TY - JOUR
T1 - Cyclin-dependent-like kinase 5 is required for pain signaling in human sensory neurons and mouse models
AU - La Montanara, Paolo
AU - Hervera, Arnau
AU - Baltussen, Lucas L.
AU - Hutson, Thomas H.
AU - Palmisano, Ilaria
AU - De Virgiliis, Francesco
AU - Kong, Guiping
AU - Chadwick, Jessica
AU - Gao, Yunan
AU - Bartus, Katalin
AU - Majid, Qasim A.
AU - Gorgoraptis, Nikos
AU - Wong, Kingsley
AU - Downs, Jenny
AU - Pizzorusso, Tommaso
AU - Ultanir, Sila K.
AU - Leonard, Helen
AU - Yu, Hongwei
AU - Millar, David S.
AU - Istvan, Nagy
AU - Mazarakis, Nicholas D.
AU - Di Giovanni, Simone
PY - 2020/7/8
Y1 - 2020/7/8
N2 - Cyclin-dependent-like kinase 5 (CDKL5) gene mutations lead to an X-linked disorder that is characterized by infantile epileptic encephalopathy, developmental delay, and hypotonia. However, we found that a substantial percentage of these patients also report a previously unrecognized anamnestic deficiency in pain perception. Consistent with a role in nociception, we found that CDKL5 is expressed selectively in nociceptive dorsal root ganglia (DRG) neurons in mice and in induced pluripotent stem cell (iPS)-derived human nociceptors. CDKL5-deficient mice display defective epidermal innervation, and conditional deletion of CDKL5 in DRG sensory neurons impairs nociception, phenocopying CDKL5 deficiency disorder in patients. Mechanistically, CDKL5 interacts with calcium/calmodulin-dependent protein kinase II α (CaMKIIα) to control outgrowth and transient receptor potential cation channel subfamily V member 1 (TRPV1)-dependent signaling, which are disrupted in both CDKL5 mutant murine DRG and human iPS-derived nociceptors. Together, these findings unveil a previously unrecognized role for CDKL5 in nociception, proposing an original regulatory mechanism for pain perception with implications for future therapeutics in CDKL5 deficiency disorder.
AB - Cyclin-dependent-like kinase 5 (CDKL5) gene mutations lead to an X-linked disorder that is characterized by infantile epileptic encephalopathy, developmental delay, and hypotonia. However, we found that a substantial percentage of these patients also report a previously unrecognized anamnestic deficiency in pain perception. Consistent with a role in nociception, we found that CDKL5 is expressed selectively in nociceptive dorsal root ganglia (DRG) neurons in mice and in induced pluripotent stem cell (iPS)-derived human nociceptors. CDKL5-deficient mice display defective epidermal innervation, and conditional deletion of CDKL5 in DRG sensory neurons impairs nociception, phenocopying CDKL5 deficiency disorder in patients. Mechanistically, CDKL5 interacts with calcium/calmodulin-dependent protein kinase II α (CaMKIIα) to control outgrowth and transient receptor potential cation channel subfamily V member 1 (TRPV1)-dependent signaling, which are disrupted in both CDKL5 mutant murine DRG and human iPS-derived nociceptors. Together, these findings unveil a previously unrecognized role for CDKL5 in nociception, proposing an original regulatory mechanism for pain perception with implications for future therapeutics in CDKL5 deficiency disorder.
UR - http://www.scopus.com/inward/record.url?scp=85087720943&partnerID=8YFLogxK
U2 - 10.1126/scitranslmed.aax4846
DO - 10.1126/scitranslmed.aax4846
M3 - Article
C2 - 32641489
AN - SCOPUS:85087720943
SN - 1946-6234
VL - 12
JO - Science Translational Medicine
JF - Science Translational Medicine
IS - 551
M1 - eaax4846
ER -