Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species

Stem Cell Research and Therapy

Volumn 6, Issue 1, 2015, Pages

  Baglio, Serena Rubina ^a,b   Rooijers, Koos ^c   Koppers Lalic, Danijela ^b   Verweij, Frederik J ^b   Pérez Lanzón, M ^b   Zini, Nicoletta ^a,d   Naaijkens, Benno ^b   Perut, Francesca ^a   Niessen, Hans W M ^b   Baldini, Nicola ^a   Pegtel, D Michiel ^b  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSFER RNA; SMALL NUCLEOLAR RNA; 3' UNTRANSLATED REGION; RNA; TRANSCRIPTOME;

3' UNTRANSLATED REGION; ADIPOSE DERIVED STEM CELL; ADIPOSE MESENCHYMAL STEM CELL; ADULT; ARTICLE; BIOINFORMATICS; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CONFOCAL LASER MICROSCOPY; ELECTRON MICROSCOPY; EXOSOME; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA ISOLATION; RNA SEQUENCE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ADIPOSE DERIVED MESENCHYMAL STEM CELL; CELL COMMUNICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; GENETIC CONSERVATION; MESENCHYMAL STEM CELL; ADIPOSE TISSUE; BONE MARROW CELL; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENETICS; ISOLATION AND PURIFICATION; MESENCHYMAL STROMA CELL; METABOLISM; NUCLEOTIDE SEQUENCE; SECRETION (PROCESS); SEQUENCE ANALYSIS;

3' UNTRANSLATED REGIONS; ADIPOSE TISSUE; BASE SEQUENCE; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; EXOSOMES; HUMANS; MESENCHYMAL STROMAL CELLS; MICRORNAS; MICROSCOPY, ELECTRON; RNA; RNA, TRANSFER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84938697816     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-015-0116-z     Document Type: Article

References (85)

1. Farini A, Sitzia C, Erratico S, Meregalli M, Torrente Y. Clinical applications of mesenchymal stem cells in chronic diseases. Stem Cells Int. 2014;2014:306573.
2. Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466:829-34.
3. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-7.
4. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-7.
5. Johnson A, Dorshkind K. Stromal cells in myeloid and lymphoid long-term bone marrow cultures can support multiple hemopoietic lineages and modulate their production of hemopoietic growth factors. Blood. 1986;68:1348-54.
6. Schreml S, Babilas P, Fruth S, Orsó E, Schmitz G, Mueller MB, et al. Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy. 2009;11:947-57.
7. Al-Nbaheen M, vishnubalaji R, Ali D, Bouslimi A, Al-Jassir F, Megges M, et al. Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev Reports. 2013;9:32-43.
8. Bianco P, Cao X, Frenette PS, Mao JJ, Robey PG, Simmons PJ, et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med. 2013;19:35-42.
9. Ranganath SH, Levy O, Inamdar MS, Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell. 2012;10:244-58.
10. Tögel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol. 2005;289:F31-42.
11. Kordelas L, Rebmann V, Ludwig A-K, Radtke S, Ruesing J, Doeppner TR, et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia. 2014;28:970-3.
12. Baglio SR, Pegtel DM, Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Front Physiol. 2012;3:359.
13. Binato R, de Souza FT, Lazzarotto-Silva C, Du Rocher B, Mencalha A, Pizzatti L, et al. Stability of human mesenchymal stem cells during in vitro culture: considerations for cell therapy. Cell Prolif. 2013;46:10-22.
14. Wang Y, Zhang Z, Chi Y, Zhang Q, Xu F, Yang Z, et al. Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis. 2013;4:e950.
15. Behnan J, Isakson P, Joel M, Cilio C, Langmoen IA, Vik-Mo EO, et al. Recruited brain tumor-derived mesenchymal stem cells contribute to brain tumor progression. Stem Cells. 2014;32:1110-23.
16. Houthuijzen JM, Daenen LGM, Roodhart JML, Voest EE. The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression. Br J Cancer. 2012;106:1901-6.
17. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449:557-63.
18. Han I, Yun M, Kim E-O, Kim B, Jung M-H, Kim S-H. Umbilical cord tissue-derived mesenchymal stem cells induce apoptosis in PC-3 prostate cancer cells through activation of JNK and downregulation of PI3K/AKT signaling. Stem Cell Res Ther. 2014;5:54.
19. Xu C, Lin L, Cao G, Chen Q, Shou P, Huang Y, et al. Interferon-α-secreting mesenchymal stem cells exert potent antitumor effect in vivo. Oncogene. 2014;33:5047-52.
20. Mittelbrunn M, Sánchez-Madrid F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol. 2012;13:328-35.
21. Lai RC, Arslan F, Lee MM, Sze NSK, Choo A, Chen TS, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010;4:214-22.
22. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654-9.
23. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MAJ, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107:6328-33.
24. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun. 2011;2:282.
25. Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, et al. Cancer-Secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014;25:501-15.
26. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012;119:756-66.
27. Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012;31:3513-23.
28. Nolte-'t Hoen ENM, Buermans HPJ, Waasdorp M, Stoorvogel W, Wauben MHM, 't Hoen PAC. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 2012;40:9272-85.
29. Hill AF, Pegtel DM, Lambertz U, Leonardi T, O'Driscoll L, Pluchino S, et al. ISEV position paper: extracellular vesicle RNA analysis and bioinformatics. J Extracell Vesicles. 2013;2. doi: 10.3402/jev.v2i0.22859.
30. Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells. 2012;30:1556-64.
31. Zhang H-C, Liu X-B, Huang S, Bi X-Y, Wang H-X, Xie L-X, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells Dev. 2012;21:3289-97.
32. Reis LA, Borges FT, Simões MJ, Borges AA, Sinigaglia-Coimbra R, Schor N. Bone marrow-derived mesenchymal stem cells repaired but did not prevent gentamicin-induced acute kidney injury through paracrine effects in rats. PLoS One. 2012;7:e44092.
33. Zhou Y, Xu H, Xu W, Wang B, Wu H, Tao Y, et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res Ther. 2013;4:34.
34. Kim H-S, Choi D-Y, Yun SJ, Choi S-M, Kang JW, Jung JW, et al. Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J Proteome Res. 2012;11:839-49.
35. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, et al. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One. 2010;5:e11803.
36. Naaijkens BA, Niessen HWM, Prins H-J, Krijnen PAJ, Kokhuis TJA, de Jong N, et al. Human platelet lysate as a fetal bovine serum substitute improves human adipose-derived stromal cell culture for future cardiac repair applications. Cell Tissue Res. 2012;348:119-30.
37. De Korte D, Curvers J, de Kort WLAM, Hoekstra T, van der Poel CL, Beckers EAM, et al. Effects of skin disinfection method, deviation bag, and bacterial screening on clinical safety of platelet transfusions in the Netherlands. Transfusion. 2006;46:476-85.
38. Baglìo SR, Devescovi V, Granchi D, Baldini N. MicroRNA expression profiling of human bone marrow mesenchymal stem cells during osteogenic differentiation reveals Osterix regulation by miR-31. Gene. 2013;527:321-31.
39. Verweij FJ, Van Eijndhoven MAJ, Middeldorp J, Pegtel DM. Analysis of viral microRNA exchange via exosomes in vitro and in vivo. Methods Mol Biol. 2013;1024:53-68.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402-8.
41. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10-2.
42. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9.
43. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 2012;22:1760-74.
44. Griffiths-Jones S. The microRNA Registry. Nucleic Acids Res. 2004;32:D109-11.
45. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955-64.
46. Rosenkranz D, Zischler H. proTRAC - a software for probabilistic piRNA cluster detection, visualization and analysis. BMC Bioinformatics. 2012;13:5.
47. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, et al. The UCSC Table Browser data retrieval tool. Nucleic Acids Res. 2004;32:D493-6.
48. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139-40.
49. Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;Chapter 3:Unit 3.22.
50. Verweij FJ, van Eijndhoven MAJ, Hopmans ES, Vendrig T, Wurdinger T, Cahir-McFarland E, et al. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation. EMBO J. 2011;30:2115-29.
51. Koppers-Lalic D, Hackenberg M, Bijnsdorp I, van Eijndhoven M, Sadek P, Ylstra B, et al. Non-templated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014;8:1649-58.
52. Li Z, Liu C, Xie Z, Song P, Zhao RCH, Guo L, et al. Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One. 2011;6:e20526.
53. Kumar P, Anaya J, Mudunuri SB, Dutta A. Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol. 2014;12:78.
54. Gebetsberger J, Polacek N. Slicing tRNAs to boost functional ncRNA diversity. RNA Biol. 2013;10:1798-806.
55. Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, Lyle R, et al. Endogenous RNAs modulate MicroRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014;8:1432-46.
56. Wang Q, Lee I, Ren J, Ajay SS, Lee YS, Bao X. Identification and functional characterization of tRNA-derived RNA fragments (tRFs) in respiratory syncytial virus infection. Mol Ther. 2013;21:368-79.
57. Yeo RWY, Lai RC, Zhang B, Tan SS, Yin Y, Teh BJ, et al. Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev. 2013;65:336-41.
58. Chen TS, Arslan F, Yin Y, Tan SS, Lai RC, Choo ABH, et al. Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J Transl Med. 2011;9:47.
59. Balaj L, Lessard R, Dai L, Cho Y-J, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180.
60. Demory Beckler M, Higginbotham JN, Franklin JL, Ham A-J, Halvey PJ, Imasuen IE, et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics. 2013;12:343-55.
61. Kim DH, Yoo KH, Choi KS, Choi J, Choi S-Y, Yang S-E, et al. Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine. 2005;31:119-26.
62. Hoch AI, Binder BY, Genetos DC, Leach JK. Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells. PLoS One. 2012;7:e35579.
63. Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 2012;40:10937-49.
64. Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, et al. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 2014;42:7290-304.
65. Chen TS, Lai RC, Lee MM, Choo ABH, Lee CN, Lim SK. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res. 2010;38:215-24.
66. Clark EA, Kalomoiris S, Nolta JA, Fierro FA. Concise review: MicroRNA function in multipotent mesenchymal stromal cells. Stem Cells. 2014;32:1074-82.
67. Kim YJ, Hwang SH, Lee SY, Shin KK, Cho HH, Bae YC, et al. miR-486-5p induces replicative senescence of human adipose tissue-derived mesenchymal stem cells and its expression is controlled by high glucose. Stem Cells Dev. 2012;21:1749-60.
68. Zhao X, Liu D, Gong W, Zhao G, Liu L, Yang L, et al. The toll-like receptor 3 ligand, poly(I:C), improves immunosuppressive function and therapeutic effect of mesenchymal stem cells on sepsis via inhibiting MiR-143. Stem Cells. 2014;32:521-33.
69. Li J, Dong J, Zhang Z-H, Zhang D-C, You X-Y, Zhong Y, et al. miR-10a restores human mesenchymal stem cell differentiation by repressing KLF4. J Cell Physiol. 2013;228:2324-36.
70. Huang S, Wang S, Bian C, Yang Z, Zhou H, Zeng Y, et al. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev. 2012;21:2531-40.
71. Zhang F, Jing S, Ren T, Lin J. microRNA-10b promotes the migration of mouse bone marrow-derived mesenchymal stem cells and downregulates the expression of E-cadherin. Mol Med Rep. 2013;8:1084-8.
72. Nagpal N, Kulshreshtha R. miR-191: an emerging player in disease biology. Front Genet. 2014;5:99.
73. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res. 2008;79:581-8.
74. Yoo JK, Kim J, Choi S, Noh HM, Kwon YD, Yoo H, et al. Discovery and characterization of novel microRNAs during endothelial differentiation of human embryonic stem cells. Stem Cells Dev. 2012;21:2049-57.
75. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F, Kooistra SM, et al. A dual program for translation regulation in cellular proliferation and differentiation. Cell. 2014;158:1281-92.
76. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 2009;23:2639-49.
77. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A, Basso K, et al. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci U S A. 2013;110:1404-9.
78. Emara MM, Ivanov P, Hickman T, Dawra N, Tisdale S, Kedersha N, et al. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J Biol Chem. 2010;285:10959-68.
79. Ye S, Li P, Tong C, Ying Q-L. Embryonic stem cell self-renewal pathways converge on the transcription factor Tfcp2l1. EMBO J. 2013;32:2548-60.
80. Komori T. Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res. 2010;339:189-95.
81. Gadi J, Jung S-H, Lee M-J, Jami A, Ruthala K, Kim K-M, et al. The transcription factor protein Sox11 enhances early osteoblast differentiation by facilitating proliferation and the survival of mesenchymal and osteoblast progenitors. J Biol Chem. 2013;288:25400-13.
82. Bibikova E, Youn M-Y, Danilova N, Ono-Uruga Y, Konto-Ghiorghi Y, Ochoa R, et al. TNF-mediated inflammation represses GATA1 and activates p38 MAP kinase in RPS19-deficient hematopoietic progenitors. Blood. 2014;124:3791-8.
83. Zhao R, Chinai JM, Buhl S, Scandiuzzi L, Ray A, Jeon H, et al. HHLA2 is a member of the B7 family and inhibits human CD4 and CD8 T-cell function. Proc Natl Acad Sci U S A. 2013;110:9879-84.
84. Yona S, Lin H-H, Dri P, Davies JQ, Hayhoe RPG, Lewis SM, et al. Ligation of the adhesion-GPCR EMR2 regulates human neutrophil function. FASEB J. 2008;22:741-51.
85. Uchil PD, Hinz A, Siegel S, Coenen-Stass A, Pertel T, Luban J, et al. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity. J Virol. 2013;87:257-72.