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James Mulé, PhD

Program: Immunology


The clinical application of immunotherapy for cancer is rapidly moving forward in multiple areas, which incorporate the adoptive transfer of antitumor-reactive T cells and the use of 'therapeutic' vaccines. Both clinical and immunologic endpoints have shown new promise to the field. Novel dendritic cell-based vaccine strategies designed in the laboratory and proven in preclinical animal tumor models are now entering the clinic, with the intent of providing therapeutic efficacy. Improvements on this approach involve breaking tolerance to tumor 'self' antigens by inhibiting regulatory cells, boosting T cell co-stimulation, and administering combinations of recombinant cytokines and other defined molecules with 'immuno-enhancing' activities. Development of these improvements is the primary research interest of Dr. Mulé.


    • Cutaneous Oncology
    • Immunology
    • Radiation Oncology
    • Immuno-Oncology
    • Melanoma Research Center of Excellence
    • Center for Immunization and Infection Research in Cancer
    • Immuno-Oncology

Education & Training


  • University of Washington School of Medicine, Postdoctoral Fellow - Tumor Immunology
  • National Cancer Institute, Senior Staff Fellow - Tumor Immunology and Immunotherapy
  • Stanford University School of Medicine, Visiting Fellow - Stem Cell Biology

On the basis of encouraging data from their preclinical studies, Dr. Mulé and his colleagues initiated and completed two phase I clinical trials of autologous tumor lysate/keyhole limpet haemocyanin (KLH)-pulsed dendritic cells (TP-DCs) in children and adults with advanced solid tumors. The DCs, characterized as immature by phenotypic marker profiling, yielded both immunologic and very modest clinical responses. Immunologic assays revealed evidence of the induction of peripheral blood T-cell reactivity to both KLH and tumor lysates after immunization, particularly in children. Because durable and complete regression of established tumors has been difficult to achieve through administration of TP-DCs alone, Dr. Mulé and his colleagues have embarked on a new series of clinical trails to evaluate potential improvements in their DC-based vaccine strategy that incorporate intratumoral delivery of KLH-pulsed DCs; systemic administration of interleukin-2 (IL-2); use of locally produced secondary lymphoid tissue chemokine; and the setting of lymphopenia-induced, homeostatic-driven T-cell proliferation. These clinical trials include (1) a phase Ib trial assessing autologous TP-DCs as a tumor vaccine administered with or without IL-2 in patients with metastatic melanoma; (2) a phase II trial assessing autologous TP-DCs as a tumor vaccine administered with low-dose IL-2 in patients with colorectal cancer; (3) a phase I trial assessing intratumoral administration of autologous DCs activated by granulocyte-macrophage colony-stimulating factor and interleukin-4 as a vaccine in muscle-invasive bladder cancer; (4) a phase I trial of escalating doses of fludarabine followed by intranodal delivery of MHC class I/II peptide-pulsed DCs in patients with chemotherapy-naive metastatic melanoma; (5) a randomized phase II trial of fludarabine followed by intranodal delivery of peptide-pulsed DCs with or without autologous lymphocyte infusion; (6) a phase II trial of TP-DC vaccines early after autologous hematopoietic stem cell transplantation to prolong progression-free survival in children with sarcoma; and (7) a phase I clinical study assessing autologous DCs gene-modified to secrete secondary lymphoid tissue chemokine as a vaccine to enhance T-cell priming in patients with advanced solid tumors.


  • Li R, Zhang J, Gilbert SM, Conejo-Garcia J, Mulé JJ. Using oncolytic viruses to ignite the tumour immune microenvironment in bladder cancer. Nat Rev Urol. 2021 Sep.18(9):543-555. Pubmedid: 34183833.
  • Chakiryan NH, Hajiran A, Kim Y, Aydin AM, Zemp L, Katende E, Nguyen J, Fan W, Cheng CH, Lopez-Blanco N, Chahoud J, Spiess PE, Fournier M, Dhillon J, Wang L, Moran-Segura C, Mulé J, Du D, Yoder SJ, Berglund A, Teer JK, Manley BJ. Correlating Immune Cell Infiltration Patterns with Recurrent Somatic Mutations in Advanced Clear Cell Renal Cell Carcinoma. Eur Urol Focus. 2021 May. Pubmedid: 33994165.
  • Aoyama S, Nakagawa R, Mulé JJ, Mailloux AW. Inducible Tertiary Lymphoid Structures: Promise and Challenges for Translating a New Class of Immunotherapy. Front Immunol. 2021 May.12:675538. Pubmedid: 34054863. Pmcid: PMC8160316.
  • Zaman S, Hajiran A, Coba GA, Robinson T, Madanayake TW, Segarra DT, Chobrutskiy BI, Boyle TA, Zhou JM, Kim Y, Mulé JJ, Teer JK, Manley BJ. Aberrant Epidermal Growth Factor Receptor RNA Splice Products Are Among the Most Frequent Somatic Alterations in Clear Cell Renal Cell Carcinoma and Are Associated with a Poor Response to Immunotherapy. Eur Urol Focus. 2021 Mar.7(2):373-380. Pubmedid: 31901438. Pmcid: PMC7771328.
  • Aoyama S, Nakagawa R, Nemoto S, Perez-Villarroel P, Mulé JJ, Mailloux AW. Checkpoint blockade accelerates a novel switch from an NKT-driven TNFα response toward a T cell driven IFN-γ response within the tumor microenvironment. J Immunother Cancer. 2021 Jun.9(6). Pubmedid: 34135102. Pmcid: PMC8211075.
  • Li R, Berglund A, Zemp L, Dhillon J, Putney R, Kim Y, Jain RK, Grass GD, Conejo-Garcia J, Mulé JJ. The 12-CK Score: Global Measurement of Tertiary Lymphoid Structures. Front Immunol. 2021 Jun.12:694079. Pubmedid: 34267760. Pmcid: PMC8276102.
  • Chakiryan NH, Kimmel GJ, Kim Y, Johnson JO, Clark N, Hajiran A, Chang A, Aydin AM, Zemp L, Katende E, Chahoud J, Ferrall-Fairbanks MC, Spiess PE, Francis N, Fournier M, Dhillon J, Park JY, Wang L, Mulé JJ, Altrock PM, Manley BJ. Geospatial Cellular Distribution of Cancer-Associated Fibroblasts Significantly Impacts Clinical Outcomes in Metastatic Clear Cell Renal Cell Carcinoma. Cancers (Basel). 2021 Jul.13(15). Pubmedid: 34359645. Pmcid: PMC8345222.
  • Mullinax JE, Hall M, Beatty M, Weber AM, Sannasardo Z, Svrdlin T, Hensel J, Richards A, Gonzalez RJ, Cox CA, Kelley L, Mulé JJ, Sarnaik AA, Pilon-Thomas S. Expanded Tumor-infiltrating Lymphocytes From Soft Tissue Sarcoma Have Tumor-specific Function. J Immunother. 2021 Feb.44(2):63-70. Pubmedid: 33443972. Pmcid: PMC8111686.
  • Hajiran A, Chakiryan N, Aydin AM, Zemp L, Nguyen J, Laborde JM, Chahoud J, Spiess PE, Zaman S, Falasiri S, Fournier M, Teer JK, Dhillon J, McCarthy S, Moran-Segura C, Katende EN, Sexton WJ, Koomen JM, Mulé J, Kim Y, Manley B. Reconnaissance of tumor immune microenvironment spatial heterogeneity in metastatic renal cell carcinoma and correlation with immunotherapy response. Clin Exp Immunol. 2021 Apr.204(1):96-106. Pubmedid: 33346915. Pmcid: PMC7944355.
  • Falahat R, Berglund A, Putney RM, Perez-Villarroel P, Aoyama S, Pilon-Thomas S, Barber GN, Mulé JJ. Epigenetic reprogramming of tumor cell-intrinsic STING function sculpts antigenicity and T cell recognition of melanoma. Proc Natl Acad Sci U S A. 2021 Apr.118(15). Pubmedid: 33827917. Pmcid: PMC8053941.
  • Chakiryan NH, Kimmel GJ, Kim Y, Hajiran A, Aydin AM, Zemp L, Katende E, Nguyen J, Lopez-Blanco N, Chahoud J, Spiess PE, Fournier M, Dhillon J, Wang L, Moran-Segura C, El-Kenawi A, Mulé J, Altrock PM, Manley BJ. Spatial clustering of CD68+ tumor associated macrophages with tumor cells is associated with worse overall survival in metastatic clear cell renal cell carcinoma. PLoS One. 2021 Apr.16(4):e0245415. Pubmedid: 33882057. Pmcid: PMC8059840.
  • Hamaidi I, Zhang L, Kim N, Wang MH, Iclozan C, Fang B, Liu M, Koomen JM, Berglund AE, Yoder SJ, Yao J, Engelman RW, Creelan BC, Conejo-Garcia JR, Antonia SJ, Mulé JJ, Kim S. Sirt2 Inhibition Enhances Metabolic Fitness and Effector Functions of Tumor-Reactive T Cells. Cell Metab. 2020 Sep.32(3):420-436.e12. Pubmedid: 32768387. Pmcid: PMC7484212.
  • Nakagawa R, Brayer J, Restrepo N, Mulé JJ, Mailloux AW. High-Dimensional Flow Cytometry Analysis of Regulatory Receptors on Human T Cells, NK Cells, and NKT Cells. Methods Mol Biol. 2020 Sep.2194:255-290. Pubmedid: 32926371. Pmcid: PMC7744271.
  • Garg SK, Welsh EA, Fang B, Hernandez YI, Rose T, Gray J, Koomen JM, Berglund A, Mulé JJ, Markowitz J. Multi-Omics and Informatics Analysis of FFPE Tissues Derived from Melanoma Patients with Long/Short Responses to Anti-PD1 Therapy Reveals Pathways of Response. Cancers (Basel). 2020 Nov.12(12). Pubmedid: 33255891. Pmcid: PMC7768436.
  • Berglund A, Mills M, Putney RM, Hamaidi I, Mulé J, Kim S. Methylation of immune synapse genes modulates tumor immunogenicity. J Clin Invest. 2020 Feb.130(2):974-980. Pubmedid: 31714899. Pmcid: PMC6994116.
  • Garg SK, Ott MJ, Mostofa AGM, Chen Z, Chen YA, Kroeger J, Cao B, Mailloux AW, Agrawal A, Schaible BJ, Sarnaik A, Weber JS, Berglund AE, Mulé JJ, Markowitz J. Multi-Dimensional Flow Cytometry Analyses Reveal a Dichotomous Role for Nitric Oxide in Melanoma Patients Receiving Immunotherapy. Front Immunol. 2020 Feb.11:164. Pubmedid: 32161584. Pmcid: PMC7052497.
  • Wu Q, Berglund AE, Wang D, MacAulay RJ, Mulé JJ, Etame AB. Paradoxical epigenetic regulation of XAF1 mediates plasticity towards adaptive resistance evolution in MGMT-methylated glioblastoma. Sci Rep. 2019 Oct.9(1):14072. Pubmedid: 31575897. Pmcid: PMC6773736.
  • Falahat R, Perez-Villarroel P, Mailloux AW, Zhu G, Pilon-Thomas S, Barber GN, Mulé JJ. STING Signaling in Melanoma Cells Shapes Antigenicity and Can Promote Antitumor T-cell Activity. Cancer Immunol Res. 2019 Nov.7(11):1837-1848. Pubmedid: 31462408. Pmcid: PMC6825582.
  • Zhu G, Brayer J, Padron E, Mulé JJ, Mailloux AW. OMIP-049: Analysis of Human Myelopoiesis and Myeloid Neoplasms. Cytometry A. 2018 Oct.93(10):982-986. Pubmedid: 30347519. Pmcid: PMC6484443.
  • Sloot S, Chen YA, Zhao X, Weber JL, Benedict JJ, Mulé JJ, Smalley KS, Weber JS, Zager JS, Forsyth PA, Sondak VK, Gibney GT. Reply to Improving the survival of patients with American Joint Committee on Cancer stage III and IV melanoma. Cancer. 2018 May.124(10):2254-2255. Pubmedid: 29543319.
  • Mullinax JE, Hall M, Prabhakaran S, Weber J, Khushalani N, Eroglu Z, Brohl AS, Markowitz J, Royster E, Richards A, Stark V, Zager JS, Kelley L, Cox C, Sondak VK, Mulé JJ, Pilon-Thomas S, Sarnaik AA. Combination of Ipilimumab and Adoptive Cell Therapy with Tumor-Infiltrating Lymphocytes for Patients with Metastatic Melanoma. Front Oncol. 2018 Mar.8:44. Pubmedid: 29552542. Pmcid: PMC5840208.
  • Zhu G, Nemoto S, Mailloux AW, Perez-Villarroel P, Nakagawa R, Falahat R, Berglund AE, Mulé JJ. Induction of Tertiary Lymphoid Structures With Antitumor Function by a Lymph Node-Derived Stromal Cell Line. Front Immunol. 2018 Jul.9:1609. Pubmedid: 30061886. Pmcid: PMC6054958.
  • Sloot S, Chen YA, Zhao X, Weber JL, Benedict JJ, Mulé JJ, Smalley KS, Weber JS, Zager JS, Forsyth PA, Sondak VK, Gibney GT. Improved survival of patients with melanoma brain metastases in the era of targeted BRAF and immune checkpoint therapies. Cancer. 2018 Jan.124(2):297-305. Pubmedid: 29023643. Pmcid: PMC7771556.
  • Konno H, Yamauchi S, Berglund A, Putney RM, Mulé JJ, Barber GN. Suppression of STING signaling through epigenetic silencing and missense mutation impedes DNA damage mediated cytokine production. Oncogene. 2018 Apr.37(15):2037-2051. Pubmedid: 29367762. Pmcid: PMC6029885.
  • Stefanski HE, Jonart L, Goren E, Mulé JJ, Blazar BR. A novel approach to improve immune effector responses post transplant by restoration of CCL21 expression. PLoS One. 2018 Apr.13(4):e0193461. Pubmedid: 29617362. Pmcid: PMC5884478.
  • Strom T, Harrison LB, Giuliano AR, Schell MJ, Eschrich SA, Berglund A, Fulp W, Thapa R, Coppola D, Kim S, Frakes J, Foekens J, Mulé JJ, Torres-Roca JF. Tumour radiosensitivity is associated with immune activation in solid tumours. Eur J Cancer. 2017 Oct.84:304-314. Pubmedid: 28863385. Pmcid: PMC5822441.
  • Yagawa Y, Robertson-Tessi M, Zhou SL, Anderson ARA, Mulé JJ, Mailloux AW. Systematic Screening of Chemokines to Identify Candidates to Model and Create Ectopic Lymph Node Structures for Cancer Immunotherapy. Sci Rep. 2017 Nov.7(1):15996. Pubmedid: 29167448. Pmcid: PMC5700067.
  • Prabhakaran S, Rizk VT, Ma Z, Cheng CH, Berglund AE, Coppola D, Khalil F, Mulé JJ, Soliman HH. Evaluation of invasive breast cancer samples using a 12-chemokine gene expression score: correlation with clinical outcomes. Breast Cancer Res. 2017 Jun.19(1):71. Pubmedid: 28629479. Pmcid: PMC5477261.
  • Zhu G, Falahat R, Wang K, Mailloux A, Artzi N, Mulé JJ. Tumor-Associated Tertiary Lymphoid Structures: Gene-Expression Profiling and Their Bioengineering. Front Immunol. 2017 Jun.8:767. Pubmedid: 28713385. Pmcid: PMC5491937.
  • Wang D, Berglund AE, Kenchappa RS, MacAulay RJ, Mulé JJ, Etame AB. BIRC3 is a biomarker of mesenchymal habitat of glioblastoma, and a mediator of survival adaptation in hypoxia-driven glioblastoma habitats. Sci Rep. 2017 Aug.7(1):9350. Pubmedid: 28839258. Pmcid: PMC5570925.
  • Strom T, Torres-Roca JF, Parekh A, Naghavi AO, Caudell JJ, Oliver DE, Messina JL, Khushalani NI, Zager JS, Sarnaik A, Mulé JJ, Trotti AM, Eschrich SA, Sondak VK, Harrison LB. Regional Radiation Therapy Impacts Outcome for Node-Positive Cutaneous Melanoma. J Natl Compr Canc Ne. 2017 Apr.15(4):473-482. Pubmedid: 28404758. Pmcid: PMC7771284.
  • Nemoto S, Mailloux AW, Kroeger J, Mulé JJ. OMIP-031: Immunologic checkpoint expression on murine effector and memory T-cell subsets. Cytometry A. 2016 May.89(5):427-429. Pubmedid: 26859685. Pmcid: PMC4879048.
  • Pilon-Thomas S, Kodumudi KN, El-Kenawi AE, Russell S, Weber AM, Luddy K, Damaghi M, Wojtkowiak JW, Mulé JJ, Ibrahim-Hashim A, Gillies RJ. Neutralization of Tumor Acidity Improves Antitumor Responses to Immunotherapy. Cancer Res. 2016 Mar.76(6):1381-1390. Pubmedid: 26719539. Pmcid: PMC4829106.
  • Wang D, Berglund A, Kenchappa RS, Forsyth PA, Mulé JJ, Etame AB. BIRC3 is a novel driver of therapeutic resistance in Glioblastoma. Sci Rep. 2016 Feb.6:21710. Pubmedid: 26888114. Pmcid: PMC4757860.
  • Sung H, Kanchi KL, Wang X, Hill KS, Messina JL, Lee JH, Kim Y, Dees ND, Ding L, Teer JK, Yang S, Sarnaik AA, Sondak VK, Mulé JJ, Wilson RK, Weber JS, Kim M. Inactivation of RASA1 promotes melanoma tumorigenesis via R-Ras activation. Oncotarget. 2016 Apr.7(17):23885-23896. Pubmedid: 26993606. Pmcid: PMC5029671.
  • Weber JS, Mulé JJ. Cancer immunotherapy meets biomaterials. Nat Biotechnol. 2015 Jan.33(1):44-45. Pubmedid: 25574635.
  • Mihm MC, Mulé JJ. Reflections on the Histopathology of Tumor-Infiltrating Lymphocytes in Melanoma and the Host Immune Response. Cancer Immunol Res. 2015 Aug.3(8):827-835. Pubmedid: 26242760. Pmcid: PMC4527084.
  • Ding L, Kim M, Kanchi KL, Dees ND, Lu C, Griffith M, Fenstermacher D, Sung H, Miller CA, Goetz B, Wendl MC, Griffith O, Cornelius LA, Linette GP, McMichael JF, Sondak VK, Fields RC, Ley TJ, Mulé JJ, Wilson RK, Weber JS. Clonal architectures and driver mutations in metastatic melanomas. PLoS One. 2014 Nov.9(11):e111153. Pubmedid: 25393105. Pmcid: PMC4230926.
  • Komine H, Kuhn L, Matsushita N, Mulé JJ, Pilon-Thomas S. Examination of MARCO activity on dendritic cell phenotype and function using a gene knockout mouse. PLoS One. 2014 Feb.8(7):e67795. Pubmedid: 23840879. Pmcid: PMC3698187.
  • Radvanyi L, Pilon-Thomas S, Peng W, Sarnaik A, Mulé JJ, Weber J, Hwu P. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer--letter. Clin Cancer Res. 2013 Oct.19(19):5541. Pubmedid: 24048330. Pmcid: PMC3823378.
  • Messina JL, Fenstermacher DA, Eschrich S, Qu X, Berglund AE, Lloyd MC, Schell MJ, Sondak VK, Weber JS, Mulé JJ. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy?. Sci Rep. 2013 Mar.2:765. Pubmedid: 23097687. Pmcid: PMC3479449.
  • Pilon-Thomas S, Kuhn L, Ellwanger S, Janssen W, Royster E, Marzban S, Kudchadkar R, Zager J, Gibney G, Sondak VK, Weber J, Mulé JJ, Sarnaik AA. Efficacy of adoptive cell transfer of tumor-infiltrating lymphocytes after lymphopenia induction for metastatic melanoma. J Immunother. 2012 Oct.35(8):615-620. Pubmedid: 22996367. Pmcid: PMC4467830.
  • Coppola D, Nebozhyn M, Khalil F, Dai H, Yeatman T, Loboda A, Mulé JJ. Unique ectopic lymph node-like structures present in human primary colorectal carcinoma are identified by immune gene array profiling. Am J Pathol. 2011 Jul.179(1):37-45. Pubmedid: 21703392. Pmcid: PMC3123872.
  • Matsushita N, Komine H, Grolleau-Julius A, Pilon-Thomas S, Mulé JJ. Targeting MARCO can lead to enhanced dendritic cell motility and anti-melanoma activity. Cancer Immunol Immun. 2010 Jun.59(6):875-884. Pubmedid: 20054688. Pmcid: PMC2861905.
  • Pilon-Thomas S, Mackay A, Vohra N, Mulé JJ. Blockade of programmed death ligand 1 enhances the therapeutic efficacy of combination immunotherapy against melanoma. J Immunol. 2010 Apr.184(7):3442-3449. Pubmedid: 20194714. Pmcid: PMC2913584.
  • Mulé JJ. Dendritic cell-based vaccines for pancreatic cancer and melanoma. Ann Ny Acad Sci. 2009 Sep.1174:33-40. Pubmedid: 19769734.
  • Yeatman TJ, Mule J, Dalton WS, Sullivan D. On the eve of personalized medicine in oncology. Cancer Res. 2008 Sep.68(18):7250-7252. Pubmedid: 18794109. Pmcid: PMC2650840.
  • Coppola D, Mule J. Ectopic lymph nodes within human solid tumors. J Clin Oncol. 2008 Sep.26(27):4369-4370. Pubmedid: 18802146.
  • Koike N, Pilon-Thomas S, Mulé JJ. Nonmyeloablative chemotherapy followed by T-cell adoptive transfer and dendritic cell-based vaccination results in rejection of established melanoma. J Immunother. 2008 May.31(4):402-412. Pubmedid: 18391755.
  • Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mule JJ, Pledger WJ, Wang HG. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol. 2007 Oct.9(10):1142-1151. Pubmedid: 17891140. Pmcid: PMC2254521.
  • Anasetti C, Mulé JJ. To ablate or not to ablate? HSCs in the T cell driver's seat. J Clin Invest. 2007 Feb.117(2):306-310. Pubmedid: 17273553. Pmcid: PMC1783831.
  • Pilon-Thomas S, Verhaegen M, Kuhn L, Riker A, Mule J. Induction of anti-tumor immunity by vaccination with dendritic cells pulsed with anti-CD44 IgG opsonized tumor cells. Cancer Immunol Immun. 2006 Oct.55(10):1238-1246. Pubmedid: 16315029.
  • Moyer J, Maine G, Mule J. Early vaccination with tumor-lysate-pulsed dendritic cells after allogeneic bone marrow transplantation has antitumor effects. Biol Blood Marrow Tr. 2006 Oct.12(10):1010-1019. Pubmedid: 17084367.
  • Sondak V, Sabel M, Mule J. Allogeneic and autologous melanoma vaccines: where have we been and where are we going?. Clin Cancer Res. 2006 Apr.12(7 Pt 2):2337s-2341s. Pubmedid: 16609055.
  • Kortylewski M, Kujawski M, Wang T, Wei S, Zhang S, Pilon-Thomas S, Niu G, Kay H, Mulé J, Kerr WG, Jove R, Pardoll D, Yu H. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med. 2005 Dec.11(12):1314-1321. Pubmedid: 16288283.
  • Terando A, Roessler B, Mule J. Chemokine gene modification of human dendritic cell-based tumor vaccines using a recombinant adenoviral vector. Cancer Gene Ther. 2004 Mar.11(3):165-173. Pubmedid: 14726959.
  • Antonia S, Mule J, Weber J. Current developments of immunotherapy in the clinic. Curr Opin Immunol. 2004 Apr.16(2):130-136. Pubmedid: 15023403.
  • Mule J, Weber J. Translation of cancer immunotherapies. Nat Med. 2004.10(11):1153-1154. Pubmedid: 15516900.
  • Pilon-Thomas S, Verhaegen M, Mule J. Dendritic cell-based therapeutics for breast cancer. Breast Dis. 2004.20:65-71. Pubmedid: 15687708.
  • Asavaroengchai W, Kotera Y, Koike N, Pilon-Thomas S, Mule J. Augmentation of antitumor immune responses after adoptive transfer of bone marrow derived from donors immunized with tumor lysate-pulsed dendritic cells. Biol Blood Marrow Tran. 2004.10:524-533. Pubmedid: 15282530.
  • Grolleau A, Misek D, Kuick R, Hanash S, Mule J. Inducible expression of macrophage receptor Marco by dendritic cells following phagocytic uptake of dead cells uncovered by oligonucleotide arrays. J Immunol. 2003 Sep.171(6):2879-2888. Pubmedid: 12960310.
  • Terando A, Mule J. On combining antineoplastic drugs with tumor vaccines. Psychooncology. 2003.52(11):680-685. Pubmedid: 12955481.
  • Quintana A, Raczka E, Piehler L, Lee I, Myc A, Majoros I, Patri AK, Thomas T, Mulé J, Baker JR. Design and function of a dendrimer-based therapeutic nanodevice targeted to tumor cells through the folate receptor. Pharm Res. 2002 Sep.19(9):1310-1316. Pubmedid: 12403067.
  • Maine GN, Mulé JJ. Making room for T cells. J Clin Invest. 2002 Jul.110(2):157-159. Pubmedid: 12122106. Pmcid: PMC151072.
  • Asavaroengchai W, Kotera Y, Mulé JJ. Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc Natl Acad Sci U S A. 2002 Jan.99(2):931-936. Pubmedid: 11792864. Pmcid: PMC117408.
  • Chang A, Redman B, Whitfield J, Nickoloff B, Braun T, Lee P, GeigerJD, Mule J. A phase I trial of tumor lysate-pulsed dendritic cells in the treatment of advanced cancer. Clin Cancer Res. 2002 Apr.8(4):1021-1032. Pubmedid: 11948109.
  • Kotera Y, Shimizu K, Mule J. Comparative analysis of necrotic and apoptotic tumor cells as a source of antigen(s) in dendritic cell-based immunization. Cancer Res. 2001 Nov.61(22):8105-8109. Pubmedid: 11719436.
  • Morita Y, Yang J, Gupta R, Shimizu K, Shelden E, Endres J, Mule J, McDonagh K, Fox D. Dendritic cells genetically engineered to express IL-4 inhibit murine collagen-induced arthritis. J Clin Invest. 2001 May.107(10):1275-1284. Pubmedid: 11375417. Pmcid: PMC209294.
  • Shimizu K, Thomas E, Giedlin M, Mule J. Enhancement of tumor lysate- and peptide-pulsed dendritic cell-based vaccines by the addition of foreign helper protein. Cancer Res. 2001 Mar.61(6):2618-2624. Pubmedid: 11289139.
  • Kirk CJ, Hartigan-O'Connor D, Nickoloff BJ, Chamberlain JS, Giedlin M, Aukerman L, Mule JJ. T cell-dependent antitumor immunity mediated by secondary lymphoid tissue chemokine: augmentation of dendritic cell-based immunotherapy. Cancer Res. 2001 Mar.61(5):2062-2070. Pubmedid: 11280767.
  • Weber J, Mule J. How much help does a vaccine-induced T-cell response need?. J Clin Invest. 2001 Mar.107(5):553-554. Pubmedid: 11238555. Pmcid: PMC199430.
  • Candido K, Shimizu K, McLaughlin J, Kunkel R, Fuller J, Redman B, Thomas E, Nickoloff B, Mule J. Local administration of dendritic cells inhibits established breast tumor growth: implications for apoptosis-inducing agents. Cancer Res. 2001 Jan.61(1):228-236. Pubmedid: 11196166.
  • Kirk C, Hartigan-O'Connor D, Mule J. The dynamics of the T-cell antitumor response: chemokine-secreting dendritic cells can prime tumor-reactive T cells extranodally. Cancer Res. 2001 Dec.61(24):8794-8802. Pubmedid: 11751401.
  • Hartigan-O'Connor D, Kirk CJ, Crawford R, Mulé JJ, Chamberlain JS. Immune evasion by muscle-specific gene expression in dystrophic muscle. Mol Ther. 2001 Dec.4(6):525-533. Pubmedid: 11735336.
  • Geiger J, Hutchinson R, Hohenkirk L, McKenna E, Yanik G, Levine J, Chang A, Braun T, Mule J. Vaccination of pediatric solid tumor patients with tumor lysate-pulsed dendritic cells can expand specific T cells and mediate tumor regression. Cancer Res. 2001 Dec.61(23):8513-8519. Pubmedid: 11731436.
  • Mulé JJ. Tumor vaccine strategies that employ dendritic cells and tumor lysates: experimental and clinical studies. Immunol Invest. 2000 May.29(2):127-129. Pubmedid: 10854180.
  • Shimizu K, Fields R, Redman B, Giedlin M, Mule J. Potentiation of immunologic responsiveness to dendritic cell-based tumor vaccines by recombinant interleukin-2. Cancer J Sci Am. 2000 Feb.6 Suppl 1:S67-S75. Pubmedid: 10685663.
  • Kirk C, Mule J. Gene-modified dendritic cells for use in tumor vaccines. Hum Gene Ther. 2000 Apr.11(6):797-806. Pubmedid: 10779157.
  • Shimizu K, Fields RC, Giedlin M, Mulé JJ. Systemic administration of interleukin 2 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines. Proc Natl Acad Sci U S A. 1999 Mar.96(5):2268-2273. Pubmedid: 10051630. Pmcid: PMC26772.
  • Xie Y, Hwang C, Overwijk W, Zeng Z, Eng M, Mule J, Imperiale M, Restifo NP, Sanda M. Induction of tumor antigen-specific immunity in vivo by a novel vaccinia vectorencoding safety-modified simian virus 40 T antigen. J Natl Cancer Inst. 1999 Jan.91(2):169-175. Pubmedid: 9923859 .
  • Fields RC, Shimizu K, Mulé JJ. Murine dendritic cells pulsed with whole tumor lysates mediate potent antitumor immune responses in vitro and in vivo. Proc Natl Acad Sci U S A. 1998 Aug.95(16):9482-9487. Pubmedid: 9689106. Pmcid: PMC21364.
  • Mule J, Custer M, Averbook B, Yang J, Weber J, Goeddel D, Rosenberg S, Schall T. RANTES secretion by gene-modified tumor cells results in loss of tumorigenicity in vivo: role of immune cell subpopulations. Hum Gene Ther. 1996 Aug.7(13):1545-1553. Pubmedid: 8864755 .
  • Mulé JJ, Custer M, Averbook B, Yang JC, Weber JS, Goeddel DV, Rosenberg SA, Schall TJ. RANTES secretion by gene-modified tumor cells results in loss of tumorigenicity in vivo: role of immune cell subpopulations. Hum Gene Ther. 1996 Aug.7(13):1545-1553. Pubmedid: 8864755.
  • Marincola FM, Shamamian P, Simonis TB, Abati A, Hackett J, O'Dea T, Fetsch P, Yannelli J, Restifo NP, Mulé JJ. Locus-specific analysis of human leukocyte antigen class I expression in melanoma cell lines. J Immunother Emphasis Tumor Immunol. 1994 Jul.16(1):13-23. Pubmedid: 8081556. Pmcid: PMC2561308.
  • Cohen PA, Cohen PJ, Rosenberg SA, Mulé JJ. CD4+ T-cells from mice immunized to syngeneic sarcomas recognize distinct, non-shared tumor antigens. Cancer Res. 1994 Feb.54(4):1055-1058. Pubmedid: 7906197.
  • Kerr WG, Mulé JJ. Gene therapy: current status and future prospects. J Leukoc Biol. 1994 Aug.56(2):210-214. Pubmedid: 8071597.
  • Marincola FM, Ettinghausen S, Cohen PA, Cheshire LB, Restifo NP, Mulé JJ, Rosenberg SA. Treatment of established lung metastases with tumor-infiltrating lymphocytes derived from a poorly immunogenic tumor engineered to secrete human TNF-alpha. J Immunol. 1994 Apr.152(7):3500-3513. Pubmedid: 8144931. Pmcid: PMC2248454.
  • Shiloni E, Karp SE, Custer MC, Shilyansky J, Restifo NP, Rosenberg SA, Mulé JJ. Retroviral transduction of interferon-gamma cDNA into a nonimmunogenic murine fibrosarcoma: generation of T cells in draining lymph nodes capable of treating established parental metastatic tumor. Cancer Immunol Immun. 1993 Oct.37(5):286-292. Pubmedid: 8402732. Pmcid: PMC2248452.
  • Karp SE, Farber A, Salo JC, Hwu P, Jaffe G, Asher AL, Shiloni E, Restifo NP, Mulé JJ, Rosenberg SA. Cytokine secretion by genetically modified nonimmunogenic murine fibrosarcoma. Tumor inhibition by IL-2 but not tumor necrosis factor. J Immunol. 1993 Feb.150(3):896-908. Pubmedid: 8423345. Pmcid: PMC2121323.
  • Restifo NP, Esquivel F, Kawakami Y, Yewdell JW, Mulé JJ, Rosenberg SA, Bennink JR. Identification of human cancers deficient in antigen processing. J Exp Med. 1993 Feb.177(2):265-272. Pubmedid: 8426105. Pmcid: PMC1950463.
  • Karp SE, Hwu P, Farber A, Restifo NP, Kriegler M, Mulé JJ, Rosenberg SA. In vivo activity of tumor necrosis factor (TNF) mutants. Secretory but not membrane-bound TNF mediates the regression of retrovirally transduced murine tumor. J Immunol. 1992 Sep.149(6):2076-2081. Pubmedid: 1517571. Pmcid: PMC2121327.
  • Restifo NP, Spiess PJ, Karp SE, Mulé JJ, Rosenberg SA. A nonimmunogenic sarcoma transduced with the cDNA for interferon gamma elicits CD8+ T cells against the wild-type tumor: correlation with antigen presentation capability. J Exp Med. 1992 Jun.175(6):1423-1431. Pubmedid: 1588273. Pmcid: PMC1974839.
  • Hwu P, Schwarz S, Custer M, Smith CA, Mulé JJ, Rosenberg SA. Use of soluble recombinant TNF receptor to improve detection of TNF secretion in cultures of tumor infiltrating lymphocytes. J Immunol Methods. 1992 Jul.151(1-2):139-147. Pubmedid: 1321199.
  • Mulé JJ, Custer MC, Travis WD, Rosenberg SA. Cellular mechanisms of the antitumor activity of recombinant IL-6 in mice. J Immunol. 1992 Apr.148(8):2622-2629. Pubmedid: 1348521.
  • Jicha DL, Schwarz S, Mulé JJ, Rosenberg SA. Interleukin-7 mediates the generation and expansion of murine allosensitized and antitumor CTL. Cell Immunol. 1992 Apr.141(1):71-83. Pubmedid: 1555257.
  • Asher AL, Mulé JJ, Kasid A, Restifo NP, Salo JC, Reichert CM, Jaffe G, Fendly B, Kriegler M, Rosenberg SA. Murine tumor cells transduced with the gene for tumor necrosis factor-alpha. Evidence for paracrine immune effects of tumor necrosis factor against tumors. J Immunol. 1991 May.146(9):3227-3234. Pubmedid: 2016545. Pmcid: PMC1950469.
  • Barth RJ, Mulé JJ, Spiess PJ, Rosenberg SA. Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. J Exp Med. 1991 Mar.173(3):647-658. Pubmedid: 1900079. Pmcid: PMC2118834.
  • Barth RJ, Mulé JJ, Asher AL, Sanda MG, Rosenberg SA. Identification of unique murine tumor associated antigens by tumor infiltrating lymphocytes using tumor specific secretion of interferon-gamma and tumor necrosis factor. J Immunol Methods. 1991 Jul.140(2):269-279. Pubmedid: 1906077.
  • Jicha DL, Mulé JJ, Rosenberg SA. Interleukin 7 generates antitumor cytotoxic T lymphocytes against murine sarcomas with efficacy in cellular adoptive immunotherapy. J Exp Med. 1991 Dec.174(6):1511-1515. Pubmedid: 1744582. Pmcid: PMC2119035.
  • Restifo NP, Esquivel F, Asher AL, Stötter H, Barth RJ, Bennink JR, Mulé JJ, Yewdell JW, Rosenberg SA. Defective presentation of endogenous antigens by a murine sarcoma. Implications for the failure of an anti-tumor immune response. J Immunol. 1991 Aug.147(4):1453-1459. Pubmedid: 1907999. Pmcid: PMC1950464.
  • Fox B, Spiess P, Kasid A, Puri R, Mule J, Weber J, Rosenberg S. In vitro and in vivo antitumor properties of a T-cell clone generated from murine tumor-infiltrating lymphocytes. J Biol Response Mod. 1990 Oct.9(5):499-511. Pubmedid: 2174966 .
  • Fox BA, Spiess PJ, Kasid A, Puri R, Mulé JJ, Weber JS, Rosenberg SA. In vitro and in vivo antitumor properties of a T-cell clone generated from murine tumor-infiltrating lymphocytes. J Biol Response Mod. 1990 Oct.9(5):499-511. Pubmedid: 2174966.
  • Mulé JJ, McIntosh JK, Jablons DM, Rosenberg SA. Antitumor activity of recombinant interleukin 6 in mice. J Exp Med. 1990 Mar.171(3):629-636. Pubmedid: 2307930. Pmcid: PMC2187775.
  • McIntosh JK, Mulé JJ, Krosnick JA, Rosenberg SA. Combination cytokine immunotherapy with tumor necrosis factor alpha, interleukin 2, and alpha-interferon and its synergistic antitumor effects in mice. Cancer Res. 1989 Mar.49(6):1408-1414. Pubmedid: 2784349.
  • Jablons DM, Mulé JJ, McIntosh JK, Sehgal PB, May LT, Huang CM, Rosenberg SA, Lotze MT. IL-6/IFN-beta-2 as a circulating hormone. Induction by cytokine administration in humans. J Immunol. 1989 Mar.142(5):1542-1547. Pubmedid: 2783945.
  • McIntosh JK, Jablons DM, Mulé JJ, Nordan RP, Rudikoff S, Lotze MT, Rosenberg SA. In vivo induction of IL-6 by administration of exogenous cytokines and detection of de novo serum levels of IL-6 in tumor-bearing mice. J Immunol. 1989 Jul.143(1):162-167. Pubmedid: 2499626.
  • Krosnick JA, McIntosh JK, Mulé JJ, Rosenberg SA. Studies of the mechanisms of toxicity of the administration of recombinant tumor necrosis factor alpha in normal and tumor-bearing mice. Cancer Immunol Immun. 1989.30(3):133-138. Pubmedid: 2598182.
  • Asher AL, Mulé JJ, Rosenberg SA. Recombinant human tumor necrosis factor mediates regression of a murine sarcoma in vivo via Lyt-2+ cells. Cancer Immunol Immun. 1989.28(2):153-156. Pubmedid: 2783890.
  • Rosenberg SA, Lotze MT, Mulé JJ. NIH conference. New approaches to the immunotherapy of cancer using interleukin-2. Ann Intern Med. 1988 Jun.108(6):853-864. Pubmedid: 3285747.
  • Mulé JJ, Asher A, McIntosh J, Lafreniere R, Shiloni E, Lefor A, Reichert CM, Rosenberg SA. Antitumor effect of recombinant tumor necrosis factor-alpha against murine sarcomas at visceral sites: tumor size influences the response to therapy. Cancer Immunol Immun. 1988.26(3):202-208. Pubmedid: 3383204.
  • Mulé JJ, Schwarz SL, Roberts AB, Sporn MB, Rosenberg SA. Transforming growth factor-beta inhibits the in vitro generation of lymphokine-activated killer cells and cytotoxic T cells. Cancer Immunol Immun. 1988.26(2):95-100. Pubmedid: 2452015.
  • Mulé JJ, Smith CA, Rosenberg SA. Interleukin 4 (B cell stimulatory factor 1) can mediate the induction of lymphokine-activated killer cell activity directed against fresh tumor cells. J Exp Med. 1987 Sep.166(3):792-797. Pubmedid: 3498002. Pmcid: PMC2188702.
  • Papa MZ, Vetto JT, Ettinghausen SE, Mulé JJ, Rosenberg SA. Effect of corticosteroid on the antitumor activity of lymphokine-activated killer cells and interleukin 2 in mice. Cancer Res. 1986 Nov.46(11):5618-5623. Pubmedid: 3489525.
  • Mulé JJ, Yang J, Shu S, Rosenberg SA. The anti-tumor efficacy of lymphokine-activated killer cells and recombinant interleukin 2 in vivo: direct correlation between reduction of established metastases and cytolytic activity of lymphokine-activated killer cells. J Immunol. 1986 May.136(10):3899-3909. Pubmedid: 2871106.
  • Yang JC, Mulé JJ, Rosenberg SA. Murine lymphokine-activated killer (LAK) cells: phenotypic characterization of the precursor and effector cells. J Immunol. 1986 Jul.137(2):715-722. Pubmedid: 2873187.
  • Rosenberg SA, Mulé JJ, Spiess PJ, Reichert CM, Schwarz SL. Regression of established pulmonary metastases and subcutaneous tumor mediated by the systemic administration of high-dose recombinant interleukin 2. J Exp Med. 1985 May.161(5):1169-1188. Pubmedid: 3886826. Pmcid: PMC2187617.
  • Mulé JJ, Rosenstein M, Shu S, Rosenberg SA. Eradication of a disseminated syngeneic mouse lymphoma by systemic adoptive transfer of immune lymphocytes and its dependence upon a host component(s). Cancer Res. 1985 Feb.45(2):526-531. Pubmedid: 3881168.
  • Mulé JJ, Shu S, Schwarz SL, Rosenberg SA. Adoptive immunotherapy of established pulmonary metastases with LAK cells and recombinant interleukin-2. Science. 1984 Sep.225(4669):1487-1489. Pubmedid: 6332379.
  • Mulé JJ, Hellström I, Hellström KE. Cell surface phenotypes of radiolabeled immune long-lived lymphocytes that selectively localize in syngeneic tumours. Am J Pathol. 1982 May.107(2):142-149. Pubmedid: 7044130. Pmcid: PMC1916015.
  • Mulé JJ, Stanton TH, Hellström I, Hellström KE. Suppressor pathways in tumor immunity: a requirement for Qa-1 positive tumor-bearer spleen T cells in suppression of the afferent immune response to tumor antigens. Int J Cancer. 1981 Sep.28(3):353-359. Pubmedid: 6459294.
  • Mulé JJ, Forstrom JW, George E, Hellström I, Hellström KE. Production of T-cell lines with inhibitory or stimulatory activity against syngeneic tumors in vivo. A preliminary report. Int J Cancer. 1981 Nov.28(5):611-614. Pubmedid: 6796530.
  • Mulé JJ, Jones FR, Hellström I, Hellström KE. Selective localization of radiolabeled immune lymphocytes into syngeneic tumors. J Immunol. 1979 Aug.123(2):600-606. Pubmedid: 458150.
  • Pilon-Thomas S, Li W, Briggs J, Djeu J, Mule J, Riker A. Immunostimulatory effects of CpG-ODN upon dendritic cell-based immunotherapy in a murine melanoma model. J Immunother. 29(4):381-387. Pubmedid: 16799333.
  • Redman BG, Chang AE, Whitfield J, Esper P, Jiang G, Braun T, Roessler B, Mulé JJ. Phase Ib trial assessing autologous, tumor-pulsed dendritic cells as a vaccine administered with or without IL-2 in patients with metastatic melanoma. J Immunother. 31(6):591-598. Pubmedid: 18528294. Pmcid: PMC2642589.
  • Dubinett SM, Lee JM, Sharma S, Mulé JJ. Chemokines: can effector cells be redirected to the site of the tumor?. Cancer J. 16(4):325-335. Pubmedid: 20693843. Pmcid: PMC3076643.


Title: Exploiting the Immune Mapping of the Tumor Microenvironment to Improve Immunotherapy of Melanoma
Sponsor: Adelson (Miriam & Sheldon) Medical Res Fdtn
PI: Mulé, J.