Cell-matrix signals specify bone endothelial cells during developmental osteogenesis

Nature Cell Biology

Volumn 19, Issue 3, 2017, Pages 189-201

  Langen, Urs H ^a   Pitulescu, Mara E ^a   Kim, Jung Mo ^a   Enriquez Gasca, Rocio ^b   Sivaraj, Kishor K ^a   Kusumbe, Anjali P ^a   Singh, Amit ^a,b   Di Russo, Jacopo ^a   Bixel, M Gabriele ^a   Zhou, Bin ^c   Sorokin, Lydia ^a   Vaquerizas, Juan M ^b   Adams, Ralf H ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c Chinese Academy of Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CELL ADHESION MOLECULE; LAMININ; LAMININ ALPHA5; UNCLASSIFIED DRUG; ADIPOCYTOKINE; APLN PROTEIN, MOUSE; CRE RECOMBINASE; INTEGRASE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE CELL; BONE DEVELOPMENT; BONE ENDOTHELIAL CELL; BONE GROWTH; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL SUBPOPULATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; LONG BONE; MOUSE; NEWBORN; NONHUMAN; OSTEOBLAST; VASCULARIZATION; ANGIOGENESIS; ANIMAL; BONE; C57BL MOUSE; CAPILLARY; CELL ADHESION; CYTOLOGY; DIAGNOSTIC IMAGING; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; MUTANT MOUSE STRAIN; PHENOTYPE; SIGNAL TRANSDUCTION;

ADIPOKINES; ANIMALS; ANTIGENS, CD29; BONE AND BONES; CAPILLARIES; CELL ADHESION; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INTEGRASES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOGENESIS; PHENOTYPE; SIGNAL TRANSDUCTION; X-RAY MICROTOMOGRAPHY;

EID: 85014267813     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3476     Document Type: Article

References (66)

1. Kronenberg, H. M. Developmental regulation of the growth plate. Nature 423, 332-336 (2003).
2. Long, F. & Ornitz, D. M. Development of the endochondral skeleton. Cold Spring Harb. Perspect. Biol. 5, a008334 (2013).
3. Eshkar-Oren, I. et al. The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation of Vegf. Development 136, 1263-1272 (2009).
4. Conen, K. L., Nishimori, S., Provot, S. & Kronenberg, H. M. The transcriptional cofactor Lbh regulates angiogenesis and endochondral bone formation during fetal bone development. Dev. Biol. 333, 348-358 (2009).
5. Maes, C. et al. Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech. Dev. 111, 61-73 (2002).
6. Maes, C. et al. Increased skeletal VEGF enhances β-catenin activity and results in excessively ossified bones. EMBO J. 29, 424-441 (2010).
7. Maes, C. et al. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev. Cell 19, 329-344 (2010).
8. Ding, B. S. et al. Divergent angiocrine signals from vascular niche balance liver regeneration and fibrosis. Nature 505, 97-102 (2014).
9. Ding, B. S. et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 468, 310-315 (2010).
10. Ding, B. S. et al. Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 147, 539-553 (2011).
11. Ramasamy, S. K., Kusumbe, A. P., Wang, L. & Adams, R. H. Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature 507, 376-380 (2014).
12. Hu, J. et al. Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat. Science 343, 416-419 (2014).
13. Kusumbe, A. P., Ramasamy, S. K. & Adams, R. H. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 507, 323-328 (2014).
14. Xie, H. et al. PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis. Nat. Med. 20, 1270-1278 (2014).
15. Alford, A. I., Kozloff, K. M. & Hankenson, K. D. Extracellular matrix networks in bone remodeling. Int. J. Biochem. Cell Biol. 65, 20-31 (2015).
16. Marie, P. J., Hay, E. & Saidak, Z. Integrin and cadherin signaling in bone: role and potential therapeutic targets. Trends Endocrinol. Metab. 25, 567-575 (2014).
17. Olsen, B. R., Reginato, A. M. & Wang, W. Bone development. Annu. Rev. Cell Dev. Biol. 16, 191-220 (2000).
18. Humphries, J. D., Byron, A. & Humphries, M. J. Integrin ligands at a glance. J. Cell Sci. 119, 3901-3903 (2006).
19. Barczyk, M., Carracedo, S. & Gullberg, D. Integrins. Cell Tissue Res. 339, 269-280 (2010).
20. Lei, L. et al. Endothelial expression of β1 integrin is required for embryonic vascular patterning and postnatal vascular remodeling. Mol. Cell Biol. 28, 794-802 (2008).
21. Carlson, T. R., Hu, H., Braren, R., Kim, Y. H. & Wang, R. A. Cell-autonomous requirement for β1 integrin in endothelial cell adhesion, migration and survival during angiogenesis in mice. Development 135, 2193-2202 (2008).
22. Tanjore, H., Zeisberg, E. M., Gerami-Naini, B. & Kalluri, R. Beta1 integrin expression on endothelial cells is required for angiogenesis but not for vasculogenesis. Dev. Dyn. 237, 75-82 (2008).
23. Zovein, A. C. et al. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev. Cell 18, 39-51 (2010).
24. Yamamoto, H. et al. Integrin β1 controls VE-cadherin localization and blood vessel stability. Nat. Commun. 6, 6429 (2015).
25. Zelzer, E. et al. Skeletal defects in VEGF (120/120) mice reveal multiple roles for VEGF in skeletogenesis. Development 129, 1893-1904 (2002).
26. Tammela, T. et al. VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat. Cell Biol. 13, 1202-1213 (2011).
27. Benedito, R. et al. Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484, 110-114 (2012).
28. Lohela, M., Bry, M., Tammela, T. & Alitalo, K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr. Opin. Cell Biol. 21, 154-165 (2009).
29. Olsson, A. K., Dimberg, A., Kreuger, J. & Claesson-Welsh, L. VEGF receptor signalling-in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371 (2006).
30. Zarkada, G., Heinolainen, K., Makinen, T., Kubota, Y. & Alitalo, K. VEGFR3 does not sustain retinal angiogenesis without VEGFR2. Proc. Natl Acad. Sci. USA 112, 761-766 (2015).
31. Nakayama, M. et al. Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat. Cell Biol. 15, 249-260 (2013).
32. Latonen, L., Taya, Y. & Laiho, M. UV-radiation induces dose-dependent regulation of p53 response and modulates p53-HDM2 interaction in human fibroblasts. Oncogene 20, 6784-6793 (2001).
33. Kikkawa, Y. & Miner, J. H. Review: Lutheran/B-CAM: a laminin receptor on red blood cells and in various tissues. Connect. Tissue Res. 46, 193-199 (2005).
34. Reznikoff, C. A., Brankow, D. W. & Heidelberger, C. Establishment and characterization of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division. Cancer Res. 33, 3231-3238 (1973).
35. Liu, Q. et al. Genetic targeting of sprouting angiogenesis using Apln-CreER. Nat. Commun. 6, 6020 (2015).
36. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
37. Luo, W., Friedman, M. S., Shedden, K., Hankenson, K. D. & Woolf, P. J. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 10, 161 (2009).
38. Yousif, L. F., Di Russo, J. & Sorokin, L. Laminin isoforms in endothelial and perivascular basement membranes. Cell Adh. Migr. 7, 101-110 (2013).
39. Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486 (2010).
40. Raghavan, S., Bauer, C., Mundschau, G., Li, Q. & Fuchs, E. Conditional ablation of β1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 150, 1149-1160 (2000).
41. Miner, J. H., Cunningham, J. & Sanes, J. R. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin α5 chain. J. Cell Biol. 143, 1713-1723 (1998).
42. Song, J. et al. Extracellular matrix of secondary lymphoid organs impacts on B-cell fate and survival. Proc. Natl Acad. Sci. USA 110, E2915-E2924 (2013).
43. Sorokin, L. M. et al. Developmental regulation of the laminin α5 chain suggests a role in epithelial and endothelial cell maturation. Dev. Biol. 189, 285-300 (1997).
44. Scoazec, J. Y., Racine, L., Couvelard, A., Flejou, J. F. & Feldmann, G. Endothelial cell heterogeneity in the normal human liver acinus: in situ immunohistochemical demonstration. Liver 14, 113-123 (1994).
45. Rajotte, D. et al. Molecular heterogeneity of the vascular endothelium revealed by in vivo phage display. J. Clin. Invest. 102, 430-437 (1998).
46. Scott, R. P. & Quaggin, S. E. Review series: the cell biology of renal filtration. J. Cell Biol. 209, 199-210 (2015).
47. Molema, G. & Aird, W. C. Vascular heterogeneity in the kidney. Semin. Nephrol. 32, 145-155 (2012).
48. Palmer, T. D., Willhoite, A. R. & Gage, F. H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494 (2000).
49. Culver, J. C., Vadakkan, T. J. & Dickinson, M. E. A specialized microvascular domain in the mouse neural stem cell niche. PLoS One 8, e53546 (2013).
50. Gumbiner, B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357 (1996).
51. Danen, E. H. & Sonnenberg, A. Integrins in regulation of tissue development and function. J. Pathol. 201, 632-641 (2003).
52. Felcht, M. et al. Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J. Clin. Invest. 122, 1991-2005 (2012).
53. Hakanpaa, L. et al. Endothelial destabilization by angiopoietin-2 via integrin β1 activation. Nat. Commun. 6, 5962 (2015).
54. Emre, Y. & Imhof, B. A. Matricellular protein CCN1/CYR61: a new player in inflammation and leukocyte trafficking. Semin. Immunopathol. 36, 253-259 (2014).
55. Ivaska, J. & Heino, J. Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu. Rev. Cell Dev. Biol. 27, 291-320 (2011).
56. Forlino, A., Cabral, W. A., Barnes, A. M. & Marini, J. C. New perspectives on osteogenesis imperfecta. Nat. Rev. Endocrinol. 7, 540-557 (2011).
57. Tosi, L. L. & Warman, M. L. Mechanistic and therapeutic insights gained from studying rare skeletal diseases. Bone 76, 67-75 (2015).
58. Tranquilli Leali, P. et al. Bone fragility: current reviews and clinical features. Clin. Cases Miner. Bone Metab. 6, 109-113 (2009).
59. Tian, X. et al. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 23, 1075-1090 (2013).
60. Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial celllineage analysis in vivo. Dev. Biol. 230, 230-242 (2001).
61. Thyboll, J. et al. Deletion of the laminin α4 chain leads to impaired microvessel maturation. Mol. Cell Biol. 22, 1194-1202 (2002).
62. Liaw, L. et al. Altered wound healing in mice lacking a functional osteopontin gene (spp1). J. Clin. Invest. 101, 1468-1478 (1998).
63. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
64. Anders, S., Pyl, P. T. & Huber, W. HTSeq-a Python framework to work with highthroughput sequencing data. Bioinformatics 31, 166-169 (2015).
65. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
66. Wold, S., Esbensen, K. & Geladi, P. Principal component analysis. Chemometr. Intel. Lab. Syst. 2, 37-52 (1987).