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SABRE Annual Report 2021

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Sandler Asthma Basic REsearch Center University of California, San Francisco Progress Report Year 22 July 2021 Figure Legend: Multi-detector computed tomography (MCTD) lung scan of a patient with poorly controlled asthma revealed occlusive mucus plugs of varying size and shape, which has been shown to correlate with worse lung function (technique developed and refined in the Fahy SABRE Center lab with UCSF Radiology). Therapeutic dissolution of plugs remains a priority in the Fahy lab. (Image contributed by Brendan Huang). TABLE OF CONTENTS Mission Statement 2 Summary of Accomplishments Overview 3 Executive Committee: Members and Functions 24 Scientific Advisory Board Susan Kaech, Ph.D. 26 Mitchell Kronenberg, Ph.D. 27 Ruslan Medzhitov, Ph.D. 28 SABRE Center Investigators Richard Locksley, M.D. 30 Christopher Allen, Ph.D. 32 K. Mark Ansel, Ph.D. 34 Esteban Burchard, M.D., M.P.H. 36 John Fahy, M.D., M.Sc. 38 Jeoung-Sook Shin, Ph.D. 40 Prescott Woodruff, M.D., M.P.H. 42 SABRE Associate Investigators Mallar Bhattacharya, M.D., MSc. 45 Erin Gordon, M.D. 47 Andrew Schroeder, M.P.H. 49 Aparna Sundaram, M.D. 50 Core Facilities Microscopy/BIDC 53 Asthma Related Research Projects Primero Birth Cohort 60 Single Cell Sequencing in Nasal Polyp Patients 70 Contributions to Relevant Scientific Activities 74 Publications Supported by the Sandler Asthma Basic Research Center 79 Looking to the future 136 Biographical Sketches 138 Mission Statement The Sandler Asthma Basic Research Center (SABRE Center) is an investigative unit dedicated to basic research discovery in asthma. Founded in 1999, the SABRE Center is nucleated by basic scientists supported by advanced technology cores and linked with the greater scientific community through Center Grants and Program Projects focused around asthma research. The SABRE Center aligned in 2014 with the Airway Clinical Research Center (ACRC) at UCSF to facilitate increased focus on and integration with asthma patient studies. Our mission remains to be a progressive, nimble, transformative scientific group that pioneers basic discovery in asthma research, a platform made possible by the generous support of the Sandler Foundation. Summary of Accomplishments over the Past Year The past year has imposed unprecedented difficulties on academic life, research and the health care system. SABRE labs were shuttered in March, 2020, and only achieved 75% occupancy with spacing in late May, 2021. Animal breeding, sequencing studies, core activities, in-person conferences and seminars were suspended to minimize human contact and to redirect resources to COVID-19-related activities, generating opportunity that could only be met by the flexibility provided through SABRE funding. Thus, SABRE Center investigators could continue to make contributions to the understanding of asthma and allergic disease, while pivoting to address the impact on COVID-19 on patients with asthma, an emphasis that continues with the ongoing pandemic. Notable accomplishments from SABRE Center members since the prior Report: (1) The COMET consortium was mobilized quickly to confront the pandemic and organized by Prescott Woodruff, David Erle, Mark Ansel, John Fahy and others on the Leadership team to rapidly phenotype COVID patients for immune studies to uncover mechanisms driving severe disease. Key findings included dysregulated anti-viral interferon pathways mediated by aberrant autoantibodies that interfere with immune control and active neutrophils that foment tissue damage, creating strategies for intervention. Of note, patients with asthma were relatively protected from severe disease. (2) Despite the pandemic, Esteban Burchard continued to enroll mother-infant pairs in the NIH-awarded PRIMERO study to follow asthma development in a prospective cohort of 3000 mother-newborn pairs in Puerto Rico, where the prevalence and severity of asthma are among the highest in the world, promising a rich dataset already being leveraged to additional SABRE investigators with collaborative grants in progress. (3) The Locksley lab leveraged SABRE-targeted single-cell RNA sequencing efforts to contribute to studies identifying ILC2 precursors in tissues and to define the trajectories by which these cells become pathologic during inflammatory and allergic reactions in the skin and lung. (4) The Allen lab discovered the role of IL-21 in inhibiting IgE class switch recombination in mouse and human B cells, and the Shin lab continued to probe the role of MARCH1 regulation in dendritic cells and its contributions to allergic T cell differentiation. 2 Overview – 2021 Richard M. Locksley, M.D. The SABRE Center continues with its discovery-oriented mission towards deeper understanding of asthma that will guide innovative therapeutics. Comprised of four basic scientists, a population geneticist, two pulmonary basic/translational scientists, a bioinformatics specialist, and young associate members, the Center has networked across the greater UCSF research and national research organizations to establish increasing recognition for contributions to asthma research. The onset of the COVID-19 pandemic in late February began an unprecedented disruption of American society, including research, with non-essential research and clinical research activities suspended at UCSF in March, 2020. Efforts were made to pivot to COVID-19-related activities, as permitted at 25% effort, and here the flexibility of SABRE support allowed a number of labs to move quickly to assess interactions between the virus, lung tissues, and among patients with asthma. These activities became unified to form COMET, a spontaneous integration of scientists across disciplines with clinicians to bring cutting-edge technologies to bear on understanding this new infectious disease. Boosted by our early commitment to single-cell RNAseq and related platforms, SABRE labs were able to contribute quickly to studies of viral receptors, cell phenotypes and transcriptomic signatures among patients, including those with airways disease, and these studies continue. With the successful rollout of vaccines, labs expanded to 50% occupancy in late 2020 and to 75% capacity in late May, 2021, although still with spacing and masking. With essentially 100% vaccination rates, we anticipate complete opening by July. Clinical research activities were impacted most due to necessity to stop all patient visits except those related to COVID or dangers to health. Planned scientific conferences, including the 2020 Keystone Symposium on Asthma Immunobiology by the former American Asthma Foundation Scientific Board assembled by the Sandler Foundation to be held in Utah, and the 4th International Conference on Innate Lymphoid Cells to be held in San Francisco were postponed until 2022. Investigators The SABRE Center consists of the Director, Dr. Locksley; core basic science faculty - Drs. Allen, Ansel, and Shin; and core translational scientists - Drs. Fahy and Woodruff, who direct the Airway Clinical Research Center (ACRC) at Parnassus, and Dr. Burchard, who directs the Asthma Collaboratory Genetics Consortium at the Mission Bay campus. Dr. Hal Chapman, whose interests in lung fibrosis and inflammation complement those of investigators in the SABRE Center, works in contiguous space with the core SABRE laboratories and is a member of the Executive Board. Associate Investigators with active laboratories on the SABRE Center floor include Drs. Erin Gordon, Mallar Bhattacharya, and Apurna Sundaram, who engage in collaborative work with SABRE investigators in addition to their primary research in aspects of lung biology, asthma, and inflammation. 3 Last year we hired a Bioinformatics Specialist, Andrew Schroeder, MPH, to help with large datasets and the need for novel analytic tools generated by next-gen sequencing efforts. Their CVs are included in this report. The SABRE Center is integrated with the Airway Clinical Research Center (ACRC) under the leadership of Dr. John Fahy and Dr. Prescott Woodruff. SABRE investigators share quarterly lab and research meetings, and attend monthly research conferences that also include outside guest investigators. The fruits of this collaborative effort resulted in an NIH Program Project Grant awarded to SABRE investigators in 2012, with a major focus centered on human patients and tissues as organized through the ACRC. The competitive renewal was renewed in 2019 for an additional 5 years, one of the few Program Projects elected for continued funding by the National Heart, Lung and Blood Institutes of the NIH. The SABRE Center remains an active research constituent on the UCSF campus with a role in generating new basic understanding with potential therapeutic approaches to asthma. Despite the pandemic, over 75 manuscripts were published over the last 2 years, many in high-impact journals, emphasizing the productive output of this collaborative Center. We briefly review the Core Principal investigators and their progress, followed by an overview of the components of the Center, a brief discussion of achievements and finally a listing of extramural grants and other resources that have been obtained to support these activities. Chris Allen, Ph.D., joined the SABRE center thirteen years ago as a UCSF Fellow. He was the first member of the UCSF Sandler Fellows Program (http://fellows.ucsf.edu/) who was selected to work on a specific human disease, in this case, asthma. This program enabled Dr. Allen to develop an independent research program combining his skills in cellular and molecular immunology with
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