Increased c-Jun expression and reduced GATA2 expression promote aberrant monocytic differentiation induced by activating PTPN11 mutants

Molecular and Cellular Biology

Volumn 29, Issue 16, 2009, Pages 4376-4393

  Yang, Zhenyun ^a,b   Kondo, Takako ^a   Voorhorst, Cara S ^a,b   Nabinger, Sarah C ^a,b   Ndong, Leila ^b   Yin, Fuqin ^a,b   Chan, Edward M ^c   Yu, Menggang ^a   Würstlin, Oliver ^d   Kratz, Christian P ^d   Niemeyer, Charlotte M ^d   Flotho, Christian ^d   Hashino, Eri ^a   Chan, Rebecca J ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ELI LILLY AND COMPANY   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; COLONY STIMULATING FACTOR RECEPTOR; LUCIFERASE; MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; MUTANT PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL STRAIN 3T3; COLONY FORMING UNIT M; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME BINDING; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECEPTOR GENE; WILD TYPE; ZINC FINGER MOTIF;

ANIMALS; ANTHRACENES; CELL DIFFERENTIATION; CHILD; ENZYME ACTIVATION; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; INFANT; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEUKEMIA, MYELOMONOCYTIC, JUVENILE; MAST CELLS; MICE; MONOCYTES; MUTATION; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RAS PROTEINS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR;

MURINAE;

EID: 68949100415     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01330-08     Document Type: Article

References (76)

1. Albajar, M., P. Gutierrez, C. Richard, M. Rosa-Garrido, M. T. Gomez-Casares, J. L. Steegmann, J. Leon, and M. D. Delgado. 2008. PU.1 expression is restored upon treatment of chronic myeloid leukemia patients. Cancer Lett. 270:328-336.
2. Altman, A. J., C. G. Palmer, and R. L. Baehner. 1974. Juvenile "chronic granulocytic" leukemia: a panmyelopathy with prominent monocytic involvement and circulating monocyte colony-forming cells. Blood 43:341-350.
3. Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55:875-885.
4. Bassuk, A. G., and J. M. Leiden. 1995. A direct physical association between ETS and AP-1 transcription factors in normal human T cells. Immunity 3:223-237.
5. Behre, G., A. J. Whitmarsh, M. P. Coghlan, T. Hoang, C. L. Carpenter, D. E. Zhang, R. J. Davis, and D. G. Tenen. 1999. c-Jun is a JNK-independent coactivator of the PU.1 transcription factor. J. Biol. Chem. 274:4939-4946.
6. Bergstraesser, E., H. Hasle, T. Rogge, A. Fischer, M. Zimmermann, P. Noellke, and C. M. Niemeyer. 2007. Non-hematopoietic stem cell transplantation treatment of juvenile myelomonocytic leukemia: a retrospective analysis and definition of response criteria. Pediatr. Blood Cancer 49:629-633.
7. Binetruy, B., T. Smeal, and M. Karin. 1991. Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature 351:122-127.
8. Braun, B. S., D. A. Tuveson, N. Kong, D. T. Le, S. C. Kogan, J. Rozmus, M. M. Le Beau, T. E. Jacks, and K. M. Shannon. 2004. Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc. Natl. Acad. Sci. USA 101:597-602.
9. Brodeur, G. M. 1994. The NF1 gene in myelopoiesis and childhood myelodysplastic syndromes. N. Engl. J. Med. 330:637-639.
10. Burgess, G. S., E. A. Williamson, L. D. Cripe, S. Litz-Jackson, J. A. Bhatt, K. Stanley, M. J. Stewart, A. S. Kraft, H. Nakshatri, and H. S. Boswell. 1998. Regulation of the c-jun gene in p210 BCR-ABL transformed cells corresponds with activity of JNK, the c-jun N-terminal kinase. Blood 92:2450-2460.
11. Chan, E. M., E. M. Comer, F. C. Brown, K. E. Richkind, M. L. Holmes, B. H. Chong, R. Shiffman, D. E. Zhang, M. L. Slovak, C. L. Willman, C. T. Noguchi, Y. Li, D. J. Heiber, L. Kwan, R. J. Chan, G. H. Vance, H. C. Ramsey, and R. A. Hromas. 2005. AML1-FOG2 fusion protein in myelodysplasia. Blood 105:4523-4526.
12. Chan, G., D. Kalaitzidis, T. Usenko, J. L. Kutok, W. Yang, M. G. Mohi, and B. G. Neel. 2009. Leukemogenic Ptpn11 causes fatal myeloproliferative disorder via cell-autonomous effects on multiple stages of hematopoiesis. Blood 113:4414-4424.
13. Chan, R. J., S. A. Johnson, Y. Li, M. C. Yoder, and G. S. Feng. 2003. A definitive role of Shp-2 tyrosine phosphatase in mediating embryonic stem cell differentiation and hematopoiesis. Blood 102:2074-2080.
14. Chan, R. J., M. B. Leedy, V. Munugalavadla, C. S. Voorhorst, Y. Li, M. Yu, and R. Kapur. 2005. Human somatic PTPN11 mutations induce hematopoietic-cell hypersensitivity to granulocyte-macrophage colony-stimulating factor. Blood 105:3737-3742.
15. Chang, H. C., S. Zhang, V. T. Thieu, R. B. Slee, H. A. Bruns, R. N. Laribee, M. J. Klemsz, and M. H. Kaplan. 2005. PU.1 expression delineates heterogeneity in primary Th2 cells. Immunity 22:693-703.
16. Dahl, R., J. C. Walsh, D. Lancki, P. Laslo, S. R. Iyer, H. Singh, and M. C. Simon. 2003. Regulation of macrophage and neutrophil cell fates by the PU.1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nat. Immunol. 4:1029-1036.
17. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288:1439-1441.
18. Della Ragione, F., V. Criniti, V. Della Pietra, A. Borriello, A. Oliva, S. Indaco, T. Yamamoto, and V. Zappia. 2001. Genes modulated by histone acetylation as new effectors of butyrate activity. FEBS Lett. 499:199-204.
19. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
20. Derijard, B., J. Raingeaud, T. Barrett, I. H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682-685.
21. Donovan, S., W. See, J. Bonifas, D. Stokoe, and K. M. Shannon. 2002. Hyperactivation of protein kinase B and ERK have discrete effects on survival, proliferation, and cytokine expression in Nf1-deficient myeloid cells. Cancer Cell 2:507-514.
22. Dorrell, C., K. Takenaka, M. D. Minden, R. G. Hawley, and J. E. Dick. 2004. Hematopoietic cell fate and the initiation of leukemic properties in primitive primary human cells are influenced by Ras activity and farnesyltransferase inhibition. Mol. Cell. Biol. 24:6993-7002.
23. Eickhoff, B., S. Ruller, T. Laue, G. Kohler, C. Stahl, M. Schlaak, and J. van der Bosch. 2000. Trichostatin A modulates expression of p21waf1/cip1, BclxL, ID1, ID2, ID3, CRAB2, GATA-2, hsp86 and TFIID/TAFII31 mRNA in human lung adenocarcinoma cells. Biol. Chem. 381:107-112.
24. Emanuel, P. D., L. J. Bates, R. P. Castleberry, R. J. Gualtieri, and K. S. Zuckerman. 1991. Selective hypersensitivity to granulocyte-macrophage colony-stimulating factor by juvenile chronic myeloid leukemia hematopoietic progenitors. Blood 77:925-929.
25. Emanuel, P. D., L. J. Bates, S. W. Zhu, R. P. Castleberry, R. J. Gualtieri, and K. S. Zuckerman. 1991. The role of monocyte-derived hemopoietic growth factors in the regulation of myeloproliferation in juvenile chronic myelogenous leukemia. Exp. Hematol. 19:1017-1024.
26. Estrov, Z., T. Grunberger, H. S. Chan, and M. H. Freedman. 1986. Juvenile chronic myelogenous leukemia: characterization of the disease using cell cultures. Blood 67:1382-1387.
27. Freedman, M. H., A. Cohen, T. Grunberger, N. Bunin, R. E. Luddy, E. F. Saunders, N. Shahidi, A. Lau, and Z. Estrov. 1992. Central role of tumour necrosis factor, GM-CSF, and interleukin 1 in the pathogenesis of juvenile chronic myelogenous leukaemia. Br. J. Haematol. 80:40-48.
28. Gaynor, R., K. Simon, and P. Koeffler. 1991. Expression of c-jun during macrophage differentiation of HL-60 cells. Blood 77:2618-2623.
29. Grondin, B., M. Lefrancois, M. Tremblay, M. Saint-Denis, A. Haman, K. Waga, A. Bedard, D. G. Tenen, and T. Hoang. 2007. c-Jun homodimers can function as a context-specific coactivator. Mol. Cell. Biol. 27:2919-2933.
30. Hattori, K., P. Angel, M. M. Le Beau, and M. Karin. 1988. Structure and chromosomal localization of the functional intronless human JUN protooncogene. Proc. Natl. Acad. Sci. USA 85:9148-9152.
31. Hawley, R. G., A. Z. Fong, B. Y. Ngan, and T. S. Hawley. 1995. Hematopoietic transforming potential of activated ras in chimeric mice. Oncogene 11:1113-1123.
32. Hess, J. L., M. M. Zutter, R. P. Castleberry, and P. D. Emanuel. 1996. Juvenile chronic myelogenous leukemia. Am. J. Clin. Pathol. 105:238-248.
33. Hibi, S., J. Lohler, J. Friel, C. Stocking, and W. Ostertag. 1993. Induction of monocytic differentiation and tumorigenicity by v-Ha-ras in differentiation arrested hematopoietic cells. Blood 81:1841-1848.
34. Kitajima, K., M. Tanaka, J. Zheng, H. Yen, A. Sato, D. Sugiyama, H. Umehara, E. Sakai, and T. Nakano. 2006. Redirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2. Blood. 107: 1857-1863.
35. Koike, K., and K. Matsuda. 2008. Recent advances in the pathogenesis and management of juvenile myelomonocytic leukaemia. Br. J. Haematol. 141: 567-575.
36. Kratz, C. P., C. M. Niemeyer, R. P. Castleberry, M. Cetin, E. Bergstrasser, P. D. Emanuel, H. Hasle, G. Kardos, C. Klein, S. Kojima, J. Stary, M. Trebo, M. Zecca, B. D. Gelb, M. Tartaglia, and M. L. Loh. 2005. The mutational spectrum of PTPN11 in juvenile myelomonocytic leukemia and Noonan syndrome/myeloproliferative disease. Blood 106:2183-2185.
37. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dai, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodgett. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369:156-160.
38. Le, D. T., N. Kong, Y. Zhu, J. O. Lauchle, A. Aiyigari, B. S. Braun, E. Wang, S. C. Kogan, M. M. Le Beau, L. Parada, and K. M. Shannon. 2004. Somatic inactivation of Nf1 in hematopoietic cells results in a progressive myeloproliferative disorder. Blood 103:4243-4250.
39. Li, J., I. King, and A. C. Sartorelli. 1994. Differentiation of WEHI-3B D+ myelomonocytic leukemia cells induced by ectopic expression of the protooncogene c-jun. Cell Growth Differ. 5:743-751.
40. Liew, C. W., K. D. Rand, R. J. Simpson, W. W. Yung, R. E. Mansfield, M. Crossley, M. Proetorius-Ibba, C. Nerlov, F. M. Poulsen, and J. P. Mackay. 2006. Molecular analysis of the interaction between the hematopoietic master transcription factors GATA-1 and PU.1. J. Biol. Chem. 281:28296-28306.
41. Locatelli, F., P. Nollke, M. Zecca, E. Korthof, E. Lanino, C. Peters, A. Pession, H. Kabisch, C. Uderzo, C. S. Bonfim, P. Bader, D. Dilloo, J. Stary, A. Fischer, T. Revesz, M. Fuhrer, H. Hasle, M. Trebo, M. M. van den Heuvel-Eibrink, S. Fenu, B. Strahm, G. Giorgiani, M. R. Bonora, U. Duffner, and C. M. Niemeyer. 2005. Hematopoietic stem cell transplantation (HSCT) in children with juvenile myelomonocytic leukemia (JMML): results of the EWOG-MDS/EBMT trial. Blood 105:410-419.
42. Loh, M. L., S. Vattikuti, S. Schubbert, M. G. Reynolds, E. Carlson, K. H. Lieuw, J. W. Cheng, C. M. Lee, D. Stokoe, J. M. Bonifas, N. P. Curtiss, J. Gotlib, S. Meshinchi, M. M. Le Beau, P. D. Emanuel, and K. M. Shannon. 2004. Mutations in PTPN11 implicate the SHP-2 phosphatase in leukemogenesis. Blood 103:2325-2331.
43. Lord, K. A., A. Abdollahi, B. Hoffman-Liebermann, and D. A. Liebermann. 1993. Proto-oncogenes of the fos/jun family of transcription factors are positive regulators of myeloid differentiation. Mol. Cell. Biol. 13:841-851.
44. Maher, J., D. Baker, N. Dibb, and I. Roberts. 1996. Mutant ras promotes haemopoietic cell proliferation or differentiation in a cell-specific manner. Leukemia 10:83-90.
45. Mohi, M. G., I. R. Williams, C. R. Dearolf, G. Chan, J. L. Kutok, S. Cohen, K. Morgan, C. Boulton, H. Shigematsu, H. Keilhack, K. Akashi, D. G. Gilliland, and B. G. Neel. 2005. Prognostic, therapeutic, and mechanistic implications of a mouse model of leukemia evoked by Shp2 (PTPN11) mutations. Cancer Cell 7:179-191.
46. Mollinedo, F., C. Gajate, A. Tugores, I. Flores, and J. R. Naranjo. 1993. Differences in expression of transcription factor AP-1 in human promyelocytic HL-60 cells during differentiation towards macrophages versus granulocytes. Biochem. J. 294:137-144.
47. Montgomery, D. C. 1997. Design and analysis of experiments, 4th ed. John Wiley & Sons, Inc., New York, NY.
48. Mueller, B. U., T. Pabst, M. Osato, N. Asou, L. M. Johansen, M. D. Minden, G. Behre, W. Hiddemann, Y. Ito, and D. G. Tenen. 2002. Heterozygous PU.1 mutations are associated with acute myeloid leukemia. Blood 100:998-1007.
49. Niemeyer, C. M., and C. P. Kratz. 2008. Paediatric myelodysplastic syndromes and juvenile myelomonocytic leukaemia: molecular classification and treatment options. Br. J. Haematol. 140:610-624.
50. Passegue, E., W. Jochum, M. Schorpp-Kistner, U. Mohle-Steinlein, and E. F. Wagner. 2001. Chronic myeloid leukemia with increased granulocyte progenitors in mice lacking junB expression in the myeloid lineage. Cell 104: 21-32.
51. Persons, D. A., J. A. Allay, E. R. Allay, R. A. Ashmun, D. Orlic, S. M. Jane, J. M. Cunningham, and A. W. Nienhuis. 1999. Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood 93:488-499.
52. Raitano, A. B., J. R. Halpern, T. M. Hambuch, and C. L. Sawyers. 1995. The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc. Natl. Acad. Sci. USA 92:11746-11750.
53. Reddy, V. A., A. Iwama, G. Iotzova, M. Schulz, A. Elsasser, R. K. Vangala, D. G. Tenen, W. Hiddemann, and G. Behre. 2002. Granulocyte inducer C/EBPalpha inactivates the myeloid master regulator PU.1: possible role in lineage commitment decisions. Blood 100:483-490.
54. Rosenbauer, F., K. Wagner, J. L. Kutok, H. Iwasaki, M. M. Le Beau, Y. Okuno, K. Akashi, S. Fiering, and D. G. Tenen. 2004. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat. Genet. 36:624-630.
55. Schubbert, S., K. Lieuw, S. L. Rowe, C. M. Lee, X. Li, M. L. Loh, D. W. Clapp, and K. M. Shannon. 2005. Functional analysis of leukemia-associated PTPN11 mutations in primary hematopoietic cells. Blood 106:311-317.
56. Sebastian, C., M. Serra, A. Yeramian, N. Serrat, J. Lloberas, and A. Celada. 2008. Deacetylase activity is required for STAT5-dependent GM-CSF functional activity in macrophages and differentiation to dendritic cells. J. Immunol. 180:5898-5906.
57. Shannon, K. M., P. O'Connell, G. A. Martin, D. Paderanga, K. Olson, P. Dinndorf, and F. McCormick. 1994. Loss of the normal NF1 allele from the bone marrow of children with type 1 neurofibromatosis and malignant myeloid disorders. N. Engl. J. Med. 330:597-601.
58. Sheng, X. M., M. Kawamura, H. Ohnishi, K. Ida, R. Hanada, S. Kojima, M. Kobayashi, F. Bessho, M. Yanagisawa, and Y. Hayashi. 1997. Mutations of the RAS genes in childhood acute myeloid leukemia, myelodysplastic syndrome and juvenile chronic myelocytic leukemia. Leuk. Res. 21:697-701.
59. Shi, Z. Q., D. H. Yu, M. Park, M. Marshall, and G. S. Feng. 2000. Molecular mechanism for the Shp-2 tyrosine phosphatase function in promoting growth factor stimulation of Erk activity. Mol. Cell. Biol. 20:1526-1536.
60. Side, L., B. Taylor, M. Cayouette, E. Conner, P. Thompson, M. Luce, and K. Shannon. 1997. Homozygous inactivation of the NF1 gene in bone marrow cells from children with neurofibromatosis type 1 and malignant myeloid disorders. N. Engl. J. Med. 336:1713-1720.
61. Skorski, T., C. Szczylik, M. Z. Ratajczak, L. Malaguarnera, A. M. Gewirtz, and B. Calabretta. 1992. Growth factor-dependent inhibition of normal hematopoiesis by N-ras antisense oligodeoxynucleotides. J. Exp. Med. 175: 743-750.
62. Smeal, T., B. Binetruy, D. A. Mercola, M. Birrer, and M. Karin. 1991. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature 354:494-496.
63. Steidl, U., F. Rosenbauer, R. G. Verhaak, X. Gu, A. Ebralidze, H. H. Otu, S. Klippel, C. Steidl, I. Bruns, D. B. Costa, K. Wagner, M. Aivado, G. Kobbe, P. J. Valk, E. Passegue, T. A. Libermann, R. Delwel, and D. G. Tenen. 2006. Essential role of Jun family transcription factors in PU.1 knockdown-induced leukemic stem cells. Nat. Genet. 38:1269-1277.
64. Steidl, U., C. Steidl, A. Ebralidze, B. Chapuy, H. J. Han, B. Will, F. Rosenbauer, A. Becker, K. Wagner, S. Koschmieder, S. Kobayashi, D. B. Costa, T. Schulz, K. B. O'Brien, R. G. Verhaak, R. Delwel, D. Haase, L. Trumper, J. Krauter, T. Kohwi-Shigematsu, F. Griesinger, and D. G. Tenen. 2007. A distal single nucleotide polymorphism alters long-range regulation of the PU.1 gene in acute myeloid leukemia. J. Clin. Investig. 117:2611-2620.
65. Szabo, E., L. H. Preis, and M. J. Birrer. 1994. Constitutive cJun expression induces partial macrophage differentiation in U-937 cells. Cell Growth Differ. 5:439-446.
66. Tartaglia, M., C. M. Niemeyer, A. Fragale, X. Song, J. Buechner, A. Jung, K. Hahlen, H. Hasle, J. D. Licht, and B. D. Gelb. 2003. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat. Genet. 34:148-150.
67. Visvader, J. E., M. Crossley, J. Hill, S. H. Orkin, and J. M. Adams. 1995. The C-terminal zinc finger of GATA-1 or GATA-2 is sufficient to induce megakaryocytic differentiation of an early myeloid cell line. Mol. Cell. Biol. 15:634-641.
68. Walsh, J. C., R. P. DeKoter, H. J. Lee, E. D. Smith, D. W. Lancki, M. F. Gurish, D. S. Friend, R. L. Stevens, J. Anastasi, and H. Singh. 2002. Cooperative and antagonistic interplay between PU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 17:665-676.
69. Xia, Y., J. Wang, T. J. Liu, W. K. Yung, T. Hunter, and Z. Lu. 2007. c-Jun downregulation by HDAC3-dependent transcriptional repression promotes osmotic stress-induced cell apoptosis. Mol. Cell 25:219-232.
70. Yamaguchi, K., A. Lantowski, A. J. Dannenberg, and K. Subbaramaiah. 2005. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J. Biol. Chem. 280:32569- 32577.
71. Yang, Z., Y. Li, F. Yin, and R. J. Chan. 2008. Activating PTPN11 mutants promote hematopoietic progenitor cell-cycle progression and survival. Exp. Hematol. 36:1285-1296.
72. Yao, Y., W. Li, M. H. Kaplan, and C. H. Chang. 2005. Interleukin (IL)-4 inhibits IL-10 to promote IL-12 production by dendritic cells. J. Exp. Med. 201:1899-1903.
73. Yoshimi, A., M. Mohamed, M. Bierings, C. Urban, E. Korthof, M. Zecca, K. W. Sykora, U. Duffner, M. Trebo, S. Matthes-Martin, P. Sedlacek, T. Klingebiel, P. Lang, M. Fuhrer, A. Claviez, W. Wossmann, A. Pession, J. Arvidson, A. S. O'Marcaigh, M. M. van den Heuvel-Eibrink, J. Stary, H. Hasle, P. Nollke, F. Locatelli, and C. M. Niemeyer. 2007. Second allogeneic hematopoietic stem cell transplantation (HSCT) results in outcome similar to that of first HSCT for patients with juvenile myelomonocytic leukemia. Leukemia 21:556-560.
74. Zhang, D. E., C. J. Hetherington, H. M. Chen, and D. G. Tenen. 1994. The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol. 14:373-381.
75. Zhang, P., G. Behre, J. Pan, A. Iwama, N. Wara-Aswapati, H. S. Radomska, P. E. Auron, D. G. Tenen, and Z. Sun. 1999. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc. Natl. Acad. Sci. USA 96:8705-8710.
76. Zhang, P., X. Zhang, A. Iwama, C. Yu, K. A. Smith, B. U. Mueller, S. Narravula, B. E. Torbett, S. H. Orkin, and D. G. Tenen. 2000. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96:2641-2648.