Heme utilization in the Caenorhabditis elegans hypodermal cells is facilitated by heme-responsive gene-2

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 9601-9612

  Chen, Caiyong ^a   Samuel, Tamika K ^a   Krause, Michael ^b   Dailey, Harry A ^c   Hamza, Iqbal ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL PLASMA MEMBRANE; CAENORHABDITIS ELEGANS; ENDOPLASMIC RETICULUM; HYPODERMAL CELLS; MEMBRANE PROTEINS; MRNA EXPRESSION; SECRETED PROTEIN; SUBMICROMOLAR CONCENTRATIONS; TRANS-MEMBRANE PROTEINS; YEAST STRAIN;

CELL MEMBRANES; GENES; PHYSIOLOGY; TISSUE;

PORPHYRINS;

CYTOCHROME; HEME; HEME RESPONSIVE GENE 2 PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGUS GROWTH; GENE; GENE EXPRESSION REGULATION; HEME DEFICIENCY; HRG2 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; UPREGULATION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; HEME; HEMEPROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SUBCUTANEOUS TISSUE;

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 84863385084     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.307694     Document Type: Article

References (59)

1. Olea, C., Jr., Kuriyan, J., and Marletta, M. A. (2010) Modulating heme redox potential through protein-induced porphyrin distortion. J. Am. Chem. Soc. 132, 12794-12795
2. Severance, S., and Hamza, I. (2009) Trafficking of heme and porphyrins in metazoa. Chem. Rev. 109, 4596-4616
3. Schultz, I. J., Chen, C., Paw, B. H., and Hamza, I. (2010) Iron and porphyrin trafficking in heme biogenesis. J. Biol. Chem. 285, 26753-26759
4. Balla, G., Vercellotti, G. M., Muller-Eberhard, U., Eaton, J., and Jacob, H. S. (1991) Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab. Invest. 64, 648-655
5. Jeney, V., Balla, J., Yachie, A., Varga, Z., Vercellotti, G. M., Eaton, J. W., and Balla, G. (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100, 879-887 (Pubitemid 34832613)
6. Rajagopal, A., Rao, A. U., Amigo, J., Tian, M., Upadhyay, S. K., Hall, C., Uhm, S., Mathew, M. K., Fleming, M. D., Paw, B. H., Krause, M., and Hamza, I. (2008) Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins. Nature 453, 1127-1131 (Pubitemid 351871730)
7. Yuan, X., Protchenko, O., Philpott, C. C., and Hamza, I. (2012) Topologically conserved residues direct heme transport in HRG-1-related proteins. J. Biol. Chem. 287, 4914-4924
8. Keel, S. B., Doty, R. T., Yang, Z., Quigley, J. G., Chen, J., Knoblaugh, S., Kingsley, P. D., De Domenico, I., Vaughn, M. B., Kaplan, J., Palis, J., and Abkowitz, J. L. (2008) A heme export protein is required for red blood cell differentiation and iron homeostasis. Science 319, 825-828 (Pubitemid 351225875)
9. Quigley, J. G., Yang, Z., Worthington, M. T., Phillips, J. D., Sabo, K. M., Sabath, D. E., Berg, C. L., Sassa, S., Wood, B. L., and Abkowitz, J. L. (2004) Identification of a human heme exporter that is essential for erythropoiesis. Cell 118, 757-766 (Pubitemid 39221734)
10. Hrkal, Z., Vodrázka, Z., and Kalousek, I. (1974) Transfer of heme from ferrihemoglobin and ferrihemoglobin-isolated chains to hemopexin. Eur. J. Biochem. 43, 73-78
11. Yang, Z., Philips, J. D., Doty, R. T., Giraudi, P., Ostrow, J. D., Tiribelli, C., Smith, A., and Abkowitz, J. L. (2010) Kinetics and specificity of feline leukemia virus subgroup C receptor (FLVCR) export function and its dependence on hemopexin. J. Biol. Chem. 285, 28874-28882
12. Taketani, S., Adachi, Y., Kohno, H., Ikehara, S., Tokunaga, R., and Ishii, T. (1998) Molecular characterization of a newly identified heme-binding protein induced during differentiation of urine erythroleukemia cells. J. Biol. Chem. 273, 31388-31394 (Pubitemid 28533157)
13. Iwahara, S., Satoh, H., Song, D. X., Webb, J., Burlingame, A. L., Nagae, Y., and Muller-Eberhard, U. (1995) Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol. Biochemistry 34, 13398-13406
14. Harvey, J. W., and Beutler, E. (1982) Binding of heme by glutathione S-transferase: a possible role of the erythrocyte enzyme. Blood 60, 1227-1230 (Pubitemid 13242308)
15. Tipping, E., Ketterer, B., Christodoulides, L., and Enderby, G. (1976) The interactions of haem with ligandin and aminoazo-dye-binding protein A. Biochem. J. 157, 461-467
16. van Rossum, A. J., Jefferies, J. R., Rijsewijk, F. A., LaCourse, E. J., Teesdale-Spittle, P., Barrett, J., Tait, A., and Brophy, P. M. (2004) Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infect. Immun. 72, 2780-2790 (Pubitemid 38542406)
17. Rao, A. U., Carta, L. K., Lesuisse, E., and Hamza, I. (2005) Lack of heme synthesis in a free-living eukaryote. Proc. Natl. Acad. Sci. U.S.A. 102, 4270-4275 (Pubitemid 40397101)
18. Chen, C., Samuel, T. K., Sinclair, J., Dailey, H. A., and Hamza, I. (2011) An intercellular heme-trafficking protein delivers maternal heme to the embryo during development in C. elegans. Cell 145, 720-731
19. Epstein, H. F., and Shakes, D. C. (eds) (1995) Caenorhabditis elegans: Modern Biological Analysis of an Organism, Vol. 48, Academic Press, San Diego
20. Nass, R., and Hamza, I. (2007) The nematode C. elegans as an animal model to explore toxicology in vivo: solid and axenic growth culture conditions and compound exposure parameters in Current Protocols in Toxicology (Costa, L. G., Hodgson, E., Lawrence, D. A., and Reed, D. J., eds) pp. 1.9.1-1.9.18, John Wiley & Sons, Inc., Somerset, NJ
21. Gengyo-Ando, K., and Mitani, S. (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 269, 64-69 (Pubitemid 30440255)
22. Praitis, V., Casey, E., Collar, D., and Austin, J. (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226 (Pubitemid 32225014)
23. Lorenz, H., Hailey, D. W., and Lippincott-Schwartz, J. (2006) Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210
24. Zhu, Y., Hon, T., Ye, W., and Zhang, L. (2002) Heme deficiency interferes with the Ras-mitogen-activated protein kinase signaling pathway and expression of a subset of neuronal genes. Cell Growth Differ. 13, 431-439
25. Crisp, R. J., Pollington, A., Galea, C., Jaron, S., Yamaguchi-Iwai, Y., and Kaplan, J. (2003) Inhibition of heme biosynthesis prevents transcription of iron uptake genes in yeast. J. Biol. Chem. 278, 45499-45506 (Pubitemid 37432689)
26. Smith, K. M. (1975) Porphyrins and Metalloporphyrins, Elsevier Scientific Publishing Co., New York
27. Rieske, J. S. (1967) The quantitative determination of mitochondrial hemoproteins. Methods Enzymol. 488-493
28. Bjellqvist, B., Basse, B., Olsen, E., and Celis, J. E. (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15, 529-539 (Pubitemid 24151853)
29. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (Pubitemid 24354800)
30. Saitou, N., and Neil, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
31. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software, version 4.0. Mol. Biol. Evol. 24, 1596-1599 (Pubitemid 47236692)
32. Severance, S., Rajagopal, A., Rao, A. U., Cerqueira, G. C., Mitreva, M., El-Sayed, N. M., Krause, M., and Hamza, I. (2010) Genome-wide analysis reveals novel genes essential for heme homeostasis in Caenorhabditis elegans. PLoS Genet. 6, e1001044
33. Cui, Y., McBride, S. J., Boyd, W. A., Alper, S., and Freedman, J. H. (2007) Toxicogenomic analysis of Caenorhabditis elegans reveals novel genes and pathways involved in the resistance to cadmium toxicity. Genome Biol. 8, R122
34. Dong, J., Song, M. O., and Freedman, J. H. (2005) Identification and characterization of a family of Caenorhabditis elegans genes that is homologous to the cadmium-responsive gene cdr-1. Biochim. Biophys. Acta 1727, 16-26 (Pubitemid 40093499)
35. Blumenthal, T., Evans, D., Link, C. D., Guffanti, A., Lawson, D., Thierry-Mieg, J., Thierry-Mieg, D., Chiu, W. L., Duke, K., Kiraly, M., and Kim, S. K. (2002) A global analysis of Caenorhabditis elegans operons. Nature 417, 851-854 (Pubitemid 34670331)
36. Cox, E. A., and Hardin, J. (2004) Sticky worms: adhesion complexes in C. elegans. J. Cell Sci. 117, 1885-1897 (Pubitemid 38745123)
37. Rolls, M. M., Hall, D. H., Victor, M., Stelzer, E. H., and Rapoport, T. A. (2002) Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. Cell 13, 1778-1791 (Pubitemid 34522655)
38. Neve, E. P., and Ingelman-Sundberg, M. (2008) Intracellular transport and localization of microsomal cytochrome P450. Anal. Bioanal. Chem. 392, 1075-1084
39. Zhan, B., Liu, S., Perally, S., Xue, J., Fujiwara, R., Brophy, P., Xiao, S., Liu, Y., Feng, J., Williamson, A., Wang, Y., Bueno, L. L., Mendez, S., Goud, G., Bethony, J. M., Hawdon, J. M., Loukas, A., Jones, K., and Hotez, P. J. (2005) Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect. Immun. 73, 6903-6911 (Pubitemid 41368859)
40. Protchenko, O., Shakoury-Elizeh, M., Keane, P., Storey, J., Androphy, R., and Philpott, C. C. (2008) Role of PUG1 in inducible porphyrin and heme transport in Saccharomyces cerevisiae. Eukaryot. Cell 7, 859-871 (Pubitemid 351968829)
41. Myers, A. M., Pape, L. K., and Tzagoloff, A. (1985) Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 4, 2087-2092
42. Dorfman, B. Z. (1969) The isolation of adenylosuccinate synthetase mutants in yeast by selection for constitutive behavior in pigmented strains. Genetics 61, 377-389
43. Shadel, G. S. (1999) Yeast as a model for human mDNA replication. Am. J. Hum. Genet. 65, 1230-1237
44. Kim, B. E., Wang, F., Dufner-Beattie, J., Andrews, G. K., Eide, D. J., and Petris, M. J. (2004) Zn2+-stimulated endocytosis of the mZIP4 zinc transporter regulates its location at the plasma membrane. J. Biol. Chem. 279, 4523-4530 (Pubitemid 38199043)
45. Wu, M. M., Llopis, J., Adams, S., McCaffery, J. M., Kulomaa, M. S., Machen, T. E., Moore, H. P., and Tsien, R. Y. (2000) Organelle pH studies using targeted avidin and fluorescein-biotin. Chem. Biol. 7, 197-209 (Pubitemid 30147204)
46. Dong, J., Boyd, W. A., and Freedman, J. H. (2008) Molecular characterization of two homologs of the Caenorhabditis elegans cadmium-responsive gene cdr-1: cdr-4 and cdr-6. J. Mol. Biol. 376, 621-633
47. Liao, V. H., Dong, J., and Freedman, J. H. (2002) Molecular characterization of a novel, cadmium-inducible gene from the nematode Caenorhabditis elegans. A new gene that contributes to the resistance to cadmium toxicity. J. Biol. Chem. 277, 42049-42059 (Pubitemid 35257519)
48. Hill, K. K., Bedian, V., Juang, J. L., and Hoffmann, F. M. (1995) Genetic interactions between the Drosophila Abelson (Abl) tyrosine kinase and failed axon connections (Fax), a novel protein in axon bundles. Genetics 141, 595-606
49. McKie, A. T., Marciani, P., Rolfs, A., Brennan, K., Wehr, K., Barrow, D., Miret, S., Bomford, A., Peters, T. J., Farzaneh, F., Hediger, M. A., Hentze, M. W., and Simpson, R. J. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 5, 299-309 (Pubitemid 30628088)
50. Ohgami, R. S., Campagna, D. R., Greer, E. L., Antiochos, B., McDonald, A., Chen, J., Sharp, J. J., Fujiwara, Y., Barker, J. E., and Fleming, M. D. (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat. Genet. 37, 1264-1269 (Pubitemid 41568711)
51. Nicholson, D. W., and Neupert, W. (1989) Import of cytochrome c into mitochondria: reduction of heme, mediated by NADH and flavin nucleotides, is obligatory for its covalent linkage to apocytochrome c. Proc. Natl. Acad. Sci. U.S.A. 86, 4340-4344 (Pubitemid 19164550)
52. Richard-Fogal, C. L., Frawley, E. R., Bonner, E. R., Zhu, H., San Francisco, B., and Kranz, R. G. (2009) A conserved haem redox and trafficking pathway for cofactor attachment. EMBO J. 28, 2349-2359
53. Allhorn, M., Klapyta, A., and Akerström, B. (2005) Redox properties of the lipocalin α1-microglobulin: reduction of cytochrome c, hemoglobin, and free iron. Free Radic. Biol. Med. 38, 557-567 (Pubitemid 40416851)
54. Nauseef, W. M., McCormick, S., and Yi, H. (1992) Roles of heme insertion and the mannose 6-phosphate receptor in processing of the human myeloid lysosomal enzyme, myeloperoxidase. Blood 80, 2622-2633
55. Harwaldt, P., Rahlfs, S., and Becker, K. (2002) Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol. Chem. 383, 821-830 (Pubitemid 34649901)
56. Hughes, A. L., Powell, D. W., Bard, M., Eckstein, J., Barbuch, R., Link, A. J., and Espenshade, P. J. (2007) Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes. Cell Metab. 5, 143-149 (Pubitemid 46172917)
57. Mallory, J. C., Crudden, G., Johnson, B. L., Mo, C., Pierson, C. A., Bard, M., and Craven, R. J. (2005) Dap1p, a heme-binding protein that regulates the cytochrome P450 protein Erg11p/Cyp51p in Saccharomyces cerevisiae. Mol. Cell. Biol. 25, 1669-1679 (Pubitemid 40280136)
58. C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018
59. Labouesse, M. (2006) Epithelial junctions and attachments. WormBook, doi/10.1895/wormbook.1.56.1