MicroRNA and mRNA cargo of extracellular vesicles from porcine adipose tissue-derived mesenchymal stem cells

Gene

Volumn 551, Issue 1, 2014, Pages 55-64

  Eirin, Alfonso ^a   Riester, Scott M ^a   Zhu, Xiang Yang ^a   Tang, Hui ^a   Evans, Jared M ^a   O'Brien, Daniel ^a   van Wijnen, Andre J ^a   Lerman, Lilach O ^a  

^a MAYO CLINIC   (United States)

Author keywords

Exosomes; Extracellular vesicles; Gene expression; Mesenchymal stem cells; Microvesicles; MiRNA; Next generation sequencing (NGS); RNASeq

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 148A; MICRORNA 378; MICRORNA 532-5P; MICRORNA LET 7F; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADIPOSE TISSUE; ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARRB1 GENE; ARTICLE; CALCIUM SIGNALING; CEBPA GENE; CELL TRANSPORT; CYTOSKELETON GENE; FEMALE; GENE; GENE EXPRESSION; GENE ONTOLOGY; GOLGA4 GENE; GOLGI COMPLEX; HES1 GENE; HGF GENE; HIGH THROUGHPUT SEQUENCING; KLF7 GENE; MDFIC GENE; MESENCHYMAL STEM CELL; MITOCHONDRION; NONHUMAN; NRIP1 GENE; POU3F1 GENE; PROTEIN DEGRADATION; RNA SEQUENCE; SWINE; TCF4 GENE; ANIMAL; CELL CULTURE; CYTOLOGY; EXOSOME; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; PIG;

SUS;

ADIPOSE TISSUE; ANIMALS; CELLS, CULTURED; EXOSOMES; GENE EXPRESSION REGULATION; GENE ONTOLOGY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MESENCHYMAL STROMAL CELLS; MICRORNAS; RNA, MESSENGER; SWINE; TRANSCRIPTION FACTORS;

EID: 84907521913     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2014.08.041     Document Type: Article

References (59)

1. Baker S.J., Ma'ayan A., Lieu Y.K., John P., Reddy M.V.R., Chen E.Y., Duan Q., Snoeck H.-W., Reddy E.P. B-myb is an essential regulator of hematopoietic stem cell and myeloid progenitor cell development. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:3122-3127.
2. Birkenmeier E.H., Gwynn B., Howard S., Jerry J., Gordon J.I., Landschulz W.H., McKnight S.L. Tissue-specific expression, developmental regulation, and genetic mapping of the gene encoding CCAAT/enhancer binding protein. Genes Dev. 1989, 3:1146-1156.
3. Blanchette F., Day R., Dong W., Laprise M.H., Dubois C.M. TGFbeta1 regulates gene expression of its own converting enzyme furin. J. Clin. Invest. 1997, 99:1974-1983.
4. Broad K.D., Curley J.P., Keverne E.B. Increased apoptosis during neonatal brain development underlies the adult behavioral deficits seen in mice lacking a functional paternally expressed gene 3 (Peg3). Dev. Neurobiol. 2009, 69:314-325.
5. Bruno S., Grange C., Collino F., Deregibus M.C., Cantaluppi V., Biancone L., Tetta C., Camussi G. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 2012, 7:e33115.
6. Charbord P. Bone marrow mesenchymal stem cells: historical overview and concepts. Hum. Gene Ther. 2010, 21:1045-1056.
7. Corrado C., Raimondo S., Chiesi A., Ciccia F., De Leo G., Alessandro R. Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int. J. Mol. Sci. 2013, 14:5338-5366.
8. Dudakovic A., Camilleri E.T., Lewallen E.A., McGee-Lawrence M.E., Riester S.M., Kakar S., Montecino M., Stein G.S., Ryoo H.M., Dietz A.B., Westendorf J.J., van Wijnen A.J. Histone deacetylase inhibition destabilizes the multi-potent state of uncommitted adipose-derived mesenchymal stromal cells. J. Cell. Physiol. 2014, Jun 9. http://dx.doi.org/10.1002/jcp.24680 (Epub ahead of print).
9. Dudakovic A., Camilleri E., Riester S.M., Lewallen E.A., Kvasha S., Chen X., Radel D.J., Anderson J.M., Nair A.A., Evans J.M., Krych A.J., Smith J., Deyle D.R., Stein J.L., Stein G.S., Im H.J., Cool S.M., Westendorf J.J., Kakar S., Dietz A.B., van Wijnen A.J. High-resolution molecular validation of self-renewal and spontaneous differentiation in adipose-tissue derived human mesenchymal stem cells. J. Cell. Biochem 2014, 115:1816-1828.
10. Ebrahimi B., Eirin A., Li Z., Zhu X.Y., Zhang X., Lerman A., Textor S.C., Lerman L.O. Mesenchymal stem cells improve medullary inflammation and fibrosis after revascularization of swine atherosclerotic renal artery stenosis. PLoS One 2013, 8:e67474.
11. Eirin A., Zhu X.-Y., Krier J.D., Tang H., Jordan K.L., Grande J.P., Lerman A., Textor S.C., Lerman L.O. Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells 2012, 30:1030-1041.
12. Gervais F.G., Singaraja R., Xanthoudakis S., Gutekunst C.-A., Leavitt B.R., Metzler M., Hackam A.S., Tam J., Vaillancourt J.P., Houtzager V., Rasper D.M., Roy S., Hayden M.R., Nicholson D.W. Recruitment and activation of caspase-8 by the huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat. Cell Biol. 2002, 4:95-105.
13. Giraud-Triboult K., Rochon-Beaucourt C., Nissan X., Champon B., Aubert S., Pietu G. Combined mRNA and microRNA profiling reveals that miR-148a and miR-20b control human mesenchymal stem cell phenotype via EPAS1. Physiol. Genomics 2011, 43:77-86.
14. Herencia C., Martinez-Moreno J.M., Herrera C., Corrales F., Santiago-Mora R., Espejo I., Barco M., Almaden Y., de la Mata M., Rodriguez-Ariza A., Munoz-Castaneda J.R. Nuclear translocation of beta-catenin during mesenchymal stem cells differentiation into hepatocytes is associated with a tumoral phenotype. PLoS One 2012, 7:e34656.
15. Herrera M.B., Fonsato V., Gatti S., Deregibus M.C., Sordi A., Cantarella D., Calogero R., Bussolati B., Tetta C., Camussi G. Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J. Cell. Mol. Med. 2010, 14:1605-1618.
16. Hill M.A., Schedlich L., Gunning P. Serum-induced signal transduction determines the peripheral location of beta-actin mRNA within the cell. J. Cell Biol. 1994, 126:1221-1229.
17. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
18. Huang D.W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
19. Hulsmans M., Holvoet P. Microrna-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc. Res. 2013, 100:7-18.
20. Hung F.C., Chang Y., Lin-Chao S., Chao C.C. Gas7 mediates the differentiation of human bone marrow-derived mesenchymal stem cells into functional osteoblasts by enhancing Runx2-dependent gene expression. J. Orthop. Res. 2011, 29:1528-1535.
21. Hunkapiller J., Shen Y., Diaz A., Cagney G., McCleary D., Ramalho-Santos M., Krogan N., Ren B., Song J.S., Reiter J.F. Polycomb-like 3 promotes polycomb repressive complex 2 binding to CpG islands and embryonic stem cell self-renewal. PLoS Genet. 2012, 8:e1002576.
22. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
23. Kakinuma T., Ichikawa H., Tsukada Y., Nakamura T., Toh B.-H. Interaction between p230 and MACF1 is associated with transport of a glycosyl phosphatidyl inositol-anchored protein from the Golgi to the cell periphery. Exp. Cell Res. 2004, 298:388-398.
24. Kalari K.R., Nair A.A., Bhavsar J.D., O'Brien D.R., Davila J.I., Bockol M.A., Nie J., Tang X., Baheti S., Doughty J.B., Middha S., Sicotte H., Thompson A.E., Asmann Y.W., Kocher J.P. MAP-RSeq: Mayo analysis pipeline for RNA sequencing. BMC Bioinforma. 2014, 15:224.
25. Kamato D., Burch M.L., Piva T.J., Rezaei H.B., Rostam M.A., Xu S., Zheng W., Little P.J., Osman N. Transforming growth factor-beta signalling: role and consequences of Smad linker region phosphorylation. Cell. Signal. 2013, 25:2017-2024.
26. Kawamura Y., Tanaka Y., Kawamori R., Maeda S. Overexpression of Kruppel-like factor 7 regulates adipocytokine gene expressions in human adipocytes and inhibits glucose-induced insulin secretion in pancreatic beta-cell line. Mol. Endocrinol. 2006, 20:844-856.
27. Kiem H.-P., Ironside C., Beard B.C., Trobridge G.D. A retroviral vector common integration site between leupaxin and zinc finger protein 91 (ZFP91) observed in baboon hematopoietic repopulating cells. Exp. Hematol. 2010, 38:819-822. (822.e811-813).
28. Kim D., Pertea G., Trapnell C., Pimentel H., Kelley R., Salzberg S.L. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013, 14:R36.
29. Kitagawa M., Hojo M., Imayoshi I., Goto M., Ando M., Ohtsuka T., Kageyama R., Miyamoto S. Hes1 and Hes5 regulate vascular remodeling and arterial specification of endothelial cells in brain vascular development. Mech. Dev. 2013, 130:458-466.
30. Kunter U., Rong S., Boor P., Eitner F., Muller-Newen G., Djuric Z., van Roeyen C.R., Konieczny A., Ostendorf T., Villa L., Milovanceva-Popovska M., Kerjaschki D., Floege J. Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J. Am. Soc. Nephrol. 2007, 18:1754-1764.
31. Lai R.C., Chen T.S., Lim S.K. Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease. Regen. Med. 2011, 6:481-492.
32. Lalu M.M., McIntyre L., Pugliese C., Fergusson D., Winston B.W., Marshall J.C., Granton J., Stewart D.J. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One 2012, 7:e47559. Canadian Critical Care Trials G.
33. Lee H.K., Lim S.H., Chung I.S., Park Y., Park M.J., Kim J.Y., Kim Y.G., Hong J.T., Kim Y., Han S.-B. Preclinical efficacy and mechanisms of mesenchymal stem cells in animal models of autoimmune diseases. Immune Netw. 2014, 14:81-88.
34. Li Q., Lozano G. Molecular pathways: targeting Mdm2 and Mdm4 in cancer therapy. Clin. Cancer Res. 2013, 19:34-41.
35. Li Z., Gilbert J.A., Zhang Y., Zhang M., Qiu Q., Ramanujan K., Shavlakadze T., Eash J.K., Scaramozza A., Goddeeris M.M., Kirsch D.G., Campbell K.P., Brack A.S., Glass D.J. An HMGA2-IGF2BP2 axis regulates myoblast proliferation and myogenesis. Dev. Cell 2012, 23:1176-1188.
36. Liao Y., Smyth G.K., Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014, 30:923-930.
37. Lightowlers R.N., Rozanska A., Chrzanowska-Lightowlers Z.M. Mitochondrial protein synthesis: figuring the fundamentals, complexities and complications, of mammalian mitochondrial translation. FEBS Lett 2014, 588:2496-2503.
38. Lu R., Qu Y., Ge J., Zhang L., Su Z., Pflugfelder S.C., Li D.Q. Transcription factor TCF4 maintains the properties of human corneal epithelial stem cells. Stem Cells 2012, 30:753-761.
39. Madison B.B., Liu Q., Zhong X., Hahn C.M., Lin N., Emmett M.J., Stanger B.Z., Lee J.-S., Rustgi A.K. LIN28B promotes growth and tumorigenesis of the intestinal epithelium via let-7. Genes Dev. 2013, 27:2233-2245.
40. Mahaira L.G., Katsara O., Pappou E., Iliopoulou E., Fortis S., Antsaklis A., Fotinopoulos P., Baxevanis C.N., Papamichail M., Perez S.A. IGF2BP1 expression in human mesenchymal stem cells significantly affects their proliferation and is under the epigenetic control of TET1/2 demethylases. Stem Cells Dev. 2014, Jul 14 (Epub ahead of print).
41. Maruotti N., Corrado A., Neve A., Cantatore F.P. Systemic effects of Wnt signaling. J. Cell. Physiol. 2013, 228:1428-1432.
42. Mathiasen A.B., Haack-Sorensen M., Kastrup J. Mesenchymal stromal cells for cardiovascular repair: current status and future challenges. Futur. Cardiol. 2009, 5:605-617.
43. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J. Proteome 2010, 73:1907-1920.
44. Morishita R., Nakamura S., Hayashi S., Taniyama Y., Moriguchi A., Nagano T., Taiji M., Noguchi H., Takeshita S., Matsumoto K., Nakamura T., Higaki J., Ogihara T. Therapeutic angiogenesis induced by human recombinant hepatocyte growth factor in rabbit hind limb ischemia model as cytokine supplement therapy. Hypertension 1999, 33:1379-1384.
45. Moriyama H., Moriyama M., Isshi H., Ishihara S., Okura H., Ichinose A., Ozawa T., Matsuyama A., Hayakawa T. Role of notch signaling in the maintenance of human mesenchymal stem cells under hypoxic conditions. Stem Cells Dev. 2014, Aug 5 (Epub ahead of print).
46. Robinson M.D., McCarthy D.J., Smyth G.K. Edger: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
47. Sobie E.A., Lederer W.J. Dynamic local changes in sarcoplasmic reticulum calcium: physiological and pathophysiological roles. J. Mol. Cell. Cardiol. 2012, 52:304-311.
48. Stewart N., Chade A.R. Renoprotective effects of hepatocyte growth factor in the stenotic kidney. Am. J. Physiol. Renal Physiol. 2013, 304:F625-F633.
49. Sun Z., Evans J., Bhagwate A., Middha S., Bockol M., Yan H., Kocher J.P. Cap-miRSeq: a comprehensive analysis pipeline for microRNA sequencing data. BMC Genomics 2014, 15:423.
50. Swindle M.M., Makin A., Herron A.J., Clubb F.J., Frazier K.S. Swine as models in biomedical research and toxicology testing. Vet. Pathol. 2012, 49:344-356.
51. Tang Q.Q., Gronborg M., Huang H., Kim J.W., Otto T.C., Pandey A., Lane M.D. Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9766-9771.
52. Timmers L., Lim S.K., Arslan F., Armstrong J.S., Hoefer I.E., Doevendans P.A., Piek J.J., El Oakley R.M., Choo A., Lee C.N., Pasterkamp G., de Kleijn D.P.V. Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium. Stem Cell Res. 2007, 1:129-137.
53. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mrnas and micrornas is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
54. Wang X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 2008, 14:1012-1017.
55. Wu X., Oatley J.M., Oatley M.J., Kaucher A.V., Avarbock M.R., Brinster R.L. The POU domain transcription factor POU3F1 is an important intrinsic regulator of GDNF-induced survival and self-renewal of mouse spermatogonial stem cells. Biol. Reprod. 2010, 82:1103-1111.
56. Yeo R.W.Y., Lai R.C., Zhang B., Tan S.S., Yin Y., Teh B.J., Lim S.K. Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv. Drug Deliv. Rev. 2013, 65:336-341.
57. Yu J., Li Q., Xu Q., Liu L., Jiang B. MiR-148a inhibits angiogenesis by targeting ERBB3. J. Biomed. Res. 2011, 25:170-177.
58. Zhang H., Li Y., Huang Q., Ren X., Hu H., Sheng H., Lai M. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ. 2011, 18:1702-1710.
59. Zhu X.-Y., Urbieta-Caceres V., Krier J.D., Textor S.C., Lerman A., Lerman L.O. Mesenchymal stem cells and endothelial progenitor cells decrease renal injury in experimental swine renal artery stenosis through different mechanisms. Stem Cells 2013, 31:117-125.