Segmentation and patterning of the vertebrate hindbrain

Krumlauf, Robb; Wilkinson, David

doi:10.1242/dev.186460

Cited by 46 publications

(53 citation statements)

References 183 publications

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“…Therefore the medullary portion (r7-r11) of the trigeminal column consists of successive rostrocaudal units that largely fit the rhombomeric map, an organization also observed in the vagal motor nucleus (Cambronero and Puelles, 2000;Marín et al, 2008), the inferior olive (Hidalgo-Sánchez et al, 2012), the reticular formation (Gray, 2013) or the raphe nuclei (Alonso et al, 2013) all of them longitudinal structures that span several rhombomeres of the medulla oblongata. Its apparent early morphologic homogeneity or uniformity contrasts with the overt segmentation of the rostral half of the hindbrain (Parker and Krumlauf, 2020;Pujades, 2020;Krumlauf and Wilkinson, 2021). However, according to current evidence the medulla oblongata emerges as a complex region formed by multiple neuromeric units with differential molecular profiles (Nieuwenhuys and Puelles, 2016;Puelles et al, 2018;Watson et al, 2019).…”

Section: The Segmentation Of the Trigeminal Column In The Medulla Oblongatamentioning

confidence: 98%

Molecular Segmentation of the Spinal Trigeminal Nucleus in the Adult Mouse Brain

García-Guillén

Martı́nez-de-la-Torre

Puelles

et al. 2021

Front. Neuroanat.

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The trigeminal column is a hindbrain structure formed by second order sensory neurons that receive afferences from trigeminal primary (ganglionic) nerve fibers. Classical studies subdivide it into the principal sensory trigeminal nucleus located next to the pontine nerve root, and the spinal trigeminal nucleus which in turn consists of oral, interpolar and caudal subnuclei. On the other hand, according to the prosomeric model, this column would be subdivided into segmental units derived from respective rhombomeres. Experimental studies have mapped the principal sensory trigeminal nucleus to pontine rhombomeres (r) r2-r3 in the mouse. The spinal trigeminal nucleus emerges as a plurisegmental formation covering several rhombomeres (r4 to r11 in mice) across pontine, retropontine and medullary hindbrain regions. In the present work we reexamined the issue of rhombomeric vs. classical subdivisions of this column. To this end, we analyzed its subdivisions in an AZIN2-lacZ transgenic mouse, known as a reference model for hindbrain topography, together with transgenic reporter lines for trigeminal fibers. We screened as well for genes differentially expressed along the axial dimension of this structure in the adult and juvenile mouse brain. This analysis yielded genes from multiple functional families that display transverse domains fitting the mentioned rhombomeric map. The spinal trigeminal nucleus thus represents a plurisegmental structure with a series of distinct neuromeric units having unique combinatorial molecular profiles.

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Section: The Segmentation Of the Trigeminal Column In The Medulla Oblongatamentioning

confidence: 98%

Molecular Segmentation of the Spinal Trigeminal Nucleus in the Adult Mouse Brain

García-Guillén

Martı́nez-de-la-Torre

Puelles

et al. 2021

Front. Neuroanat.

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“…Different anteroposterior identities are provided to each rhombomere by virtue of the combinations of Hox genes expressed within each segment (Trainor and Krumlauf, 2000;Marín et al, 2008;Tümpel et al, 2009;Tomás-Roca et al, 2016;Krumlauf and Wilkinson, 2021; Figure 2). Therefore, at least eight rostrocaudal vestibular subpopulations, spanning eight consecutive rhombomeres (r2-r9) can be conceived on the basis of differential Hox gene expression alone.…”

Section: Molecular Profiling Of the Classical Vestibular Nucleimentioning

confidence: 99%

The Vestibular Column in the Mouse: A Rhombomeric Perspective

Dı́az

Glover

2022

Front. Neuroanat.

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The vestibular column is located in the hindbrain between the sensory auditory (dorsal) and trigeminal (ventral) columns, spanning rhombomeres r1 (or r2) to r9. It contains the vestibular nuclear complex that receives sensory innervation from the labyrinthine end organs in the inner ear. Gene expression studies and experimental manipulations of developmental genes, particularly Hox genes and other developmental patterning genes, are providing insight into the morphological and functional organization of the vestibular nuclear complex, particularly from a segmental standpoint. Here, we will review studies of the classical vestibular nuclei and of vestibular projection neurons that innervate distinct targets in relation to individual rhombomeres and the expression of specific genes. Studies in different species have demonstrated that the vestibular complex is organized into a hodological mosaic that relates axon trajectory and target to specific hindbrain rhombomeres and intrarhombomeric domains, with a molecular underpinning in the form of transcription factor signatures, which has been highly conserved during the evolution of the vertebrate lineage.

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“…For example, in vertebrate model systems, opposing gradients of RA and FGFs have been shown to regulate nested domains of Hox expression in the CNS and in mesodermal domains that control specification of vertebral identities and axial elongation (Figure 1a,b) [91,[94][95][96][97][98][99]. In the hindbrain, RA signaling plays a key role in triggering the process of segmentation and establishes segmental patterning of Hox expression [43,91,. In addition, in cultured cells differentiated into neural fates, Hox genes display temporal collinearity in response to treatment with RA [125][126][127][128][129].…”

Section: Introductionmentioning

confidence: 99%

Retinoic Acid Signaling in Vertebrate Hindbrain Segmentation: Evolution and Diversification

2021

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In metazoans, Hox genes are key drivers of morphogenesis. In chordates, they play important roles in patterning the antero-posterior (A-P) axis. A crucial aspect of their role in axial patterning is their collinear expression, a process thought to be linked to their response to major signaling pathways such as retinoic acid (RA) signaling. The amplification of Hox genes following major events of genome evolution can contribute to morphological diversity. In vertebrates, RA acts as a key regulator of the gene regulatory network (GRN) underlying hindbrain segmentation, which includes Hox genes. This review investigates how the RA signaling machinery has evolved and diversified and discusses its connection to the hindbrain GRN in relation to diversity. Using non-chordate and chordate deuterostome models, we explore aspects of ancient programs of axial patterning in an attempt to retrace the evolution of the vertebrate hindbrain GRN. In addition, we investigate how the RA signaling machinery has evolved in vertebrates and highlight key examples of regulatory diversification that may have influenced the GRN for hindbrain segmentation. Finally, we describe the value of using lamprey as a model for the early-diverged jawless vertebrate group, to investigate the elaboration of A-P patterning mechanisms in the vertebrate lineage.

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Segmentation and patterning of the vertebrate hindbrain

Cited by 46 publications

References 183 publications

Molecular Segmentation of the Spinal Trigeminal Nucleus in the Adult Mouse Brain

Molecular Segmentation of the Spinal Trigeminal Nucleus in the Adult Mouse Brain

The Vestibular Column in the Mouse: A Rhombomeric Perspective

Retinoic Acid Signaling in Vertebrate Hindbrain Segmentation: Evolution and Diversification

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