A retroviral mutagenesis screen identifies Cd74 as a common insertion site in murine B-lymphomas and reveals the existence of a novel IFNγ-inducible Cd74 isoform

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Pyrz, Magdalena ^a   Wang, Bruce ^b   Wabl, Matthias ^c   Pedersen, Finn S ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b Picobella   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD74 ANTIGEN; GAMMA INTERFERON; B LYMPHOCYTE ANTIGEN; HLA ANTIGEN CLASS 2; ISOPROTEIN;

ANTIGEN PRESENTATION; ARTICLE; B CELL LYMPHOMA; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INSERTION; GENE LOCUS; GENE TARGETING; GENETIC ASSOCIATION; GENETIC SCREENING; HOMEOSTASIS; INTRON; MURINE LEUKEMIA VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; PROMOTER REGION; TRANSCRIPTION REGULATION; VIRUS MUTATION; ANIMAL; CELL STRAIN 3T3; GENETICS; INVARIANT CHAIN; METABOLISM; MOUSE; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING;

MURINAE; MURINE LEUKEMIA VIRUS; MUS;

ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BLOTTING, SOUTHERN; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON-GAMMA; LYMPHOMA, B-CELL; MICE; MUTAGENESIS, INSERTIONAL; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77951144286     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-86     Document Type: Article

References (73)

1. Stumptner-Cuvelette P, Benaroch P. Multiple roles of the invariant chain in MHC class II function. Biochim Biophys Acta 2002, 1542:1-13. 10.1016/S0167-4889(01)00166-5, 11853874.
2. Cresswell P. Invariant chain structure and MHC class II function. Cell 1996, 84:505-507. 10.1016/S0092-8674(00)81025-9, 8598037.
3. Rocha N, Neefjes J. MHC class II molecules on the move for successful antigen presentation. EMBO J 2008, 27:1-5. 10.1038/sj.emboj.7601945, 2206127, 18046453.
4. Shachar I, Flavell RA. Requirement for invariant chain in B cell maturation and function. Science 1996, 274:106-108. 10.1126/science.274.5284.106, 8810244.
5. Benlagha K, Park SH, Guinamard R, Forestier C, Karlsson L, Chang CH, Bendelac A. Mechanisms governing B cell developmental defects in invariant chain-deficient mice. J Immunol 2004, 172:2076-2083.
6. Matza D, Lantner F, Bogoch Y, Flaishon L, Hershkoviz R, Shachar I. Invariant chain induces B cell maturation in a process that is independent of its chaperonic activity. Proc Natl Acad Sci USA 2002, 99:3018-3023. 10.1073/pnas.052703299, 122465, 11867743.
7. Henne C, Schwenk F, Koch N, Moller P. Surface expression of the invariant chain (CD74) is independent of concomitant expression of major histocompatibility complex class II antigens. Immunology 1995, 84:177-182. 1415095, 7750992.
8. Sant AJ, Cullen SE, Schwartz BD. Biosynthetic relationships of the chondroitin sulfate proteoglycan with Ia and invariant chain glycoproteins. J Immunol 1985, 135:416-422.
9. Wraight CJ, van Endert P, Moller P, Lipp J, Ling NR, MacLennan IC, Koch N, Moldenhauer G. Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J Biol Chem 1990, 265:5787-5792.
10. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R. MIF signal transduction initiated by binding to CD74. J Exp Med 2003, 197:1467-1476. 10.1084/jem.20030286, 2193907, 12782713.
11. Shi X, Leng L, Wang T, Wang W, Du X, Li J, McDonald C, Chen Z, Murphy JW, Lolis E, et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006, 25:595-606. 10.1016/j.immuni.2006.08.020, 17045821.
12. Starlets D, Gore Y, Binsky I, Haran M, Harpaz N, Shvidel L, Becker-Herman S, Berrebi A, Shachar I. Cell-surface CD74 initiates a signaling cascade leading to cell proliferation and survival. Blood 2006, 107:4807-4816. 10.1182/blood-2005-11-4334, 16484589.
13. Matza D, Wolstein O, Dikstein R, Shachar I. Invariant chain induces B cell maturation by activating a TAF(II)105-NF-kappaB-dependent transcription program. J Biol Chem 2001, 276:27203-27206. 10.1074/jbc.M104684200, 11371575.
14. Gore Y, Starlets D, Maharshak N, Becker-Herman S, Kaneyuki U, Leng L, Bucala R, Shachar I. Macrophage Migration Inhibitory Factor Induces B Cell Survival by Activation of a CD74-CD44 Receptor Complex. J Biol Chem 2008, 283:2784-2792. 10.1074/jbc.M703265200, 18056708.
15. Lantner F, Starlets D, Gore Y, Flaishon L, Yamit-Hezi A, Dikstein R, Leng L, Bucala R, Machluf Y, Oren M, Shachar I. CD74 induces TAp63 expression leading to B-cell survival. Blood 2007, 110:4303-4311. 10.1182/blood-2007-04-087486, 17846227.
16. Faure-Andre G, Vargas P, Yuseff MI, Heuze M, Diaz J, Lankar D, Steri V, Manry J, Hugues S, Vascotto F, et al. Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. Science 2008, 322:1705-1710. 10.1126/science.1159894, 19074353.
17. Badve S, Deshpande C, Hua Z, Logdberg L. Expression of invariant chain (CD 74) and major histocompatibility complex (MHC) class II antigens in the human fetus. J Histochem Cytochem 2002, 50:473-482.
18. Zhu L, Jones PP. Transcriptional control of the invariant chain gene involves promoter and enhancer elements common to and distinct from major histocompatibility complex class II genes. Mol Cell Biol 1990, 10:3906-3916. 360901, 2115116.
19. Krawczyk M, Peyraud N, Rybtsova N, Masternak K, Bucher P, Barras E, Reith W. Long distance control of MHC class II expression by multiple distal enhancers regulated by regulatory factor X complex and CIITA. J Immunol 2004, 173:6200-6210.
20. Moore BB, Cao ZA, McRae TL, Woo CH, Conley S, Jones PP. The invariant chain gene intronic enhancer shows homology to class II promoter elements. J Immunol 1998, 161:1844-1852.
21. Koch N, Lauer W, Habicht J, Dobberstein B. Primary structure of the gene for the murine Ia antigen-associated invariant chains (Ii). An alternatively spliced exon encodes a cysteine-rich domain highly homologous to a repetitive sequence of thyroglobulin. Embo J 1987, 6:1677-1683. 553541, 3038530.
22. Strubin M, Berte C, Mach B. Alternative splicing and alternative initiation of translation explain the four forms of the Ia antigen-associated invariant chain. Embo J 1986, 5:3483-3488. 1167384, 3104027.
23. Strubin M, Long EO, Mach B. Two forms of the Ia antigen-associated invariant chain result from alternative initiations at two in-phase AUGs. Cell 1986, 47:619-625. 10.1016/0092-8674(86)90626-4, 3779839.
24. Naujokas MF, Arneson LS, Fineschi B, Peterson ME, Sitterding S, Hammond AT, Reilly C, Lo D, Miller J. Potent effects of low levels of MHC class II-associated invariant chain on CD4+ T cell development. Immunity 1995, 3:359-372. 10.1016/1074-7613(95)90120-5, 7553000.
25. Takaesu NT, Lower JA, Robertson EJ, Bikoff EK. Major histocompatibility class II peptide occupancy, antigen presentation, and CD4+ T cell function in mice lacking the p41 isoform of invariant chain. Immunity 1995, 3:385-396. 10.1016/1074-7613(95)90122-1, 7553002.
26. Shachar I, Elliott EA, Chasnoff B, Grewal IS, Flavell RA. Reconstitution of invariant chain function in transgenic mice in vivo by individual p31 and p41 isoforms. Immunity 1995, 3:373-383. 10.1016/1074-7613(95)90121-3, 7553001.
27. Burton JD, Ely S, Reddy PK, Stein R, Gold DV, Cardillo TM, Goldenberg DM. CD74 is expressed by multiple myeloma and is a promising target for therapy. Clin Cancer Res 2004, 10:6606-6611. 10.1158/1078-0432.CCR-04-0182, 15475450.
28. Koch N, Harris AW. Differential expression of the invariant chain in mouse tumor cells: relationship to B lymphoid development. J Immunol 1984, 132:12-15.
29. Momburg F, Herrmann B, Moldenhauer G, Moller P. B-cell lymphomas of high-grade malignancy frequently lack HLA-DR, -DP and -DQ antigens and associated invariant chain. Int J Cancer 1987, 40:598-603. 10.1002/ijc.2910400504, 3316049.
30. Binsky I, Haran M, Starlets D, Gore Y, Lantner F, Harpaz N, Leng L, Goldenberg DM, Shvidel L, Berrebi A, et al. IL-8 secreted in a macrophage migration-inhibitory factor- and CD74-dependent manner regulates B cell chronic lymphocytic leukemia survival. Proc Natl Acad Sci USA 2007, 104:13408-13413. 10.1073/pnas.0701553104, 1948950, 17686984.
31. Ioachim HL, Pambuccian SE, Hekimgil M, Giancotti FR, Dorsett BH. Lymphoid monoclonal antibodies reactive with lung tumors. Diagnostic applications. Am J Surg Pathol 1996, 20:64-71. 10.1097/00000478-199601000-00007, 8540610.
32. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Iwashige H, Aridome K, Hokita S, Aikou T. Invariant chain expression in gastric cancer. Cancer Lett 2001, 168:87-91. 10.1016/S0304-3835(01)00503-1, 11368882.
33. Jiang Z, Xu M, Savas L, LeClair P, Banner BF. Invariant chain expression in colon neoplasms. Virchows Arch 1999, 435:32-36. 10.1007/s004280050391, 10431843.
34. Young AN, Amin MB, Moreno CS, Lim SD, Cohen C, Petros JA, Marshall FF, Neish AS. Expression profiling of renal epithelial neoplasms: a method for tumor classification and discovery of diagnostic molecular markers. Am J Pathol 2001, 158:1639-1651. 1891957, 11337362.
35. Stein R, Mattes MJ, Cardillo TM, Hansen HJ, Chang CH, Burton J, Govindan S, Goldenberg DM. CD74: a new candidate target for the immunotherapy of B-cell neoplasms. Clin Cancer Res 2007, 13:5556s-5563s. 10.1158/1078-0432.CCR-07-1167, 17875789.
36. Stein R, Qu Z, Cardillo TM, Chen S, Rosario A, Horak ID, Hansen HJ, Goldenberg DM. Antiproliferative activity of a humanized anti-CD74 monoclonal antibody, hLL1, on B-cell malignancies. Blood 2004, 104:3705-3711. 10.1182/blood-2004-03-0890, 15297317.
37. Accessed January 2010., http://clinicaltrials.gov/
38. Kool J, Berns A. High-throughput insertional mutagenesis screens in mice to identify oncogenic networks. Nat Rev Cancer 2009, 9:389-399. 10.1038/nrc2647, 19461666.
39. Uren AG, Kool J, Berns A, van Lohuizen M. Retroviral insertional mutagenesis: past, present and future. Oncogene 2005, 24:7656-7672. 10.1038/sj.onc.1209043, 16299527.
40. Ethelberg S, Lovmand J, Schmidt J, Luz A, Pedersen FS. Increased lymphomagenicity and restored disease specificity of AML1 site (core) mutant SL3-3 murine leukemia virus by a second-site enhancer variant evolved in vivo. J Virol 1997, 71:7273-7280. 192069, 9311802.
41. Lovmand J, Sorensen AB, Schmidt J, Ostergaard M, Luz A, Pedersen FS. B-Cell lymphoma induction by akv murine leukemia viruses harboring one or both copies of the tandem repeat in the U3 enhancer. J Virol 1998, 72:5745-5756. 110375, 9621033.
42. Akagi K, Suzuki T, Stephens RM, Jenkins NA, Copeland NG. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res 2004, 32:D523-527. 10.1093/nar/gkh013, 308748, 14681473.
43. http://rtcgd.ncifcrf.gov/
44. Sørensen KD, Quintanilla-Martinez L, Kunder S, Schmidt J, Pedersen FS. Mutation of all Runx (AML1/core) sites in the enhancer of T-lymphomagenic SL3-3 murine leukemia virus unmasks a significant potential for myeloid leukemia induction and favors enhancer evolution toward induction of other disease patterns. J Virol 2004, 78:13216-13231. 10.1128/JVI.78.23.13216-13231.2004, 524987, 15542674.
45. Garcia MJ, Martinez-Delgado B, Granizo JJ, Benitez J, Rivas C. IgH, TCR-gamma, and TCR-beta gene rearrangement in 80 B- and T-cell non-Hodgkin's lymphomas: study of the association between proliferation and the so-called "aberrant" patterns. Diagn Mol Pathol 2001, 10:69-77. 10.1097/00019606-200106000-00001, 11385314.
46. Sørensen KD, Kunder S, Quintanilla-Martinez L, Sorensen J, Schmidt J, Pedersen FS. Enhancer mutations of Akv murine leukemia virus inhibit the induction of mature B-cell lymphomas and shift disease specificity towards the more differentiated plasma cell stage. Virology 2007, 362:179-191. 10.1016/j.virol.2006.12.016, 17258785.
47. Liu J, Sorensen AB, Wang B, Wabl M, Nielsen AL, Pedersen FS. Identification of novel Bach2 transcripts and protein isoforms through tagging analysis of retroviral integrations in B-cell lymphomas. BMC Mol Biol 2009, 10:2. 10.1186/1471-2199-10-2, 2635362, 19159451.
48. Ma SL, Sorensen AB, Kunder S, Sorensen KD, Quintanilla-Martinez L, Morris DW, Schmidt J, Pedersen FS. The Icsbp locus is a common proviral insertion site in mature B-cell lymphomas/plasmacytomas induced by exogenous murine leukemia virus. Virology 2006, 352:306-318. 10.1016/j.virol.2006.05.006, 16780917.
49. Brudno M, Chapman M, Gottgens B, Batzoglou S, Morgenstern B. Fast and sensitive multiple alignment of large genomic sequences. BMC Bioinformatics 2003, 4:66. 10.1186/1471-2105-4-66, 521198, 14693042.
50. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21:2933-2942. 10.1093/bioinformatics/bti473, 15860560.
51. Tokusumi Y, Ma Y, Song X, Jacobson RH, Takada S. The new core promoter element XCPE1 (X Core Promoter Element 1) directs activator-, mediator-, and TATA-binding protein-dependent but TFIID-independent RNA polymerase II transcription from TATA-less promoters. Mol Cell Biol 2007, 27:1844-1858. 10.1128/MCB.01363-06, 1820453, 17210644.
52. Cao ZA, Moore BB, Quezada D, Chang CH, Jones PP. Identification of an IFN-gamma responsive region in an intron of the invariant chain gene. Eur J Immunol 2000, 30:2604-2611. 10.1002/1521-4141(200009)30:9<2604::AID-IMMU2604>3.0.CO;2-6, 11009094.
53. Eades AM, Litfin M, Rahmsdorf HJ. The IFN-gamma response of the murine invariant chain gene is mediated by a complex enhancer that includes several MHC class II consensus elements. J Immunol 1990, 144:4399-4409.
54. Muller F, Demeny MA, Tora L. New problems in RNA polymerase II transcription initiation: matching the diversity of core promoters with a variety of promoter recognition factors. J Biol Chem 2007, 282:14685-14689. 10.1074/jbc.R700012200, 17395580.
55. Gaboli M, Kotsi PA, Gurrieri C, Cattoretti G, Ronchetti S, Cordon-Cardo C, Broxmeyer HE, Hromas R, Pandolfi PP. Mzf1 controls cell proliferation and tumorigenesis. Genes Dev 2001, 15:1625-1630. 10.1101/gad.902301, 312729, 11445537.
56. Sharrocks AD. The ETS-domain transcription factor family. Nat Rev Mol Cell Biol 2001, 2:827-837. 10.1038/35099076, 11715049.
57. Lennon AM, Ottone C, Rigaud G, Deaven LL, Longmire J, Fellous M, Bono R, Alcaide-Loridan C. Isolation of a B-cell-specific promoter for the human class II transactivator. Immunogenetics 1997, 45:266-273. 10.1007/s002510050202, 9002447.
58. Vascotto F, Lankar D, Faure-Andre G, Vargas P, Diaz J, Le Roux D, Yuseff MI, Sibarita JB, Boes M, Raposo G, et al. The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J Cell Biol 2007, 176:1007-1019. 10.1083/jcb.200611147, 2064085, 17389233.
59. Bijlmakers MJ, Benaroch P, Ploegh HL. Mapping functional regions in the lumenal domain of the class II-associated invariant chain. J Exp Med 1994, 180:623-629. 10.1084/jem.180.2.623, 2191624, 7519244.
60. Sarzotti M, Robbins DS, Hoffman PM. Induction of protective CTL responses in newborn mice by a murine retrovirus. Science 1996, 271:1726-1728. 10.1126/science.271.5256.1726, 8596933.
61. Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 2009, 139:693-706. 10.1016/j.cell.2009.10.014, 19878981.
62. Belli B, Wolff L, Nazarov V, Fan H. Proviral activation of the c-myb proto-oncogene is detectable in preleukemic mice infected neonatally with Moloney murine leukemia virus but not in resulting end stage T lymphomas. J Virol 1995, 69:5138-5141. 189334, 7609084.
63. Armstrong TD, Clements VK, Martin BK, Ting JP, Ostrand-Rosenberg S. Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumor-specific immunity. Proc Natl Acad Sci USA 1997, 94:6886-6891. 10.1073/pnas.94.13.6886, 21254, 9192661.
64. Clements VK, Baskar S, Armstrong TD, Ostrand-Rosenberg S. Invariant chain alters the malignant phenotype of MHC class II+ tumor cells. J Immunol 1992, 149:2391-2396.
65. Bakke O, Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990, 63:707-716. 10.1016/0092-8674(90)90137-4, 2121367.
66. Wang CL, Wang BB, Bartha G, Li L, Channa N, Klinger M, Killeen N, Wabl M. Activation of an oncogenic microRNA cistron by provirus integration. Proc Natl Acad Sci USA 2006, 103:18680-18684. 10.1073/pnas.0609030103, 1693722, 17121985.
67. Sørensen AB, Lund AH, Kunder S, Quintanilla-Martinez L, Schmidt J, Wang B, Wabl M, Pedersen FS. Impairment of alternative splice sites defining a novel gammaretroviral exon within gag modifies the oncogenic properties of Akv murine leukemia virus. Retrovirology 2007, 4:46. 10.1186/1742-4690-4-46, 1936429, 17617899.
68. Sørensen KD, Sørensen AB, Quintanilla-Martinez L, Kunder S, Schmidt J, Pedersen FS. Distinct roles of enhancer nuclear factor 1 (NF1) sites in plasmacytoma and osteopetrosis induction by Akv1-99 murine leukemia virus. Virology 2005, 334:234-244. 10.1016/j.virol.2005.01.039, 15780873.
69. Amtoft HW, Sorensen AB, Bareil C, Schmidt J, Luz A, Pedersen FS. Stability of AML1 (core) site enhancer mutations in T lymphomas induced by attenuated SL3-3 murine leukemia virus mutants. J Virol 1997, 71:5080-5087. 191741, 9188573.
70. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.
71. UCSC Genome Bioinformatics Site. , http://genome.ucsc.edu/
72. DIALIGN multiple-alignment program at Göttingen Bioinformatics Compute Server (GOBICS). , http://dialign.gobics.de/
73. Genomatix software. , http://www.genomatix.de