P75NTR-dependent activation of NF-κB regulates microRNA-503 transcription and pericyte-endothelial crosstalk in diabetes after limb ischaemia

Nature Communications

Volumn 6, Issue , 2015, Pages

  Caporali, Andrea ^a,b   Meloni, Marco ^a,f   Nailor, Audrey ^a   Mitić, Tijana ^a   Shantikumar, Saran ^a   Riu, Federica ^a   Sala Newby, Graciela B ^a   Rose, Lorraine ^b   Besnier, Marie ^a   Katare, Rajesh ^a,g   Voellenkle, Christine ^c   Verkade, Paul ^d   Martelli, Fabio ^c   Madeddu, Paolo ^a   Emanueli, Costanza ^a,e  

^a Bristol Heart Institute   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c IRCCS POLICLINICO SAN DONATO   (Italy)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

^g UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN B2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 503; NEUROTROPHIN RECEPTOR P75; RHO KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN A; MIRN503 MICRORNA, HUMAN; MIRN503 MICRORNA, MOUSE; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NGFR PROTEIN, HUMAN; TNFRSF16 PROTEIN, MOUSE;

BLOOD; CARDIOVASCULAR SYSTEM; CELLS AND CELL COMPONENTS; DIABETES; ENZYME ACTIVITY; GENE EXPRESSION; MECHANORECEPTION; MUSCLE; RNA; RODENT;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL COMMUNICATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIAL MICROPARTICLE; ENDOTHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; LIMB ISCHEMIA; MICROVASCULATURE; MOUSE; NONHUMAN; PERICYTE; PROMOTER REGION; RNA EXTRACTION; RNA TRANSCRIPTION; UPREGULATION; ANIMAL; CELL CULTURE; DNA MICROARRAY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HINDLIMB; ISCHEMIA; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HINDLIMB; HUMANS; ISCHEMIA; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; NERVE TISSUE PROTEINS; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PERICYTES; RECEPTORS, NERVE GROWTH FACTOR; TRANSCRIPTION, GENETIC;

EID: 84939130561     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9024     Document Type: Article

References (63)

1. Dinh, T., Scovell, S. & Veves, A. Peripheral arterial disease and diabetes: a clinical update. Int. J. Low. Extrem. Wounds 8, 75-81 (2009).
2. Hinchliffe, R. J. et al. A systematic review of the effectiveness of revascularization of the ulcerated foot in patients with diabetes and peripheral arterial disease. Diabetes Metab. Res. Rev. 28(Suppl 1), 179-217 (2012).
3. Emanueli, C. et al. Prevention of diabetes-induced microangiopathy by human tissue kallikrein gene transfer. Circulation 106, 993-999 (2002).
4. Giacco, F. & Brownlee, M. Oxidative stress and diabetic complications. Circ. Res. 107, 1058-1070 (2010).
5. Hammes, H. P. et al. Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51, 3107-3112 (2002).
6. Siemionow, M. & Demir, Y. Diabetic neuropathy: pathogenesis and treatment. J. Reconstruct. Microsurg. 20, 241-252 (2004).
7. Tilton, R. G., Hoffmann, P. L., Kilo, C. & Williamson, J. R. Pericyte degeneration and basement membrane thickening in skeletal muscle capillaries of human diabetics. Diabetes 30, 326-334 (1981).
8. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
9. Quiat, D. & Olson, E. N. MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J. Clin. Invest. 123, 11-18 (2013).
10. Caporali, A. et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation 123, 282-291 (2011).
11. Caporali, A. et al. Neurotrophin p75 receptor (p75NTR) promotes endothelial cell apoptosis and inhibits angiogenesis: implications for diabetes-induced impaired neovascularization in ischemic limb muscles. Circ. Res. 103, e15-e26 (2008).
12. Salis, M. B. et al. Nerve growth factor supplementation reverses the impairment, induced by Type 1 diabetes, of hindlimb post-ischaemic recovery in mice. Diabetologia 47, 1055-1063 (2004).
13. Caporali, A. & Emanueli, C. Cardiovascular actions of neurotrophins. Physiol. Rev. 89, 279-308 (2009).
14. Zhang, Y. et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell 39, 133-144 (2010).
15. Zernecke, A. et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal. 2, ra81 (2009).
16. Hergenreider, E. et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14, 249-256 (2012).
17. Loyer, X., Vion, A. C., Tedgui, A. & Boulanger, C. M. Microvesicles as cell-cell messengers in cardiovascular diseases. Circ. Res. 114, 345-353 (2014).
18. Armulik, A., Abramsson, A. & Betsholtz, C. Endothelial/pericyte interactions. Circ. Res. 97, 512-523 (2005).
19. Caporali, A. et al. Soluble ST2 is regulated by p75 neurotrophin receptor and predicts mortality in diabetic patients with critical limb ischemia. Arterioscler. Thromb. Vasc. Biol. 32, e149-e160 (2012).
20. Byrd, A. E., Aragon, I. V. & Brewer, J. W. MicroRNA-30c-2∗ limits expression of proadaptive factor XBP1 in the unfolded protein response. J. Cell Biol. 196, 689-698 (2012).
21. Marin-Muller, C. et al. A tumorigenic factor interactome connected through tumor suppressor microRNA-198 in human pancreatic cancer. Clin. Cancer Res. 19, 5901-5913 (2013).
22. Liu, W. H. & Chang, L. S. Suppression of Akt/Foxp3-mediated miR-183 expression blocks Sp1-mediated ADAM17 expression and TNFalpha-mediated NFkappaB activation in piceatannol-treated human leukemia U937 cells. Biochem. Pharmacol. 84, 670-680 (2012).
23. Chien, C. H. et al. Identifying transcriptional start sites of human microRNAs based on high-throughput sequencing data. Nucleic Acids Res. 39, 9345-9356 (2011).
24. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
25. Oitzinger, W. et al. Adenovirus-mediated expression of a mutant IkappaB kinase 2 inhibits the response of endothelial cells to inflammatory stimuli. Blood 97, 1611-1617 (2001).
26. Vion, A. C. et al. Shear stress regulates endothelial microparticle release. Circ. Res. 112, 1323-1333 (2013).
27. Sapet, C. et al. Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood 108, 1868-1876 (2006).
28. Tesse, A. et al. Upregulation of proinflammatory proteins through NF-kappaB pathway by shed membrane microparticles results in vascular hyporeactivity. Arterioscler. Thromb. Vasc. Biol. 25, 2522-2527 (2005).
29. Sebbagh, M. et al. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3, 346-352 (2001).
30. Ibanez, C. F. & Simi, A. p75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Trends Neurosci. 35, 431-440 (2012).
31. Khromov, A., Choudhury, N., Stevenson, A. S., Somlyo, A. V. & Eto, M. Phosphorylation-dependent autoinhibition of myosin light chain phosphatase accounts for Ca2+ sensitization force of smooth muscle contraction. J. Biol. Chem. 284, 21569-21579 (2009).
32. Grimson, A. et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (2007).
33. Foo, S. S. et al. Ephrin-B2 controls cell motility and adhesion during bloodvessel-wall assembly. Cell 124, 161-173 (2006).
34. Darland, D. C. et al. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev. Biol. 264, 275-288 (2003).
35. Essayagh, S. et al. Microparticles from apoptotic vascular smooth muscle cells induce endothelial dysfunction, a phenomenon prevented by beta3-integrin antagonists. Thromb. Haemost. 94, 853-858 (2005).
36. Terrisse, A. D. et al. Internalization of microparticles by endothelial cells promotes platelet/endothelial cell interaction under flow. J. Thromb. Haemost. 8, 2810-2819 (2010).
37. O'Shea, J. C. & Tcheng, J. E. Eptifibatide: a potent inhibitor of the platelet receptor integrin glycoprotein IIb/IIIa. Exp. Opin. Pharmacother. 3, 1199-1210 (2002).
38. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2011).
39. El-Osta, A. et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J. Exp. Med. 205, 2409-2417 (2008).
40. Geevarghese, A. & Herman, I. M. Pericyte-endothelial crosstalk: implications and opportunities for advanced cellular therapies. Transl. Res. 163, 296-306 (2014).
41. Franco, M., Roswall, P., Cortez, E., Hanahan, D. & Pietras, K. Pericytes promote endothelial cell survival through induction of autocrine VEGF-A signaling and Bcl-w expression. Blood 118, 2906-2917 (2011).
42. Salvucci, O. et al. EphrinB reverse signaling contributes to endothelial and mural cell assembly into vascular structures. Blood 114, 1707-1716 (2009).
43. von Tell, D., Armulik, A. & Betsholtz, C. Pericytes and vascular stability. Exp. Cell Res. 312, 623-629 (2006).
44. Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
45. Daneman, R., Zhou, L., Kebede, A. A. & Barres, B. A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468, 562-566 (2010).
46. Hellstrom, M. et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153, 543-553 (2001).
47. Hammes, H. P. Pericytes and the pathogenesis of diabetic retinopathy. Horm. Metab. Res. 37(Suppl 1), 39-43 (2005).
48. Hayden, M. R. et al. Ultrastructure of islet microcirculation, pericytes and the islet exocrine interface in the HIP rat model of diabetes. Exp. Biol. Med. 233, 1109-1123 (2008).
49. Boon, R. A. & Vickers, K. C. Intercellular transport of microRNAs. Arterioscler. Thromb. Vasc. Biol. 33, 186-192 (2013).
50. Thery, C., Zitvogel, L. & Amigorena, S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579 (2002).
51. Koga, H. et al. Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J. Am. Coll. Cardiol. 45, 1622-1630 (2005).
52. Jansen, F. et al. Endothelial microparticle uptake in target cells is annexin I/phosphatidylserine receptor dependent and prevents apoptosis. Arterioscler. Thromb. Vasc. Biol. 32, 1925-1935 (2012).
53. Carnevale, E. et al. Regulation of postangiogenic neovessel survival by beta1 and beta3 integrins in collagen and fibrin matrices. J. Vasc. Res. 44, 40-50 (2007).
54. Sabatier, F. et al. Interaction of endothelial microparticles with monocytic cells in vitro induces tissue factor-dependent procoagulant activity. Blood 99, 3962-3970 (2002).
55. Campagnolo, P. et al. Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121, 1735-1745 (2010).
56. Caporali, A. & Emanueli, C. MicroRNA regulation in angiogenesis. Vascul. Pharmacol. 55, 79-86 (2011).
57. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108 (2008).
58. Robert, S. et al. High-sensitivity flow cytometry provides access to standardized measurement of small-size microparticles-brief report. Arterioscler. Thromb. Vasc. Biol. 32, 1054-1058 (2012).
59. Lahtinen, U., Honsho, M., Parton, R. G., Simons, K. & Verkade, P. Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. FEBS Lett. 538, 85-88 (2003).
60. Lee, K. F. et al. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749 (1992).
61. Emanueli, C. et al. Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia. Circulation 103, 125-132 (2001).
62. Larsson, E. et al. Discovery of microvascular miRNAs using public gene expression data: miR-145 is expressed in pericytes and is a regulator of Fli1. Genome Med. 1, 108 (2009).
63. Radu, M. & Chernoff, J. An in vivo assay to test blood vessel permeability. J. Vis. Exp. 16, e50062 (2013).