Adipose-derived stem cells induce angiogenesis via microvesicle transport of miRNA-31

Stem Cells Translational Medicine

Volumn 5, Issue 4, 2016, Pages 440-450

  Kang, Ting ^a,b   Jones, Tia M ^b   Naddell, Clayton ^b   Bacanamwo, Methode ^b   Calvert, John W ^c   Thompson, Winston E ^b   Bond, Vincent C ^b   Eugene Chen, Y ^d   Liu, Dong ^b  

^a NANCHANG UNIVERSITY   (China)

^b MOREHOUSE SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Adipose stem cell; Angiogenesis; Endothelial cell; Microvesicle; miRNA

Indexed keywords

LUCIFERASE; MATRIGEL; MICRORNA 31; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MIRN31 MICRORNA, MOUSE;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; ANGIOGENIC GENE THERAPY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MIGRATION ASSAY; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LENTIVIRINAE; MEMBRANE MICROPARTICLE; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SPECTROPHOTOMETRY; TUBE FORMATION ASSAY; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VASCULAR RING; WESTERN BLOTTING; ADIPOSE TISSUE; ADULT STEM CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL MOTION; CYTOLOGY; GENETICS; MALE; METABOLISM; MICROVASCULATURE; NUDE MOUSE; PHYSIOLOGY;

ADIPOSE TISSUE; ADULT STEM CELLS; ANIMALS; CELL MOVEMENT; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; MICRORNAS; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84961253699     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0177     Document Type: Article

References (66)

1. Gupta R, Tongers J, Losordo DW. Human studies of angiogenic gene therapy. Circ Res 2009;105:724–736.
2. Beohar N, Rapp J, Pandya S et al. Rebuilding thedamaged heart: The potential of cytokines and growth factors in the treatment of ischemic heart disease. J Am Coll Cardiol 2010;56:1287–1297.
3. Tongers J, Losordo DW, Landmesser U. Stem and progenitor cell-based therapy in ischaemic heart disease: Promise, uncertainties, and challenges. Eur Heart J 2011; 32:1197–1206.
4. Madonna R, Geng YJ, De Caterina R. Adipose tissue-derived stem cells: Characterization and potential for cardiovascular repair. Arterioscler Thromb Vasc Biol 2009;29:1723–1729.
5. Cai X, Lin Y, Hauschka PV et al. Adipose stem cells originate from perivascular cells. Biol Cell 2011;103:435–447.
6. Szöke K, Brinchmann JE. Concise review: Therapeutic potential of adipose tissue-derived angiogenic cells. STEMCELLSTRANSLATIONALMEDICINE 2012;1:658–667.
7. Cronk SM, Kelly-Goss MR, Ray HC et al. Adipose-derived stem cells from diabetic mice showimpaired vascular stabilization in a murine model of diabetic retinopathy. STEM CELLS TRANSLATIONAL MEDICINE 2015;4:459–467.
8. Miranville A, Heeschen C, Sengenès C et al. Improvement of postnatal neovascularization byhumanadipose tissue-derived stem cells. Circulation 2004;110:349–355.
9. Nakagami H, Maeda K, Morishita R et al. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 2005; 25:2542–2547.
10. Valina C, Pinkernell K, Song YH et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 2007; 28:2667–2677.
11. Camussi G, Deregibus MC, Bruno S et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78:838–848.
12. Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 2013;200:373–383.
13. Martinez MC, Andriantsitohaina R. Microparticles in angiogenesis: Therapeutic potential. Circ Res 2011;109:110–119.
14. Ratajczak MZ, Kucia M, Jadczyk T et al. Pivotal role of paracrine effects in stemcell therapies in regenerativemedicine: Can wetranslate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia 2012;26:1166–1173.
15. Lopatina T, Bruno S, Tetta C et al. Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential. Cell Commun Signal 2014;12:26.
16. Marędziak M, Marycz K, Lewandowski D et al. Static magnetic field enhances synthesis andsecretionofmembrane-derivedmicrovesicles (MVs) rich in VEGF and BMP-2 in equine adiposederived stromal cells (EqASCs)-a new approach in veterinary regenerativemedicine. InVitro CellDev Biol Anim 2015;51:230–240.
17. Farinazzo A, Turano E, Marconi S et al. Murine adipose-derived mesenchymal stromal cell vesicles: In vitro clues for neuroprotective and neuroregenerative approaches. Cytotherapy 2015;17:571–578.
18. Lai RC, Chen TS, Lim SK. Mesenchymal stemcell exosome: A novel stemcell-based therapy for cardiovascular disease. Regen Med 2011; 6:481–492.
19. Ratajczak J, Miekus K, Kucia M et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006;20:847–856.
20. 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.
21. Skog J, Würdinger T, van Rijn S et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008;10: 1470–1476.
22. Valadi H, Ekström K, Bossios A et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9:654–659.
23. Chen TS, Lai RC, Lee MM et al. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res 2010;38:215–224.
24. Eirin A, Riester SM, Zhu XY et al. Micro-RNA and mRNA cargo of extracellular vesicles from porcine adipose tissue-derived mesenchymal stem cells. Gene 2014;551: 55–64.
25. Park JE, Tan HS, Datta A et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010;9:1085–1099.
26. Lai RC, Arslan F, Lee MM et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2010;4:214–222.
27. Sahoo S, Klychko E, Thorne T et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res 2011;109:724–728.
28. Arslan F, Lai RC, Smeets MB et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2013;10:301–312.
29. Trajkovic K, Hsu C, Chiantia S et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008;319: 1244–1247.
30. Ali SA, Huang MB, Campbell PE et al. Genetic characterization of HIV type 1. Nef-induced vesicle secretion. AIDS Res Hum Retroviruses 2010;26:173–192.
31. Liu D, Hou J, Hu X et al. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ Res 2006;98:480–489.
32. Kang T, Lu W, Xu W et al. MicroRNA-27 (miR-27) targets prohibitin and impairs adipocyte differentiation and mitochondrial function in human adipose-derived stem cells. J Biol Chem 2013;288:34394–34402.
33. Soo CY, Song Y, Zheng Y et al. Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology 2012;136:192–197.
34. Liu CJ, Tsai MM, Hung PS et al. miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res 2010;70: 1635–1644.
35. Liu D, Lin Y, Kang T et al. Mitochondrial dysfunction and adipogenic reduction by prohibitin silencing in 3T3-L1 cells. PLoS One 2012;7:e34315.
36. Wei Y, Gong J, Thimmulappa RK et al. Nrf2 acts cell-autonomously in endothelium to regulate tip cell formation and vascular branching. Proc Natl Acad Sci USA 2013;110: E3910–E3918.
37. Jain S, Gabunia K, Kelemen SE et al. The anti-inflammatory cytokine interleukin 19 is expressed by and angiogenic for human endothelial cells. Arterioscler Thromb Vasc Biol 2011;31:167–175.
38. Pang X, Yi T, Yi Z et al. Morelloflavone, a biflavonoid, inhibits tumor angiogenesis by targeting rho GTPases and extracellular signal-regulated kinase signaling pathways. Cancer Res 2009;69:518–525.
39. Brill A, Dashevsky O, Rivo J et al. Plateletderived microparticles induce angiogenesis and stimulate post-ischemic revascularization. Cardiovasc Res 2005;67:30–38.
40. Wu YH, Hu TF, Chen YC et al. The manipulation of miRNA-gene regulatory networks by KSHV induces endothelial cell motility. Blood 2011;118:2896–2905.
41. Benndorf RA, Schwedhelm E, Gnann A et al. Isoprostanes inhibit vascular endothelial growth factor-induced endothelial cell migration, tube formation, and cardiac vessel sprouting in vitro, as well as angiogenesis in vivo via activation of the thromboxane A(2) receptor: A potential link between oxidative stress and impaired angiogenesis. Circ Res 2008;103: 1037–1046.
42. Albig AR, Schiemann WP. Identification and characterization of regulator of G protein signaling 4 (RGS4) as a novel inhibitor of tubulogenesis: RGS4 inhibits mitogen-activated protein kinases and vascular endothelial growth factor signaling. Mol Biol Cell 2005; 16:609–625.
43. Suárez Y, Sessa WC. MicroRNAs as novel regulators of angiogenesis. Circ Res 2009;104: 442–454.
44. Wang S, Olson EN. AngiomiRs–key regulators of angiogenesis. Curr Opin Genet Dev 2009;19:205–211.
45. Chang SH, Hla T. Gene regulation by RNA binding proteins and microRNAs in angiogenesis. Trends Mol Med 2011;17:650–658.
46. Patella F, Rainaldi G. MicroRNAs mediate metabolic stresses and angiogenesis. Cell Mol Life Sci 2012;69:1049–1065.
47. Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med 2012;4: 3–14.
48. Suárez Y, Fernández-Hernando C, Yu J et al. Dicer-dependent endothelial micro-RNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA 2008;105: 14082–14087.
49. Greco S, De Simone M, Colussi C et al. Commonmicro-RNAsignature in skeletalmuscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J 2009;23:3335–3346.
50. Wang HW, Huang TS, Lo HH et al. Deficiency of the microRNA-31-microRNA-720 pathway in the plasma and endothelial progenitor cells from patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2014;34: 857–869.
51. Huang M, Nguyen P, Jia F et al. Double knockdown of prolyl hydroxylase and factorinhibiting hypoxia-inducible factor with nonviral minicircle gene therapy enhances stem cell mobilization and angiogenesis after myocardial infarction. Circulation 2011;124(suppl): S46–S54.
52. Ashton AW, Cheng Y, Helisch A et al. Thromboxane A2 receptor agonists antagonize the proangiogenic effects of fibroblast growth factor-2: Role of receptor internalization, thrombospondin-1, and alpha(v)beta3. Circ Res 2004;94:735–742.
53. Lee SH, Kunz J, Lin SH et al. 16-kDa prolactin inhibits endothelial cell migration by down-regulating the Ras-Tiam1-Rac1-Pak1 signaling pathway. Cancer Res 2007;67: 11045–11053.
54. Cottonham CL, Kaneko S, Xu L. miR-21 and miR-31 converge on TIAM1 to regulate migration and invasion of colon carcinoma cells. J Biol Chem 2010;285:35293–35302.
55. Zhang T, Wang Q, Zhao D et al. The oncogenetic role of microRNA-31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond) 2011;121: 437–447.
56. Jaba IM, Zhuang ZW, Li N et al. NO triggers RGS4 degradation to coordinate angiogenesis and cardiomyocyte growth. J Clin Invest 2013;123:1718–1731.
57. Roccaro AM, Sacco A, Maiso P et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 2013;123:1542–1555.
58. Cantaluppi V, Gatti S, Medica D et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemiareperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int 2012;82:412–427.
59. Valastyan S, Reinhardt F, Benaich N et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis [retracted Cell. 2015. Apr 9;161(2):417]. Cell 2009;137: 1032–1046.
60. Krek A, Grün D, Poy MN et al. Combinatorial microRNA target predictions. Nat Genet 2005;37:495–500.
61. Tsai YH, Wu MF, Wu YH et al. TheMtype K15 protein of Kaposi’s sarcoma-associated herpesvirus regulates microRNA expression via its SH2-binding motif to induce cell migration and invasion. J Virol 2009;83:622–632.
62. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004; 116:281–297.
63. Peng H, Kaplan N, Hamanaka RB et al. microRNA-31/factor-inhibiting hypoxia-inducible factor 1 nexus regulates keratinocyte differentiation. Proc Natl Acad Sci USA 2012;109: 14030–14034.
64. Lando D, Peet DJ, Gorman JJ et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxiainducible factor. GenesDev 2002;16:1466–1471.
65. Rey S, Semenza GL. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 2010;86:236–242.
66. Castanotto D, Rossi JJ. The promises and pitfalls of RNA-interference-based therapeutics. Nature 2009;457:426–433.