865
Views
2
CrossRef citations to date
0
Altmetric
Reports

Differentiation of lepidoptera scale cells from epidermal stem cells followed by ecdysone-regulated DNA duplication and scale secreting

, , , , ORCID Icon &
Pages 2156-2167 | Received 23 Jun 2017, Accepted 01 Sep 2017, Published online: 21 Sep 2017

References

  • Reynolds SE, Samuels RI, Physiology and biochemistry of insect moulting fluid, In: Evans PD, Editor. Adv In Insect Phys. Academic Press; 1996. p. 157-232. Philadelphia, PA: Elsevier Ltd.
  • Payre F, Genetic control of epidermis differentiation in Drosophila. Int J Dev Biol. 2004;48(2-3):207-15. doi:10.1387/ijdb.15272387. PMID:15272387
  • Riddiford L, Hiruma K, Zhou X, Nelson CA. Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol. 2003;33:1327-38. doi:10.1016/j.ibmb.2003.06.001. PMID:14599504
  • Truman JW, Riddiford LM, The origins of insect metamorphosis. Nature 1999. 401(6752):447-52. doi:10.1038/46737. PMID:10519548
  • Nijhout HF, Williams CM, Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J Exp Biol. 1974;61(2):481-91. PMID:4443740
  • Han F, Lu A, Yuan Y, Huang W, Beerntsen BT, Huang J, Ling E. Characterization of an entomopathogenic fungi target integument protein, Bombyx mori single domain von Willebrand factor type C, in the silkworm, Bombyx mori. Insect Mol Biol. 2017;26(3):308-316. doi:10.1111/imb.12293. PMID:28168773
  • Brey PT, Lee WJ, Yamakawa M, Koizumi Y, Perrot S, François M, Ashida M. Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proc Natl Acad Sci U S A. 1993;90(13):6275-9. doi:10.1073/pnas.90.13.6275. PMID:8327509
  • Truman JW, Riddiford LM, The morphostatic actions of juvenile hormone. Insect Biochem Mol Biol. 2007;37(8):761-70. doi:10.1016/j.ibmb.2007.05.011. PMID:17628276
  • Riddiford LM, Cherbas P, Truman JW, Ecdysone receptors and their biological actions. Vitam Horm. 2000;60:1-73. doi:10.1016/S0083-6729(00)60016-X. PMID:11037621
  • Gruntenko NE, Rauschenbach IY, Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J Insect Physiol. 2008. 54(6):902-8;doi:10.1016/j.jinsphys.2008.04.004. PMID:18511066
  • Dubrovsky EB, Hormonal cross talk in insect development. Trends Endocrinol Metab. 2005;16(1):6-11. doi:10.1016/j.tem.2004.11.003. PMID:15620543
  • Chen L, Zhu J, Sun G, Raikhel AS. The early gene Broad is involved in the ecdysteroid hierarchy governing vitellogenesis of the mosquito Aedes aegypti. J Mol Endocrinol. 2004;33(3):743-61. doi:10.1677/jme.1.01531. PMID:15591032
  • Pierceall WE, Li C, Biran A, Miura K, Raikhel AS, Segraves WA. E75 expression in mosquito ovary and fat body suggests reiterative use of ecdysone-regulated hierarchies in development and reproduction. Mol Cell Endocrinol. 1999;150(1-2):73-89. doi:10.1016/S0303-7207(99)00022-2. PMID:10411302
  • Sun G, Zhu J, Li C, Tu Z, Raikhel AS. Two isoforms of the early E74 gene, an Ets transcription factor homologue, are implicated in the ecdysteroid hierarchy governing vitellogenesis of the mosquito, Aedes aegypti. Mol Cell Endocrinol. 2002;190(1-2):147-57. doi:10.1016/S0303-7207(01)00726-2. PMID:11997188
  • Gonzy G, Pokholkova GV, Peronnet F, Mugat B, Demakova OV, Kotlikova IV, Lepesant JA, Zhimulev IF. Isolation and characterization of novel mutations of the Broad-Complex, a key regulatory gene of ecdysone induction in Drosophila melanogaster. Insect Biochem Mol Biol. 2002;32(2):121-32. doi:10.1016/S0965-1748(01)00097-2. PMID:11755053
  • Liu X, Dai F, Guo E, Li K, Ma L, Tian L, Cao Y, Zhang G, Palli SR, Li S. 20-Hydroxyecdysone (20E) primary response gene E93 Modulates 20E signaling to promote Bombyx larval-pupal metamorphosis. J Biol Chem. 2015;290(45):27370-83. doi:10.1074/jbc.M115.687293. PMID:26378227
  • de Rosny E, de Groot A, Jullian-Binard C, Gaillard J, Borel F, Pebay-Peyroula E, Fontecilla-Camps JC, Jouve HM. Drosophila nuclear receptor E75 is a thiolate hemoprotein. Biochemistry. 2006;45(32):9727-34. doi:10.1021/bi060537a. PMID:16893174
  • Karim FD, Guild GM, Thummel CS, The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development. 1993;118(3):977-988. PMID:8076529
  • Muramatsu D, Kinjoh T, Shinoda T, Hiruma K The role of 20-hydroxyecdysone and juvenile hormone in pupal commitment of the epidermis of the silkworm, Bombyx mori. Mech Dev. 2008;125(5-6):411-20. doi:10.1016/j.mod.2008.02.001. PMID:18331786
  • Uhlirova M, Foy BD, Beaty BJ, Olson KE, Riddiford LM, Jindra M. Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc Natl Acad Sci U S A. 2003;100(26):15607-15612. doi:10.1073/pnas.2136837100. PMID:14668449
  • Zhou B, Riddiford LM, Hormonal regulation and patterning of the broad-complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta. Dev Biol. 2001;231(1):125-37. doi:10.1006/dbio.2000.0143. PMID:11180957
  • Kiss I, Beaton AH, Tardiff J, Fristrom D, Fristrom JW. Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 1988;118(2):247-259. PMID:3129334
  • Kayukawa T, Jouraku A, Ito Y, Shinoda T. Molecular mechanism underlying juvenile hormone-mediated repression of precocious larval-adult metamorphosis. Proc Natl Acad Sci U S A. 2017;114(5):1057-1062. doi:10.1073/pnas.1615423114. PMID:28096379
  • Truman JW, Riddiford LM, Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol. 2002;47(1):467-500. doi:10.1146/annurev.ento.47.091201.145230. PMID:11729082
  • Ali MS, Iwanaga M, Kawasaki H, Ecdysone-responsive transcription factors determine the expression region of target cuticular protein genes in the epidermis of Bombyx mori. Dev Genes Evol. 2012;222(2):89-97. doi:10.1007/s00427-012-0392-x. PMID:22460818
  • Ali MS, Wang HB, Iwanaga M, Kawasaki H. Expression of cuticular protein genes, BmorCPG11 and BMWCP5 is differently regulated at the pre-pupal stage in wing discs of Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol. 2012;162(1-3):44-50. doi:10.1016/j.cbpb.2012.02.001. PMID:22366249
  • Wang HB, Nita M, Iwanaga M, Kawasaki H. betaFTZ-F1 and Broad-Complex positively regulate the transcription of the wing cuticle protein gene, BMWCP5, in wing discs of Bombyx mori. Insect Biochem Mol Biol. 2009;39(9):624-33. doi:10.1016/j.ibmb.2009.06.007. PMID:19580866
  • Shahin R, Iwanaga M, and Kawasaki H, Cuticular protein and transcription factor genes expressed during prepupal-pupal transition and by ecdysone pulse treatment in wing discs of Bombyx mori. Insect Mol Biol. 2016;25(2):138-52. doi:10.1111/imb.12207. PMID:26748620
  • Garcia-Bellido A, de Celis JF, The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics. 2009;182(3):631-9. doi:10.1534/genetics.109.104083. PMID:19622761
  • Garcia-Bellido A, Genetic analysis of the Achaete-Scute System of Drosophila melanogaster Genetics. 1979;91(3):491-520. PMID:17248895
  • Campuzano S, Balcells L, Villares R, Carramolino L, García-Alonso L, Modolell J, Excess function hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell. 1986;44(2):303-12. doi:10.1016/0092-8674(86)90764-6. PMID:3002632
  • Balcells L, Modolell J, and Ruiz-Gomez M, A unitary basis for different Hairy-wing mutations of Drosophila melanogaster. EMBO J. 1988;7(12):3899-906. PMID:3145198
  • Galant R, Skeath JB, Paddock S, Lewis DL, Carroll SB. Expression pattern of a butterfly achaete-scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Curr Biol. 1998;8(14):807-13. doi:10.1016/S0960-9822(98)70322-7. PMID:9663389
  • Zhou Q, Tang S, Chen Y, Yi Y, Zhang Z, Shen G. A scaleless wings mutant associated with tracheal system developmental deficiency in wing discs in the silkworm, Bombyx mori. Int J Dev Biol. 2004;48(10):1113-7. doi:10.1387/ijdb.041845qz. PMID:15602697
  • Zhou QX, Li YN, Shen XJ, Yi YZ, Zhang YZ, Zhang ZF. The scaleless wings mutant in Bombyx mori is associated with a lack of scale precursor cell differentiation followed by excessive apoptosis. Dev Genes Evol. 2006;216(11):721-6. doi:10.1007/s00427-006-0091-6. PMID:16773336
  • Shao HL, Zheng WW, Liu PC, Wang Q, Wang JX, Zhao XF, Establishment of a new cell line from lepidopteran epidermis and hormonal regulation on the genes. PLoS One 2008;3(9):e3127. doi:10.1371/journal.pone.0003127. PMID:18769621
  • Hatt PJ, Moriniere M, Oberlander H, Porcheron P. Roles for insulin and ecdysteroids in differentiation of an insect cell line of epidermal origin. In Vitro Cell Dev Biol Anim. 1994;30a(10):717-20. doi:10.1007/BF02631276. PMID:7842173
  • Caruelle JP, Cassier P, Hormonal stimulation and in vitro cellular differentiation in the integument of the desert locust Schistocerca gregaria (author's transl). Arch Anat Microsc Morphol Exp. 1979;68(2):127-38. PMID:533279
  • Ling E, Shirai K, Kanekatsu R, Kobayashi Y, Tu Z, Funayama T, Watanabe H, Kiguchi K. Why does hemocyte density rise at the wandering stage in the silkworm, Bombyx mori? J Insect Biotechnol Sericol. 2003;72:101-9.
  • Satake S, Kaya M, Sakurai S, Hemolymph ecdysteroid titer and ecdysteroid-dependent developmental events in the last-larval stadium of the silkworm, Bombyx mori: role of low ecdysteroid titer in larval-pupal metamorphosis and a reappraisal of the head critical period. J Insect Physiol. 1998;44(10):867-81. doi:10.1016/S0022-1910(98)00075-4. PMID:12770423
  • Moriyama M, Osanai K, Ohyoshi T, Wang HB, Iwanaga M, Kawasaki H. Ecdysteroid promotes cell cycle progression in the Bombyx wing disc through activation of c-Myc. Insect Biochem Mol Biol. 2016;70:1-9. doi:10.1016/j.ibmb.2015.11.008. PMID:26696544
  • Nishita Y and Takiya S, Structure and expression of the gene encoding a Broad-Complex homolog in the silkworm, Bombyx mori. Gene. 2004;339:161-72. doi:10.1016/j.gene.2004.06.039. PMID:15363856
  • Reza AM, Kanamori Y, Shinoda T, Shimura S, Mita K, Nakahara Y, Kiuchi M, Kamimura M, Hormonal control of a metamorphosis-specific transcriptional factor Broad-Complex in silkworm. Comp Biochem Physiol B Biochem Mol Biol. 2004;139(4):753-61. doi:10.1016/j.cbpc.2004.09.009. PMID:15581808
  • Xu Q, Lu A, Xiao G, Yang B, Zhang J, Li X, Guan J, Shao Q, Beerntsen BT, Zhang P, et al., Transcriptional profiling of midgut immunity response and degeneration in the wandering silkworm, Bombyx mori. PLoS ONE. 2012;7(8):e43769. doi:10.1371/journal.pone.0043769. PMID:22937093
  • Tsuzuki S, Iwami M, Sakurai S, Ecdysteroid-inducible genes in the programmed cell death during insect metamorphosis. Insect Biochem Mol Biol. 2001;31(4-5):321-31. doi:10.1016/S0965-1748(00)00124-7. PMID:11222941
  • Li TR, White KP, Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell. 2003;5(1):59-72. doi:10.1016/S1534-5807(03)00192-8. PMID:12852852
  • Edgar BA, Lehner CF, Developmental control of cell cycle regulators: a fly's perspective. Science. 1996;274(5293):1646-52. doi:10.1126/science.274.5293.1646. PMID:8939845
  • Ninov N, Manjon C, Martin-Blanco E, Dynamic control of cell cycle and growth coupling by ecdysone, EGFR, and PI3K signaling in Drosophila histoblasts. PLoS Biol. 2009;7(4):e1000079. doi:10.1371/journal.pbio.1000079. PMID:19355788
  • Stevens B, Alvarez CM, Bohman R, O'Connor JD, An ecdysteroid-induced alteration in the cell cycle of cultured Drosophila cells. Cell 1980;22(3):675-82. doi:10.1016/0092-8674(80)90543-7. PMID:6780197
  • Cranna N, Quinn L, Impact of steroid hormone signals on Drosophila cell cycle during development. Cell Div. 2009;4:3. doi:10.1186/1747-1028-4-3. PMID:19154610
  • Shao Q, Yang B, Xu Q, Li X, Lu Z, Wang C, Huang Y, Söderhäll K, Ling E. Hindgut innate immunity and regulation of fecal microbiota through melanization in insects. J Biol Chem. 2012;287(17):14270-9. doi:10.1074/jbc.M112.354548. PMID:22375003
  • Yang B, Huang W, Zhang J, Xu Q, Zhu S, Zhang Q, Beerntsen BT, Song H, Ling E, Analysis of gene expression in the midgut of Bombyx mori during the larval molting stage. BMC Genomics 2016;17(1):866. doi:10.1186/s12864-016-3162-8. PMID:27809786
  • Reese MG, Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem. 2001;26(1):51-6. doi:10.1016/S0097-8485(01)00099-7. PMID:11765852

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.