Camp signalling in mushroom bodies modulates temperature preference behaviour in drosophila

Camp signalling in mushroom bodies modulates temperature preference behaviour in drosophila

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ABSTRACT Homoiotherms, for example mammals, regulate their body temperature with physiological responses such as a change of metabolic rate and sweating. In contrast, the body temperature of


poikilotherms, for example _Drosophila_, is the result of heat exchange with the surrounding environment as a result of the large ratio of surface area to volume of their bodies1,2.


Accordingly, these animals must instinctively move to places with an environmental temperature as close as possible to their genetically determined desired temperature. The temperature that


_Drosophila_ instinctively prefers has a function equivalent to the ‘set point’ temperature in mammals. Although various temperature-gated TRP channels have been discovered3,4, molecular and


cellular components in _Drosophila_ brain responsible for determining the desired temperature remain unknown. We identified these components by performing a large-scale genetic screen of


temperature preference behaviour (TPB) in _Drosophila_5,6. In parallel, we mapped areas of the _Drosophila_ brain controlling TPB by targeted inactivation of neurons with tetanus toxin7 and


a potassium channel (Kir2.1)8 driven with various brain-specific GAL4s. Here we show that mushroom bodies (MBs) and the cyclic AMP–cAMP-dependent protein kinase A (cAMP–PKA) pathway are


essential for controlling TPB. Furthermore, targeted expression of cAMP–PKA pathway components in only the MB was sufficient to rescue abnormal TPB of the corresponding mutants. Preferred


temperatures were affected by the level of cAMP and PKA activity in the MBs in various PKA pathway mutants. Access through your institution Buy or subscribe This is a preview of subscription


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ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS THERMORESPONSIVE MOTOR BEHAVIOR IS


MEDIATED BY RING NEURON CIRCUITS IN THE CENTRAL COMPLEX OF _DROSOPHILA_ Article Open access 08 January 2021 G PROTEIN-COUPLED RECEPTOR-BASED THERMOSENSATION DETERMINES TEMPERATURE


ACCLIMATIZATION OF _CAENORHABDITIS ELEGANS_ Article Open access 23 February 2024 METABOLIC CONTROL OF DAILY LOCOMOTOR ACTIVITY MEDIATED BY _TACHYKININ_ IN _DROSOPHILA_ Article Open access 07


June 2021 REFERENCES * Bear, M. F., Connors, B. W. & Paradiso, M. A. Neuroscience: exploring the brain (Lippincott Williams & Wilkins, Baltimore, MD, 2001) * Zars, T. Two


thermosensors in _Drosophila_ have different behavioral functions. _J. Comp. Physiol. A_ 187, 235–242 (2001) Article  CAS  Google Scholar  * Liu, L., Yermolaieva, O., Johnson, W. A., Abboud,


F. M. & Welsh, M. J. Identification and function of thermosensory neurons in _Drosophila_ larvae. _Nature Neurosci._ 6, 267–273 (2003) Article  CAS  Google Scholar  * Rosenzweig, M. et


al. The _Drosophila_ ortholog of vertebrate _TRPA1_ regulates thermotaxis. _Genes Dev._ 19, 419–424 (2005) Article  CAS  Google Scholar  * Lee, Y. et al. Pyrexia is a new thermal transient


receptor potential channel endowing tolerance to high temperatures in _Drosophila_ melanogaster. _Nature Genet._ 37, 305–310 (2005) Article  CAS  Google Scholar  * Hong, S. T. et al.


Histamine and its receptors modulate temperature-preference behaviors in _Drosophila_ . _J. Neurosci._ 26, 7245–7256 (2006) Article  CAS  Google Scholar  * Sweeney, S. T., Broadie, K.,


Keane, J., Niemann, H. & O’Kane, C. J. Targeted expression of tetanus toxin light chain in _Drosophila_ specifically eliminates synaptic transmission and causes behavioral defects.


_Neuron_ 14, 341–351 (1995) Article  CAS  Google Scholar  * Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Altered electrical properties in _Drosophila_ neurons


developing without synaptic transmission. _J. Neurosci._ 21, 1523–1531 (2001) Article  CAS  Google Scholar  * Keene, A. C. & Waddell, S. _Drosophila_ olfactory memory: single genes to


complex neural circuits. _Nature Rev. Neurosci._ 8, 341–354 (2007) Article  CAS  Google Scholar  * Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D. & Waddell, S. Sequential use


of mushroom body neuron subsets during _Drosophila_ odor memory processing. _Neuron_ 53, 103–115 (2007) Article  CAS  Google Scholar  * Sayeed, O. & Benzer, S. Behavioral genetics of


thermosensation and hygrosensation in _Drosophila_ . _Proc. Natl Acad. Sci. USA_ 93, 6079–6084 (1996) Article  ADS  CAS  Google Scholar  * Thum, A. S. et al. Differential potencies of


effector genes in adult _Drosophila_ . _J. Comp. Neurol._ 498, 194–203 (2006) Article  CAS  Google Scholar  * Rister, J. & Heisenberg, M. Distinct functions of neuronal synaptobrevin in


developing and mature fly photoreceptors. _J. Neurobiol._ 66, 1271–1284 (2006) Article  CAS  Google Scholar  * de Belle, J. S. & Heisenberg, M. Expression of _Drosophila_ mushroom body


mutations in alternative genetic backgrounds: a case study of the _mushroom body miniature_ gene (_mbm_). _Proc. Natl Acad. Sci. USA_ 93, 9875–9880 (1996) Article  ADS  CAS  Google Scholar 


* Davis, R. L. Olfactory memory formation in _Drosophila_: from molecular to systems neuroscience. _Annu. Rev. Neurosci._ 28, 275–302 (2005) Article  CAS  Google Scholar  * Skoulakis, E. M.


& Grammenoudi, S. Dunces and da Vincis: the genetics of learning and memory in _Drosophila_ . _Cell. Mol. Life Sci._ 63, 975–988 (2006) Article  CAS  Google Scholar  * Levin, L. R. et


al. The _Drosophila_ learning and memory gene _rutabaga_ encodes a Ca2+/calmodulin-responsive adenylyl cyclase. _Cell_ 68, 479–489 (1992) Article  CAS  Google Scholar  * Davis, R. L. &


Kiger, J. A. Dunce mutants of _Drosophila melanogaster_: mutants defective in the cyclic AMP phosphodiesterase enzyme system. _J. Cell Biol._ 90, 101–107 (1981) Article  CAS  Google Scholar


  * Ferris, J., Ge, H., Liu, L. & Roman, G. Go signaling is required for _Drosophila_ associative learning. _Nature Neurosci._ 9, 1036–1040 (2006) Article  CAS  Google Scholar  * Zars,


T., Fischer, M., Schulz, R. & Heisenberg, M. Localization of a short-term memory in _Drosophila_ . _Science_ 288, 672–675 (2000) Article  ADS  CAS  Google Scholar  * Isabel, G., Pascual,


A. & Preat, T. Exclusive consolidated memory phases in _Drosophila_ . _Science_ 304, 1024–1027 (2004) Article  ADS  CAS  Google Scholar  * Rodan, A. R., Kiger, J. A. & Heberlein, U.


Functional dissection of neuroanatomical loci regulating ethanol sensitivity in _Drosophila_ . _J. Neurosci._ 22, 9490–9501 (2002) Article  CAS  Google Scholar  * McBride, S. M. et al.


Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in _Drosophila melanogaster_ . _Neuron_ 24, 967–977 (1999) Article  CAS  Google Scholar  *


Gray, J. M. et al. Oxygen sensation and social feeding mediated by a _C. elegans_ guanylate cyclase homologue. _Nature_ 430, 317–322 (2004) Article  ADS  CAS  Google Scholar  * Eisel, U. et


al. Tetanus toxin light chain expression in Sertoli cells of transgenic mice causes alterations of the _actin_ cytoskeleton and disrupts spermatogenesis. _EMBO J._ 12, 3365–3372 (1993)


Article  CAS  Google Scholar  * McGuire, S. E., Roman, G. & Davis, R. L. Gene expression systems in _Drosophila_: a synthesis of time and space. _Trends Genet._ 20, 384–391 (2004)


Article  CAS  Google Scholar  * Riemensperger, T., Voller, T., Stock, P., Buchner, E. & Fiala, A. Punishment prediction by dopaminergic neurons in _Drosophila_ . _Curr. Biol._ 15,


1953–1960 (2005) Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS We thank D. Stafford for help in manuscript preparation. This work was supported by grants from the Brain


Research Center of the 21st Century Frontier Program funded by the Korean Ministry of Science and Technology and a grant from the Science Research Center (SRC) for Functional Cellulomics of


the Korea Science and Engineering Foundation (KOSEF). AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Biological Sciences, Korea Advanced Institute of Science & Technology,


Guseong-Dong, Yusong-Gu, Daejeon, 305-701, Korea, Sung-Tae Hong, Sunhoe Bang, Seogang Hyun, Jongkyun Kang, Kyunghwa Jeong, Donggi Paik, Jongkyeong Chung & Jaeseob Kim Authors * Sung-Tae


Hong View author publications You can also search for this author inPubMed Google Scholar * Sunhoe Bang View author publications You can also search for this author inPubMed Google Scholar *


Seogang Hyun View author publications You can also search for this author inPubMed Google Scholar * Jongkyun Kang View author publications You can also search for this author inPubMed 


Google Scholar * Kyunghwa Jeong View author publications You can also search for this author inPubMed Google Scholar * Donggi Paik View author publications You can also search for this


author inPubMed Google Scholar * Jongkyeong Chung View author publications You can also search for this author inPubMed Google Scholar * Jaeseob Kim View author publications You can also


search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Jaeseob Kim. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION The file contains Supplementary Figures


S1-S15 and Legends; Supplementary Tables S1-S7 (Statistical analysis on TPBs); Supplementary Results and Discussion (Mainly describe TPB genetic screen and involvement of other brain parts


except MB in TPB control), and additional references. (PDF 4613 kb) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Hong, ST., Bang, S., Hyun, S. _et


al._ cAMP signalling in mushroom bodies modulates temperature preference behaviour in _Drosophila_. _Nature_ 454, 771–775 (2008). https://doi.org/10.1038/nature07090 Download citation *


Received: 04 February 2008 * Accepted: 15 May 2008 * Published: 29 June 2008 * Issue Date: 07 August 2008 * DOI: https://doi.org/10.1038/nature07090 SHARE THIS ARTICLE Anyone you share the


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