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Alternating zinc fingers in the human male associated protein ZFY: 2D NMR structure of an even finger and implications for "jumping-linker" DNA recognition.

Kochoyan M, Havel TF, Nguyen DT, Dahl CE, Keutmann HT, Weiss MA
Biochemistry 30 3371-86 (1991)
Cited: 44 times
EuropePMC logo PMID: 1849423

Abstract

ZFY, a sex-related Zn-finger protein encoded by the human Y chromosome, is distinguished from the general class of Zn-finger proteins by the presence of a two-finger repeat. Whereas odd-numbered domains and linkers fit a general consensus, even-numbered domains and linkers exhibit systematic differences. Because this alternation may have fundamental implications for the mechanism of protein-DNA recognition, we have undertaken biochemical and structural studies of fragments of ZFY. We describe here the solution structure of a representative nonconsensus (even-numbered) Zn finger based on 2D NMR studies of a 30-residue peptide. Structural modeling by distance geometry and simulated annealing (DG/SA) demonstrates that this peptide folds as a miniglobular domain containing a C-terminal beta--hairpin and N-terminal alpha-helix (beta beta alpha motif). These features are similar to (but not identical with) those previously described in consensus-type Zn fingers (derived from ADR1 and Xfin); the similarities suggest that even and odd ZFY domains bind DNA by a common mechanism. A model of the protein-DNA complex (designated the "jumping-linker" model) is presented and discussed in terms of the ZFY two-finger repeat. In this model every other linker is proposed to cross the minor groove by means of a putative finger/linker submotif HX4HX3-hydrophobic residue-X3. Analogous use of a hydrophobic residue in a linker that spans the minor groove has recently been described in crystallographic and 3D NMR studies of homeodomain-DNA complexes. The proposed model of ZFY is supported in part by the hydroxyl radical footprint of the TFIIIA-DNA complex [Churchill, M.E.A., Tullius, T.D., & Klug, A. (1990) Proc. Natl. Acad. Sci. U.S.A. 87, 5528-5532].

Articles - 5znf mentioned but not cited (5)

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  2. Solvation studies of a zinc finger protein in hydrated ionic liquids. Haberler M, Schröder C, Steinhauser O. Phys Chem Chem Phys 13 6955-6969 (2011)
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  5. Letter Native, sequential protein folding via anchored N and C protein termini. Alberti S. Proc Natl Acad Sci U S A 113 E3189-91 (2016)


Reviews citing this publication (2)

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  2. Sequence-specific DNA recognition by Cys2, His2 zinc fingers. Bernstein BE, Hoffman RC, Klevit RE. Ann N Y Acad Sci 726 92-102; discussion 102-4 (1994)

Articles citing this publication (37)

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  14. Solution structure of NEMO zinc finger and impact of an anhidrotic ectodermal dysplasia with immunodeficiency-related point mutation. Cordier F, Vinolo E, Véron M, Delepierre M, Agou F. J Mol Biol 377 1419-1432 (2008)
  15. Adjacent zinc-finger motifs in multiple zinc-finger peptides from SWI5 form structurally independent, flexibly linked domains. Nakaseko Y, Neuhaus D, Klug A, Rhodes D. J Mol Biol 228 619-636 (1992)
  16. NMR structure of the single QALGGH zinc finger domain from the Arabidopsis thaliana SUPERMAN protein. Isernia C, Bucci E, Leone M, Zaccaro L, Di Lello P, Digilio G, Esposito S, Saviano M, Di Blasio B, Pedone C, Pedone PV, Fattorusso R. Chembiochem 4 171-180 (2003)
  17. Relationship between 1H and 13C NMR chemical shifts and the secondary and tertiary structure of a zinc finger peptide. Lee MS, Palmer AG, Wright PE. J Biomol NMR 2 307-322 (1992)
  18. The solution structure of the first zinc finger domain of SWI5: a novel structural extension to a common fold. Dutnall RN, Neuhaus D, Rhodes D. Structure 4 599-611 (1996)
  19. Solution structures of two CCHC zinc fingers from the FOG family protein U-shaped that mediate protein-protein interactions. Liew CK, Kowalski K, Fox AH, Newton A, Sharpe BK, Crossley M, Mackay JP. Structure 8 1157-1166 (2000)
  20. The hidden thermodynamics of a zinc finger. Lachenmann MJ, Ladbury JE, Phillips NB, Narayana N, Qian X, Weiss MA. J Mol Biol 316 969-989 (2002)
  21. Three-dimensional 1H NMR structure of the nucleocapsid protein NCp10 of Moloney murine leukemia virus. Déméné H, Jullian N, Morellet N, de Rocquigny H, Cornille F, Maigret B, Roques BP. J Biomol NMR 4 153-170 (1994)
  22. Time-resolved energy transfer measurements of donor-acceptor distance distributions and intramolecular flexibility of a CCHH zinc finger peptide. Eis PS, Lakowicz JR. Biochemistry 32 7981-7993 (1993)
  23. A new approach to the analysis of DNase I footprinting data and its application to the TFIIIA/5S DNA complex. Fairall L, Rhodes D. Nucleic Acids Res 20 4727-4731 (1992)
  24. Structure and dynamics of des-pentapeptide-insulin in solution: the molten-globule hypothesis. Hua QX, Kochoyan M, Weiss MA. Proc Natl Acad Sci U S A 89 2379-2383 (1992)
  25. Design, synthesis and structure of a zinc finger with an artificial beta-turn. Viles JH, Patel SU, Mitchell JB, Moody CM, Justice DE, Uppenbrink J, Doyle PM, Harris CJ, Sadler PJ, Thornton JM. J Mol Biol 279 973-986 (1998)
  26. Molecular biology of vertebrate transcription factor IIIA: cloning and characterization of TFIIIA from channel catfish oocytes. Ogilvie MK, Hanas JS. Gene 203 103-112 (1997)
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  28. The study of the conformation and interaction of two tachykinin peptides in membrane mimicking systems by NMR spectroscopy and pulsed field gradient diffusion. Gao X, Wong TC. Biopolymers 50 555-568 (1999)
  29. Replacement of His23 by Cys in a zinc finger of HIV-1 NCp7 led to a change in 1H NMR-derived 3D structure and to a loss of biological activity. Julian N, Demene H, Morellet N, Maigret B, Roques BP. FEBS Lett 331 43-48 (1993)
  30. Architectural rules of the zinc-finger motif: comparative two-dimensional NMR studies of native and "aromatic-swap" domains define a "weakly polar switch". Kochoyan M, Keutmann HT, Weiss MA. Proc Natl Acad Sci U S A 88 8455-8459 (1991)
  31. Aromatic-aromatic interactions in the zinc finger motif. Analysis of the two-dimensional nuclear magnetic resonance structure of a mutant domain. Jasanoff A, Kochoyan M, Fraenkel E, Lee JP, Weiss MA. J Mol Biol 225 1035-1047 (1992)
  32. Isolation and characterization of a small putative zinc finger protein from cuttlefish epididymal sperm cells. Martin-Ponthieu A, Wouters-Tyrou D, Pudlo B, Buisine E, Sautière P. Eur J Biochem 220 463-468 (1994)
  33. Structures of DNA-binding mutant zinc finger domains: implications for DNA binding. Hoffman RC, Horvath SJ, Klevit RE. Protein Sci 2 951-965 (1993)
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  35. 1H, 15N and 13C resonance assignments for the first three zinc fingers of transcription factor IIIA. Liao X, Clemens K, Cavanagh J, Tennant L, Wright PE. J Biomol NMR 4 433-454 (1994)
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Related citations provided by authors (2)

  1. Alternating zinc fingers in the human male associated protein ZFY: refinement of the NMR structure of an even finger by selective deuterium labeling and implications for DNA recognition.. Kochoyan M, Keutmann HT, Weiss MA Biochemistry 30 7063-72 (1991)
  2. Architectural Rules of the Zinc-Finger Motif: Comparative Two-Dimensional NMR Studies of Native and "Aromatic-Swap" Domains Define a "Weakly Polar Switch". Kochoyan M, Keutmann HT, Weiss MA Proc. Natl. Acad. Sci. U.S.A. 88 8455- (1991)

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