Role of HIF-1 on phosphofructokinase and fructose 1, 6-bisphosphatase expression during hypoxia in the white shrimp Litopenaeus vannamei

Gene expression and energetic metabolism changes in the whiteleg shrimp (Litopenaeus vannamei) in response to short‐term hypoxia

“…An increase in the expression of the genes encoding the α and β subunits of the HIF‐1 was also observed; the direct relationship between the expression of genes from anaerobic glycolysis (PFK, LDH1, LDH2) and subunits of HIF‐1 (α, β) support its presumed function as regulator in the activation of genes to maintain the cellular energy state during hypoxia. A similar response has been observed in the expression of the genes PFK and fructose 1,6‐bisphosphatase (FBP) in hepatopancreas and LDH and hexokinase in gills, in response to hypoxia which has been attributed to the activation of genes related to anaerobic metabolism during hypoxic stress via HIF‐1 (Cota‐Ruiz et al, ; Soñanez‐Organis, Peregrino‐Uriarte, Sotelo‐Mundo, Forman, & Yepiz‐Plascencia, ; Soñanez‐Organis et al, ).…”

“…The metabolism of carbohydrates together with the transcriptional response in different tissues integrates the strategy of energy used by shrimp to counteract hypoxia stress. In the present work it was possible to observe the mobilization of carbohydrates through different tissues with the simultaneous decrease in LAC and the increase in anaerobic glycolysis gene expression; the pathway linking anaerobic glycolysis and gluconeogenesis of different tissues is known as the Cori cycle, the results on the increase in carbohydrates in the gills, muscle and haemolymph and the increase in transcripts of PFK and LDH in gills registered in this work together with the accumulation of LAC and increased activity of PFK and FBP enzymes in hepatopancreas after short‐term exposure to hypoxia reported by Cota‐Ruiz et al () support the activation of this pathway in L. vannamei . We hypothesize that hypoxia induces the accumulation of LAC in the muscle and gills (anaerobic glycolysis) which is transported by the haemolymph to the digestive gland, where it is used as a glycogenic substrate (gluconeogenesis); which then, in the form of GLU returns to other tissues (i.e., gills, muscle) or is metabolised in the hepatopancreas where there is a highly active metabolism (Figure ).…”

“…Cursive letters represent metabolic pathways and underlined letters represent tissues. Blue abbreviations represent results in this work and green abbreviations represent results reported by Cota‐Ruiz et al () and Sánchez‐Paz et al (). GLU: glucose; LAC: lactate; GCG: glycogen; CHO: total carbohydrates; HK: hexokinase; FBP: fructose 1,6‐bisphosphatase; PFK: phosphofructokinase; LDH: lactate dehydrogenase [Colour figure can be viewed at wileyonlinelibrary.com]…”

“…Most of the studies focus on the molecular response mediated by the hypoxia inducible factor (HIF), a heterodimeric transcription factor that activates or deactivates genes related to the synthesis of oxygen transporters, GLU transporters and glycolytic pathways (Schito & Rey, 2017;Semenza, 2012; Soñanez-Organis, Racotta, & Yepiz-Plascencia, 2010). In addition, the induction of gene expression or increase in enzyme activity of glycolytic enzymes in shrimp was demonstrated during exposure to hypoxia, for example, phosphofructokinase (PFK), an enzyme that catalyses the non-reciprocal inter-conversion between fructose 6-phosphate and fructose 1,6-bisphosphate and a key regulatory enzyme of glycolysis is induced during hypoxia supporting the assumption that glycolysis rate rises in hepatopancreatic shrimp cells (Cota-Ruiz et al, 2016;Cota-Ruiz, Peregrino-Uriarte, Felix-Portillo, Martínez-Quintana, & Yepiz-Plascencia, 2015; Sánchez-Paz, Soñanez-Organis, Peregrino-Uriarte, Muhlia-Almazán, & Yepiz-Plascencia, 2008). On the other hand, LAC dehydrogenase (LDH) transcript concentration is considered as a marker to analyse the transition of aerobic to anaerobic glycolysis during hypoxia since it is well known that this gene is induced and regulated in gills through the action of hypoxia inducible factor 1 (HIF-1) in L. vannamei (Soñanez-Organis et al, 2012).…”

“…Crustaceans can tolerate low concentrations of DO through the use of coordinated pathways of gene regulation. Novel stress-specific genes as well as shared multiple-stress-responsive genes have been identified through gene expression studies in shrimp species like Palaemonetes pugio, Penaeus monodon and Litopenaeus vannamei (Brouwer et al, 2007;Cota-Ruiz et al, 2016;de la Vega et al, 2007;Gorr et al, 2010). Most of the studies focus on the molecular response mediated by the hypoxia inducible factor (HIF), a heterodimeric transcription factor that activates or deactivates genes related to the synthesis of oxygen transporters, GLU transporters and glycolytic pathways (Schito & Rey, 2017;Semenza, 2012; Soñanez-Organis, Racotta, & Yepiz-Plascencia, 2010).…”