Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 2000 Sep 15;350(Pt 3):609–629.

Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism.

B E Maden 1
PMCID: PMC1221290  PMID: 10970772

Abstract

In most organisms, tetrahydrofolate (H(4)folate) is the carrier of C(1) fragments between formyl and methyl oxidation levels. The C(1) fragments are utilized in several essential biosynthetic processes. In addition, C(1) flux through H(4)folate is utilized for energy metabolism in some groups of anaerobic bacteria. In methanogens and several other Archaea, tetrahydromethanopterin (H(4)MPT) carries C(1) fragments between formyl and methyl oxidation levels. At first sight H(4)MPT appears to resemble H(4)folate at the sites where C(1) fragments are carried. However, the two carriers are functionally distinct, as discussed in the present review. In energy metabolism, H(4)MPT permits redox-flux features that are distinct from the pathway on H(4)folate. In the reductive direction, ATP is consumed in the entry of carbon from CO(2) into the H(4)folate pathway, but not in entry into the H(4)MPT pathway. In the oxidative direction, methyl groups are much more readily oxidized on H(4)MPT than on H(4)folate. Moreover, the redox reactions on H(4)MPT are coupled to more negative reductants than the pyridine nucleotides which are generally used in the H(4)folate pathway. Thermodynamics of the reactions of C(1) reduction via the two carriers differ accordingly. A major underlying cause of the thermodynamic differences is in the chemical properties of the arylamine nitrogen N(10) on the two carriers. In H(4)folate, N(10) is subject to electron withdrawal by the carbonyl group of p-aminobenzoate, but in H(4)MPT an electron-donating methylene group occurs in the corresponding position. It is also proposed that the two structural methyl groups of H(4)MPT tune the carrier's thermodynamic properties through an entropic contribution. H(4)MPT appears to be unsuited to some of the biosynthetic functions of H(4)folate, in particular the transfer of activated formyl groups, as in purine biosynthesis. Evidence bearing upon whether H(4)MPT participates in thymidylate synthesis is discussed. Findings on the biosynthesis and phylogenetic distribution of the two carriers and their evolutionary implications are briefly reviewed. Evidence suggests that the biosynthetic pathways to the two carriers are largely distinct, suggesting the possibility of (ancient) separate origins rather than divergent evolution. It has recently been discovered that some eubacteria which gain energy by oxidation of C(1) compounds contain an H(4)MPT-related carrier, which they are thought to use in energy metabolism, as well as H(4)folate, which they are thought to use for biosynthetic reactions.

Full Text

The Full Text of this article is available as a PDF (316.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Afting C, Hochheimer A, Thauer RK. Function of H2-forming methylenetetrahydromethanopterin dehydrogenase from methanobacterium thermoautotrophicum in coenzyme F420 reduction with H2 . Arch Microbiol. 1998 Mar;169(3):206–210. doi: 10.1007/s002030050562. [DOI] [PubMed] [Google Scholar]
  2. Allaire M., Li Y., MacKenzie R. E., Cygler M. The 3-D structure of a folate-dependent dehydrogenase/cyclohydrolase bifunctional enzyme at 1.5 A resolution. Structure. 1998 Feb 15;6(2):173–182. doi: 10.1016/s0969-2126(98)00019-7. [DOI] [PubMed] [Google Scholar]
  3. Allen J. R., Clark D. D., Krum J. G., Ensign S. A. A role for coenzyme M (2-mercaptoethanesulfonic acid) in a bacterial pathway of aliphatic epoxide carboxylation. Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8432–8437. doi: 10.1073/pnas.96.15.8432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. Methanogens: reevaluation of a unique biological group. Microbiol Rev. 1979 Jun;43(2):260–296. doi: 10.1128/mr.43.2.260-296.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Balch W. E., Magrum L. J., Fox G. E., Wolfe R. S., Woese C. R. An ancient divergence among the bacteria. J Mol Evol. 1977 Aug 5;9(4):305–311. doi: 10.1007/BF01796092. [DOI] [PubMed] [Google Scholar]
  6. Barlowe C. K., Appling D. R. Isolation and characterization of a novel eukaryotic monofunctional NAD(+)-dependent 5,10-methylenetetrahydrofolate dehydrogenase. Biochemistry. 1990 Jul 31;29(30):7089–7094. doi: 10.1021/bi00482a020. [DOI] [PubMed] [Google Scholar]
  7. Bayley S. T., Morton R. A. Recent developments in the molecular biology of extremely halophilic bacteria. CRC Crit Rev Microbiol. 1978;6(2):151–205. doi: 10.3109/10408417809090622. [DOI] [PubMed] [Google Scholar]
  8. Benkovic S. J. On the mechanism of action of folate- and biopterin-requiring enzymes. Annu Rev Biochem. 1980;49:227–251. doi: 10.1146/annurev.bi.49.070180.001303. [DOI] [PubMed] [Google Scholar]
  9. Bertram P. A., Thauer R. K. Thermodynamics of the formylmethanofuran dehydrogenase reaction in Methanobacterium thermoautotrophicum. Eur J Biochem. 1994 Dec 15;226(3):811–818. doi: 10.1111/j.1432-1033.1994.t01-1-00811.x. [DOI] [PubMed] [Google Scholar]
  10. Blakley R. L. Eukaryotic dihydrofolate reductase. Adv Enzymol Relat Areas Mol Biol. 1995;70:23–102. doi: 10.1002/9780470123164.ch2. [DOI] [PubMed] [Google Scholar]
  11. Bobik T. A., Wolfe R. S. Activation of formylmethanofuran synthesis in cell extracts of Methanobacterium thermoautotrophicum. J Bacteriol. 1989 Mar;171(3):1423–1427. doi: 10.1128/jb.171.3.1423-1427.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Breitung J., Thauer R. K. Formylmethanofuran: tetrahydromethanopterin formyltransferase from Methanosarcina barkeri. Identification of N5-formyltetrahydromethanopterin as the product. FEBS Lett. 1990 Nov 26;275(1-2):226–230. doi: 10.1016/0014-5793(90)81477-6. [DOI] [PubMed] [Google Scholar]
  13. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. doi: 10.1126/science.273.5278.1058. [DOI] [PubMed] [Google Scholar]
  14. Bystroff C., Oatley S. J., Kraut J. Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate.NADP+ ternary complex. Substrate binding and a model for the transition state. Biochemistry. 1990 Apr 3;29(13):3263–3277. doi: 10.1021/bi00465a018. [DOI] [PubMed] [Google Scholar]
  15. Carreras C. W., Santi D. V. The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem. 1995;64:721–762. doi: 10.1146/annurev.bi.64.070195.003445. [DOI] [PubMed] [Google Scholar]
  16. Champness J. N., Stammers D. K., Beddell C. R. Crystallographic investigation of the cooperative interaction between trimethoprim, reduced cofactor and dihydrofolate reductase. FEBS Lett. 1986 Apr 7;199(1):61–67. doi: 10.1016/0014-5793(86)81224-8. [DOI] [PubMed] [Google Scholar]
  17. Chen L., MacMillan A. M., Chang W., Ezaz-Nikpay K., Lane W. S., Verdine G. L. Direct identification of the active-site nucleophile in a DNA (cytosine-5)-methyltransferase. Biochemistry. 1991 Nov 19;30(46):11018–11025. doi: 10.1021/bi00110a002. [DOI] [PubMed] [Google Scholar]
  18. Chen Z., Crippen K., Gulati S., Banerjee R. Purification and kinetic mechanism of a mammalian methionine synthase from pig liver. J Biol Chem. 1994 Nov 4;269(44):27193–27197. [PubMed] [Google Scholar]
  19. Chistoserdova L. V., Lidstrom M. E. Genetics of the serine cycle in Methylobacterium extorquens AM1: identification of sgaA and mtdA and sequences of sgaA, hprA, and mtdA. J Bacteriol. 1994 Apr;176(7):1957–1968. doi: 10.1128/jb.176.7.1957-1968.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Chistoserdova L., Vorholt J. A., Thauer R. K., Lidstrom M. E. C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science. 1998 Jul 3;281(5373):99–102. doi: 10.1126/science.281.5373.99. [DOI] [PubMed] [Google Scholar]
  21. Clark J. E., Ljungdahl L. G. Purification and properties of 5,10-methenyltetrahydrofolate cyclohydrolase from Clostridium formicoaceticum. J Biol Chem. 1982 Apr 10;257(7):3833–3836. [PubMed] [Google Scholar]
  22. Clark J. E., Ljungdahl L. G. Purification and properties of 5,10-methylenetetrahydrofolate reductase, an iron-sulfur flavoprotein from Clostridium formicoaceticum. J Biol Chem. 1984 Sep 10;259(17):10845–10849. [PubMed] [Google Scholar]
  23. Conway J. G., Kauffman F. C., Thurman R. G. Genetic regulation of NADPH supply in perfused mouse liver. Role of the Ah locus during induction by 3-methylcholanthrene. J Biol Chem. 1983 Mar 25;258(6):3825–3831. [PubMed] [Google Scholar]
  24. Curthoys N. P., Rabinowitz J. C. Formyltetrahydrofolate synthetase. Binding of folate substrates and kinetics of the reverse reaction. J Biol Chem. 1972 Apr 10;247(7):1965–1971. [PubMed] [Google Scholar]
  25. Delk A. S., Nagle D. P., Jr, Rabinowitz J. C. Methylenetetrahydrofolate-dependent biosynthesis of ribothymidine in transfer RNA of Streptococcus faecalis. Evidence for reduction of the 1-carbon unit by FADH2. J Biol Chem. 1980 May 25;255(10):4387–4390. [PubMed] [Google Scholar]
  26. Delle Fratte S., White R. H., Maras B., Bossa F., Schirch V. Purification and properties of serine hydroxymethyltransferase from Sulfolobus solfataricus. J Bacteriol. 1997 Dec;179(23):7456–7461. doi: 10.1128/jb.179.23.7456-7461.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Dev I. K., Harvey R. J. A complex of N5,N10-methylenetetrahydrofolate dehydrogenase and N5,N10-methenyltetrahydrofolate cyclohydrolase in Escherichia coli. Purification, subunit structure, and allosteric inhibition by N10-formyltetrahydrofolate. J Biol Chem. 1978 Jun 25;253(12):4245–4253. [PubMed] [Google Scholar]
  28. DiMarco A. A., Bobik T. A., Wolfe R. S. Unusual coenzymes of methanogenesis. Annu Rev Biochem. 1990;59:355–394. doi: 10.1146/annurev.bi.59.070190.002035. [DOI] [PubMed] [Google Scholar]
  29. DiMarco A. A., Donnelly M. I., Wolfe R. S. Purification and properties of the 5,10-methenyltetrahydromethanopterin cyclohydrolase from Methanobacterium thermoautotrophicum. J Bacteriol. 1986 Dec;168(3):1372–1377. doi: 10.1128/jb.168.3.1372-1377.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Dimri G. P., Ames G. F., D'Ari L., Rabinowitz J. C. Physical map location of the Escherichia coli gene encoding the bifunctional enzyme 5,10-methylene-tetrahydrofolate dehydrogenase/5,10-methenyl-tetrahydrofolate cyclohydrolase. J Bacteriol. 1991 Sep;173(17):5251–5251. doi: 10.1128/jb.173.17.5251.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Donnelly M. I., Wolfe R. S. The role of formylmethanofuran: tetrahydromethanopterin formyltransferase in methanogenesis from carbon dioxide. J Biol Chem. 1986 Dec 15;261(35):16653–16659. [PubMed] [Google Scholar]
  32. Ermler U., Grabarse W., Shima S., Goubeaud M., Thauer R. K. Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science. 1997 Nov 21;278(5342):1457–1462. doi: 10.1126/science.278.5342.1457. [DOI] [PubMed] [Google Scholar]
  33. Ermler U., Merckel M., Thauer R., Shima S. Formylmethanofuran: tetrahydromethanopterin formyltransferase from Methanopyrus kandleri - new insights into salt-dependence and thermostability. Structure. 1997 May 15;5(5):635–646. doi: 10.1016/s0969-2126(97)00219-0. [DOI] [PubMed] [Google Scholar]
  34. Escalante-Semerena J. C., Leigh J. A., Rinehart K. L., Wolfe R. S. Formaldehyde activation factor, tetrahydromethanopterin, a coenzyme of methanogenesis. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1976–1980. doi: 10.1073/pnas.81.7.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Escalante-Semerena J. C., Rinehart K. L., Jr, Wolfe R. S. Tetrahydromethanopterin, a carbon carrier in methanogenesis. J Biol Chem. 1984 Aug 10;259(15):9447–9455. [PubMed] [Google Scholar]
  36. FLAKS J. G., COHEN S. S. The enzymic synthesis of 5-hydroxymethyldeoxycytidylic acid. Biochim Biophys Acta. 1957 Sep;25(3):667–668. doi: 10.1016/0006-3002(57)90553-x. [DOI] [PubMed] [Google Scholar]
  37. Ferry J. G. CO dehydrogenase. Annu Rev Microbiol. 1995;49:305–333. doi: 10.1146/annurev.mi.49.100195.001513. [DOI] [PubMed] [Google Scholar]
  38. Ferry J. G. Enzymology of the fermentation of acetate to methane by Methanosarcina thermophila. Biofactors. 1997;6(1):25–35. doi: 10.1002/biof.5520060104. [DOI] [PubMed] [Google Scholar]
  39. Fox G. E., Magrum L. J., Balch W. E., Wolfe R. S., Woese C. R. Classification of methanogenic bacteria by 16S ribosomal RNA characterization. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4537–4541. doi: 10.1073/pnas.74.10.4537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Friedmann H. C., Klein A., Thauer R. K. Structure and function of the nickel porphinoid, coenzyme F430 and of its enzyme, methyl coenzyme M reductase. FEMS Microbiol Rev. 1990 Dec;7(3-4):339–348. doi: 10.1111/j.1574-6968.1990.tb04934.x. [DOI] [PubMed] [Google Scholar]
  41. González J. C., Banerjee R. V., Huang S., Sumner J. S., Matthews R. G. Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: two solutions to the same chemical problem. Biochemistry. 1992 Jul 7;31(26):6045–6056. doi: 10.1021/bi00141a013. [DOI] [PubMed] [Google Scholar]
  42. González J. C., Peariso K., Penner-Hahn J. E., Matthews R. G. Cobalamin-independent methionine synthase from Escherichia coli: a zinc metalloenzyme. Biochemistry. 1996 Sep 24;35(38):12228–12234. doi: 10.1021/bi9615452. [DOI] [PubMed] [Google Scholar]
  43. Gorris L. G., van der Drift C. Cofactor contents of methanogenic bacteria reviewed. Biofactors. 1994 May;4(3-4):139–145. [PubMed] [Google Scholar]
  44. Green J. M., Ballou D. P., Matthews R. G. Examination of the role of methylenetetrahydrofolate reductase in incorporation of methyltetrahydrofolate into cellular metabolism. FASEB J. 1988 Jan;2(1):42–47. doi: 10.1096/fasebj.2.1.3335280. [DOI] [PubMed] [Google Scholar]
  45. Guenther B. D., Sheppard C. A., Tran P., Rozen R., Matthews R. G., Ludwig M. L. The structure and properties of methylenetetrahydrofolate reductase from Escherichia coli suggest how folate ameliorates human hyperhomocysteinemia. Nat Struct Biol. 1999 Apr;6(4):359–365. doi: 10.1038/7594. [DOI] [PubMed] [Google Scholar]
  46. Gunsalus R. P., Wolfe R. S. Stimulation of CO2 reduction to methane by methylcoenzyme M in extracts Methanobacterium. Biochem Biophys Res Commun. 1977 Jun 6;76(3):790–795. doi: 10.1016/0006-291x(77)91570-4. [DOI] [PubMed] [Google Scholar]
  47. Gärtner P., Ecker A., Fischer R., Linder D., Fuchs G., Thauer R. K. Purification and properties of N5-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanobacterium thermoautotrophicum. Eur J Biochem. 1993 Apr 1;213(1):537–545. doi: 10.1111/j.1432-1033.1993.tb17792.x. [DOI] [PubMed] [Google Scholar]
  48. HIMES R. H., RABINOWITZ J. C. Formyltetrahydrofolate synthetase. II. Characteristics of the enzyme and the enzymic reaction. J Biol Chem. 1962 Sep;237:2903–2914. [PubMed] [Google Scholar]
  49. Harms U., Thauer R. K. Identification of the active site histidine in the corrinoid protein MtrA of the energy-conserving methyltransferase complex from Methanobacterium thermoautotrophicum. Eur J Biochem. 1997 Dec 15;250(3):783–788. doi: 10.1111/j.1432-1033.1997.00783.x. [DOI] [PubMed] [Google Scholar]
  50. Harms U., Weiss D. S., Gärtner P., Linder D., Thauer R. K. The energy conserving N5-methyltetrahydromethanopterin:coenzyme M methyltransferase complex from Methanobacterium thermoautotrophicum is composed of eight different subunits. Eur J Biochem. 1995 Mar 15;228(3):640–648. doi: 10.1111/j.1432-1033.1995.0640m.x. [DOI] [PubMed] [Google Scholar]
  51. Hartmann G. C., Klein A. R., Linder M., Thauer R. K. Purification, properties and primary structure of H2-forming N5 ,N10 -methylenetetrahydromethanopterin dehydrogenase from Methanococcus thermolithotrophicus. Arch Microbiol. 1996 Mar;165(3):187–193. doi: 10.1007/BF01692860. [DOI] [PubMed] [Google Scholar]
  52. Hartzell P. L., Zvilius G., Escalante-Semerena J. C., Donnelly M. I. Coenzyme F420 dependence of the methylenetetrahydromethanopterin dehydrogenase of Methanobacterium thermoautotrophicum. Biochem Biophys Res Commun. 1985 Dec 31;133(3):884–890. doi: 10.1016/0006-291x(85)91218-5. [DOI] [PubMed] [Google Scholar]
  53. Hayasaka K., Tada K., Kikuchi G., Winter S., Nyhan W. L. Nonketotic hyperglycinemia: two patients with primary defects of P-protein and T-protein, respectively, in the glycine cleavage system. Pediatr Res. 1983 Dec;17(12):967–970. doi: 10.1203/00006450-198312000-00008. [DOI] [PubMed] [Google Scholar]
  54. Hedderich R., Berkessel A., Thauer R. K. Purification and properties of heterodisulfide reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem. 1990 Oct 5;193(1):255–261. doi: 10.1111/j.1432-1033.1990.tb19331.x. [DOI] [PubMed] [Google Scholar]
  55. Himes R. H., Harmony J. A. Formyltetrahydrofolate synthetase. CRC Crit Rev Biochem. 1973 Sep;1(4):501–535. doi: 10.3109/10409237309105441. [DOI] [PubMed] [Google Scholar]
  56. Hochheimer A., Linder D., Thauer R. K., Hedderich R. The molybdenum formylmethanofuran dehydrogenase operon and the tungsten formylmethanofuran dehydrogenase operon from Methanobacterium thermoautotrophicum. Structures and transcriptional regulation. Eur J Biochem. 1996 Nov 15;242(1):156–162. doi: 10.1111/j.1432-1033.1996.0156r.x. [DOI] [PubMed] [Google Scholar]
  57. Howell D. M., White R. H. D-erythro-neopterin biosynthesis in the methanogenic archaea Methanococcus thermophila and Methanobacterium thermoautotrophicum deltaH. J Bacteriol. 1997 Aug;179(16):5165–5170. doi: 10.1128/jb.179.16.5165-5170.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Jarrett J. T., Huang S., Matthews R. G. Methionine synthase exists in two distinct conformations that differ in reactivity toward methyltetrahydrofolate, adenosylmethionine, and flavodoxin. Biochemistry. 1998 Apr 21;37(16):5372–5382. doi: 10.1021/bi9730893. [DOI] [PubMed] [Google Scholar]
  59. Jones W. J., Nagle D. P., Jr, Whitman W. B. Methanogens and the diversity of archaebacteria. Microbiol Rev. 1987 Mar;51(1):135–177. doi: 10.1128/mr.51.1.135-177.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. KATZEN H. M., BUCHANAN J. M. ENZYMATIC SYNTHESIS OF THE METHYL GROUP OF METHIONINE. 8. REPRESSION-DEREPRESSION, PURIFICATION, AND PROPERTIES OF 5,10-METHYLENETETRAHYDROFOLATE REDUCTASE FROM ESCHERICHIA COLI. J Biol Chem. 1965 Feb;240:825–835. [PubMed] [Google Scholar]
  61. KAY L. D., OSBORN M. J., HATEFI Y., HUENNEKENS F. M. The enzymatic conversion of N5-formyl tetrahydrofolic acid (folinic acid) to N10-formyl tetrahydrofolic acid. J Biol Chem. 1960 Jan;235:195–201. [PubMed] [Google Scholar]
  62. Kallen R. G., Jencks W. P. The dissociation constants of tetrahydrofolic acid. J Biol Chem. 1966 Dec 25;241(24):5845–5850. [PubMed] [Google Scholar]
  63. Kallen R. G., Jencks W. P. The mechanism of the condensation of formaldehyde with tetrahydrofolic acid. J Biol Chem. 1966 Dec 25;241(24):5851–5863. [PubMed] [Google Scholar]
  64. Keltjens J. T., Brugman A. J., Kesseleer J. M., te Brömmelstroet B. W., van der Drift C., Vogels G. D. 5-Formyl-5,6,7,8-tetrahydromethanopterin is the intermediate in the process of methanogenesis in Methanosarcina barkeri. Biofactors. 1992 Apr;3(4):249–255. [PubMed] [Google Scholar]
  65. Keltjens J. T., Huberts M. J., Laarhoven W. H., Vogels G. D. Structural elements of methanopterin, a novel pterin present in Methanobacterium thermoautotrophicum. Eur J Biochem. 1983 Feb 15;130(3):537–544. doi: 10.1111/j.1432-1033.1983.tb07183.x. [DOI] [PubMed] [Google Scholar]
  66. Keltjens J. T., Vogels G. D. Methanopterin and methanogenic bacteria. Biofactors. 1988 Jan;1(1):95–103. [PubMed] [Google Scholar]
  67. Kersten H., Sandig L., Arnold H. H. Tetrahydrofolate-dependent 5-methyluracil-tRNA transferase activity in B. subtilis. FEBS Lett. 1975 Jul 15;55(1):57–60. doi: 10.1016/0014-5793(75)80956-2. [DOI] [PubMed] [Google Scholar]
  68. Klein A. R., Thauer R. K. Overexpression of the coenzyme-F420-dependent N5,N10-methylenetetrahydromethanopterin dehydrogenase gene from the hyperthermophilic Methanopyrus kandleri. Eur J Biochem. 1997 Apr 15;245(2):386–391. doi: 10.1111/j.1432-1033.1997.t01-1-00386.x. [DOI] [PubMed] [Google Scholar]
  69. Klein A. R., Thauer R. K. Re-face specificity at C14a of methylenetetrahydromethanopterin and Si-face specificity at C5 of coenzyme F420 for coenzyme F420-dependent methylenetetrahydromethanopterin dehydrogenase from methanogenic Archaea. Eur J Biochem. 1995 Jan 15;227(1-2):169–174. doi: 10.1111/j.1432-1033.1995.tb20373.x. [DOI] [PubMed] [Google Scholar]
  70. Klenk H. P., Clayton R. A., Tomb J. F., White O., Nelson K. E., Ketchum K. A., Dodson R. J., Gwinn M., Hickey E. K., Peterson J. D. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997 Nov 27;390(6658):364–370. doi: 10.1038/37052. [DOI] [PubMed] [Google Scholar]
  71. Krone U. E., McFarlan S. C., Hogenkamp H. P. Purification and partial characterization of a putative thymidylate synthase from Methanobacterium thermoautotrophicum. Eur J Biochem. 1994 Mar 15;220(3):789–794. doi: 10.1111/j.1432-1033.1994.tb18680.x. [DOI] [PubMed] [Google Scholar]
  72. Künkel A., Vaupel M., Heim S., Thauer R. K., Hedderich R. Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme. Eur J Biochem. 1997 Feb 15;244(1):226–234. doi: 10.1111/j.1432-1033.1997.00226.x. [DOI] [PubMed] [Google Scholar]
  73. Leigh J. A. Levels of water-soluble vitamins in methanogenic and non-methanogenic bacteria. Appl Environ Microbiol. 1983 Mar;45(3):800–803. doi: 10.1128/aem.45.3.800-803.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Ljungdahl L. G., O'Brien W. E., Moore M. R., Liu M. T. Methylenetetrahydrofolate dehydrogenase from Clostridium formicoaceticum and methylenetetrahydrofolate dehydrogenase, methenyltetrahydrofolate cyclohydrolase (combined) from Clostridium thermoaceticum. Methods Enzymol. 1980;66:599–609. doi: 10.1016/0076-6879(80)66513-6. [DOI] [PubMed] [Google Scholar]
  75. Ludwig M. L., Matthews R. G. Structure-based perspectives on B12-dependent enzymes. Annu Rev Biochem. 1997;66:269–313. doi: 10.1146/annurev.biochem.66.1.269. [DOI] [PubMed] [Google Scholar]
  76. Ma K., Linder D., Stetter K. O., Thauer R. K. Purification and properties of N5,N10-methylenetetrahydromethanopterin reductase (coenzyme F420-dependent) from the extreme thermophile Methanopyrus kandleri. Arch Microbiol. 1991;155(6):593–600. doi: 10.1007/BF00245355. [DOI] [PubMed] [Google Scholar]
  77. Ma K., Thauer R. K. Purification and properties of N5, N10-methylenetetrahydromethanopterin reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem. 1990 Jul 20;191(1):187–193. doi: 10.1111/j.1432-1033.1990.tb19109.x. [DOI] [PubMed] [Google Scholar]
  78. Marolewski A., Smith J. M., Benkovic S. J. Cloning and characterization of a new purine biosynthetic enzyme: a non-folate glycinamide ribonucleotide transformylase from E. coli. Biochemistry. 1994 Mar 8;33(9):2531–2537. doi: 10.1021/bi00175a023. [DOI] [PubMed] [Google Scholar]
  79. Morgan R. M., Pihl T. D., Nölling J., Reeve J. N. Hydrogen regulation of growth, growth yields, and methane gene transcription in Methanobacterium thermoautotrophicum deltaH. J Bacteriol. 1997 Feb;179(3):889–898. doi: 10.1128/jb.179.3.889-898.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Mukhopadhyay B., Purwantini E., Pihl T. D., Reeve J. N., Daniels L. Cloning, sequencing, and transcriptional analysis of the coenzyme F420-dependent methylene-5,6,7,8-tetrahydromethanopterin dehydrogenase gene from Methanobacterium thermoautotrophicum strain Marburg and functional expression in Escherichia coli. J Biol Chem. 1995 Feb 10;270(6):2827–2832. doi: 10.1074/jbc.270.6.2827. [DOI] [PubMed] [Google Scholar]
  81. Nar H., Huber R., Auerbach G., Fischer M., Hösl C., Ritz H., Bracher A., Meining W., Eberhardt S., Bacher A. Active site topology and reaction mechanism of GTP cyclohydrolase I. Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12120–12125. doi: 10.1073/pnas.92.26.12120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Nunn D. N., Lidstrom M. E. Phenotypic characterization of 10 methanol oxidation mutant classes in Methylobacterium sp. strain AM1. J Bacteriol. 1986 May;166(2):591–597. doi: 10.1128/jb.166.2.591-597.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Nyce G. W., White R. H. dTMP biosynthesis in Archaea. J Bacteriol. 1996 Feb;178(3):914–916. doi: 10.1128/jb.178.3.914-916.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Osterman D. G., DePillis G. D., Wu J. C., Matsuda A., Santi D. V. 5-Fluorocytosine in DNA is a mechanism-based inhibitor of HhaI methylase. Biochemistry. 1988 Jul 12;27(14):5204–5210. doi: 10.1021/bi00414a039. [DOI] [PubMed] [Google Scholar]
  85. Perry K. M., Fauman E. B., Finer-Moore J. S., Montfort W. R., Maley G. F., Maley F., Stroud R. M. Plastic adaptation toward mutations in proteins: structural comparison of thymidylate synthases. Proteins. 1990;8(4):315–333. doi: 10.1002/prot.340080406. [DOI] [PubMed] [Google Scholar]
  86. Peterson D. S., Milhous W. K., Wellems T. E. Molecular basis of differential resistance to cycloguanil and pyrimethamine in Plasmodium falciparum malaria. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3018–3022. doi: 10.1073/pnas.87.8.3018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Raemakers-Franken P. C., Bongaerts R., Fokkens R., van der Drift C., Vogels G. D. Characterization of two pterin derivatives isolated from Methanoculleus thermophilicum. Eur J Biochem. 1991 Sep 15;200(3):783–787. doi: 10.1111/j.1432-1033.1991.tb16245.x. [DOI] [PubMed] [Google Scholar]
  88. Ragsdale S. W., Ljungdahl L. G. Purification and properties of NAD-dependent 5,10-methylenetetrahydrofolate dehydrogenase from Acetobacterium woodii. J Biol Chem. 1984 Mar 25;259(6):3499–3503. [PubMed] [Google Scholar]
  89. Rasche M. E., White R. H. Mechanism for the enzymatic formation of 4-(beta-D-ribofuranosyl)aminobenzene 5'-phosphate during the biosynthesis of methanopterin. Biochemistry. 1998 Aug 11;37(32):11343–11351. doi: 10.1021/bi973086q. [DOI] [PubMed] [Google Scholar]
  90. Reeve J. N., Nölling J., Morgan R. M., Smith D. R. Methanogenesis: genes, genomes, and who's on first? J Bacteriol. 1997 Oct;179(19):5975–5986. doi: 10.1128/jb.179.19.5975-5986.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Romesser J. A., Wolfe R. S. Coupling of methyl coenzyme M reduction with carbon dioxide activation in extracts of Methanobacterium thermoautotrophicum. J Bacteriol. 1982 Nov;152(2):840–847. doi: 10.1128/jb.152.2.840-847.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Rothman S. W., Kisliuk R. L., Langerman N. Calorimetric studies of thymidylate synthesis. J Biol Chem. 1973 Nov 25;248(22):7845–7851. [PubMed] [Google Scholar]
  93. Rüdiger H., Jaenicke L. Methionine synthesis: Demonstration of the reversibility of the reaction. FEBS Lett. 1969 Aug;4(4):316–318. doi: 10.1016/0014-5793(69)80264-4. [DOI] [PubMed] [Google Scholar]
  94. SILVERMAN M., KERESZTESY J. C., KOVAL G. J., GARDINER R. C. Citrovorum factor and the synthesis of formylglutamic acid. J Biol Chem. 1957 May;226(1):83–94. [PubMed] [Google Scholar]
  95. Schirch L. V., Tatum C. M., Jr, Benkovic S. J. Serine transhydroxymethylase: evidence for a sequential random mechanism. Biochemistry. 1977 Feb 8;16(3):410–419. doi: 10.1021/bi00622a011. [DOI] [PubMed] [Google Scholar]
  96. Schleucher J., Griesinger C., Schwörer B., Thauer R. K. H2-forming N5, N10-methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum catalyzes a stereoselective hydride transfer as determined by two-dimensional NMR spectroscopy. Biochemistry. 1994 Apr 5;33(13):3986–3993. doi: 10.1021/bi00179a027. [DOI] [PubMed] [Google Scholar]
  97. Schleucher J., Schwörer B., Zirngibl C., Koch U., Weber W., Egert E., Thauer R. K., Griesinger C. Determination of the relative configuration of 5,6,7,8-tetrahydromethanopterin by two-dimensional NMR spectroscopy. FEBS Lett. 1992 Dec 21;314(3):440–444. doi: 10.1016/0014-5793(92)81522-n. [DOI] [PubMed] [Google Scholar]
  98. Schröder I., Thauer R. K. Methylcobalamin:homocysteine methyltransferase from Methanobacterium thermoautotrophicum. Identification as the metE gene product. Eur J Biochem. 1999 Aug;263(3):789–796. doi: 10.1046/j.1432-1327.1999.00559.x. [DOI] [PubMed] [Google Scholar]
  99. Schwörer B., Breitung J., Klein A. R., Stetter K. O., Thauer R. K. Formylmethanofuran: tetrahydromethanopterin formyltransferase and N5,N10-methylenetetrahydromethanopterin dehydrogenase from the sulfate-reducing Archaeoglobus fulgidus: similarities with the enzymes from methanogenic Archaea. Arch Microbiol. 1993;159(3):225–232. doi: 10.1007/BF00248476. [DOI] [PubMed] [Google Scholar]
  100. Setzke E., Hedderich R., Heiden S., Thauer R. K. H2: heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum. Composition and properties. Eur J Biochem. 1994 Feb 15;220(1):139–148. doi: 10.1111/j.1432-1033.1994.tb18608.x. [DOI] [PubMed] [Google Scholar]
  101. Shane B. Folylpolyglutamate synthesis and role in the regulation of one-carbon metabolism. Vitam Horm. 1989;45:263–335. doi: 10.1016/s0083-6729(08)60397-0. [DOI] [PubMed] [Google Scholar]
  102. Shane B., Stokstad E. L. Vitamin B12-folate interrelationships. Annu Rev Nutr. 1985;5:115–141. doi: 10.1146/annurev.nu.05.070185.000555. [DOI] [PubMed] [Google Scholar]
  103. Smith D. R., Doucette-Stamm L. A., Deloughery C., Lee H., Dubois J., Aldredge T., Bashirzadeh R., Blakely D., Cook R., Gilbert K. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol. 1997 Nov;179(22):7135–7155. doi: 10.1128/jb.179.22.7135-7155.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Teller J. H., Powers S. G., Snell E. E. Ketopantoate hydroxymethyltransferase. I. Purification and role in pantothenate biosynthesis. J Biol Chem. 1976 Jun 25;251(12):3780–3785. [PubMed] [Google Scholar]
  105. Thauer R. K. Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology. 1998 Sep;144(Pt 9):2377–2406. doi: 10.1099/00221287-144-9-2377. [DOI] [PubMed] [Google Scholar]
  106. Thauer R. K., Jungermann K., Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977 Mar;41(1):100–180. doi: 10.1128/br.41.1.100-180.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Thauer Rudolf K., Klein Andreas R., Hartmann Gudrun C. Reactions with Molecular Hydrogen in Microorganisms: Evidence for a Purely Organic Hydrogenation Catalyst. Chem Rev. 1996 Nov 7;96(7):3031–3042. doi: 10.1021/cr9500601. [DOI] [PubMed] [Google Scholar]
  108. Uyeda K., Rabinowitz J. C. Enzymes of clostridial purine fermentation. Methylenetetrahydrofolate dehydrogenase. J Biol Chem. 1967 Oct 10;242(19):4378–4385. [PubMed] [Google Scholar]
  109. Uyeda K., Rabinowitz J. C. Metabolism of formiminoglycine. Formiminotetrahydrofolate cyclodeaminase. J Biol Chem. 1967 Jan 10;242(1):24–31. [PubMed] [Google Scholar]
  110. Vanoni M. A., Matthews R. G. Kinetic isotope effects on the oxidation of reduced nicotinamide adenine dinucleotide phosphate by the flavoprotein methylenetetrahydrofolate reductase. Biochemistry. 1984 Oct 23;23(22):5272–5279. doi: 10.1021/bi00317a027. [DOI] [PubMed] [Google Scholar]
  111. Vaupel M., Dietz H., Linder D., Thauer R. K. Primary structure of cyclohydrolase (Mch) from Methanobacterium thermoautotrophicum (strain Marburg) and functional expression of the mch gene in Escherichia coli. Eur J Biochem. 1996 Feb 15;236(1):294–300. doi: 10.1111/j.1432-1033.1996.00294.x. [DOI] [PubMed] [Google Scholar]
  112. Vaupel M., Thauer R. K. Coenzyme F420-dependent N5,N10-methylenetetrahydromethanopterin reductase (Mer) from Methanobacterium thermoautotrophicum strain Marburg. Cloning, sequencing, transcriptional analysis, and functional expression in Escherichia coli of the mer gene. Eur J Biochem. 1995 Aug 1;231(3):773–778. doi: 10.1111/j.1432-1033.1995.0773d.x. [DOI] [PubMed] [Google Scholar]
  113. Vaupel M., Vorholt J. A., Thauer R. K. Overproduction and one-step purification of the N5,N10-methenyltetrahydromethanopterin cyclohydrolase (Mch) from the hyperthermophilic Methanopyrus kandleri. Extremophiles. 1998 Jan;2(1):15–22. doi: 10.1007/s007920050038. [DOI] [PubMed] [Google Scholar]
  114. Vorholt J. A., Chistoserdova L., Lidstrom M. E., Thauer R. K. The NADP-dependent methylene tetrahydromethanopterin dehydrogenase in Methylobacterium extorquens AM1. J Bacteriol. 1998 Oct;180(20):5351–5356. doi: 10.1128/jb.180.20.5351-5356.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Vorholt J. A., Chistoserdova L., Stolyar S. M., Thauer R. K., Lidstrom M. E. Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol. 1999 Sep;181(18):5750–5757. doi: 10.1128/jb.181.18.5750-5757.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Vorholt J. A., Thauer R. K. The active species of 'CO2' utilized by formylmethanofuran dehydrogenase from methanogenic Archaea. Eur J Biochem. 1997 Sep 15;248(3):919–924. doi: 10.1111/j.1432-1033.1997.00919.x. [DOI] [PubMed] [Google Scholar]
  117. Vorholt J. A., Vaupel M., Thauer R. K. A polyferredoxin with eight [4Fe-4S] clusters as a subunit of molybdenum formylmethanofuran dehydrogenase from Methanosarcina barkeri. Eur J Biochem. 1996 Feb 15;236(1):309–317. doi: 10.1111/j.1432-1033.1996.t01-1-00309.x. [DOI] [PubMed] [Google Scholar]
  118. Weiss D. S., Gärtner P., Thauer R. K. The energetics and sodium-ion dependence of N5-methyltetrahydromethanopterin:coenzyme M methyltransferase studied with cob(I)alamin as methyl acceptor and methylcob(III)alamin as methyl donor. Eur J Biochem. 1994 Dec 15;226(3):799–809. doi: 10.1111/j.1432-1033.1994.00799.x. [DOI] [PubMed] [Google Scholar]
  119. White B. N., Bayley S. T. Methionine transfer RNAs from the extreme halophile, Halobacterium cutirubrum. Biochim Biophys Acta. 1972 Jul 31;272(4):583–587. doi: 10.1016/0005-2787(72)90513-8. [DOI] [PubMed] [Google Scholar]
  120. White R. H. Biosynthesis of methanopterin. Biochemistry. 1996 Mar 19;35(11):3447–3456. doi: 10.1021/bi952308m. [DOI] [PubMed] [Google Scholar]
  121. White R. H. Distribution of folates and modified folates in extremely thermophilic bacteria. J Bacteriol. 1991 Mar;173(6):1987–1991. doi: 10.1128/jb.173.6.1987-1991.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. White R. H. Methanopterin biosynthesis: methylation of the biosynthetic intermediates. Biochim Biophys Acta. 1998 Apr 10;1380(2):257–267. doi: 10.1016/s0304-4165(97)00148-7. [DOI] [PubMed] [Google Scholar]
  123. White R. H. Purine biosynthesis in the domain Archaea without folates or modified folates. J Bacteriol. 1997 May;179(10):3374–3377. doi: 10.1128/jb.179.10.3374-3377.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. White R. H. Structures of the modified folates in the thermophilic archaebacteria Pyrococcus furiosus. Biochemistry. 1993 Jan 26;32(3):745–753. doi: 10.1021/bi00054a003. [DOI] [PubMed] [Google Scholar]
  125. Wilhelm K., Rüger W. Deoxyuridylate-hydroxymethylase of bacteriophage SPO1. Virology. 1992 Aug;189(2):640–646. doi: 10.1016/0042-6822(92)90587-f. [DOI] [PubMed] [Google Scholar]
  126. Williamson D. H., Lund P., Krebs H. A. The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J. 1967 May;103(2):514–527. doi: 10.1042/bj1030514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Wohlfarth G., Geerligs G., Diekert G. Purification and characterization of NADP(+)-dependent 5,10-methylenetetrahydrofolate dehydrogenase from Peptostreptococcus productus marburg. J Bacteriol. 1991 Feb;173(4):1414–1419. doi: 10.1128/jb.173.4.1414-1419.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Wohlfarth G., Geerligs G., Diekert G. Purification and properties of a NADH-dependent 5,10-methylenetetrahydrofolate reductase from Peptostreptococcus productus. Eur J Biochem. 1990 Sep 11;192(2):411–417. doi: 10.1111/j.1432-1033.1990.tb19242.x. [DOI] [PubMed] [Google Scholar]
  132. Wolfe R. S. My kind of biology. Annu Rev Microbiol. 1991;45:1–35. doi: 10.1146/annurev.mi.45.100191.000245. [DOI] [PubMed] [Google Scholar]
  133. Worrell V. E., Nagle D. P., Jr Folic acid and pteroylpolyglutamate contents of archaebacteria. J Bacteriol. 1988 Sep;170(9):4420–4423. doi: 10.1128/jb.170.9.4420-4423.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Wu J. C., Santi D. V. Kinetic and catalytic mechanism of HhaI methyltransferase. J Biol Chem. 1987 Apr 5;262(10):4778–4786. [PubMed] [Google Scholar]
  135. Xu H., Aurora R., Rose G. D., White R. H. Identifying two ancient enzymes in Archaea using predicted secondary structure alignment. Nat Struct Biol. 1999 Aug;6(8):750–754. doi: 10.1038/11525. [DOI] [PubMed] [Google Scholar]
  136. Yamamoto I., Saiki T., Liu S. M., Ljungdahl L. G. Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J Biol Chem. 1983 Feb 10;258(3):1826–1832. [PubMed] [Google Scholar]
  137. Zhou D., White R. H. 5-(p-aminophenyl)-1,2,3,4-tetrahydroxypentane, a structural component of the modified folate in Sulfolobus solfataricus. J Bacteriol. 1992 Jul;174(14):4576–4582. doi: 10.1128/jb.174.14.4576-4582.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. te Brömmelstroet B. W., Hensgens C. M., Keltjens J. T., van der Drift C., Vogels G. D. Purification and characterization of coenzyme F420-dependent 5,10-methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum strain delta H. Biochim Biophys Acta. 1991 Jan 23;1073(1):77–84. doi: 10.1016/0304-4165(91)90185-j. [DOI] [PubMed] [Google Scholar]
  139. te Brömmelstroet B. W., Hensgens C. M., Keltjens J. T., van der Drift C., Vogels G. D. Purification and properties of 5,10-methylenetetrahydromethanopterin reductase, a coenzyme F420-dependent enzyme, from Methanobacterium thermoautotrophicum strain delta H. J Biol Chem. 1990 Feb 5;265(4):1852–1857. [PubMed] [Google Scholar]
  140. van Beelen P., Labro J. F., Keltjens J. T., Geerts W. J., Vogels G. D., Laarhoven W. H., Guijt W., Haasnoot C. A. Derivatives of methanopterin, a coenzyme involved in methanogenesis. Eur J Biochem. 1984 Mar 1;139(2):359–365. doi: 10.1111/j.1432-1033.1984.tb08014.x. [DOI] [PubMed] [Google Scholar]
  141. van Beelen P., Stassen A. P., Bosch J. W., Vogels G. D., Guijt W., Haasnoot C. A. Elucidation of the structure of methanopterin, a coenzyme from Methanobacterium thermoautotrophicum, using two-dimensional nuclear-magnetic-resonance techniques. Eur J Biochem. 1984 Feb 1;138(3):563–571. doi: 10.1111/j.1432-1033.1984.tb07951.x. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES