Comparative proteomic analysis of all-trans-retinoic acid treatment reveals systematic posttranscriptional control mechanisms in acute promyelocytic leukemia

Blood

Volumn 104, Issue 5, 2004, Pages 1314-1323

  Harris, Michael N ^c   Ozpolat, Bulent ^c   Abdi, Fadi ^c   Gu, Sheng ^c   Legler, Allison ^c   Mawuenyega, Kwasi G ^c   Tirado Gomez, Maribel ^c   Lopez Berestein, Gabriel ^b   Chen, Xian ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

DEATH ASSOCIATED PROTEIN KINASE; DEATH ASSOCIATED PROTEIN KINASE 5; ELONGATION FACTOR; ELONGATION FACTOR 1DELTA; ELONGATION FACTOR 1GAMMA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN F; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U2; HYBRID PROTEIN; INITIATION FACTOR 2; INITIATION FACTOR 4A; INITIATION FACTOR 4A1; INITIATION FACTOR 4G; INITIATION FACTOR 5; INITIATION FACTOR 6; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE 2A; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN 14 3 3; PROTEIN 14 3 3DELTA; PROTEIN 14 3 3EPSILON; PROTEIN 14 3 3THETA; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CELL DIFFERENTIATION; ELECTROSPRAY MASS SPECTROMETRY; EUKARYOTIC CELL; GEL ELECTROPHORESIS; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE;

EID: 4444363680     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-01-0046     Document Type: Article

References (76)

1. Rowley JD, Golomb HM, Dougherty C. 15/17 translocation, a consistent chromosomal change in acute promyelocytic leukaemia. Lancet. 1977;1:549-550.
2. Melnick A, Licht JD. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood. 1999;93:3167-3215.
3. Dyck JA, Maul GG, Miller WH Jr, Chen JD, Kakizuka A, Evans RM. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell. 1994;76:333-343.
4. Grignani F, Ferrucci PF, Testa U, et al. The acute promyelocytic leukemia-specific PML-RAR alpha fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell. 1993;74:423-431.
5. Altucci L, Gronemeyer H. The promise of retinoids to fight against cancer. Nat Rev Cancer. 2001;1:181-193.
6. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 1996;10:940-954.
7. Breitman TR, Collins SJ, Keene BR. Terminal differentiation of human promyelocytic leukemic cells in primary culture in response to retinoic acid. Blood. 1981;57:1000-1004.
8. Tallman MS, Andersen JW, Schiffer CA, et al. All-trans retinoic acid in acute promyelocytic leukemia: long-term outcome and prognostic factor analysis from the North American Intergroup protocol. Blood. 2002;100:4298-4302.
9. Yoshida H, Kitamura K, Tanaka K, et al. Accelerated degradation of PML-retinoic acid receptor alpha (PML-RARA) oncoprotein by all-trans-retinoic acid in acute promyelocytic leukemia: possible role of the proteasome pathway. Cancer Res. 1996;56:2945-2948.
10. Grignani F, De Matteis S, Nervi C, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature. 1998;391:815-818.
11. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 1997;389:349-352.
12. Heinzel T, Lavinsky RM, Mullen TM, et al. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature. 1997;387:43-48.
13. Kouzarides T. Histone acetylases and deacetylases in cell proliferation. Curr Opin Genet Dev. 1999;9:40-48.
14. Collingwood TN, Urnov FD, Wolffe AP. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription. J Mol Endocrinol. 1999;23:255-275.
15. Glass CK, Rosenfeld MG, Rose DW, et al. Mechanisms of transcriptional activation by retinoic acid receptors. Biochem Soc Trans. 1997;25:602-605.
16. Glass CK, Rose DW, Rosenfeld MG. Nuclear receptor coactivators. Curr Opin Cell Biol. 1997;9:222-232.
17. Nagy L, Kao HY, Chakravarti D, et al. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell. 1997;89:373-380.
18. Casini T, Pelicci PG. A function of p21 during promyelocytic leukemia cell differentiation independent of CDK inhibition and cell cycle arrest. Oncogene. 1999;18:3235-3243.
19. Duprez E, Wagner K, Koch H, Tenen DG. C/EBP-beta: a major PML-RARA-responsive gene in retinoic acid-induced differentiation of APL cells. EMBO J. 2003;22:5806-5816.
20. Morosetti R, Park DJ, Chumakov AM, et al. A novel, myeloid transcription factor, C/EBP epsilon, is upregulated during granulocytic, but not monocytic, differentiation. Blood. 1997;90:2591-2600.
21. Pelicano L, Li F, Schindler C, Chelbi-Alix MK. Retinoic acid enhances the expression of interferon-induced proteins: evidence for multiple mechanisms of action. Oncogene. 1997;15:2349-2359.
22. Weis K, Rambaud S, Lavau C, et al. Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell. 1994;76:345-356.
23. Liu TX, Zhang JW, Tao J, et al. Gene expression networks underlying retinoic acid-induced differentiation of acute promyelocytic leukemia cells. Blood. 2000;96:1496-1504.
24. Yang L, Zhao H, Li SW, et al. Gene expression profiling during all-trans retinoic acid-induced cell differentiation of acute promyelocytic leukemia cells. J Mol Diagn. 2003;5:212-221.
25. Lee KH, Chang MY, Ahn JI, et al. Differential gene expression in retinoic acid-induced differentiation of acute promyelocytic leukemia cells, NB4 and HL-60 cells. Biochem Biophys Res Commun. 2002;296:1125-1133.
26. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol. 1999;19:1720-1730.
27. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature. 2003;422:198-207.
28. Verrills NM, Walsh BJ, Cobon GS, Hains PG, Kavallaris M. Proteome analysis of vinca alkaloid response and resistance in acute lymphoblastic leukemia reveals novel cytoskeletal alterations. J Biol Chem. 2003;278:45082-45093.
29. Chen X, Smith LM, Bradbury EM. Site-specific mass tagging with stable isotopes in proteins for accurate and efficient protein identification. Anal Chem. 2000;72:1134-1143.
30. Gu S, Pan S, Bradbury EM, Chen X. Precise peptide sequencing and protein quantification in the human proteome through in vivo lysine-specific mass tagging. J Am Soc Mass Spectrom. 2003;14:1-7.
31. Zhu H, Pan S, Gu S, Bradbury EM, Chen X. Amino acid residue specific stable isotope labeling for quantitative proteomics. Rapid Commun Mass Spectrom. 2002;16:2115-2123.
32. Bae W, Chen X. Proteomic study for the cellular responses to Cd2+ in schizosaccharomyces pombe through amino acid-coded mass tagging and LC-MS/MS. Mol Cell Proteomics. 2004;3:596-607.
33. Ozpolat B, Actor JK, Rao XM, et al. Quantitation of Helicobacter pylori in the stomach using quantitative polymerase chain reaction assays. Helicobacter. 2000;5:13-21.
34. Ozpolat B, Mehta K, Tari AM, Lopez-Berestein G. all-trans-Retinoic acid-induced expression and regulation of retinoic acid 4-hydroxylase (CYP26) in human promyelocytic leukemia. Am J Hematol. 2002;70:39-47.
35. Gotham SM, Fryer PJ, Paterson WR. The measurement of insoluble proteins using a modified Bradford assay. Anal Biochem. 1988;173:353-358.
36. Link AJ. 2-D proteome analysis protocols. Totowa, NJ: Humana Press; 1999.
37. Toothaker LE, Gonzalez DA, Tung N, et al. Cellular myosin heavy chain in human leukocytes: isolation of 5′ cDNA clones, characterization of the protein, chromosomal localization, and upregulation during myeloid differentiation. Blood. 1991;78:1826-1833.
38. Perrotti D, Bonatti S, Trotta R, et al. TLS/FUS, a pro-oncogene involved in multiple chromosomal translocations, is a novel regulator of BCR/ABL-mediated leukemogenesis. EMBO J. 1998;17:4442-4455.
39. Perrotti D, Calabretta B. Post-transcriptional mechanisms in BCR/ABL leukemogenesis: role of shuttling RNA-binding proteins. Oncogene. 2002;21:8577-8583.
40. Perrotti D, Cesi V, Trotta R, et al. BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nat Genet. 2002;30:48-58.
41. Kim JH, Paek KY, Choi K, et al. Heterogeneous nuclear ribonucleoprotein C modulates translation of c-myc mRNA in a cell cycle phase-dependent manner. Mol Cell Biol. 2003;23:708-720.
42. Evans JR, Mitchell SA, Spriggs KA, et al. Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo. Oncogene. 2003;22:8012-8020.
43. Dimberg A, Bahram F, Karlberg I, Larsson LG, Nilsson K, Oberg F. Retinoic acid-induced cell cycle arrest of human myeloid cell lines is associated with sequential down-regulation of c-Myc and cyclin E and posttranscriptional up-regulation of p27(Kip1). Blood. 2002;99:2199-2206.
44. Linder P, Lasko PF, Ashburner M, et al. Birth of the D-E-A-D box. Nature. 1989;337:121-122.
45. Rozen F, Edery I, Meerovitch K, Dever TE, Merrick WC, Sonenberg N. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol. 1990;10:1134-1144.
46. Rogers GW Jr, Komar AA, Merrick WC. eIF4A: the godfather of the DEAD box helicases. Prog Nucleic Acid Res Mol Biol. 2002;72:307-331.
47. De Gregorio E, Preiss T, Hentze MW. Translational activation of uncapped mRNAs by the central part of human eIF4G is 5′ end-dependent. RNA. 1998;4:828-836.
48. De Gregorio E, Preiss T, Hentze MW. Translation driven by an eIF4G core domain in vivo. EMBO J. 1999;18:4865-4874.
49. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J. 1999;18:270-279.
50. Morino S, Imataka H, Svitkin YV, Pestova TV, Sonenberg N. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol Cell Biol. 2000;20:468-477.
51. Li W, Belsham GJ, Proud CG. Eukaryotic initiation factors 4A (eIF4A) and 4G (eIF4G) mutually interact in a 1:1 ratio in vivo. J Biol Chem. 2001;276:29111-29115.
52. Imataka H, Olsen HS, Sonenberg N. A new translational regulator with homology to eukaryotic translation initiation factor 4G. EMBO J. 1997;16:817-825.
53. Graff JR, Zimmer SG. Translational control and metastatic progression: enhanced activity of the mRNA cap-binding protein eIF-4E selectively enhances translation of metastasis-related mRNAs. Clin Exp Metastasis. 2003;20:265-273.
54. Sheu GT, Traugh JA. Recombinant subunits of mammalian elongation factor 1 expressed in Escherichia coli: subunit interactions, elongation activity, and phosphorylation by protein kinase CKII. J Biol Chem. 1997;272:33290-33297.
55. Browne GJ, Proud CG. Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem. 2002;269:5360-5368.
56. Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell. 2002;108:557-572.
57. Jing Y, Xia L, Lu M, Waxman S. The cleavage product deltaPML-RARalpha contributes to all-trans retinoic acid-mediated differentiation in acute promyelocytic leukemia cells. Oncogene. 2003;22:4083-4091.
58. Quignon F, De Bels F, Koken M, Feunteun J, Ameisen JC, de The H. PML induces a novel caspase-independent death process. Nat Genet. 1998;20:259-265.
59. Strudwick S, Borden KL. Finding a role for PML in APL pathogenesis: a critical assessment of potential PML activities. Leukemia. 2002;16:1906-1917.
60. Lai HK, Borden KL. The promyelocytic leukemia (PML) protein suppresses cyclin D1 protein production by altering the nuclear cytoplasmic distribution of cyclin D1 mRNA. Oncogene. 2000;19:1623-1634.
61. Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N. 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 U S A. 1996;93:1065-1070.
62. Topisirovic I, Culjkovic B, Cohen N, Perez JM, Skrabanek L, Borden KL. The proline-rich homeodomain protein, PRH, is a tissue-specific inhibitor of eIF4E-dependent cyclin D1 mRNA transport and growth. EMBO J. 2003;22:689-703.
63. Eberle J, Krasagakis K, Orfanos CE. Translation initiation factor eIF-4A1 mRNA is consistently overexpressed in human melanoma cells in vitro. Int J Cancer. 1997;71:396-401.
64. De Benedetti A, Harris AL. eIF4E expression in tumors: its possible role in progression of malignancies. Int J Biochem Cell Biol. 1999;31:59-72.
65. Bauer C, Brass N, Diesinger I, Kayser K, Grasser FA, Meese E. Overexpression of the eukaryotic translation initiation factor 4G (eIF4G-1) in squamous cell lung carcinoma. Int J Cancer. 2002;98:181-185.
66. Mologni L, Ponzanelli I, Bresciani F, et al. The novel synthetic retinoid 6-[3-adamantyl-4-hydroxyphenyl]-2-naphthalene carboxylic acid (CD437) causes apoptosis in acute promyelocytic leukemia cells through rapid activation of caspases. Blood. 1999;93:1045-1061.
67. Gianni M, Ponzanelli I, Mologni L, et al. Retinoid-dependent growth inhibition, differentiation and apoptosis in acute promyelocytic leukemia cells: expression and activation of caspases. Cell Death Differ. 2000;7:447-460.
68. Wan J, Wang J, Cheng H, et al. Proteomic analysis of apoptosis initiation induced by all-trans retinoic acid in human acute promyelocytic leukemia cells. Electrophoresis. 2001;22:3026-3037.
69. Isobe T, Hiyane Y, Ichimura T, et al. Activation of protein kinase C by the 14-3-3 proteins homologous with Exo1 protein that stimulates calcium-dependent exocytosis. FEBS Lett. 1992;308:121-124.
70. Van Der Hoeven PC, Van Der Wal JC, Ruurs P, Van Blitterswijk WJ. Protein kinase C activation by acidic proteins including 14-3-3. Biochem J. 2000;347(pt 3):781-785.
71. Tanji M, Horwitz R, Rosenfeld G, Waymire JC. Activation of protein kinase C by purified bovine brain 14-3-3: comparison with tyrosine hydroxylase activation. J Neurochem. 1994;63:1908-1916.
72. Gannon-Murakami L, Murakami K. Selective association of protein kinase C with 14-3-3 zeta in neuronally differentiated PC12 cells: stimulatory and inhibitory effect of 14-3-3 zeta in vivo. J Biol Chem. 2002;277:23116-23122.
73. Dai JG, Murakami K. Constitutively and autonomously active protein kinase C associated with 14-3-3 zeta in the rodent brain. J Neurochem. 2003;84:23-34.
74. Barragan M, Bellosillo B, Campas C, Colomer D, Pons G, Gil J. Involvement of protein kinase C and phosphatidylinositol 3-kinase pathways in the survival of B-cell chronic lymphocytic leukemia cells. Blood. 2002;99:2969-2976.
75. Barragan M, Campas C, Bellosillo B, Gil J. Protein kinases in the regulation of apoptosis in B-cell chronic lymphocytic leukemia. Leuk Lymphoma. 2003;44:1865-1870.
76. Amin HM, Ergin M, Denning MF, Quevedo ME, Alkan S. Characterization of apoptosis induced by protein kinase C inhibitors and its modulation by the caspase pathway in acute promyelocytic leukaemia. Br J Haematol. 2000;110:552-562.