Hydrogen bond donation to the heme distal ligand of Staphylococcus aureus IsdG tunes the electronic structure

详细信息    查看全文

• 作者：Cheryl L. Lockhart ; Matthew A. Conger…
• 关键词：Circular dichroism ; Density functional theory ; Heme oxygenase ; Magnetic circular dichroism ; Second ; sphere interactions
• 刊名：Journal of Biological Inorganic Chemistry
• 出版年：2015
• 出版时间：July 2015
• 年：2015
• 卷：20
• 期：5
• 页码：757-770
• 全文大小：2,177 KB
• 参考文献：1.David MZ, Daum RS (2010) Clin Microbiol Rev 23:616-87PubMed Central PubMed View Article
  2.Weinberg ED (1978) Microbiol Rev 42:45-6PubMed Central PubMed
  3.Bridges K, Seligman PA (1995) Blood: principles and practice of hematology. J.B. Lippincott Company, Philadelphia
  4.Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM, Schneewind O (2003) Science 299:906-09PubMed View Article
  5.Reniere ML, Skaar EP (2008) Mol Microbiol 69:1304-315PubMed Central PubMed View Article
  6.Stranger-Jones YK, Bae T, Schneewind O (2006) Proc Natl Acad Sci 103:16942-6947PubMed Central PubMed View Article
  7.Takayama SJ, Ukpabi G, Murphy MEP, Mauk AG (2011) Proc Natl Acad Sci 108:13071-3076PubMed Central PubMed View Article
  8.Ukpabi G, Takayama SJ, Mauk AG, Murphy MEP (2012) J Biol Chem 287:34179-4188PubMed Central PubMed View Article
  9.Skaar EP, Gaspar AH, Schneewind O (2004) J Biol Chem 279:436-43PubMed View Article
  10.Wu R, Skaar EP, Zhang R, Joachimiak G, Gornicki P, Schneewind O, Joachimiak A (2005) J Biol Chem 280:2840-846PubMed Central PubMed View Article
  11.Reniere ML, Ukpabi G, Harry SR, Stec DF, Krull R, Wright DW, Bachmann BO, Murphy ME, Skaar EP (2010) Mol Microbiol 75:1529-538PubMed Central PubMed View Article
  12.Matsui T, Nambu S, Ono Y, Goulding CW, Tsumoto K, Ikeda-Saito M (2013) Biochemistry 52:3025-027PubMed Central PubMed View Article
  13.Loutet SA, Kobylarz MJ, Chau CHT, Murphy MEP (2013) J Biol Chem 288:25749-5759PubMed Central PubMed View Article
  14.Ragsdale SW, Yi L (2011) Antioxid Redox Signal 14:1039-047PubMed Central PubMed View Article
  15.Reniere ML, Haley KP, Skaar EP (2011) Biochemistry 50:6730-737PubMed Central PubMed View Article
  16.Takahashi S, Wang J, Rousseau DL, Ishikawa K, Yoshida T, Host JR, Ikeda-Saito M (1994) J Biol Chem 269:1010-014PubMed
  17.Ishikawa K, Takeuchi N, Takahashi S, Matera KM, Sato M, Shibahara S, Rousseau DL, Ikeda-Saito M, Yoshida T (1995) J Biol Chem 270:6345-350PubMed View Article
  18.Gardner JD, Yi L, Ragsdale SW, Brunold TC (2010) J Biol Inorg Chem 15:1117-127PubMed Central PubMed View Article
  19.Lee WC, Reniere ML, Skaar EP, Murphy ME (2008) J Biol Chem 283:30957-0963PubMed Central PubMed View Article
  20.Rivera M, Rodriguez JC (2009) In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences. Royal Society of Chemistry, Cambridge, pp 241-93
  21.Matsui T, Unno M, Ikeda-Saito M (2010) Acc Chem Res 43:240-47PubMed View Article
  22.Wilks A, Heinzl G (2014) Arch Biochem Biophys 544:87-5PubMed View Article
  23.Wilks A, Ikeda-Saito M (2014) Acc Chem Res 47:2291-298PubMed Central PubMed View Article
  24.Sugishima M, Sakamoto H, Higashimoto Y, Omata Y, Hayashi S, Noguchi M, Fukuyama K (2002) J Biol Chem 277:45086-5090PubMed View Article
  25.Rodríguez JC, Wilks A, Rivera M (2006) Biochemistry 45:4578-592PubMed View Article
  26.Schuller DJ, Wilks A, Ortiz de Montellano PR, Poulos TL (1999) Nat Struct Biol 6:860-67PubMed View Article
  27.Li Y, Syvitski RT, Auclair K, Wilks A, Ortiz de Montellano PR, La Mar GN (2002) J Biol Chem 277:33018-3031PubMed View Article
  28.Syvitski RT, Li Y, Auclair K, Ortiz de Montellano PR, La Mar GN (2002) J Am Chem Soc 124:14296-4297PubMed View Article
  29.Li Y, Syvitski RT, Auclair K, Ortiz de Montellano PR, La Mar GN (2003) J Am Chem Soc 125:13392-3403PubMed View Article
  30.Chen H, Moreau Y, Derat E, Shaik S (2008) J Am Chem Soc 130:1953-965PubMed View Article
  31.Gouterman M (1959) J Chem Phys 30:1139-161View Article
  32.Schweitzer-Stenner R (2011) J Porphyrins Phthalocyanines 15:312-37View Article
  33.Hsu M, Woody RW (1971) J Am Chem Soc 93:3515-525PubMed View Article
  34.Du J, Sono M, Dawson JH (2011) Coord Chem Rev 255:700-16PubMed Central PubMed View Article
  35.Graves AB, Morse RP, Chao A, Iniguez A, Goulding CW, Liptak MD (2014) Inorg Chem 53:5931-940PubMed Central PubMed View Article
  36.Lehnert N (2012) J Inorg Biochem 110:83-3PubMed View Article
  37.Kapust RB, T?zsér J, Fox JD, Anderson DE, Cherry S, Copeland TD, Waugh DS (2001) Protein Eng 14:993-000PubMed View Article
  38.Nallamsetty S, Kapust RB, T?zsér J, Cherry S, Tropea JE, Copeland TD, Waugh DS (2004) Protein Expr Purif 37:108-15View Article
  39.Kim Y, Dementieva I, Zhou M, Wu R, Lezondra L, Quartey P, Joachimiak G, Korolev O, Li H, Joachimiak A (2004) J Struct Funct Genomics 5:111-18PubMed Central PubMed View Article
  40.Chim N, Iniguez A, Nguyen TQ, Goulding CW (2010) J Mol Biol 395:595-08PubMed Central PubMed View Article
  41.Berry EA, Trumpower BL (1987) Anal Biochem 161:1-5PubMed View Article
  42.Cheesman MR, Walker FA (1996) J Am Chem Soc 118:7373-380View Article
  43.Neese F (2012) Wiley Interdiscip Rev Comput Mol Sci 2:73-8View Article
  44.Thompson MA (2004) Planaria Software LLC, Seattle
  45.Perdew JP, Burke K, Ernzerhof M (1996) Phys Rev Lett
• 作者单位：Cheryl L. Lockhart (1)
  Matthew A. Conger (1)
  Dylanger S. Pittman (1)
  Matthew D. Liptak (1)
  
  1. Department of Chemistry, University of Vermont, 82 University Place, Burlington, VT, 05405, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Microbiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1327

文摘

Staphylococcus aureus IsdG catalyzes the final step of staphylococcal iron acquisition from host hemoglobin, whereby host-derived heme is converted to iron and organic products. The Asn7 distal pocket residue is known to be critical for enzyme activity, but the influence of this residue on the substrate electronic structure was unknown prior to this work. Here, an optical spectroscopic and density functional theory characterization of azide- and cyanide-inhibited wild type and N7A IsdG is presented. Magnetic circular dichroism data demonstrate that Asn7 perturbs the electronic structure of azide-inhibited, but not cyanide-inhibited, IsdG. As the iron-ligating α-atom of azide, but not cyanide, can act as a hydrogen bond acceptor, these data indicate that the terminal amide of Asn7 is a hydrogen bond donor to the α-atom of a distal ligand to heme in IsdG. Circular dichroism characterization of azide- and cyanide-inhibited forms of WT and N7A IsdG strongly suggests that the Asn7···N3 hydrogen bond influences the orientation of a distal azide ligand with respect to the heme substrate. Specifically, density functional theory calculations suggest that Asn7···N3 hydrogen bond donation causes the azide ligand to rotate about an axis perpendicular to the porphyrin plane and weakens the π-donor strength of the azide ligand. This lowers the energies of the Fe 3d xz and 3d yz orbitals, mixes Fe 3d xy and porphyrin a 2u character into the singly-occupied molecular orbital, and results in spin delocalization onto the heme meso carbons. These discoveries have important implications for the mechanism of heme oxygenation catalyzed by IsdG.