DOI: 10.1111/j.1432-1033.1981.tb05598.x. Formation of Magnesium‐Phosphoenzyme and Magnesium‐Calcium‐Phosphoenzyme in the Phosphorylation of Adenosine Triphosphatase by Orthophosphate in Sarcoplasmic Reticulum

Formation of Magnesium‐Phosphoenzyme and Magnesium‐Calcium‐Phosphoenzyme in the Phosphorylation of Adenosine Triphosphatase by Orthophosphate in Sarcoplasmic Reticulum

10.1111/j.1432-1033.1981.tb05598.x

Crossref journal-article

Wiley

European Journal of Biochemistry (311)

Abstract

The aim of the present study was to test simple reaction sequences which describe calcium‐independent plus calcium‐dependent phosphorylation of sarcoplasmic reticulum transport ATPase by orthophosphate including the function of magnesium in phosphoenzyme formation. The reaction schemes considered were based on the reaction sequence for calcium‐independent phosphorylation proposed previously; namely that the transport enzyme (E) forms a ternary complex (Mg. E. P), by random binding of free magnesium and free orthophosphate, which is in equilibrium with the magnesium‐phosphoenzyme (Mg.E‐P).Phosphorylation, performed at pH 7.0 20°C and a constant free orthophosphate concentration using sarco‐plasmic reticulum vesicles either unloaded or loaded passively with calcium in the presence of 5 mM or 40 mM CaCl2. resulted in a gradual decrease in the apparent magnesium half‐saturation constant and an increase in maximum phosphoprotein formation with increasing calciumloads. When phosphorylation of sarcoplasmicreticulum vesicles preloaded in the presence of 5 mM CaCl2 was performed at a constant free magnesium concentration, a decrease in the apparent otthophosphate half‐saturation constant and an increase in maximum phosphoprotein formation was observed as compared with vesicles from which calcium inside has been removed by ionophore X‐537A plus EGTA treatment; however, both parameters remained unchanged by increasing free magnesium from 20 mM to 30 mM. When phosphorylation of sarcoplasmic reticulum vesicles passively loaded with calcium in the presence of 40 mM CaCl2, at which the saturation of the low‐affinity calcium binding sites of the ATPase is presumably near maximum, was performed at increasing concentrations of free orthophosphate, there was a parallel shift of phosphoprotein formation as a function of free magnesium and vice versa, with no change in the maximum phosphoenzyme formation.Comparison of the experimental data with the pattern of phosphoprotein formation predicted from model equations for various theoretical possible reaction sequences suggests that phosphoenzyme formation from orthophosphate possesses the following features. Firstly, calcium present at the sarcoplasmic reticulum membrane binds to the free enzyme and in sequential order to E. Mg P1 or Mg E‐P or to both, but neither to E. Mg nor to E‐ P1 Secondly, calcium‐independent and calcium‐dependent phosphoproteins are magnesium‐phosphoenzymes. Calcium‐dependent phosphoenzyme is a magnesium‐calcium‐enzyme phosphate complex with 1 magnesium, 2 calciums and 1 orthophosphate (the last covalently) bound to the enzyme [Mg. E‐P. (Cal) 2], and not a ‘calcium‐phosphoprotein’ without bound magnesium.

Bibliography

SUKO, J., PLANK, B., PREIS, P., KOLASSA, N., HELLMANN, G., & CONCA, W. (1981). Formation of MagnesiumâPhosphoenzyme and MagnesiumâCalciumâPhosphoenzyme in the Phosphorylation of Adenosine Triphosphatase by Orthophosphate in Sarcoplasmic Reticulum. European Journal of Biochemistry, 119(2), 225â236. Portico.

Authors 6

Josef SUKO (first)
Brigitte PLANK (additional)
Peter PREIS (additional)
Norbert KOLASSA (additional)
Gertrude HELLMANN (additional)
Walter CONCA (additional)

References 51 Referenced 17

10.1016/0014-5793(71)80196-5
10.1016/0014-5793(72)80466-6
10.1093/oxfordjournals.jbchem.a130045
10.1111/j.1432-1033.1977.tb11705.x
10.1007/BF01906353
10.1007/BFb0048191
10.1021/bi00747a006
10.1016/S0021-9258(19)41988-1
10.1016/S0021-9258(19)41788-2
10.1111/j.1432-1033.1977.tb11936.x
10.1515/znc-1977-9-1027
10.1111/j.1432-1033.1978.tb12754.x
10.1016/0014-5793(79)80596-7
10.1111/j.1432-1033.1979.tb13108.x
10.1021/bi00620a023
10.1016/S0021-9258(19)83539-1
10.1021/bi00559a017
10.1016/S0021-9258(19)69778-4
10.1016/0014-5793(73)80443-0
10.1144/GSL.SP.2005.004.01.09
10.1016/S0021-9258(17)33654-2 / J. Biol. Chem. by Meis L. (1976)
10.1016/0006-291X(78)90867-7
{'key': 'e_1_2_1_24_2', 'first-page': '456', 'volume': '1', 'author': 'Suko J.', 'year': '1980', 'journal-title': 'J. Muscle Res. Cell Motility'} / J. Muscle Res. Cell Motility by Suko J. (1980)
{'key': 'e_1_2_1_25_2', 'first-page': '94', 'volume': '339', 'author': 'Hasselbach W.', 'year': '1963', 'journal-title': 'Biochem. Z.'} / Biochem. Z. by Hasselbach W. (1963)
10.1042/bj0800324
10.1111/j.1432-1033.1978.tb12017.x
10.1016/S0021-9258(17)34244-8
10.1016/0014-5793(78)80806-0
10.1016/S0021-9258(19)86032-5 / J. Biol. Chem. by Michalek M. (1980)
10.1021/bi00639a020
10.1016/S0021-9258(17)33587-1
10.1093/oxfordjournals.jbchem.a132034 / J. Biochem. (Tokyo) by Takisawa H. (1978)
10.1016/S0021-9258(19)86718-2 / J. Biol. Chem. by Chiesi M. (1979)
10.1016/0006-291X(62)90161-4
{'key': 'e_1_2_1_36_2', 'first-page': '80', 'volume': '345', 'author': 'Makinose M.', 'year': '1966', 'journal-title': 'Biochem. Z.'} / Biochem. Z. by Makinose M. (1966)
10.1111/j.1432-1033.1969.tb00657.x
10.1111/j.1432-1033.1976.tb10280.x
10.1111/j.1432-1033.1979.tb19754.x
10.1016/B978-0-12-511050-1.50015-6
10.1016/0005-2736(73)90395-7
{'key': 'e_1_2_1_42_2', 'first-page': '456', 'volume': '1', 'author': 'Makinose M.', 'year': '1980', 'journal-title': 'J. Muscle Res. Cell Motility'} / J. Muscle Res. Cell Motility by Makinose M. (1980)
10.1016/S0021-9258(19)85859-3 / J. Biol. Chem. by Yamada S. (1980)
10.1111/j.1432-1033.1980.tb04788.x
10.1016/S0021-9258(18)43717-9
10.1093/oxfordjournals.jbchem.a129631
10.1016/S0021-9258(17)40816-7 / J. Biol. Chem. by Ribero J. M. C. (1978)
10.1016/S0021-9258(17)30072-8 / J. Biol. Chem. by Shegekawa M. (1979)
10.1016/S0021-9258(17)34914-1 / J. Biol. Chem. by Jones L. R. (1978)
{'key': 'e_1_2_1_50_2', 'first-page': '48', 'volume': '209', 'author': 'Jones L. R.', 'year': '1979', 'journal-title': 'J. Pharmacol. Exp. Ther.'} / J. Pharmacol. Exp. Ther. by Jones L. R. (1979)
10.1007/BF01976037
10.1085/jgp.74.4.457

Dates

Type	When
Created	20 years, 5 months ago (March 3, 2005, 4:26 p.m.)
Deposited	1 year, 9 months ago (Nov. 22, 2023, 11:09 p.m.)
Indexed	1 year, 9 months ago (Nov. 22, 2023, 11:40 p.m.)
Issued	43 years, 11 months ago (Oct. 1, 1981)
Published	43 years, 11 months ago (Oct. 1, 1981)
Published Online	20 years, 6 months ago (March 3, 2005)
Published Print	43 years, 11 months ago (Oct. 1, 1981)

Funders 0

None

BibTeX

@article{SUKO_1981, title={Formation of Magnesium‐Phosphoenzyme and Magnesium‐Calcium‐Phosphoenzyme in the Phosphorylation of Adenosine Triphosphatase by Orthophosphate in Sarcoplasmic Reticulum: Models of a Reaction Sequence}, volume={119}, ISSN={1432-1033}, url={http://dx.doi.org/10.1111/j.1432-1033.1981.tb05598.x}, DOI={10.1111/j.1432-1033.1981.tb05598.x}, number={2}, journal={European Journal of Biochemistry}, publisher={Wiley}, author={SUKO, Josef and PLANK, Brigitte and PREIS, Peter and KOLASSA, Norbert and HELLMANN, Gertrude and CONCA, Walter}, year={1981}, month=oct, pages={225–236} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2023,
        11,
        23
      ]
    ],
    "date-time": "2023-11-23T04:40:09Z",
    "timestamp": 1700714409796
  },
  "reference-count": 51,
  "publisher": "Wiley",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2005,
            3,
            3
          ]
        ],
        "date-time": "2005-03-03T00:00:00Z",
        "timestamp": 1109808000000
      },
      "content-version": "vor",
      "delay-in-days": 8554,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1981,
        10
      ]
    ]
  },
  "abstract": "<jats:p>The aim of the present study was to test simple reaction sequences which describe calcium\u2010independent plus calcium\u2010dependent phosphorylation of sarcoplasmic reticulum transport ATPase by orthophosphate including the function of magnesium in phosphoenzyme formation. The reaction schemes considered were based on the reaction sequence for calcium\u2010independent phosphorylation proposed previously; namely that the transport enzyme (E) forms a ternary complex (Mg. E. P), by random binding of free magnesium and free orthophosphate, which is in equilibrium with the magnesium\u2010phosphoenzyme (Mg.E\u2010P).</jats:p><jats:p>Phosphorylation, performed at pH 7.0 20\u00b0C and a constant free orthophosphate concentration using sarco\u2010plasmic reticulum vesicles either unloaded or loaded passively with calcium in the presence of 5 mM or 40 mM CaCl<jats:sub>2</jats:sub>. resulted in a gradual decrease in the apparent magnesium half\u2010saturation constant and an increase in maximum phosphoprotein formation with increasing calciumloads. When phosphorylation of sarcoplasmicreticulum vesicles preloaded in the presence of 5 mM CaCl<jats:sub>2</jats:sub> was performed at a constant free magnesium concentration, a decrease in the apparent otthophosphate half\u2010saturation constant and an increase in maximum phosphoprotein formation was observed as compared with vesicles from which calcium inside has been removed by ionophore X\u2010537A plus EGTA treatment; however, both parameters remained unchanged by increasing free magnesium from 20 mM to 30 mM. When phosphorylation of sarcoplasmic reticulum vesicles passively loaded with calcium in the presence of 40 mM CaCl<jats:sub>2</jats:sub>, at which the saturation of the low\u2010affinity calcium binding sites of the ATPase is presumably near maximum, was performed at increasing concentrations of free orthophosphate, there was a parallel shift of phosphoprotein formation as a function of free magnesium and vice versa, with no change in the maximum phosphoenzyme formation.</jats:p><jats:p>Comparison of the experimental data with the pattern of phosphoprotein formation predicted from model equations for various theoretical possible reaction sequences suggests that phosphoenzyme formation from orthophosphate possesses the following features. Firstly, calcium present at the sarcoplasmic reticulum membrane binds to the free enzyme and in sequential order to E. Mg P<jats:sub>1</jats:sub> or Mg E\u2010P or to both, but neither to E. Mg nor to E\u2010 P<jats:sub>1</jats:sub> Secondly, calcium\u2010independent and calcium\u2010dependent phosphoproteins are magnesium\u2010phosphoenzymes. Calcium\u2010dependent phosphoenzyme is a magnesium\u2010calcium\u2010enzyme phosphate complex with 1 magnesium, 2 calciums and 1 orthophosphate (the last covalently) bound to the enzyme [Mg. E\u2010P. (Cal) <jats:sub>2</jats:sub>], and not a \u2018calcium\u2010phosphoprotein\u2019 without bound magnesium.</jats:p>",
  "DOI": "10.1111/j.1432-1033.1981.tb05598.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        3,
        3
      ]
    ],
    "date-time": "2005-03-03T21:26:34Z",
    "timestamp": 1109885194000
  },
  "page": "225-236",
  "source": "Crossref",
  "is-referenced-by-count": 17,
  "title": "Formation of Magnesium\u2010Phosphoenzyme and Magnesium\u2010Calcium\u2010Phosphoenzyme in the Phosphorylation of Adenosine Triphosphatase by Orthophosphate in Sarcoplasmic Reticulum",
  "prefix": "10.1111",
  "volume": "119",
  "author": [
    {
      "given": "Josef",
      "family": "SUKO",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Brigitte",
      "family": "PLANK",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Peter",
      "family": "PREIS",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Norbert",
      "family": "KOLASSA",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Gertrude",
      "family": "HELLMANN",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Walter",
      "family": "CONCA",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2005,
        3,
        3
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(71)80196-5"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(72)80466-6"
    },
    {
      "key": "e_1_2_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/oxfordjournals.jbchem.a130045"
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1977.tb11705.x"
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01906353"
    },
    {
      "key": "e_1_2_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BFb0048191"
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00747a006"
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)41988-1"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)41788-2"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1977.tb11936.x"
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1515/znc-1977-9-1027"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1978.tb12754.x"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(79)80596-7"
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1979.tb13108.x"
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00620a023"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)83539-1"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00559a017"
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)69778-4"
    },
    {
      "key": "e_1_2_1_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(73)80443-0"
    },
    {
      "key": "e_1_2_1_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1144/GSL.SP.2005.004.01.09"
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "2055",
      "DOI": "10.1016/S0021-9258(17)33654-2",
      "volume": "251",
      "author": "Meis L.",
      "year": "1976",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(78)90867-7"
    },
    {
      "key": "e_1_2_1_24_2",
      "first-page": "456",
      "volume": "1",
      "author": "Suko J.",
      "year": "1980",
      "journal-title": "J. Muscle Res. Cell Motility"
    },
    {
      "key": "e_1_2_1_25_2",
      "first-page": "94",
      "volume": "339",
      "author": "Hasselbach W.",
      "year": "1963",
      "journal-title": "Biochem. Z."
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj0800324"
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1978.tb12017.x"
    },
    {
      "key": "e_1_2_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)34244-8"
    },
    {
      "key": "e_1_2_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(78)80806-0"
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "1317",
      "DOI": "10.1016/S0021-9258(19)86032-5",
      "volume": "255",
      "author": "Michalek M.",
      "year": "1980",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00639a020"
    },
    {
      "key": "e_1_2_1_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)33587-1"
    },
    {
      "key": "e_1_2_1_33_2",
      "doi-asserted-by": "crossref",
      "first-page": "1275",
      "DOI": "10.1093/oxfordjournals.jbchem.a132034",
      "volume": "83",
      "author": "Takisawa H.",
      "year": "1978",
      "journal-title": "J. Biochem. (Tokyo)"
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "10370",
      "DOI": "10.1016/S0021-9258(19)86718-2",
      "volume": "254",
      "author": "Chiesi M.",
      "year": "1979",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(62)90161-4"
    },
    {
      "key": "e_1_2_1_36_2",
      "first-page": "80",
      "volume": "345",
      "author": "Makinose M.",
      "year": "1966",
      "journal-title": "Biochem. Z."
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1969.tb00657.x"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1976.tb10280.x"
    },
    {
      "key": "e_1_2_1_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1979.tb19754.x"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/B978-0-12-511050-1.50015-6"
    },
    {
      "key": "e_1_2_1_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2736(73)90395-7"
    },
    {
      "key": "e_1_2_1_42_2",
      "first-page": "456",
      "volume": "1",
      "author": "Makinose M.",
      "year": "1980",
      "journal-title": "J. Muscle Res. Cell Motility"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "crossref",
      "first-page": "3108",
      "DOI": "10.1016/S0021-9258(19)85859-3",
      "volume": "255",
      "author": "Yamada S.",
      "year": "1980",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1980.tb04788.x"
    },
    {
      "key": "e_1_2_1_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)43717-9"
    },
    {
      "key": "e_1_2_1_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/oxfordjournals.jbchem.a129631"
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "crossref",
      "first-page": "3153",
      "DOI": "10.1016/S0021-9258(17)40816-7",
      "volume": "253",
      "author": "Ribero J. M. C.",
      "year": "1978",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "crossref",
      "first-page": "4726",
      "DOI": "10.1016/S0021-9258(17)30072-8",
      "volume": "254",
      "author": "Shegekawa M.",
      "year": "1979",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "crossref",
      "first-page": "1643",
      "DOI": "10.1016/S0021-9258(17)34914-1",
      "volume": "253",
      "author": "Jones L. R.",
      "year": "1978",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_50_2",
      "first-page": "48",
      "volume": "209",
      "author": "Jones L. R.",
      "year": "1979",
      "journal-title": "J. Pharmacol. Exp. Ther."
    },
    {
      "key": "e_1_2_1_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01976037"
    },
    {
      "key": "e_1_2_1_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1085/jgp.74.4.457"
    }
  ],
  "container-title": "European Journal of Biochemistry",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1432-1033.1981.tb05598.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://febs.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1432-1033.1981.tb05598.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        11,
        23
      ]
    ],
    "date-time": "2023-11-23T04:09:29Z",
    "timestamp": 1700712569000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://febs.onlinelibrary.wiley.com/doi/10.1111/j.1432-1033.1981.tb05598.x"
    }
  },
  "subtitle": [
    "Models of a Reaction Sequence"
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1981,
        10
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1981,
          10
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1432-1033.1981.tb05598.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1432-1033.1981.tb05598.x",
  "relation": {},
  "ISSN": [
    "0014-2956",
    "1432-1033"
  ],
  "subject": [],
  "container-title-short": "European Journal of Biochemistry",
  "published": {
    "date-parts": [
      [
        1981,
        10
      ]
    ]
  }
}