家蚕中调控胚胎滞育的滞育激素及其受体研究概况
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摘要
滞育是昆虫为躲避不良生存环境而进化出的一种个体发育停滞的生存策略和状态,家蚕Bombyx mori滞育发生于胚胎发育早期,为卵滞育型。家蚕胚胎滞育是由咽下神经节分泌的滞育激素作用于卵巢,通过卵巢细胞膜上的滞育激素受体介导,引发卵内一系列物质代谢变化而引发的发育事件。本文综述了家蚕滞育激素的发现及其结构与功能,以及滞育激素受体的基因克隆与表达、信号转导与机理等研究概况,并展望了其研究前景,以期推进家蚕胚胎滞育诱导、阻止和解除全过程的分子机理研究,并为进一步利用家蚕胚胎滞育进行传统养蚕业的技术提升等提供理论依据。
Diapause is an adaptive developmental strategy and state adopted by insects to survive in challenging environments. The silkworm, Bombyx mori, is a typical egg diapause insect, and the diapause happens in the early stages of its embryonic development. The diapause hormone(DH) is secreted by the suboesophageal ganglion of B. mori, playing a key role in the process of egg diapause. DH transmits signals via diapause hormone receptor(DHR) on the surface of silkworm ovarian cells, regulating the material metabolism and then determining the diapause of eggs. In this article, we summarized the discovery process and structure and function of DH, reviewed the gene cloning and expression, signal transduction and mechanism of DHR in the silkworm, and put forward the research prospects. It is expected to provide a molecular theoretical basis for studying the whole process of induction, inhibition and termination of embryonic diapause and further utilizing silkworm embryo diapause to improve the technology of traditional silkworm rearing.
Diapause is an adaptive developmental strategy and state adopted by insects to survive in challenging environments. The silkworm, Bombyx mori, is a typical egg diapause insect, and the diapause happens in the early stages of its embryonic development. The diapause hormone(DH) is secreted by the suboesophageal ganglion of B. mori, playing a key role in the process of egg diapause. DH transmits signals via diapause hormone receptor(DHR) on the surface of silkworm ovarian cells, regulating the material metabolism and then determining the diapause of eggs. In this article, we summarized the discovery process and structure and function of DH, reviewed the gene cloning and expression, signal transduction and mechanism of DHR in the silkworm, and put forward the research prospects. It is expected to provide a molecular theoretical basis for studying the whole process of induction, inhibition and termination of embryonic diapause and further utilizing silkworm embryo diapause to improve the technology of traditional silkworm rearing.
引文
Denlinger DL, 2002. Regulation of diapause. Annu. Rev. Entomol., 47(1): 93-122.
Einstein R, Jordan H, Zhou W, Brenner M, Mose EG, Liggett SB, 2008. Alternative splicing of the G protein-coupled receptor superfamily in human airway smooth muscle diversifies the complement of receptors. Proc. Natl. Acad. Sci. USA, 105(13): 5230-5235.
Fan LF, Zhong YS, Lin JR, 2011. Comparisons of related enzymes activities between diapause and non-diapause silkworm eggs, Bombyx mori. Acta Entomol. Sin., 54(11): 1258-1263. [范兰芬, 钟杨生, 林健荣, 2011. 家蚕滞育卵与非滞育卵中几种关键酶活性的比较研究. 昆虫学报, 54(11): 1258-1263]
Fan Y, Sun P, Wang Y, He X, Deng X, Chen X, Zhang G, Chen X, Zhou N, 2010. The G protein-coupled receptors in the silkworm, Bombyx mori. Insect Biochem. Molec. Biol., 40(8): 581-591.
Filmore D, 2004. It’s a GPCR world. Mod. Drug Discov., 7(11): 24-28.
Fukuda S, 1951. The production of the diapause eggs by transplanting the suboesophageal ganglion in the silkworm. Proc. Jpn. Acad., 27: 672-677.
Fukuda S, 1952. Function of the pupal brain and suboesophageal ganglion in the production of non-diapause and diapause eggs in the silkworm. Annot. Zool. Japon., 25: 149-155.
Gan L, Liang JB, Liu XL, He NJ, 2010. Neuropeptide gene screening and mature peptide prediction in the silkworm, Bombyx mori. Acta Entomol. Sin., 53(1): 9-19. [甘玲, 梁九波, 刘喜龙, 何宁佳, 2010. 家蚕神经肽基因的筛查及成熟肽的预测. 昆虫学报, 53(1): 9-19]
Gkouvitsas T, Kontogiannatos D, Kourti A, 2009. Cognate HSP70 gene is induced during deep larval diapause in the moth Sesamia nonagrioides. Insect Mol. Biol., 18(2): 253-264.
Grenier AM, Rocha MD, Jalabert A, Royer C, Mauchamp B, Chavancy G, 2004. Artificial parthenogenesis and control of voltinism to manage transgenic populations in Bombyx mori. J. Insect Physiol., 50(8): 751-760.
Gu YY, Hua RS, Zhou NM, Shi LG, 2008. Cloning and quantitative analysis of diapause hormone receptor gene in the silkworm, Bombyx mori. Acta Sericol. Sin., 34(3): 417-423. [顾燕燕, 华荣胜, 周耐明, 时连根, 2008. 家蚕滞育激素受体基因(BmDHR)的分子克隆及定量分析. 蚕业科学, 34(3): 417-423]
Hare JD, 1983. Seasonal variation in plant-insect associations: utilization of Solanum dulcamara by Leptinotarsa decemlineata. Ecology, 64(2): 345-361.
Hasegawa K, 1957. The diapause hormone of the silkworm, Bombyx mori. Nature, 179(4573): 1300-1301.
Hasegawa K, 1963. Studies on the mode of action of the diapause hormone in the silkworm, Bombyx mori. I. The action of diapause hormone injected into pupae of different ages. J. Exp. Biol., 40: 517-530.
Hodek I, Kostál V, 1997. Photoperiodism and control of summer diapause in the Mediterranean tiger moth Cymbalophora pudica. J. Insect Physiol., 43(8): 767-777.
Hökfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M, 2000. Neuropeptides-an overview. Neuropharmacology, 39(8): 1337-1356.
Homma T, Watanabe K, Tsurumaru S, Kataoka H, Imai K, Kamba M, Niimi T, Yamashita O, Yaginuma T, 2006. G protein-coupled receptor for diapause hormone, an inducer of Bombyx embryonic diapause. Biochem. Biophys. Res. Commun., 344(1): 386-393.
Huang JT, 2003. Studies on the molecular mechanism of diapause in the silkworm, Bombyx mori. Acta sericol. Sin., 29(1): 1-6. [黄君霆, 2003. 家蚕滞育分子机制的研究. 蚕业科学, 29(1): 1-6]
Isobe M, Hasegawa K, Goto T, 1973. Isolation of the diapause hormone from the silkworm, Bombyx mori. J. Insect Physiol., 19(6): 1221-1239.
Isobe M, Hasegawa K, Goto T, 1975. Further characterization of the silkworm diapause hormone A. J. Insect Physiol., 21(12): 1917-1920.
Jiang MX, Xie LQ, Zhang XX, 1999. Characteristics of diapause induction of cotton bollworm. Chin. J. Appl. Ecol., 10(1): 60-62. [蒋明星, 谢立群, 张孝羲, 1999. 棉铃虫的滞育诱导特性. 应用生态学报, 10(1): 60-62]
Jiang X, Yang JW, Shen ZF, Chen YJ, Shi LG, Zhou NM, 2016. Agonist-mediated activation of Bombyx mori diapause hormone receptor signals to extracellular signal-regulated kinases 1 and 2 through Gq-PLC-PKC-dependent cascade. Insect Biochem. Molec. Biol., 75: 78-88.
Kitagawa N, Shiomi K, Imai K, Niimi T, Yaginuma T, Yamashita O, 2005a. Establishment of a sandwich ELISA system to detect diapause hormone, and developmental profile of hormone levels in egg and subesophageal ganglion of the silkworm, Bombyx mori. Zool. Sci., 22(2): 213-221.
Kitagawa N, Shiomi K, Imai K, Yamashita O, Yaginuma T, 2005b. Diapause hormone levels in subesophageal ganglia of uni-, bi- and poly-voltine races during pupal-adult development of Bombyx mori, and the effects of ouabain, an inhibitor of Na+-K+ ATPase, on the hormone levels. J. Insect Biotech. Sericol., 74(2): 57-62.
Kobayashi N, Takahashi M, Kihara S, Niimi T, Yamashita O, Yaginuma T, 2014. Cloning of cDNA encoding a Bombyx mori homolog of human oxidation resistance 1 (OXR1) protein from diapause eggs, and analyses of its expression and function. J. Insect Physiol., 68(3): 58-68.
Lee HJ, Wall B, Chen S, 2008. G-protein-coupled receptors and melanoma. Pigment Cell Melanoma Res., 21(4): 415-428.
Lee JM, Hull JJ, Kawai T, Goto C, Kurihara M, Tanokura M, Nagata K, Nagasawa H, Matsumoto S, 2012. Re-evaluation of the PBAN receptor molecule: characterization of PBANR variants expressed in the pheromone glands of moths. Front. Endocrinol., 3: 6.
Lee REJr, Denlinger DL, 1991. Insects at Low Temperature. Springer, New York. 119-121.
Li XT, Shi LG, 2016. Progress in functions and underlying signal transduction mechanisms of neuropeptides and their receptors in the silkworm Bombyx mori. Acta Entomol. Sin., 59(7): 759-766. [李晓童, 时连根, 2016. 家蚕神经肽及其受体的功能和信号转导机制研究进展. 昆虫学报, 59(7): 759-766]
Liu L, He LF, Liu H, Yan R, 2010. Research progress of insects diapause. J. Anhui Agric. Sci., 38(14): 7409-7411. [刘流, 贺莉芳, 刘晖, 晏容, 2010. 昆虫滞育的研究进展. 安徽农业科学, 38(14): 7409-7411]
Majumdar S, Grinnell S, Le Rouzic V, Burgman M, Polikar L, Ansonoff M, Pintar J, Pan YX, Pasternak GW, 2011. Truncated G protein-coupled mu opioid receptor MOR-1 splice variants are targets for highly potent opioid analgesics lacking side effects. Proc. Natl. Acad. Sci. USA, 108(49): 19778-19783.
Makka T, Sonobe H, 2000. Ecdysone metabolism in diapause eggs and non-diapause eggs of the silkworm, Bombyx mori. Zool. Sci., 17(1): 89-95.
Markovic D, Challiss RA, 2009. Alternative splicing of G protein-coupled receptors: physiology and pathophysiology. Cell. Mol. Life Sci., 66(20): 3337-3352.
Morita A, Niimi T, Yamashita O, 2003. Physiological differentiation of DH-PBAN-producing neurosecretory cells in the silkworm embryo. J. Insect Physiol., 49(12): 1093-1102.
Niimi T, Yamashita O, Yaginuma T, 1992. Activity of NAD-sorbitol dehydrogenase is caused by biosynthesis of enzyme protein in diapause and non-diapause eggs of the silkworm, Bombyx mori. Comp. Biochem. Physiol. B, 103(3): 657-661.
Niimi T, Yamashita O, Yaginuma T, 1993. A cold-inducible Bombyx gene encoding a protein similar to mammalian sorbitol dehydrogenase. Yolk nuclei-dependent gene expression in diapause eggs. Eur. J. Biochem., 213(3): 1125-1131.
Numata H, Hidaka T, 1982. Photoperiodic control of adult diapause in the bean bug Riptortus clavatus Thunberg (Heteroptera: Coreidae). I. Reversible induction and termination of diapause. Appl. Entomol. Zool., 17(4): 530-538.
Saito H, Takeuchi Y, Takeda R, Hayashi Y, Watanabe K, Shin M, Imai K, Isobe M, Yamashita O, 1994. The core and complementary sequence responsible for biological activity of the diapause hormone of the silkworm, Bombyx mori. Peptides, 15(7): 1173-1178.
Sasibhushan S, Rao CGP, Ponnuvel KM, 2013. Genome wide microarray based expression profiles during early embryogenesis in diapause induced and non-diapause eggs of polyvoltine silkworm Bombyx mori. Genomics, 102(4): 379-387.
Sato Y, Oguchi M, Menjo N, Imai K, Saito H, Ikeda M, Isobe M, Yamashita O, 1993. Precursor polyprotein for multiple neuropeptides secreted from the suboesophageal ganglion of the silkworm Bombyx mori: characterization of the cDNA encoding the diapause hormone precursor and identification of additional peptides. Proc. Natl. Acad. Sci. USA, 90(8): 3251-3255.
Saunders DS, 2010. Under-sized larvae from short-day adults of the blow fly, Calliphora vicina, side-step the diapause programme. Physiol. Entomol., 22(3): 249-255.
Shen Z, Jiang X, Yan L, Chen Y, Wang W, Shi Y, Shi L, Liu D, Zhou N, 2018. Structural basis for the interaction of diapause hormone with its receptor in the silkworm, Bombyx mori. FASEB J., 32(3): 1338-1353.
Shi LG, 2004. Studies of Sericulture. China Agricultural Scientech Press, Beijing. 570-572. [时连根, 2004. 蚕学研究. 北京: 中国农业科学技术出版社. 570-572]
Sun JS, Zhang TY, Zhang QR, Xu WH, 2003. Effect of the brain and suboesophageal ganglion on pupal development in Helicoverpa armigera through regulation of FXPRLamide neuropeptides. Regul. Pep., 116(1-3): 163-171.
Tauber MJ, Tauber CA, 1973. Seasonal regulation of dormancy in Chrysopa carnea (Neuroptera). J. Insect Physiol., 19(7): 1455-1463.
Tauber MJ, Tauber CA, Masaki S, 1986. Seasonal Adaptations of Insects. Oxford University Press, New York. 37-106.
Trzaskowski B, Latek D, Yuan S, Ghoshdastider U, Debinski A, Filipek S, 2012. Action of molecular switches in GPCRs-theoretical and experimental studies. Curr. Med. Chem., 19(8): 1090-1109.
Veenstra JA, Khammassi H, 2017. Rudimentary expression of RYamide in Drosophila melanogaster relative to other Drosophila species points to a functional decline of this neuropeptide gene. Insect Biochem. Molec. Biol., 83: 68-79.
Wang JE, Liu J, 2009. Research progress of insect trehalase. Guizhou Agr. Sci., 37(4): 88-90. [王军娥, 刘静, 2009. 昆虫海藻糖酶的研究进展. 贵州农业科学, 37(4): 88-90]
Wang LG, 2011. Analysis of Structure, Expression and Function of Bombyx mori Diapause Receptor Gene. MSc Thesis, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu. [王力刚, 2011. 家蚕滞育激素受体基因的结构和表达特性及功能分析. 江苏镇江: 江苏科技大学硕士学位论文]
Wang LG, Song HT, Huang Y, Wang SP, Tang SM, Zhao QL, Shen XJ, 2011. Influence of incubation temperature on expression of diapause hormone receptor genes in bivoltine Bombyx mori variety and structural features of the gene. Acta Sericol. Sin., 37(2): 215-223. [王力刚, 宋海韬, 黄勇, 汪生鹏, 唐顺明, 赵巧玲, 沈兴家, 2011. 催青温度对家蚕二化性品种滞育激素受体基因表达的影响及基因的结构特征. 蚕业科学, 37(2): 215-223]
Wang M, Li Z, 2004. The research advance of insect diapause. J. Nanjing For. Univ. (Nat. Sci. Ed.), 28(1): 71-76. [王满囷, 李周直, 2004. 昆虫滞育的研究进展. 南京林业大学学报(自然科学版), 28(1): 71-76]
Williams CM, 1952. Physiology of insect diapause IV. The brain and prothoracic glands as an endocrine system in the cecropia silkworm. Biol. Bull., 103(1): 120-138.
Wu DY, Xiang ZH, Toshihara F, 2002. Influence of synthetic diapause hormone on carbohydrate metabolism in silkworm eggs. Acta Sericol. Sin., 28(2): 99-103. [吴大洋, 向仲怀, 古泽寿治, 2002. 合成滞育激素对家蚕卵碳水化合物代谢的影响. 蚕业科学, 28(2): 99-103]
Xie LQ, Jiang MX, Zhang XX, 1997. Studies on the diapause characteristics of oriental tabacco budworm. Acta Phyptohyl. Sin., 24(3): 199-203. [谢立群, 蒋明星, 张孝羲, 1997. 烟青虫滞育特性的研究. 植物保护学报, 24(3): 199-203]
Xu WH, 1998. The regulation of the DH-PBAN gene expression in Bombyx mori. Chin. J. Biochem. Mol. Biol., 14(5): 557-561. [徐卫华, 1998. 家蚕滞育激素-性信息素合成激活肽基因表达的调节. 中国生物化学与分子生物学报, 14(5): 557-561]
Xu WH, 1999a. Advances in insect diapause studies. Acta Entomol. Sin., 42(1): 100-107. [徐卫华, 1999a. 昆虫滞育研究进展. 昆虫学报, 42(1): 100-107]
Xu WH, 1999b. Molecular mechanism of diapause in Bombyx mori. 2. Diapause determination and expression of diapause hormone gene in pupal stage. Acta Genet. Sin., 26(2): 107-111. [徐卫华, 1999b. 家蚕滞育的分子机理. 2. 蛹期滞育激素的表达与滞育决定. 遗传学报, 26(2): 107-111]
Xu WH, 2008. Advances in insect diapause studies. Chin. Bull. Entomol., 45(4): 512-517. [徐卫华, 2008. 昆虫滞育研究进展. 昆虫知识, 45(4): 512-517]
Xu WH, Sato Y, Ikeda M, Yamashita O, 1995. Molecular characterization of the gene encoding the precursor protein of diapause hormone and pheromone biosynthesis activating neuropeptide (DH-PBAN) of the silkworm, Bombyx mori and its distribution in some insects. Biochim. Biophys. Acta, 1261(1): 83-89.
Xu WH, Yamashita O, 1996. Expression of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide during post-embryonic development in the silkworm, Bombyx mori. Acta Biochim. Biophys. Sin., 28(2): 214-217. [徐卫华, 山下兴亚, 1996. 家蚕滞育激素-性信息素合成激活肽基因的表达. 生物化学与生物物理学报, 28(2): 214-217]
Xu WH, Yukihiro S, Yamashita O, 1995. Cloning of the diapause hormone gene of the silkworm (Bombyx mori). Acta Genet. Sin., 22(3): 178-184. [徐卫华, 佐藤行洋, 山下兴亚, 1995. 家蚕滞育激素基因的克隆. 遗传学报, 22(3): 178-184]
Xu WH, Zhang Y, Wang Y, Ding L, Liu J, 1998. Molecular mechanism of diapause in insect (I). Expression of diapause hormone gene and incubation temperature in embryonic stage of Bombyx mori. Sci. China Life Sci., 41(3): 344-350.
Yaginuma T, Kobayashi M, Yamashita O, 1990. Distinct effects of different low temperatures on the induction of NAD-sorbitol dehydrogenase activity in diapause eggs of the silkworm, Bombyx mori. J. Comp. Physiol. B, 160(3): 277-285.
Yamanaka N, Yamamoto S, Zitnan D, Watanabe K, Kawada T, Satake H, Kaneko Y, Hiruma K, Tanaka Y, Shinoda T, Kataoka H, 2008. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE, 3(8): e3048.
Yamashita O, 1995. Diapause hormone of the silkworm, Bombyx mori: structure, gene expression and function. J. Insect Physiol., 42(7): 669-679.
Yamashita O, Hasegawa K, 1970. Oöcyte age sensitive to the diapause hormone from the standpoint of glycogen synthesis in the silkworm, Bombyx mori. J. Insect Physiol., 16(12): 2377-2383.
Yamashita O, Hasegawa K, Seki M, 1972. Effect of the diapause hormone on trehalase activity in pupal ovaries of the silkworm, Bombyx mori. Gen. Comp. Endocr., 18(3): 515-523.
Yin CM, Wang ZS, Chaw WD, 1985. Brain neurosecretory cell and ecdysiotropin activity of the non-diapausing, pre-diapausing and diapausing southwestern corn borer, Diatraea grandiosella Dyar. J. Insect Physiol., 31(8): 659, 661-663, 667.
Yocum GD, 2001. Differential expression of two HSP70 transcripts in response to cold, thermoperiod, and adult diapause in the Colorado potato beetle. J. Insect Physiol., 47(10): 1139-1145.
Zhang Q, Denlinger DL, 2012. Dynamics of diapause hormone and prothoracicotropic hormone transcript expression at diapause termination in pupae of the corn earworm, Helicoverpa zea. Peptides, 34(1): 120-126.
Zhang TY, Kang L, Zhang ZF, Xu WH, 2004b. Identification of a POU factor involved in regulating the neuron-specific expression of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide in Bombyx mori. Biochem. J., 380(1): 255-263.
Zhang TY, Sun JS, Zhang LB, Shen JL, Xu WH, 2004a. Cloning and expression of the cDNA encoding the FXPRL family of peptides and a functional analysis of their effect on breaking pupal diapause in Helicoverpa armigera. J. Insect Physiol., 50(1): 25-33.
Zhao L, Shi L, 2009. Metabolism of hydrogen peroxide in univoltine and polyvoltine strains of silkworm (Bombyx mori). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 152(4): 339-345.
Einstein R, Jordan H, Zhou W, Brenner M, Mose EG, Liggett SB, 2008. Alternative splicing of the G protein-coupled receptor superfamily in human airway smooth muscle diversifies the complement of receptors. Proc. Natl. Acad. Sci. USA, 105(13): 5230-5235.
Fan LF, Zhong YS, Lin JR, 2011. Comparisons of related enzymes activities between diapause and non-diapause silkworm eggs, Bombyx mori. Acta Entomol. Sin., 54(11): 1258-1263. [范兰芬, 钟杨生, 林健荣, 2011. 家蚕滞育卵与非滞育卵中几种关键酶活性的比较研究. 昆虫学报, 54(11): 1258-1263]
Fan Y, Sun P, Wang Y, He X, Deng X, Chen X, Zhang G, Chen X, Zhou N, 2010. The G protein-coupled receptors in the silkworm, Bombyx mori. Insect Biochem. Molec. Biol., 40(8): 581-591.
Filmore D, 2004. It’s a GPCR world. Mod. Drug Discov., 7(11): 24-28.
Fukuda S, 1951. The production of the diapause eggs by transplanting the suboesophageal ganglion in the silkworm. Proc. Jpn. Acad., 27: 672-677.
Fukuda S, 1952. Function of the pupal brain and suboesophageal ganglion in the production of non-diapause and diapause eggs in the silkworm. Annot. Zool. Japon., 25: 149-155.
Gan L, Liang JB, Liu XL, He NJ, 2010. Neuropeptide gene screening and mature peptide prediction in the silkworm, Bombyx mori. Acta Entomol. Sin., 53(1): 9-19. [甘玲, 梁九波, 刘喜龙, 何宁佳, 2010. 家蚕神经肽基因的筛查及成熟肽的预测. 昆虫学报, 53(1): 9-19]
Gkouvitsas T, Kontogiannatos D, Kourti A, 2009. Cognate HSP70 gene is induced during deep larval diapause in the moth Sesamia nonagrioides. Insect Mol. Biol., 18(2): 253-264.
Grenier AM, Rocha MD, Jalabert A, Royer C, Mauchamp B, Chavancy G, 2004. Artificial parthenogenesis and control of voltinism to manage transgenic populations in Bombyx mori. J. Insect Physiol., 50(8): 751-760.
Gu YY, Hua RS, Zhou NM, Shi LG, 2008. Cloning and quantitative analysis of diapause hormone receptor gene in the silkworm, Bombyx mori. Acta Sericol. Sin., 34(3): 417-423. [顾燕燕, 华荣胜, 周耐明, 时连根, 2008. 家蚕滞育激素受体基因(BmDHR)的分子克隆及定量分析. 蚕业科学, 34(3): 417-423]
Hare JD, 1983. Seasonal variation in plant-insect associations: utilization of Solanum dulcamara by Leptinotarsa decemlineata. Ecology, 64(2): 345-361.
Hasegawa K, 1957. The diapause hormone of the silkworm, Bombyx mori. Nature, 179(4573): 1300-1301.
Hasegawa K, 1963. Studies on the mode of action of the diapause hormone in the silkworm, Bombyx mori. I. The action of diapause hormone injected into pupae of different ages. J. Exp. Biol., 40: 517-530.
Hodek I, Kostál V, 1997. Photoperiodism and control of summer diapause in the Mediterranean tiger moth Cymbalophora pudica. J. Insect Physiol., 43(8): 767-777.
Hökfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M, 2000. Neuropeptides-an overview. Neuropharmacology, 39(8): 1337-1356.
Homma T, Watanabe K, Tsurumaru S, Kataoka H, Imai K, Kamba M, Niimi T, Yamashita O, Yaginuma T, 2006. G protein-coupled receptor for diapause hormone, an inducer of Bombyx embryonic diapause. Biochem. Biophys. Res. Commun., 344(1): 386-393.
Huang JT, 2003. Studies on the molecular mechanism of diapause in the silkworm, Bombyx mori. Acta sericol. Sin., 29(1): 1-6. [黄君霆, 2003. 家蚕滞育分子机制的研究. 蚕业科学, 29(1): 1-6]
Isobe M, Hasegawa K, Goto T, 1973. Isolation of the diapause hormone from the silkworm, Bombyx mori. J. Insect Physiol., 19(6): 1221-1239.
Isobe M, Hasegawa K, Goto T, 1975. Further characterization of the silkworm diapause hormone A. J. Insect Physiol., 21(12): 1917-1920.
Jiang MX, Xie LQ, Zhang XX, 1999. Characteristics of diapause induction of cotton bollworm. Chin. J. Appl. Ecol., 10(1): 60-62. [蒋明星, 谢立群, 张孝羲, 1999. 棉铃虫的滞育诱导特性. 应用生态学报, 10(1): 60-62]
Jiang X, Yang JW, Shen ZF, Chen YJ, Shi LG, Zhou NM, 2016. Agonist-mediated activation of Bombyx mori diapause hormone receptor signals to extracellular signal-regulated kinases 1 and 2 through Gq-PLC-PKC-dependent cascade. Insect Biochem. Molec. Biol., 75: 78-88.
Kitagawa N, Shiomi K, Imai K, Niimi T, Yaginuma T, Yamashita O, 2005a. Establishment of a sandwich ELISA system to detect diapause hormone, and developmental profile of hormone levels in egg and subesophageal ganglion of the silkworm, Bombyx mori. Zool. Sci., 22(2): 213-221.
Kitagawa N, Shiomi K, Imai K, Yamashita O, Yaginuma T, 2005b. Diapause hormone levels in subesophageal ganglia of uni-, bi- and poly-voltine races during pupal-adult development of Bombyx mori, and the effects of ouabain, an inhibitor of Na+-K+ ATPase, on the hormone levels. J. Insect Biotech. Sericol., 74(2): 57-62.
Kobayashi N, Takahashi M, Kihara S, Niimi T, Yamashita O, Yaginuma T, 2014. Cloning of cDNA encoding a Bombyx mori homolog of human oxidation resistance 1 (OXR1) protein from diapause eggs, and analyses of its expression and function. J. Insect Physiol., 68(3): 58-68.
Lee HJ, Wall B, Chen S, 2008. G-protein-coupled receptors and melanoma. Pigment Cell Melanoma Res., 21(4): 415-428.
Lee JM, Hull JJ, Kawai T, Goto C, Kurihara M, Tanokura M, Nagata K, Nagasawa H, Matsumoto S, 2012. Re-evaluation of the PBAN receptor molecule: characterization of PBANR variants expressed in the pheromone glands of moths. Front. Endocrinol., 3: 6.
Lee REJr, Denlinger DL, 1991. Insects at Low Temperature. Springer, New York. 119-121.
Li XT, Shi LG, 2016. Progress in functions and underlying signal transduction mechanisms of neuropeptides and their receptors in the silkworm Bombyx mori. Acta Entomol. Sin., 59(7): 759-766. [李晓童, 时连根, 2016. 家蚕神经肽及其受体的功能和信号转导机制研究进展. 昆虫学报, 59(7): 759-766]
Liu L, He LF, Liu H, Yan R, 2010. Research progress of insects diapause. J. Anhui Agric. Sci., 38(14): 7409-7411. [刘流, 贺莉芳, 刘晖, 晏容, 2010. 昆虫滞育的研究进展. 安徽农业科学, 38(14): 7409-7411]
Majumdar S, Grinnell S, Le Rouzic V, Burgman M, Polikar L, Ansonoff M, Pintar J, Pan YX, Pasternak GW, 2011. Truncated G protein-coupled mu opioid receptor MOR-1 splice variants are targets for highly potent opioid analgesics lacking side effects. Proc. Natl. Acad. Sci. USA, 108(49): 19778-19783.
Makka T, Sonobe H, 2000. Ecdysone metabolism in diapause eggs and non-diapause eggs of the silkworm, Bombyx mori. Zool. Sci., 17(1): 89-95.
Markovic D, Challiss RA, 2009. Alternative splicing of G protein-coupled receptors: physiology and pathophysiology. Cell. Mol. Life Sci., 66(20): 3337-3352.
Morita A, Niimi T, Yamashita O, 2003. Physiological differentiation of DH-PBAN-producing neurosecretory cells in the silkworm embryo. J. Insect Physiol., 49(12): 1093-1102.
Niimi T, Yamashita O, Yaginuma T, 1992. Activity of NAD-sorbitol dehydrogenase is caused by biosynthesis of enzyme protein in diapause and non-diapause eggs of the silkworm, Bombyx mori. Comp. Biochem. Physiol. B, 103(3): 657-661.
Niimi T, Yamashita O, Yaginuma T, 1993. A cold-inducible Bombyx gene encoding a protein similar to mammalian sorbitol dehydrogenase. Yolk nuclei-dependent gene expression in diapause eggs. Eur. J. Biochem., 213(3): 1125-1131.
Numata H, Hidaka T, 1982. Photoperiodic control of adult diapause in the bean bug Riptortus clavatus Thunberg (Heteroptera: Coreidae). I. Reversible induction and termination of diapause. Appl. Entomol. Zool., 17(4): 530-538.
Saito H, Takeuchi Y, Takeda R, Hayashi Y, Watanabe K, Shin M, Imai K, Isobe M, Yamashita O, 1994. The core and complementary sequence responsible for biological activity of the diapause hormone of the silkworm, Bombyx mori. Peptides, 15(7): 1173-1178.
Sasibhushan S, Rao CGP, Ponnuvel KM, 2013. Genome wide microarray based expression profiles during early embryogenesis in diapause induced and non-diapause eggs of polyvoltine silkworm Bombyx mori. Genomics, 102(4): 379-387.
Sato Y, Oguchi M, Menjo N, Imai K, Saito H, Ikeda M, Isobe M, Yamashita O, 1993. Precursor polyprotein for multiple neuropeptides secreted from the suboesophageal ganglion of the silkworm Bombyx mori: characterization of the cDNA encoding the diapause hormone precursor and identification of additional peptides. Proc. Natl. Acad. Sci. USA, 90(8): 3251-3255.
Saunders DS, 2010. Under-sized larvae from short-day adults of the blow fly, Calliphora vicina, side-step the diapause programme. Physiol. Entomol., 22(3): 249-255.
Shen Z, Jiang X, Yan L, Chen Y, Wang W, Shi Y, Shi L, Liu D, Zhou N, 2018. Structural basis for the interaction of diapause hormone with its receptor in the silkworm, Bombyx mori. FASEB J., 32(3): 1338-1353.
Shi LG, 2004. Studies of Sericulture. China Agricultural Scientech Press, Beijing. 570-572. [时连根, 2004. 蚕学研究. 北京: 中国农业科学技术出版社. 570-572]
Sun JS, Zhang TY, Zhang QR, Xu WH, 2003. Effect of the brain and suboesophageal ganglion on pupal development in Helicoverpa armigera through regulation of FXPRLamide neuropeptides. Regul. Pep., 116(1-3): 163-171.
Tauber MJ, Tauber CA, 1973. Seasonal regulation of dormancy in Chrysopa carnea (Neuroptera). J. Insect Physiol., 19(7): 1455-1463.
Tauber MJ, Tauber CA, Masaki S, 1986. Seasonal Adaptations of Insects. Oxford University Press, New York. 37-106.
Trzaskowski B, Latek D, Yuan S, Ghoshdastider U, Debinski A, Filipek S, 2012. Action of molecular switches in GPCRs-theoretical and experimental studies. Curr. Med. Chem., 19(8): 1090-1109.
Veenstra JA, Khammassi H, 2017. Rudimentary expression of RYamide in Drosophila melanogaster relative to other Drosophila species points to a functional decline of this neuropeptide gene. Insect Biochem. Molec. Biol., 83: 68-79.
Wang JE, Liu J, 2009. Research progress of insect trehalase. Guizhou Agr. Sci., 37(4): 88-90. [王军娥, 刘静, 2009. 昆虫海藻糖酶的研究进展. 贵州农业科学, 37(4): 88-90]
Wang LG, 2011. Analysis of Structure, Expression and Function of Bombyx mori Diapause Receptor Gene. MSc Thesis, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu. [王力刚, 2011. 家蚕滞育激素受体基因的结构和表达特性及功能分析. 江苏镇江: 江苏科技大学硕士学位论文]
Wang LG, Song HT, Huang Y, Wang SP, Tang SM, Zhao QL, Shen XJ, 2011. Influence of incubation temperature on expression of diapause hormone receptor genes in bivoltine Bombyx mori variety and structural features of the gene. Acta Sericol. Sin., 37(2): 215-223. [王力刚, 宋海韬, 黄勇, 汪生鹏, 唐顺明, 赵巧玲, 沈兴家, 2011. 催青温度对家蚕二化性品种滞育激素受体基因表达的影响及基因的结构特征. 蚕业科学, 37(2): 215-223]
Wang M, Li Z, 2004. The research advance of insect diapause. J. Nanjing For. Univ. (Nat. Sci. Ed.), 28(1): 71-76. [王满囷, 李周直, 2004. 昆虫滞育的研究进展. 南京林业大学学报(自然科学版), 28(1): 71-76]
Williams CM, 1952. Physiology of insect diapause IV. The brain and prothoracic glands as an endocrine system in the cecropia silkworm. Biol. Bull., 103(1): 120-138.
Wu DY, Xiang ZH, Toshihara F, 2002. Influence of synthetic diapause hormone on carbohydrate metabolism in silkworm eggs. Acta Sericol. Sin., 28(2): 99-103. [吴大洋, 向仲怀, 古泽寿治, 2002. 合成滞育激素对家蚕卵碳水化合物代谢的影响. 蚕业科学, 28(2): 99-103]
Xie LQ, Jiang MX, Zhang XX, 1997. Studies on the diapause characteristics of oriental tabacco budworm. Acta Phyptohyl. Sin., 24(3): 199-203. [谢立群, 蒋明星, 张孝羲, 1997. 烟青虫滞育特性的研究. 植物保护学报, 24(3): 199-203]
Xu WH, 1998. The regulation of the DH-PBAN gene expression in Bombyx mori. Chin. J. Biochem. Mol. Biol., 14(5): 557-561. [徐卫华, 1998. 家蚕滞育激素-性信息素合成激活肽基因表达的调节. 中国生物化学与分子生物学报, 14(5): 557-561]
Xu WH, 1999a. Advances in insect diapause studies. Acta Entomol. Sin., 42(1): 100-107. [徐卫华, 1999a. 昆虫滞育研究进展. 昆虫学报, 42(1): 100-107]
Xu WH, 1999b. Molecular mechanism of diapause in Bombyx mori. 2. Diapause determination and expression of diapause hormone gene in pupal stage. Acta Genet. Sin., 26(2): 107-111. [徐卫华, 1999b. 家蚕滞育的分子机理. 2. 蛹期滞育激素的表达与滞育决定. 遗传学报, 26(2): 107-111]
Xu WH, 2008. Advances in insect diapause studies. Chin. Bull. Entomol., 45(4): 512-517. [徐卫华, 2008. 昆虫滞育研究进展. 昆虫知识, 45(4): 512-517]
Xu WH, Sato Y, Ikeda M, Yamashita O, 1995. Molecular characterization of the gene encoding the precursor protein of diapause hormone and pheromone biosynthesis activating neuropeptide (DH-PBAN) of the silkworm, Bombyx mori and its distribution in some insects. Biochim. Biophys. Acta, 1261(1): 83-89.
Xu WH, Yamashita O, 1996. Expression of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide during post-embryonic development in the silkworm, Bombyx mori. Acta Biochim. Biophys. Sin., 28(2): 214-217. [徐卫华, 山下兴亚, 1996. 家蚕滞育激素-性信息素合成激活肽基因的表达. 生物化学与生物物理学报, 28(2): 214-217]
Xu WH, Yukihiro S, Yamashita O, 1995. Cloning of the diapause hormone gene of the silkworm (Bombyx mori). Acta Genet. Sin., 22(3): 178-184. [徐卫华, 佐藤行洋, 山下兴亚, 1995. 家蚕滞育激素基因的克隆. 遗传学报, 22(3): 178-184]
Xu WH, Zhang Y, Wang Y, Ding L, Liu J, 1998. Molecular mechanism of diapause in insect (I). Expression of diapause hormone gene and incubation temperature in embryonic stage of Bombyx mori. Sci. China Life Sci., 41(3): 344-350.
Yaginuma T, Kobayashi M, Yamashita O, 1990. Distinct effects of different low temperatures on the induction of NAD-sorbitol dehydrogenase activity in diapause eggs of the silkworm, Bombyx mori. J. Comp. Physiol. B, 160(3): 277-285.
Yamanaka N, Yamamoto S, Zitnan D, Watanabe K, Kawada T, Satake H, Kaneko Y, Hiruma K, Tanaka Y, Shinoda T, Kataoka H, 2008. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE, 3(8): e3048.
Yamashita O, 1995. Diapause hormone of the silkworm, Bombyx mori: structure, gene expression and function. J. Insect Physiol., 42(7): 669-679.
Yamashita O, Hasegawa K, 1970. Oöcyte age sensitive to the diapause hormone from the standpoint of glycogen synthesis in the silkworm, Bombyx mori. J. Insect Physiol., 16(12): 2377-2383.
Yamashita O, Hasegawa K, Seki M, 1972. Effect of the diapause hormone on trehalase activity in pupal ovaries of the silkworm, Bombyx mori. Gen. Comp. Endocr., 18(3): 515-523.
Yin CM, Wang ZS, Chaw WD, 1985. Brain neurosecretory cell and ecdysiotropin activity of the non-diapausing, pre-diapausing and diapausing southwestern corn borer, Diatraea grandiosella Dyar. J. Insect Physiol., 31(8): 659, 661-663, 667.
Yocum GD, 2001. Differential expression of two HSP70 transcripts in response to cold, thermoperiod, and adult diapause in the Colorado potato beetle. J. Insect Physiol., 47(10): 1139-1145.
Zhang Q, Denlinger DL, 2012. Dynamics of diapause hormone and prothoracicotropic hormone transcript expression at diapause termination in pupae of the corn earworm, Helicoverpa zea. Peptides, 34(1): 120-126.
Zhang TY, Kang L, Zhang ZF, Xu WH, 2004b. Identification of a POU factor involved in regulating the neuron-specific expression of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide in Bombyx mori. Biochem. J., 380(1): 255-263.
Zhang TY, Sun JS, Zhang LB, Shen JL, Xu WH, 2004a. Cloning and expression of the cDNA encoding the FXPRL family of peptides and a functional analysis of their effect on breaking pupal diapause in Helicoverpa armigera. J. Insect Physiol., 50(1): 25-33.
Zhao L, Shi L, 2009. Metabolism of hydrogen peroxide in univoltine and polyvoltine strains of silkworm (Bombyx mori). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 152(4): 339-345.