Hypoxia Inducible Factor-1α Potentiates Jagged 1-Mediated Angiogenesis by Mesenchymal Stem Cell-Derived Exosomes

Stem Cells

Volumn 35, Issue 7, 2017, Pages 1747-1759

  Gonzalez King, Hernán ^a   García, Nahuel A ^a   Ontoria Oviedo, Imelda ^a   Ciria, María ^a   Montero, José Anastasio ^a   Sepúlveda, Pilar ^a  

^a INSTITUTO DE INVESTIGACIÓN SANITARIA DEL HOSPITAL CLÍNICO SAN CARLOS IDISSC   (Spain)

Author keywords

Angiogenesis; Exosomes; Hypoxia inducible factor; Jagged 1; Mesenchymal stem cells

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; NOTCH RECEPTOR; PROTEIN JAGGED 1; CD63 ANTIGEN; CD63 PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; HIF1A PROTEIN, HUMAN; NEUTRALIZING ANTIBODY; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXOME; EXOSOME; FLUORESCENCE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF QUANTITATION; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL HYPOXIA; CHEMISTRY; COCULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; NUDE MOUSE; PRIMARY CELL CULTURE; REPORTER GENE; TOOTH PULP; XENOGRAFT;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELL HYPOXIA; COCULTURE TECHNIQUES; DENTAL PULP; EXOSOMES; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; JAGGED-1 PROTEIN; LUMINESCENT PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, NUDE; NEOVASCULARIZATION, PHYSIOLOGIC; PRIMARY CELL CULTURE; TETRASPANIN 30; TRANSDUCTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS;

EID: 85018933821     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2618     Document Type: Article

References (66)

1. Karantalis V, Hare JM. Use of mesenchymal stem cells for therapy of cardiac disease. Circ Res 2015;116:1413–1430.
2. Phinney DG, Prockop DJ. Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair–current views. Stem Cells 2007;25:2896–2902.
3. Satija NK, Singh VK, Verma YK et al. Mesenchymal stem cell-based therapy: A new paradigm in regenerative medicine. J Cell Mol Med 2009;13:4385–4402.
4. Lu D, Chen B, Liang Z et al. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: A double-blind, randomized, controlled trial. Diab Res Clin Pract 2011;92:26–36.
5. Samper E, Diez-Juan A, Montero JA et al. Cardiac cell therapy: Boosting mesenchymal stem cells effects. Stem Cell Rev 2013;9:266–280.
6. Rosova I, Dao M, Capoccia B et al. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008;26:2173–2182.
7. Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit Rev Oncol Hematol 2006;59:15–26.
8. Semenza GL. Hypoxia-inducible factor 1: Master regulator of O2 homeostasis. Curr Opin Genet Dev 1998;8:588–594.
9. Cerrada I, Ruiz-Sauri A, Carrero R et al. Hypoxia-inducible factor 1 alpha contributes to cardiac healing in mesenchymal stem cells-mediated cardiac repair. Stem Cells Dev 2013;22:501–511.
10. Gnecchi M, He H, Noiseux N et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006;20:661–669.
11. Lu A, Pfeffer SR. A CULLINary ride across the secretory pathway: More than just secretion. Trend Cell Biol 2014;24:389–399.
12. Mittelbrunn M, Sanchez-Madrid F. Intercellular communication: Diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 2012;13:328–335.
13. Clayton A, Turkes A, Dewitt S et al. Adhesion and signaling by B cell-derived exosomes: The role of integrins. FASEB J 2004;18:977–979.
14. Morelli AE, Larregina AT, Shufesky WJ et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004;104:3257–3266.
15. Deregibus MC, Cantaluppi V, Calogero R et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007;110:2440–2448.
16. Janowska-Wieczorek A, Majka M, Kijowski J et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood 2001;98:3143–3149.
17. Hoshino A, Costa-Silva B, Shen TL et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015;527:329–335.
18. Marino J, Babiker-Mohamed MH, Crosby-Bertorini P et al. Donor exosomes rather than passenger leukocytes initiate alloreactive T cell responses after transplantation. Sci Immunol 2016;1:
19. Garcia NA, Moncayo-Arlandi J, Sepulveda P et al. Cardiomyocyte exosomes regulate glycolytic flux in endothelium by direct transfer of GLUT transporters and glycolytic enzymes. Cardiovascular Res 2016;109:397–408.
20. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: Cell fate control and signal integration in development. Science 1999;284:770–776.
21. Gridley T. Human genetics. Notch, stroke and dementia. Nature 1996;383:673.
22. Limbourg FP, Takeshita K, Radtke F et al. Essential role of endothelial Notch1 in angiogenesis. Circulation 2005;111:1826–1832.
23. Olsauskas-Kuprys R, Zlobin A, Osipo C. Gamma secretase inhibitors of Notch signaling. Onco Target Ther 2013;6:943–955.
24. Sassoli C, Pini A, Mazzanti B et al. Mesenchymal stromal cells affect cardiomyocyte growth through juxtacrine Notch-1/Jagged-1 signaling and paracrine mechanisms: Clues for cardiac regeneration. J Mol Cell Cardiol 2011;51:399–408.
25. Diez H, Fischer A, Winkler A et al. Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp Cell Res 2007;313:1–9.
26. D'Souza B, Miyamoto A, Weinmaster G. The many facets of Notch ligands. Oncogene 2008;27:5148–5167.
27. Meier-Stiegen F, Schwanbeck R, Bernoth K et al. Activated Notch1 target genes during embryonic cell differentiation depend on the cellular context and include lineage determinants and inhibitors. PloS One 2010;5:e11481.
28. Sheldon H, Heikamp E, Turley H et al. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 2010;116:2385–2394.
29. Benedito R, Roca C, Sorensen I et al. The notch ligands Dll4 and Jagged 1 have opposing effects on angiogenesis. Cell 2009;137:1124–1135.
30. Thery C, Amigorena S, Raposo G et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006;Chapter 3:Unit 3 22.
31. Garcia NA, Ontoria-Oviedo I, Gonzalez-King H et al. Glucose Starvation in cardiomyocytes enhances exosome secretion and promotes angiogenesis in endothelial cells. PloS One 2015;10:e0138849.
32. Manderfield LJ, High FA, Engleka KA et al. Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation 2012;125:314–323.
33. Malinda KM. In vivo matrigel migration and angiogenesis assay. Methods Mol Biol 2009;467:287–294.
34. King HW, Michael MZ, Gleadle JM. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012;12:421.
35. Savina A, Vidal M, Colombo MI. The exosome pathway in K562 cells is regulated by Rab11. J Cell Sci 2002;115:2505–2515.
36. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009;9:581–593.
37. Buschow SI, Liefhebber JM, Wubbolts R et al. Exosomes contain ubiquitinated proteins. Blood Cells, Mol Dis 2005;35:398–403.
38. Smith VL, Jackson L, Schorey JS. Ubiquitination as a mechanism To Transport soluble mycobacterial and eukaryotic proteins to exosomes. J Immunol 2015;195:2722–2730.
39. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
40. Kang T, Jones TM, Naddell C et al. Adipose-derived stem cells induce angiogenesis via microvesicle transport of miRNA-31. Stem Cells Transl Med 2016;5:440–450.
41. Amado LC, Saliaris AP, Schuleri KH et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci USA 2005;102:11474–11479.
42. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003;108:863–868.
43. Gandia C, Arminan A, Garcia-Verdugo JM et al. Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction. Stem Cells 2008;26:638–645.
44. Kim SW, Han H, Chae GT et al. Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger's disease and ischemic limb disease animal model. Stem Cells 2006;24:1620–1626.
45. Capoccia BJ, Robson DL, Levac KD et al. Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity. Blood 2009;113:5340–5351.
46. Deuse T, Peter C, Fedak PW et al. Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction. Circulation 2009;120:S247–S254.
47. Ding W, Knox TR, Tschumper RC et al. Platelet-derived growth factor (PDGF)-PDGF receptor interaction activates bone marrow-derived mesenchymal stromal cells derived from chronic lymphocytic leukemia: Implications for an angiogenic switch. Blood 2010;116:2984–2993.
48. Fierro FA, Kalomoiris S, Sondergaard CS et al. Effects on proliferation and differentiation of multipotent bone marrow stromal cells engineered to express growth factors for combined cell and gene therapy. Stem Cells 2011;29:1727–1737.
49. Bronckaers A, Hilkens P, Martens W et al. Mesenchymal stem/stromal cells as a pharmacological and therapeutic approach to accelerate angiogenesis. Pharmacol Ther 2014;143:181–196.
50. Meyerrose T, Olson S, Pontow S et al. Mesenchymal stem cells for the sustained in vivo delivery of bioactive factors. Adv Drug Deliv Rev 2010;62:1167–1174.
51. Ma J, Zhao Y, Sun L et al. Exosomes derived from Akt-modified human umbilical cord mesenchymal stem cells improve cardiac regeneration and promote angiogenesis via activating platelet-derived growth factor D. Stem Cells Transl Med 2016.
52. Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C et al. Sorting it out: Regulation of exosome loading. Semin Cancer Biol 2014;28:3–13.
53. Bobrie A, Colombo M, Raposo G et al. Exosome secretion: Molecular mechanisms and roles in immune responses. Traffic 2011;12:1659–1668.
54. Wang T, Gilkes DM, Takano N et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci USA 2014;111:E3234–E3242.
55. Guimbellot JS, Erickson SW, Mehta T et al. Correlation of microRNA levels during hypoxia with predicted target mRNAs through genome-wide microarray analysis. BMC Med Genom 2009;2:15.
56. Kulshreshtha R, Ferracin M, Wojcik SE et al. A microRNA signature of hypoxia. Mol Cell Biol 2007;27:1859–1867.
57. Lee M, Rentz J, Bikram M et al. Hypoxia-inducible VEGF gene delivery to ischemic myocardium using water-soluble lipopolymer. Gene Ther 2003;10:1535–1542.
58. Mazumdar J, O'brien WT, Johnson RS et al. O2 regulates stem cells through Wnt/beta-catenin signalling. Nat Cell Biol 2010;12:1007–1013.
59. Wu C, Chen J, Chen C et al. Wnt/beta-catenin coupled with HIF-1alpha/VEGF signaling pathways involved in galangin neurovascular unit protection from focal cerebral ischemia. Sci Rep 2015;5:16151.
60. Qiang L, Wu T, Zhang HW et al. HIF-1alpha is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway. Cell Death Differ 2012;19:284–294.
61. Tian Q, Xue Y, Zheng W et al. Overexpression of hypoxia-inducible factor 1alpha induces migration and invasion through Notch signaling. Int J Oncol 2015;47:728–738.
62. Villa JC, Chiu D, Brandes AH et al. Nontranscriptional role of Hif-1alpha in activation of gamma-secretase and notch signaling in breast cancer. Cell Rep 2014;8:1077–1092.
63. Anderson JD, Johansson HJ, Graham CS et al. Comprehensive Proteomic Analysis of Mesenchymal Stem Cell Exosomes Reveals Modulation of Angiogenesis via Nuclear Factor-KappaB Signaling. Stem Cells 2016;34:601–613.
64. Dufraine J, Funahashi Y Kitajewski J. Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 2008;27:5132–5137.
65. Ge X, Han Z, Chen F et al. MiR-21 alleviates secondary blood-brain barrier damage after traumatic brain injury in rats. Brain Res 2015;1603:150–157.
66. Liu ZJ, Shirakawa T, Li Y et al. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: Implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol 2003;23:14–25.