二化螟体内生物胺受体的药理学与生理学研究
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摘要
昆虫体内的生物胺,主要包括章鱼胺(octopamine, OA)、酪胺(tyramine, TA)(?)口多巴胺(dopamine, DA)等。它们在昆虫体内扮演着各种重要的生理角色,协同或各自调控着昆虫的多种行为和生理过程,如影响昆虫的产卵、昼夜节律、嗅觉、抉择、相变、好斗和飞翔以及学习和记忆等。三者的合成底物都是氨基酸酪氨酸,且酪胺是章鱼胺的合成前体。在昆虫体内,它们主要是通过结合各自特异性的G蛋白偶联受体来发挥作用。由于昆虫体内的生物胺受体一直被视为杀虫剂的潜在作用靶标,近年来,对昆虫体内生物胺,尤其是其对应受体的药理学性质和生理学功能研究日益受到关注。有鉴于此,本研究以水稻生产上的重要害虫二化螟Chilo suppressalis(鳞翅目Lepidoptera:草螟科Crambidae)为研究对象,采用分子生物学等手段对其体内的章鱼胺受体(octopamine receptors, OARs),酪胺受体(tyramine receptos, TARs)和多巴胺受体(dopamine receptors, DARs)的药理学与生理学功能做了系统研究。
1. CsOAl受体调控细胞免疫的研究
本研究探索了章鱼胺对昆虫细胞免疫影响的分子机制(第二信使系统)。章鱼胺在低浓度时(<10-6M)能够提高二化螟幼虫血细胞的延展和吞噬能力,然而在高浓度(>10-5M)时却抑制血细胞的延展和吞噬反应。相应的,章鱼胺刺激血细胞能够偶联胞内两种不同的信号通路,钙离子(Ca2+)和环腺昔酸(cAMP)。在低浓度章鱼胺刺激血细胞时,其仅能提高胞内Ca2+浓度,而在高浓度章鱼胺刺激血细胞时,其既能引起Ca2+上升,又能引起胞内cAMP升高。我们在血细胞上克隆到1型章鱼胺受体(CsOA1),通过原位杂交和免疫荧光等实验技术确定其mRNA和受体蛋白表达于二化螟血细胞上。将其异源表达于HEK-293细胞后,与章鱼胺对血细胞所引起的反应类似,CsOA1也展示出了不同浓度章鱼胺刺激可偶联两种信号通路的特性。因此,本实验支持了以前的研究,章鱼胺对昆虫先天免疫反应的激活或抑制和其胞内浓度有很大的关系。我们的结果也揭示出章鱼胺很有可能是通过结合于血细胞膜上的CsOA1受体进而偶联不同信号通路来发挥免疫功能的。生物应激反应时所产生的激素对其免疫系统有着复杂的作用,本研究所得的结果可为肾上腺素及其受体是如何参与调控脊椎动物免疫反应的研究提供参考。
2. CsOA2B2受体的药理学与生理学研究
从二化螟体内克隆得到一类2型章鱼胺受体(CsOA2B2),该基因与果蝇体内的CG6989(DmOA2B2)基因同源。表达谱分析表明,该基因主要表达于二化螟幼虫神经组织中。将其表达于HEK-293细胞后,在受到章鱼胺刺激时,该受体能够偶联Gs蛋白引起胞内cAMP的上升,EC50值为2.33nM,在章鱼胺浓度为100nM时所引起的cAMP反应最大。药理学实验表明,激动剂中naphazoline特异性大于clonidine;拮抗剂中phentolamine,mianserin和chlorpromazine能够显著拮抗章鱼胺的激动效果。用这3种拮抗剂对二化螟幼虫进行活体药理学干扰后,进行行为测定的数据表明,经mianserin和phentolamine处理的幼虫运动能力显著下降。
3.一种新型章鱼胺受体CsOA3的功能研究
从二化螟体内克隆得到一类孤儿受体,生物信息学分析表明其与果蝇体内的CG18208基因同源,可能属于生物胺受体家族成员。该基因通过可变剪切可产生两个剪切体,CsOA3S和CsOA3L。CsOA3L在内膜3区处比CsOA3S多了30个氨基酸,该区域可能参与了受体与G蛋白的结合。为了研究其配体信息,偶联的下游信号通路以及药理学性质,我们分别将两种剪切体真核表达于HEK-293细胞中。实验表明,两类受体均能引起胞内Ca2+的上升,而CsOA3S受体还可被章鱼胺激活引起胞内cAMP的下降,酪胺虽也可激活此类受体但特异性没有章鱼胺高。药理学实验表明,CsOA3受体可被多种激动剂激活,包括有机氮类杀虫剂杀虫脒和双甲脒等,而拮抗剂中唯有phentolamine和epinastine具有显著的拮抗效果。定量PCR实验表明,该基因主要以短剪切体CsOA3S的形式出现,并且广泛表达于各类受测组织中,其中在神经节和马氏管中表达量最高。据我们所知,CsOA3是一类新型的章鱼胺受体。
4. CsTyR1受体的药理学研究
从二化螟内获得一个全长cDNA,序列分析表明,其为昆虫TyR1受体家族,将其命名为CsTyR1。CsTyR1基因表达于各组织中,包括血细胞,脂肪体,中肠,马氏管,神经节和表皮,而在神经节中的表达量是其它组织的16-80倍。我们将构建的CsTyR1真核表达质粒转染于HEK-293细胞中,对其功能和药理学特性做了系统研究。结果表明,酪胺和章鱼胺能够显著降低forskolin诱导的cAMP含量,并且存在剂量效应反应(酪胺,ECso=369nM；章鱼胺,EC50=978nM).结果表明,该类受体主要是偶联Gi蛋白引起胞内cAMP的下降。在受测的激动剂中,CsTyR1可被clonidine和双甲脒激活而不能被naphazoline和杀虫脒激活。拮抗剂中,酪胺的作用可被10μM的yohimbine,phentolamine和chlorpromazine所阻断。
5. CsTyR2受体的药理学研究
克隆到编码CsTyR2受体的基因全长,序列分析表明其与果蝇和家蚕体内克隆到的2型酪胺受体同源。组织分布研究发现,其主要表达于二化螟幼虫的神经节和马氏管中。将该基因表达于HEK-293细胞所做的功能试验表明,其特异性的被酪胺激活后引起胞内Ca2+的上升,EC50值约为20nM。而另3种生物胺,章鱼胺,多巴胺和5-羟色胺在10μM浓度下刺激该受体也未见有Ca2+反应,表明该类受体是特异性的酪胺受体,且偶联G。蛋白引起胞内Ca2+上升。所测定的4种激动剂,双甲脒、杀虫脒、clonidine和naphazoline在10μM浓度下均不能有效刺激该受体,表明该类受体与之前的章鱼胺和酪胺受体在药理学上差异甚大。
6. D1-like和D2-like多巴胺受体的药理学研究
从二化螟体内克隆得到3种多巴胺受体,分别命名为CsDOP1, CsDOP2和CsDOP3,其中CsDOP1和CsDOP3获得了全长序列。序列分析表明,CsDOP1和CsDOP2属于昆虫D1-like受体家族,偶联Gs蛋白引起胞内cAMP的上升,CsDOP3属于昆虫D2-like受体家族,偶联Gi蛋白引起胞内cAMP的降低。将CsDOP1和CsDOP3受体分别表达于HEK-293细胞后,对它们的药理学性质做了研究,多巴胺对两受体的激活都有明显的剂量效应(CsDOP1, EC50=20nM; CsDOP3, EC50=670nM)。我们测定了一系列的激动剂和拮抗剂对CsDOP1和CsDOP3受体的影响。CsDOP1中,激动剂效能大小顺序为6,7-ADTN>多巴胺>bromocriptine>pramipexole;而受测的拮抗剂中,有拮抗效果的拮抗剂,其效能大小顺序为,SCH23390>butaclamol>chlorpromazine>phentolamine>yohimbine>propranolol> ketanserin>flupenthixol>mianserin; CsDOP3不但偶联的信号通路与CsDOP1截然相反,它们之间的药理学性质也差异较大,激动剂bromocriptine(EC50=280nM)的效能大于多巴胺,而拮抗剂中epinastine=mianserin>SCH23390=chlorpromazine,其它4种拮抗剂,flupenthixol, propranolol, spiperone和butaclamol均未有显著拮抗效果。
本研究从二化螟体内克隆得到3种章鱼胺受体,2种酪胺受体和3种多巴胺受体,系统性的研究了这些受体的药理学性质及其参与调控昆虫先天免疫及运动行为的分子机制。
The biogenic amines, octopamine, tyramine and dopamine regulate many essential processes in insects, such as egg-laying, circadian rhythm, olfactory, decision-making, phase transition, fight and flight, learning and memory. They are products of the amino acid tyrosine and tyramine is the biological precursor of octopamine. All of them are independent neurotransmitters, exert their effects by binding to specific receptor proteins that belong to the superfamily of G-protein-coupled receptors. Because these receptors have been recognized as very suitable and specific insecticide and acaricide targets, the studies of octopamine, tyramine and dopamine in insects, especially the studies about their receptors, have been paid more attentions in recent years. In this study, we chose the rice striped stem borer, Chilo suppressalis Walker (Lepidoptera: Crambidae), one of the main herbivorous pests that cause serious damage to rice production in Asia, as object. Using modern molecular biology methods, we investigated the pharmacological properties and physiological roles of octopamine receptors, tyramine receptors and dopamine receptors in the rice striped stem borer.
1. Characterization of an a-adrenergic-like octopamine receptor from the rice stem borer(Chilo suppressalis) and its potential role involved in insect cellular immunity
Octopamine, the insect equivalent of norepinephrine, links the nervous system and immune system in insects. This study examines the underlying molecular mechanisms (i.e. second messenger systems) mediating octopamine effects on insect immune cells. At low concentrations (<1μM), octopamine stimulated hemocyte spreading and phagocytosis in the larval Lepidopteran (caterpillar) Chilo suppressalis, whereas at high concentrations (>10μM), octopamine inhibited hemocyte spreading and phagocytosis. Similarly, octopamine concentration had differential effects on two intracellular signaling pathways, Ca2+and cAMP. Low concentrations of octopamine increased intracellular Ca2+, but only high concentrations of octopamine (>1μM) led to an increase in both Ca2+and cAMP. We identified an a-adrenergic-like octopamine receptor in this species (CsOA1) and confirmed that it is expressed in hemocytes. After heterologous expression in HEK-293cells, the CsOAl receptor produced the same octopamine concentration-dependent responses on intracellular Ca2+and cAMP as had been observed in hemocytes. These findings support earlier work showing that octopamine has both stimulatory and suppressive effects on immune responses, depending on the octopamine concentration. Our evidence suggests that these biphasic effects are mediated by an octopamine receptor signaling through intracellular Ca2+and cAMP second messenger pathways. Stress hormones/neuromodulators have complex effects on immune function in animals across phyla. This complexity may be mediated, in part, by conserved connections between adrenergic-like G-coupled-protein receptors and second messenger systems.
2. Characterization of a P-adrenergic-like octopamine receptor from the rice stem borer (Chilo suppressalis)
Octopamine, the invertebrate counterpart of adrenaline and noradrenaline, plays a key role in regulation of many physiological and behavioral processes in insects. It modulates these functions through binding to specific octopamine receptors, which are typical rhodopsin-like G-protein-coupled receptors. A cDNA encoding a seven-transmembrane receptor was cloned from the nerve cord of the rice stem borer, Chilo suppressalis, viz. CsOA2B2, which shares high sequence similarity to CG6989, a Drosophila β-adrenergic-like octopamine receptor (DmOctβ2R). We generated an HEK-293cell line that stably expresses CsOA2B2in order to examine the functional and pharmacological properties of this receptor. Activation of CsOA2B2by octopamine increased the production of cAMP in a dose-dependent manner (EC50=2.33×10-9M), with a maximum response at100nM. Tyramine also activated the receptor but with much less potency than octopamine. Dopamine and serotonin had marginal effects on cAMP production. Using a series of known agonists and antagonists for octopamine receptors, we observed a rather unique pharmacological profile for CsOA2B2through measurements of cAMP. The rank order of potency of the agonists was naphazoline> clonidine. The activated effect of octopamine is abolished by co-incubation with phentolamine, mianserin or chlorpromazine. Using in vivo pharmacology, CsOA2B2antagonists mianserin and phentolamine impaired the motor ability of individual rice stem borers. The results of the present study are important for a better functional understanding of this receptor as well as for practical applications in the development of environmentally sustainable pesticides.
3. Two splicing variants of a novel family of octopamine receptors with different signaling properties
The octopamine and tyramine, as the invertebrate counterparts of the vertebrate adrenergic transmitters, control, regulate, and modulate many physiological and behavioral processes. Both compounds mediate their effects by binding to specific receptors belonging to the superfamily of G-protein-coupled receptors. Activation of different receptor types is coupled with different second messenger pathways. Here we described the functional characterization of one octopamine receptor gene from Chilo suppressails. As a result of alternative splicing, this octopamine receptor gene (CsOA3) encodes two molecularly distinct isoforms, CsOA3S and CsOA3L. CsOA3L differs from CsOA3S by the presence of an additional30amino acids within the third intracellular loop. This region is implicated in the receptor interaction with G-proteins. When heterologously expressed, both receptors cause increases of intracellular Ca2+concentration in response to applying nanomolar concentrations of octopamine. The short form, CsOA3S, was activated by both octopamine and tyramine, resulting in decreased intracellular cAMP levels ([cAMP]i) in a dose-dependent manner (EC50～39nM, octopamine;～94nM, tyamine). Tyramine activated the receptor but much lesser potency than octopamine, whereas dopamine and serotonin are not-effective. While CsOA3L did not show this properties. Tissues distribution pattern of CsOA3genes were assessed by qRT-PCR. Overlapping but not identical expression patterns were observed for the individual transcrpts. The CsOA3is, to our knowledge, a new family of insect octopamine receptors.
4. Molecular cloning and pharmacological characterisation of a tyramine receptor from the rice stem borer, Chilo suppressalis (Walker)
A full-length cDNA (designated CsTyR1) from the rice stem borer, Chilo suppressalis (Walker), has been obtained through homology cloning in combination with rapid amplification of cDNA ends/polymerase chain reaction (RACE-PCR). The mRNA of CsTyR1is present in various tissues, including hemocytes, fat body, midgut, Malpighian tubules, nerve cord and epidermis, and it is found predominantly in the larval nerve cord with16-80-fold enrichment compared with other tissues. The authors generated a HEK-293cell line stably expressing CsTyRl in order to examine functional and pharmacological properties of this receptor. Both TA and OA at0.01-100μM can reduce forskolin-stimulated intracellular cAMP levels in a dose-dependent manner (TA, EC50=369nm; OA, EC50=978nm). In agonist assays, activation of CsTyR1by clonidine and amitraz but not by naphazoline and chlordimeform can also significantly inhibit forskolin-stimulated cAMP production. The inhibitory effect of TA at10μM is eliminated by coincubation with yohimbine, phentolamine or chlorpromazine (each10μM).
5. Cloning, expression and functional analysis of a tyramine receptor type2from striped stem borer, Chilo suppressalis
Biogenic amines such as octopamine, tyramine, dopamine and serotonin play various important physiological roles in insects by activating distinct G-protein-coupled receptors (GPCRs) that share a putative seven transmembrane domain structure. Here, we report the first cloning and pharmacological characterization of a tyramine receptor type2in the striped stem borer, Chilo suppressalis, viz., CsTyR2, which shares high sequence similarity to members of the invertebrate tyramine receptor family. The CsTyR2receptor was stably expressed in HEK-293cells, and its ligand response has been examined. Receptor activation with TA induced a dose-dependent increase in intracellular Ca2+concentration ([Ca2+]i) in cells, with an EC50value of20nM, whereas octopamine, dopamine and serotonin increased ([Ca2+]i) only at concentrations above100μM. The mRNA is present in various tissues including hemocytes, fatbody, midgut, Malpighian tubules, nerve cord and epidermis in the larva stage. The CsTyR2transcript was detected predominantly in the Malpighian tubules and nerve cord. This expression plasticity indicates that CsTyR2might be involved in excretory system and nervous system in C. suppressalis. This study marks the first comprehensive molecular, pharmacological, and functional characterization of a tyramine receptor in the rice stem borer.
6. Molecular and pharmacological characterization of dopamine receptors in the rice stem borer, Chilo suppressalis
We identified two full (CsDOP1and CsDOP3) and one partial (CsDOP2) sequences of putative dopamine receptors in the rice stem borer Chilo suppressalis. The genes CsDOP1and CsDOP2were predicted as orthologs of previously characterized D1-like dopamine receptors in the silkworm Bombyx mori and fruitfly Dmsophila melanogaster. CsDOP3shows high sequence homology with other D2-like dopamine receptors. Heterologous expression of CsDOP1and CsDOP3in HEK-293cells demonstrated dose-dependent responses to dopamine (EC50:CsDOP1=2.0±0.19×10-8M; CsDOP3=6.7±0.58×10-7M). Experiments with agonists and antagonists revealed that the rank order of potency for the active synthetic agonists and antagonists tested was different for each of the receptors (CsDOP1:agonists,6,7-ADTN> dopamine> bromocriptine> pramipexole; antagonists, SCH23390>butaclamol>chlorpromazine>phentolamine> yohimbine>propranolol>ketanserin>flupenthixol> mianserin; CsDOP3:agonists, bromocriptine>DA; antagonists, epinastine=mianserin> SCH23390=chlorpromazine).
In this study, we have cloned three octopamine receptors, two tyramine receptors and three dopamine receptors from the rice stem borer, Chilo suppressalis. And we have investigated the pharmacological properties and physiological roles related to innate immunity and motor ability in insects of these receptors.
1. CsOAl受体调控细胞免疫的研究
本研究探索了章鱼胺对昆虫细胞免疫影响的分子机制(第二信使系统)。章鱼胺在低浓度时(<10-6M)能够提高二化螟幼虫血细胞的延展和吞噬能力,然而在高浓度(>10-5M)时却抑制血细胞的延展和吞噬反应。相应的,章鱼胺刺激血细胞能够偶联胞内两种不同的信号通路,钙离子(Ca2+)和环腺昔酸(cAMP)。在低浓度章鱼胺刺激血细胞时,其仅能提高胞内Ca2+浓度,而在高浓度章鱼胺刺激血细胞时,其既能引起Ca2+上升,又能引起胞内cAMP升高。我们在血细胞上克隆到1型章鱼胺受体(CsOA1),通过原位杂交和免疫荧光等实验技术确定其mRNA和受体蛋白表达于二化螟血细胞上。将其异源表达于HEK-293细胞后,与章鱼胺对血细胞所引起的反应类似,CsOA1也展示出了不同浓度章鱼胺刺激可偶联两种信号通路的特性。因此,本实验支持了以前的研究,章鱼胺对昆虫先天免疫反应的激活或抑制和其胞内浓度有很大的关系。我们的结果也揭示出章鱼胺很有可能是通过结合于血细胞膜上的CsOA1受体进而偶联不同信号通路来发挥免疫功能的。生物应激反应时所产生的激素对其免疫系统有着复杂的作用,本研究所得的结果可为肾上腺素及其受体是如何参与调控脊椎动物免疫反应的研究提供参考。
2. CsOA2B2受体的药理学与生理学研究
从二化螟体内克隆得到一类2型章鱼胺受体(CsOA2B2),该基因与果蝇体内的CG6989(DmOA2B2)基因同源。表达谱分析表明,该基因主要表达于二化螟幼虫神经组织中。将其表达于HEK-293细胞后,在受到章鱼胺刺激时,该受体能够偶联Gs蛋白引起胞内cAMP的上升,EC50值为2.33nM,在章鱼胺浓度为100nM时所引起的cAMP反应最大。药理学实验表明,激动剂中naphazoline特异性大于clonidine;拮抗剂中phentolamine,mianserin和chlorpromazine能够显著拮抗章鱼胺的激动效果。用这3种拮抗剂对二化螟幼虫进行活体药理学干扰后,进行行为测定的数据表明,经mianserin和phentolamine处理的幼虫运动能力显著下降。
3.一种新型章鱼胺受体CsOA3的功能研究
从二化螟体内克隆得到一类孤儿受体,生物信息学分析表明其与果蝇体内的CG18208基因同源,可能属于生物胺受体家族成员。该基因通过可变剪切可产生两个剪切体,CsOA3S和CsOA3L。CsOA3L在内膜3区处比CsOA3S多了30个氨基酸,该区域可能参与了受体与G蛋白的结合。为了研究其配体信息,偶联的下游信号通路以及药理学性质,我们分别将两种剪切体真核表达于HEK-293细胞中。实验表明,两类受体均能引起胞内Ca2+的上升,而CsOA3S受体还可被章鱼胺激活引起胞内cAMP的下降,酪胺虽也可激活此类受体但特异性没有章鱼胺高。药理学实验表明,CsOA3受体可被多种激动剂激活,包括有机氮类杀虫剂杀虫脒和双甲脒等,而拮抗剂中唯有phentolamine和epinastine具有显著的拮抗效果。定量PCR实验表明,该基因主要以短剪切体CsOA3S的形式出现,并且广泛表达于各类受测组织中,其中在神经节和马氏管中表达量最高。据我们所知,CsOA3是一类新型的章鱼胺受体。
4. CsTyR1受体的药理学研究
从二化螟内获得一个全长cDNA,序列分析表明,其为昆虫TyR1受体家族,将其命名为CsTyR1。CsTyR1基因表达于各组织中,包括血细胞,脂肪体,中肠,马氏管,神经节和表皮,而在神经节中的表达量是其它组织的16-80倍。我们将构建的CsTyR1真核表达质粒转染于HEK-293细胞中,对其功能和药理学特性做了系统研究。结果表明,酪胺和章鱼胺能够显著降低forskolin诱导的cAMP含量,并且存在剂量效应反应(酪胺,ECso=369nM；章鱼胺,EC50=978nM).结果表明,该类受体主要是偶联Gi蛋白引起胞内cAMP的下降。在受测的激动剂中,CsTyR1可被clonidine和双甲脒激活而不能被naphazoline和杀虫脒激活。拮抗剂中,酪胺的作用可被10μM的yohimbine,phentolamine和chlorpromazine所阻断。
5. CsTyR2受体的药理学研究
克隆到编码CsTyR2受体的基因全长,序列分析表明其与果蝇和家蚕体内克隆到的2型酪胺受体同源。组织分布研究发现,其主要表达于二化螟幼虫的神经节和马氏管中。将该基因表达于HEK-293细胞所做的功能试验表明,其特异性的被酪胺激活后引起胞内Ca2+的上升,EC50值约为20nM。而另3种生物胺,章鱼胺,多巴胺和5-羟色胺在10μM浓度下刺激该受体也未见有Ca2+反应,表明该类受体是特异性的酪胺受体,且偶联G。蛋白引起胞内Ca2+上升。所测定的4种激动剂,双甲脒、杀虫脒、clonidine和naphazoline在10μM浓度下均不能有效刺激该受体,表明该类受体与之前的章鱼胺和酪胺受体在药理学上差异甚大。
6. D1-like和D2-like多巴胺受体的药理学研究
从二化螟体内克隆得到3种多巴胺受体,分别命名为CsDOP1, CsDOP2和CsDOP3,其中CsDOP1和CsDOP3获得了全长序列。序列分析表明,CsDOP1和CsDOP2属于昆虫D1-like受体家族,偶联Gs蛋白引起胞内cAMP的上升,CsDOP3属于昆虫D2-like受体家族,偶联Gi蛋白引起胞内cAMP的降低。将CsDOP1和CsDOP3受体分别表达于HEK-293细胞后,对它们的药理学性质做了研究,多巴胺对两受体的激活都有明显的剂量效应(CsDOP1, EC50=20nM; CsDOP3, EC50=670nM)。我们测定了一系列的激动剂和拮抗剂对CsDOP1和CsDOP3受体的影响。CsDOP1中,激动剂效能大小顺序为6,7-ADTN>多巴胺>bromocriptine>pramipexole;而受测的拮抗剂中,有拮抗效果的拮抗剂,其效能大小顺序为,SCH23390>butaclamol>chlorpromazine>phentolamine>yohimbine>propranolol> ketanserin>flupenthixol>mianserin; CsDOP3不但偶联的信号通路与CsDOP1截然相反,它们之间的药理学性质也差异较大,激动剂bromocriptine(EC50=280nM)的效能大于多巴胺,而拮抗剂中epinastine=mianserin>SCH23390=chlorpromazine,其它4种拮抗剂,flupenthixol, propranolol, spiperone和butaclamol均未有显著拮抗效果。
本研究从二化螟体内克隆得到3种章鱼胺受体,2种酪胺受体和3种多巴胺受体,系统性的研究了这些受体的药理学性质及其参与调控昆虫先天免疫及运动行为的分子机制。
The biogenic amines, octopamine, tyramine and dopamine regulate many essential processes in insects, such as egg-laying, circadian rhythm, olfactory, decision-making, phase transition, fight and flight, learning and memory. They are products of the amino acid tyrosine and tyramine is the biological precursor of octopamine. All of them are independent neurotransmitters, exert their effects by binding to specific receptor proteins that belong to the superfamily of G-protein-coupled receptors. Because these receptors have been recognized as very suitable and specific insecticide and acaricide targets, the studies of octopamine, tyramine and dopamine in insects, especially the studies about their receptors, have been paid more attentions in recent years. In this study, we chose the rice striped stem borer, Chilo suppressalis Walker (Lepidoptera: Crambidae), one of the main herbivorous pests that cause serious damage to rice production in Asia, as object. Using modern molecular biology methods, we investigated the pharmacological properties and physiological roles of octopamine receptors, tyramine receptors and dopamine receptors in the rice striped stem borer.
1. Characterization of an a-adrenergic-like octopamine receptor from the rice stem borer(Chilo suppressalis) and its potential role involved in insect cellular immunity
Octopamine, the insect equivalent of norepinephrine, links the nervous system and immune system in insects. This study examines the underlying molecular mechanisms (i.e. second messenger systems) mediating octopamine effects on insect immune cells. At low concentrations (<1μM), octopamine stimulated hemocyte spreading and phagocytosis in the larval Lepidopteran (caterpillar) Chilo suppressalis, whereas at high concentrations (>10μM), octopamine inhibited hemocyte spreading and phagocytosis. Similarly, octopamine concentration had differential effects on two intracellular signaling pathways, Ca2+and cAMP. Low concentrations of octopamine increased intracellular Ca2+, but only high concentrations of octopamine (>1μM) led to an increase in both Ca2+and cAMP. We identified an a-adrenergic-like octopamine receptor in this species (CsOA1) and confirmed that it is expressed in hemocytes. After heterologous expression in HEK-293cells, the CsOAl receptor produced the same octopamine concentration-dependent responses on intracellular Ca2+and cAMP as had been observed in hemocytes. These findings support earlier work showing that octopamine has both stimulatory and suppressive effects on immune responses, depending on the octopamine concentration. Our evidence suggests that these biphasic effects are mediated by an octopamine receptor signaling through intracellular Ca2+and cAMP second messenger pathways. Stress hormones/neuromodulators have complex effects on immune function in animals across phyla. This complexity may be mediated, in part, by conserved connections between adrenergic-like G-coupled-protein receptors and second messenger systems.
2. Characterization of a P-adrenergic-like octopamine receptor from the rice stem borer (Chilo suppressalis)
Octopamine, the invertebrate counterpart of adrenaline and noradrenaline, plays a key role in regulation of many physiological and behavioral processes in insects. It modulates these functions through binding to specific octopamine receptors, which are typical rhodopsin-like G-protein-coupled receptors. A cDNA encoding a seven-transmembrane receptor was cloned from the nerve cord of the rice stem borer, Chilo suppressalis, viz. CsOA2B2, which shares high sequence similarity to CG6989, a Drosophila β-adrenergic-like octopamine receptor (DmOctβ2R). We generated an HEK-293cell line that stably expresses CsOA2B2in order to examine the functional and pharmacological properties of this receptor. Activation of CsOA2B2by octopamine increased the production of cAMP in a dose-dependent manner (EC50=2.33×10-9M), with a maximum response at100nM. Tyramine also activated the receptor but with much less potency than octopamine. Dopamine and serotonin had marginal effects on cAMP production. Using a series of known agonists and antagonists for octopamine receptors, we observed a rather unique pharmacological profile for CsOA2B2through measurements of cAMP. The rank order of potency of the agonists was naphazoline> clonidine. The activated effect of octopamine is abolished by co-incubation with phentolamine, mianserin or chlorpromazine. Using in vivo pharmacology, CsOA2B2antagonists mianserin and phentolamine impaired the motor ability of individual rice stem borers. The results of the present study are important for a better functional understanding of this receptor as well as for practical applications in the development of environmentally sustainable pesticides.
3. Two splicing variants of a novel family of octopamine receptors with different signaling properties
The octopamine and tyramine, as the invertebrate counterparts of the vertebrate adrenergic transmitters, control, regulate, and modulate many physiological and behavioral processes. Both compounds mediate their effects by binding to specific receptors belonging to the superfamily of G-protein-coupled receptors. Activation of different receptor types is coupled with different second messenger pathways. Here we described the functional characterization of one octopamine receptor gene from Chilo suppressails. As a result of alternative splicing, this octopamine receptor gene (CsOA3) encodes two molecularly distinct isoforms, CsOA3S and CsOA3L. CsOA3L differs from CsOA3S by the presence of an additional30amino acids within the third intracellular loop. This region is implicated in the receptor interaction with G-proteins. When heterologously expressed, both receptors cause increases of intracellular Ca2+concentration in response to applying nanomolar concentrations of octopamine. The short form, CsOA3S, was activated by both octopamine and tyramine, resulting in decreased intracellular cAMP levels ([cAMP]i) in a dose-dependent manner (EC50～39nM, octopamine;～94nM, tyamine). Tyramine activated the receptor but much lesser potency than octopamine, whereas dopamine and serotonin are not-effective. While CsOA3L did not show this properties. Tissues distribution pattern of CsOA3genes were assessed by qRT-PCR. Overlapping but not identical expression patterns were observed for the individual transcrpts. The CsOA3is, to our knowledge, a new family of insect octopamine receptors.
4. Molecular cloning and pharmacological characterisation of a tyramine receptor from the rice stem borer, Chilo suppressalis (Walker)
A full-length cDNA (designated CsTyR1) from the rice stem borer, Chilo suppressalis (Walker), has been obtained through homology cloning in combination with rapid amplification of cDNA ends/polymerase chain reaction (RACE-PCR). The mRNA of CsTyR1is present in various tissues, including hemocytes, fat body, midgut, Malpighian tubules, nerve cord and epidermis, and it is found predominantly in the larval nerve cord with16-80-fold enrichment compared with other tissues. The authors generated a HEK-293cell line stably expressing CsTyRl in order to examine functional and pharmacological properties of this receptor. Both TA and OA at0.01-100μM can reduce forskolin-stimulated intracellular cAMP levels in a dose-dependent manner (TA, EC50=369nm; OA, EC50=978nm). In agonist assays, activation of CsTyR1by clonidine and amitraz but not by naphazoline and chlordimeform can also significantly inhibit forskolin-stimulated cAMP production. The inhibitory effect of TA at10μM is eliminated by coincubation with yohimbine, phentolamine or chlorpromazine (each10μM).
5. Cloning, expression and functional analysis of a tyramine receptor type2from striped stem borer, Chilo suppressalis
Biogenic amines such as octopamine, tyramine, dopamine and serotonin play various important physiological roles in insects by activating distinct G-protein-coupled receptors (GPCRs) that share a putative seven transmembrane domain structure. Here, we report the first cloning and pharmacological characterization of a tyramine receptor type2in the striped stem borer, Chilo suppressalis, viz., CsTyR2, which shares high sequence similarity to members of the invertebrate tyramine receptor family. The CsTyR2receptor was stably expressed in HEK-293cells, and its ligand response has been examined. Receptor activation with TA induced a dose-dependent increase in intracellular Ca2+concentration ([Ca2+]i) in cells, with an EC50value of20nM, whereas octopamine, dopamine and serotonin increased ([Ca2+]i) only at concentrations above100μM. The mRNA is present in various tissues including hemocytes, fatbody, midgut, Malpighian tubules, nerve cord and epidermis in the larva stage. The CsTyR2transcript was detected predominantly in the Malpighian tubules and nerve cord. This expression plasticity indicates that CsTyR2might be involved in excretory system and nervous system in C. suppressalis. This study marks the first comprehensive molecular, pharmacological, and functional characterization of a tyramine receptor in the rice stem borer.
6. Molecular and pharmacological characterization of dopamine receptors in the rice stem borer, Chilo suppressalis
We identified two full (CsDOP1and CsDOP3) and one partial (CsDOP2) sequences of putative dopamine receptors in the rice stem borer Chilo suppressalis. The genes CsDOP1and CsDOP2were predicted as orthologs of previously characterized D1-like dopamine receptors in the silkworm Bombyx mori and fruitfly Dmsophila melanogaster. CsDOP3shows high sequence homology with other D2-like dopamine receptors. Heterologous expression of CsDOP1and CsDOP3in HEK-293cells demonstrated dose-dependent responses to dopamine (EC50:CsDOP1=2.0±0.19×10-8M; CsDOP3=6.7±0.58×10-7M). Experiments with agonists and antagonists revealed that the rank order of potency for the active synthetic agonists and antagonists tested was different for each of the receptors (CsDOP1:agonists,6,7-ADTN> dopamine> bromocriptine> pramipexole; antagonists, SCH23390>butaclamol>chlorpromazine>phentolamine> yohimbine>propranolol>ketanserin>flupenthixol> mianserin; CsDOP3:agonists, bromocriptine>DA; antagonists, epinastine=mianserin> SCH23390=chlorpromazine).
In this study, we have cloned three octopamine receptors, two tyramine receptors and three dopamine receptors from the rice stem borer, Chilo suppressalis. And we have investigated the pharmacological properties and physiological roles related to innate immunity and motor ability in insects of these receptors.
引文
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