PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis

Luca Bartesaghi, Yiqiao Wang, Paula Fontanet, Simone Wanderoy, Finja Berger, Haohao Wu, Natalia Akkuratova, Filipa Bouçanova, Jean Jacques Médard, Charles Petitpré, Mark A. Landy, Ming Dong Zhang, Philip Harrer, Claudia Stendel, Rolf Stucka, Marina Dusl, Maria Eleni Kastriti, Laura Croci, Helen C. Lai, Gian Giacomo ConsalezAlexandre Pattyn, Patrik Ernfors, Jan Senderek, Igor Adameyko, Francois Lallemend, Saida Hadjab, Roman Chrast

Research output

2 Citations (Scopus)

Abstract

The sensation of pain is essential for the preservation of the functional integrity of the body. However, the key molecular regulators necessary for the initiation of the development of pain-sensing neurons have remained largely unknown. Here, we report that, in mice, inactivation of the transcriptional regulator PRDM12, which is essential for pain perception in humans, results in a complete absence of the nociceptive lineage, while proprioceptive and touch-sensitive neurons remain. Mechanistically, our data reveal that PRDM12 is required for initiation of neurogenesis and activation of a cascade of downstream pro-neuronal transcription factors, including NEUROD1, BRN3A, and ISL1, in the nociceptive lineage while it represses alternative fates other than nociceptors in progenitor cells. Our results thus demonstrate that PRDM12 is necessary for the generation of the entire lineage of pain-initiating neurons. The sensation of pain, temperature, and itch by neurons of the nociceptive lineage is essential for animal survival. Bartesaghi et al. report that the transcriptional regulator PRDM12 is indispensable in neural crest cells (NCCs) for the initiation of the sensory neuronal differentiation program that generates the entire nociceptive lineage.

Original languageEnglish
Pages (from-to)3484-3492.e4
Number of pages13
JournalCell Reports
Volume26
Issue number13
DOIs
Publication statusPublished - 26 Mar 2019

Fingerprint

Nociceptors
Neurogenesis
Neurons
Pain
Pain Perception
Neural Crest
Touch
Animals
Transcription Factors
Stem Cells
Chemical activation
Temperature

Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Bartesaghi, L., Wang, Y., Fontanet, P., Wanderoy, S., Berger, F., Wu, H., ... Chrast, R. (2019). PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis. Cell Reports, 26(13), 3484-3492.e4. https://doi.org/10.1016/j.celrep.2019.02.098
Bartesaghi, Luca ; Wang, Yiqiao ; Fontanet, Paula ; Wanderoy, Simone ; Berger, Finja ; Wu, Haohao ; Akkuratova, Natalia ; Bouçanova, Filipa ; Médard, Jean Jacques ; Petitpré, Charles ; Landy, Mark A. ; Zhang, Ming Dong ; Harrer, Philip ; Stendel, Claudia ; Stucka, Rolf ; Dusl, Marina ; Kastriti, Maria Eleni ; Croci, Laura ; Lai, Helen C. ; Consalez, Gian Giacomo ; Pattyn, Alexandre ; Ernfors, Patrik ; Senderek, Jan ; Adameyko, Igor ; Lallemend, Francois ; Hadjab, Saida ; Chrast, Roman. / PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis. In: Cell Reports. 2019 ; Vol. 26, No. 13. pp. 3484-3492.e4.
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abstract = "The sensation of pain is essential for the preservation of the functional integrity of the body. However, the key molecular regulators necessary for the initiation of the development of pain-sensing neurons have remained largely unknown. Here, we report that, in mice, inactivation of the transcriptional regulator PRDM12, which is essential for pain perception in humans, results in a complete absence of the nociceptive lineage, while proprioceptive and touch-sensitive neurons remain. Mechanistically, our data reveal that PRDM12 is required for initiation of neurogenesis and activation of a cascade of downstream pro-neuronal transcription factors, including NEUROD1, BRN3A, and ISL1, in the nociceptive lineage while it represses alternative fates other than nociceptors in progenitor cells. Our results thus demonstrate that PRDM12 is necessary for the generation of the entire lineage of pain-initiating neurons. The sensation of pain, temperature, and itch by neurons of the nociceptive lineage is essential for animal survival. Bartesaghi et al. report that the transcriptional regulator PRDM12 is indispensable in neural crest cells (NCCs) for the initiation of the sensory neuronal differentiation program that generates the entire nociceptive lineage.",
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Bartesaghi, L, Wang, Y, Fontanet, P, Wanderoy, S, Berger, F, Wu, H, Akkuratova, N, Bouçanova, F, Médard, JJ, Petitpré, C, Landy, MA, Zhang, MD, Harrer, P, Stendel, C, Stucka, R, Dusl, M, Kastriti, ME, Croci, L, Lai, HC, Consalez, GG, Pattyn, A, Ernfors, P, Senderek, J, Adameyko, I, Lallemend, F, Hadjab, S & Chrast, R 2019, 'PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis', Cell Reports, vol. 26, no. 13, pp. 3484-3492.e4. https://doi.org/10.1016/j.celrep.2019.02.098

PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis. / Bartesaghi, Luca; Wang, Yiqiao; Fontanet, Paula; Wanderoy, Simone; Berger, Finja; Wu, Haohao; Akkuratova, Natalia; Bouçanova, Filipa; Médard, Jean Jacques; Petitpré, Charles; Landy, Mark A.; Zhang, Ming Dong; Harrer, Philip; Stendel, Claudia; Stucka, Rolf; Dusl, Marina; Kastriti, Maria Eleni; Croci, Laura; Lai, Helen C.; Consalez, Gian Giacomo; Pattyn, Alexandre; Ernfors, Patrik; Senderek, Jan; Adameyko, Igor; Lallemend, Francois; Hadjab, Saida; Chrast, Roman.

In: Cell Reports, Vol. 26, No. 13, 26.03.2019, p. 3484-3492.e4.

Research output

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AU - Bartesaghi, Luca

AU - Wang, Yiqiao

AU - Fontanet, Paula

AU - Wanderoy, Simone

AU - Berger, Finja

AU - Wu, Haohao

AU - Akkuratova, Natalia

AU - Bouçanova, Filipa

AU - Médard, Jean Jacques

AU - Petitpré, Charles

AU - Landy, Mark A.

AU - Zhang, Ming Dong

AU - Harrer, Philip

AU - Stendel, Claudia

AU - Stucka, Rolf

AU - Dusl, Marina

AU - Kastriti, Maria Eleni

AU - Croci, Laura

AU - Lai, Helen C.

AU - Consalez, Gian Giacomo

AU - Pattyn, Alexandre

AU - Ernfors, Patrik

AU - Senderek, Jan

AU - Adameyko, Igor

AU - Lallemend, Francois

AU - Hadjab, Saida

AU - Chrast, Roman

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N2 - The sensation of pain is essential for the preservation of the functional integrity of the body. However, the key molecular regulators necessary for the initiation of the development of pain-sensing neurons have remained largely unknown. Here, we report that, in mice, inactivation of the transcriptional regulator PRDM12, which is essential for pain perception in humans, results in a complete absence of the nociceptive lineage, while proprioceptive and touch-sensitive neurons remain. Mechanistically, our data reveal that PRDM12 is required for initiation of neurogenesis and activation of a cascade of downstream pro-neuronal transcription factors, including NEUROD1, BRN3A, and ISL1, in the nociceptive lineage while it represses alternative fates other than nociceptors in progenitor cells. Our results thus demonstrate that PRDM12 is necessary for the generation of the entire lineage of pain-initiating neurons. The sensation of pain, temperature, and itch by neurons of the nociceptive lineage is essential for animal survival. Bartesaghi et al. report that the transcriptional regulator PRDM12 is indispensable in neural crest cells (NCCs) for the initiation of the sensory neuronal differentiation program that generates the entire nociceptive lineage.

AB - The sensation of pain is essential for the preservation of the functional integrity of the body. However, the key molecular regulators necessary for the initiation of the development of pain-sensing neurons have remained largely unknown. Here, we report that, in mice, inactivation of the transcriptional regulator PRDM12, which is essential for pain perception in humans, results in a complete absence of the nociceptive lineage, while proprioceptive and touch-sensitive neurons remain. Mechanistically, our data reveal that PRDM12 is required for initiation of neurogenesis and activation of a cascade of downstream pro-neuronal transcription factors, including NEUROD1, BRN3A, and ISL1, in the nociceptive lineage while it represses alternative fates other than nociceptors in progenitor cells. Our results thus demonstrate that PRDM12 is necessary for the generation of the entire lineage of pain-initiating neurons. The sensation of pain, temperature, and itch by neurons of the nociceptive lineage is essential for animal survival. Bartesaghi et al. report that the transcriptional regulator PRDM12 is indispensable in neural crest cells (NCCs) for the initiation of the sensory neuronal differentiation program that generates the entire nociceptive lineage.

KW - neural crest cells

KW - neurogenesis

KW - nociceptive neurons

KW - pain

KW - Prdm12

KW - CREST

KW - GENES

KW - DIFFERENTIATION

KW - SPECIFICATION

KW - FAMILY

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SP - 3484-3492.e4

JO - Cell Reports

JF - Cell Reports

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Bartesaghi L, Wang Y, Fontanet P, Wanderoy S, Berger F, Wu H et al. PRDM12 Is Required for Initiation of the Nociceptive Neuron Lineage during Neurogenesis. Cell Reports. 2019 Mar 26;26(13):3484-3492.e4. https://doi.org/10.1016/j.celrep.2019.02.098