莲草直胸跳甲胰岛素样生长因子系统相关基因IGFALS和IMP3的表达模式
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摘要
莲草直胸跳甲Agasicles hygrophila是恶性入侵杂草空心莲子草Alternanthera philoxeroides的专食性天敌。为阐明该跳甲生殖调控的分子机制,筛选其卵巢转录组数据得到3个胰岛素样生长因子系统相关基因,分别为胰岛素样生长因子酸不稳定亚基(IGFALS)和其亚型X1 (IGFALS X1)以及胰岛素样生长因子II mRNA结合蛋白3 (IMP3),利用半定量PCR方法检测3个基因在雌成虫不同发育时期的表达模式,并通过荧光定量PCR技术检测其在不同组织及不同发育时期的表达水平。结果显示,筛选到的IGFALS、IGFALS X1和IMP3基因在莲草直胸跳甲蛹期和成虫期均有表达,且3个基因在蛹期和成虫期均为全身性表达,IGFALS和IMP3 mRNA在成虫卵巢组织中表达量显著高于其他组织,峰值分别出现在成虫羽化后第5天和第1天,较蛹期第1天分别增加了3.56和3.81倍,因此推测IGFALS和IMP3基因在莲草直胸跳甲卵子发生过程中发挥重要的调控作用。
Agasicles hygrophila is a monophagous natural enemies of the malignant invasive alligatorweed Alternanthera philoxeroides. To explore the molecular mechanism of reproduction regulation of A. hygrophila, three insulin-like growth factor system related genes, namely insulin-like growth factor acid-labile subunit(IGFALS), its isoform X1(IGFALS X1) and insulin-like growth factor II mRNA binding protein 3(IMP3) were screened through bioinformatics analysis of the A.hygrophila ovarian transcriptome database generated in the laboratory. The expression pattern of three genes were detected in A. hygrophila at different developmental stages in female adults by semi-qPCR. Meanwhile, the transcript level of three genes were analyzed in A. hygrophila at different developmental stages and in various tissues by qPCR. The results showed that IGFALS、IGFALS X1 and IMP3 genes were expressed in the pupae and adult stages of A. hygrophila. And three genes were generally expressed in the pupae and adult stage of A. hygrophila. IGFALS and IMP3 mRNA were significantly higher than other tissues in adult ovarian, with the peak values appears on the fifth day and the first day of adult stages respectively, increasing by 3.56 and 3.81 times respectively compared with the first day of pupal stage. It is speculated that IGFALS and IMP3 genes play an important regulatory role in the process of oogenesis of A. hygrophila.
Agasicles hygrophila is a monophagous natural enemies of the malignant invasive alligatorweed Alternanthera philoxeroides. To explore the molecular mechanism of reproduction regulation of A. hygrophila, three insulin-like growth factor system related genes, namely insulin-like growth factor acid-labile subunit(IGFALS), its isoform X1(IGFALS X1) and insulin-like growth factor II mRNA binding protein 3(IMP3) were screened through bioinformatics analysis of the A.hygrophila ovarian transcriptome database generated in the laboratory. The expression pattern of three genes were detected in A. hygrophila at different developmental stages in female adults by semi-qPCR. Meanwhile, the transcript level of three genes were analyzed in A. hygrophila at different developmental stages and in various tissues by qPCR. The results showed that IGFALS、IGFALS X1 and IMP3 genes were expressed in the pupae and adult stages of A. hygrophila. And three genes were generally expressed in the pupae and adult stage of A. hygrophila. IGFALS and IMP3 mRNA were significantly higher than other tissues in adult ovarian, with the peak values appears on the fifth day and the first day of adult stages respectively, increasing by 3.56 and 3.81 times respectively compared with the first day of pupal stage. It is speculated that IGFALS and IMP3 genes play an important regulatory role in the process of oogenesis of A. hygrophila.
引文
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Baxter RC.Insulin-like growth factor binding proteins in the human circulation: A review [J]. Hormone Research, 1994, 42 (4-5): 140-144.
Boisclair YR, Rhoads RP, Ueki I,et al. The acid-labile subunit (ALS) of the 150 kDa IGF-binding protein complex: An important but forgotten component of the circulating IGF system [J]. Journal of Endocrinology, 2001, 170 (1): 63-70.
Boylan KLM, Mische S, Li M,et al. Motility screen identifies Drosophila IGF-II mRNA-binding protein—Zipcode-binding protein acting in oogenesis and synaptogenesis [J]. PLoS Genetics, 2008, 4 (2): e36.
Brants JR, Ayoubi TA, Chada K,et al. Differential regulation of the insulin-like growth factor II mRNA—Binding protein genes by architectural transcription factor HMGA2 [J]. Febs Letters, 2004, 569 (1): 277-283.
Cao QP, Duguay SJ, Plisetskaya E,et al. Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor l mRNA [J]. Molecular Endocrinology, 1989, 3 (12): 2005-2010.
Chen L, Cai DC, Chen Q,et al. The reproductive system and reproductive biology of the alligatorweed flea beetle, Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Acta Entomologica Sinica, 2009, 52 (11): 1255-1260. [陈磊, 蔡笃程, 陈青, 等. 莲草直胸跳甲生殖系统与繁殖特性研究 [J]. 昆虫学报, 2009, 52 (11): 1255-1260]
Colegrove-Otero LJ, Devaux A, Standart N. The Xenopus ELAV protein EIrB represses Vg1 mRNA translation during oogenesis [J]. Molecular and Cellular Biology, 2005, 25 (20): 9028-9039.
Fu JW, Gou JY, Li ZB,et al. Effects of temperature on the reproduction and egg hatching of Agasicles hygrophila (Coleoptera: Chrysomelidae), a biological control agent of the invasive alligator weed [J]. Journal of Biosafety, 2011, 20 (2): 119-123. [傅建炜, 郭建英, 李赞斌, 等. 温度对莲草直胸跳甲成虫繁殖特性和卵孵化的影响 [J]. 生物安全学报, 2011, 20 (2): 119-123]
Fu LJ, Wu ZQ, Fu ZJ. Studies on the ovary development and emergence rhythm of Agasicles hygrophila [J]. Wuyi Science Journal, 1999, 15: 74-78. [付丽君, 吴珍泉, 付志坚. 条纹叶甲羽化节律与卵巢发育进度的研究 [J]. 武夷科学, 1999, 15: 74-78]
Geng C, Macdonald PM. Imp associates with squid and Hrp48 and contributes to localized expression of gurken in the oocyte [J]. Molecular Cell Biology, 2006, 26 (24): 9508-9516.
Guler HP, Zapf J, Schmid C,et al. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates [J]. Acta Endocrinologica, 1989, 121 (6): 753-758.
Hansen TV, Hammer NA, Nielsen J,et al. Dwarfism and impaired gut development in insulin-like growth factor II mRNA-binding protein1-deficient mice [J]. Molecular of Cellular Biology, 2004, 24 (10): 4448-4464.
Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins:Biological actions [J]. Endocrine Reviews, 1995, 16 (1): 3-34.
Julien MH, Skarratt B, Maywald GF.Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila [J]. Journal of Aquatic Plant Management, 1995, 33 (4): 55-60.
LeRoith D, Werner H, Beitner-Johnson D,et al. Molecular and cellular aspects of the insulin-like growth factor I receptor [J]. Endocrine Reviews, 1995, 16 (2): 143-63.
Li C, Rock KL, Woda BA, et al. IMP3 is a novel biomarker for adenocarcinoma in situ of the uterine cervix: An immunohistochemical study in comparison with p16 INK4a expression [J]. Modern Pathology, 2007, 20 (2): 242.
Li C, Zota V, Woda BA,et al. Expression of a novel oncofetal mRNA-binding protein IMP3 in endometrial carcinomas: Diagnostic significance and clinicopathologic correlations [J]. Modern Pathology, 2007, 20 (12): 1263-1268.
Li GL, Niu LL, Liu HF, et al. Structure and function of insulin-like growth factor acid-labile subunits in mammalian homologues [J]. Hereditas, 2015, 37 (12): 1185-1193. [李贵林, 牛丽莉, 刘海峰, 等. 哺乳动物胰岛素样生长因子酸不稳定亚基的结构与功能 [J]. 遗传, 2015, 37 (12): 1185-1193]
LiaoBS, Hu Y, Herrick DJ, et al. The RNA-binding protein IMP-3 is a translational activator of insulin-like growth factor II leader-3 mRNA during proliferation of human K562 leukemia cells [J]. Journal of Biological Chemistry, 2005, 280 (18): 18517-18524.
Livak KJ, Schmittgen TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method [J]. Methods, 2001, 25 (4): 402-408.
Ma RY, Wang R. Invasive mechanism and biological control of Alternanthera philoxeroides in China [J]. Chinese Journal of Applied and Environmental Biology, 2005, 11 (2): 246-250. [马瑞燕, 王韧. 空心莲子草在中国的入侵机理及其生物防治 [J]. 应用与环境生物学报, 2005, 11 (2): 246-250]
Maddox DM, Andres LA, Hennessey RD,et al. Insects to control alligatorweed: An invader of aquatic ecosystems in the United States [J]. BioScience, 1971, 21 (19): 985-91.
Mazerbourg S, Bondy CA, Zhou J,et al. The Insulin-like growth factor system: A key determinant role in the growth and selection of ovarian follicles? A comparative species study [J]. Reproduction of Domestic Animals, 2003, 38 (4): 247-258.
Munro TP, Kwon S, Schnapp BJ,et al. A repeated IMP-binding motif controls oskar mRNA translation and anchoring independently of Drosophila melanogaster IMP [J]. Journal of Cell Biology, 2006, 172 (4): 577-588.
Philippe M, Stéphane F, Philippe M,et al. Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals [J]. Domestic Animal Endocrinology, 2002, 23 (1): 139-154.
Rechler MM.Insulin-like growth factor binding proteins [J]. Vitamins and Hormones, 1993, 47 (5): 1-114.
Takahashi K, Kotani T, Katsu Y,et al. Possible involvement of insulin-like growth factor 2 mRNA-binding protein 3 in zebrafish oocyte maturation as a novel cyclin B1 mRNA-binding protein that represses the translation in immature oocytes [J]. Biochemical and Biophysical Research Communications, 2014, 448 (1): 22-27.
Wandji SA, Gadsby JE, Simmen FA,et al. Porcine ovarian cells express messenger ribonucleic acids for the acid-labile subunit and insulin-like growth factor binding protein-3 during follicular and luteal phases of the estrous cycle [J]. Endocrinology, 2000, 141 (7): 2638-2647.
Wang R, Wang Y, Zhang GC. Host specificity test of Agasicles hygrophila [J]. Chinese Journal of Biological Control, 1988, 4 (1): 14-17. [王韧, 王远, 张格成. 空心莲子草叶甲寄主专一性测验 [J]. 生物防治通报, 1988, 4 (1): 14-17]
Werner H, Woloschak M, Stannard B,et al. Insulin-like growth factor receptor: Molecular biology, heterogeneity, and regulation. In: LeRoith D, ed. Insulin-like Growth Factors: Molecular and Cellular Aspects [C]. Boca Raton, CRC Press. 1991: 17-47.
Wu LM, Tian SY, Wang XR,et al. Biological observations of Agasicles hygrophila in Guangdong [J]. Chinese Journal of Biological Control, 2000, 16 (3): 144-145. [吴浪明, 田世尧, 王晓容, 等. 广东莲草直胸跳甲生物学的观察 [J]. 中国生物防治, 2000, 16 (3): 144-145]
Xi GS, Liang KD, Fan DH,et al. Research advances in regulatory factors of insect oogenesis [J]. Chinese Bulletin of Entomology, 2010, 47 (5): 848-855. [奚耕思, 梁开丹, 范东芬, 等. 昆虫卵子发生调控因素的研究进展 [J]. 昆虫知识, 2010, 47 (5): 848-855]
Yisraeli JK. VICKZ proteins:A multi-talented family of regulatory RNA-binding proteins [J]. Biology of the Cell, 2005, 97 (1): 87-96.
Zapf J, Hauri C, Futo E,et al. Intravenously injected insulin-like growth factor (IGF) I/IGF binding protein-3 complex exerts insulin-like effects in hypophysectomized, but not in normal rats [J]. Journal of Clinical Investigation, 1995, 95 (1): 179-186.
Zhao MT, Wang Y, Zhou ZS,et al. Effects of periodically repeated heat events on reproduction and ovary development of Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Journal of Economic Entomology, 2016, 109 (4): 1586-1594.
Zhao X, Fu JW, Wan FH,et al. Effects of brief high temperature exposure on reproductive characteristics of Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Acta Entomologica Sinica, 2009, 52 (10): 1110-1114. [赵鑫, 傅建炜, 万方浩, 等. 短时高温暴露对莲草直胸跳甲生殖特性的影响 [J]. 昆虫学报, 2009, 52 (10): 1110-1114]
Zhao Z, Xi GS. Statistical analysis of oogenesis stages and interspecific differences of four locusts from Oedipodidae [J]. Acta Zootaxonomica Sinica, 2006, 31 (3): 501-508. [赵卓, 奚耕思. 斑翅蝗科四种蝗虫卵子发生阶段及种间差异的统计分析 [J]. 动物分类学报, 2006, 31 (3): 501-508]
Zheng KD. Expression, Transcriptional Regulation and Function of Insulin-like Growth Factor Acid-labile Subunit (Igfals) in Zebrafish [D]. Chongqing: Southwest University, 2010. [郑凯迪. 斑马鱼Igfals的表达、转录调控及功能研究 [D]. 重庆: 西南大学, 2010]
Baxter RC.Insulin-like growth factor binding proteins in the human circulation: A review [J]. Hormone Research, 1994, 42 (4-5): 140-144.
Boisclair YR, Rhoads RP, Ueki I,et al. The acid-labile subunit (ALS) of the 150 kDa IGF-binding protein complex: An important but forgotten component of the circulating IGF system [J]. Journal of Endocrinology, 2001, 170 (1): 63-70.
Boylan KLM, Mische S, Li M,et al. Motility screen identifies Drosophila IGF-II mRNA-binding protein—Zipcode-binding protein acting in oogenesis and synaptogenesis [J]. PLoS Genetics, 2008, 4 (2): e36.
Brants JR, Ayoubi TA, Chada K,et al. Differential regulation of the insulin-like growth factor II mRNA—Binding protein genes by architectural transcription factor HMGA2 [J]. Febs Letters, 2004, 569 (1): 277-283.
Cao QP, Duguay SJ, Plisetskaya E,et al. Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor l mRNA [J]. Molecular Endocrinology, 1989, 3 (12): 2005-2010.
Chen L, Cai DC, Chen Q,et al. The reproductive system and reproductive biology of the alligatorweed flea beetle, Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Acta Entomologica Sinica, 2009, 52 (11): 1255-1260. [陈磊, 蔡笃程, 陈青, 等. 莲草直胸跳甲生殖系统与繁殖特性研究 [J]. 昆虫学报, 2009, 52 (11): 1255-1260]
Colegrove-Otero LJ, Devaux A, Standart N. The Xenopus ELAV protein EIrB represses Vg1 mRNA translation during oogenesis [J]. Molecular and Cellular Biology, 2005, 25 (20): 9028-9039.
Fu JW, Gou JY, Li ZB,et al. Effects of temperature on the reproduction and egg hatching of Agasicles hygrophila (Coleoptera: Chrysomelidae), a biological control agent of the invasive alligator weed [J]. Journal of Biosafety, 2011, 20 (2): 119-123. [傅建炜, 郭建英, 李赞斌, 等. 温度对莲草直胸跳甲成虫繁殖特性和卵孵化的影响 [J]. 生物安全学报, 2011, 20 (2): 119-123]
Fu LJ, Wu ZQ, Fu ZJ. Studies on the ovary development and emergence rhythm of Agasicles hygrophila [J]. Wuyi Science Journal, 1999, 15: 74-78. [付丽君, 吴珍泉, 付志坚. 条纹叶甲羽化节律与卵巢发育进度的研究 [J]. 武夷科学, 1999, 15: 74-78]
Geng C, Macdonald PM. Imp associates with squid and Hrp48 and contributes to localized expression of gurken in the oocyte [J]. Molecular Cell Biology, 2006, 26 (24): 9508-9516.
Guler HP, Zapf J, Schmid C,et al. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates [J]. Acta Endocrinologica, 1989, 121 (6): 753-758.
Hansen TV, Hammer NA, Nielsen J,et al. Dwarfism and impaired gut development in insulin-like growth factor II mRNA-binding protein1-deficient mice [J]. Molecular of Cellular Biology, 2004, 24 (10): 4448-4464.
Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins:Biological actions [J]. Endocrine Reviews, 1995, 16 (1): 3-34.
Julien MH, Skarratt B, Maywald GF.Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila [J]. Journal of Aquatic Plant Management, 1995, 33 (4): 55-60.
LeRoith D, Werner H, Beitner-Johnson D,et al. Molecular and cellular aspects of the insulin-like growth factor I receptor [J]. Endocrine Reviews, 1995, 16 (2): 143-63.
Li C, Rock KL, Woda BA, et al. IMP3 is a novel biomarker for adenocarcinoma in situ of the uterine cervix: An immunohistochemical study in comparison with p16 INK4a expression [J]. Modern Pathology, 2007, 20 (2): 242.
Li C, Zota V, Woda BA,et al. Expression of a novel oncofetal mRNA-binding protein IMP3 in endometrial carcinomas: Diagnostic significance and clinicopathologic correlations [J]. Modern Pathology, 2007, 20 (12): 1263-1268.
Li GL, Niu LL, Liu HF, et al. Structure and function of insulin-like growth factor acid-labile subunits in mammalian homologues [J]. Hereditas, 2015, 37 (12): 1185-1193. [李贵林, 牛丽莉, 刘海峰, 等. 哺乳动物胰岛素样生长因子酸不稳定亚基的结构与功能 [J]. 遗传, 2015, 37 (12): 1185-1193]
LiaoBS, Hu Y, Herrick DJ, et al. The RNA-binding protein IMP-3 is a translational activator of insulin-like growth factor II leader-3 mRNA during proliferation of human K562 leukemia cells [J]. Journal of Biological Chemistry, 2005, 280 (18): 18517-18524.
Livak KJ, Schmittgen TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method [J]. Methods, 2001, 25 (4): 402-408.
Ma RY, Wang R. Invasive mechanism and biological control of Alternanthera philoxeroides in China [J]. Chinese Journal of Applied and Environmental Biology, 2005, 11 (2): 246-250. [马瑞燕, 王韧. 空心莲子草在中国的入侵机理及其生物防治 [J]. 应用与环境生物学报, 2005, 11 (2): 246-250]
Maddox DM, Andres LA, Hennessey RD,et al. Insects to control alligatorweed: An invader of aquatic ecosystems in the United States [J]. BioScience, 1971, 21 (19): 985-91.
Mazerbourg S, Bondy CA, Zhou J,et al. The Insulin-like growth factor system: A key determinant role in the growth and selection of ovarian follicles? A comparative species study [J]. Reproduction of Domestic Animals, 2003, 38 (4): 247-258.
Munro TP, Kwon S, Schnapp BJ,et al. A repeated IMP-binding motif controls oskar mRNA translation and anchoring independently of Drosophila melanogaster IMP [J]. Journal of Cell Biology, 2006, 172 (4): 577-588.
Philippe M, Stéphane F, Philippe M,et al. Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals [J]. Domestic Animal Endocrinology, 2002, 23 (1): 139-154.
Rechler MM.Insulin-like growth factor binding proteins [J]. Vitamins and Hormones, 1993, 47 (5): 1-114.
Takahashi K, Kotani T, Katsu Y,et al. Possible involvement of insulin-like growth factor 2 mRNA-binding protein 3 in zebrafish oocyte maturation as a novel cyclin B1 mRNA-binding protein that represses the translation in immature oocytes [J]. Biochemical and Biophysical Research Communications, 2014, 448 (1): 22-27.
Wandji SA, Gadsby JE, Simmen FA,et al. Porcine ovarian cells express messenger ribonucleic acids for the acid-labile subunit and insulin-like growth factor binding protein-3 during follicular and luteal phases of the estrous cycle [J]. Endocrinology, 2000, 141 (7): 2638-2647.
Wang R, Wang Y, Zhang GC. Host specificity test of Agasicles hygrophila [J]. Chinese Journal of Biological Control, 1988, 4 (1): 14-17. [王韧, 王远, 张格成. 空心莲子草叶甲寄主专一性测验 [J]. 生物防治通报, 1988, 4 (1): 14-17]
Werner H, Woloschak M, Stannard B,et al. Insulin-like growth factor receptor: Molecular biology, heterogeneity, and regulation. In: LeRoith D, ed. Insulin-like Growth Factors: Molecular and Cellular Aspects [C]. Boca Raton, CRC Press. 1991: 17-47.
Wu LM, Tian SY, Wang XR,et al. Biological observations of Agasicles hygrophila in Guangdong [J]. Chinese Journal of Biological Control, 2000, 16 (3): 144-145. [吴浪明, 田世尧, 王晓容, 等. 广东莲草直胸跳甲生物学的观察 [J]. 中国生物防治, 2000, 16 (3): 144-145]
Xi GS, Liang KD, Fan DH,et al. Research advances in regulatory factors of insect oogenesis [J]. Chinese Bulletin of Entomology, 2010, 47 (5): 848-855. [奚耕思, 梁开丹, 范东芬, 等. 昆虫卵子发生调控因素的研究进展 [J]. 昆虫知识, 2010, 47 (5): 848-855]
Yisraeli JK. VICKZ proteins:A multi-talented family of regulatory RNA-binding proteins [J]. Biology of the Cell, 2005, 97 (1): 87-96.
Zapf J, Hauri C, Futo E,et al. Intravenously injected insulin-like growth factor (IGF) I/IGF binding protein-3 complex exerts insulin-like effects in hypophysectomized, but not in normal rats [J]. Journal of Clinical Investigation, 1995, 95 (1): 179-186.
Zhao MT, Wang Y, Zhou ZS,et al. Effects of periodically repeated heat events on reproduction and ovary development of Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Journal of Economic Entomology, 2016, 109 (4): 1586-1594.
Zhao X, Fu JW, Wan FH,et al. Effects of brief high temperature exposure on reproductive characteristics of Agasicles hygrophila (Coleoptera: Chrysomelidae) [J]. Acta Entomologica Sinica, 2009, 52 (10): 1110-1114. [赵鑫, 傅建炜, 万方浩, 等. 短时高温暴露对莲草直胸跳甲生殖特性的影响 [J]. 昆虫学报, 2009, 52 (10): 1110-1114]
Zhao Z, Xi GS. Statistical analysis of oogenesis stages and interspecific differences of four locusts from Oedipodidae [J]. Acta Zootaxonomica Sinica, 2006, 31 (3): 501-508. [赵卓, 奚耕思. 斑翅蝗科四种蝗虫卵子发生阶段及种间差异的统计分析 [J]. 动物分类学报, 2006, 31 (3): 501-508]
Zheng KD. Expression, Transcriptional Regulation and Function of Insulin-like Growth Factor Acid-labile Subunit (Igfals) in Zebrafish [D]. Chongqing: Southwest University, 2010. [郑凯迪. 斑马鱼Igfals的表达、转录调控及功能研究 [D]. 重庆: 西南大学, 2010]