Bone Marrow Adipocytes and Hematology: A Literature Review

Nataliia A. Kriventsova, Alexander V. Shestopalov, Galina V. Tereshchenko

 
International Journal of Biomedicine. 2021;11(2):123-130.
DOI: 10.21103/Article11(2)_RA2
Originally published June 5, 2021

Abstract: 

This review focuses on the impact of bone marrow adipocytes on hematopoiesis and the development of hematological diseases. Bone marrow fat is a metabolically active organ capable of accumulating energy required for active hematopoiesis as well as of performing endocrine functions and participating in bone formation. Adipocytes can interact with the surrounding cells both directly and indirectly via cytokines and chemokines. Apart from their active involvement in the normal hematopoiesis, BMA have also been shown to play an important role in such diseases as leukemia, multiple myeloma and aplastic anemia. The role of fat cells in hematopoiesis is still unclear and not well studied, yet it is undoubtedly important, as demonstrated by the ever increasing number of publications supporting this conclusion.

Keywords: 
fat cells • hematopoiesis • leukemia • multiple myeloma • aplastic anemia
References: 

1. Piney A. The anatomy of the bone marrow: with special reference to the distribution of the red marrow. Br Med J. 1922:792-795.
2. Tavassoli M, Crosby WH. Bone marrow histogenesis: a comparison of fatty and red marrow. Science. 1970 Jul 17;169(3942):291-3. doi: 10.1126/science.169.3942.291.
3. Tavassoli M. Ultrastructural development of bone marrow adipose cell. Acta Anat (Basel). 1976;94(1):65-77. doi: 10.1159/000144545.
4. Tavassoli M. Marrow adipose cells. Histochemical identification of labile and stable components. Arch Pathol Lab Med. 1976 Jan;100(1):16-8.
5. Li Y, Meng Y, Yu X. The Unique Metabolic Characteristics of Bone Marrow Adipose Tissue. Front Endocrinol (Lausanne). 2019 Feb 8;10:69. doi: 10.3389/fendo.2019.00069.
6. Burkhardt R, Kettner G, Böhm W, Schmidmeier M, Schlag R, Frisch B, Mallmann B, Eisenmenger W, Gilg T. Changes in trabecular bone, hematopoiesis and bone marrow vessels in aplastic anemia, primary osteoporosis, and old age: a comparative histomorphometric study. Bone. 1987;8(3):157-64. doi: 10.1016/8756-3282(87)90015-9.
7. Wöhrer S, Rabitsch W, Shehata M, Kondo R, Esterbauer H, Streubel B, Sillaber C, Raderer M, Jaeger U, Zielinski C, Valent P. Mesenchymal stem cells in patients with chronic myelogenous leukaemia or bi-phenotypic Ph+ acute leukaemia are not related to the leukaemic clone. Anticancer Res. 2007 Nov-Dec;27(6B):3837-41.
8. Askmyr M, Quach J, Purton LE. Effects of the bone marrow microenvironment on hematopoietic malignancy. Bone. 2011 Jan;48(1):115-20. doi: 10.1016/j.bone.2010.06.003.
9. Cawthorn WP, Scheller EL, Learman BS, Parlee SD, Simon BR, Mori H, Ning X, Bree AJ, Schell B, Broome DT, Soliman SS, DelProposto JL, Lumeng CN, Mitra A, Pandit SV, Gallagher KA, Miller JD, Krishnan V, Hui SK, Bredella MA, Fazeli PK, Klibanski A, Horowitz MC, Rosen CJ, MacDougald OA. Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab. 2014 Aug 5;20(2):368-375. doi: 10.1016/j.cmet.2014.06.003.
10. Hardaway AL, Herroon MK, Rajagurubandara E, Podgorski I. Bone marrow fat: linking adipocyte-induced inflammation with skeletal metastases. Cancer Metastasis Rev. 2014 Sep;33(2-3):527-43. doi: 10.1007/s10555-013-9484-y.
11. Karampinos DC, Ruschke S, Dieckmeyer M, Diefenbach M, Franz D, Gersing AS, Krug R, Baum T. Quantitative MRI and spectroscopy of bone marrow. J Magn Reson Imaging. 2018 Feb;47(2):332-353. doi: 10.1002/jmri.25769.
12. Veldhuis-Vlug AG, Rosen CJ. Clinical implications of bone marrow adiposity. J Intern Med. 2018 Feb;283(2):121-139. doi: 10.1111/joim.12718.
13. EMERY JL, FOLLETT GF. REGRESSION OF BONE-MARROW HAEMOPOIESIS FROM THE TERMINAL DIGITS IN THE FOETUS AND INFANT. Br J Haematol. 1964 Oct;10:485-9. doi: 10.1111/j.1365-2141.1964.tb00725.x.
14. Custer RP, Ahlfeldt FE. Studies on the structure and function of bone marrow: II. Variations in cellularity in various bones with advancing years of life and their relative response to stimuli. J Lab Clin Med. 1932;17(10):960-962.
15. Ono N, Kronenberg HM. Mesenchymal progenitor cells for the osteogenic lineage. Curr Mol Biol Rep. 2015 Sep;1(3):95-100. doi: 10.1007/s40610-015-0017-z.
16. Wend K, Wend P, Drew BG, Hevener AL, Miranda-Carboni GA, Krum SA. ERα regulates lipid metabolism in bone through ATGL and perilipin. J Cell Biochem. 2013 Jun;114(6):1306-14. doi: 10.1002/jcb.24470.
17. Okazaki R, Inoue D, Shibata M, Saika M, Kido S, Ooka H, Tomiyama H, Sakamoto Y, Matsumoto T. Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology. 2002 Jun;143(6):2349-56. doi: 10.1210/endo.143.6.8854.
18. Fan Y, Hanai JI, Le PT, Bi R, Maridas D, DeMambro V, Figueroa CA, Kir S, Zhou X, Mannstadt M, Baron R, Bronson RT, Horowitz MC, Wu JY, Bilezikian JP, Dempster DW, Rosen CJ, Lanske B. Parathyroid Hormone Directs Bone Marrow Mesenchymal Cell Fate. Cell Metab. 2017 Mar 7;25(3):661-672. doi: 10.1016/j.cmet.2017.01.001.
19. Griffith JF, Yeung DK, Ma HT, Leung JC, Kwok TC, Leung PC. Bone marrow fat content in the elderly: a reversal of sex difference seen in younger subjects. J Magn Reson Imaging. 2012 Jul;36(1):225-30. doi: 10.1002/jmri.23619.
20. Naot D, Musson DS, Cornish J. The Activity of Adiponectin in Bone. Calcif Tissue Int. 2017 May;100(5):486-499. doi: 10.1007/s00223-016-0216-5.
21. Masamoto Y, Arai S, Sato T, Kubota N, Takamoto I, Kadowaki T, Kurokawa M. Adiponectin Enhances Quiescence Exit of Murine Hematopoietic Stem Cells and Hematopoietic Recovery Through mTORC1 Potentiation. Stem Cells. 2017 Jul;35(7):1835-1848. doi: 10.1002/stem.2640.
22. Zhou BO, Yu H, Yue R, Zhao Z, Rios JJ, Naveiras O, Morrison SJ. Bone marrow adipocytes promote the regeneration of stem cells and haematopoiesis by secreting SCF. Nat Cell Biol. 2017 Aug;19(8):891-903. doi: 10.1038/ncb3570.
23. Mattiucci D, Maurizi G, Izzi V, Cenci L, Ciarlantini M, Mancini S, Mensà E, Pascarella R, Vivarelli M, Olivieri A, Leoni P, Poloni A. Bone marrow adipocytes support hematopoietic stem cell survival. J Cell Physiol. 2018 Feb;233(2):1500-1511. doi: 10.1002/jcp.26037.
24. Gasparrini M, Rivas D, Elbaz A, Duque G. Differential expression of cytokines in subcutaneous and marrow fat of aging C57BL/6J mice. Exp Gerontol. 2009 Sep;44(9):613-8. doi: 10.1016/j.exger.2009.05.009.
25. Elbaz A, Wu X, Rivas D, Gimble JM, Duque G. Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro. J Cell Mol Med. 2010 Apr;14(4):982-91. doi: 10.1111/j.1582-4934.2009.00751.x.
26. Bennett BD, Solar GP, Yuan JQ, Mathias J, Thomas GR, Matthews W. A role for leptin and its cognate receptor in hematopoiesis. Curr Biol. 1996 Sep 1;6(9):1170-80. doi: 10.1016/s0960-9822(02)70684-2.
27. Diedrich JD, Rajagurubandara E, Herroon MK, Mahapatra G, Hüttemann M, Podgorski I. Bone marrow adipocytes promote the Warburg phenotype in metastatic prostate tumors via HIF-1α activation. Oncotarget. 2016 Oct 4;7(40):64854-64877. doi: 10.18632/oncotarget.11712.
28. Lassailly F, Foster K, Lopez-Onieva L, Currie E, Bonnet D. Multimodal imaging reveals structural and functional heterogeneity in different bone marrow compartments: functional implications on hematopoietic stem cells. Blood. 2013 Sep 5;122(10):1730-40. doi: 10.1182/blood-2012-11-467498.
29. Robles H, Park S, Joens MS, Fitzpatrick JAJ, Craft CS, Scheller EL. Characterization of the bone marrow adipocyte niche with three-dimensional electron microscopy. Bone. 2019 Jan;118:89-98. doi: 10.1016/j.bone.2018.01.020.
30. DiMascio L, Voermans C, Uqoezwa M, Duncan A, Lu D, Wu J, Sankar U, Reya T. Identification of adiponectin as a novel hemopoietic stem cell growth factor. J Immunol. 2007 Mar 15;178(6):3511-20. doi: 10.4049/jimmunol.178.6.3511.
31. Dias CC, Nogueira-Pedro A, Tokuyama PY, Martins MN, Segreto HR, Buri MV, Miranda A, Paredes-Gamero EJ. A synthetic fragment of leptin increase hematopoietic stem cell population and improve its engraftment ability. J Cell Biochem. 2015 Jul;116(7):1334-40. doi: 10.1002/jcb.25090.
32. Claycombe K, King LE, Fraker PJ. A role for leptin in sustaining lymphopoiesis and myelopoiesis. Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2017-21. doi: 10.1073/pnas.0712053105.
33. Poloni A, Maurizi G, Serrani F, Mancini S, Zingaretti MC, Frontini A, Cinti S, Olivieri A, Leoni P. Molecular and functional characterization of human bone marrow adipocytes. Exp Hematol. 2013 Jun;41(6):558-566.e2. doi: 10.1016/j.exphem.2013.02.005.
34. Shimozato T, Kincade PW. Prostaglandin E(2) and stem cell factor can deliver opposing signals to B lymphocyte precursors. Cell Immunol. 1999 Nov 25;198(1):21-9. doi: 10.1006/cimm.1999.1575.
35. Bilwani FA, Knight KL. Adipocyte-derived soluble factor(s) inhibits early stages of B lymphopoiesis. J Immunol. 2012 Nov 1;189(9):4379-86. doi: 10.4049/jimmunol.1201176.
36. Kennedy DE, Knight KL. Inhibition of B Lymphopoiesis by Adipocytes and IL-1-Producing Myeloid-Derived Suppressor Cells. J Immunol. 2015 Sep 15;195(6):2666-74. doi: 10.4049/jimmunol.1500957.
37. Kennedy DE, Knight KL. Inflammatory Changes in Bone Marrow Microenvironment Associated with Declining B Lymphopoiesis. J Immunol. 2017 May 1;198(9):3471-3479. doi: 10.4049/jimmunol.1601643.
38. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011 Feb;17(2):179-88. doi: 10.1038/nm.2279.
39. Salminen A, Kaarniranta K, Kauppinen A. Inflammaging: disturbed interplay between autophagy and inflammasomes. Aging (Albany NY). 2012 Mar;4(3):166-75. doi: 10.18632/aging.100444.
40. Youm YH, Kanneganti TD, Vandanmagsar B, Zhu X, Ravussin A, Adijiang A, Owen JS, Thomas MJ, Francis J, Parks JS, Dixit VD. The Nlrp3 inflammasome promotes age-related thymic demise and immunosenescence. Cell Rep. 2012 Jan 26;1(1):56-68. doi: 10.1016/j.celrep.2011.11.005.
41. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009 Jul 9;460(7252):259-63. doi: 10.1038/nature08099.
42. Baker AH, Wu TH, Bolt AM, Gerstenfeld LC, Mann KK, Schlezinger JJ. From the Cover: Tributyltin Alters the Bone Marrow Microenvironment and Suppresses B Cell Development. Toxicol Sci. 2017 Jul 1;158(1):63-75. doi: 10.1093/toxsci/kfx067.
43. Umemoto Y, Tsuji K, Yang FC, Ebihara Y, Kaneko A, Furukawa S, Nakahata T. Leptin stimulates the proliferation of murine myelocytic and primitive hematopoietic progenitor cells. Blood. 1997 Nov 1;90(9):3438-43.
44. Laharrague P, Oppert JM, Brousset P, Charlet JP, Campfield A, Fontanilles AM, Guy-Grand B, Corberand JX, Pénicaud L, Casteilla L. High concentration of leptin stimulates myeloid differentiation from human bone marrow CD34+ progenitors: potential involvement in leukocytosis of obese subjects. Int J Obes Relat Metab Disord. 2000 Sep;24(9):1212-6. doi: 10.1038/sj.ijo.0801377.
45. Manwani D, Bieker JJ. The erythroblastic island. Curr Top Dev Biol. 2008;82:23-53. doi: 10.1016/S0070-2153(07)00002-6.
46. Bathija A, Davis S, Trubowitz S. Marrow adipose tissue: response to erythropoiesis. Am J Hematol. 1978;5(4):315-21. doi: 10.1002/ajh.2830050406.
47. Suresh S, Alvarez JC, Noguchi CT. Erythropoietin eliminates increased bone marrow adiposity and alters bone features in obese mice. Blood. 2017; 130 (Suppl 1):3778-3778.
48. Wang H, Leng Y, Gong Y. Bone Marrow Fat and Hematopoiesis. Front Endocrinol (Lausanne). 2018 Nov 28;9:694. doi: 10.3389/fendo.2018.00694.
49. Battula VL, Chen Y, Cabreira Mda G, Ruvolo V, Wang Z, Ma W, Konoplev S, Shpall E, Lyons K, Strunk D, Bueso-Ramos C, Davis RE, Konopleva M, Andreeff M. Connective tissue growth factor regulates adipocyte differentiation of mesenchymal stromal cells and facilitates leukemia bone marrow engraftment. Blood. 2013 Jul 18;122(3):357-66. doi: 10.1182/blood-2012-06-437988.
50. Butturini AM, Dorey FJ, Lange BJ, Henry DW, Gaynon PS, Fu C, Franklin J, Siegel SE, Seibel NL, Rogers PC, Sather H, Trigg M, Bleyer WA, Carroll WL. Obesity and outcome in pediatric acute lymphoblastic leukemia. J Clin Oncol. 2007 May 20;25(15):2063-9. doi: 10.1200/JCO.2006.07.7792.
51. Styner M, Thompson WR, Galior K, Uzer G, Wu X, Kadari S, Case N, Xie Z, Sen B, Romaine A, Pagnotti GM, Rubin CT, Styner MA, Horowitz MC, Rubin J. Bone marrow fat accumulation accelerated by high fat diet is suppressed by exercise. Bone. 2014 Jul;64:39-46. doi: 10.1016/j.bone.2014.03.044.
52. Scheller EL, Khoury B, Moller KL, Wee NK, Khandaker S, Kozloff KM, Abrishami SH, Zamarron BF, Singer K. Changes in Skeletal Integrity and Marrow Adiposity during High-Fat Diet and after Weight Loss. Front Endocrinol (Lausanne). 2016 Jul 27;7:102. doi: 10.3389/fendo.2016.00102.
53. Doucette CR, Horowitz MC, Berry R, MacDougald OA, Anunciado-Koza R, Koza RA, Rosen CJ. A High Fat Diet Increases Bone Marrow Adipose Tissue (MAT) But Does Not Alter Trabecular or Cortical Bone Mass in C57BL/6J Mice. J Cell Physiol. 2015 Sep;230(9):2032-7. doi: 10.1002/jcp.24954.
54. T Tabe Y, Konopleva M, Munsell MF, Marini FC, Zompetta C, McQueen T, Tsao T, Zhao S, Pierce S, Igari J, Estey EH, Andreeff M. PML-RARalpha is associated with leptin-receptor induction: the role of mesenchymal stem cell-derived adipocytes in APL cell survival. Blood. 2004 Mar 1;103(5):1815-22. doi: 10.1182/blood-2003-03-0802.
55. Sheng X, Tucci J, Parmentier JH, Ji L, Behan JW, Heisterkamp N, Mittelman SD. Adipocytes cause leukemia cell resistance to daunorubicin via oxidative stress response. Oncotarget. 2016 Nov 8;7(45):73147-73159. doi: 10.18632/oncotarget.12246.
56. Behan JW, Yun JP, Proektor MP, Ehsanipour EA, Arutyunyan A, Moses AS, Avramis VI, Louie SG, Butturini A, Heisterkamp N, Mittelman SD. Adipocytes impair leukemia treatment in mice. Cancer Res. 2009 Oct 1;69(19):7867-74. doi: 10.1158/0008-5472.CAN-09-0800.
57. Frączak E, Olbromski M, Piotrowska A, Glatzel-Plucińska N, Dzięgiel P, Dybko J, Kuliczkowski K, Wróbel T. Bone marrow adipocytes in haematological malignancies. Acta Histochem. 2018 Jan;120(1):22-27. doi: 10.1016/j.acthis.2017.10.010.
58. Tung S, Shi Y, Wong K, Zhu F, Gorczynski R, Laister RC, Minden M, Blechert AK, Genzel Y, Reichl U, Spaner DE. PPARα and fatty acid oxidation mediate glucocorticoid resistance in chronic lymphocytic leukemia. Blood. 2013 Aug 8;122(6):969-80. doi: 10.1182/blood-2013-03-489468.
59. Shafat MS, Oellerich T, Mohr S, Robinson SD, Edwards DR, Marlein CR, Piddock RE, Fenech M, Zaitseva L, Abdul-Aziz A, Turner J, Watkins JA, Lawes M, Bowles KM, Rushworth SA. Leukemic blasts program bone marrow adipocytes to generate a protumoral microenvironment. Blood. 2017 Mar 9;129(10):1320-1332. doi: 10.1182/blood-2016-08-734798.
60. Han TJ, Wang X. Leptin and its receptor in hematologic malignancies. Int J Clin Exp Med. 2015 Nov 15;8(11):19840-9.
61. Gorska E, Popko K, Wasik M. Leptin receptor in childhood acute leukemias. Adv Exp Med Biol. 2013;756:155-61. doi: 10.1007/978-94-007-4549-0_20.
62. Yokota T, Oritani K, Takahashi I, Ishikawa J, Matsuyama A, Ouchi N, Kihara S, Funahashi T, Tenner AJ, Tomiyama Y, Matsuzawa Y. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood. 2000 Sep 1;96(5):1723-32.
63. Diaz-Blanco E, Bruns I, Neumann F, Fischer JC, Graef T, Rosskopf M, Brors B, Pechtel S, Bork S, Koch A, Baer A, Rohr UP, Kobbe G, von Haeseler A, Gattermann N, Haas R, Kronenwett R. Molecular signature of CD34(+) hematopoietic stem and progenitor cells of patients with CML in chronic phase. Leukemia. 2007 Mar;21(3):494-504. doi: 10.1038/sj.leu.2404549.
64. Beaulieu A, Poncin G, Belaid-Choucair Z, Humblet C, Bogdanovic G, Lognay G, Boniver J, Defresne MP. Leptin reverts pro-apoptotic and antiproliferative effects of α-linolenic acids in BCR-ABL positive leukemic cells: involvement of PI3K pathway. PLoS One. 2011;6(10):e25651. doi: 10.1371/journal.pone.0025651. E
65. Rozovski U, Hazan-Halevy I, Barzilai M, Keating MJ, Estrov Z. Metabolism pathways in chronic lymphocytic leukemia. Leuk Lymphoma. 2016;57(4):758-65. doi: 10.3109/10428194.2015.1106533.
66. Rozovski U, Grgurevic S, Bueso-Ramos C, Harris DM, Li P, Liu Z, Wu JY, Jain P, Wierda W, Burger J, O'Brien S, Jain N, Ferrajoli A, Keating MJ, Estrov Z. Aberrant LPL Expression, Driven by STAT3, Mediates Free Fatty Acid Metabolism in CLL Cells. Mol Cancer Res. 2015 May;13(5):944-53. doi: 10.1158/1541-7786.MCR-14-0412.
67. Ruby MA, Goldenson B, Orasanu G, Johnston TP, Plutzky J, Krauss RM. VLDL hydrolysis by LPL activates PPAR-alpha through generation of unbound fatty acids. J Lipid Res. 2010 Aug;51(8):2275-81. doi: 10.1194/jlr.M005561.
68. Caers J, Deleu S, Belaid Z, De Raeve H, Van Valckenborgh E, De Bruyne E, Defresne MP, Van Riet I, Van Camp B, Vanderkerken K. Neighboring adipocytes participate in the bone marrow microenvironment of multiple myeloma cells. Leukemia. 2007 Jul;21(7):1580-4. doi: 10.1038/sj.leu.2404658.
69. Pang J, Shi Q, Liu Z, He J, Liu H, Lin P, Cui J, Yang J. Resistin induces multidrug resistance in myeloma by inhibiting cell death and upregulating ABC transporter expression. Haematologica. 2017 Jul;102(7):1273-1280. doi: 10.3324/haematol.2016.154062.
70. Liu Z, Xu J, He J, Liu H, Lin P, Wan X, Navone NM, Tong Q, Kwak LW, Orlowski RZ, Yang J. Mature adipocytes in bone marrow protect myeloma cells against chemotherapy through autophagy activation. Oncotarget. 2015 Oct 27;6(33):34329-41. doi: 10.18632/oncotarget.6020.
71. Fain JN, Cheema PS, Bahouth SW, Lloyd Hiler M. Resistin release by human adipose tissue explants in primary culture. Biochem Biophys Res Commun. 2003 Jan 17;300(3):674-8. doi: 10.1016/s0006-291x(02)02864-4. Erratum in: Biochem Biophys Res Commun. 2003 Mar 21;302(4):917-8.
72. Shipounova IN, Petrova TV, Svinareva DA, Momotuk KS, Mikhailova EA, Drize NI. Alterations in hematopoietic microenvironment in patients with aplastic anemia. Clin Transl Sci. 2009 Feb;2(1):67-74. doi: 10.1111/j.1752-8062.2008.00074.x.
73. Chen YH, Yeh FL, Yeh SP, Ma HT, Hung SC, Hung MC, Li LY. Myocyte enhancer factor-2 interacting transcriptional repressor (MITR) is a switch that promotes osteogenesis and inhibits adipogenesis of mesenchymal stem cells by inactivating peroxisome proliferator-activated receptor gamma-2. J Biol Chem. 2011 Mar 25;286(12):10671-80. doi: 10.1074/jbc.M110.199612.
74. Hoshiba T, Kawazoe N, Chen G. The balance of osteogenic and adipogenic differentiation in human mesenchymal stem cells by matrices that mimic stepwise tissue development. Biomaterials. 2012 Mar;33(7):2025-31. doi: 10.1016/j.biomaterials.2011.11.061.
75. Tripathy NK, Singh SP, Nityanand S. Enhanced adipogenicity of bone marrow mesenchymal stem cells in aplastic anemia. Stem Cells Int. 2014;2014:276862. doi: 10.1155/2014/276862.
76. Zhao J, Wang C, Song Y, Fang B. Arsenic trioxide and microRNA-204 display contrary effects on regulating adipogenic and osteogenic differentiation of mesenchymal stem cells in aplastic anemia. Acta Biochim Biophys Sin (Shanghai). 2014 Oct;46(10):885-93. doi: 10.1093/abbs/gmu082.
77. Fujimaki S, Harigae H, Sugawara T, Takasawa N, Sasaki T, Kaku M. Decreased expression of transcription factor GATA-2 in haematopoietic stem cells in patients with aplastic anaemia. Br J Haematol. 2001 Apr;113(1):52-7. doi: 10.1046/j.1365-2141.2001.02736.x.
78. Zeng W, Chen G, Kajigaya S, Nunez O, Charrow A, Billings EM, Young NS. Gene expression profiling in CD34 cells to identify differences between aplastic anemia patients and healthy volunteers. Blood. 2004 Jan 1;103(1):325-32. doi: 10.1182/blood-2003-02-0490.
79. Tong Q, Tsai J, Hotamisligil GS. GATA transcription factors and fat cell formation. Drug News Perspect. 2003 Nov;16(9):585-8. doi: 10.1358/dnp.2003.16.9.829340.

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