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NAD-preferring malic enzyme: localization, regulation and its potential role in herring (Clupea harengus) sperm cells

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Abstract

Herring spermatozoa exhibit a high activity of NAD-preferring malic enzyme (NAD-ME). This enzyme is involved in the generation of NADH or NADPH in the decarboxylation of malate to form pyruvate and requires some divalent cations to express its activity. In order to confirm that NAD-ME isolated from herring sperm cells is localized in mitochondria, we performed immunofluorescent analysis and assayed spectrophotometrically the malic enzyme reaction. Production of polyclonal rabbit antibodies against NAD-ME from herring spermatozoa enabled identification of mitochondrial localization of this enzyme inside herring spermatozoa. The kinetic studies revealed that NAD-ME was competitively inhibited by ATP up to tenfold. Addition of fumarate reversed ATP-dependent inhibition of NAD-ME to 55 % of its maximum activity. The pH-dependent regulation of malic enzyme activity was also examined. Malic enzyme showed maximum activity at pH near 7.0 in all studied conditions. Finally, the role of malic enzyme activity regulation in mitochondria of herring sperm cells was discussed.

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References

  • Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030–4034

    Article  CAS  PubMed  Google Scholar 

  • Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5:593–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biegniewska A, Thebault MT, Ziętara M, Skorkowski EF (1993) Antagonism between cadmium chloride and divalent metal cations in the activation of malic enzyme. Comp Biochem Physiol C 104:155–158

    Article  Google Scholar 

  • Biegniewska A, Zietara MS, Rurangwa E, Ollevier F, Swierczynski J, Skorkowski EF (2010) Some differences between carp (Cyprinus carpio) and African catfish (Clarias gariepinus) spermatoza motility. J Appl Ichthyol 26:674–677

    Article  Google Scholar 

  • Christen R, Gatti JL, Billard R (1987) Trout sperm motility. The transient movement of trout sperm is related to changes in the concentration of ATP following the activation of the flagellar movement. Eur J Biochem 166:667–671

    Article  CAS  PubMed  Google Scholar 

  • Cosson JJ (2008) The motility apparatus of fish spermatozoa. In: Alavi SMH, Cosson JJ, Coward K, Rafiee G (eds) Fish spermatology. Alpha Science International Ltd, Oxford, pp 281–316

    Google Scholar 

  • Dreanno C, Cosson J, Suquet M, Seguin F, Dorange G, Billard R (1999) Nucleotide content, oxidative phosphorylation, morphology, and fertilizing capacity of turbot (Psetta maxima) spermatozoa during the motility period. Mol Reprod Dev 53:230–243

    Article  CAS  PubMed  Google Scholar 

  • Dzyuba V, Cosson J (2014) Motility of fish spermatozoa: from external signaling to flagella response. Reprod Biol 14:165–175

    Article  PubMed  Google Scholar 

  • Geffen AJ (2009) Advances in herring biology: from simple to complex, coping with plasticity and adaptability. ICES J Mar Sci 66:1688–1695

    Article  Google Scholar 

  • Gronczewska J, Zietara MS, Biegniewska A, Skorkowski EF (2003) Enzyme activities in fish spermatozoa with focus on lactate dehydrogenase isoenzymes from herring Clupea harengus. Comp Biochem Physiol B Biochem Mol Biol 134:399–406

    Article  PubMed  Google Scholar 

  • Grzyb K, Skorkowski EF (2005) Characterization of creatine kinase isoforms in herring (Clupea harengus) skeletal muscle. Comp Biochem Physiol 140B:629–634

    Article  CAS  Google Scholar 

  • Grzyb K, Skorkowski EF (2006) Purification and some properties of two creatine kinase isoforms from herring (Clupea harengus) spermatozoa. Comp Biochem Physiol 144B:152–158

    Article  CAS  Google Scholar 

  • Grzyb K, Rychłowski M, Biegniewska A, Skorkowski EF (2003) Quantitative determination of creatine kinase release from herring (Clupea harengus) spermatozoa induced by tributyltin. Comp Biochem Physiol 134C:207–213

    CAS  Google Scholar 

  • Hsieh JY, Liu GY, Hung HC (2008) Influential factor contributing to the isoform-specific inhibition by ATP of human mitochondrial NAD(P)+-dependent malic enzyme: functional roles of the nucleotide binding site Lys346. FEBS J 21:5383–5392

    Article  Google Scholar 

  • Hsieh JY, Chen SH, Hung HC (2009) Functional roles of the tetramer organization of malic enzyme. J Biol Chem 284:18096–18105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu WC, Hung HC, Tong L, Chang GG (2004) Dual functional roles of ATP in the human mitochondrial malic enzyme. Biochemistry 43:7382–7390

    Article  CAS  PubMed  Google Scholar 

  • Ingermann RL (2008) Energy metabolism and respiration in fish spermatozoa. Fish spermatology. Alpha Science Intl Ltd, Oxford, pp 241–266

    Google Scholar 

  • Lahnsteiner F, Patzner RA, Weismann T (1993) Energy resources of spermatozoa of the rainbow trout Oncorhynchus mykiss (Pisces, Teleostei). Reprod Nutr Dev 33:349–360

    Article  CAS  PubMed  Google Scholar 

  • Lin RC, Davis EJ (1974) Malic enzyme of rabbit heart mitochondria. J Biol Chem 249:3867–3875

    CAS  PubMed  Google Scholar 

  • Mansour N, Lahnsteiner F, Berger B (2003) Metabolism of intratesticular spermatozoa of a tropical teleost fish (Clarias garienpinus). Comp Biochem Physiol 135B:285–296

    Article  CAS  Google Scholar 

  • Mommsen TP (2004) Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Comp Biochem Physiol 139B:383–400

    Article  CAS  Google Scholar 

  • Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58:1785–1799

    Article  CAS  Google Scholar 

  • Niedźwiecka N, Skorkowski EF (2013) Purification and properties of malic enzyme from herring Clupea harengus spermatozoa. Comp Biochem Physiol 164B:216–220

    Article  Google Scholar 

  • Oda S, Igarashi Y, Ohtake H, Sakai K, Shimizu N, Morisawa M (1995) Sperm-activating proteins from unfertilized eggs of the Pacific herring, Clupea pallasii. Dev Growth Differ 37:257–261

    Article  CAS  Google Scholar 

  • Oda S, Igarashi Y, Manak K, Koibuchi N, Sakai-Sawada M, Sakai K, Morisawa M, Ohtake H, Shimizu N (1998) Sperm-activating proteins obtained from the herring eggs are homologous to trypsin inhibitors and synthesized in follicle cells. Dev Biol 204:55–63

    Article  CAS  PubMed  Google Scholar 

  • Rurangwa E, Biegniewska A, Swierczynski J, Ollevier F, Skorkowski EF (2001) Adenylate energy charge in fish spermatozoa: influence of pituitary hormons? In: Goos HJTh, Rastogi RK, Vaudry H, Pierantoni R (eds) Perspective in comparative endocrinology: unity and diversity. Menduzzi Editore, Bologna, pp 1203–1208

    Google Scholar 

  • Saudrais C, Garber AT, McKay DJ, Dixon GH, Loir M (1996) Creatine kinase in trout male germ cells: purification, gene expression, and localization in the testis. Mol Reprod Dev 44:433–442

    Article  CAS  PubMed  Google Scholar 

  • Saudrais C, Fierville F, Loir M, Le Rumeur E, Cibert C, Cosson J (1998) The use of phosphocreatine plus ADP as energy source for motility of membrane-deprived trout spermatozoa. Cell Motil Cytoskelet 41:91–106

    Article  CAS  Google Scholar 

  • Sauer LA (1973) Mitochondrial NAD-dependent malic enzyme: a new regulatory enzyme. FEBS Lett 33:251–255

    Article  CAS  PubMed  Google Scholar 

  • Schlegel J, Wyss M, Eppenberger HM, Wallimann T (1990) Functional studies with the octameric and dimeric form of mitochondrial creatine kinase. Differential pH- dependent association of the two oligomeric forms with the inner mitochondrial membrane. J Biol Chem 265:9221–9227

    CAS  PubMed  Google Scholar 

  • Skorkowski EF (1988) Mitochondrial malic enzyme from crustacean and fish muscle. Comp Biochem Physiol 90B:19–24

    CAS  Google Scholar 

  • Skorkowski EF, Storey KB (1988) Mitochondrial NAD(P)-malic enzyme from herring skeletal muscle. Fish Physiol Biochem 5:241–248

    Article  CAS  PubMed  Google Scholar 

  • Skorkowski EF, Aleksandrowicz Z, Scislowski PWD, Swierczynski J (1984) Evidence for the role of malic enzyme in the rapid oxidation of malate by cod heart mitochondria. Comp Biochem Physiol 77B:379–384

    CAS  Google Scholar 

  • Tombes RM, Shapiro BM (1989) Energy transport and cell polarity: relationship of phosphagen kinase activity to sperm function. J Exp Zool 251:82–90

    Article  CAS  PubMed  Google Scholar 

  • Vines CA, Yoshida K, Griffin FJ, Pillai MC, Morisawa M, Yanagimachi R, Cherr GN (2002) Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange. Proc Natl Acad Sci 99:2026–2031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Zhang H, Hung HC, Kuo CC, Tsai LC, Yuan HS, Chou WY, Chang GG, Tong L (2002) Structural studies of the pigeon cytosolic NADP(+)-dependent malic enzyme. Protein Sci 11:332–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziętara MS, Biegniewska A, Rurangwa E, Świerczyński J, Ollevier F, Skorkowski EF (2009) Bioenergetics of fish spermatozoa during semen storage. Fish Physiol Biochem 35:607–614

    Article  PubMed  Google Scholar 

  • Żołnierowicz S, Świerczyński J, Żelewski L (1988) Purification and properties of the NAD(P)-dependent malic enzyme from human placental mitochondria. Biochem Med Metab 39:208–216

    Article  Google Scholar 

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Acknowledgments

This paper is dedicated to Professor Mariusz M. Żydowo former head of the Department of Biochemistry, Medical University of Gdańsk and lecturer at Gdańsk University on his 90th birthday. This study was supported by the Polish Ministry of Science and Higher Education Project No. 538-L165-0807-12.

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  1. Department of Molecular Evolution, Faculty of Biology, University of Gdańsk, 80-308, Gdańsk, Poland

    Natalia Niedźwiecka, Jadwiga Gronczewska & Edward F. Skorkowski

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  1. Natalia Niedźwiecka
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  2. Jadwiga Gronczewska
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  3. Edward F. Skorkowski
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Correspondence to Natalia Niedźwiecka.

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Niedźwiecka, N., Gronczewska, J. & Skorkowski, E.F. NAD-preferring malic enzyme: localization, regulation and its potential role in herring (Clupea harengus) sperm cells. Fish Physiol Biochem 43, 351–360 (2017). https://doi.org/10.1007/s10695-016-0291-6

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