دورية أكاديمية
Shrimp Glucose-6-phosphatase 2 (G6Pase 2): a second isoform of G6Pase in the Pacific white shrimp and regulation of G6Pase 1 and 2 isoforms via HIF-1 during hypoxia and reoxygenation in juveniles.
العنوان: | Shrimp Glucose-6-phosphatase 2 (G6Pase 2): a second isoform of G6Pase in the Pacific white shrimp and regulation of G6Pase 1 and 2 isoforms via HIF-1 during hypoxia and reoxygenation in juveniles. |
---|---|
المؤلفون: | Hernández-Aguirre LE; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México., Peregrino-Uriarte AB; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México., Duarte-Gutiérrez JL; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México., Leyva-Carrillo L; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México., Ezquerra-Brauer JM; Departamento de Investigación y Posgrado en Alimentos, Universidad de Sonora, Blvd Luis Encinas y Rosales s/n, Hermosillo, Sonora, CP 83000, México., Valenzuela-Soto EM; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México., Yepiz-Plascencia G; Centro de Investigación en Alimentación y Desarrollo (CIAD), A.C, Carretera Gustavo Enrique Astiazarán Rosas, no. 46, Col La Victoria, Hermosillo, Sonora, C.P. 83304, México. gyepiz@ciad.mx. |
المصدر: | Journal of bioenergetics and biomembranes [J Bioenerg Biomembr] 2023 Apr; Vol. 55 (2), pp. 137-150. Date of Electronic Publication: 2023 Feb 28. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Springer Country of Publication: United States NLM ID: 7701859 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-6881 (Electronic) Linking ISSN: 0145479X NLM ISO Abbreviation: J Bioenerg Biomembr Subsets: MEDLINE |
أسماء مطبوعة: | Publication: 1999- : New York, NY : Springer Original Publication: New York, Plenum Press. |
مواضيع طبية MeSH: | Glucose-6-Phosphatase*/genetics , Glucose-6-Phosphatase*/metabolism , Penaeidae*/genetics , Penaeidae*/metabolism, Animals ; Hypoxia/metabolism ; Oxygen/metabolism ; Protein Isoforms/metabolism |
مستخلص: | Animals suffer hypoxia when their oxygen consumption is larger than the oxygen available. Hypoxia affects the white shrimp Penaeus (Litopenaeus) vannamei, both in their natural habitat and in cultivation farms. Shrimp regulates some enzymes that participate in energy production pathways as a strategy to survive during hypoxia. Glucose-6-phosphatase (G6Pase) is key to maintain blood glucose homeostasis through gluconeogenesis and glycogenolysis. We previously reported a shrimp G6Pase gene (G6Pase1) and in this work, we report a second isoform that we named G6Pase2. The expression of the two isoforms was evaluated in oxygen limited conditions and during silencing of the transcription factor HIF-1. High G6Pase activity was detected in hepatopancreas followed by muscle and gills under good oxygen and feeding conditions. Gene expression of both isoforms was analyzed in normoxia, hypoxia and reoxygenation in hepatopancreas and gills, and in HIF-1-silenced shrimp. In fed shrimp with normal dissolved oxygen (DO) (5.0 mg L - 1 DO) the expression of G6Pase1 was detected in gills, but not in hepatopancreas or muscle, while G6Pase2 expression was undetectable in all three tissues. In hepatopancreas, G6Pase1 is induced at 3 and 48 h of hypoxia, while G6Pase2 is down-regulated in the same time points but in reoxygenation, both due to the knock-down of HIF-1. In gills, only G6Pase1 was detected, and was induced by the silencing of HIF-1 only after 3 h of reoxygenation. Therefore, the expression of the two isoforms appears to be regulated by HIF-1 at transcriptional level in response to oxygen deprivation and subsequent recovery of oxygen levels. (© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.) |
References: | Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2. (PMID: 10.1016/S0022-2836(05)80360-22231712) Arion WJ (1989) [7] Measurement of intactness of rat liver endoplasmic reticulum. In: Methods in Enzymology. Academic, Cambridge, pp 58–67. Baker R, Fujiwara M, Minello TJ (2014) Juvenile growth and mortality effects on white shrimp Litopenaeus setiferus population dynamics in the northern Gulf of Mexico. Fish Res 155:74–82. https://doi.org/10.1016/j.fishres.2014.02.026. (PMID: 10.1016/j.fishres.2014.02.026) Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3. (PMID: 10.1016/0003-2697(76)90527-3942051) Breitburg D, Levin LA, Oschlies A et al (2018) Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240. https://doi.org/10.1126/science.aam7240. (PMID: 10.1126/science.aam724029301986) Burchell A, Hume R, Burchell B (1988) A new microtechnique for the analysis of the human hepatic microsomal glucose-6-phosphatase system. Clin Chim Acta 173:183–191. https://doi.org/10.1016/0009-8981(88)90256-2. (PMID: 10.1016/0009-8981(88)90256-22837351) Camacho-Jiménez L, Peregrino-Uriarte AB, Martínez-Quintana JA, Yepiz-Plascencia G (2018) The glyceraldehyde-3-phosphate dehydrogenase of the shrimp Litopenaeus vannamei: molecular cloning, characterization and expression during hypoxia. Mar Environ Res 138:65–75. https://doi.org/10.1016/j.marenvres.2018.04.003. (PMID: 10.1016/j.marenvres.2018.04.00329699713) Camacho-Jiménez L, Leyva-Carrillo L, Peregrino-Uriarte AB et al (2019) Regulation of glyceraldehyde-3-phosphate dehydrogenase by hypoxia inducible factor 1 in the white shrimp Litopenaeus vannamei during hypoxia and reoxygenation. Comp Biochem Physiol Part A Mol Integr Physiol 235:56–65. https://doi.org/10.1016/j.cbpa.2019.05.006. (PMID: 10.1016/j.cbpa.2019.05.006) Chang ES, Thiel M (2015) The natural history of the crustacea. Oxford University Press, New York City, pp 391–419. Chausson F, Regnault M (1995) Teneur en glycogène des branchies de Carcinus maenas (Crustacé, Décapode): Comparaison entre branchies antérieures et postérieures. Cah Biol Mar 36:291–297. Cota-Ruiz K, Peregrino-Uriarte AB, Felix-Portillo M et al (2015) Expression of fructose 1,6-bisphosphatase and phosphofructokinase is induced in hepatopancreas of the white shrimp Litopenaeus vannamei by hypoxia. Mar Environ Res 106:1–9. https://doi.org/10.1016/j.marenvres.2015.02.003. (PMID: 10.1016/j.marenvres.2015.02.00325725474) Cota-Ruiz K, Leyva-Carrillo L, Peregrino-Uriarte AB et al (2016) Role of HIF-1 on phosphofructokinase and fructose 1, 6-bisphosphatase expression during hypoxia in the white shrimp Litopenaeus vannamei Comp Biochem Physiol Part A Mol Integr Physiol 198:1–7. https://doi.org/10.1016/j.cbpa.2016.03.015. Dobson L, Reményi I, Tusnády GE (2015) CCTOP: a Consensus constrained TOPology prediction web server. Nucleic Acids Res 43:W408–W412. https://doi.org/10.1093/nar/gkv451. (PMID: 10.1093/nar/gkv451259435494489262) Duarte-Gutiérrez J, Peregrino-Uriarte AB, Gómez-Jiménez S et al (2021) HIF-1 is involved in the regulation of expression of metallothionein and apoptosis incidence in different oxygen conditions in the white shrimp Litopenaeus vannamei Comp Biochem Physiol Part A Mol Integr Physiol 262:111072. https://doi.org/10.1016/j.cbpa.2021.111072. Ghaffari N, Sanchez-Flores A, Doan R et al (2014) Novel transcriptome assembly and improved annotation of the whiteleg shrimp (Litopenaeus vannamei), a dominant crustacean in global seafood mariculture. Sci Rep 4:7081. https://doi.org/10.1038/srep07081. (PMID: 10.1038/srep07081254208804243063) Ghosh A, Shieh JJ, Pan CJ et al (2002) The catalytic center of glucose-6-phosphatase HIS176 is the nucleophile forming the phosphohistidine-enzyme intermediate during catalysis. J Biol Chem 277:32837–32842. https://doi.org/10.1074/jbc.M201853200. (PMID: 10.1074/jbc.M20185320012093795) Giraud-Billoud M, Rivera-Ingraham GA, Moreira DC et al (2019) Twenty years of the ‘Preparation for oxidative stress’ (POS) theory: ecophysiological advantages and molecular strategies. Comp Biochem Physiol Part A Mol Integr Physiol 234:36–49. https://doi.org/10.1016/j.cbpa.2019.04.004. (PMID: 10.1016/j.cbpa.2019.04.004) Granillo-Luna ON, Hernandez-Aguirre LE, Peregrino-Uriarte AB et al (2022) The anaplerotic pyruvate carboxylase from white shrimp Litopenaeus vannamei: gene structure, molecular characterization, protein modelling and expression during hypoxia. Comp Biochem Physiol Part A Mol Integr Physiol 269:111212. https://doi.org/10.1016/j.cbpa.2022.111212. (PMID: 10.1016/j.cbpa.2022.111212) Han SY, Wang BJ, Liu M et al (2017) Effect of cyclic serious/medium hypoxia stress on the survival, growth performance and resistance against Vibrio parahemolyticus of white shrimp Litopenaeus vannamei Invertebr Surviv J 14:259–270. https://doi.org/10.25431/1824-307X/isj.v14i1.259-270. Hernández-Aguirre LE, Cota-Ruiz K, Peregrino-Uriarte AB et al (2021) The gluconeogenic glucose-6-phosphatase gene is expressed during oxygen-limited conditions in the white shrimp Penaeus (Litopenaeus) vannamei: molecular cloning, membrane protein modeling and transcript modulation in gills and hepatopancreas. J Bioenerg Biomembr 3:449–461. https://doi.org/10.1007/s10863-021-09903-6. (PMID: 10.1007/s10863-021-09903-6) Hutton JC, O’Brien RM (2009) Glucose-6-phosphatase catalytic subunit gene family. J Biol Chem 284:29241–29245. https://doi.org/10.1074/jbc.R109.025544. (PMID: 10.1074/jbc.R109.025544197004062785553) Jitrapakdee S (2012) Transcription factors and coactivators controlling nutrient and hormonal regulation of hepatic gluconeogenesis. Int J Biochem Cell Biol 44:33–45. https://doi.org/10.1016/j.biocel.2011.10.001. (PMID: 10.1016/j.biocel.2011.10.00122004992) Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320. https://doi.org/10.1093/molbev/msn067. (PMID: 10.1093/molbev/msn06718367465) Lord-Dufour S, Copland IB, Levros L-C et al (2009) Evidence for transcriptional regulation of the glucose-6-phosphate transporter by HIF-1α: Targeting G6PT with mumbaistatin analogs in hypoxic mesenchymal stromal cells. Stem Cells 27:489–497. https://doi.org/10.1634/stemcells.2008-0855. (PMID: 10.1634/stemcells.2008-085519074414) Martins TL, Chittó ALF, Rossetti CL et al (2011) Effects of hypo- or hyperosmotic stress on lipid synthesis and gluconeogenic activity in tissues of the crab neohelice granulata Comp Biochem Physiol Part A Mol Integr Physiol 158:400–405. https://doi.org/10.1016/j.cbpa.2010.11.023. Pérez-Rostro CI, Racotta IS, Ibarra AM (2004) Decreased genetic variation in metabolic variables of Litopenaeus vannamei shrimp after exposure to acute hypoxia. J Exp Mar Biol Ecol 302:189–200. https://doi.org/10.1016/j.jembe.2003.10.010. (PMID: 10.1016/j.jembe.2003.10.010) Reyes-Ramos CA, Peregrino-Uriarte AB, Cota-Ruiz K et al (2018) Phosphoenolpyruvate carboxykinase cytosolic and mitochondrial isoforms are expressed and active during hypoxia in the white shrimp Litopenaeus vannamei Comp Biochem Physiol B Biochem Mol Biol 226:1–9. https://doi.org/10.1016/j.cbpb.2018.08.001. Rosas C, Martinez E, Gaxiola G et al (1999) The effect of dissolved oxygen and salinity on oxygen consumption, ammonia excretion and osmotic pressure of Penaeus setiferus (Linnaeus) juveniles. J Exp Mar Biol Ecol 234:41–57. https://doi.org/10.1016/S0022-0981(98)00139-7. (PMID: 10.1016/S0022-0981(98)00139-7) Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73. (PMID: 10.1038/nprot.2008.7318546601) Scholnick DA, Barabas AE, Cowan SS (2006) The influence of chloride on glucose export in marine crabs: sensitivity of glucose-6-phosphatase to chloride ion. J Crustacean Biol 26:510–514. https://doi.org/10.1651/S-2669a.1. (PMID: 10.1651/S-2669a.1) Seidman ER, Lawrence AL (1985) Growth, feed digestibility, and proximate body composition of juvenile Penaeus vannamei and Penaeus monodon grown at different dissolved oxygen levels. J World Aquac Soc 16:333–346. https://doi.org/10.1111/j.1749-7345.1985.tb00214.x. Semenza GL (2007) Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007:cm8. https://doi.org/10.1126/stke.4072007cm8. Soñanez-Organis JG, Peregrino-Uriarte AB, Gómez-Jiménez S et al (2009) Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp Biochem Physiol C Toxicol Pharmacol 150:395–405. https://doi.org/10.1016/j.cbpc.2009.06.005. (PMID: 10.1016/j.cbpc.2009.06.00519540931) Soñanez-Organis JG, Racotta IS, Yepiz-Plascencia G (2010) Silencing of the hypoxia inducible factor 1 –HIF-1- obliterates the effects of hypoxia on glucose and lactate concentrations in a tissue-specific manner in the shrimp Litopenaeus vannamei J Exp Mar Biol Ecol 393:51–58. https://doi.org/10.1016/j.jembe.2010.06.031. Soñanez-Organis JG, Peregrino-Uriarte AB, Sotelo-Mundo RR et al (2011) Hexokinase from the white shrimp Litopenaeus vannamei: cDNA sequence, structural protein model and regulation via HIF-1 in response to hypoxia. Comp Biochem Physiol B Biochem Mol Biol 158:242–249. https://doi.org/10.1016/j.cbpb.2010.12.006. Soñanez-Organis JG, Rodriguez-Armenta M, Leal-Rubio B et al (2012) Alternative splicing generates two lactate dehydrogenase subunits differentially expressed during hypoxia via HIF-1 in the shrimp Litopenaeus vannamei Biochimie 94:1250–1260. https://doi.org/10.1016/j.biochi.2012.02.015. Spyropoulos IC, Liakopoulos TD, Bagos PG, Hamodrakas SJ (2004) TMRPres2D: high quality visual representation of transmembrane protein models. Bioinformatics 20:3258–3260. https://doi.org/10.1093/bioinformatics/bth358. (PMID: 10.1093/bioinformatics/bth35815201184) Stukey J, Carman GM (1997) Identification of a novel phosphatase sequence motif. Protein Sci 6:469–472. (PMID: 10.1002/pro.556006022690416522143653) Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120. (PMID: 10.1093/molbev/msab120338924918233496) Thabrew MI, Poat PC, Munday KA (1971) Carbohydrate metabolism in Carcinus maenas gill tissue. Comp Biochem Physiol B Biochem Mol Biol 40:531–541. https://doi.org/10.1016/0305-0491(71)90238-0. (PMID: 10.1016/0305-0491(71)90238-0) Trasviña-Arenas CH, Garcia-Triana A, Peregrino-Uriarte AB, Yepiz-Plascencia G (2013) White shrimp Litopenaeus vannamei catalase: gene structure, expression and activity under hypoxia and reoxygenation. Comp Biochem Physiol B Biochem Mol Biol 164:44–52. https://doi.org/10.1016/j.cbpb.2012.10.004. (PMID: 10.1016/j.cbpb.2012.10.00423142216) Wallert MA, Foster JD, Scholnick DA et al (2001) Kinetic analysis of glucose-6-phosphatase: an investigative approach to carbohydrate metabolism and kinetics. Biochem Mol Biol Educ 29:199–203. https://doi.org/10.1111/j.1539-3429.2001.tb00121.x. (PMID: 10.1111/j.1539-3429.2001.tb00121.x) Wang Y, Wang H, Li M et al (2015) Identification, expression and regulation of amphioxus G6Pase gene with an emphasis on origin of liver. Gen Comp Endocrinol 214:9–16. https://doi.org/10.1016/j.ygcen.2014.12.021. (PMID: 10.1016/j.ygcen.2014.12.02125745818) Yun Z, Maecker HL, Johnson RS, Giaccia AJ (2002) Inhibition of PPARγ2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev Cell 2:331–341. https://doi.org/10.1016/S1534-5807(02)00131-4. (PMID: 10.1016/S1534-5807(02)00131-411879638) Zhang X, Yuan J, Sun Y et al (2019) Penaeid shrimp genome provides insights into benthic adaptation and frequent molting. Nat Commun 10:356. https://doi.org/10.1038/s41467-018-08197-4. (PMID: 10.1038/s41467-018-08197-4306646546341167) Zhang Y, Zhang Z, Liang XF et al (2021) Response of g6p homologous genes in chinese perch to high-carbohydrate diets. Aquac Rep 19:100581. https://doi.org/10.1016/J.AQREP.2020.100581. (PMID: 10.1016/J.AQREP.2020.100581) |
فهرسة مساهمة: | Keywords: G6Pase2; HIF-1; Hypoxia; Penaeus (Litopenaeus) vannamei; Reoxygenation |
المشرفين على المادة: | EC 3.1.3.9 (Glucose-6-Phosphatase) S88TT14065 (Oxygen) 0 (Protein Isoforms) |
تواريخ الأحداث: | Date Created: 20230228 Date Completed: 20230517 Latest Revision: 20230601 |
رمز التحديث: | 20231215 |
DOI: | 10.1007/s10863-023-09960-z |
PMID: | 36853470 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1573-6881 |
---|---|
DOI: | 10.1007/s10863-023-09960-z |