The Fowler syndrome-associated protein FLVCR2 is an importer of heme

Molecular and Cellular Biology

Volumn 30, Issue 22, 2010, Pages 5318-5324

  Duffy, Simon P ^a,b   Shing, Jennifer ^a   Saraon, Punit ^a   Berger, Lloyd C ^b   Eiden, Maribeth V ^c   Wilde, Andrew ^b   Tailor, Chetankumar S ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAROSE; CELL SURFACE PROTEIN; ENVELOPE PROTEIN; HEME; HEMIN; PROTEIN FLVCR2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING COMPETITION; BLOOD TOXICITY; BONE MARROW; BRAIN TISSUE; CELL FUNCTION; CELL TRANSPORT; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FETUS; FETUS LIVER; FOWLER SYNDROME; HEMATOPOIETIC TISSUE; HUMAN; HUMAN TISSUE; KIDNEY PARENCHYMA; LEUKOCYTE; LIVER; LYMPH NODE; MAMMAL CELL; NONHUMAN; OOCYTE; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; SPLEEN; THYMUS; TRANSPORT KINETICS; VASCULAR DISEASE; XENOPUS LAEVIS;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN DISEASES; CATS; CELL LINE; CRICETINAE; CRICETULUS; FEMALE; HEME; HUMANS; MEMBRANE TRANSPORT PROTEINS; OOCYTES; PREGNANCY; RECEPTORS, VIRUS; RNA, SMALL INTERFERING; SYNDROME; TISSUE DISTRIBUTION; XENOPUS LAEVIS;

FELINE LEUKEMIA VIRUS; MAMMALIA; XENOPUS LAEVIS;

EID: 78649568177     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00690-10     Document Type: Article

References (49)

1. Abkowitz, J. L., R. D. Holly, and C. K. Grant. 1987. Retrovirus-induced feline pure red cell aplasia. Hematopoietic progenitors are infected with feline leukemia virus and erythroid burst-forming cells are uniquely sensitive to heterologous complement. J. Clin. Invest. 80:1056-1063.
2. Atamna, H., J. Liu, and B. N. Ames. 2001. Heme deficiency selectively interrupts assembly of mitochondrial complex IV in human fibroblasts: relevance to aging. J. Biol. Chem. 276:48410-48416.
3. Ball, S. E., C. P. McGuckin, G. Jenkins, and E. C. Gordon-Smith. 1996. Diamond-Blackfan anaemia in the U.K.: analysis of 80 cases from a 20-year birth cohort. Br. J. Haematol. 94:645-653.
4. Bodmer, D., M. Eleveld, E. Kater-Baats, I. Janssen, B. Janssen, M. Weterman, E. Schoenmakers, M. Nickerson, M. Linehan, B. Zbar, and A. G. van Kessel. 2002. Disruption of a novel MFS transporter gene, DIRC2, by a familial renal cell carcinoma-associated t(2;3)(q35;q21). Hum. Mol. Genet. 11:641-649.
5. Boomer, S., M. Eiden, C. C. Burns, and J. Overbaugh. 1997. Three distinct envelope domains, variably present in subgroup B feline leukemia virus recombinants, mediate Pit1 and Pit2 receptor recognition. J. Virol. 71:8116-8123.
6. Brasier, G., C. Tikellis, L. Xuereb, J. Craigie, D. Casley, C. S. Kovacs, N. J. Fudge, R. Kalnins, M. E. Cooper, and P. J. Wookey. 2004. Novel hexad repeats conserved in a putative transporter with restricted expression in cell types associated with growth, calcium exchange and homeostasis. Exp. Cell Res. 293:31-42.
7. Brown, J. K., C. Fung, and C. S. Tailor. 2006. Comprehensive mapping of receptor-functioning domains in feline leukemia virus subgroup C receptor FLVCR1. J. Virol. 80:1742-1751.
8. Carpenter, C. E., and A. W. Mahoney. 1992. Contributions of heme and nonheme iron to human nutrition. Crit. Rev. Food Sci. Nutr. 31:333-367.
9. Castro-Gago, M., A. Alonso, E. Pintos-Martinez, A. Beiras-Iglesias, Y. Campos, J. Arenas, M. I. Novo-Rodriguez, and J. Eiris-Punal. 1999. Congenital hydranencephalic-hydrocephalic syndrome associated with mitochondrial dysfunction. J. Child Neurol. 14:131-135. (Pubitemid 29146626)
10. Castro-Gago, M., E. Pintos-Martinez, J. Forteza-Vila, M. Iglesias-Diz, R. Ucieda-Somoza, I. Silva-Villar, J. Codesido-Lopez, A. Viso-Lorenzo, Y. Campos, J. Arenas, and J. Eiris-Punal. 2001. Congenital hydranencephalic-hydrocephalic syndrome with proliferative vasculopathy: a possible relation with mitochondrial dysfunction. J. Child Neurol. 16:858-862.
11. Cosset, F. L., Y. Takeuchi, J. L. Battini, R. A. Weiss, and M. K. L. Collins. 1995. High-titer packaging cells producing recombinant retroviruses resistant to human serum. J. Virol. 69:7430-7436.
12. Diamond, L. K. 1978. Congenital hypoplastic anemia: Diamond-Blackfan syndrome. Historical and clinical aspects. Blood Cells 4:209-213.
13. Dianzani, I., E. Garelli, and U. Ramenghi. 1996. Diamond-Blackfan anemia: a congenital defect in erythropoiesis. Haematologica 81:560-572.
14. Diaz, G. A., M. Banikazemi, K. Oishi, R. J. Desnick, and B. D. Gelb. 1999. Mutations in a new gene encoding a thiamine transporter cause thiamine-responsive megaloblastic anaemia syndrome. Nat. Genet. 22:309-312.
15. Dutta, B., W. Huang, M. Molero, R. Kekuda, F. H. Leibach, L. D. Devoe, V. Ganapathy, and P. D. Prasad. 1999. Cloning of the human thiamine transporter, a member of the folate transporter family. J. Biol. Chem. 274:31925-31929.
16. Fowler, M., R. Dow, T. A. White, and C. H. Greer. 1972. Congenital hydrocephalus-hydrencephaly in five siblings, with autopsy studies: a new disease. Dev. Med. Child Neurol. 14:173-188.
17. Hirsch, V., and J. Dunn. 1983. Megaloblastic anemia in the cat. J. Am. Anim. Hosp. Assoc. 19:873-880.
18. Kavanaugh, M. P., D. G. Miller, W. Zhang, W. Law, S. L. Kozak, D. Kabat, and A. D. Miller. 1994. Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters. Proc. Natl. Acad. Sci. U. S. A. 91:7071-7075.
19. Keel, S. B., R. T. Doty, Z. Yang, J. G. Quigley, J. Chen, S. Knoblaugh, P. D. Kingsley, I. De Domenico, M. B. Vaughn, J. Kaplan, J. Palis, and J. L. Abkowitz. 2008. A heme export protein is required for red blood cell differentiation and iron homeostasis. Science 319:825-828.
20. Krishnamurthy, P., D. D. Ross, T. Nakanishi, K. Bailey-Dell, S. Zhou, K. E. Mercer, B. Sarkadi, B. P. Sorrentino, and J. D. Schuetz. 2004. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol. Chem. 279:24218-24225.
21. Labay, V., T. Raz, D. Baron, H. Mandel, H. Williams, T. Barrett, R. Szargel, L. McDonald, A. Shalata, K. Nosaka, S. Gregory, and N. Cohen. 1999. Mutations in SLC19A2 cause thiamine-responsive megaloblastic anaemia associated with diabetes mellitus and deafness. Nat. Genet. 22:300-304.
22. Lalonde, E., S. Albrecht, K. C. Ha, K. Jacob, N. Bolduc, C. Polychronakos, P. Dechelotte, J. Majewski, and N. Jabado. 2010. Unexpected allelic heterogeneity and spectrum of mutations in Fowler syndrome revealed by nextgeneration exome sequencing. Hum. Mutat. 31:918-923. doi:10.1002/humu.21293.
23. Lein, E. S., M. J. Hawrylycz, N. Ao, M. Ayres, A. Bensinger, A. Bernard, A. F. Boe, M. S. Boguski, K. S. Brockway, E. J. Byrnes, L. Chen, T. M. Chen, M. C. Chin, J. Chong, B. E. Crook, A. Czaplinska, C. N. Dang, S. Datta, N. R. Dee, A. L. Desaki, T. Desta, E. Diep, T. A. Dolbeare, M. J. Donelan, H. W. Dong, J. G. Dougherty, B. J. Duncan, A. J. Ebbert, G. Eichele, L. K. Estin, C. Faber, B. A. Facer, R. Fields, S. R. Fischer, T. P. Fliss, C. Frensley, S. N. Gates, K. J. Glattfelder, K. R. Halverson, M. R. Hart, J. G. Hohmann, M. P. Howell, D. P. Jeung, R. A. Johnson, P. T. Karr, R. Kawal, J. M. Kidney, R. H. Knapik, C. L. Kuan, J. H. Lake, A. R. Laramee, K. D. Larsen, C. Lau, T. A. Lemon, A. J. Liang, Y. Liu, L. T. Luong, J. Michaels, J. J. Morgan, R. J. Morgan, M. T. Mortrud, N. F. Mosqueda, L. L. Ng, R. Ng, G. J. Orta, C. C. Overly, T. H. Pak, S. E. Parry, S. D. Pathak, O. C. Pearson, R. B. Puchalski, Z. L. Riley, H. R. Rockett, S. A. Rowland, J. J. Royall, M. J. Ruiz, N. R. Sarno, K. Schaffnit, N. V. Shapovalova, T. Sivisay, C. R. Slaughterbeck, S. C. Smith, K. A. Smith, B. I. Smith, A. J. Sodt, N. N. Stewart, K. R. Stumpf, S. M. Sunkin, M. Sutram, A. Tam, C. D. Teemer, C. Thaller, C. L. Thompson, L. R. Varnam, A. Visel, R. M. Whitlock, P. E. Wohnoutka, C. K. Wolkey, V. Y. Wong, M. Wood, et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176.
24. Marin, M., C. S. Tailor, A. Nouri, and D. Kabat. 2000. Sodium dependent neutral amino acid transporter type 1 (ASCT1) is an auxiliary receptor for baboon endogenous retrovirus. J. Virol. 74:8085-8093.
25. Mendoza, R., M. M. Anderson, and J. Overbaugh. 2006. A putative thiamine transport protein is a receptor for feline leukemia virus subgroup A. J. Virol. 80:3378-3385.
26. Meyer, E., C. Ricketts, N. V. Morgan, M. R. Morris, S. Pasha, L. J. Tee, F. Rahman, A. Bazin, B. Bessieres, P. Dechelotte, M. T. Yacoubi, M. Al-Adnani, T. Marton, D. Tannahill, R. C. Trembath, C. Fallet-Bianco, P. Cox, D. Williams, and E. R. Maher. 2010. Mutations in FLVCR2 are associated with proliferative vasculopathy and hydranencephaly-hydrocephaly syndrome (Fowler syndrome). Am. J. Hum. Genet. 86:471-478.
27. Miller, D. G., and A. D. Miller. 1994. A family of retroviruses that utilize related phosphate transporters for cell entry. J. Virol. 68:8270-8276.
28. Neil, J. C., R. Fulton, M. Rigby, and M. Stewart. 1991. Feline leukaemia virus: generation of pathogenic and oncogenic variants. Curr. Top. Microbiol. Immunol. 171:67-93.
29. Nicholls, D. G. 2002. Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease. Int. J. Biochem. Cell Biol. 34:1372-1381.
30. Overbaugh, J., A. D. Miller, and M. V. Eiden. 2001. Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol. Mol. Biol. Rev. 65:371-389.
31. Pao, S. S., I. T. Paulsen, and M. H. Saier, Jr. 1998. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62:1-34.
32. Ponka, P. 1999. Cell biology of heme. Am. J. Med. Sci. 318:241-256.
33. Ponka, P. 2004. Hereditary causes of disturbed iron homeostasis in the central nervous system. Ann. N. Y. Acad. Sci. 1012:267-281.
34. Ponka, P. 1997. Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood 89:1-25.
35. Poss, K. D., and S. Tonegawa. 1997. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U. S. A. 94:10925-10930.
36. Quigley, J. G., C. C. Burns, M. M. Anderson, E. D. Lynch, K. M. Sabo, J. Overbaugh, and J. L. Abkowitz. 2000. Cloning of the cellular receptor for feline leukemia virus subgroup C (FeLV-C), a retrovirus that induces red cell aplasia. Blood 95:1093-1099.
37. Quigley, J. G., Z. Yang, M. T. Worthington, J. D. Phillips, K. M. Sabo, D. E. Sabath, C. L. Berg, S. Sassa, B. L. Wood, and J. L. Abkowitz. 2004. Identification of a human heme exporter that is essential for erythropoiesis. Cell 118:757-766.
38. Rajagopal, A., A. U. Rao, J. Amigo, M. Tian, S. K. Upadhyay, C. Hall, S. Uhm, M. K. Mathew, M. D. Fleming, B. H. Paw, M. Krause, and I. Hamza. 2008. Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins. Nature 453:1127-1131.
39. Rasko, J. E., J. L. Battini, R. J. Gottschalk, I. Mazo, and A. D. Miller. 1999. The RD114/simian type D retrovirus receptor is a neutral amino acid transporter. Proc. Natl. Acad. Sci. U. S. A. 96:2129-2134.
40. Rey, M. A., S. P. Duffy, J. K. Brown, J. A. Kennedy, J. E. Dick, Y. Dror, and C. S. Tailor. 2008. Enhanced alternative splicing of the FLVCR1 gene in Diamond Blackfan anemia disrupts FLVCR1 expression and function that are critical for erythropoiesis. Haematologica 93:1617-1626.
41. Saier, M. H., Jr., M. R. Yen, K. Noto, D. G. Tamang, and C. Elkan. 2009. The Transporter Classification Database: recent advances. Nucleic Acids Res. 37:D274-D278.
42. Shalev, Z., S. P. Duffy, K. W. Adema, R. Prasad, N. Hussain, B. J. Willett, and C. S. Tailor. 2009. Identification of a feline leukemia virus variant that can use THTR1, FLVCR1, and FLVCR2 for infection. J. Virol. 83:6706-6716.
43. Shayeghi, M., G. O. Latunde-Dada, J. S. Oakhill, A. H. Laftah, K. Takeuchi, N. Halliday, Y. Khan, A. Warley, F. E. McCann, R. C. Hider, D. M. Frazer, G. J. Anderson, C. D. Vulpe, R. J. Simpson, and A. T. McKie. 2005. Identification of an intestinal heme transporter. Cell 122:789-801.
44. Tailor, C. S., D. Lavillette, M. Marin, and D. Kabat. 2003. Cell surface receptors for gammaretroviruses. Curr. Top. Microbiol. Immunol. 281:29-106.
45. Tailor, C. S., A. Nouri, Y. Zhao, Y. Takeuchi, and D. Kabat. 1999. A sodium dependent neutral amino acid transporter mediates infections of feline and baboon endogenous retroviruses and simian type D retroviruses. J. Virol. 73:4470-4474.
46. Tailor, C. S., B. J. Willet, and D. Kabat. 1999. A putative cell surface receptor for anemia-inducing subgroup C feline leukemia virus is a member of a transporter superfamily. J. Virol. 73:6500-6505.
47. Tsay, J., Z. Yang, F. P. Ross, S. Cunningham-Rundles, H. Lin, R. Coleman, P. Mayer-Kuckuk, S. B. Doty, R. W. Grady, P. J. Giardina, A. L. Boskey, and M. G. Vogiatzi. Bone loss due to iron overload in a murine model: importance of oxidative stress. Blood, in press.
48. Visel, A., C. Thaller, and G. Eichele. 2004. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res. 32:D552-D556.
49. Wang, H., M. P. Kavanaugh, and D. Kabat. 1994. A critical site in the cell surface receptor for ecotropic murine retroviruses required for amino acid transport but not for viral reception. Virology 202:1058-1060.