Skip to main content
SpringerLink
Log in

The nuclear encoded subunits gamma, delta and epsilon from the shrimp mitochondrial F1-ATP synthase, and their transcriptional response during hypoxia

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

The mitochondrial FOF1 ATP synthase produces ATP in a reaction coupled to an electrochemical proton gradient generated by the electron transfer chain. The enzyme also hydrolyzes ATP according to the energy requirements of the organism. Shrimp need to overcome low oxygen concentrations in water and other energetic stressors, which in turn lead to mitochondrial responses. The aim of this study was to characterize the full-length cDNA sequences of three subunits that form the central stalk of the F1 catalytic domain of the ATP synthase of the white shrimp Litopenaeus vannamei and their deduced proteins. The effect of hypoxia on shrimp was also evaluated by measuring changes in the mRNA amounts of these subunits. The cDNA sequences of the nucleus-encoded ATPγ, ATPδ and ATPε subunits are 1382, 477 and 277 bp long, respectively. The three deduced amino acid sequences exhibited highly conserved regions when compared to homologous sequences, and specific substitutions found in shrimp subunits are discussed through an homology structural model of F1 ATP-synthase that included the five deduced proteins, which confirm their functional structures and specific characteristics from the cognate complex of ATP synthases. Genes expression was evaluated during hypoxia-reoxygenation, and resulted in a generalized down-regulation of the F1 subunits and no coordinated changes were detected among these five subunits. The reduced mRNA levels suggest a mitochondrial response to an oxidative stress event, similar to that observed at ischemia-reperfusion in mammals. This model analysis and responses to hypoxia-reoxygenation may help to better understand additional mitochondrial adaptive mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abe H, Hirai S, Okada S (2007) Metabolic responses and arginine kinase expression under hypoxic stress of the kuruma prawn Marsupenaeus japonicus. Comp Biochem Physiol A Mol Integr Physiol 146(1):40–46

    Article  Google Scholar 

  • Abele D, Philipp E, Gonzalez PM, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12:933–946

    Article  CAS  Google Scholar 

  • Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  Google Scholar 

  • Boyer PD (1997) The ATP synthase—a splendid molecular machine. Annu Rev Biochem 66:717–749

    Article  CAS  Google Scholar 

  • Boyer PD (2000) Catalytic site forms and controls in ATP synthase catalysis. Biochim Biophys Acta 1458:252–262

    Article  CAS  Google Scholar 

  • Brouwer M, Brown-Peterson NJ, Hoexum-Brouwer T, Manning S, Denslow N (2008) Changes in mitochondrial gene and protein expression in grass shrimp, Palaemonetes pugio, exposed to chronic hypoxia. Mar Environ Res 66(1):143–145

    Article  CAS  Google Scholar 

  • Bulygin VV, Duncan TM, Cross RL (2004) Rotor/stator ineractions of the e subunit in Escherichia coli ATP synthase and implications for enzyme regulation. J Biol Chem 279:35616–35621

    Article  CAS  Google Scholar 

  • Butler JE, Young ND, Lovley DR (2010) Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40–51

    Article  Google Scholar 

  • Chimeo C (2013) Caracterizacion parcial y evaluacion de la expresión génica del inhibidor endógeno IF1 de la ATPasa mitocondrial del camarón blanco (Litopenaeus vannamei). Master of Science Thesis. Centro de Investigación en Alimentación y Desarrollo, pp 55

  • Claros MG, Vincens P (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241(3):779–786

    Article  CAS  Google Scholar 

  • Cross RL (2000) The rotary binding change mechanism of ATP synthases. Biochim Biophys Acta 1458(2–3):270–275

    Article  CAS  Google Scholar 

  • DeLano WL (2002) The PyMol molecular graphics system. DeLano Scientific, San Carlos

    Google Scholar 

  • Duncan TM, Düser MG, Heitkamp T, McMillan DGG, Börsch M (2014) Regulatory conformational changes of the e subunit in single FRET-labeled FoF1-ATP synthase. Proc Soc Photo Opt Instrum Eng 8948:89481J

    Google Scholar 

  • Eads BD, Hand SC (2003) Transcriptional initiation under conditions of anoxia-induced quiescence in mitochondria from Artemia franciscana embryos. J Exp Biol 206:577–589

    Article  CAS  Google Scholar 

  • Elimadi A, Sapena R, Settaf A, Le Louet H, Tillement J, Morin D (2001) Attenuation of liver normothermic ischemia-reperfusion injury by preservation of mitochondrial functions with S-15176, a potent trimetazidine derivative. Biochem Pharmacol 62(4):509–516

    Article  CAS  Google Scholar 

  • Feniouk BA, Suzuki T, Yoshida M (2006) The role of subunit epsilon in the catalysis and regulation of FOF1-ATP synthase. Biochim Biophys Acta 1757:326–338

    Article  CAS  Google Scholar 

  • Gibbons C, Montgomery MG, Leslie AGW, Walker JE (2000) The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution. Nat Struct Biol 7(11):1055–1061

    Article  CAS  Google Scholar 

  • Hand SC (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233–1242

    CAS  Google Scholar 

  • Havlickova V, Kaplanova V, Nuskova H, Drahota Z, Houstek J (2010) Knockdown of F1 epsilon subunit decreases mitochondrial content of ATP synthase and leads to accumulation of subunit c. Biochim Biophys Acta 1797(6–7):1124–1129

    Article  CAS  Google Scholar 

  • Holman JD, Hand SC (2009) Metabolic depression is delayed and mitochondrial impairment averted during prolonged anoxia in the ghost shrimp, Lepidophthlamus louisianensis (Schimtt, 1935). J Exp Mar Biol Ecol 376(2):85–93

    Article  CAS  Google Scholar 

  • Iwamoto A, Miki J, Maeda M, Futai M (1990) H(+)-ATPase gamma subunit of Escherichia coli. Role of the conserved carboxyl-terminal region. J Biol Chem 265:5043–5048

    CAS  Google Scholar 

  • Jaeschke H (2003) Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284(1):G15–G26

    Article  CAS  Google Scholar 

  • Jimenez-Gutierrez LR, Hernandez-Lopez J, Islas-Osuna MA, Muhlia-Almazán A (2013) Three nucleus-encoded subunits of mitochondrial cytochrome c oxidase of the whiteleg shrimp Litopenaeus vannamei: cDNA characterization, phylogeny and mRNA expression during hypoxia and reoxygenation. Comp Biochem Physiol B Biochem Mol Biol 166(1):30–39

    Article  CAS  Google Scholar 

  • Jimenez-Gutierrez LR, Uribe-Carvajal S, Sanchez-Paz A, Chimeo C, Muhlia-Almazan A (2014) The cytochrome c oxidase and its mitochondrial function in the whiteleg shrimp Litopenaeus vannamei during hypoxia. J Bioenerg Biomembr 46(3):189–196

    Article  CAS  Google Scholar 

  • Kane LA, Van Eyk JE (2009) Post-translational modifications of ATP synthase in the heart: biology and function. J Bioenerg Biomembr 41:145–150

    Article  CAS  Google Scholar 

  • Kim HK, Kang SW, Jeong SH, Kim N, Ko JH, Bang H, Park WS, Choi T-H, Ha Y-R, Lee YS, Youm JB, Ko KS, Rhee BD, Han J (2012) Identification of potential target genes of cardioprotection against ischemia-reperfusion injury by express sequence tags analysis in rat hearts. J Cardiol 60:98–110

    Article  Google Scholar 

  • Klionsky DJ, Brusilow WS, Simoni RD (1984) In vivo evidence for the role of the epsilon subunit as an inhibitor of the proton-translocating ATPase of Escherichia coli. J Bacteriol 160(3):1055–1060

    CAS  Google Scholar 

  • Kol S, Nouwen N, Driessen AJM (2008) Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes. J Biol Chem 283(46):31269

    Article  CAS  Google Scholar 

  • Lai Zhang J, Mueller DM (2000) Complementation of deletion mutants in the genes encoding the F1-ATPase by expression of the corresponding bovine subunits in yeast S. cerevisiae. Eur J Biochem 267(8):2409–2418

    Article  CAS  Google Scholar 

  • Li T, Brouwer M (2013) Field study of cyclic hypoxic effects on gene expression in grass shrimp hepatopancreas. Comp Biochem Physiol Part D Genomics Proteomics 8(4):309–316

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆C T method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Mailloux RJ, Jin X, Willmore WG (2014) Redox regulation of mitochondrial function with emphasis on cysteine oxidation reactions. Redox Biol 2:123–139

    Article  CAS  Google Scholar 

  • Martinez-Cruz O, Garcia-Carreño F, Robles-Romo A, Varela-Romero A, Muhlia-Almazan A (2011) Catalytic subunits atpα and atpβ from the Pacific white shrimp Litopenaeus vannamei FOF1 ATP-synthase complex: cDNA sequences, phylogenies, and mRNA quantification during hypoxia. J Bioenerg Biomembr 43(2):119–133

    Article  CAS  Google Scholar 

  • Martinez-Cruz O, Calderon de la Barca AM, Uribe-Carvajal S, Muhlia-Almazan A (2012a) The function of mitochondrial FOF1 ATP-synthase from the whiteleg shrimp Litopenaeus vannamei muscle during hypoxia. Comp Biochem Physiol B Biochem Mol Biol 162(4):107–112

    Article  CAS  Google Scholar 

  • Martinez-Cruz O, Sanchez-Paz JA, Garcia-Carreño FL, Jimenez-Gutierrez LR, Navarrete del Toro MA, Muhlia-Almazan A (2012b) Invertebrates mitochondrial function and energetic challenges. In: Clark K (ed) Bioenergetics. INTECH, Croatia, pp 181–218

    Google Scholar 

  • Matsuda C, Endo H, Ohta S, Kagawa Y (1993) Gene structure of human mitochondrial ATP synthase gamma-subunit. Tissue specificity produced by alternative RNA splicing. J Biol Chem 268(33):24950–24958

    CAS  Google Scholar 

  • Mueller DM, Puri N, Kabaleeswaran V, Terry C, Leslie AGW, Walker JE (2004) Ni-chelate-affinity purification and crystallization of the yeast mitochondrial F1-ATPase. Protein Expr Purif 37(2):479–485

    Article  CAS  Google Scholar 

  • Muhlia-Almazan A, Martinez-Cruz O, Navarrete del Toro ML, Garcia-Carreño F, Arreola R, Sotelo-Mundo R, Yepiz-Plascencia G (2008) Nuclear and mitochondrial subunits from the white shrimp Litopenaeus vannamei F0F1 ATP-synthase complex: cDNA sequence, molecular modeling, and mRNA quantification of atp9 and atp6. J Bioenerg Biomembr 40(4):359–369

    Article  CAS  Google Scholar 

  • Ong S-G, Lee W-G, Theodorou L, Kodo K, Lim SY, Shukla DH, Briston T, Kiriakidis S, Ashcroft M, Davidson SM, Maxwell PH, Yellon DM, Hausenloy DJ (2014) HIF-1 reduces ischemia-reperfusion injury in the heart by targeting the mitochondrial permeability transition pore. Cardiovasc Res 104:24–36

    Article  Google Scholar 

  • Petrosillo G, Di Venosa N, Ruggiero FM, Pistolese M, D’Agostino D, Tiravanti E, Fiore T, Paradies G (2005) Mitochondrial dysfunction associated with cardiac ischemia/reperfusion can be attenuated by oxygen tension control. Role of oxygen-free radicals and cardiolipin. Biochim Biophys Acta 1710:78–86

    Article  CAS  Google Scholar 

  • Rehm P, Borner J, Meusemann K, von Reumont BM, Simon S, Hadrys H, Misof B, Burmester T (2011) Daring the arthropod tree based on laerge-sacale transcriptome data. Mol Phylogenet Evol 61(3):880–887

    Article  Google Scholar 

  • Rubinstein JL, Walker JE, Henderson R (2003) Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J 22(23):6182–6192

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York

    Google Scholar 

  • Scheffler IE (1999) Metabolic pathways inside mitochondria. In: Mitochondria. Wiley, New York, pp 246–272

    Chapter  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  CAS  Google Scholar 

  • Tuena de Gómez‐Puyou M, G. P‐H, Gómez‐Puyou A (1999) Synthesis and hydrolysis of ATP and the phosphate-ATP exchange reaction in soluble mitochondrial F1 in the presence of dimethylsulfoxide. Eur J Biochem 266(2):691–696

    Article  Google Scholar 

  • Uhlin U, Cox GB, Guss JM (1997) Crystal Structure of the e subunit of the proton-translocating ATP synthase from Escherichia coli. Structure 5(9):1219–1230

    Article  CAS  Google Scholar 

  • Viñas O, Powell S, Runswick M, Iacobazzi V, Walker J (1990) The epsilon-subunit of ATP synthase from bovine heart mitochondria. Complementary DNA sequence, expression in bovine tissues and evidence of homologous sequences in man and rat. Biochem J 265:321–326

    Google Scholar 

  • Walker JE (2013) The ATP synthase: the understood, the uncertain and the unknown. Biochem Soc Trans 41:1–16

    Article  CAS  Google Scholar 

  • Walker JE, Lutter R, Dupuis A, Runswick MJ (1991) Identification of the subunits of F1F0-ATPase from bovine heart mitochondria. Biochemistry 30(22):5369–5378

    Article  CAS  Google Scholar 

  • Wilkens S, Capali RA (1998) Solution structure of the ε subunit of the F1- ATPase from Escherichia coli and interactions of this subunit with b subunits in the complex. J Biol Chem 273(41):26645–26651

    Article  CAS  Google Scholar 

  • Zhang P, Zhang X, Li J, Huang G (2006) The effects of body weight, temperature, salinity, pH, light intensity and feeding condition on lethal DO levels of whiteleg shrimp, Litopenaeus vannamei (Boone, 1931). Aquaculture 256(1–4):579–587

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Sandra Araujo Bernal for technical support and to Consejo Nacional de Ciencia y Tecnologia (CONACYT, National Council for Research and Technology, Mexico) for grant 133174 to AMA and for a graduate scholarship to OMC.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Universidad de Sonora, Rosales y Blvd. Luis Encinas s/n, Hermosillo, Sonora, 83000, Mexico

    Oliviert Martinez-Cruz & Aldo Arvizu-Flores

  2. Centro de Investigacion en Alimentacion y Desarrollo (CIAD), A.C, Carretera a Ejido La Victoria Km 0.6, PO Box. 1735, Hermosillo, Sonora, Mexico

    Rogerio R. Sotelo-Mundo & Adriana Muhlia-Almazan

Authors
  1. Oliviert Martinez-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aldo Arvizu-Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rogerio R. Sotelo-Mundo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adriana Muhlia-Almazan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adriana Muhlia-Almazan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinez-Cruz, O., Arvizu-Flores, A., Sotelo-Mundo, R.R. et al. The nuclear encoded subunits gamma, delta and epsilon from the shrimp mitochondrial F1-ATP synthase, and their transcriptional response during hypoxia. J Bioenerg Biomembr 47, 223–234 (2015). https://doi.org/10.1007/s10863-015-9605-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-015-9605-0

Keywords

Search

Navigation