A juvenile hormone transcription factor Bmdimm-fibroin H chain pathway is involved in the synthesis of silk protein in silkworm, Bombyx mori

Journal of Biological Chemistry

Volumn 290, Issue 2, 2015, Pages 972-986

  Zhao, Xiao Ming ^a,b   Liu, Chun ^a   Jiang, Li Jun ^a   Li, Qiong Yan ^a   Zhou, Meng Ting ^a   Cheng, Ting Cai ^a   Mita, Kazuei ^a   Xia, Qing You ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b SHANXI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BIOCHEMISTRY; BIOSYNTHESIS; CELL CULTURE; CHAINS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES; HORMONES; PLANTS (BOTANY); PROTEINS; RNA; TRANSCRIPTION FACTORS;

AFTER-TREATMENT; BASIC HELIX LOOP HELIXES; CO-IMMUNOPRECIPITATION ASSAYS; ENZYME LINKED IMMUNOSORBENT ASSAY; JUVENILE HORMONE; MOLECULAR MECHANISM; REGULATORY PATHWAY; RNA INTERFERENCE;

TRANSCRIPTION;

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DOUBLE STRANDED RNA; E BOX PROTEIN; FIBROIN H; JUVENILE HORMONE; NUCLEIC ACID BINDING PROTEIN; SILK FIBROIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BMDIMM; TRANSCRIPTION FACTOR BMSAGE; UNCLASSIFIED DRUG; FIBROIN; INSECT PROTEIN; SERICIN; SILK;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BMDIMM GENE; BOMBYX MORI; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FAR WESTERN BLOTTING; FIB H GENE; GENE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HORMONAL REGULATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; METAMORPHOSIS; NONHUMAN; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA INTERFERENCE; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; BOMBYX; GENETICS; LARVA; METABOLISM;

BOMBYX MORI;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BOMBYX; FIBROINS; INSECT PROTEINS; JUVENILE HORMONES; LARVA; PROMOTER REGIONS, GENETIC; SERICINS; SILK;

EID: 84920997242     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.606921     Document Type: Article

References (55)

1. Xia, Q., Li, S., and Feng, Q. (2014) Advances in silkworm studies accelerated by the genome sequencing of Bombyx mori. Annu. Rev. Entomol. 59, 513-536
2. Inoue, S., Tanaka, K., Arisaka, F., Kimura, S., Ohtomo, K., and Mizuno, S. (2000) Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and p25, with a 6:6:1 molar ratio. J. Biol. Chem. 275, 40517-40528
3. Maekawa, H., and Suzuki, Y. (1980) Repeated turn-offand turn-on of fibroin gene transcription during silk gland development of Bombyx mori. Dev. Biol. 78, 394-406
4. Ohta, S., and Suzuki, Y. (1988) Fibroin gene transcription in the embryonic stages of the silkworm, Bombyx mori. Develop. Growth & Differ. 30, 293-299
5. Mach, V. (1995) Silk gland factor-1 involved in the regulation of Bombyx sericin-1 gene contains Fork head motif. J. Biol. Chem. 270, 9340-9346
6. Weigel, D., Jürgens, G., Küttner, F., Seifert, E., and Jäckle, H. (1989) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658
7. Ohno, K., Sawada, J., Takiya, S., Kimoto, M., Matsumoto, A., Tsubota, T., Uchino, K., Hui, C.-C., Sezutsu, H., Handa, H., and Suzuki, Y. (2013) Silk gland factor-2, involved in Fibroin gene transcription, consists of LIM homeodomain, LIM-interacting, and single-stranded DNA-binding proteins. J. Biol. Chem. 288, 31581-31591
8. Xu, P.-X., Fukuta, M., Takiya, S., Matsuno, K., Xu, X., and Suzuki, Y. (1994) Promoter of the POU-M1/SGF-3 gene involved in the expression of Bombyx silk genes. J. Biol. Chem. 269, 2733-2742
9. Kimoto, M., Kitagawa, T., Kobayashi, I., Nakata, T., Kuroiwa, A., and Takiya, S. (2012) Inhibition of the binding of MSG-intermolt-specific complex, MIC, to the sericin-1 gene promoter and sericin-1 gene expression by POU-M1/SGF-3. Dev. Genes Evol. 222, 351-359
10. Takiya, S., Kokubo, H., and Suzuki, Y. (1997) Transcriptional regulatory elements in the upstream and intron of the fibroin gene bind three specific factors POU-M1, BmFkh, and FMBP-1. Biochem. J. 321, 645-653
11. Kokubo, H., Takiya, S., Mach, V., and Suzuki, Y. (1996) Spatial and temporal expression pattern of Bombyx fork head/SGF-1 gene in embryogenesis. Dev. Genes Evol. 206, 80-85
12. Li, M., Wang, I. X., Li, Y., Bruzel, A., Richards, A. L., Toung, J. M., and Cheung, V. G. (2011) Widespread RNA and DNA sequence differences in the human transcriptome. Science 333, 53-58
13. Abrams, E. W., Mihoulides, W. K., and Andrew, D. J. (2006) Fork head and Sage maintain a uniform and patent salivary gland lumen through regulation of two downstream target genes, PH4&SG1 and PH4&SG2. Development 133, 3517-3527
14. Fox, R. M., Vaishnavi, A., Maruyama, R., and Andrew, D. J. (2013) Organspecific gene expression: thebHLHprotein Sage provides tissue specificity to Drosophila FoxA. Development 140, 2160-2171
15. Zhao, X. M., Liu, C., Li, Q. Y., Hu, W. B., Zhou, M. T., Nie, H. Y., Zhang, Y. X., Peng, Z. C., Zhao, P., and Xia, Q. Y. (2014) Basic helix-loop-helix transcription factor bmsage is involved in regulation of fibroin H-chain gene via interaction with SGF1 in Bombyx mori. PLoS One 9, e94091
16. Ferré-D'Amaré, A. R., Prendergast, G. C., Ziff, E. B., and Burley, S. K. (1993) Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363, 38-45
17. Blackwell, T. K., Huang, J., Ma, A., Kretzner, L., Alt, F. W., Eisenman, R. N., and Weintraub, H. (1993) Binding of myc proteins to canonical and noncanonical DNA sequences. Mol. Cell. Biol. 13, 5216-5224
18. Ellenberger, T., Fass, D., Arnaud, M., and Harrison, S. C. (1994) Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8, 970-980
19. Murre, C., McCaw, P. S., and Baltimore, D. (1989) A new DNA-binding and dimerization motif in immunoglobulin enhancer binding, daughterless, myod, and myc proteins. Cell 56, 777-783
20. Ma, P. C., Rould, M. A., Weintraub, H., and Pabo, C. O. (1994) Crystal structure of myoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77, 451-459
21. Park, D. (2008) Mapping peptidergic cells in Drosophila where dimm fits in. PLoS One 3, e1896
22. Park, D., Shafer, O. T., Shepherd, S. P., Suh, H., Trigg, J. S., and Taghert, P. H. (2008) The Drosophila basic helix-loop-helix protein DIMMED directly activates PHM, a gene encoding a neuropeptide-amidating enzyme. Mol. Cell Biol. 28, 410-421
23. Wang, Y., Chen, K., Yao, Q., Wang, W., and Zhi, Z. (2007) The basic helix-loop-helix transcription factor family in Bombyx mori. Dev. Genes Evol. 217, 715-723
24. Riddiford, L. M. (1996) Juvenile hormone: The status of its "status quo" action. Arch. Insect Biochem. Physiol. 32, 271-286
25. Minakuchi, C., Zhou, X., and Riddiford, L. M. (2008) Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech. Dev. 125, 91-105
26. Wilson, T. G., and Fabian, J. (1986) A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118, 190-201
27. Miura, K., Oda, M., Makita, S., and Chinzei, Y. (2005) Characterization of the Drosophila Methoprene-tolerant gene product-Juvenile hormone binding and ligand-dependent gene regulation. FEBS J. 272, 1169-1178
28. Charles, J.-P., Iwema, T., Epa, V. C., Takaki, K., Rynes, J., and Jindra, M. (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene- tolerant. Proc. Natl. Acad. Sci. U.S.A. 108, 21128-21133
29. Li, M., Mead, E. A., and Zhu, J. (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc. Natl. Acad. Sci. U.S.A. 108, 638-643
30. Zhang, H. J., Anderson, A. R., Trowell, S. C., Luo, A. R., Xiang, Z. H., and Xia, Q. Y. (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6, e24111
31. Kayukawa, T., Minakuchi, C., Namiki, T., Togawa, T., Yoshiyama, M., Kamimura, M., Mita, K., Imanishi, S., Kiuchi, M., Ishikawa, Y., and Shinoda, T. (2012) Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc. Natl. Acad. Sci. U.S.A. 109, 11729-11734
32. Kayukawa, T., Tateishi, K., and Shinoda, T. (2013) Establishment of a versatile cell line for juvenile hormone signaling analysis in Tribolium castaneum. Sci. Rep. 3, 1570
33. Minakuchi, C., Namiki, T., and Shinoda, T. (2009) Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev. Biol. 325, 341-350
34. Lozano, J., and Belles, X. (2011) Conserved repressive function of Kruppel homolog 1 on insect metamorphosis in hemimetabolous and holometabolous species. Sci. Rep. 1, 163
35. Kayukawa, T., Murata, M., Kobayashi, I., Muramatsu, D., Okada, C., Uchino, K., Sezutsu, H., Kiuchi, M., Tamura, T., Hiruma, K., Ishikawa, Y., and Shinoda, T. (2014) Hormonal regulation and developmental role of Krüppel homolog 1, a repressor of metamorphosis, in the silkworm Bombyx mori. Dev. Biol. 388, 48-56
36. Daillie, J. (1979) Juvenile-hormone modifies larvae and silk gland development in Bombyx mori. Biochimie 61, 275-281
37. Kurata, S., Koga, K., and Sakaguchi, B. (1978) Nucleolar size in parallel with ribosomalRNAsynthesis at diapause termination in the eggs of Bombyx mori. Chromosoma 68, 313-317
38. Kurata, K. (1984) Effect of a juvenile hormon analogue given at various ages of 5th instar larvae on RNA synthesis in the posterior silk gland of the silkworm, Bombyx mori. J. Seric. Sci. Jpn. 53, 421-426
39. Pan, M. H., Xiao, S. Q., Chen, M., Hong, X. J., and Lu, C. (2007) Establishment and characterization of two embryonic cell lines of Bombyx mori. In Vitro Cell. Dev. Biol. Anim. 43, 101-104
40. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882
41. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
42. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2Δ ΔCt method. Methods 25, 402-408
43. Aslam, A. F., Kiya, T., Mita, K., and Iwami, M. (2011) Identification of novel bombyxin genes from the genome of the silkmoth Bombyx mori and analysis of their expression. Zool. Sci. 28, 609-616
44. Wu, Y., Li, Q., and Chen, X. Z. (2007) Detecting protein-protein interactions by far Western blotting. Nat. Protoc. 2, 3278-3284
45. Bobrovnik, S. A. (2003) Determination of antibody affinity by ELISA. Theory. J. Biochem. Biophys. Methods 57, 213-236
46. Liu, Q. X., Ueda, H., and Hirose, S. (2000) MBF2 is a tissue- and stagespecific coactivator that is regulated at the step of nuclear transport in the silkworm Bombyx mori. Dev. Biol. 225, 437-446
47. Lin, Y., Meng, Y., Wang, Y. X., Luo, J., Katsuma, S., Yang, C. W., Banno, Y., Kusakabe, T., Shimada, T., and Xia, Q. Y. (2013) Vitellogenin receptor mutation leads to the oogenesis mutant phenotype "scanty vitellin" of the silkworm, Bombyx mori. J. Biol. Chem. 288, 13345-13355
48. Kethidi, D. R., Perera, S. C., Zheng, S., Feng, Q. L., Krell, P., Retnakaran, A., and Palli, S. R. (2004) Identification and characterization of a juvenile hormone (JH) response region in the JH esterase gene from the spruce budworm, Choristoneura fumiferana. J. Biol. Chem. 279, 19634-19642
49. Chaitanya, R. K., Sridevi, P., Senthilkumaran, B., and Dutta Gupta, A. (2013) Effect of juvenile hormone analog, methoprene on H-fibroin regulation during the last instar larval development of Corcyra cephalonica. Gen. Comp. Endocrinol. 181, 10-17
50. Grzelak, K., Szczesna, E., and Sehnal, F. (1982) Stimulation of RNA-transcription by juvenile-hormone in degenerating silk glands. Mol. Cell. Endocrinol. 26, 341-351
51. Tripoulas, N. A., and Samols, D. (1986) Developmental and hormonal regulation of sericin RNA in the silkworm, Bombyx mori. Dev. Biol. 116, 328-336
52. Sehnal, F., and Akai, H. (1990) Insect silk glands: their types, development and function, and effects of environmental factors and morphogenetic hormones on them. Int. J. Insect Morphol. Embryol. 19, 79-132
53. Suzuki, Y., Tsuda, M., Takiya, S., Hirose, S., Suzuki, E., Kameda, M., and Ninaki, O. (1986) Tissue-specific transcription enhancement of the fibroin gene characterized by cell-free systems. Proc. Natl. Acad. Sci. U.S.A. 83, 9522-9526
54. Ishizaki, H., and Suzuki, A. (1994) The brain secretory peptides that control moulting and metamorphosis of the silkmoth, Bombyx mori. Int. J. Dev. Biol. 38, 301-310
55. Durand, B., Drevet, J., and Couble, P. (1992) p25 Gene regulation in Bombyx mori silk gland: two promoter-binding factors have distinct tissue and developmental specificities. Mol. Cell. Biol. 12, 5768-5777