The David H. Koch Institute for Integrative Cancer Research at MITThe David H. Koch Institute for Integrative Cancer Research at MIT

Massachusetts Institute of Technology

National Cancer Institute Cancer Center

Science + Engineering... Conquering Cancer Together

Progress: January 2019

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1. DNA intercalation facilitates efficient DNA-targeted covalent binding of phenanthriplatin. Almaqwashi AA, Zhou W, Naufer MN, Riddell IA, Yilmaz OH, Lippard SJ, Williams MC. J Am Chem Soc. pubmed:30599508;  doi:10.1021/jacs.8b10252

2. Small and Large Ribosomal Subunit Deficiencies Lead to Distinct Gene Expression Signatures that Reflect Cellular Growth Rate. Cheng Z, Mugler CF, Keskin A, Hodapp S, Chan LY, Weis K, Mertins P, Regev A, Jovanovic M, Brar GA. Mol Cell. pubmed:30503772;  doi:10.1016/j.molcel.2018.10.032

3. WNT/beta-catenin pathway activation correlates with immune exclusion across human cancers. Luke JJ, Bao R, Sweis RF, Spranger S, Gajewski TF. Clin Cancer Res. pubmed:30635339;  doi:10.1158/1078-0432.CCR-18-1942

4. WNT Signaling in Cancer Immunosurveillance. Galluzzi L, Spranger S, Fuchs E, Lopez-Soto A. Trends Cell Biol. pubmed:30220580;  doi:10.1016/j.tcb.2018.08.005

5. Phenotypic Plasticity: Driver of Cancer Initiation, Progression, and Therapy Resistance. Gupta PB, Pastushenko I, Skibinski A, Blanpain C, Kuperwasser C. Cell Stem Cell. pubmed:30554963;  doi:10.1016/j.stem.2018.11.011

6. Genome-Wide CRISPR/Cas9 Screening for Identification of Cancer Genes in Cell Lines. Adelmann CH, Wang T, Sabatini DM, Lander ES. Methods Mol Biol. pubmed:30542996;  doi:10.1007/978-1-4939-8967-6_10

7. MITO-Tag Mice enable rapid isolation and multimodal profiling of mitochondria from specific cell types in vivo. Bayraktar EC, Baudrier L, Ozerdem C, Lewis CA, Chan SH, Kunchok T, Abu-Remaileh M, Cangelosi AL, Sabatini DM, Birsoy K, Chen WW. Proc Natl Acad Sci U S A. pubmed:30541894;  doi:10.1073/pnas.1816656115

8. Deptor modulates activation responses in CD4(+) T cells and enhances immunoregulation following transplantation. Wedel J, Bruneau S, Liu K, Kong SW, Sage PT, Sabatini DM, Laplante M, Briscoe DM. Am J Transplant. pubmed:29969188;  doi:10.1111/ajt.14995

9. Tranexamic acid mediates proinflammatory and anti-inflammatory signaling via complement C5a regulation in a plasminogen activator-dependent manner. Barrett CD, Moore HB, Kong YW, Chapman MP, Sriram G, Lim D, Moore EE, Yaffe MB. J Trauma Acute Care Surg. pubmed:30575685;  doi:10.1097/TA.0000000000002092

10. The Mitotic Exit Network integrates temporal and spatial signals by distributing regulation across multiple components. Campbell IW, Zhou X, Amon A. Elife. pubmed:30672733;  doi:10.7554/eLife.41139

11. Efficacy and tolerability of EH301 for amyotrophic lateral sclerosis: a randomized, double-blind, placebo-controlled human pilot study. de la Rubia JE, Drehmer E, Platero JL, Benlloch M, Caplliure-Llopis J, Villaron-Casales C, de Bernardo N, AlarcOn J, Fuente C, Carrera S, Sancho D, GarcIa-Pardo P, Pascual R, JuArez M, Cuerda-Ballester M, Forner A, Sancho-Castillo S, Barrios C, Obrador E, Marchio P, Salvador R, Holmes HE, Dellinger RW, Guarente L, Estrela JM. Amyotroph Lateral Scler Frontotemporal Degener. pubmed:30668199;  doi:10.1080/21678421.2018.1536152

12. Optofluidic real-time cell sorter for longitudinal CTC studies in mouse models of cancer. Hamza B, Ng SR, Prakadan SM, Delgado FF, Chin CR, King EM, Yang LF, Davidson SM, DeGouveia KL, Cermak N, Navia AW, Winter PS, Drake RS, Tammela T, Li CM, Papagiannakopoulos T, Gupta AJ, Shaw Bagnall J, Knudsen SM, Vander Heiden MG, Wasserman SC, Jacks T, Shalek AK, Manalis SR. Proc Natl Acad Sci U S A. pubmed:30674677;  doi:10.1073/pnas.1814102116

13. Why geneticists stole cancer research even though cancer is primarily a signaling disease. Yaffe MB. Sci Signal. pubmed:30670634;  doi:10.1126/scisignal.aaw3483

14. TAZ couples Hippo/Wnt signalling and insulin sensitivity through Irs1 expression. Hwang JH, Kim AR, Kim KM, Il Park J, Oh HT, Moon SA, Byun MR, Jeong H, Kim HK, Yaffe MB, Hwang ES, Hong JH. Nat Commun. pubmed:30679431;  doi:10.1038/s41467-019-08287-x

15. Structural basis for species-selective targeting of Hsp90 in a pathogenic fungus. Whitesell L, Robbins N, Huang DS, McLellan CA, Shekhar-Guturja T, LeBlanc EV, Nation CS, Hui R, Hutchinson A, Collins C, Chatterjee S, Trilles R, Xie JL, Krysan DJ, Lindquist S, Porco JAJr, Tatu U, Brown LE, Pizarro J, Cowen LE. Nat Commun. pubmed:30679438;  doi:10.1038/s41467-018-08248-w

16. A quantitative framework for characterizing the evolutionary history of mammalian gene expression. Chen J, Swofford R, Johnson J, Cummings BB, Rogel N, Lindblad-Toh K, Haerty W, di Palma F, Regev A. Genome Res. pubmed:30552105;  doi:10.1101/gr.237636.118

17. Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Keskin DB, Anandappa AJ, Sun J, Tirosh I, Mathewson ND, Li S, Oliveira G, Giobbie-Hurder A, Felt K, Gjini E, Shukla SA, Hu Z, Li L, Le PM, Allesoe RL, Richman AR, Kowalczyk MS, Abdelrahman S, Geduldig JE, Charbonneau S, Pelton K, Iorgulescu JB, Elagina L, Zhang W, Olive O, McCluskey C, Olsen LR, Stevens J, Lane WJ, Salazar AM, Daley H, Wen PY, Chiocca EA, Harden M, Lennon NJ, Gabriel S, Getz G, Lander ES, Regev A, Ritz J, Neuberg D, Rodig SJ, Ligon KL, Suva ML, Wucherpfennig KW, Hacohen N, Fritsch EF, Livak KJ, Ott PA, Wu CJ, Reardon DA. Nature. pubmed:30568305;  doi:10.1038/s41586-018-0792-9

18. Checkpoint Blockade Immunotherapy Induces Dynamic Changes in PD-1(-)CD8(+) Tumor-Infiltrating T Cells. Kurtulus S, Madi A, Escobar G, Klapholz M, Nyman J, Christian E, Pawlak M, Dionne D, Xia J, Rozenblatt-Rosen O, Kuchroo VK, Regev A, Anderson AC. Immunity. pubmed:30635236;  doi:10.1016/j.immuni.2018.11.014

19. Loss of function of NF1 is a mechanism of acquired resistance to endocrine therapy in lobular breast cancer. Sokol ES, Feng YX, Jin DX, Basudan A, Lee AV, Atkinson JM, Chen J, Stephens PJ, Frampton GM, Gupta PB, Ross JS, Chung JH, Oesterreich S, Ali SM, Hartmaier RJ. Ann Oncol. pubmed:30423024;  doi:10.1093/annonc/mdy497

20. Commensal Microbiota Promote Lung Cancer Development via gammadelta T Cells. Jin C, Lagoudas GK, Zhao C, Bullman S, Bhutkar A, Hu B, Ameh S, Sandel D, Liang XS, Mazzilli S, Whary MT, Meyerson M, Germain R, Blainey PC, Fox JG, Jacks T. Cell. pubmed:30712876;  doi:10.1016/j.cell.2018.12.040

21. Molecular Classification and Comparative Taxonomics of Foveal and Peripheral Cells in Primate Retina. Peng YR, Shekhar K, Yan W, Herrmann D, Sappington A, Bryman GS, van Zyl T, Do MTH, Regev A, Sanes JR. Cell. pubmed:30712875;  doi:10.1016/j.cell.2019.01.004

22. Excessive Cell Growth Causes Cytoplasm Dilution And Contributes to Senescence. Neurohr GE, Terry RL, Lengefeld J, Bonney M, Brittingham GP, Moretto F, Miettinen TP, Vaites LP, Soares LM, Paulo JA, Harper JW, Buratowski S, Manalis S, van Werven FJ, Holt LJ, Amon A. Cell. pubmed:30739799;  doi:10.1016/j.cell.2019.01.018

23. Initiation-specific alleles of the Cdc45 helicase-activating protein. Rios-Morales RY, Chan SH, Bell SP. PLoS One. pubmed:30913274;  doi:10.1371/journal.pone.0214426

24. Robust gold nanorods stabilized by bidentate N-heterocyclic-carbene-thiolate ligands. MacLeod MJ, Goodman AJ, Ye HZ, Nguyen HV, Van Voorhis T, Johnson JA. Nat Chem. pubmed:30420777;  doi:10.1038/s41557-018-0159-8

25. A chemoselective strategy for late-stage functionalization of complex small molecules with polypeptides and proteins. Cohen DT, Zhang C, Fadzen CM, Mijalis AJ, Hie L, Johnson KD, Shriver Z, Plante O, Miller SJ, Buchwald SL, Pentelute BL. Nat Chem. pubmed:30397320;  doi:10.1038/s41557-018-0154-0

26. Comparison of Integrases Identifies Bxb1-GA Mutant as the Most Efficient Site-Specific Integrase System in Mammalian Cells. Jusiak B, Jagtap K, Gaidukov L, Duportet X, Bandara K, Chu J, Zhang L, Weiss R, Lu TK. ACS Synth Biol. pubmed:30609349;  doi:10.1021/acssynbio.8b00089

27. Position Paper Computational Cardiology. Athanasiou L, Nezami FR, Edelman ER. IEEE J Biomed Health Inform. pubmed:30346296;  doi:10.1109/JBHI.2018.2877044

28. Uremic Toxin Indoxyl Sulfate Promotes Proinflammatory Macrophage Activation Via the Interplay of OATP2B1 and Dll4-Notch Signaling. Nakano T, Katsuki S, Chen M, Decano JL, Halu A, Lee LH, Pestana DVS, Kum AST, Kuromoto RK, Golden WS, Boff MS, Guimaraes GC, Higashi H, Kauffman KJ, Maejima T, Suzuki T, Iwata H, Barabasi AL, Aster JC, Anderson DG, Sharma A, Singh SA, Aikawa E, Aikawa M. Circulation. pubmed:30586693;  doi:10.1161/CIRCULATIONAHA.118.034588

29. Publisher Correction: Encryption and steganography of synthetic gene circuits. Purcell O, Wang J, Siuti P, Lu TK. Nat Commun. pubmed:30622250;  doi:10.1038/s41467-018-07844-0

30. Peptide Design Principles for Antimicrobial Applications. Torres MDT, Sothiselvam S, Lu TK, de la Fuente-Nunez C. J Mol Biol. pubmed:30611750;  doi:10.1016/j.jmb.2018.12.015

31. Programmable and printable Bacillus subtilis biofilms as engineered living materials. Huang J, Liu S, Zhang C, Wang X, Pu J, Ba F, Xue S, Ye H, Zhao T, Li K, Wang Y, Zhang J, Wang L, Fan C, Lu TK, Zhong C. Nat Chem Biol. pubmed:30510190;  doi:10.1038/s41589-018-0169-2

32. Photopolymerized Micelle-Laden Hydrogels Can Simultaneously Form and Encapsulate Nanocrystals to Improve Drug Substance Solubility and Expedite Drug Product Design. Godfrin PD, Lee H, Lee JH, Doyle PS. Small. pubmed:30645039;  doi:10.1002/smll.201803372

33. Calcium-Mediated Protein Folding and Stabilisation of Salmonella Biofilm-Associated Protein a. Guttula D, Yao M, Baker K, Liang Y, Goult BT, Doyle PS, Yan J. J Mol Biol. pubmed:30452884;  doi:10.1016/j.jmb.2018.11.014

34. Amphiphilic nanoparticle delivery enhances the anticancer efficacy of a TLR7 ligand via local immune activation. Mottas I, Bekdemir A, Cereghetti A, Spagnuolo L, Yang YS, Muller M, Irvine DJ, Stellacci F, Bourquin C. Biomaterials. pubmed:30415018;  doi:10.1016/j.biomaterials.2018.10.031

35. Targeting individual cells by barcode in pooled sequence libraries. Ranu N, Villani AC, Hacohen N, Blainey PC. Nucleic Acids Res. pubmed:30256981;  doi:10.1093/nar/gky856

36. Multidimensional screening yields channelrhodopsin variants having improved photocurrent and order-of-magnitude reductions in calcium and proton currents. Cho YK, Park D, Yang A, Chen F, Chuong AS, Klapoetke NC, Boyden ES. J Biol Chem. pubmed:30610117;  doi:10.1074/jbc.RA118.006996

37. What, Why, Where, and When: Bringing Timing to Immuno-Oncology. Rothschilds AM, Wittrup KD. Trends Immunol. pubmed:30545676;  doi:10.1016/j.it.2018.11.003

38. Computational translation of genomic responses from experimental model systems to humans. Brubaker DK, Proctor EA, Haigis KM, Lauffenburger DA. PLoS Comput Biol. pubmed:30629591;  doi:10.1371/journal.pcbi.1006286

39. Melanopsin for precise optogenetic activation of astrocyte-neuron networks. Mederos S, Hernandez-Vivanco A, Ramirez-Franco J, Martin-Fernandez M, Navarrete M, Yang A, Boyden ES, Perea G. Glia. pubmed:30632636;  doi:10.1002/glia.23580

40. Expansion microscopy: principles and uses in biological research. Wassie AT, Zhao Y, Boyden ES. Nat Methods. pubmed:30573813;  doi:10.1038/s41592-018-0219-4

41. Imaging cellular ultrastructures using expansion microscopy (U-ExM). Gambarotto D, Zwettler FU, Le Guennec M, Schmidt-Cernohorska M, Fortun D, Borgers S, Heine J, Schloetel JG, Reuss M, Unser M, Boyden ES, Sauer M, Hamel V, Guichard P. Nat Methods. pubmed:30559430;  doi:10.1038/s41592-018-0238-1

42. Delivery technologies for cancer immunotherapy. Riley RS, June CH, Langer R, Mitchell MJ. Nat Rev Drug Discov. pubmed:30622344;  doi:10.1038/s41573-018-0006-z

43. Inhaled Nanoformulated mRNA Polyplexes for Protein Production in Lung Epithelium. Patel AK, Kaczmarek JC, Bose S, Kauffman KJ, Mir F, Heartlein MW, DeRosa F, Langer R, Anderson DG. Adv Mater. pubmed:30609147;  doi:10.1002/adma.201805116

44. Estrogen Activation of G protein-coupled Estrogen Receptor 1 Regulates Phosphoinositide 3-kinase and mTOR Signaling to Promote Liver Growth in Zebrafish and Proliferation of Human Hepatocytes. Chaturantabut S, Shwartz A, Evason KJ, Cox AG, Labella K, Schepers AG, Yang S, Aravena M, Houvras Y, Mancio-Silva L, Romano S, Gorelick DA, Cohen DE, Zon LI, Bhatia SN, North TE, Goessling W. Gastroenterology. pubmed:30641053;  doi:10.1053/j.gastro.2019.01.010

45. Intracochlear drug delivery: Fluorescent tracer evaluation for quantification of distribution in the cochlear partition. Ayoob AM, Peppi M, Tandon V, Langer R, Borenstein JT. Eur J Pharm Sci. pubmed:30195649;  doi:10.1016/j.ejps.2018.09.007

46. Mammographic Breast Density Assessment Using Deep Learning: Clinical Implementation. Lehman CD, Yala A, Schuster T, Dontchos B, Bahl M, Swanson K, Barzilay R. Radiology. pubmed:30325282;  doi:10.1148/radiol.2018180694

47. Biohybrid valveless pump-bot powered by engineered skeletal muscle. Li Z, Seo Y, Aydin O, Elhebeary M, Kamm RD, Kong H, Saif MTA. Proc Natl Acad Sci U S A. pubmed:30635415;  doi:10.1073/pnas.1817682116

48. Investigating the feasibility of channelrhodopsin variants for nanoscale optogenetics. Stahlberg MA, Ramakrishnan C, Willig KI, Boyden ES, Deisseroth K, Dean C. Neurophotonics. pubmed:30854405;  doi:10.1117/1.NPh.6.1.015007

49. Cortical column and whole-brain imaging with molecular contrast and nanoscale resolution. Gao R, Asano SM, Upadhyayula S, Pisarev I, Milkie DE, Liu TL, Singh V, Graves A, Huynh GH, Zhao Y, Bogovic J, Colonell J, Ott CM, Zugates C, Tappan S, Rodriguez A, Mosaliganti KR, Sheu SH, Pasolli HA, Pang S, Xu CS, Megason SG, Hess H, Lippincott-Schwartz J, Hantman A, Rubin GM, Kirchhausen T, Saalfeld S, Aso Y, Boyden ES, Betzig E. Science. pubmed:30655415;  doi:10.1126/science.aau8302

50. Multiplexed enrichment and genomic profiling of peripheral blood cells reveal subset-specific immune signatures. Reyes M, Vickers D, Billman K, Eisenhaure T, Hoover P, Browne EP, Rao DA, Hacohen N, Blainey PC. Sci Adv. pubmed:30746468;  doi:10.1126/sciadv.aau9223

51. Systemic analysis of tyrosine kinase signaling reveals a common adaptive response program in a HER2-positive breast cancer. Schwill M, Tamaskovic R, Gajadhar AS, Kast F, White FM, Pluckthun A. Sci Signal. pubmed:30670633;  doi:10.1126/scisignal.aau2875

52. CRISPR-Cas: a tool for cancer research and therapeutics. Yin H, Xue W, Anderson DG. Nat Rev Clin Oncol. pubmed:30664678;  doi:10.1038/s41571-019-0166-8

53. A genetically encoded near-infrared fluorescent calcium ion indicator. Qian Y, Piatkevich KD, Mc Larney B, Abdelfattah AS, Mehta S, Murdock MH, Gottschalk S, Molina RS, Zhang W, Chen Y, Wu J, Drobizhev M, Hughes TE, Zhang J, Schreiter ER, Shoham S, Razansky D, Boyden ES, Campbell RE. Nat Methods. pubmed:30664778;  doi:10.1038/s41592-018-0294-6

54. Alveolar proteins stabilize cortical microtubules in Toxoplasma gondii. Harding CR, Gow M, Kang JH, Shortt E, Manalis SR, Meissner M, Lourido S. Nat Commun. pubmed:30674885;  doi:10.1038/s41467-019-08318-7

55. Atypical ductal hyperplasia in men with gynecomastia: what is their breast cancer risk?. Coopey SB, Kartal K, Li C, Yala A, Barzilay R, Faulkner HR, King TA, Acevedo F, Garber JE, Guidi AJ, Hughes KS. Breast Cancer Res Treat. pubmed:30666539;  doi:10.1007/s10549-018-05117-4

56. Exploration of CTCF post-translation modifications uncovers Serine-224 phosphorylation by PLK1 at pericentric regions during the G2/M transition. Del Rosario BC, Kriz AJ, Del Rosario AM, Anselmo A, Fry CJ, White FM, Sadreyev RI, Lee JT. Elife. pubmed:30676316;  doi:10.7554/eLife.42341

57. Dissecting N-Glycosylation Dynamics in Chinese Hamster Ovary Cells Fed-batch Cultures using Time Course Omics Analyses. Sumit M, Dolatshahi S, Chu AA, Cote K, Scarcelli JJ, Marshall JK, Cornell RJ, Weiss R, Lauffenburger DA, Mulukutla BC, Figueroa BJr. iScience. pubmed:30682623;  doi:10.1016/j.isci.2019.01.006

58. Blocking CXCR4 alleviates desmoplasia, increases T-lymphocyte infiltration, and improves immunotherapy in metastatic breast cancer. Chen IX, Chauhan VP, Posada J, Ng MR, Wu MW, Adstamongkonkul P, Huang P, Lindeman N, Langer R, Jain RK. Proc Natl Acad Sci U S A. pubmed:30700545;  doi:10.1073/pnas.1815515116

59. Redox-responsive interleukin-2 nanogel specifically and safely promotes the proliferation and memory precursor differentiation of tumor-reactive T-cells. Xie YQ, Arik H, Wei L, Zheng Y, Suh H, Irvine DJ, Tang L. Biomater Sci. pubmed:30698174;  doi:10.1039/c8bm01556b

60. A graph-convolutional neural network model for the prediction of chemical reactivity. Coley CW, Jin W, Rogers L, Jamison TF, Jaakkola TS, Green WH, Barzilay R, Jensen KF. Chem Sci. pubmed:30746086;  doi:10.1039/c8sc04228d

61. Making the case: developing innovative adherence solutions for the treatment of tuberculosis. Verma M, Furin J, Langer R, Traverso G. BMJ Glob Health. pubmed:30815283;  doi:10.1136/bmjgh-2018-001323

62. Quantification of human neuromuscular function through optogenetics. Vila OF, Uzel SGM, Ma SP, Williams D, Pak J, Kamm RD, Vunjak-Novakovic G. Theranostics. pubmed:30867827;  doi:10.7150/thno.25735

63. A theoretical analysis of single molecule protein sequencing via weak binding spectra. Rodriques SG, Marblestone AH, Boyden ES. PLoS One. pubmed:30921350;  doi:10.1371/journal.pone.0212868

64. Leveraging device-arterial coupling to determine cardiac and vascular state. Chang BY, Keller SP, Edelman ER. IEEE Trans Biomed Eng. pubmed:30703007;  doi:10.1109/TBME.2019.2895752