Hemogenic endothelium generates mesoangioblasts that contribute to several mesodermal lineages in vivo

Development (Cambridge)

Volumn 141, Issue 9, 2014, Pages 1821-1834

  Azzoni, Emanuele ^a,b,f   Conti, Valentina ^a,b   Campana, Lara ^b   Dellavalle, Arianna ^b   Adams, Ralf H ^c,d   Cossu, Giulio ^b,e   Brunelli, Silvia ^a,b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Hemogenic endothelium; Mesoangioblasts; Mouse; Muscle; VE Cadherin

Indexed keywords

CRE RECOMBINASE;

ANIMAL EXPERIMENT; ARTERY; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; FEMALE; HEMANGIOBLAST; HEMATOPOIETIC CELL; MACROPHAGE; MESENCHYME; MESOANGIOBLAST; MESODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; SMOOTH MUSCLE;

HEMOGENIC ENDOTHELIUM; MESOANGIOBLASTS; MOUSE; MUSCLE; VE-CADHERIN;

ANIMALS; BIOLOGICAL MARKERS; CADHERINS; CELL LINEAGE; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; HEMANGIOBLASTS; HEMATOPOIETIC STEM CELLS; INTEGRASES; MACROPHAGES; MESODERM; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; MUSCLE, SMOOTH; RECEPTORS, COMPLEMENT 3B; RECOMBINATION, GENETIC;

EID: 84899636141     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.103242     Document Type: Article

References (46)

1. Balconi, G., Spagnuolo, R. and Dejana, E. (2000). Development of endothelial cell lines from embryonic stem cells: a tool for studying genetically manipulated endothelial cells in vitro. Arterioscler. Thromb. Vasc. Biol. 20, 1443-1451.
2. Bertrand, J. Y., Jalil, A., Klaine, M., Jung, S., Cumano, A. and Godin, I. (2005). Three pathways to mature macrophages in the early mouse yolk sac. Blood 106, 3004-3011.
3. Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. R. and Traver, D. (2010). Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111.
4. Biressi, S., Tagliafico, E., Lamorte, G., Monteverde, S., Tenedini, E., Roncaglia, E., Ferrari, S., Ferrari, S., Cusella-De Angelis, M. G., Tajbakhsh, S. et al. (2007). Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Dev. Biol. 304, 633-651.
5. Boisset, J.-C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E. and Robin, C. (2010). In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120.
6. Borges, L., Iacovino, M., Koyano-Nakagawa, N., Baik, J., Garry, D. J., Kyba, M. and Perlingeiro, R. C. R. (2013). Expression levels of endoglin distinctively identify hematopoietic and endothelial progeny at different stages of yolk sac hematopoiesis. Stem Cells 31, 1893-1901.
7. Brunelli, S., Tagliafico, E., De Angelis, F. G., Tonlorenzi, R., Baesso, S., Ferrari, S., Niinobe, M., Yoshikawa, K., Schwartz, R. J., Bozzoni, I. et al. (2004). Msx2 and necdin combined activities are required for smooth muscle differentiation in mesoangioblast stem cells. Circ. Res. 94, 1571-1578.
8. Brunelli, S., Sciorati, C., D'Antona, G., Innocenzi, A., Covarello, D., Galvez, B. G., Perrotta, C., Monopoli, A., Sanvito, F., Bottinelli, R. et al. (2007). Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc. Natl. Acad. Sci. U. S. A. 104, 264-269.
9. Chen, M. J., Li, Y., DeObaldia, M. E., Yang, Q., Yzaguirre, A. D., Yamada-Inagawa, T., Vink, C. S., Bhandoola, A., Dzierzak, E. and Speck, N. A. (2011). Erythroid/myeloid progenitors and hematopoietic stem cells originate from distinct populations of endothelial cells. Cell Stem Cell 9, 541-552.
10. Costa, G., Mazan, A., Gandillet, A., Pearson, S., Lacaud, G. and Kouskoff, V. (2012). SOX7 regulates the expression of VE-cadherin in the haemogenic endothelium at the onset of haematopoietic development. Development 139, 1587-1598.
11. Crawford, K., Flick, R., Close, L., Shelly, D., Paul, R., Bove, K., Kumar, A. and Lessard, J. (2002). Mice lacking skeletal muscle actin show reduced muscle strength and growth deficits and die during the neonatal period. Mol. Cell. Biol. 22, 5887-5896.
12. Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Galvez, B. G., Messina, G., Morosetti, R. et al. (2007). Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat. Cell Biol. 9, 255-267.
13. Dellavalle, A., Maroli, G., Covarello, D., Azzoni, E., Innocenzi, A., Perani, L., Antonini, S., Sambasivan, R., Brunelli, S., Tajbakhsh, S. et al. (2011). Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2, 499.
14. DeRuiter, M. C., Poelmann, R. E., VanMunsteren, J. C., Mironov, V., Markwald, R. R. and Gittenberger-de Groot, A. C. (1997). Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ. Res. 80, 444-451.
15. Doyonnas, R., LaBarge, M. A., Sacco, A., Charlton, C. and Blau, H. M. (2004). Hematopoietic contribution to skeletal muscle regeneration by myelomonocytic precursors. Proc. Natl. Acad. Sci. U. S. A. 101, 13507-13512.
16. Drake, C. J. and Fleming, P. A. (2000). Vasculogenesis in the day 6. 5 to 9. 5 mouse embryo. Blood 95, 1671-1679.
17. Dzierzak, E. and Robin, C. (2010). Placenta as a source of hematopoietic stem cells. Trends Mol. Med. 16, 361-367.
18. Huber, T. L., Kouskoff, V., Fehling, H. J., Palis, J. and Keller, G. (2004). Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432, 625-630.
19. Kissa, K. and Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115.
20. Kumaravelu, P., Hook, L., Morrison, A. M., Ure, J., Zhao, S., Zuyev, S., Ansell, J. and Medvinsky, A. (2002). Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 129, 4891-4899.
21. Lancrin, C., Sroczynska, P., Stephenson, C., Allen, T., Kouskoff, V. and Lacaud, G. (2009). The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457, 892-895.
22. Li, W., Ferkowicz, M. J., Johnson, S. A., Shelley, W. C. and Yoder, M. C. (2005). Endothelial cells in the early murine yolk sac give rise to CD41-expressing hematopoietic cells. Stem Cells Dev. 14, 44-54.
23. Liebner, S., Cattelino, A., Gallini, R., Rudini, N., Iurlaro, M., Piccolo, S. and Dejana, E. (2004). Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J. Cell Biol. 166, 359-367.
24. Medvinsky, A., Rybtsov, S. and Taoudi, S. (2011). Embryonic origin of the adult hematopoietic system: advances and questions. Development 138, 1017-1031.
25. Mendes, S. C. (2005). Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Development 132, 1127-1136.
26. Minasi, M. G., Riminucci, M., De Angelis, L., Borello, U., Berarducci, B., Innocenzi, A., Caprioli, A., Sirabella, D., Baiocchi, M., De Maria, R. et al. (2002). The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129, 2773-2783.
27. Mitchell, K. J., Pannerec, A., Cadot, B., Parlakian, A., Besson, V., Gomes, E. R., Marazzi, G. and Sassoon, D. A. (2010). Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat. Cell Biol. 12, 257-266.
28. Ojima, K., Uezumi, A., Miyoshi, H., Masuda, S., Morita, Y., Fukase, A., Hattori, A., Nakauchi, H., Miyagoe-Suzuki, Y. and Takeda, S.-I. (2004). Mac-1(low) early myeloid cells in the bone marrow-derived SP fraction migrate into injured skeletal muscle and participate in muscle regeneration. Biochem. Biophys. Res. Commun. 321, 1050-1061.
29. Ovchinnikov, D. A. (2008). Macrophages in the embryo and beyond: much more than just giant phagocytes. Genesis 46, 447-462.
30. Park, E. J., Sun, X., Nichol, P., Saijoh, Y., Martin, J. F. and Moon, A. M. (2007). System for tamoxifen-inducible expression of cre-recombinase from the Foxa2 locus in mice. Dev. Dyn. 237, 447-453.
31. Pessina, P., Conti, V., Tonlorenzi, R., Touvier, T., Meneveri, R., Cossu, G. and Brunelli, S. (2011). Necdin enhances muscle reconstitution of dystrophic muscle by vessel-associated progenitors, by promoting cell survival and myogenic differentiation. Cell Death Differ. 19, 827-838.
32. Pucci, F., Venneri, M. A., Biziato, D., Nonis, A., Moi, D., Sica, A., Di Serio, C., Naldini, L. and De Palma, M. (2009). A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 114, 901-914.
33. Rhodes, K. E., Gekas, C., Wang, Y., Lux, C. T., Francis, C. S., Chan, D. N., Conway, S., Orkin, S. H., Yoder, M. C. and Mikkola, H. K. A. (2008). The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2, 252-263.
34. Russo, V., Zhou, D., Sartirana, C., Rovere, P., Villa, A., Rossini, S., Traversari, C. and Bordignon, C. (2000). Acquisition of intact allogeneic human leukocyte antigen molecules by human dendritic cells. Blood 95, 3473-3477.
35. Sampaolesi, M., Torrente, Y., Innocenzi, A., Tonlorenzi, R., D'Antona, G., Pellegrino, M. A., Barresi, R., Bresolin, N., De Angelis, M. G. C., Campbell, K. P. et al. (2003). Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301, 487-492.
36. Schulz, C., Perdiguero, E. G., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S. E. W., Pollard, J. W. et al. (2012). A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336, 86-90.
37. Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
38. Tagliafico, E., Brunelli, S., Bergamaschi, A., DeAngelis, L., Scardigli, R., Galli, D., Battini, R., Bianco, P., Ferrari, S. and Cossu, G. (2004). TGFbeta/BMP activate the smooth muscle/bone differentiation programs in mesoangioblasts. J. Cell Sci. 117, 4377-4388.
39. Tonlorenzi, R., Dellavalle, A., Schnapp, E., Cossu, G. and Sampaolesi, M. (2007). Isolation and characterization of mesoangioblasts from mouse, dog, and human tissues. Curr. Protoc. Stem Cell Biol. Chapter 2, Unit 2B 1.
40. Wang, L. D. and Wagers, A. J. (2011). Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat. Rev. Mol. Cell Biol. 12, 643-655.
41. Wang, Y., Nakayama, M., Pitulescu, M. E., Schmidt, T. S., Bochenek, M. L., Sakakibara, A., Adams, S., Davy, A., Deutsch, U., Lüthi, U. et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
42. Yamashita, J., Itoh, H., Hirashima, M., Ogawa, M., Nishikawa, S., Yurugi, T., Naito, M., Nakao, K. and Nishikawa, S.-I. (2000). Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408, 92-96.
43. Yoder, M. C., Hiatt, K. and Mukherjee, P. (1997). In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9. 0 postcoitus. Proc. Natl. Acad. Sci. U. S. A. 94, 6776-6780.
44. Yokomizo, T., Ng, C. E. L., Osato, M. and Dzierzak, E. (2011). Three-dimensional imaging of whole midgestation murine embryos shows an intravascular localization for all hematopoietic clusters. Blood 117, 6132-6134.
45. Zovein, A. C., Hofmann, J. J., Lynch, M., French, W. J., Turlo, K. A., Yang, Y., Becker, M. S., Zanetta, L., Dejana, E., Gasson, J. C. et al. (2008). Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3, 625-636.
46. Zovein, A. C., Turlo, K. A., Ponec, R. M., Lynch, M. R., Chen, K. C., Hofmann, J. J., Cox, T. C., Gasson, J. C. and Iruela-Arispe, M. L. (2010). Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters. Blood 116, 3435-3444.