304
Views
17
CrossRef citations to date
0
Altmetric
Review

The role of proteasome inhibition in the treatment of malignant and non-malignant hematologic disorders

, &
Pages 873-889 | Received 12 Apr 2016, Accepted 20 Jul 2016, Published online: 05 Aug 2016

References

  • Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer. 2004b;4(5):349–360.
  • Adams J. Development of the proteasome inhibitor PS-341. Oncologist. 2002;7:9–16.
  • Adams J. The development of proteasome inhibitors as anticancer drugs. Cancer Cell. 2004a;5:417–421.
  • Nussbaum AK, Dick TP, Keilholz W, et al. Cleavage motifs of the yeast 20S proteasome B subunit deduced from digests of enolase 1. Proc Natl Acad Sci. 1998;95:12504–12509.
  • Almond JB, Cohen GM. The proteasome: a novel target for cancer chemotherapy. Leukemia. 2002;16:433–443.
  • Li B, Dou QP. Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc Natl Acad Sci U S A. 2000;97(8):3850–3855.
  • Karin M, Cao Y, Greten FR, et al. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer. 2002;2(4):301–310.
  • Zhang HG, Wang J, Yang X, et al. Regulation of apoptosis proteins in cancer cells by ubiquitin. Oncogene. 2004;23(11):2009–2015.
  • Sunwoo JB, Chen Z, Dong G, et al. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-κB, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res. 2001;7:1419–1428.
  • Lee AH, Iwakoshi NN, Anderson KC, et al. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci U S A. 2003;100(17):9946–9951.
  • Wang C, Cusack JC, Liu R, et al. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-κB. Nat Am. 1999;5(4):412–417.
  • Kordes U, Krappmann D, Heissmeyer V, et al. Transcription factor NF-kappaB is constitutively activated in acute lymphoblastic leukemia cells. Leukemia. 2000;14(3):399–402.
  • Guzman ML, Neering SJ, Upchurch D, et al. Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood. 2001;98(8):2301–2307.
  • Ni H, Ergin M, Huang Q, et al. Analysis of expression of nuclear factor κB (NF-κB) in multiple myeloma: downregulation of NF-κB induces apoptosis. Br J Hematol. 2001;115:279–286.
  • Brown CJ, Lain S, Verma CS, et al. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer. 2009;9(12):862–873.
  • An WG, Hwang SG, Trepel JB, et al. Protease inhibitor-induced apoptosis: accumulation of wt p53, p21WAF1/CIP1, and induction of apoptosis are independent markers of proteasome inhibition. Leukemia. 2000;14(7):1276–1283.
  • Schwartz R, Davidson T. Pharmacology, pharmacokinetics, and practical applications of bortezomib. Oncology. 2004;18(14 Suppl 11):14–21.
  • Velcade [package insert]. Cambridge (MA): Millenium Pharmaceuticals; 2003.
  • Bross PF, Kane R, Farrell AT, et al. Approval summary for bortezomib for injection in the treatment of multiple myeloma. Clin Cancer Res. 2004;10:3954–3964.
  • Moreau P, Pylypenko H, Grosicki S, et al. Subcutaneous versus intravenous administration of bortezomib in patients with relapsed multiple myeloma: a randomised, phase 3, non-inferiority study. Lancet Oncol. 2011;12(5):431–440.
  • Eriksson E, Zaman F, Chrysis D, et al. Bortezomib is cytotoxic to the human growth plate and permanently impairs bone growth in young mice. PLoS One. 2012;7(11):e50523.
  • Hou M, Eriksson E, Svechnikov K, et al. Bortezomib treatment causes long-term testicular dysfunction in young male mice. Mol Cancer. 2014;13:155.
  • Imajoh-Ohmi S, Kawaguchi T, Sugiyama S, et al. Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem Biophys Res Commun. 1995;217(3):1070–1077.
  • Shinohara K, Tomioka M, Nakano H, et al. Apoptosis induction resulting from proteasome inhibition. Biochem J. 1996;317 (Pt 2):385–388.
  • Tan C, Waldmann TA. Proteasome inhibitor PS-341, a potential therapeutic agent for adult T-cell leukemia. Cancer Res. 2002;62:1083–1086.
  • Masdehors P, Merle-Béral H, Maloum K, et al. Deregulation of the ubiquitin system and p53 proteolysis modify the apoptotic response in B-CLL lymphocytes. Blood. 2000;96(1):269–274.
  • Delic J, Masdehors P, Omura S, et al. The proteasome inhibitor lactacystin induces apoptosis and sensitizes chemo- and radioresistant human chronic lymphocytic leukaemia lymphocytes to TNF-α-initiated apoptosis. Br J Cancer. 1998;77(7):1103–1107.
  • Cusack JC, Liu R, Houston M, et al. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-κB inhibition. Cancer Res. 2001;61:3535–3540.
  • Ma MH, Yang HH, Parker K, et al. The proteasome inhibitor PS-341 markedly enhances sensitivity of multiple myeloma tumor cells to chemotherapeutic agents. Clin Cancer Res. 2003;9:1136–1144.
  • Horton TM, Gannavarapu A, Blaney SM, et al. Bortezomib interactions with chemotherapy agents in acute leukemia in vitro. Cancer Chemother Pharmacol. 2006;58(1):13–23.
  • Minderman H, Zhou Y, O’Loughlin KL, et al. Bortezomib activity and in vitro interactions with anthracyclines and cytarabine in acute myeloid leukemia cells are independent of multidrug resistance mechanisms and p53 status. Cancer Chemother Pharmacol. 2007;60(2):245–255.
  • Junk S, Cario G, Wittner N, et al. Bortezomib treatment can overcome glucocorticoid resistance in childhood B-cell precursor acute lymphoblastic leukemia cell lines. Klin Padiatr. 2015;227(3):123–130.
  • Wang H, Wang X, Li Y, et al. The proteasome inhibitor bortezomib reverses P-glycoprotein-mediated leukemia multi-drug resistance through the NF-kappaB pathway. Pharmazie. 2012;67(2):187–192.
  • Kurkland JF, Meyn RE. Protease inhibitors restore radiation-induced apoptosis to Bcl-2-expressing lymphoma cells. Int J Cancer. 2001;96:327–333.
  • Russo SM, Tepper JE, Baldwin AS, et al. Enhancement of radiosensitivity by proteasome inhibition: implicaitons for a role of NF-κB. Int J Radiation Oncology Biol Phys. 2001;50(1):183–193.
  • LeBlanc R, Catley LP, Hideshima T, et al. Proteasome inhibitor PS-341 inhibits human myeloma cell growth in vivo and prolongs survival in a murine model. Cancer Res. 2002;62:4996–5000.
  • Nawrocki ST, Bruns CJ, Harbison MT, et al. Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther. 2002;1:1243–1253.
  • Orlowski RZ. Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol. 2002;20(22):4420–4427.
  • Papandreou CN, Daliani DD, Nix D, et al. 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(11):2108–2121.
  • Aghajanian C, Soignet S, Dizon DS, et al. A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res. 2002;8:2505–2511.
  • Orlowski RZ, Voorhees PM, Garcia RA, et al. Phase 1 trial of the proteasome inhibitor bortezomib and pegylated liposomal doxorubicin in patients with advanced hematologic malignancies. Blood. 2005;105(8):3058–3065.
  • Jagannath S, Barlogie B, Berenson J, et al. A phase 2 study of two doses of bortezomib in relapsed or refractory myeloma. Br J Haematol. 2004;127:165–172.
  • Richardson PG, Barlogie B, Berenson JR, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003;348(26):2609–2617.
  • Kane RC, Bross PF, Farrell AT, et al. Velcade: US FDA approval for the treatment of multiple myeloma progressing on prior therapy. Oncologist. 2003;8:508–513.
  • Richardson P, Hideshima T, Mitsiades C, et al. Proteasome inhibition in hematologic malignancies. Ann Med. 2004;36(4):304–314.
  • Kane RC, Farrell AT, Sridhara R, et al. United States Food and Drug Administration approval summary: bortezomib for the treatment of progressive multiple myeloma after one prior therapy. Clin Cancer Res. 2006;12(10):2955–2960.
  • Richardson PG, Sonneveld P, Schuster M, et al. Extended follow-up of a phase 3 trial in relapsed multiple myeloma: final time-to-event results of the APEX trial. Blood. 2007;110(10):3557–3560.
  • San Miguel JF, Schlag R, Khuageva NK, et al. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. Leukemia. 2008;359(9):906–917.
  • Teicher BA, Anderson KC. CCR 20th Anniversary Commentary: in the beginning, there was PS-341. Clin Cancer Res. 2015;21(5):939–941.
  • Sonneveld P, Goldschmidt H, Rosinol L, et al. Bortezomib-based versus nonbortezomib-based induction treatment before autologous stem-cell transplantation in patients with previously untreated multiple myeloma: a meta-analysis of phase III randomized, controlled trials. J Clin Oncol. 2013;31(26):3279–3287.
  • Harousseau JL, Attal M, Avet-Loiseau H, et al. Bortezomib plus dexamethasone is superior to vincristine plus doxorubicin plus dexamethasone as induction treatment prior to autologous stem-cell transplantation in newly diagnosed multiple myeloma: results of the IFM 2005-01 phase III trial. J Clin Oncol. 2010;28(30):4621–4629.
  • Cavo M, Tacchetti P, Patriarca F, et al. Bortezomib with thalidomide plus dexamethasone compared with thalidomide plus dexamethasone as induction therapy before, and consolidation therapy after, double autologous stem-cell transplantation in newly diagnosed multiple myeloma: a randomised phase 3 study. Lancet. 2010;376(9758):2075–2085.
  • Sonneveld P, Schmidt-Wolf IG, Van Der Holt B. et al. Bortezomib induction and maintenance treatment in patients with newly diagnosed multiple myeloma: results of the randomized phase III HOVON-65/GMMG-HD4 trial. J Clin Oncol. 2012;30(24):2946–2955.
  • Rosinol L, Oriol A, Teruel AI, et al. Superiority of bortezomib, thalidomide, and dexamethasone (VTD) as induction pretransplantation therapy in multiple myeloma: a randomized phase 3 PETHEMA/GEM study. Blood. 2012;120(8):1589–1596.
  • Bringhen S, Larocca A, Rossi D, et al. Efficacy and safety of once-weekly bortezomib in multiple myeloma patients. Blood. 2010;116(23):4745–4753.
  • Totani H, Ri M, Kato C, et al. Phase I study of once weekly treatment with bortezomib in combination with lenalidomide and dexamethasone for relapsed or refractory multiple myeloma. Int J Hematol. 2016;103(3):316–321.
  • O’Connor OA, Wright J, Moskowitz C, et al. 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(4):676–684.
  • Goy A, Bernstein SH, Kahl BS, et al. Bortezomib in patients with relapsed or refractory mantle cell lymphoma: updated time-to-event analyses of the multicenter phase 2 PINNACLE study. Ann Oncol. 2009;20(3):520–525.
  • Goy A, Younes A, McLaughlin P, et al. Phase II study of proteasome inhibitor bortezomib in relapsed or refractory B-cell non-Hodgkin’s lymphoma. J Clin Oncol. 2005;23(4):667–675.
  • Strauss SJ, Maharaj L, Hoare S, et al. 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(13):2105–2112.
  • Fisher RI, Bernstein SH, Kahl BS, et al. Multicenter phase II study of bortezomib in patients with relapsed or refractory mantle cell lymphoma. J Clin Oncol. 2006;24(30):4867–4874.
  • Mato AR, Feldman T, Goy A. Proteasome inhibition and combination therapy for non-Hogkin’s lymphoma: from bench to bedside. Oncologist. 2012;17:694–707.
  • Cortes J, Thomas D, Koller C, et al. Phase I study of bortezomib in refractory or relapsed acute leukemias. Clin Cancer Res. 2004;10:3371–3376.
  • Attar EC, De Angelo DJ, Supko JG, et al. Phase I and pharmacokinetic study of bortezomib in combination with idarubicin and cytarabine in patients with acute myelogenous leukemia. Clin Cancer Res. 2008;14(5):1446–1454.
  • Attar EC, Johnson JL, Amrein PC, et al. Bortezomib added to daunorubicin and cytarabine during induction therapy and to intermediate-dose cytarabine for consolidation in patients with previously untreated acute myeloid leukemia age 60 to 75 years: CALGB (Alliance) study 10502. J Clin Oncol. 2013;31(7):923–929.
  • Houghton PJ, Morton CL, Kolb EA, et al. Initial testing (stage 1) of the proteasome inhibitor bortezomib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2008;50:37–45.
  • Blaney SM, Bernstein M, Neville K, et al. Phase I study of the proteasome inhibitor bortezomib in pediatric patients with refractory solid tumors: a Children’s Oncology Group study (ADVL0015). J Clin Oncol. 2004;22(23):4804–4809.
  • Horton TM, Pati D, Plon SE, et al. A phase 1 study of the proteasome inhibitor bortezomib in pediatric patients with refractory leukemia: a Children’s Oncology Group study. Clin Cancer Res. 2007;13(5):1516–1522.
  • Messinger Y, Gaynon P, Raetz E, et al. 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. 2010;55(2):254–259.
  • Messinger YH, Gaynon PS, Sposto R, et al. Bortezomib with chemotherapy is highly active in advanced B-precursor acute lymphoblastic leukemia: Therapeutic Advances in Childhood Leukemia & Lymphoma (TACL) Study. Blood. 2012;120(2):285–290.
  • Horton TM, Lu X, O’Brien MM, et al. Bortezomib reinduction therapy to improve response rates in pediatric ALL in first relapse: a Children’s Oncology Group (COG) study (AALL07P1) [abstract]. J Clin Oncol. 2013;31:10003.
  • Horton TM, Perentesis JP, Gamis AS, et al. A phase 2 study of bortezomib combined with either idarubicin/cytarabine or cytarabine/etoposide in children with relapsed, refractory or secondary acute myeloid leukemia: a report from the Children’s Oncology Group. Pediatr Blood Cancer. 2014;61(10):1754–1760.
  • Horton TM, Drachtman RA, Chen L, et al. A phase 2 study of bortezomib in combination with ifosfamide/vinorelbine in paediatric patients and young adults with refractory/recurrent Hodgkin lymphoma: a Children’s Oncology Group study. Br J Haematol. 2015;170(1):118–122.
  • Combination chemotherapy with or without bortezomib in treating younger patients with newly diagnosed T-cell acute lymphoblastic leukemia or stage II-IV T-cell lymphoblastic lymphoma. Available from: https://clinicaltrials.gov/ct2/show/NCT02112916
  • Bortezomib and sorafenib tosylate in treating patients with newly diagnosed acute myeloid leukemia. Available from: https://clinicaltrials.gov/ct2/show/NCT01371981
  • Aplenc R. Personal communication. 2016 Apr 1.
  • Roccaro AM, Vacca A, Ribatti D. Bortezomib in the treatment of cancer. Recent Pat Anticancer Drug Discov. 2006;1(3):397–403.
  • Blanco B, Perez-Simon JA, Sanchez-Abarca LI, et al. Treatment with bortezomib of human CD4+ T cells preserves natural regulatory T cells and allows the emergence of a distinct suppressor T-cell population. Haematologica. 2009;94(7):975–983.
  • Cenci S, Mezghrani A, Cascio P, et al. Progressively impaired proteasomal capacity during terminal plasma cell differentiation. Embo J. 2006;25:1104–1113.
  • Nencioni A, Garuti A, Schwarzenberg K, et al. Proteasome inhibitor-induced apoptosis in human monocyte-derived dendritic cells. Eur J Immunol. 2006;36(3):681–689.
  • Moran E, Carbone F, Augusti V, et al. Proteasome inhibitors as immunosuppressants: biological rationale and clinical experience. Semin Hematol. 2012;49(3):270–276.
  • Everly M, Everly J, Susskind B, et al. Bortezomib provides effective therapy for antibody- and cell-mediated acute rejection. Transplantation. 2008;86(12): 1754–1761.
  • Flechner S, Fatica R, Askar M, et al. The role of proteasome inhibition with bortezomib in the treatment of antibody-mediated rejection after kidney-only or kidney-combined organ transplantation. Transplantation. 2010;90(12):1486–1492.
  • Waiser J, Budde K, Schutz M, et al. Comparison between bortezomib and rituximab in the treatment of antibody-mediated renal allograft rejection. Nephrol Dial Transplant. 2012;27(3):1246–1251.
  • Desensitization with bortezomib before a living kidney donation. Available from: https://clinicaltrials.gov/ct2/show/NCT01842074
  • Bortezomib in late antibody-mediated kidney transplant rejection. Available from: https://clinicaltrials.gov/ct2/show/NCT01873157
  • Multi-drug desensitization protocol for heart transplant candidates. Available from: https://clinicaltrials.gov/ct2/show/NCT01556347
  • El-Cheikh J, Michallet M, Nagler A, et al. High response rate and improved graft-versus-host disease following bortezomib as salvage therapy after reduced intensity conditioning allogeneic stem cell transplantation for multiple myeloma. Haematologica. 2008;93(3):455–458.
  • Pai CC, Chen M, Mirsoian A, et al. Treatment of chronic graft-versus-host disease with bortezomib. Blood. 2014;124(10): 1677–1688.
  • Al-Homsi AS, Cole K, Bogema M, et al. Short course of post-transplantation cyclophosphamide and bortezomib for graft-versus-host disease prevention after allogeneic peripheral blood stem cell transplantation is feasible and yields favorable results: a phase I study. Biol Blood Marrow Transplant. 2015;21(7):1315–1320.
  • Koreth J, Kim HT, Lange PB, et al. A bortezomib-based regimen offers promising survival and graft-versus-host disease prophylaxis in myeloablative HLA-mismatched and unrelated donor transplantation: a phase II trial. Biol Blood Marrow Transplant. 2015;21(11): 1907–1913.
  • A study using tacrolimus, sirolimus and bortezomib as acute graft versus host disease (GVHD) prophylaxis in allogeneic peripheral blood stem cell (PBSC) transplantation. Available from: https://clinicaltrials.gov/ct2/show/NCT00670423
  • Bortezomib for the treatment of refractory chronic graft-vs-host disease(cGVHD). Available from: https://clinicaltrials.gov/ct2/show/NCT01158105
  • Bortezomib in patients with chronic graft versus host disease. Available from: https://clinicaltrials.gov/ct2/show/NCT01672229
  • Carson KR, Beckwith LG, Mehta J. Successful treatment of IgM-mediated autoimmune hemolytic anemia with bortezomib. Blood. 2010;115(4):915.
  • Danchaivijitr P, Yared J, Rapoport AP. Successful treatment of IgG and complement-mediated autoimmune hemolytic anemia with bortezomib and low-dose cyclophosphamide. Am J Hematol. 2011;86(3):331–332.
  • Hosoba S, Jaye DL, Cohen C, et al. Successful treatment of severe immune hemolytic anemia after allogeneic stem cell transplantation with bortezomib: report of a case and review of literature. Transfusion. 2015;55(2):259–264.
  • Khandelwal P, Davies SM, Grimley MS, et al. Bortezomib for refractory autoimmunity in pediatrics. Biol Blood Marrow Transplant. 2014;20(10): 1654–1659.
  • Sugumar D, Keller J, Vij R. Targeted treatments for multiple myeloma: specific role of carfilzomib. Pharmgenomics Pers Med. 2015;8:23–33.
  • Allegra A, Alonci A, Gerace D, et al. New orally active proteasome inhibitors in multiple myeloma. Leuk Res. 2014;38:1–9.
  • Teicher BA, Tomaszewski JE. Proteasome inhibitors. Biochem Pharmacol. 2015;96:1–9.
  • Dimopoulos MA, Moreau P, Palumbo A, et al. Carfilzomib and dexamethasone versus bortezomib and dexamethasone for patients with relapsed or refractory multiple myeloma (ENDEAVOR): a randomised, phase 3, open-label, multicentre study. Lancet Oncol. 2016;17(1):27–38.
  • Study of carfilzomib in combination with dexamethasone, mitoxantrone, PEG-asparaginase, and vincristine in children with relapsed or refractory acute lymphoblastic leukemia. Available from: https://clinicaltrials.gov/ct2/show/NCT02303821
  • Offidani M, Corvatta L, Caraffa P, et al. An evidence-based review of ixazomib citrate and its potential in the treatment of newly diagnosed multiple myeloma. Onco Targets Ther. 2014;7:1793–1800.
  • Moreau P, Masszi T, Grzasko N, et al. Oral ixazomib, lenalidomide, and dexamethasone for multiple myeloma. N Engl J Med. 2016;374(17):1621–1634.
  • Kyprolis [package insert]. Thousand Oaks (CA): Onyx Pharmaceuticals; 2012.
  • Ninlaro [package insert]. Cambridge (MA): Millenium Pharmaceuticals; 2015.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.