Glucose transporter GLUT1 expression is important for oriental river prawn (Macrobrachium nipponense) hemocyte adaptation to hypoxic conditions

Abstract

Crustaceans have an open vascular system in which hemocytes freely circulate in hemolymph. Hemocytes are rich in hemocyanin, a specific oxygen-transport protein in crustaceans; therefore, understanding the response of hemocytes to hypoxia is crucial. Although hemocytes take up glucose during hypoxia, the molecular mechanism of glucose uptake in crustaceans remains unclear. Herein, we identified two highly conserved glucose transporters (GLUT1 and GLUT2) in Macrobrachium nipponense (oriental river prawn) and analyzed their tissue-specific expression patterns. Our immunofluorescence assays showed that GLUT1 and GLUT2 are located on the cell membrane, with a strong GLUT1 signal in primary hemocytes under hypoxia. We found that during acute hypoxia, hypoxia-inducible factor-1α–related metabolic alterations result in decreased mitochondrial cytochrome c oxidase activity, implying a classic glycolytic mechanism. As a proof of concept, we replicated these findings in insect S2 cells. Acute hypoxia significantly induced hypoxia-inducible factor-1α, GLUT1, and pyruvate dehydrogenase kinase isozyme 1 expression in primary hemocytes, and hypoxia-induced increases in glucose uptake and lactate secretion were observed. GLUT1 knockdown induced intracellular reactive oxygen species generation and apoptosis in vitro and in vivo, resulting in increased prawn mortality and more apoptotic cells in their brains, implying a vital function of GLUT1 in hypoxia adaptation. Taken together, our results suggest a close relationship between hypoxia-mediated glycolysis and GLUT1 in hemocytes. These results demonstrated that in crustaceans, adaptation to hypoxia involves glucose metabolic plasticity. Crustaceans have an open vascular system in which hemocytes freely circulate in hemolymph. Hemocytes are rich in hemocyanin, a specific oxygen-transport protein in crustaceans; therefore, understanding the response of hemocytes to hypoxia is crucial. Although hemocytes take up glucose during hypoxia, the molecular mechanism of glucose uptake in crustaceans remains unclear. Herein, we identified two highly conserved glucose transporters (GLUT1 and GLUT2) in Macrobrachium nipponense (oriental river prawn) and analyzed their tissue-specific expression patterns. Our immunofluorescence assays showed that GLUT1 and GLUT2 are located on the cell membrane, with a strong GLUT1 signal in primary hemocytes under hypoxia. We found that during acute hypoxia, hypoxia-inducible factor-1α–related metabolic alterations result in decreased mitochondrial cytochrome c oxidase activity, implying a classic glycolytic mechanism. As a proof of concept, we replicated these findings in insect S2 cells. Acute hypoxia significantly induced hypoxia-inducible factor-1α, GLUT1, and pyruvate dehydrogenase kinase isozyme 1 expression in primary hemocytes, and hypoxia-induced increases in glucose uptake and lactate secretion were observed. GLUT1 knockdown induced intracellular reactive oxygen species generation and apoptosis in vitro and in vivo, resulting in increased prawn mortality and more apoptotic cells in their brains, implying a vital function of GLUT1 in hypoxia adaptation. Taken together, our results suggest a close relationship between hypoxia-mediated glycolysis and GLUT1 in hemocytes. These results demonstrated that in crustaceans, adaptation to hypoxia involves glucose metabolic plasticity. Oxygen has low solubility in water (only 3% of the equivalent volume of air), yet is indispensable for aquatic animals' behavior, development, and survival (1Rytkönen K.T. Vuori K.A.M. Primmer C.R. Nikinmaa M. Comparison of hypoxia-inducible factor-1alpha in hypoxia-sensitive and hypoxia-tolerant fish species.Comp. Biochem. Physiol. Part D Genom. Proteom. 2007; 2: 177-186PubMed Google Scholar). Hypoxia occurs when dissolved oxygen (DO) falls below 2.8 mg/l in aquatic environments (2Wu R.S.S. Hypoxia: from molecular responses to ecosystem responses.Mar. Pollut. Bull. 2002; 45: 35-45Crossref PubMed Scopus (628) Google Scholar). During evolution, aquatic animals have acquired complex mechanisms to detect and respond to hypoxia, in addition to physiological adaptions to hypoxia (3Wu R.S. Zhou B.S. Randall D.J. Woo N.Y. Lam P.K. Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction.Environ. Sci. Technol. 2003; 37: 1137-1141Crossref PubMed Scopus (286) Google Scholar, 4Abdel-Tawwab M. Monier M.N. Hoseinifar S.H. Faggio C. Fish response to hypoxia stress: growth, physiological, and immunological biomarkers.Fish Physiol. Biochem. 2019; 45: 997-1013Crossref PubMed Scopus (211) Google Scholar, 5Wang S.Y. Lau K. Lai K.P. Zhang J.W. Tse C.K. Li J.W. et al.Hypoxia causes transgenerational impairments in reproduction of fish.Nat. Commun. 2016; 7: 12114Crossref PubMed Scopus (143) Google Scholar, 6Yang S. Yan T. Wu H. Xiao Q. Fu H.M. 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Hemocytes are cells that circulate in the and that from hemocytes are oxygen in of hemocytes oxygen its is therefore, metabolic pathway in hemocytes under hypoxia remains to hypoxia, cells glucose an metabolic Q. Wang Qin X. B. et glucose and cell function in under PubMed Scopus Google Scholar). of glucose cell is by the glucose which identified 1 to and Yan and and of the glucose Sci. 2016; PubMed Scopus Google Scholar). hypoxia-induced increases in glycolysis are by of 1 with in the C. A. A. of by hypoxia-inducible between and PubMed Scopus Google Scholar, Y. regulation of GLUT1 and expression by hypoxia in J. Physiol. Integr. Comp. Physiol. PubMed Scopus Google Scholar, V. S. J. V. H. et al.Hypoxia glucose expression hypoxia-inducible factor of the PubMed Scopus Google Scholar). GLUT2 in the and the secretion of glucose the blood B. G. A. A. A. of the glucose in the response of the pyruvate kinase gene to glucose in PubMed Scopus Google Scholar). GLUT1 to hypoxia signaling the that GLUT1 from is during hypoxia Peregrino-Uriarte A.B. Gollas-Galván T. Gómez-Jiménez S. Yepiz-Plascencia G. glucose 1 from the white shrimp Litopenaeus is during PubMed Scopus Google detailed mechanisms of the regulation of GLUT1 by remain to In of GLUT1 and its to the are for increased glucose uptake R.S. S. T. and PubMed Scopus Google Scholar). However, GLUT1 and GLUT2 expression is by hypoxia in crustaceans is unknown. the to glucose in primary hemocytes and showed that GLUT1 glucose uptake and production under hypoxia. In we demonstrated that GLUT1 is involved in the regulation of cell function in under hypoxia in and in GLUT1 and GLUT2 were from hemocytes of the river GLUT1 and GLUT2 a open of and and a and a and M. nipponense GLUT1 and GLUT2 have to with and river prawn are and their is to that in their and in the river prawn protein are to in GLUT2 1, and the of the river prawn GLUT1 and GLUT2 are conserved with their in and analysis identified two and and the of which prawn GLUT1 and GLUT2 which with In we that the of river prawn GLUT1 and in the are highly conserved with of crustaceans result showed that river prawn GLUT1 has with GLUT1 of Litopenaeus and with that of and GLUT2 showed with GLUT2 from We identified GLUT1 and GLUT2 expression in that hemocytes and a for their in prawn hypoxia GLUT1 and GLUT2 at mg/l to hypoxia in expression of GLUT1 and GLUT2 were in under hypoxia for and its in the response to hypoxic We the and of the two GLUT1 and GLUT2 gene of the river prawn and and these were to We the of these GLUT1 and GLUT2 in gene regulation by a of GLUT1 and GLUT2 which were of a gene of these hemocytes and under of the and cells under hypoxia for in significantly in to that under the to showed decreased with that from the under hypoxic conditions that the of the GLUT1 is involved in under hypoxic conditions we which a of to which to the function of in the of the GLUT1 showed that of the decreased the of the GLUT1 significantly these results showed that is for and of the GLUT1 assays showed that is involved in hypoxia-induced GLUT1 GLUT1 is a that in B. G. A. A. A. of the glucose in the response of the pyruvate kinase gene to glucose in PubMed Scopus Google Scholar). We hypoxia GLUT1 results showed that GLUT1 in the cell with a strong signal hypoxia for that GLUT1 is induced and in the cell under hypoxia. GLUT2 signal in the cell of hemocytes under with that under hypoxia for that hypoxia GLUT1 in hemocytes. In hypoxia GLUT1 to cell in hemocytes in response to hypoxia for that of GLUT2 the of and GLUT1 in hemocytes hypoxia for were of and GLUT1 were significantly increased in hemocytes in response to hypoxia for and results showed a hypoxia of and and pyruvate which is a that the of pyruvate the We found that were increased significantly hypoxia for implying that under hypoxic the causes glycolytic by pyruvate the In hypoxia induced glycolysis in prawn hemocytes in the glucose of primary hemocytes hypoxia for the of cytochrome c oxidase in the of and which an of for cytochrome c c oxidase decreased at of 1 to under hypoxia which our that of glucose glucose uptake in hemocytes significantly increased by hypoxia for with that in the with lactate production and that glucose is in hemocytes to in response to hypoxia. our findings that GLUT1 to hypoxic in hemocytes by their glucose we the of in the hypoxic GLUT1, and knockdown of expression in hemocytes under hypoxia for the of to knockdown of in in the primary hemocytes knockdown the hypoxia-induced in the protein of significantly the hypoxia-induced expression of GLUT1 and and that the hypoxic of GLUT1 and These results the that with the GLUT1 by to and GLUT1 that in addition to GLUT1 is a of in in response to hypoxia. hypoxia induced the expression of genes and lactate of significantly the hypoxic of and and oxygen with glucose the in cells to glucose We the under conditions and the the cells were to oxygen between in hemocytes decreased significantly at 1 to that to glucose of oxygen in knockdown cells to the function of in glycolytic knockdown the in the under hypoxia vital function of in glycolytic under hypoxia in S2 cells which the that the function of is vital to the Although glucose uptake significantly glucose uptake and lactate were by that in cells for glycolysis in the of 1 to and GLUT1 glucose uptake under hypoxia, we GLUT1 in hemocytes. GLUT1 knockdown the hypoxia-induced in the GLUT1 protein and Hypoxia increased glucose uptake and lactate which GLUT1 knockdown and we GLUT1 knockdown the hypoxia-induced changes in intracellular reactive oxygen species in hemocytes. results showed that hypoxia significantly intracellular production with that in the and significantly by GLUT1 knockdown in vitro and to GLUT1 knockdown the cell from the 1 to the and significantly GLUT1 knockdown and In a showed that the of hypoxia-induced apoptosis in hemocytes significantly increased by GLUT1 in vitro with that in the to hypoxia and the of GLUT1 in the regulation in vivo, the of and were their in the of with significantly in the GLUT1 knockdown the significantly that of the the production of and during hypoxia is by GLUT1, GLUT1 by of GLUT1 protein expression by GLUT1 and We that under hypoxia, a of of the result in in the increased production of R.S. S. T. and PubMed Scopus Google Scholar, V. S. C. H. C. et of dehydrogenase and reactive oxygen species 2003; PubMed Scopus Google Scholar). In hypoxia in increased intracellular in GLUT1 knockdown with in the under hypoxia In GLUT1 knockdown the under hypoxia with that in the under hypoxia have from production by to the mitochondrial In apoptosis R.S. S. T. and PubMed Scopus Google Scholar). we the of apoptotic cells of GLUT1 knockdown and in the under hypoxia of the GLUT1 knockdown significantly more apoptotic cells that of the of hypoxia and These that GLUT1 expression the apoptosis induced by hypoxia. GLUT1 knockdown in their survival with hypoxia In the of signaling in the hypoxic response has A. glucose analysis of and PubMed Scopus Google Scholar, T. of hypoxia-inducible factor in of a hypoxia-induced of the gene PubMed Scopus Google Scholar). mechanisms of the hypoxic response in different and cells have in in B. in is for adaptation to hypoxia in Commun. 2019; PubMed Scopus Google C. of is with hypoxia in the PubMed Scopus Google and blood cells T. L. between and in and survival of blood PubMed Scopus Google Scholar). in that the HIF-1 pathway is its In the of protein have which to highly conserved their conserved genes have and in GLUT1 Peregrino-Uriarte A.B. Gollas-Galván T. Gómez-Jiménez S. Yepiz-Plascencia G. glucose 1 from the white shrimp Litopenaeus is during PubMed Scopus Google GLUT2 S. M. Peregrino-Uriarte A.B. Yepiz-Plascencia G. glucose in the white shrimp Litopenaeus is during hypoxia in PubMed Scopus Google and Wang and are involved in the regulation of glucose in the 2017; Google Scholar). Herein, our of the function of GLUT1 in river prawn the of hypoxic and GLUT1 GLUT2) significantly glucose in prawn hemocytes in Hypoxia increased glucose uptake and production in prawn hemocytes the and the of GLUT1 in the prawn during hypoxia Our that GLUT1 by involved in hypoxia-mediated glycolysis regulation and is to of glucose to glycolysis and in hemocytes. GLUT1 glucose uptake and glucose uptake B. G. A. A. A. of the glucose in the response of the pyruvate kinase gene to glucose in PubMed Scopus Google and is in to our results for the expression of GLUT1, which demonstrated to and in the with the expression in hemocytes the that the have a tissue-specific expression and are for glucose in crustaceans in response to hypoxia. the signaling pathway has in the Y. Wang Zhou B. signaling in 2019; 2: PubMed Scopus Google Scholar). Although the signaling pathway remains largely in our showed a of in M. nipponense with in and demonstrated the of S. C. S. K. Y. Zhang et of the river Macrobrachium 2021; PubMed Scopus Google Scholar). we hypoxia significantly induced GLUT1 and GLUT2 in hemocytes. result showed that the GLUT2 in hemocytes under at the protein level, the of GLUT1 in prawn hemocytes under hypoxia, that GLUT1 is for the response to hypoxia in hemocytes and the Hypoxia to glycolysis in the and of S. Fu H. X. J. on the the responses of river prawn Macrobrachium nipponense to acute hypoxia and Physiol. 2018; PubMed Scopus Google Scholar, S. Fu H. J. X. and analysis of in the river prawn in response to hypoxia and Pollut. 2018; PubMed Scopus Google Scholar). In analysis of S. Fu H. J. X. and analysis of and of river prawn in response to PubMed Scopus (81) Google showed of to glycolysis we that the hypoxia-induced in glucose uptake is with glycolysis function of glucose uptake under hypoxia is unknown. which glucose metabolic are and their in hypoxia in hemocytes blood cells are cells that have a of oxygen to of the S. M. Peregrino-Uriarte A.B. Yepiz-Plascencia G. glucose in the white shrimp Litopenaeus is during hypoxia in PubMed Scopus Google Scholar). with blood hemocytes hemocyanin oxygen have an of oxygen an open system in to that hemocytes involved in the regulation of a mitochondrial is for glucose in hypoxic hemocytes cytochrome c oxidase is a metabolic glycolysis to have a effect on under hypoxic conditions blood a of Sci. PubMed Scopus Google Scholar). Herein, the glucose from glucose to resulting in decreased and the of in GLUT1 by glucose from the to implying that a of glycolysis to survival under hypoxia. to our results for the effect of GLUT1 knockdown on production and showed that these cell and decreased were by increased glucose uptake and increased GLUT-1 expression uptake and glycolysis hypoxia-induced apoptosis in PubMed Scopus Google Scholar, apoptosis in cell PubMed Scopus Google Scholar, S. et al.Role of GLUT1 in regulation of reactive oxygen 2: PubMed Scopus Google Scholar). Our in the river prawn that the glycolytic pathway is by of glycolytic genes in prawn in response to hypoxia, and S. Fu H. J. X. Molecular and characterization of a from the river prawn Macrobrachium nipponense in response to J. Mol. Sci. 2017; PubMed Scopus (16) Google Scholar, S. Fu H. J. X. Wu X. H. et and expression analysis of lactate dehydrogenase from the river prawn Macrobrachium nipponense in response to J. Mol. 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However, is to in glucose uptake in cells. results in metabolic by a of glucose uptake by the system M. and a 2021; PubMed Scopus Google Scholar). In prawn hemocytes during hypoxia in of GLUT1 the uptake of glucose by cell and GLUT1 knockdown in significantly increased hypoxia-mediated the increased apoptosis in the of GLUT1 knockdown under hypoxia to of glucose the Y. Y. K. Y. K. et factor glucose glucose 1 induced by hypoxia-inducible in J. Biochem. PubMed Scopus Google Scholar, A. T. M. et al.Role of the GLUT1 glucose in and PubMed Scopus Google Scholar). GLUT1 to the in of hemocytes. GLUT2 a glucose of the cells A. H. B. J. in the gene for the glucose in with PubMed Scopus Google Scholar). During hypoxia, GLUT2 in the glucose of hemocytes, that hypoxia the increased of to the GLUT2 Hypoxia two of the in their expression are These results that in crustaceans, the two in the of is that yet are a glycolysis regulation in hypoxic hemocytes Our findings a between intracellular production and hypoxia-induced metabolic we suggest that in hemocytes, GLUT1 increased glucose uptake during hypoxia, which is by increased and GLUT2 in the to the of glucose to hemocytes. on the of in and of the the prawn aquatic river which were to the at were in and and were a were to to their for at in conditions and from a and an volume of the hemocytes were to at for and the We the and from Zhang X. 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Sci. 2018; PubMed Scopus Google Scholar). the of were hemocytes the were to hypoxia for system to the activity, which to the of the to the GLUT1 of the to the from M. nipponense cells and and to to the the system and a S2 the to the genes and the an of were to from which from to gene expression were the of gene expression and the PubMed Scopus Google Scholar). to the were to and GLUT1 which were to an from the In the M. nipponense hemocytes with the of In vivo, we the prawn hemolymph. the effect of a to prawn at the to the of with the up the hypoxia for to hemocytes in vitro in were to two in the two were with the GLUT1 GLUT1 were hypoxia In were for to hemocytes were to hypoxia for the to the intracellular in the hemocytes. the hemocytes were with and at 1, and apoptosis to and the apoptotic cells were a C. C. a for in hypoxia signaling in of river prawn 2021; PubMed Scopus (7) Google Scholar). were were from hemocytes hypoxia and a protein to the protein of protein were by to a Fu J. Molecular and expression analysis of from the river Macrobrachium in response to Shellfish Immunol. 2016; PubMed Scopus Google Scholar). GLUT1 and were from that these the were with the were with in for and to the system to the protein on the were of and of GLUT1 were to of and a of the the prawn hemocytes were for in in cells were to and on were with primary and with cells were and under an the detailed in our C. C. a for in hypoxia signaling in of river prawn 2021; PubMed Scopus (7) Google Scholar). of the hemocytes were for GLUT1 and GLUT2 expression We the from in the with the primary from from the the were to the a the for hemocytes under hypoxic conditions As a for the were to H. M. 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C. and C. B. X. C. and C. B. X. C. and Y. J. X. C. and Y. J. X. C. C. and S. S. X. S. and S. S. X. and S. S. X. C. C. and S. S. S. S. with and

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