Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome.

Carfilzomib is a proteasome inhibitor in clinical development that primarily targets the chymotrypsin-like (CT-L) subunits in both the constitutive proteasome (c20S) and the immunoproteasome (i20S). To investigate the impact of inhibiting the CT-L activity with carfilzomib, we set out to quantitate the levels of CT-L subunits beta5 from the c20S and LMP7 from the i20S in normal and malignant hematopoietic cells. We found that the i20S is a major form of the proteasome expressed in cells of hematopoietic origin, including multiple myeloma (MM) CD138+ tumor cells. Although specific inhibition of either LMP7 or beta5 alone was insufficient to produce an antitumor response, inhibition of all proteasome subunits was cytotoxic to both hematologic tumor cells and peripheral blood mononuclear cells. However, selective inhibition of both beta5 and LMP7 was sufficient to induce an antitumor effect in MM, non-Hodgkin lymphoma, and leukemia cells while minimizing the toxicity toward nontransformed cells. In MM tumor cells, CT-L inhibition alone was sufficient to induce proapoptotic sequelae, including proteasome substrate accumulation, Noxa and caspase 3/7 induction, and phospho-eIF2alpha suppression. These data support a hypothesis that hematologic tumor cells are uniquely sensitive to CT-L inhibition and provide a mechanistic understanding of the clinical safety profile and antitumor activity of proteasome inhibitors.

[1]  S. Demo,et al.  Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. , 2007, Cancer research.

[2]  J. Aguirre-Ghiso,et al.  Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. , 2009, Cancer research.

[3]  S. Demo,et al.  Design and synthesis of an orally bioavailable and selective peptide epoxyketone proteasome inhibitor (PR-047). , 2009, Journal of medicinal chemistry.

[4]  N. Munshi,et al.  NF-κB as a Therapeutic Target in Multiple Myeloma* , 2002, The Journal of Biological Chemistry.

[5]  J. Monaco,et al.  Beta 2 subunit propeptides influence cooperative proteasome assembly. , 2003, The Journal of biological chemistry.

[6]  M. Bennett,et al.  Development of proteasome inhibitors in oncology and autoimmune diseases. , 2008, Current opinion in drug discovery & development.

[7]  H. Ovaa,et al.  Characterization of the ubiquitin–proteasome system in bortezomib-adapted cells , 2009, Leukemia.

[8]  R. Wek,et al.  Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. , 2005, The Journal of biological chemistry.

[9]  S. Beck,et al.  A proteasome-related gene between the two ABC transporter loci in the class II region of the human MHC , 1991, Nature.

[10]  G. Peters,et al.  Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein. , 2008, Blood.

[11]  H. Ovaa,et al.  CEP-18770: A novel, orally active proteasome inhibitor with a tumor-selective pharmacologic profile competitive with bortezomib. , 2008, Blood.

[12]  L. Sorell,et al.  Immunological methods to quantify and characterize proteasome complexes: development and application. , 2008, Journal of immunological methods.

[13]  A. Goldberg,et al.  Importance of the Different Proteolytic Sites of the Proteasome and the Efficacy of Inhibitors Varies with the Protein Substrate* , 2006, Journal of Biological Chemistry.

[14]  P. Elliott,et al.  The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. , 2001, Cancer research.

[15]  Peter R Jungblut,et al.  Intermediate-type 20 S proteasomes in HeLa cells: "asymmetric" subunit composition, diversity and adaptation. , 2007, Journal of molecular biology.

[16]  A. Ciechanover,et al.  Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins. , 1982, The Journal of biological chemistry.

[17]  J. Leonard,et al.  Multicenter phase II study of bortezomib in patients with relapsed or refractory mantle cell lymphoma. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[18]  H. Jäck,et al.  Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. , 2007, Cancer research.

[19]  L. Boise,et al.  Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. , 2006, Blood.

[20]  S. Lowe,et al.  Differential regulation of noxa in normal melanocytes and melanoma cells by proteasome inhibition: therapeutic implications. , 2005, Cancer research.

[21]  K. Anderson,et al.  Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib , 2005, Nature Methods.

[22]  M. Hendrix,et al.  Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. , 2005, Cancer research.

[23]  A. Goldberg,et al.  A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. Agostinelli,et al.  Selective apoptosis of monocytes and monocyte-derived DCs induced by bortezomib (Velcade) , 2009, Bone Marrow Transplantation.

[25]  N. Hastie,et al.  Transcriptome analysis of human autosomal trisomy. , 2002, Human molecular genetics.

[26]  J. Adams The development of proteasome inhibitors as anticancer drugs. , 2004, Cancer cell.

[27]  I. Shih,et al.  Ubiquitin-proteasome system stress sensitizes ovarian cancer to proteasome inhibitor-induced apoptosis. , 2006, Cancer research.

[28]  J. Monaco,et al.  Homology of proteasome subunits to a major histocompatibility complex-linked LMP gene , 1991, Nature.

[29]  R. Wek,et al.  Phosphorylation of the α-Subunit of the Eukaryotic Initiation Factor-2 (eIF2α) Reduces Protein Synthesis and Enhances Apoptosis in Response to Proteasome Inhibition* , 2005, Journal of Biological Chemistry.

[30]  D. Kuhn,et al.  Targeted inhibition of the immunoproteasome is a potent strategy against models of multiple myeloma that overcomes resistance to conventional drugs and nonspecific proteasome inhibitors. , 2009, Blood.

[31]  R. Kozłowski,et al.  The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. , 1993, Journal of immunological methods.

[32]  L. Bruhn,et al.  Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. , 2007, Cancer cell.

[33]  D. McConkey,et al.  Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. , 2005, Cancer research.

[34]  H. Ovaa,et al.  Activity patterns of proteasome subunits reflect bortezomib sensitivity of hematologic malignancies and are variable in primary human leukemia cells , 2007, Leukemia.

[35]  L. Staudt,et al.  Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. , 2007, Cancer cell.

[36]  Maitreya J. Dunham,et al.  Effects of Aneuploidy on Cellular Physiology and Cell Division in Haploid Yeast , 2007, Science.

[37]  Hartmut Goldschmidt,et al.  Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. , 2005, The New England journal of medicine.

[38]  J. Monaco,et al.  β2 Subunit Propeptides Influence Cooperative Proteasome Assembly* , 2003, The Journal of Biological Chemistry.

[39]  J. W. Findlay,et al.  Validation of immunoassays for bioanalysis: a pharmaceutical industry perspective. , 2000, Journal of pharmaceutical and biomedical analysis.

[40]  D. McConkey,et al.  Mechanisms of proteasome inhibitor action and resistance in cancer. , 2008, Drug resistance updates : reviews and commentaries in antimicrobial and anticancer chemotherapy.

[41]  S. Demo,et al.  Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. , 2005, Blood.

[42]  K. Tanaka,et al.  Abnormally high expression of proteasomes in human leukemic cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Monaco,et al.  Identification of MECL-1 (LMP-10) as the third IFN-gamma-inducible proteasome subunit. , 1996, Journal of immunology.

[44]  A. Ciechanover Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin–proteasome system and onto human diseases and drug targeting* , 2005, Cell Death and Differentiation.

[45]  Christian A. Rees,et al.  Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  K. Tanaka,et al.  Half-life of proteasomes (multiprotease complexes) in rat liver. , 1989, Biochemical and biophysical research communications.

[47]  N. Munshi,et al.  Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. , 2007, Blood.

[48]  R. Millikan,et al.  Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[49]  K. Anderson,et al.  The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. , 2009, Blood.

[50]  Li Chen,et al.  Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. , 2005, Cancer research.