Abstract
Epigenetics can be explored at different levels and can be divided into two major areas: epigenetics of nuclear-encoded DNA and epigenetics of mitochondrial-encoded DNA. In epigenetics of nuclear-encoded DNA, the main roles are played by DNA methylation, changes in histone structure and several types of non-coding RNAs. Mitochondrial epigenetics seems to be similar in the aspect of DNA methylation and to some extent in the role of non-coding RNAs but differs significantly in changes in components coiling DNA. Nuclear DNA is coiled around histones, but mitochondrial DNA, together with associated proteins, is located in mitochondrial pseudocompartments called nucleoids. It has been shown that mitochondrial epigenetic mechanisms influence cell fate, transcription regulation, cell division, cell cycle, physiological homeostasis, bioenergetics and even pathologies, but not all of these mechanisms have been explored in stem cells. The main issue is that most of these mechanisms have only recently been discovered in mitochondria, while improvements in methodology, especially next-generation sequencing, have enabled in-depth studies. Because studies exploring mitochondria from other aspects show that mitochondria are crucial for the normal behavior of stem cells, it is suggested that precise mitochondrial epigenetics in stem cells should be studied more intensively.
KeywordsMitochondria Mitochondrial DNA Epigenetics Stem cell References
1.Eridani, S. (2014). Types of human stem cells and their therapeutic applications. Stem Cell Discovery, 4(2), 13–26.CrossRefGoogle Scholar
2.Dodson, B. P., & Levine, A. D. (2015). Challenges in the translation and commercialization of cell therapies. BMC Biotechnology, 15, 70.PubMedPubMedCentralCrossRefGoogle Scholar
3.Garitaonandia, I., Amir, H., Boscolo, F. S., et al. (2015). Increased risk of genetic and epigenetic instability in human embryonic stem cells associated with specific culture conditions. PLoS One, 10(2), e0118307.PubMedPubMedCentralCrossRefGoogle Scholar
4.Nguyen, H. T., Geens, M., & Spits, C. (2013). Genetic and epigenetic instability in human pluripotent stem cells. Human Reproduction Update, 19(2), 187–205.PubMedCrossRefGoogle Scholar
5.Anderson, S., Bankier, A. T., Barrell, B. G., et al. (1981). Sequence and organization of the human mitochondrial genome. Nature, 290(5806), 457–465.PubMedCrossRefGoogle Scholar
6.Nicholls, T. J., & Minczuk, M. (2014). In D-loop: 40 years of mitochondrial 7S DNA. Experimental Gerontology, 56, 175–181.PubMedCrossRefGoogle Scholar
7.Schon, E. A., DiMauro, S., & Hirano, M. (2012). Human mitochondrial DNA: roles of inherited and somatic mutations. Nature Reviews Genetics, 13(12), 878–890.PubMedPubMedCentralCrossRefGoogle Scholar
8.MITOMAP. A human mitochondrial genome database. Available at http://www.mitomap.org/MITOMAP.
9.Zeviani, M., & Di Donato, S. (2004). Mitochondrial disorders. Brain, 127(Pt 10), 2153–2172.PubMedCrossRefGoogle Scholar
10.Spelbrink, J. N., Toivonen, J. M., Hakkaart, G. A., et al. (2000). In vivo functional analysis of the human mitochondrial DNA polymerase POLG expressed in cultured human cells. The Journal of Biological Chemistry, 275(32), 24818–24828.PubMedCrossRefGoogle Scholar
11.Luoma, P., Melberg, A., Rinne, J. O., et al. (2004). Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet, 364(9437), 875–882.PubMedCrossRefGoogle Scholar
12.Mancuso, M., Filosto, M., Bellan, M., et al. (2004). POLG mutations causing ophthalmoplegia, sensorimotor polyneuropathy, ataxia, and deafness. Neurology, 62(2), 316–318.PubMedCrossRefGoogle Scholar
13.St John, J. C., Ramalho-Santos, J., Gray, H. L., et al. (2005). The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning and Stem Cells, 7(3), 141–153.PubMedCrossRefGoogle Scholar
14.Facucho-Oliveira, J. M., & St John, J. C. (2009). The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Reviews, 5(2), 140–158.PubMedCrossRefGoogle Scholar
15.Simsek, T., Kocabas, F., Zheng, J., et al. (2010). The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell, 7(3), 380–390.PubMedPubMedCentralCrossRefGoogle Scholar
16.Nuschke, A., Rodrigues, M., Wells, A. W., Sylakowski, K., & Wells, A. (2016). Mesenchymal stem cells/multipotent stromal cells (MSCs) are glycolytic and thus glucose is a limiting factor of in vitro models of MSC starvation. Stem Cell Research & Therapy, 7(1), 179.CrossRefGoogle Scholar
17.Folmes, C. D., Nelson, T. J., Martinez-Fernandez, A., et al. (2011). Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metabolism, 14(2), 64–271.CrossRefGoogle Scholar
18.Zhang, J., Khvorostov, I., Hong, J. S., et al. (2011). UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. The EMBO Journal, 30(24), 4860–4873.PubMedPubMedCentralCrossRefGoogle Scholar
19.Khacho, M., Clark, A., Svoboda, D. S., et al. (2016). Mitochondrial dynamics impacts stem cell identity and fate decisions by regulating a nuclear transcriptional program. Cell Stem Cell, 19(2), 232–247.PubMedCrossRefGoogle Scholar
20.Detmer, S. A., & Chan, D. C. (2007). Functions and dysfunctions of mitochondrial dynamics. Nature Reviews Molecular Cell Biology, 8(11), 870–879.PubMedCrossRefGoogle Scholar
21.Murphy, M. P. (2009). How mitochondria produce reactive oxygen species. The Biochemical Journal, 417(1), 1–13.PubMedCrossRefGoogle Scholar
22.Atashi, F., Modarressi, A., & Pepper, M. S. (2015). The role of reactive oxygen species in mesenchymal stem cell adipogenic and osteogenic differentiation: a review. Stem Cells and Development, 24(10), 1150–1163.PubMedPubMedCentralCrossRefGoogle Scholar
23.Fandel, T. M., Albersen, M., Lin, G., et al. (2012). Recruitment of intracavernously injected adipose-derived stem cells to the major pelvic ganglion improves erectile function in a rat model of cavernous nerve injury. European Urology, 61(1), 201–210.PubMedCrossRefGoogle Scholar
24.Bivalacqua, T. J., Deng, W., Kendirci, M., et al. (2007). Mesenchymal stem cells alone or ex vivo gene modified with endothelial nitric oxide synthase reverse age-associated erectile dysfunction. American Journal of Physiology Heart and Circulatory Physiology, 292(3), H1278–H1290.PubMedCrossRefGoogle Scholar
25.Rodrigues, M., Turner, O., Stolz, D., Griffith, L. G., & Wells, A. (2012). Production of reactive oxygen species by multipotent stromal cells/mesenchymal stem cells upon exposure to fas ligand. Cell Transplantation, 21(10), 2171–2187.PubMedCrossRefGoogle Scholar
26.Liu, G. Y., Jiang, X. X., Zhu, X., et al. (2015). ROS activates JNK-mediated autophagy to counteract apoptosis in mouse mesenchymal stem cells in vitro. Acta Pharmacologica Sinica, 36(12), 1473–1479.PubMedPubMedCentralCrossRefGoogle Scholar
27.Xu, J., Qian, J., Xie, X., et al. (2012). High density lipoprotein protects mesenchymal stem cells from oxidative stress-induced apoptosis via activation of the PI3K/Akt pathway and suppression of reactive oxygen species. International Journal of Molecular Sciences, 13(12), 17104–17120.PubMedPubMedCentralCrossRefGoogle Scholar
28.Li, S., Bian, H., Liu, Z., et al. (2012). Chlorogenic acid protects MSCs against oxidative stress by altering FOXO family genes and activating intrinsic pathway. European Journal of Pharmacology, 674(2–3), 65–72.PubMedCrossRefGoogle Scholar
29.Liu, G. S., Chan, E. C., Higuchi, M., Dusting, G. J., & Jiang, F. (2012). Redox mechanisms in regulation of adipocyte differentiation: beyond a general stress response. Cells, 1(4), 976–993.PubMedPubMedCentralCrossRefGoogle Scholar
30.Shao, J. S., Aly, Z. A., Lai, C. F., et al. (2007). Vascular Bmp Msx2 Wnt signaling and oxidative stress in arterial calcification. Annals of the New York Academy of Sciences, 1117, 40–50.PubMedCrossRefGoogle Scholar
31.Mateos, J., De la Fuente, A., Lesende-Rodriguez, I., Fernández-Pernas, P., Arufe, M. C., & Blanco, F. J. (2013). Lamin A deregulation in human mesenchymal stem cells promotes an impairment in their chondrogenic potential and imbalance in their response to oxidative stress. Stem Cell Research, 11(3), 1137–1148.PubMedCrossRefGoogle Scholar
32.Boopathy, A. V., Pendergrass, K. D., Che, P. L., Yoon, Y. S., & Davis, M. E. (2013). Oxidative stress-induced Notch1 signaling promotes cardiogenic gene expression in mesenchymal stem cells. Stem Cell Research & Therapy, 4(2), 43.CrossRefGoogle Scholar
33.Higuchi, M., Dusting, G. J., Peshavariya, H., et al. (2013). Differentiation of human adipose-derived stem cells into fat involves reactive oxygen species and Forkhead box O1 mediated upregulation of antioxidant enzymes. Stem Cells and Development, 22(6), 878–888.PubMedCrossRefGoogle Scholar
34.Drehmer, D. L., de Aguiar, A. M., Brandt, A. P., et al. (2016). Metabolic switches during the first steps of adipogenic stem cells differentiation. Stem Cell Research, 17(2), 413–421.PubMedCrossRefGoogle Scholar
35.Maekawa, M., Taniguchi, T., Higashi, H., Sugimura, H., Sugano, K., & Kanno, T. (2004). Methylation of mitochondrial DNA is not a useful marker for cancer detection. Clinical Chemistry, 50(8), 1480–1481.PubMedCrossRefGoogle Scholar
36.Kafri, T., Ariel, M., Brandeis, M., et al. (1992). Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes and Development, 6(5), 705–714.PubMedCrossRefGoogle Scholar
37.Straussman, R., Nejman, D., Roberts, D., et al. (2009). Developmental programming of CpG island methylation profiles in the human genome. Nature Structural & Molecular Biology, 16(5), 564–571.CrossRefGoogle Scholar
38.Dawid, I. B. (1974). 5-Methylcytidylic acid: absence from mitochondrial DNA of frogs and HeLa cells. Science, 184(4132), 80–81.PubMedCrossRefGoogle Scholar
39.Nass, M. M. (1973). Differential methylation of mitochondrial and nuclear DNA in cultured mouse, hamster and virus-transformed hamster cells. In vivo and in vitro methylation. Journal of Molecular Biology, 80(1), 155–175.PubMedCrossRefGoogle Scholar
40.Hong, E. E., Okitsu, C. Y., Smith, A. D., & Hsieh, C. L. (2013). Regionally specific and genome-wide analyses conclusively demonstrate the absence of CpG methylation in human mitochondrial DNA. Molecular and Cellular Biology, 33(14), 2683–2690.PubMedPubMedCentralCrossRefGoogle Scholar
41.Pollack, Y., Kasir, J., Shemer, R., Metzger, S., & Szyf, M. (1984). Methylation pattern of mouse mitochondrial DNA. Nucleic Acids Research, 12(12), 4811–4824.PubMedPubMedCentralCrossRefGoogle Scholar
42.Liu, B., Du, Q., Chen, L., et al. (2016). CpG methylation patterns of human mitochondrial DNA. Scientific Reports, 6, 23421.PubMedPubMedCentralCrossRefGoogle Scholar
43.Shock, L. S., Thakkar, P. V., Peterson, E. J., Moran, R. G., & Taylor, S. M. (2011). DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 108(9), 3630–3635.PubMedPubMedCentralCrossRefGoogle Scholar
44.Chestnut, B. A., Chang, Q., Price, A., Lesuisse, C., Wong, M,, & Martin, L. J. (2011). Epigenetic regulation of motor neuron cell death through DNA methylation. The Journal of Neuroscience, 31(46), 16619–16636.PubMedPubMedCentralCrossRefGoogle Scholar
45.Kohli, R. M., & Zhang, Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature, 502(7472), 472–479.PubMedPubMedCentralCrossRefGoogle Scholar
46.Tahiliani, M., Koh, K. P., Shen, Y., et al. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324(5929), 930–935.PubMedPubMedCentralCrossRefGoogle Scholar
47.Liutkeviciute, Z., Lukinavicius, G., Masevicius, V., Daujotyte, D., & Klimasauskas, S. (2009). Cytosine-5-methyltransferases add aldehydes to DNA. Nature Chemical Biology, 5(6), 400–402.PubMedCrossRefGoogle Scholar
48.Ghosh, S., Sengupta, S., & Scaria, V. (2016). Hydroxymethyl cytosine marks in the human mitochondrial genome are dynamic in nature. Mitochondrion, 27, 25–31.PubMedCrossRefGoogle Scholar
49.Bellizzi, D., D’Aquila, P., Scafone, T., et al. (2013). The control region of mitochondrial DNA shows an unusual CpG and non-CpG methylation pattern. DNA Research, 20(6), 537–547.PubMedPubMedCentralCrossRefGoogle Scholar
50.Yu, D., Du, Z., Pian, L., et al. (2017). Mitochondrial DNA hypomethylation is a biomarker associated with induced senescence in human fetal heart mesenchymal stem cells. Stem Cells International, 2017, 1764549.PubMedPubMedCentralGoogle Scholar
51.Bonab, M. M., Alimoghaddam, K., Talebian, F., Ghaffari, S. H., Ghavamzadeh, A., & Nikbin, B. (2006). Aging of mesenchymal stem cell in vitro. BMC Cell Biology, 7, 14.PubMedPubMedCentralCrossRefGoogle Scholar
52.Zaim, M., Karaman, S., Cetin, G., & Isik, S. (2012). Donor age and long-term culture affect differentiation and proliferation of human bone marrow mesenchymal stem cells. Annals of Hematology, 91(8), 1175–1186.PubMedCrossRefGoogle Scholar
53.Kasper, G., Mao, L., Geissler, S., et al. (2009). Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells, 27(6), 1288–1297.PubMedCrossRefGoogle Scholar
54.Bentivegna, A., Roversi, G., Riva, G., et al. (2016). The effect of culture on human bone marrow mesenchymal stem cells: focus on DNA methylation profiles. Stem Cells International, 2016, 5656701.PubMedPubMedCentralCrossRefGoogle Scholar
55.Laurent, L., Wong, E., Li, G., et al. (2010). Dynamic changes in the human methylome during differentiation. Genome Research, 20(3), 320–331.PubMedPubMedCentralCrossRefGoogle Scholar
56.Sørensen, A. L., Jacobsen, B. M., Reiner, A. H., Andersen, I. S., & Collas, P. (2010). Promoter DNA methylation patterns of differentiated cells are largely programmed at the progenitor stage. Molecular Biology of the Cell, 21(12), 2066–2077.PubMedPubMedCentralCrossRefGoogle Scholar
57.Sørensen, A. L., Timoskainen, S., West, F. D., et al. (2010). Lineage-specific promoter DNA methylation patterns segregate adult progenitor cell types. Stem Cells and Development, 19(8), 1257–1266.PubMedCrossRefGoogle Scholar
58.Franzen, J., Zirkel, A., Blake, J., et al. (2017). Senescence-associated DNA methylation is stochastically acquired in subpopulations of mesenchymal stem cells. Aging Cell, 16(1), 183–191.PubMedCrossRefGoogle Scholar
59.Kukat, C., Wurm, C. A., Spåhr, H., Falkenberg, M., Larsson, N. G., & Jakobs, S. (2011). Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proceedings of the National Academy of Sciences of the United States of America, 108(33), 13534–13539.PubMedPubMedCentralCrossRefGoogle Scholar
60.Kolesnikov, A. A. (2016). The mitochondrial genome. The nucleoid. Biochemistry (Mosc), 81(10), 1057–1065.CrossRefGoogle Scholar
61.Kaufman, B. A., Durisic, N., Mativetsky, J. M., et al. (2007). The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Molecular Biology of the Cell, 18(9), 3225–3236.PubMedPubMedCentralCrossRefGoogle Scholar
62.Ekstrand, M. I., Falkenberg, M., Rantanen, A., et al. (2004). Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Human Molecular Genetics, 13(9), 935–944.PubMedCrossRefGoogle Scholar
63.Campbell, C. T., Kolesar, J. E., & Kaufman, B. A. (2012). Mitochondrial transcription factor A regulates mitochondrial transcription initiation, DNA packaging, and genome copy number. Biochimica et Biophysica Acta, 1819(9–10), 921–929.PubMedCrossRefGoogle Scholar
64.Audano, M., Ferrari, A., Fiorino, E., et al. (2014). Energizing genetics and Epi-genetics: role in the regulation of mitochondrial function. Current Genomics, 15(6), 436–456.PubMedPubMedCentralCrossRefGoogle Scholar
65.Lu, B., Lee, J., Nie, X., et al. (2013). Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Molecular Cell, 49(1), 121–132.PubMedCrossRefGoogle Scholar
66.Spikings, E. C., Alderson, J., & St John, J. C. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biology of Reproduction, 76(2), 327–335.PubMedCrossRefGoogle Scholar
67.Cho, Y. M., Kwon, S., Pak, Y. K., et al. (2006). Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochemical and Biophysical Research Communications, 348(4), 1472–1478.PubMedCrossRefGoogle Scholar
68.Prigione, A., Fauler, B., Lurz, R., Lehrach, H., & Adjaye, J. (2010). The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells, 28(4), 721–733.PubMedCrossRefGoogle Scholar
69.Prigione, A., & Adjaye, J. (2010). Modulation of mitochondrial biogenesis and bioenergetic metabolism upon in vitro and in vivo differentiation of human ES and iPS cells. The International Journal of Developmental Biology, 54(11–12), 1729–1741.PubMedCrossRefGoogle Scholar
70.Armstrong, L., Tilgner, K., Saretzki, G., et al. (2010). Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells, 28(4), 661–673.PubMedCrossRefGoogle Scholar
71.Chen, C. T., Shih, Y. R., Kuo, T. K., Lee, O. K., & Wei, Y. H. (2008). Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells, 26(4), 960–968.PubMedCrossRefGoogle Scholar
72.Zhang, Y., Marsboom, G., Toth, P. T., & Rehman, J. (2013). Mitochondrial respiration regulates adipogenic differentiation of human mesenchymal stem cells. PLoS One, 8(10), e77077.PubMedPubMedCentralCrossRefGoogle Scholar
73.Facucho-Oliveira, J. M., Alderson, J., Spikings, E. C., Egginton, S., & St John, J. C. (2007). Mitochondrial DNA replication during differentiation of murine embryonic stem cells. Journal of Cell Science, 120, 4025–4034.PubMedCrossRefGoogle Scholar
74.Masotti, A., Celluzzi, A., Petrini, S., Bertini, E., Zanni, G., & Compagnucci, C. (2014). Aged iPSCs display an uncommon mitochondrial appearance and fail to undergo in vitro neurogenesis. Aging (Albany NY), 6(12), 1094–1108.CrossRefGoogle Scholar
75.Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., & Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648), 251–260.PubMedCrossRefGoogle Scholar
76.Kanherkar, R. R., Bhatia-Dey, N., & Csoka, A. B. (2014). Epigenetics across the human lifespan. Frontiers in Cell and Development Biology, 2, 49.Google Scholar
77.Hawkins, R. D., Hon, G. C., Lee, L. K., et al. (2010). Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell, 6(5), 479–491.PubMedPubMedCentralCrossRefGoogle Scholar
78.Pan, G., Tian, S., Nie, J., et al. (2007). Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell, 1(3), 299–312.PubMedCrossRefGoogle Scholar
79.Bernstein, B. E., Mikkelsen, T. S., Xie, X., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125(2), 315–326.PubMedCrossRefGoogle Scholar
80.Noer, A., Lindeman, L. C., & Collas, P. (2009). Histone H3 modifications associated with differentiation and long-term culture of mesenchymal adipose stem cells. Stem Cells and Development, 18(5), 725–736.PubMedCrossRefGoogle Scholar
81.Matsui, M., & Corey, D. R. (2017). Non-coding RNAs as drug targets. Nature Reviews Drug Discovery, 16(3), 167–179.PubMedCrossRefGoogle Scholar
82.Bergmann, J. H., & Spector, D. L. (2014). Long non-coding RNAs: modulators of nuclear structure and function. Current Opinion in Cell Biology, 26, 10–18.PubMedCrossRefGoogle Scholar
83.Chuang, J. C., & Jones, P. A. (2007). Epigenetics and microRNAs. Pediatric Research, 61(5 Pt 2), 24R-29R.PubMedGoogle Scholar
84.Sato, F., Tsuchiya, S., Meltzer, S. J., & Shimizu, K. (2011). MicroRNAs and epigenetics. The FEBS Journal, 278(10), 1598–1609.PubMedCrossRefGoogle Scholar
85.Carthew, R. W., & Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136(4), 642–655.PubMedPubMedCentralCrossRefGoogle Scholar
86.Meister, G. (2013). Argonaute proteins: functional insights and emerging roles. Nature Reviews Genetics, 14(7), 447–459.PubMedCrossRefGoogle Scholar
87.Ha, H., Song, J., Wang, S., et al. (2014). A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics, 15, 545.PubMedPubMedCentralCrossRefGoogle Scholar
88.Le Thomas, A., Tóth, K. F., & Aravin, A. A. (2014). To be or not to be a piRNA: genomic origin and processing of piRNAs. Genome Biology, 15(1), 204.PubMedPubMedCentralCrossRefGoogle Scholar
89.Girard, A., Sachidanandam, R., Hannon, G. J., & Carmell, M. A. (2006). A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature, 442(7099), 199–202.PubMedGoogle Scholar
90.Lukic, S., & Chen, K. (2011). Human piRNAs are under selection in Africans and repress transposable elements. Molecular Biology and Evolution, 28(11), 3061–3067.PubMedPubMedCentralCrossRefGoogle Scholar
91.Hezroni, H., Koppstein, D., Schwartz, M. G., Avrutin, A., Bartel, D. P., & Ulitsky, I. (2015). Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell Reports, 11(7), 1110–1122.PubMedPubMedCentralCrossRefGoogle Scholar
92.Perry, R. B., & Ulitsky, I. (2016). The functions of long noncoding RNAs in development and stem cells. Development, 143(21), 3882–3894.PubMedCrossRefGoogle Scholar
93.Rackham, O., Shearwood, A. M., Mercer, T. R., Davies, S. M., Mattick, J. S., & Filipovska, A. (2011). Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA, 17(12), 2085–2093.PubMedPubMedCentralCrossRefGoogle Scholar
94.Burzio, V. A., Villota, C., Villegas, J., et al. (2009). Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 106(23), 9430–9434.PubMedPubMedCentralCrossRefGoogle Scholar
95.Noh, J. H., Kim, K. M., Abdelmohsen, K., et al. (2016). HuR and GRSF1 modulate the nuclear export and mitochondrial localization of the lncRNA RMRP. Genes and Development, 30(10), 1224–1239.PubMedPubMedCentralGoogle Scholar
96.Wang, Y., Pang, W. J., Wei, N., et al. (2014). Identification, stability and expression of Sirt1 antisense long non-coding RNA. Gene, 539(1), 117–124.PubMedCrossRefGoogle Scholar
97.Leucci, E., Vendramin, R., Spinazzi, M., et al. (2016). Melanoma addiction to the long non-coding RNA SAMMSON. Nature, 531(7595), 518–522.PubMedCrossRefGoogle Scholar
98.Mourtada-Maarabouni, M., Hasan, A. M., Farzaneh, F., & Williams, G. T. (2010). Inhibition of human T-cell proliferation by mammalian target of rapamycin (mTOR) antagonists requires noncoding RNA growth-arrest-specific transcript 5 (GAS5). Molecular Pharmacology, 78(1), 19–28.PubMedPubMedCentralCrossRefGoogle Scholar
99.Yang, F., Zhang, H., Mei, Y., & Wu, M. (2014). Reciprocal regulation of HIF-1α and lincRNA-p21 modulates the Warburg effect. Molecular Cell, 53(1), 88–100.PubMedCrossRefGoogle Scholar
100.Guttman, M., Donaghey, J., Carey, B. W., et al. (2011). lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 477(7364), 295–300.PubMedPubMedCentralCrossRefGoogle Scholar
101.Tsai, M. C., Manor, O., Wan, Y., et al. (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science, 329(5992), 689–693.PubMedPubMedCentralCrossRefGoogle Scholar
102.Kalwa, M., Hänzelmann, S., Otto, S., et al. (2016). The lncRNA HOTAIR impacts on mesenchymal stem cells via triple helix formation. Nucleic Acids Research, 44(22), 10631–10643.PubMedPubMedCentralCrossRefGoogle Scholar
103.Bao, X., Wu, H., Zhu, X., et al. (2015). The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters. Cell Research, 25(1), 80–92.PubMedCrossRefGoogle Scholar
104.Ramos, A. D., Andersen, R. E., Liu, S. J., et al. (2015). The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell, 16(4), 439–447.PubMedPubMedCentralCrossRefGoogle Scholar
105.Luo, M., Jeong, M., Sun, D., et al. (2015). Long non-coding RNAs control hematopoietic stem cell function. Cell Stem Cell, 16(4), 426–438.PubMedPubMedCentralCrossRefGoogle Scholar
106.Geiger, J., & Dalgaard, L. T. (2017). Interplay of mitochondrial metabolism and microRNAs. Cellular and Molecular Life Sciences, 74(4), 631–646.PubMedCrossRefGoogle Scholar
107.Ro, S., Ma, H. Y., Park, C., et al. (2013). The mitochondrial genome encodes abundant small noncoding RNAs. Cell Research, 23(6), 759–774.PubMedPubMedCentralCrossRefGoogle Scholar
108.Jagannathan, R., Thapa, D., Nichols, C. E., et al. (2015). Translational regulation of the mitochondrial genome following redistribution of mitochondrial microRNA in the diabetic heart. Circulation Cardiovascular Genetics, 8(6), 785–802.PubMedPubMedCentralCrossRefGoogle Scholar
109.Vidaurre, S., Fitzpatrick, C., Burzio, V. A., et al. (2014). Down-regulation of the antisense mitochondrial non-coding RNAs (ncRNAs) is a unique vulnerability of cancer cells and a potential target for cancer therapy. The Journal of Biological Chemistry, 289(39), 27182–27198.PubMedPubMedCentralCrossRefGoogle Scholar
110.Wang, W. X., Visavadiya, N. P., Pandya, J. D., Nelson, P. T., Sullivan, P. G., & Springer, J. E. (2015). Mitochondria-associated microRNAs in rat hippocampus following traumatic brain injury. Experimental Neurology, 265, 84–93.PubMedPubMedCentralCrossRefGoogle Scholar
111.Mercer, T. R., Neph, S., Dinger, M. E., et al. (2011). The human mitochondrial transcriptome. Cell, 146(4), 645–658.PubMedPubMedCentralCrossRefGoogle Scholar
112.Sripada, L., Tomar, D., Prajapati, P., Singh, R., Singh, A. K., & Singh, R. (2012). Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One, 7(9), e44873.PubMedPubMedCentralCrossRefGoogle Scholar
113.Bian, Z., Li, L. M., Tang, R., et al. (2010). Identification of mouse liver mitochondria-associated miRNAs and their potential biological functions. Cell Research, 20(9), 1076–1078.PubMedCrossRefGoogle Scholar
114.Kren, B. T., Wong, P. Y., Sarver, A., Zhang, X., Zeng, Y., & Steer, C. J. (2009). MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis. RNA Biology, 6(1), 65–72.PubMedPubMedCentralCrossRefGoogle Scholar
115.Barrey, E., Saint-Auret, G., Bonnamy, B., Damas, D., Boyer, O., & Gidrol, X. (2011). Pre-microRNA and mature microRNA in human mitochondria. PLoS One, 6(5), e20220.PubMedPubMedCentralCrossRefGoogle Scholar
116.Watanabe, T., Chuma, S., Yamamoto, Y., et al. (2011). MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Developmental Cell, 20(3), 364–375.PubMedPubMedCentralCrossRefGoogle Scholar
117.Huang, H., Gao, Q., Peng, X., et al. (2011). piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Developmental Cell, 20(3), 376–387.PubMedPubMedCentralCrossRefGoogle Scholar
118.Shiromoto, Y., Kuramochi-Miyagawa, S., Daiba, A., et al. (2013). GPAT2, a mitochondrial outer membrane protein, in piRNA biogenesis in germline stem cells. RNA, 19(6), 803–810.PubMedPubMedCentralCrossRefGoogle Scholar
119.Ng, K. W., Anderson, C., Marshall, E. A., et al. (2016). Piwi-interacting RNAs in cancer: emerging functions and clinical utility. Molecular Cancer, 15, 5.PubMedPubMedCentralCrossRefGoogle Scholar
120.Suzuki, R., Honda, S., & Kirino, Y. (2012). PIWI expression and function in cancer. Frontiers Genetics, 3, 204.CrossRefGoogle Scholar
121.Siddiqi, S., & Matushansky, I. (2012). Piwis and piwi-interacting RNAs in the epigenetics of cancer. Journal of Cellular Biochemistry, 113(2), 373–380.PubMedCrossRefGoogle Scholar
122.Kwon, C., Tak, H., Rho, M., et al. (2014). Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells. Biochemical and Biophysical Research Communications, 446(1), 218–223.PubMedCrossRefGoogle Scholar
123.Shang, J., Yao, Y., Fan, X., et al. (2016). miR-29c-3p promotes senescence of human mesenchymal stem cells by targeting CNOT6 through p53-p21 and p16-pRB pathways. Biochimica et Biophysica Acta, 1863(4), 520–532.Google Scholar
124.Park, H., Park, H., Pak, H. J., et al. (2015). miR-34a inhibits differentiation of human adipose tissue-derived stem cells by regulating cell cycle and senescence induction. Differentiation, 90(4–5), 91–100.PubMedCrossRefGoogle Scholar
125.Clark, E. A., Kalomoiris, S., Nolta, J. A., & Fierro, F. A. (2014). Concise review: microRNA function in multipotent mesenchymal stromal cells. Stem Cells, 32(5), 1074–1082.PubMedCrossRefGoogle Scholar
126.Mathieu, J., & Ruohola-Baker, H. (2013). Regulation of stem cell populations by microRNAs. Advances in Experimental Medicine and Biology, 786, 329–351.PubMedPubMedCentralCrossRefGoogle Scholar
127.Ma, Y., Lin, H., & Qiu, C. (2012). High-efficiency transfection and siRNA-mediated gene knockdown in human pluripotent stem cells. Current Protocols in Stem Cell Biology, Chap. 2:Unit 5C.2.Google Scholar
128.Renz, P. F., & Beyer, T. A. (2016). A Concise protocol for siRNA-mediated gene suppression in human embryonic stem cells. Methods in Molecular Biology, 134, 369–376.Google Scholar
129.Zoldan, J., Lytton-Jean, A. K., Karagiannis, E. D., et al. (2011). Directing human embryonic stem cell differentiation by non-viral delivery of siRNA in 3D culture. Biomaterials, 32(31), 7793–7800.PubMedPubMedCentralCrossRefGoogle Scholar
130.Wang, Z., Hu, Z., Zhang, D., et al. (2016). Silencing tumor necrosis factor-alpha in vitro from small interfering RNA-decorated titanium nanotube array can facilitate osteogenic differentiation of mesenchymal stem cells. International Journal of NanoMedicine, 11, 3205–3214.PubMedPubMedCentralGoogle Scholar
131.Wu, Y., Zhou, B., Xu, F., et al. (2016). Functional quantum dot-siRNA nanoplexes to regulate chondrogenic differentiation of mesenchymal stem cells. Acta Biomaterialia, 46, 165–176.PubMedCrossRefGoogle Scholar
132.Teoh, H. K., Chong, P. P., Abdullah, M., et al. (2016). Small interfering RNA silencing of interleukin-6 in mesenchymal stromal cells inhibits multiple myeloma cell growth. Leukemia Research, 40, 44–53.PubMedCrossRefGoogle Scholar
133.Bamezai, S., Rawat, V. P., & Buske, C. (2012). Concise review: the Piwi-piRNA axis: pivotal beyond transposon silencing. Stem Cells, 30(12), 2603–2611.PubMedCrossRefGoogle Scholar
134.Peng, J. C., & Lin, H. (2013). Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Current Opinion in Cell Biology, 25(2), 190–194.PubMedPubMedCentralCrossRefGoogle Scholar
135.De Luca, L., Trino, S., Laurenzana, I., et al. (2016). MiRNAs and piRNAs from bone marrow mesenchymal stem cell extracellular vesicles induce cell survival and inhibit cell differentiation of cord blood hematopoietic stem cells: a new insight in transplantation. Oncotarget, 7(6), 6676–6692.PubMedCrossRefGoogle Scholar
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