PMID- 38520956 OWN - NLM STAT- MEDLINE DCOM- 20240422 LR - 20240422 IS - 1879-0291 (Electronic) IS - 0141-1136 (Linking) VI - 197 DP - 2024 May TI - Impact of hypoxia on glucose metabolism and hypoxia signaling pathways in juvenile horseshoe crabs Tachypleus tridentatus. PG - 106467 LID - S0141-1136(24)00128-4 [pii] LID - 10.1016/j.marenvres.2024.106467 [doi] AB - Marine hypoxia poses a significant challenge in the contemporary marine environment. The horseshoe crab, an ancient benthic marine organism, is confronted with the potential threat of species extinction due to hypoxia, making it an ideal candidate for studying hypoxia tolerance mechanisms. In this experiment, juvenile Tachypleus tridentatus were subjected to a 21-day trial at DO:2 mg/L (hypoxia) and DO:6 mg/L conditions. The experimental timeline included a 14-day exposure phase followed by a 7-day recovery period. Sampling occurred on days 0, 7, 14, and 21, where the period from day 14 to day 21 corresponds to seven days of recuperation. Several enzymatic activities of important proteins throughout this investigation were evaluated, such as succinate dehydrogenase (SDH), phosphofructokinase (PFK), hexokinase (HK), lactate dehydrogenase (LDH), and pyruvate kinase (PK). Concurrently, the relative expression of hexokinase-1 (HK), hypoxia-inducible factor 1-alpha inhibitor (FIH), and hypoxia-inducible factor 1-alpha (HIF-1alpha), pyruvate dehydrogenase phosphatase (PDH), succinate dehydrogenase assembly factor 4 (SDH), and Glucose-6-phosphatase (G6Pase) were also investigated. These analyses aimed to elucidate alterations in the hypoxia signaling pathway and respiratory energy metabolism. It is revealed that juvenile T. tridentatus initiated the HIF pathway under hypoxic conditions, resulting in an upregulation of HIF-1alpha and FIH-1 gene expression, which in turn, influenced a shift in metabolic patterns. Particularly, the activity of glycolysis-related enzymes was promoted significantly, including PK, HK, PKF, LDH, and the related HK gene. In contrast, enzymes linked to aerobic respiration, PDH, and SDH, as well as the related PDH and SDH genes, displayed down-regulation, signifying a transition from aerobic to anaerobic metabolism. Additionally, the activity of gluconeogenesis-related enzymes such as PK and G6Pase gene expression were significantly elevated, indicating the activation of gluconeogenesis and glycogenolysis pathways. Consequently, juvenile T. tridentatus demonstrated an adaptive response to hypoxic conditions, marked by changes in respiratory energy metabolism modes and the activation of hypoxia signaling pathways. CI - Copyright (c) 2024 Elsevier Ltd. All rights reserved. FAU - Jiang, Lingfeng AU - Jiang L AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Shang, Yueyong AU - Shang Y AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Shi, Yuntian AU - Shi Y AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Ma, Xiaowan AU - Ma X AD - Key Laboratory of Tropical Marine Ecosystem and Bioresource, Fourth Institute of Oceanography, Ministry of Natural Resources, Beihai, 536000, China. FAU - Khalid, Malik ShahZaib AU - Khalid MS AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Huang, Meilian AU - Huang M AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Fang, James Kar-Hei AU - Fang JK AD - Department of Food Science and Nutrition, The Hong Kong Polytechnic University, Hung Hom, China. FAU - Wang, Youji AU - Wang Y AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China. FAU - Tan, Kianann AU - Tan K AD - Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Beibu Gulf University, Qinzhou, 535011, Guangxi, China. Electronic address: tankianann@bbgu.edu.cn. FAU - Hu, Menghong AU - Hu M AD - International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China; Marine Biomedical Science and Technology Innovation Platform of Lin-gang Special Area, Shanghai, China. Electronic address: mhhu@shou.edu.cn. LA - eng PT - Journal Article DEP - 20240319 PL - England TA - Mar Environ Res JT - Marine environmental research JID - 9882895 RN - EC 1.3.99.1 (Succinate Dehydrogenase) RN - EC 2.7.1.1 (Hexokinase) RN - IY9XDZ35W2 (Glucose) RN - 0 (Hypoxia-Inducible Factor 1) RN - 0 (Hypoxia-Inducible Factor 1, alpha Subunit) SB - IM MH - Animals MH - *Horseshoe Crabs/genetics/metabolism MH - *Succinate Dehydrogenase/metabolism MH - Hexokinase/metabolism MH - Hypoxia/metabolism MH - Signal Transduction MH - Glucose/metabolism MH - Hypoxia-Inducible Factor 1/metabolism MH - Hypoxia-Inducible Factor 1, alpha Subunit/metabolism OTO - NOTNLM OT - Aerobic respiration OT - Gluconeogenesis OT - Glycolysis OT - Hypoxia OT - Tachypleus tridentatus COIS- Declaration of competing interest The authors state that they have no known competing financial interests or personal relationships that could affect the work reported in this article. EDAT- 2024/03/24 00:42 MHDA- 2024/04/22 06:43 CRDT- 2024/03/23 19:19 PHST- 2024/01/27 00:00 [received] PHST- 2024/03/12 00:00 [revised] PHST- 2024/03/19 00:00 [accepted] PHST- 2024/04/22 06:43 [medline] PHST- 2024/03/24 00:42 [pubmed] PHST- 2024/03/23 19:19 [entrez] AID - S0141-1136(24)00128-4 [pii] AID - 10.1016/j.marenvres.2024.106467 [doi] PST - ppublish SO - Mar Environ Res. 2024 May;197:106467. doi: 10.1016/j.marenvres.2024.106467. Epub 2024 Mar 19.