Aberrant Eukaryotic Translation Initiation Factor 4E-Dependent mRNA Transport Impedes Hematopoietic Differentiation and Contributes to Leukemogenesis

Molecular and Cellular Biology

Volumn 23, Issue 24, 2003, Pages 8992-9002

  Topisirovic, Ivan ^a   Guzman, Monica L ^b,c   McConnell, Melanie J ^a   Licht, Jonathan D ^a   Culjkovic, Biljana ^a   Neering, Sarah J ^b,c   Jordan, Craig T ^b,c   Borden, Katherine L B ^a  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; HOMEODOMAIN PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR; INITIATION FACTOR 4E; MESSENGER RNA; PROLINE;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL NUCLEUS INCLUSION BODY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CYTOPLASM; GRANULOCYTE; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKEMOGENESIS; MONOCYTE; MUTAGENESIS; PRIORITY JOURNAL; RNA TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; BASE SEQUENCE; CELL DIFFERENTIATION; CYCLIN D1; DNA, COMPLEMENTARY; DNA, NEOPLASM; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; HEMATOPOIESIS; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA; NF-KAPPA B; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EUKARYOTA;

EID: 0344629665     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.24.8992-9002.2003     Document Type: Article

References (47)

1. Borden, K. L. 2002. Pondering the promyelocytic leukemia protein (PML) puzzle: possible functions for PML nuclear bodies. Mol. Cell. Biol. 22:5259-5269.
2. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of a signal response domain in IκBαa to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15:2809-2818.
3. Carlile, G. W., W. G. Tatton, and K. L. Borden. 1998. Demonstration of a RNA-dependent nuclear interaction between the promyelocytic leukaemia protein and glyceraldehyde-3-phosphate dehydrogenase. Biochem. J. 335:691-696.
4. Cohen, N., M. Sharma, A. Kentsis, J. M. Perez, S. Strudwick, and K. L. Borden. 2001. PML RING suppresses oncogenic transformation by reducing the affinity of eIF4E for mRNA. EMBO J. 20:4547-4559.
5. Crompton, M. R., T. J. Bartlett, A. D. MacGregor, G. Manfioletti, E. Buratti, V. Giancotti, and G. H. Goodwin. 1992. Identification of a novel vertebrate homeobox gene expressed in haematopoietic cells. Nucleic Acids Res. 20:5661-5667.
6. De Benedetti, A., and A. L. Harris. 1999. eIF4E expression in tumors: its possible role in progression and malignacies. Int. J. Biochem. Cell Biol. 31:59-72.
7. D'Elia, A. V., G. Tell, D. Russo, F. Arturi, F. Puglisi, G. Manfioletti, V. Gattei, D. L. Mack, P. Cataldi, S. Filetti, C. Di Loreto, and G. Damante. 2002. Expression and localization of the homeodomain-containing protein HEX in human thyroid tumors. J. Clin. Endocrinol. Metab. 87:1376-1383.
8. Dokter, W. H., L. Tuyt, S. J. Sierdsema, M. T. Esselink, and E. Vellenga. 1995. The spontaneous expression of interleukin-1β and interleukin-6 is associated with spontaneous expression of AP-1 and NF-κB transcription factor in acute myeloblastic leukemia cells. Leukemia 9:425-432.
9. Duyao, M. P., D. J. Kessler, D. B. Spicer, and G. E. Sonenshein. 1992. Transactivation of the c-myc gene by HTLV-1 tax is mediated by NFκB. Curr. Top. Microbiol. Immunol. 182:421-424.
10. Gingras, A. C., B. Raught, and N. Sonenberg. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
11. Guzman, M. L., S. J. Neering, D. Upchurch, B. Grimes, D. S. Howard, D. A. Rizzieri, S. M. Luger, and C. T. Jordan. 2001. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 98:2301-2307.
12. Guzman, M. L., C. F. Swiderski, D. S. Howard, B. A. Grimes, R. M. Rossi, S. J. Szilvassy, and C. T. Jordan. 2002. Preferential induction of apoptosis for primary human leukemic stem cells. Proc. Natl. Acad. Sci. USA 99:16220-16225.
13. Howard, D. S., D. A. Rizzierri, B. Grimes, D. Upchurch, G. L. Phillips, A. K. Stewart, J. R. Yannelli, and C. T. Jordan. 1999. Genetic manipulation of primitive leukemic and normal hematopoietic cells using a novel method of adenovirus-mediated gene transfer. Leukemia 13:1608-1616.
14. Hromas, R., J. Radich, and S. Collins. 1993. PCR cloning of an orphan homeobox gene (PRH) preferentially expressed in myeloid and liver cells. Biochem. Biophys. Res. Commun. 195:976-983.
15. Iborra, F. J., D. A. Jackson, and P. R. Cook. 2001. Coupled transcription and translation within nuclei of mammalian cells. Science 293:1139-1142.
16. Iervolino, A., G. Santilli, R. Trotta, C. Guerzoni, V. Cesi, A. Bergamaschi, C. Gambacorti-Passerini, B. Calabretta, and D. Perrotti. 2002. hnRNP A1 nucleocytoplasmic shuttling activity is required for normal myelopoiesis and BCR/ABL leukemogenesis. Mol. Cell. Biol. 22:2255-2266.
17. Jordan, C. T., D. Upchurch, S. J. Szilvassy, M. L. Guzman, D. S. Howard, A. L. Pettigrew, T. Meyerrose, R. Rossi, B. Grimes, D. A. Rizzieri, S. M. Luger, and G. L. Phillips. 2000. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 14:1777-1784.
18. Kentsis, A., E. C. Dwyer, J. M. Perez, M. Sharma, A. Chen, Z. Q. Pan, and K. L. Borden. 2001. The RING domains of the promyelocytic leukemia protein PML and the arenaviral protein Z repress translation by directly inhibiting translation initiation factor eIF4E. J. Mol. Biol. 312:609-623.
19. Kordes, U., D. Krappmann, V. Heissmeyer, W. D. Ludwig, and C. Scheidereit. 2000. Transcription factor NF-κB is constitutively activated in acute lymphoblastic leukemia cells. Leukemia 14:399-402.
20. Lai, H. K., and K. L. Borden. 2000. The promyelocytic leukemia (PML) protein suppresses cyclin D1 protein production by altering the nuclear cytoplasmic distribution of cyclin D1 mRNA. Oncogene 19:1623-1634.
21. Lazaris-Karatzas, A., K. S. Montine, and N. Sonenberg. 1990. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature 345:544-547.
22. Lazaris-Karatzas, A., M. R. Smith, R. M. Frederickson, M. L. Jaramillo, Y. L. Liu, H. F. Kung, and N. Sonenberg. 1992. Ras mediates translation initiation factor 4E-induced malignant transformation. Genes Dev. 6:1631-1642.
23. Lazaris-Karatzas, A., and N. Sonenberg. 1992. The mRNA 5′ cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts. Mol. Cell. Biol. 12:1234-1238.
24. Lejbkowicz, F., C. Goyer, A. Darveau, S. Neron, R. Lemieux, and N. Sonenberg. 1992. A fraction of the mRNA 5′ cap-binding protein, eukaryotic initiation factor 4E, localizes to the nucleus. Proc. Natl. Acad. Sci. USA 89:9612-9616.
25. Liao, W., C. Y. Ho, Y. L. Yan, J. Postlethwait, and D. Y. Stainier. 2000. Hhex and scl function in parallel to regulate early endothelial and blood differentiation in zebrafish. Development 127:4303-4313.
26. Manfioletti, G., V. Gattei, E. Buratti, A. Rustighi, A. De Iuliis, D. Aldinucci, G. H. Goodwin, and A. Pinto. 1995. Differential expression of a novel proline-rich homeobox gene (Prh) in human hematolymphopoietic cells. Blood 85:1237-1245.
27. Martinez Barbera, J. P., M. Clements, P. Thomas, T. Rodriguez, D. Meloy, D. Kioussis, and R. S. Beddington. 2000. The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127:2433-2445.
28. Nathan, C. A., P. Carter, L. Liu, B. D. Li, F. Abreo, A. Tudor, S. G. Zimmer, and A. De Benedetti. 1997. Elevated expression of eIF4E and FGF-2 isoforms during vascularization of breast carcinomas. Oncogene 15:1087-1094.
29. Nathan, C. A., L. Liu, B. D. Li, F. W. Abreo, I. Nandy, and A. De Benedetti. 1997. Detection of the proto-oncogene eIF4E in surgical margins may predict recurrence in head and neck cancer. Oncogene 15:579-584.
30. Newman, C. S., F. Chia, and P. A. Krieg. 1997. The XHex homeobox gene is expressed during development of the vascular endothelium: overexpression leads to an increase in vascular endothelial cell number. Mech. Dev. 66:83-93.
31. Obinata, A., Y. Akimoto, Y. Omoto, and H. Hirano. 2002. Expression of Hex homeobox gene during skin development: increase in epidermal cell proliferation by transfecting the Hex to the dermis. Dev. Growth Differ. 44:281-292.
32. Olivieri, N. F. 1999. The beta-thalassemias. N. Engl. J. Med. 341:99-109.
33. Pearson, M., R. Carbone, C. Sebastiani, M. Cioce, M. Fagioli, S. Saito, Y. Higashimoto, E. Appella, S. Minucci, P. P. Pandolfi, and P. G. Pelicci. 2000. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406:207-210.
34. Perrotti, D., V. Cesi, R. Trotta, C. Guerzoni, G. Santilli, K. Campbell, A. Iervolino, F. Condorelli, C. Gambacorti-Passerini, M. A. Caligiuri, and B. Calabretta. 2002. BCR-ABL suppresses C/EBPα expression through inhibitory action of hnRNP E2. Nat. Genet. 30:48-58.
35. Rousseau, D., R. Kaspar, I. Rosenwald, L. Gehrke, and N. Sonenberg. 1996. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc. Natl. Acad. Sci. USA 93:1065-1070.
36. Sonenberg, N., and A. C. Gingras. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10:268-275.
37. Strudwick, S., and K. L. Borden. 2002. The emerging roles of translation factor eIF4E in the nucleus. Differentiation 70:10-22.
38. Stuurman, N., A. de Graaf, A. Floore, A. Josso, B. Humbel, L. de Jong, and R. van Driel. 1992. A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies. J. Cell Sci. 101:773-784.
39. Tan, A., P. Bitterman, N. Sonenberg, M. Peterson, and V. Polunovsky. 2000. Inhibition of Myc-dependent apoptosis by eukaryotic translation initiation factor 4E requires cyclin D1. Oncogene 19:1437-1447.
40. Tanaka, T., T. Inazu, K. Yamada, Z. Myint, V. W. Keng, Y. Inoue, N. Taniguchi, and T. Noguchi. 1999. cDNA cloning and expression of rat homeobox gene, Hex, and functional characterization of the protein. Biochem. J. 339:111-117.
41. Thomas, P. Q., A. Brown, and R. S. Beddington. 1998. Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 125:85-94.
42. Topcu, Z., D. L. Mack, R. A. Hromas, and K. L. Borden. 1999. The promyelocytic leukemia protein PML interacts with the proline-rich homeodomain protein PRH: a RING may link hematopoiesis and growth control. Oncogene 18:7091-7100.
43. Topisirovic, I., A. D. Capili, and K. L. Borden. 2002. Gamma interferon and cadmium treatments modulate eukaryotic initiation factor 4E-dependent mRNA transport of cyclin D1 in a PML-dependent manner. Mol. Cell. Biol. 22:6183-6198.
44. Topisirovic, I., B. Culjkovic, N. Cohen, J. M. Perez, L. Skrabanek, and K. L. Borden. 2003. The proline-rich homeodomain protein, PRH, is a tissue-specific inhibitor of eIF4E-dependent cyclin D1 mRNA transport and growth. EMBO J. 22:689-703.
45. Wang, S., I. B. Rosenwald, M. J. Hutzler, G. A. Pihan, L. Savas, J. J. Chen, and B. A. Woda. 1999. Expression of the eukaryotic translation initiation factors 4E and 2α in non-Hodgkin's lymphomas. Am. J. Pathol. 155:247-255.
46. Ward, J. O., M. J. McConnell, G. W. Carlile, P. P. Pandolfi, J. D. Licht, and L. P. Freedman. 2001. The acute promyelocytic leukemia-associated protein, promyelocytic leukemia zinc finger, regulates 1,25-dihydroxyvitamin D3-induced monocytic differentiation of U937 cells through a physical interaction with vitamin D(3) receptor. Blood 98:3290-3300.
47. Yatskievych, T. A., S. Pascoe, and P. B. Antin. 1999. Expression of the homebox gene Hex during early stages of chick embryo development. Mech. Dev. 80:107-109.