Regulatory RNAs in Planarians

  • Kamila Pawlicka Intstitute of Bioorganic Chemistry, Polish Academy of Sciences
  • Patrick McDevitt Perrigue Intstitute of Bioorganic Chemistry, Polish Academy of Sciences
  • Jan Barciszewski Intstitute of Bioorganic Chemistry, Polish Academy of Sciences
Keywords: planarians, RNAi, miRNA, regeneration, stem cells

Abstract

The full scope of regulatory RNA evolution and function in epigenetic processes is still not well understood. The development of planarian flatworms to be used as a simple model organism for research has shown great potential to address gaps in knowledge in this field of study. The genomes of planarians encode a wide array of regulatory RNAs that function in gene regulation. Here we review planarians as a suitable model organism for the identification and function of regulatory RNAs.

References

Aboobaker AA (2011) Planarian stem cells: a simple paradigm for regeneration. Trends Cell Biol 21: 304-311.

Alvarado AS (2003) The freshwater planarian Schmidtea mediterranea: embryogenesis, stem cells and regeneration - Commentary. Curr Opin Genet Dev 13: 438-444.

Alvarado AS (2012) Q&A: What is regeneration, and why look to planarians for answers? BMC Biol 10.

Alvarado AS, Kang H (2005) Multicellularity, stem cells, and the neoblasts of the planarian Schmidtea mediterranea. Exp Cell Res 306: 299-308.

Alvarado AS, Newmark PA (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96: 5049-5054.

Alvarado AS, Newmark PA, Robb SMC, Juste R (2002) The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129: 5659-5665.

Bamezai S, Rawat VPS, Buske C (2012) Concise Review: The Piwi-piRNA Axis: Pivotal Beyond Transposon Silencing. Stem Cells 30: 2603-2611.

Cebria F, Kobayashi C, Umesono Y, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Itoh M, Taira M, Alvarado AS, Agata K (2002) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419: 620-624.

Cowles MW, Omuro KC, Stanley BN, Quintanilla CG, Zayas RM (2014) COE Loss-of-Function Analysis Reveals a Genetic Program Underlying Maintenance and Regeneration of the Nervous System in Planarians. Plos Genet 10.

Currie KW, Pearson BJ (2013) Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 140: 3577-3588.

Deng CW, Li Y, Zhou L, Cho J, Patel B, Terada N, Li YQ, Bungert J, Qiu Y, Huang SM (2016) HoxBlinc RNA Recruits Set1/MLL Complexes to Activate Hox Gene Expression Patterns and Mesoderm Lineage Development. Cell Rep 14: 103-114.

Denli AM, Tops BBJ, Plasterk RHA, Ketting RF, Hannon GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432: 231-235.

Duncan EM, Chitsazan AD, Seidel CW, Sanchez Alvarado A (2015) Set1 and MLL1/2 Target Distinct Sets of Functionally Different Genomic Loci In Vivo. Cell Rep 13: 2741-2755.

Eisenhoffer GT, Kang H, Alvarado AS (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.

Friedlander MR, Adamidi C, Han T, Lebedeva S, Isenbarger TA, Hirst M, Marra M, Nusbaum C, Lee WL, Jenkin JC, Alvarado AS, Kim JK, Rajewsky N (2009) High-resolution profiling and discovery of planarian small RNAs. Proc Natl Acad Sci USA 106: 11546-11551.

Gonzalez-Estevez C, Arseni V, Thambyrajah RS, Felix DA, Aboobaker AA (2009) Diverse miRNA spatial expression patterns suggest important roles in homeostasis and regeneration in planarians. Int J Dev Biol 53: 493-505.

He L, Hannon GJ (2004) Micrornas: Small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531.

Hubert A, Henderson JM, Ross KG, Cowles MW, Torres J, Zayas RM (2013) Epigenetic regulation of planarian stem cells by the SET1/MLL family of histone methyltransferases. Epigenetics 8: 79-91.

Johnson CD, Esquela-Kerscher A, Stefani G, Byrom N, Kelnar K, Ovcharenko D, Wilson M, Wang XW, Shelton J, Shingara J, Chin L, Brown D, Slack FJ (2007) The let-7 MicroRNA represses cell proliferation pathways in human cells. Cancer Res 67: 7713-7722.

Juliano C, Wang JQ, Lin HF (2011) Uniting Germline and Stem Cells: The Function of Piwi Proteins and the piRNA Pathway in Diverse Organisms. Annu Rev Genet 45: 447-469.

Kang H, Alvarado AS (2009) Flow Cytometry Methods for the Study of Cell-Cycle Parameters of Planarian Stem Cells. Dev Dynam 238: 1111-1117.

Kao D, Felix D, Aboobaker A (2013) The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios. BMC Genomics 14.

Kennell JA, Gerin I, MacDougald OA, Cadigan KM (2008) The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc Natl Acad Sci USA 105: 15417-15422.

Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ, Brown DDR, Ross EJ, Voisin V, Bader GD, Blencowe BJ, Pearson BJ (2012) A Comparative Transcriptomic Analysis Reveals Conserved Features of Stem Cell Pluripotency in Planarians and Mammals. Stem Cells 30: 1734-1745.

Li TG, Kelly WG (2011) A Role for Set1/MLL-Related Components in Epigenetic Regulation of the Caenorhabditis elegans Germ Line. Plos Genet 7.

Li YQ, Zeng A, Han XS, Wang C, Li G, Zhang ZC, Wang JY, Qin YW, Jing Q (2011) Argonaute-2 regulates the proliferation of adult stem cells in planarian. Cell Res 21: 1750-1754.

Lobo D, Beane WS, Levin M (2012) Modeling Planarian Regeneration: A Primer for Reverse-Engineering the Worm. Plos Comput Biol 8.

Lu YC, Smielewska M, Palakodeti D, Lovci MT, Aigner S, Yeo GW, Graveley BR (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. RNA 15: 1483-1491.

Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15: 423-437.

Newmark PA, Alvarado AS (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220: 142-153.

Newmark PA, Alvarado AS (2002) Not your father's planarian: A classic model enters the era of functional genomics. Nat Rev Genet 3: 210-219.

Newmark PA, Reddien PW, Cebria F, Sanchez Alvarado A (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci USA 100 Suppl 1: 11861-11865.

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.

Palakodeti D, Smielewska M, Graveley BR (2006) MicroRNAs from the Planarian Schmidtea mediterranea: A model system for stem cell biology. RNA 12: 1640-1649.

Palakodeti D, Smielewska M, Lu YC, Yeo GW, Graveley BR (2008) The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14: 1174-1186.

Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, Sanchez Alvarado A (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238: 443-450.

Pellettieri J, Alvarado AS (2007) Cell turnover and adult tissue homeostasis: From humans to planarians. Annu Rev Genet 41: 83-105.

Petersen CP, Reddien PW (2009) Wnt Signaling and the Polarity of the Primary Body Axis. Cell 139: 1056-1068.

Qin YF, Zhao JM, Bao ZX, Zhu ZY, Mai J, Huang YB, Li JB, Chen G, Lu P, Chen SJ, Su LL, Fang HM, Lu JK, Zhang YZ, Zhang ST (2012) Identification of small non-coding RNAs in the planarian Dugesia japonica via deep sequencing. Genomics 99: 315-321.

Reddien PW, Alvarado AS (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Bio 20: 725-757.

Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sanchez Alvarado A (2005a) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8: 635-649.

Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Alvarado AS (2005b) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.

Resch AM, Palakodeti D (2012) Small RNA pathways in Schmidtea mediterranea. Int J Dev Biol 56: 67-74.

Rink JC (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223: 67-84.

Robb SMC, Alvarado AS (2002) Identification of immunological reagents for use in the study of freshwater planarians by means of whole-mount immunofluorescence and confocal microscopy. Genesis 32: 293-298.

Roberts-Galbraith RH, Newmark PA (2015) On the organ trail: insights into organ regeneration in the planarian. Curr Opin Genet Dev 32: 37-46.

Ross E, Blair D, Guerrero-Hernandez C, Sanchez Alvarado A (2016) Comparative and Transcriptome Analyses Uncover Key Aspects of Coding- and Long Non-Coding RNAs in Flatworm Mitochondrial Genomes. G3.

Ross KG, Omuro KC, Taylor MR, Munday RK, Hubert A, King RS, Zayas RM (2015) Novel monoclonal antibodies to study tissue regeneration in planarians. BMC Dev Biol 15.

Rossi L, Salvetti A, Batistoni R, Deri P, Gremigni V (2008) Planarians, a tale of stem cells. Cell Mol Life Sci 65: 16-23.

Rouhana L, Weiss JA, Forsthoefel DJ, Lee H, King RS, Inoue T, Shibata N, Agata K, Newmark PA (2013) RNA interference by feeding in vitro-synthesized double-stranded RNA to planarians: methodology and dynamics. Dev Dyn 242: 718-730.

Rouhana L, Weiss JA, King RS, Newmark PA (2014) PIWI homologs mediate Histone H4 mRNA localization to planarian chromatoid bodies. Development 141: 2592-2601.

Roush S, Slack FJ (2008) The let-7 family of microRNAs. Trends Cell Biol 18: 505-516.

Sanchez-Alvarado A (2006) Planarian regeneration: Its end is its beginning. Cell 124: 241-245.

Sasidharan V, Lu YC, Bansal D, Dasari P, Poduval D, Seshasayee A, Resch AM, Graveley BR, Palakodeti D (2013) Identification of neoblast- and regeneration-specific miRNAs in the planarian Schmidtea mediterranea. RNA 19: 1394-1404.

Scimone ML, Kravarik KM, Lapan SW, Reddien PW (2014) Neoblast Specialization in Regeneration of the Planarian Schmidtea mediterranea. Stem Cell Rep 3: 339-352.

Thomson T, Lin HF (2009) The Biogenesis and Function of PIWI Proteins and piRNAs: Progress and Prospect. Annu Rev Cell Dev Bio 25: 355-376.

Tian QN, Bao ZX, Lu P, Qin YF, Chen SJ, Liang F, Mai J, Zhao JM, Zhu ZY, Zhang YZ, Zhang ST (2012) Differential expression of microRNA patterns in planarian normal and regenerative tissues. Mol Biol Rep 39: 2653-2658.

Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.

van Wolfswinkel JC, Wagner DE, Reddien PW (2014) Single-Cell Analysis Reveals Functionally Distinct Classes within the Planarian Stem Cell Compartment. Cell Stem Cell 15: 326-339.

Vogg MC, Owlarn N, Rico YAP, Xie J, Suzuki Y, Gentile L, Wu W, Bartscherer K (2014) Stem cell-dependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Dev Biol 390: 136-148.

Weick EM, Miska EA (2014) piRNAs: from biogenesis to function. Development 141: 3458-3471.

Wulczyn FG, Smirnova L, Rybak A, Brandt C, Kwidzinski E, Ninnemann O, Strehle M, Sefler A, Schumacher S, Nitsch R (2007) Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J 21: 415-426.

Zhu SJ, Hallows SE, Currie KW, Xu C, Pearson BJ (2015) A mex3 homolog is required for differentiation during planarian stem cell lineage development. eLife 4.

Published
2017-03-04