Journal of Microbiology and Biotechnology

  • 제26권12호
  • /
  • Pages.2019-2029
  • /
  • 2016
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Structural Analyses of Zinc Finger Domains for Specific Interactions with DNA

  • Eom, Ki Seong (Department of Neurosurgery, School of Medicine and Hospital, Wonkwang University) ;
  • Cheong, Jin Sung (Department of Neurology, School of Medicine and Hospital, Wonkwang University) ;
  • Lee, Seung Jae (Department of Chemistry and Research Institute of Physic and Chemistry, Chonbuk National University)
  • 투고 : 2016.09.19
  • 심사 : 2016.09.28
  • 발행 : 2016.12.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Zinc finger proteins are among the most extensively applied metalloproteins in the field of biotechnology owing to their unique structural and functional aspects as transcriptional and translational regulators. The classical zinc fingers are the largest family of zinc proteins and they provide critical roles in physiological systems from prokaryotes to eukaryotes. Two cysteine and two histidine residues ($Cys_2His_2$) coordinate to the zinc ion for the structural functions to generate a ${\beta}{\beta}{\alpha}$ fold, and this secondary structure supports specific interactions with their binding partners, including DNA, RNA, lipids, proteins, and small molecules. In this account, the structural similarity and differences of well-known $Cys_2His_2$-type zinc fingers such as zinc interaction factor 268 (ZIF268), transcription factor IIIA (TFIIIA), GAGA, and Ros will be explained. These proteins perform their specific roles in species from archaea to eukaryotes and they show significant structural similarity; however, their aligned amino acids present low sequence homology. These zinc finger proteins have different numbers of domains for their structural roles to maintain biological progress through transcriptional regulations from exogenous stresses. The superimposed structures of these finger domains provide interesting details when these fingers are applied to specific gene binding and editing. The structural information in this study will aid in the selection of unique types of zinc finger applications in vivo and in vitro approaches, because biophysical backgrounds including complex structures and binding affinities aid in the protein design area.

키워드

참고문헌

  1. Archdeacon J, Bouhouche N, O'Connell F, Kado CI. 2000. A single amino acid substitution beyond the C2H2-zinc finger in Ros derepresses virulence and T-DNA genes in Agrobacterium tumefaciens. FEMS Microbiol. Lett. 187: 175-178. https://doi.org/10.1111/j.1574-6968.2000.tb09156.x
  2. Bai CY, Tolias PP. 1998. Drosophila clipper/CPSF 30K is a post-transcriptionally regulated nuclear protein that binds RNA containing GC clusters. Nucleic Acids Res. 26: 1597-1604. https://doi.org/10.1093/nar/26.7.1597
  3. Beckmann AM, Davidson MS, Goodenough S, Wilce PA. 1997. Differential expression of Egr-1-like DNA-binding activities in the naive rat brain and after excitatory stimulation. J. Neurochem. 69: 2227-2237.
  4. Beckmann AM, Wilce PA. 1997. Egr transcription factors in the nervous system. Neurochem. Int. 31: 477-510. https://doi.org/10.1016/S0197-0186(96)00136-2
  5. Beerli RR, Barbas CF. 2002. Engineering polydactyl zincfinger transcription factors. Nat. Biotechnol. 20: 135-141. https://doi.org/10.1038/nbt0202-135
  6. Berg JM. 1986. Potential metal-binding domains in nucleic acid binding proteins. Science 232: 485-487. https://doi.org/10.1126/science.2421409
  7. Berg JM. 1988. Proposed structure for the zinc-binding domains from transcription factor IIIA and related proteins. Proc. Natl. Acad. Sci. USA 85: 99-102. https://doi.org/10.1073/pnas.85.1.99
  8. Berg JM. 1989. Zinc fingers: the role of zinc(II) in transcription factor IIIA and related proteins. Met. Ions Biol. Syst. 25: 235-254.
  9. Berg JM. 1990. Zinc finger domains: hypotheses and current knowledge. Annu. Rev. Biophys. Biophys. Chem. 19: 405-421. https://doi.org/10.1146/annurev.bb.19.060190.002201
  10. Berg JM. 1990. Zinc fingers and other metal-binding domains. Elements for interactions between macromolecules. J. Biol. Chem. 265: 6513-6516.
  11. Berg JM, Godwin HA. 1997. Lessons from zinc-binding peptides. Annu. Rev. Biophys. Biomol. Struct. 26: 357-371. https://doi.org/10.1146/annurev.biophys.26.1.357
  12. Berg JM, Merkle DL. 1989. On the metal ion specificity of zinc finger proteins. J. Am. Chem. Soc. 111: 3759-3761. https://doi.org/10.1021/ja00192a050
  13. Berg JM, Shi YG. 1996. The galvanization of biology: a growing appreciation for the roles of zinc. Science 271: 1081- 1085. https://doi.org/10.1126/science.271.5252.1081
  14. Bouhouche N, Syvanen M, Kado CI. 2000. A mitochondrial origin for eukaryotic C2H2 zinc finger regulators? Trends Microbiol. 8: 449-450. https://doi.org/10.1016/S0966-842X(00)01851-5
  15. Bozon B, Davis S, Laroche S. 2003. A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40: 695-701. https://doi.org/10.1016/S0896-6273(03)00674-3
  16. Chen PR, He C. 2008. Selective recognition of metal ions by metalloregulatory proteins. Curr. Opin. Chem. Biol. 12: 214-221. https://doi.org/10.1016/j.cbpa.2007.12.010
  17. Chiou SJ, Riordan CG, Rheingold AL. 2003. Synthetic modeling of zinc thiolates: quantitative assessment of hydrogen bonding in modulating sulfur alkylation rates. Proc. Natl. Acad. Sci. USA 100: 3695-3700. https://doi.org/10.1073/pnas.0637221100
  18. Clemens KR, Zhang PH, Liao XB, Mcbryant SJ, Wright PE, Gottesfeld JM. 1994. Relative contributions of the zinc fingers of transcription factor IIIA to the energetics of DNA binding. J. Mol. Biol. 244: 23-35. https://doi.org/10.1006/jmbi.1994.1701
  19. Cox EH, McLendon GL. 2000. Zinc-dependent protein folding. Curr. Opin. Chem. Biol. 4: 162-165. https://doi.org/10.1016/S1367-5931(99)00070-8
  20. Davis D, Stokoe D. 2010. Zinc finger nucleases as tools to understand and treat human diseases. BMC Medicine. 8: 42. https://doi.org/10.1186/1741-7015-8-42
  21. Davis S, Bozon B, Laroche S. 2003. How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav. Brain Res. 142: 17-30. https://doi.org/10.1016/S0166-4328(02)00421-7
  22. Del Rio S, Menezes SR, Setzer DR. 1993. The function of individual zinc fingers in sequence-specific DNA recognition by transcription factor IIIA. J. Mol. Biol. 233: 567-579. https://doi.org/10.1006/jmbi.1993.1536
  23. Dyson HJ, Wright PE. 2002. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12: 54-60. https://doi.org/10.1016/S0959-440X(02)00289-0
  24. Dyson HJ, Wright PE. 2004. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104: 3607-3622. https://doi.org/10.1021/cr030403s
  25. Elrod-Erickson M, Rould MA, Nekludova L, Pabo CO. 1996. Zif268 protein-DNA complex refined at 1.6 angstrom: a model system for understanding zinc finger-DNA interactions. Structure 4: 1171-1180. https://doi.org/10.1016/S0969-2126(96)00125-6
  26. Foster MP, Wuttke DS, Radhakrishnan I, Case DA, Gottesfeld JM, Wright PE. 1997. Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIIIA. Nat. Struct. Biol. 4: 605-608. https://doi.org/10.1038/nsb0897-605
  27. Gaj T, Gersbach CA, Barbas CF. 2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31: 397-405. https://doi.org/10.1016/j.tibtech.2013.04.004
  28. Green LM, Berg JM. 1989. A retroviral Cys-$X_aa2$-Cys-$X_aa4$-His- $X_aa4$-Cys peptide binds metal ions: spectroscopic studies and a proposed 3-dimensional structure. Proc. Natl. Acad. Sci. USA 86: 4047-4051. https://doi.org/10.1073/pnas.86.11.4047
  29. Guerra AJ, Giedroc DP. 2012. Metal site occupancy and allosteric switching in bacterial metal sensor proteins. Arch. Biochem. Biophys. 519: 210-222. https://doi.org/10.1016/j.abb.2011.11.021
  30. Hanas JS, Hazuda DJ, Bogenhagen DF, Wu FYH, Wu CW. 1983. Xenopus transcription factor A requires zinc for binding to the 5S RNA gene. J. Biol. Chem. 258: 4120-4125.
  31. He C, Hus JC, Sun LJ, Zhou P, Norman DPG, Dotsch V, et al. 2005. A methylation-dependent electrostatic switch controls DNA repair and transcriptional activation by E. coli Ada. Mol. Cell 20: 117-129. https://doi.org/10.1016/j.molcel.2005.08.013
  32. Jantz D, Amann BT, Gatto GJ, Berg JM. 2004. The design of functional DNA-binding proteins based on zinc finger domains. Chem. Rev. 104: 789-799. https://doi.org/10.1021/cr020603o
  33. Klug A. 2010. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79: 213-231. https://doi.org/10.1146/annurev-biochem-010909-095056
  34. Klug A. 2010. The discovery of zinc fingers and their development for practical applications in gene regulation and genome manipulation. Q. Rev. Biophys. 43: 1-21. https://doi.org/10.1017/S0033583510000089
  35. Knapska E, Kaczmarek L. 2004. A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/ Krox-24/TIS8/ZENK? Prog. Neurobiol. 74: 183-211. https://doi.org/10.1016/j.pneurobio.2004.05.007
  36. Kothinti R, Blodgett A, Tabatabai NM, Petering DH. 2010. Zinc finger transcription factor $Zn_3$-SP1 reactions with $Cd^2+$ Chem. Res. Toxicol. 23: 405-412. https://doi.org/10.1021/tx900370u
  37. Krepkiy D, Forsterling FH, Petering DH. 2004. Interaction of $Cd^2+$ with Zn finger 3 of transcription factor IIIA: structures and binding to cognate DNA. Chem. Res. Toxicol. 17: 863-870. https://doi.org/10.1021/tx030057+
  38. Krizek BA, Merkle DL, Berg JM. 1993. Ligand variation and metal ion binding specificity in zinc finger peptides. Inorg. Chem. 32: 937-940. https://doi.org/10.1021/ic00058a030
  39. Kroncke KD, Klotz LO. 2009. Zinc fingers as biologic redox switches? Antioxid. Redox Signal. 11: 1015-1027. https://doi.org/10.1089/ars.2008.2269
  40. Lachenmann MJ, Ladbury JE, Dong J, Huang K, Carey P, Weiss MA. 2004. Why zinc fingers prefer zinc: ligand-field symmetry and the hidden thermodynamics of metal ion selectivity. Biochemistry 43: 13910-13925. https://doi.org/10.1021/bi0491999
  41. Lai ZH, Freedman DA, Levine AJ, McLendon GL. 1998. Metal and RNA binding properties of the hdm2 RING finger domain. Biochemistry 37: 17005-17015. https://doi.org/10.1021/bi980596r
  42. Layat E, Probst AV, Tourmente S. 2013. Structure, function and regulation of transcription factor IIIA: from Xenopus to Arabidopsis. Biochim. Biophys. Acta 1829: 274-282. https://doi.org/10.1016/j.bbagrm.2012.10.013
  43. Lee SJ, Michel SL. 2014. Structural metal sites in nonclassical zinc finger proteins involved in transcriptional and translational regulation. Acc. Chem. Res. 47: 2643-2650. https://doi.org/10.1021/ar500182d
  44. Lee SJ, Michel SLJ. 2010. Cysteine oxidation enhanced by iron in tristetraprolin, a zinc finger peptide. Inorg. Chem. 49: 1211-1219. https://doi.org/10.1021/ic9024298
  45. Lee YM, Lim C. 2008. Physical basis of structural and catalytic Zn-binding sites in proteins. J. Mol. Biol. 379: 545-553. https://doi.org/10.1016/j.jmb.2008.04.004
  46. Li WF, Zhang J, Wang J, Wang W. 2008. Metal-coupled folding of Cys2His2 zinc-finger. J. Am. Chem. Soc. 130: 892-900. https://doi.org/10.1021/ja075302g
  47. Malgieri G, Russo L, Esposito S, Baglivo I, Zaccaro L, Peclone EM, et al. 2007. The prokaryotic $Cys_2$$His_2$ zinc-finger adopts a novel fold as revealed by the NMR structure of Agrobacterium tumefaciens Ros DNA-binding domain. Proc. Natl. Acad. Sci. USA 104: 17341-17346. https://doi.org/10.1073/pnas.0706659104
  48. Mandell JG, Barbas CF. 2006. Zinc finger tools: custom DNA-binding domains for transcription factors and nucleases. Nucleic Acids Res. 34: W516-W523. https://doi.org/10.1093/nar/gkl209
  49. Maret W, Li Y. 2009. Coordination dynamics of zinc in proteins. Chem. Rev. 109: 4682-4707. https://doi.org/10.1021/cr800556u
  50. Maret W, Vallee BL. 1993. Cobalt as probe and label of proteins. Methods Enzymol. 226: 52-71.
  51. Matthews JM, Sunde M. 2002. Zinc fingers - folds for many occasions. IUBMB Life 54: 351-355. https://doi.org/10.1080/15216540216035
  52. Maynard AT, Covell DG. 2001. Reactivity of zinc finger cores: analysis of protein packing and electrostatic screening. J. Am. Chem. Soc. 123: 1047-1058. https://doi.org/10.1021/ja0011616
  53. McCall M, Brown T, Hunter WN, Kennard O. 1986. The crystal structure of D(GGATGGGAG) forms an essential part of the binding site for transcription factor IIIa. Nature 322: 661-664. https://doi.org/10.1038/322661a0
  54. Michalek JL, Besold AN, Michel SLJ. 2011. Cysteine and histidine shuffling: mixing and matching cysteine and histidine residues in zinc finger proteins to afford different folds and function. Dalton Trans. 40: 12619-12632. https://doi.org/10.1039/c1dt11071c
  55. Michalek JL, Lee SJ, Michel SLJ. 2012. Cadmium coordination to the zinc binding domains of the non-classical zinc finger protein tristetraprolin affects RNA binding selectivity. J. Inorg. Biochem. 112: 32-38. https://doi.org/10.1016/j.jinorgbio.2012.02.023
  56. Miller J, Mclachlan AD, Klug A. 1985. Repetitive zinc binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 4: 1609-1614.
  57. Nanami M, Ookawara T, Otaki Y, Ito K, Moriguchi R, Miyagawa K, et al. 2005. Tumor necrosis factor-${\alpha}$-induced iron sequestration and oxidative stress in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 25: 2495-2501. https://doi.org/10.1161/01.ATV.0000190610.63878.20
  58. Nolte RT, Conlin RM, Harrison SC, Brown RS. 1998. Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex. Proc. Natl. Acad. Sci. USA 95: 2938-2943. https://doi.org/10.1073/pnas.95.6.2938
  59. Omichinski JG, Pedone PV, Felsenfeld G, Gronenborn AM, Clore GM. 1997. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat. Struct. Biol. 4: 122-132. https://doi.org/10.1038/nsb0297-122
  60. Pabo CO, Sauer RT. 1992. Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem. 61: 1053-1095. https://doi.org/10.1146/annurev.bi.61.070192.005201
  61. Parkin G. 2004. Synthetic analogues relevant to the structure and function of zinc enzymes. Chem. Rev. 104: 699-767. https://doi.org/10.1021/cr0206263
  62. Pavletich NP, Pabo CO. 1991. Zinc finger DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 ${\AA}$. Science 252: 809-817. https://doi.org/10.1126/science.2028256
  63. Payne JC, Rous BW, Tenderholt AL, Godwin HA. 2003. Spectroscopic determination of the binding affinity of zinc to the DNA-binding domains of nuclear hormone receptors. Biochemistry 42: 14214-14224. https://doi.org/10.1021/bi035002l
  64. Pedone PV, Ghirlando R, Clore GM, Gronenborn AM, Felsenfeld G, Omichinski JG. 1996. The single $Cys_2$-$His_2$ zinc finger domain of the GAGA protein flanked by basic residues is sufficient for high-affinity specific DNA binding. Proc. Natl. Acad. Sci. USA 93: 2822-2826. https://doi.org/10.1073/pnas.93.7.2822
  65. Pedone PV, Omichinski JG, Nony P, Trainor C, Gronenborn AM, Clore GM, Felsenfeld G. 1997. The N-terminal fingers of chicken GATA-2 and GATA-3 are independent sequencespecific DNA binding domains. EMBO J. 16: 2874-2882. https://doi.org/10.1093/emboj/16.10.2874
  66. Penner-Hahn J. 2007. Zinc-promited alkyl transfer: a new role for zinc. Curr. Opin. Chem. Biol. 11: 166-171. https://doi.org/10.1016/j.cbpa.2007.02.038
  67. Petersohn D, Thiel G. 1996. Role of zinc-finger proteins Sp1 and Zif268/egr-1 in transcriptional regulation of the human synaptobrevin II gene. Eur. J. Biochem. 239: 827-834. https://doi.org/10.1111/j.1432-1033.1996.0827u.x
  68. Quintal SM, dePaula QA, Farrell NP. 2011. Zinc finger proteins as templates for metal ion exchange and ligand reactivity. Chemical and biological consequences. Metallomics 3: 121-139.
  69. Roehm PC, B erg JM. 1997. Sequential metal b inding b y the RING finger domain of BRCA1. Biochemistry. 36: 10240-10245. https://doi.org/10.1021/bi970863d
  70. Ryan RF, Darby MK. 1998. The role of zinc finger linkers in p43 and TFIIIA binding to 5S rRNA and DNA. Nucleic Acids Res. 26: 703-709. https://doi.org/10.1093/nar/26.3.703
  71. Shastry BS. 1996. Transcription factor IIIA (TFIIIA) in the second decade. J. Cell Sci. 109: 535-539.
  72. Summers MF. 1988. 113Cd NMR spectroscopy of coordination compounds and proteins. Coord. Chem. Rev. 86: 43-134. https://doi.org/10.1016/0010-8545(88)85012-4
  73. Takeuchi T, Bottcher A, Quezada CM, Meade TJ, Gray HB. 1999. Inhibition of thermolysin and human ${\alpha}$-thrombin by cobalt(III) Schiff base complexes. Bioorg. Med. Chem. 7: 815-819. https://doi.org/10.1016/S0968-0896(98)00272-7
  74. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. 2010. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11: 636-646. https://doi.org/10.1038/nrg2842
  75. Veyrac A, Besnard A, Caboche J, Davis S, Laroche S. 2014. The transcription factor Zif268/Egr1, brain plasticity, and memory. Prog. Mol. Biol. Transl. Sci. 122: 89-129.
  76. Wolfe SA, Nekludova L, Pabo CO. 2000. DNA recognition by $Cys_2$$His_2$ zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29: 183-212. https://doi.org/10.1146/annurev.biophys.29.1.183
  77. Wuttke DS, Foster MP, Case DA, Gottesfeld JM, Wright PE. 1997. Solution structure of the first three zinc fingers of TFIIIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity. J. Mol. Biol. 273: 183-206. https://doi.org/10.1006/jmbi.1997.1291
  78. Zandarashvili L, White MA, Esadze A, Iwahara J. 2015. Structural impact of complete CpG methylation within target DNA on specific complex formation of the inducible transcription factor Egr-1. FEBS Lett. 589: 1748-1753. https://doi.org/10.1016/j.febslet.2015.05.022

피인용 문헌

  1. Viral-mediated overexpression of the Myelin Transcription Factor 1 (MyT1) in the dentate gyrus attenuates anxiety- and ethanol-related behaviors in rats vol.234, pp.12, 2016, https://doi.org/10.1007/s00213-017-4588-7
  2. Zinc-finger proteins in health and disease vol.3, pp.None, 2017, https://doi.org/10.1038/cddiscovery.2017.71
  3. Transcriptome using Illumina sequencing reveals the traits of spermatogenesis and developing testes in Eriocheir sinensis vol.12, pp.2, 2017, https://doi.org/10.1371/journal.pone.0172478
  4. ZNF545 suppresses human hepatocellular carcinoma growth by inhibiting NF-kB signaling vol.8, pp.3, 2017, https://doi.org/10.18632/genesandcancer.137
  5. An emerging link between LIM domain proteins and nuclear receptors vol.75, pp.11, 2016, https://doi.org/10.1007/s00018-018-2774-3
  6. Expression, purification and DNA-binding properties of zinc finger domains of DOF proteins from Arabidopsis thaliana vol.8, pp.3, 2018, https://doi.org/10.15171/bi.2018.19
  7. Early-Life Exposure to Cadmium Triggers Distinct Zn-Dependent Protein Expression Patterns and Impairs Brain Development vol.184, pp.2, 2016, https://doi.org/10.1007/s12011-017-1201-1
  8. Large‐Scale Analysis of Redox‐Sensitive Conditionally Disordered Protein Regions Reveals Their Widespread Nature and Key Roles in High‐Level Eukaryotic Processes vol.19, pp.6, 2016, https://doi.org/10.1002/pmic.201800070
  9. Several One-Domain Zinc Finger µ-Proteins of Haloferax Volcanii Are Important for Stress Adaptation, Biofilm Formation, and Swarming vol.10, pp.5, 2019, https://doi.org/10.3390/genes10050361
  10. Zinc finger protein 593 is upregulated during skeletal muscle atrophy and modulates muscle cell differentiation vol.383, pp.2, 2019, https://doi.org/10.1016/j.yexcr.2019.111563
  11. Genome wide survey, evolution and expression analysis of PHD finger genes reveal their diverse roles during the development and abiotic stress responses in Brassica rapa L. vol.20, pp.1, 2016, https://doi.org/10.1186/s12864-019-6080-8
  12. Analysis of the role of the Hippo pathway in cancer vol.17, pp.None, 2016, https://doi.org/10.1186/s12967-019-1869-4
  13. Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming vol.11, pp.1, 2020, https://doi.org/10.1038/s41467-020-19624-w
  14. Crystal structures of REF6 and its complex with DNA reveal diverse recognition mechanisms vol.6, pp.None, 2020, https://doi.org/10.1038/s41421-020-0150-6
  15. The NFκB Antagonist CDGSH Iron-Sulfur Domain 2 Is a Promising Target for the Treatment of Neurodegenerative Diseases vol.22, pp.2, 2016, https://doi.org/10.3390/ijms22020934
  16. ZNF213 Facilitates ER Alpha Signaling in Breast Cancer Cells vol.11, pp.None, 2016, https://doi.org/10.3389/fonc.2021.638751
  17. Biological functions, genetic and biochemical characterization, and NMR structure determination of the small zinc finger protein HVO_2753 from Haloferax volcanii vol.288, pp.6, 2016, https://doi.org/10.1111/febs.15559
  18. Screening and Identification of Key Biomarkers in Melanoma: Evidence from Bioinformatic Analyses vol.28, pp.3, 2016, https://doi.org/10.1089/cmb.2019.0400
  19. Cysteine residues in the fourth zinc finger are important for activation of the nitric oxide‐inducible transcription factor Fzf1 in the yeast Saccharomyces cerevisiae vol.26, pp.10, 2016, https://doi.org/10.1111/gtc.12885
  20. p66α Suppresses Breast Cancer Cell Growth and Migration by Acting as Co-Activator of p53 vol.10, pp.12, 2021, https://doi.org/10.3390/cells10123593