The role of host heme in bacterial infection

References

Aich, A., Freundlich, M., and Vekilov, P.G. (2015). The free heme concentration in healthy human erythrocytes. Blood Cell Mol. Dis. 55: 402–409. https://doi.org/10.1016/j.bcmd.2015.09.003.Search in Google Scholar PubMed PubMed Central

Akhter, F., Womack, E., Vidal, J.E., Le Breton, Y., Mciver, K.S., Pawar, S., and Eichenbaum, Z. (2020). Hemoglobin stimulates vigorous growth of Streptococcus pneumoniae and shapes the pathogen’s global transcriptome. Sci. Rep. 10: 15202. https://doi.org/10.1038/s41598-020-71910-1.Search in Google Scholar PubMed PubMed Central

Akhter, F., Womack, E., Vidal, J.E., Le Breton, Y., Mciver, K.S., Pawar, S., and Eichenbaum, Z. (2021). Hemoglobin induces early and robust biofilm development in Streptococcus pneumoniae by a pathway that involves comC but not the cognate comDE two-component system. Infect. Immun. 89: e007799–e820. https://doi.org/10.1128/iai.00779-20.Search in Google Scholar PubMed PubMed Central

Allen, C.E., Burgos, J.M., and Schmitt, M.P. (2013). Analysis of novel iron-regulated, surface-anchored hemin-binding proteins in Corynebacterium diphtheriae. J. Bacteriol. 195: 2852–2863. https://doi.org/10.1128/jb.00244-13.Search in Google Scholar PubMed PubMed Central

Allen, C.E. and Schmitt, M.P. (2009). HtaA is an iron-regulated hemin binding protein involved in the utilization of heme iron in Corynebacterium diphtheriae. J. Bacteriol. 191: 2638–2648. https://doi.org/10.1128/jb.01784-08.Search in Google Scholar

Allen, C.E. and Schmitt, M.P. (2011). Novel hemin binding domains in the Corynebacterium diphtheriae HtaA protein interact with hemoglobin and are critical for heme iron utilization by HtaA. J. Bacteriol. 193: 5374–5385. https://doi.org/10.1128/jb.05508-11.Search in Google Scholar

Allen, C.E. and Schmitt, M.P. (2015). Utilization of host iron sources by Corynebacterium diphtheriae: multiple hemoglobin-binding proteins are essential for the use of iron from the hemoglobin-haptoglobin complex. J. Bacteriol. 197: 553–562. https://doi.org/10.1128/jb.02413-14.Search in Google Scholar PubMed PubMed Central

Amorim, G.C.D., Prochnicka-Chalufour, A., Delepelaire, P., Lefèvre, J., Simenel, C., Wandersman, C., Delepierre, M., and Izadi-Pruneyre, N. (2013). The structure of HasB reveals a new class of TonB protein fold. PLoS One 8: e58964. https://doi.org/10.1371/journal.pone.0058964.Search in Google Scholar PubMed PubMed Central

Anzaldi, L.L. and Skaar, E.P. (2010). Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect. Immun. 78: 4977–4989. https://doi.org/10.1128/iai.00613-10.Search in Google Scholar

Ates, L.S. (2020). New insights into the mycobacterial Pe and PPE proteins provide a framework for future research. Mol. Microbiol. 113: 4–21. https://doi.org/10.1111/mmi.14409.Search in Google Scholar PubMed PubMed Central

Barañano, D.E., Rao, M., Ferris, C.D., and Snyder, S.H. (2002). Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. USA 99: 16093–16098. https://doi.org/10.1073/pnas.252626999.Search in Google Scholar PubMed PubMed Central

Bibb, L.A., Kunkle, C.A., and Schmitt, M.P. (2007). The ChrA-ChrS and HrrA-HrrS signal transduction systems are required for activation of the hmuO promoter and repression of the hemA promoter in Corynebacterium diphtheriae. Infect. Immun. 75: 2421–2431. https://doi.org/10.1128/iai.01821-06.Search in Google Scholar

Bozza, M.T. and Jeney, V. (2020). Pro-inflammatory actions of heme and other hemoglobin-derived DAMPs. Front. Immunol. 11: 1323. https://doi.org/10.3389/fimmu.2020.01323.Search in Google Scholar PubMed PubMed Central

Briaud, P., Camus, L., Bastien, S., Doléans-Jordheim, A., Vandenesch, F., and Moreau, K. (2019). Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells. Sci. Rep. 9: 16564. https://doi.org/10.1038/s41598-019-52975-z.Search in Google Scholar PubMed PubMed Central

Celis, A.I. and Dubois, J.L. (2019). Making and breaking heme. Curr. Opin. Struct. Biol. 59: 19–28. https://doi.org/10.1016/j.sbi.2019.01.006.Search in Google Scholar PubMed PubMed Central

Ch’ng, J.-H., Muthu, M., Chong, K.K.L., Wong, J.J., Tan, C.A.Z., Koh, Z.J.S., Lopez, D., Matysik, A., Nair, Z.J., Barkham, T., et al.. (2022). Heme cross-feeding can augment Staphylococcus aureus and Enterococcus faecalis dual species biofilms. ISME J. 16: 2015–2026. https://doi.org/10.1038/s41396-022-01248-1.Search in Google Scholar PubMed PubMed Central

Chao, A., Sieminski, P.J., Owens, C.P., and Goulding, C.W. (2018). Iron acquisition in Mycobacterium tuberculosis. Chem. Rev. 119: 1193–1220. https://doi.org/10.1021/acs.chemrev.8b00285.Search in Google Scholar PubMed PubMed Central

Chim, N., Iniguez, A., Nguyen, T.Q., and Goulding, C.W. (2010). Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. J. Mol. Biol. 395: 595–608. https://doi.org/10.1016/j.jmb.2009.11.025.Search in Google Scholar PubMed PubMed Central

Choby, J.E., Grunenwald, C.M., Celis, A.I., Gerdes, S.Y., Dubois, J.L., and Skaar, E.P. (2018). Staphylococcus aureus HemX modulates glutamyl-tRNA reductase abundance to regulate heme biosynthesis. mBio 9: e022877–e2317. https://doi.org/10.1128/mbio.02287-17.Search in Google Scholar PubMed PubMed Central

Choby, J.E. and Skaar, E.P. (2016). Heme synthesis and acquisition in bacterial pathogens. J. Mol. Biol. 428: 3408–3428. https://doi.org/10.1016/j.jmb.2016.03.018.Search in Google Scholar PubMed PubMed Central

Conroy, B.S., Grigg, J.C., Kolesnikov, M., Morales, L.D., and Murphy, M.E.P. (2019). Staphylococcus aureus heme and siderophore-iron acquisition pathways. Biometals 32: 409–424. https://doi.org/10.1007/s10534-019-00188-2.Search in Google Scholar PubMed

Contreras, H., Chim, N., Credali, A., and Goulding, C.W. (2014). Heme uptake in bacterial pathogens. Curr. Opin. Chem. Biol. 19: 34–41. https://doi.org/10.1016/j.cbpa.2013.12.014.Search in Google Scholar PubMed PubMed Central

Cornforth, D.M., Dees, J.L., Ibberson, C.B., Huse, H.K., Mathiesen, I.H., Kirketerp-Møller, K., Wolcott, R.D., Rumbaugh, K.P., Bjarnsholt, T., and Whiteley, M. (2018). Pseudomonas aeruginosa transcriptome during human infection. Proc. Natl. Acad. Sci. USA 115: E5125–E5134. https://doi.org/10.1073/pnas.1717525115.Search in Google Scholar PubMed PubMed Central

Costa, D.L., Amaral, E.P., Andrade, B.B., and Sher, A. (2020). Modulation of inflammation and immune responses by heme oxygenase-1: implications for infection with intracellular pathogens. Antioxidants 9: 1205. https://doi.org/10.3390/antiox9121205.Search in Google Scholar PubMed PubMed Central

Costa, D.L., Namasivayam, S., Amaral, E.P., Arora, K., Chao, A., Mittereder, L.R., Maiga, M., Boshoff, H.I., Barry, C.E.III, and Goulding, C.W. (2016). Pharmacological inhibition of host heme oxygenase-1 suppresses Mycobacterium tuberculosis infection in vivo by a mechanism dependent on T lymphocytes. mBio 7: e016755–e1716. https://doi.org/10.1128/mbio.01675-16.Search in Google Scholar PubMed PubMed Central

Dailey, H.A., Dailey, T.A., Gerdes, S., Jahn, D., Jahn, M., O’brian, M.R., and Warren, M.J. (2017). Prokaryotic heme biosynthesis: multiple pathways to a common essential product. Microbiol. Mol. Biol. Rev. 81: e000488–e116. https://doi.org/10.1128/mmbr.00048-16.Search in Google Scholar PubMed PubMed Central

Dailey, H.A., Gerdes, S., Dailey, T.A., Burch, J.S., and Phillips, J.D. (2015). Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin. Proc. Natl. Acad. Sci. USA 112: 2210–2215. https://doi.org/10.1073/pnas.1416285112.Search in Google Scholar PubMed PubMed Central

Dailey, T.A., Boynton, T.O., Albetel, A.-N., Gerdes, S., Johnson, M.K., and Dailey, H.A. (2010). Discovery and characterization of HemQ an essential heme biosynthetic pathway component. J. Biol. Chem. 285: 25978–25986. https://doi.org/10.1074/jbc.m110.142604.Search in Google Scholar

Dauros-Singorenko, P., Wiles, S., and Swift, S. (2020). Staphylococcus aureus biofilms and their response to a relevant in vivo iron source. Front. Microbiol. 11: 509525. https://doi.org/10.3389/fmicb.2020.509525.Search in Google Scholar PubMed PubMed Central

Deniau, C., Gilli, R., Izadi-Pruneyre, N., Létoffé, S., Delepierre, M., Wandersman, C., Briand, C., and Lecroisey, A. (2003). Thermodynamics of heme binding to the HasASM hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42: 10627–10633. https://doi.org/10.1021/bi030015k.Search in Google Scholar PubMed

Dent, A.T., Mouriño, S., Huang, W., and Wilks, A. (2019). Post-transcriptional regulation of the Pseudomonas aeruginosa heme assimilation system (Has) fine-tunes extracellular heme sensing. J. Biol. Chem. 294: 2771–5555. https://doi.org/10.1074/jbc.ra118.006185.Search in Google Scholar

Dent, A.T. and Wilks, A. (2020). Contributions of the heme coordinating ligands of the Pseudomonas aeruginosa outer membrane receptor HasR to extracellular heme sensing and transport. J. Biol. Chem. 295: 10456–10467. https://doi.org/10.1074/jbc.ra120.014081.Search in Google Scholar PubMed PubMed Central

Donegan, R.K., Moore, C.M., Hanna, D.A., and Reddi, A.R. (2019). Handling heme: the mechanisms underlying the movement of heme within and between cells. Free Radic. Biol. Med. 133: 88–100. https://doi.org/10.1016/j.freeradbiomed.2018.08.005.Search in Google Scholar PubMed PubMed Central

Dutra, F.F. and Bozza, M.T. (2014). Heme on innate immunity and inflammation. Front. Pharmacol. 5: 115. https://doi.org/10.3389/fphar.2014.00115.Search in Google Scholar PubMed PubMed Central

Ellis-Guardiola, K., Mahoney, B.J., and Clubb, R.T. (2021). NEAr transporter (NEAT) domains: unique surface displayed heme chaperones that enable Gram-positive bacteria to capture heme-iron from hemoglobin. Front. Microbiol. 11: 607679. https://doi.org/10.3389/fmicb.2020.607679.Search in Google Scholar PubMed PubMed Central

Fernandez, P.L., Dutra, F.F., Alves, L., Figueiredo, R.T., Mourão-Sa, D., Fortes, G.B., Bergstrand, S., Lönn, D., Cevallos, R.R., and Pereira, R.M. (2010). Heme amplifies the innate immune response to microbial molecules through spleen tyrosine kinase (Syk)-dependent reactive oxygen species generation. J. Biol. Chem. 285: 32844–32851. https://doi.org/10.1074/jbc.m110.146076.Search in Google Scholar PubMed PubMed Central

Fontán, P.A., Aris, V., Alvarez, M.E., Ghanny, S., Cheng, J., Soteropoulos, P., Trevani, A., Pine, R., and Smith, I. (2008). Mycobacterium tuberculosis sigma factor E regulon modulates the host inflammatory response. J. Infect. Dis. 198: 877–885. https://doi.org/10.1086/591098.Search in Google Scholar PubMed

Frankenberg, L., Brugna, M., and Hederstedt, L. (2002). Enterococcus faecalis heme-dependent catalase. Am Soc Microbiol 184: 6351–6356.10.1128/JB.184.22.6351-6356.2002Search in Google Scholar PubMed PubMed Central

Frunzke, J., Gätgens, C., Brocker, M., and Bott, M. (2011). Control of heme homeostasis in Corynebacterium glutamicum by the two-component system HrrSA. J. Bacteriol. 193: 1212–1221. https://doi.org/10.1128/jb.01130-10.Search in Google Scholar PubMed PubMed Central

Ghigo, J.-M., Letoffe, S., and Wandersman, C. (1997). A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J. Bacteriol. 179: 3572–3579. https://doi.org/10.1128/jb.179.11.3572-3579.1997.Search in Google Scholar PubMed PubMed Central

Ghio, A.J., Roggli, V.L., Soukup, J.M., Richards, J.H., Randell, S.H., and Muhlebach, M.S. (2013). Iron accumulates in the lavage and explanted lungs of cystic fibrosis patients. J. Cyst. Fibros. 12: 390–398. https://doi.org/10.1016/j.jcf.2012.10.010.Search in Google Scholar PubMed

Glasser, N.R., Hunter, R.C., Liou, T.G., Newman, D.K., and Investigators, M.W.C.C. (2019). Refinement of metabolite detection in cystic fibrosis sputum reveals heme correlates with lung function decline. PLoS One 14: e0226578. https://doi.org/10.1371/journal.pone.0226578.Search in Google Scholar PubMed PubMed Central

Hammer, N.D., Reniere, M.L., Cassat, J.E., Zhang, Y., Hirsch, A.O., Indriati Hood, M., and Skaar, E.P. (2013). Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. mBio 4: e002411–e313. https://doi.org/10.1128/mBio.00241-13.Search in Google Scholar PubMed PubMed Central

Hammer, N.D. and Skaar, E.P. (2011). Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65: 129–147. https://doi.org/10.1146/annurev-micro-090110-102851.Search in Google Scholar PubMed PubMed Central

Hooda, J., Shah, A., and Zhang, L. (2014). Heme, an essential nutrient from dietary proteins, critically impacts diverse physiological and pathological processes. Nutrients 6: 1080–1102. https://doi.org/10.3390/nu6031080.Search in Google Scholar PubMed PubMed Central

Hvidberg, V., Maniecki, M.B., Jacobsen, C., Højrup, P., Møller, H.J., and Moestrup, S.K. (2005). Identification of the receptor scavenging hemopexin-heme complexes. Blood 106: 2572–2579. https://doi.org/10.1182/blood-2005-03-1185.Search in Google Scholar PubMed

Ibberson, C.B., Whiteley, M., and Sperandio, V. (2019). The Staphylococcus aureus transcriptome during cystic fibrosis lung infection. mBio 10: e027744–e2819. https://doi.org/10.1128/mbio.02774-19.Search in Google Scholar

Jepkorir, G., Rodríguez, J.C., Rui, H., Im, W., Lovell, S., Battaile, K.P., Alontaga, A.Y., Yukl, E.T., Moënne-Loccoz, P., and Rivera, M. (2010). Structural, NMR spectroscopic, and computational investigation of hemin loading in the hemophore HasAp from Pseudomonas aeruginosa. J. Am. Chem. Soc. 132: 9857–9872. https://doi.org/10.1021/ja103498z.Search in Google Scholar PubMed PubMed Central

Jones, C.M. and Niederweis, M. (2011). Mycobacterium tuberculosis can utilize heme as an iron source. J. Bacteriol. 193: 1767–1770. https://doi.org/10.1128/jb.01312-10.Search in Google Scholar

Knippel, R.J., Wexler, A.G., Miller, J.M., Beavers, W.N., Weiss, A., De Crécy-Lagard, V., Edmonds, K.A., Giedroc, D.P., and Skaar, E.P. (2020). Clostridioides difficile senses and hijacks host heme for incorporation into an oxidative stress defense system. Cell Host Microbe 28: 411–421.e6. https://doi.org/10.1016/j.chom.2020.05.015.Search in Google Scholar PubMed PubMed Central

Lansky, I.B., Lukat-Rodgers, G.S., Block, D., Rodgers, K.R., Ratliff, M., and Wilks, A. (2006). The cytoplasmic heme-binding protein (PhuS) from the heme uptake system of Pseudomonas aeruginosa is an intracellular heme-trafficking protein to the δ-regioselective heme oxygenase. J. Biol. Chem. 281: 13652–13662. https://doi.org/10.1074/jbc.m600824200.Search in Google Scholar

Lee, T.-S. and Chau, L.-Y. (2002). Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8: 240–246. https://doi.org/10.1038/nm0302-240.Search in Google Scholar PubMed

Letoffe, S., Ghigo, J., and Wandersman, C. (1994). Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc. Natl. Acad. Sci. USA 91: 9876–9880. https://doi.org/10.1073/pnas.91.21.9876.Search in Google Scholar PubMed PubMed Central

Liu, M., Ferrandez, Y., Bouhsira, E., Monteil, M., Franc, M., Boulouis, H.-J., and Biville, F. (2012). Heme binding proteins of Bartonella henselae are required when undergoing oxidative stress during cell and Flea invasion. PLoS One 7: e48408. https://doi.org/10.1371/journal.pone.0048408.Search in Google Scholar PubMed PubMed Central

Llamas, M.A., Imperi, F., Visca, P., and Lamont, I.L. (2014). Cell-surface signaling in Pseudomonas: stress responses, iron transport, and pathogenicity. FEMS Microbiol. Rev. 38: 569–597. https://doi.org/10.1111/1574-6976.12078.Search in Google Scholar PubMed

Mack, J., Vermeiren, C., Heinrichs, D.E., and Stillman, M.J. (2004). In vivo heme scavenging by Staphylococcus aureus IsdC and IsdE proteins. Biochem. Biophys. Res. Commun. 320: 781–788. https://doi.org/10.1016/j.bbrc.2004.06.025.Search in Google Scholar PubMed

Marvig, R.L., Damkiær, S., Khademi, S.H., Markussen, T.M., Molin, S., and Jelsbak, L. (2014). Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. mBio 5: e009666–e1014. https://doi.org/10.1128/mBio.00966-14.Search in Google Scholar PubMed PubMed Central

Matthews, S.J., Pacholarz, K.J., France, A.P., Jowitt, T.A., Hay, S., Barran, P.E., and Munro, A.W. (2019). MhuD from Mycobacterium tuberculosis: probing a dual role in heme storage and degradation. ACS Infect. Dis. 5: 1855–1866. https://doi.org/10.1021/acsinfecdis.9b00181.Search in Google Scholar PubMed

Mayfield, J.A., Hammer, N.D., Kurker, R.C., Chen, T.K., Ojha, S., Skaar, E.P., and Dubois, J.L. (2013). The chlorite dismutase (HemQ) from Staphylococcus aureus has a redox-sensitive heme and is associated with the small colony variant phenotype. J. Biol. Chem. 288: 23488–23504. https://doi.org/10.1074/jbc.m112.442335.Search in Google Scholar

Mazmanian, S.K., Skaar, E.P., Gaspar, A.H., Humayun, M., Gornicki, P., Jelenska, J., Joachmiak, A., Missiakas, D.M., and Schneewind, O. (2003). Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906–909. https://doi.org/10.1126/science.1081147.Search in Google Scholar PubMed

Mitra, A., Ko, Y.-H., Cingolani, G., and Niederweis, M. (2019). Heme and hemoglobin utilization by Mycobacterium tuberculosis. Nat. Commun. 10: 4260. https://doi.org/10.1038/s41467-019-12109-5.Search in Google Scholar PubMed PubMed Central

Mitra, A., Speer, A., Lin, K., Ehrt, S., and Niederweis, M. (2017). PPE surface proteins are required for heme utilization by Mycobacterium tuberculosis. mBio 8: e017200–e1816. https://doi.org/10.1128/mbio.01720-16.Search in Google Scholar PubMed PubMed Central

Morgan, W.T., Heng Liem, H., Sutor, R.P., and Muller-Eberhard, U. (1976). Transfer of heme from heme-albumin to hemopexin. Biochim. Biophys. Acta Gen. Subj. 444: 435–445. https://doi.org/10.1016/0304-4165(76)90387-1.Search in Google Scholar PubMed

Mouriño, S., Giardina, B.J., Reyes-Caballero, H., and Wilks, A. (2016). Metabolite-driven regulation of heme uptake by the biliverdin IXβ/δ-selective heme oxygenase (HemO) of Pseudomonas aeruginosa. J. Biol. Chem. 291: 20503–20515. https://doi.org/10.1074/jbc.M116.728527.Search in Google Scholar PubMed PubMed Central

Mouriño, S. and Wilks, A. (2021). Extracellular haem utilization by the opportunistic pathogen Pseudomonas aeruginosa and its role in virulence and pathogenesis. Adv. Microb. Physiol. 79: 89–132.10.1016/bs.ampbs.2021.07.004Search in Google Scholar PubMed PubMed Central

Muller-Eberhard, U. (1970). Hemopexin. N. Engl. J. Med. 283: 1090–1094. https://doi.org/10.1056/nejm197011122832007.Search in Google Scholar

Nielsen, M.J., Petersen, S.V., Jacobsen, C., Thirup, S., Enghild, J.J., Graversen, J.H., and Moestrup, S.K. (2007). A unique loop extension in the serine protease domain of haptoglobin is essential for CD163 recognition of the haptoglobin-hemoglobin complex. J. Biol. Chem. 282: 1072–1079. https://doi.org/10.1074/jbc.m605684200.Search in Google Scholar PubMed

Nobles, C.L. and Maresso, A.W. (2011). The theft of host heme by Gram-positive pathogenic bacteria. Metallomics 3: 788–796. https://doi.org/10.1039/c1mt00047k.Search in Google Scholar PubMed

O’neill, M.J. and Wilks, A. (2013). The P. aeruginosa heme binding protein PhuS is a heme oxygenase Titratable regulator of heme uptake. ACS Chem. Biol. 8: 1794–1802.10.1021/cb400165bSearch in Google Scholar PubMed PubMed Central

Ochsner, U.A., Johnson, Z., and Vasil, M.L. (2000). Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146: 185–198. https://doi.org/10.1099/00221287-146-1-185.Search in Google Scholar PubMed

Otterbein, L.E., Bach, F.H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R.J., Flavell, R.A., and Choi, A.M. (2000). Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6: 422–428. https://doi.org/10.1038/74680.Search in Google Scholar PubMed

Owens, C.P., Chim, N., and Goulding, C.W. (2013a). Insights on how the Mycobacterium tuberculosis heme uptake pathway can be used as a drug target. Future Med. Chem. 5: 1391–1403. https://doi.org/10.4155/fmc.13.109.Search in Google Scholar PubMed PubMed Central

Owens, C.P., Chim, N., Graves, A.B., Harmston, C.A., Iniguez, A., Contreras, H., Liptak, M.D., and Goulding, C.W. (2013b). The Mycobacterium tuberculosis secreted protein Rv0203 transfers heme to membrane proteins MmpL3 and MmpL11. J. Biol. Chem. 288: 21714–21728. https://doi.org/10.1074/jbc.m113.453076.Search in Google Scholar

Owens, C.P., Du, J., Dawson, J.H., and Goulding, C.W. (2012). Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake. Biochemistry 51: 1518–1531. https://doi.org/10.1021/bi2018305.Search in Google Scholar PubMed PubMed Central

Parish, T., Schaeffer, M., Roberts, G., and Duncan, K. (2005). HemZ is essential for heme biosynthesis in Mycobacterium tuberculosis. Tuberculosis 85: 197–204. https://doi.org/10.1016/j.tube.2005.01.002.Search in Google Scholar PubMed

Philippidis, P., Mason, J., Evans, B., Nadra, I., Taylor, K., Haskard, D., and Landis, R. (2004). Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 94: 119–126. https://doi.org/10.1161/01.res.0000109414.78907.f9.Search in Google Scholar PubMed

Quaye, I.K. (2008). Haptoglobin, inflammation and disease. Trans. R. Soc. Trop. Med. Hyg. 102: 735–742. https://doi.org/10.1016/j.trstmh.2008.04.010.Search in Google Scholar PubMed

Runyen-Janecky, L.J. (2013). Role and regulation of heme iron acquisition in Gram-negative pathogens. Front. Cell. Infect. Microbiol. 3: 55. https://doi.org/10.3389/fcimb.2013.00055.Search in Google Scholar PubMed PubMed Central

Severance, S. and Hamza, I. (2009). Trafficking of heme and porphyrins in metazoa. Chem. Rev. 109: 4596–4616. https://doi.org/10.1021/cr9001116.Search in Google Scholar PubMed PubMed Central

Shaver, C.M., Upchurch, C.P., Janz, D.R., Grove, B.S., Putz, N.D., Wickersham, N.E., Dikalov, S.I., Ware, L.B., and Bastarache, J.A. (2016). Cell-free hemoglobin: a novel mediator of acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 310: L532–L541. https://doi.org/10.1152/ajplung.00155.2015.Search in Google Scholar PubMed PubMed Central

Silva, G., Jeney, V., Chora, Â., Larsen, R., Balla, J., and Soares, M.P. (2009). Oxidized hemoglobin is an endogenous proinflammatory agonist that targets vascular endothelial cells. J. Biol. Chem. 284: 29582–29595. https://doi.org/10.1074/jbc.m109.045344.Search in Google Scholar PubMed PubMed Central

Singla, S., Sysol, J.R., Dille, B., Jones, N., Chen, J., and Machado, R.F. (2017). Hemin causes lung microvascular endothelial barrier dysfunction by necroptotic cell death. Am. J. Respir. Cell Mol. Biol. 57: 307–314. https://doi.org/10.1165/rcmb.2016-0287oc.Search in Google Scholar PubMed PubMed Central

Skaar, E.P., Humayun, M., Bae, T., Debord, K.L., and Schneewind, O. (2004). Iron-source preference of Staphylococcus aureus infections. Science 305: 1626–1628. https://doi.org/10.1126/science.1099930.Search in Google Scholar PubMed

Smith, A. and Mcculloh, R.J. (2015). Hemopexin and haptoglobin: allies against heme toxicity from hemoglobin not contenders. Front. Physiol. 6: 187. https://doi.org/10.3389/fphys.2015.00187.Search in Google Scholar PubMed PubMed Central

Smith, A.D. and Wilks, A. (2012). Extracellular heme uptake and the challenges of bacterial cell membranes. Curr. Top. Membr. 69: 359–392. https://doi.org/10.1016/b978-0-12-394390-3.00013-6.Search in Google Scholar

Smith, A.D. and Wilks, A. (2015). Differential contributions of the outer membrane receptors PhuR and HasR to heme acquisition in Pseudomonas aeruginosa. J. Biol. Chem. 290: 7756–7766. https://doi.org/10.1074/jbc.m114.633495.Search in Google Scholar

Soares, M.P. and Bach, F.H. (2009). Heme oxygenase-1: from biology to therapeutic potential. Trends Mol. Med. 15: 50–58. https://doi.org/10.1016/j.molmed.2008.12.004.Search in Google Scholar PubMed

Speziali, C.D., Dale, S.E., Henderson, J.A., Vinés, E.D., and Heinrichs, D.E. (2006). Requirement of Staphylococcus aureus ATP-binding cassette-ATPase FhuC for iron-restricted growth and evidence that it functions with more than one iron transporter. J. Bacteriol. 188: 2048–2055. https://doi.org/10.1128/jb.188.6.2048-2055.2006.Search in Google Scholar PubMed PubMed Central

Spittaels, K.-J., Van Uytfanghe, K., Zouboulis, C.C., Stove, C., Crabbé, A., and Coenye, T. (2021). Porphyrins produced by acneic Cutibacterium acnes strains activate the inflammasome by inducing K+ leakage. iScience 24: 102575. https://doi.org/10.1016/j.isci.2021.102575.Search in Google Scholar PubMed PubMed Central

Stauff, D.L. and Skaar, E.P. (2009). The heme sensor system of Staphylococcus aureus. Contrib. Microbiol. 16: 120–135. https://doi.org/10.1159/000219376.Search in Google Scholar PubMed PubMed Central

Tong, Y. and Guo, M. (2007). Cloning and characterization of a novel periplasmic heme-transport protein from the human pathogen Pseudomonas aeruginosa. J. Biol. Inorg Chem. 12: 735–750. https://doi.org/10.1007/s00775-007-0226-x.Search in Google Scholar PubMed

Torres, V.J., Stauff, D.L., Pishchany, G., Bezbradica, J.S., Gordy, L.E., Iturregui, J., Anderson, K.L., Dunman, P.M., Joyce, S., and Skaar, E.P. (2007). A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1: 109–119. https://doi.org/10.1016/j.chom.2007.03.001.Search in Google Scholar PubMed PubMed Central

Tullius, M.V., Harmston, C.A., Owens, C.P., Chim, N., Morse, R.P., Mcmath, L.M., Iniguez, A., Kimmey, J.M., Sawaya, M.R., Whitelegge, J.P., et al.. (2011). Discovery and characterization of a unique mycobacterial heme acquisition system. Proc. Natl. Acad. Sci. USA 108: 5051–5056. https://doi.org/10.1073/pnas.1009516108.Search in Google Scholar PubMed PubMed Central

Tullius, M.V., Nava, S., and Horwitz, M.A. (2019). PPE37 is essential for Mycobacterium tuberculosis heme-iron acquisition (HIA), and a defective PPE37 in Mycobacterium bovis BCG prevents HIA. Infect. Immun. 87: e005400–e618. https://doi.org/10.1128/IAI.00540-18.Search in Google Scholar PubMed PubMed Central

Verstraete, M.M., Morales, L.D., Kobylarz, M.J., Loutet, S.A., Laakso, H.A., Pinter, T.B., Stillman, M.J., Heinrichs, D.E., and Murphy, M.E.P. (2019). The heme-sensitive regulator SbnI has a bifunctional role in staphyloferrin B production by Staphylococcus aureus. J. Biol. Chem. 294: 11622–11636. https://doi.org/10.1074/jbc.ra119.007757.Search in Google Scholar

Wang, Q., Boshoff, H.I.M., Harrison, J.R., Ray, P.C., Green, S.R., Wyatt, P.G., and Barry, C.E. (2020). PE/PPE proteins mediate nutrient transport across the outer membrane of Mycobacterium tuberculosis. Science 367: 1147–1151. https://doi.org/10.1126/science.aav5912.Search in Google Scholar PubMed

Whitby, P.W., Seale, T.W., Vanwagoner, T.M., Morton, D.J., and Stull, T.L. (2009). The iron/heme regulated genes of Haemophilus influenzae: comparative transcriptional profiling as a tool to define the species core modulon. BMC Genom. 10: 6. https://doi.org/10.1186/1471-2164-10-6.Search in Google Scholar PubMed PubMed Central

Wilson, T., Mouriño, S., and Wilks, A. (2021). The heme-binding protein PhuS transcriptionally regulates the Pseudomonas aeruginosa tandem sRNA prrF1,F2 locus. J. Biol. Chem. 296: 100275. https://doi.org/10.1016/j.jbc.2021.100275.Search in Google Scholar PubMed PubMed Central

Wollenberg, M.S., Claesen, J., Escapa, I.F., Aldridge, K.L., Fischbach, M.A., Lemon, K.P., and Kolter, R. (2014). Propionibacterium produced coproporphyrin III induces Staphylococcus aureus aggregation and biofilm formation. mBio 5: e012866–e1314. https://doi.org/10.1128/mBio.01286-14.Search in Google Scholar PubMed PubMed Central

Yukl, E.T., Jepkorir, G., Alontaga, A.Y., Pautsch, L., Rodriguez, J.C., Rivera, M., and Moënne-Loccoz, P. (2010). Kinetic and spectroscopic studies of hemin acquisition in the hemophore HasAp from Pseudomonas aeruginosa. Biochemistry 49: 6646–6654. https://doi.org/10.1021/bi100692f.Search in Google Scholar PubMed PubMed Central

Zhang, L., Hendrickson, R.C., Meikle, V., Lefkowitz, E.J., Ioerger, T.R., and Niederweis, M. (2020). Comprehensive analysis of iron utilization by Mycobacterium tuberculosis. PLoS Pathog. 16: e1008337. https://doi.org/10.1371/journal.ppat.1008337.Search in Google Scholar PubMed PubMed Central