Notch1 regulates chemotaxis and proliferation by controlling the CC-chemokine receptors 5 and 9 in T cell acute lymphoblastic leukaemia

Journal of Pathology

Volumn 226, Issue 5, 2012, Pages 713-722

  Mirandola, Leonardo ^a,b   Chiriva Internati, Maurizio ^b   Montagna, Daniela ^c,d   Locatelli, Franco ^d,e   Zecca, Marco ^c   Ranzani, Marco ^a   Basile, Andrea ^a   Locati, Massimo ^a,f   Cobos, Everardo ^b   Kast, W Martin ^g,h   Asselta, Rosanna ^a   Paraboschi, Elvezia Maria ^a   Comi, Paola ^a   Chiaramonte, Raffaella ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^d UNIVERSITY OF PAVIA   (Italy)

^e BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^f HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^h UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

CCL25; CCR5; CCR7; CCR9; Chemokine receptor; Chemotaxis; CXCR4; Notch; Proliferation; T cell acute lymphoblastic leukaemia

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR4; GAMMA SECRETASE INHIBITOR; NOTCH1 RECEPTOR; SMALL INTERFERING RNA;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; ARTICLE; CELL PROLIFERATION; CHEMOTAXIS; CHILD; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKEMIA CELL; LEUKEMIA CELL LINE; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SCHOOL CHILD;

ADOLESCENT; AMYLOID PRECURSOR PROTEIN SECRETASES; CELL PROLIFERATION; CHEMOKINES, CC; CHEMOTAXIS; CHILD; CHILD, PRESCHOOL; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; MALE; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTOR, NOTCH1; RECEPTORS, CCR; RECEPTORS, CCR5; RECEPTORS, CXCR4; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84858000851     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.3015     Document Type: Article

References (51)

1. Ellisen LW, Bird J, West DC, et al. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 1991; 66: 649-661. (Pubitemid 121001701)
2. Chiaramonte R, Calzavara E, Balordi F, et al. Differential regulation of Notch signal transduction in leukaemia and lymphoma cells in culture. J Cell Biochem 2003; 88: 569-577. (Pubitemid 36158276)
3. Chiaramonte R, Basile A, Tassi E, et al. A wide role for NOTCH1 signaling in acute leukemia. Cancer Lett 2005; 219: 113-120. (Pubitemid 40203178)
4. Weng AP, Ferrando AA, Lee W, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004; 306: 269-271. (Pubitemid 39336870)
5. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004; 4: 540-550. (Pubitemid 38868623)
6. Tang CH, Yamamoto A, Lin YT, et al. Involvement of matrix metalloproteinase-3 in CCL5/CCR5 pathway of chondrosarcomas metastasis. Biochem Pharmacol 2010; 79: 209-217.
7. Chuang JY, Yang WH, Chen HT, et al. CCL5/CCR5 axis promotes the motility of human oral cancer cells. J Cell Physiol 2009; 220: 418-426.
8. Makishima H, Ito T, Momose K, et al. Chemokine system and tissue infiltration in aggressive NK-cell leukemia. Leuk Res 2007; 31: 1237-1245.
9. Menu E, De Leenheer E, De Raeve H, et al. Role of CCR1 and CCR5 in homing and growth of multiple myeloma and in the development of osteolytic lesions: a study in the 5TMM model. Clin Exp Metast 2006; 23: 291-300.
10. Vandenabeele S, Hochrein H, Mavaddat N, et al. Human thymus contains two distinct dendritic cell populations. Blood 2001; 97: 1733-1741. (Pubitemid 32217241)
11. Wurbel MA, Philippe JM, Nguyen C, et al. The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol 2000; 30: 262-271. (Pubitemid 30011788)
12. Letsch A, Keilholz U, Schadendorf D, et al. Functional CCR9 expression is associated with small intestinal metastasis. J Invest Dermatol 2004; 122: 685-690. (Pubitemid 38471337)
13. Annels NE, Willemze AJ, van der Velden VH, et al. Possible link between unique chemokine and homing receptor expression at diagnosis and relapse location in a patient with childhood T-ALL. Blood 2004; 103: 2806-2808. (Pubitemid 38393042)
14. +T cells from patients with T-cell lineage acute lymphocytic leukemia. Cancer Res 2003; 63: 6469-6477.
15. + T cells from patients with T-cell lineage acute and chronic lymphocytic leukemia by means of livin activation. Cancer Res 2004; 64: 7579-7587.
16. Alsayed Y, Ngo H, Runnels J, et al. Mechanisms of regulation of CXCR4/SDF-1 (CXCL12)-dependent migration and homing in multiple myeloma. Blood 2007; 109: 2708-2717. (Pubitemid 46482062)
17. Martin SK, Dewar AL, Farrugia AN, et al. Tumor angiogenesis is associated with plasma levels of stromal-derived factor-1αin patients with multiple myeloma. Clin Cancer Res 2006; 12: 6973-6977. (Pubitemid 44974491)
18. Narducci MG, Scala E, Bresin A, et al. Skin homing of Sezary cells involves SDF-1-CXCR4 signaling and down-regulation of CD26/dipeptidylpeptidase IV. Blood 2006; 107: 1108-1115. (Pubitemid 43156312)
19. Maerki S, Ceredig R, Rolink A. Induction of chemokine receptor expression during early stages of T cell development. Immunol Lett 2006; 104: 110-117. (Pubitemid 43330716)
20. Hoshino N, Katayama N, Shibasaki T, et al. A novel role for Notch ligand δ1 as a regulator of human Langerhans cell development from blood monocytes. J Leukoc Biol 2005; 78: 921-929. (Pubitemid 41384408)
21. Buonamici S, Trimarchi T, Ruocco MG, et al. CCR7 signalling as an essential regulator of CNS infiltration in T-cell leukaemia. Nature 2009; 459: 1000-1004.
22. van Meerloo J, Kaspers GJ, Cloos J. Cell sensitivity assays: the MTT assay. Methods Mol Biol 2011; 731: 237-245.
23. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.
24. Asselta R, Duga S, Spena S, et al. Congenital afibrinogenemia: mutations leading to premature termination codons in fibrinogen A α-chain gene are not associated with the decay of the mutant mRNAs. Blood 2001; 98: 3685-3692.
25. Weng AP, Millholland JM, Yashiro-Ohtani Y, et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev 2006; 20: 2096-2109. (Pubitemid 44157460)
26. Gomez-del Arco P, Kashiwagi M, Jackson AF, et al. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity 2010; 33: 685-698.
27. Jeannet R, Mastio J, Macias-Garcia A, et al. Oncogenic activation of the Notch1 gene by deletion of its promoter in Ikaros-deficient T-ALL. Blood 2010; 116: 5443-5454.
28. Weijzen S, Rizzo P, Braid M, et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med 2002; 8: 979-986. (Pubitemid 35033702)
29. Gothert JR, Brake RL, Smeets M, et al. NOTCH1 pathway activation is an early hallmark of SCL T leukemogenesis. Blood 2007; 110: 3753-3762. (Pubitemid 350159646)
30. Cullion K, Draheim KM, Hermance N, et al. Targeting the Notch1 and mTOR pathways in a mouse T-ALL model. Blood 2009; 113: 6172-6181.
31. Yan XQ, Sarmiento U, Sun Y, et al. A novel Notch ligand, Dll4, induces T-cell leukemia/lymphoma when overexpressed in mice by retroviral-mediated gene transfer. Blood 2001; 98: 3793-3799.
32. Indraccolo S, Minuzzo S, Masiero M, et al. Ligand-driven activation of the notch pathway in T-ALL and solid tumors: why Not(ch)? Cell Cycle 2010; 9: 80-85.
33. Fung E, Tang SM, Canner JP, et al. δ-like 4 induces notch signaling in macrophages: implications for inflammation. Circulation 2007; 115: 2948-2956. (Pubitemid 46912098)
34. Huang MT, Dai YS, Chou YB, et al. Regulatory T cells negatively regulate neovasculature of airway remodeling via DLL4- Notch signaling. J Immunol 2009; 183: 4745-4754.
35. Bellavia D, Campese AF, Checquolo S, et al. Combined expression of pTα and Notch3 in T cell leukemia identifies the requirement of preTCR for leukemogenesis. Proc Natl Acad Sci USA 2002; 99: 3788-3793. (Pubitemid 34252184)
36. Nagel S, Venturini L, Przybylski GK, et al. NK-like homeodomain proteins activate NOTCH3-signaling in leukemic T-cells. BMC Cancer 2009; 9: 371.
37. O'Neil J, Grim J, Strack P, et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to γ-secretase inhibitors. J Exp Med 2007; 204: 1813-1824. (Pubitemid 47236319)
38. Palomero T, Sulis ML, Cortina M, et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med 2007; 13: 1203-1210. (Pubitemid 47530629)
39. Palomero T, Ferrando A. Oncogenic NOTCH1 control of MYC and PI3K: challenges and opportunities for anti-NOTCH1 therapy in T-cell acute lymphoblastic leukemias and lymphomas. Clin Cancer Res 2008; 14: 5314-5317.
40. Silva A, Yunes JA, Cardoso BA, et al. PTEN posttranslational inactivation and hyperactivation of the PI3K/Akt pathway sustain primary T cell leukemia viability. J Clin Invest 2008; 118: 3762-3774.
41. Bonnet M, Loosveld M, Montpellier B, et al. Posttranscriptional deregulation of MYC via PTEN constitutes a major alternative pathway of MYC activation in T-cell acute lymphoblastic leukemia. Blood 2011; 117: 6650-6659.
42. Arnold HK, Sears RC. Protein phosphatase 2A regulatory subunit B56α associates with c-myc and negatively regulates c-myc accumulation. Mol Cell Biol 2006; 26: 2832-2844.
43. Yeh E, Cunningham M, Arnold H, et al. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 2004; 6: 308-318. (Pubitemid 38584820)
44. Mathiasen DP, Egebjerg C, Andersen SH, et al. Identification of a c-Jun N-terminal kinase-2-dependent signal amplification cascade that regulates c-Myc levels in ras transformation. Oncogene 2011; 27: 230.
45. Papadakis KA, Prehn J, Nelson V, et al. The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol 2000; 165: 5069-5076.
46. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006; 6: 127-135. (Pubitemid 43361588)
47. Makishima H, Ito T, Asano N, et al. Significance of chemokine receptor expression in aggressive NK cell leukemia. Leukemia 2005; 19: 1169-1174. (Pubitemid 40946000)
48. Balint K, Xiao M, Pinnix CC, et al. Activation of Notch1 signaling is required for β-catenin-mediated human primary melanoma progression. J Clin Invest 2005; 115: 3166-3176. (Pubitemid 41567581)
49. *Asnafi V, Buzyn A, Le Noir S, et al. NOTCH1/FBXW7 mutation identifies a large subgroup with favorable outcome in adult T-cell acute lymphoblastic leukemia (T-ALL): a Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL) study. Blood 2009; 113: 3918-3924.
50. *Van Grotel M, Meijerink JP, van Wering ER, et al. Prognostic significance of molecular-cytogenetic abnormalities in pediatric T-ALL is not explained by immunophenotypic differences. Leukemia 2008; 22: 124-131.
51. *Zuurbier L, Homminga I, Calvert V, et al. NOTCH1 and/or FBXW7 mutations predict for initial good prednisone response but not for improved outcome in pediatric T-cell acute lymphoblastic leukemia patients treated on DCOG or COALL protocols. Leukemia 2010; 24: 2014-2022.