The TRP Channels Pkd2, NompC, and Trpm Act in Cold-Sensing Neurons to Mediate Unique Aversive Behaviors to Noxious Cold in Drosophila.
The basic mechanisms underlying noxious cold perception are not well understood. We developed Drosophila assays for noxious cold responses. Larvae respond to near-freezing temperatures via a mutually exclusive set of singular behaviors-in particular, a full-body contraction (CT). Class III (CIII) multidendritic sensory neurons are specifically activated by cold and optogenetic activation of these neurons elicits CT. Blocking synaptic transmission in CIII neurons inhibits CT. Genetically, the transient receptor potential (TRP) channels Trpm, NompC, and Polycystic kidney disease 2 (Pkd2) are expressed in CIII neurons, where each is required for CT. Misexpression of Pkd2 is sufficient to confer cold responsiveness. The optogenetic activation level of multimodal CIII neurons determines behavioral output, and visualization of neuronal activity supports this conclusion. Coactivation of cold- and heat-responsive sensory neurons suggests that the cold-evoked response circuitry is dominant. Our Drosophila model will enable a sophisticated molecular genetic dissection of cold nociceptive genes and circuits.
Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA; Neuroscience Program, Graduate School of Biomedical Sciences, Houston, TX 77030, USA.
Heather N
HN
Turner
School of Systems Biology, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA 22030, USA.
Kevin
K
Armengol
Neuroscience Institute, Georgia State University, Atlanta, GA 30303, USA.
Atit A
AA
Patel
Neuroscience Institute, Georgia State University, Atlanta, GA 30303, USA.
Nathaniel J
NJ
Himmel
School of Systems Biology, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA 22030, USA.
Luis
L
Sullivan
School of Systems Biology, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA 22030, USA.
Srividya Chandramouli
SC
Iyer
Neuroscience Institute, Georgia State University, Atlanta, GA 30303, USA.
Surajit
S
Bhattacharya
School of Systems Biology, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA 22030, USA.
Eswar Prasad R
EPR
Iyer
ProDev Engineering, Missouri City, TX 77459, USA.
Christian
C
Landry
Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA; Neuroscience Program, Graduate School of Biomedical Sciences, Houston, TX 77030, USA; Genes and Development Program, Graduate School of Biomedical Sciences, Houston, TX 77030, USA. Electronic address: mjgalko@mdanderson.org.
Michael J
MJ
Galko
School of Systems Biology, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA 22030, USA; Neuroscience Institute, Georgia State University, Atlanta, GA 30303, USA. Electronic address: dcox18@gsu.edu.
Daniel N
DN
Cox
D000818:Animals; D003080:Cold Temperature; D004330:Drosophila / Q000502:physiology*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D005786:Gene Expression Regulation; D007814:Larva / Q000502:physiology; D059225:Nociception / Q000502:physiology; D011984:Sensory Receptor Cells / Q000502:physiology*; D050051:Transient Receptor Potential Channels / Q000502:physiology*
D029721:Drosophila Proteins; D050051:Transient Receptor Potential Channels
Drosophila; TRP channels; behavior; multimodal sensory processing; nociception; noxious cold