Subcellular localization of coagulation factor II receptor-like 1 in neurons governs angiogenesis

Nature Medicine

Volumn 20, Issue 10, 2014, Pages 1165-1173

  Joyal, Jean Sébastien ^a,b,c,d   Nim, Satra ^d   Zhu, Tang ^a   Sitaras, Nicholas ^b,c   Rivera, José Carlos ^a,b   Shao, Zhuo ^d   Sapieha, Przemyslaw ^b   Hamel, David ^c   Sanchez, Melanie ^d   Zaniolo, Karine ^a   St Louis, Manon ^d   Ouellette, Johanne ^d   Montoya Zavala, Martin ^e   Zabeida, Alexandra ^a   Picard, Emilie ^a   Hardy, Pierre ^a   Bhosle, Vikrant ^d   Varma, Daya R ^d   Gobeil, Fernand ^f   Beauséjour, Christian ^c   Boileau, Christelle ^c   Klein, William ^g   Hollenberg, Morley ^h   Ribeiro Da Silva, Alfredo ^d   Andelfinger, Gregor ⁱ   Chemtob, Sylvain ^a,b,c,d   more..

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e HARVARD UNIVERSITY   (United States)

^f UNIVERSITÉ DE SHERBROOKE   (Canada)

^g UNIVERSITY OF TEXAS   (United States)

^h UNIVERSITY OF CALGARY   (Canada)

ⁱ UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COAGULATION FACTOR 2 RECEPTOR LIKE 1; G PROTEIN COUPLED RECEPTOR; KARYOPHERIN ALPHA; KARYOPHERIN ALPHA 3; KARYOPHERIN ALPHA 5; KARYOPHERIN BETA; KARYOPHERIN BETA 1; MESSENGER RNA; OMEGA CONOTOXIN MVIIA; PROTHROMBIN; SORTING NEXIN; SORTING NEXIN 11; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; VASCULOTROPIN; ANGIOPOIETIN 1; ANGPT1 PROTEIN, MOUSE; MUTANT PROTEIN; PROTEINASE ACTIVATED RECEPTOR 2; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

AMINO ACID SEQUENCE; ANG1 GENE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL FRACTIONATION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; ELECTRON MICROSCOPY; EMBRYO; ENZYME ACTIVATION; GENE; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MATURATION; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NERVE CELL; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RETINA GANGLION CELL; RETINA NEOVASCULARIZATION; SCANNING ELECTRON MICROSCOPY; ACTIVE TRANSPORT; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; KNOCKOUT MOUSE; METABOLISM; MICROTUBULE; RETINA BLOOD VESSEL;

ACTIVE TRANSPORT, CELL NUCLEUS; ANGIOPOIETIN-1; ANIMALS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULES; MUTANT PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; PROMOTER REGIONS, GENETIC; RECEPTOR, PAR-2; RETINAL GANGLION CELLS; RETINAL VESSELS; SORTING NEXINS; SP1 TRANSCRIPTION FACTOR; SUBCELLULAR FRACTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84921993333     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3669     Document Type: Article

References (80)

1. Saito, T. & Bunnett, N.W. Protease-activated receptors: regulation of neuronal function. Neuromolecular Med. 7, 79-99 (2005).
2. Adams, M.N. et al. Structure, function and pathophysiology of protease activated receptors. Pharmacol. Ther. 130, 248-282 (2011).
3. Milia, A.F. et al. Protease-activated receptor-2 stimulates angiogenesis and accelerates hemodynamic recovery in a mouse model of hindlimb ischemia. Circ. Res. 91, 346-352 (2002).
4. Zhu, T. et al. Proangiogenic effects of protease-activated receptor 2 are tumor necrosis factor-α and consecutively Tie2 dependent. Arterioscler. Thromb. Vasc. Biol. 26, 744-750 (2006).
5. Hughes, S., Yang, H. & Chan-Ling, T. Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Invest. Ophthalmol. Vis. Sci. 41, 1217-1228 (2000).
6. Cringle, S.J., Yu, P.K., Su, E.N. & Yu, D.Y. Oxygen distribution and consumption in the developing rat retina. Invest. Ophthalmol. Vis. Sci. 47, 4072-4076 (2006).
7. Gerhardt, H. et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
8. Scott, A. et al. Astrocyte-derived vascular endothelial growth factor stabilizes vessels in the developing retinal vasculature. PLoS ONE 5, e11863 (2010).
9. Weidemann, A. et al. Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina. Glia 58, 1177-1185 (2010).
10. Bai, Y. et al. Müller cell-derived VEGF is a significant contributor to retinal neovascularization. J. Pathol. 219, 446-454 (2009).
11. Sapieha, P. et al. The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat. Med. 14, 1067-1076 (2008).
12. Mukouyama, Y.S., Shin, D., Britsch, S., Taniguchi, M. & Anderson, D.J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109, 693-705 (2002).
13. Gobeil, F. et al. G-protein-coupled receptors signalling at the cell nucleus: an emerging paradigm. Can. J. Physiol. Pharmacol. 84, 287-297 (2006).
14. Maraldi, N.M. et al. Morphological evidence of function-related localization of phospholipids in the cell nucleus. Adv. Enzyme Regul. 32, 73-90 (1992).
15. Kang, J. et al. A nuclear function of β-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 123, 833-847 (2005).
16. Zhang, Y. et al. Nuclear effects of G-protein receptor kinase 5 on histone deacetylase 5-regulated gene transcription in heart failure. Circ Heart Fail 4, 659-668 (2011).
17. Panicker, L.M. et al. Nuclear localization of the G protein β5/R7-regulator of G protein signaling protein complex is dependent on R7 binding protein. J. Neurochem. 113, 1101-1112 (2010).
18. Zimber, A., Nguyen, Q.-D. & Gespach, C. Nuclear bodies and compartments: functional roles and cellular signalling in health and disease. Cell. Signal. 16, 1085-1104 (2004).
19. Fricker, M., Hollinshead, M., White, N. & Vaux, D. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136, 531-544 (1997).
20. Linde, N. & Stick, R. Intranuclear membranes induced by lipidated proteins are derived from the nuclear envelope. Nucleus 1, 343-353 (2010).
21. Mathew, D. et al. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 310, 1344-1347 (2005).
22. Uusitalo-Jarvinen, H. et al. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler. Thromb. Vasc. Biol. 27, 1456-1462 (2007).
23. Zhu, T. et al. Cortactin activation by FVIIa/tissue factor and PAR2 promotes endothelial cell migration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R577-R585 (2011).
24. Luo, W., Wang, Y. & Reiser, G. Two types of protease-activated receptors (PAR-1 and PAR-2) mediate calcium signaling in rat retinal ganglion cells RGC-5. Brain Res. 1047, 159-167 (2005).
25. Cho, J.-H., Mu, X., Wang, S.W. & Klein, W.H. Retinal ganglion cell death and optic nerve degeneration by genetic ablation in adult mice. Exp. Eye Res. 88, 542-552 (2009).
26. Maxfield, F.R. & McGraw, T.E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132 (2004).
27. King, M.C., Lusk, C.P. & Blobel, G. Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003-1007 (2006).
28. Lusk, C.P., Blobel, G. & King, M.C. Highway to the inner nuclear membrane: rules for the road. Nat. Rev. Mol. Cell Biol. 8, 414-420 (2007).
29. Cullen, P.J. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat. Rev. Mol. Cell Biol. 9, 574-582 (2008).
30. Gullapalli, A., Wolfe, B.L., Griffin, C.T., Magnuson, T. & Trejo, J. An essential role for Snx1 in lysosomal sorting of protease-activated receptor-1: evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol. Biol. Cell 17, 1228-1238 (2006).
31. Traer, C.J. et al. Snx4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9, 1370-1380 (2007).
32. Caviston, J.P. & Holzbaur, E.L. Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol. 16, 530-537 (2006).
33. King, M.C., Drivas, T.G. & Blobel, G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134, 427-438 (2008).
34. Aniento, F., Emans, N., Griffiths, G. & Gruenberg, J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123, 1373-1387 (1993).
35. Roth, D.M., Moseley, G.W., Glover, D., Pouton, C.W. & Jans, D.A. A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 8, 673-686 (2007).
36. Thyberg, J. & Moskalewski, S. Microtubules and the organization of the Golgi complex. Exp. Cell Res. 159, 1-16 (1985).
37. Ray, E. & Samanta, A.K. Dansyl cadaverine regulates ligand induced endocytosis of interleukin-8 receptor in human polymorphonuclear neutrophils. FEBS Lett. 378, 235-239 (1996).
38. Pagès, G. & Pouysségur, J. Transcriptional regulation of the vascular endothelial growth factor gene-a concert of activating factors. Cardiovasc. Res. 65, 564-573 (2005).
39. Gobeil, F. et al. Nitric oxide signaling via nuclearized endothelial nitric-oxide synthase modulates expression of the immediate early genes iNOS and mPGES-1. J. Biol. Chem. 281, 16058-16067 (2006).
40. Ghosh, K. & Ghosh, H.P. Role of the membrane anchoring and cytoplasmic domains in intracellular transport and localization of viral glycoproteins. Biochem. Cell Biol. 77, 165-178 (1999).
41. Augustin, H.G., Koh, G.Y., Thurston, G. & Alitalo, K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 10, 165-177 (2009).
42. Joyal, J.-S. et al. Ischemic neurons prevent vascular regeneration of neural tissue by secreting semaphorin 3A. Blood 117, 6024-6035 (2011).
43. Belting, M. et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat. Med. 10, 502-509 (2004).
44. Eddleston, M. et al. Astrocytes are the primary source of tissue factor in the murine central nervous system. A role for astrocytes in cerebral hemostasis. J. Clin. Invest. 92, 349-358 (1993).
45. Vandell, A.G. et al. Protease-activated receptor dependent and independent signaling by kallikreins 1 and 6 in CNS neuron and astroglial cell lines. J. Neurochem. 107, 855-870 (2008).
46. Sawada, K., Nishibori, M., Nakaya, N., Wang, Z. & Saeki, K. Purification and characterization of a trypsin-like serine proteinase from rat brain slices that degrades laminin and type IV collagen and stimulates protease-activated receptor-2. J. Neurochem. 74, 1731-1738 (2000).
47. Payne, V. & Kam, P.C. Mast cell tryptase: a review of its physiology and clinical significance. Anaesthesia 59, 695-703 (2004).
48. Takeuchi, T. et al. Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and single-chain urokinase-type plasminogen activator as substrates. J. Biol. Chem. 275, 26333-26342 (2000).
49. Aimes, R.T. et al. Endothelial cell serine proteases expressed during vascular morphogenesis and angiogenesis. Thromb. Haemost. 89, 561-572 (2003).
50. Qiu, D., Owen, K., Gray, K., Bass, R. & Ellis, V. Roles and regulation of membrane-associated serine proteases. Biochem. Soc. Trans. 35, 583-587 (2007).
51. Marrache, A.M. et al. Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. J. Immunol. 169, 6474-6481 (2002).
52. Riccio, A., Pierchala, B.A., Ciarallo, C.L. & Ginty, D.D. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277, 1097-1100 (1997).
53. Osborne, K.D., Lee, W., Malarkey, E.B., Irving, A.J. & Parpura, V. Dynamic imaging of cannabinoid receptor 1 vesicular trafficking in cultured astrocytes. ASN Neuro. 1, AN20090040 (2009).
54. Lelouvier, B. et al. Dynamics of somatostatin type 2A receptor cargoes in living hippocampal neurons. J. Neurosci. 28, 4336-4349 (2008).
55. Strochlic, T.I., Schmiedekamp, B.C., Lee, J., Katzmann, D.J. & Burd, C.G. Opposing activities of the Snx3-retromer complex and ESCRT proteins mediate regulated cargo sorting at a common endosome. Mol. Biol. Cell 19, 4694-4706 (2008).
56. Bhattacharya, M. et al. Nuclear localization of prostaglandin E2 receptors. Proc. Natl. Acad. Sci. USA 95, 15792-15797 (1998).
57. Savard, M. et al. Expression of endogenous nuclear bradykinin B2 receptors mediating signaling in immediate early gene activation. J. Cell. Physiol. 216, 234-244 (2008).
58. Carmeliet, P. et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439 (1996).
59. Suri, C. et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180 (1996).
60. Jeansson, M. et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J. Clin. Invest. 121, 2278-2289 (2011).
61. Frassetto, L.J. et al. Kinase-dependent differentiation of a retinal ganglion cell precursor. Invest. Ophthalmol. Vis. Sci. 47, 427-438 (2006).
62. Déry, O., Thoma, M.S., Wong, H., Grady, E.F. & Bunnett, N.W. Trafficking of proteinase-activated receptor-2 and β-arrestin-1 tagged with green fluorescent protein. β-arrestin-dependent endocytosis of a proteinase receptor. J. Biol. Chem. 274, 18524-18535 (1999).
63. Roosterman, D., Schmidlin, F. & Bunnett, N.W. Rab5a and rab11a mediate agonist-induced trafficking of protease-activated receptor 2. Am. J. Physiol. Cell Physiol. 284, C1319-C1329 (2003).
64. Kunkel, T.A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82, 488-492 (1985).
65. Dull, T. et al. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471 (1998).
66. Sirinyan, M. et al. Hyperoxic exposure leads to nitrative stress and ensuing microvascular degeneration and diminished brain mass and function in the immature subject. Stroke 37, 2807-2815 (2006).
67. Stahl, A. et al. The mouse retina as an angiogenesis model. Invest. Ophthalmol. Vis. Sci. 51, 2813-2826 (2010).
68. Sapieha, P. et al. Retinopathy of prematurity: understanding ischemic retinal vasculopathies at an extreme of life. J. Clin. Invest. 120, 3022-3032 (2010).
69. Connor, K.M. et al. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat. Protoc. 4, 1565-1573 (2009).
70. Smith, L.E. et al. Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35, 101-111 (1994).
71. Stahl, A. et al. Computer-aided quantification of retinal neovascularization. Angiogenesis 12, 297-301 (2009).
72. Stahl, A. et al. Postnatal weight gain modifies severity and functional outcome of oxygen-induced proliferative retinopathy. Am. J. Pathol. 177, 2715-2723 (2010).
73. Kong, W. et al. Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc. Natl. Acad. Sci. USA 94, 8884-8889 (1997).
74. McLeod, A.L., Krause, J.E., Cuello, A.C. & Ribeiro-da-Silva, A. Preferential synaptic relationships between substance P-immunoreactive boutons and neurokinin 1 receptor sites in the rat spinal cord. Proc. Natl. Acad. Sci. USA 95, 15775-15780 (1998).
75. Grynkiewicz, G., Poenie, M. & Tsien, R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (1985).
76. Johnson, D.S., Mortazavi, A., Myers, R.M. & Wold, B. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502 (2007).
77. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
78. Matys, V. et al. TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31, 374-378 (2003).
79. Truax, A.D. & Greer, S.F. ChIP and Re-ChIP assays: investigating interactions between regulatory proteins, histone modifications, and the DNA sequences to which they bind. Methods Mol. Biol. 809, 175-188 (2012).
80. Zaniolo, K., Desnoyers, S., Leclerc, S. & Guérin, S.L. Regulation of poly(ADP-ribose) polymerase-1 (PARP-1) gene expression through the post-translational modification of Sp1: a nuclear target protein of PARP-1. BMC Mol. Biol. 8, 96 (2007).