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Analysis of lamprey meis genes reveals that conserved inputs from Hox, Meis and Pbx proteins control their expression in the hindbrain and neural tube

Parker, Hugo J. and De Kumar, Bony and Pushel, Irina and Bronner, Marianne E. and Krumlauf, Robb (2021) Analysis of lamprey meis genes reveals that conserved inputs from Hox, Meis and Pbx proteins control their expression in the hindbrain and neural tube. Developmental Biology, 479 . pp. 61-76. ISSN 0012-1606. doi:10.1016/j.ydbio.2021.07.014.

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Meis genes are known to play important roles in the hindbrain and neural crest cells of jawed vertebrates. To explore the roles of Meis genes in head development during evolution of vertebrates, we have identified four meis genes in the sea lamprey genome and characterized their patterns of expression and regulation, with a focus on the hindbrain and pharynx. Each of the lamprey meis genes displays temporally and spatially dynamic patterns of expression, some of which are coupled to rhombomeric domains in the developing hindbrain and select pharyngeal arches. Studies of Meis loci in mouse and zebrafish have identified enhancers that are bound by Hox and TALE (Meis and Pbx) proteins, implicating these factors in the direct regulation of Meis expression. We examined the lamprey meis loci and identified a series of cis-elements conserved between lamprey and jawed vertebrate meis genes. In transgenic reporter assays we demonstrated that these elements act as neural enhancers in lamprey embryos, directing reporter expression in appropriate domains when compared to expression of their associated endogenous meis gene. Sequence alignments reveal that these conserved elements are in similar relative positions of the meis loci and contain a series of consensus binding motifs for Hox and TALE proteins. This suggests that ancient Hox and TALE-responsive enhancers regulated expression of ancestral vertebrate meis genes in segmental domains in the hindbrain and have been retained in the meis loci during vertebrate evolution. The presence of conserved Meis, Pbx and Hox binding sites in these lamprey enhancers links Hox and TALE factors to regulation of lamprey meis genes in the developing hindbrain, indicating a deep ancestry for these regulatory interactions prior to the divergence of jawed and jawless vertebrates.

Item Type:Article
Related URLs:
URLURL TypeDescription
Parker, Hugo J.0000-0001-7646-2007
De Kumar, Bony0000-0001-8398-3775
Pushel, Irina0000-0002-0862-1923
Bronner, Marianne E.0000-0003-4274-1862
Krumlauf, Robb0000-0001-9102-7927
Additional Information:© 2021 Elsevier Inc. Received 15 January 2021, Revised 10 June 2021, Accepted 22 July 2021, Available online 24 July 2021. We thank Stephen Green, Dorit Hockman, Tetsuto Miyashita, and Megan Martik for lamprey husbandry assistance, the Stowers Institute Histology facility for sectioning assistance and the aquatics facility for help in maintenance of zebrafish. HJP, BDK and RK were supported by funds from the Stowers Institute (RK grant #2020–1001). MEB was supported by NIH grant R35 NS111564. This work was performed to fulfill, in part, requirements for IP's thesis research in the Graduate School of the Stowers Institute for Medical Research.
Funding AgencyGrant Number
Stowers Institute for Medical Research2020-1001
NIHR35 NS111564
Subject Keywords:Meis genes; Hox genes; Lamprey; Hindbrain segmentation; Neural crest cells; Gene regulatory networks; cis-Regulatory elements; Vertebrate evolution; Head development
Record Number:CaltechAUTHORS:20210809-181055002
Persistent URL:
Official Citation:Hugo J. Parker, Bony De Kumar, Irina Pushel, Marianne E. Bronner, Robb Krumlauf, Analysis of lamprey meis genes reveals that conserved inputs from Hox, Meis and Pbx proteins control their expression in the hindbrain and neural tube, Developmental Biology, Volume 479, 2021, Pages 61-76, ISSN 0012-1606,
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110173
Deposited By: Tony Diaz
Deposited On:09 Aug 2021 20:12
Last Modified:09 Aug 2021 20:12

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