Leukemic blasts program bone marrow adipocytes to generate a protumoral microenvironment

Blood

Volumn 129, Issue 10, 2017, Pages 1320-1332

  Shafat, Manar S ^a   Oellerich, Thomas ^b,c,d   Mohr, Sebastian ^b   Robinson, Stephen D ^e   Edwards, Dylan R ^a,e   Marlein, Christopher R ^a   Piddock, Rachel E ^a   Fenech, Matthew ^a,f   Zaitseva, Lyubov ^a   Abdul Aziz, Amina ^a   Turner, Jeremy ^a,f   Watkins, Johnathan A ^g   Lawes, Matthew ^f   Bowles, Kristian M ^a,f   Rushworth, Stuart A ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b GOETHE UNIVERSITY   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^f NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

^g Pilar Research and Education   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ACIPIMOX; CARNITINE PALMITOYLTRANSFERASE; CARNITINE PALMITOYLTRANSFERASE I; CARNITINE PALMITOYLTRANSFERASE IA; CARNITINE PALMITOYLTRANSFERASE II; CCAAT ENHANCER BINDING PROTEIN ALPHA; CD33 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; ENDOGLIN; ETOMOXIR; FATTY ACID; FATTY ACID BINDING PROTEIN 4; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HORMONE SENSITIVE LIPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIPID; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MESSENGER RNA; PROTEIN; SHORT HAIRPIN RNA; THY 1 ANTIGEN; TRANSCRIPTION FACTOR HOXA9; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN;

ACUTE MYELOID LEUKEMIA; ADIPOCYTE; ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLAST CELL; BONE MARROW ADIPOCYTE; BONE MARROW CELL; BONE MARROW STROMA CELL; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CELL DIFFERENTIATION; CELL INTERACTION; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; LEUKEMOGENESIS; LIPOLYSIS; MALE; MIDDLE AGED; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; UPREGULATION; VERY ELDERLY; ANIMAL; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; XENOGRAFT;

ADIPOCYTES; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; COCULTURE TECHNIQUES; FATTY ACID-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; LEUKEMIA, MYELOID, ACUTE; MALE; MICE; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT;

EID: 85015176412     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-08-734798     Document Type: Article

References (44)

1. Rowe JM, Tallman MS. How I treat acute myeloid leukemia. Blood. 2010;116(17):3147-3156.
2. Matsunaga T, Takemoto N, Sato T, et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med. 2003;9(9):1158-1165.
3. Nervi B, Ramirez P, Rettig MP, et al. Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood. 2009;113(24): 6206-6214.
4. Rushworth SA, Murray MY, Zaitseva L, Bowles KM, MacEwan DJ. Identification of Bruton's tyrosine kinase as a therapeutic target in acute myeloid leukemia. Blood. 2014;123(8):1229-1238.
5. Lane SW, Scadden DT, Gilliland DG. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood. 2009;114(6): 1150-1157.
6. Reuss-Borst MA, Klein G, Waller HD, Müller CA. Differential expression of adhesion molecules in acute leukemia. Leukemia. 1995;9(5):869-874.
7. Zaitseva L, Murray MY, Shafat MS, et al. Ibrutinib inhibits SDF1/CXCR4 mediated migration in AML. Oncotarget. 2014;5(20):9930-9938.
8. Cawthorn WP, Scheller EL, Learman BS, et al. Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab. 2014;20(2):368-375.
9. Steiner RM, Mitchell DG, Rao VM, et al. Magnetic resonance imaging of bone marrow: diagnostic value in diffuse hematologic disorders. Magn Reson Q. 1990;6(1):17-34.
10. Custer RPA. F.E. Studies on the structure and function of bone marrow II. J Lab Clin Med. 1932; 17:960-962.
11. Iversen PO, Wiig H. Tumor necrosis factor alpha and adiponectin in bone marrow interstitial fluid from patients with acute myeloid leukemia inhibit normal hematopoiesis. Clin Cancer Res. 2005; 11(19 Pt 1):6793-6799.
12. Dirat B, Bochet L, Dabek M, et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011;71(7):2455-2465.
13. Gazi E, Gardner P, Lockyer NP, Hart CA, Brown MD, Clarke NW. Direct evidence of lipid translocation between adipocytes and prostate cancer cells with imaging FTIR microspectroscopy. J Lipid Res. 2007;48(8): 1846-1856.
14. Nieman KM, Kenny HA, Penicka CV, et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med. 2011;17(11):1498-1503.
15. Herroon MK, Rajagurubandara E, Hardaway AL, et al. Bone marrow adipocytes promote tumor growth in bone via FABP4-dependent mechanisms. Oncotarget. 2013;4(11):2108-2123.
16. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315-317.
17. Rushworth SA, Zaitseva L, Murray MY, Shah NM, Bowles KM, MacEwan DJ. The high Nrf2 expression in human acute myeloid leukemia is driven by NF-kB and underlies its chemo-resistance. Blood. 2012;120(26):5188-5198.
18. Oellerich T, Oellerich MF, Engelke M, et al. b2 integrin-derived signals induce cell survival and proliferation of AML blasts by activating a Syk/STAT signaling axis. Blood. 2013;121(19): 3889-3899, S1-S66.
19. Rushworth SA, Pillinger G, Abdul-Aziz A, et al. Activity of Bruton's tyrosine-kinase inhibitor ibrutinib in patients with CD117-positive acute myeloid leukaemia: a mechanistic study using patient-derived blast cells. Lancet Haematol. 2015;2(5):e204-e211.
20. Macrae T, Sargeant T, Lemieux S, Hébert J, Deneault E, Sauvageau G. RNA-Seq reveals spliceosome and proteasome genes as most consistent transcripts in human cancer cells. PLoS One. 2013;8(9):e72884.
21. Yang Z, Jones A, Widschwendter M, Teschendorff AE. An integrative pan-cancer-wide analysis of epigenetic enzymes reveals universal patterns of epigenomic deregulation in cancer. Genome Biol. 2015;16:140.
22. Zimmerlin L, Donnenberg VS, Rubin JP, Donnenberg AD. Mesenchymal markers on human adipose stem/progenitor cells. Cytometry A. 2013;83(1):134-140.
23. Marr E, Tardie M, Carty M, et al. Expression, purification, crystallization and structure of human adipocyte lipid-binding protein (aP2). Acta Crystallogr Sect F Struct Biol Cryst Commun. 2006;62(Pt 11):1058-1060.
24. Saavedra P, Girona J, Bosquet A, et al. New insights into circulating FABP4: Interaction with cytokeratin 1 on endothelial cell membranes. Biochim Biophys Acta. 2015;1853(11 Pt A): 2966-2974.
25. Gargiulo CE, Stuhlsatz-Krouper SM, Schaffer JE. Localization of adipocyte long-chain fatty acyl-CoA synthetase at the plasma membrane. J Lipid Res. 1999;40(5):881-892.
26. Schlottmann I, Ehrhart-Bornstein M, Wabitsch M, Bornstein SR, Lamounier-Zepter V. Calcium-dependent release of adipocyte fatty acid binding protein from human adipocytes. Int J Obes. 2014; 38(9):1221-1227.
27. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 1998;17(13):3714-3725.
28. Weis BC, Cowan AT, Brown N, Foster DW, McGarry JD. Use of a selective inhibitor of liver carnitine palmitoyltransferase I (CPT I) allows quantification of its contribution to total CPT I activity in rat heart. Evidence that the dominant cardiac CPT I isoform is identical to the skeletal muscle enzyme. J Biol Chem. 1994;269(42): 26443-26448.
29. Devlin MJ. Why does starvation make bones fat? Am J Hum Biol. 2011;23(5):577-585.
30. Hardaway AL, Herroon MK, Rajagurubandara E, Podgorski I. Bone marrow fat: linking adipocyte-induced inflammation with skeletal metastases. Cancer Metastasis Rev. 2014;33(2-3):527-543.
31. Hotamisligil GS, Bernlohr DA. Metabolic functions of FABPs-mechanisms and therapeutic implications. Nat Rev Endocrinol. 2015;11(10): 592-605.
32. Uehara H, Takahashi T, Oha M, Ogawa H, Izumi K. Exogenous fatty acid binding protein 4 promotes human prostate cancer cell progression. Int J Cancer. 2014;135(11): 2558-2568.
33. Cao H, Sekiya M, Ertunc ME, et al. Adipocyte lipid chaperone AP2 is a secreted adipokine regulating hepatic glucose production. Cell Metab. 2013; 17(5):768-778.
34. Meyer LH, Debatin KM. Diversity of human leukemia xenograft mouse models: implications for disease biology. Cancer Res. 2011;71(23): 7141-7144.
35. Vick B, Rothenberg M, Sandhofer N, et al. An advanced preclinical mouse model for acute myeloid leukemia using patients' cells of various genetic subgroups and in vivo bioluminescence imaging. PLoS One. 2015;10(3):e0120925.
36. Pabst C, Krosl J, Fares I, et al. Identification of small molecules that support human leukemia stem cell activity ex vivo. Nat Methods. 2014; 11(4):436-442.
37. Ye H, Adane B, Khan N, et al. Leukemic stem cells evade chemotherapy by metabolic adaptation to an adipose tissue niche. Cell Stem Cell. 2016;19(1):23-37.
38. Cheng WL, Wang CS, Huang YH, Tsai MM, Liang Y, Lin KH. Overexpression of CXCL1 and its receptor CXCR2 promote tumor invasion in gastric cancer. Ann Oncol. 2011;22(10): 2267-2276.
39. Cheng X, Liu Y, Chu H, Kao H-Y. Promyelocytic leukemia protein (PML) regulates endothelial cell network formation and migration in response to tumor necrosis factor a (TNFa) and interferon a (IFNa). J Biol Chem. 2012;287(28): 23356-23367.
40. Lee K, Kerner J, Hoppel CL. Mitochondrial carnitine palmitoyltransferase 1a (CPT1a) is part of an outer membrane fatty acid transfer complex. J Biol Chem. 2011;286(29):25655-25662.
41. Samudio I, Harmancey R, Fiegl M, et al. Pharmacologic inhibition of fatty acid oxidation sensitizes human leukemia cells to apoptosis induction. J Clin Invest. 2010;120(1):142-156.
42. Ricciardi MR, Mirabilii S, Allegretti M, et al. Targeting the leukemia cell metabolism by the CPT1a inhibition: functional preclinical effects in leukemias. Blood. 2015;126(16):1925-1929.
43. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009;460(7252): 259-263.
44. Scheller EL, Rosen CJ. What's the matter with MAT? Marrow adipose tissue, metabolism, and skeletal health. Ann N Y Acad Sci. 2014;1311: 14-30.