Transferrin receptor hyperexpression in primary erythroblasts is lost on transformation by avian erythroblastosis virus

Blood

Volumn 100, Issue 1, 2002, Pages 289-298

  Lobmayr, Lioba ^a,b,c,d   Sauer, Thomas ^a,b,c,d   Killisch, Iris ^a,b,c,d   Schranzhofer, Matthias ^a,b,c,d   Wilson, Robert B ^a,b,c,d   Ponka, Prem ^a,b,c,d   Beug, Hartmut ^a,b,c,d   Müllner, Ernst W ^a,b,c,d,e  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e Vienna Biocenter   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; AVIAN ERYTHROBLASTOSIS ONCOVIRUS; BLAST TRANSFORMATION; CHICKEN; CONTROLLED STUDY; ELECTROPHORESIS; ENDOSOME; ERYTHROBLAST; FLOW CYTOMETRY; GENE OVEREXPRESSION; IMMUNOELECTRON MICROSCOPY; IRON STORAGE; LEUKEMIA; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RNA BINDING; RNA STABILITY;

EID: 0036660209     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V100.1.289     Document Type: Article

References (68)

1. Aisen P, Wessling-Resnick M, Leibold EA. Iron metabolism. Curr Opin Chem Biol. 1999;3:200-206.
2. Brittenham GM. Disorders of iron metabolism: iron deficiency and overload. In: Hoffman R, Benz EJ, Shattil SJ, Furie B, Cohen HJ, eds. Hematology: Basic Principles and Practice. Vol 29. New York, NY: Churchill Livingstone; 1991:327-349.
3. Dautry-Varsat A, Ciechanover A, Lodish HF. pH and the recycling of transferrin during receptormediated endocytosis. Proc Natl Acad Sci U S A. 1983;80:2258-2262.
4. Harford JB, Klausner RD. Coordinate post-transcriptional regulation of ferritin and transferrin receptor expression: the role of regulated RNA-protein interaction. Enzyme. 1990;44:28-41.
5. Klausner RD, Rouault TA, Harford JB. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell. 1993;72:19-28.
6. Melefors O, Hentze MW. Iron regulatory factor - the conductor of cellular iron regulation. Blood Rev. 1993;7:251-258.
7. Rouault T, Klausner R. Regulation of iron metabolism in eukaryotes. Curr Top Cell Regul. 1997;35:1-19.
8. Cox TC, Bawden MJ, Martin A, May BK. Human erythroid 5-aminolevulinate synthase: promoter analysis and identification of an iron-responsive element in the mRNA. EMBO J. 1991;10:1891-1902.
9. Dandekar T, Stripecke R, Gray NK, et al. Identification of a novel iron-responsive element in murine and human erythroid delta-aminolevulinic acid synthase mRNA. EMBO J. 1991;10:1903-1909.
10. Ponka P. Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood. 1997;89:1-25.
11. Beug H, Metz T, Mullner EW, Hayman MJ. Self renewal and differentiation in primary avian hematopoietic cells: an alternative to mammalian in vitro models? Curr Top Microbiol Immunol. 1996;211:29-39.
12. Alitalo R, Partanen J, Pertovaara L, et al. Increased erythroid potentiating activity/tissue inhibitor of metalloproteinases and jun/fos transcription factor complex characterize tumor promoter-induced megakaryoblastic differentiation of K562 leukemia cells. Blood. 1990;75:1974-1982.
13. Marks PA, Breslow R, Rifkind RA, Ngo L, Singh R. Polar/apolar chemical inducers of differentiation of transformed cells: strategies to improve therapeutic potential. Proc Natl Acad Sci U S A. 1989;86:6358-6362.
14. Hayman MJ, Meyer S, Martin F, Steinlein P, Beug H. Self-renewal and differentiation of normal avian erythroid progenitor cells: regulatory roles of the TGF alpha/c-ErbB and SCF/c-kit receptors. Cell. 1993;74:157-169.
15. Schroeder C, Gibson L, Nordstrom C, Beug H. The estrogen receptor cooperates with the TGF alpha receptor (c-erbB) in regulation of chicken erythroid progenitor self-renewal. EMBO J. 1993;12:951-960.
16. Steinlein P, Wessely O, Meyer S, Deiner EM, Hayman MJ, Beug H. Primary, self-renewing erythroid progenitors develop through activation of both tyrosine kinase and steroid hormone receptors. Curr Biol. 1995;5:191-204.
17. Wessely O, Deiner EM, Beug H, von Lindern M. The glucocorticoid receptor is a key regulator of the decision between self-renewal and differentiation in erythroid progenitors. EMBO J. 1997;16:267-280.
18. Beug H, Mullner EW, Hayman MJ. Insights into erythroid differentiation obtained from studies on avian erythroblastosis virus. Curr Opin Cell Biol. 1994;6:816-824.
19. Wessely O, Bauer A, Quang CT, et al. A novel way to induce erythroid progenitor self renewal: cooperation of c-Kit with the erythropoietin receptor. Biol Chem. 1999;380:187-202.
20. Beug H, Hayman MJ, Graf T. Myeloblasts transformed by the avian acute leukemia virus E26 are hormone-dependent for growth and for the expression of a putative myb-containing protein, p135 E26. EMBO J. 1982;1:1069-1073.
21. Steinlein P, Deiner E, Leutz A, Beug H. Recombinant murine erythropoietin receptor expressed in avian erythroid progenitors mediates terminal erythroid differentiation in vitro. Growth Factors. 1994;10:1-16.
22. Mikulits W, Schranzhofer M, Bauer A, et al. Impaired ferritin mRNA translation in primary erythroid progenitors: shift to iron-dependent regulation by the v-ErbA oncoprotein. Blood. 1999;94:4321-4332.
23. Beug H, Dahl R, Steinlein P, Meyer S, Deiner EM, Hayman MJ. In vitro growth of factor-dependent multipotential hematopoietic cells is induced by the nuclear oncoprotein v-Ski. Oncogene. 1995;11:59-72.
24. Graf T, van Kirchbach A, Beug H. Characterization of the hematopoietic target cells of AEV, MC29 and AMV avian leukemia viruses. Exp Cell Res. 1981;131:331-343.
25. Beug H, von Kirchbach A, Doderlein G, Conscience JF, Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell. 1979;18:375-390.
26. Graf T, Friis RR. Differential expression of transformation in rat and chicken cells infected with an avian sarcoma virus ts mutant. Virology. 1973;56:369-374.
27. Kawaguchi T, Nomura K, Hirayama Y, Kitagawa T. Establishment and characterization of a chicken hepatocellular carcinoma cell line, LMH. Cancer Res. 1987;47:4460-4464.
28. Beug H, Steinlein P, Bartunek P, Hayman MJ. Avian hematopoietic cell culture: in vitro model systems to study oncogenic transformation of hematopoietic cells. Methods Enzymol. 1995;254:41-76.
29. Quang CT, Wessely O, Pironin M, Beug H, Ghysdael J. Cooperation of Spi-1/PU.1 with an activated erythropoietin receptor inhibits apoptosis and Epo-dependent differentiation in primary erythroblasts and induces their Kit ligand-dependent proliferation. EMBO J. 1997;16:5639-5653.
30. Kieslinger M, Woldman I, Moriggl R, et al. Antiapoptotic activity of Stat5 required during terminal stages of myeloid differentiation. Genes Dev. 2000;14:232-244.
31. Schmidt JA, Marshall J, Hayman MJ, Ponka P, Beug H. Control of erythroid differentiation: possible role of the transferrin cycle. Cell. 1986;46:41-51.
32. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanatephenol-chloroform extraction. Anal Biochem. 1987;162:156-159.
33. Chan LN, Gerhardt EM, Transferrin receptor gene is hyperexpressed and transcriptionally regulated in differentiating erythroid cells. J Biol Chem. 1992;267:8254-8259.
34. Hedges SB, Moberg KD, Maxson LR. Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences and a review of the evidence for amniote relationships [published erratum appears in Mol Biol Evol 1991 May;8(3):398]. Mol Biol Evol. 1990;7:607-633.
35. Mullner EW, Neupert B, Kuhn LC. A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell. 1989;58:373-382.
36. Hentze MW, Rouault TA, Harford JB, Klausner RD. Oxidation-reduction and the molecular mechanism of a regulatory RNA-protein interaction. Science. 1989;244:357-359.
37. Pantopoulos K, Mueller S, Atzberger A, Ansorge W, Stremmel W, Hentze MW. Differences in the regulation of iron regulatory protein-1 (IRP-1) by extra- and intracellular oxidative stress. J Biol Chem. 1997;272:9802-9808.
38. Killisch I, Steinlein P, Romisch K, Hollinshead R, Beug H, Griffiths G. Characterization of early and late endocytic compartments of the transferrin cycle. Transferrin receptor antibody blocks erythroid differentiation by trapping the receptor in the early endosome. J Cell Sci. 1992;103:211-232.
39. Busfield SJ, Tilbrook PA, Callus BA, Spadaccini A, Kuhn L, Klinken SP. Complex regulation of transferrin receptors during erythropoietin- induced differentiation of J2E erythroid cells - elevated transcription and mRNA stabilisation produce only a modest rise in protein content. Eur J Biochem. 1997;249:77-84.
40. Mullner EW, Kuhn LC. A stem-loop in the 3′ untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell. 1988;53:815-825.
41. Moura E, Noordermeer MA, Verhoeven N, Verheul AF, Marx JJ. Iron release from human monocytes after erythrophagocytosis in vitro: an investigation in normal subjects and hereditary hemochromatosis patients. Blood. 1998;92:2511-2519.
42. Rothenberger S, Mullner EW, Kuhn LC. The mRNA-binding protein which controls ferritin and transferrin receptor expression is conserved during evolution. Nucleic Acids Res. 1990;18:1175-1179.
43. Pantopoulos K, Gray NK, Hentze MW. Differential regulation of two related RNA-binding proteins, iron regulatory protein (IRP) and IRPB. RNA. 1995;1:155-163.
44. Binder R, Horowitz JA, Basilion JP, Koeller DM, Klausner RD, Harford JB. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. Embo J. 1994;13:1969-1980.
45. Chan RY, Seiser C, Schulman HM, Kuhn LC, Ponka P. Regulation of transferrin receptor mRNA expression. Distinct regulatory features in erythroid cells. Eur J Biochem. 1994;220:683-692.
46. Posch M, Sutterluety H, Skern T, Seiser C. Characterization of the translation-dependent step during iron-regulated decay of transferrin receptor mRNA. J Biol Chem. 1999;274:16611-16618.
47. Bauer A, Mikulits W, Lagger G, Stengl G, Brosch G, Beug H. The thyroid hormone receptor functions as a ligand-operated developmental switch between proliferation and differentiation of erythroid progenitors. EMBO J. 1998;17:4291-4303.
48. Ponka P, Beaumont C, Richardson DR. Function and regulation of transferrin and ferritin. Semin Hematol. 1998;35:35-54.
49. Levy JE, Jin O, Fujiwara Y, Kuo F, Andrews NC. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat Genet. 1999;21:396-399.
50. Trenor CC 3rd, Campagna DR, Sellers VM, Andrews NC, Fleming MD. The molecular defect in hypotransferrinemic mice. Blood. 2000;96:1113-1118.
51. Dolznig H, Boulme F, Stangl K, et al. Establishment of normal, terminally differentiating mouse erythroid progenitors: molecular characterization by cDNA arrays. FASEB J. 2001;15:1442-1444.
52. Papayannopoulou T, Abkowitz J. Biology of erythropoiesis, erythroid differentiation, and maturation. In: Hoffman R, Benz EJ, Shattil SJ, Furie B, Cohen HJ, eds. Hematology: Basic Principles and Practice. Vol. 21. New York, NY: Churchill Livingstone; 1991:252-263.
53. Kornfeld S, Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 1989;5:483-525.
54. Fleming MD, Trenor CCr, Su MA, et al. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet. 1997;16:383-386.
55. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A. 1998;95:1148-1153.
56. Andrews NC. The iron transporter DMT1. Int J Biochem Cell Biol. 1999;31:991-994.
57. Su MA, Trenor CC, Fleming JC, Fleming MD, Andrews NC. The G185R mutation disrupts function of the iron transporter Nramp2. Blood. 1998;92: 2157-2163.
58. Nunez MT, Gaete V, Escobar A. Endocytic vesicles contain a calmodulin-activated Ca2+ pump that mediates the inhibition of acidification by calcium. Biochim Biophys Acta. 1990;1028:21-24.
59. Gunshin H, Mackenzie B, Berger UV, et al. Cloning and characterization of a mammalian protoncoupled metal-ion transporter. Nature. 1997;388:482-488.
60. Allikmets R, Raskind WH, Hutchinson A, Schueck ND, Dean M, Koeller DM. Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A). Hum Mol Genet. 1999;8:743-749.
61. Fitzsimons EJ, May A. The molecular basis of the sideroblastic anemias. Curr Opin Hematol. 1996;3:167-172.
62. Richardson DR, Ponka P, Vyoral D. Distribution of iron in reticulocytes after inhibition of heme synthesis with succinylacetone: examination of the intermediates involved in iron metabolism. Blood. 1996;87:3477-3488.
63. Richardson DR, Ponka P. The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta. 1997;1331:1-40.
64. Freshney RI. Culture of Animal Cells: A Manual of Basic Technique. 3rd ed. New York, NY: Wiley-Liss; 1994.
65. Sawyers CL, Denny CT, Witte ON. Leukemia and the disruption of normal hematopoiesis. Cell. 1991;64:337-350.
66. Kispal G, Csere P, Prohl C, Lill R. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J. 1999;18:3981-3989.
67. Csere P, Lill R, Kispal G. Identification of a human mitochondrial ABC transporter, the functional orthologue of yeast Arm1p. FEBS Lett. 1998;441:266-270.
68. Shirihai OS, Gregory T, Yu C, Orkin SH, Weiss MJ. ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation. EBMO J. 2000;19:2492-2502.