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Elucidating the Roles of Il-15 in the Tumor Microenvironment

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Elucidating the Roles of Il-15 in the Tumor Microenvironment The Texas Medical Center Library DigitalCommons@TMC The University of Texas MD Anderson Cancer Center UTHealth Graduate School of The University of Texas MD Anderson Cancer Biomedical Sciences Dissertations and Theses Center UTHealth Graduate School of (Open Access) Biomedical Sciences 12-2020 ELUCIDATING THE ROLES OF IL-15 IN THE TUMOR MICROENVIRONMENT Rosa Maria Santana Carrero Follow this and additional works at: https://digitalcommons.library.tmc.edu/utgsbs_dissertations Part of the Immunity Commons, Immunotherapy Commons, and the Medicine and Health Sciences Commons Recommended Citation Santana Carrero, Rosa Maria, "ELUCIDATING THE ROLES OF IL-15 IN THE TUMOR MICROENVIRONMENT" (2020). The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences Dissertations and Theses (Open Access). 1057. https://digitalcommons.library.tmc.edu/utgsbs_dissertations/1057 This Dissertation (PhD) is brought to you for free and open access by the The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences at DigitalCommons@TMC. It has been accepted for inclusion in The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences Dissertations and Theses (Open Access) by an authorized administrator of DigitalCommons@TMC. For more information, please contact [email protected]. ELUCIDATING THE ROLES OF IL-15 IN THE TUMOR MICROENVIRONMENT by Rosa M. Santana Carrero, B.S. APPROVED: Shao-Cong Sun , Ph.D. Advisory Professor Kimberly S. Schlu~s, Ph.D. ~,Ph.D. ia cAllister, M.D. WH Jagannadha Sastry, Ph.D. Joya Chandra, Ph .D. APPROVED: Dean, The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences ELUCIDATING THE ROLES OF IL-15 IN THE TUMOR MICROENVIRONMENT A DISSERTATION Presented to the Faculty of The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY by Rosa M. Santana Carrero, B.S. Houston, Texas December, 2020 ACKNOWLEDGEMENTS I would first like to thank my family and loved ones for the unconditional love and support that they have shown me throughout my life, but especially as I embarked on my graduate school journey. A special and most deserved mention to my husband, Cristian, who has been my rock, protector and counselor through this incredible experience. Thank you, my love, for taking the risk of moving away from all our friends and family to take on the challenge of starting new careers and starting over in a new city. Your strength and kindness have helped me thrive and overcome all the obstacles that come with having a career in science and being an almost perpetual student. As I am closing this chapter as a graduate student, we are undertaking new challenges as a family to ensure that we grow in love and as professionals. I can’t imagine sharing this journey with anybody else. I would also like to thank my parents for the support they have provided, including listening to me talk incessantly about my research and discussing difficult biological concepts. They have provided wisdom to overcome the obstacles and challenges that I have faced, and they have cheered me on when I achieved new milestones in my career. Thank you Mami and Papi for teaching me perseverance and to never give up on my dreams. Most importantly, thank you for teaching me that, as long as I give it my very best effort the outcomes don’t really make much of a difference, because the lessons learned will provide more than enough compensation. I would also like to thank my mentor Dr. Kimberly Schluns for all the guidance and advice that she has provided me along my time in her lab. Kim, thank you for being supportive but firm as my advisor and my colleague. I have learned that true leadership is achieved by setting an example and executing every day to ensure we live up to that iii standard. Moreover, thank you for your support as I dared to take on responsibilities outside of lab and thank you for keeping me in check when I was veering off track. You have been the best mentor that I could have asked for, and I wish you all the best in your new endeavors. Other important people that I would like to thank are the current and past members of the Schluns’ lab for making my long days in lab more enjoyable. I would especially like to mention Shweta Hegde, because you have been an amazing co- worker and friend. Thank you, Shweta, for always lending a hand during the long days of tumor experiments and for always listening to me talk about food, my dogs, my family and all the happenings at the graduate school. Your loving and open spirit have made you one of my favorite people to be around. I will miss you so much, but I hope to maintain our friendship through the distance and through the years. I would like to acknowledge my advisory committee members and the administrative staff at the GSBS for playing important roles as advisors and problem solvers during my time as a graduate student. Lastly, I would like to thank all my friends in Houston and at the GSBS for sharing amazing moments and memories throughout these past 5 years. You all made Houston my home, and I will always carry our memories together in my heart. iv ELUCIDATING THE ROLES OF IL-15 IN THE TUMOR MICROENVIRONMENT Rosa M. Santana Carrero, B.S. Advisory Professors: Shao-Cong Sun, Ph.D. & Kimberly S. Schluns, Ph.D. Interleukin-15 (IL-15) is a factor that promotes activation, proliferation, cytotoxicity, and survival of CD8 T cells and NK cells, and has been shown to have anti-tumor effects. Moreover, loss of IL-15 expression in human colorectal tumors correlates with increased risk of relapse, diminished survival, decreased density and proliferation of T cells. All together these findings suggest that IL-15 expressed locally in the tumor microenvironment (TME) is an important mediator of anti-tumor responses by tumor infiltrating lymphocytes (TILs) representing a potentially powerful immunotherapeutic target. Unfortunately, the regulation and roles of IL-15 within the TME is unclear. I hypothesized that IL-15 produced in the TME is an important factor promoting anti- tumor responses by cytotoxic lymphocytes stimulating their optimal numbers, enhancing their effector functions and metabolic fitness. In this dissertation I investigated the cellular sources and regulation of IL-15 in the TME and its roles in enhancing anti-tumor immunity. I showed, using several murine tumor models, that soluble IL-15/IL- 15R complexes (sIL-15 complexes) are present at high levels in the interstitial fluid of early tumors and decrease with tumor growth. Depletion of local IL -15 in tumors led to decreased numbers of TILs without directly affecting tumor growth, likely by promoting their infiltration into tumors. I also found that levels of sIL-15 complexes could be upregulated in advanced tumors by local activation of the Stimulator v of Interferon Genes (STING) pathway. While treatment of tumors with STING agonists induces tumor regression, optimal STING-mediated systemic anti- tumor immunity required IL-15 expression. In addition, I examined the direct effect of IL-15 agonists in poorly T-cell infiltrated tumors and found that recombinant sIL-15/IL- 15R-Fc complexes (rsIL-15c) and a polymer-conjugated IL-15R agonist significantly slowed tumor growth and increased the total numbers of TILs. Moreover, intratumoral IL- 15 agonists in combination with anti-CTLA-4 immune checkpoint blockade synergistically induced better tumor growth control and enhanced mouse survival in a poorly infiltrated melanoma tumor model. These findings reveal the ability of IL-15 expressed within the TME to regulate TIL numbers and upon upregulation by inflammatory signals, contribute to enhanced anti-tumor responses. vi TABLE OF CONTENTS APPROVAL PAGE ................................................................................................... I TITLE PAGE .......................................................................................................... II ACKNOWLEDGEMENTS ......................................................................................... III ABSTRACT ........................................................................................................... V TABLE OF CONTENTS .......................................................................................... VII LIST OF FIGURES .................................................................................................. X CHAPTER 1: INTRODUCTION ....................................................................... 1-57 1.1 TUMOR MICROENVIRONMENT .......................................................................... 2 1.1.1 Detection of tumors by the immune system ........................................... 3 1.1.2 Composition of the tumor microenvironment ......................................... 5 1.1.3 Mechanisms of evasion and suppression of anti-tumor immunity ....... 15 1.2 TYPE I INTERFERONS IN CANCER ................................................................... 19 1.2.1 IFN-I signaling ...................................................................................... 19 1.2.2 IFN-I roles in cancer immunoediting .................................................... 21 1.2.3 Anti-metastatic and immunostimulatory effects of IFN-I ....................... 23 1.2.4 IFN-I therapy in cancer .......................................................................
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