The Impacts of Hypertonic Conditions on Larval Cool Cells

Overview

Journal Front Cell Neurosci

Specialty Cell Biology

Date 2024 Oct 9

PMID 39381503

Authors

Hua Bai

Trisha Naidu

James B Anderson

Hector Montemayor

Camie Do

Lina Ni

Affiliations

Soon will be listed here.

Abstract

exhibits multiple highly sophisticated temperature-sensing systems, enabling its effective response and navigation to temperature changes. Previous research has identified three dorsal organ cool cells (DOCCs) in fly larvae, consisting of two A-type and one B-type cell with distinct calcium dynamics. When subjected to hypertonic conditions, calcium imaging shows that A-type DOCCs maintain their responses to cool temperatures. In contrast, a subset of B-type DOCCs does not exhibit detectable GCaMP baseline signals, and the remaining detectable B-type DOCCs exhibit reduced temperature responses. The activation of both A-type and B-type DOCCs depends on the same members of the ionotropic receptor (IR) family: IR21a, IR93a, and IR25a. A-type DOCCs exhibit a higher somal level of IR93a than B-type DOCCs. Overexpression of restores B-type calcium responses to cool temperatures, but not the proportion of B-type cells with a detectable GCaMP baseline, in a hypertonic environment, suggesting a selective role of IR93a in maintaining the temperature responses under hypertonic conditions. Our findings identify a novel function of B-type DOCCs in integrating temperature and tonic stimuli.

References

Urso S, Lamitina T . The C. elegans Hypertonic Stress Response: Big Insights from Shrinking Worms. Cell Physiol Biochem. 2021; 55(S1):89-105. PMC: 8265315. DOI: 10.33594/000000332. View

Garrity P, Goodman M, Samuel A, Sengupta P . Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes Dev. 2010; 24(21):2365-82. PMC: 2964747. DOI: 10.1101/gad.1953710. View

Barbagallo B, Garrity P . Temperature sensation in Drosophila. Curr Opin Neurobiol. 2015; 34:8-13. PMC: 4508239. DOI: 10.1016/j.conb.2015.01.002. View

Bargmann C, Thomas J, Horvitz H . Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1990; 55:529-38. DOI: 10.1101/sqb.1990.055.01.051. View

Benton R, Vannice K, Gomez-Diaz C, Vosshall L . Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 2009; 136(1):149-62. PMC: 2709536. DOI: 10.1016/j.cell.2008.12.001. View

Rytz R, Croset V, Benton R . Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol. 2013; 43(9):888-97. DOI: 10.1016/j.ibmb.2013.02.007. View

Kang K, Panzano V, Chang E, Ni L, Dainis A, Jenkins A . Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature. 2011; 481(7379):76-80. PMC: 3272886. DOI: 10.1038/nature10715. View

Chen T, Wardill T, Sun Y, Pulver S, Renninger S, Baohan A . Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature. 2013; 499(7458):295-300. PMC: 3777791. DOI: 10.1038/nature12354. View

Lamitina S, Morrison R, Moeckel G, Strange K . Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress. Am J Physiol Cell Physiol. 2003; 286(4):C785-91. DOI: 10.1152/ajpcell.00381.2003. View

10.

Omelchenko A, Bai H, Hussain S, Tyrrell J, Klein M, Ni L . TACI: An ImageJ Plugin for 3D Calcium Imaging Analysis. J Vis Exp. 2023; (190). PMC: 10388512. DOI: 10.3791/64953. View

11.

Abuin L, Bargeton B, Ulbrich M, Isacoff E, Kellenberger S, Benton R . Functional architecture of olfactory ionotropic glutamate receptors. Neuron. 2011; 69(1):44-60. PMC: 3050028. DOI: 10.1016/j.neuron.2010.11.042. View

12.

Pfeiffer B, Truman J, Rubin G . Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci U S A. 2012; 109(17):6626-31. PMC: 3340069. DOI: 10.1073/pnas.1204520109. View

13.

Omelchenko A, Bai H, Spina E, Tyrrell J, Wilbourne J, Ni L . Cool and warm ionotropic receptors control multiple thermotaxes in larvae. Front Mol Neurosci. 2022; 15:1023492. PMC: 9701816. DOI: 10.3389/fnmol.2022.1023492. View

14.

Ni L . The Structure and Function of Ionotropic Receptors in . Front Mol Neurosci. 2021; 13:638839. PMC: 7882480. DOI: 10.3389/fnmol.2020.638839. View

15.

Knecht Z, Silbering A, Cruz J, Yang L, Croset V, Benton R . Ionotropic Receptor-dependent moist and dry cells control hygrosensation in . Elife. 2017; 6. PMC: 5495567. DOI: 10.7554/eLife.26654. View

16.

Tinevez J, Perry N, Schindelin J, Hoopes G, Reynolds G, Laplantine E . TrackMate: An open and extensible platform for single-particle tracking. Methods. 2016; 115:80-90. DOI: 10.1016/j.ymeth.2016.09.016. View

17.

Ni L, Klein M, Svec K, Budelli G, Chang E, Ferrer A . The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife. 2016; 5. PMC: 4851551. DOI: 10.7554/eLife.13254. View

18.

Rondon-Berrios H, Argyropoulos C, Ing T, Raj D, Malhotra D, Agaba E . Hypertonicity: Clinical entities, manifestations and treatment. World J Nephrol. 2017; 6(1):1-13. PMC: 5215203. DOI: 10.5527/wjn.v6.i1.1. View

19.

Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R . Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron. 2002; 35(2):307-18. DOI: 10.1016/s0896-6273(02)00757-2. View

20.

Li K, Gong Z . Feeling Hot and Cold: Thermal Sensation in Drosophila. Neurosci Bull. 2016; 33(3):317-322. PMC: 5567507. DOI: 10.1007/s12264-016-0087-9. View