A forward genetic screen reveals novel independent regulators of ULBP1, an activating ligand for natural killer cells

eLife

Volumn 4, Issue NOVEMBER2015, 2015, Pages

  Gowen, Benjamin G ^a   Chim, Bryan ^b   Marceau, Caleb D ^c   Greene, Trever T ^a   Burr, Patrick ^b   Gonzalez, Jeanmarie R ^a   Hesser, Charles R ^a   Dietzen, Peter A ^a   Russell, Teal ^a   Iannello, Alexandre ^a   Coscoy, Laurent ^a   Sentman, Charles L ^d   Carette, Jan E ^c   Muljo, Stefan A ^b   Raulet, David H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; DECAY ACCELERATING FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 2ALPHA; LENTIVIRUS VECTOR; LUCIFERASE; MEMBRANE PROTEIN; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2D; RNA BINDING PROTEIN; RNA BINDING PROTEIN 4; UL16 BINDING PROTEIN 1; UNCLASSIFIED DRUG; ATF4 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; KLRK1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; RBM4 PROTEIN, HUMAN; SIGNAL PEPTIDE; ULBP1 PROTEIN, HUMAN;

ARTICLE; BIOGENESIS; CANCER CELL LINE; CELL STRESS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; FLOW CYTOMETRY; GENE EXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; LUCIFERASE ASSAY; MUTAGENESIS; NATURAL KILLER CELL; OXIDATIVE STRESS; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; RNA SPLICING; TUMOR CELL; TUMOR GROWTH; UNFOLDED PROTEIN RESPONSE; UPREGULATION; GENETIC SCREENING; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTOR 4; CELL LINE, TUMOR; GENETIC TESTING; GPI-LINKED PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RNA-BINDING PROTEINS;

EID: 84949435161     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08474     Document Type: Article

References (73)

1. Ameri K, Lewis CE, Raida M, Sowter H, Hai T, Harris AL. 2004. Anoxic induction of ATF-4 through HIF-1- independent pathways of protein stabilization in human cancer cells. Blood 103:1876-1882. doi: 10.1182/blood- 2003-06-1859.
2. Bae JS, Koo NY, Namkoong E, Davies AJ, Choi SK, Shin Y, Jin M, Hwang SM, Mikoshiba K, Park K. 2013. Chaperone stress 70 protein (STCH) binds and regulates two acid/base transporters NBCe1-B and NHE1. The Journal of Biological Chemistry 288:6295-6305. doi: 10.1074/jbc.M112.392001.
3. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, Harding H, Novoa I, Varia M, Raleigh J, Scheuner D, Kaufman RJ, Bell J, Ron D, Wouters BG, Koumenis C. 2005. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. The EMBO Journal 24:3470-3481. doi: 10.1038/sj.emboj.7600777.
4. Butler JE, Moore MB, Presnell SR, Chan HW, Chalupny NJ, Lutz CT. 2009. Proteasome regulation of ULBP1 transcription. Journal of Immunology 182:6600-6609. doi: 10.4049/jimmunol.0801214.
5. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, Godarova A, Kotecki M, Cochran BH, Spooner E, Ploegh HL, Brummelkamp TR. 2009. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326:1231-1235. doi: 10.1126/science.1178955.
6. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, Mulherkar N, Kuehne AI, Kranzusch PJ, Griffin AM, Ruthel G, Dal Cin P, Dye JM, Whelan SP, Chandran K, Brummelkamp TR. 2011. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477:340-343. doi: 10.1038/nature10348.
7. Chen H, Pan YX, Dudenhausen EE, Kilberg MS. 2004. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrientresponsive basic region/leucine zipper transcription factors as well as localized histone acetylation. The Journal of Biological Chemistry 279:50829-50839. doi: 10.1074/jbc.M409173200.
8. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. 2001. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413:165-171. doi: 10.1038/35093109.
9. Escobar TM, Kanellopoulou C, Kugler DG, Kilaru G, Nguyen CK, Nagarajan V, Bhairavabhotla RK, Northrup D, Zahr R, Burr P, Liu X, Zhao K, Sher A, Jankovic D, Zhu J, Muljo SA. 2014. miR-155 activates cytokine gene expression in Th17 cells by regulating the DNA-binding protein Jarid2 to relieve polycomb-mediated repression. Immunity 40:865-879. doi: 10.1016/j.immuni.2014.03.014.
10. Fang H, Panzner S, Mullins C, Hartmann E, Green N. 1996. The homologue of mammalian SPC12 is important for efficient signal peptidase activity in Saccharomyces cerevisiae. The Journal of Biological Chemistry 271:16460-16465. doi: 10.1074/jbc.271.28.16460.
11. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM, Kennedy KA, Patierno SR. 2000. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Research and Treatment 59:15-26. doi: 10.1023/A:1006332011207.
12. Fujimoto T, Onda M, Nagai H, Nagahata T, Ogawa K, Emi M. 2003. Upregulation and overexpression of human X-box binding protein 1 (hXBP-1) gene in primary breast cancers. Breast Cancer 10:301-306. doi: 10.1007/ BF02967649.
13. Gasser S, Orsulic S, Brown EJ, Raulet DH. 2005. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436:1186-1190. doi: 10.1038/nature03884
14. Gasser S, Raulet DH. 2006. Activation and self-tolerance of natural killer cells. Immunological Reviews 214:130-142. doi: 10.1111/j.1600-065X.2006.00460.x.
15. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, Guimaraes C, Panning B, Ploegh HL, Bassik MC, Qi LS, Kampmann M, Weissman JS. 2014. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159:647-661. doi: 10.1016/j.cell.2014.09.029.
16. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, Knoblaugh S, Cado D, Greenberg NM, Raulet DH. 2008. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28:571-580. doi: 10.1016/j.immuni.2008.02.016.
17. Hamerman JA, Ogasawara K, Lanier LL. 2004. Cutting edge: toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. Journal of Immunology 172:2001-2005. doi: 10.4049/jimmunol.172.4.2001.
18. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, Shan J, Yuan CL, Krokowski D, Wang S, Hatzoglou M, Kilberg MS, Sartor MA, Kaufman RJ. 2013. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nature Cell Biology 15:481-490. doi: 10.1038/ncb2738.
19. Hansen BS, Vaughan MH, Wang L. 1972. Reversible inhibition by histidinol of protein synthesis in human cells at the activation of histidine. The Journal of Biological Chemistry 247:3854-3857.
20. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Molecular Cell 6:1099-1108. doi: 10.1016/S1097-2765(00) 00108-8.
21. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molecular Cell 11:619-633. doi: 10.1016/S1097-2765(03)00105-9.
22. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell 38:576-589. doi: 10.1016/j.molcel.2010.05.004.
23. Hilpert J, Grosse-Hovest L, Gr ünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. 2012. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. Journal of Immunology 189:1360-1371. doi: 10.4049/jimmunol.1200796.
24. Jain RK. 2005. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58-62. doi: 10.1126/science.1104819.
25. Jheng JR, Ho JY, Horng JT. 2014. ER stress, autophagy, and RNA viruses. Frontiers in Microbiology 5:388. doi: 10.3389/fmicb.2014.00388.
26. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. 2013. RNA-programmed genome editing in human cells. eLife 2:e00471. doi: 10.7554/eLife.00471.
27. Jung H, Hsiung B, Pestal K, Procyk E, Raulet DH. 2012. RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry. Journal of Experimental Medicine 209:2409-2422. doi: 10.1084/jem.20120565.
28. Katz Y, Wang ET, Airoldi EM, Burge CB. 2010. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nature Methods 7:1009-1015. doi: 10.1038/nmeth.1528.
29. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/gb-2013-14-4-r36.
30. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357-359. doi: 10. 1038/nmeth.1923.
31. Lin JC, Hsu M, Tarn WY. 2007. Cell stress modulates the function of splicing regulatory protein RBM4 in translation control. Proceedings of the National Academy of Sciences of USA 104:2235-2240. doi: 10.1073/pnas. 0611015104.
32. Lin JC, Tarn WY. 2009. RNA-binding motif protein 4 translocates to cytoplasmic granules and suppresses translation via argonaute2 during muscle cell differentiation. The Journal of Biological Chemistry 284:34658-34665. doi: 10.1074/jbc.M109.032946.
33. López-Soto A, Quioñes-Lombraña A, López-Arbesu R, López-Larrea C, González S. 2006.Transcriptional regulation of ULBP1, a human ligand of the NKG2D receptor. The Journal of Biological Chemistry 281:30419-30430. doi: 10.1074/jbc.M604868200.
34. Ma Y, Hendershot LM. 2004. The role of the unfolded protein response in tumour development: friend or foe? Nature Reviews Cancer 4:966-977. doi: 10.1038/nrc1505.
35. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826. doi: 10.1126/science.1232033.
36. Maquat LE. 2004. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nature Reviews Molecular Cell Biology 5:89-99. doi: 10.1038/nrm1310.
37. Marcus A, Gowen BG, Thompson TW, Iannello A, Ardolino M, Deng W, Wang L, Shifrin N, Raulet DH. 2014. Recognition of tumors by the innate immune system and natural killer cells. Advances in Immunology 122:91-128. doi: 10.1016/B978-0-12-800267-4.00003-1.
38. Markus MA, Morris BJ. 2009. RBM4: a multifunctional RNA-binding protein. The International Journal of Biochemistry & Cell Biology 41:740-743. doi: 10.1016/j.biocel.2008.05.027.
39. McGilvray RW, Eagle RA, Watson NF, Al-Attar A, Ball G, Jafferji I, Trowsdale J, Durrant LG. 2009. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clinical Cancer Research 15:6993-7002. doi: 10.1158/1078-0432.CCR-09-0991.
40. Mittal D, Gubin MM, Schreiber RD, Smyth MJ. 2014. New insights into cancer immunoediting and its three component phases-elimination, equilibrium and escape. Current Opinion in Immunology 27:16-25. doi: 10.1016/j.coi.2014.01.004.
41. Mohr I, Sonenberg N. 2012. Host translation at the nexus of infection and immunity. Cell Host & Microbe 12:470-483. doi: 10.1016/j.chom.2012.09.006.
42. Mullins C, Meyer HA, Hartmann E, Green N, Fang H. 1996. Structurally related Spc1p and Spc2p of yeast signal peptidase complex are functionally distinct. The Journal of Biological Chemistry 271:29094-29099. doi: 10.1074/jbc.271.46.29094.
43. Munshi NC, Hideshima T, Carrasco D, Shammas M, Auclair D, Davies F, Mitsiades N, Mitsiades C, Kim RS, Li C, Rajkumar SV, Fonseca R, Bergsagel L, Chauhan D, Anderson KC. 2004. Identification of genes modulated in multiple myeloma using genetically identical twin samples. Blood 103:1799-1806. doi: 10.1182/blood-2003-02-0402.
44. Nice TJ, Coscoy L, Raulet DH. 2009. Posttranslational regulation of the NKG2D ligand Mult1 in response to cell stress. Journal of Experimental Medicine 206:287-298. doi: 10.1084/jem.20081335.
45. Oslowski CM, Urano F. 2011. Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods in Enzymology 490:71-92. doi: 10.1016/B978-0-12-385114-7.00004-0.
46. Otterson GA, Flynn GC, Kratzke RA, Coxon A, Johnston PG, Kaye FJ. 1994. Stch encodes the’ATPase core’ of a microsomal stress 70 protein. The EMBO Journal 13:1216-1225.
47. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. doi: 10.1093/bioinformatics/btq033.
48. Raulet DH. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nature Reviews Immunology 3:781-790. doi: 10.1038/nri1199.
49. Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. 2013. Regulation of ligands for the NKG2D activating receptor. Annual Review of Immunology 31:413-441. doi: 10.1146/annurev-immunol-032712-095951.
50. Raulet DH, Guerra N. 2009. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nature Reviews Immunology 9:568-580. doi: 10.1038/nri2604.
51. Reimold AM, Ponath PD, Li YS, Hardy RR, David CS, Strominger JL, Glimcher LH. 1996. Transcription factor B cell lineage-specific activator protein regulates the gene for human X-box binding protein 1. Journal of Experimental Medicine 183:393-401. doi: 10.1084/jem.183.2.393.
52. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nature Biotechnology 29:24-26. doi: 10.1038/nbt.1754.
53. Roybal CN, Hunsaker LA, Barbash O, Vander Jagt DL, Abcouwer SF. 2005. The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. The Journal of Biological Chemistry 280:20331-20339. doi: 10.1074/jbc.M411275200.
54. Rutkowski DT, Kaufman RJ. 2003. All roads lead to ATF4. Developmental Cell 4:442-444. doi: 10.1016/S1534- 5807(03)00100-X.
55. Schreiber RD, Old LJ, Smyth MJ. 2011. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565-1570. doi: 10.1126/science.1203486.
56. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84-87. doi: 10.1126/science.1247005.
57. Shifrin N, Raulet DH, Ardolino M. 2014. NK cell self tolerance, responsiveness and missing self recognition. Seminars in Immunology 26:138-144. doi: 10.1016/j.smim.2014.02.007.
58. Shuda M, Kondoh N, Imazeki N, Tanaka K, Okada T, Mori K, Hada A, Arai M, Wakatsuki T, Matsubara O, Yamamoto N, Yamamoto M. 2003. Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis. Journal of Hepatology 38:605-614. doi: 10.1016/S0168-8278(03)00029-1.
59. Soriani A, Iannitto ML, Ricci B, Fionda C, Malgarini G, Morrone S, Peruzzi G, Ricciardi MR, Petrucci MT, Cippitelli M, Santoni A. 2014. Reactive oxygen species- and DNA damage response-dependent NK cell activating ligand upregulation occurs at transcriptional levels and requires the transcriptional factor E2F1. Journal of Immunology 193:950-960. doi: 10.4049/jimmunol.1400271.
60. Soriani A, Zingoni A, Cerboni C, Iannitto ML, Ricciardi MR, Di Gialleonardo V, Cippitelli M, Fionda C, Petrucci MT, Guarini A, Foa R, Santoni A. 2009. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 113:3503-3511. doi: 10.1182/blood-2008-08-173914.
61. Suragani RN, Zachariah RS, Velazquez JG, Liu S, Sun CW, Townes TM, Chen JJ. 2012. Heme-regulated eIF2α kinase activated Atf4 signaling pathway in oxidative stress and erythropoiesis. Blood 119:5276-5284. doi: 10.1182/blood-2011-10-388132.
62. Suzuki R, Matsuda M, Watashi K, Aizaki H, Matsuura Y, Wakita T, Suzuki T. 2013. Signal peptidase complex subunit1 participates in the assembly of hepatitis C virus through an interaction with E2 and NS2. PLOS Pathogens 9:e1003589. doi: 10.1371/journal.ppat.1003589.
63. Tabas I, Ron D. 2011. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nature Cell Biology 13:184-190. doi: 10.1038/ncb0311-184.
64. Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. 2011. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Research 71:5998-6009. doi: 10.1158/0008-5472.CAN-10-3211.
65. Thiaville MM, Dudenhausen EE, Zhong C, Pan YX, Kilberg MS. 2008. Deprivation of protein or amino acid induces C/EBPbeta synthesis and binding to amino acid response elements, but its action is not an absolute requirement for enhanced transcription. The Biochemical Journal 410:473-484. doi: 10.1042/BJ20071252.
66. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7:562-578. doi: 10.1038/nprot.2012.016.
67. Uniacke J, Holterman CE, Lachance G, Franovic A, Jacob MD, Fabian MR, Payette J, Holcik M, Pause A, Lee S. 2012. An oxygen-regulated switch in the protein synthesis machinery. Nature 486:126-129. doi: 10.1038/nature11055.
68. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3:RESEARCH0034. doi: 10.1186/gb-2002-3-7-research0034.
69. Venkataraman GM, Suciu D, Groh V, Boss JM, Spies T. 2007. Promoter region architecture and transcriptional regulation of the genes for the MHC class I-related chain A and B ligands of NKG2D. Journal of Immunology 178:961-969. doi: 10.4049/jimmunol.178.2.961.
70. Vetter CS, Groh V, Thor Straten P, Spies T, Brocker EB, Becker JC. 2002. Expression of stress-induced MHC class I related chain molecules on human melanoma. Journal of Investigative Dermatology 118:600-605. doi: 10.1046/j. 1523-1747.2002.01700.x.
71. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. 2011. Innate or adaptive immunity? the example of natural killer cells. Science 331:44-49. doi: 10.1126/science.1198687
72. Wang T, Wei JJ, Sabatini DM, Lander ES. 2014a. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:80-84. doi: 10.1126/science.1246981.
73. Wang Y, Chen D, Qian H, Tsai YS, Shao S, Liu Q, Dominguez D, Wang Z. 2014b. The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression. Cancer Cell 26:374-389. doi: 10.1016/j. ccr.2014.07.010.