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Blood Cells of Adult Drosophila Do Not Expand, But Control Survival after Bacterial Infection by Induction of Drosocin Around Their Reservoir at the Respiratory Epithelia

69 Pages Posted: 2 Apr 2019 Sneak Peek Status: Review Complete

See all articles by Pablo Sanchez Bosch

Pablo Sanchez Bosch

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Kalpana Makhijani

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Leire Herboso

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Katrina S. Gold

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Rowan Baginsky

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Katie J. Woodcock

King's College London

Brandy Alexander

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Katelyn Kukar

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Sean Corcoran

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Debra Ouyang

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Corinna Wong

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

Elodie JV Ramond

Ecole Polytechnique Fédérale de Lausanne

Christa Rhiner

Champalimaud Center for the Unknown

Eduardo Moreno

Champalimaud Center for the Unknown

Bruno Lemaitre

Ecole Polytechnique Fédérale de Lausanne

Frederic Geissmann

King's College London; Memorial Sloan Kettering Cancer Center

Katja Brückner

Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research; University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology; University of California, San Francisco (UCSF) - Cardiovascular Research Institute

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Abstract

Drosophila melanogaster has been an excellent model for innate immunity, but the role and regulation of adult blood cells and organismal immunity have remained incompletely understood. Here we address these questions in a comprehensive investigation of the blood cell system in adult Drosophila. As a central finding, we reveal the largest reservoir of blood cells (hemocytes) at the respiratory epithelia (tracheal air sacs) and fat body of the thorax and head. We show that most hemocytes of adult Drosophila are phagocytic macrophages (plasmatocytes), derived by more than 60% from the embryonic lineage that parallels vertebrate tissue macrophages. Surprisingly, in contrast to hemocytes at the larval stage, we find no capacity of the adult blood cell system to expand. Instead, we demonstrate its central role in relaying an innate immune response to tissues surrounding the blood cell reservoir: Hemocytes, through Imd signaling and the Jak/Stat pathway ligand Upd3, act as sentinels of bacterial infection that induce expression of the antimicrobial peptide gene Drosocin in the respiratory epithelia and colocalizing domains of the fat body. We demonstrate that endogenous Drosocin expression in these tissues promotes animal survival after bacterial infection. Our work identifies the first molecular step in a new relay of organismal immunity, establishing adult Drosophila as model to dissect mechanisms of inter-organ immunity.

Keywords: Drosophila melanogaster, hemocyte, macrophage, innate immunity, local humoral immune response, antimicrobial peptide, Drosocin, NFκB, imd, Jak/Stat, upd3, respiratory epithelia, tracheal air sacs, fat body, hematopoiesis

Suggested Citation

Bosch, Pablo Sanchez and Makhijani, Kalpana and Herboso, Leire and Gold, Katrina S. and Baginsky, Rowan and Woodcock, Katie J. and Alexander, Brandy and Kukar, Katelyn and Corcoran, Sean and Ouyang, Debra and Wong, Corinna and Ramond, Elodie JV and Rhiner, Christa and Moreno, Eduardo and Lemaitre, Bruno and Geissmann, Frederic and Brückner, Katja, Blood Cells of Adult Drosophila Do Not Expand, But Control Survival after Bacterial Infection by Induction of Drosocin Around Their Reservoir at the Respiratory Epithelia (April 1, 2019). Available at SSRN: https://ssrn.com/abstract=3363774 or http://dx.doi.org/10.2139/ssrn.3363774
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Pablo Sanchez Bosch (Contact Author)

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Kalpana Makhijani

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Leire Herboso

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Katrina S. Gold

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Rowan Baginsky

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Katie J. Woodcock

King's College London

Strand
London, England WC2R 2LS
United Kingdom

Brandy Alexander

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Katelyn Kukar

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Sean Corcoran

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Debra Ouyang

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Corinna Wong

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology

San Francisco, CA
United States

Elodie JV Ramond

Ecole Polytechnique Fédérale de Lausanne

Station 5
Odyssea 1.04
1015 Lausanne, CH-1015
Switzerland

Christa Rhiner

Champalimaud Center for the Unknown

Avenida Brasília
Lisboa, 1400-038
Portugal

Eduardo Moreno

Champalimaud Center for the Unknown

Avenida Brasília
Lisboa, 1400-038
Portugal

Bruno Lemaitre

Ecole Polytechnique Fédérale de Lausanne

Station 5
Odyssea 1.04
1015 Lausanne, CH-1015
Switzerland

Frederic Geissmann

King's College London

Strand
London, England WC2R 2LS
United Kingdom

Memorial Sloan Kettering Cancer Center

New York, NY 10065
United States

Katja Brückner

Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research ( email )

615 Charles E Young Dr. S.
Los Angeles, CA 90095
United States

University of California, San Francisco (UCSF) - Department of Cell and Tissue Biology ( email )

San Francisco, CA
United States

University of California, San Francisco (UCSF) - Cardiovascular Research Institute ( email )

555 Mission Bay Boulevard South
San Francisco, CA 94158
United States

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