Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans

R. Brian Roome; Farin B. Bourojeni; Bishakha Mona; Shima Rastegar-Pouyani; Raphael Blain; Annie Dumouchel; Charleen Salesse; W. Scott Thompson; Megan Brookbank; Yorick Gitton; Lino Tessarollo; Martyn Goulding; Jane E. Johnson; Marie Kmita; Alain Chédotal; Artur Kania

doi:10.1016/j.celrep.2020.108425

Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans

R. Brian Roome, Farin B. Bourojeni, Bishakha Mona, Shima Rastegar-Pouyani, Raphael Blain, Annie Dumouchel, Charleen Salesse, W. Scott Thompson, Megan Brookbank, Yorick Gitton, Lino Tessarollo, Martyn Goulding, Jane E. Johnson, Marie Kmita, Alain Chédotal, Artur Kania

Research output: Contribution to journal › Article › peer-review

Abstract

Anterolateral system neurons relay pain, itch, and temperature information from the spinal cord to pain-related brain regions, but the differentiation of these neurons and their specific contribution to pain perception remain poorly defined. Here, we show that most mouse spinal neurons that embryonically express the autonomic-system-associated Paired-like homeobox 2A (Phox2a) transcription factor innervate nociceptive brain targets, including the parabrachial nucleus and the thalamus. We define the Phox2a anterolateral system neuron birth order, migration, and differentiation and uncover an essential role for Phox2a in the development of relay of nociceptive signals from the spinal cord to the brain. Finally, we also demonstrate that the molecular identity of Phox2a neurons is conserved in the human fetal spinal cord, arguing that the developmental expression of Phox2a is a prominent feature of anterolateral system neurons.

Original language	English (US)
Article number	108425
Journal	Cell Reports
Volume	33
Issue number	8
DOIs	https://doi.org/10.1016/j.celrep.2020.108425
State	Published - Nov 24 2020

Keywords

LSN
Phox2a
anterolateral tract
autonomic
dI5
dorsal horn
lamina I
lamina V
pain
spinoparabrachial

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

Access to Document

10.1016/j.celrep.2020.108425

Fingerprint Dive into the research topics of 'Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans'. Together they form a unique fingerprint.

Cite this

Roome, R. B., Bourojeni, F. B., Mona, B., Rastegar-Pouyani, S., Blain, R., Dumouchel, A., Salesse, C., Thompson, W. S., Brookbank, M., Gitton, Y., Tessarollo, L., Goulding, M., Johnson, J. E., Kmita, M., Chédotal, A., & Kania, A. (2020). Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans. Cell Reports, 33(8), [108425]. https://doi.org/10.1016/j.celrep.2020.108425

Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans. / Roome, R. Brian; Bourojeni, Farin B.; Mona, Bishakha; Rastegar-Pouyani, Shima; Blain, Raphael; Dumouchel, Annie; Salesse, Charleen; Thompson, W. Scott; Brookbank, Megan; Gitton, Yorick; Tessarollo, Lino; Goulding, Martyn; Johnson, Jane E.; Kmita, Marie; Chédotal, Alain; Kania, Artur.

In: Cell Reports, Vol. 33, No. 8, 108425, 24.11.2020.

Research output: Contribution to journal › Article › peer-review

Roome, RB, Bourojeni, FB, Mona, B, Rastegar-Pouyani, S, Blain, R, Dumouchel, A, Salesse, C, Thompson, WS, Brookbank, M, Gitton, Y, Tessarollo, L, Goulding, M, Johnson, JE, Kmita, M, Chédotal, A & Kania, A 2020, 'Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans', Cell Reports, vol. 33, no. 8, 108425. https://doi.org/10.1016/j.celrep.2020.108425

Roome, R. Brian ; Bourojeni, Farin B. ; Mona, Bishakha ; Rastegar-Pouyani, Shima ; Blain, Raphael ; Dumouchel, Annie ; Salesse, Charleen ; Thompson, W. Scott ; Brookbank, Megan ; Gitton, Yorick ; Tessarollo, Lino ; Goulding, Martyn ; Johnson, Jane E. ; Kmita, Marie ; Chédotal, Alain ; Kania, Artur. / Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans. In: Cell Reports. 2020 ; Vol. 33, No. 8.

@article{3355af00f1314f7eabc9ac2c6fc80523,

title = "Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans",

abstract = "Anterolateral system neurons relay pain, itch, and temperature information from the spinal cord to pain-related brain regions, but the differentiation of these neurons and their specific contribution to pain perception remain poorly defined. Here, we show that most mouse spinal neurons that embryonically express the autonomic-system-associated Paired-like homeobox 2A (Phox2a) transcription factor innervate nociceptive brain targets, including the parabrachial nucleus and the thalamus. We define the Phox2a anterolateral system neuron birth order, migration, and differentiation and uncover an essential role for Phox2a in the development of relay of nociceptive signals from the spinal cord to the brain. Finally, we also demonstrate that the molecular identity of Phox2a neurons is conserved in the human fetal spinal cord, arguing that the developmental expression of Phox2a is a prominent feature of anterolateral system neurons.",

keywords = "LSN, Phox2a, anterolateral tract, autonomic, dI5, dorsal horn, lamina I, lamina V, pain, spinoparabrachial",

author = "Roome, {R. Brian} and Bourojeni, {Farin B.} and Bishakha Mona and Shima Rastegar-Pouyani and Raphael Blain and Annie Dumouchel and Charleen Salesse and Thompson, {W. Scott} and Megan Brookbank and Yorick Gitton and Lino Tessarollo and Martyn Goulding and Johnson, {Jane E.} and Marie Kmita and Alain Ch{\'e}dotal and Artur Kania",

note = "Funding Information: R.B.R. was a recipient of a PhD studentship from Fonds de Recherche du Qu{\'e}bec - Sant{\'e} . S.R.-P. received a studentship from McGill University {\textquoteright}s Healthy Brains, Healthy Lives (HBHL) initiative supported, in part, by the Canada First Research Excellence Fund . J.E.J. was supported by the National Institutes of Health grant R37 HD091856 . A.C. was supported by the Agence Nationale de la Recherche and Inserm (transversal program HuDeCa). L.T. was supported by the Intramural Research Program of NCI , NIH. A.K. and M.K. were funded by operating and project grants from the Canadian Institutes of Health Research ( PJT-162225 , MOP-77556 , PJT-153053 , and PJT-159839 to A.K. and MOP-127110 and PJT-162143 to M.K.). ",

year = "2020",

month = nov,

day = "24",

doi = "10.1016/j.celrep.2020.108425",

language = "English (US)",

volume = "33",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "8",

}

TY - JOUR

T1 - Phox2a Defines a Developmental Origin of the Anterolateral System in Mice and Humans

AU - Roome, R. Brian

AU - Bourojeni, Farin B.

AU - Mona, Bishakha

AU - Rastegar-Pouyani, Shima

AU - Blain, Raphael

AU - Dumouchel, Annie

AU - Salesse, Charleen

AU - Thompson, W. Scott

AU - Brookbank, Megan

AU - Gitton, Yorick

AU - Tessarollo, Lino

AU - Goulding, Martyn

AU - Johnson, Jane E.

AU - Kmita, Marie

AU - Chédotal, Alain

AU - Kania, Artur

N1 - Funding Information: R.B.R. was a recipient of a PhD studentship from Fonds de Recherche du Québec - Santé . S.R.-P. received a studentship from McGill University ’s Healthy Brains, Healthy Lives (HBHL) initiative supported, in part, by the Canada First Research Excellence Fund . J.E.J. was supported by the National Institutes of Health grant R37 HD091856 . A.C. was supported by the Agence Nationale de la Recherche and Inserm (transversal program HuDeCa). L.T. was supported by the Intramural Research Program of NCI , NIH. A.K. and M.K. were funded by operating and project grants from the Canadian Institutes of Health Research ( PJT-162225 , MOP-77556 , PJT-153053 , and PJT-159839 to A.K. and MOP-127110 and PJT-162143 to M.K.).

PY - 2020/11/24

Y1 - 2020/11/24

N2 - Anterolateral system neurons relay pain, itch, and temperature information from the spinal cord to pain-related brain regions, but the differentiation of these neurons and their specific contribution to pain perception remain poorly defined. Here, we show that most mouse spinal neurons that embryonically express the autonomic-system-associated Paired-like homeobox 2A (Phox2a) transcription factor innervate nociceptive brain targets, including the parabrachial nucleus and the thalamus. We define the Phox2a anterolateral system neuron birth order, migration, and differentiation and uncover an essential role for Phox2a in the development of relay of nociceptive signals from the spinal cord to the brain. Finally, we also demonstrate that the molecular identity of Phox2a neurons is conserved in the human fetal spinal cord, arguing that the developmental expression of Phox2a is a prominent feature of anterolateral system neurons.

AB - Anterolateral system neurons relay pain, itch, and temperature information from the spinal cord to pain-related brain regions, but the differentiation of these neurons and their specific contribution to pain perception remain poorly defined. Here, we show that most mouse spinal neurons that embryonically express the autonomic-system-associated Paired-like homeobox 2A (Phox2a) transcription factor innervate nociceptive brain targets, including the parabrachial nucleus and the thalamus. We define the Phox2a anterolateral system neuron birth order, migration, and differentiation and uncover an essential role for Phox2a in the development of relay of nociceptive signals from the spinal cord to the brain. Finally, we also demonstrate that the molecular identity of Phox2a neurons is conserved in the human fetal spinal cord, arguing that the developmental expression of Phox2a is a prominent feature of anterolateral system neurons.

KW - LSN

KW - Phox2a

KW - anterolateral tract

KW - autonomic

KW - dI5

KW - dorsal horn

KW - lamina I

KW - lamina V

KW - pain

KW - spinoparabrachial

UR - http://www.scopus.com/inward/record.url?scp=85096817530&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85096817530&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2020.108425

DO - 10.1016/j.celrep.2020.108425

M3 - Article

C2 - 33238113

AN - SCOPUS:85096817530

VL - 33

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 8

M1 - 108425

ER -