Interferon regulatory factor 4 attenuates Notch signaling to suppress the development of chronic lymphocytic leukemia

Oncotarget

Volumn 7, Issue 27, 2016, Pages 41081-41094

  Shukla, Vipul ^a   Shukla, Ashima ^a   Joshi, Shantaram S ^a   Lu, Runqing ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

B1 cells; CLL; IRF4; Notch signaling

Indexed keywords

INTERFERON REGULATORY FACTOR 4; NOTCH RECEPTOR; UBIQUITIN PROTEIN LIGASE NEDD4; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR-4; NOTCH2 PROTEIN, HUMAN; NOTCH2 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL; LEUKEMOGENESIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; DOWN REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DOWN-REGULATION; GENES, TUMOR SUPPRESSOR; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INTERFERON REGULATORY FACTORS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; RECEPTOR, NOTCH2; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 85016091426     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9596     Document Type: Article

References (36)

1. Fabbri G, Khiabanian H, Holmes AB, Wang J, Messina M, Mullighan CG, Pasqualucci L, Rabadan R and Dalla-Favera R. Genetic lesions associated with chronic lymphocytic leukemia transformation to Richter syndrome. The Journal of experimental medicine. 2013; 210:2273-2288.
2. Fabbri G, Rasi S, Rossi D, Trifonov V, Khiabanian H, Ma J, Grunn A, Fangazio M, Capello D, Monti S, Cresta S, Gargiulo E, Forconi F, Guarini A, Arcaini L, Paulli M, et al. Analysis of the chronic lymphocytic leukemia coding genome: role of NOTCH1 mutational activation. The Journal of experimental medicine. 2011; 208:1389-1401.
3. Kiel MJ, Velusamy T, Betz BL, Zhao L, Weigelin HG, Chiang MY, Huebner-Chan DR, Bailey NG, Yang DT, Bhagat G, Miranda RN, Bahler DW, Medeiros LJ, Lim MS and Elenitoba-Johnson KS. Whole-genome sequencing identifies recurrent somatic NOTCH2 mutations in splenic marginal zone lymphoma. The Journal of experimental medicine. 2012; 209:1553-1565.
4. Puente XS, Bea S, Valdes-Mas R, Villamor N, Gutierrez-Abril J, Martin-Subero JI, Munar M, Rubio-Perez C, Jares P, Aymerich M, Baumann T, Beekman R, Belver L, Carrio A, Castellano G, Clot G, et al. Non-coding recurrent mutations in chronic lymphocytic leukaemia. Nature. 2015; 526:519-524.
5. Puente XS, Pinyol M, Quesada V, Conde L, Ordonez GR, Villamor N, Escaramis G, Jares P, Bea S, Gonzalez-Diaz M, Bassaganyas L, Baumann T, Juan M, Lopez-Guerra M, Colomer D, Tubio JM, et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature. 2011; 475:101-105.
6. Rossi D, Rasi S, Fabbri G, Spina V, Fangazio M, Forconi F, Marasca R, Laurenti L, Bruscaggin A, Cerri M, Monti S, Cresta S, Fama R, De Paoli L, Bulian P, Gattei V, et al. Mutations of NOTCH1 are an independent predictor of survival in chronic lymphocytic leukemia. Blood. 2012; 119:521-529.
7. Kopan R and Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 2009; 137:216-233.
8. Rosati E, Sabatini R, Rampino G, Tabilio A, Di Ianni M, Fettucciari K, Bartoli A, Coaccioli S, Screpanti I and Marconi P. Constitutively activated Notch signaling is involved in survival and apoptosis resistance of B-CLL cells. Blood. 2009; 113:856-865.
9. Arruga F, Gizdic B, Serra S, Vaisitti T, Ciardullo C, Coscia M, Laurenti L, D'Arena G, Jaksic O, Inghirami G, Rossi D, Gaidano G and Deaglio S. Functional impact of NOTCH1 mutations in chronic lymphocytic leukemia. Leukemia. 2014; 28:1060-1070.
10. Nwabo Kamdje AH, Bassi G, Pacelli L, Malpeli G, Amati E, Nichele I, Pizzolo G and Krampera M. Role of stromal cell-mediated Notch signaling in CLL resistance to chemotherapy. Blood cancer journal. 2012; 2:e73.
11. De Silva NS, Simonetti G, Heise N and Klein U. The diverse roles of IRF4 in late germinal center B-cell differentiation. Immunological reviews. 2012; 247:73-92.
12. Shukla V and Lu R. IRF4 and IRF8: Governing the virtues of B Lymphocytes. Frontiers in biology. 2014; 9:269-282.
13. Di Bernardo MC, Crowther-Swanepoel D, Broderick P, Webb E, Sellick G, Wild R, Sullivan K, Vijayakrishnan J, Wang Y, Pittman AM, Sunter NJ, Hall AG, Dyer MJ, Matutes E, Dearden C, Mainou-Fowler T, et al. A genomewide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nature genetics. 2008; 40:1204-1210.
14. Ma S, Shukla V, Fang L, Gould KA, Joshi SS and Lu R. Accelerated development of chronic lymphocytic leukemia in New Zealand Black mice expressing a low level of interferon regulatory factor 4. The Journal of biological chemistry. 2013; 288:26430-26440.
15. Shukla V, Ma S, Hardy RR, Joshi SS and Lu R. A role for IRF4 in the development of CLL. Blood. 2013; 122:2848-2855.
16. Allan JM, Sunter NJ, Bailey JR, Pettitt AR, Harris RJ, Pepper C, Fegan C, Hall AG, Deignan L, Bacon CM, Pointon JC, Houlston RS, Broderick P, Mainou-Fowler T, Jackson GH, Summerfield G, et al. Variant IRF4/MUM1 associates with CD38 status and treatment-free survival in chronic lymphocytic leukaemia. Leukemia. 2010; 24:877-881.
17. Wen L, Shinton SA, Hardy RR and Hayakawa K. Association of B-1 B cells with follicular dendritic cells in spleen. Journal of immunology. 2005; 174:6918-6926.
18. Raveche ES, Salerno E, Scaglione BJ, Manohar V, Abbasi F, Lin YC, Fredrickson T, Landgraf P, Ramachandra S, Huppi K, Toro JR, Zenger VE, Metcalf RA and Marti GE. Abnormal microRNA-16 locus with synteny to human 13q14 linked to CLL in NZB mice. Blood. 2007; 109:5079-5086.
19. Simonetti G, Carette A, Silva K, Wang H, De Silva NS, Heise N, Siebel CW, Shlomchik MJ and Klein U. IRF4 controls the positioning of mature B cells in the lymphoid microenvironments by regulating NOTCH2 expression and activity. The Journal of experimental medicine. 2013; 210:2887-2902.
20. Zhong Y and Byrd JC. IRF4(-/-)Vh11 mice: a novel mouse model of CLL. Blood. 2013; 122:2769-2770.
21. Saito T, Chiba S, Ichikawa M, Kunisato A, Asai T, Shimizu K, Yamaguchi T, Yamamoto G, Seo S, Kumano K, Nakagami-Yamaguchi E, Hamada Y, Aizawa S and Hirai H. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity. 2003; 18:675-685.
22. Koncarevic A, Jackman RW and Kandarian SC. The ubiquitin-protein ligase Nedd4 targets Notch1 in skeletal muscle and distinguishes the subset of atrophies caused by reduced muscle tension. FASEB journal. 2007; 21:427-437.
23. Sakata T, Sakaguchi H, Tsuda L, Higashitani A, Aigaki T, Matsuno K and Hayashi S. Drosophila Nedd4 regulates endocytosis of notch and suppresses its ligand-independent activation. Current biology. 2004; 14:2228-2236.
24. Sorensen EB and Conner SD. gamma-secretase-dependent cleavage initiates notch signaling from the plasma membrane. Traffic. 2010; 11:1234-1245.
25. Wilkin MB, Carbery AM, Fostier M, Aslam H, Mazaleyrat SL, Higgs J, Myat A, Evans DA, Cornell M and Baron M. Regulation of notch endosomal sorting and signaling by Drosophila Nedd4 family proteins. Current biology. 2004; 14:2237-2244.
26. Johnson K, Hashimshony T, Sawai CM, Pongubala JM, Skok JA, Aifantis I and Singh H. Regulation of immunoglobulin light-chain recombination by the transcription factor IRF-4 and the attenuation of interleukin-7 signaling. Immunity. 2008; 28:335-345.
27. Ochiai K, Maienschein-Cline M, Simonetti G, Chen J, Rosenthal R, Brink R, Chong AS, Klein U, Dinner AR, Singh H and Sciammas R. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity. 2013; 38:918-929.
28. Ye M, Ermakova O and Graf T. PU.1 is not strictly required for B cell development and its absence induces a B-2 to B-1 cell switch. The Journal of experimental medicine. 2005; 202:1411-1422.
29. Damm F, Mylonas E, Cosson A, Yoshida K, Della Valle V, Mouly E, Diop M, Scourzic L, Shiraishi Y, Chiba K, Tanaka H, Miyano S, Kikushige Y, Davi F, Lambert J, Gautheret D, et al. Acquired initiating mutations in early hematopoietic cells of CLL patients. Cancer discovery. 2014; 4:1088-1101.
30. De Falco F, Sabatini R, Del Papa B, Falzetti F, Di Ianni M, Sportoletti P, Baldoni S, Screpanti I, Marconi P and Rosati E. Notch signaling sustains the expression of Mcl-1 and the activity of eIF4E to promote cell survival in CLL. Oncotarget. 2015; 6:16559-16572. doi: 10.18632/ oncotarget.4116.
31. Crowther-Swanepoel D, Broderick P, Di Bernardo MC, Dobbins SE, Torres M, Mansouri M, Ruiz-Ponte C, Enjuanes A, Rosenquist R, Carracedo A, Jurlander J, Campo E, Juliusson G, Montserrat E, Smedby KE, Dyer MJ, et al. Common variants at 2q37.3, 8q24.21, 15q21.3 and 16q24.1 influence chronic lymphocytic leukemia risk. Nature genetics. 2010; 42:132-136.
32. McCright B, Lozier J and Gridley T. Generation of new Notch2 mutant alleles. Genesis. 2006; 44:29-33.
33. Belteki G, Haigh J, Kabacs N, Haigh K, Sison K, Costantini F, Whitsett J, Quaggin SE and Nagy A. Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction. Nucleic acids research. 2005; 33:e51.
34. Rickert RC, Roes J and Rajewsky K. B lymphocytespecific, Cre-mediated mutagenesis in mice. Nucleic acids research. 1997; 25:1317-1318.
35. Pathak S, Ma S, Trinh L, Eudy J, Wagner KU, Joshi SS and Lu R. IRF4 is a suppressor of c-Myc induced B cell leukemia. PloS one. 2011; 6:e22628.
36. Shukla A, Rai K, Shukla V, Chaturvedi NK, Bociek RG, Pirruccello SJ, Band H, Lu R and Joshi SS. Sprouty 2: a novel attenuator of B-cell receptor and MAPK-Erk signaling in CLL. Blood. 2016; 127:2310-21. doi: 10.1182/ blood-2015-09-669317.