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Calcium signaling mediates cold sensing in insect tissues
Friday, 2013/05/31 | 09:37:20
  1. Nicholas M. Teetsa,1,
  2. Shu-Xia Yib,
  3. Richard E. Lee, Jr.b, and
  4. David L. Denlingera,c,1

 

Author Affiliations


1.aDepartment of Entomology, Ohio State University, Columbus, OH 43210;
2.bDepartment of Zoology, Miami University, Oxford, OH 45056; and
3.cDepartment of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
  1. Contributed by David L. Denlinger, April 10, 2013 (sent for review January 30, 2013)

 

Abstract

 

The ability to rapidly respond to changes in temperature is a critical adaptation for insects and other ectotherms living in thermally variable environments. In a process called rapid cold hardening (RCH), insects significantly enhance cold tolerance following brief (i.e., minutes to hours) exposure to nonlethal chilling. Although the ecological relevance of RCH is well-established, the underlying physiological mechanisms that trigger RCH are poorly understood. RCH can be elicited in isolated tissues ex vivo, suggesting cold-sensing and downstream hardening pathways are governed by brain-independent signaling mechanisms. We previously provided preliminary evidence that calcium is involved in RCH, and here we firmly establish that calcium signaling mediates cold sensing in insect tissues. In tracheal cells of the freeze-tolerant goldenrod gall fly, Eurosta solidaginis, chilling to 0 °C evoked a 40% increase in intracellular calcium concentration as determined by live-cell confocal imaging. Downstream of calcium entry, RCH conditions significantly increased the activity of calcium/calmodulin-dependent protein kinase II (CaMKII) while reducing phosphorylation of the inhibitory Thr306 residue. Pharmacological inhibitors of calcium entry, calmodulin activation, and CaMKII activity all prevented ex vivo RCH in midgut and salivary gland tissues, indicating that calcium signaling is required for RCH to occur. Similar results were obtained for a freeze-intolerant species, adults of the flesh fly, Sarcophaga bullata, suggesting that calcium-mediated cold sensing is a general feature of insects. Our results imply that insect tissues use calcium signaling to instantly detect decreases in temperature and trigger downstream cold-hardening mechanisms.

Fig. 4. Working model for the role of calcium signaling during cold sensing and rapid cold hardening. Low temperature causes an increase in intracellular calcium concentration, and we hypothesize that this calcium influx occurs by low temperature inhibition of ATP-dependent calcium export mechanisms coupled with calcium entry through calcium leak channels (CLC). In this model, low temperature inhibits the activity of both sarcoplasmic endo-plasmic reticulum calcium ATPase (SERCA) and sodium/potassium ATPase (Na/KATPase) coupled to the sodium calcium exchanger (NCX). Inside the cell, calcium, via calcium/calmodulin-dependent protein kinase II (CaMKII) and other unknown mechanisms, triggers pathways involved in rapid cold hard-ening, thereby enhancing the cell’s cold tolerance. Dashed lines and arrows indicate speculative relationships that were not experimentally determined in the present study.

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