Molecular Dynamics of Retinoic Acid-Induced Craniofacial Malformations: Implications for the Origin of Gnathostome Jaws

Vieux-Rochas, Maxence; Coen, Laurent; Sato, Takahiro; Kurihara, Yukiko; Gitton, Yorick; Barbieri, Ottavia; Blay, Karine Le; Merlo, Giorgio R.; Ekker, Marc; Kurihara, Hiroki; Janvier, Philippe; Levi, Giovanni

doi:10.1371/journal.pone.0000510

Cited by 45 publications

(58 citation statements)

References 68 publications

(71 reference statements)

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“…The dlx genes encode homeodomain transcription factors that are involved in branchial arch patterning and craniofacial development, and have been proposed to be regulated by retinoid signaling (Vieux-Rochas et al, 2007). The expression of Dlx1, 2, 5, and 6 was analyzed, and no changes in branchial arch expression were observed in Cyp26b1 Ϫ/Ϫ embryos at E10.5 (results not shown).…”

Section: Embryosmentioning

confidence: 97%

Genetic disruption of CYP26B1 severely affects development of neural crest derived head structures, but does not compromise hindbrain patterning

MacLean

Dollé

Petkovich

2009

Developmental Dynamics

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Cyp26b1 encodes a cytochrome-P450 enzyme that catabolizes retinoic acid (RA), a vitamin A derived signaling molecule. We have examined Cyp26b1 ؊/؊ mice and report that mutants exhibit numerous abnormalities in cranial neural crest cell derived tissues. At embryonic day (E) 18.5 Cyp26b1 ؊/؊ animals exhibit a truncated mandible, abnormal tooth buds, reduced ossification of calvaria, and are missing structures of the maxilla and nasal process. Some of these abnormalities may be due to defects in formation of Meckel's cartilage, which is truncated with an unfused distal region at E14.5 in mutant animals. Despite the severe malformations, we did not detect any abnormalities in rhombomere segmentation, or in patterning and migration of anterior hindbrain derived neural crest cells. Abnormal migration of neural crest cells toward the posterior branchial arches was observed, which may underlie defects in larynx and hyoid development. These data suggest different periods of sensitivity of anterior and posterior hindbrain neural crest derivatives to elevated levels of RA in the absence of CYP26B1. Developmental Dynamics 238: 732-745, 2009.

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Section: Embryosmentioning

confidence: 97%

Genetic disruption of CYP26B1 severely affects development of neural crest derived head structures, but does not compromise hindbrain patterning

MacLean

Dollé

Petkovich

2009

Developmental Dynamics

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“…It may represent an important mechanism for driving morphological changes in facial architecture during evolution. Such a mechanism is reinforced by experiments implicating elevation of RA that also lead to skull and face bone defects (Vieux-Rochas et al, 2007;Maclean et al, 2009). In both Rara/g-and Rara/b-null mutants, the alisphenoid and incus, which are derived from the maxillary process of BA1, are fused through a supernumerary piece of cartilage to form a pterygoquadrate element that has been lost during mammalian evolution .…”

Section: Rars Are Largely Dispensable In Ncc For the Early Morphogenementioning

confidence: 97%

“…FB, forebrain; NP, nasal process. Huang et al, 1998), and considering that BA endoderm is a primary target tissue of RA-induced teratogenesis (Matt et al, 2003;VieuxRochas et al, 2007), a model in which RARs in the endoderm regulate the formation of the pharyngeal pouches has been proposed (Mark et al, 2004;Vieux-Rochas et al, 2007).…”

Section: Rars Are Not Required In Ncc For the Formation Of Branchial mentioning

confidence: 99%

“…Malformations of cranial NCCderived structures are generated upon impairment of retinoic acid (RA) signaling in various vertebrate species Mark et al, 1998;Schneider et al, 2001;Jiang et al, 2002a,b;Kopinke et al, 2006;Halilagic et al, 2007;Vieux-Rochas et al, 2007). The effects of RA on embryonic development are mediated by heterodimers between RA receptor (RAR) isotypes (RARa, b, and c) that are widely expressed in the embryo (Mollard et al, 2000;Dollé, 2009) and rexinoid receptors (RXRs; Chambon, 1996;Mark et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Retinoic acid receptors exhibit cell‐autonomous functions in cranial neural crest cells

Dupé

Pellerin

2009

Developmental Dynamics

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Previous work has emphasized the crucial role of retinoic acid (RA) in the ontogenesis of the vast majority of mesenchymal structures derived from the neural crest cells (NCC), which migrate through, or populate, the frontonasal process and branchial arches. Using somatic mutagenesis in the mouse, we have selectively ablated two or three retinoic acid receptors (i.e., RARa/RARb, RARa/RARc and RARa/RARb/ RARc) in NCC. By rigorously analyzing these mutant mice, we found that survival and migration of NCC is normal until gestational day 10.5, suggesting that RAR-dependent signaling is not intrinsically required for the early steps of NCC development. However, ablation of Rara and Rarg genes in NCC yields an agenesis of the median portion of the face, demonstrating that RARa and RARc act cell-autonomously in postmigratory NCC to control the development of structures derived from the frontonasal process. In contrast, ablation of the three Rar genes in NCC leads to less severe defects of the branchial arches derived structures compared with Rar compound null mutants. Therefore, RARs exert a function in the NCC as well as in a separated cell population. This work demonstrates that RARs use distinct mechanisms to pattern cranial NCC. INTRODUCTIONThe morphogenesis of the craniofacial region results from complex developmental processes involving the migration of neural crest cells (NCC) and their subsequent differentiation through interactions with endoderm and ectoderm (Veitch et al., 1999;Trainor and Krumlauf, 2001). Cranial NCC arise from fore-, mid-, and hindbrain in distinct migratory streams. Fore-and midbrain NCC give rise to the frontonasal skeleton, whereas pre-otic hindbrain populations colonize the first two branchial arches (BAs), where they differentiate to form skeletal elements of the jaw, middle ear and tongue. Cardiac NCC participate in the development of aortic arch arteries, as well as thymus, thyroid, and parathyroid glands (Le Douarin et al., 1993;Santagati and Rijli, 2003). Because patterning and morphogenesis of these craniofacial structures require a finely orchestrated series of tissue interactions (Graham and Smith, 2001;Trainor and Krumlauf, 2001), perturbation of different processes may yield similar developmental abnormalities. For instance, inactivation of genes expressed in either NCC, endoderm, or ectoderm, results in similar cardiovascular defects, as remodeling of BA arteries into the definitive arterial vessels and heart outflow tract requires coordinated communication between NCC, endoderm and ectoderm (Depew ABBREVIATIONS BA branchial arch E embryonic day NCC neural crest cells RA retinoic acid ALDH1A retinaldehyde dehydrogenase RAR retinoic acid receptor RXR rexinoid receptor VAD vitamin A-deficient

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“…Surgical removal and grafting of small territories of the foregut endoderm at different developmental stages has shown that this epithelium provides to CNCCs part of the topographic information needed to form jaw structures (Couly et al, 1993;Kontges and Lumsden, 1996;Kurihara et al, 1994;Le Douarin and Dupin, 2003;Noden and Trainor, 2005;Trainor and Tam, 1995). The molecular nature of the endodermal signals is only partly known, as experimental evidence suggest that FGFs, BMPs, Edn1, and Shh are surely involved (Benouaiche et al, 2008;Ozeki et al, 2004;Vieux-Rochas et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Spatio‐temporal dynamics of gene expression of the Edn1‐Dlx5/6 pathway during development of the lower jaw

Vieux-Rochas

Mantero

Heude

et al. 2010

Genesis

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Summary: The morphogenesis of the vertebrate skull results from highly dynamic integrated processes involving the exchange of signals between the ectoderm, the endoderm, and cephalic neural crest cells (CNCCs). Before migration CNCCs are not committed to form any specific skull element, molecular signals exchanged in restricted regions of tissue interaction are crucial in providing positional identity to the CNCCs mesenchyme and activate the specific morphogenetic process of different skeletal components of the head. In particular, the endothelin-1 (Edn1)-dependent activation of Dlx5 and Dlx6 in CNCCs that colonize the first pharyngeal arch (PA1) is necessary and sufficient to specify maxillo-mandibular identity. Here, to better analyze the spatio-temporal dynamics of this process, we associate quantitative gene expression analysis with detailed examination of skeletal phenotypes resulting from combined allelic reduction of Edn1, Dlx5, and Dlx6. We show that Edn1-dependent and -independent regulatory pathways act at different developmental times in distinct regions of PA1. The Edn1?Dlx5/6?Hand2 pathway is already active at E9.5 during early stages of CNCCs colonization. At later stages (E10.5) the scenario is more complex: we propose a model in which PA1 is subdivided into four adjacent territories in which distinct regulations are taking place. This new developmental model may provide a conceptual framework to interpret the craniofacial malformations present in several mouse mutants and in human first arch syndromes. More in general, our findings emphasize the importance of quantitative gene expression in the fine control of morphogenetic events. genesis 48:362-373, 2010.

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Molecular Dynamics of Retinoic Acid-Induced Craniofacial Malformations: Implications for the Origin of Gnathostome Jaws

Cited by 45 publications

References 68 publications

Genetic disruption of CYP26B1 severely affects development of neural crest derived head structures, but does not compromise hindbrain patterning

Genetic disruption of CYP26B1 severely affects development of neural crest derived head structures, but does not compromise hindbrain patterning

Retinoic acid receptors exhibit cell‐autonomous functions in cranial neural crest cells

Spatio‐temporal dynamics of gene expression of the Edn1‐Dlx5/6 pathway during development of the lower jaw

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