MiR-422a promotes adipogenesis via MeCP2 downregulation in human bone marrow mesenchymal stem cells.
Adipogenesis
Mesenchymal stromal cells
Methyl CpG binding protein 2
MicroRNA
Osteogenesis
Osteoporosis
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
27 Feb 2023
27 Feb 2023
Historique:
received:
14
04
2022
accepted:
22
01
2023
revised:
16
12
2022
entrez:
27
2
2023
pubmed:
28
2
2023
medline:
3
3
2023
Statut:
epublish
Résumé
Methyl-CpG binding protein 2 (MeCP2) is a ubiquitous transcriptional regulator. The study of this protein has been mainly focused on the central nervous system because alterations of its expression are associated with neurological disorders such as Rett syndrome. However, young patients with Rett syndrome also suffer from osteoporosis, suggesting a role of MeCP2 in the differentiation of human bone marrow mesenchymal stromal cells (hBMSCs), the precursors of osteoblasts and adipocytes. Here, we report an in vitro downregulation of MeCP2 in hBMSCs undergoing adipogenic differentiation (AD) and in adipocytes of human and rat bone marrow tissue samples. This modulation does not depend on MeCP2 DNA methylation nor on mRNA levels but on differentially expressed miRNAs during AD. MiRNA profiling revealed that miR-422a and miR-483-5p are upregulated in hBMSC-derived adipocytes compared to their precursors. MiR-483-5p, but not miR-422a, is also up-regulated in hBMSC-derived osteoblasts, suggesting a specific role of the latter in the adipogenic process. Experimental modulation of intracellular levels of miR-422a and miR-483-5p affected MeCP2 expression through direct interaction with its 3' UTR elements, and the adipogenic process. Accordingly, the knockdown of MeCP2 in hBMSCs through MeCP2-targeting shRNA lentiviral vectors increased the levels of adipogenesis-related genes. Finally, since adipocytes released a higher amount of miR-422a in culture medium compared to hBMSCs we analyzed the levels of circulating miR-422a in patients with osteoporosis-a condition characterized by increased marrow adiposity-demonstrating that its levels are negatively correlated with T- and Z-scores. Overall, our findings suggest that miR-422a has a role in hBMSC adipogenesis by downregulating MeCP2 and its circulating levels are associated with bone mass loss in primary osteoporosis.
Identifiants
pubmed: 36847916
doi: 10.1007/s00018-023-04719-6
pii: 10.1007/s00018-023-04719-6
pmc: PMC9971129
doi:
Substances chimiques
3' Untranslated Regions
0
Mecp2 protein, rat
0
Methyl-CpG-Binding Protein 2
0
MicroRNAs
0
MECP2 protein, human
0
MIRN422 microRNA, human
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
75Subventions
Organisme : Università Politecnica delle Marche
ID : RSA Grant
Organisme : Università Politecnica delle Marche
ID : RSA Grant
Organisme : Università Politecnica delle Marche
ID : RSA Grant
Organisme : Ministero della Salute
ID : Ricerca Corrente
Informations de copyright
© 2023. The Author(s).
Références
Kaludov NK, Wolffe AP (2000) MeCP2 driven transcriptional repression in vitro: selectivity for methylated DNA, action at a distance and contacts with the basal transcription machinery. Nucleic Acids Res 28(9):1921–1928. https://doi.org/10.1093/nar/28.9.1921
doi: 10.1093/nar/28.9.1921
pubmed: 10756192
pmcid: 103274
Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320(5880):1224–1229. https://doi.org/10.1126/science.1153252
doi: 10.1126/science.1153252
pubmed: 18511691
pmcid: 2443785
Schmidt A, Zhang H, Cardoso MC (2020) MeCP2 and chromatin compartmentalization. Cells 9(4):878. https://doi.org/10.3390/cells9040878
doi: 10.3390/cells9040878
pubmed: 32260176
pmcid: 7226738
Li R, Dong Q, Yuan X, Zeng X, Gao Y, Chiao C, Li H, Zhao X, Keles S, Wang Z et al (2016) Misregulation of alternative splicing in a mouse model of Rett syndrome. PLoS Genet 12(6):e1006129. https://doi.org/10.1371/journal.pgen.1006129
doi: 10.1371/journal.pgen.1006129
pubmed: 27352031
pmcid: 4924826
Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23(2):185–188. https://doi.org/10.1038/13810
doi: 10.1038/13810
pubmed: 10508514
Hagberg B, Aicardi J, Dias K, Ramos O (1983) A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett’s syndrome: report of 35 cases. Ann Neurol 14(4):471–479. https://doi.org/10.1002/ana.410140412
doi: 10.1002/ana.410140412
pubmed: 6638958
Kyle SM, Saha PK, Brown HM, Chan LC, Justice MJ (2016) MeCP2 co-ordinates liver lipid metabolism with the NCoR1/HDAC3 corepressor complex. Hum Mol Genet 25(14):3029–3041. https://doi.org/10.1093/hmg/ddw156
doi: 10.1093/hmg/ddw156
pubmed: 27288453
pmcid: 5181597
Justice MJ, Buchovecky CM, Kyle SM, Djukic A (2013) A role for metabolism in Rett syndrome pathogenesis: new clinical findings and potential treatment targets. Rare Dis 1:e27265. https://doi.org/10.4161/rdis.27265
doi: 10.4161/rdis.27265
pubmed: 25003017
pmcid: 3978897
Shapiro JR, Bibat G, Hiremath G, Blue ME, Hundalani S, Yablonski T, Kantipuly A, Rohde C, Johnston M, Naidu S (2010) Bone mass in Rett syndrome: association with clinical parameters and MECP2 mutations. Pediatr Res 68(5):446–451. https://doi.org/10.1203/PDR.0b013e3181f2edd2
doi: 10.1203/PDR.0b013e3181f2edd2
pubmed: 20661168
pmcid: 3074246
O’Connor RD, Zayzafoon M, Farach-Carson MC, Schanen NC (2009) Mecp2 deficiency decreases bone formation and reduces bone volume in a rodent model of Rett syndrome. Bone 45(2):346–356. https://doi.org/10.1016/j.bone.2009.04.251
doi: 10.1016/j.bone.2009.04.251
pubmed: 19414073
pmcid: 2739100
Chen Q, Shou P, Zheng C, Jiang M, Cao G, Yang Q, Cao J, Xie N, Velletri T, Zhang X et al (2016) Fate decision of mesenchymal stem cells: adipocytes or osteoblasts? Cell Death Differ 23(7):1128–1139. https://doi.org/10.1038/cdd.2015.168
doi: 10.1038/cdd.2015.168
pubmed: 26868907
pmcid: 4946886
Kang H, Hata A (2015) The role of microRNAs in cell fate determination of mesenchymal stem cells: balancing adipogenesis and osteogenesis. BMB Rep 48(6):319–323. https://doi.org/10.5483/bmbrep.2015.48.6.206
doi: 10.5483/bmbrep.2015.48.6.206
pubmed: 25341923
pmcid: 4578617
Horowitz MC, Berry R, Holtrup B, Sebo Z, Nelson T, Fretz JA, Lindskog D, Kaplan JL, Ables G, Rodeheffer MS et al (2017) Bone marrow adipocytes. Adipocyte 6(3):193–204. https://doi.org/10.1080/21623945.2017.1367881
doi: 10.1080/21623945.2017.1367881
pubmed: 28872979
pmcid: 5638373
Cawthorn WP, Scheller EL, Learman BS, Parlee SD, Simon BR, Mori H, Ning X, Bree AJ, Schell B, Broome DT et al (2014) Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab 20(2):368–375. https://doi.org/10.1016/j.cmet.2014.06.003
doi: 10.1016/j.cmet.2014.06.003
pubmed: 24998914
pmcid: 4126847
Scheller EL, Rosen CJ (2014) What’s the matter with MAT? Marrow adipose tissue, metabolism, and skeletal health. Ann N Y Acad Sci 1311:14–30. https://doi.org/10.1111/nyas.12327
doi: 10.1111/nyas.12327
pubmed: 24650218
pmcid: 4049420
Ghaben AL, Scherer PE (2019) Adipogenesis and metabolic health. Nat Rev Mol Cell Biol. https://doi.org/10.1038/s41580-018-0093-z
doi: 10.1038/s41580-018-0093-z
pubmed: 30610207
Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, Gonzalez FJ, Spiegelman BM (2002) C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev 16(1):22–26. https://doi.org/10.1101/gad.948702
doi: 10.1101/gad.948702
pubmed: 11782441
pmcid: 155311
Rosen ED, Sarraf P, Troy AE, Bradwin G, Moore K, Milstone DS, Spiegelman BM, Mortensen RM (1999) PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell 4(4):611–617
doi: 10.1016/S1097-2765(00)80211-7
pubmed: 10549292
Lefterova MI, Haakonsson AK, Lazar MA, Mandrup S (2014) PPARgamma and the global map of adipogenesis and beyond. Trends Endocrinol Metab 25(6):293–302. https://doi.org/10.1016/j.tem.2014.04.001
doi: 10.1016/j.tem.2014.04.001
pubmed: 24793638
pmcid: 4104504
Oskowitz A, McFerrin H, Gutschow M, Carter ML, Pochampally R (2011) Serum-deprived human multipotent mesenchymal stromal cells (MSCs) are highly angiogenic. Stem cell Res 6(3):215–225. https://doi.org/10.1016/j.scr.2011.01.004
doi: 10.1016/j.scr.2011.01.004
pubmed: 21421339
pmcid: 4920087
Engin AB (2017) MicroRNA and Adipogenesis. Adv Exp Med Biol 960:489–509. https://doi.org/10.1007/978-3-319-48382-5_21
doi: 10.1007/978-3-319-48382-5_21
pubmed: 28585213
McGregor RA, Choi MS (2011) microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med 11(4):304–316
doi: 10.2174/156652411795677990
pubmed: 21506921
pmcid: 3267163
Hilton C, Neville MJ, Karpe F (2013) MicroRNAs in adipose tissue: their role in adipogenesis and obesity. Int J Obes 37(3):325–332. https://doi.org/10.1038/ijo.2012.59
doi: 10.1038/ijo.2012.59
Wang J, Guan X, Guo F, Zhou J, Chang A, Sun B, Cai Y, Ma Z, Dai C, Li X et al (2013) miR-30e reciprocally regulates the differentiation of adipocytes and osteoblasts by directly targeting low-density lipoprotein receptor-related protein 6. Cell Death Dis 4:e845. https://doi.org/10.1038/cddis.2013.356
doi: 10.1038/cddis.2013.356
pubmed: 24113179
pmcid: 3824666
Hamam D, Ali D, Vishnubalaji R, Hamam R, Al-Nbaheen M, Chen L, Kassem M, Aldahmash A, Alajez NM (2014) microRNA-320/RUNX2 axis regulates adipocytic differentiation of human mesenchymal (skeletal) stem cells. Cell Death Dis 5:e1499. https://doi.org/10.1038/cddis.2014.462
doi: 10.1038/cddis.2014.462
pubmed: 25356868
pmcid: 4237271
Zhang XY, Xu YY, Chen WY (2020) MicroRNA-1324 inhibits cell proliferative ability and invasiveness by targeting MECP2 in gastric cancer. Eur Rev Med Pharmacol Sci 24(9):4766–4774. https://doi.org/10.26355/eurrev_202005_21165
doi: 10.26355/eurrev_202005_21165
pubmed: 32432740
Zhai K, Liu B, Teng J (2020) MicroRNA-212-3p regulates early neurogenesis through the AKT/mTOR pathway by targeting MeCP2. Neurochem Int 137:104734. https://doi.org/10.1016/j.neuint.2020.104734
doi: 10.1016/j.neuint.2020.104734
pubmed: 32246981
Zhang N, Wei ZL, Yin J, Zhang L, Wang J, Jin ZL (2018) MiR-106a* inhibits oral squamous cell carcinoma progression by directly targeting MeCP2 and suppressing the Wnt/beta-Catenin signaling pathway. Am J Transl Res 10(11):3542–3554
pubmed: 30662606
pmcid: 6291734
Yao ZH, Yao XL, Zhang Y, Zhang SF, Hu J (2017) miR-132 down-regulates methyl CpG binding protein 2 (MeCP2) during cognitive dysfunction following chronic cerebral hypoperfusion. Curr Neurovasc Res 14(4):385–396. https://doi.org/10.2174/1567202614666171101115308
doi: 10.2174/1567202614666171101115308
pubmed: 29090669
Yan B, Hu Z, Yao W, Le Q, Xu B, Liu X, Ma L (2017) MiR-218 targets MeCP2 and inhibits heroin seeking behavior. Sci Rep 7:40413. https://doi.org/10.1038/srep40413
doi: 10.1038/srep40413
pubmed: 28074855
pmcid: 5225456
Zhao H, Wen G, Huang Y, Yu X, Chen Q, Afzal TA, le Luong A, Zhu J, Ye S, Zhang L et al (2015) MicroRNA-22 regulates smooth muscle cell differentiation from stem cells by targeting methyl CpG-binding protein 2. Arterioscler Thromb Vasc Biol 35(4):918–929. https://doi.org/10.1161/ATVBAHA.114.305212
doi: 10.1161/ATVBAHA.114.305212
pubmed: 25722434
Han K, Gennarino VA, Lee Y, Pang K, Hashimoto-Torii K, Choufani S, Raju CS, Oldham MC, Weksberg R, Rakic P et al (2013) Human-specific regulation of MeCP2 levels in fetal brains by microRNA miR-483-5p. Genes Dev 27(5):485–490. https://doi.org/10.1101/gad.207456.112
doi: 10.1101/gad.207456.112
pubmed: 23431031
pmcid: 3605462
Poloni A, Maurizi G, Leoni P, Serrani F, Mancini S, Frontini A, Zingaretti MC, Siquini W, Sarzani R, Cinti S (2012) Human dedifferentiated adipocytes show similar properties to bone marrow-derived mesenchymal stem cells. Stem Cells 30(5):965–974. https://doi.org/10.1002/stem.1067
doi: 10.1002/stem.1067
pubmed: 22367678
Poloni A, Maurizi G, Anastasi S, Mondini E, Mattiucci D, Discepoli G, Tiberi F, Mancini S, Partelli S, Maurizi A et al (2015) Plasticity of human dedifferentiated adipocytes toward endothelial cells. Exp Hematol 43(2):137–146. https://doi.org/10.1016/j.exphem.2014.10.003
doi: 10.1016/j.exphem.2014.10.003
pubmed: 25448487
Saben J, Thakali KM, Lindsey FE, Zhong Y, Badger TM, Andres A, Shankar K (2014) Distinct adipogenic differentiation phenotypes of human umbilical cord mesenchymal cells dependent on adipogenic conditions. Exp Biol Med 239(10):1340–1351. https://doi.org/10.1177/1535370214539225
doi: 10.1177/1535370214539225
Chen K, He H, Xie Y, Zhao L, Zhao S, Wan X, Yang W, Mo Z (2015) miR-125a-3p and miR-483-5p promote adipogenesis via suppressing the RhoA/ROCK1/ERK1/2 pathway in multiple symmetric lipomatosis. Sci Rep 5:11909. https://doi.org/10.1038/srep11909
doi: 10.1038/srep11909
pubmed: 26148871
pmcid: 4493643
Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89(5):747–754. https://doi.org/10.1016/s0092-8674(00)80257-3
doi: 10.1016/s0092-8674(00)80257-3
pubmed: 9182762
Kawai M, de Paula FJ, Rosen CJ (2012) New insights into osteoporosis: the bone-fat connection. J Intern Med 272(4):317–329. https://doi.org/10.1111/j.1365-2796.2012.02564.x
doi: 10.1111/j.1365-2796.2012.02564.x
pubmed: 22702419
pmcid: 3634716
Stachecka J, Lemanska W, Noak M, Szczerbal I (2020) Expression of key genes involved in DNA methylation during in vitro differentiation of porcine mesenchymal stem cells (MSCs) into adipocytes. Biochem Biophys Res Commun 522(3):811–818. https://doi.org/10.1016/j.bbrc.2019.11.175
doi: 10.1016/j.bbrc.2019.11.175
pubmed: 31791576
Liu C, Wang J, Wei Y, Zhang W, Geng M, Yuan Y, Chen Y, Sun Y, Chen H, Zhang Y et al (2020) Fat-specific knockout of Mecp2 upregulates Slpi to reduce obesity by enhancing browning. Diabetes 69(1):35–47. https://doi.org/10.2337/db19-0502
doi: 10.2337/db19-0502
pubmed: 31597640
Styner M, Sen B, Xie Z, Case N, Rubin J (2010) Indomethacin promotes adipogenesis of mesenchymal stem cells through a cyclooxygenase independent mechanism. J Cell Biochem 111(4):1042–1050. https://doi.org/10.1002/jcb.22793
doi: 10.1002/jcb.22793
pubmed: 20672310
pmcid: 3627539
Fujita K, Iwama H, Oura K, Tadokoro T, Hirose K, Watanabe M, Sakamoto T, Katsura A, Mimura S, Nomura T et al (2016) Metformin-suppressed differentiation of human visceral preadipocytes: involvement of microRNAs. Int J Mol Med 38(4):1135–1140. https://doi.org/10.3892/ijmm.2016.2729
doi: 10.3892/ijmm.2016.2729
pubmed: 27600587
pmcid: 5029962
Blardi P, de Lalla A, D’Ambrogio T, Zappella M, Cevenini G, Ceccatelli L, Auteri A, Hayek J (2007) Rett syndrome and plasma leptin levels. J Pediatr 150(1):37–39. https://doi.org/10.1016/j.jpeds.2006.10.061
doi: 10.1016/j.jpeds.2006.10.061
pubmed: 17188610
Acampa M, Guideri F, Hayek J, Blardi P, De Lalla A, Zappella M, Auteri A (2008) Sympathetic overactivity and plasma leptin levels in Rett syndrome. Neurosci Lett 432(1):69–72. https://doi.org/10.1016/j.neulet.2007.12.030
doi: 10.1016/j.neulet.2007.12.030
pubmed: 18226448
Blardi P, de Lalla A, D’Ambrogio T, Vonella G, Ceccatelli L, Auteri A, Hayek J (2009) Long-term plasma levels of leptin and adiponectin in Rett syndrome. Clin Endocrinol (Oxf) 70(5):706–709. https://doi.org/10.1111/j.1365-2265.2008.03386.x
doi: 10.1111/j.1365-2265.2008.03386.x
pubmed: 18710461
Liu Y, Palanivel R, Rai E, Park M, Gabor TV, Scheid MP, Xu A, Sweeney G (2015) Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice. Diabetes 64(1):36–48. https://doi.org/10.2337/db14-0267
doi: 10.2337/db14-0267
pubmed: 25071026
Parida S, Siddharth S, Sharma D (2019) Adiponectin, obesity, and cancer: clash of the bigwigs in health and disease. Int J Mol Sci 20(10):2519. https://doi.org/10.3390/ijms20102519
doi: 10.3390/ijms20102519
pubmed: 31121868
pmcid: 6566909
Hu L, Yin C, Zhao F, Ali A, Ma J, Qian A (2018) Mesenchymal stem cells: cell fate decision to osteoblast or adipocyte and application in osteoporosis treatment. Int J Mol Sci 19(2):360. https://doi.org/10.3390/ijms19020360
doi: 10.3390/ijms19020360
pubmed: 29370110
pmcid: 5855582
Pecorelli A, Cordone V, Schiavone ML, Caffarelli C, Cervellati C, Cerbone G, Gonnelli S, Hayek J, Valacchi G (2021) Altered bone status in Rett syndrome. Life (Basel) 11(6):521. https://doi.org/10.3390/life11060521
doi: 10.3390/life11060521
pubmed: 34205017
Kamal B, Russell D, Payne A, Constante D, Tanner KE, Isaksson H, Mathavan N, Cobb SR (2015) Biomechanical properties of bone in a mouse model of Rett syndrome. Bone 71:106–114. https://doi.org/10.1016/j.bone.2014.10.008
doi: 10.1016/j.bone.2014.10.008
pubmed: 25445449
pmcid: 4289916
Blue ME, Boskey AL, Doty SB, Fedarko NS, Hossain MA, Shapiro JR (2015) Osteoblast function and bone histomorphometry in a murine model of Rett syndrome. Bone 76:23–30. https://doi.org/10.1016/j.bone.2015.01.024
doi: 10.1016/j.bone.2015.01.024
pubmed: 25769649
pmcid: 7455889
Ross PD, Guy J, Selfridge J, Kamal B, Bahey N, Tanner KE, Gillingwater TH, Jones RA, Loughrey CM, McCarroll CS et al (2016) Exclusive expression of MeCP2 in the nervous system distinguishes between brain and peripheral Rett syndrome-like phenotypes. Hum Mol Genet 25(20):4389–4404. https://doi.org/10.1093/hmg/ddw269
doi: 10.1093/hmg/ddw269
pubmed: 28173151
pmcid: 5886038
Ji W, Sun X (2022) Methyl-CpG-binding protein 2 promotes osteogenic differentiation of bone marrow mesenchymal stem cells through regulating forkhead box F1/Wnt/beta-Catenin axis. Bioengineered 13(1):583–592. https://doi.org/10.1080/21655979.2021.2012357
doi: 10.1080/21655979.2021.2012357
pubmed: 34967263
Wang H, Zhang H, Sun Q, Wang Y, Yang J, Yang J, Zhang T, Luo S, Wang L, Jiang Y et al (2017) Intra-articular delivery of antago-miR-483-5p inhibits osteoarthritis by modulating matrilin 3 and tissue inhibitor of metalloproteinase 2. Mol Ther 25(3):715–727. https://doi.org/10.1016/j.ymthe.2016.12.020
doi: 10.1016/j.ymthe.2016.12.020
pubmed: 28139355
pmcid: 5363189
Liu M, Roth A, Yu M, Morris R, Bersani F, Rivera MN, Lu J, Shioda T, Vasudevan S, Ramaswamy S et al (2013) The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev 27(23):2543–2548. https://doi.org/10.1101/gad.224170.113
doi: 10.1101/gad.224170.113
pubmed: 24298054
pmcid: 3861668
Uchimura T, Hollander JM, Nakamura DS, Liu Z, Rosen CJ, Georgakoudi I, Zeng L (2017) An essential role for IGF2 in cartilage development and glucose metabolism during postnatal long bone growth. Development 144(19):3533–3546. https://doi.org/10.1242/dev.155598
doi: 10.1242/dev.155598
pubmed: 28974642
pmcid: 5665487
Cao Z, Moore BT, Wang Y, Peng XH, Lappe JM, Recker RR, Xiao P (2014) MiR-422a as a potential cellular microRNA biomarker for postmenopausal osteoporosis. PLoS One 9(5):e97098. https://doi.org/10.1371/journal.pone.0097098
doi: 10.1371/journal.pone.0097098
pubmed: 24820117
pmcid: 4018259
De-Ugarte L, Yoskovitz G, Balcells S, Guerri-Fernandez R, Martinez-Diaz S, Mellibovsky L, Urreizti R, Nogues X, Grinberg D, Garcia-Giralt N et al (2015) MiRNA profiling of whole trabecular bone: identification of osteoporosis-related changes in MiRNAs in human hip bones. BMC Med Genomics 8:75. https://doi.org/10.1186/s12920-015-0149-2
doi: 10.1186/s12920-015-0149-2
pubmed: 26555194
pmcid: 4640351
Martin PJ, Haren N, Ghali O, Clabaut A, Chauveau C, Hardouin P, Broux O (2015) Adipogenic RNAs are transferred in osteoblasts via bone marrow adipocytes-derived extracellular vesicles (EVs). BMC Cell Biol 16:10. https://doi.org/10.1186/s12860-015-0057-5
doi: 10.1186/s12860-015-0057-5
pubmed: 25887582
pmcid: 4369894
Rippo MR, Babini L, Prattichizzo F, Graciotti L, Fulgenzi G, TomassoniArdori F, Olivieri F, Borghetti G, Cinti S, Poloni A et al (2013) Low FasL levels promote proliferation of human bone marrow-derived mesenchymal stem cells, higher levels inhibit their differentiation into adipocytes. Cell Death Dis 4(4):e591. https://doi.org/10.1038/cddis.2013.115
doi: 10.1038/cddis.2013.115
Olivieri F, Lazzarini R, Recchioni R, Marcheselli F, Rippo MR, Di Nuzzo S, Albertini MC, Graciotti L, Babini L, Mariotti S et al (2013) MiR-146a as marker of senescence-associated pro-inflammatory status in cells involved in vascular remodelling. Age (Dordr) 35(4):1157–1172. https://doi.org/10.1007/s11357-012-9440-8
doi: 10.1007/s11357-012-9440-8
pubmed: 22692818
Olivieri F, Spazzafumo L, Santini G, Lazzarini R, Albertini MC, Rippo MR, Galeazzi R, Abbatecola AM, Marcheselli F, Monti D et al (2012) Age-related differences in the expression of circulating microRNAs: miR-21 as a new circulating marker of inflammaging. Mech Ageing Dev 133(11–12):675–685. https://doi.org/10.1016/j.mad.2012.09.004
doi: 10.1016/j.mad.2012.09.004
pubmed: 23041385
Li JH, Liu S, Zhou H, Qu LH, Yang JH (2014) starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res 42(D1):D92–D97. https://doi.org/10.1093/nar/gkt1248
doi: 10.1093/nar/gkt1248
pubmed: 24297251
Giuliani A, Cirilli I, Prattichizzo F, Mensà E, Fulgenzi G, Sabbatinelli J, Graciotti L, Olivieri F, Procopio AD, Tiano L et al (2018) The mitomiR/Bcl-2 axis affects mitochondrial function and autophagic vacuole formation in senescent endothelial cells. Aging (Albany NY) 10(10):2855–2873. https://doi.org/10.18632/aging.101591
doi: 10.18632/aging.101591
pubmed: 30348904
Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT et al (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33(3):401–406. https://doi.org/10.1038/ng1117
doi: 10.1038/ng1117
pubmed: 12590264
Amatori S, Papalini F, Lazzarini R, Donati B, Bagaloni I, Rippo MR, Procopio A, Pelicci PG, Catalano A, Fanelli M (2009) Decitabine, differently from DNMT1 silencing, exerts its antiproliferative activity through p21 upregulation in malignant pleural mesothelioma (MPM) cells. Lung Cancer 66(2):184–190. https://doi.org/10.1016/j.lungcan.2009.01.015
doi: 10.1016/j.lungcan.2009.01.015
pubmed: 19233506