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Pax6 organizes the anterior eye segment by guiding two distinct neural crest waves


Autoři: Masanari Takamiya aff001;  Johannes Stegmaier aff002;  Andrei Yu Kobitski aff001;  Benjamin Schott aff002;  Benjamin D. Weger aff001;  Dimitra Margariti aff001;  Angel R. Cereceda Delgado aff001;  Victor Gourain aff001;  Tim Scherr aff002;  Lixin Yang aff001;  Sebastian Sorge aff001;  Jens C. Otte aff001;  Volker Hartmann aff004;  Jos van Wezel aff005;  Rainer Stotzka aff004;  Thomas Reinhard aff006;  Günther Schlunck aff006;  Thomas Dickmeis aff001;  Sepand Rastegar aff001;  Ralf Mikut aff002;  Gerd Ulrich Nienhaus aff001;  Uwe Strähle aff001
Působiště autorů: Institute of Biological and Chemical Systems - Biological Information Processing, Karlsruhe Institute of Technology, Karlsruhe, Germany aff001;  Institute for Biological and Chemical Systems - Biological Information Processing, Karlsruhe Institute of Technology, Karlsruhe, Germany aff001;  Institute for Automation and Applied Informatics, Karlsruhe Institute of Technology, Karlsruhe, Germany aff002;  Institute of Applied Physics, Karlsruhe Institute of Technology, Karlsruhe, Germany aff003;  Institute for Data Processing and Electronics, Karlsruhe Institute of Technology, Karlsruhe, Germany aff004;  Steinbuch Centre for Computing, Karlsruhe Institute of Technology, Karlsruhe, Germany aff005;  Eye Center, Freiburg University Medical Center, Freiburg, Germany aff006;  Institute of Nanotechnology, Karlsruhe Institute of Technology, Karlsruhe, Germany aff007;  Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America aff008
Vyšlo v časopise: Pax6 organizes the anterior eye segment by guiding two distinct neural crest waves. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008774
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008774

Souhrn

Cranial neural crest (NC) contributes to the developing vertebrate eye. By multidimensional, quantitative imaging, we traced the origin of the ocular NC cells to two distinct NC populations that differ in the maintenance of sox10 expression, Wnt signalling, origin, route, mode and destination of migration. The first NC population migrates to the proximal and the second NC cell group populates the distal (anterior) part of the eye. By analysing zebrafish pax6a/b compound mutants presenting anterior segment dysgenesis, we demonstrate that Pax6a/b guide the two NC populations to distinct proximodistal locations. We further provide evidence that the lens whose formation is pax6a/b-dependent and lens-derived TGFβ signals contribute to the building of the anterior segment. Taken together, our results reveal multiple roles of Pax6a/b in the control of NC cells during development of the anterior segment.

Klíčová slova:

Cell migration – Cornea – Embryos – Endothelium – Eye lens – Eyes – Zebrafish – Diencephalon


Zdroje

1. Le Douarin NM, Kalcheim C. The neural crest [Internet]. Developmental and Cell Biology. Cambridge University Press; 1999. https://doi.org/10.1017/CBO9780511897948

2. Reis LM, Semina EV. Genetics of anterior segment dysgenesis disorders. Current Opinion in Ophthalmology. 2011. pp. 314–324. doi: 10.1097/ICU.0b013e328349412b 21730847

3. Gage PJ, Rhoades W, Prucka SK, Hjalt T. Fate maps of neural crest and mesoderm in the mammalian eye. Investig Ophthalmol Vis Sci. 2005; doi: 10.1167/iovs.05-0691 16249499

4. Seo S, Chen L, Liu W, Zhao D, Schultz KM, Sasman A, et al. Foxc1 and foxc2 in the neural crest are required for ocular anterior segment development. Investig Ophthalmol Vis Sci. 2017; doi: 10.1167/iovs.16-21217 28253399

5. Ittner LM, Wurdak H, Schwerdtfeger K, Kunz T, Ille F, Leveen P, et al. Compound developmental eye disorders following inactivation of TGFβ signaling in neural-crest stem cells. J Biol. 2005; doi: 10.1186/jbiol29 16403239

6. Saika S, Saika S, Liu CY, Azhar M, Sanford LP, Doetschman T, et al. Tgfβ2 in corneal morphogenesis during mouse embryonic development. Dev Biol. 2001; doi: 10.1006/dbio.2001.0480 11784073

7. Matsuo T, Osumi-Yamashita N, Noji S, Ohuchi H, Koyama E, Myokai F, et al. A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells. Nat Genet. 1993; doi: 10.1038/ng0493-299 7981749

8. Kroeber M, Davis N, Holzmann S, Kritzenberger M, Shelah-Goraly M, Ofri R, et al. Reduced expression of Pax6 in lens and cornea of mutant mice leads to failure of chamber angle development and juvenile glaucoma. Hum Mol Genet. 2010; doi: 10.1093/hmg/ddq237 20538882

9. Favor J, Gloeckner CJ, Neuhaüser-Klaus A, Pretsch W, Sandulache R, Saule S, et al. Relationship of Pax6 activity levels to the extent of eye development in the mouse, Mus musculus. Genetics. 2008; doi: 10.1534/genetics.108.088591 18562673

10. Bäumer N, Marquardt T, Stoykova A, Ashery-Padan R, Chowdhury K, Gruss P. Pax6 is required for establishing naso-temporal and dorsal characteristics of the optic vesicle. Development. 2002; doi: 10.2337/dc07-0281 17536073

11. Davis-Silberman N, Kalich T, Oron-Karni V, Marquardt T, Kroeber M, Tamm ER, et al. Genetic dissection of Pax6 dosage requirements in the developing mouse eye. Hum Mol Genet. 2005; doi: 10.1093/hmg/ddi231 15987699

12. Schwarz M, Cecconi F, Bernier G, Andrejewski N, Kammandel B, Wagner M, et al. Spatial specification of mammalian eye territories by reciprocal transcriptional repression of pax2 and pax6. Development. 2000; 11003833

13. Macdonald R, Barth KA, Xu Q, Holder N, Mikkola I, Wilson SW. Midline signalling is required for Pax gene regulation and patterning of the eyes. Development. 1995; doi: 10.1016/0168-9525(95)90453-0 7588061

14. Soules KA, Link BA. Morphogenesis of the anterior segment in the zebrafish eye. BMC Dev Biol. 2005; doi: 10.1186/1471-213X-5-12 15985175

15. Zhao XC, Yee RW, Norcom E, Burgess H, Avanesov AS, Barrish JP, et al. The zebrafish cornea: Structure and development. Investig Ophthalmol Vis Sci. 2006; doi: 10.1167/iovs.05-1611 17003424

16. Takamiya M, Weger BD, Schindler S, Beil T, Yang L, Armant O, et al. Molecular description of eye defects in the zebrafish pax6b mutant, sunrise, reveals a pax6b-dependent genetic network in the developing anterior chamber. PLoS One. 2015; doi: 10.1371/journal.pone.0117645 25692557

17. Wiedenmann J, Ivanchenko S, Oswald F, Schmitt F, Röcker C, Salih A, et al. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci. 2004; doi: 10.1073/pnas.0403668101 15505211

18. Nienhaus GU, Nienhaus K, Hölzle A, Ivanchenko S, Renzi F, Oswald F, et al. Photoconvertible Fluorescent Protein EosFP: Biophysical Properties and Cell Biology Applications. Photochem Photobiol. 2006; doi: 10.1562/2005-05-19-RA-533 16613485

19. Greenhill ER, Rocco A, Vibert L, Nikaido M, Kelsh RN. An iterative genetic and dynamical modelling approach identifies novel features of the gene regulatory network underlying melanocyte development. PLoS Genet. 2011; doi: 10.1371/journal.pgen.1002265 21909283

20. Wiedenmann J, Nienhaus GU. Live-cell imaging with EosFP and other photoactivatable marker proteins of the GFP family. Expert Review of Proteomics. 2006. doi: 10.1586/14789450.3.3.361 16771707

21. Dorsky RI, Moon RT, Raible DW. Control of neural crest cell fate by the Wnt signalling pathway. Nature. 1998; doi: 10.1038/24620 9845073

22. Moro E, Ozhan-Kizil G, Mongera A, Beis D, Wierzbicki C, Young RM, et al. In vivo Wnt signaling tracing through a transgenic biosensor fish reveals novel activity domains. Dev Biol. 2012; doi: 10.1016/j.ydbio.2012.03.023 22546689

23. Kobitski AY, Otte JC, Takamiya M, Schäfer B, Mertes J, Stegmaier J, et al. An ensemble-averaged, cell density-based digital model of zebrafish embryo development derived from light-sheet microscopy data with single-cell resolution. Sci Rep. 2015;5. doi: 10.1038/srep08601 25712513

24. Chen B, Dodge ME, Tang W, Lu J, Ma Z, Fan CW, et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol. 2009; doi: 10.1038/nchembio.137 19125156

25. Schott B, Traub M, Schlagenhauf C, Takamiya M, Antritter T, Bartschat A, et al. EmbryoMiner: A new framework for interactive knowledge discovery in large-scale cell tracking data of developing embryos. PLoS Comput Biol. 2018;14. doi: 10.1371/journal.pcbi.1006128 29672531

26. Li M, Zhao C, Wang Y, Zhao Z, Meng A. Zebrafish sox9b is an early neural crest marker. Dev Genes Evol. 2002; doi: 10.1007/s00427-002-0235-2 12012235

27. Krauss S, Johansen T, Korzh V, Fjose A. Expression pattern of zebrafish pax genes suggests a role in early brain regionalization. Nature. 1991; doi: 10.1038/353267a0 1680220

28. Quillien A, Blanco-Sanchez B, Halluin C, Moore JC, Lawson ND, Blader P, et al. BMP signaling orchestrates photoreceptor specification in the zebrafish pineal gland in collaboration with Notch. Development. 2011; doi: 10.1242/dev.060988 21558377

29. Arkhipova V, Wendik B, Devos N, Ek O, Peers B, Meyer D. Characterization and regulation of the hb9/mnx1 beta-cell progenitor specific enhancer in zebrafish. Dev Biol. 2012; doi: 10.1016/j.ydbio.2012.03.001 22426004

30. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, et al. Zebrafish colourless encodes sox10 and speci es non-ectomesenchymal neural crest fates. Development. 2001; doi: 10.1093/hmg/4.12.2407 8634719

31. Dutton K, Dutton JR, Pauliny A, Kelsh RN. A morpholino phenocopy of the colourless mutant. Genesis. 2001; doi: 10.1002/gene.1062 11477705

32. Kleinjan DA, Bancewicz RM, Gautier P, Dahm R, Schonthaler HB, Damante G, et al. Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet. 2008; doi: 10.1371/journal.pgen.0040029 18282108

33. Schedl A, Ross A, Lee M, Engelkamp D, Rashbass P, Van Heyningen V, et al. Influence of PAX6 gene dosage on development: Overexpression causes severe eye abnormalities. Cell. 1996; doi: 10.1016/S0092-8674(00)80078-1

34. Bäumer N, Marquardt T, Stoykova A, Ashery-Padan R, Chowdhury K, Gruss P. Pax6 is required for establishing naso-temporal and dorsal characteristics of the optic vesicle. Development. 2002; doi: 10.2337/dc07-0281 12223410

35. Worzfeld T, Offermanns S. Semaphorins and plexins as therapeutic targets. Nature Reviews Drug Discovery. 2014. doi: 10.1038/nrd4337 25082288

36. Brors D, Bodmer D, Pak K, Aletsee C, Schäkfers M, Dazert S, et al. EphA4 provides repulsive signals to developing cochlear ganglion neurites mediated through ephrin-B2 and -B3. J Comp Neurol. 2003; doi: 10.1002/cne.10707 12761826

37. Murai KK, Nguyen LN, Irie F, Yu Y, Pasquale EB. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci. 2003; doi: 10.1038/nn994 12496762

38. Nakayama Y, Miyake A, Nakagawa Y, Mido T, Yoshikawa M, Konishi M, et al. Fgf19 is required for zebrafish lens and retina development. Dev Biol. 2008; doi: 10.1016/j.ydbio.2007.11.013 18089288

39. Yu HH, Moens CB. Semaphorin signaling guides cranial neural crest cell migration in zebrafish. Dev Biol. 2005; doi: 10.1016/j.ydbio.2005.01.029 15882579

40. Tanaka H, Maeda R, Shoji W, Wada H, Masai I, Shiraki T, et al. Novel mutations affecting axon guidance in zebrafish and a role for plexin signalling in the guidance of trigeminal and facial nerve axons. Development. 2007; doi: 10.1242/dev.004267 17699608

41. Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT, Wang RA, et al. Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science (80-). 2009; doi: 10.1126/science.1178577 19815777

42. Yamamoto Y, Jeffery WR. Central role for the lens in cave fish eye degeneration. Science (80-). 2000; doi: 10.1126/science.289.5479.631 10915628

43. Takamiya M, Xu F, Suhonen H, Gourain V, Yang L, Ho NY, et al. Melanosomes in pigmented epithelia maintain eye lens transparency during zebrafish embryonic development. Sci Rep. 2016;6: 25046. doi: 10.1038/srep25046 27141993

44. Saika S, Saika S, Liu CY, Azhar M, Sanford LP, Doetschman T, et al. Tgfβ2 in corneal morphogenesis during mouse embryonic development. Dev Biol. 2001; doi: 10.1006/dbio.2001.0480 11784073

45. Silla ZTV, Naidoo J, Kidson SH, Sommer P. Signals from the lens and Foxc1 regulate the expression of key genes during the onset of corneal endothelial development. Exp Cell Res. 2014; doi: 10.1016/j.yexcr.2014.01.016 24472616

46. Casari A, Schiavone M, Facchinello N, Vettori A, Meyer D, Tiso N, et al. A Smad3 transgenic reporter reveals TGF-beta control of zebrafish spinal cord development. Dev Biol. 2014; doi: 10.1016/j.ydbio.2014.09.025 25286120

47. DaCosta Byfield S. SB-505124 Is a Selective Inhibitor of Transforming Growth Factor- Type I Receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 2004; doi: 10.1124/mol.65.3.744 14978253

48. John N, Cinelli P, Wegner M, Sommer L. Transforming growth factor β-mediated sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells. Stem Cells. 2011; doi: 10.1002/stem.607 21308864

49. Schilling TF, Kimmel CB. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development. 1994; 8162849

50. Langenberg T, Kahana A, Wszalek JA, Halloran MC. The eye organizes neural crest cell migration. Dev Dyn. 2008; doi: 10.1002/dvdy.21577 18498099

51. Chibon P. Analyse expérimentale de la régionalisation et des capacités morphogénétiques de la crête neurale chez l’Amphibien Urodèle Pleurodeles waltlii Michah. Mémoires la Société Zool Fr. 1966;36: 1–107, 5 plates.

52. Osumi-Yamashita N, Ninomiya Y, Doi H, Eto K. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev Biol. 1994; doi: 10.1006/dbio.1994.1211 8045344

53. O’Rahilly R, Müller F. The development of the neural crest in the human. J Anat. 2007; doi: 10.1111/j.1469-7580.2007.00773.x 17848161

54. Lwigale PY, Bronner-Fraser M. Semaphorin3A/neuropilin-1 signaling acts as a molecular switch regulating neural crest migration during cornea development. Dev Biol. 2009; doi: 10.1016/j.ydbio.2009.10.008 19833121

55. Osumi-Yamashita N, Kuratani S, Ninomiya Y, Aoki K, Iseki S, Chareonvit S, et al. Cranial anomaly of homozygous rSey rat is associated with a defect in the migration pathway of midbrain crest cells. Dev Growth Differ. 1997; doi: 10.1046/j.1440-169X.1997.00007.x 9079035

56. Chen KH, Harris DL, Joyce NC. TGF-β2 in aqueous humor suppresses S-phase entry in cultured corneal endothelial cells. Investig Ophthalmol Vis Sci. 1999; doi: 10.1158/0008-5472.CAN-05-4673 16778164

57. Wolf L V., Yang Y, Wang J, Xie Q, Braunger, B Tamm ER, et al. Identification of Pax6-dependent gene regulatory networks in the mouse lens. PLoS One. 2009; doi: 10.1371/journal.pone.0004159 19132093

58. Shaham O, Gueta K, Mor E, Oren-Giladi P, Grinberg D, Xie Q, et al. Pax6 Regulates Gene Expression in the Vertebrate Lens through miR-204. PLoS Genet. 2013; doi: 10.1371/journal.pgen.1003357 23516376

59. Sun J, Rockowitz S, Xie Q, Ashery-Padan R, Zheng D, Cvekl A. Identification of in vivo DNA-binding mechanisms of Pax6 and reconstruction of Pax6-dependent gene regulatory networks during forebrain and lens development. Nucleic Acids Res. 2015; doi: 10.1093/nar/gkv589 26138486

60. Grocott T, Lozano-Velasco E, Mok GF, Münsterberg AE. The Pax6 master control gene initiates spontaneous retinal development via a self-organising Turing network. bioRxiv. 2019; doi: 10.1101/583807

61. Wang X, Shan X, Gregory-Evans CY. A mouse model of aniridia reveals the in vivo downstream targets of Pax6 driving iris and ciliary body development in the eye. Biochim Biophys Acta—Mol Basis Dis. 2017; doi: 10.1016/j.bbadis.2016.10.018 27771509

62. Hogan BLM, Horsburgh G, Cohen J, Hetherington CM, Fisher G, Lyon MF. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J Embryol Exp Morphol. 1986; 3794606

63. Hingorani M, Hanson I, Van Heyningen V. Aniridia. European Journal of Human Genetics. 2012. doi: 10.1038/ejhg.2012.100 22692063

64. Yeyati PL, Bancewicz RM, Maule J, Van Heyningen V. Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet. 2007; doi: 10.1371/journal.pgen.0030043 17397257

65. Clegg JM, Li Z, Molinek M, Caballero IM, Manuel MN, Price DJ. Pax6 is required intrinsically by thalamic progenitors for the normal molecular patterning of thalamic neurons but not the growth and guidance of their axons. Neural Dev. 2015; doi: 10.1186/s13064-015-0053-7 26520399

66. Aleström P, D’Angelo L, Midtlyng PJ, Schorderet DF, Schulte-Merker S, Sohm F, et al. Zebrafish: Housing and husbandry recommendations. Lab Anim. 2019; doi: 10.1177/0023677219869037 31510859

67. Westerfield M. The Zebrafish Book: A guide for the laboratory use of zebrafish (Danio rerio). Eugene. 2007. doi: 10.1890/13-0905.1 24834735

68. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, et al. The Tol2kit: A multisite gateway-based construction Kit for Tol2 transposon transgenesis constructs. Dev Dyn. 2007; doi: 10.1002/dvdy.21343 17937395

69. Gagnon JA, Valen E, Thyme SB, Huang P, Ahkmetova L, Pauli A, et al. Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS One. 2014; doi: 10.1371/journal.pone.0098186 24873830

70. Meeker ND, Hutchinson SA, Ho L, Trede NS. Method for isolation of PCR-ready genomic DNA from zebrafish tissues. Biotechniques. 2007; doi: 10.2144/000112619 18072590

71. Langheinrich U, Hennen E, Stott G, Vacun G. Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol. 2002; doi: 10.1016/S0960-9822(02)01319-2

72. Strähle U, Blader P, Adam J, Ingham PW. A simple and efficient procedure for non-isotopic in situ hybridization to sectioned material. Trends Genet. 1994; doi: 10.1016/0168-9525(94)90221-6

73. Armant O, März M, Schmidt R, Ferg M, Diotel N, Ertzer R, et al. Genome-wide, whole mount in situ analysis of transcriptional regulators in zebrafish embryos. Dev Biol. 2013; doi: 10.1016/j.ydbio.2013.05.006 23684812

74. Blader P, Strähle U, Ingham PW. Three Wnt genes expressed in a wide variety of tissues during development of the zebrafish, Danio revio: Developmental and evolutionary perspectives. Dev Genes Evol. 1996; doi: 10.1007/s004270050025 24173392

75. Mane SR, Hsiao IL, Takamiya M, Le D, Straehle U, Barner-Kowollik C, et al. Intrinsically Fluorescent, Stealth Polypyrazoline Nanoparticles with Large Stokes Shift for In Vivo Imaging. Small. 2018;14. doi: 10.1002/smll.201801571 30079605

76. R Core Team. R Core Team (2014). R: A language and environment for statistical computing. R Found Stat Comput Vienna, Austria URL http://www.R-project.org/. 2014;

77. Nepal C, Hadzhiev Y, Previti C, Haberle V, Li N, Takahashi H, et al. Dynamic regulation of the transcription initiation landscape at single nucleotide resolution during vertebrate embryogenesis. Genome Res. 2013; doi: 10.1101/gr.153692.112 24002785


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