Experimental Hematology
Volume 36, Issue 9 , Pages 1110-1120 , September 2008

E3 ligase FLRF (Rnf41) regulates differentiation of hematopoietic progenitors by governing steady-state levels of cytokine and retinoic acid receptors

Received 10 March 2008 ,Revised 1 April 2008 ,Accepted 1 April 2008.

References 

  1. Metcalf D. Lineage commitment of hemopoietic progenitor cells in developing blast cell colonies: influence of colony-stimulating factors. Proc Natl Acad Sci U S A. 1991;88:11310–11314
  2. Smithgall TE. Signal transduction pathways regulating hematopoietic differentiation. Pharmacol Rev. 1998;50:1–19
  3. Thomas D, Vadas M, Lopez A. Regulation of haematopoiesis by growth factors—emerging insights and therapies. Expert Opin Biol Ther. 2004;4:869–879
  4. Barreda DR, Hanington PC, Belosevic M. Regulation of myeloid development and function by colony stimulating factors. Dev Comp Immunol. 2004;28:509–554
  5. Richmond TD, Chohan M, Barber DL. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol. 2005;15:146–155
  6. Yasukawa H, Sasaki A, Yoshimura A. Negative regulation of cytokine signaling pathways. Annu Rev Immunol. 2000;18:143–164
  7. Jackson PK, Eldridge AG, Freed E, et al. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol. 2000;10:429–439
  8. Joazeiro CA, Weissman AM. RING finger proteins: mediators of ubiquitin ligase activity. Cell. 2000;102:549–552
  9. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem. 2000;70:503–533
  10. Ben-Neriah Y. Regulatory functions of ubiquitination in the immune system. Nat Immunol. 2002;3:20–26
  11. Sakamoto KM. Ubiquitin-dependent proteolysis: its role in human diseases and the design of therapeutic strategies. Mol Genet Metab. 2002;77:44–56
  12. Pagano M, Benmaamar R. When protein destruction runs amok, malignancy is on the loose. Cancer Cell. 2003;4:251–256
  13. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol. 2001;2:294–307
  14. Fang D, Wang HY, Fang N, Altman Y, Elly C, Liu YC. Cbl-b, a RING-type E3 ubiquitin ligase, targets phosphatidylinositol 3- kinase for ubiquitination in T cells. J Biol Chem. 2001;276:4872–4878
  15. Fang D, Liu YC. Proteolysis-independent regulation of PI3K by Cbl-b-mediated ubiquitination in T cells. Nat Immunol. 2001;2:870–875
  16. Fujimoto M, Naka T. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol. 2003;24:659–666
  17. Kubo M, Hanada T, Yoshimura A. Suppressors of cytokine signaling and immunity. Nat Immunol. 2003;4:1169–1176
  18. Alexander WS, Hilton DJ. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol. 2004;22:503–529
  19. Abdullah JM, Li X, Nachtman RG, Jurecic R. FLRF, a novel evolutionarily conserved RING finger gene, differentially expressed in mouse fetal and adult hematopoietic stem cells and progenitors. Blood Cells Mol Dis. 2001;27:320–333
  20. Diamonti AJ, Guy PM, Ivanof C, Wong K, Sweeney C, Carraway KL. An RBCC protein implicated in maintenance of steady-state neuregulin receptor levels. Proc Natl Acad Sci U S A. 2002;99:2866–2871
  21. Qiu XB, Goldberg AL. Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3. Proc Natl Acad Sci U S A. 2002;99:14843–14848
  22. Qiu XB, Markant SL, Yuan J, Goldberg AL. Nrdp1-mediated degradation of the gigantic IAP, BRUCE, is a novel pathway for triggering apoptosis. EMBO J. 2004;23:800–810
  23. Zhong L, Tan Y, Zhou A, Yu Q, Zhou J. RING finger ubiquitin-protein isopeptide ligase Nrdp1/FLRF regulates parkin stability and activity. J Biol Chem. 2005;280:9425–9430
  24. Tsai S, Bartelmez S, Sitnicka E, Collins S. Lymphohematopoietic progenitors immortalized by a retroviral vector harboring a dominant-negative retinoic acid receptor can recapitulate lymphoid, myeloid, and erythroid development. Genes Dev. 1994;8:2831–2841
  25. Zayas J, Spassov DS, Nachtman RG, Jurecic R. Hematopoietic stem cells and multipotent progenitors express new truncated intracellular form of c-kit receptor. Stem Cells Dev. 2008;17:351–361
  26. Christensen JL, Weissman IL. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A. 2001;98:14541–14546
  27. Terskikh AV, Miyamoto T, Chang C, Diatchenko L, Weissman IL. Gene expression analysis of purified hematopoietic stem cells and committed progenitors. Blood. 2003;102:94–101
  28. Tsai S. Differential effects of c-fms and c-kit ligands on the lineage development of the lymphohematopoietic cell line EML C1. Cancer Chemother Pharmacol. 1996;38(suppl):S58–S63
  29. Lawson ND, Krause DS, Berliner N. Normal neutrophil differentiation and secondary granule gene expression in the EML and MPRO cell lines. Exp Hematol. 1998;26:1178–1185
  30. Schmitt TM, Zuniga-Pflucker JC. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity. 2002;17:749–756
  31. Chiang MY, Monroe JG. BSAP/Pax5A expression blocks survival and expansion of early myeloid cells implicating its involvement in maintaining commitment to the B-lymphocyte lineage. Blood. 1999;94:3621–3632
  32. Pawlak G, Grasset MF, Arnaud S, Blanchet JP, Mouchiroud G. Receptor for macrophage colony-stimulating factor transduces a signal decreasing erythroid potential in the multipotent hematopoietic EML cell line. Exp Hematol. 2000;28:1164–1173
  33. Bourette RP, De Sepulveda P, Arnaud S, Dubreuil P, Rottapel R, Mouchiroud G. Suppressor of cytokine signaling 1 interacts with the macrophage colony-stimulating factor receptor and negatively regulates its proliferation signal. J Biol Chem. 2001;276:22133–22139
  34. Du Y, Campbell JL, Nalbant D, et al. Mapping gene expression patterns during myeloid differentiation using the EML hematopoietic progenitor cell line. Exp Hematol. 2002;30:649–658
  35. Kirito K, Fox N, Kaushansky K. Thrombopoietin stimulates Hoxb4 expression: an explanation for the favorable effects of TPO on hematopoietic stem cells. Blood. 2003;102:3172–3178
  36. Metcalf D. Clonal Culture of Hematopoietic Cells: Techniques and Applications. New York: Elsevier Press; 1984;
  37. Heyworth CM, Spooncer E. In vitro clonal assays for murine multipotential and lineage restricted myeloid progenitor cells. In:  Testa NG,  Molineux G editor. Haemopoiesis: A Practical Approach. Oxford, UK: IRL Press; 1993;p. 37–53
  38. Chen C, Sytkowski AJ. Erythropoietin regulation of Raf-1 and MEK: evidence for a Ras-independent mechanism. Blood. 2004;104:73–80
  39. Miyakawa Y, Rojnuckarin P, Habib T, Kaushansky K. Thrombopoietin induces phosphoinositol 3-kinase activation through SHP2, Gab, and insulin receptor substrate proteins in BAF3 cells and primary murine megakaryocytes. J Biol Chem. 2000;276:2494–2502
  40. Collins SJ. The role of retinoids and retinoic acid receptors in normal hematopoiesis. Leukemia. 2002;16:1896–1905
  41. Klein ES, Wang JW, Khalifa B, Gavigan SA, Chandraratna RA. Recruitment of nuclear receptor corepressor and coactivator to the retinoic acid receptor by retinoid ligands. Influence of DNA-heterodimer interactions. J Biol Chem. 2000;275:19401–19408
  42. Zhu J, Gianni M, Kopf E, et al. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RAR alpha) and oncogenic RAR alpha fusion proteins. Proc Natl Acad Sci U S A. 1999;96:14807–14812
  43. Zandstra PW, Lauffenburger DA, Eaves CJ. A ligand-receptor signaling threshold model of stem cell differentiation control: a biologically conserved mechanism applicable to hematopoiesis. Blood. 2000;96:1215–1222
  44. Viswanathan S, Benatar T, Rose-John S, Lauffenburger DA, Zandstra PW. Ligand/receptor signaling threshold (LIST) model accounts for gp130-mediated embryonic stem cell self-renewal responses to LIF and HIL-6. Stem Cells. 2002;20:119–138
  45. Rubin C, Gur G, Yarden Y. Negative regulation of receptor tyrosine kinases: unexpected links to c-Cbl and receptor ubiquitylation. Cell Res. 2005;15:66–71
  46. Katz M, Shtiegman K, Tal-Or P, et al. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic. 2002;3:740–751
  47. Liu J, Plotnikov A, Banerjee A, et al. Ligand-independent pathway that controls stability of interferon alpha receptor. Biochem Biophys Res Commun. 2008;367:388–393
  48. Cao Z, Wu X, Yen L, Sweeney C, Carraway KL. Neuregulin-induced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol Cell Biol. 2007;27:2180–2188
  49. Johnson BS, Mueller L, Si J, Collins SJ. The cytokines IL-3 and GM-CSF regulate the transcriptional activity of retinoic acid receptors in different in vitro models of myeloid differentiation. Blood. 2002;99:746–753
  50. Jutong S, Collins SJ. IL-3–induced enhancement of retinoic acid receptor activity is mediated through Stat5, which physically associates with retinoic acid receptors in an IL-3–dependent manner. Blood. 2003;100:4401–4409
  51. Ferrucci PF, Grignani F, Pearson M, Fagioli M, Nicoletti I, Pelicci PG. Cell death induction by the acute promyelocytic leukemia-specific PML/RARalpha fusion protein. Proc Natl Acad Sci U S A. 1997;94:10901–10906
  52. Fanelli M, Minucci S, Gelmetti V, Nervi C, Gambacorti-Passerini C, Pelicci PG. Constitutive degradation of PML/RARalpha through the proteasome pathway mediates retinoic acid resistance. Blood. 1999;93:1477–1481
  53. Fenaux P, Wang ZZ, Degos L. Treatment of acute promyelocytic leukemia by retinoids. Curr Top Microbiol Immunol. 2007;313:101–128
  54. Scaglioni PP, Pandolfi PP. The theory of APL revisited. Curr Top Microbiol Immunol. 2007;313:85–100
  55. Alcalay M, Meani N, Gelmetti V, et al. Acute myeloid leukemia fusion proteins deregulate genes involved in stem cell maintenance and DNA repair. J Clin Invest. 2003;112:1751–1761
  56. Yen L, Cao Z, Wu X, et al. Loss of Nrdp1 enhances ErbB2/ErbB3-dependent breast tumor cell growth. Cancer Res. 2006;66:11279–11286

PII: S0301-472X(08)00155-0

doi: 10.1016/j.exphem.2008.04.001

Experimental Hematology
Volume 36, Issue 9 , Pages 1110-1120 , September 2008