Activation of transferrin receptor 1 by c-Myc enhances cellular proliferation and tumorigenesis

Molecular and Cellular Biology

Volumn 26, Issue 6, 2006, Pages 2373-2386

  O'Donnell, Kathryn A ^a   Yu, Duonan ^b   Zeller, Karen I ^a   Kim, Jung Whan ^a   Racke, Frederick ^a   Thomas Tikhonenko, Andrei ^b   Dang, Chi V ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Ross Research Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD71 ANTIGEN; MYC PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LYMPHOMA; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL GROWTH; CELL PROLIFERATION; CELL SIZE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TARGETING; GENETIC CONSERVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; IRON METABOLISM; IRON TRANSPORT; MALE; MAMMAL CELL; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; REGULATORY MECHANISM;

ANIMALS; ANTIGENS, CD; APOPTOSIS; CARCINOGENICITY TESTS; CELL CYCLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; HUMANS; IRON CHELATING AGENTS; LYMPHOMA, B-CELL; MALE; MICE; MICE, NUDE; PHYLOGENY; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RECEPTORS, TRANSFERRIN; TUMOR CELLS, CULTURED;

ANIMALIA; MAMMALIA;

EID: 33644770587     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.6.2373-2386.2006     Document Type: Article

References (64)

1. Adhikary, S., and M. Eilers. 2005. Transcriptional regulation and transformation by Myc proteins. Nat. Rev. Mol. Cell. Biol. 6:635-645.
2. Alizadeh, A. A., M. B. Eisen, R. E. Davis, C. Ma, I. S. Lossos, A. Rosenwald, J. C. Boldrick, H. Sabet, T. Tran, X. Yu, J. I. Powell, L. Yang, G. E. Marti, T. Moore, J. Hudson, Jr., L. Lu, D. B. Lewis, R. Tibshirani, G. Sherlock, W. C. Chan, T. C. Greiner, D. D. Weisenburger, J. O. Armitage, R. Warnke, R. Levy, W. Wilson, M. R. Grever, J. C. Byrd, D. Botstein, P. O. Brown, and L. M. Staudt. 2000. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503-511.
3. Becton, D. L., and P. Bryles. 1988. Deferoxamine inhibition of human neuroblastoma viability and proliferation. Cancer Res. 48:7189-7192.
4. Blatt, J., and S. Stitely. 1987. Antineuroblastoma activity of desferoxamine in human cell lines. Cancer Res. 47:1749-1750.
5. Bowen, H., T. E. Biggs, S. T. Baker, E. Phillips, V. H. Perry, D. A. Mann, and C. H. Barton. 2002. c-Myc represses the murine Nramp1 promoter. Biochem. Soc. Trans. 30:774-777.
6. Bowen, H., A. Lapham, E. Phillips, I. Yeung, M. Alter-Koltunoff, B. Z. Levi, V. H. Perry, D. A. Mann, and C. H. Barton. 2003. Characterization of the murine Nramp1 promoter: requirements for transactivation by Miz-1. J. Biol. Chem. 278:36017-36026.
7. Boyd, K. E., J. Wells, J. Gutman, S. M. Bartley, and P. J. Farnham. 1998. c-Myc target gene specificity is determined by a post-DNAbinding mechanism. Proc. Natl. Acad. Sci. USA 95:13887-13892.
8. Cheng, Y., O. Zak, P. Aisen, S. C. Harrison, and T. Walz. 2004. Structure of the human transferrin receptor-transferrin complex. Cell 116:565-576.
9. Chitambar, C. R., E. J. Massey, and P. A. Seligman. 1983. Regulation of transferrin receptor expression on human leukemic cells during proliferation and induction of differentiation. Effects of gallium and dimethylsulfoxide. J. Clin. Investig. 72:1314-1325.
10. Cole, M. D., and S. B. McMahon. 1999. The Myc oncoprotein: a critical evaluation of transactivation and target gene regulation. Oncogene 18:2916-2924.
11. Coller, H. A., C. Grandori, P. Tamayo, T. Colbert, E. S. Lander, R. N. Eisenman, and T. R. Golub. 2000. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. USA 97:3260-3265.
12. Dang, C. V. 1999. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol. Cell. Biol. 19:1-11.
13. Eilers, M., D. Picard, K. R. Yamamoto, and J. M. Bishop. 1989. Chimaeras of myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature 340:66-68.
14. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
15. Ellwood-Yen, K., T. G. Graeber, J. Wongvipat, M. L. Iruela-Arispe, J. Zhang, R. Matusik, G. V. Thomas, and C. L. Sawyers. 2003. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 4:223-238.
16. Fan, L., J. Iyer, S. Zhu, K. K. Frick, R. K. Wada, A. E. Eskenazi, P. E. Berg, N. Ikegaki, R. H. Kennett, and C. N. Frantz. 2001. Inhibition of N-myc expression and induction of apoptosis by iron chelation in human neuroblastoma cells. Cancer Res. 61:1073-1079.
17. Feremans, W., W. Bujan, P. Neve, J. P. Delville, and L. Schandene. 1991. CD71 phenotype and the value of gallium imaging in lymphomas. Am. J. Hematol. 36:215-216.
18. Fernandez, P. C., S. R. Frank, L. Wang, M. Schroeder, S. Liu, J. Greene, A. Cocito, and B. Amati. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115-1129.
19. Gatter, K. C., G. Brown, I. S. Trowbridge, R. E. Woolston, and D. Y. Mason. 1983. Transferrin receptors in human tissues: their distribution and possible clinical relevance. J. Clin. Pathol. 36:539-545.
20. Grandori, C., and R. N. Eisenman. 1997. Myc target genes. Trends Biochem. Sci. 22:177-181.
21. Grandori, C., J. Mac, F. Siebelt, D. E. Ayer, and R. N. Eisenman. 1996. Myc-Max heterodimers activate a DEAD box gene and interact with multiple E box-related sites in vivo. EMBO J. 15:4344-4357.
22. Haggerty, T. J., K. I. Zeller, R. C. Osthus, D. R. Wonsey, and C. V. Dang. 2003. A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc target sites. Proc. Natl. Acad. Sci. USA 100:5313-5318.
23. Hanson, K. D., M. Shichiri, M. R. Follansbee, and J. M. Sedivy. 1994. Effects of c-myc expression on cell cycle progression. Mol. Cell. Biol. 14:5748-5755.
24. Hosack, D. A., G. Dennis, Jr., B. T. Sherman, H. C. Lane, and R. A. Lempicki. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol. 4:R70.
25. Iritani, B. M., and R. N. Eisenman. 1999. c-Myc enhances protein synthesis and cell size during B lymphocyte development. Proc. Natl. Acad. Sci. USA 96:13180-13185.
26. Kemp, J. D., K. M. Smith, J. M. Mayer, F. Gomez, J. A. Thorson, and P. W. Naumann. 1992. Effects of anti-transferrin receptor antibodies on the growth of neoplastic cells. Pathobiology 60:27-32.
27. Kuhn, L. C. 1989. The transferrin receptor: a key function in iron metabolism. Schweiz. Med. Wochenschr. 119:1319-1326.
28. Larrick, J. W., and P. Cresswell. 1979. Modulation of cell surface iron transferrin receptors by cellular density and state of activation. J. Supramol. Struct. 11:579-586.
29. Li, F., Y. Wang, K. I. Zeller, J. J. Potter, D. R. Wonsey, K. A. O'Donnell, J. W. Kim, J. T. Yustein, L. A. Lee, and C. V. Dang. 2005. Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol. Cell. Biol. 25:6225-6234.
30. Li, Z., S. Van Calcar, C. Qu, W. K. Cavenee, M. Q. Zhang, and B. Ren. 2003. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc. Natl. Acad. Sci. USA 100:8164-8169.
31. 0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:934-947.
32. Lossos, I. S., A. A. Alizadeh, M. Diehn, R. Warnke, Y. Thorstenson, P. J. Oefner, P. O. Brown, D. Botstein, and R. Levy. 2002. Transformation of follicular lymphoma to diffuse large-cell lymphoma: alternative patterns with increased or decreased expression of c-myc and its regulated genes. Proc. Natl. Acad. Sci. USA 99:8886-8891.
33. Mateyak, M. K., A. J. Obaya, S. Adachi, and J. M. Sedivy. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8:1039-1048.
34. Moura, I. C., Y. Lepelletier, B. Arnulf, P. England, C. Baude, C. Beaumont, A. Bazarbachi, M. Benhamou, R. C. Monteiro, and O. Hermine. 2003. A neutralizing monoclonal antibody (mAb A24) directed against the transferrin receptor induces apoptosis of tumor T lymphocytes from ATL patients. Blood 103:1838-1845.
35. Neckers, L. M., and J. B. Trepel. 1986. Transferrin receptor expression and the control of cell growth. Cancer Investig. 4:461-470.
36. Nikiforov, M. A., S. Chandriani, B. O'Connell, O. Petrenko, I. Kotenko, A. Beavis, J. M. Sedivy, and M. D. Cole. 2002. A functional screen for Myc-responsive genes reveals serine hydroxymethyltransferase, a major source of the one-carbon unit for cell metabolism. Mol. Cell. Biol. 22:5793-5800.
37. O'Connell, B. C., A. F. Cheung, C. P. Simkevich, W. Tam, X. Ren, M. K. Mateyak, and J. M. Sedivy. 2003. A large scale genetic analysis of c-Myc-regulated gene expression patterns. J. Biol. Chem. 278:12563-12573.
38. O'Donnell, K. A., E. A. Wentzel, K. I. Zeller, C. V. Dang, and J. T. Mendell. 2005. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839-843.
39. Orian, A., B. van Steensel, J. Delrow, H. J. Bussemaker, L. Li, T. Sawado, E. Williams, L. W. Loo, S. M. Cowley, C. Yost, S. Pierce, B. A. Edgar, S. M. Parkhurst, and R. N. Eisenman. 2003. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 17:1101-1114.
40. Oster, S. K., C. S. Ho, E. L. Soucie, and L. Z. Penn. 2002. The myc oncogene: MarvelouslY Complex. Adv. Cancer Res. 84:81-154.
41. Oster, S. K., D. Y. Mao, J. Kennedy, and L. Z. Penn. 2003. Functional analysis of the N-terminal domain of the Myc oncoprotein. Oncogene 22:1998-2010.
42. Pajic, A., D. Spitkovsky, B. Christoph, B. Kempkes, M. Schuhmacher, M. S. Staege, M. Brielmeier, J. Ellwart, F. Kohlhuber, G. W. Bornkamm, A. Polack, and D. Eick. 2000. Cell cycle activation by c-myc in a burkitt lymphoma model cell line. Int. J. Cancer 87:787-793.
43. Pelengaris, S., M. Khan, and G. Evan. 2002. c-MYC: more than just a matter of life and death. Nat Rev. Cancer 2:764-776.
44. 43a. Remondini, D., B. O'Connell, B. Intrator, J. M. Sedivy, N. Neretti, G. C. Castellani, and L. N. Cooper. 2005. Targeting c-Myc activated genes with a correlation method: detection of global changes in large gene expression network dynamics. Proc. Natl. Acad. Sci. USA 102:6902-6906.
45. Rhodes, D. R., J. Yu, K. Shanker, N. Deshpande, R. Varambally, D. Ghosh, T. Barrette, A. Pandey, and A. M. Chinnaiyan. 2004. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6:1-6.
46. Richardson, D. R. 2002. Iron chelators as therapeutic agents for the treatment of cancer. Crit. Rev. Oncol. Hematol. 42:267-281.
47. Richardson, D. R. 2002. Therapeutic potential of iron chelators in cancer therapy. Adv. Exp. Med. Biol. 509:231-249.
48. Schuhmacher, M., F. Kohlhuber, M. Holzel, C. Kaiser, H. Burtscher, M. Jarsch, G. W. Bornkamm, G. Laux, A. Polack, U. H. Weidle, and D. Eick. 2001. The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res. 29:397-406.
49. Secombe, J., S. B. Pierce, and R. N. Eisenman. 2004. Myc: a weapon of mass destruction. Cell 117:153-156.
50. Sherr, C. J., and R. A. DePinho. 2000. Cellular senescence: mitotic clock or culture shock? Cell 102:407-410.
51. Small, M. B., N. Hay, M. Schwab, and J. M. Bishop. 1987. Neoplastic transformation by the human gene N-myc. Mol. Cell. Biol. 7:1638-1645.
52. Stone, J., T. de Lange, G. Ramsay, E. Jakobovits, J. M. Bishop, H. Varmus, and W. Lee. 1987. Definition of regions in human c-myc that are involved in transformation and nuclear localization. Mol. Cell. Biol. 7:1697-1709.
53. Su, A. I., M. P. Cooke, K. A. Ching, Y. Hakak, J. R. Walker, T. Wiltshire, A. P. Orth, R. G. Vega, L. M. Sapinoso, A. Moqrich, A. Patapoutian, G. M. Hampton, P. G. Schultz, and J. B. Hogenesch. 2002. Large-scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. USA 99:4465-4470.
54. Taetle, R., J. M. Honeysett, and I. Trowbridge. 1983. Effects of anti-transferrin receptor antibodies on growth of normal and malignant myeloid cells. Int. J. Cancer 32:343-349.
55. Vindelov, L. L., I. J. Christensen, and N. I. Nissen. 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3:323-327.
56. Weiner, R. E. 1996. The mechanism of 67Ga localization in malignant disease. Nucl. Med. Biol. 23:745-751.
57. Wonsey, D. R., K. I. Zeller, and C. V. Dang. 2002. The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc. Natl. Acad. Sci. USA 99:6649-6654.
58. Woo, R. A., and R. Y. Poon. 2004. Activated oncogenes promote and cooperate with chromosomal instability for neoplastic transformation. Genes Dev. 18:1317-1330.
59. Wu, K. J., A. Polack, and R. Dalla-Favera. 1999. Coordinated regulation of iron-controlling genes, H-ferritin and IRP2, by c-MYC. Science 283:676-679.
60. Yu, D., D. Allman, M. H. Goldschmidt, M. L. Atchison, J. G. Monroe, and A. Thomas-Tikhonenko. 2003. Oscillation between B-lymphoid and myeloid lineages in Myc-induced hematopoietic tumors following spontaneous silencing/reactivation of the EBF/Pax5 pathway. Blood 101:1950-1955.
61. Yu, D., M. Dews, A. Park, J. W. Tobias, and A. Thomas-Tikhonenko. 2005. Inactivation of Myc in murine two-hit B lymphomas causes dormancy with elevated levels of interleukin 10 receptor and CD20: implications for adjuvant therapies. Cancer Res. 65:5454-5461.
62. Yu, D., and A. Thomas-Tikhonenko. 2002. A non-transgenic mouse model for B-cell lymphoma: in vivo infection of p53-null bone marrow progenitors by a Myc retrovirus is sufficient for tumorigenesis. Oncogene 21:1922-1927.
63. Zeller, K. I., T. J. Haggerty, J. F. Barrett, Q. Guo, D. R. Wonsey, and C. V. Dang. 2001. Characterization of nucleophosmin (B23) as a Myc target by scanning chromatin immunoprecipitation. J. Biol. Chem. 276:48285-48291.
64. Zeller, K. I., A. G. Jegga, B. J. Aronow, K. A. O'Donnell, and C. V. Dang. 2003. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol. 4:R69.