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The shrimp mitochondrial FoF1-ATPase inhibitory factor 1 (IF1)

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Abstract

The whiteleg shrimp species Litopenaeus vannamei is exposed to cyclic changes of the dissolved oxygen concentration of seawater and must neutralize the adverse effects of hypoxia by using ATP as energy source. In crustaceans, the mitochondrial FOF1-ATP synthase is pivotal to the homeostasis of ATP and function prevalently as a FOF1-ATPase. Hitherto, it is unknown whether these marine invertebrates are equipped with molecules able to control the FOF1-ATPase inhibiting the ATP consumption. In this study, we report two variants of the mitochondrial FOF1-ATPase Inhibitory Factor 1 (IF1) ubiquitously expressed across tissues of the Litopenaeus vannamei transcriptome: the IF1_Lv1 and the IF1_Lv2. The IF1_Lv1, with a full-length sequence of 550 bp, encodes a 104 aa long protein and its mRNA amounts are significantly affected by hypoxia and re-oxygenation. The IF1_Lv2, with a sequence of 654 bp, encodes instead for a protein of 85 aa. Both proteins share a 69 % homology and contain a conserved minimal inhibitory sequence (IATP domain) along with a G-rich region on their N-terminus typical of the invertebrate. In light of this characterization IF1 is here discussed as an adaptive mechanism evolved by this marine species to inhibit the FOF1-ATPase activity and avoid ATP dissipation to thrive in spite of the changes in oxygen tension.

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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 Phys A 146:40–46. doi:10.1016/j.cbpa.2006.08.027

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    Article  CAS  Google Scholar 

  • Ando C, Ichikawa N (2008) Glutamic acid in the inhibitory site of mitochondrial ATPase inhibitor, IF1, participates in pH sensing in both mammals and yeast. J Biochem 144:547–553. doi:10.1093/jb/mvn100

    Article  CAS  Google Scholar 

  • Andrew DR (2011) A new view of insect- crustacean relationships I. Inferences from expressed sequence tags and comparison with neural cladistics. Arthropod Struct Dev 40:289–302. doi:10.1016/j.asd.2011.02.002

    Article  Google Scholar 

  • Bason JV, Runswick MJ, Fearnley IM, Walker JE (2011) Binding of the inhibitor protein IF1 to bovine F1-ATPase. J Mol Biol 406:443–453. doi:10.1016/j.jmb.2010.12.025

    Article  CAS  Google Scholar 

  • Bason JV, Montgomery MG, Leslie AGW, Walker JE (2014) Pathway of binding of the intrinsically disordered mitochondrial inhibitor protein to F1-ATPAse. PNAS 111(31):11306–11310. doi:10.1073/pnas.141156111/-/DCSuplemental

    Article  Google Scholar 

  • Benkert P, Biasini M, Schwede T (2011) Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27:343–350. doi:10.1093/bioinformatics/btq662

    Article  CAS  Google Scholar 

  • Boyer PD (1997) The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66:717–749. doi:10.1146/annurev.biochem.66.1.717

    Article  CAS  Google Scholar 

  • Brown-Peterson NJ, Steve-Manning C, Patel V, Denslow ND, Brouwer M (2008) Effects of cyclic hypoxia on gene expression and reproduction in a grass shrimp Palaemonetes pugio. Biol Bull 214:6–16

    Article  CAS  Google Scholar 

  • Burgents JE, Burnett KG, Burnett LE (2005) Effects of hypoxia and hypercapnic hypoxia on the localization and the elimination of Vibrio campbellii in Litopenaeus vannamei, the pacific white shrimp. Biol Bull 208:159–168

    Article  Google Scholar 

  • Cabezon E, Butler PJG, Runswick MJ, Walker JE (2000a) Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH. J Biol Chem 275:25460–25464. doi:10.1074/jbc.M003859200

    Article  CAS  Google Scholar 

  • Cabezon E, Arechaga I, Butler PJG, Walker JE (2000b) Dimerization of bovine F1- ATPase by binding the inhibitor protein IF1. J Biol Chem 275:28353–28355. doi:10.1074/jbc.C000427200

    Article  CAS  Google Scholar 

  • Cabezon E, Runswick MJ, Leslie AGW, Walker JE (2001) The structure of bovine IF1, the regulatory subunit of mitochondrial F1-ATPase. EMBO J 20:6990–6996. doi:10.1093/emboj/20.24.6990

    Article  CAS  Google Scholar 

  • Cabezon E, Montgomery MG, Leslie AGW, Walker JE (2003) The structure of bovine F1-ATPase in complex with is regulatory protein IF1. Nat Struct Biol 10:744–750. doi:10.1038/nsb966

    Article  CAS  Google Scholar 

  • Campanella M, Casswell E, Chong S, Farah Z, Wieckowski MR, Abramov AY, Tinker A, Duchen MR (2008) Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab 8:13–25. doi:10.1016/j.cmet.2008.06.001

    Article  CAS  Google Scholar 

  • Campanella M, Parker N, Tan CH, Hall AM, Duchen MR (2009) IF(1): setting the pace of the F(1)F(0)-ATP synthase. Trends Biochem Sci 34(7):343–350. doi:10.1016/j.tibs.2009.03.006

    Article  CAS  Google Scholar 

  • Eads BD, Hand SC (2003) Mitochondrial mRNA stability and polyadenylation during anoxia-induced quiescence in the brine shrimp Artemia franciscana. J Exp Biol 206:3681–3692. doi:10.1242/jeb.00595

    Article  Google Scholar 

  • Faccenda D, Campanella M (2012) Molecular regulation of the mitochondrial F1F0-ATPsynthase: Physiological and pathological significance of the inhibitory factor 1 (IF1). Int J Cell Biol 2012, ID 367934. doi: 10.1155/2012/367934

  • Fujikawa M, Imamura H, Nakamura J, Yoshida M (2012) Assessing actual contribution of IF1, inhibitor of mitochondrial FoF1, to ATP homeostasis, cell growth, mitochondrial morphology, and cell viability. J Biol Chem 287:18781–18787. doi:10.1074/jbc.M112.345793

    Article  CAS  Google Scholar 

  • Garrido A, Teijon JM, Blanco D, Villaverde C, Mendoza C, Ramirez J (2006) Desnaturalizacion e hibridacion. In: Teijon JM, Garrido A (eds) Fundamentos de bioquimica estructural. Tebar, España, p. 444

    Google Scholar 

  • Gledhill JR, Montgomery MG, Leslie AGW, Walker JE (2007) How the regulatory protein, IF1,inhibits F1-ATPase from bovine mitochondria. Proc Natl Acad Sci U S A 104:15671–15676. doi:10.1073/pnas.0707326104

    Article  CAS  Google Scholar 

  • Gordon-Smith DJ, Carbajo RJ, Yang JC, Videler H, Runswick MJ, Walker JE, Neuhaus D (2001) Solution structure of a C-terminal coiled-coil domain from bovine IF1: the inhibitor protein of F1 ATPase. J Mol Biol 308:325–339. doi:10.1006/jmbi.2001.4570

    Article  CAS  Google Scholar 

  • Grey MW (2015) Mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. PNAS 201421379. doi:10.1073/pnas.1421379112

  • Grover GJ, Atwal KS, Sleph PG, Wang FL, Monshizadegan H, Monticello T, Green DW (2004) Excessive ATP hydrolysis in ischemic myocardium by mitochondrial F1F0-ATPase: effect of selective pharmacological inhibition of mitochondrial ATPase hydrolase activity. Am J Physiol-Heart C 287:H1747–H1755. doi:10.1152/ajpheart.01019.2003

    Article  CAS  Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the swiss-Pdb viewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723. doi:10.1002/elps.1150181505

    Article  CAS  Google Scholar 

  • Guex N, Diemand A, Peitsch MC (1999) Protein modelling for all. Trends Biochem Sci 24:364–367. doi:10.1016/S0968-0004(99)01427-9

    Article  CAS  Google Scholar 

  • Guhaniyogi J, Brewer G (2001) Regulation of mRNA stability in mammalian cells. Gene 265:11–23

    Article  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. BBA-Bioenergetics 1797:1124–1129. doi:10.1016/j.bbabio.2009.12.009

    Article  CAS  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192. doi:10.1093/sysbio/42.2.182

    Article  Google Scholar 

  • Ichikawa N, Ogura C (2003) Overexpression, purification and characterization of human and bovine mitochondrial ATPase inhibitors: comparison of the properties of mammalian and yeast ATPase inhibitors. J Bioenerg Biomembr 35:399–405. doi:10.1023/A:1027383629565

    Article  CAS  Google Scholar 

  • Ichikawa N, Karaki A, Kawabata M, Ushida S, Mizushima M, Hashimoto T (2001) The region from phenylalanine-17 to phenylalanine-28 of a yeast mitochondrial ATPase inhibitor is essential for its ATPase inhibitory activity. J Biochem 130:687–693

    Article  CAS  Google Scholar 

  • Ichikawa N, Chisuwa N, Tanase M, Nakamura M (2005) Mitochondrial ATP synthase residue βArginine-408, which interacts with the inhibitory site of regulatory protein IF1, is essential for the function of the enzyme. J Biochem 138:201–207. doi:10.1093/jb/mvi116

    Article  CAS  Google Scholar 

  • Ichikawa N, Ando C, Fumino M (2006) Caenorhabditis elegans MAI-1 protein, which is similar to mitochondrial ATPase inhibitor (IF1), can inhibit yeast F0F1-ATPase but cannot be transported to yeast mitochondria. J Bioenerg Biomembr 38:93–99. doi:10.1007/s10863-006-9009-2

    Article  CAS  Google Scholar 

  • Jimenez-Gutierrez LR, Hernandez-Lopez J, Islas-Osuna MA, Muhlia-Almazan 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 166:30–39. doi:10.1016/j.cbpb.2013.06.008

    Article  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282. doi:10.1093/bioinformatics/8.3.275

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2_ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262

    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 F0F1ATP-synthase complex: cDNA sequences, phylogenies, and mRNA quantification during hypoxia. J Bioenerg Biomembr 43:119–133. doi:10.1007/s10863-011-9340-0

    Article  CAS  Google Scholar 

  • Martinez-Cruz O, Calderon de la Barca AM, Uribe-Carvajal S, Muhlia-Almazan A (2012a) The function of mitochondrial F0F1 ATP-synthase function from the whiteleg shrimp Litopenaeus vannamei during hypoxia. Comp Biochem Phys B 162:107–112. doi:10.1016/j.cbpb.2012.03.004

    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. doi:10.5772/32309

    Google Scholar 

  • Martinez-Cruz O, Arvizu-Flores A, Sotelo-Mundo R, Muhlia-Almazan A (2015) 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. doi:10.1007/s10863-015-9605-0

    Article  CAS  Google Scholar 

  • Matsubara H, Inoue K, Hashimoto T, Yoshida Y, Tagawa K (1983) A stabilizing factor of yeast mitochondrial F1F0-ATPase-inhibitor complex: common amino acid sequence with yeast ATPase inhibitor and E. coli ε and bovine δ subunits. J Biochem 94:315–318

    CAS  Google Scholar 

  • Muhlia-Almazan A, Martinez-Cruz O, Navarrete del Toro MA, Garcia-Carreño FL, Arreola R, Sotelo-Mundo R, Yepiz-Plascencia G (2008) Nuclear and mitochondrial subunits from the white shrimp Litopenaeus vannamei FoF1 ATP-synthase complex: cDNA sequence, molecular modeling, and mRNA quantification of atp9 and atp6. J Bioenerg Biomembr 40:359–369. doi:10.1007/s10863-008-9162-x

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Separation of RNA according to size: electrophoresis of RNA through agarose gels containing formaldehyde. In: Sambrook J, Russell DW (eds) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York 2028 pp

    Google Scholar 

  • Samuel DS, Belote JM, Chan SHP (1995) Isolation of the rat F1-ATPase inhibitor gene and its pseudogenes. BBA-Bioenergetics 1230:81–85. doi:10.1016/0005-2728(95)00049-O

    Article  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385. doi:10.1093/nar/gkg520

    Article  CAS  Google Scholar 

  • Shah DI, Takahashi-Makise N, Cooney JD, Li L, Schultz IJ, Pierce EL, Narla A, Seguin A, Hattangadi SM, Medlock AE, Langer NB, Dailey TA, Hurst SN, Faccenda D, Wiwczar JM, Heggers SK, Vogin G, Chen W, Chen C, Campagna DR, Brugnara C, Zhou Y, Ebert BL, Danial NN, Fleming MD, Ward DM, Campanella M, Dailey HA, Kaplan J, Paw BH (2012) Mitochondrial Atpif1 regulates haem synthesis in developing erythroblasts. Nature 491:608–612. doi:10.1038/nature11536

    Article  CAS  Google Scholar 

  • Solaini G, Harris DA (2005) Biohemical dysfunction in heart mitochondria exposed to ischemia and reperfusion. Biochem J 390:377–394. doi:10.1042/BJ20042006

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4.1: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  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 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  CAS  Google Scholar 

  • Van Raaij MJ, Orriss GL, Montgomery MG, Runswick MJ, Fearnley IM, Skehel JM, Walker JE (1996) The ATPase inhibitor protein from bovine heart mitochondria: the minimal inhibitory sequence. Biochemistry 35:15618–15625. doi:10.1021/bi960628f

    Article  Google Scholar 

  • Walker JE (1994) The regulation of catalysis in the ATP synthase. Curr Opin Struct Biol 4:912–918

    Article  CAS  Google Scholar 

  • Wang T, Lefevre S, van Cong N, Bayley M (2009) The effects of hypoxia on growth and digestion. Fish Physiol 27:361–396. doi:10.1016/S1546-5098(08)00008-3

    Article  CAS  Google Scholar 

  • Wei LZ, Zhang XM, Li J, Huang GQ (2008) Compensatory growth of Chinese shrimp, Fenneropenaeus chinensis following hypoxic exposure. Aquacult Int 16:455–470. doi:10.1007/s10499-007-9158-2

    Article  Google Scholar 

  • Zar JH (1984) Analisys of variance. In: Zar JH (ed) Biostatistical analysis. Prentice-Hall, Englewood Cliffs 718 pp

    Google Scholar 

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Acknowledgments

We thank MS Magdalena Pacheco-Sanchez and Sandra Araujo-Bernal for technical support, and the National Council for Research and Technology, Mexico (CONACyT) for grant 241670 to Adriana Muhlia and for a graduate scholarship to Cindy Chimeo.

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Authors and Affiliations

  1. Bioenergetics and Molecular Genetics Lab, Centro de Investigacion en Alimentacion y Desarrollo (CIAD) A. C., Carretera a Ejido La Victoria Km 0.6, PO Box 1735, 83000, Hermosillo, Sonora, Mexico

    Cindy Chimeo, Ofelia Mendez-Romero & Adriana Muhlia-Almazan

  2. Laboratorio Fisiologia de Organismos Acuaticos. Instituto de Investigaciones Marinas y Costeras, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Buenos Aires, Argentina

    Analia Veronica Fernandez-Gimenez

  3. Department of Comparative Biomedical Sciences, The Royal Veterinary College, University of London, London, UK

    Michelangelo Campanella

  4. University College London Consortium for Mitochondrial Research, Royal College Street NW1 0TU, London, UK

    Michelangelo Campanella

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  1. Cindy Chimeo
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  2. Analia Veronica Fernandez-Gimenez
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  3. Michelangelo Campanella
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  4. Ofelia Mendez-Romero
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  5. Adriana Muhlia-Almazan
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Correspondence to Adriana Muhlia-Almazan.

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Chimeo, C., Fernandez-Gimenez, A.V., Campanella, M. et al. The shrimp mitochondrial FoF1-ATPase inhibitory factor 1 (IF1). J Bioenerg Biomembr 47, 383–393 (2015). https://doi.org/10.1007/s10863-015-9621-0

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