Ecdysteroid receptor signaling disruption obstructs blastemal cell proliferation during limb regeneration in the fiddler crab, Uca pugilator

Molecular and Cellular Endocrinology

Volumn 365, Issue 2, 2013, Pages 249-259

  Das, Sunetra ^a   Durica, David S ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Cell proliferation; DsRNA; EcR; Limb regeneration; RXR; Uca pugilator

Indexed keywords

DOUBLE STRANDED RNA; ECDYSONE RECEPTOR;

ANIMAL CELL; ARTICLE; BLASTEMA; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ECDYSONE RECEPTOR GENE; GENE SILENCING; GENETIC CODE; GENETIC TRANSCRIPTION; HISTOLOGY; LIMB REGENERATION; MALE; MOLTING; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECEPTOR GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UCA PUGILATOR;

ANIMALS; ARTHROPOD PROTEINS; BRACHYURA; CELL PROLIFERATION; ECDYSTEROIDS; EXTREMITIES; GENE KNOCKDOWN TECHNIQUES; PHENOTYPE; RECEPTORS, STEROID; REGENERATION; RETINOID X RECEPTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84871396908     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.10.026     Document Type: Article

References (74)

1. Adiyodi R.G. Wound healing and regeneration in the crab Paratelphusa hydrodromous. International Review of Cytology 1972, 257-289. Academic Press.
2. Berrill M. The life cycle of the green crab Carcinus maenas at the northern end of its range. J. Crustacean Biol. 1982, 31-39.
3. Bliss D.E. Neurosecretion and control of growth in a decapod crustacean. Bertil Hanstrom: Zoological Papers in Honour of His Sixty-fifth Birthday 1956, 56-75. Zoological Institute, Lund. K.G. Wingstrand (Ed.).
4. Blum N., Begemann G. Retinoic acid signaling controls the formation, proliferation and survival of the blastema during adult zebrafish fin regeneration. Development 2011, 139:107-116.
5. Brockes J.P. Amphibian limb regeneration: rebuilding a complex structure. Science 1997, 276:81-87.
6. Carlberg C., Seuter S. Dynamics of nuclear receptor target gene regulation. Chromosoma 2010, 119:479-484.
7. Chang E.S., Mykles D.L. Regulation of crustacean molting: a review and our perspectives. Gen. Comp. Endocrinol. 2011, 172:323-330.
8. Chang E.S., O'Connor J.D. Secretion of alpha-ecdysone by crab Y-organs in vitro. Proc. Natl. Acad. Sci. 1977, 74:615-618.
9. Chang E.S., Sage B.A., O'Connor J.D. The qualitative and quantitative determinations of ecdysones in tissues of the crab, Pachygrapsus crassipes, following molt induction. Gen. Comp. Endocrinol. 1976, 30:21-33.
10. Chen J.D., Evans R.M. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 1995, 377:454-457.
11. Chung A.C., Durica D.S., Hopkins P.M. Tissue-specific patterns and steady-state concentrations of ecdysteroid receptor and retinoid-X-receptor mRNA during the molt cycle of the fiddler crab, Uca pugilator. Gen. Comp. Endocrinol. 1998, 109:375-389.
12. Colombani J., Andersen D.S., Léopold P. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 2012, 336:582-585.
13. Copf T., Rabet N., Averof M. Knockdown of spalt function by RNAi causes de-repression of Hox genes and homeotic transformations in the crustacean Artemia franciscana. Dev. Biol. 2006, 298:87-94.
14. Cranna N., Quinn L. Impact of steroid hormone signals on Drosophila cell cycle during development. Cell Div. 2009, 4:3.
15. Cruz J., Mané-Padrós D., Bellés X., Martín D. Functions of the ecdysone receptor isoform-A in the hemimetabolous insect Blattella germanica revealed by systemic RNAi in vivo. Dev. Biol. 2006, 297:158-171.
16. De Loof A. Ecdysteroids, juvenile hormone and insect neuropeptides: recent successes and remaining major challenges. Gen. Comp. Endocrinol. 2008, 155:3-13.
17. Drach P. Mue et cycle d'intermue chez les Crustacés décapodes 1939, Masson.
18. Durica D.S., Chung A.C., Hopkins P.M. Characterization of EcR and RXR gene homologs and receptor expression during the molt cycle in the crab, Uca pugilator. Am. Zool. 1999, 39:758-773.
19. Durica D.S., Kupfer D., Najar F., Lai H., Tang Y., Griffin K., Hopkins P.M., Roe B. EST library sequencing of genes expressed during early limb regeneration in the fiddler crab and transcriptional responses to ecdysteroid exposure in limb bud explants. Integr. Comp. Biol. 2006, 46:948-964.
20. Durica D.S., Wu X., Anilkumar G., Hopkins P.M., Chung A.C.-K. Characterization of crab EcR and RXR homologs and expression during limb regeneration and oocyte maturation. Mol. Cell. Endocrinol. 2002, 189:59-76.
21. Emmel V.E. A study of the differentiation of tissues in the regenerating crustacean limb. Am. J. Anat. 1910, 10:109-158.
22. Fahrbach S.E., Smagghe G., Velarde R.A. Insect nuclear receptors. Annu. Rev. Entomol. 2012, 57:83-106.
23. Findlay I., McVean A. The Nervous Control of Limb Autotomy in the Hermit Crab Pagurus Bernhardus (L.) and the Role of the Cuticular Stress Detector, CSD1. J. Exp. Biol. 1977, 70:93-104.
24. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408:325-330.
25. Galliot B., Chera S. The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol. 2010, 20:514-523.
26. Garelli A., Gontijo A.M., Miguela V., Caparros E., Dominguez M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 2012, 336:579-582.
27. Giudice G., Turturici G., Geraci F., Sconzo G. Regeneration in invertebrates. Rendiconti Lincei 2008, 19:311-324.
28. Gunamalai V., Kirubagaran R., Subramoniam T. Hormonal coordination of molting and female reproduction by ecdysteroids in the mole crab Emerita asiatica (Milne Edwards). Gen. Comp. Endocrinol. 2004, 138:128-138.
29. Hopkins P.M. Growth and regeneration patterns in the fiddler crab, Uca pugilator. Biol. Bull. 1982, 163:301-319.
30. Hopkins P.M. Patterns of serum ecdysteroids during induced and uninduced proecdysis in the fiddler crab, Uca pugilator. Gen. Comp. Endocrinol. 1983, 52:350-356.
31. Hopkins P.M. Ecdysteroid titers and Y-organ activity during late anecdysis and proecdysis in the fiddler crab, Uca pugilator. Gen. Comp. Endocrinol. 1986, 63:362-373.
32. Hopkins P.M. Ecdysteroids and regeneration in the fiddler crab Uca pugilator. J. Exp. Zool. 1989, 252:293-299.
33. Hopkins P.M. Hormonal control of the molt cycle in the fiddler crab Uca Pugilator. Am. Zool. 1992, 32:450-458.
34. Hopkins P.M. Regeneration of walking legs in the fiddler crab Uca pugilator. Am. Zool. 1993, 33:348-356.
35. Hopkins P.M. Limb regeneration in the fiddler crab, Uca pugilator: hormonal and growth factor control. Am. Zool. 2001, 41:389-398.
36. Hopkins P.M., Bliss D.E., Sheehan S.W., Boyer J.R. Limb growth-controlling factors in the crab Gecarcinus lateralis, with special reference to the limb growth-inhibiting factor. Gen. Comp. Endocrinol. 1979, 39:192-207.
37. Hopkins P.M., Chung A.C., Durica D.S. Limb regeneration in the fiddler crab, Uca pugilator: histological, physiological and molecular considerations. Am. Zool. 1999, 39:513-526.
38. Hopkins P.M., Durica D.S. Effects of all-trans retinoic acid on regenerating limbs of the fiddler crab, Uca pugilator. J. Exp. Zool. 1995, 272:455-463.
39. Hopkins P.M., Durica D., Washington T. RXR isoforms and endogenous retinoids in the fiddler crab, Uca pugilator. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2008, 151:602-614.
40. Hörlein A.J., Näär A.M., Heinzel T., Torchia J., Gloss B., Kurokawa R., Ryan A., Kamei Y., Söderström M., Glass C.K. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 1995, 377:397-404.
41. Hui J.H.L., Tobe S.S., Chan S.-M. Characterization of the putative farnesoic acid O-methyltransferase (LvFAMeT) cDNA from white shrimp, Litopenaeus vannamei: evidence for its role in molting. Peptides 2008, 29:252-260.
42. Kato S., Fujiki R. Transcriptional controls by nuclear fat-soluble vitamin receptors through chromatin reorganization. Biosci., Biotechnol., Biochem. 2011, 75:410-413.
43. Kato Y., Shiga Y., Kobayashi K., Tokishita S., Yamagata H., Iguchi T., Watanabe H. Development of an RNA interference method in the cladoceran crustacean Daphnia magna. Dev. Genes Evol. 2011, 220:337-345.
44. King-Jones K., Thummel C.S. Nuclear receptors - a perspective from Drosophila. Nat. Rev. Genet. 2005, 6:311-323.
45. Kragl M., Knapp D., Nacu E., Khattak S., Maden M., Epperlein H.H., Tanaka E.M. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 2009, 460:60-65.
46. Lachaise F., Le Rox A., Hubert M., Lafont R. The molting gland of crustaceans: localization, activity and endocrine control (a review). J. Crustacean Biol. 1993, 13:198-234.
47. Maginnis T.L. The costs of autotomy and regeneration in animals: a review and framework for future research. Behav. Ecol. 2006, 17:857-872.
48. Martín D., Maestro O., Cruz J., Mané-Padrós D., Bellés X. RNAi studies reveal a conserved role for RXR in molting in the cockroach Blattella germanica. J. Insect Physiol. 2006, 52:410-416.
49. Meister G., Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
50. Mitchell N., Cranna N., Richardson H., Quinn L. The Ecdysone-inducible zinc-finger transcription factor Crol regulates Wg transcription and cell cycle progression in Drosophila. Development 2008, 135:2707-2716.
51. Mittenthal J.E. Intercalary regeneration in legs of crayfish: distal segments. Dev. Biol. 1981, 88:1-14.
52. Musatov S., Chen W., Pfaff D.W., Kaplitt M.G., Ogawa S. RNAi-mediated silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc. Natl. Acad. Sci. USA 2006, 103:10456-10460.
53. Mykles D.L. Interactions between limb regeneration and molting in decapod crustaceans. Am. Zool. 2001, 41:399-406.
54. Nakagawa Y., Henrich V.C. Arthropod nuclear receptors and their role in molting. FEBS J. 2009, 276:6128-6157.
55. Paddison P.J., Hannon G.J. RNA interference: the new somatic cell genetics?. Cancer Cell 2002, 2:17-23.
56. Priya T.A.J., Li F., Zhang J., Yang C., Xiang J. Molecular characterization of an ecdysone inducible gene E75 of Chinese shrimp Fenneropenaeus chinensis and elucidation of its role in molting by RNA interference. Comp. Biochem. Physiol., B 2010, 156:149-157.
57. Repiso A., Bergantiños C., Corominas M., Serras F. Tissue repair and regeneration in Drosophila imaginal discs. Dev. Growth Differ. 2011, 53:177-185.
58. Riddiford L.M., Cherbas P., Truman J.W. Ecdysone receptors and their biological actions. Vitam. Horm. 2000, 60:1-73.
59. Rijiravanich A., Browdy C.L., Withyachumnarnkul B. Knocking down caspase-3 by RNAi reduces mortality in Pacific white shrimp Penaeus (Litopenaeus) vannamei challenged with a low dose of white-spot syndrome virus. Fish Shellfish Immunol. 2008, 24:308-313.
60. Rohlf F.J. tpsDig, Version 212 2008, Department of Ecology and Evolution, State University of New York, Stony Brook, NY.
61. Segraves W.A. Steroid receptors and orphan receptors in Drosophila development. Semin. Cell Biol. 1994, 5:105-113.
62. Shechter A., Glazer L., Cheled S., Mor E., Weil S., Berman A., Bentov S., Aflalo E.D., Khalaila I., Sagi A. A gastrolith protein serving a dual role in the formation of an amorphous mineral containing extracellular matrix. Proc. Natl. Acad. Sci. 2008, 105:7129.
63. Shelley, C., Lovatelli, A., 2011. Mud crab aquaculture - a practical manual. FAO Fisheries and Aquaculture Technical Paper, Rome.
64. Shrivastava N., Srivastava A. RNA interference: an emerging generation of biologicals. Biotechnol. J. 2008, 3:339-353.
65. Skinner D.M. Molting and regeneration. The Biology of Crustacea 1985, 43-146. Academic Press, New York. D.E. Bliss, L.H. Mantel (Eds.).
66. Skinner D.M., Graham D.E. Loss of limbs as a stimulus to ecdysis in Brachyura (true crabs). Biol. Bull. 1972, 143:222-233.
67. Swevers L., Iatrou K. The ecdysone regulatory cascade and ovarian development in lepidopteran insects: insights from the silkmoth paradigm. Insect Biochem. Mol. Biol. 2003, 33:1285-1297.
68. Thummel C.S. Flies on steroids - Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet. 1996, 12:306-310.
69. Tijsterman M., Plasterk R.H.A. Dicers at RISC; the mechanism of RNAi. Cell 2004, 117:1-3.
70. Tiu S.H.-K., Chan S.-M. The use of recombinant protein and RNA interference approaches to study the reproductive functions of a gonad-stimulating hormone from the shrimp Metapenaeus ensis. FEBS J. 2007, 274:4385-4395.
71. Tsai M.J., O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 1994, 63:451-486.
72. Vastenhouw N.L., Brunschwig K., Okihara K.L., Müller F., Tijsterman M., Plasterk R.H. Gene expression: long-term gene silencing by RNAi. Nature 2006, 442:882.
73. Vigh D.A., Fingerman Milton Molt staging in the fiddler crab Uca pugilator. J. Crustacean Biol. 1985, 5:386-396.
74. Yu X., Chang E.S., Mykles D.L. Characterization of limb autotomy factor-proecdysis (LAFpro), isolated from limb regenerates, that suspends molting in the land crab Gecarcinus lateralis. Biol. Bull. 2002, 202:204-212.