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3. Valosin-Containing Protein/p97 as a Novel Therapeutic Target in Acute Lymphoblastic Leukemia

Author

Gugliotta, Gabriele, Sudo, Makoto, Cao, Qi, Lin, De-Chen, Sun, Haibo, Takao, Sumiko, Le Moigne, Ronan, Rolfe, Mark, Gery, Sigal, Müschen, Markus, Cavo, Michele, and Koeffler, H Phillip

Subjects
Biomedical and Clinical Sciences, Clinical Sciences, Oncology and Carcinogenesis, Cancer, Pediatric Cancer, Genetics, Hematology, Rare Diseases, Pediatric, Aetiology, 2.1 Biological and endogenous factors, Antineoplastic Agents, Apoptosis, Biomarkers, Cell Cycle, Cell Line, Tumor, Cell Proliferation, Cell Survival, Drug Synergism, Endoplasmic Reticulum Chaperone BiP, Endoplasmic Reticulum Stress, Gene Expression Regulation, Gene Knockout Techniques, Humans, Molecular Targeted Therapy, Precursor Cell Lymphoblastic Leukemia-Lymphoma, Signal Transduction, Unfolded Protein Response, Valosin Containing Protein, Oncology & Carcinogenesis, Clinical sciences, Oncology and carcinogenesis
Abstract

B acute lymphoblastic leukemia (B-ALL) cells are distinctively vulnerable to endoplasmic reticulum (ER) stress. Recently, inhibition of p97 was shown to induce ER stress and subsequently cell death in solid tumors and in multiple myeloma. We investigated the role of a novel, orally available, p97 inhibitor (CB-5083; Cleave Biosciences) in B-ALL. CB-5083 induced a significant reduction in viability in 10 human B-ALL cell lines, harboring the most common fusion-genes involved in pediatric and adult B-ALL, with IC50s ranging from 0.34 to 0.76 μM. Moreover, CB-5083 significantly reduced the colony formation of OP1 and NALM6 cells. Early and strong induction of apoptosis was demonstrated in BALL1 and OP1 cells, together with a robust cleavage of PARP. CB-5083 induced ER stress, as documented through: 1) prominent expression of chaperones (GRP78, GRP94, PDI, DNAJC3, and DNAJB9); 2) increased activation of IRE1-alpha, as demonstrated by the splicing of XBP1; and 3) activation of PERK, which resulted in a significant overexpression of CHOP, and its downstream genes. CB-5083 reduced the viability also in GRP78-/-, GRP94-/-, and XBP1-/- cells, suggesting that none of these proteins alone was strictly required for CB-5083 activity. Moreover, we showed that the absence of XBP1 (XBP1-/-) increased the sensitivity to CB-5083, leading to the hypothesis that XBP1 splicing counteracts the activity of CB-5083, probably mitigating ER stress. Finally, vincristine was synergistic with CB-5083 in both BALL1 and OP1 cells. In summary, the targeting of p97 with CB-5083 is a novel promising therapeutic approach that should be further evaluated in B-ALL.

Published
2017

5. Data S4 from MEF2C Phosphorylation Is Required for Chemotherapy Resistance in Acute Myeloid Leukemia

Author

Brown, Fiona C., primary, Still, Eric, primary, Koche, Richard P., primary, Yim, Christina Y., primary, Takao, Sumiko, primary, Cifani, Paolo, primary, Reed, Casie, primary, Gunasekera, Shehana, primary, Ficarro, Scott B., primary, Romanienko, Peter, primary, Mark, Willie, primary, McCarthy, Craig, primary, de Stanchina, Elisa, primary, Gonen, Mithat, primary, Seshan, Venkatraman, primary, Bhola, Patrick, primary, O'Donnell, Conor, primary, Spitzer, Barbara, primary, Stutzke, Crystal, primary, Lavallée, Vincent-Philippe, primary, Hébert, Josée, primary, Krivtsov, Andrei V., primary, Melnick, Ari, primary, Paietta, Elisabeth M., primary, Tallman, Martin S., primary, Letai, Anthony, primary, Sauvageau, Guy, primary, Pouliot, Gayle, primary, Levine, Ross, primary, Marto, Jarrod A, primary, Armstrong, Scott A., primary, and Kentsis, Alex, primary

Published
2023
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6. Data from MEF2C Phosphorylation Is Required for Chemotherapy Resistance in Acute Myeloid Leukemia

Author

Brown, Fiona C., primary, Still, Eric, primary, Koche, Richard P., primary, Yim, Christina Y., primary, Takao, Sumiko, primary, Cifani, Paolo, primary, Reed, Casie, primary, Gunasekera, Shehana, primary, Ficarro, Scott B., primary, Romanienko, Peter, primary, Mark, Willie, primary, McCarthy, Craig, primary, de Stanchina, Elisa, primary, Gonen, Mithat, primary, Seshan, Venkatraman, primary, Bhola, Patrick, primary, O'Donnell, Conor, primary, Spitzer, Barbara, primary, Stutzke, Crystal, primary, Lavallée, Vincent-Philippe, primary, Hébert, Josée, primary, Krivtsov, Andrei V., primary, Melnick, Ari, primary, Paietta, Elisabeth M., primary, Tallman, Martin S., primary, Letai, Anthony, primary, Sauvageau, Guy, primary, Pouliot, Gayle, primary, Levine, Ross, primary, Marto, Jarrod A, primary, Armstrong, Scott A., primary, and Kentsis, Alex, primary

Published
2023
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7. Supplementary files from MEF2C Phosphorylation Is Required for Chemotherapy Resistance in Acute Myeloid Leukemia

Author

Brown, Fiona C., primary, Still, Eric, primary, Koche, Richard P., primary, Yim, Christina Y., primary, Takao, Sumiko, primary, Cifani, Paolo, primary, Reed, Casie, primary, Gunasekera, Shehana, primary, Ficarro, Scott B., primary, Romanienko, Peter, primary, Mark, Willie, primary, McCarthy, Craig, primary, de Stanchina, Elisa, primary, Gonen, Mithat, primary, Seshan, Venkatraman, primary, Bhola, Patrick, primary, O'Donnell, Conor, primary, Spitzer, Barbara, primary, Stutzke, Crystal, primary, Lavallée, Vincent-Philippe, primary, Hébert, Josée, primary, Krivtsov, Andrei V., primary, Melnick, Ari, primary, Paietta, Elisabeth M., primary, Tallman, Martin S., primary, Letai, Anthony, primary, Sauvageau, Guy, primary, Pouliot, Gayle, primary, Levine, Ross, primary, Marto, Jarrod A, primary, Armstrong, Scott A., primary, and Kentsis, Alex, primary

Published
2023
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10. Therapeutic remodeling of CBP transcription factor complex controls oncogenic gene expression in acute myeloid leukemia

Author

Forbes, Lauren, Cifani, Paolo, Minuesa, Gerard, Chen, Celine, Takao, Sumiko, Kharas, Michael G, Koche, Richard P., and Kentsis, Alex

Subjects
hemic and lymphatic diseases
Abstract

Highlights Cell-penetrant peptidomimetic inhibitor selectively blocks oncogenic MYB:CBP/P300 activity in diverse leukemias but not normal blood cells MYB assembles aberrant transcription factor complexes in AML required for programming leukemic gene expression CBP/P300 sequestration contributes to MYB-dependent leukemogenic gene expression and chromatin organization Summary Dysregulated gene expression is one of the most prevalent features in human cancers. Here, we show that most subtypes of acute myeloid leukemia (AML) depend on the aberrant assembly of the MYB transcriptional co-activator complex. By rapid and selective peptidomimetic interference with the binding of CBP/P300 to MYB, but not CREB or MLL, we find that the leukemic functions of MYB are mediated by CBP/P300-mediated co-activation of a distinct set of transcriptional factor complexes that are aberrantly assembled with MYB in AML cells. This therapeutic remodeling is accompanied by dynamic redistribution of CBP/P300 complexes to genes that control cellular differentiation and growth. We propose that convergently organized transcription factor complexes in AML cells control oncogenic gene expression programs. These findings establish a compelling strategy for pharmacologic reprogramming of oncogenic gene expression that supports its targeting for leukemias and possibly other human cancers caused by dysregulated gene control.

Published
2020
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11. Convergent organization of aberrant MYB complex controls oncogenic gene expression in acute myeloid leukemia

Author

Takao, Sumiko, primary, Forbes, Lauren, additional, Uni, Masahiro, additional, Cheng, Shuyuan, additional, Pineda, Jose Mario Bello, additional, Tarumoto, Yusuke, additional, Cifani, Paolo, additional, Minuesa, Gerard, additional, Chen, Celine, additional, Kharas, Michael G, additional, Bradley, Robert K, additional, Vakoc, Christopher R, additional, Koche, Richard P, additional, and Kentsis, Alex, additional

Published
2021
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12. Author response: Convergent organization of aberrant MYB complex controls oncogenic gene expression in acute myeloid leukemia

Author

Takao, Sumiko, primary, Forbes, Lauren, additional, Uni, Masahiro, additional, Cheng, Shuyuan, additional, Pineda, Jose Mario Bello, additional, Tarumoto, Yusuke, additional, Cifani, Paolo, additional, Minuesa, Gerard, additional, Chen, Celine, additional, Kharas, Michael G, additional, Bradley, Robert K, additional, Vakoc, Christopher R, additional, Koche, Richard P, additional, and Kentsis, Alex, additional

Published
2021
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13. Author Reply to Peer Reviews of Convergent organization of aberrant MYB complex controls oncogenic gene expression in acute myeloid leukemia

Author

Kentsis, Alex, primary, Koche, Richard P., additional, Vakoc, Christopher R., additional, Bradley, Robert K., additional, Kharas, Michael G., additional, Chen, Celine, additional, Minuesa, Gerard, additional, Cifani, Paolo, additional, Tarumoto, Yusuke, additional, Pineda, Jose Mario Bello, additional, Cheng, Shuyuan, additional, Uni, Masahiro, additional, Forbes, Lauren, additional, and Takao, Sumiko, additional

Published
2020
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14. Convergent organization of aberrant MYB complex controls oncogenic gene expression in acute myeloid leukemia

Author

Takao, Sumiko, primary, Forbes, Lauren, additional, Uni, Masahiro, additional, Cheng, Shuyuan, additional, Pineda, Jose Mario Bello, additional, Tarumoto, Yusuke, additional, Cifani, Paolo, additional, Minuesa, Gerard, additional, Chen, Celine, additional, Kharas, Michael G., additional, Bradley, Robert K., additional, Vakoc, Christopher R., additional, Koche, Richard P., additional, and Kentsis, Alex, additional

Published
2020
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16. MEF2C Phosphorylation Is Required for Chemotherapy Resistance in Acute Myeloid Leukemia

Author

Brown, Fiona C., primary, Still, Eric, additional, Koche, Richard P., additional, Yim, Christina Y., additional, Takao, Sumiko, additional, Cifani, Paolo, additional, Reed, Casie, additional, Gunasekera, Shehana, additional, Ficarro, Scott B., additional, Romanienko, Peter, additional, Mark, Willie, additional, McCarthy, Craig, additional, de Stanchina, Elisa, additional, Gonen, Mithat, additional, Seshan, Venkatraman, additional, Bhola, Patrick, additional, O'Donnell, Conor, additional, Spitzer, Barbara, additional, Stutzke, Crystal, additional, Lavallée, Vincent-Philippe, additional, Hébert, Josée, additional, Krivtsov, Andrei V., additional, Melnick, Ari, additional, Paietta, Elisabeth M., additional, Tallman, Martin S., additional, Letai, Anthony, additional, Sauvageau, Guy, additional, Pouliot, Gayle, additional, Levine, Ross, additional, Marto, Jarrod A, additional, Armstrong, Scott A., additional, and Kentsis, Alex, additional

Published
2018
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17. Abstract 2450: Mutational profiling of MLL-PTD acute myeloid leukemia

Author

Ding, Lingwen, primary, Sun, Qiaoyang, additional, Tan, Kar-Tong, additional, Chien, Wenwen, additional, Mayakonda, Anand, additional, Lin, Dechen, additional, Loh, Xinyi, additional, Xiao, Jinfen, additional, Meggendorfer, Manja, additional, Alpermann, Tamara, additional, Garg, Manoj, additional, Lim, Su-Lin, additional, Madan, Vikas, additional, Hattori, Norimichi, additional, Nagata, Yasunobu, additional, Miyano, Satoru, additional, Juh, Allen Yeoh Eng, additional, Hou, Hsin-An, additional, Jiang, Yan-Yi, additional, Takao, Sumiko, additional, Liu, Li-Zhen, additional, Tan, Siew-Zhuan, additional, Lill, Michael, additional, Hayashi, Mutsumi, additional, Kinoshita, Akitoshi, additional, Kantarjian, Hagop M., additional, Kornblau, Steven M., additional, Ogawa, Seishi, additional, Haferlach, Torsten, additional, Yang, Henry, additional, and Koeffler, H. Phillip, additional

Published
2017
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18. MEF2C phosphorylation is required for chemotherapy resistance in acute myeloid leukemia

Author

Brown, Fiona C., primary, Still, Eric, additional, Cifani, Paolo, additional, Takao, Sumiko, additional, Reed, Casie, additional, Ficarro, Scott B., additional, Koche, Richard P., additional, Romanienko, Peter, additional, Mark, Willie, additional, O’Donnell, Conor, additional, Spitzer, Barbara, additional, Stutzke, Crystal, additional, Krivtsov, Andrei V., additional, Pouliot, Gayle, additional, Gray, Nathanael, additional, Marto, Jarrod A., additional, Armstrong, Scott, additional, and Kentsis, Alex, additional

Published
2017
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20. Selective inhibition of unfolded protein response induces apoptosis in pancreatic cancer cells

Author

Chien, Wenwen, primary, Ding, Ling-Wen, additional, Sun, Qiao-Yang, additional, Torres-Fernandez, Lucia A., additional, Tan, Siew Zhuan, additional, Xiao, Jinfen, additional, Lim, Su Lin, additional, Garg, Manoj, additional, Lee, Kian Leong, additional, Kitajima, Shojiro, additional, Takao, Sumiko, additional, Leong, Wei Zhong, additional, Sun, Haibo, additional, Tokatly, Itay, additional, Poellinger, Lorenz, additional, Gery, Sigal, additional, and Koeffler, Phillip H., additional

Published
2014
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28. Valosin-Containing Protein/p97 as a Novel Therapeutic Target in Acute Lymphoblastic Leukemia

Author

Qi Cao, De-Chen Lin, H. Phillip Koeffler, Sumiko Takao, Mark Rolfe, Ronan Le Moigne, Markus Müschen, Sigal Gery, Gabriele Gugliotta, Haibo Sun, Makoto Sudo, Michele Cavo, Gugliotta, Gabriele, Sudo, Makoto, Cao, Qi, Lin, De-chen, Sun, Haibo, Takao, Sumiko, Le Moigne, Ronan, Rolfe, Mark, Gery, Sigal, Müschen, Marku, Cavo, Michele, and Koeffler, H. Phillip

Subjects
PEI, polyethylenimine, 0301 basic medicine, Cancer Research, Apoptosis, ERAD, ER-associated degradation, MTT, 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide, Gene Knockout Techniques, chemistry.chemical_compound, UPR, unfolded protein response, Valosin Containing Protein, Molecular Targeted Therapy, Endoplasmic Reticulum Chaperone BiP, Tumor, Cell Cycle, Drug Synergism, Precursor Cell Lymphoblastic Leukemia-Lymphoma, lcsh:Neoplasms. Tumors. Oncology. Including cancer and carcinogens, Endoplasmic Reticulum Stress, Biochemistry, Signal Transduction, medicine.drug, Original article, Vincristine, Programmed cell death, XBP1, HNA, 2-hydroxy-1-naphthaldehyde, Cell Survival, Clinical Sciences, B-ALL, B acute lymphoblastic leukemia, Antineoplastic Agents, Biology, lcsh:RC254-282, 4-OHT, 4-hydroxy tamoxifen, Cell Line, ER, endoplasmic reticulum, PI, propidium iodide, 03 medical and health sciences, Cell Line, Tumor, medicine, Humans, Oncology & Carcinogenesis, Propidium iodide, Cell Proliferation, Endoplasmic reticulum, 030104 developmental biology, Gene Expression Regulation, chemistry, Cell culture, Unfolded Protein Response, Cancer research, Unfolded protein response, Biomarkers
Abstract

B acute lymphoblastic leukemia (B-ALL) cells are distinctively vulnerable to endoplasmic reticulum (ER) stress. Recently, inhibition of p97 was shown to induce ER stress and subsequently cell death in solid tumors and in multiple myeloma. We investigated the role of a novel, orally available, p97 inhibitor (CB-5083; Cleave Biosciences) in B-ALL. CB-5083 induced a significant reduction in viability in 10 human B-ALL cell lines, harboring the most common fusion-genes involved in pediatric and adult B-ALL, with IC50s ranging from 0.34 to 0.76 μM. Moreover, CB-5083 significantly reduced the colony formation of OP1 and NALM6 cells. Early and strong induction of apoptosis was demonstrated in BALL1 and OP1 cells, together with a robust cleavage of PARP. CB-5083 induced ER stress, as documented through: 1) prominent expression of chaperones (GRP78, GRP94, PDI, DNAJC3, and DNAJB9); 2) increased activation of IRE1-alpha, as demonstrated by the splicing of XBP1; and 3) activation of PERK, which resulted in a significant overexpression of CHOP, and its downstream genes. CB-5083 reduced the viability also in GRP78−/−, GRP94−/−, and XBP1−/− cells, suggesting that none of these proteins alone was strictly required for CB-5083 activity. Moreover, we showed that the absence of XBP1 (XBP1−/−) increased the sensitivity to CB-5083, leading to the hypothesis that XBP1 splicing counteracts the activity of CB-5083, probably mitigating ER stress. Finally, vincristine was synergistic with CB-5083 in both BALL1 and OP1 cells. In summary, the targeting of p97 with CB-5083 is a novel promising therapeutic approach that should be further evaluated in B-ALL.

Published
2017

29. Integrative proteogenomics using ProteomeGenerator2.

Author

Kwok N, Aretz Z, Takao S, Ser Z, Cifani P, and Kentsis A

Abstract

Recent advances in nucleic acid sequencing now permit rapid and genome-scale analysis of genetic variation and transcription, enabling population-scale studies of human biology, disease, and diverse organisms. Likewise, advances in mass spectrometry proteomics now permit highly sensitive and accurate studies of protein expression at the whole proteome-scale. However, most proteomic studies rely on consensus databases to match spectra to peptide and proteins sequences, and thus remain limited to the analysis of canonical protein sequences. Here, we develop ProteomeGenerator2 (PG2), based on the scalable and modular ProteomeGenerator framework. PG2 integrates genome and transcriptome sequencing to incorporate protein variants containing amino acid substitutions, insertions, and deletions, as well as non-canonical reading frames, exons, and other variants caused by genomic and transcriptomic variation. We benchmarked PG2 using synthetic data and genomic, transcriptomic, and proteomic analysis of human leukemia cells. PG2 can be integrated with current and emerging sequencing technologies, assemblers, variant callers, and mass spectral analysis algorithms, and is available open-source from https://github.com/kentsisresearchgroup/ProteomeGenerator2 .

Published
2023
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30. [Successful treatment of acute promyelocytic leukemia in a pregnant patient with all-trans retinoic acid and chemotherapy resulting in a safe delivery].

Author

Itoh M, Takao S, Yago K, and Shimada H

Subjects
Adult, Cesarean Section, Cytarabine administration & dosage, Daunorubicin administration & dosage, Female, Humans, Infant, Newborn, Male, Pregnancy, Pregnancy Outcome, Remission Induction, Antineoplastic Combined Chemotherapy Protocols therapeutic use, Leukemia, Promyelocytic, Acute drug therapy, Pregnancy Complications, Hematologic drug therapy, Tretinoin administration & dosage
Abstract

A 32-year-old woman at 21 gestational weeks was admitted because of leukocytosis with DIC. She was diagnosed as having acute promyelocytic leukemia and treated with all-trans retinoic acid (70 mg/body) in combination with daunorubicin and cytosine arabinoside. She achieved complete remission, and continuously received a second treatment with daunorubicin and cytosine arabinoside. Cesarean section was performed, and a live male infant was born in the 30th week of pregnancy. The mother and baby have progressed excellently to date. In a such case, the choice of treatment and time of birth should be considered depending on the individual situation.

Published
2003

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