Collinear Hox-Hox interactions are involved in patterning the vertebrate anteroposterior (A-P) axis

Zhu, Kangshun; Spaink, Herman P.; Durston, Antony J.

doi:10.1371/journal.pone.0175287

Cited by 26 publications

(50 citation statements)

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“…Posterior induction (PI) is likely to be the basis of temporal collinearity (Faiella et al, 1994;Hooiveld et al, 1999;McNulty et al, 2005;Zhu et al, 2017aZhu et al, , 2017b. This regulatory mechanism works sequentially.…”

Section: The Early A-p Axis Is Made By Tstmentioning

confidence: 99%

“…The evidence that these three types of Hox-Hox interactions mediate Hox collinearities and TST comes principally from gain and loss of function experiments, especially from the cascade phenotypes ( Figure 2) that are sometimes seen (Faiella et al, 1994;Hooiveld et al, 1999;McNulty et al, 2005;Zhu et al, 2017aZhu et al, , 2017b.…”

Section: Posterior Dominance (Pd)mentioning

confidence: 99%

“…In the trunk-tail part of the axis, these determinants are the Hox genes (Figure 3a). The anterior boundary for the earliest Hoxc6 expression is always at the cervical-thoracic transition in PM (Burke et al, 1995;Gaunt, 2000;McIntyre et al, 2007;Zhu et al, 2017aZhu et al, , 2017b. The anterior boundary for Hoxb4 is close to the boundary between posterior head and neck and the occipital/cervical transition in the PM.…”

Section: What Are the Roles Of Bmp And Anti-bmp?mentioning

confidence: 99%

“…The head and tail of the A-P timer are close together because of their representation on a clock face. No statement about molecular identities is intended 3.3.1 | The induction of expression of more 5 0 posterior Hox genes by more 3 0 anterior Hox genesreferred to as posterior induction (PI) Posterior induction (PI) is likely to be the basis of temporal collinearity (Faiella et al, 1994;Hooiveld et al, 1999;McNulty et al, 2005;Zhu et al, 2017aZhu et al, , 2017b. This regulatory mechanism works sequentially.…”

Section: The Early A-p Axis Is Made By Tstmentioning

confidence: 99%

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What are the roles of retinoids, other morphogens, and Hox genes in setting up the vertebrate body axis?

Durston

2019

Genesis

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Summary This article is concerned with the roles of retinoids and other known anterior–posterior morphogens in setting up the embryonic vertebrate anterior–posterior axis. The discussion is restricted to the very earliest events in setting up the anterior–posterior axis (from blastula to tailbud stages in Xenopus embryos). In these earliest developmental stages, morphogen concentration gradients are not relevant for setting up this axis. It emerges that at these stages, the core patterning mechanism is timing: BMP‐anti BMP mediated time space translation that regulates Hox temporal and spatial collinearities and Hox‐Hox auto‐ and cross‐ regulation. The known anterior–posterior morphogens and signaling pathways––retinoids, FGF's, Cdx, Wnts, Gdf11 and others––interact with this core mechanism at and after space–time defined “decision points,” leading to the separation of distinct axial domains. There are also other roles for signaling pathways. Besides the Hox regulated hindbrain/trunk part of the axis, there is a rostral part (including the anterior part of the head and the extreme anterior domain [EAD]) that appears to be regulated by additional mechanisms. Key aspects of anterior–posterior axial patterning, including: the nature of different phases in early patterning and in the whole process; the specificities of Hox action and of intercellular signaling; and the mechanisms of Hox temporal and spatial collinearities, are discussed in relation to the facts and hypotheses proposed above.

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Section: The Early A-p Axis Is Made By Tstmentioning

confidence: 99%

Section: Posterior Dominance (Pd)mentioning

confidence: 99%

Section: What Are the Roles Of Bmp And Anti-bmp?mentioning

confidence: 99%

Section: The Early A-p Axis Is Made By Tstmentioning

confidence: 99%

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What are the roles of retinoids, other morphogens, and Hox genes in setting up the vertebrate body axis?

Durston

2019

Genesis

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“…While at first sight this may seem contradictory to posterior prevalence, it is compatible with and explainable by our recent result that posterior prevalence starts to exert its influence from st.15 in paraxial mesoderm. 7 What is important is that results in Fig. 1D and E suggest hoxc6 LOF cuts off the temporal sequence of Hox expression and stops the Hox timer.…”

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confidence: 91%

Hoxc6 loss of function truncates the main body axis in Xenopus

2017

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During animal development, the formation of the anteriorposterior (A-P) axis is of fundamental importance, because it sets the stage for subsequent tissue differentiation and organogenesis. Patterning along the A-P axis requires the expression of Hox genes to specify positional information. 1 In mammals, these genes are organized into 4 chromosomal (HOXA-D) clusters containing 39 members. Equivalent genes within each cluster are divided into 13 paralogous groups (HOX1-13). During A-P patterning, Hox genes are expressed in a temporal sequence that matches their 3' to 5' arrangement on the chromosome (temporal collinearity). 2This precisely controlled timing in Hox gene expression potentially provides a timing mechanism for the formation of A-P structures, that are laid down from head to tail progressively during early development.3 Actually, Hox temporal collinearity is prerequisite for establishing the correct spatial pattern of Hox gene expression, 4 which also reflects their 3' to 5' order on the chromosome (spatial collinearity). Therefore, not only is temporal collinearity an interesting feature of Hox genes, it is also likely to play a crucial role in A-P patterning. Nonetheless, the nature of Hox temporal collinearity has yet to be fully elucidated.In an attempt to understand what drives the Hox timer (temporal collinearity), we did hoxc6 loss of function (LOF) in the Xenopus by injection of a hoxc6 morpholino (MO) (5'-ATTCATATCTTCTCCTTTACCTGCC-3') at 2-cell or 4-cell stage. The effectiveness and specificity of this MO have been demonstrated previously.5 Remarkably, injection of 60ng hoxc6 MO cut off the posterior part of the axis completely, whereas injection of the same amount of control MO did not affect axis formation (Fig. 1A). Consistent with the phenotype, we observed that the expression domains of krox-20, a rhombomere marker, and otx-2, a midbrain marker, expanded posteriorly (Fig. 1B).We then asked: why did hoxc6 LOF give such a severe developmental consequence? To answer this question, we examined the expression of all the 9 genes in the HOXC cluster (hoxc4, 5, 6, 8, 9, 10, 11, 12 and13) and all the 3 genes in the hox6 paralogous group (hoxa6, b6 and c6) at st.26 (Fig. 1C). In hoxc6 LOF embryos, hoxc6 was downregulated by 50%, confirming the morpholino worked. The downregulation of hoxc6 was accompanied by upregulation of hoxc4 and c5 and by downregulation of most Hox genes that are posterior to hoxc6 in the HOXC cluster. These results indicate 2 previously identified types of Hox interactions within the HOXC cluster: posterior prevalence (the repression or antagonism of anterior Hox genes by posterior ones, e.g. the repression of hoxc4 and c5 by hoxc6), and posterior induction (the induction of posterior Hox genes by anterior ones, e.g., the induction of hoxc8,9, and 10-13 by hoxc6) (reviewed in Ref.4). Interestingly, hoxa6 and b6 were also downregulated by hoxc6 LOF, suggesting interactions also exist among Hox clusters. This explains why Hox genes from other clusters (e.g., hoxd3, a5, and d...

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Human colon organoid differentiation from induced pluripotent stem cells using an improved method

Lee,

Takahashi,

Sasaki

et al. 2024

FEBS Letters

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The colonic epithelium plays a crucial role in gastrointestinal homeostasis, and colon organoids enable investigation into the molecular mechanisms underlying colonic physiology. However, the method for differentiating induced pluripotent stem cells (iPSCs) into human colon organoids (HCOs) is not necessarily standardized, and studies using HCOs are limited. This study refines the differentiation of HCOs by comparing two protocols reported in Cell Stem Cell and Nature Medicine journals. The former protocol, which uses transient bone morphogenetic protein 2 (BMP2) signaling activation, demonstrated superior efficacy in upregulating colon‐specific markers. Additionally, adenovirus‐mediated transduction of the transcription factors HOXD13 or SATB2 during hindgut endoderm development, together with BMP2 treatment, enhanced colonic identity, suggesting improved colonic maturation. This optimized protocol advances the generation of mature HCOs, offering a better model for investigating colonic epithelial biology and pathology.

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Collinear Hox-Hox interactions are involved in patterning the vertebrate anteroposterior (A-P) axis

Cited by 26 publications

References 48 publications

What are the roles of retinoids, other morphogens, and Hox genes in setting up the vertebrate body axis?

What are the roles of retinoids, other morphogens, and Hox genes in setting up the vertebrate body axis?

Hoxc6 loss of function truncates the main body axis in Xenopus

Human colon organoid differentiation from induced pluripotent stem cells using an improved method

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