The aryl hydrocarbon receptor nuclear translocator is an essential regulator of murine hematopoietic stem cell viability

Blood

Volumn 125, Issue 21, 2015, Pages 3263-3272

  Krock, Bryan L ^a   Eisinger Mathason, Tzipora S ^a   Giannoukos, Dionysios N ^a,b   Shay, Jessica E ^a   Gohil, Mercy ^a   Lee, David S ^a   Nakazawa, Michael S ^a   Sesen, Julie ^c   Skuli, Nicolas ^c   Simon, M Celeste ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c INSTITUT CLAUDIUS REGAUD   (France)

Author keywords

Arnt promotes adult hematopoietic stem cell viability through regulation of bcl 2 and vegf a expression; Fetal liver hematopoietic progenitors experience hypoxia and loss of hypoxiainduced transcription decreases their survival

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; PROTEIN BCL 2; VASCULOTROPIN A; ARNT PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HIF1A PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DIMERIZATION; FEMALE; FETUS; FETUS LIVER; GENE DELETION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; KNOCKOUT GENE; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL SURVIVAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84943612165     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-10-607267     Document Type: Article

References (48)

1. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008;132(4): 598-611.
2. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012; 481(7382):457-462.
3. 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.
4. Sacchetti B, Funari A, Michienzi S, et al. Selfrenewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131(2):324-336.
5. Suda T, Takubo K, Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell. 2011;9(4):298-310.
6. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129(3): 465-472.
7. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA. 2007;104(13): 5431-5436.
8. Kubota Y, Takubo K, Suda T. Bone marrow long label-retaining cells reside in the sinusoidal hypoxic niche. Biochem Biophys Res Commun. 2008;366(2):335-339.
9. Spencer JA, Ferraro F, Roussakis E, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature. 2014; 508(7495):269-273.
10. Nombela-Arrieta C, Pivarnik G, Winkel B, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol. 2013;15(5):533-543.
11. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270(3):1230-1237.
12. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 1997;11(1):72-82.
13. Wood SM, Gleadle JM, Pugh CW, Hankinson O, Ratcliffe PJ. The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNTdeficient cells. J Biol Chem. 1996;271(25): 15117-15123.
14. Majmundar AJ, Wong WJ, Simon MC. Hypoxiainducible factors and the response to hypoxic stress. Mol Cell. 2010;40(2):294-309.
15. Imanirad P, Solaimani Kartalaei P, Crisan M, et al. HIF1a is a regulator of hematopoietic progenitor and stem cell development in hypoxic sites of the mouse embryo. Stem Cell Res (Amst). 2014; 12(1):24-35.
16. Adelman DM, Maltepe E, Simon MC. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes Dev. 1999;13(19):2478-2483.
17. Ramírez-Bergeron DL, Runge A, Dahl KD, Fehling HJ, Keller G, Simon MC. Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development. 2004;131(18):4623-4634.
18. Ramírez-Bergeron DL, Runge A, Adelman DM, Gohil M, Simon MC. HIF-dependent hematopoietic factors regulate the development of the embryonic vasculature. Dev Cell. 2006;11(1): 81-92.
19. Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC. Acute postnatal ablation of Hif-2alpha results in anemia. Proc Natl Acad Sci USA. 2007;104(7):2301-2306.
20. Rankin EB, Biju MP, Liu Q, et al. Hypoxiainducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest. 2007;117(4): 1068-1077.
21. Takubo K, Goda N, Yamada W, et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell. 2010; 7(3):391-402.
22. Forristal CE, Winkler IG, Nowlan B, Barbier V, Walkinshaw G, Levesque JP. Pharmacologic stabilization of HIF-1a increases hematopoietic stem cell quiescence in vivo and accelerates blood recovery after severe irradiation. Blood. 2013;121(5):759-769.
23. Tomita S, Sinal CJ, Yim SH, Gonzalez FJ. Conditional disruption of the aryl hydrocarbon receptor nuclear translocator (Arnt) gene leads to loss of target gene induction by the aryl hydrocarbon receptor and hypoxia-inducible factor 1alpha. Mol Endocrinol. 2000;14(10): 1674-1681.
24. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 1998;17(11): 3005-3015.
25. Stadtfeld M, Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development. 2005;132(1):203-213.
26. Scortegagna M, Morris MA, Oktay Y, Bennett M, Garcia JA. The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice. Blood. 2003;102(5):1634-1640.
27. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121.
28. Schioppa T, Uranchimeg B, Saccani A, et al. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med. 2003;198(9):1391-1402.
29. Speth JM, Hoggatt J, Singh P, Pelus LM. Pharmacologic increase in HIF1a enhances hematopoietic stem and progenitor homing and engraftment. Blood. 2014;123(2):203-207.
30. Takubo K, Nagamatsu G, Kobayashi CI, et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell. 2013; 12(1):49-61.
31. Rouault-Pierre K, Lopez-Onieva L, Foster K, et al. HIF-2a protects human hematopoietic stem/ progenitors and acute myeloid leukemic cells from apoptosis induced by endoplasmic reticulum stress. Cell Stem Cell. 2013;13(5):549-563.
32. Varia MA, Calkins-Adams DP, Rinker LH, et al. Pimonidazole: a novel hypoxia marker for complementary study of tumor hypoxia and cell proliferation in cervical carcinoma. Gynecol Oncol. 1998;71(2):270-277.
33. Kim I, He S, Yilmaz OH, Kiel MJ, Morrison SJ. Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood. 2006;108(2):737-744.
34. Brugarolas J, Lei K, Hurley RL, et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 2004;18(23):2893-2904.
35. Chen C, Liu Y, Liu R, et al. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med. 2008; 205(10):2397-2408.
36. Gressner AM, Wool IG. The phosphorylation of liver ribosomal proteins in vivo. Evidence that only a single small subunit protein (S6) is phosphorylated. J Biol Chem. 1974;249(21): 6917-6925.
37. Simsek T, Kocabas F, Zheng J, et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell. 2010;7(3):380-390.
38. Singh KP, Garrett RW, Casado FL, Gasiewicz TA. Aryl hydrocarbon receptor-null allele mice have hematopoietic stem/progenitor cells with abnormal characteristics and functions. Stem Cells Dev. 2011;20(5):769-784.
39. Freeland K, Boxer LM, Latchman DS. The cyclic AMP response element in the Bcl-2 promoter confers inducibility by hypoxia in neuronal cells. Brain Res Mol Brain Res. 2001;92(1-2):98-106.
40. Hu J, Van Valckenborgh E, Xu D, et al. Synergistic induction of apoptosis in multiple myeloma cells by bortezomib and hypoxiaactivated prodrug TH-302, in vivo and in vitro. Mol Cancer Ther. 2013;12(9):1763-1773.
41. Hu J, Handisides DR, Van Valckenborgh E, et al. Targeting the multiple myeloma hypoxic niche with TH-302, a hypoxia-activated prodrug. Blood. 2010;116(9):1524-1527.
42. Kocabas F, Zheng J, Thet S, et al. Meis1 regulates the metabolic phenotype and oxidant defense of hematopoietic stem cells. Blood. 2012; 120(25):4963-4972.
43. Guitart AV, Subramani C, Armesilla-Diaz A, et al. Hif-2a is not essential for cell-autonomous hematopoietic stem cell maintenance. Blood. 2013;122(10):1741-1745.
44. Gerber HP, Malik AK, Solar GP, et al. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature. 2002; 417(6892):954-958.
45. Tang N, Wang L, Esko J, et al. Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell. 2004;6(5):485-495.
46. Rehn M, Olsson A, Reckzeh K, et al. Hypoxic induction of vascular endothelial growth factor regulates murine hematopoietic stem cell function in the low-oxygenic niche. Blood. 2011;118(6): 1534-1543.
47. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112(5):645-657.
48. Warr MR, Binnewies M, Flach J, et al. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature. 2013; 494(7437):323-327.