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Journal of Integrative Agriculture  2024, Vol. 23 Issue (02): 605-620    DOI: 10.1016/j.jia.2023.07.016
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The role of cAMP-dependent protein kinase A in the formation of long-term memory in Bactrocera dorsalis

Jinxin Yu1*, Yanmin Hui1*, Jiayi He1*, Yinghao Yu1, Zhengbing Wang2, Siquan Ling3, Wei Wang1, Xinnian Zeng1#, Jiali Liu1#

1 National Key Laboratory of Green Pesticides/Guangdong Engineering Research Center for Insect Behavior Regulation/College of Plant Protection, South China Agricultural University, Guangzhou 510642, China

2 College of Life Science and Agronomy, Zhoukou Normal University, Zhoukou 466001, China

3 Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, China

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摘要  

环磷酸腺苷(cyclic AMP,cAMP)依赖的蛋白激酶Aprotein kinase A,PKA)信号通路一直被认为是长期记忆(long-term Memory,LTM)形成的关键。先前的研究大多基于PKA信号在多次间隔训练诱导的LTM中的作用,而对单次训练诱导的LTM的研究较少。本研究通过行为药理学、酶联免疫吸附测定(enzyme linked immunosorbent assay,ELISA)和RNA干扰实验,究了PKA信号通路在农业害虫小实蝇LTM形成中的作用。小实蝇具有较强的记忆能力,在训练试验中也能形成持续两天的长期记忆。研究结果发现,在条件训练前阻断或激活PKA,两种处理方式均影响桔小实蝇间隔训练形成的LTM,但不会影响训练形成的LTM通过ELISA以及沉默蛋白激酶调节亚基2和催化亚基1的进一步证实了这一结论。综上所述,激活PKA有助于诱导多次间隔训练形成的LTM,而训练形成的LTM并不受其影响。这一发现挑战了PKA信号在LTM形成中的保守作用,这为跨物种LTM形成的分子机制多样性以及可能的功能和进化意义提供了基础。



Abstract  

The cAMP-dependent protein kinase A (PKA) signaling pathway has long been considered critical for long-term memory (LTM) formation.  Previous studies have mostly focused on the role of PKA signaling in LTM induction by multiple spaced conditioning with less attention to LTM induction by a single conditioning.  Here, we conducted behavioral-pharmacology, enzyme immunoassay and RNA interference experiments to study the role of the PKA signaling pathway in LTM formation in the agricultural pest Bactrocera dorsalis, which has a strong memory capacity allowing it to form a two-day memory even from a single conditioning trial.  We found that either blocking or activating PKA prior to conditioning pretreatment affected multiple spaced LTM, and conversely, they did not affect LTM formed by single conditioning.  This was further confirmed by enzyme-linked immunosorbent assay (ELISA) and silencing of the protein kinase regulatory subunit 2 and catalytic subunit 1.  Taken together, these results suggest that activating PKA during memory acquisition helps to induce the LTM formed by multiple spaced conditioning but not by a single conditioning.  Our findings challenge the conserved role of PKA signaling in LTM, which provides a basis for the greater diversity of molecular mechanisms underlying LTM formation across species, as well as possible functional and evolutionary implications.

Keywords:  Bactrocera dorsalis        LTM        multiple spaced        PKA        single   
Online: 22 February 2023   Accepted: 17 May 2023
Fund: 

This work was funded by the National Natural Science Foundation of China (32072486 and 31971424).

About author:  Jinxin Yu, E-mail: jinxinyu1994@163.com; #Correspondence Xinnian Zeng, E-mail: zengxn@scau.edu.cn; Jiali Liu, E-mail: shirley4461@scau.edu.cn *These authors contributed equally to this study.

Cite this article: 

Jinxin Yu, Yanmin Hui, Jiayi He, Yinghao Yu, Zhengbing Wang, Siquan Ling, Wei Wang, Xinnian Zeng, Jiali Liu. 2024.

The role of cAMP-dependent protein kinase A in the formation of long-term memory in Bactrocera dorsalis . Journal of Integrative Agriculture, 23(02): 605-620.

Abel T, Nguyen P V, Barad M, Deuel T A, Kandel E R, Bourtchouladze R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell, 88, 615–626.

Amaral I M, Lemos C, Cera I, Dechant G, Hofer A, El Rawas R. 2020. Involvement of camp-dependent protein kinase in the nucleus accumbens in cocaine versus social interaction reward. International Journal of Molecular Sciences, 22, 345.

Blum A L, Li W, Cressy M, Dubnau J. 2009. Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Current Biology, 19, 1341–1350.

Chen M B, Jiang X, Quake S R, Südhof T C. 2020. Persistent transcriptional programmes are associated with remote memory. Nature, 587, 437–442.

Chen M L, Zhang S X, Guo P Y, Qin Q S, Meng L W, Yuan G R, Wang J J. 2023. Identification and characterization of UDP-glycosyltransferase genes and the potential role in response to insecticides exposure in Bactrocera dorsalis. Pest Management Science, 79, 666–677.

Choi K M, Cho S H, Kim J H, Kim A R L, Kong X, Yoon J C. 2023. CFTR regulates brown adipocyte thermogenesis via the cAMP/PKA signaling pathway. Journal of Cystic Fibrosis, 22, 132–139.

Clarke A R, Leach P, Measham P F. 2022. The fallacy of year-round breeding in polyphagous tropical fruit flies (Diptera: Tephritidae): Evidence for a seasonal reproductive arrestment in Bactrocera Species. Insects, 13, 882.

Copf T, Kamara M, Venkatesh T. 2019. Axon length maintenance and synapse integrity are regulated by cAMP-dependent protein kinase A (PKA) during larval growth of the Drosophila sensory neurons. Journal of Neurogenetics, 33, 157–163.

Davis R L. 2011. Traces of Drosophila memory. Neuron, 70, 8–19.

Fan Y, Zhang C, Qin Y, Yin X, Dong X, Desneux N, Zhou H. 2022. Monitoring the methyl eugenol response and non-responsiveness mechanisms in oriental fruit fly Bactrocera dorsalis in China. Insects, 13, 1004.

Fiala A, Müller U, Menzel R. 1999. Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. Journal of Neuroscience, 19, 10125–10134.

Giese K P, Mizuno K. 2013. The roles of protein kinases in learning and memory. Learning & Memory, 20, 540–552.

Happ J T, Arveseth C D, Bruystens J, Bertinetti D, Nelson I B, Olivieri C, Zhang J, Hedeen D S, Zhu J F, Capener J L. 2022. A PKA inhibitor motif within SMOOTHENED controls Hedgehog signal transduction. Nature Structural & Molecular Biology, 29, 990–999.

Hart A K, Fioravante D, Liu R Y, Phares G A, Cleary L J, Byrne J H. 2011. Serotonin-mediated synapsin expression is necessary for long-term facilitation of the Aplysia sensorimotor synapse. Journal of Neuroscience, 31, 18401–18411.

He Y, Xu Y, Chen X. 2023. Biology, ecology and management of tephritid fruit flies in China: A review. Insects, 14, 196.

Horiuchi J, Yamazaki D, Naganos S, Aigaki T, Saitoe M. 2008. Protein kinase A inhibits a consolidated form of memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 105, 20976–20981.

Hosono S, Matsumoto Y, Mizunami M. 2016. Interaction of inhibitory and facilitatory effects of conditioning trials on long-term memory formation. Learning & Memory, 23, 669–678.

Kandel E R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science, 294, 1030–1038.

Kandel E R, Dudai Y, Mayford M R. 2014. The molecular and systems biology of memory. Cell, 157, 163–186.

Kim S M, Zhang S, Park J, Sung H J, Tran T D T, Chung C, Han I O. 2021. REM sleep deprivation impairs learning and memory by decreasing brain O-GlcNAc cycling in mouse. Neurotherapeutics, 18, 2504–2517.

Krashes M J, Waddell S. 2008. Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. Journal of Neuroscience, 28, 3103–3113.

Kutlu M G, Gould T J. 2016. Nicotinic modulation of hippocampal cell signaling and associated effects on learning and memory. Physiology & Behavior, 155, 162–171.

Leboulle G, Müller U. 2004. Synergistic activation of insect cAMP-dependent protein kinase A (type II) by cyclicAMP and cyclicGMP. FEBS Letters, 576, 216–220.

Lee D. 2015. Global and local missions of cAMP signaling in neural plasticity, learning, and memory. Frontiers in Pharmacology, 6, 161.

Li H, Huang X, Yang Y, Chen X, Yang Y, Wang J, Jiang H. 2022. The short neuropeptide F receptor regulates olfaction-mediated foraging behavior in the oriental fruit fly Bactrocera dorsalis (Hendel). Insect Biochemistry and Molecular Biology, 140, 103697.

Liu J L, Chen X Y, Zeng X N. 2015. Classical olfactory conditioning in the oriental fruit fly, Bactrocera dorsalis. PLoS ONE, 10, e0122155.

Liu R Y, Fioravante D, Shah S, Byrne J H. 2008. cAMP response element-binding protein 1 feedback loop is necessary for consolidation of long-term synaptic facilitation in Aplysia. Journal of Neuroscience, 28, 1970–1976.

Liu Z, Xie Q P, Guo H W, Xu W, Wang J J. 2022. An odorant binding protein mediates Bactrocera dorsalis olfactory sensitivity to host plant volatiles and male attractant compounds. International Journal of Biological Macromolecules, 219, 538–544.

Lonze B E, Ginty D D. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron, 35, 605–623.

Lu Y, Zhao Z, Cai X, Cui L, Zhang H, Xiao H, Li Z, Zhang L, Zeng J. 2017. Progresses on integrated pest management (IPM) of agricultural insect pests in China. Chinese Journal of Applied Entomology, 54, 349–363. (in Chinese)

Martin K C, Michael D, Rose J C, Barad M, Casadio A, Zhu H, Kandel E R. 1997. MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron, 18, 899–912.

Massengill C I, Day Cooney J, Mao T, Zhong H. 2021. Genetically encoded sensors towards imaging cAMP and PKA activity in vivo. Journal of Neuroscience Methods, 362, 109298.

Matsumoto Y. 2022. Learning and memory in the cricket Gryllus bimaculatus. Physiological Entomology, 47, 147–161.

Matsumoto Y, Matsumoto C S, Mizunami M. 2018. Signaling pathways for long-term memory formation in the cricket. Frontiers in Psychology, 9, 1014.

Matsumoto Y, Menzel R, Sandoz J C, Giurfa M. 2012. Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: A step toward standardized procedures. Journal of Neuroscience Methods, 211, 159–167.

Matsumoto Y, Mizunami M. 2002. Temporal determinants of long-term retention of olfactory memory in the cricket Gryllus bimaculatus. Journal of Experimental Biology, 205, 1429–1437.

Matsumoto Y, Sandoz J C, Devaud J M, Lormant F, Mizunami M, Giurfa M. 2014. Cyclic nucleotide-gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee. Learning & Memory, 21, 272–286.

Matsumoto Y, Unoki S, Aonuma H, Mizunami M. 2006. Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory. Learning & Memory, 13, 35–44.

Matsushita M, Tomizawa K, Moriwaki A, Li S T, Terada H, Matsui H. 2001. A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. Journal of Neuroscience, 21, 6000–6007.

McGuire S E, Deshazer M, Davis R L. 2005. Thirty years of olfactory learning and memory research in Drosophila melanogaster. Progress in Neurobiology, 76, 328–347.

Menzel R, Manz G, Menzel R, Greggers U. 2001. Massed and spaced learning in honeybees: The role of CS, US, the intertrial interval, and the test interval. Learning & Memory, 8, 198–208.

Milner B, Squire L R, Kandel E R. 1998. Cognitive neuroscience and the study of memory. Neuron, 20, 445–468.

Mizunami M, Nemoto Y, Terao K, Hamanaka Y, Matsumoto Y. 2014. Roles of calcium/calmodulin-dependent kinase II in long-term memory formation in crickets. PLoS ONE, 9, e107442.

Müller U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron, 27, 159–168.

Müller U. 2012. The molecular signalling processes underlying olfactory learning and memory formation in honeybees. Apidologie, 43, 322–333.

Müßig L, Richlitzki A, Rößler R, Eisenhardt D, Menzel R, Leboulle G. 2010. Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. Journal of Neuroscience, 30, 7817–7825.

Naqib F, Sossin W S, Farah C A. 2012. Molecular determinants of the spacing effect. Neural Plasticity, 2012, 581291.

Nguyen P V, Abel T, Kandel E R. 1994. Requirement of a critical period of transcription for induction of a late phase of LTP. Science, 265, 1104–1107.

Nguyen P V, Kandel E R. 1997. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learning & Memory, 4, 230–243.

Pagani M R, Oishi K, Gelb B D, Zhong Y. 2009. The phosphatase SHP2 regulates the spacing effect for long-term memory induction. Cell, 139, 186–198.

Philips G T, Tzvetkova E I, Carew T J. 2007. Transient mitogen-activated protein kinase activation is confined to a narrow temporal window required for the induction of two-trial long-term memory in Aplysia. Journal of Neuroscience, 27, 13701–13705.

Prickaerts J, de Vente J, Honig W, Steinbusch H W, Blokland A. 2002. cGMP, but not cAMP, in rat hippocampus is involved in early stages of object memory consolidation. European Journal of Pharmacology, 436, 83–87.

Qin Y J, Krosch M N, Schutze M K, Zhang Y, Wang X X, Prabhakar C S, Susanto A, Hee A K, Ekesi S, Badji K. 2018. Population structure of a global agricultural invasive pest, Bactrocera dorsalis (Diptera: Tephritidae). Evolutionary Applications, 11, 1990–2003.

Quevedo J, Vianna M R, Martins M R, Barichello T, Medina J H, Roesler R, Izquierdo I. 2004. Protein synthesis, PKA, and MAP kinase are differentially involved in short-and long-term memory in rats. Behavioural Brain Research, 154, 339–343.

Rieche F, Carmine-Simmen K, Poeck B, Kretzschmar D, Strauss R. 2018. Drosophila full-length amyloid precursor protein is required for visual working memory and prevents age-related memory impairment. Current Biology, 28, 817–823.

Riveros A J, Entler B V, Seid M A. 2021. Stimulus-dependent learning and memory in the neotropical ant Ectatomma ruidum. Journal of Experimental Biology, 224, jeb238535.

Silva A J, Kogan J H, Frankland P W, Kida S. 1998. CREB and memory. Annual Review of Neuroscience, 21, 127–148.

Skeberdis V A, Chevaleyre V, Lau C G, Goldberg J H, Pettit D L, Suadicani S O, Lin Y, Bennett M V, Yuste R, Castillo P E. 2006. Protein kinase A regulates calcium permeability of NMDA receptors. Nature Neuroscience, 9, 501–510.

Smid H M, Vet L E. 2016. The complexity of learning, memory and neural processes in an evolutionary ecological context. Current Opinion in Insect Science, 15, 61–69.

Smid H M, Wang G, Bukovinszky T, Steidle J L, Bleeker M A, van Loon J J, Vet L E. 2007. Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proceedings of the Royal Society (B: Biological Sciences), 274, 1539–1546.

Smolen P, Zhang Y, Byrne J H. 2016. The right time to learn: mechanisms and optimization of spaced learning. Nature Reviews Neuroscience, 17, 77–88.

Sutton M A, Ide J, Masters S E, Carew T J. 2002. Interaction between amount and pattern of training in the induction of intermediate-and long-term memory for sensitization in Aplysia. Learning & Memory, 9, 29–40.

Sweatt J D. 2009. Mechanisms of Memory. Academic Press, London. pp. 105–126.

Tully T, Preat T, Boynton S, Del Vecchio M. 1994. Genetic dissection of consolidated memory in Drosophila. Cell, 79, 35–47.

Turrel O, Rabah Y, Plaçais P Y, Goguel V, Preat T. 2020. Drosophila middle-term memory: Amnesiac is required for PKA activation in the mushroom bodies, a function modulated by neprilysin 1. Journal of Neuroscience, 40, 4219–4229.

Upadhya S C, Smith T K, Hegde A N. 2004. Ubiquitin‐proteasome‐mediated CREB repressor degradation during induction of long-term facilitation. Journal of Neurochemistry, 91, 210–219.

Vagnoni A, Bullock S L. 2018. A cAMP/PKA/Kinesin-1 axis promotes the axonal transport of mitochondria in aging Drosophila neurons. Current Biology, 28, 1265–1272.

Villar M E, Marchal P, Viola H, Giurfa M. 2020. Redefining single-trial memories in the honeybee. Cell Reports, 30, 2603–2613.

Vossler M R, Yao H, York R D, Pan M G, Rim C S, Stork P J. 1997. cAMP activates MAP kinase and Elk-1 through a B-Raf-and Rap1-dependent pathway. Cell, 89, 73–82.

Wu Y B, Yang W J, Xie Y F, Xu K K, Tian Y, Yuan G R, Wang J J. 2016. Molecular characterization and functional analysis of BdFoxO gene in the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Gene, 578, 219–224.

Yang B, Liu Y, Wang B, Wang G. 2020. Olfaction-based behaviorally manipulated technology of pest insects research progress, opportunities and challenges. Bulletin of National Natural Science Foundation of China, 34, 441–446. (in Chinese)

Yin J, Del Vecchio M, Zhou H, Tully T. 1995. CREB as a memory modulator: Induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell, 81, 107–115.

Yu J, Yang W, Lin T, Zeng X, Liu J. 2020. Unequal rewarding of three metabolizable sugars - sucrose, fructose and glucose - in olfactory learning and memory in Bactrocera dorsalis. Journal of Experimental Biology, 223, jeb225219.

Yu J, Yang W, Zeng X, Liu J. 2019. The oriental fruit fly Bactrocera dorsalis learns and remembers sugar quality. Journal of Insect Physiology, 117, 103895.

Yu J X, Hui Y M, Xue J A, Qu J B, Ling S Q, Wang W, Zeng X N, Liu J L. 2022a. Formation characteristics of long‐term memory in Bactrocera dorsalis. Insect Science, 30, 829–843.

Yu J X, Xiang Q, Qu J B, Hui Y M, Lin T, Zeng X N, Liu J L. 2022b. Octopaminergic neurons function in appetitive but not aversive olfactory learning and memory in Bactrocera dorsalis. Insect Science, 29, 1747–1760.

Zeng Y, Reddy G V, Li Z, Qin Y, Wang Y, Pan X, Jiang F, Gao F, Zhao Z H. 2019. Global distribution and invasion pattern of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Journal of Applied Entomology, 143, 165–176.

Zhang Y, Liu R Y, Heberton G A, Smolen P, Baxter D A, Cleary L J, Byrne J H. 2012. Computational design of enhanced learning protocols. Nature Neuroscience, 15, 294–297.

Zhao B, Sun J, Zhang X, Mo H, Niu Y, Li Q, Wang L, Zhong Y. 2019. Long-term memory is formed immediately without the need for protein synthesis-dependent consolidation in Drosophila. Nature Communications, 10, 4550.

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