Aryl hydrocarbon receptor inhibition promotes hematolymphoid development from human pluripotent stem cells

Blood

Volumn 129, Issue 26, 2017, Pages 3428-3439

  Angelos, Mathew G ^a   Ruh, Paige N ^a   Webber, Beau R ^a   Blum, Robert H ^b   Ryan, Caitlin D ^a   Bendzick, Laura ^a   Shim, Seonhui ^a,c   Yingst, Ashley M ^a,c   Tufa, Dejene M ^a,c   Verneris, Michael R ^a,c   Kaufman, Dan S ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; CD31 ANTIGEN; CD34 ANTIGEN; CRISPR ASSOCIATED PROTEIN; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 22; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; STEMREGININ 1; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ADAPTIVE IMMUNITY; AMPLICON; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL TRANSFORMATION; CFU COUNTING; CONTROLLED STUDY; EMBRYO; ENDOTHELIAL TO HEMATOPOIETIC TRANSITION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; INNATE IMMUNITY; LYMPHOID CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL EXPANSION; AGONISTS; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; EMBRYONIC STEM CELL; LYMPHOCYTE SUBPOPULATION;

CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; LYMPHOCYTE SUBSETS; PLURIPOTENT STEM CELLS; RECEPTORS, ARYL HYDROCARBON;

EID: 85021716115     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-07-730440     Document Type: Article

References (65)

1. Toscano MG, Navarro-Montero O, Ayllon V, et al. SCL/TAL1-mediated transcriptional network enhances megakaryocytic specification of human embryonic stem cells. Mol Ther. 2015;23(1): 158-170.
2. Woll PS, Morris JK, Painschab MS, et al. Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood. 2008;111(1):122-131.
3. Slukvin II. Deciphering the hierarchy of angiohematopoietic progenitors from human pluripotent stem cells. Cell Cycle. 2013;12(5): 720-727.
4. Hirose S, Takayama N, Nakamura S, et al. Immortalization of erythroblasts by c-MYC and BCL-XL enables large-scale erythrocyte production from human pluripotent stem cells. Stem Cell Rep. 2013;1(6):499-508.
5. Kobari L, Yates F, Oudrhiri N, et al. Human induced pluripotent stem cells can reach complete terminal maturation: In vivo and in vitro evidence in the erythropoietic differentiation model. Haematologica. 2012;97(12):1795-1803.
6. Choi K-D, Vodyanik M, Slukvin II. Hematopoietic differentiation and production of mature myeloid cells from human pluripotent stem cells. Nat Protoc. 2011;6(3):296-313.
7. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD341 cells: Efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105(2):617-626.
8. Chadwick K, Wang L, Li L, et al. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood. 2003; 102(3):906-915.
9. Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci USA. 2001;98(19):10716-10721.
10. Knorr DA, Bock A, Brentjens RJ, Kaufman DS. Engineered human embryonic stem cellderived lymphocytes to study in vivo trafficking and immunotherapy. Stem Cells Dev. 2013; 22(13):1861-1869.
11. Ni Z, Knorr DA, Kaufman DS. Hematopoietic and natural killer cell development from human pluripotent stem cells. Methods Mol Biol. 2013;1029:33-41.
12. Kennedy M, Awong G, Sturgeon CM, et al. T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures. Cell Reports. 2012;2(6):1722-1735.
13. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature. 2010;464(7285):108-111.
14. Zape JP, Zovein AC. Hemogenic endothelium: Origins, regulation, and implications for vascular biology. Semin Cell Dev Biol. 2011;22(9): 1036-1047.
15. Choi K-D, Vodyanik MA, Togarrati PP, et al. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell Reports. 2012;2(3):553-567.
16. Ditadi A, Sturgeon CM, Tober J, et al. Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages. Nat Cell Biol. 2015;17(5):580-591.
17. Lindsey S, Papoutsakis ET. The evolving role of the aryl hydrocarbon receptor (AHR) in the normophysiology of hematopoiesis. Stem Cell Rev. 2012;8(4):1223-1235.
18. Singh KP, Wyman A, Casado FL, Garrett RW, Gasiewicz TA. Treatment of mice with the Ah receptor agonist and human carcinogen dioxin results in altered numbers and function of hematopoietic stem cells. Carcinogenesis. 2009; 30(1):11-19.
19. Smith BW, Rozelle SS, Leung A, et al. The aryl hydrocarbon receptor directs hematopoietic progenitor cell expansion and differentiation. Blood. 2013;122(3):376-385.
20. 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.
21. Boitano AE, Wang J, Romeo R, et al. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science. 2010;329(5997):1345-1348.
22. Wagner JE Jr, Brunstein CG, Boitano AE, et al. Phase I/II trial of StemRegenin-1 expanded umbilical cord blood hematopoietic stem cells supports testing as a stand-alone graft. Cell Stem Cell. 2016;18(1):144-155.
23. Ferrell PI, Xi J, Ma C, Adlakha M, Kaufman DS. The RUNX1 124 enhancer and P1 promoter identify a unique subpopulation of hematopoietic progenitor cells derived from human pluripotent stem cells. Stem Cells. 2015;33(4):1130-1141.
24. Ng ES, Davis R, Stanley EG, Elefanty AG. A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat Protoc. 2008;3(5):768-776.
25. Hermanson DL, Bendzick L, Pribyl L, et al. Induced pluripotent stem cell-derived natural killer cells for treatment of ovarian cancer. Stem Cells. 2016;34(1):93-101.
26. Martin CH, Woll PS, Ni Z, Zúñiga-Pflücker JC, Kaufman DS. Differences in lymphocyte developmental potential between human embryonic stem cell and umbilical cord bloodderived hematopoietic progenitor cells. Blood. 2008;112(7):2730-2737.
27. La Motte-Mohs RN, Herer E, Zúñiga-Pflücker JC. Induction of T-cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro. Blood. 2005;105(4):1431-1439.
28. Kerzee JK, Ramos KS. Constitutive and inducible expression of Cyp1a1 and Cyp1b1 in vascular smooth muscle cells: Role of the Ahr bHLH/PAS transcription factor. Circ Res. 2001;89(7): 573-582.
29. Whitelaw ML, Göttlicher M, Gustafsson JA, Poellinger L. Definition of a novel ligand binding domain of a nuclear bHLH receptor: Colocalization of ligand and hsp90 binding activities within the regulable inactivation domain of the dioxin receptor. EMBO J. 1993;12(11):4169-4179.
30. Whitlock JPJ Jr. Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol. 1999; 39:103-125.
31. Shaw AT, Kim D-W, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013;368(25): 2385-2394.
32. Pollenz RS. The mechanism of AH receptor protein down-regulation (degradation) and its impact on AH receptor-mediated gene regulation. Chem Biol Interact. 2002;141(1-2):41-61.
33. Shimada T, Fujii-Kuriyama Y. Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci. 2004;95(1):1-6.
34. Tian X, Hexum MK, Penchev VR, Taylor RJ, Shultz LD, Kaufman DS. Bioluminescent imaging demonstrates that transplanted human embryonic stem cell-derived CD34(1) cells preferentially develop into endothelial cells. Stem Cells. 2009; 27(11):2675-2685.
35. Bai H, Gao Y, Arzigian M, Wojchowski DM, Wu WS, Wang ZZ. BMP4 regulates vascular progenitor development in human embryonic stem cells through a Smad-dependent pathway. J Cell Biochem. 2010;109(2):363-374.
36. Bai H, Liu Y, Xie Y, et al. Definitive hematopoietic multipotent progenitor cells are transiently generated from hemogenic endothelial cells in human pluripotent stem cells. J Cell Physiol. 2016;231(5):1065-1076.
37. Nakajima-Takagi Y, Osawa M, Oshima M, et al. Role of SOX17 in hematopoietic development from human embryonic stem cells. Blood. 2013; 121(3):447-458.
38. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood. 2006;108(6): 2095-2105.
39. Choi KD, Yu J, Smuga-Otto K, et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells. 2009;27(3):559-567.
40. Gori JL, Butler JM, Chan YY, et al. Vascular niche promotes hematopoietic multipotent progenitor formation from pluripotent stem cells. J Clin Invest. 2015;125(3):1243-1254.
41. Doré LC, Crispino JD. Transcription factor networks in erythroid cell and megakaryocyte development. Blood. 2011;118(2):231-239.
42. Challen GA, Goodell MA. Runx1 isoforms show differential expression patterns during hematopoietic development but have similar functional effects in adult hematopoietic stem cells. Exp Hematol. 2010;38(5):403-416.
43. Soza-Ried C, Hess I, Netuschil N, Schorpp M, Boehm T. Essential role of c-myb in definitive hematopoiesis is evolutionarily conserved. Proc Natl Acad Sci USA. 2010;107(40):17304-17308.
44. Ferreira R, Ohneda K, Yamamoto M, Philipsen S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol. 2005; 25(4):1215-1227.
45. Lohmann F, Bieker JJ. Activation of Eklf expression during hematopoiesis by Gata2 and Smad5 prior to erythroid commitment. Development. 2008;135(12):2071-2082.
46. Boitano AE, Wang J, Romeo R, et al. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science. 2010;329(5997):1345-1348.
47. Roeven MW, Thordardottir S, Kohela A, et al. The aryl hydrocarbon receptor antagonist StemRegenin1 improves in vitro generation of highly functional natural killer cells from CD34(1) hematopoietic stem and progenitor cells. Stem Cells Dev. 2015;24(24):2886-2898.
48. Zhou L. AHR function in lymphocytes: Emerging concepts. Trends Immunol. 2016;37(1):17-31.
49. Julliard W, Fechner JH, Mezrich JD. The aryl hydrocarbon receptor meets immunology: Friend or foe? A little of both. Front Immunol. 2014;5:458.
50. Scoville SD, Mundy-Bosse BL, Zhang MH, et al. A progenitor cell expressing transcription factor RORgt generates all human innate lymphoid cell subsets. Immunity. 2016;44(5):1140-1150.
51. Hazenberg MD, Spits H. Human innate lymphoid cells. Blood. 2014;124(5):700-709.
52. Ahn YO, Blazar BR, Miller JS, Verneris MR. Lineage relationships of human interleukin-22-producing CD561 RORgt1 innate lymphoid cells and conventional natural killer cells. Blood. 2013; 121(12):2234-2243.
53. Yagi R, Zhong C, Northrup DL, et al. The transcription factor GATA3 is critical for the development of all IL-7Ra-expressing innate lymphoid cells. Immunity. 2014;40(3):378-388.
54. Gori JL, Chandrasekaran D, Kowalski JP, et al. Efficient generation, purification, and expansion of CD34(1) hematopoietic progenitor cells from nonhuman primate-induced pluripotent stem cells. Blood. 2012;120(13):e35-e44.
55. Flaveny C, Reen RK, Kusnadi A, Perdew GH. The mouse and human Ah receptor differ in recognition of LXXLL motifs. Arch Biochem Biophys. 2008;471(2):215-223.
56. Flaveny CA, Murray IA, Perdew GH. Differential gene regulation by the human and mouse aryl hydrocarbon receptor. Toxicol Sci. 2010;114(2): 217-225.
57. Forgacs AL, Dere E, Angrish MM, Zacharewski TR. Comparative analysis of temporal and dosedependent TCDD-elicited gene expression in human, mouse, and rat primary hepatocytes. Toxicol Sci. 2013;133(1):54-66.
58. Sturgeon CM, Ditadi A, Awong G, Kennedy M, Keller G. Wnt signaling controls the specification of definitive and primitive hematopoiesis from human pluripotent stem cells. Nat Biotechnol. 2014;32(6):554-561.
59. Kawajiri K, Kobayashi Y, Ohtake F, et al. Aryl hydrocarbon receptor suppresses intestinal carcinogenesis in ApcMin/1 mice with natural ligands. Proc Natl Acad Sci USA. 2009;106(32): 13481-13486.
60. Schneider AJ, Branam AM, Peterson RE. Intersection of AHR and Wnt signaling in development, health, and disease. Int J Mol Sci. 2014;15(10):17852-17885.
61. Singh KP, Bennett JA, Casado FL, Walrath JL, Welle SL, Gasiewicz TA. Loss of aryl hydrocarbon receptor promotes gene changes associated with premature hematopoietic stem cell exhaustion and development of a myeloproliferative disorder in aging mice. Stem Cells Dev. 2014;23(2): 95-106.
62. Montaldo E, Teixeira-Alves LG, Glatzer T, et al. Human RORgt(1)CD34(1) cells are lineagespecified progenitors of group 3 RORgt(1) innate lymphoid cells. Immunity. 2014;41(6):988-1000.
63. Wagage S, Harms Pritchard G, Dawson L, Buza EL, Sonnenberg GF, Hunter CA. The group 3 innate lymphoid cell defect in aryl hydrocarbon receptor deficient mice is associated with T cell hyperactivation during intestinal infection. PLoS One. 2015;10(5):e0128335.
64. Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med. 2015;21(7):698-708.
65. Karrich JJ, Cupedo T. Group 3 innate lymphoid cells in tissue damage and graft-versus-host disease pathogenesis. Curr Opin Hematol. 2016; 23(4):410-415.