PTEN mediates Notch-dependent stalk cell arrest in angiogenesis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Serra, Helena ^a   Chivite, Iñigo ^a   Angulo Urarte, Ana ^a   Soler, Adriana ^a   Sutherland, James D ^b   Arruabarrena Aristorena, Amaia ^b   Ragab, Anan ^c   Lim, Radiance ^d   Malumbres, Marcos ^e   Fruttiger, Marcus ^f   Potente, Michael ^d   Serrano, Manuel ^e   Fabra, Àngels ^g   Viñals, Francesc ^g   Casanovas, Oriol ^g   Pandolfi, Pier Paolo ^h   Bigas, Anna ⁱ   Carracedo, Arkaitz ^b,j,k   Gerhardt, Holger ^c,l   Graupera, Mariona ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b CIC BIOGUNE   (Spain)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^e Structural Biology and Biocomputing Programme   (Spain)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY OF BARCELONA   (Spain)

^h HARVARD MEDICAL SCHOOL   (United States)

ⁱ INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^j BASQUE FOUNDATION FOR SCIENCE   (Spain)

^k UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^l MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; ANAPHASE PROMOTING COMPLEX; FIZZY RELATED PROTEIN; FZR1 PROTEIN, MOUSE; MESSENGER RNA; PTEN PROTEIN, MOUSE;

CATALYSIS; CELL ORGANELLE; ENZYME ACTIVITY; GENE EXPRESSION; LIPID; PHYSIOLOGY; PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CATALYST; CELL CYCLE ARREST; CELL PROLIFERATION; EMBRYONIC STEM CELL; GENE OVEREXPRESSION; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; ANIMAL; ENDOTHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; METABOLISM; POLYMERASE CHAIN REACTION;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CDH1 PROTEINS; CELL PROLIFERATION; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; POLYMERASE CHAIN REACTION; PTEN PHOSPHOHYDROLASE; RECEPTORS, NOTCH; RNA, MESSENGER;

EID: 84938510798     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8935     Document Type: Article

References (55)

1. Adams, R. H. & Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478 (2007).
2. Potente, M., Gerhardt, H. & Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887 (2011).
3. Ruhrberg, C. et al. Spatially restricted patterning cues provided by heparinbinding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16, 2684-2698 (2002).
4. Gerhardt, H. et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
5. Blanco, R. & Gerhardt, H. VEGF and Notch in tip and stalk cell selection. Cold Spring Harb. Perspect. Med. 3, a006569 (2012).
6. Roca, C. & Adams, R. H. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524 (2007).
7. Phng, L. K. & Gerhardt, H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208 (2009).
8. Noseda, M. et al. Notch activation induces endothelial cell cycle arrest and participates in contact inhibition: role of p21Cip1 repression. Mol. Cell Biol. 24, 8813-8822 (2004).
9. Hellstrom, M. et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780 (2007).
10. Phng, L. K. et al. Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16, 70-82 (2009).
11. Benedito, R. et al. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135 (2009).
12. Benedito, R. & Hellstrom, M. Notch as a hub for signaling in angiogenesis. Exp. Cell Res. 319, 1281-1288 (2013).
13. Song, M. S., Salmena, L. & Pandolfi, P. P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 13, 283-296 (2013).
14. Leslie, N. R., Maccario, H., Spinelli, L. & Davidson, L. The significance of PTEN's protein phosphatase activity. Adv. Enzyme Regul. 49, 190-196 (2009).
15. Hopkins, B. D., Hodakoski, C., Barrows, D., Mense, S. M. & Parsons, R. E. PTEN function: the long and the short of it. Trends Biochem. Sci. 39, 183-190 (2014).
16. Cantley, L. C. The phosphoinositide 3-kinase pathway. Science 296, 1655-1657 (2002).
17. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. & Bilanges, B. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11, 329-341 (2010).
18. Hawkins, P. T., Anderson, K. E., Davidson, K. & Stephens, L. R. Signalling through Class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34, 647-662 (2006).
19. Hamada, K. et al. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev. 19, 2054-2065 (2005).
20. Choorapoikayil, S., Weijts, B., Kers, R., de Bruin, A. & den Hertog, J. Loss of Pten promotes angiogenesis and enhanced vegfaa expression in zebrafish. Dis. Model Mech. 6, 1159-1166 (2013).
21. Lindsay, Y. et al. Localization of agonist-sensitive PtdIns(3,4,5)P3 reveals a nuclear pool that is insensitive to PTEN expression. J. Cell Sci. 119, 5160-5168 (2006).
22. Song, M. S. et al. Nuclear PTEN regulates the APC-CDH1 tumor-suppressive complex in a phosphatase-independent manner. Cell 144, 187-199 (2011).
23. Whiteman, D. C. et al. Nuclear PTEN expression and clinicopathologic features in a population-based series of primary cutaneous melanoma. Int. J. Cancer 99, 63-67 (2002).
24. Ginn-Pease, M. E. & Eng, C. Increased nuclear phosphatase and tensin homologue deleted on chromosome 10 is associated with G0-G1 in MCF-7 cells. Cancer Res. 63, 282-286 (2003).
25. Manchado, E., Eguren, M. & Malumbres, M. The anaphase-promoting complex/cyclosome (APC/C): cell-cycle-dependent and -independent functions. Biochem. Soc. Trans. 38, 65-71 (2010).
26. Claxton, S. et al. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis 46, 74-80 (2008).
27. Jakobsson, L. et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625-634 (2006).
28. Ortega-Molina, A. et al. Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab. 15, 382-394 (2012).
29. Graupera, M. et al. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 453, 662-666 (2008).
30. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2010).
31. Edgar, K. A. et al. Isoform-specific phosphoinositide 3-kinase inhibitors exert distinct effects in solid tumors. Cancer Res. 70, 1164-1172 (2010).
32. Nelen, M. R. et al. Germline mutations in the PTEN/MMAC1 gene in patients with Cowden disease. Hum. Mol. Genet. 6, 1383-1387 (1997).
33. Wang, H. et al. Allele-specific tumor spectrum in pten knockin mice. Proc. Natl Acad. Sci. USA 107, 5142-5147 (2010).
34. Siekmann, A. F. & Lawson, N. D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784 (2007).
35. Moya, I. M. et al. Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev. Cell 22, 501-514 (2012).
36. Bertrand, F. E., McCubrey, J. A., Angus, C. W., Nutter, J. M. & Sigounas, G. NOTCH and PTEN in prostate cancer. Adv. Biol. Regul. 56, 51-65 (2014).
37. Palomero, T. et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13, 1203-1210 (2007).
38. Wong, G. W., Knowles, G. C., Mak, T. W., Ferrando, A. A. & Zuniga-Pflucker, J. C. HES1 opposes a PTEN-dependent check on survival, differentiation, and proliferation of TCRbeta-selected mouse thymocytes. Blood 120, 1439-1448 (2012).
39. Benedito, R. et al. Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484, 110-114 (2012).
40. Shen, W. H. et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128, 157-170 (2007).
41. Trotman, L. C. et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128, 141-156 (2007).
42. Howitt, J. et al. Ndfip1 regulates nuclear Pten import in vivo to promote neuronal survival following cerebral ischemia. J. Cell Biol. 196, 29-36 (2012).
43. Freeman, D. J. et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 3, 117-130 (2003).
44. Herbert, S. P. et al. Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 326, 294-298 (2009).
45. Nicoli, S., Knyphausen, C. P., Zhu, L. J., Lakshmanan, A. & Lawson, N. D. wmiR-221 is required for endothelial tip cell behaviors during vascular development. Dev. Cell 22, 418-429 (2012).
46. Graupera, M. & Potente, M. Regulation of angiogenesis by PI3K signaling networks. Exp. Cell Res. 319, 1348-1355 (2013).
47. Soler, A. et al. Inhibition of the p110alpha isoform of PI 3-kinase stimulates nonfunctional tumor angiogenesis. J. Exp. Med. 210, 1937-1945 (2013).
48. Wustehube, J. et al. Cerebral cavernous malformation protein CCM1 inhibits sprouting angiogenesis by activating DELTA-NOTCH signaling. Proc. Natl Acad. Sci. USA 107, 12640-12645 (2010).
49. Carmeliet, P. & Jain, R. K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10, 417-427 (2011).
50. Suzuki, A. et al. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 14, 523-534 (2001).
51. Garcia-Higuera, I. et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 10, 802-811 (2008).
52. Brooker, R., Hozumi, K. & Lewis, J. Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133, 1277-1286 (2006).
53. Di Cristofano, A., Pesce, B., Cordon-Cardo, C. & Pandolfi, P. P. Pten is essential for embryonic development and tumour suppression. Nat. Genet. 19, 348-355 (1998).
54. Guarani, V. et al. Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature 473, 234-238 (2011).
55. Guiu, J. et al. Hes repressors are essential regulators of hematopoietic stem cell development downstream of Notch signaling. J. Exp. Med. 210, 71-84 (2013).