Abstract
Limb autotomy and regeneration represent distinctive responses of crustaceans to environmental stress. Glucose metabolism plays a pivotal role in energy generation for tissue development and regeneration across various species. However, the relationship between glucose metabolism and tissue regeneration in crustaceans remains elusive. Therefore, this study is aimed at analyzing the alterations of glucose metabolic profile during limb autotomy and regeneration in Eriocheir sinensis, while also evaluating the effects of carbohydrate supplementation on limb regeneration. The results demonstrated that limb autotomy triggered a metabolic profile adaption at the early stage of regeneration. Hemolymph glucose levels were elevated, and multiple glucose catabolic pathways were enhanced in the hepatopancreas. Additionally, glucose and ATP levels in the regenerative limb were upregulated, along with increased expression of glucose transporters. Furthermore, the gene expression and activity of enzymes involved in gluconeogenesis were repressed in the hepatopancreas. These findings indicate that limb regeneration triggers metabolic profile adaptations to meet the elevated energy requirements. Moreover, the study observed that supplementation with corn starch enhanced limb regeneration capacity by promoting wound healing and blastema growth. Interestingly, dietary carbohydrate addition influenced limb regeneration by stimulating gluconeogenesis rather than glycolysis in the regenerative limb. Thus, these results underscore the adaptation of glucose metabolism during limb autotomy and regeneration, highlighting its essential role in the limb regeneration process of E. sinensis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated and analyzed in this study are available within the article and the supplementary information.
References
Abrams MJ, Tan FH, Li Y et al (2021) A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice. Elife 10. https://doi.org/10.7554/eLife.65092
Brandão AS, Borbinha J, Pereira T et al (2022) A regeneration-triggered metabolic adaptation is necessary for cell identity transitions and cell cycle re-entry to support blastema formation and bone regeneration. Elife 11. https://doi.org/10.7554/eLife.76987
Cui Z, Liu Y, Yuan J et al (2021) The Chinese mitten crab genome provides insights into adaptive plasticity and developmental regulation. Nat Commun 12:2395. https://doi.org/10.1038/s41467-021-22604-3
Das S, Durica DS (2013) Ecdysteroid receptor signaling disruption obstructs blastemal cell proliferation during limb regeneration in the fiddler crab, Uca pugilator. Mol Cell Endocrinol 365:249–259
Fleming PA, Muller D, Bateman PW (2007) Leave it all behind: a taxonomic perspective of autotomy in invertebrates. Biol Rev 82:481–510
Folmes CDL, Dzeja PP, Nelson TJ, Terzic A (2012) Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11:596–606
Folmes CDL, Nelson TJ, Martinez-Fernandez A et al (2011) Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14:264–271
Fukuda R, Marín‐Juez R, El‐Sammak H et al (2020) Stimulation of glycolysis promotes cardiomyocyte proliferation after injury in adult zebrafish. EMBO Rep 21. https://doi.org/10.15252/embr.201949752
Ghosh-Choudhary S, Liu J, Finkel T (2020) Metabolic regulation of cell fate and function. Trends Cell Biol 30:201–212
Goldstein SA, Elwyn DH (1989) The effects of injury and sepsis on fuel utilization. Annu Rev Nutr 9:445–473
Li J, Tian Y, Li X et al (2022) Insulin-like signaling promotes limb regeneration in the Chinese mitten crab (Eriocheir sinensis). Fish Shellfish Immunol 122:268–275
Li W-F, Li S, Liu J et al (2021) Vital carbohydrate and lipid metabolites in serum involved in energy metabolism during pubertal molt of mud crab (Scylla paramamosain). Metabolites 11:651. https://doi.org/10.3390/metabo11100651
Loeffler J, Duda GN, Sass FA, Dienelt A (2018) The metabolic microenvironment steers bone tissue regeneration. Trends Endocrinol Metab 29:99–110
Love NR, Chen Y, Bonev B et al (2011) Genome-wide analysis of gene expression during Xenopus tropicalis tadpole tail regeneration. BMC Dev Biol 11:70. https://doi.org/10.1186/1471-213X-11-70
Love NR, Ziegler M, Chen Y, Amaya E (2014) Carbohydrate metabolism during vertebrate appendage regeneration: what is its role? How is it regulated? BioEssays 36:27–33
Ly CH, Lynch GS, Ryall JG (2020) A metabolic roadmap for somatic stem cell fate. Cell Metab 31:1052–1067
Osuma EA, Riggs DW, Gibb AA, Hill BG (2018) High throughput measurement of metabolism in planarians reveals activation of glycolysis during regeneration. Regeneration 5:78–86
Panopoulos AD, Yanes O, Ruiz S et al (2012) The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 22:168–177
Patel JH, Ong DJ, Williams CR et al (2022) Elevated pentose phosphate pathway flux supports appendage regeneration. Cell Rep 41:111552. https://doi.org/10.1016/j.celrep.2022.111552
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108
Shinji J, Gotoh H, Miyanishi H et al (2019) The activin signaling transcription factor Smox is an essential regulator of appendage size during regeneration after autotomy in the crayfish. Evol Dev 21:44–55
Shyh-Chang N, Zhu H, Yvanka de Soysa T et al (2013) Lin28 enhances tissue repair by reprogramming cellular metabolism. Cell 155:778–792
Sinclair JW, Hoying DR, Bresciani E et al (2021) The Warburg effect is necessary to promote glycosylation in the blastema during zebrafish tail regeneration. NPJ Regen Med 6:55. https://doi.org/10.1038/s41536-021-00163-x
Varela-Rodríguez H, Abella-Quintana DG, Espinal-Centeno A et al (2020) Functional characterization of the Lin28/let-7 circuit during forelimb regeneration in Ambystoma mexicanum and its influence on metabolic reprogramming. Front Cell Dev Biol 8. https://doi.org/10.3389/fcell.2020.562940
Vogg MC, Buzgariu W, Suknovic NS, Galliot B (2021) Cellular, metabolic, and developmental dimensions of whole-body regeneration in Hydra. Cold Spring Harb Perspect Biol 13:a040725. https://doi.org/10.1101/cshperspect.a040725
Wang J, Chen X, Hou X et al (2022) “Omics” data unveil early molecular response underlying limb regeneration in the Chinese mitten crab, Eriocheir sinensis. Sci Adv 8. https://doi.org/10.1126/sciadv.abl4642
Wang L, Chen H, Wang L, Song L (2020) An insulin-like peptide serves as a regulator of glucose metabolism in the immune response of Chinese mitten crab Eriocheir sinensis. Dev Comp Immunol 108:103686. https://doi.org/10.1016/j.dci.2020.103686
Yang X, Zhang C, Huang G et al (2018) Cellular and biochemical parameters following autotomy and ablation-mediated cheliped loss in the Chinese mitten crab, Eriocheir sinensis. Dev Comp Immunol 81:33–43
Zhang C, Yang X, Xu M et al (2018) Melatonin promotes cheliped regeneration, digestive enzyme function, and immunity following autotomy in the Chinese mitten crab, Eriocheir sinensis. Front Physiol 9. https://doi.org/10.3389/fphys.2018.00269
Zhang X, Huang C, Yang Y et al (2022) Dietary corn starch levels regulated insulin-mediated glycemic responses and glucose homeostasis in swimming crab (Portunus trituberculatus). Aquac Nutr 2022:1–15
Funding
This work was supported by the National Natural Science Foundation of China (81903776) and the National Key R&D Program of China (2018YFD0901301).
Author information
Authors and Affiliations
Contributions
JL designed the experiment, performed the experiments, and revised the manuscript. XL performed the experiments, analyzed the data, and prepared all figures. SF participated in the enzyme activity assay and qRT-PCR analysis. YM participated in the enzyme activity analysis. XL participated in the feed trail and sample collection. XZ participated in sample collection and analysis. GL raised the crabs and participated the feed trail. JS supervised the study and provided funding. All authors reviewed and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethical Approval
All animal protocols were approved by the Ethics Committee of Tianjin Normal University (Registration number: SD2020009).
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, J., Li, X., Fu, S. et al. Adaptation of Glucose Metabolism to Limb Autotomy and Regeneration in the Chinese Mitten Crab. Mar Biotechnol 26, 205–213 (2024). https://doi.org/10.1007/s10126-024-10290-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-024-10290-3