Microvesicles from Mesenchymal Stromal Cells Are Involved in HPC-Microenvironment Crosstalk in Myelodysplastic Patients

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Muntión, Sandra ^a,b,c   Ramos, Teresa L ^a   Diez Campelo, María ^a,b,c   Rosón, Beatriz ^c   Sánchez Abarca, Luis Ignacio ^a,b,c,d   Misiewicz Krzeminska, Irena ^a,d,e   Preciado, Silvia ^a,b,c,d   Sarasquete, María Eugenia ^a   De Las Rivas, Javier ^c   González, Marcos ^a,d   Sánchez Guijo, Fermín ^a,b,c,d   Del Cañizo, María Consuelo ^a,b,c,d  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^b ISCIII)   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d CSIC   (Spain)

^e NATIONAL MEDICINES INSTITUTE   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CD63 ANTIGEN; MICRORNA; MICRORNA 10A; MICRORNA 15A; PROTEIN MDM2; PROTEIN P53; UNCLASSIFIED DRUG; CD34 ANTIGEN;

ADULT; AGED; ARTICLE; CD34 SELECTION; CELL ISOLATION; CELL VIABILITY ASSAY; CLINICAL ARTICLE; CLONOGENIC ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LOW RISK PATIENT; MALE; MDM2 GENE; MEMBRANE MICROPARTICLE; MESENCHYMAL STROMA CELL; MOLECULAR INTERACTION; MYELODYSPLASTIC SYNDROME; P53 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION; WESTERN BLOTTING; CELL COMMUNICATION; CELL SURVIVAL; EXOSOME; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; TUMOR MICROENVIRONMENT; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD34; CELL COMMUNICATION; CELL SURVIVAL; CELLULAR MICROENVIRONMENT; EXOSOMES; FEMALE; GENE EXPRESSION; HEMATOPOIETIC STEM CELLS; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICRORNAS; MIDDLE AGED; MYELODYSPLASTIC SYNDROMES;

EID: 84958794074     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146722     Document Type: Article

References (46)

1. Corey SJ, Minden MD, Barber DL, Kantarjian H, Wang JC, Schimmer AD. Myelodysplastic syndromes: the complexity of stem-cell diseases. Nature reviews Cancer. 2007; 7(2):118-29. Epub 2007/01/26. doi: 10.1038/nrc2047 PMID: 17251918.
2. Nimer SD. Myelodysplastic syndromes. Blood. 2008; 111(10):4841-51. Epub 2008/05/10. doi: 10. 1182/blood-2007-08-078139 PMID: 18467609.
3. Issa JP. The myelodysplastic syndrome as a prototypical epigenetic disease. Blood. 2013; 121 (19):3811-7. Epub 2013/05/11. doi: 10.1182/blood-2013-02-451757 PMID: 23660859; PubMed Central PMCID: PMC3650703.
4. Tauro S, Hepburn MD, Bowen DT, Pippard MJ. Assessment of stromal function, and its potential contribution to deregulation of hematopoiesis in the myelodysplastic syndromes. Haematologica. 2001; 86 (10):1038-45. Epub 2001/10/17. PMID: 11602409.
5. Lopez-Villar O, Garcia JL, Sanchez-Guijo FM, Robledo C, Villaron EM, Hernandez-Campo P, et al. Both expanded and uncultured mesenchymal stem cells from MDS patients are genomically abnormal, showing a specific genetic profile for the 5q-syndrome. Leukemia. 2009; 23(4):664-72. Epub 2009/01/20. doi: 10.1038/leu.2008.361 PMID: 19151777.
6. Blau O, Baldus CD, Hofmann WK, Thiel G, Nolte F, Burmeister T, et al. Mesenchymal stromal cells of myelodysplastic syndrome and acute myeloid leukemia patients have distinct genetic abnormalities compared with leukemic blasts. Blood. 2011; 118(20):5583-92. Epub 2011/09/29. doi: 10.1182/blood-2011-03-343467 PMID: 21948175; PubMed Central PMCID: PMC3217359.
7. Flores-Figueroa E, Montesinos JJ, Flores-Guzman P, Gutierrez-Espindola G, Arana-Trejo RM, Castillo-Medina S, et al. Functional analysis of myelodysplastic syndromes-derived mesenchymal stem cells. Leukemia research. 2008; 32(9):1407-16. Epub 2008/04/15. doi: 10.1016/j.leukres.2008.02.013 PMID: 18405968.
8. Zhao ZG, Xu W, Yu HP, Fang BL, Wu SH, Li F, et al. Functional characteristics of mesenchymal stem cells derived from bone marrow of patients with myelodysplastic syndromes. Cancer letters. 2012; 317 (2):136-43. Epub 2012/01/14. doi: 10.1016/j.canlet.2011.08.030 PMID: 22240014.
9. Raaijmakers MH, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker JA, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature. 2010; 464(7290):852-7. Epub 2010/03/23. doi: 10.1038/nature08851 PMID: 20305640; PubMed Central PMCID: PMC3422863.
10. Santamaria C, Muntion S, Roson B, Blanco B, Lopez-Villar O, Carrancio S, et al. Impaired expression of DICER, DROSHA, SBDS and some microRNAs in mesenchymal stromal cells from myelodysplastic syndrome patients. Haematologica. 2012; 97(8):1218-24. Epub 2012/03/01. doi: 10.3324/haematol. 2011.054437 PMID: 22371183; PubMed Central PMCID: PMC3409820.
11. Yuana Y, Sturk A, Nieuwland R. Extracellular vesicles in physiological and pathological conditions. Blood reviews. 2013; 27(1):31-9. Epub 2012/12/25. doi: 10.1016/j.blre.2012.12.002 PMID: 23261067.
12. 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(7):e11803. Epub 2010/07/30. doi: 10.1371/journal.pone.0011803 PMID: 20668554; PubMed Central PMCID: PMC2910725.
13. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012; 119 (3):756-66. Epub 2011/10/28. doi: 10.1182/blood-2011-02-338004 PMID: 22031862; PubMed Central PMCID: PMC3265200.
14. 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(4):315-7. Epub 2006/08/23. doi: 10.1080/14653240600855905 PMID: 16923606.
15. Villaron EM, Almeida J, Lopez-Holgado N, Sanchez-Guijo FM, Alberca M, Blanco B, et al. In leukapheresis products from non-Hodgkin's lymphoma patients, the immature hematopoietic progenitors show higher CD90 and CD34 antigenic expression. Transfusion and apheresis science: official journal of the World Apheresis Association: official journal of the European Society for Haemapheresis. 2007; 37 (2):145-56. Epub 2007/11/07. doi: 10.1016/j.transci.2007.05.001 PMID: 17983836.
16. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current protocols in cell biology/editorial board, Juan S Bonifacino [et al]. 2006;Chapter 3:Unit 3 Epub 2008/01/30. doi: 10.1002/0471143030.cb0322s30 PMID: 18228490.
17. Gelderman MP, Simak J. Flow cytometric analysis of cell membrane microparticles. Methods Mol Biol. 2008; 484:79-93. Epub 2008/07/02. doi: 10.1007/978-1-59745-398-1-6 PMID: 18592174.
18. Dvinge H, Bertone P. HTqPCR: high-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics. 2009; 25(24):3325-6. Epub 2009/10/08. doi: 10.1093/bioinformatics/btp578 PMID: 19808880; PubMed Central PMCID: PMC2788924.
19. Vergoulis T, Vlachos IS, Alexiou P, Georgakilas G, Maragkakis M, Reczko M, et al. TarBase 6.0: capturing the exponential growth of miRNA targets with experimental support. Nucleic acids research. 2012; 40(Database issue):D222-9. Epub 2011/12/03. doi: 10.1093/nar/gkr1161 PMID: 22135297; PubMed Central PMCID: PMC3245116.
20. Grange C, Tapparo M, Bruno S, Chatterjee D, Quesenberry PJ, Tetta C, et al. Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. International journal of molecular medicine. 2014; 33(5):1055-63. Epub 2014/02/28. doi: 10. 3892/ijmm.2014.1663 PMID: 24573178; PubMed Central PMCID: PMC4020482.
21. Herrera Sanchez MB, Bruno S, Grange C, Tapparo M, Cantaluppi V, Tetta C, et al. Human liver stem cells and derived extracellular vesicles improve recovery in a murine model of acute kidney injury. Stem cell research & therapy. 2014; 5(6):124. Epub 2014/11/12. doi: 10.1186/scrt514 PMID: 25384729.
22. Gentalen ET, Proctor JM. Using the Peggy Simple Western system for fine needle aspirate analysis. Methods Mol Biol. 2015; 1219:139-55. Epub 2014/10/14. doi: 10.1007/978-1-4939-1661-0-11 PMID: 25308267.
23. Rustandi RR, Anderson C, Hamm M. Application of capillary electrophoresis in glycoprotein analysis. Methods Mol Biol. 2013; 988:181-97. Epub 2013/03/12. doi: 10.1007/978-1-62703-327-5-11 PMID: 23475720.
24. Fang J, Varney M, Starczynowski DT. Implication of microRNAs in the pathogenesis of MDS. Current pharmaceutical design. 2012; 18(22):3170-9. Epub 2012/05/11. PMID: 22571695.
25. Chen L, Marechal V, Moreau J, Levine AJ, Chen J. Proteolytic cleavage of the mdm2 oncoprotein during apoptosis. The Journal of biological chemistry. 1997; 272(36):22966-73. Epub 1997/09/05. PMID: 9278461.
26. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature cell biology. 2007; 9(6):654-9. Epub 2007/05/09. doi: 10.1038/ncb1596 PMID: 17486113.
27. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, et al. Transfer of microRNAs by embryonic stem cell microvesicles. PloS one. 2009; 4(3):e4722. Epub 2009/03/07. doi: 10.1371/journal.pone.0004722 PMID: 19266099; PubMed Central PMCID: PMC2648987.
28. Gajos-Michniewicz A, Duechler M, Czyz M. MiRNA in melanoma-derived exosomes. Cancer letters. 2014; 347(1):29-37. Epub 2014/02/12. doi: 10.1016/j.canlet.2014.02.004 PMID: 24513178.
29. Hannafon BN, Ding WQ. Intercellular Communication by Exosome-Derived microRNAs in Cancer. International journal of molecular sciences. 2013; 14(7):14240-69. Epub 2013/07/11. doi: 10.3390/ijms140714240 PMID: 23839094; PubMed Central PMCID: PMC3742242.
30. Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem cells and development. 2013; 22 (5):758-71. Epub 2012/10/05. doi: 10.1089/scd.2012.0304 PMID: 23034046.
31. Roccaro AM, Sacco A, Maiso P, Azab AK, Tai YT, Reagan M, et al. BM mesenchymal stromal cellderived exosomes facilitate multiple myeloma progression. The Journal of clinical investigation. 2013; 123(4):1542-55. Epub 2013/03/05. doi: 10.1172/JCI66517 PMID: 23454749; PubMed Central PMCID: PMC3613927.
32. Wang J, Hendrix A, Hernot S, Lemaire M, De Bruyne E, Van Valckenborgh E, et al. Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood. 2014; 124(4):555-66. Epub 2014/06/15. doi: 10.1182/blood-2014-03-562439 PMID: 24928860.
33. Ramos TL, Sánchez-Abarca LI, Muntión S, Preciado S, Puig Morón N, López-Ruano G, et al. Human mesenchymal stromal cell (hMSC)-derived extracellular vesicles: Optimization of immunophenotypic characterization. Cell Communications and Signalling. 2015.
34. Aliotta JM, Sanchez-Guijo FM, Dooner GJ, Johnson KW, Dooner MS, Greer KA, et al. Alteration of marrow cell gene expression, protein production, and engraftment into lung by lung-derived microvesicles: a novel mechanism for phenotype modulation. Stem Cells. 2007; 25(9):2245-56. Epub 2007/06/09. doi: 10.1634/stemcells.2007-0128 PMID: 17556595; PubMed Central PMCID: PMC3376082.
35. Havelange V, Garzon R. MicroRNAs: emerging key regulators of hematopoiesis. American journal of hematology. 2010; 85(12):935-42. Epub 2010/10/14. doi: 10.1002/ajh.21863 PMID: 20941782.
36. Vasilatou D, Papageorgiou SG, Dimitriadis G, Pappa V. Epigenetic alterations and microRNAs: new players in the pathogenesis of myelodysplastic syndromes. Epigenetics: official journal of the DNA Methylation Society. 2013; 8(6):561-70. Epub 2013/06/14. doi: 10.4161/epi.24897 PMID: 23760524; PubMed Central PMCID: PMC3857336.
37. Li X, Xu F, Chang C, Byon J, Papayannopoulou T, Deeg HJ, et al. Transcriptional regulation of miR-10a/b by TWIST-1 in myelodysplastic syndromes. Haematologica. 2013; 98(3):414-9. Epub 2012/09/ doi: 10.3324/haematol.2012.071753 PMID: 22983574; PubMed Central PMCID: PMC3659943.
38. Pons A, Nomdedeu B, Navarro A, Gaya A, Gel B, Diaz T, et al. Hematopoiesis-related microRNA expression in myelodysplastic syndromes. Leukemia & lymphoma. 2009; 50(11):1854-9. Epub 2009/11/04. doi: 10.3109/10428190903147645 PMID: 19883312.
39. Abbas HA, Pant V, Lozano G. The ups and downs of p53 regulation in hematopoietic stem cells. Cell Cycle. 2011; 10(19):3257-62. Epub 2011/10/01. doi: 10.4161/cc.10.19.17721 PMID: 21957490; PubMed Central PMCID: PMC3233622.
40. Maetens M, Doumont G, Clercq SD, Francoz S, Froment P, Bellefroid E, et al. Distinct roles of Mdm2 and Mdm4 in red cell production. Blood. 2007; 109(6):2630-3. Epub 2006/11/16. doi: 10.1182/blood-2006-03-013656 PMID: 17105817.
41. Abbas HA, Maccio DR, Coskun S, Jackson JG, Hazen AL, Sills TM, et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell stem cell. 2010; 7(5):606-17. Epub 2010/11/03. doi: 10.1016/j.stem.2010.09.013 PMID: 21040902; PubMed Central PMCID: PMC3026610.
42. Corrado C, Raimondo S, Saieva L, Flugy AM, De Leo G, Alessandro R. Exosome-mediated crosstalk between chronic myelogenous leukemia cells and human bone marrow stromal cells triggers an interleukin 8-dependent survival of leukemia cells. Cancer letters. 2014; 348(1-2):71-6. Epub 2014/03/25. doi: 10.1016/j.canlet.2014.03.009 PMID: 24657661.
43. Pereira JK, Traina F, Machado-Neto JA, Duarte Ada S, Lopes MR, Saad ST, et al. Distinct expression profiles of MSI2 and NUMB genes in myelodysplastic syndromes and acute myeloid leukemia patients. Leukemia research. 2012; 36(10):1300-3. Epub 2012/07/13. doi: 10.1016/j.leukres.2012.06.010 PMID: 22784712.
44. Schepers K, Pietras EM, Reynaud D, Flach J, Binnewies M, Garg T, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell stem cell. 2013; 13(3):285-99. Epub 2013/07/16. doi: 10.1016/j.stem.2013.06.009 PMID: 23850243; PubMed Central PMCID: PMC3769504.
45. Geyh S, Oz S, Cadeddu RP, Frobel J, Bruckner B, Kundgen A, et al. Insufficient stromal support in MDS results from molecular and functional deficits of mesenchymal stromal cells. Leukemia. 2013; 27 (9):1841-51. Epub 2013/06/26. doi: 10.1038/leu.2013.193 PMID: 23797473.
46. Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. Journal of cell science. 2010; 123(Pt 10):1603-11. Epub 2010/05/07. doi: 10.1242/jcs.064386 PMID: 20445011; PubMed Central PMCID: PMC2864708.