FoxO1-dependent induction of acute myeloid leukemia by osteoblasts in mice

Leukemia

Volumn 30, Issue 1, 2016, Pages 1-13

  Kode, A ^a   Mosialou, I ^a   Manavalan, S J ^a   Rathinam, C V ^a   Friedman, R A ^a   Teruya Feldstein, J ^b   Bhagat, G ^a,c   Berman, E ^b   Kousteni, S ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c Memorial Sloan Kettering Cancer Center ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; JAGGED1; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR FKHR; CALCIUM BINDING PROTEIN; CTNNB1 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; JAG1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NOTCH RECEPTOR; PROTEIN JAGGED 1; SERRATE JAGGED PROTEIN; SIGNAL PEPTIDE;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL DIFFERENTIATION; CELL EXPANSION; CELL SPECIFICITY; CELL TRANSFORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE INACTIVATION; HAPLOINSUFFICIENCY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LEUKEMOGENESIS; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANEMIA; ANIMAL; GENETICS; LEUKEMIA, MYELOID, ACUTE; PHYSIOLOGY;

ANEMIA; ANIMALS; BETA CATENIN; CALCIUM-BINDING PROTEINS; FORKHEAD BOX PROTEIN O1; FORKHEAD TRANSCRIPTION FACTORS; HEMATOPOIETIC STEM CELLS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; JAGGED-1 PROTEIN; LEUKEMIA, MYELOID, ACUTE; MEMBRANE PROTEINS; MICE; OSTEOBLASTS; RECEPTORS, NOTCH; SERRATE-JAGGED PROTEINS; SIGNAL TRANSDUCTION;

EID: 84953352790     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2015.161     Document Type: Article

References (60)

1. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010; 466: 829-834.
2. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012; 481: 457-462.
3. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149-161.
4. Lo CC, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009; 457: 92-96.
5. 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: 1109-1121.
6. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977-988.
7. Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT et al. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 2010; 6: 251-264.
8. Winkler IG, Barbier V, Nowlan B, Jacobsen RN, Forristal CE, Patton JT et al. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med 2012; 18: 1651-1657.
9. Levesque JP, Helwani FM, Winkler IG. The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 2010; 24: 1979-1992.
10. Oh IH, Kwon KR. Concise review: multiple niches for hematopoietic stem cell regulations. Stem Cells 2010; 28: 1243-1249.
11. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-846.
12. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836-841.
13. El-Badri NS, Wang BY, Cherry, Good RA. Osteoblasts promote engraftment of allogeneic hematopoietic stem cells. Exp Hematol 1998; 26: 110-116.
14. Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005; 106: 1232-1239.
15. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007; 1: 685-697.
16. Janzen V, Fleming HE, Riedt T, Karlsson G, Riese MJ, Lo CC et al. Hematopoietic stem cell responsiveness to exogenous signals is limited by caspase-3. Cell Stem Cell 2008; 2: 584-594.
17. Mayack SR, Wagers AJ. Osteolineage niche cells initiate hematopoietic stem cell mobilization. Blood 2008; 112: 519-531.
18. Wang LD, Wagers AJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol 2011; 12: 643-655.
19. Chan CK, Chen CC, Luppen CA, Kim JB, DeBoer AT, Wei K et al. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 2009; 457: 490-494.
20. Wu JY, Purton LE, Rodda SJ, Chen M, Weinstein LS, McMahon AP et al. Osteoblastic regulation of B lymphopoiesis is mediated by Gs{alpha}-dependent signaling pathways. Proc Natl Acad Sci USA 2008; 105: 16976-16981.
21. Fulzele K, Krause DS, Panaroni C, Saini V, Barry KJ, Liu X et al. Myelopoiesis is regulated by osteocytes through Gsalpha-dependent signaling. Blood 2013; 121: 930-939.
22. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006; 124: 407-421.
23. Walkley CR, Olsen GH, Dworkin S, Fabb SA, Swann J, McArthur GA et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 2007; 129: 1097-1110.
24. Kim YW, Koo BK, Jeong HW, Yoon MJ, Song R, Shin J et al. Defective Notch activation in microenvironment leads to myeloproliferative disease. Blood 2008; 112: 4628-4638.
25. Raaijmakers MH, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker JA et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 2010; 464: 852-857.
26. Krause DS, Fulzele K, Catic A, Sun CC, Dombkowski D, Hurley MP et al. Differential regulation of myeloid leukemias by the bone marrow microenvironment. Nat Med 2013; 19: 1513-1517.
27. Kode A, Manavalan JS, Mosialou I, Bhagat G, Rathinam CV, Luo N et al. Leukaemogenesis induced by an activating beta-catenin mutation in osteoblasts. Nature 2014; 506: 240-244.
28. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 2005; 308: 1181-1184.
29. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC. Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor-to forkhead box O-mediated transcription. J Biol Chem 2007; 282: 27298-27305.
30. Iyer S, Han L, Bartell SM, Kim HN, Gubrij I, de CR et al. Sirtuin1 (Sirt1) Promotes Cortical Bone Formation by Preventing beta (beta)-Catenin Sequestration by FoxO Transcription Factors in Osteoblast Progenitors. J Biol Chem 2014; 289: 24069-24078.
31. Iyer S, Ambrogini E, Bartell SM, Han L, Roberson PK, de CR et al. FOXOs attenuate bone formation by suppressing Wnt signaling. J Clin Invest 2013; 123: 3409-3419.
32. Sykes SM, Lane SW, Bullinger L, Kalaitzidis D, Yusuf R, Saez B et al. AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias. Cell 2011; 146: 697-708.
33. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007; 128: 309-323.
34. Dacquin R, Starbuck M, Schinke T, Karsenty G. Mouse alpha1(I)-collagen promoter is the best known promoter to drive efficient Cre recombinase expression in osteoblast. Dev Dyn 2002; 224: 245-251.
35. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 1999; 18: 5931-5942.
36. Rached MT, Kode A, Silva BC, Jung DY, Gray S, Ong H et al. FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Invest 2010; 120: 357-368.
37. Pan Y, Lin MH, Tian X, Cheng HT, Gridley T, Shen J et al. gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev Cell 2004; 7: 731-743.
38. de BJ, Williams A, Skavdis G, Harker N, Coles M, Tolaini M et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur J Immunol 2003; 33: 314-325.
39. Rossert J, Eberspaecher H, de CB. Separate cis-acting DNA elements of the mouse pro-alpha 1(I) collagen promoter direct expression of reporter genes to different type I collagen-producing cells in transgenic mice. J Cell Biol 1995; 129: 1421-1432.
40. Kogan SC, Ward JM, Anver MR, Berman JJ, Brayton C, Cardiff RD et al. Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood 2002; 100: 238-245.
41. Cuenco GM, Nucifora G, Ren R. Human AML1/MDS1/EVI1 fusion protein induces an acute myelogenous leukemia (AML) in mice: a model for human AML. Proc Natl Acad Sci USA 2000; 97: 1760-1765.
42. Rached MT, Kode A, Xu L, Yoshikawa Y, Paik JH, DePinho RA et al. FoxO1 is a positive regulator of bone formation by favoring protein synthesis and resistance to oxidative stress in osteoblasts. Cell Metab 2010; 11: 147-160.
43. Ambrogini E, Almeida M, Martin-Millan M, Paik JH, DePinho RA, Han L et al. FoxOmediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab 2010; 11: 136-146.
44. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128: 325-339.
45. Santamaria CM, Chillon MC, Garcia-Sanz R, Perez C, Caballero MD, Ramos F et al. High FOXO3a expression is associated with a poorer prognosis in AML with normal cytogenetics. Leuk Res 2009; 33: 1706-1709.
46. Naka K, Hoshii T, Muraguchi T, Tadokoro Y, Ooshio T, Kondo Y et al. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 2010; 463: 676-680.
47. Zhu J, Garrett R, Jung Y, Zhang Y, Kim N, Wang J et al. Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood 2007; 109: 3706-3712.
48. Taichman RS, Reilly MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells in in vitro bone marrow cultures. Blood 1996; 87: 518-524.
49. Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 2008; 322: 1861-1865.
50. Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grunewald E et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 2005; 201: 1781-1791.
51. Sneddon JB, Werb Z. Location, location, location: the cancer stem cell niche. Cell Stem Cell 2007; 1: 607-611.
52. Miyamoto K, Yoshida S, Kawasumi M, Hashimoto K, Kimura T, Sato Y et al. Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization. J Exp Med 2011; 208: 2175-2181.
53. Lowell CA, Niwa M, Soriano P, Varmus HE. Deficiency of the Hck and Src tyrosine kinases results in extreme levels of extramedullary hematopoiesis. Blood 1996; 87: 1780-1792.
54. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res 1999; 14: 1654-1663.
55. Sugimura R, He XC, Venkatraman A, Arai F, Box A, Semerad C et al. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 2012; 150: 351-365.
56. Schaniel C, Sirabella D, Qiu J, Niu X, Lemischka IR, Moore KA. Wnt-inhibitory factor 1 dysregulation of the bone marrow niche exhausts hematopoietic stem cells. Blood 2011; 118: 2420-2429.
57. Rankin EB, Wu C, Khatri R, Wilson TL, Andersen R, Araldi E et al. The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell 2012; 149: 63-74.
58. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006; 12: 1167-1174.
59. Krause DS, Lazarides K, von Andrian UH, Van Etten RA. Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat Med 2006; 12: 1175-1180.
60. Reynaud D, Pietras E, Barry-Holson K, Mir A, Binnewies M, Jeanne M et al. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 2011; 20: 661-673.