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The CRISPR System and Cancer Immunotherapy Biomarkers

  • Vitaly Balan
  • Jianbin WangEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2055)

Abstract

Recent advances in cancer immunotherapy have shed new light on the possibility to cure most, if not all, cancer patients with further development of various treatment options. The emergency of a new genome editing tool, the clustered regularly interspaced short palindromic repeats (CRISPR) technology, revolutionized the biomedical research field. We envision application of the CRISPR technology in cancer research, diagnosis, and therapy will markedly speed up the development of new treatment options for cancer patients. The CRISPR system and its applications in biomedical research will be discussed with an emphasis on cancer immunotherapy and biomarker development.

Key words

CRISPR Cas9 dCas9 sgRNA Cancer Immunotherapy Biomarker 

Notes

Acknowledgments

We thank Bing C. Wang, Francesco Marincola, and other colleagues of Refuge Biotechnologies for their support.

References

  1. 1.
    McCarthy EF (2006) The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas. Iowa Orthop J 26:154–158PubMedPubMedCentralGoogle Scholar
  2. 2.
    Leach DR, Krummel MF, Allison JP (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271(5256):1734–1736CrossRefGoogle Scholar
  3. 3.
    Nishimura H, Nose M, Hiai H, Minato N, Honjo T (1999) Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11(2):141–151CrossRefGoogle Scholar
  4. 4.
    Nishimura H, Minato N, Nakano T, Honjo T (1998) Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int Immunol 10(10):1563–1572CrossRefGoogle Scholar
  5. 5.
    Lander ES (2016) The heroes of CRISPR. Cell 164(1–2):18–28.  https://doi.org/10.1016/j.cell.2015.12.041CrossRefPubMedGoogle Scholar
  6. 6.
    Morange M (2015) What history tells us XXXVII. CRISPR-Cas: the discovery of an immune system in prokaryotes. J Biosci 40(2):221–223CrossRefGoogle Scholar
  7. 7.
    Morange M (2015) What history tells us XXXIX. CRISPR-Cas: from a prokaryotic immune system to a universal genome editing tool. J Biosci 40(5):829–832CrossRefGoogle Scholar
  8. 8.
    Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169(12):5429–5433CrossRefGoogle Scholar
  9. 9.
    Mojica FJ, Ferrer C, Juez G, Rodriguez-Valera F (1995) Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol Microbiol 17(1):85–93CrossRefGoogle Scholar
  10. 10.
    Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151(Pt 3):653–663.  https://doi.org/10.1099/mic.0.27437-0CrossRefPubMedGoogle Scholar
  11. 11.
    Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60(2):174–182.  https://doi.org/10.1007/s00239-004-0046-3CrossRefPubMedGoogle Scholar
  12. 12.
    Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(Pt 8):2551–2561.  https://doi.org/10.1099/mic.0.28048-0CrossRefPubMedGoogle Scholar
  13. 13.
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821.  https://doi.org/10.1126/science.1225829CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 109(39):E2579–E2586.  https://doi.org/10.1073/pnas.1208507109CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823.  https://doi.org/10.1126/science.1231143CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    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(6121):823–826.  https://doi.org/10.1126/science.1232033CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Cho SW, Kim S, Kim JM, Kim JS (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31(3):230–232.  https://doi.org/10.1038/nbt.2507CrossRefPubMedGoogle Scholar
  18. 18.
    Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227–229.  https://doi.org/10.1038/nbt.2501CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7):397–405.  https://doi.org/10.1016/j.tibtech.2013.04.004CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–383.  https://doi.org/10.1146/annurev.genet.40.110405.090451CrossRefPubMedGoogle Scholar
  21. 21.
    Sharma R, Anguela XM, Doyon Y, Wechsler T, DeKelver RC, Sproul S, Paschon DE, Miller JC, Davidson RJ, Shivak D, Zhou S, Rieders J, Gregory PD, Holmes MC, Rebar EJ, High KA (2015) In vivo genome editing of the albumin locus as a platform for protein replacement therapy. Blood 126(15):1777–1784.  https://doi.org/10.1182/blood-2014-12-615492CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Nishimasu H, Cong L, Yan WX, Ran FA, Zetsche B, Li Y, Kurabayashi A, Ishitani R, Zhang F, Nureki O (2015) Crystal structure of Staphylococcus aureus Cas9. Cell 162(5):1113–1126.  https://doi.org/10.1016/j.cell.2015.08.007CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152(5):1173–1183.  https://doi.org/10.1016/j.cell.2013.02.022CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6):1380–1389.  https://doi.org/10.1016/j.cell.2013.08.021CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154(2):442–451.  https://doi.org/10.1016/j.cell.2013.06.044CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Chavez A, Scheiman J, Vora S, Pruitt BW, Tuttle M, E PRI, Lin S, Kiani S, Guzman CD, Wiegand DJ, Ter-Ovanesyan D, Braff JL, Davidsohn N, Housden BE, Perrimon N, Weiss R, Aach J, Collins JJ, Church GM (2015) Highly efficient Cas9-mediated transcriptional programming. Nat Methods 12(4):326–328.  https://doi.org/10.1038/nmeth.3312CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H, Nureki O, Zhang F (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517(7536):583–588.  https://doi.org/10.1038/nature14136CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ, Joung J, Zhang F (2017) RNA editing with CRISPR-Cas13. Science 358(6366):1019–1027.  https://doi.org/10.1126/science.aaq0180CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J, Belanto JJ, Verdine V, Cox DBT, Kellner MJ, Regev A, Lander ES, Voytas DF, Ting AY, Zhang F (2017) RNA targeting with CRISPR-Cas13. Nature 550(7675):280–284.  https://doi.org/10.1038/nature24049CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Amabile A, Migliara A, Capasso P, Biffi M, Cittaro D, Naldini L, Lombardo A (2016) Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell 167(1):219–232 e214.  https://doi.org/10.1016/j.cell.2016.09.006CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Cano-Rodriguez D, Gjaltema RA, Jilderda LJ, Jellema P, Dokter-Fokkens J, Ruiters MH, Rots MG (2016) Writing of H3K4Me3 overcomes epigenetic silencing in a sustained but context-dependent manner. Nat Commun 7:12284.  https://doi.org/10.1038/ncomms12284CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Choudhury SR, Cui Y, Lubecka K, Stefanska B, Irudayaraj J (2016) CRISPR-dCas9 mediated TET1 targeting for selective DNA demethylation at BRCA1 promoter. Oncotarget 7(29):46545–46556.  https://doi.org/10.18632/oncotarget.10234CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33(5):510–517.  https://doi.org/10.1038/nbt.3199CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Kearns NA, Pham H, Tabak B, Genga RM, Silverstein NJ, Garber M, Maehr R (2015) Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods 12(5):401–403.  https://doi.org/10.1038/nmeth.3325CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kwon DY, Zhao YT, Lamonica JM, Zhou Z (2017) Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC. Nat Commun 8:15315.  https://doi.org/10.1038/ncomms15315CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD (2014) A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159(3):635–646.  https://doi.org/10.1016/j.cell.2014.09.039CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2017) Programmable base editing of A∗T to G∗C in genomic DNA without DNA cleavage. Nature 551(7681):464–471.  https://doi.org/10.1038/nature24644CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32(6):569–576.  https://doi.org/10.1038/nbt.2908CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Guilinger JP, Thompson DB, Liu DR (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32(6):577–582.  https://doi.org/10.1038/nbt.2909CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Evers B, Jastrzebski K, Heijmans JP, Grernrum W, Beijersbergen RL, Bernards R (2016) CRISPR knockout screening outperforms shRNA and CRISPRi in identifying essential genes. Nat Biotechnol 34(6):631–633.  https://doi.org/10.1038/nbt.3536CrossRefPubMedGoogle Scholar
  41. 41.
    Munoz DM, Cassiani PJ, Li L, Billy E, Korn JM, Jones MD, Golji J, Ruddy DA, Yu K, McAllister G, DeWeck A, Abramowski D, Wan J, Shirley MD, Neshat SY, Rakiec D, de Beaumont R, Weber O, Kauffmann A, McDonald ER 3rd, Keen N, Hofmann F, Sellers WR, Schmelzle T, Stegmeier F, Schlabach MR (2016) CRISPR screens provide a comprehensive assessment of Cancer vulnerabilities but generate false-positive hits for highly amplified genomic regions. Cancer Discov 6(8):900–913.  https://doi.org/10.1158/2159-8290.CD-16-0178CrossRefPubMedGoogle Scholar
  42. 42.
    Aguirre AJ, Meyers RM, Weir BA, Vazquez F, Zhang CZ, Ben-David U, Cook A, Ha G, Harrington WF, Doshi MB, Kost-Alimova M, Gill S, Xu H, Ali LD, Jiang G, Pantel S, Lee Y, Goodale A, Cherniack AD, Oh C, Kryukov G, Cowley GS, Garraway LA, Stegmaier K, Roberts CW, Golub TR, Meyerson M, Root DE, Tsherniak A, Hahn WC (2016) Genomic copy number dictates a gene-independent cell response to CRISPR/Cas9 targeting. Cancer Discov 6(8):914–929.  https://doi.org/10.1158/2159-8290.CD-16-0154CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Hart T, Chandrashekhar M, Aregger M, Steinhart Z, Brown KR, MacLeod G, Mis M, Zimmermann M, Fradet-Turcotte A, Sun S, Mero P, Dirks P, Sidhu S, Roth FP, Rissland OS, Durocher D, Angers S, Moffat J (2015) High-resolution CRISPR screens reveal fitness genes and genotype-specific Cancer liabilities. Cell 163(6):1515–1526.  https://doi.org/10.1016/j.cell.2015.11.015CrossRefGoogle Scholar
  44. 44.
    Tzelepis K, Koike-Yusa H, De Braekeleer E, Li Y, Metzakopian E, Dovey OM, Mupo A, Grinkevich V, Li M, Mazan M, Gozdecka M, Ohnishi S, Cooper J, Patel M, McKerrell T, Chen B, Domingues AF, Gallipoli P, Teichmann S, Ponstingl H, McDermott U, Saez-Rodriguez J, Huntly BJP, Iorio F, Pina C, Vassiliou GS, Yusa K (2016) A CRISPR dropout screen identifies genetic vulnerabilities and therapeutic targets in acute myeloid leukemia. Cell Rep 17(4):1193–1205.  https://doi.org/10.1016/j.celrep.2016.09.079CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Wang T, Yu H, Hughes NW, Liu B, Kendirli A, Klein K, Chen WW, Lander ES, Sabatini DM (2017) Gene essentiality profiling reveals gene networks and synthetic lethal interactions with oncogenic ras. Cell 168(5):890–903 e815.  https://doi.org/10.1016/j.cell.2017.01.013CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Steinhart Z, Pavlovic Z, Chandrashekhar M, Hart T, Wang X, Zhang X, Robitaille M, Brown KR, Jaksani S, Overmeer R, Boj SF, Adams J, Pan J, Clevers H, Sidhu S, Moffat J, Angers S (2017) Genome-wide CRISPR screens reveal a Wnt-FZD5 signaling circuit as a druggable vulnerability of RNF43-mutant pancreatic tumors. Nat Med 23(1):60–68.  https://doi.org/10.1038/nm.4219CrossRefPubMedGoogle Scholar
  47. 47.
    Zhan T, Boutros M (2016) Towards a compendium of essential genes - from model organisms to synthetic lethality in cancer cells. Crit Rev Biochem Mol Biol 51(2):74–85.  https://doi.org/10.3109/10409238.2015.1117053CrossRefPubMedGoogle Scholar
  48. 48.
    Shifrut E, Carnevale J, Tobin V, Roth TL, Woo JM, Bui CT, Li PJ, Diolaiti ME, Ashworth A, Marson A (2018) Genome-wide CRISPR screens in primary human T cells reveal key regulators of immune function. Cell 175:1958.  https://doi.org/10.1016/j.cell.2018.10.024CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Patel SJ, Sanjana NE, Kishton RJ, Eidizadeh A, Vodnala SK, Cam M, Gartner JJ, Jia L, Steinberg SM, Yamamoto TN, Merchant AS, Mehta GU, Chichura A, Shalem O, Tran E, Eil R, Sukumar M, Guijarro EP, Day CP, Robbins P, Feldman S, Merlino G, Zhang F, Restifo NP (2017) Identification of essential genes for cancer immunotherapy. Nature 548(7669):537–542.  https://doi.org/10.1038/nature23477CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Kearney CJ, Vervoort SJ, Hogg SJ, Ramsbottom KM, Freeman AJ, Lalaoui N, Pijpers L, Michie J, Brown KK, Knight DA, Sutton V, Beavis PA, Voskoboinik I, Darcy PK, Silke J, Trapani JA, Johnstone RW, Oliaro J (2018) Tumor immune evasion arises through loss of TNF sensitivity. Sci Immunol 3(23):eaar3451.  https://doi.org/10.1126/sciimmunol.aar3451CrossRefPubMedGoogle Scholar
  51. 51.
    Finucane HK, Bulik-Sullivan B, Gusev A, Trynka G, Reshef Y, Loh PR, Anttila V, Xu H, Zang C, Farh K, Ripke S, Day FR, ReproGen C, Schizophrenia Working Group of the Psychiatric Genomics C, Consortium R, Purcell S, Stahl E, Lindstrom S, Perry JR, Okada Y, Raychaudhuri S, Daly MJ, Patterson N, Neale BM, Price AL (2015) Partitioning heritability by functional annotation using genome-wide association summary statistics. Nat Genet 47(11):1228–1235.  https://doi.org/10.1038/ng.3404CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sanjana NE, Wright J, Zheng K, Shalem O, Fontanillas P, Joung J, Cheng C, Regev A, Zhang F (2016) High-resolution interrogation of functional elements in the noncoding genome. Science 353(6307):1545–1549.  https://doi.org/10.1126/science.aaf7613CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Fulco CP, Munschauer M, Anyoha R, Munson G, Grossman SR, Perez EM, Kane M, Cleary B, Lander ES, Engreitz JM (2016) Systematic mapping of functional enhancer-promoter connections with CRISPR interference. Science 354(6313):769–773.  https://doi.org/10.1126/science.aag2445CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Gao Y, Xiong X, Wong S, Charles EJ, Lim WA, Qi LS (2016) Complex transcriptional modulation with orthogonal and inducible dCas9 regulators. Nat Methods 13(12):1043–1049.  https://doi.org/10.1038/nmeth.4042CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Gjaltema RAF, Schulz EG (2018) CRISPR/dCas9 switch systems for temporal transcriptional control. Methods Mol Biol 1767:167–185.  https://doi.org/10.1007/978-1-4939-7774-1_8CrossRefPubMedGoogle Scholar
  56. 56.
    Zuckermann M, Hovestadt V, Knobbe-Thomsen CB, Zapatka M, Northcott PA, Schramm K, Belic J, Jones DT, Tschida B, Moriarity B, Largaespada D, Roussel MF, Korshunov A, Reifenberger G, Pfister SM, Lichter P, Kawauchi D, Gronych J (2015) Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling. Nat Commun 6:7391.  https://doi.org/10.1038/ncomms8391CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Walter DM, Venancio OS, Buza EL, Tobias JW, Deshpande C, Gudiel AA, Kim-Kiselak C, Cicchini M, Yates TJ, Feldser DM (2017) Systematic in vivo inactivation of chromatin-regulating enzymes identifies Setd2 as a potent tumor suppressor in lung adenocarcinoma. Cancer Res 77(7):1719–1729.  https://doi.org/10.1158/0008-5472.CAN-16-2159CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Matano M, Date S, Shimokawa M, Takano A, Fujii M, Ohta Y, Watanabe T, Kanai T, Sato T (2015) Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat Med 21(3):256–262.  https://doi.org/10.1038/nm.3802CrossRefPubMedGoogle Scholar
  59. 59.
    Drost J, van Jaarsveld RH, Ponsioen B, Zimberlin C, van Boxtel R, Buijs A, Sachs N, Overmeer RM, Offerhaus GJ, Begthel H, Korving J, van de Wetering M, Schwank G, Logtenberg M, Cuppen E, Snippert HJ, Medema JP, Kops GJ, Clevers H (2015) Sequential cancer mutations in cultured human intestinal stem cells. Nature 521(7550):43–47.  https://doi.org/10.1038/nature14415CrossRefPubMedGoogle Scholar
  60. 60.
    Ogawa J, Pao GM, Shokhirev MN, Verma IM (2018) Glioblastoma model using human cerebral organoids. Cell Rep 23(4):1220–1229.  https://doi.org/10.1016/j.celrep.2018.03.105CrossRefPubMedGoogle Scholar
  61. 61.
    Oldrini B, Curiel-Garcia A, Marques C, Matia V, Uluckan O, Grana-Castro O, Torres-Ruiz R, Rodriguez-Perales S, Huse JT, Squatrito M (2018) Somatic genome editing with the RCAS-TVA-CRISPR-Cas9 system for precision tumor modeling. Nat Commun 9(1):1466.  https://doi.org/10.1038/s41467-018-03731-wCrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Torres R, Martin MC, Garcia A, Cigudosa JC, Ramirez JC, Rodriguez-Perales S (2014) Engineering human tumour-associated chromosomal translocations with the RNA-guided CRISPR-Cas9 system. Nat Commun 5:3964.  https://doi.org/10.1038/ncomms4964CrossRefPubMedGoogle Scholar
  63. 63.
    Maddalo D, Manchado E, Concepcion CP, Bonetti C, Vidigal JA, Han YC, Ogrodowski P, Crippa A, Rekhtman N, de Stanchina E, Lowe SW, Ventura A (2014) In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516(7531):423–427.  https://doi.org/10.1038/nature13902CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Lagutina IV, Valentine V, Picchione F, Harwood F, Valentine MB, Villarejo-Balcells B, Carvajal JJ, Grosveld GC (2015) Modeling of the human alveolar rhabdomyosarcoma Pax3-Foxo1 chromosome translocation in mouse myoblasts using CRISPR-Cas9 nuclease. PLoS Genet 11(2):e1004951.  https://doi.org/10.1371/journal.pgen.1004951CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Engelholm LH, Riaz A, Serra D, Dagnaes-Hansen F, Johansen JV, Santoni-Rugiu E, Hansen SH, Niola F, Frodin M (2017) CRISPR/Cas9 engineering of adult mouse liver demonstrates that the Dnajb1-Prkaca gene fusion is sufficient to induce tumors resembling Fibrolamellar hepatocellular carcinoma. Gastroenterology 153(6):1662–1673 e1610.  https://doi.org/10.1053/j.gastro.2017.09.008CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L, Kempton HR, Dahlman JE, Parnas O, Eisenhaure TM, Jovanovic M, Graham DB, Jhunjhunwala S, Heidenreich M, Xavier RJ, Langer R, Anderson DG, Hacohen N, Regev A, Feng G, Sharp PA, Zhang F (2014) CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159(2):440–455.  https://doi.org/10.1016/j.cell.2014.09.014CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Xue W, Chen S, Yin H, Tammela T, Papagiannakopoulos T, Joshi NS, Cai W, Yang G, Bronson R, Crowley DG, Zhang F, Anderson DG, Sharp PA, Jacks T (2014) CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514(7522):380–384.  https://doi.org/10.1038/nature13589CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Maresch R, Mueller S, Veltkamp C, Ollinger R, Friedrich M, Heid I, Steiger K, Weber J, Engleitner T, Barenboim M, Klein S, Louzada S, Banerjee R, Strong A, Stauber T, Gross N, Geumann U, Lange S, Ringelhan M, Varela I, Unger K, Yang F, Schmid RM, Vassiliou GS, Braren R, Schneider G, Heikenwalder M, Bradley A, Saur D, Rad R (2016) Multiplexed pancreatic genome engineering and cancer induction by transfection-based CRISPR/Cas9 delivery in mice. Nat Commun 7:10770.  https://doi.org/10.1038/ncomms10770CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Schokrpur S, Hu J, Moughon DL, Liu P, Lin LC, Hermann K, Mangul S, Guan W, Pellegrini M, Xu H, Wu L (2016) CRISPR-mediated VHL knockout generates an improved model for metastatic renal cell carcinoma. Sci Rep 6:29032.  https://doi.org/10.1038/srep29032CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155(7):1479–1491.  https://doi.org/10.1016/j.cell.2013.12.001CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Chen B, Hu J, Almeida R, Liu H, Balakrishnan S, Covill-Cooke C, Lim WA, Huang B (2016) Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucleic Acids Res 44(8):e75.  https://doi.org/10.1093/nar/gkv1533CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Ma H, Tu LC, Naseri A, Huisman M, Zhang S, Grunwald D, Pederson T (2016) Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow. Nat Biotechnol 34(5):528–530.  https://doi.org/10.1038/nbt.3526CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Ma H, Tu LC, Naseri A, Chung YC, Grunwald D, Zhang S, Pederson T (2018) CRISPR-Sirius: RNA scaffolds for signal amplification in genome imaging. Nat Methods 15(11):928–931.  https://doi.org/10.1038/s41592-018-0174-0CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Pardee K, Green AA, Takahashi MK, Braff D, Lambert G, Lee JW, Ferrante T, Ma D, Donghia N, Fan M, Daringer NM, Bosch I, Dudley DM, O'Connor DH, Gehrke L, Collins JJ (2016) Rapid, low-cost detection of Zika virus using programmable biomolecular components. Cell 165(5):1255–1266.  https://doi.org/10.1016/j.cell.2016.04.059CrossRefPubMedGoogle Scholar
  75. 75.
    Guk K, Keem JO, Hwang SG, Kim H, Kang T, Lim EK, Jung J (2017) A facile, rapid and sensitive detection of MRSA using a CRISPR-mediated DNA FISH method, antibody-like dCas9/sgRNA complex. Biosens Bioelectron 95:67–71.  https://doi.org/10.1016/j.bios.2017.04.016CrossRefPubMedGoogle Scholar
  76. 76.
    Deng W, Shi X, Tjian R, Lionnet T, Singer RH (2015) CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci U S A 112(38):11870–11875.  https://doi.org/10.1073/pnas.1515692112CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Gootenberg JS, Abudayyeh OO, Lee JW, Essletzbichler P, Dy AJ, Joung J, Verdine V, Donghia N, Daringer NM, Freije CA, Myhrvold C, Bhattacharyya RP, Livny J, Regev A, Koonin EV, Hung DT, Sabeti PC, Collins JJ, Zhang F (2017) Nucleic acid detection with CRISPR-Cas13a/C2c2. Science 356(6336):438–442.  https://doi.org/10.1126/science.aam9321CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Gootenberg JS, Abudayyeh OO, Kellner MJ, Joung J, Collins JJ, Zhang F (2018) Multiplexed and portable nucleic acid detection platform with Cas13, Cas12a, and Csm6. Science 360(6387):439–444.  https://doi.org/10.1126/science.aaq0179CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Myhrvold C, Freije CA, Gootenberg JS, Abudayyeh OO, Metsky HC, Durbin AF, Kellner MJ, Tan AL, Paul LM, Parham LA, Garcia KF, Barnes KG, Chak B, Mondini A, Nogueira ML, Isern S, Michael SF, Lorenzana I, Yozwiak NL, MacInnis BL, Bosch I, Gehrke L, Zhang F, Sabeti PC (2018) Field-deployable viral diagnostics using CRISPR-Cas13. Science 360(6387):444–448.  https://doi.org/10.1126/science.aas8836CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Barrangou R, Marraffini LA (2014) CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol Cell 54(2):234–244.  https://doi.org/10.1016/j.molcel.2014.03.011CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    McKenna A, Findlay GM, Gagnon JA, Horwitz MS, Schier AF, Shendure J (2016) Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353(6298):aaf7907.  https://doi.org/10.1126/science.aaf7907CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Kalhor R, Mali P, Church GM (2017) Rapidly evolving homing CRISPR barcodes. Nat Methods 14(2):195–200.  https://doi.org/10.1038/nmeth.4108CrossRefPubMedGoogle Scholar
  83. 83.
    Michlits G, Hubmann M, Wu SH, Vainorius G, Budusan E, Zhuk S, Burkard TR, Novatchkova M, Aichinger M, Lu Y, Reece-Hoyes J, Nitsch R, Schramek D, Hoepfner D, Elling U (2017) CRISPR-UMI: single-cell lineage tracing of pooled CRISPR-Cas9 screens. Nat Methods 14(12):1191–1197.  https://doi.org/10.1038/nmeth.4466CrossRefPubMedGoogle Scholar
  84. 84.
    Alemany A, Florescu M, Baron CS, Peterson-Maduro J, van Oudenaarden A (2018) Whole-organism clone tracing using single-cell sequencing. Nature 556(7699):108–112.  https://doi.org/10.1038/nature25969CrossRefPubMedGoogle Scholar
  85. 85.
    Kalhor R, Kalhor K, Mejia L, Leeper K, Graveline A, Mali P, Church GM (2018) Developmental barcoding of whole mouse via homing CRISPR. Science 361(6405):eaat9804.  https://doi.org/10.1126/science.aat9804CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Guernet A, Mungamuri SK, Cartier D, Sachidanandam R, Jayaprakash A, Adriouch S, Vezain M, Charbonnier F, Rohkin G, Coutant S, Yao S, Ainani H, Alexandre D, Tournier I, Boyer O, Aaronson SA, Anouar Y, Grumolato L (2016) CRISPR-barcoding for intratumor genetic heterogeneity modeling and functional analysis of oncogenic driver mutations. Mol Cell 63(3):526–538.  https://doi.org/10.1016/j.molcel.2016.06.017CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Kampmann M (2017) Elucidating drug targets and mechanisms of action by genetic screens in mammalian cells. Chem Commun (Camb) 53(53):7162–7167.  https://doi.org/10.1039/c7cc02349aCrossRefGoogle Scholar
  88. 88.
    Shi J, Wang E, Milazzo JP, Wang Z, Kinney JB, Vakoc CR (2015) Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat Biotechnol 33(6):661–667.  https://doi.org/10.1038/nbt.3235CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Hess GT, Fresard L, Han K, Lee CH, Li A, Cimprich KA, Montgomery SB, Bassik MC (2016) Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat Methods 13(12):1036–1042.  https://doi.org/10.1038/nmeth.4038CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Ma Y, Zhang J, Yin W, Zhang Z, Song Y, Chang X (2016) Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat Methods 13(12):1029–1035.  https://doi.org/10.1038/nmeth.4027CrossRefPubMedGoogle Scholar
  91. 91.
    Jost M, Chen Y, Gilbert LA, Horlbeck MA, Krenning L, Menchon G, Rai A, Cho MY, Stern JJ, Prota AE, Kampmann M, Akhmanova A, Steinmetz MO, Tanenbaum ME, Weissman JS (2017) Combined CRISPRi/a-based chemical genetic screens reveal that Rigosertib is a microtubule-destabilizing agent. Mol Cell 68(1):210–223 e216.  https://doi.org/10.1016/j.molcel.2017.09.012CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Zimmermann M, Murina O, Reijns MAM, Agathanggelou A, Challis R, Tarnauskaite Z, Muir M, Fluteau A, Aregger M, McEwan A, Yuan W, Clarke M, Lambros MB, Paneesha S, Moss P, Chandrashekhar M, Angers S, Moffat J, Brunton VG, Hart T, de Bono J, Stankovic T, Jackson AP, Durocher D (2018) CRISPR screens identify genomic ribonucleotides as a source of PARP-trapping lesions. Nature 559(7713):285–289.  https://doi.org/10.1038/s41586-018-0291-zCrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Castro NP, Fedorova-Abrams ND, Merchant AS, Rangel MC, Nagaoka T, Karasawa H, Klauzinska M, Hewitt SM, Biswas K, Sharan SK, Salomon DS (2015) Cripto-1 as a novel therapeutic target for triple negative breast cancer. Oncotarget 6(14):11910–11929.  https://doi.org/10.18632/oncotarget.4182CrossRefPubMedGoogle Scholar
  94. 94.
    Pan D, Kobayashi A, Jiang P, Ferrari de Andrade L, Tay RE, Luoma AM, Tsoucas D, Qiu X, Lim K, Rao P, Long HW, Yuan GC, Doench J, Brown M, Liu XS, Wucherpfennig KW (2018) A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science 359(6377):770–775.  https://doi.org/10.1126/science.aao1710CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Manguso RT, Pope HW, Zimmer MD, Brown FD, Yates KB, Miller BC, Collins NB, Bi K, LaFleur MW, Juneja VR, Weiss SA, Lo J, Fisher DE, Miao D, Van Allen E, Root DE, Sharpe AH, Doench JG, Haining WN (2017) In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target. Nature 547(7664):413–418.  https://doi.org/10.1038/nature23270CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Ribeiro JR, Schorl C, Yano N, Romano N, Kim KK, Singh RK, Moore RG (2016) HE4 promotes collateral resistance to cisplatin and paclitaxel in ovarian cancer cells. J Ovarian Res 9(1):28.  https://doi.org/10.1186/s13048-016-0240-0CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    van Diemen FR, Lebbink RJ (2017) CRISPR/Cas9, a powerful tool to target human herpesviruses. Cell Microbiol 19(2).  https://doi.org/10.1111/cmi.12694CrossRefGoogle Scholar
  98. 98.
    Wang J, Quake SR (2014) RNA-guided endonuclease provides a therapeutic strategy to cure latent herpesviridae infection. Proc Natl Acad Sci U S A 111(36):13157–13162.  https://doi.org/10.1073/pnas.1410785111CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Kennedy EM, Kornepati AV, Goldstein M, Bogerd HP, Poling BC, Whisnant AW, Kastan MB, Cullen BR (2014) Inactivation of the human papillomavirus E6 or E7 gene in cervical carcinoma cells by using a bacterial CRISPR/Cas RNA-guided endonuclease. J Virol 88(20):11965–11972.  https://doi.org/10.1128/JVI.01879-14CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Kennedy EM, Bassit LC, Mueller H, Kornepati AVR, Bogerd HP, Nie T, Chatterjee P, Javanbakht H, Schinazi RF, Cullen BR (2015) Suppression of hepatitis B virus DNA accumulation in chronically infected cells using a bacterial CRISPR/Cas RNA-guided DNA endonuclease. Virology 476:196–205.  https://doi.org/10.1016/j.virol.2014.12.001CrossRefPubMedGoogle Scholar
  101. 101.
    Zhen S, Hua L, Liu YH, Gao LC, Fu J, Wan DY, Dong LH, Song HF, Gao X (2015) Harnessing the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated Cas9 system to disrupt the hepatitis B virus. Gene Ther 22(5):404–412.  https://doi.org/10.1038/gt.2015.2CrossRefPubMedGoogle Scholar
  102. 102.
    Sakuma T, Masaki K, Abe-Chayama H, Mochida K, Yamamoto T, Chayama K (2016) Highly multiplexed CRISPR-Cas9-nuclease and Cas9-nickase vectors for inactivation of hepatitis B virus. Genes Cells 21(11):1253–1262.  https://doi.org/10.1111/gtc.12437CrossRefPubMedGoogle Scholar
  103. 103.
    Eyquem J, Mansilla-Soto J, Giavridis T, van der Stegen SJ, Hamieh M, Cunanan KM, Odak A, Gonen M, Sadelain M (2017) Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection. Nature 543(7643):113–117.  https://doi.org/10.1038/nature21405CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Ren J, Liu X, Fang C, Jiang S, June CH, Zhao Y (2017) Multiplex genome editing to generate universal CAR T cells resistant to PD1 inhibition. Clin Cancer Res 23(9):2255–2266.  https://doi.org/10.1158/1078-0432.CCR-16-1300CrossRefPubMedGoogle Scholar
  105. 105.
    Ren J, Zhang X, Liu X, Fang C, Jiang S, June CH, Zhao Y (2017) A versatile system for rapid multiplex genome-edited CAR T cell generation. Oncotarget 8(10):17002–17011.  https://doi.org/10.18632/oncotarget.15218CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Rupp LJ, Schumann K, Roybal KT, Gate RE, Ye CJ, Lim WA, Marson A (2017) CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells. Sci Rep 7(1):737.  https://doi.org/10.1038/s41598-017-00462-8CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Guo X, Jiang H, Shi B, Zhou M, Zhang H, Shi Z, Du G, Luo H, Wu X, Wang Y, Sun R, Li Z (2018) Disruption of PD-1 enhanced the anti-tumor activity of chimeric antigen receptor T cells against hepatocellular carcinoma. Front Pharmacol 9:1118.  https://doi.org/10.3389/fphar.2018.01118CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Zhang Y, Zhang X, Cheng C, Mu W, Liu X, Li N, Wei X, Liu X, Xia C, Wang H (2017) CRISPR-Cas9 mediated LAG-3 disruption in CAR-T cells. Front Med 11(4):554–562.  https://doi.org/10.1007/s11684-017-0543-6CrossRefPubMedGoogle Scholar
  109. 109.
    Jung IY, Kim YY, Yu HS, Lee M, Kim S, Lee J (2018) CRISPR/Cas9-mediated knockout of DGK improves antitumor activities of human T cells. Cancer Res 78(16):4692–4703.  https://doi.org/10.1158/0008-5472.CAN-18-0030CrossRefPubMedGoogle Scholar
  110. 110.
    Kipniss NH, Dingal P, Abbott TR, Gao Y, Wang H, Dominguez AA, Labanieh L, Qi LS (2017) Engineering cell sensing and responses using a GPCR-coupled CRISPR-Cas system. Nat Commun 8(1):2212.  https://doi.org/10.1038/s41467-017-02075-1CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Sterner RM, Sakemura R, Cox MJ, Yang N, Khadka RH, Forsman CL, Hansen MJ, Jin F, Ayasoufi K, Hefazi M, Schick KJ, Walters DK, Ahmed O, Chappell D, Sahmoud T, Durrant C, Nevala WK, Patnaik MM, Pease L, Hedin KE, Kay NE, Johnson AJ, Kenderian SS (2018) GM-CSF inhibition reduces cytokine release syndrome and neuroinflammation but enhances CAR-T cell function in xenografts. Blood 133:697.  https://doi.org/10.1182/blood-2018-10-881722CrossRefPubMedGoogle Scholar
  112. 112.
    Kim MY, Yu KR, Kenderian SS, Ruella M, Chen S, Shin TH, Aljanahi AA, Schreeder D, Klichinsky M, Shestova O, Kozlowski MS, Cummins KD, Shan X, Shestov M, Bagg A, Morrissette JJD, Sekhri P, Lazzarotto CR, Calvo KR, Kuhns DB, Donahue RE, Behbehani GK, Tsai SQ, Dunbar CE, Gill S (2018) Genetic inactivation of CD33 in hematopoietic stem cells to enable CAR T cell immunotherapy for acute myeloid leukemia. Cell 173(6):1439–1453 e1419.  https://doi.org/10.1016/j.cell.2018.05.013CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Minagawa A, Yoshikawa T, Yasukawa M, Hotta A, Kunitomo M, Iriguchi S, Takiguchi M, Kassai Y, Imai E, Yasui Y, Kawai Y, Zhang R, Uemura Y, Miyoshi H, Nakanishi M, Watanabe A, Hayashi A, Kawana K, Fujii T, Nakatsura T, Kaneko S (2018) Enhancing T cell receptor stability in rejuvenated iPSC-derived T cells improves their use in Cancer immunotherapy. Cell Stem Cell 23:850.  https://doi.org/10.1016/j.stem.2018.10.005CrossRefPubMedGoogle Scholar
  114. 114.
    Hu JH, Miller SM, Geurts MH, Tang W, Chen L, Sun N, Zeina CM, Gao X, Rees HA, Lin Z, Liu DR (2018) Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 556(7699):57–63.  https://doi.org/10.1038/nature26155CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Vakulskas CA, Dever DP, Rettig GR, Turk R, Jacobi AM, Collingwood MA, Bode NM, McNeill MS, Yan S, Camarena J, Lee CM, Park SH, Wiebking V, Bak RO, Gomez-Ospina N, Pavel-Dinu M, Sun W, Bao G, Porteus MH, Behlke MA (2018) A high-fidelity Cas9 mutant delivered as a ribonucleoprotein complex enables efficient gene editing in human hematopoietic stem and progenitor cells. Nat Med 24(8):1216–1224.  https://doi.org/10.1038/s41591-018-0137-0CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Jiang J, Zhang L, Zhou X, Chen X, Huang G, Li F, Wang R, Wu N, Yan Y, Tong C, Srivastava S, Wang Y, Liu H, Ying QL (2016) Induction of site-specific chromosomal translocations in embryonic stem cells by CRISPR/Cas9. Sci Rep 6:21918.  https://doi.org/10.1038/srep21918CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Refuge Biotechnologies Inc.Menlo ParkUSA

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