JAK3 pathway is constitutively active in B-lineage acute lymphoblastic leukemia

Expert Review of Anticancer Therapy

Volumn 11, Issue 1, 2011, Pages 37-48

  Uckun, Fatih M ^a,b   Pitt, Jason ^c   Qazi, Sanjive ^d  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d GUSTAVUS ADOLPHUS COLLEGE   (United States)

Author keywords

Janus kinase 3; leukemia; leukemic B cell precursors; lymphoma; nanomedicines

Indexed keywords

ASPARAGINASE; DAUNORUBICIN; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 7; INTERLEUKIN 9; JANUS KINASE 3; JANUS KINASE 3 INHIBITOR; STEROID; VINCRISTINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CANCER RELAPSE; CANCER RESISTANCE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; GENE AMPLIFICATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INFANT; JAK3 DEFICIENCY; LEUKEMIA CELL; MOLECULARLY TARGETED THERAPY; NUCLEOTIDE SEQUENCE; PRE B LYMPHOCYTE; PRESCHOOL CHILD; PROTEIN EXPRESSION; SCHOOL CHILD;

CYTOKINES; HUMANS; JANUS KINASE 3; MOLECULAR TARGETED THERAPY; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTORS, CYTOKINE; SIGNAL TRANSDUCTION;

EID: 78650500208     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/era.10.203     Document Type: Article

References (60)

1. Miosge LA, Goodnow CC. Genes, pathways and checkpoints in lymphocyte development and homeostasis. Immunol. Cell Biol. 83, 318-335 (2005).
2. Tortolani PJ, Lal BK, Riva A et al. Regulation of JAK3 expression and activation in human B cells and B cell malignancies. J. Immunol. 155, 5220-5226 (1995).
3. Sharfe N, Dadi HK, O'Shea JJ, Roifman CM. JAK3 activation in human lymphocyte precursor cells. Clin. Exp. Immunol. 108, 552-556 (1997).
4. Sudbeck EA, Liu X-P, Narla RK et al. Structure-based design of specifc inhibitors of Janus kinase 3 as apoptosis-inducing antileukemic agents. Clin. Cancer Res. 5, 1569-1582 (1999).
5. Scharfe N, Dadi HK, Roifman CM. JAK3 protein tyrosine kinase mediates interleukin-7 induced activation of phosphatidylinositol-3 kinase. Blood 86, 2077-2085 (1995).
6. Malin S, McManus S, Cobaleda C et al. Role of STAT5 in controlling cell survival and immunoglobulin gene recombination during pro-B cell development. Nat. Immunol. 11, 171-179 (2010).
7. Lin Q, Lai R, Chirieac LR et al. Constitutive activation of JAK3/STAT3 in colon carcinoma tumors and cell lines. Am. J. Pathol. 167, 969-980 (2005).
8. Cornejo MG, Boggon TJ, Mercher T. JAK3: a two-faced player in hematologic disorders. Int. J. Biochem. Cell Biol. 41, 2376-2379 (2009).
9. Kawahara A, Minami Y, Miyazaki T, Ihle JN, Taniguchi T. Critical role of the interleukin 2 (IL-2) receptor y-chain associated JAK3 in the IL-2 induced c-fos and c-myc, but not bcl-1 gene induction. Proc. Natl Acad. Sci. USA 92, 8724-8728 (1995).
10. Walker SR, Nelson EA, Frank DA. STAT5 represses BCL6 expression by binding to a regulatory region frequently mutated in lymphomas. Oncogene 26, 224-233 (2007).
11. Duy C, Yu JJ, Nahar R et al. BCL6 is critical for the development of a diverse B cell repertoire. J. Exp. Med. 207, 1209-1221 (2009).
12. Han S-S, Yun H, Son D-J et al. NF-KB/STAT3/PI3K signaling crosstalk in iMycEμ B lymphoma. Mol. Cancer 9, 97 (2010).
13. Juarez J, Baraz R, Gaundar S, Bradstock K, Bendall L. Interaction of interleukin-7 and interleukin-3 with the CXCL12-induced proliferation of B-cell progenitor acute lymphoblastic leukemia. Haematologica 92, 450-459 (2007).
14. Juarez J, Thien M, Dela Pena A, Baraz R, Bradstock KF, Bendall LJ. CXCR4 mediates the homing of B cell progenitor acute lymphoblastic leukemia cells to the bone marrow via activation of p38MAPK. Br. J. Haematol. 145, 491-499 (2009).
15. Vila-Coro AJ, Rodriguez-Frade JM, DeAna AM, Moreno-Ortiz MC, Martinez C, Mellado M. The chemokine SDF-1 triggers CXCR4 receptor dimerization and activates the JAK-STAT pathway. FASEB J. 13, 1699-1710 (1999).
16. Wang L, Fortney JE, Gibson LF. Stromal cell protection of B-lineage acute lymphoblastic leukemic cells during chemotherapy requires active Akt. Leuk. Res. 28, 733-742 (2004).
17. Hornakova T, Staerk J, Royer Y et al. Acute lymphoblastic leukemia-associated JAK1 mutants activate the Janus kinase/STAT pathway via interleukin 9 receptor a homodimers. J. Biol. Chem. 284, 6773-6781 (2009).
18. Lu X, Huang LJ, Lodish HF. Dimerization by a cytokine receptor is necessary for constitutive activation of JAK2V617F. J. Biol. Chem. 283, 5258-5266 (2008).
19. Malka Y, Hornakova T, Royer Y et al Ligand-independent homomeric and heteromeric complexes between interleukin-2 or -9 receptor subunits and the y chain. J. Biol. Chem. 283, 33569-33577 (2008).
20. Qazi S, Uckun FM. Gene expression profles of infant acute lymphoblastic leukaemia and its pro gnostic ally distinct subsets. Br. J. Haematol. 149(6), 865-873 (2010).
21. Mulligan CG, Zhang J, Harvey RC et al JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc. Natl Acad. Sci. USA 106, 9414-9418 (2009).
22. Uckun FM, Goodman P, Ma H, Dibirdik I, Qazi S. CD22 exon 12 deletion as a novel pathogenic mechanism of human B-precursor leukemia. Proc. Natl Acad. Sci. USA 107, 16852-16857 (2010).
23. Irizarry RA, Hobbs B, Collin F et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4(2), 249-264 (2003).
24. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bio informatics 19(2), 185-193 (2003).
25. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3(1), Article 3 (2004).
26. Wettenhall JM, Simpson KM, Satterley K, Smyth GK. affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bio informatics 22(7), 897-899 (2006).
27. Takeshita T, Arita T, Higuchi M et al. STAM, signal transducing adaptor molecule, is associated with Janus kinases and involved in signaling for cell growth and c-myc induction. Immunity 6, 449-457 (1997).
28. Rochman Y, Spolski R, Leonard WJ. New insights into the regulation of T-cells by y(c) family cytokines. Nat. Rev. Immunol 9, 480-490 (2009).
29. Walters DK, Mercher T, Gu TL et al Activating alleles of JAK3 in acute megakaryoblastic leukemia. Cancer Cell 10, 65-75 (2006).
30. Sato T, Toki T, Kanezaki R et al Functional analysis of JAK3 mutations in transient myeloproliferative disorder and acute megakaryoblastic leukemia accompanying Down syndrome. Br. J. Hematol. 141, 681-688 (2008).
31. Malinge S, Ragu C, Della-Valle V et al Activating mutations in human acute megakaryoblastic leukemia. Blood 112, 4220-4226 (2008).
32. Cornejo MG, Kharas MG, Werneck MB et al. Constitutive JAK3 activation induces lymphoproliferative syndromes in murine bone marrow transplantation models. Blood 113, 2746-2754 (2009).
33. Yamashita Y, Yuan J, Suetake I et al Array-based genomic resequencing of human leukemia. Oncogene 29, 3723-3731 (2010).
34. + anaplastic large-cell lymphoma cells. Blood 108, 2407-2415 (2006).
35. Bard JD, Gelebart P, Anand M et al IL-21 contributes to JAK3/STAT3 activation and promotes cell growth in ALK-positive anaplastic large cell lymphoma. Am. J. Pathol. 175, 825-834 (2009).
36. Amin HM, Medeiros LJ, Ma Y et al Inhibition of JAK3 induces apoptosis and decreases anaplastic lymphoma kinase activity in anaplastic large cell lymphoma. Oncogene 22, 5399-5407 (2003).
37. Steele AJ, Prentice AG, Cwynarski K et al The JAK3 selective inhibitor PF-956980 reverses resistance to cytotoxic agents induced by interleukin-4 treatment of chronic lymphocytic leukemia cells: potential for reversal of cytoprotection by the microenvironment. Blood DOI: 10.1182/blood-20 09-20 09-245811 (2010) (Epub ahead of print).
38. Martinez-Lostao L, Briones J, Forne I et al Role of STAT1 pathway in apoptosis induced by fudarabine and JAK kinase inhibitors in B-cell chronic lymphocytic leukemia. Leukemia 46, 435-442 (2005).
39. + anaplastic large-cell lymphoma. Blood 108, 2796-2803 (2006).
40. Piessevaux J, Lavens D, Peelman F, Tavernier J. The many faces of the SOCS box. Cytokine Growth Factor Rev. 19, 371-381 (2008).
41. Endo TA, Masuhara M, Yokouchi M et al A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924 (1997).
42. Jumaa H, Bossaller L, Portugal K et al Defciency of the adaptor SLP-65 in pre-B cell acute lymphoblastic leukemia. Nature 423, 452-456 (2003). (Pubitemid 36626998)
43. + acute lymphoblastic leukemia. Blood (ASH Annual Meeting Abstracts) 114 (2009) (Abstract 579).
44. Nakayama J, Yamamoto M, Hayashi K et al. BLNK suppresses pre-B cell leukemogenesis through inhibition of JAK3. Blood 113, 1483-1492 (2009).
45. Uckun FM, Dibirdik I, Smith R et al. Interleukin 7 receptor ligation stimulates tyrosine phosphorylation, inositol phospholipid turnover, and clonal proliferation of human B-cell precursors. Proc. Natl Acad. Sci. USA 88(9), 3589-3593 (1991).
46. Morrissey PJ, Conlon P, Charrier K et al. Administration of IL-7 to normal mice stimulates B-lymphopoiesis and peripheral lymph adenopathy. J. Immunol. 147, 561-568 (1991).
47. Fisher AG, Burdet C, Bunce C et al. Lymphoproliferative disorders in IL-7 transgenic mice: expansion of immature B-cells which retain macrophage potential. Int. Immunol. 7, 415-423 (1995).
48. Mertshing E, Grawunder U, Meyer V et al. Phenotypic and functional analysis of B-lymphopoiesis in interleukin-7 transgenic mice: expansion of pro-B/ pre-B cell number and persistence of B lymphocyte development in lymph nodes and spleen. Eur. J. Immunol. 26, 28-33 (1996).
49. Rich BE, Campos-Torres J, Tepper RI, Moradith FW, Leder P. Cutaneous lymphoproliferation and lymphomas in interleukin 7 transgenic mice. J. Exp. Med. 177, 305-316 (1993).
50. Touw I, Pouweis K, van Agthoven T et al. Interleukin 7 is a growth factor of precursor B and T acute lymphoblastic leukemia. Blood 75, 2097-2101 (1990). (Pubitemid 20181157)
51. Henney CS. Interleukin 7: effects on early events in lymphopoiesis. Immunol. Today 10, 170-173 (1989).
52. Knoops L, Hornakova T, Royer Y, Constantinescu SN, Renauld JC. JAK kinases over expression promotes in vitro cell transformation. Oncogene 27, 1511-1519 (2008).
53. Bonetta L. Leukemia case triggers tighter gene therapy controls. Nat. Med. 8, 1189 (2002).
54. Witthuhn BA, Williams MD, Kerawalla H, Uckun FM. Differential substrate recgnition capabilities of Janus protein tyrosine kinases within the interleukin 2 receptor system: JAK3 as a potential molecular target for treatment of leukemias with a hyperactive JAK-STAT signaling machinery. Leuk. Lymphoma 32, 289-297 (1999).
55. Zhu MH, Berry JA, Russell SM, Leonard WJ. Delineation of the regions of interleukin 2 (IL-2) receptor b chain important for association of JAK1 and JAK3. J. Biol. Chem. 273, 10719-10725 (1998).
56. Fujii H. Receptor expression is essential for proliferation induced by dimerized JAK kinases. Biochem. Biophys. Res. Commun. 370, 557-560 (2008).
57. James C, Ugo V, Le Couedic JP et al. A unique clonal JAK2 mutation leading to constitutive signaling causes polycythemia vera. Nature 434, 1144-1148 (2005). (Pubitemid 40663494)
58. Kralovics R, Passamonti F, Buser AS et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N. Engl. J. Med. 352, 1779-1790 (2005). (Pubitemid 40570926)
59. Jeong EG, Kim MS, Nam HK et al. Somatic mutations of JAK1 and JAK3 in acute leukemias and solid cancers. Clin. Cancer Res. 14, 3716-3722 (2008).
60. Thompson JE, Cubbon RM, Cummings RT et al. Photochemical preparation of a pyridone containing tetracycle: a JAK protein kinase inhibitor. Bioorg. Med. Chem. Lett. 12, 1219-1223 (2002).