Editorial highlights

IF 2 3区 生物学 Q2 ANATOMY & MORPHOLOGY
Paul A. Trainor
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Over time, limbs acquired complex characteristics built upon anterior-posterior, proximal-distal, and dorsal-ventral axes. Although limb development and patterning has been well studied, we still have much to learn about the dorsal-ventral axis. The dorsal domain of the limb houses the extensor muscles, ligaments, tendons, nerves, and vessels, whereas the ventral region contains flexor muscles among other tissues and structures. This review discusses our current understanding of dorsal-ventral patterning of the limb, bringing together the results of classic experiments with modern research, concepts, and interpretations. With an emphasis on Lmx1b, which specifies dorsal character and subsequently fate, the authors consider the role of dorsal-ventral patterning in the evolution of paired appendages and the association of variants in LMX1B in association with nail-patella syndrome. Finally, the role of dorsoventral patterning and polarity in digit tip regeneration in mammals is also considered further informing our understanding of limb function and evolutionary adaptations.</p><p><b>Neurodevelopment</b> “Disruption of Fuz in mouse embryos generates hypoplastic hindbrain development and reduced cranial nerve ganglia” by Carlo Donato Caiaffa, Yogeshwari Ambekar, Manmohan Singh, Ying Linda Lin, Bogdan Wlodarczyk, Salavat Aglyamov, Giuliano Scarcelli, Kirill Larin, and Richard Finnell. <i>Dev Dyn</i>. 253:9, pp. 846–858. https://doi.org/10.1002/dvdy.702. Neurulation is the process of neural tube formation from the neural plate, which subsequently forms the central nervous system, while also contributing to the peripheral nervous system. Perturbation of the early steps of neurulation can lead to neural tube defects, which are one of the most common birth defects, affecting about two in every 100 live births, or about 300,000 cases per year worldwide. Genetic mutations, environmental factors, and nutritional imbalances critically underpin the pathogenesis of most neural tube defects. The Fuz gene forms part of a macromolecular planar polarity effector required for ciliogenesis, and consequently, <i>Fuz</i> knockout mice exhibit exencephaly of spina bifida. Underpinning these phenotypes, <i>Fuz</i> mutant embryos exhibit hypoplastic cranial and paravertebral ganglia, and a smaller hindbrain, in association with persistent reduction of ventral neuroepithelial stiffness in the notochord. Fuz is required for sustaining neuroepithelial integrity during neural tube closure and development. This work shows for the first time that abnormal hindbrain morphology and persistent loss of neuroepithelial stiffness precede exencephaly in <i>Fuz</i> mutant mouse embryos.</p><p><b>Whale Embryogenesis</b> “Protein signaling and morphological development of the tail fluke in the embryonic beluga whale” by Lia. Gavazzi, Manas Nair, Robert. Suydam, Sharon Usip, Hans Thewissen, and Lisa Cooper. <i>Dev Dyn</i>. 253:9, pp. 859–874. https://doi.org/10.1002/dvdy.704. During the land-to-sea transition of cetaceans (whales, dolphins, and porpoises), the hindlimbs were lost and replaced by an elaborate tail fluke. Modern cetaceans utilize flukes for lift-based propulsion, but nothing is known about the molecular origins of underpinning of their anatomical development and function during embryogenesis. This study tests the hypothesis that classic well recognized signals associated with outgrowth and patterning of tetrapod limbs, also regulate tail fluke development. Focusing on the beluga whale (<i>Delphinapterus leucas</i>) as a case study, the authors initially show that bilaterally symmetrical flukes of cetaceans are supported by caudal tail vertebrae and dense connective tissues that are enveloped by skin. Next the authors show that epidermal WNT and FGF signals, and mesenchymal/epidermal SHH and GREM signals, mimic the patterns characteristic of vertebrate limb development. This implies that the genes and proteins that regulate limb outgrowth and patterning also govern the outgrowth and shape of the evolutionarily novel tail fluke appendage in cetaceans. 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引用次数: 0

Abstract

Every organism is a model organism for understanding development, evolution, disease, and regeneration, and we have only begun to scratch the surface of the interdisciplinary genetic, molecular, cellular, and developmental mechanisms that regulate these biological processes. These “Highlights” denote exciting advances recently reported in Developmental Dynamics that illustrate the complex dynamics of developmental biology.

Limb Development “The limb dorsoventral axis: Lmx1b's role in development, pathology, evolution, and regeneration” by Alejandro Castilla-Ibeas, Sofía Zdral, Kerby Oberg, and Marian Ros. Dev Dyn. 253:9, pp. 798–814. https://doi.org/10.1002/dvdy.695. Limbs, which are crucial for locomotion, are thought to have evolved from fins in an aquatic ancestor as an adaptation to shallow water. Over time, limbs acquired complex characteristics built upon anterior-posterior, proximal-distal, and dorsal-ventral axes. Although limb development and patterning has been well studied, we still have much to learn about the dorsal-ventral axis. The dorsal domain of the limb houses the extensor muscles, ligaments, tendons, nerves, and vessels, whereas the ventral region contains flexor muscles among other tissues and structures. This review discusses our current understanding of dorsal-ventral patterning of the limb, bringing together the results of classic experiments with modern research, concepts, and interpretations. With an emphasis on Lmx1b, which specifies dorsal character and subsequently fate, the authors consider the role of dorsal-ventral patterning in the evolution of paired appendages and the association of variants in LMX1B in association with nail-patella syndrome. Finally, the role of dorsoventral patterning and polarity in digit tip regeneration in mammals is also considered further informing our understanding of limb function and evolutionary adaptations.

Neurodevelopment “Disruption of Fuz in mouse embryos generates hypoplastic hindbrain development and reduced cranial nerve ganglia” by Carlo Donato Caiaffa, Yogeshwari Ambekar, Manmohan Singh, Ying Linda Lin, Bogdan Wlodarczyk, Salavat Aglyamov, Giuliano Scarcelli, Kirill Larin, and Richard Finnell. Dev Dyn. 253:9, pp. 846–858. https://doi.org/10.1002/dvdy.702. Neurulation is the process of neural tube formation from the neural plate, which subsequently forms the central nervous system, while also contributing to the peripheral nervous system. Perturbation of the early steps of neurulation can lead to neural tube defects, which are one of the most common birth defects, affecting about two in every 100 live births, or about 300,000 cases per year worldwide. Genetic mutations, environmental factors, and nutritional imbalances critically underpin the pathogenesis of most neural tube defects. The Fuz gene forms part of a macromolecular planar polarity effector required for ciliogenesis, and consequently, Fuz knockout mice exhibit exencephaly of spina bifida. Underpinning these phenotypes, Fuz mutant embryos exhibit hypoplastic cranial and paravertebral ganglia, and a smaller hindbrain, in association with persistent reduction of ventral neuroepithelial stiffness in the notochord. Fuz is required for sustaining neuroepithelial integrity during neural tube closure and development. This work shows for the first time that abnormal hindbrain morphology and persistent loss of neuroepithelial stiffness precede exencephaly in Fuz mutant mouse embryos.

Whale Embryogenesis “Protein signaling and morphological development of the tail fluke in the embryonic beluga whale” by Lia. Gavazzi, Manas Nair, Robert. Suydam, Sharon Usip, Hans Thewissen, and Lisa Cooper. Dev Dyn. 253:9, pp. 859–874. https://doi.org/10.1002/dvdy.704. During the land-to-sea transition of cetaceans (whales, dolphins, and porpoises), the hindlimbs were lost and replaced by an elaborate tail fluke. Modern cetaceans utilize flukes for lift-based propulsion, but nothing is known about the molecular origins of underpinning of their anatomical development and function during embryogenesis. This study tests the hypothesis that classic well recognized signals associated with outgrowth and patterning of tetrapod limbs, also regulate tail fluke development. Focusing on the beluga whale (Delphinapterus leucas) as a case study, the authors initially show that bilaterally symmetrical flukes of cetaceans are supported by caudal tail vertebrae and dense connective tissues that are enveloped by skin. Next the authors show that epidermal WNT and FGF signals, and mesenchymal/epidermal SHH and GREM signals, mimic the patterns characteristic of vertebrate limb development. This implies that the genes and proteins that regulate limb outgrowth and patterning also govern the outgrowth and shape of the evolutionarily novel tail fluke appendage in cetaceans. This body of work therefore provides key insights into the evolution and development of a novel organ.

社论要点
每种生物都是了解发育、进化、疾病和再生的模式生物,而我们对调控这些生物过程的跨学科遗传、分子、细胞和发育机制的研究才刚刚起步。这些 "亮点 "指出了《发育生物学》最近报道的令人兴奋的进展,说明了发育生物学的复杂动态:Lmx1b 在发育、病理、进化和再生中的作用",作者:Alejandro Castilla-Ibeas、Sofía Zdral、Kerby Oberg 和 Marian Ros。Dev Dyn.253:9, pp. 798-814. https://doi.org/10.1002/dvdy.695。四肢对运动至关重要,人们认为四肢是由水生祖先的鳍进化而来,以适应浅水环境。随着时间的推移,四肢在前-后、近-远和背-腹轴的基础上获得了复杂的特征。尽管对四肢的发育和模式化已经进行了深入研究,但我们对背腹轴仍有很多需要了解的地方。肢体的背侧区域包括伸肌、韧带、肌腱、神经和血管,而腹侧区域则包括屈肌以及其他组织和结构。这篇综述讨论了我们目前对肢体背-腹模式化的理解,将经典实验结果与现代研究、概念和解释结合在一起。Lmx1b 规定了肢体的背侧特征以及随后的命运,作者以 Lmx1b 为重点,探讨了背腹模式化在成对附肢进化中的作用,以及 LMX1B 变异与甲髌综合征的关联。最后,作者还探讨了背腹形态和极性在哺乳动物指尖再生中的作用,进一步加深了我们对肢体功能和进化适应性的理解。神经发育 "小鼠胚胎中 Fuz 的破坏导致后脑发育不良和颅神经节减少":Carlo Donato Caiaffa、Yogeshwari Ambekar、Manmohan Singh、Ying Linda Lin、Bogdan Wlodarczyk、Salavat Aglyamov、Giuliano Scarcelli、Kirill Larin 和 Richard Finnell。Dev Dyn.253:9, pp. 846-858. https://doi.org/10.1002/dvdy.702。神经形成是从神经板开始的神经管形成过程,随后形成中枢神经系统,同时也对周围神经系统做出贡献。神经形成的早期步骤受到干扰会导致神经管缺陷,而神经管缺陷是最常见的出生缺陷之一,每 100 个活产婴儿中就有 2 例,全球每年约有 30 万例。基因突变、环境因素和营养失衡是大多数神经管缺陷的重要发病机制。Fuz 基因是纤毛生成所需的大分子平面极性效应子的一部分,因此,Fuz 基因敲除小鼠表现出脊柱裂的无脑畸形。在这些表型的基础上,Fuz突变体胚胎的颅神经节和椎旁神经节发育不良,后脑较小,同时脊索腹侧神经上皮硬度持续降低。在神经管闭合和发育过程中,Fuz 是维持神经上皮完整性所必需的。这项研究首次表明,在 Fuz 突变的小鼠胚胎中,异常的后脑形态和神经上皮硬度的持续丧失先于无脑畸形。Gavazzi, Manas Nair, Robert.Suydam、Sharon Usip、Hans Thewissen 和 Lisa Cooper。Dev Dyn.253:9, pp. 859-874. https://doi.org/10.1002/dvdy.704。在鲸目动物(鲸鱼、海豚和鼠海豚)从陆地向海洋过渡的过程中,后肢消失了,取而代之的是精致的尾鳍。现代鲸目动物利用尾鳍进行升力推进,但对其在胚胎发育过程中的解剖结构和功能的分子起源却一无所知。本研究验证了一个假设,即公认的与四足动物四肢的生长和模式化有关的经典信号也能调节尾鳍的发育。作者以白鲸(Delphinapterus leucas)为研究对象,首先展示了鲸类动物两侧对称的尾鳍由尾部椎骨和皮肤包裹的致密结缔组织支撑。接下来,作者表明,表皮 WNT 和 FGF 信号以及间质/表皮 SHH 和 GREM 信号模仿了脊椎动物肢体发育的特征模式。这意味着,调控肢体生长和模式化的基因和蛋白质也调控着鲸类进化过程中新颖的尾套附属物的生长和形状。因此,这些研究成果为了解一种新型器官的进化和发育提供了重要的启示。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Developmental Dynamics
Developmental Dynamics 生物-发育生物学
CiteScore
5.10
自引率
8.00%
发文量
116
审稿时长
3-8 weeks
期刊介绍: Developmental Dynamics, is an official publication of the American Association for Anatomy. This peer reviewed journal provides an international forum for publishing novel discoveries, using any model system, that advances our understanding of development, morphology, form and function, evolution, disease, stem cells, repair and regeneration.
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