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Shotaro Iwamoto, … , Ching-Hon Pui, Dario Campana
Published April 2, 2007
Citation Information: J Clin Invest. 2007;117(4):1049-1057. https://doi.org/10.1172/JCI30235.
Citation Information: J Clin Invest. 2007;117(4):1049-1057. https://doi.org/10.1172/JCI30235.
Abstract
Because of their low asparagine synthetase (ASNS) expression and asparagine biosynthesis, acute lymphoblastic leukemia (ALL) cells are exquisitely sensitive to asparagine depletion. Consequently, asparaginase is a major component of ALL therapy, but the mechanisms regulating the susceptibility of leukemic cells to this agent are unclear. In 288 children with ALL, cellular ASNS expression was more likely to be high in T-lineage ALL and low in B-lineage ALL with TEL-AML1 or hyperdiploidy. However, ASNS expression levels in bone marrow–derived mesenchymal cells (MSCs), which form the microenvironment where leukemic cells grow, were on average 20 times higher than those in ALL cells. MSCs protected ALL cells from asparaginase cytotoxicity in coculture experiments. This protective effect correlated with levels of ASNS expression: downregulation by RNA interference decreased the capacity of MSCs to protect ALL cells from asparaginase, whereas enforced ASNS expression conferred enhanced protection. Asparagine secretion by MSCs was directly related to their ASNS expression levels, suggesting a mechanism — increased concentrations of asparagine in the leukemic cell microenvironment — for the protective effects we observed. These results provide what we believe to be a new basis for understanding asparaginase resistance in ALL and indicate that MSC niches in the bone marrow can form a safe haven for leukemic cells.
Authors
Shotaro Iwamoto, Keichiro Mihara, James R. Downing, Ching-Hon Pui, Dario Campana
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H Dimitriou, C Choulaki, C Perdikogianni, E Stiakaki, M Kalmanti |
International Journal of Hematology | 2014 |
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Advances in understanding the leukaemia microenvironment
Y Tabe, M Konopleva |
British Journal of Haematology | 2014 |
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Umbilical cord tissue-derived mesenchymal stem cells induce apoptosis in PC-3 prostate cancer cells through activation of JNK and downregulation of PI3K/AKT signaling
I Han, M Yun, EO Kim, B Kim, MH Jung, SH Kim |
Stem Cell Research & Therapy | 2014 |
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Update on the Use of l-Asparaginase in Infants and Adolescent Patients with Acute Lymphoblastic Leukemia
AF Andrade, KS Borges, VS Silveira |
Clinical Medicine Insights. Oncology | 2014 |
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Activation of the vascular niche supports leukemic progression and resistance to chemotherapy
MG Poulos, EJ Gars, MC Gutkin, CC Kloss, M Ginsberg, JM Scandura, S Rafii, JM Butler |
Experimental Hematology | 2014 |
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Rationale for a pediatric-inspired approach in the adolescent and young adult population with acute lymphoblastic leukemia, with a focus on asparaginase treatment
C Rizzari, MC Putti, A Colombini, S Casagranda, GM Ferrari, C Papayannidis, I Iacobucci, MC Abbenante, C Sartor, G Martinelli |
Hematology Reports | 2014 |
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Polymorphisms of Asparaginase Pathway and Asparaginase-Related Complications in Children with Acute Lymphoblastic Leukemia
MB Tanfous, B Sharif-Askari, F Ceppi, H Laaribi, V Gagne, J Rousseau, M Labuda, LB Silverman, SE Sallan, D Neuberg, JL Kutok, D Sinnett, C Laverdiere, M Krajinovic |
Clinical cancer research | 2014 |
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EMP1, a novel poor prognostic factor in pediatric leukemia regulates prednisolone resistance, cell proliferation, migration and adhesion
IM Ariës, IS Jerchel, RE van den Dungen, LC van den Berk, JM Boer, MA Horstmann, G Escherich, R Pieters, ML den Boer |
Leukemia | 2014 |
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Image-based RNA interference screening reveals an individual dependence of acute lymphoblastic leukemia on stromal cysteine support
Boutter J, Huang Y, Marovca B, Vonderheit A, Grotzer MA, Eckert C, Cario G, Wollscheid B, Horvath P, Bornhauser BC, Bourquin JP |
Oncotarget | 2014 |
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Osteoblasts Protect AML Cells from SDF-1-Induced Apoptosis
Kremer KN, Dudakovic A, McGee-Lawrence ME, Philips RL, Hess AD, Smith BD, van Wijnen AJ, Karp JE, Kaufmann SH, Westendorf JJ, Hedin KE |
Journal of Cellular Biochemistry | 2014 |
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Plerixafor as a chemosensitizing agent in pediatric acute lymphoblastic leukemia: efficacy and potential mechanisms of resistance to CXCR4 inhibition
Sison EA, Magoon D, Li L, Annesley CE, Rau RE, Small D, Brown P |
Oncotarget | 2014 |
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Cancer associated fibroblasts in hematological malignancies
Raffaghello L, Vacca A, Pistoia V, Ribatti D |
Oncotarget | 2014 |
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Adipocytes Cause Leukemia Cell Resistance to L-Asparaginase via Release of Glutamine
EA Ehsanipour, X Sheng, JW Behan, X Wang, A Butturini, VI Avramis, SD Mittelman |
Cancer research | 2013 |
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Asparagine synthetase is an independent predictor of surgical survival and a potential therapeutic target in hepatocellular carcinoma
B Zhang, LW Dong, YX Tan, J Zhang, YF Pan, C Yang, MH Li, ZW Ding, LJ Liu, TY Jiang, JH Yang, HY Wang |
British Journal of Cancer | 2013 |
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Role of mesenchymal stem cells in leukaemia: Dr. Jekyll or Mr. Hyde?
RS Wong, SK Cheong |
Clinical and Experimental Medicine | 2013 |
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Targeting arginine-dependent cancers with arginine-degrading enzymes: opportunities and challenges
MM Phillips, MT Sheaff, PW Szlosarek |
Cancer Research and Treatment | 2013 |
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Mesenchymal stem cells derived from breast cancer tissue promote the proliferation and migration of the MCF-7 cell line in vitro
C Zhang, W Zhai, Y Xie, Q Chen, W Zhu, X Sun |
Oncology Letters | 2013 |
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Vincristine could partly suppress stromal support to T-ALL blasts during pegylated arginase I treatment
F Kwong-Lam, CG Chi-Fung |
Experimental Hematology and Oncology | 2013 |
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Dynamic chemotherapy-induced upregulation of CXCR4 expression: a mechanism of therapeutic resistance in pediatric AML
EA Sison, E McIntyre, D Magoon, P Brown |
Molecular cancer research : MCR | 2013 |
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CXCR4 chemokine receptor signaling induces apoptosis in acute myeloid leukemia cells via regulation of the Bcl-2 family members Bcl-XL, Noxa, and Bak
KN Kremer, KL Peterson, PA Schneider, XW Meng, H Dai, AD Hess, BD Smith, C Rodriguez-Ramirez, JE Karp, SH Kaufmann, KE Hedin |
The Journal of biological chemistry | 2013 |
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L-asparaginase inhibits invasive and angiogenic activity and induces autophagy in ovarian cancer
M Yu, R Henning, A Walker, G Kim, A Perroy, R Alessandro, V Virador, EC Kohn |
Journal of Cellular and Molecular Medicine | 2012 |
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The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression
JM Houthuijzen, LG Daenen, JM Roodhart, EE Voest |
British Journal of Cancer | 2012 |
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Acute myeloid leukemia with mediastinal myeloid sarcoma refractory to acute myeloid leukemia therapy but responsive to l-asparaginase
H Takahashi, K Koh, M Kato, H Kishimoto, E Oguma, R Hanada |
International Journal of Hematology | 2012 |
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Genome-wide association study identifies germline polymorphisms associated with relapse of childhood acute lymphoblastic leukemia
JJ Yang, C Cheng, M Devidas, X Cao, D Campana, W Yang, Y Fan, G Neale, N Cox, P Scheet, MJ Borowitz, NJ Winick, PL Martin, WP Bowman, B Camitta, GH Reaman, WL Carroll, CL Willman, SP Hunger, WE Evans, CH Pui, M Loh, MV Relling |
Blood | 2012 |
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Regulation of HIF-1α signaling and chemoresistance in acute lymphocytic leukemia under hypoxic conditions of the bone marrow microenvironment
O Frolova, I Samudio, JM Benito, R Jacamo, SM Kornblau, A Markovic, W Schober, H Lu, YH Qiu, D Buglio, T McQueen, S Pierce, EJ Shpall, S Konoplev, D Thomas, H Kantarjian, R Lock, M Andreeff, M Konopleva |
Cancer biology & therapy | 2012 |
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Development of an ELISA to detect circulating anti-asparaginase antibodies in dogs with lymphoid neoplasia treated with Escherichia coli l-asparaginase(*)
JA Kidd, P Ross, AS Buntzman, PR Hess |
Veterinary and Comparative Oncology | 2012 |
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Cancer Cell Metabolism: One Hallmark, Many Faces
J R., DM Sabatini |
Cancer Discovery | 2012 |
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Identification of Hepatic Niche Harboring Human Acute Lymphoblastic Leukemic Cells via the SDF-1/CXCR4 Axis
I Kato, A Niwa, T Heike, H Fujino, MK Saito, K Umeda, H Hiramatsu, M Ito, M Morita, Y Nishinaka, S Adachi, F Ishikawa, T Nakahata |
PloS one | 2011 |
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The bone marrow microenvironment and leukemia: biology and therapeutic targeting
EA Sison, P Brown |
Expert Review of Hematology | 2011 |
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Asparagine synthetase is partially localized to the plasma membrane and upregulated by L-asparaginase in U937 cells
Y He, B Li, C Luo, S Shen, J Chen, H Xue, J Tang, L Gu |
Journal of Huazhong University of Science and Technology [Medical Sciences] | 2011 |
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ETV6-RUNX1-positive childhood acute lymphoblastic leukemia: improved outcome with contemporary therapy
D Bhojwani, D Pei, JT Sandlund, S Jeha, RC Ribeiro, JE Rubnitz, SC Raimondi, S Shurtleff, M Onciu, C Cheng, E Coustan-Smith, WP Bowman, SC Howard, ML Metzger, H Inaba, W Leung, WE Evans, D Campana, MV Relling, CH Pui |
Leukemia | 2011 |
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Mesenchymal niches of bone marrow in cancer
A Abarrategi, L Mariñas-Pardo, I Mirones, E Rincón, J García-Castro |
Clinical and Translational Oncology | 2011 |
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Modeling sarcomagenesis using multipotent mesenchymal stem cells
R Rodriguez, R Rubio, P Menendez |
Cell Research | 2011 |
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ATF5 polymorphisms influence ATF function and response to treatment in children with childhood acute lymphoblastic leukemia
J Rousseau, V Gagne, M Labuda, C Beaubois, D Sinnett, C Laverdiere, A Moghrabi, SE Sallan, LB Silverman, D Neuberg, JL Kutok, M Krajinovic |
Blood | 2011 |
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Cancer-stromal interactions: Role in cell survival, metabolism and drug sensitivity
W Zhang, P Huang |
Cancer biology & therapy | 2011 |
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Induction of autophagy-dependent necroptosis is required to overcome glucocorticoid resistance in acute lymphoblastic leukemia
Laura Bonapace, Beat Bornhauser, Maike Schmitz, Gunnar Cario, Urs Ziegler, Felix Niggli, Beat Schafer, Martin Schrappe, Martin Stanulla, Jean-Pierre Bourquin |
Journal of Clinical Investigation | 2010 |
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Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis
F Vianello, F Villanova, V Tisato, S Lymperi, KK Ho, AR Gomes, D Marin, D Bonnet, J Apperley, EW Lam, F Dazzi |
Haematologica | 2010 |
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Mesenchymal Stem Cells as Therapeutics
B Parekkadan, JM Milwid |
Annual Review of Biomedical Engineering | 2010 |
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VE-cadherin Regulates Philadelphia Chromosome Positive Acute Lymphoblastic Leukemia Sensitivity to Apoptosis
H O'Leary, SM Akers, D Piktel, C Walton, JE Fortney, KH Martin, M Craig, J Coad, LF Gibson |
Cancer Microenvironment | 2010 |
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Human bone marrow mesenchymal stem cells display anti-cancer activity in SCID mice bearing disseminated non-Hodgkin's lymphoma xenografts
P Secchiero, S Zorzet, C Tripodo, F Corallini, E Melloni, L Caruso, R Bosco, S Ingrao, B Zavan, G Zauli |
PloS one | 2010 |
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A genome-wide approach identifies that the aspartate metabolism pathway contributes to asparaginase sensitivity
SH Chen, W Yang, Y Fan, G Stocco, KR Crews, JJ Yang, SW Paugh, CH Pui, WE Evans, MV Relling |
Leukemia | 2010 |
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Adult stem cels and their niches
F Ferraro, CL Celso, D Scadden |
Advances in experimental medicine and biology | 2010 |
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Adult acute lymphoblastic leukemia: Concepts and strategies
S Faderl, S O'Brien, CH Pui, W Stock, M Wetzler, D Hoelzer, HM Kantarjian |
Cancer | 2010 |
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A Dyad of Lymphoblastic Lysosomal Cysteine Proteases Degrades the Key Anti-Leukemic Drug L-Asparaginase
Naina Patel, Shekhar Krishnan, Marc N Offman, Marcin Krol, Catherine X Moss, Carly Leighton, Frederik W van Delft, Mark Holland, JiZhong Liu, Seema Alexander, Clare Dempsey, Hany Ariffin, Monika Essink, Tim OB Eden, Colin Watts, Paul A Bates, Vaskar Saha |
Journal of Clinical Investigation | 2009 |
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Immunotherapy in acute leukemia
W Leung |
Seminars in Hematology | 2009 |
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Cancer-Stromal Cell Interaction and Tumor Angiogenesis in Gastric Cancer
Y Kitadai |
Cancer Microenvironment | 2009 |
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Pharmacogenetics in acute lymphoblastic leukemia
MH Cheok, N Pottier, L Kager, WE Evans |
Seminars in Hematology | 2009 |
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Expansion of highly cytotoxic human natural killer cells for cancer cell therapy
H Fujisaki, H Kakuda, N Shimasaki, C Imai, J Ma, T Lockey, P Eldridge, WH Leung, D Campana |
Cancer research | 2009 |
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Comparison of native E. coli and PEG asparaginase pharmacokinetics and pharmacodynamics in pediatric acute lymphoblastic leukemia
JC Panetta, A Gajjar, N Hijiya, LJ Hak, C Cheng, W Liu, CH Pui, MV Relling |
Clinical Pharmacology & Therapeutics | 2009 |
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The leukemic stem cell niche: current concepts and therapeutic opportunities
SW Lane, DT Scadden, DG Gilliland |
Blood | 2009 |
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Functional analysis of a novel DNA polymorphism of a tandem repeated sequence in the asparagine synthetase gene in acute lymphoblastic leukemia cells
T Akagi, D Yin, N Kawamata, CR Bartram, WK Hofmann, JH Song, CW Miller, ML Boer, HP Koeffler |
Leukemia Research | 2009 |
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Contribution of bone microenvironment to leukemogenesis and leukemia progression
F Ayala, R Dewar, M Kieran, R Kalluri |
Leukemia | 2009 |
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Therapeutic targeting of microenvironmental interactions in leukemia: Mechanisms and approaches
M Konopleva, Y Tabe, Z Zeng, M Andreeff |
Drug Resistance Updates | 2009 |
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Diverse marrow stromal cells protect CLL cells from spontaneous and drug-induced apoptosis: development of a reliable and reproducible system to assess stromal cell adhesion-mediated drug resistance
AV Kurtova, K Balakrishnan, R Chen, W Ding, S Schnabl, MP Quiroga, M Sivina, WG Wierda, Z Estrov, MJ Keating, M Shehata, U Jager, V Gandhi, NE Kay, W Plunkett, JA Burger |
Blood | 2009 |
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The bone marrow niche: habitat to hematopoietic and mesenchymal stem cells and unwitting host to molecular parasites
Y Shiozawa, AM Havens, KJ Pienta, RS Taichman |
Leukemia | 2008 |
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Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool
J García-Castro, C Trigueros, J Madrenas, JA Pérez-Simón, R Rodriguez, P Menendez |
Journal of Cellular and Molecular Medicine | 2008 |
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Role of minimal residual disease evaluation in leukemia therapy
D Campana |
Current Hematologic Malignancy Reports | 2008 |
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Mesenchymal Stem Cells in Cancer
J Stagg |
Stem Cell Reviews and Reports | 2008 |
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