Evidence for direct binding between hetr from anabaena sp. PCC 7120 and pats-5

Biochemistry

Volumn 50, Issue 43, 2011, Pages 9212-9224

  Feldmann, Erik A ^a   Ni, Shuisong ^a   Sahu, Indra D ^a   Mishler, Clay H ^a   Risser, Douglas D ^b   Murakami, Jodi L ^b   Tom, Sasa K ^b   McCarrick, Robert M ^a   Lorigan, Gary A ^a   Tolbert, Blanton S ^a   Callahan, Sean M ^b   Kennedy, Michael A ^a  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC EFFECT; ANABAENA SP. PCC 7120; AUTOREGULATIONS; BASE PAIRS; CONSTRAINED MOTION; CYANOBACTERIUM ANABAENA; CYSTEINE-SCANNING MUTAGENESIS; DOUBLE ELECTRON-ELECTRON RESONANCE; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; EXPERIMENTAL EVIDENCE; GEL SHIFT ASSAYS; HETEROCYSTS; ISOTHERMAL TITRATION CALORIMETRY; MASTER REGULATORS; REDUCED SENSITIVITY; REMOTE SITES; SPIN LABEL MOTION; TERTIARY STRUCTURES;

AMINO ACIDS; ELECTRON RESONANCE; EXPERIMENTS; PARAMAGNETIC RESONANCE; PARAMAGNETISM; STOICHIOMETRY; TITRATION;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

CYSTEINE; DIMER; PENTAPEPTIDE; PROTEIN HETR; PROTEIN PATS 5; REGULATOR PROTEIN; REPETITIVE DNA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANABAENA; ARTICLE; BACTERIAL STRAIN; BASE PAIRING; BINDING ASSAY; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA SEQUENCE; ELECTRON SPIN RESONANCE; ISOTHERMAL TITRATION CALORIMETRY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SPIN LABELING; STOICHIOMETRY;

AMINO ACID SUBSTITUTION; ANABAENA; BACTERIAL PROTEINS; DNA, BACTERIAL; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; THERMODYNAMICS;

ANABAENA SP.; NOSTOC SP. PCC 7120;

EID: 80054998162     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201226e     Document Type: Article

References (79)

1. Fritsch, F. (1904) Studies on cyanophyceae New Phytol. 3, 85-96
2. Fogg, G. (1944) Growth and heterocyst production in Anabaena cylindrica Lemm New Phytol. 43, 164-175
3. Fogg, G. (1949) Growth and heterocyst production in Anabaena Cylindrica Lemm. II In relation to carbon and nitrogen metabolism Ann. Bot. 13, 241-259
4. Haselkorn, R. (1978) Heterocysts Ann. Rev. Plant Physiol. Plant Mol. Biol. 319-344
5. Adams, D. G. and Carr, N. G. (1981) The developmental biology of heterocyst and akinete formation in cyanobacteria Crit. Rev. Microbiol. 9, 45-100
6. Wolk, C. P. (1996) Heterocyst formation Annu. Rev. Genet. 30, 59-78 (Pubitemid 27014463)
7. Adams, D. G. (2000) Heterocyst formation in cyanobacteria Curr. Opin. Microbiol. 3, 618-624
8. Meeks, J. C. and Elhai, J. (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol. Mol. Biol. Rev. 66, 94-121; table of contents. (Pubitemid 34213970)
9. Golden, J. W. and Yoon, H. S. (2003) Heterocyst development in Anabaena Curr. Opin. Microbiol. 6, 557-563 (Pubitemid 38020051)
10. El-Shehawy, R. and Kleiner, D. (2003) The mystique of irreversibility in cyanobacterial heterocyst formation: parallels to differentiation and senescence in eukaryotic cells Physiol. Plant. 49-55 (Pubitemid 37110602)
11. Zhang, C. C., Laurent, S., Sakr, S., Peng, L., and Bèdu, S. (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals Mol. Microbiol. 59, 367-375
12. Kumar, K., Mella-Herrera, R. A., and Golden, J. W. (2010) Cyanobacterial heterocysts Cold Spring Harbor Perspect. Biol. 2, a000315
13. Brocks, J. J., Logan, G. A., Buick, R., and Summons, R. E. (1999) Archean molecular fossils and the early rise of eukaryotes Science 285, 1033-1036
14. Tomitani, A., Knoll, A. H., Cavanaugh, C. M., and Ohno, T. (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives Proc. Natl. Acad. Sci. U.S.A. 103, 5442-5447
15. Fay, P. (1992) Oxygen relations of nitrogen fixation in cyanobacteria Microbiol. Rev. 56, 340-373
16. Gallon, J. (1992) Reconciling the incompatible: N2 fixation and O2 New Phytol. 122, 571-609
17. Haselkorn, R. (2008) Cell-cell communication in filamentous cyanobacteria Mol. Microbiol. 70, 783-785
18. Fritsch, F. (1951) The heterocyst: a botanical enigma Proc. Linn. Soc. London 162, 194-211
19. Wolk, C. P. and Quine, M. P. (1975) Formation of one-dimensional patterns by stochastic processes and by filamentous blue-green algae Dev. Biol. 46, 370-382
20. Lambein, F. and Wolk, C. P. (1973) Structural studies on the glycolipids from the envelope of the heterocyst of Anabaena cylindrica Biochemistry 12, 791-798
21. Khudyakov, I. and Wolk, C. P. (1997) hetC, a gene coding for a protein similar to bacterial ABC protein exporters, is involved in early regulation of heterocyst differentiation in Anabaena sp. strain PCC 7120 J. Bacteriol. 179, 6971-6978 (Pubitemid 27492480)
22. Nicolaisen, K., Hahn, A., and Schleiff, E. (2009) The cell wall in heterocyst formation by Anabaena sp. PCC 7120 J. Basic Microbiol. 49, 5-24
23. Buikema, W. J. and Haselkorn, R. (1991) Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120 Genes Dev. 5, 321-330 (Pubitemid 21905956)
24. Black, T. A., Cai, Y., and Wolk, C. P. (1993) Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena Mol. Microbiol. 9, 77-84 (Pubitemid 23217739)
25. Yoon, H. S. and Golden, J. W. (1998) Heterocyst pattern formation controlled by a diffusible peptide Science 282, 935-938 (Pubitemid 28507524)
26. Callahan, S. M. and Buikema, W. J. (2001) The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120 Mol. Microbiol. 40, 941-950 (Pubitemid 32523191)
27. Zhang, J. Y., Chen, W. L., and Zhang, C. C. (2009) hetR and patS, two genes necessary for heterocyst pattern formation, are widespread in filamentous nonheterocyst-forming cyanobacteria Microbiology 155, 1418-1426
28. Risser, D. D. and Callahan, S. M. (2009) Genetic and cytological evidence that heterocyst patterning is regulated by inhibitor gradients that promote activator decay Proc. Natl. Acad. Sci. U.S.A. 106, 19884-19888
29. Huang, X., Dong, Y., and Zhao, J. (2004) HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS Proc. Natl. Acad. Sci. U.S.A. 101, 4848-4853 (Pubitemid 38469166)
30. Zhou, R., Wei, X., Jiang, N., Li, H., Dong, Y., Hsi, K. L., and Zhao, J. (1998) Evidence that HetR protein is an unusual serine-type protease Proc. Natl. Acad. Sci. U.S.A. 95, 4959-4963 (Pubitemid 28208532)
31. Zhou, R., Cao, Z., and Zhao, J. (1998) Characterization of HetR protein turnover in Anabaena sp. PCC 7120 Arch. Microbiol. 169, 417-423 (Pubitemid 28204284)
32. Dong, Y, Huang, X, Wu, X. Y., and Zhao, J. (2000) Identification of the active site of HetR protease and its requirement for heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120 J. Bacteriol. 182, 1575-9 (Pubitemid 30121121)
33. Risser, D. D. and Callahan, S. M. (2007) Mutagenesis of hetR reveals amino acids necessary for HetR function in the heterocystous cyanobacterium Anabaena sp. strain PCC 7120 J. Bacteriol. 189, 2460-2467 (Pubitemid 46411360)
34. Wu, X., Liu, D., Lee, M. H., and Golden, J. W. (2004) patS minigenes inhibit heterocyst development of Anabaena sp. strain PCC 7120 J. Bacteriol. 186, 6422-6429 (Pubitemid 39258123)
35. Khudyakov, I. Y. and Golden, J. W. (2004) Different functions of HetR, a master regulator of heterocyst differentiation in Anabaena sp. PCC 7120, can be separated by mutation Proc. Natl. Acad. Sci. U.S.A. 101, 16040-16045 (Pubitemid 39507923)
36. Reeves, R. and Nissen, M. S. (1990) The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure J. Biol. Chem. 265, 8573-8582
37. Banks, G. C., Mohr, B., and Reeves, R. (1999) The HMG-I(Y) A.T-hook peptide motif confers DNA-binding specificity to a structured chimeric protein J. Biol. Chem. 274, 16536-16544
38. Goodwin, G. H. and Johns, E. W. (1973) Isolation and characterisation of two calf-thymus chromatin non-histone proteins with high contents of acidic and basic amino acids Eur. J. Biochem. 40, 215-219
39. Goodwin, G. H., Sanders, C., and Johns, E. W. (1973) A new group of chromatin-associated proteins with a high content of acidic and basic amino acids Eur. J. Biochem. 38, 14-19
40. Grosschedl, R., Giese, K., and Pagel, J. (1994) HMG Domain Proteins-Architectural Elements in the Assembly of Nucleoprotein Structures Trends Genet. 94-100 (Pubitemid 24075089)
41. Reeves, R., Leonard, W. J., and Nissen, M. S. (2000) Binding of HMG-I(Y) imparts architectural specificity to a positioned nucleosome on the promoter of the human interleukin-2 receptor alpha gene Mol. Cell. Biol. 20, 4666-4679 (Pubitemid 30396114)
42. Huth, J. R., Bewley, C. A., Nissen, M. S., Evans, J. N., Reeves, R., Gronenborn, A. M., and Clore, G. M. (1997) The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif Nat. Struct. Biol. 4, 657-665 (Pubitemid 27323449)
43. Kim, Y., Joachimiak, G., Ye, Z., Binkowski, T. A., Zhang, R., Gornicki, P., Callahan, S. M., Hess, W. R., Haselkorn, R., and Joachimiak, A. (2011) Structure of transcription factor HetR required for heterocyst differentiation in cyanobacteria Proc. Natl. Acad. Sci. U.S.A. 108, 10109-10114
44. Elhai, J. and Wolk, C. P. (1988) Conjugal transfer of DNA to cyanobacteria Methods Enzymol. 167, 747-754
45. Limphong, P., Crowder, M. W., Bennett, B., and Makaroff, C. A. (2009) Arabidopsis thaliana GLX2-1 contains a dinuclear metal binding site, but is not a glyoxalase 2 Biochem. J. 417, 323-330
46. Schneider, D. and Freed, J. (1989) Calculating slow motional magnetic resonance spectra: A users guide, in Biological Magnetic Resonance (Berliner, L. and Reuben, J., Eds.), pp 1-76, Plenum, New York, NY.
47. Budil, D., Lee, S., Saxena, S., and Freed, J. (1996) Nonlinear-least- squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm J. Magn. Reson., Ser. A 155-189 (Pubitemid 126751752)
48. Hoofnagle, A. N., Stoner, J. W., Lee, T., Eaton, S. S., and Ahn, N. G. (2004) Phosphorylation-dependent changes in structure and dynamics in ERK2 detected by SDSL and EPR Biophys. J. 86, 395-403 (Pubitemid 38067467)
49. Zhang, Z., Fleissner, M. R., Tipikin, D. S., Liang, Z., Moscicki, J. K., Earle, K. A., Hubbell, W. L., and Freed, J. H. (2010) Multifrequency electron spin resonance study of the dynamics of spin labeled T4 lysozyme J. Phys. Chem. B 114, 5503-5521
50. Nesmelov, Y. E., Agafonov, R. V., Burr, A. R., Weber, R. T., and Thomas, D. D. (2008) Structure and dynamics of the force-generating domain of myosin probed by multifrequency electron paramagnetic resonance Biophys. J. 95, 247-256
51. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., Timmel, C., Hilger, D., and Jung, H. (2006) DeerAnalysis2006 - a comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 473-498
52. Chiang, Y. W., Borbat, P. P., and Freed, J. H. (2005) The determination of pair distance distributions by pulsed ESR using Tikhonov regularization J. Magn. Reson. 172, 279-295 (Pubitemid 40072533)
53. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalè, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
54. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics J. Mol. Graphics 14 (33-38) 27-38
55. Polyhach, Y., Bordignon, E., and Jeschke, G. (2011) Rotamer libraries of spin labelled cysteines for protein studies Phys. Chem. Chem. Phys. 13, 2356-2366
56. Frías, J. E., Flores, E., and Herrero, A. (1997) Nitrate assimilation gene cluster from the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 J. Bacteriol. 179, 477-486 (Pubitemid 27030402)
57. Borthakur, P. B., Orozco, C. C., Young-Robbins, S. S., Haselkorn, R., and Callahan, S. M. (2005) Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120 Mol. Microbiol. 57, 111-123 (Pubitemid 40896601)
58. Klug, C. S., Eaton, S. S., Eaton, G. R., and Feix, J. B. (1998) Ligand-induced conformational change in the ferric enterobactin receptor FepA as studied by site-directed spin labeling and time-domain ESR Biochemistry 37, 9016-9023 (Pubitemid 28299672)
59. Buchaklian, A. H. and Klug, C. S. (2005) Characterization of the Walker A motif of MsbA using site-directed spin labeling electron paramagnetic resonance spectroscopy Biochemistry 44, 5503-5509 (Pubitemid 40489990)
60. Hanson, S. M., Francis, D. J., Vishnivetskiy, S. A., Kolobova, E. A., Hubbell, W. L., Klug, C. S., and Gurevich, V. V. (2006) Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin Proc. Natl. Acad. Sci. U.S.A. 103, 4900-4905
61. Fanucci, G. E. and Cafiso, D. S. (2006) Recent advances and applications of site-directed spin labeling Curr. Opin. Struct. Biol. 16, 644-653 (Pubitemid 44466409)
62. Klug, C. S. and Feix, J. B. (2008) Methods and applications of site-directed spin labeling EPR spectroscopy Methods Cell Biol. 84, 617-658
63. Altenbach, C., Marti, T., Khorana, H. G., and Hubbell, W. L. (1990) Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants Science 248, 1088-1092
64. Mchaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics Biochemistry 35, 7692-7704 (Pubitemid 26202511)
65. Mchaourab, H. S., Kalai, T., Hideg, K., and Hubbell, W. L. (1999) Motion of spin-labeled side chains in T4 lysozyme: effect of side chain structure Biochemistry 38, 2947-2955
66. Milov, A., Ponomarev, A., and Tsvetkov, Y. (1984) Electron electron double-resonance in electron-spin echo - model biradical systems and the sensitized photolysis of decalin Chem. Phys. Lett. 67-72
67. Milov, A., Salikhov, K., and Shirov, M. (1981) Application of ELDOR in electron-spin echo for paramagnetic center space distribution in solids Fiz Tverd Tela (Leningrad) 23, 957-982
68. Borbat, P. P., Davis, J. H., Butcher, S. E., and Freed, J. H. (2004) Measurement of large distances in biomolecules using double-quantum filtered refocused electron spin-echoes J. Am. Chem. Soc. 126, 7746-7747 (Pubitemid 38812745)
69. Borbat, P. and Freed, J. (2001) Double Quantum ESR and Distance Measurements, Kluwer, New York, NY.
70. Higa, K. C. and Callahan, S. M. (2010) Ectopic expression of hetP can partially bypass the need for hetR in heterocyst differentiation by Anabaena sp. strain PCC 7120 Mol. Microbiol. 77, 562-574
71. Harrison, S. C. (1991) A structural taxonomy of DNA-binding domains Nature 353, 715-719
72. Latchman, D. S. (1997) Transcription factors: an overview Int. J. Biochem. Cell Biol. 29, 1305-1312 (Pubitemid 28153484)
73. Huffman, J. L. and Brennan, R. G. (2002) Prokaryotic transcription regulators: more than just the helix-turn-helix motif Curr. Opin. Struct. Biol. 12, 98-106 (Pubitemid 34142727)
74. Feig, A. L. (2007) Applications of isothermal titration calorimetry in RNA biochemistry and biophysics Biopolymers 87, 293-301
75. Streicher, W. W., Lopez, M. M., and Makhatadze, G. I. (2009) Annexin I and annexin II N-terminal peptides binding to S100 protein family members: specificity and thermodynamic characterization Biochemistry 48, 2788-2798
76. Connelly, P. R., Aldape, R. A., Bruzzese, F. J., Chambers, S. P., Fitzgibbon, M. J., Fleming, M. A., Itoh, S., Livingston, D. J., Navia, M. A., and Thomson, J. A. (1994) Enthalpy of hydrogen bond formation in a protein-ligand binding reaction Proc. Natl. Acad. Sci. U.S.A. 91, 1964-1968 (Pubitemid 24080327)
77. Calderone, C. T. and Williams, D. H. (2001) An enthalpic component in cooperativity: the relationship between enthalpy, entropy, and noncovalent structure in weak associations J. Am. Chem. Soc. 123, 6262-6267 (Pubitemid 32904653)
78. Williams, D. H., Stephens, E., OBrien, D. P., and Zhou, M. (2004) Understanding noncovalent interactions: ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes Angew. Chem., Int. Ed. 43, 6596-6616 (Pubitemid 40018986)
79. Harishchandra, G., McCarrick, R. M., Budil, D. E., and Lorigan, G. A. (2009) Significantly improved sensitivity of Q-Band PELDOR/DEER experiments relative to X-Band is observed in measuring the intercoil distance of a leucine zipper motif peptide (GCN4-LZ). Biochemistry 48, 5782-5784