Stromal cell-mediated mitochondrial redox adaptation regulates drug resistance in childhood acute lymphoblastic leukemia

Oncotarget

Volumn 6, Issue 40, 2015, Pages 43048-43064

  Liu, Jizhong ^a   Masurekar, Ashish ^a   Johnson, Suzanne ^a   Chakraborty, Sohini ^b   Griffiths, John ^c   Smith, Duncan ^c   Alexander, Seema ^a   Dempsey, Clare ^a   Parker, Catriona ^a   Harrison, Stephanie ^a   Li, Yaoyong ^c   Miller, Crispin ^c   Di, Yujun ^a   Ghosh, Zhumur ^b   Krishnan, Shekhar ^a,d   Saha, Vaskar ^a,d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BOSE INSTITUTE   (India)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d Department of Paediatric Oncology Tata Translational Cancer Research Centre   (India)

Author keywords

ALL; Drug resistance; Metabolic stress response; Oxidative stress; Tumor microenvironment

Indexed keywords

ASPARAGINASE; BUTHIONINE SULFOXIMINE; DEXAMETHASONE; DOXORUBICIN; GLUTATHIONE; HISTONE H2AX; MITOXANTRONE; PHENETHYL ISOTHIOCYANATE; PROTEIN MCL 1; REACTIVE OXYGEN METABOLITE; VINCRISTINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW STROMA CELL; CALCIUM TRANSPORT; CANCER RESISTANCE; CELL PROLIFERATION; CHILD; CHILDHOOD LEUKEMIA; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MINIMAL RESIDUAL DISEASE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; UPREGULATION; ADAPTATION; ANIMAL; BONE MARROW; DNA MICROARRAY; DRUG RESISTANCE; DRUG SCREENING; FLOW CYTOMETRY; GENETIC TRANSFECTION; IMMUNOBLOTTING; METABOLISM; MITOCHONDRION; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; STROMA CELL; TUMOR MICROENVIRONMENT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BONE MARROW; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; MICE; MICE, INBRED NOD; MICE, SCID; MITOCHONDRIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; REACTIVE OXYGEN SPECIES; STROMAL CELLS; TRANSFECTION; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84952317566     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5528     Document Type: Article

References (58)

1. Bhojwani D, Kang HN, Moskowitz NP, Min DJ, Lee H, Potter JW, Davidson G, Willman CL, Borowitz MJ, Belitskaya-Levy I, Hunger SP, Raetz EA, Carroll WL. Biologic pathways associated with relapse in childhood acute lymphoblastic leukemia: a Children's Oncology Group study. Blood. 2006; 108:711-717.
2. Conter V, Bartram CR, Valsecchi MG, Schrauder A, Panzer-Grumayer R, Moricke A, Arico M, Zimmermann M, Mann G, De Rossi G, Stanulla M, Locatelli F, Basso G, Niggli F, Barisone E, Henze G, et al. Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood. 2010; 115:3206-3214.
3. Parker C, Waters R, Leighton C, Hancock J, Sutton R, Moorman AV, Ancliff P, Morgan M, Masurekar A, Goulden N, Green N, Revesz T, Darbyshire P, Love S, Saha V. Effect of mitoxantrone on outcome of children with first relapse of acute lymphoblastic leukaemia (ALL R3): an open-label randomised trial. Lancet. 2010; 376:2009-2017.
4. Meads MB, Gatenby RA, Dalton WS. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nature Reviews Cancer. 2009; 9:665-A674.
5. Abdi J, Chen G, Chang H. Drug resistance in multiple myeloma: latest findings and new concepts on molecular mechanisms. Oncotarget. 2013; 4:2186-2207.
6. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nature Reviews Cancer. 2011; 11:85-95.
7. Shehata M, Schnabl S, Demirtas D, Hilgarth M, Hubmann R, Ponath E, Badrnya S, Lehner C, Hoelbl A, Duechler M, Gaiger A, Zielinski C, Schwarzmeier JD, Jaeger U. Reconstitution of PTEN activity by CK2 inhibitors and interference with the PI3-K/Akt cascade counteract the antiapoptotic effect of human stromal cells in chronic lymphocytic leukemia. Blood. 2010; 116:2513-2521.
8. Tabe Y, Jin LH, Tsutsumi-Ishii Y, Xu YY, McQueen T, Priebe W, Mills GB, Ohsaka A, Nagaoka I, Andreeff M, Konopleva M. Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells. Cancer Research. 2007; 67:684-694.
9. Yang F, Chen YZ, Shen T, Guo D, Dakhova O, Ittmann MM, Creighton CJ, Zhang YQ, Dang TD, Rowley DR. Stromal TGF-beta signaling induces AR activation in prostate cancer. Oncotarget. 2014; 5:10854-10869.
10. Iwamoto S, Mihara K, Downing JR, Pui CH, Campana D. Mesenchymal cells regulate the response of acute lymphoblastic leukemia cells to asparaginase. Journal of Clinical Investigation. 2007; 117:1049-1057.
11. Roodhart JML, Daenen LGM, Stigter ECA, Prins HJ, Gerrits J, Houthuijzen JM, Gerritsen MG, Schipper HS, Backer MJG, van Amersfoort M, Vermaat JSP, Moerer P, Ishihara K, Kalkhoven E, Beijnen JH, Derksen PWB, et al. Mesenchymal Stem Cells Induce Resistance to Chemotherapy through the Release of Platinum-Induced Fatty Acids. Cancer Cell. 2011; 20:370-383.
12. Zhang W, Trachootham D, Liu JY, Chen G, Pelicano H, Garcia-Prieto C, Lu WQ, Burger JA, Croce CM, Plunkett W, Keating MJ, Huang P. Stromal control of cystine metabolism promotes cancer cell survival in chronic lymphocytic leukaemia. Nature Cell Biology. 2012; 14:276-+.
13. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov. 2009; 8:579-591.
14. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008; 134:703-707.
15. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian DL, Lam JS, Ailles LE, Wong MZ, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009; 458:780-U123.
16. Nishigaki H, Ito C, Manabe A, Kumagai M, Coustan-Smith E, Yanishevski Y, Behm FG, Raimondi SC, Pui CH, Campana D. Prevalence and growth characteristics of malignant stem cells in B-lineage acute lymphoblastic leukemia. Blood. 1997; 89:3735-3744.
17. Ito C, Evans WE, McNinch L, Coustan-Smith E, Mahmoud H, Pui CH, Campana D. Comparative cytotoxicity of dexamethasone and prednisolone in childhood acute lymphoblastic leukemia. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1996; 14:2370-2376.
18. Suryani S, Carol H, Chonghaile TN, Frismantas V, Sarmah C, High L, Bornhauser B, Cowley MJ, Szymanska B, Evans K, Boehm I, Tonna E, Jones L, Manesh DM, Kurmasheva RT, Billups C, et al. Cell and molecular determinants of in vivo efficacy of the BH3 mimetic ABT-263 against pediatric acute lymphoblastic leukemia xenografts. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20:4520-4531.
19. Boutter J, Huang Y, Marovca B, Vonderheit A, Grotzer MA, Eckert C, Cario G, Wollscheid B, Horvath P, Bornhauser BC, Bourquin JP. Image-based RNA interference screening reveals an individual dependence of acute lymphoblastic leukemia on stromal cysteine support. Oncotarget. 2014.
20. Kiel MJ, Morrison SJ. Uncertainty in the niches that maintain haematopoietic stem cells. Nature Reviews Immunology. 2008; 8:290-301.
21. Keating A. Mesenchymal Stromal Cells: New Directions. Cell Stem Cell. 2012; 10:709-716.
22. Windus LCE, Glover TT, Avery VM. Bone-stromal cells up-regulate tumourigenic markers in a tumour-stromal 3D model of prostate cancer. Mol Cancer. 2013; 12.
23. Pampaloni F, Reynaud EG, Stelzer EHK. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Bio. 2007; 8:839-845.
24. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science. 2001; 294:1708-1712.
25. Sharma SV, Lee DY, Li BH, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, Wong KK, Brandstetter K, Wittner B, Ramaswamy S, Classon M, Settleman J. A Chromatin-Mediated Reversible Drug-Tolerant State in Cancer Cell Subpopulations. Cell. 2010; 141:69-80.
26. Altomare DA, Testa JR. Perturbations of the AKT signaling pathway in human cancer. Oncogene. 2005; 24:7455-7464.
27. Davies MA. Regulation, Role, and Targeting of Akt in Cancer. Journal of Clinical Oncology. 2011; 29:4715-4717.
28. Wong J, Welschinger R, Hewson J, Bradstock KF, Bendall LJ. Efficacy of dual PI-3K and mTOR inhibitors in Vitro and in Vivo in acute lymphoblastic leukemia. Oncotarget. 2014; 5:10460-10472.
29. Cani A, Simioni C, Martelli AM, Zauli G, Tabellini G, Ultimo S, McCubrey JA, Capitani S, Neri LM. Triple Akt inhibition as a new therapeutic strategy in T-cell acute lymphoblastic leukemia. Oncotarget. 2015; 6:6597-6610.
30. Glennie S, Soeiro I, Dyson PJ, Lam EWF, Dazzi F. Bone marrow mesenchymal stem cefls induce division arrest anergy of activated T cells. Blood. 2005; 105:2821-2827.
31. Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V, Uccelli A. Human mesenchymal stem cells modulate B-cell functions. Blood. 2006; 107:367-372.
32. Brookes PS, Yoon YS, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. American Journal of Physiology-Cell Physiology. 2004; 287:C817-C833.
33. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, et al. The landscape of somatic copy-number alteration across human cancers. Nature. 2010; 463:899-905.
34. Kornblau SM, Singh N, Qiu YH, Chen WJ, Zhang NX, Coombes KR. Highly Phosphorylated FOXO3A Is an Adverse Prognostic Factor in Acute Myeloid Leukemia. Clinical Cancer Research. 2010; 16:1865-1874.
35. Kuiper RP, Schoenmakers EFPM, van Reijmersdal SV, Hehir-Kwa JY, van Kessel AG, van Leeuwen FN, Hoogerbruggey PM. High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression. Leukemia. 2007; 21:1258-1266.
36. Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li XY, Tolliday NJ, Golub TR, Carr SA, Shamji AF, Stern AM, Mandinova A, Schreiber SL, Lee SW. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature. 2011; 475:231-234.
37. Roh JL, Kim EH, Park JY, Kim JW, Kwon M, Lee BH. Piperlongumine selectively kills cancer cells and increases cisplatin antitumor activity in head and neck cancer. Oncotarget. 2014; 5:9227-9238.
38. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu JS, Huang P. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell. 2006; 10:241-252.
39. Le SB, Hailer MK, Buhrow S, Wang Q, Flatten K, Pediaditakis P, Bible KC, Lewis LD, Sausville EA, Pang YP, Ames MM, Lemasters JJ, Holmuhamedov EL, Kaufmann SH. Inhibition of mitochondrial respiration as a source of adaphostin-induced reactive oxygen species and cytotoxicity. Journal of Biological Chemistry. 2007; 282:8860-8872.
40. Ji Y, Morris ME. Determination of phenethyl isothiocyanate in human plasma and urine by ammonia derivatization and liquid chromatography-tandem mass spectrometry. Analytical Biochemistry. 2003; 323:39-47.
41. Offman MN, Krol M, Patel N, Krishnan S, Liu JZ, Saha V, Bates PA. Rational engineering of L-asparaginase reveals importance of dual activity for cancer cell toxicity. Blood. 2011; 117:1614-1621.
42. Avramis VI, Panosyan EH. Pharmacokinetic/pharmacodynamic relationships of asparaginase formulations - The past, the present and recommendations for the future. Clinical Pharmacokinetics. 2005; 44:367-393.
43. Vora A, Goulden N, Wade R, Mitchell C, Hancock J, Hough R, Rowntree C, Richards S. Treatment reduction for children and young adults with low-risk acute lymphoblastic leukaemia defined by minimal residual disease (UKALL 2003): a randomised controlled trial. The lancet oncology. 2013; 14:199-209.
44. Masurekar A, Fong C, Hussein A, Revesz T, Hoogerbrugge PM, Love S, Ciria C, Parker C, Krishnan S, Saha V. The optimal use of PEG-asparaginase in relapsed ALL-lessons from the ALLR3 Clinical Trial. Blood cancer journal. 2014; 4:e203.
45. Clarkson B, Ohkita T, Ota K, Fried J. Studies of Cellular Proliferation in Human Leukemia. I. Estimation of Growth Rates of Leukemic and Normal Hematopoietic Cells in 2 Adults with Acute Leukemia Given Single Injections of Tritiated Thymidine. J Clin Invest. 1967; 46:506.
46. Rhein P, Scheid S, Ratei R, Hagemeier C, Seeger K, Kirschner-Schwabe R, Moericke A, Schrappe M, Spang R, Ludwig WD, Karawajew L. Gene expression shift towards normal B cells, decreased proliferative capacity and distinct surface receptors characterize leukemic blasts persisting during induction therapy in childhood acute lymphoblastic leukemia. Leukemia. 2007; 21:897-905.
47. Eckert C, Henze G, Seeger K, Hagedorn N, Mann G, Panzer-Grumayer R, Peters C, Klingebiel T, Borkhardt A, Schrappe M, Schrauder A, Escherich G, Sramkova L, Niggli F, Hitzler J, von Stackelberg A. Use of allogeneic hematopoietic stem-cell transplantation based on minimal residual disease response improves outcomes for children with relapsed acute lymphoblastic leukemia in the intermediate-risk group. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2013; 31:2736-2742.
48. Hof J, Krentz S, van Schewick C, Korner G, Shalapour S, Rhein P, Karawajew L, Ludwig WD, Seeger K, Henze G, von Stackelberg A, Hagemeier C, Eckert C, Kirschner-Schwabe R. Mutations and Deletions of the TP53 Gene Predict Nonresponse to Treatment and Poor Outcome in First Relapse of Childhood Acute Lymphoblastic Leukemia. J Clin Oncol. 2011; 29:3185-3193.
49. Sykes SM, Lane SW, Bullinger L, Kalaitzidis D, Yusuf R, Saez B, Ferraro F, Mercier F, Singh H, Brumme KM, Acharya SS, Scholl C, Tothova Z, Attar EC, Frohling S, DePinho RA, et al. AKT/FOXO Signaling Enforces Reversible Differentiation Blockade in Myeloid Leukemias. (vol 146, pg 697, 2011). Cell. 2011; 147:247-247.
50. Harper ME, Antoniou A, Villalobos-Menuey E, Russo A, Trauger R, Vendemelio M, George A, Bartholomew R, Carlo D, Shaikh A, Kupperman J, Newell EW, Bespalov IA, Wallace SS, Liu Y, Rogers JR, et al. Characterization of a novel metabolic strategy used by drug-resistant tumor cells. Faseb Journal. 2002; 16:1550-1557.
51. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood. 2007; 110:3056-3063.
52. Li CP, Thompson MA, Tamayo AT, Zuo Z, Lee J, Vega F, Ford RJ, Pham LV. Over-expression of Thioredoxin-1 mediates growth, survival, and chemoresistance and is a druggable target in diffuse large B-cell lymphoma. Oncotarget. 2012; 3:314-326.
53. Jonchere B, Vetillard A, Toutain B, Lam D, Bernard AC, Henry C, Trecesson SD, Gamelin E, Juin P, Guette C, Coqueret O. Irinotecan treatment and senescence failure promote the emergence of more transformed and invasive cells that depend on anti-apoptotic Mcl-1. Oncotarget. 2015; 6:409-426.
54. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Molecular Cell. 2006; 21:749-760.
55. Perciavalle RM, Stewart DP, Koss B, Lynch J, Milasta S, Bathina M, Temirov J, Cleland MM, Pelletier S, Schuetz JD, Youle RJ, Green DR, Opferman JT. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nature Cell Biology. 2012; 14:575-+.
56. Kroemer G, Pouyssegur J. Tumor cell metabolism: Cancer's Achilles' heel. Cancer Cell. 2008; 13:472-482.
57. Duan CW, Shi J, Chen J, Wang B, Yu YH, Qin X, Zhou XC, Cai YJ, Li ZQ, Zhang F, Yin MZ, Tao Y, Mi JQ, Li LH, Enver T, Chen GQ, et al. Leukemia propagating cells rebuild an evolving niche in response to therapy. Cancer cell. 2014; 25:778-793.
58. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012; 12:252-264.