Vasculature-associated cells expressing nestin in developing bones encompass early cells in the osteoblast and endothelial lineage

Developmental Cell

Volumn 29, Issue 3, 2014, Pages 330-339

  Ono, Noriaki ^a   Ono, Wanida ^a   Mizoguchi, Toshihide ^b   Nagasawa, Takashi ^c,d   Frenette, Paul S ^b   Kronenberg, Henry M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CRE RECOMBINASE; NESTIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX2; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; CARTILAGE CELL; CELL LINEAGE; EMBRYO DEVELOPMENT; ENCHONDRAL OSSIFICATION; MOUSE; NONHUMAN; OSTEOBLAST; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASCULARIZATION; ANIMAL CELL; CELL COUNT; CELL POPULATION; ENDOTHELIUM CELL; ENHANCER REGION; HEDGEHOG; OSSIFICATION; POSTNATAL CARE; POSTNATAL DEVELOPMENT; STROMA CELL;

ANIMALS; BONE AND BONES; CELL LINEAGE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; ENDOTHELIAL CELLS; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; HEMATOPOIESIS; MICE; MICE, KNOCKOUT; NESTIN; OSTEOBLASTS; PROMOTER REGIONS, GENETIC;

EID: 84900301554     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.03.014     Document Type: Article

References (27)

1. Ara T., Tokoyoda K., Sugiyama T., Egawa T., Kawabata K., Nagasawa T. Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity 2003, 19:257-267.
2. Balordi F., Fishell G. Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for self-renewal. J. Neurosci. 2007, 27:14248-14259.
3. 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.
4. Chan C.K., Chen C.C., Luppen C.A., Kim J.B., Deboer A.T., Wei K., Helms J.A., Kuo C.J., Kraft D.L., Weissman I.L. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 2009, 457:490-494.
5. Christensen J.L., Wright D.E., Wagers A.J., Weissman I.L. Circulation and chemotaxis of fetal hematopoietic stem cells. PLoS Biol. 2004, 2:E75.
6. Ding L., Morrison S.J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013, 495:231-235.
7. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481:457-462.
8. Greenbaum A., Hsu Y.M., Day R.B., Schuettpelz L.G., Christopher M.J., Borgerding J.N., Nagasawa T., Link D.C. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013, 495:227-230.
9. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
10. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
11. Maes C., Kobayashi T., Selig M.K., Torrekens S., Roth S.I., Mackem S., Carmeliet G., Kronenberg H.M. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev. Cell 2010, 19:329-344.
12. 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.
13. Mignone J.L., Kukekov V., Chiang A.S., Steindler D., Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 2004, 469:311-324.
14. Mizoguchi T., Ahmed J., Kunisaki Y., Pinho S., Ono N., Kronenberg H.M., Frenette P.S. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev. Cell 2014, 29:340-349. this issue.
15. Mokrý J., Cízková D., Filip S., Ehrmann J., Osterreicher J., Kolár Z., English D. Nestin expression by newly formed human blood vessels. Stem Cells Dev. 2004, 13:658-664.
16. Nagasawa T., Hirota S., Tachibana K., Takakura N., Nishikawa S., Kitamura Y., Yoshida N., Kikutani H., Kishimoto T. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382:635-638.
17. Nakamura E., Nguyen M.T., Mackem S. Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 2006, 235:2603-2612.
18. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771.
19. Ovchinnikov D.A., Deng J.M., Ogunrinu G., Behringer R.R. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 2000, 26:145-146.
20. Rodda S.J., Mcmahon A.P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006, 133:3231-3244.
21. Sacchetti B., Funari A., Michienzi S., Di Cesare S., Piersanti S., Saggio I., Tagliafico E., Ferrari S., Robey P.G., Riminucci M., Bianco P. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007, 131:324-336.
22. St-Jacques B., Hammerschmidt M., Mcmahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999, 13:2072-2086.
23. 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.
24. Szabova L., Yamada S.S., Wimer H., Chrysovergis K., Ingvarsen S., Behrendt N., Engelholm L.H., Holmbeck K. MT1-MMP and type II collagen specify skeletal stem cells and their bone and cartilage progeny. J. Bone Miner. Res. 2009, 24:1905-1916.
25. Teranishi N., Naito Z., Ishiwata T., Tanaka N., Furukawa K., Seya T., Shinji S., Tajiri T. Identification of neovasculature using nestin in colorectal cancer. Int. J. Oncol. 2007, 30:593-603.
26. Wroblewski J., Engström M., Edwall-Arvidsson C., Sjöberg G., Sejersen T., Lendahl U. Distribution of nestin in the developing mouse limb bud in vivo and in micro-mass cultures of cells isolated from limb buds. Differentiation 1997, 61:151-159.
27. Zhang J., Niu C., Ye L., Huang H., He X., Tong W.G., Ross J., Haug J., Johnson T., Feng J.Q., et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.