang M Broglio K Samuels B Gilles F Sarris AH Hart S Trehu E Schenkein D Cabanillas F Rodriguez AM Phase II study of proteasome inhibitor bortezomib in relapsed or refractory B-cell non-hodgkin's lymphoma J Clin Oncol 2005, 23:667-75 10.1200/ JCO.2005.03.108 15613697
23. Strauss SJ Maharaj L Hoare S Johnson PW Radford JA Vinnecombe S Millard L Rohatiner A Boral A Trehu E Schenkein D Balkwill F Joel SP Lister TA Bortezomib therapy in patients with relapsed or refractory lymphoma: Potential correlation of in vitro sensitivity and tumor necrosis factor alpha response with clinical activity J Clin Oncol 2006, 24:2105-12 10.1200/JCO.2005.04.6789 16606971
24. Belch A Kouroukis C Crump M Sehn L Gascoyne R Klasa R Powers J Wright J Eisenhauer E A phase II study of bortezomib in mantle cell lymphoma: The national cancer institute of canada clinical trials group trial IND.150 Ann Oncol 2007, 18:116-21 10.1093/annonc/mdl316 16971665
25. Pham LV Tamayo AT Yoshimura LC Lo P Ford RJ Inhibition of constitutive NF-kappa B activation in mantle cell lymphoma B cells leads to induction of cell cycle arrest and apoptosis J Immunol 2003, 171:88-95 12816986
26. Fu L Lin-Lee YC Pham LV Tamayo A Yoshimura L Ford RJ Constitutive NF-kappaB and NFAT activation leads to stimulation of the BLyS survival pathway in aggressive B-cell lymphomas Blood 2006, 107:4540-8 1895801 16497967 10.1182/blood-2005-10-4042
27. Perez-Galan P Roue G Villamor N Montserrat E Campo E Colomer D The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and noxa activation independent of p53 status Blood 2006, 107:257-64 10.1182/blood-2005-05-2091 16166592
28. Karin M Nuclear factor-kappaB in cancer development and progression Nature 2006, 441:431-6 10.1038/nature04870 16724054
29. Hayden MS Ghosh S Signaling to NF-kappaB Genes Dev 2004, 18:2195-224 10.1101/gad.1228704 15371334
30. Kim HJ Hawke N Baldwin AS NF-kappaB and IKK as therapeutic targets in cancer Cell Death Differ 2006, 13:738-47 10.1038/sj.cdd.4401877 16485028
31. Luo JL Kamata H Karin M IKK/NF-kappaB signaling: Balancing life and death - a new approach to cancer therapy J Clin Invest 2005, 115:2625-32 1236696 16200195 10.1172/JCI26322
32. Keutgens A Robert I Viatour P Chariot A Deregulated NF-kappaB activity in haematological malignancies Biochem Pharmacol 2006, 72:1069-80 10.1016/j.bcp.2006.06.011 16854381
33. Shishodia S Amin HM Lai R Aggarwal BB Curcumin (diferuloylmethane) inhibits constitutive NF-kappaB activation, induces G1/S arrest, suppresses proliferation, and induces apoptosis in mantle cell lymphoma Biochem Pharmacol 2005, 70:700-13 10.1016/j.bcp.2005.04.043 16023083
34. Ghosh S Karin M Missing pieces in the NF-kappaB puzzle Cell 2002, 109(Suppl):S81-96 10.1016/S0092-8674(02)00703-1 11983155
35. Xiao G Harhaj EW Sun SC NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100 Mol Cell 2001, 7:401-9 10.1016/ S1097-2765(01)00187-3 11239468
36. Xiao G Cvijic ME Fong A Harhaj EW Uhlik MT Waterfield M Sun SC Retroviral oncoprotein tax induces processing of NF-kappaB2/p100 in T cells: Evidence for the involvement of IKKalpha Embo J 2001, 20:6805-15 125766 11726516 10.1093/emboj/20.23.6805
37. Senftleben U Cao Y Xiao G Greten FR Krahn G Bonizzi G Chen Y Hu Y Fong A Sun SC Karin M Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway Science 2001, 293:1495-9 10.1126/ science.1062677 11520989
38. Han Y Weinman S Boldogh I Walker RK Brasier AR Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation J Biol Chem 1999, 274:787-794 10.1074/ jbc.274.2.787 9873017
39. Baghdiguian S Martin M Richard I Pons F Astier C Bourg N Hay RT Chemaly R Halaby G Loiselet J Anderson LV Lopez de Munain A Fardeau M Mangeat P Beckmann JS Lefranc G Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A Nat Med 1999, 5:503-511 10.1038/10579 10229226
40. Marcilhac A Raynaud F Clerc I Benyamin Y Detection and localization of calpain 3-like protease in a neuronal cell line: Possible regulation of apoptotic cell death through degradation of nuclear IkappaBalpha Int J Biochem Cell Biol 2006, 38:2128-2140 10.1016/j.biocel.2006.06.005 16938483
41. Canty TG Jr Boyle EM Jr Farr A Morgan EN Verrier ED Pohlman TH Oxidative stress induces NF-kappaB nuclear translocation without degradation of IkappaBalpha Circulation 1999, 100:II361-4 10567330
42. Kato T Jr Delhase M Hoffmann A Karin M CK2 is a C-terminal IkappaB kinase responsible for NF-kappaB activation during the UV response Mol Cell 2003, 12:829-839 10.1016/S1097-2765(03)00358-7 14580335
43. Shumway SD Berchtold CM Gould MN Miyamoto S Evidence for unique calmodulin-dependent nuclear factor-kappaB regulation in WEHI-231 B cells Mol Pharmacol 2002, 61:177-85 10.1124/mol.61.1.177 11752219
44. Miyamoto S Seufzer BJ Shumway SD Novel IkappaB alpha proteolytic pathway in WEHI231 immature B cells Mol Cell Biol 1998, 18:19-29 121444 9418849
45. O'Connor S Shumway SD Amanna IJ Hayes CE Miyamoto S Regulation of constitutive p50/c-rel activity via proteasome inhibitor-resistant IkappaBalpha degradation in B cells Mol Cell Biol 2004, 24:4895-908 416427 15143182 10.1128/MCB.24.11.4895-4908.2004
46. Berchtold CM Chen KS Miyamoto S Gould MN Perillyl alcohol inhibits a calcium-dependent constitutive nuclear factor-kappaB pathway Cancer Res 2005, 65:8558-66 10.1158/0008-5472.CAN-04-4072 16166337
47. Mori N Fujii M Ikeda S Yamada Y Tomonaga M Ballard DW Yamamoto N Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells Blood 1999, 93:2360-8 10090947
48. Davis RE Brown KD Siebenlist U Staudt LM Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells J Exp Med 2001, 194:1861-74 2193582 11748286 10.1084/jem.194.12.1861
49. Bargou RC Emmerich F Krappmann D Bommert K Mapara MY Arnold W Royer HD Grinstein E Greiner A Scheidereit C Dorken B Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of hodgkin's disease tumor cells J Clin Invest 1997, 100:2961-9 508507 9399941 10.1172/JCI119849
50. Wang W Abbruzzese JL Evans DB Larry L Cleary KR Chiao PJ The nuclear factor-kappa B RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells Clin Cancer Res 1999, 5:119-27 9918209
51. Zerbini LF Wang Y Cho JY Libermann TA Constitutive activation of nuclear factor kappaB p50/p65 and fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer Cancer Res 2003, 63:2206-15 12727841
52. Duffey DC Chen Z Dong G Ondrey FG Wolf JS Brown K Siebenlist U Van Waes C Expression of a dominant-negative mutant inhibitor-kappaBalpha of nuclear factor-kappaB in human head and neck squamous cell carcinoma inhibits survival, proinflammatory cytokine expression, and tumor growth in vivo Cancer Res 1999, 59:3468-74 10416612
53. Sovak MA Bellas RE Kim DW Zanieski GJ Rogers AE Traish AM Sonenshein GE Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer J Clin Invest 1997, 100:2952-60 508506 9399940 10.1172/ JCI119848
54. Annunziata CM Davis RE Demchenko Y Bellamy W Gabrea A Zhan F Lenz G Hanamura I Wright G Xiao W Dave S Hurt EM Tan B Zhao H Stephens O Santra M Williams DR Dang L Barlogie B Shaughnessy JD Jr Kuehl WM Staudt LM Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma Cancer Cell 2007, 12:115-130 10.1016/j.ccr.2007.07.004 17692804
55. Keats JJ Fonseca R Chesi M Schop R Baker A Chng WJ Van Wier S Tiedemann R Shi CX Sebag M Braggio E Henry T Zhu YX Fogle H Price-Troska T Ahmann G Mancini C Brents LA Kumar S Greipp P Dispenzieri A Bryant B Mulligan G Bruhn L Barrett M Valdez R Trent J Stewart AK Carpten J Bergsagel PL Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma Cancer Cell 2007, 12:131-144 10.1016/j.ccr.2007.07.003 17692805
56. Fields ER Seufzer BJ Oltz EM Miyamoto S A switch in distinct I kappa B alpha degradation mechanisms mediates constitutive NF-kappa B activation in mature B cells J Immunol 2000, 164:4762-7 10779782
57. O'Connor S Markovina S Miyamoto S Evidence for a phosphorylation-independent role for ser 32 and 36 in proteasome inhibitor-resistant (PIR) IkappaBalpha degradation in B cells Exp Cell Res 2005, 307:15-25 10.1016/j.yexcr.2005.02.015 15922723
58. Shumway SD Miyamoto S A mechanistic insight into a proteasome-independent constitutive inhibitor kappaBalpha (IkappaBalpha) degradation and nuclear factor kappaB (NF-kappaB) activation pathway in WEHI-231 B-cells Biochem J 2004, 380:173-80 1224141 14763901 10.1042/ BJ20031796
59. Nakamura Y Grumont RJ Gerondakis S NF-kappaB1 can inhibit v-abl-induced lymphoid transformation by functioning as a negative regulator of cyclin D1 expression Mol Cell Biol 2002, 22:5563-5574 133951 12101248 10.1128/ MCB.22.15.5563-5574.2002
60. Gould MN Cancer chemoprevention and therapy by monoterpenes Environ Health Perspect 1997, 105(Suppl 4):977-979 1470060 9255590 10.2307/ 3433313
61. Salaverria I Perez-Galan P Colomer D Campo E Mantle cell lymphoma: From pathology and molecular pathogenesis to new therapeutic perspectives Haematologica 2006, 91:11-6 16434365
62. Miyamoto S Schmitt MJ Verma IM Qualitative changes in the subunit composition of kappa B-binding complexes during murine B-cell differentiation Proc Natl Acad Sci USA 1994, 91:5056-60 43930 8197184 10.1073/pnas.91.11.5056
63. Zamai L Falcieri E Marhefka G Vitale M Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation Cytometry 1996, 23:303-11 10.1002/ (SICI)1097-0320(19960401)23:4<303::AID-CYTO6>3.0.CO;2-H 8900473
64. Chou TC Talalay P Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors Adv Enzyme Regul 1984, 22:27-55 10.1016/0065-2571(84)90007-4 6382953
65. Chou TC Talalay P Generalized equations for the analysis of inhibitions of michaelis-menten and higher-order kinetic systems with two or more mutually exclusive and nonexclusive inhibitors Eur J Biochem 1981, 115:207-216 7227366
66. Herrero JA Mathew P Paya CV LMP-1 activates NF-kappa B by targeting the inhibitory molecule I kappa B alpha J Virol 1995, 69:2168-74 188885 7884865
67. Haag JD Gould MN Mammary carcinoma regression induced by perillyl alcohol, a hydroxylated analog of limonene Cancer Chemother Pharmacol 1994, 34:477-483 10.1007/BF00685658 7923558
68. Mills JJ Chari RS Boyer IJ Gould MN Jirtle RL Induction of apoptosis in liver tumors by the monoterpene perillyl alcohol Cancer Res 1995, 55:979-983 7867007
69. Stark MJ Burke YD McKinzie JH Ayoubi AS Crowell PL Chemotherapy of pancreatic cancer with the monoterpene perillyl alcohol Cancer Lett 1995, 96:15-21 10.1016/0304-3835(95)03912-G 7553603
70. Xu M Floyd HS Greth SM Chang WC Lohman K Stoyanova R Kucera GL Kute TE Willingham MC Miller MS Perillyl alcohol-mediated inhibition of lung cancer cell line proliferation: Potential mechanisms for its chemotherapeutic effects Toxicol Appl Pharmacol 2004, 195:232-246 10.1016/j.taap.2003.11.013 14998688
71. Ryan DP Appleman LJ Lynch T Supko JG Fidias P Clark JW Fishman M Zhu AX Enzinger PC Kashala O J C Jr Eder JP Phase I clinical trial of bortezomib in combination with gemcitabine in patients with advanced solid tumors Cancer 2006, 107:2482-9 10.1002/cncr.22264 17036355
72. Papandreou CN Daliani DD Nix D Yang H Madden T Wang X Pien CS Millikan RE Tu SM Pagliaro L Kim J Adams J Elliott P Esseltine D Petrusich A Dieringer P Perez C Logothetis CJ Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer J Clin Oncol 2004, 22:2108-21 10.1200/JCO.2004.02.106 15169797
73. Richardson PG Mitsiades C Hideshima T Anderson KC Bortezomib: Proteasome inhibition as an effective anticancer therapy Annu Rev Med 2006, 57:33-47 10.1146/annurev.med.57.042905.122625 16409135
74. Crowell PL Chang RR Ren ZB Elson CE Gould MN Selective inhibition of isoprenylation of 21-26-kDa proteins by the anticarcinogen d-limonene and its metabolites J Biol Chem 1991, 266:17679-17685 1894647
75. Stayrook KR McKinzie JH Barbhaiya LH Crowell PL Effects of the antitumor agent perillyl alcohol on H-ras vs. K-ras farnesylation and signal transduction in pancreatic cells Anticancer Res 1998, 18:823-828 9615726
76. Sherr CJ Roberts JM Inhibitors of mammalian G1 cyclin-dependent kinases Genes Dev 1995, 9:1149-1163 10.1101/gad.9.10.1149 7758941
77. Alexandrow MG Moses HL Transforming growth factor beta and cell cycle regulation Cancer Res 1995, 55:1452-1457 7882352
78. Hideshima T Mitsiades C Akiyama M Hayashi T Chauhan D Richardson P Schlossman R Podar K Munshi NC Mitsiades N Anderson KC Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341 Blood 2003, 101:1530-4 10.1182/blood-2002-08-2543 12393500
79. Mitsiades N Mitsiades CS V P Chauhan D Fanourakis G Gu X Bailey C Joseph M Libermann TA Treon SP Munshi NC Richardson PG Hideshima T Anderson KC Molecular sequelae of proteasome inhibition in human multiple myeloma cells Proc Natl Acad Sci USA 2002, 99:14374-9 137891 12391322 10.1073/ pnas.202445099
80. Ling YH Liebes L Jiang JD Holland JF Elliott PJ Adams J Muggia FM Perez-Soler R Mechanisms of proteasome inhibitor PS-341-induced G(2)-M-phase arrest and apoptosis in human non-small cell lung cancer cell lines Clin Cancer Res 2003, 9:1145-54 12631620
81. Fribley A Zeng Q Wang CY Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells Mol Cell Biol 2004, 24:9695-704 525474 15509775 10.1128/MCB.24.22.9695-9704.2004
82. Fribley AM Evenchik B Zeng Q Park BK Guan JY Zhang H Hale TJ Soengas MS Kaufman RJ Wang CY Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of noxa J Biol Chem 2006, 281:31440-7 10.1074/jbc.M604356200 16928686