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Molecular biology reports
Oct 08, 2024;51 (1): 1045.

Mining of potentially stem cell-related miRNAs in planarians.

Nianhong Xing, Lili Gao, Wenshuo Xie, Hongkuan Deng, Fengtang Yang, Dongwu Liu, Ao Li, Qiuxiang Pang
Author Information
  1. Nianhong Xing: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  2. Lili Gao: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China. gaoli96@sdut.edu.cn.
  3. Wenshuo Xie: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  4. Hongkuan Deng: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  5. Fengtang Yang: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  6. Dongwu Liu: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  7. Ao Li: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China.
  8. Qiuxiang Pang: Anti-aging & Regenerative Medicine Research Institute, School of Life Sciences and Medicine, Shandong University of Technology, Zibo, 255049, China. pangqiuxiang@sdut.edu.cn.
PMID: 39377855 DOI: 10.1007/s11033-024-09977-6

Abstract

Stem cells and regenerative medicine have recently become important research topics. However, the complex stem cell regulatory networks involved in various microRNA (miRNA)-mediated mechanisms have not yet been fully elucidated. Planarians are ideal animal models for studying stem cells owing to their rich stem cell populations (neoblasts) and extremely strong regeneration capacity. The roles of planarian miRNAs in stem cells and regeneration have long attracted attention. However, previous studies have generally provided simple datasets lacking integrative analysis. Here, we have summarized the miRNA family reported in planarians and highlighted conservation in both sequence and function. Furthermore, we summarized miRNA data related to planarian stem cells and regeneration and screened potential involved candidates. Nevertheless, the roles of these miRNAs in planarian regeneration and stem cells remain unclear. The identification of potential stem cell-related miRNAs offers more precise suggestions and references for future investigations of miRNAs in planarians. Furthermore, it provides potential research avenues for understanding the mechanisms of stem cell regulatory networks. Finally, we compiled a summary of the experimental methods employed for studying planarian miRNAs, with the aim of highlighting special considerations in certain procedures and providing more convenient technical support for future research endeavors.

Keywords

Methods Planarian Regeneration Research progress miRNA

References

  1. Hoang DM, Pham PT, Bach TQ et al (2022) Stem cell-based therapy for human diseases. Signal Transduct Target Ther 7:272. https://doi.org/10.1038/s41392-022-01134-4 [DOI: 10.1038/s41392-022-01134-4]
  2. Dattani A, Sridhar D, Aziz Aboobaker A (2019) Planarian flatworms as a new model system for understanding the epigenetic regulation of stem cell pluripotency and differentiation. Semin Cell Dev Biol 87:79–94. https://doi.org/10.1016/j.semcdb.2018.04.007 [DOI: 10.1016/j.semcdb.2018.04.007]
  3. Ivankovic M, Haneckova R, Thommen A et al (2019) Model systems for regeneration: planarians. Development 146(17):dev167684. https://doi.org/10.1242/dev.167684
  4. Chen JJ, Lei K (2023) The known, unknown, and unknown unknowns of cell-cell communication in planarian regeneration. Zool Res 44:981–992. https://doi.org/10.24272/j.issn.2095-8137.2023.044 [DOI: 10.24272/j.issn.2095-8137.2023.044]
  5. Rossi L, Salvetti A, Batistoni R et al (2008) Planarians, a tale of stem cells. Cell Mol Life Sci 65:16–23. https://doi.org/10.1007/s00018-007-7426-y [DOI: 10.1007/s00018-007-7426-y]
  6. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332:811–816. https://doi.org/10.1126/science.1203983 [DOI: 10.1126/science.1203983]
  7. Solana J, Kao D, Mihaylova Y et al (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol 13:R19. https://doi.org/10.1186/gb-2012-13-3-r19 [DOI: 10.1186/gb-2012-13-3-r19]
  8. Resch AM, Palakodeti D (2012) Small RNA pathways in Schmidtea mediterranea. Int J Dev Biol 56:67–74. https://doi.org/10.1387/ijdb.113436ar [DOI: 10.1387/ijdb.113436ar]
  9. Sanchez Alvarado A, Kang H (2005) Multicellularity, stem cells, and the neoblasts of the planarian Schmidtea mediterranea. Exp Cell Res 306:299–308. https://doi.org/10.1016/j.yexcr.2005.03.020 [DOI: 10.1016/j.yexcr.2005.03.020]
  10. Barghouth PG, Thiruvalluvan M, LeGro M et al (2019) DNA damage and tissue repair: what we can learn from planaria. Semin Cell Dev Biol 87:145–159. https://doi.org/10.1016/j.semcdb.2018.04.013 [DOI: 10.1016/j.semcdb.2018.04.013]
  11. Witchley JN, Mayer M, Wagner DE et al (2013) Muscle cells provide instructions for planarian regeneration. Cell Rep 4:633–641. https://doi.org/10.1016/j.celrep.2013.07.022 [DOI: 10.1016/j.celrep.2013.07.022]
  12. Reddien PW (2022) Positional information and stem cells combine to result in planarian regeneration. Cold Spring Harb Perspect Biol 14(4):a040717. https://doi.org/10.1101/cshperspect.a040717
  13. Reddien PW (2021) Principles of regeneration revealed by the planarian eye. Curr Opin Cell Biol 73:19–25. https://doi.org/10.1016/j.ceb.2021.05.001 [DOI: 10.1016/j.ceb.2021.05.001]
  14. Reddien PW (2018) The Cellular and molecular basis for Planarian Regeneration. Cell 175:327–345. https://doi.org/10.1016/j.cell.2018.09.021 [DOI: 10.1016/j.cell.2018.09.021]
  15. Tewari AG, Stern SR, Oderberg IM et al (2018) Cellular and molecular responses unique to Major Injury Are Dispensable for Planarian Regeneration. Cell Rep 25:2577–2590e2573. https://doi.org/10.1016/j.celrep.2018.11.004 [DOI: 10.1016/j.celrep.2018.11.004]
  16. Rink JC, Gurley KA, Elliott SA et al (2009) Planarian Hh signaling regulates regeneration polarity and links hh pathway evolution to cilia. Science 326:1406–1410. https://doi.org/10.1126/science.1178712 [DOI: 10.1126/science.1178712]
  17. Nogi T, Zhang D, Chan JD et al (2009) A novel biological activity of praziquantel requiring voltage-operated Ca2 + channel beta subunits: subversion of flatworm regenerative polarity. PLoS Negl Trop Dis 3:e464. https://doi.org/10.1371/journal.pntd.0000464 [DOI: 10.1371/journal.pntd.0000464]
  18. Sasidharan V, Marepally S, Elliott SA et al (2017) The miR-124 family of microRNAs is crucial for regeneration of the brain and visual system in the planarian Schmidtea mediterranea. Development 144:3211–3223. https://doi.org/10.1242/dev.144758 [DOI: 10.1242/dev.144758]
  19. Kim IV, Riedelbauch S, Kuhn CD (2020) The piRNA pathway in planarian flatworms: new model, new insights. Biol Chem 401:1123–1141. https://doi.org/10.1515/hsz-2019-0445 [DOI: 10.1515/hsz-2019-0445]
  20. Allikka Parambil S, Li D, Zelko M et al (2024) piRNA generation is associated with the pioneer round of translation in stem cells. Nucleic Acids Res 52:2590–2608. https://doi.org/10.1093/nar/gkad1212 [DOI: 10.1093/nar/gkad1212]
  21. Cui G, Zhou JY, Ge XY et al (2023) M(6) a promotes planarian regeneration. Cell Prolif 56:e13481. https://doi.org/10.1111/cpr.13481 [DOI: 10.1111/cpr.13481]
  22. Barberan S, Fraguas S, Cebria F (2016) The EGFR signaling pathway controls gut progenitor differentiation during planarian regeneration and homeostasis. Development 143:2089–2102. https://doi.org/10.1242/dev.131995 [DOI: 10.1242/dev.131995]
  23. Deb S, Felix DA, Koch P et al (2021) Tnfaip2/exoc3-driven lipid metabolism is essential for stem cell differentiation and organ homeostasis. EMBO Rep 22:e49328. https://doi.org/10.15252/embr.201949328 [DOI: 10.15252/embr.201949328]
  24. Coronel-Cordoba P, Molina MD, Cardona G et al (2022) FoxK1 is required for ectodermal cell differentiation during Planarian Regeneration. Front Cell Dev Biol 10:808045. https://doi.org/10.3389/fcell.2022.808045 [DOI: 10.3389/fcell.2022.808045]
  25. Wu W, Liu S, Wu H et al (2022) DjPtpn11 is an essential modulator of planarian (Dugesia japonica) regeneration. Int J Biol Macromol 209:1054–1064. https://doi.org/10.1016/j.ijbiomac.2022.04.095 [DOI: 10.1016/j.ijbiomac.2022.04.095]
  26. Ma K, Li R, Song G et al (2022) Djhsp60 is required for planarian regeneration and homeostasis. Biomolecules 12(6):808. https://doi.org/10.3390/biom12060808
  27. Zhen H, Huang M, Zheng M et al (2023) WTAP regulates stem cells via TRAF6 to maintain planarian homeostasis and regeneration. Int J Biol Macromol 242:124932. https://doi.org/10.1016/j.ijbiomac.2023.124932 [DOI: 10.1016/j.ijbiomac.2023.124932]
  28. Resch AM, Palakodeti D, Lu YC et al (2012) Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS ONE 7:e34447. https://doi.org/10.1371/journal.pone.0034447 [DOI: 10.1371/journal.pone.0034447]
  29. Hayashi T, Asami M, Higuchi S et al (2006) Isolation of planarian x-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48:371–380. https://doi.org/10.1111/j.1440-169X.2006.00876.x [DOI: 10.1111/j.1440-169X.2006.00876.x]
  30. Eisenhoffer GT, Kang H, Sanchez Alvarado A (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3:327–339. https://doi.org/10.1016/j.stem.2008.07.002 [DOI: 10.1016/j.stem.2008.07.002]
  31. Labbe RM, Irimia M, Currie KW et al (2012) A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30:1734–1745. https://doi.org/10.1002/stem.1144 [DOI: 10.1002/stem.1144]
  32. Onal P, Grun D, Adamidi C et al (2012) Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO J 31:2755–2769. https://doi.org/10.1038/emboj.2012.110 [DOI: 10.1038/emboj.2012.110]
  33. Sahu S, Dattani A, Aboobaker AA (2017) Secrets from immortal worms: what can we learn about biological ageing from the planarian model system? Semin Cell Dev Biol 70:108–121. https://doi.org/10.1016/j.semcdb.2017.08.028 [DOI: 10.1016/j.semcdb.2017.08.028]
  34. Zeng A, Li H, Guo L et al (2018) Prospectively isolated tetraspanin(+) neoblasts are adult pluripotent stem cells underlying Planaria Regeneration. Cell 173:1593–1608e1520. https://doi.org/10.1016/j.cell.2018.05.006 [DOI: 10.1016/j.cell.2018.05.006]
  35. Fincher CT, Wurtzel O, de Hoog T et al (2018) Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360(6391):eaaq1736. https://doi.org/10.1126/science.aaq1736
  36. Plass M, Solana J, Wolf FA et al (2018) Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360(6391):eaaq1723. https://doi.org/10.1126/science.aaq1723
  37. De Marco P, Merello E, Piatelli G et al (2014) Planar cell polarity gene mutations contribute to the etiology of human neural tube defects in our population. Birth Defects Res Clin Mol Teratol 100:633–641. https://doi.org/10.1002/bdra.23255 [DOI: 10.1002/bdra.23255]
  38. Petersen CP, Reddien PW (2009) Wnt signaling and the polarity of the primary body axis. Cell 139:1056–1068. https://doi.org/10.1016/j.cell.2009.11.035 [DOI: 10.1016/j.cell.2009.11.035]
  39. Sturm A, Perczel A, Ivics Z et al (2017) The Piwi-piRNA pathway: road to immortality. Aging Cell 16:906–911. https://doi.org/10.1111/acel.12630 [DOI: 10.1111/acel.12630]
  40. Rizzo F, Rinaldi A, Marchese G et al (2016) Specific patterns of PIWI-interacting small noncoding RNA expression in dysplastic liver nodules and hepatocellular carcinoma. Oncotarget 7:54650–54661. https://doi.org/10.18632/oncotarget.10567 [DOI: 10.18632/oncotarget.10567]
  41. Reddien PW, Oviedo NJ, Jennings JR et al (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–1330. https://doi.org/10.1126/science.1116110 [DOI: 10.1126/science.1116110]
  42. Tesar PJ, Chenoweth JG, Brook FA et al (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196–199. https://doi.org/10.1038/nature05972 [DOI: 10.1038/nature05972]
  43. Huang Y, Osorno R, Tsakiridis A et al (2012) In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep 2:1571–1578. https://doi.org/10.1016/j.celrep.2012.10.022 [DOI: 10.1016/j.celrep.2012.10.022]
  44. Li N, Long B, Han W et al (2017) microRNAs: important regulators of stem cells. Stem Cell Res Ther 8(1):110. https://doi.org/10.1186/s13287-017-0551-0 [DOI: 10.1186/s13287-017-0551-0]
  45. Pasquinelli AE, Ruvkun G (2002) Control of developmental timing by micrornas and their targets. Annu Rev Cell Dev Biol 18:495–513. https://doi.org/10.1146/annurev.cellbio.18.012502.105832 [DOI: 10.1146/annurev.cellbio.18.012502.105832]
  46. Fava P, Bergallo M, Astrua C et al (2017) miR-155 expression in primary cutaneous T-Cell lymphomas (CTCL). J Eur Acad Dermatol Venereol 31:e27–e29. https://doi.org/10.1111/jdv.13597 [DOI: 10.1111/jdv.13597]
  47. Gulyaeva LF, Kushlinskiy NE (2016) Regulatory mechanisms of microRNA expression. J Transl Med 14(1):143. https://doi.org/10.1186/s12967-016-0893-x [DOI: 10.1186/s12967-016-0893-x]
  48. Walker SE, Spencer GE, Necakov A et al (2018) Identification and characterization of microRNAs during retinoic acid-induced regeneration of a molluscan central nervous system. Int J Mol Sci 19(9):2741. https://doi.org/10.3390/ijms19092741
  49. Palakodeti D, Smielewska M, Graveley BR (2006) MicroRNAs from the Planarian Schmidtea mediterranea: a model system for stem cell biology. RNA 12:1640–1649. https://doi.org/10.1261/rna.117206 [DOI: 10.1261/rna.117206]
  50. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338. https://doi.org/10.1126/science.1085242 [DOI: 10.1126/science.1085242]
  51. Lagos-Quintana M, Rauhut R, Lendeckel W et al (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858. https://doi.org/10.1126/science.1064921 [DOI: 10.1126/science.1064921]
  52. Lau NC, Lim LP, Weinstein EG et al (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862. https://doi.org/10.1126/science.1065062 [DOI: 10.1126/science.1065062]
  53. Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864. https://doi.org/10.1126/science.1065329 [DOI: 10.1126/science.1065329]
  54. Moss EG (2002) MicroRNAs: hidden in the genome. Curr Biol 12:R138–140. https://doi.org/10.1016/s0960-9822(02)00708-x [DOI: 10.1016/s0960-9822(02)00708-x]
  55. Angelopoulou E, Paudel YN, Piperi C (2019) miR-124 and Parkinson’s disease: a biomarker with therapeutic potential. Pharmacol Res 150:104515. https://doi.org/10.1016/j.phrs.2019.104515 [DOI: 10.1016/j.phrs.2019.104515]
  56. Meng Y, Shang F, Zhu Y (2019) miR-124 participates in the proliferation and differentiation of brain glioma stem cells through regulating Nogo/NgR expression. Exp Ther Med 18:2783–2788. https://doi.org/10.3892/etm.2019.7914 [DOI: 10.3892/etm.2019.7914]
  57. Clark AM, Goldstein LD, Tevlin M et al (2010) The microRNA miR-124 controls gene expression in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Res 38:3780–3793. https://doi.org/10.1093/nar/gkq083 [DOI: 10.1093/nar/gkq083]
  58. Peng XH, Huang HR, Lu J et al (2014) MiR-124 suppresses tumor growth and metastasis by targeting Foxq1 in nasopharyngeal carcinoma. Mol Cancer 13:186. https://doi.org/10.1186/1476-4598-13-186 [DOI: 10.1186/1476-4598-13-186]
  59. Sasidharan V, Lu Y-C, Bansal D et al (2013) Identification of neoblast- and regeneration-specific miRNAs in the planarian Schmidtea mediterranea. RNA 19:1394–1404. https://doi.org/10.1261/rna.038653.113 [DOI: 10.1261/rna.038653.113]
  60. González-Estévez C, Arseni V, Thambyrajah RS et al (2009) Diverse miRNA spatial expression patterns suggest important roles in homeostasis and regeneration in planarians. Int J Dev Biol 53:493–505. https://doi.org/10.1387/ijdb.082825cg [DOI: 10.1387/ijdb.082825cg]
  61. Cao Z, Rosenkranz D, Wu S et al (2020) Different classes of small RNAs are essential for head regeneration in the planarian Dugesia japonica. BMC Genomics 21(1):876. https://doi.org/10.1186/s12864-020-07234-1 [DOI: 10.1186/s12864-020-07234-1]
  62. Trumbach D, Prakash N (2015) The conserved miR-8/miR-200 microRNA family and their role in invertebrate and vertebrate neurogenesis. Cell Tissue Res 359:161–177. https://doi.org/10.1007/s00441-014-1911-z [DOI: 10.1007/s00441-014-1911-z]
  63. Liu H, Song Q, Zhen H et al (2021) miR-8b is involved in brain and eye regeneration of Dugesia japonica in head regeneration. Biol Open 10(6):bio058538. https://doi.org/10.1242/bio.058538
  64. Xiao J, Liu H, Cretoiu D et al (2017) miR-31a-5p promotes postnatal cardiomyocyte proliferation by targeting RhoBTB1. Exp Mol Med 49:e386. https://doi.org/10.1038/emm.2017.150 [DOI: 10.1038/emm.2017.150]
  65. Feng Q, Tian T, Liu J et al (2018) Deregulation of microRNA–31a–5p is involved in the development of primary hypertension by suppressing apoptosis of pulmonary artery smooth muscle cells via targeting TP53. Int J Mol Med 42:290–298. https://doi.org/10.3892/ijmm.2018.3597 [DOI: 10.3892/ijmm.2018.3597]
  66. Yan MJ, Tian ZS, Zhao ZH et al (2018) MiR-31a-5p protects myocardial cells against apoptosis by targeting Tp53. Mol Med Rep 17:3898–3904. https://doi.org/10.3892/mmr.2017.8357 [DOI: 10.3892/mmr.2017.8357]
  67. Roush S, Slack FJ (2008) The let-7 family of microRNAs. Trends Cell Biol 18:505–516. https://doi.org/10.1016/j.tcb.2008.07.007 [DOI: 10.1016/j.tcb.2008.07.007]
  68. Kitatani Y, Tezuka A, Hasegawa E et al (2020) Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69. PLoS Genet 16:e1008942. https://doi.org/10.1371/journal.pgen.1008942 [DOI: 10.1371/journal.pgen.1008942]
  69. Sun B, Meng M, Wei J et al (2020) Long noncoding RNA PVT1 contributes to vascular endothelial cell proliferation via inhibition of miR-190a-5p in diagnostic biomarker evaluation of chronic heart failure. Exp Ther Med 19:3348–3354. https://doi.org/10.3892/etm.2020.8599 [DOI: 10.3892/etm.2020.8599]
  70. Wenemoser D, Reddien PW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344:979–991. https://doi.org/10.1016/j.ydbio.2010.06.017 [DOI: 10.1016/j.ydbio.2010.06.017]
  71. Wenemoser D, Lapan SW, Wilkinson AW et al (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26:988–1002. https://doi.org/10.1101/gad.187377.112 [DOI: 10.1101/gad.187377.112]
  72. Li Y, Zeng A, Han XS et al (2017) Small RNAome sequencing delineates the small RNA landscape of pluripotent adult stem cells in the planarian Schmidtea mediterranea. Genom Data 14:114–125. https://doi.org/10.1016/j.gdata.2017.10.004 [DOI: 10.1016/j.gdata.2017.10.004]
  73. Ambros V (2001) microRNAs: tiny regulators with great potential. Cell 107:823–826. https://doi.org/10.1016/s0092-8674(01)00616-x [DOI: 10.1016/s0092-8674(01)00616-x]
  74. Xu Z, Chen M, Ren Z et al (2013) Deep sequencing identifies regulated small RNAs in Dugesia japonica. Mol Biol Rep 40:4075–4081. https://doi.org/10.1007/s11033-012-2485-z [DOI: 10.1007/s11033-012-2485-z]
  75. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. https://doi.org/10.1016/s0092-8674(04)00045-5 [DOI: 10.1016/s0092-8674(04)00045-5]
  76. Li YQ, Zeng A, Han XS et al (2011) Argonaute-2 regulates the proliferation of adult stem cells in planarian. Cell Res 21:1750–1754. https://doi.org/10.1038/cr.2011.151 [DOI: 10.1038/cr.2011.151]
  77. Krishna S, Palakodeti D, Solana J (2019) Post-transcriptional regulation in planarian stem cells. Semin Cell Dev Biol 87:69–78. https://doi.org/10.1016/j.semcdb.2018.05.013 [DOI: 10.1016/j.semcdb.2018.05.013]
  78. Lu YC, Smielewska M, Palakodeti D et al (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. RNA 15:1483–1491. https://doi.org/10.1261/rna.1702009 [DOI: 10.1261/rna.1702009]
  79. Friedlander MR, Adamidi C, Han T et al (2009) High-resolution profiling and discovery of planarian small RNAs. Proc Natl Acad Sci U S A 106:11546–11551. https://doi.org/10.1073/pnas.0905222106 [DOI: 10.1073/pnas.0905222106]
  80. Tian QN, Bao ZX, Lu P et al (2012) Differential expression of microRNA patterns in planarian normal and regenerative tissues. Mol Biol Rep 39:2653–2658. https://doi.org/10.1007/s11033-011-1018-5 [DOI: 10.1007/s11033-011-1018-5]
  81. Bussing I, Slack FJ, Grosshans H (2008) let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 14:400–409. https://doi.org/10.1016/j.molmed.2008.07.001 [DOI: 10.1016/j.molmed.2008.07.001]
  82. Cui Y, Xiao Z, Chen T et al (2014) The miR-7 identified from collagen biomaterial-based three-dimensional cultured cells regulates neural stem cell differentiation. Stem Cells Dev 23:393–405. https://doi.org/10.1089/scd.2013.0342 [DOI: 10.1089/scd.2013.0342]
  83. Kang T, Jones TM, Naddell C et al (2016) Adipose-derived stem cells induce Angiogenesis via Microvesicle Transport of miRNA-31. Stem Cells Transl Med 5:440–450. https://doi.org/10.5966/sctm.2015-0177 [DOI: 10.5966/sctm.2015-0177]
  84. Zhen L, Jiang X, Chen Y et al (2017) MiR-31 is involved in the high glucose-suppressed osteogenic differentiation of human periodontal ligament stem cells by targeting Satb2. Am J Transl Res 9:2384–2393 [PMID: 28559988]
  85. Biamonte F, Santamaria G, Sacco A et al (2019) MicroRNA let-7 g acts as tumor suppressor and predictive biomarker for chemoresistance in human epithelial ovarian cancer. Sci Rep 9:5668. https://doi.org/10.1038/s41598-019-42221-x [DOI: 10.1038/s41598-019-42221-x]
  86. Chen CY, Choong OK, Liu LW et al (2019) MicroRNA let-7-TGFBR3 signalling regulates cardiomyocyte apoptosis after infarction. EBioMedicine 46:236–247. https://doi.org/10.1016/j.ebiom.2019.08.001 [DOI: 10.1016/j.ebiom.2019.08.001]
  87. Kloosterman WP, Wienholds E, Ketting RF et al (2016) Substrate requirements for let-7 function in the developing zebrafish embryo. Nucleic Acids Res 44:5993. https://doi.org/10.1093/nar/gkw173 [DOI: 10.1093/nar/gkw173]
  88. Tokumaru S, Suzuki M, Yamada H et al (2008) let-7 regulates dicer expression and constitutes a negative feedback loop. Carcinogenesis 29:2073–2077. https://doi.org/10.1093/carcin/bgn187 [DOI: 10.1093/carcin/bgn187]
  89. Kim YK, Yeo J, Kim B et al (2012) Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 46:893–895. https://doi.org/10.1016/j.molcel.2012.05.036 [DOI: 10.1016/j.molcel.2012.05.036]
  90. Moldovan L, Batte K, Wang Y et al (2013) Analyzing the circulating microRNAs in exosomes/extracellular vesicles from serum or plasma by qRT-PCR. Methods Mol Biol 1024:129–145. https://doi.org/10.1007/978-1-62703-453-1_10 [DOI: 10.1007/978-1-62703-453-1_10]
  91. Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39:519–525. https://doi.org/10.2144/000112010 [DOI: 10.2144/000112010]
  92. Wu YY, Zhao JM, Liu Q et al (2015) miR-71b regulation of insulin/IGF-1 signaling during starvation in planarians. Genet Mol Res 14:11905–11914. https://doi.org/10.4238/2015.October.5.4 [DOI: 10.4238/2015.October.5.4]
  93. Lennox KA, Behlke MA (2011) Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther 18:1111–1120. https://doi.org/10.1038/gt.2011.100 [DOI: 10.1038/gt.2011.100]
  94. Orii H, Mochii M, Watanabe K (2003) A simple soaking method for RNA interference in the planarian Dugesia japonica. Dev Genes Evol 213:138–141. https://doi.org/10.1007/s00427-003-0310-3 [DOI: 10.1007/s00427-003-0310-3]
  95. Martin-Duran JM, Duocastella M, Serra P et al (2008) New method to deliver exogenous material into developing planarian embryos. J Exp Zool B Mol Dev Evol 310:668–681. https://doi.org/10.1002/jez.b.21243 [DOI: 10.1002/jez.b.21243]
  96. Gonzalez-Estevez C, Momose T, Gehring WJ et al (2003) Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proc Natl Acad Sci U S A 100:14046–14051. https://doi.org/10.1073/pnas.2335980100 [DOI: 10.1073/pnas.2335980100]
  97. Sanchez Alvarado A, Newmark PA (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci U S A 96:5049–5054. https://doi.org/10.1073/pnas.96.9.5049 [DOI: 10.1073/pnas.96.9.5049]
  98. Lim WF, Inoue-Yokoo T, Tan KS et al (2013) Hematopoietic cell differentiation from embryonic and induced pluripotent stem cells. Stem Cell Res Ther 4(3):71. https://doi.org/10.1186/scrt222 [DOI: 10.1186/scrt222]
  99. Sarkar A, Saha S, Paul A et al (2021) Understanding stem cells and its pivotal role in regenerative medicine. Life Sci 273:119270. https://doi.org/10.1016/j.lfs.2021.119270 [DOI: 10.1016/j.lfs.2021.119270]

MeSH Term

Animals
Planarians
MicroRNAs
Stem Cells
Regeneration
Gene Regulatory Networks

Chemicals

MicroRNAs
Journal Article Review
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Word Cloud

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