5
Highlights of This Issue 5997 SPECIAL FEATURES CCR Translations 5999 On OX40 and PD-1 Combination: Why Should OX40 Be First in Sequence? Mario P. Colombo See related article, p. 6165 Reviews 6002 Clinical Development of PD-1/PD-L1 Immunotherapy for Gastrointestinal Cancers: Facts and Hopes Ian Chau 6012 T-cell Receptors for Clinical Therapy: In Vitro Assessment of Toxicity Risk Andre Kunert, Matthias Obenaus, Cor H.J. Lamers, Thomas Blankenstein, and Reno Debets CANCER THERAPY: CLINICAL 6021 The c.1085A>G Genetic Variant of CSF1R Gene Regulates Tumor Immunity by Altering the Proliferation, Polarization, and Function of Macrophages Yu-Min Yeh, Shan-Ju Hsu, Peng-Chan Lin, Keng-Fu Hsu, Pei-Ying Wu, Wu-Chou Su, Jang-Yang Chang, and Meng-Ru Shen 6031 Increased IFNg þ T Cells Are Responsible for the Clinical Responses of Low-Dose DNA- Demethylating Agent Decitabine Antitumor Therapy Xiang Li, Yan Zhang, Meixia Chen, Qian Mei, Yang Liu, Kaichao Feng, Hejin Jia, Liang Dong, Lu Shi, Lin Liu, Jing Nie, and Weidong Han 6044 Radiosensitization of Adenoid Cystic Carcinoma with MDM2 Inhibition Prashanth J. Prabakaran, Amal M. Javaid, Adam D. Swick, Lauryn R. Werner, Kwangok P. Nickel, Emmanuel Sampene, Rong Hu, Irene M. Ong, Justine Y. Bruce, Gregory K. Hartig, Aaron M. Wieland, Jude Canon, Paul M. Harari, and Randall J. Kimple 6054 PD-L1 Expression and Immune Escape in Melanoma Resistance to MAPK Inhibitors Hojabr Kakavand, Robert V. Rawson, Gulietta M. Pupo, Jean Y. H. Yang, Alexander M. Menzies, Matteo S. Carlino, Richard F. Kefford, Julie R. Howle, Robyn P.M. Saw, John F. Thompson, James S. Wilmott, Georgina V. Long, Richard A. Scolyer, and Helen Rizos 6062 Pediatric Phase I Trial and Pharmacokinetic Study of Trebananib in Relapsed Solid Tumors, Including Primary Tumors of the Central Nervous System ADVL1115: A Children's Oncology Group Phase I Consortium Report Sarah E.S. Leary, Julie R. Park, Joel M. Reid, Andrew T. Ralya, Sylvain Baruchel, Bing Wu, Timothy P.L. Roberts, Xiaowei Liu, Charles G. Minard, Elizabeth Fox, Brenda Weigel, and Susan Blaney 6070 Gene Copy Number Estimation from Targeted Next-Generation Sequencing of Prostate Cancer Biopsies: Analytic Validation and Clinical Qualification George Seed, Wei Yuan, Joaquin Mateo, Suzanne Carreira, Claudia Bertan, Maryou Lambros, Gunther Boysen, Roberta Ferraldeschi, Susana Miranda, Ines Figueiredo, Ruth Riisnaes, Mateus Crespo, Daniel Nava Rodrigues, Eric Talevich, Dan R. Robinson, Lakshmi P. Kunju, Yi-Mi Wu, Robert Lonigro, Shahneen Sandhu, Arul M. Chinnaiyan, and Johann S. de Bono 6078 T2FLAIR Mismatch, an Imaging Biomarker for IDH and 1p/19q Status in Lower-grade Gliomas: A TCGA/TCIA Project Sohil H. Patel, Laila M. Poisson, Daniel J. Brat, Yueren Zhou, Lee Cooper, Matija Snuderl, Cheddhi Thomas, Ana M. Franceschi, Brent Griffith, Adam E. Flanders, John G. Golfinos, Andrew S. Chi, and Rajan Jain PERSONALIZED MEDICINE AND IMAGING 6086 Detection of Activating Estrogen Receptor Gene (ESR1) Mutations in Single Circulating Tumor Cells Carmela Paolillo, Zhaomei Mu, Giovanna Rossi, Matthew J. Schiewer, Thomas Nguyen, Laura Austin, Ettore Capoluongo, Karen Knudsen, Massimo Cristofanilli, and Paolo Fortina October 15, 2017 Volume 23 Number 20 Clinical Cancer Research Table of Contents iv on August 30, 2021. © 2017 American Association for Cancer Research. clincancerres.aacrjournals.org Downloaded from

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Page 1: Clinical Cancer Research Table of ContentsCatherine Gratas, Fanny Geraldo, Ulrich Jarry, Emmanuel Scotet, Marion Rabe, Marie-Clotilde Alves-Guerra, Raluca Teusan, Fabien Gautier, Delphine

Highlights of This Issue 5997

SPECIAL FEATURES

CCR Translations

5999 On OX40 and PD-1 Combination: Why ShouldOX40 Be First in Sequence?Mario P. ColomboSee related article, p. 6165

Reviews

6002 Clinical Development of PD-1/PD-L1Immunotherapy for Gastrointestinal Cancers:Facts and HopesIan Chau

6012 T-cell Receptors for Clinical Therapy: In VitroAssessment of Toxicity RiskAndre Kunert, Matthias Obenaus, Cor H.J. Lamers,Thomas Blankenstein, and Reno Debets

CANCER THERAPY: CLINICAL

6021 The c.1085A>G Genetic Variant of CSF1R GeneRegulates Tumor Immunity by Altering theProliferation, Polarization, and Function ofMacrophagesYu-Min Yeh, Shan-Ju Hsu, Peng-Chan Lin, Keng-Fu Hsu,Pei-Ying Wu, Wu-Chou Su, Jang-Yang Chang, andMeng-Ru Shen

6031 Increased IFNgþ T Cells Are Responsible forthe Clinical Responses of Low-Dose DNA-Demethylating Agent Decitabine AntitumorTherapyXiang Li, Yan Zhang, Meixia Chen, Qian Mei, Yang Liu,Kaichao Feng, Hejin Jia, Liang Dong, Lu Shi, Lin Liu,Jing Nie, and Weidong Han

6044 Radiosensitization of Adenoid Cystic Carcinomawith MDM2 InhibitionPrashanth J. Prabakaran, Amal M. Javaid, Adam D. Swick,Lauryn R. Werner, Kwangok P. Nickel,Emmanuel Sampene, Rong Hu, Irene M. Ong,Justine Y. Bruce, Gregory K. Hartig, Aaron M. Wieland,Jude Canon, Paul M. Harari, and Randall J. Kimple

6054 PD-L1 Expression and Immune Escape inMelanoma Resistance to MAPK InhibitorsHojabr Kakavand, Robert V. Rawson, Gulietta M. Pupo,Jean Y. H. Yang, Alexander M. Menzies, Matteo S. Carlino,Richard F. Kefford, Julie R. Howle, Robyn P.M. Saw,John F. Thompson, James S. Wilmott, Georgina V. Long,Richard A. Scolyer, and Helen Rizos

6062 Pediatric Phase I Trial and PharmacokineticStudy of Trebananib in Relapsed Solid Tumors,Including Primary Tumors of the CentralNervous System ADVL1115: A Children'sOncology Group Phase I Consortium ReportSarah E.S. Leary, Julie R. Park, Joel M. Reid,Andrew T. Ralya, Sylvain Baruchel, Bing Wu,Timothy P.L. Roberts, Xiaowei Liu, Charles G. Minard,Elizabeth Fox, Brenda Weigel, and Susan Blaney

6070 Gene Copy Number Estimation from TargetedNext-Generation Sequencing of Prostate CancerBiopsies: Analytic Validation and ClinicalQualificationGeorge Seed, Wei Yuan, Joaquin Mateo, Suzanne Carreira,Claudia Bertan, Maryou Lambros, Gunther Boysen,Roberta Ferraldeschi, Susana Miranda, Ines Figueiredo,Ruth Riisnaes, Mateus Crespo, Daniel Nava Rodrigues,Eric Talevich, Dan R. Robinson, Lakshmi P. Kunju,Yi-Mi Wu, Robert Lonigro, Shahneen Sandhu,Arul M. Chinnaiyan, and Johann S. de Bono

6078 T2–FLAIR Mismatch, an Imaging Biomarker forIDH and 1p/19q Status in Lower-gradeGliomas: A TCGA/TCIA ProjectSohil H. Patel, Laila M. Poisson, Daniel J. Brat,Yueren Zhou, Lee Cooper, Matija Snuderl,Cheddhi Thomas, Ana M. Franceschi, Brent Griffith,Adam E. Flanders, John G. Golfinos, Andrew S. Chi, andRajan Jain

PERSONALIZED MEDICINE AND IMAGING

6086 Detection of Activating Estrogen ReceptorGene (ESR1) Mutations in Single CirculatingTumor CellsCarmela Paolillo, Zhaomei Mu, Giovanna Rossi,Matthew J. Schiewer, Thomas Nguyen, Laura Austin,Ettore Capoluongo, Karen Knudsen,Massimo Cristofanilli,and Paolo Fortina

October 15, 2017 � Volume 23 � Number 20

Clinical Cancer Research

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6094 Real-Time Genomic Profiling of Pancreatic DuctalAdenocarcinoma: Potential Actionability andCorrelation with Clinical PhenotypeMaeve A. Lowery, Emmet J. Jordan, Olca Basturk,Ryan N. Ptashkin, Ahmet Zehir, Michael F. Berger,Tanisha Leach, Brian Herbst, Gokce Askan,Hannah Maynard, Danielle Glassman,Christina Covington, Nikolaus Schultz,Ghassan K. Abou-Alfa, James J. Harding, David S. Klimstra,Jaclyn F. Hechtman, David M. Hyman, Peter J. Allen,William R. Jarnagin, Vinod P. Balachandran,Anna M. Varghese, Mark A. Schattner, Kenneth H. Yu,Leonard B. Saltz, David B. Solit,Christine A. Iacobuzio-Donahue, Steven D. Leach, andEileen M. O'Reilly

6101 Molecular Screening for Cancer TreatmentOptimization (MOSCATO-01) in PediatricPatients: A Single-Institutional ProspectiveMolecular Stratification TrialAnne C. Harttrampf, Ludovic Lacroix, Marc Deloger,Frederic Deschamps, Stephanie Puget, Nathalie Auger,Philippe Vielh, Pascale Varlet, Zsofia Balogh,Samuel Abbou, Adrien Allorant,Dominique Valteau-Couanet, Sabine Sarnacki,Louise Gamiche-Rolland, Guillaume Meurice,Veronique Minard-Colin, Jacques Grill,Laurence Brugieres, Christelle Dufour, Nathalie Gaspar,Stefan Michiels, Gilles Vassal, Jean-Charles Soria, andBirgit Geoerger

6113 Germline Mutations in Cancer SusceptibilityGenes in a Large Series of Unselected BreastCancer PatientsJie Sun, Hua Meng, Lu Yao, Meng Lv, Jian Bai,Jianguang Zhang, Lientu Wang, Tao Ouyang, Jinfeng Li,Tianfeng Wang, Zhaoqing Fan, Tie Fan, Benyao Lin, andYuntao Xie

6120 MAPK Pathway and TERT Promoter GeneMutation Pattern and Its Prognostic Value inMelanoma Patients: A Retrospective Study of2,793 CasesXue Bai, Yan Kong, Zhihong Chi, Xinan Sheng,Chuanliang Cui, Xuan Wang, Lili Mao, Bixia Tang,Siming Li, Bin Lian, Xieqiao Yan, Li Zhou, Jie Dai, Jun Guo,and Lu Si

6128 89Zr-Lumretuzumab PET Imaging before andduring HER3 Antibody Lumretuzumab Treatmentin Patients with Solid TumorsFrederike Bensch, Laetitia E. Lamberts,Micha€el M. Smeenk, Annelies Jorritsma-Smit,Marjolijn N. Lub-de Hooge,Anton G.T. Terwisscha van Scheltinga, Johan R. de Jong,Jourik A. Gietema, Carolien P. Schr€oder, Marlene Thomas,Wolfgang Jacob, Keelara Abiraj, Celine Adessi,Georgina Meneses-Lorente, Ian James, Martin Weisser,Adrienne H. Brouwers, and Elisabeth G.E. de Vries

CANCER THERAPY: PRECLINICAL

6138 Association of FGFR1 with ERa MaintainsLigand-Independent ER Transcription andMediates Resistance to Estrogen Deprivationin ERþ Breast CancerLuigi Formisano, Kimberly M. Stauffer, Christian D. Young,Neil E. Bhola, Angel L. Guerrero-Zotano, Valerie M. Jansen,M�onica M. Estrada, Katherine E. Hutchinson,JenniferM.Giltnane, Luis J. Schwarz, YaoLu, JustinM.Balko,Olivier Deas, Stefano Cairo, Jean-Gabriel Judde,Ingrid A. Mayer, Melinda Sanders, Teresa C. Dugger,Roberto Bianco, Thomas Stricker, and Carlos L. Arteaga

6151 Multifaceted Role of BTLA in the Control of CD8þ

T-cell Fate after Antigen EncounterKrit Ritthipichai, Cara L. Haymaker, Melisa Martinez,Andrew Aschenbrenner, Xiaohui Yi, Minying Zhang,Charuta Kale, Luis M. Vence, Jason Roszik,Yared Hailemichael, Willem W. Overwijk,Navin Varadarajan, Roza Nurieva, Laszlo G. Radvanyi,Patrick Hwu, and Chantale Bernatchez

6165 Timing of PD-1 Blockade Is Critical to EffectiveCombination Immunotherapy with Anti-OX40David J. Messenheimer, Shawn M. Jensen,Michael E. Afentoulis, Keith W. Wegmann, Zipei Feng,David J. Friedman, Michael J. Gough, Walter J. Urba, andBernard A. FoxSee related commentary, p. 5999

6178 Ex Vivo PD-L1/PD-1 Pathway Blockade ReversesDysfunction of Circulating CEA-Specific T Cells inPancreatic Cancer PatientsYuan Chen, Shao-An Xue, Shahriar Behboudi,Goran H. Mohammad, Stephen P. Pereira, andEmma C. Morris

6190 Local Delivery of OncoVEXmGM-CSF GeneratesSystemic Antitumor Immune ResponsesEnhanced by Cytotoxic T-Lymphocyte–AssociatedProtein BlockadeAchim K. Moesta, Keegan Cooke, Julia Piasecki,Petia Mitchell, James B. Rottman, Karen Fitzgerald,Jinghui Zhan, Becky Yang, Tiep Le, Brian Belmontes,Oluwatayo F. Ikotun, Kim Merriam, Charles Glaus,Kenneth Ganley, David H. Cordover, Andrea M. Boden,Rafael Ponce, Courtney Beers, and Pedro J. Beltran

6203 BRAF Inhibitors Amplify the Proapoptotic Activityof MEK Inhibitors by Inducing ER Stress in NRAS-Mutant MelanomaHeike Niessner, Tobias Sinnberg, Corinna Kosnopfel,Keiran S.M. Smalley, Daniela Beck, Christian Praetorius,Marion Mai, Stefan Beissert, Dagmar Kulms,Martin Schaller, Claus Garbe, Keith T. Flaherty,Dana Westphal, Ines Wanke, and Friedegund Meier

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6215 Efficacy of Onalespib, a Long-Acting Second-Generation HSP90 Inhibitor, as a Single Agentand in Combination with Temozolomide againstMalignant GliomasAlessandro Canella, Alessandra M. Welker, Ji Young Yoo,Jihong Xu, Fazly S. Abas, Divya Kesanakurti,PrabakaranNagarajan,Christine E. Beattie, Erik P. Sulman,Joseph Liu, JoyGumin, Frederick F. Lang,MetinN.Gurcan,Balveen Kaur, Deepa Sampath, and Vinay K. Puduvalli

6227 FUS–DDIT3 Fusion Protein-Driven IGF-IRSignaling is a Therapeutic Target in MyxoidLiposarcomaMarcel Trautmann, Jasmin Menzel, Christian Bertling,Magdalene Cyra, Ilka Isfort, Konrad Steinestel,Sandra Elges, Inga Gr€unewald, Bianca Altvater,Claudia Rossig, Stefan Fr€ohling, Susanne Hafner,Thomas Simmet, Pierre Åman, Eva Wardelmann,Sebastian Huss, and Wolfgang Hartmann

6239 Targeting AXL and mTOR Pathway OvercomesPrimary and Acquired Resistance to WEE1Inhibition in Small-Cell Lung CancerTriparna Sen, Pan Tong, Lixia Diao, Lerong Li,Youhong Fan, Jennifer Hoff, John V. Heymach, JingWang,and Lauren Averett Byers

6254 Inactivation of Receptor Tyrosine Kinases RevertsAberrant DNA Methylation in Acute MyeloidLeukemiaNa Shen, Fei Yan, Jiuxia Pang, Na Zhao, Naseema Gangat,Laichu Wu, Ann M. Bode, Aref Al-Kali, Mark R. Litzow,and Shujun Liu

6267 Aspirin Inhibits Cancer Metastasis andAngiogenesis via Targeting HeparanaseXiaoyang Dai, Juan Yan, Xuhong Fu, Qiuming Pan,Danni Sun, Yuan Xu, Jiang Wang, Litong Nie,Linjiang Tong, Aijun Shen, Mingyue Zheng, Min Huang,Minjia Tan, Hong Liu, Xun Huang, Jian Ding, andMeiyu Geng

BIOLOGY OF HUMAN TUMORS

6279 Tumor Purity as an Underlying Key Factor inGliomaChuanbao Zhang, Wen Cheng, Xiufang Ren, ZhengWang,Xing Liu, Guanzhang Li, Sheng Han, Tao Jiang, andAnhua Wu

6292 Efficient Mitochondrial Glutamine TargetingPrevails Over Glioblastoma Metabolic PlasticityKristell Oizel, Cynthia Chauvin, Lisa Oliver,Catherine Gratas, Fanny Geraldo, Ulrich Jarry,Emmanuel Scotet, Marion Rabe,Marie-Clotilde Alves-Guerra, Raluca Teusan,Fabien Gautier, Delphine Loussouarn, Vincent Compan,Jean-Claude Martinou, Francois M. Vallette, andClaire Pecqueur

6305 Shallow Whole Genome Sequencing onCirculating Cell-Free DNA Allows ReliableNoninvasive Copy-Number Profiling inNeuroblastoma PatientsNadine Van Roy, Malaïka Van Der Linden, Bj€orn Menten,Annelies Dheedene, Charlotte Vandeputte, Jo Van Dorpe,Genevi�eve Laureys, Marleen Renard, Tom Sante,Tim Lammens, Bram De Wilde, Frank Speleman, andKatleen De Preter

6315 Targeted Exome Sequencing of Krebs CycleGenes Reveals Candidate Cancer–PredisposingMutations in Pheochromocytomas andParagangliomasLaura Remacha, I~naki Comino-M�endez, Susan Richter,Laura Contreras, María Curr�as-Freixes, Guillermo Pita,Rocío Let�on, Antonio Galarreta, Rafael Torres-P�erez,Emiliano Honrado, Scherezade Jim�enez, Lorena Maestre,Sebastian Moran, Manel Esteller, Jorgina Satrústegui,Graeme Eisenhofer, Mercedes Robledo, andAlberto Casc�on

6325 TP53 Mutation and Its Prognostic Significancein Waldenstrom's MacroglobulinemiaSt�ephanie Poulain, Christophe Roumier,Elisabeth Bertrand, Aline Renneville,Aur�elie Caillault-Venet, Emmanuelle Doye,Sandrine Geffroy, Sheherazade Sebda, Olivier Nibourel,Morgane Nudel, Charles Herbaux, Loic Renaud,C�ecile Tomowiak, St�ephanie Guidez, Sabine Tricot,Catherine Roche-Lestienne, Bruno Quesnel,Claude Preudhomme, and Xavier Leleu

6336 miRomics and Proteomics Reveal a miR-296-3p/PRKCA/FAK/Ras/c-Myc Feedback LoopModulated by HDGF/DDX5/b-catenin Complexin Lung AdenocarcinomaQiaofen Fu, Xin Song, Zhen Liu, Xiaojie Deng,Rongcheng Luo, Chunlei Ge, Ruilei Li, Zhen Li,Mengyang Zhao, Yiyu Chen, Xian Lin, Qianbing Zhang,and Weiyi Fang

6351 Direct Metabolic Interrogation ofDihydrotestosterone Biosynthesis from AdrenalPrecursors in Primary Prostatectomy TissuesCharles Dai, Yoon-Mi Chung, Evan Kovac, Ziqi Zhu,Jianneng Li, Cristina Magi-Galluzzi,Andrew J. Stephenson, Eric A. Klein, and Nima Sharifi

6363 Immunodeficiency in PancreaticAdenocarcinoma with Diabetes Revealed byComparative GenomicsYuanqing Yan, Ruli Gao, Thao L.P. Trinh, andMaria B. Grant

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LETTERS TO THE EDITOR

6374 Genomics of Immunotherapy-AssociatedHyperprogressors—LetterAndrea Forschner, Heike Niessner, Yvonne M€oller,Peter Horak, Martina Fr€ohlich, Gregor Warsow,Albrecht Stenzinger, Stefan Fr€ohling, Hanno Glimm,Bernhard Klumpp, Claus Garbe, and Tobias Sinnberg

6376 Genomics of Immunotherapy-AssociatedHyperprogressors—ResponseShumei Kato and Razelle Kurzrock

6377 Individualized Pazopanib Dosing—LetterAudrey Bellesoeur, Pascaline Boudou-Rouquette,Audrey Thomas-Schoemann, Charlotte Joly,Camille Tlemsani, Michel Vidal, Francois Goldwasser, andBenoit Blanchet

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ABOUT THE COVER

The cover shows a section of liver from a mouse with acute myeloid leukemia. Hematoxylinand eosin staining shows infiltration of leukemic cells to the liver. For details, see the article byShen and colleagues on page 6254 of this issue.

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