Neoblast-enriched zinc finger protein FIR1 triggers local proliferation during planarian regeneration
Received date: 06 Jul 2017
Accepted date: 09 Jan 2018
Published date: 31 Jan 2019
Copyright
Regeneration, relying mainly on resident adult stem cells, is widespread. However, the mechanism by which stem cells initiate proliferation during this process in vivo is unclear. Using planarian as a model, we screened 46 transcripts showing potential function in the regulation of local stem cell proliferation following 48 h regeneration. By analyzing the regeneration defects and the mitotic activity of animals under administration of RNA interference (RNAi), we identified factor for initiating regeneration 1 (Fir1) required for local proliferation. Our findings reveal that Fir1, enriched in neoblasts, promotes planarian regeneration in any tissue-missing context. Further, we demonstrate that DIS3 like 3′-5′ exoribonuclease 2 (Dis3l2) is required for Fir1 phenotype. Besides, RNAi knockdown of Fir1 causes a decrease of neoblast wound response genes following amputation. These findings suggest that Fir1 recognizes regenerative signals and promotes DIS3L2 proteins to trigger neoblast proliferation following amputation and provide a mechanism critical for stem cell response to injury.
Xiao-Shuai Han , Chen Wang , Fang-hao Guo , Shuang Huang , Yong-Wen Qin , Xian-Xian Zhao , Qing Jing . Neoblast-enriched zinc finger protein FIR1 triggers local proliferation during planarian regeneration[J]. Protein & Cell, 2019 , 10(1) : 43 -59 . DOI: 10.1007/s13238-018-0512-0
1 |
Almuedo-Castillo M, Crespo X, Seebeck F, Bartscherer K, Salò E, Adell T, Aboobaker AA (2014) JNK Controls the onset of mitosis in planarian stem cells and triggers apoptotic cell death required for regeneration and remodeling. PLoS Genetics 10(6):e1004400
|
2 |
Astuti D, Morris MR, Cooper WN, Staals RH, Wake NC, Fews GA, Gill H, Gentle D, Shuib S, Ricketts CJ
|
3 |
Bardeen C, Baetjer F (1904) The inhibitive action of the Roentgen rays onregeneration in planarians. J Exp Zool 1:191–195
|
4 |
Beachy PA, Karhadkar SS, Berman DM (2004) Tissue repair and stem cell renewal in carcinogenesis. Nature 432:324–331
|
5 |
Best JB, Hand S, Rosenvold R (1968) Mitosis in normal and regenerating planarians. J Exp Zool 168(2):157–167
|
6 |
Blassberg RA, Felix DA, Tejada-Romero B, Aboobaker AA (2013) PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration. Development 140(4):730–739
|
7 |
Bonuccelli L, Rossi L, Lena A, Scarcelli V, Rainaldi G, Evangelista M, Iacopetti P, Gremigni V, Salvetti A (2010) An RbAp48-like gene regulates adult stem cells in planarians. J Cell Sci 123(5):690–698
|
8 |
Böser A, Drexler HC, Reuter H, Schmitz H, Wu G, Schöler HR, Gentile L, Bartscherer K (2013) SILAC proteomics of planarians identifies Ncoa5 as a conserved component of pluripotent stem cells. Cell Rep 5(4):1142–1155
|
9 |
Carlson ME, Hsu M, Conboy IM (2008) Imbalance between pSmad3 andNotch induces CDK inhibitors in old muscle stem cells. Nature 454:528–532
|
10 |
Chang HM, Triboulet R, Thornton JE, Gregory RI (2013) A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497:244–248
|
11 |
Chen CCG, Wang IE, Reddien PW (2013) pbx is required for pole and eye regeneration in planarians. Development 140(4):719–729
|
12 |
Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H, Lendahl U, Frisen J (2000) Generalized potential of adult neural stem cells. Science 288:1660–1663
|
13 |
Cowles MW, Hubert A, Zayas RM (2012) A Lissencephaly-1 homologue is essential for mitotic progression in the planarian Schmidtea mediterranea. Dev Dyn 241:901–910
|
14 |
Dubois F (1949) Contribution á l ’ètude de la migration des cellules de règènèration chez les Planaires dulcicoles. Bull Biol Fr Belg 83:213–283
|
15 |
Fuchs E, Segre JA (2000) Stem cells: a new lease on life. Cell 100:143–155
|
16 |
Fuchs Y, Steller H (2015) Live to die another way: modes of programmed cell death and the signals emanating from dying cells. Nature Reviews Molecular Cell Biology 16(6):329–344
|
17 |
Gavino MA, Wenemoser D, Wang IE, Reddien PW (2013) Tissue absence initiates regeneration through follistatin-mediated inhibition of activin signaling. Elife 2:e00247
|
18 |
Gentile L, Cebria F, Bartscherer K (2011) The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis Models Mech 4:12–19
|
19 |
Gonzalez-Estevez C, Felix DA, Smith MD, Paps J, Morley SJ, James V, Sharp TV, Aboobaker AA (2012) SMG-1 and mTORC1 act antagonistically to regulate response to injury and growth in planarians. Plos Genetics 8:e1002619
|
20 |
Govindasamy N, Murthy S, Ghanekar Y (2014) Slow-cycling stem cells in hydra contribute to head regeneration. Biol Open 3:1236–1244
|
21 |
Guo T, Peters AH, Newmark PA (2006) A bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11(2):159–169
|
22 |
Hayashi T, Asami M, Higuchi S, Shibata N, Agata K (2006) Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48:371–380
|
23 |
Hollenbach JP, Resch AM, Palakodeti D, Graveley BR, Heinen CD, Martin G (2011) Loss of DNA mismatch repair imparts a selective advantage in planarian adult stem cells. PLoS ONE 6(7):e21808
|
24 |
Hopman AH, Ramaekers FC, Speel EJ (1998) Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for In situ hybridization using CARD amplification. J Histochem Cytochem 46:771–777
|
25 |
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 14:797
|
26 |
King RS, Newmark PA (2013) In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev Biol 13:8
|
27 |
Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ, Brown DD, Ross EJ, Voisin V, Bader GD, Blencowe BJ
|
28 |
Lapan SW, Reddien PW (2011) dlx and sp6-9 Control optic cup regeneration in a prototypic eye. PLoS Genet 7:e1002226
|
29 |
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
|
30 |
Morgan T (1898) Experimental studies of the regeneration of Planaria maculata. Arch Entw Mech Org 7:364–397
|
31 |
Morgan TH (1901) Regeneration. Macmillan, New York, p 316
|
32 |
Newmark PA, Sanchez AAlvarado (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142–153
|
33 |
Onal P, Grun D, Adamidi C, Rybak A, Solana J, Mastrobuoni G, Wang Y, Rahn HP, Chen W, Kempa S
|
34 |
Oviedo NJ, Levin M (2007) smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 134(17):3121–3131
|
35 |
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 (6):1174–1186
|
36 |
Passamaneck YJ, Martindale MQ (2012) Cell proliferation is necessary for the regeneration of oral structures in the anthozoan cnidarian Nematostella vectensis. BMC Dev Biol 12:34
|
37 |
Pearson BJ, Sanchez Alvarado A(2010) A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development 137:213–221
|
38 |
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
|
39 |
Pellettieri J, Sanchez Alvarado A (2007) Cell turnover and adult tissue homeostasis: from humans to planarians. Annu Rev Genet 41:83–105
|
40 |
Pellettieri J, Fitzgerald P, Watanabe S, Mancuso J, Green DR, Sanchez Alvarado A (2010) Cell death and tissue remodeling in planarian regeneration. Dev Biol 338:76–85
|
41 |
Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA (2011) Transient regenerative potential of the neonatal mouse heart. Science 331:1078–1080
|
42 |
Reddien PW, Sanchez AAlvarado (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20:725–757
|
43 |
Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Alvarado AS (2005a) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–1330
|
44 |
Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A (2005b) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–1330
|
45 |
Rossi L, Salvetti A, Marincola FM, Lena A, Deri P, Mannini L, Batistoni R, Wang E, Gremigni V (2007) Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol 8:R62
|
46 |
Rouhana L, Shibata N, Nishimura O, Agata K (2010) Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Dev Biol 341(2):429–443
|
47 |
Rouhana L, Vieira AP, Roberts-Galbraith RH, Newmark PA (2012) PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development 139:1083–1094
|
48 |
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
|
49 |
Salvetti A (2005) DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132 (8):1863–1874
|
50 |
Sanchez Alvarado A (2000) Regeneration in the metazoans: why does it happen? BioEssays 22:578–590
|
51 |
Sanchez Alvarado A (2003) The freshwater planarian Schmidtea mediterranea: embryogenesis, stem cells and regeneration. Curr Opin Genet Dev 13:438–444
|
52 |
Sanchez Alvarado A, Newmark PA, Robb SM, Juste R (2002) The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129:5659–5665
|
53 |
Scimone ML, Meisel J, Reddien PW (2010) The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 137:1231–1241
|
54 |
Scimone ML, Kravarik KM, Lapan SW, Reddien PW (2014) Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Rep 3:339–352
|
55 |
Seifert AW, Kiama SG, Seifert MG, Goheen JR, Palmer TM, Maden M (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489:561–565
|
56 |
Shaw RL, Kohlmaier A, Polesello C, Veelken C, Edgar BA, Tapon N (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137:4147–4158
|
57 |
Solana J, Kao D, Mihaylova Y, Jaber-Hijazi F, Malla S, Wilson R, Aboobaker A (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol 13:R19
|
58 |
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
|
59 |
Ustianenko D, Hrossova D, Potesil D, Chalupnikova K, Hrazdilova K, Pachernik J, Cetkovska K, Uldrijan S, Zdrahal Z, Vanacova S (2013) Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 19:1632–1638
|
60 |
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
|
61 |
Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332:811–816
|
62 |
Wagner DE, Ho JJ, Reddien PW (2012) Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10:299–311
|
63 |
Wang YZ, Yamagami T, Gan Q, Wang Y, Zhao T, Hamad S, Lott P, Schnittke N, Schwob JE, Zhou CJ (2011) Canonical Wnt signaling promotes the proliferation and neurogenesis of peripheral olfactory stem cells during postnatal development and adult regeneration. J Cell Sci 124:1553–1563
|
64 |
Wang C, Han XS, Li FF, Huang S, Qin YW, Zhao XX, Jing Q (2016) Forkhead containing transcription factor Albino controls tetrapyrrole-based body pigmentation in planarian. C ell Discov. https://doi.org/10.1038/celldisc.2016.29
|
65 |
Wenemoser D, Reddien PW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344:979–991
|
66 |
Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26:988–1002
|
67 |
Wurtzel O, Cote LE, Poirier A, Satija R, Regev A, Reddien PW (2015) A Generic and Cell-Type-Specific Wound Response Precedes Regeneration in Planarians. Dev Cell 35:632–645
|
68 |
Zayas RM, Hernández A, Habermann B, Wang Y, Stary JM, Newmark PA (2005) The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: Analysis of ESTs from the hermaphroditic strain. Proc Nat Acad Sci 102 (51):18491–18496
|
69 |
Zeng A, Li YQ, Wang C, Han XS, Li G, Wang JY, Li DS, Qin YW, Shi Y, Brewer G
|
70 |
Zhu SJ, Pearson BJ (2013) The Retinoblastoma pathway regulates stem cell proliferation in freshwater planarians. Dev Biol 373 (2):442–452
|
71 |
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
|
/
〈 | 〉 |