Dlk1 is a negative regulator of emerging hematopoietic stem and progenitor cells

Haematologica

Volumn 98, Issue 2, 2013, Pages 163-171

  Mirshekar Syahkal, Bahar ^a   Haak, Esther ^b   Kimber, Gillian M ^a   van Leusden, Kevin ^b   Harvey, Kirsty ^b   O'Rourke, John ^c   Laborda, Jorge ^d   Bauer, Steven R ^e   de Bruijn, Marella F T R ^c   Ferguson Smith, Anne C ^f   Dzierzak, Elaine ^b   Ottersbach, Katrin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^e CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; IMMUNOGLOBULIN FC FRAGMENT; SEROTONIN 2A AGONIST; TRANSCRIPTION FACTOR RUNX1; DLK1 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; CELL CULTURE; DELTA LIKE HOMOLOGUE 1 GENE; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; GONAD; HEMATOPOIETIC STEM CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESONEPHROS; MOUSE; NONHUMAN; RADIATION DOSE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE; STEM CELL TRANSPLANTATION; ADRENERGIC SYSTEM; ANIMAL; ANIMAL EMBRYO; CELL MEMBRANE; EMBRYOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PROTEIN TRANSPORT; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA; CELL MEMBRANE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; EMBRYO, MAMMALIAN; GENE EXPRESSION; GONADS; HEMATOPOIETIC STEM CELLS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESONEPHROS; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; PROTEIN TRANSPORT; SYMPATHETIC NERVOUS SYSTEM;

EID: 84875325826     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2012.070789     Document Type: Article

References (45)

1. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 1996;86(6):897-906.
2. Medvinsky A, Rybtsov S, Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011;138(6):1017-31.
3. Kumaravelu P, Hook L, Morrison AM, Ure J, Zhao S, Zuyev S, et al. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aortagonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development. 2002;129 (21):4891-9.
4. Mascarenhas MI, Parker A, Dzierzak E, Ottersbach K. Identification of novel regulators of hematopoietic stem cell development through refinement of stem cell localization and expression profiling. Blood. 2009;114 (21):4645-53.
5. Schmidt JV, Matteson PG, Jones BK, Guan XJ, Tilghman SM. The Dlk1 and Gtl2 genes are linked and reciprocally imprinted. Genes Dev. 2000;14(16):1997-2002.
6. Takada S, Tevendale M, Baker J, Georgiades P, Campbell E, Freeman T, et al. Delta-like and gtl2 are reciprocally expressed, differentially methylated linked imprinted genes on mouse chromosome 12. Curr Biol. 2000;10 (18):1135-8.
7. da Rocha ST, Tevendale M, Knowles E, Takada S, Watkins M, Ferguson-Smith AC. Restricted co-expression of Dlk1 and the reciprocally imprinted non-coding RNA, Gtl2: implications for cis-acting control. Dev Biol. 2007;306(2):810-23.
8. Laborda J. The role of the epidermal growth factor-like protein dlk in cell differentiation. Histol Histopathol. 2000;15(1):119-29.
9. Cooper MJ, Hutchins GM, Cohen PS, Helman LJ, Mennie RJ, Israel MA. Human neuroblastoma tumor cell lines correspond to the arrested differentiation of chromaffin adrenal medullary neuroblasts. Cell Growth Differ. 1990;1(4):149-59.
10. Halder SK, Takemori H, Hatano O, Nonaka Y, Wada A, Okamoto M. Cloning of a membrane-spanning protein with epidermal growth factor-like repeat motifs from adrenal glomerulosa cells. Endocrinology. 1998; 139(7):3316-28.
11. Nueda ML, Baladron V, Sanchez-Solana B, Ballesteros MA, Laborda J. The EGF-like protein dlk1 inhibits notch signaling and potentiates adipogenesis of mesenchymal cells. J Mol Biol. 2007;367(5):1281-93.
12. Sakajiri S, O'Kelly J, Yin D, Miller CW, Hofmann WK, Oshimi K, et al. Dlk1 in normal and abnormal hematopoiesis. Leukemia. 2005;19(8):1404-10.
13. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, et al. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood. 2003;101(2):383-9.
14. Chambers SM, Boles NC, Lin KY, Tierney MP, Bowman TV, Bradfute SB, et al. Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell. 2007;1(5):578-91.
15. Komor M, Guller S, Baldus CD, de Vos S, Hoelzer D, Ottmann OG, et al. Transcriptional profiling of human hematopoiesis during in vitro lineage-specific differentiation. Stem Cells. 2005;23(8): 1154-69.
16. Raghunandan R, Ruiz-Hidalgo M, Jia Y, Ettinger R, Rudikoff E, Riggins P, et al. Dlk1 influences differentiation and function of B lymphocytes. Stem Cells Dev. 2008;17(3): 495-507.
17. Moore KA, Pytowski B, Witte L, Hicklin D, Lemischka IR. Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc Natl Acad Sci USA. 1997;94 (8):4011-6.
18. Kaneta M, Osawa M, Sudo K, Nakauchi H, Farr AG, Takahama Y. A role for pref-1 and HES-1 in thymocyte development. J Immunol. 2000;164(1):256-64.
19. Abdallah BM, Boissy P, Tan Q, Dahlgaard J, Traustadottir GA, Kupisiewicz K, et al. dlk1/FA1 regulates the function of human bone marrow mesenchymal stem cells by modulating gene expression of pro-inflammatory cytokines and immune responserelated factors. J Biol Chem. 2007;282 (10):7339-51.
20. Oostendorp RA, Harvey KN, Kusadasi N, de Bruijn MF, Saris C, Ploemacher RE, et al. Stromal cell lines from mouse aorta-gonadsmesonephros subregions are potent supporters of hematopoietic stem cell activity. Blood. 2002;99(4):1183-9.
21. Krogh TN, Bachmann E, Teisner B, Skjodt K, Hojrup P. Glycosylation analysis and protein structure determination of murine fetal antigen 1 (mFA1)--the circulating gene product of the delta-like protein (dlk), preadipocyte factor 1 (Pref-1) and stromal-cell-derived protein 1 (SCP-1) cDNAs. Eur J Biochem. 1997;244(2):334-42.
22. Wang Y, Sul HS. Ectodomain shedding of preadipocyte factor 1 (Pref-1) by tumor necrosis factor alpha converting enzyme (TACE) and inhibition of adipocyte differentiation. Mol Cell Biol. 2006;26(14):5421-35.
23. Smas CM, Chen L, Sul HS. Cleavage of membrane-associated pref-1 generates a soluble inhibitor of adipocyte differentiation. Mol Cell Biol. 1997;17(2):977-88.
24. Moriguchi T, Takako N, Hamada M, Maeda A, Fujioka Y, Kuroha T, et al. Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation. Development. 2006;133(19):3871-81.
25. Durand C, Robin C, Bollerot K, Baron MH, Ottersbach K, Dzierzak E. Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Proc Natl Acad Sci USA. 2007;104(52):20838-43.
26. North T, Gu TL, Stacy T, Wang Q, Howard L, Binder M, et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 1999;126(11):2563-75.
27. Peeters M, Ottersbach K, Bollerot K, Orelio C, de Bruijn M, Wijgerde M, et al. Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development. Development. 2009;136(15): 2613-21.
28. Cai Z, de Bruijn M, Ma X, Dortland B, Luteijn T, Downing RJ, et al. Haploinsufficiency of AML1 affects the temporal and spatial generation of hematopoietic stem cells in the mouse embryo. Immunity. 2000;13(4):423-31.
29. da Rocha ST, Charalambous M, Lin SP, Gutteridge I, Ito Y, Gray D, et al. Gene dosage effects of the imprinted delta-like homologue 1 (dlk1/pref1) in development: implications for the evolution of imprinting. PLoS Genet. 2009;5(2):e1000392.
30. Moon YS, Smas CM, Lee K, Villena JA, Kim KH, Yun EJ, et al. Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol Cell Biol. 2002;22(15):5585-92.
31. Toksoz D, Zsebo KM, Smith KA, Hu S, Brankow D, Suggs SV, et al. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci USA. 1992;89(16):7350-4.
32. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3): 301-13.
33. 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(7308):829-34.
34. Mendes SC, Robin C, Dzierzak E. Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Development. 2005;132(5):1127-36.
35. Ferron SR, Charalambous M, Radford E, McEwen K, Wildner H, Hind E, et al. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature. 2011;475(7356):381-5.
36. Delorme B, Ringe J, Pontikoglou C, Gaillard J, Langonne A, Sensebe L, et al. Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity. Stem Cells. 2009;27(5):1142-51.
37. Baladron V, Ruiz-Hidalgo MJ, Nueda ML, Diaz-Guerra MJ, Garcia-Ramirez JJ, Bonvini E, et al. dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp Cell Res. 2005;303(2):343-59.
38. Bray SJ, Takada S, Harrison E, Shen SC, Ferguson-Smith AC. The atypical mammalian ligand Delta-like homologue 1 (Dlk1) can regulate Notch signalling in Drosophila. BMC Dev Biol. 2008;8:11.
39. Kumano K, Chiba S, Kunisato A, Sata M, Saito T, Nakagami-Yamaguchi E, et al. Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity. 2003;18(5):699-711.
40. Robert-Moreno A, Guiu J, Ruiz-Herguido C, Lopez ME, Ingles-Esteve J, Riera L, et al. Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J. 2008;27(13):1886-95.
41. Ohno N, Izawa A, Hattori M, Kageyama R, Sudo T. dlk inhibits stem cell factor-induced colony formation of murine hematopoietic progenitors: Hes-1-independent effect. Stem Cells. 2001;19(1):71-9.
42. Fleming HE, Janzen V, Lo Celso C, Guo J, Leahy KM, Kronenberg HM, et al. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell. 2008;2(3):274-83.
43. Larsson J, Ohishi M, Garrison B, Aspling M, Janzen V, Adams GB, et al. Nf2/merlin regulates hematopoietic stem cell behavior by altering microenvironmental architecture. Cell Stem Cell. 2008;3(2):221-7.
44. 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. The J Exp Med. 2005;201(11):1781-91.
45. Tanimizu N, Nishikawa M, Saito H, Tsujimura T, Miyajima A. Isolation of hepatoblasts based on the expression of Dlk/Pref- 1. J Cell Sci. 2003;116(Pt 9):1775-86.