Forkhead containing transcription factor Albino controls tetrapyrrole-based body pigmentation in planarian

Cell Discovery

Volumn 2, Issue , 2016, Pages

  Wang, Chen ^a   Han, Xiao Shuai ^a   Li, Fang Fang ^a   Huang, Shuang ^b   Qin, Yong Wen ^b   Zhao, Xian Xian ^b   Jing, Qing ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

body color; FoxP; PBGD; pigmentation; planarian; tetrapyrrole

Indexed keywords

DOUBLE STRANDED RNA; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR ALBINO; MOLECULAR MARKER; TETRAPYRROLE DERIVATIVE; UNCLASSIFIED DRUG;

ALAD GENE; ALAS GENE; ALBINISM; ARTICLE; DEVELOPMENT; GENE EXPRESSION PROFILING; MICROBIAL GENE; NONHUMAN; PBGD GENE; PHENOTYPE; PIGMENT CELL; PIGMENTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; RNA INTERFERENCE; TURBELLARIA;

EID: 85034834464     PISSN: None     EISSN: 20565968     Source Type: Journal    
DOI: 10.1038/celldisc.2016.29     Document Type: Article

References (62)

1. Reddien PW, Sanchez Alvarado A. Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 2004; 20: 725-757.
2. Rink JC. Stem cell systems and regeneration in planaria. Dev Genes Evol 2013; 223: 67-84.
3. Salo E, Baguna J. Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J Embryol Exp Morphol 1984; 83: 63-80.
4. Guedelhoefer OCT, Sanchez Alvarado A. Amputation induces stem cell mobilization to sites of injury during planarian regeneration. Development 2012; 139: 3510-3520.
5. Wenemoser D, Lapan SW, Wilkinson AW et al. A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 2012; 26: 988-1002.
6. Zeng A, Li YQ, Wang C et al. Heterochromatin protein 1 promotes self-renewal and triggers regenerative proliferation in adult stem cells. J Cell Biol 2013; 201: 409-425.
7. Wagner DE, Wang IE, Reddien PW. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011; 332: 811-816.
8. Scimone ML, Kravarik KM, Lapan SW et al. Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Rep 2014; 3: 339-352.
9. Roberts-Galbraith RH, Newmark PA. On the organ trail: insights into organ regeneration in the planarian. Curr Opin Genet Dev 2015; 32C: 37-46.
10. Koinuma S, Umesono Y, Watanabe Ket al. The expression of planarian brain factor homologs, DjFoxG and DjFoxD. Gene Express Patterns 2003; 3: 21-27.
11. Scimone ML, Lapan SW, Reddien PW. A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet 2014; 10: e1003999.
12. Vogg MC, Owlarn S, Perez Rico YA et al. Stem celldependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Dev Biol 2014; 390: 136-148.
13. Blassberg RA, Felix DA, Tejada-Romero B et al. PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration. Development 2013; 140: 730-739.
14. Chen CC, Wang IE, Reddien PW. pbx is required for pole and eye regeneration in planarians. Development 2013; 140: 719-729.
15. Cowles MW, Brown DD, Nisperos SV et al. Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 2013; 140: 4691-4702.
16. Currie KW, Pearson BJ. Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 2013; 140: 3577-3588.
17. Marz M, Seebeck F, Bartscherer K. A Pitx transcription factor controls the establishment and maintenance of the serotonergic lineage in planarians. Development 2013; 140: 4499-4509.
18. Mannini L, Rossi L, Deri P et al. Djeyes absent (Djeya) controls prototypic planarian eye regeneration by cooperating with the transcription factor Djsix-1. Dev Biol 2004; 269: 346-359.
19. Lapan SW, Reddien PW. dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet 2011; 7: e1002226.
20. Lapan SW, Reddien PW. Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration. Cell Rep 2012; 2: 294-307.
21. Adler CE, Seidel CW, McKinney SA et al. Selective amputation of the pharynx identifies a FoxAdependent regeneration program in planaria. eLife 2014; 3: e02238.
22. Koinuma S, Umesono Y, Watanabe K et al. Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells. Gene 2000; 259: 171-176.
23. Wang Y, Zayas RM, Guo T et al. Nanos function is essential for development and regeneration of planarian germ cells. Proc Natl Acad Sci USA 2007; 104: 5901-5906.
24. Wang Y, Stary JM, Wilhelm JE et al. A functional genomic screen in planarians identifies novel regulators of germ cell development. Genes Dev 2010; 24: 2081-2092.
25. Chong T, Stary JM, Wang Y et al. Molecular markers to characterize the hermaphroditic reproductive system of the planarian Schmidtea mediterranea. BMC Dev Biol 2011; 11: 69.
26. Forsthoefel DJ, James NP, Escobar DJ et al. An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev Cell 2012; 23: 691-704.
27. Scimone ML, Srivastava M, Bell GW et al. A regulatory program for excretory system regeneration in planarians. Development 2011; 138: 4387-4398.
28. Cirillo LA, Barton MC. Many forkheads in the road to regulation. Symposium on forkhead transcription factor networks in development, signalling and disease. EMBO Rep 2008; 9: 721-724.
29. Pineda D, Gonzalez J, Callaerts P et al. Searching for the prototypic eye genetic network: Sine oculis is essential for eye regeneration in planarians. Proc Natl Acad Sci USA 2000; 97: 4525-4529.
30. Krugelis-Macrae E. The occurrence of porphyrin in the planarian. Biol Bull 1956; 110: 69-76.
31. Macrae EK. Porphyrin synthesis in the pianarian. I. Conversion of delta-aminolevulinic acid to porphobilinogen. J Exp Zool 1959; 142: 667-674.
32. Macrae EK. Porphyrin synthesis in the planarian. Ii. Incorporation of delta-aminolevulinic acid-4-C14 into uroporphyrin. J Exp Zool 1963; 153: 255-262.
33. Macrae EK. Localization of porphyrin fluorescence in planarians. Science 1961; 134: 331-332.
34. Hase S, Wakamatsu K, Fujimoto K et al. Characterization of the pigment produced by the planarian, Dugesia ryukyuensis. Pigment Cell Res 2006; 19: 248-249.
35. Brubacher JL, Vieira AP, Newmark PA. Preparation of the planarian Schmidtea mediterranea for high-resolution histology and transmission electron microscopy. Nat Protoc 2014; 9: 661-673.
36. Palladini G, Medolago-Albani L, Margotta V et al. The pigmentary system of planaria. I. Morphology. Cell Tissue Res 1979; 199: 197-202.
37. Palladini G, Medolago-Albani L, Margotta V et al. The pigmentary system of planaria. II. Physiology and functional morphology. Cell Tissue Res 1979; 199: 203-211.
38. Battersby AR, Fookes CJ, Matcham GW et al. Biosynthesis of the pigments of life: formation of the macrocycle. Nature 1980; 285: 17-21.
39. Mochizuki N, Tanaka R, Grimm B et al. The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 2010; 15: 488-498.
40. Vavilin DV, Vermaas WF. Regulation of the tetrapyrrole biosynthetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiol Plant 2002; 115: 9-24.
41. Breinig S, Kervinen J, Stith L et al. Control of tetrapyrrole biosynthesis by alternate quaternary forms of porphobilinogen synthase. Nat Struct Biol 2003; 10: 757-763.
42. Kauppinen R. Porphyrias. Lancet 2005; 365: 241-252.
43. Yin L, Bauer CE. Controlling the delicate balance of tetrapyrrole biosynthesis. Philos Trans R Soc Lond B Biol Sci 2013; 368: 20120262.
44. Reddien PW, Oviedo NJ, Jennings JR et al. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005; 310: 1327-1330.
45. Smith AT, Pazicni S, Marvin KA et al. Functional divergence of heme-thiolate proteins: a classification based on spectroscopic attributes. Chem Rev 2015; 115: 2532-2558.
46. Stubenhaus BM, Dustin JP, Neverett ER et al. Light-induced depigmentation in planarians models the pathophysiology of acute porphyrias. eLife 2016; 5: e14175.
47. Wenemoser D, Reddien PW. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 2010; 344: 979-991.
48. Nicolaidou E, Katsambas AD. Pigmentation disorders: hyperpigmentation and hypopigmentation. Clin Dermatol 2014; 32: 66-72.
49. Reddien PW. Specialized progenitors and regeneration. Development 2013; 140: 951-957.
50. Gendreau I, Angers L, Jean J, Pouliot R. In: Andrades JA (ed.), Pigmented Skin Models: Understand the Mechanisms of Melanocytes, Regenerative Medicine and Tissue Engineering. InTech: Croatia, 2013.
51. Hoekstra HE. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 2006; 97: 222-234.
52. Newmark PA, Sanchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 2000; 220: 142-153.
53. Robb SM, Gotting K, Ross E et al. SmedGD 2.0: the Schmidtea mediterranea genome database. Genesis 2015; 53: 535-546.
54. Robb SM, Ross E, Sanchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res 2008; 36: D599-D606.
55. Zayas RM, Hernandez A, Habermann B et al. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 2005; 102: 18491-18496.
56. Pearson BJ, Eisenhoffer GT, Gurley KA et al. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 2009; 238: 443-450.
57. 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.
58. Hopman AH, Ramaekers FC, Speel EJ. Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochromelabeled tyramides and their application for in situ hybridization using CARD amplification. J Histochem Cytochem 1998; 46: 771-777.
59. Tu KC, Pearson BJ, Sanchez Alvarado A. TORC1 is required to balance cell proliferation and cell death in planarians. Dev Biol 2012; 365: 458-469.
60. Li YQ, Zeng A, Han XS et al. Argonaute-2 regulates the proliferation of adult stem cells in planarian. Cell Res 2011; 21: 1750-1754.
61. Hayashi T, Asami M, Higuchi S et al. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 2006; 48: 371-380.
62. Peiris TH, Weckerle F, Ozamoto E et al. TOR signaling regulates planarian stem cells and controls localized and organismal growth. J Cell Sci 2012; 125: 1657-1665.