Neural Regeneration in<i>Xenopus</i>Tadpoles during Metamorphosis

Moreno, Mauricio; Tapia, Karina; Larraı́n, Juan

doi:10.1002/9781118492833.ch15

“…It involves dramatic changes in morphology and physiology, including remodeling of tadpole organs (e.g., the oral and gastrointestinal tract) into their adult form, resorption of tadpole-specific structures (e.g., the gill and tail), and development of adult-specific tissues such as limbs [ 6 , 7 ]. It is a model system for studying the molecular network underlying the T3-mediated apoptosis, cellular reprogramming, and organogenesis in vertebrates [ 8 – 11 ]. Metamorphic climax is also a focus in ecology and toxicology studies of amphibians because it is a critical stage determining individual survival and population dynamics [ 12 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

Zhu

¹

,

Zhao

²

,

Wang

³

et al. 2020

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Background Metamorphic climax is the crucial stage of amphibian metamorphosis responsible for the morphological and functional changes necessary for transition to a terrestrial habitat. This developmental period is sensitive to environmental changes and pollution. Understanding its metabolic basis and requirements is significant for ecological and toxicological research. Rana omeimontis tadpoles are a useful model for investigating this stage as their liver is involved in both metabolic regulation and fat storage. Results We used a combined approach of transcriptomics and metabolomics to study the metabolic reorganization during natural and T3-driven metamorphic climax in the liver and tail of Rana omeimontis tadpoles. The metabolic flux from the apoptotic tail replaced hepatic fat storage as metabolic fuel, resulting in increased hepatic amino acid and fat levels. In the liver, amino acid catabolism (transamination and urea cycle) was upregulated along with energy metabolism (TCA cycle and oxidative phosphorylation), while the carbohydrate and lipid catabolism (glycolysis, pentose phosphate pathway (PPP), and β-oxidation) decreased. The hepatic glycogen phosphorylation and gluconeogenesis were upregulated, and the carbohydrate flux was used for synthesis of glycan units (e.g., UDP-glucuronate). In the tail, glycolysis, β-oxidation, and transamination were all downregulated, accompanied by synchronous downregulation of energy production and consumption. Glycogenolysis was maintained in the tail, and the carbohydrate flux likely flowed into both PPP and the synthesis of glycan units (e.g., UDP-glucuronate and UDP-glucosamine). Fatty acid elongation and desaturation, as well as the synthesis of bioactive lipid (e.g., prostaglandins) were encouraged in the tail during metamorphic climax. Protein synthesis was downregulated in both the liver and tail. The significance of these metabolic adjustments and their potential regulation mechanism are discussed. Conclusion The energic strategy and anabolic requirements during metamorphic climax were revealed at the molecular level. Amino acid made an increased contribution to energy metabolism during metamorphic climax. Carbohydrate anabolism was essential for the body construction of the froglets. The tail was critical in anabolism including synthesizing bioactive metabolites. These findings increase our understanding of amphibian metamorphosis and provide background information for ecological, evolutionary, conservation, and developmental studies of amphibians.

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“…Since the mid‐20th century, the African clawed frog, Xenopus laevis , has become one of the most widely used model organisms in biology (Harland & Grainger, ; Porro & Richards, ). Especially in neurobiology, Xenopus embryos, tadpoles, and adults are used as models in pathological, developmental, physiological, and behavioral studies (Cannatella & De Sa, ; Cervino, Paz, & Frontera, ; Cline & Kelly, ; Dong et al, ; Edwards‐Faret et al, ; Frankenhaeuser & Huxley, ; Gouchie, Roberts, & Wassersug, ; Katz, Potel, & Wassersug, ; Lee‐Liu, Méndez‐Olivos, Muñoz, & Larraín, ; McKeown, Sharma, Sharipov, Shen, & Cline, ; Moreno, Tapia, & Larrain, ; Pieper, Eagleson, Wosniok, & Schlosser, ; Pratt & Khakhalin, ; Roberts, Walford, Soffe, & Yoshida, ; Schlosser & Northcutt, ; Simmons, Costa, & Gerstein, ; Wassersug & Hessler, ; Young & Poo, ). It is therefore surprising, that only one study (Paterson, ) on the anatomy of the cranial nerves of X. laevis tadpoles exists.…”

Section: Introductionmentioning

confidence: 99%

Three‐dimensional reconstruction of the cranial and anterior spinal nerves in early tadpoles of Xenopus laevis (Pipidae, Anura)

Naumann

¹

,

Olsson

²

2017

J of Comparative Neurology

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Xenopus laevis is one of the most widely used model organism in neurobiology. It is therefore surprising, that no detailed and complete description of the cranial nerves exists for this species. Using classical histological sectioning in combination with fluorescent whole mount antibody staining and micro-computed tomography we prepared a detailed innervation map and a freely-rotatable three-dimensional (3D) model of the cranial nerves and anterior-most spinal nerves of early X. laevis tadpoles. Our results confirm earlier descriptions of the pre-otic cranial nerves and present the first detailed description of the post-otic cranial nerves. Tracing the innervation, we found two previously undescribed head muscles (the processo-articularis and diaphragmatico-branchialis muscles) in X. laevis. Data on the cranial nerve morphology of tadpoles are scarce, and only one other species (Discoglossus pictus) has been described in great detail. A comparison of Xenopus and Discoglossus reveals a relatively conserved pattern of the post-otic and a more variable morphology of the pre-otic cranial nerves. Furthermore, the innervation map and the 3D models presented here can serve as an easily accessible basis to identify alterations of the innervation produced by experimental studies such as genetic gain- and loss of function experiments.

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“…It involves dramatic changes in morphology and physiology, including remodeling of tadpole organs (e.g., the oral and gastrointestinal tract) into their adult form, resorption of tadpole-speci c structures (e.g., the gill and tail), and development of adultspeci c tissues such as limbs [6,7]. It is a model system for studying the molecular network underlying the T3-mediated apoptosis, cellular reprogramming, and organogenesis in vertebrates [8][9][10][11].…”

Section: Introductionmentioning

confidence: 99%

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

Zhu

¹

,

Zhao

²

,

Wang

³

et al. 2020

Preprint

0

View full text Add to dashboard Cite

Background Metamorphic climax is the crucial stage of amphibian metamorphosis responsible for the morphological and functional changes necessary for transition to a terrestrial habitat. This developmental period is sensitive to environmental changes and pollution. Understanding its metabolic basis and requirements is significant for ecological and toxicological research. Rana omeimontis tadpoles are a useful model for investigating this stage as their liver is involved in both metabolic regulation and fat storage. Results We used a combined approach of transcriptomics and metabolomics to study the metabolic reorganization during natural and T3-driven metamorphic climax in the liver and tail of Rana omeimontis tadpoles. The metabolic flux from the apoptotic tail replaced hepatic fat storage as metabolic fuel, resulting in increased hepatic amino acid and fat levels. In the liver, amino acid catabolism (transamination and urea cycle) was upregulated along with energy metabolism (TCA cycle and oxidative phosphorylation), while the carbohydrate and lipid catabolism (glycolysis, pentose phosphate pathway (PPP), and β-oxidation) decreased. The hepatic glycogen phosphorylation and gluconeogenesis were upregulated, and the carbohydrate flux was used for synthesis of glycan units (e.g., UDP-glucuronate). In the tail, glycolysis, β-oxidation, and transamination were all downregulated, accompanied by synchronous downregulation of energy production and consumption. Glycogenolysis was maintained in the tail, and the carbohydrate flux likely flowed into both PPP and the synthesis of glycan units (e.g., UDP-glucuronate and UDP-glucosamine). Fatty acid elongation and desaturation, as well as the synthesis of bioactive lipid (e.g., prostaglandins) were encouraged in the tail during metamorphic climax. Protein synthesis was downregulated in both the liver and tail. The significance of these metabolic adjustments and their potential regulation mechanism are discussed. Conclusion The energic strategy and anabolic requirements during metamorphic climax were revealed at the molecular level. Amino acid made an increased contribution to energy metabolism during metamorphic climax. Carbohydrate anabolism was essential for the body construction of the froglets. The tail was critical in anabolism including synthesizing bioactive metabolites. These findings increase our understanding of amphibian metamorphosis and provide background information for ecological, evolutionary, conservation, and developmental studies of amphibians.

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Neural Regeneration inXenopusTadpoles during Metamorphosis

Cited by 4 publications

References 71 publications

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

Three‐dimensional reconstruction of the cranial and anterior spinal nerves in early tadpoles of Xenopus laevis (Pipidae, Anura)

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

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