Summary
Pyruvate kinase (PK) exists as at least two electrophoretically distinguishable, tissue specific form in the river sturgeonAcipenser fulvenscens. In contrast with the PK isozyme system in other vertebrates, the isozyme present in muscle is also present in non-musclce tissues, notably the spleen. The presence of a five membered set of hybrids in liver, gills, eyes and intestine suggests that the synthesis of this isozyme occurs in other tissues as well. Thus, in this primitive vertebrate, the specialization of one PK isozyme for function in muscle tissues is not complete. Sturgeon muscle PK had slightly cooperative phosphoenolpyruvate (PEP) saturation curves (S0.5=0.33 mM) and a Hill coefficient,n H, of 1.24, and was strongly activated by fructose 1,6 bisphosphate (PEP S0.5=0.098 mM;n H=1.0). The enzyme was strongly inhibited by phenylalanine, alanine and MgATP. Fructose 1,6 bisphosphate (FBP) not only totally reversed these inhibitory effects, but also activated the enzyme to the same extent as in the absence of the inhibitors. These kinetic properties closely resemble those of vertebrate type K pyruvate kinases, and are quite distinct from those of higher vertebrate type M isozymes. Nevertheless, immunotitration studies indicate structural homology among the sturgeon, frog and dog muscle PK's as they are all precipitated by antisera to the other forms. This maintenance of structural homology, despite a marked degree of functional differentiation, suggests that only small structural modifications were required to generate the functionally specialized forms of muscle PK found among the vertebrates.
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Abbreviations
- PK :
-
pyruvate kinase
- PEP :
-
phosphoenolpyruvate
- FBP :
-
fructose 1,6-bisphosphate
References
Anderson PJ, Randall RF (1975) Comparison of the subunit and primary structures of the pyruvate kinases from rabbit and sturgeon muscles. Biochem J 145:575–579
Beis I, Newsholme EA (1975) The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem J 152:23–32
Berglund L, Humble E (1979) Kinetic properties of pig pyruvate kinases type A from kidney and type M from muscle. Arch Biochem Biophys 195:347–361
Black JA, Harkins RN (1977) Amino acid compositions and evolutionary relationships with protein families. J Theor Biol 66:281–295
Bücher T, Pfleiderer G (1955) Pyruvate kinase from muscle. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 1. Academic Press, New York, pp 435–440
Cardenas JM, Dyson RD, Strandholm JJ (1973) Bovine pyruvate kinases I. Purification and characterization of the skeletal muscle isozyme. J Biol Chem 248:6931–6937
Cardenas JM, Blachly EG, Ceccotti PL, Dyson RD (1975a) Properties of chicken skeletal muscle pyruvate kinase and a proposal for its evolutionary relationship to the other avian and mammalian isozymes. Biochemistry 14:2247–2252
Cardenas JM, Strandholm JJ, Miller JN (1975b) Effects of phenylalanine and alanine on the kinetics of bovine pyruvate kinase isozymes. Biochemistry 14:4041–4045
Cardenas JM, Dyson RD, Strandholm JJ (1975c) Bovine and chicken pyruvate kinase isozymes intraspecies and interspecies hybrids. In: Markert CL (ed) Isozymes, vol 1, Molecular function. Academic Press, New York, pp 523–541
Eigenbrodt E, Schoner W (1977) Purification and properties of the pyruvate kinase isozymes type L and M2 from chicken liver. Hoppe Seyler's Z Physiol Chem 358:1033–1046
Feliu JE, Sols A (1976) Interconversion phenomena between two kinetic forms of class A pyruvate kinase from Ehrlich ascites tumor cells. Mol Cell Biochem 13:31–44
Fields JHA, Driedzic WR, French CJ, Hochachka PW (1978) Some kinetic properties of skeletal muscle pyruvate kinase from air-breathing and water-breathing fish of the Amazon. Can J Zool 56:751–758
Flanders LE, Bamburg JR, Sallach HJ (1971) Pyruvate kinase isozymes in adult tissue and eggs ofRana pipiens II. Physical and kinetic studies of purified skeletal and heart muscle pyruvate kinases. Biochim Biophys Acta 242:566–579
Guderley HE, Storey KB, Fields JHA, Hochachka PW (1976) Catalytic and regulatory properties of pyruvate kinase isozymes from octopus mantle muscle and liver. Can J Zool 54:863–870
Guderley HE, Fields JHA, Cardenas JM, Hochachka PW (1978) Pyruvate kinase from the liver and kidney ofArapaima gigas. Can J Zool 56:852–859
Guderley HE, Cardenas JM (1979) Developmental changes in the pyruvate kinase isozymes of coho salmon. J Exp Zool 208:1–12
Guderley HE, Cardenas JM (1980) A study of the catalytic properties of pyruvate kinase isozymes from salmon and an examination of their functional relationships. J Exp Zool 212:269–277
Hance AJ, Lee J, Feitelson M (1982) The M1 and M2 isozymes of pyruvate kinase are products of the same gene. Biochem Biophys Res Commun 106:492–499
Harris W, Days R, Johnson C, Finkelstein I, Stallworth J, Hubert C (1977) Studies on avian heart pyruvate kinase during development. Biochem Biophys Res Commun 75:1117–1121
Ibsen KH, Trippet P (1974) Effects of amino acids on the kinetic properties of three noninterconvertible rat pyruvate kinases. Arch Biochem Biophys 163:570–580
Ibsen KH, Marles SW (1976) Inhibition of chicken pyruvate kinases by amino acids. Biochemistry 15:1073–1079
Ibsen KH, Murray L, Marles SW (1976) Electrofocusing and kinetic studies of adult and embryonic chicken pyruvate kinases. Biochemistry 15:1064–1073
Ibsen KH, Cardin JP Jr, Chiu RHC, Garratt KN, Marles SW, Doty JR (1980) Distribution of pyruvate kinase isozymes in adult and developingXenopus laevis. Comp Biochem Physiol 65B:473–480
Ibsen KH, Chiu RHC, Park HR, Sanders DA, Roy S, Garratt KN, Mueller MK (1981) Purification and properties of mouse pyruvate kinases K and M and of a modified K subunit. Biochemistry 20:1497–1506
Imamura K, Tanaka T (1972) Multimolecular forms of pyruvate kinase from rat and other mammalian tissues. I. Electrophoretic studies. J Biochem 71:1043–1051
Imamura K, Taniuchi K, Tanaka T (1972) Multimolecular forms of pyruvate kinase. II. Purification of M2-type pyruvate kinase from Yoshida ascites hepatoma 130 cells and comparative studies of the enzymological and immunological properties of the three types of pyruvate kinase L, M, and M2. J Biochem 72:1001–1015
Kwan CY, Gabriel JL, Davis RC (1980) Comparative studies of kinetic and optical properties of rabbit muscle, sturgeon muscle and yeast pyruvate kinase. Can J Biochem 58:194–200
Levin MJ, Daegelen D, Meinehofer MC, Dreyfus JC, Kahn A (1982) Two different species of messenger RNAs specify synthesis of M1 and M2 pyruvate kinase subunits. Biochim Biophys Acta 699:77–83
Low PS, Somero GN (1976) Adaptation of muscle pyruvate kinases to environmental temperatures and pressures. J Exp Zool 198:1–12
Munday KA, Giles IG, Poat PC (1980) Review of the comparative biochemistry of pyruvate kinase. Comp Biochem Physiol 67B:403–411
Mustafa T, Moon TW, Hochachka PW (1971) Effects of pressure and temperature on the catalytic and regulatory properties of muscle pyruvate kinase from an off-shore benthic fish. Am Zool 11:451–466
Peters J, Nash HR, Eicher EM, Bulfield G (1981) Polymorphism of kidney pyruvate kinase in mouse is determined by a gene, PK-3, on chromosome 9. Biochem Genet 19:757–769
Philipps FC, Ainsworth S (1977) Allosteric properties of rabbit muscle pyruvate kinase. Int J Biochem 8:729–735
Randall RF, Anderson PJ (1975) Purification and properties of the pyruvate kinase of sturgeon muscle. Biochem J 145:569–573
Schloen LH, Bamburg JR, Sallach HJ (1969) Isozymes of pyruvate kinase in tissues and eggs ofRana pipiens. Biochem Biophys Res Commun 36:823–829
Schloen LH, Kmiotek EH, Sallach HJ (1974) Pyruvate kinase isozymes in adult tissues and eggs ofRana pipiens. Arch Biochem Biophys 164:254–265
Scrutton MC, Utter UF (1968) The regulation of glycolysis and gluconeogenesis in animal tissues. Annu Rev Biochem 37:249–302
Somero GN, Hochachka PW (1968) The effect of temperature on catalytic and regulatory functions of pyruvate kinases of the rainbow trout and the antarctic fish,Trematomus bernacchii. Biochem J 110:395–400
Storey KB, Hochachka PW (1974) Enzymes of energy metabolism in a vertebrate facultative anaerobe,Pseudemys scripta, turtle heart pyruvate kinase. J Biol Chem 249:1423–1427
Strandholm JJ, Cardenas JM, Dyson RD (1975) Pyruvate kinase isozymes in adult and fetal tissues of chicken. Biochemistry 14:2242–2246
Susor WA, Rutter WJ (1971) Method for the detection of pyruvate kinase, aldolase and other pyridine nucleotide linked enzyme activities after electrophoresis. Anal Biochem 43:147–155
Van Berkel TJC, Koster JF, Hulsmann WC (1973) Some kinetic properties of the allosteric M type pyruvate kinase from rat liver; influence of pH and the nature of amino acid inhibition. Biochim Biophys Acta 321:171–180
Wu SWN, Wong SC, Yeung D (1978) Comparative studies of vertebrate and invertebrate pyruvate kinases. Comp Biochem Physiol 61B:93–98
Zammit VA, Beis I, Newsholme EA (1978) Maximum activities and effects of fructose bisphosphate on pyruvate kinase from muscles of vertebrates and invertebrates in relation to the control of glycolysis. Biochem J 174:989–998
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Guderley, H., Hamel, L. & Lafond, J. Close resemblance between muscle pyruvate kinase from a primitive vertebrate, the river sturgeonAcipenser fulvenscens, and the ancestral type K isozyme. J Comp Physiol B 153, 247–256 (1983). https://doi.org/10.1007/BF00689628
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DOI: https://doi.org/10.1007/BF00689628