Endothelial Jagged-1 Is necessary for homeostatic and regenerative hematopoiesis

Cell Reports

Volumn 4, Issue 5, 2013, Pages 1022-1034

  Poulos, MichaelG ^a   Guo, Peipei ^a   Kofler, NatalieM ^b   Pinho, Sandra ^c   Gutkin, MichaelC ^a   Tikhonova, Anastasia ^d   Aifantis, Iannis ^d   Frenette, PaulS ^c   Kitajewski, Jan ^b   Rafii, Shahin ^a,d   Butler, JasonM ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; JAGGED1; NOTCH RECEPTOR; VASCULAR ENDOTHELIAL CADHERIN;

ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL EXPANSION; CELL REGENERATION; CELL RENEWAL; ENDOTHELIUM CELL; EXON; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL NICHE; VASCULAR SMOOTH MUSCLE;

MUS;

ANIMALS; CALCIUM-BINDING PROTEINS; ENDOTHELIAL CELLS; HEMATOPOIESIS; HOMEOSTASIS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 84884157062     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.048     Document Type: Article

References (49)

1. Adams G.B., Chabner K.T., Alley I.R., Olson D.P., Szczepiorkowski Z.M., Poznansky M.C., Kos C.H., Pollak M.R., Brown E.M., Scadden D.T. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006, 439:599-603.
2. Benedito R., Roca C., Sörensen I., Adams S., Gossler A., Fruttiger M., Adams R.H. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 2009, 137:1124-1135.
3. Butler J.M., Nolan D.J., Vertes E.L., Varnum-Finney B., Kobayashi H., Hooper A.T., Seandel M., Shido K., White I.A., Kobayashi M., 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.
4. Calvi L.M., Adams G.B., Weibrecht K.W., Weber J.M., Olson D.P., Knight M.C., Martin R.P., Schipani E., Divieti P., Bringhurst F.R., et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
5. Ding L., Morrison S.J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013, 495:231-235.
6. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481:457-462.
7. Duncan A.W., Rattis F.M., DiMascio L.N., Congdon K.L., Pazianos G., Zhao C., Yoon K., Cook J.M., Willert K., Gaiano N., Reya T. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 2005, 6:314-322.
8. Fehrenbach M.L., Cao G., Williams J.T., Finklestein J.M., Delisser H.M. Isolation of murine lung endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296:L1096-L1103.
9. Fre S., Hannezo E., Sale S., Huyghe M., Lafkas D., Kissel H., Louvi A., Greve J., Louvard D., Artavanis-Tsakonas S. Notch lineages and activity in intestinal stem cells determined by a new set of knock-in mice. PLoS ONE 2011, 6:e25785.
10. Frenette P.S., Pinho S., Lucas D., Scheiermann C. Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu. Rev. Immunol. 2013, 31:285-316.
11. Harrison D.E. Competitive repopulation: a new assay for long-term stem cell functional capacity. Blood 1980, 55:77-81.
12. High F.A., Lu M.M., Pear W.S., Loomes K.M., Kaestner K.H., Epstein J.A. Endothelial expression of the Notch ligand Jagged1 is required forvascular smooth muscle development. Proc. Natl. Acad. Sci. USA 2008, 105:1955-1959.
13. Hilton M.J., Tu X., Wu X., Bai S., Zhao H., Kobayashi T., Kronenberg H.M., Teitelbaum S.L., Ross F.P., Kopan R., Long F. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat. Med. 2008, 14:306-314.
14. Himburg H.A., Muramoto G.G., Daher P., Meadows S.K., Russell J.L., Doan P., Chi J.T., Salter A.B., Lento W.E., Reya T., et al. Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat. Med. 2010, 16:475-482.
15. Hofmann J.J., Briot A., Enciso J., Zovein A.C., Ren S., Zhang Z.W., Radtke F., Simons M., Wang Y., Iruela-Arispe M.L. Endothelial deletion of murine Jag1 leads to valve calcification and congenital heart defects associated with Alagille syndrome. Development 2012, 139:4449-4460.
16. Hooper A.T., Butler J.M., Nolan D.J., Kranz A., Iida K., Kobayashi M., Kopp H.G., Shido K., Petit I., Yanger K., et al. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 2009, 4:263-274.
17. Hsieh J.J., Zhou S., Chen L., Young D.B., Hayward S.D. CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proc. Natl. Acad. Sci. USA 1999, 96:23-28.
18. Kao H.Y., Ordentlich P., Koyano-Nakagawa N., Tang Z., Downes M., Kintner C.R., Evans R.M., Kadesch T. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 1998, 12:2269-2277.
19. Karanu F.N., Murdoch B., Gallacher L., Wu D.M., Koremoto M., Sakano S., Bhatia M. The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J.Exp. Med. 2000, 192:1365-1372.
20. Kim I., Yilmaz O.H., Morrison S.J. CD144 (VE-cadherin) is transiently expressed by fetal liver hematopoietic stem cells. Blood 2005, 106:903-905.
21. Kobayashi H., Butler J.M., O'Donnell R., Kobayashi M., Ding B.S., Bonner B., Chiu V.K., Nolan D.J., Shido K., Benjamin L., Rafii S. Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat. Cell Biol. 2010, 12:1046-1056.
22. Lai E.C. Keeping a good pathway down: transcriptional repression of Notch pathway target genes by CSL proteins. EMBO Rep. 2002, 3:840-845.
23. Lambeng N., Wallez Y., Rampon C., Cand F., Christé G., Gulino-Debrac D., Vilgrain I., Huber P. Vascular endothelial-cadherin tyrosine phosphorylation in angiogenic and quiescent adult tissues. Circ. Res. 2005, 96:384-391.
24. Lapidot T., Dar A., Kollet O. How do stem cells find their way home?. Blood 2005, 106:1901-1910.
25. Lo Celso C., Fleming H.E., Wu J.W., Zhao C.X., Miake-Lye S., Fujisaki J., CÔté D., Rowe D.W., Lin C.P., Scadden D.T. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009, 457:92-96.
26. Loomes K.M., Russo P., Ryan M., Nelson A., Underkoffler L., Glover C., Fu H., Gridley T., Kaestner K.H., Oakey R.J. Bile duct proliferation in liver-specific Jag1 conditional knockout mice: effects of gene dosage. Hepatology 2007, 45:323-330.
27. Maillard I., Koch U., Dumortier A., Shestova O., Xu L., Sai H., Pross S.E., Aster J.C., Bhandoola A., Radtke F., Pear W.S. Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2008, 2:356-366.
28. Mancini S.J., Mantei N., Dumortier A., Suter U., MacDonald H.R., Radtke F. Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood 2005, 105:2340-2342.
29. Méndez-Ferrer S., Michurina T.V., Ferraro F., Mazloom A.R., Macarthur B.D., Lira S.A., Scadden D.T., Ma'ayan A., Enikolopov G.N., Frenette P.S. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466:829-834.
30. Morrison S.J., Spradling A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132:598-611.
31. Nagel A.C., Krejci A., Tenin G., Bravo-Patiño A., Bray S., Maier D., Preiss A. Hairless-mediated repression of notch target genes requires the combined activity of Groucho and CtBP corepressors. Mol. Cell. Biol. 2005, 25:10433-10441.
32. Nilsson S.K., Johnston H.M., Whitty G.A., Williams B., Webb R.J., Denhardt D.T., Bertoncello I., Bendall L.J., Simmons P.J., Haylock D.N. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005, 106:1232-1239.
33. Oh P., Lobry C., Gao J., Tikhonova A., Loizou E., Manent J., van Handel B., Ibrahim S., Greve J., Mikkola H., et al. Invivo mapping of notch pathway activity in normal and stress hematopoiesis. Cell Stem Cell 2013, 13:190-204.
34. Oyama T., Harigaya K., Muradil A., Hozumi K., Habu S., Oguro H., Iwama A., Matsuno K., Sakamoto R., Sato M., et al. Mastermind-1 is required for Notch signal-dependent steps in lymphocyte development invivo. Proc. Natl. Acad. Sci. USA 2007, 104:9764-9769.
35. Oyama T., Harigaya K., Sasaki N., Okamura Y., Kokubo H., Saga Y., Hozumi K., Suganami A., Tamura Y., Nagase T., et al. Mastermind-like 1 (MamL1) and mastermind-like 3 (MamL3) are essential for Notch signaling invivo. Development 2011, 138:5235-5246.
36. Papayannopoulou T., Craddock C. Homing and trafficking of hemopoietic progenitor cells. Acta Haematol. 1997, 97:97-104.
37. Pinho S., Oliveira A., Costa I., Gouveia C.A., Carvalho F., Moreira R.F., Dinis-Oliveira R.J. Simultaneous quantification of tramadol and O-desmethyltramadol in hair samples by gas chromatography-electron impact/mass spectrometry. Biomed. Chromatogr. 2013, 27:1003-1011.
38. Robert-Moreno A., Guiu J., Ruiz-Herguido C., López M.E., Inglés-Esteve J., Riera L., Tipping A., Enver T., Dzierzak E., Gridley T., et al. Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J. 2008, 27:1886-1895.
39. Stier S., Cheng T., Dombkowski D., Carlesso N., Scadden D.T. Notch1 activation increases hematopoietic stem cell self-renewal invivo and favors lymphoid over myeloid lineage outcome. Blood 2002, 99:2369-2378.
40. 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.
41. Szilvassy S.J., Humphries R.K., Lansdorp P.M., Eaves A.C., Eaves C.J. Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc. Natl. Acad. Sci. USA 1990, 87:8736-8740.
42. Varnum-Finney B., Purton L.E., Yu M., Brashem-Stein C., Flowers D., Staats S., Moore K.A., Le Roux I., Mann R., Gray G., et al. The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood 1998, 91:4084-4091.
43. Varnum-Finney B., Xu L., Brashem-Stein C., Nourigat C., Flowers D., Bakkour S., Pear W.S., Bernstein I.D. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 2000, 6:1278-1281.
44. Varnum-Finney B., Halasz L.M., Sun M., Gridley T., Radtke F., Bernstein I.D. Notch2 governs the rate of generation of mouse long- and short-term repopulating stem cells. J.Clin. Invest. 2011, 121:1207-1216.
45. Wu L., Maillard I., Nakamura M., Pear W.S., Griffin J.D. The transcriptional coactivator Maml1 is required for Notch2-mediated marginal zone B-cell development. Blood 2007, 110:3618-3623.
46. Xie Y., Yin T., Wiegraebe W., He X.C., Miller D., Stark D., Perko K., Alexander R., Schwartz J., Grindley J.C., et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 2009, 457:97-101.
47. Xue Y., Gao X., Lindsell C.E., Norton C.R., Chang B., Hicks C., Gendron-Maguire M., Rand E.B., Weinmaster G., Gridley T. Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum. Mol. Genet. 1999, 8:723-730.
48. Yamazaki S., Ema H., Karlsson G., Yamaguchi T., Miyoshi H., Shioda S., Taketo M.M., Karlsson S., Iwama A., Nakauchi H. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 2011, 147:1146-1158.
49. Yoshihara H., Arai F., Hosokawa K., Hagiwara T., Takubo K., Nakamura Y., Gomei Y., Iwasaki H., Matsuoka S., Miyamoto K., et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007, 1:685-697.