publication . Article . Other literature type . 2018

Staphylococcus aureus HemX Modulates Glutamyl-tRNA Reductase Abundance To Regulate Heme Biosynthesis

Jacob E. Choby; Caroline M. Grunenwald; Arianna I. Celis; Svetlana Y. Gerdes; Jennifer L. DuBois; Eric P. Skaar; Kimberly A. Kline;
Open Access English
  • Published: 06 Feb 2018 Journal: mBio, volume 9, issue 1 (eissn: 2150-7511, Copyright policy)
  • Publisher: American Society for Microbiology
Abstract
is a leading cause of skin and soft tissue infections, endocarditis, bacteremia, and osteomyelitis, making it a critical health care concern. Development of new antimicrobials against requires knowledge of the physiology that supports this organism’s pathogenesis. One component of staphylococcal physiology that contributes to growth and virulence is heme. Heme is a widely utilized cofactor that enables diverse chemical reactions across many enzyme families. relies on many critical heme-dependent proteins and is sensitive to excess heme toxicity, suggesting must maintain proper intracellular heme homeostasis. Because provides heme for heme-dependent enzymes via s...
Subjects
free text keywords: Research Article, Staphylococcus aureus, heme, tetrapyrroles, Microbiology, QR1-502, Biochemistry, Cofactor, biology.protein, biology, Mutant, chemistry.chemical_compound, chemistry, Reductase, Membrane protein, Glutamyl-tRNA reductase, Genetics, Integral membrane protein, Enzyme, chemistry.chemical_classification
Funded by
NIH| Regulation of HemA, the initial enzyme in Staphylococcus aureus heme biosynthesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1F31AI126662-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Chemistry-Biology Interface Training Grant
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 3T32GM065086-07S1
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Chlorite dismutase: a novel heme enzyme and its implications for human health
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01GM090260-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Understanding the Contributions of Commensal Bacteria to Human Fe Metabolism
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R21DK114607-01
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Interdisciplinary Training Program in Lung Research
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2T32HL094296-11
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
Download fromView all 4 versions
mBio
Article . 2018
mBio
Article . 2018
Provider: Crossref
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Article
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62 references, page 1 of 5

1.Choby JE, Skaar EP 2016 Heme synthesis and acquisition in bacterial pathogens. J Mol Biol 428:3408–3428. doi:10.1016/j.jmb.2016.03.018.27019298 [OpenAIRE] [PubMed] [DOI]

2.Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK, Active Bacterial Core surveillance (ABCs) MRSA Investigators 2007 Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763–1771. doi:10.1001/jama.298.15.1763.17940231 [PubMed] [DOI]

3.Hammer ND, Reniere ML, Cassat JE, Zhang Y, Hirsch AO, Hood MI, Skaar EP 2013 Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. mBio 4:e00241-13. doi:10.1128/mBio.00241-13.23900169 [OpenAIRE] [PubMed] [DOI]

4.Hammer ND, Schurig-Briccio LA, Gerdes SY, Gennis RB, Skaar EP 2016 CtaM is required for menaquinol oxidase aa3 function in Staphylococcus aureus. mBio 7:e00823-16. doi:10.1128/mBio.00823-16.27406563 [OpenAIRE] [PubMed] [DOI]

5.Dailey HA, Gerdes S, Dailey TA, Burch JS, Phillips JD 2015 Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin. Proc Natl Acad Sci U S A 112:2210–2215. doi:10.1073/pnas.1416285112.25646457 [OpenAIRE] [PubMed] [DOI]

6.Lobo SA, Scott A, Videira MA, Winpenny D, Gardner M, Palmer MJ, Schroeder S, Lawrence AD, Parkinson T, Warren MJ, Saraiva LM 2015 Staphylococcus aureus haem bio synthesis: characterisation of the enzymes involved in final steps of the pathway. Mol Microbiol 97:472–487. doi:10.1111/mmi.13041.25908396 [OpenAIRE] [PubMed] [DOI]

7.Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ 2007 Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035. doi:10.1128/JB.01524-06.17114262 [OpenAIRE] [PubMed] [DOI]

8.van Sorge NM, Beasley FC, Gusarov I, Gonzalez DJ, von Köckritz-Blickwede M, Anik S, Borkowski AW, Dorrestein PC, Nudler E, Nizet V 2013 Methicillin-resistant Staphylococcus aureus bacterial nitric-oxide synthase affects antibiotic sensitivity and skin abscess development. J Biol Chem 288:6417–6426. doi:10.1074/jbc.M112.448738.23322784 [OpenAIRE] [PubMed] [DOI]

9.Mogen AB, Carroll RK, James KL, Lima G, Silva D, Culver JA, Petucci C, Shaw LN, Rice KC 2017 Staphylococcus aureus nitric oxide synthase (saNOS) modulates aerobic respiratory metabolism and cell physiology. Mol Microbiol 105:139–157. doi:10.1111/mmi.13693.28431199 [OpenAIRE] [PubMed] [DOI]

10.Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, Iturregui J, Anderson KL, Dunman PM, Joyce S, Skaar EP 2007 A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109–119. doi:10.1016/j.chom.2007.03.001.18005689 [OpenAIRE] [PubMed] [DOI]

11.Beale SI, Castelfranco PA 1973 14 C incorporation from exogenous compounds into δ-aminolevulinic acid by greening cucumber cotyledons. Biochem Biophys Res Commun 52:143–149. doi:10.1016/0006-291X(73)90966-2.4712185 [PubMed] [DOI]

12.Schön A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Söll D 1986 The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322:281–284. doi:10.1038/322281a0.3637637 [OpenAIRE] [PubMed] [DOI]

13.Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW 2001 V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20:6583–6590. doi:10.1093/emboj/20.23.6583.11726494 [OpenAIRE] [PubMed] [DOI]

14.Dailey HA, Dailey TA, Gerdes S, Jahn D, Jahn M, O’Brian MR, Warren MJ 2017 Prokaryotic heme biosynthesis: multiple pathways to a common essential product. Microbiol Mol Biol Rev 81:81:e00048-16. doi:10.1128/MMBR.00048-16. [DOI]

15.Hansson M, Gustafsson MC, Kannangara CG, Hederstedt L 1997 Isolated Bacillus subtilis HemY has coproporphyrinogen III to coproporphyrin III oxidase activity. Biochim Biophys Acta 1340:97–104. doi:10.1016/S0167-4838(97)00030-7.9217019 [PubMed] [DOI]

62 references, page 1 of 5
Abstract
is a leading cause of skin and soft tissue infections, endocarditis, bacteremia, and osteomyelitis, making it a critical health care concern. Development of new antimicrobials against requires knowledge of the physiology that supports this organism’s pathogenesis. One component of staphylococcal physiology that contributes to growth and virulence is heme. Heme is a widely utilized cofactor that enables diverse chemical reactions across many enzyme families. relies on many critical heme-dependent proteins and is sensitive to excess heme toxicity, suggesting must maintain proper intracellular heme homeostasis. Because provides heme for heme-dependent enzymes via s...
Subjects
free text keywords: Research Article, Staphylococcus aureus, heme, tetrapyrroles, Microbiology, QR1-502, Biochemistry, Cofactor, biology.protein, biology, Mutant, chemistry.chemical_compound, chemistry, Reductase, Membrane protein, Glutamyl-tRNA reductase, Genetics, Integral membrane protein, Enzyme, chemistry.chemical_classification
Funded by
NIH| Regulation of HemA, the initial enzyme in Staphylococcus aureus heme biosynthesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1F31AI126662-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Chemistry-Biology Interface Training Grant
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 3T32GM065086-07S1
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Chlorite dismutase: a novel heme enzyme and its implications for human health
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01GM090260-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Understanding the Contributions of Commensal Bacteria to Human Fe Metabolism
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R21DK114607-01
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Interdisciplinary Training Program in Lung Research
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2T32HL094296-11
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
Download fromView all 4 versions
mBio
Article . 2018
mBio
Article . 2018
Provider: Crossref
mBio
Article
Provider: UnpayWall
62 references, page 1 of 5

1.Choby JE, Skaar EP 2016 Heme synthesis and acquisition in bacterial pathogens. J Mol Biol 428:3408–3428. doi:10.1016/j.jmb.2016.03.018.27019298 [OpenAIRE] [PubMed] [DOI]

2.Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK, Active Bacterial Core surveillance (ABCs) MRSA Investigators 2007 Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763–1771. doi:10.1001/jama.298.15.1763.17940231 [PubMed] [DOI]

3.Hammer ND, Reniere ML, Cassat JE, Zhang Y, Hirsch AO, Hood MI, Skaar EP 2013 Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. mBio 4:e00241-13. doi:10.1128/mBio.00241-13.23900169 [OpenAIRE] [PubMed] [DOI]

4.Hammer ND, Schurig-Briccio LA, Gerdes SY, Gennis RB, Skaar EP 2016 CtaM is required for menaquinol oxidase aa3 function in Staphylococcus aureus. mBio 7:e00823-16. doi:10.1128/mBio.00823-16.27406563 [OpenAIRE] [PubMed] [DOI]

5.Dailey HA, Gerdes S, Dailey TA, Burch JS, Phillips JD 2015 Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin. Proc Natl Acad Sci U S A 112:2210–2215. doi:10.1073/pnas.1416285112.25646457 [OpenAIRE] [PubMed] [DOI]

6.Lobo SA, Scott A, Videira MA, Winpenny D, Gardner M, Palmer MJ, Schroeder S, Lawrence AD, Parkinson T, Warren MJ, Saraiva LM 2015 Staphylococcus aureus haem bio synthesis: characterisation of the enzymes involved in final steps of the pathway. Mol Microbiol 97:472–487. doi:10.1111/mmi.13041.25908396 [OpenAIRE] [PubMed] [DOI]

7.Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ 2007 Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035. doi:10.1128/JB.01524-06.17114262 [OpenAIRE] [PubMed] [DOI]

8.van Sorge NM, Beasley FC, Gusarov I, Gonzalez DJ, von Köckritz-Blickwede M, Anik S, Borkowski AW, Dorrestein PC, Nudler E, Nizet V 2013 Methicillin-resistant Staphylococcus aureus bacterial nitric-oxide synthase affects antibiotic sensitivity and skin abscess development. J Biol Chem 288:6417–6426. doi:10.1074/jbc.M112.448738.23322784 [OpenAIRE] [PubMed] [DOI]

9.Mogen AB, Carroll RK, James KL, Lima G, Silva D, Culver JA, Petucci C, Shaw LN, Rice KC 2017 Staphylococcus aureus nitric oxide synthase (saNOS) modulates aerobic respiratory metabolism and cell physiology. Mol Microbiol 105:139–157. doi:10.1111/mmi.13693.28431199 [OpenAIRE] [PubMed] [DOI]

10.Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, Iturregui J, Anderson KL, Dunman PM, Joyce S, Skaar EP 2007 A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109–119. doi:10.1016/j.chom.2007.03.001.18005689 [OpenAIRE] [PubMed] [DOI]

11.Beale SI, Castelfranco PA 1973 14 C incorporation from exogenous compounds into δ-aminolevulinic acid by greening cucumber cotyledons. Biochem Biophys Res Commun 52:143–149. doi:10.1016/0006-291X(73)90966-2.4712185 [PubMed] [DOI]

12.Schön A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Söll D 1986 The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322:281–284. doi:10.1038/322281a0.3637637 [OpenAIRE] [PubMed] [DOI]

13.Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW 2001 V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20:6583–6590. doi:10.1093/emboj/20.23.6583.11726494 [OpenAIRE] [PubMed] [DOI]

14.Dailey HA, Dailey TA, Gerdes S, Jahn D, Jahn M, O’Brian MR, Warren MJ 2017 Prokaryotic heme biosynthesis: multiple pathways to a common essential product. Microbiol Mol Biol Rev 81:81:e00048-16. doi:10.1128/MMBR.00048-16. [DOI]

15.Hansson M, Gustafsson MC, Kannangara CG, Hederstedt L 1997 Isolated Bacillus subtilis HemY has coproporphyrinogen III to coproporphyrin III oxidase activity. Biochim Biophys Acta 1340:97–104. doi:10.1016/S0167-4838(97)00030-7.9217019 [PubMed] [DOI]

62 references, page 1 of 5
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publication . Article . Other literature type . 2018

Staphylococcus aureus HemX Modulates Glutamyl-tRNA Reductase Abundance To Regulate Heme Biosynthesis

Jacob E. Choby; Caroline M. Grunenwald; Arianna I. Celis; Svetlana Y. Gerdes; Jennifer L. DuBois; Eric P. Skaar; Kimberly A. Kline;