A small set of conserved genes, including sp5 and Hox, are activated by Wnt signaling in the posterior of planarians and acoels


Autoři: Aneesha G. Tewari aff001;  Jared H. Owen aff001;  Christian P. Petersen aff001;  Daniel E. Wagner aff001;  Peter W. Reddien aff001
Působiště autorů: Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, United States of America aff001;  Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America aff002;  Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America aff003
Vyšlo v časopise: A small set of conserved genes, including sp5 and Hox, are activated by Wnt signaling in the posterior of planarians and acoels. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008401
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008401

Souhrn

Wnt signaling regulates primary body axis formation across the Metazoa, with high Wnt signaling specifying posterior identity. Whether a common Wnt-driven transcriptional program accomplishes this broad role is poorly understood. We identified genes acutely affected after Wnt signaling inhibition in the posterior of two regenerative species, the planarian Schmidtea mediterranea and the acoel Hofstenia miamia, which are separated by >550 million years of evolution. Wnt signaling was found to maintain positional information in muscle and regional gene expression in multiple differentiated cell types. sp5, Hox genes, and Wnt pathway components are down-regulated rapidly after β-catenin RNAi in both species. Brachyury, a vertebrate Wnt target, also displays Wnt-dependent expression in Hofstenia. sp5 inhibits trunk gene expression in the tail of planarians and acoels, promoting separate tail-trunk body domains. A planarian posterior Hox gene, Post-2d, promotes normal tail regeneration. We propose that common regulation of a small gene set–Hox, sp5, and Brachyury–might underlie the widespread utilization of Wnt signaling in primary axis patterning across the Bilateria.

Klíčová slova:

Epidermis – Gene expression – Gene regulation – RNA interference – RNA sequencing – Wnt signaling cascade – Planarians – Tails


Zdroje

1. Petersen CP, Reddien PW. Wnt signaling and the polarity of the primary body axis. Cell. 2009;139(6):1056–68. doi: 10.1016/j.cell.2009.11.035 20005801

2. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, et al. Multiple Wnts are involved in Hydra organizer formation and regeneration. Developmental Biology. 2009;330(1):186–99. doi: 10.1016/j.ydbio.2009.02.004 19217898

3. Gurley KA, Rink JC, Sánchez Alvarado A. β-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science. 2008;319(5861):323–7. doi: 10.1126/science.1150029 18063757

4. Iglesias M, Gomez-Skarmeta JL, Salό E, Adell T. Silencing of Smed-βcatenin1 generates radial-like hypercephalized planarians. Development. 2008;135(7):1215–21. doi: 10.1242/dev.020289 18287199

5. Petersen CP, Reddien PW. Smed-βcatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science. 2008;319(5861):327–30. doi: 10.1126/science.1149943 18063755

6. Kiecker C, Niehrs C. A morphogen gradient of Wnt/β-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development. 2001;128(21):4189–201. 11684656

7. Niehrs C. On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development. 2010;137(6):845–57. doi: 10.1242/dev.039651 20179091

8. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development. 1995;121(11):3529–37. 8582267

9. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. Requirement for β-catenin in anterior-posterior axis formation in mice. J Cell Biol. 2000;148(3):567–78. doi: 10.1083/jcb.148.3.567 10662781

10. Ruiz-Trillo I, Riutort M, Littlewood DT, Herniou EA, Baguna J. Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science. 1999;283(5409):1919–23. doi: 10.1126/science.283.5409.1919 10082465

11. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci. 2009;276(1677):4261–70. doi: 10.1098/rspb.2009.0896 19759036

12. Srivastava M, Mazza-Curll KL, van Wolfswinkel JC, Reddien PW. Whole-body acoel regeneration is controlled by Wnt and Bmp-Admp signaling. Current biology: CB. 2014;24(10):1107–13. doi: 10.1016/j.cub.2014.03.042 24768051

13. Arroyo AS, López-Escardó D, de Vargas C, Ruiz-Trillo I. Hidden diversity of Acoelomorpha revealed through metabarcoding. Biol Lett. 2016;12(9).

14. Cannon JT, Vellutini BC, Smith J 3rd, Ronquist F, Jondelius U, Hejnol A. Xenacoelomorpha is the sister group to Nephrozoa. Nature. 2016;530(7588):89–93. doi: 10.1038/nature16520 26842059

15. Rouse GW, Wilson NG, Carvajal JI, Vrijenhoek RC. New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature. 2016;530(7588):94–7. doi: 10.1038/nature16545 26842060

16. Peterson KJ, Lyons JB, Nowak KS, Takacs CM, Wargo MJ, McPeek MA. Estimating metazoan divergence times with a molecular clock. Proc Natl Acad Sci U S A. 2004;101(17):6536–41. doi: 10.1073/pnas.0401670101 15084738

17. Newmark P, Sánchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol. 2000;220(2):142–53. doi: 10.1006/dbio.2000.9645 10753506

18. Gehrke AR, Srivastava M. Neoblasts and the evolution of whole-body regeneration. Curr Opin Genet Dev. 2016;40:131–7. doi: 10.1016/j.gde.2016.07.009 27498025

19. Reddien PW. The Cellular and Molecular Basis for Planarian Regeneration. Cell. 2018;175(2):327–45. doi: 10.1016/j.cell.2018.09.021 30290140

20. Iglesias M, Almuedo-Castillo M, Aboobaker AA, Salό E. Early planarian brain regeneration is independent of blastema polarity mediated by the Wnt/β-catenin pathway. Developmental Biology. 2011;358(1):68–78. doi: 10.1016/j.ydbio.2011.07.013 21806978

21. Adell T, Salό E, Boutros M, Bartscherer K. Smed-Evi/Wntless is required for β-catenin-dependent and -independent processes during planarian regeneration. Development. 2009;136(6):905–10. doi: 10.1242/dev.033761 19211673

22. Petersen CP, Reddien PW. A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci U S A. 2009;106(40):17061–6. doi: 10.1073/pnas.0906823106 19805089

23. Gurley KA, Elliott SA, Simakov O, Schmidt HA, Holstein TW, Sánchez Alvarado A. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol. 2010;347(1):24–39. doi: 10.1016/j.ydbio.2010.08.007 20707997

24. Owen JH, Wagner DE, Chen CC, Petersen CP, Reddien PW. teashirt is required for head-versus-tail regeneration polarity in planarians. Development. 2015;142(6):1062–72. doi: 10.1242/dev.119685 25725068

25. Reuter H, Marz M, Vogg MC, Eccles D, Grifol-Boldu L, Wehner D, et al. β-catenin-dependent control of positional information along the AP body axis in planarians involves a Teashirt family member. Cell Rep. 2015;10(2):253–65. doi: 10.1016/j.celrep.2014.12.018 25558068

26. Sureda-Gόmez M, Pascual-Carreras E, Adell T. Posterior Wnts Have Distinct Roles in Specification and Patterning of the Planarian Posterior Region. Int J Mol Sci. 2015;16(11):26543–54. doi: 10.3390/ijms161125970 26556349

27. Lander R, Petersen CP. Wnt, Ptk7, and FGFRL expression gradients control trunk positional identity in planarian regeneration. eLife. 2016;5: e12850. doi: 10.7554/eLife.12850 27074666

28. Scimone ML, Cote LE, Rogers T, Reddien PW. Two FGFRL-Wnt circuits organize the planarian anteroposterior axis. eLife. 2016;5: e12845. doi: 10.7554/eLife.12845 27063937

29. Sureda-Gómez M, Martín-Durán JM, Adell T. Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior posterior regeneration and organogenesis. Development. 2016;143(22):4149–60. doi: 10.1242/dev.135152 27737903

30. Stückemann T, Cleland JP, Werner S, Thi-Kim Vu H, Bayersdorf R, Liu SY, et al. Antagonistic Self-Organizing Patterning Systems Control Maintenance and Regeneration of the Anteroposterior Axis in Planarians. Dev Cell. 2017;40(3):248–63 e4. doi: 10.1016/j.devcel.2016.12.024 28171748

31. Weidinger G, Thorpe CJ, Wuennenberg-Stapleton K, Ngai J, Moon RT. The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/β-catenin signaling in mesoderm and neuroectoderm patterning. Curr Biol. 2005;15(6):489–500. doi: 10.1016/j.cub.2005.01.041 15797017

32. Fujimura N, Vacik T, Machon O, Vlcek C, Scalabrin S, Speth M, et al. Wnt-mediated down-regulation of Sp1 target genes by a transcriptional repressor Sp5. J Biol Chem. 2007;282(2):1225–37. doi: 10.1074/jbc.M605851200 17090534

33. Vogg MC, Beccari L, Iglesias Olle L, Rampon C, Vriz S, Perruchoud C, et al. An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra. Nat Commun. 2019;10(1):312. doi: 10.1038/s41467-018-08242-2 30659200

34. Witchley JN, Mayer M, Wagner DE, Owen JH, Reddien PW. Muscle cells provide instructions for planarian regeneration. Cell Reports. 2013;4(4):633–41. doi: 10.1016/j.celrep.2013.07.022 23954785

35. Fincher CT, Wurtzel O, de Hoog T, Kravarik KM, Reddien PW. Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science. 2018;360(6391).

36. Raz AA, Srivastava M, Salvamoser R, Reddien PW. Acoel regeneration mechanisms indicate an ancient role for muscle in regenerative patterning. Nat Commun. 2017;8(1):1260. doi: 10.1038/s41467-017-01148-5 29084955

37. Felix DA, Aboobaker AA. The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS genetics. 2010;6(4):e1000915. doi: 10.1371/journal.pgen.1000915 20422023

38. Vásquez-Doorman C, Petersen CP. zic-1 Expression in planarian neoblasts after injury controls anterior pole regeneration. PLoS genetics. 2014;10(7):e1004452. doi: 10.1371/journal.pgen.1004452 24992682

39. Vogg MC, Owlarn S, Perez Rico YA, Xie J, Suzuki Y, Gentile L, et al. Stem cell-dependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Developmental Biology. 2014;390(2):136–48. doi: 10.1016/j.ydbio.2014.03.016 24704339

40. Currie KW, Brown DD, Zhu S, Xu C, Voisin V, Bader GD, et al. HOX gene complement and expression in the planarian Schmidtea mediterranea. Evodevo. 2016;7:7. doi: 10.1186/s13227-016-0044-8 27034770

41. Cook CE, Jimenez E, Akam M, Salo E. The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol Dev. 2004;6(3):154–63. doi: 10.1111/j.1525-142X.2004.04020.x 15099302

42. Hejnol A, Martindale MQ. Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura. BMC Biol. 2009;7:65. doi: 10.1186/1741-7007-7-65 19796382

43. Derbyshire ER, Marletta MA. Structure and regulation of soluble guanylate cyclase. Annu Rev Biochem. 2012;81:533–59. doi: 10.1146/annurev-biochem-050410-100030 22404633

44. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 1999;13(24):3185–90. doi: 10.1101/gad.13.24.3185 10617567

45. Vonica A, Gumbiner BM. Zygotic Wnt activity is required for Brachyury expression in the early Xenopus laevis embryo. Dev Biol. 2002;250(1):112–27. doi: 10.1006/dbio.2002.0786 12297100

46. Martín-Dúran JM, Romero R. Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol. 2011;352(1):164–76. doi: 10.1016/j.ydbio.2011.01.032 21295562

47. Scimone ML, Wurtzel O, Malecek K, Fincher CT, Oderberg IM, Kravarik KM, et al. foxF-1 Controls Specification of Non-body Wall Muscle and Phagocytic Cells in Planarians. Curr Biol. 2018;28(23):3787–801 e6. doi: 10.1016/j.cub.2018.10.030 30471994

48. Kennedy MW, Chalamalasetty RB, Thomas S, Garriock RJ, Jailwala P, Yamaguchi TP. Sp5 and Sp8 recruit β-catenin and Tcf1-Lef1 to select enhancers to activate Wnt target gene transcription. Proc Natl Acad Sci U S A. 2016;113(13):3545–50. doi: 10.1073/pnas.1519994113 26969725

49. Huggins IJ, Bos T, Gaylord O, Jessen C, Lonquich B, Puranen A, et al. The WNT target SP5 negatively regulates WNT transcriptional programs in human pluripotent stem cells. Nat Commun. 2017;8(1):1034. doi: 10.1038/s41467-017-01203-1 29044119

50. Rink JC, Gurley KA, Elliott SA, Sánchez Alvarado A. Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science. 2009;326(5958):1406–10. doi: 10.1126/science.1178712 19933103

51. Thorpe CJ, Weidinger G, Moon RT. Wnt/β-catenin regulation of the Sp1-related transcription factor sp5l promotes tail development in zebrafish. Development. 2005;132(8):1763–72. doi: 10.1242/dev.01733 15772132

52. Dunty WC Jr., Kennedy MW, Chalamalasetty RB, Campbell K, Yamaguchi TP. Transcriptional profiling of Wnt3a mutants identifies Sp transcription factors as essential effectors of the Wnt/β-catenin pathway in neuromesodermal stem cells. PLoS One. 2014;9(1):e87018. doi: 10.1371/journal.pone.0087018 24475213

53. Dailey SC, Kozmikova I, Somorjai IML. Amphioxus Sp5 is a member of a conserved Specificity Protein complement and is modulated by Wnt/beta-catenin signalling. Int J Dev Biol. 2017;61(10-11-12):723–32. doi: 10.1387/ijdb.170205is 29319119

54. Rinn JL, Bondre C, Gladstone HB, Brown PO, Chang HY. Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS genetics. 2006;2(7):e119. doi: 10.1371/journal.pgen.0020119 16895450

55. Rinn JL, Wang JK, Allen N, Brugmann SA, Mikels AJ, Liu H, et al. A dermal HOX transcriptional program regulates site-specific epidermal fate. Genes & development. 2008;22(3):303–7.

56. DuBuc TQ, Stephenson TB, Rock AQ, Martindale MQ. Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation. Nat Commun. 2018;9(1):2007. doi: 10.1038/s41467-018-04184-x 29789526

57. Reddy PC, Unni MK, Gungi A, Agarwal P, Galande S. Evolution of Hox-like genes in Cnidaria: Study of Hydra Hox repertoire reveals tailor-made Hox-code for Cnidarians. Mech Dev. 2015;138 Pt 2:87–96.

58. Gluecksohn-Schoenheimer S. The Development of Normal and Homozygous Brachy (T/T) Mouse Embryos in the Extraembryonic Coelom of the Chick. Proc Natl Acad Sci U S A. 1944;30(6):134–40. doi: 10.1073/pnas.30.6.134 16588636

59. Halpern ME, Ho RK, Walker C, Kimmel CB. Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell. 1993;75(1):99–111. 8402905

60. Schulte-Merker S, van Eeden FJ, Halpern ME, Kimmel CB, Nusslein-Volhard C. no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development. 1994;120(4):1009–15. 7600949

61. Martin BL, Kimelman D. Regulation of canonical Wnt signaling by Brachyury is essential for posterior mesoderm formation. Dev Cell. 2008;15(1):121–33. doi: 10.1016/j.devcel.2008.04.013 18606146

62. Technau U, Bode HR. HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development. 1999;126(5):999–1010. 9927600

63. Broun M, Gee L, Reinhardt B, Bode HR. Formation of the head organizer in hydra involves the canonical Wnt pathway. Development. 2005;132(12):2907–16. doi: 10.1242/dev.01848 15930119

64. Oberhofer G, Grossmann D, Siemanowski JL, Beissbarth T, Bucher G. Wnt/β-catenin signaling integrates patterning and metabolism of the insect growth zone. Development. 2014;141(24):4740–50. doi: 10.1242/dev.112797 25395458

65. Satoh N, Tagawa K, Takahashi H. How was the notochord born? Evol Dev. 2012;14(1):56–75. doi: 10.1111/j.1525-142X.2011.00522.x 23016975

66. Yasuoka Y, Shinzato C, Satoh N. The Mesoderm-Forming Gene brachyury Regulates Ectoderm-Endoderm Demarcation in the Coral Acropora digitifera. Curr Biol. 2016;26(21):2885–92. doi: 10.1016/j.cub.2016.08.011 27693135

67. Hejnol A, Martindale MQ. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature. 2008;456(7220):382–6. doi: 10.1038/nature07309 18806777

68. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, et al. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos Cell. 1994;79(5):791–803. doi: 10.1016/0092-8674(94)90069-8 7528101

69. De Robertis EM, Larrain J, Oelgeschlager M, Wessely O. The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat Rev Genet. 2000;1(3):171–81. doi: 10.1038/35042039 11252746

70. Bellipanni G, Varga M, Maegawa S, Imai Y, Kelly C, Myers AP, et al. Essential and opposing roles of zebrafish β-catenins in the formation of dorsal axial structures and neurectoderm. Development. 2006;133(7):1299–309. doi: 10.1242/dev.02295 16510506

71. Martin BL, Kimelman D. Wnt signaling and the evolution of embryonic posterior development. Curr Biol. 2009;19(5):R215–9. doi: 10.1016/j.cub.2009.01.052 19278640

72. Sánchez Alvarado A, Newmark PA, Robb SM, Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development. 2002;129(24):5659–65. doi: 10.1242/dev.00167 12421706

73. Rouhana L, Weiss JA, Forsthoefel DJ, Lee H, King RS, Inoue T, et al. RNA interference by feeding in vitro-synthesized double-stranded RNA to planarians: methodology and dynamics. Developmental dynamics: an official publication of the American Association of Anatomists. 2013;242(6):718–30.

74. Benian GM, Kiff JE, Neckelmann N, Moerman DG, Waterston RH. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature. 1989;342(6245):45–50. doi: 10.1038/342045a0 2812002

75. King RS, Newmark PA. In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev Biol. 2013;13:8. doi: 10.1186/1471-213X-13-8 23497040

76. Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, Sánchez Alvarado A. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn. 2009;238(2):443–50. doi: 10.1002/dvdy.21849 19161223

77. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25. doi: 10.1186/gb-2009-10-3-r25 19261174

78. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106. doi: 10.1186/gb-2010-11-10-r106 20979621

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2019 Číslo 10

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Farmaceutická péče o pacienta s inhalační terapií
nový kurz
Autoři: Mgr. Ondřej Šimandl

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se