Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies (original) (raw)
Goldman JM, Melo JV . Chronic myeloid leukemia – advances in biology and new approaches to treatment. N Engl J Med 2003; 349: 1451–1464. ArticleCASPubMed Google Scholar
Lugo TG, Pendergast AM, Muller AJ, Witte ON . Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 1990; 247: 1079–1082. ArticleCASPubMed Google Scholar
Holyoake TL, Jiang X, Drummond MW, Eaves AC, Eaves CJ . Elucidating critical mechanisms of deregulated stem cell turnover in the chronic phase of chronic myeloid leukemia. Leukemia 2002; 16: 549–558. ArticleCASPubMed Google Scholar
Penserga ET, Skorski T . Fusion tyrosine kinases: a result and cause of genomic instability. Oncogene 2007; 4: 11–20. Article Google Scholar
Dube ID, Arlin ZA, Kalousek DK, Eaves CJ, Eaves AC . Nonclonal hemopoietic progenitor cells detected in long-term marrow cultures from a Turner syndrome mosaic with chronic myeloid leukemia. Blood 1984; 64: 1284–1287. CASPubMed Google Scholar
Hogge DE, Coulombel L, Kalousek DK, Eaves CJ, Eaves AC . Nonclonal hemopoietic progenitors in a G6PD heterozygote with chronic myelogenous leukemia revealed after long-term marrow culture. Am J Hematol 1987; 24: 389–394. ArticleCASPubMed Google Scholar
Eaves CJ, Eaves AC . Progenitor cell dynamics. In: Carella AM, Daley GQ, Eaves CJ, Goldman JM, Hehlmann R (eds). Chronic Myeloid Leukemia: Biology & Treatment. Martin Dunitz: London, 2001, pp. 73–100. Google Scholar
Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996; 2: 561–566. ArticleCASPubMed Google Scholar
Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL . Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 2004; 305: 399–401. ArticleCASPubMed Google Scholar
Carter TA, Wodicka LM, Shah NP, Velasco AM, Fabian MA, Treiber DK et al. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci USA 2005; 102: 11011–11016. ArticleCASPubMedPubMed Central Google Scholar
Weisberg E, Manley PW, Breitenstein W, Bruggen J, Cowan-Jacob SW, Ray A et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 2005; 7: 129–141. ArticleCASPubMed Google Scholar
Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002; 99: 319–325. ArticleCASPubMed Google Scholar
Holtz MS, Slovak ML, Zhang F, Sawyers CL, Forman SJ, Bhatia R . Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood 2002; 99: 3792–3800. ArticleCASPubMed Google Scholar
Bhatia R, Holtz M, Niu N, Gray R, Snyder DS, Sawyers CL et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 2003; 101: 4701–4707. ArticleCASPubMed Google Scholar
Copland M, Hamilton A, Elrick LJ, Baird JW, Allan EK, Jordanides N et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML, but does not eliminate the quiescent fraction. Blood 2006; 107: 4532–4539. ArticleCASPubMed Google Scholar
Holyoake TL, Jiang X, Jorgensen HG, Graham S, Alcorn MJ, Laird C et al. Primitive quiescent leukemic cells from patients with chronic myeloid leukemia spontaneously initiate factor-independent growth in vitro in association with up-regulation of expression of interleukin-3. Blood 2001; 97: 720–728. ArticleCASPubMed Google Scholar
Jiang X, Lopez A, Holyoake T, Eaves A, Eaves C . Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc Natl Acad Sci USA 1999; 96: 12804–12809. ArticleCASPubMedPubMed Central Google Scholar
Holyoake T, Jiang X, Eaves C, Eaves A . Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 1999; 94: 2056–2064. CASPubMed Google Scholar
Dugray A, Geay JF, Foudi A, Bonnet ML, Vainchenker W, Wendling F et al. Rapid generation of a tetracycline-inducible BCR-ABL defective retrovirus using a single autoregulatory retroviral cassette. Leukemia 2001; 15: 1658–1662. ArticleCASPubMed Google Scholar
Jiang X, Ng E, Yip C, Eisterer W, Chalandon Y, Stuible M et al. Primitive interleukin 3 null hematopoietic cells transduced with BCR-ABL show accelerated loss after culture of factor-independence in vitro and leukemogenic activity in vivo. Blood 2002; 100: 3731–3740. ArticleCASPubMed Google Scholar
Jiang X, Zhao Y, Chan WY, Vercauteren S, Pang E, Kennedy S et al. Deregulated expression in Ph+ human leukemias of AHI-1, a gene activated by insertional mutagenesis in mouse models of leukemia. Blood 2004; 103: 3897–3904. ArticleCASPubMed Google Scholar
Dorsey JF, Cunnick JM, Lanehart R, Huang M, Kraker AJ, Bhalla KN et al. Interleukin-3 protects Bcr-Abl-transformed hematopoietic progenitor cells from apoptosis induced by Bcr-Abl tyrosine kinase inhibitors. Leukemia 2002; 16: 1589–1595. ArticleCASPubMed Google Scholar
Jiang X, Fujisaki T, Nicolini F, Berger M, Holyoake T, Eisterer W et al. Autonomous multi-lineage differentiation in vitro of primitive CD34+ cells from patients with chronic myeloid leukemia. Leukemia 2000; 14: 1112–1121. ArticleCASPubMed Google Scholar
Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004; 351: 657–667. ArticleCASPubMed Google Scholar
Barnes DJ, Palaiologou D, Panousopoulou E, Schultheis B, Yong AS, Wong A et al. Bcr-Abl expression levels determine the rate of development of resistance to imatinib mesylate in chronic myeloid leukemia. Cancer Res 2005; 65: 8912–8919. ArticleCASPubMed Google Scholar
ten Hoeve J, Arlinghaus RB, Guo JQ, Heisterkamp N, Groffen J . Tyrosine phosphorylation of CRKL in Philadelphia+ leukemia. Blood 1994; 84: 1731–1736. CASPubMed Google Scholar
Hamilton A, Elrick L, Myssina S, Copland M, Jorgensen H, Melo JV et al. BCR-ABL activity and its response to drugs can be determined in CD34+ CML stem cells by CrkL phosphorylation status using flow cytometry. Leukemia 2006; 20: 1035–1039. ArticleCASPubMed Google Scholar
White DL, Saunders VA, Dang P, Engler J, Zannettino AC, Cambareri AC et al. OCT-1 mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107); reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib. Blood 2006; 108: 697–704. ArticleCASPubMed Google Scholar
Thomas J, Wang L, Clark RE, Pirmohamed M . Active transport of imatinib into and out of cells: implications for drug resistance. Blood 2004; 104: 3739–3745. ArticleCASPubMed Google Scholar
Lepper ER, Nooter K, Verweij J, Acharya MR, Figg WD, Sparreboom A . Mechanisms of resistance to anticancer drugs: the role of the polymorphic ABC transporters ABCB1 and ABCG2. Pharmacogenomics 2005; 6: 115–138. ArticleCASPubMed Google Scholar
Scharenberg CW, Harkey MA, Torok-Storb B . The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002; 99: 507–512. ArticleCASPubMed Google Scholar
Mahon FX, Belloc F, Lagarde V, Chollet C, Moreau-Gaudry F, Reiffers J et al. MDR1 gene overexpression confers resistance to imatinib mesylate in leukemia cell line models. Blood 2003; 101: 2368–2373. ArticleCASPubMed Google Scholar
Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001; 344: 1031–1037. ArticleCASPubMed Google Scholar
Kantarjian H, Sawyers C, Hochhaus A, Guilhot F, Schiffer C, Gambacorti-Passerini C et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002; 346: 645–652. ArticleCASPubMed Google Scholar
Nowell PC . Progress with chronic myelogenous leukemia: a personal perspective over four decades. Annu Rev Med 2002; 53: 1–13. ArticleCASPubMed Google Scholar
Hughes TP, Kaeda J, Branford S, Rudzki Z, Hochhaus A, Hensley ML et al. Frequency of major molecular responses to imatinib or interferon alfa plus cytarabine in newly diagnosed chronic myeloid leukemia. N Engl J Med 2003; 349: 1423–1432. ArticleCASPubMed Google Scholar
Branford S, Rudzki Z, Walsh S, Parkinson I, Grigg A, Szer J et al. Detection of BCR-ABL mutations in patients with CML treated with imatinib is virtually always accompanied by clinical resistance, and mutations in the ATP phosphate-binding loop (P-loop) are associated with a poor prognosis. Blood 2003; 102: 276–283. ArticleCASPubMed Google Scholar
Deininger M, Buchdunger E, Druker BJ . The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 2005; 105: 2640–2653. ArticleCASPubMed Google Scholar
Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001; 293: 876–880. ArticleCASPubMed Google Scholar
Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2002; 2: 117–125. ArticleCASPubMed Google Scholar
Chu S, Xu H, Shah NP, Snyder DS, Forman SJ, Sawyers CL et al. Detection of BCR-ABL kinase mutations in CD34+ cells from chronic myelogenous leukemia patients in complete cytogenetic remission on imatinib mesylate treatment. Blood 2005; 105: 2093–2098. ArticleCASPubMed Google Scholar
Li S, Ilaria RL, Million RP, Daley GQ, Van Etten RA . The p190, p210, and p230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med 1999; 189: 1399–1412. ArticleCASPubMedPubMed Central Google Scholar
Chalandon Y, Jiang X, Loutet S, Eaves AC, Eaves CJ . Growth autonomy and lineage switching in BCR-ABL-transduced human cord blood cells depend on different functional domains of BCR-ABL. Leukemia 2004; 18: 1006–1012. ArticleCASPubMed Google Scholar
Crossman LC, Druker BJ, Deininger MW, Pirmohamed M, Wang L, Clark RE . hOCT 1 and resistance to imatinib. Blood 2005; 106: 1133–1134. ArticleCASPubMed Google Scholar
Jordanides NE, Jorgensen HG, Holyoake TL, Mountford JC . Functional ABCG2 is over-expressed on primary CML CD34+ cells and is inhibited by imatinib mesylate. Blood 2006; 108: 1370–1373. ArticleCASPubMed Google Scholar
Ozvegy-Laczka C, Hegedus T, Varady G, Ujhelly O, Schuetz JD, Varadi A et al. High-affinity interaction of tyrosine kinase inhibitors with the ABCG2 multidrug transporter. Mol Pharmacol 2004; 65: 1485–1495. ArticlePubMed Google Scholar
Burger H, van Tol H, Boersma AW, Brok M, Wiemer EA, Stoter G et al. Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump. Blood 2004; 104: 2940–2942. ArticleCASPubMed Google Scholar
Burger H, van Tol H, Brok M, Wiemer EA, de Bruijn EA, Guetens G et al. Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps. Cancer Biol Ther 2005; 4: 747–752. ArticleCASPubMed Google Scholar
Zhou S, Scheutz JD, Bunting KD, Colapietro A-M, Sampath J, Morris JJ et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001; 7: 1028–1034. ArticleCASPubMed Google Scholar
Hogge DE, Lansdorp PM, Reid D, Gerhard B, Eaves CJ . Enhanced detection, maintenance and differentiation of primitive human hematopoietic cells in cultures containing murine fibroblasts engineered to produce human Steel factor, interleukin-3 and granulocyte colony-stimulating factor. Blood 1996; 88: 3765–3773. CASPubMed Google Scholar
Fraser C, Eaves CJ, Kalousek DK . Fluorodeoxyuridine synchronization of hemopoietic colonies. Cancer Genet Cytogenet 1987; 24: 1–6. ArticleCASPubMed Google Scholar