Hemoglobin and heme scavenging

IUBMB Life

Volumn 57, Issue 11, 2005, Pages 749-759

  Ascenzi, Paolo ^a,b   Bocedi, Alessio ^a   Visca, Paolo ^a,b   Altruda, Fiorella ^c   Tolosano, Emanuela ^c   Beringhelli, Tiziana ^d   Fasano, Mauro ^e  

^a NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

chain hemoglobin stabilizing protein; 1 microglobulin; Albumin; Haptoglobin; Heme; Heme scavenging; Hemoglobin trapping; Hemopexin; Hemophore; High and low density lipoproteins

Indexed keywords

ALPHA 1 MICROGLOBULIN; HEME; HEMOGLOBIN; HEMOGLOBIN ALPHA CHAIN;

ALPHA HELIX; BINDING AFFINITY; CELL LINEAGE; ENDOCYTOSIS; ERYTHROPOIESIS; GENE AMPLIFICATION; GENE EXPRESSION; HEMOLYSIS; HUMAN; LIVER; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW;

ANIMALS; HAPTOGLOBINS; HEME; HEMOGLOBINS; HUMANS; MEMBRANE GLYCOPROTEINS; TRYPSIN INHIBITOR, KUNITZ SOYBEAN;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 28944447412     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1080/15216540500380871     Document Type: Review

References (129)

1. Bunn, H. F., and Forget, B. G. (1986) Hemoglobin: Molecular, Genetic and Clinical Aspects. Saunders, Philadelphia.
2. Perutz, M. F. (1990) Mechanisms regulating the reactions of human hemoglobin with oxygen and carbon monoxide. Annu. Rev. Physiol. 52, 1-25.
3. Brunori, M. (1999) Hemoglobin is an honorary enzyme. Trends Biochem. Sci. 24, 158-161.
4. Gow, A. J., Luchsinger, B. P., Pawloski, J. R., Singel, D. J., and Stamler, J. S. (1999) The oxyhemoglobin reaction of nitric oxide. Proc. Natl. Acad. Sci. USA 96, 9027-9032.
5. Imai, K. (1999) The hemoglobin enzyme. Nature 401, 437-439.
6. McMahon, T. J., Moon, R. E., Luschinger, B. P., Carraway, M. S., Stone, A. E., Stolp, B. W., Gow, A. J., Pawloski, J. R., Watke, P., Singel, D. J., Piantadosi, C. A., and Stamler, J. S. (2002) Nitric oxide in the human respiratory cycle. Nat. Med. 8, 711-717.
7. Fagoonee, S., Gburek, J., Hirsch, E., Marro, S., Moestrup, S. K., Laurberg, J. M., Christensen, E. I., Silengo, L., Altruda, F., and Tolosano, E. (2005) Plasma protein haptoglobin modulates renal iron loading. Am. J. Pathol. 166, 973-983.
8. Rother, R. P., Bell, L., Hillmen, P., and Gladwin, M. T. (2005) The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA 293, 1653-1662.
9. Goswami, T., Rolfs, A., and Hediger, M. A. (2002) Iron transport: emerging roles in health and disease. Biochem. Cell. Biol. 80, 679-689.
10. Baker, H. M., Anderson, B. F., and Baker, E. N. (2003) Dealing with iron: common structural principles in proteins that transport iron and heme. Proc. Natl. Acad. Sci. USA 100, 3579-3583.
11. Kong, Y., Zhou, S., Kihm, A. J., Katein, A. M., Yu, X., Gell, D. A., Mackay, J. P., Adachi, K., Foster-Brown, L., Louden, C. S., Gow, A. J., and Weiss, M. J. (2004) Loss of α-hemoglobin-stabilizing protein impairs erythropoiesis and exacerbates β-thalassemia. J. Clin. Invest. 114, 1457-1466.
12. Smith, A., and Hunt, R. C. (1990) Hemopexin joins transferrin as representative members of a distinct class of receptor-mediated endocytic transport systems. Eur. J. Cell Biol. 53, 234-245.
13. Peters, T., Jr., ed. (1996) All about Albumin: Biochemistry, Genetics and Medical Applications. Academic Press, San Diego and London.
14. Conrad, M. E., Umbreit, J. N., and Moore, E. G. (1999) Iron absorption and transport. Am. J. Med. Sci. 318, 213-229.
15. Miller, Y. I., and Shaklai, N. (1999) Kinetics of hemin distribution in plasma reveals its role in lipoprotein oxidation. Biochim. Biophys. Acta 1454, 153-164.
16. Conrad, M. E., and Umbreit, J. N. (2000) Iron absorption and transport - an update. Am. J. Hematol. 64, 287-298.
17. Delanghe, J. R., and Langlois, M. R. (2001) Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin. Chim. Acta 312, 13-23.
18. Conrad, M. E., and Umbreit, J. N. (2002) Pathways of iron absorption. Blood Cells Mol. Dis. 29, 336-355.
19. Mattu, M., Fasano, M., Spallarossa, A., Bolognesi, M., and Ascenzi, P. (2002) Hemopexin: the primary specific carrier of plasma heme. Biochem. Mol. Biol. Educ. 30, 332-335.
20. Tolosano E., and Altruda F. (2002) Hemopexin: structure, function, and regulation. DNA Cell Biol. 21, 297-306.
21. Ascenzi, P., Bocedi, A., Bolli, A., Fasano, M., Notari, S., and Polticelli, F. (2005) Allosteric modulation of monomeric proteins. Biochem. Mol. Biol. Educ. 33, 169-176.
22. Hvidberg, V., Maniecki, M. B., Jacobsen, C., Hojrup, P., Moller, H. J., and Moestrup, S. K. (2005) Identification of the receptor scavenging hemopexin-heme complexes. Blood 106, 2572-2579.
23. 1- microglobulin by hemoglobin induces heme-binding and heme-degradation properties. Blood 99, 1894-1901.
24. 1-microglobulin in chronic ulcers. J. Invest. Dermatol. 121, 640-646.
25. 1-microglobulin binds heme in different species. Arch. Biochim. Biophys. 432, 196-204.
26. Kihm, A. J., Kong, Y., Hong, W., Russell, J. E., Rouda, S., Adachi, K., Simon, M. C., Blobel, G. A., and Weiss, M. J. (2002) An abundant erythroid protein that stabilizes free α-haemoglobin. Nature 417, 758-763.
27. Feng, L., Gell, D. A., Zhou, S., Gu, L., Kong, Y., Li, J., Hu, M., Yan, N., Lee, C., Rich, A. M., Armstrong, R. S., Lay, P. A., Gow, A. J., Weiss, M. J., Mackay, J. P., and Shi, Y. (2004) Molecular mechanism of AHSP-mediated stabilization of α-hemoglobin. Cell 119, 629-640.
28. Feng, L., Zhou, S., Gu, L., Gell, D. A., Mackay, J. P., Weiss, M. J., Gow, A. J., and Shi, Y. (2005) Structure of oxidized α-haemoglobin bound to AHSP reveals a protective mechanism for haem. Nature 435, 697-701.
29. Lee B. C. (1995) Quelling the red menace: haem capture by bacteria. Mol. Microbiol. 18, 383-390.
30. Braun, V., and Killmann, H. (1999) Bacterial solutions to the iron-supply problem. Trends Biochem. Sci. 24, 104-109.
31. Braun V. (2005) Bacterial iron transport related to virulence. Contrib. Microbiol. 12, 210-233.
32. Wandersman, C., and Stojiljkovic, I. (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr. Opin. Microbiol. 3, 215-220.
33. Genco, C. A., and Dixon, D. W. (2001) Emerging strategies in microbial haem capture. Mol. Microbiol. 39, 1-11.
34. Wandersman C, and Delepelaire P. (2004) Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58, 611-647.
35. Sparling P. F. (1998) Iron and infection. Clin. Infect. Dis. 27, 1367-1368.
36. Rouault, T. A. (2004) Pathogenic bacteria prefer heme. Science 305, 1577-1578.
37. Bullen, J. J., Rogers, H. J., Spalding, P. B., and Ward, C. G. (2005) Iron and infection: the heart of the matter. FEMS Immunol. Med. Microbiol. 43, 325-330.
38. Ganz, T. (2005) Hepcidin. A regulator of intestinal iron absorption and iron recycling by macrophages. Best Pract. Res. Clin. Haematol. 18, 171-182.
39. Wang, Y., Kinzie, E., Berger, F. G., Lim, S. K., and Baumann, H. (2001) Haptoglobin, an inflammation-inducible plasma protein. Redox Rep. 6, 379-385.
40. Ettrich, R., Brandt, W. Jr, Kopecky, V., Baumruk, V., Hofbauerova, K., and Pavlicek, Z. (2002) Study of chaperone-like activity of human haptoglobin: conformational changes under heat shock conditions and localization of interaction sites. Biol. Chem. 383, 1667-1676.
41. Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H. J., Law, S. K., and Moestrup, S. K. (2001) Identification of the haemoglobin scavenger receptor. Nature 409, 198-201.
42. Graversen, J. H., Madsen, M., and Moestrup, S. K. (2002) CD163: a signal receptor scavenging haptoglobin-hemoglobin complexes from plasma. Int. J. Biochem. Cell Biol. 34, 309-414.
43. Philippidis, P., Mason, J. C., Evans, B. J., Nadra, I., Taylor, K. M., Haskard, D. O., and Landis, R. C. (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.
44. Aristoteli, L. P., Moller, H. J., Bailey, B., Moestrup, S. K., and Kritharides, L. (2005) The monocytic lineage specific soluble CD163 is a plasma marker of coronary atherosclerosis. Atherosclerosis, in press.
45. Kino, K., Tsunoo, H., Higa, Y., Takami, M., and Nakajima, H. (1982) Kinetic aspects of hemoglobin.haptoglobin-receptor interaction in rat liver plasma membranes, isolated liver cells, and liver cells in primary culture. J. Biol. Chem. 257, 4828-4833.
46. Oshiro, S., and Nakajima, H. (1988) Intrahepatocellular site of the catabolism of heme and globin moiety of hemoglobin-haptoglobin after intravenous administration to rats. J. Biol. Chem. 263, 16032-16038.
47. Okuda, M., Tokunaga, R., and Taketani, S. (1992) Expression of haptoglobin receptors in human hepatoma cells. Biochim. Biophys. Acta 1136, 143-149.
48. Oshiro, S., Yajima, Y., Kawamura, K., Kubota, M., Yokofujita, J., Nishibe, Y., Takahama, M., and Nakajima, H. (1992) Catabolism of hemoglobin-haptoglobin complex in microsome subfractions. Chem. Pharm. Bull. (Tokyo) 40, 1847-1851.
49. Zuwala-Jagiello, J., and Osada, J. (1998) Internalization study using EDTA-prepared hepatocytes for receptor-mediated endocytosis of haemoglobin-haptoglobin. Int. J. Biochem. Cell Biol. 30, 923-931.
50. Lim, S. K., Kim, H., bin Ali, A., Lim, Y. K., Wang, Y., Chong, S. M., Costantini, F., and Baumman, H. (1998) Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 92, 1870-1877.
51. Lim, Y. K., Jenner, A., bin Ali, A., Wang, Y., Hsu, S. I., Chong, S. M., Baumman, H., Halliwell, B., and Lim, S. K. (2000) Haptoglobin reduces renal oxidative DNA and tissue damage during phenylhydrazine-induced hemolysis. Kidney Int. 58, 1033-1044.
52. Christensen, E. I., and Birn, H. (2002) Megalin and cubilin: multifunctional endocytic receptors. Nat. Rev. Mol. Cell Biol. 3, 256-266.
53. Gburek, J., Verroust, P. J., Willnow, T. E., Fyfe, J. C., Nowacki, W., Jacobsen, C., Moestrup, S. K., and Christensen, E. I. (2002) Megalin and cubilin are endocytic receptors involved in renal clearance of hemoglobin. J. Am. Soc. Nephrol. 13, 423-430.
54. Garby, L., and Noyes, W. D. (1959) Studies on hemoglobin metabolism. I. The kinetic properties of the plasma hemoglobin pool in normal man. J. Clin. Invest. 38, 1479-1483.
55. Tolosano, E., Fagoonee, S., Garuti, C., Valli, L., Andrews, N. C., Altruda, F., and Pietrangelo, A. (2005) Haptoglobin modifies the hemochromatosis phenotype in mice. Blood 105, 3353-3355.
56. Gell, D., Kong, Y., Eaton, S. A., Weiss, M. J., and Mackay, J. P. (2002) Biophysical characterization of the α-globin binding protein α-hemoglobin stabilizing protein. J. Biol. Chem. 277, 40602-40609.
57. Santiveri, C. M., Perez-Canadillas, J. M., Vadivelu, M. K., Allen, M. D., Rutherford, T. J., Watkins, N. A., and Bycroft, M. (2004) NMR structure of the α-hemoglobin stabilizing protein: insights into conformational heterogeneity and binding. J. Biol. Chem. 279, 34963-34970.
58. Everse J., and Hsia, N. (1997) The toxicities of native and modified hemoglobins. Free Radic. Biol. Med. 22, 1075-1099.
59. Wagener, F. A., Abraham, N. G., van Kooyk, Y., de Witte, T., and Figdor, C. G. (2001) Heme-induced cell adhesion in the pathogenesis of sickle-cell disease and inflammation. Trends Pharmacol. Sci. 22, 52-54.
60. Grinshtein, N., Bamm, V. V., Tsemakhovich, V. A., and Shaklai, N. (2003) Mechanism of low-density lipoprotein oxidation by hemoglobin-derived iron. Biochemistry 42, 6977-6985.
61. Carter, D. C., and Ho, J. X. (1994) Structure of serum albumin. Adv. Protein Chem. 45, 153-203.
62. Curry, S. (2002) Beyond expansion: structural studies on the transport roles of human serum albumin. Vox Sang. 83 (Suppl. 1), 315-319.
63. He, X., and Carter, D. C. (1992) Atomic structure and chemistry of human serum albumin. Nature 358, 209-215.
64. Curry, S., Mandelkow, H., Brick, P., and Franks, N. (1998) Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nat. Struct. Biol. 5, 827-835.
65. Sugio, S., Kashima, A., Mochizuki, S., Noda, M., and Kobayashi, K. (1999) Crystal structure of human serum albumin at 2.5 Å resolution. Protein Eng. 12, 439-446.
66. Bhattacharya, A. A., Grüne, T., and Curry, S. (2000) Crystallographic analysis reveals common modes of binding of medium and long chain fatty acids to human serum albumin. J. Mol. Biol. 303, 721-732.
67. Ghuman, J., Zunszain, P. A., Petitpas, I., Bhattacharya, A. A., Otagiri, M., and Curry, S. (2005) Structural basis of the drug-binding specificity of human serum albumin. J. Mol. Biol. 353, 38-52.
68. Wardell, M., Wang, Z., Ho, J. X., Robert, J., Rüker, F., Ruble, J., and Carter, D. C. (2002) The atomic structure of human methemalbumin at 1.9 Å. Biochem. Biophys. Res. Commun. 291, 813-819.
69. Zunszain, P. A., Ghuman, J., Komatsu, T., Tsuchida, E., and Curry, S. (2003) Crystal structural analysis of human serum albumin complexed with hemin and fatty acid. BMC Struct. Biol. 3, 6.
70. Petitpas, I., Bhattacharya, A. A., Twine, S., East, M., and Curry, S. (2001) Crystal structure analysis of warfarin binding to human serum albumin: anatomy of drug site I. J. Biol. Chem. 276, 22804-22809.
71. Chuang, V. T. G., and Otagiri, M. (2002) How do fatty acids cause allosteric binding of drugs to human serum albumin? Pharm. Res. 19, 1458-1464.
72. Fanali, G., Fesce, R., Agrati, C., Ascenzi, P., and Fasano, M. (2005) Allosteric modulation of myristate and Mn(III)heme binding to human serum albumin - Optical and NMR spectroscopy characterization. FEBS J. 272, 4672-4683.
73. Baroni, S., Mattu, M., Vannini, A., Cipollone, R., Aime, S., Ascenzi, P., and Fasano, M. (2001) Effect of ibuprofen and warfarin on the allosteric properties of haem-human serum albumin. A spectroscopic study. Eur. J. Biochem. 268, 6214-6220.
74. Ascenzi, P., Bocedi, A., Notari, S., Menegatti, E., and Fasano, M. (2005) Heme impairs allosterically drug binding to human serum albumin Sudlow's site I. Biochem. Biophys. Res. Commun. 334, 481-486.
75. Bocedi, A., Notari, S., Narciso, P., Bolli, A., Fasano, M., and Ascenzi, P. (2004) Binding of anti-HIV drugs to human serum albumin. IUBMB Life 56, 609-614.
76. Paoli, M., Anderson, B. F., Baker, H. M., Morgan, W. T., Smith, A., and Baker, E. N. (1999) Crystal structure of hemopexin reveals a novel high-affinity heme site formed between two β-propeller domains. Nat. Struct. Biol. 6, 926-931.
77. Morgan, W. T., and Smith, A. (1984) Domain structure of rabbit hemopexin: isolation and characterization of a heme-binding glycopeptide. J. Biol. Chem. 259, 12001-12006.
78. Morgan, W. T., Muster, P., Tatum, F., Kao, S. M., Alam, J., and Smith, A. (1993) Identification of the histidine residues of hemopexin that coordinate with heme-iron and of a receptor-binding region. J. Biol. Chem. 268, 6256-6262.
79. Shipulina, N., Hunt, R. C., Shaklai, N., and Smith, A. (1998) Coordination of nitric oxide by heme-hemopexin. J. Protein Chem. 17, 255-260.
80. Shipulina, N. V., Smith, A., and Morgan, W.T. (2001) Effects of reduction and ligation of heme iron on the thermal stability of heme-hemopexin complexes. J. Protein Chem. 20, 145-154.
81. Fasano, M., Bocedi, A., Mattu, M., Coletta, M., and Ascenzi, P. (2004) Nitrosylation of rabbit ferrous heme-hemopexin. J. Biol. Inorg. Chem. 9, 800-806.
82. Mauk, M. R., Rosell, F. I., Lelj-Garolla, B., Moore, G. R., and Mauk, A. G. (2005) Metal ion binding to human hemopexin. Biochemistry 44, 1864-1871.
83. Rosell, F. I., Mauk, M. R., and Mauk, A.G. (2005) pH- and metal ion-linked stability of the hemopexin-heme complex. Biochemistry 44, 1872-1879.
84. Shaklai, N., Sharma, V. S., Muller-Eberhard, U., and Morgan, W. T. (1981) The interaction of heme-hemopexin with CO. J. Biol. Chem. 256, 1544-1548.
85. Kharitonov, V. G., Sharma, V. S., Magde, D., and Koesling, D. (1997) Kinetics of nitric oxide dissociation from five- and six-coordinate nitrosyl hemes and heme proteins, including soluble guanylate cyclase. Biochemistry 36, 6814-6818.
86. Carter, D. C., Ho, J. X., and Rüker, F. (1999) Oxygen-transporting albumin-based blood replacement composition and blood volume expander. U.S. Pat. No. 5,948,609.
87. 2 binding to human serum albumin-heme hybrid. Bioconjug. Chem. 11, 772-776.
88. Komatsu, T., Matsukawa, Y., and Tsuchida, E. (2001) Reaction of nitric oxide with synthetic hemoprotein, human serum albumin incorporating tetraphenylporphinatoiron(II) derivatives. Bioconjug. Chem. 12, 71-75.
89. Monzani, E., Bonafè, B., Fallarini, A., Redaelli, C., Casella, L., Minchiotti, L., and Galliano, M. (2001) Enzymatic properties of hemalbumin. Biochim. Biophys. Acta 1547, 302-312.
90. Fasano, M., Mattu, M., Coletta, M., and Ascenzi, P. (2002) The heme-iron geometry of ferrous nitrosylated heme-serum lipoproteins, hemopexin, and albumin: a comparative EPR study. J. Inorg. Biochem. 91, 487-490.
91. Komatsu, T., Ohmichi, N., Patricia, A., Zunszain, P.A., Curry, S., and Tsuchida, E. (2004) Dioxygenation of human serum albumin having a prosthetic heme group in a tailor-made heme pocket. J. Am. Chem. Soc. 126, 14304-14305.
92. Antonini, E., Ascenzi, P., Bolognesi, M., Menegatti, E., and Guarneri, M. (1983) Transient removal of proflavine inhibition of bovine β-trypsin by the bovine basic pancreatic trypsin inhibitor (Kunitz). A case for "chronosteric effects". J. Biol. Chem. 258, 4676-4678.
93. 1-glycoprotein of low molecular weight: isolation and some properties. Biochem. Biophys. Res. Commun. 65, 1427-1433.
94. 1-microglobulin: purification procedure, chemical and physicochemical properties. J. Biol. Chem. 252, 8048-8057.
95. Pervaiz, S., and Brew, K. (1985) Homology of β-lactoglobulin, serum retinol-binding protein, and protein HC. Science 228, 335-337.
96. 1-microglobulin. Trends Biochem. Sci. 15, 240-243.
97. Åkerström, B., Flower, D. R., and Salier, J.-P. (2000) Lipocalins: unity in diversity. Biochim. Biophys. Acta 1482, 1-8.
98. Flower, D. R., North, A. C. T., and Sansom, C. E. (2000) The lipocalin protein family: structural and sequence overview. Biochim. Biophys. Acta 1482, 9-24.
99. Qin, B. Y., Bewley, M. C., Creamer, L. K., Baker, H. M., Baker, E. N., and Jameson, G. B. (1998) Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry 37, 14014-14023.
100. Skerra A. (2000) Lipocalins as a scaffold. Biochim. Biophys. Acta 1482, 337-350.
101. Ragona, L., Fogolari, F., Catalano, M., Ugolini, R., Zetta, L., and Molinari, H. (2003) EF loop conformational change triggers ligand binding in β-lactoglobulins. J. Biol. Chem. 278, 38840-38846.
102. a calculations. Proteins 54, 744-758.
103. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2004) Interstrand loops CD and EF act as pH-dependent gates to regulate fatty acid ligand binding in tear lipocalin. Biochemistry 43, 12894-12904.
104. 1-microglobulin chromophores are located to three lysine residues semiburied in the lipocalin pocket and associated with a novel lipophilic compound. Protein Sci. 8, 2611-2620.
105. 1- microglobulin is covalently bound to kynurenine-derived chromophores. J. Biol. Chem. 279, 51033-51041.
106. Montfort, W. R., Weichsel, A., and Andersen, J. F. (2000) Nitrophorins and related antihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods. Biochim. Biophys. Acta 1482, 110-118.
107. Ascenzi, P., Nardini., M., Bolognesi, M., and Montfort, W. R. (2002) Nitrophorins. Lipocalins-based heme proteins transporting nitric oxide. Biochem. Mol. Biol. Educ. 30, 68-71.
108. Faraldo-Gomez, J. D., and Sansom, M. S. (2003) Acquisition of siderophores in gram-negative bacteria. Nat. Rev. Mol. Cell Biol. 4, 105-116.
109. Perkins-Balding, D., Ratliff-Griffin, M., and Stojiljkovic, I. (2004) Iron transport systems in Neisseria meningitidis. Microbiol. Mol. Biol. Rev. 68, 154-171.
110. Létoffé, S., Ghigo, J. M., and Wandersman, C. (1994) Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc. Natl. Acad. Sci. USA 91, 9876-9880.
111. Izadi, N., Henry, Y., Haladjian, J., Goldberg, M. E., Wandersman, C., Delepierre, M., and Lecroisey, A. (1997) Purification and characterization of an extracellular heme-binding protein, HasA, involved in heme iron acquisition. Biochemistry 36, 7050-7057.
112. Clarke, T. E., Tari, L. W., and Vogel, H. J. (2001) Structural biology of bacterial iron uptake systems. Curr. Top. Med. Chem. 1, 7-30.
113. Létoffé, S., Nato, F., Goldberg, M. E., and Wandersman, C. (1999) Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33, 546-555.
114. Létoffé, S., Debarbieux, L., Izadi, N., Delepelaire, P., and Wandersman, C. (2003) Ligand delivery by haem carrier proteins: the binding of Serratia marcescens haemophore to its outer membrane receptor is mediated by two distinct peptide regions. Mol. Microbiol. 50, 77-88.
115. Létoffé, S., Delepelaire, P., and Wandersman, C. (2004) Free and hemophore-bound heme acquisitions through the outer membrane receptor HasR have different requirements for the TonB-ExbB-ExbD complex. J. Bacteriol. 186, 4067-4074.
116. Arnoux, P., Haser, R., Izadi, N., Lecroisey, A., Delepierre, M., Wandersman, C., and Czjzek, M. (1999) The crystal structure of HasA, a hemophore secreted by Serratia marcescens. Nat. Struct. Biol. 6, 516-520.
117. Létoffé, S. Ghigo, J. M., and Wandersman, C. (1994) Secretion of the Serratia marcescens HasA protein by an ABC transporter. J. Bacteriol. 176, 5372-5377.
118. Delepelaire, P., and Wandersman, C. (1998) The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. EMBO J. 17, 936-944.
119. Debarbieux, L., and Wandersman, C. (2001) Folded HasA inhibits its own secretion through its ABC exporter. EMBO J. 20, 4657-4663.
120. Sapriel, G., Wandersman, C., and Delepelaire, P. (2003) The SecB chaperone is bifunctional in Serratia marcescens: SecB is involved in the Sec pathway and required for HasA secretion by the ABC transporter. J. Bacteriol. 185, 80-88.
121. Davidson, A. L., and Chen, J. (2004) ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73, 241-268.
122. Létoffé, S., Wecker, K., Delepierre, M., Delepelaire, P., and Wandersman, C. (2005) Activities of the Serratia marcescens heme receptor HasR and isolated plug and β-barrel domains: the β-barrel forms a heme-specific channel. J. Bacteriol. 187, 4637-4645.
123. Rossi, M. S., Paquelin, A., Ghigo, J. M., and Wandersman, C. (2003) Haemophore-mediated signal transduction across the bacterial cell envelope in Serratia marcescens: the inducer and the transported substrate are different molecules. Mol. Microbiol. 48, 1467-1480.
124. Biville, F., Cwerman, H., Letoffe, S., Rossi, M. S., Drouet, V., Ghigo, J. M., and Wandersman, C. (2004) Haemophore-mediated signalling in Serratia marcescens: a new mode of regulation for an extra cytoplasmic function (ECF) sigma factor involved in haem acquisition. Mol. Microbiol. 53, 1267-1277.
125. Lund, O., Nielsen, M., Lundegaard, C., and Worning, P. (2002) CPHmodels 2.0: X3M a Computer Program to Extract 3D Models. CASP5 Conference, A102.
126. Budayova-Spano, M., Lacroix, M., Thielens, N. M., Arlaud, G. J., Fontecilla-Camps, J. C., and Gaboriaud, C. (2002) The crystal structure of the zymogen catalytic domain of complement protease C1r reveals that a disruptive mechanical stress is required to trigger activation of the C1 complex. EMBO J. 21, 231-239.
127. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723.
128. Roberts, S. A., Weichsel, A., Qiu, Y., Shelnutt, J. A., Walker, F. A., and Montfort, W. R. (2001) Ligand-induced heme ruffling and bent NO geometry in ultra-high-resolution structures of nitrophorin 4. Biochemistry 40, 11327-11337.
129. Ortlund, E., Parker, C. L., Schreck, S. F., Ginell, S., Minor, W., Sodetz, J. M., and Lebioda, L. (2002) Crystal structure of human complement protein C8γ at 1.2 Å resolution reveals a lipocalin fold and a distinct ligand binding site. Biochemistry 41, 7030-7037.