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Article: Caspase-1 activates gasdermin A in non-mammals.

Billman, Zachary P / Kovacs, Stephen B / Wei, Bo / Kang, Kidong / Cissé, Ousmane H / Miao, Edward A

bioRxiv : the preprint server for biology

2024

Abstract: Gasdermins oligomerize to form pores in the cell membrane, causing regulated lytic cell death called pyroptosis. Mammals encode five gasdermins that can trigger pyroptosis: GSDMA, B, C, D, and E. Caspase and granzyme proteases cleave the linker regions ... ...

Abstract	Gasdermins oligomerize to form pores in the cell membrane, causing regulated lytic cell death called pyroptosis. Mammals encode five gasdermins that can trigger pyroptosis: GSDMA, B, C, D, and E. Caspase and granzyme proteases cleave the linker regions of and activate GSDMB, C, D, and E, but no endogenous activation pathways are yet known for GSDMA. Here, we perform a comprehensive evolutionary analysis of the gasdermin family. A gene duplication of GSDMA in the common ancestor of caecilian amphibians, reptiles and birds gave rise to GSDMA-D in mammals. Uniquely in our tree, amphibian, reptile and bird GSDMA group in a separate clade than mammal GSDMA. Remarkably, GSDMA in numerous bird species contain caspase-1 cleavage sites like YVAD or FASD in the linker. We show that GSDMA from birds, amphibians, and reptiles are all cleaved by caspase-1. Thus, GSDMA was originally cleaved by the host-encoded protease caspase-1. In mammals the caspase-1 cleavage site in GSDMA is disrupted; instead, a new protein, GSDMD, is the target of caspase-1. Mammal caspase-1 uses exosite interactions with the GSDMD C-terminal domain to confer the specificity of this interaction, whereas we show that bird caspase-1 uses a stereotypical tetrapeptide sequence to confer specificity for bird GSDMA. Our results reveal an evolutionarily stable association between caspase-1 and the gasdermin family, albeit a shifting one. Caspase-1 repeatedly changes its target gasdermin over evolutionary time at speciation junctures, initially cleaving GSDME in fish, then GSDMA in amphibians/reptiles/birds, and finally GSDMD in mammals.
Language	English
Publishing date	2024-01-03
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.28.559989
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Article ; Online: Overexpression of T3SS translocation signals in

Abele, Taylor J / Billman, Zachary P / Harvest, Carissa K / Bryan, Alexia K / Larson, Heather N / Coers, Jörn / Miao, Edward A

Infection and immunity

2023 Volume 92, Issue 1, Page(s) e0032923

Abstract: Engineering pathogens is a useful method for discovering new details of microbial pathogenesis and host defense. However, engineering can result in off-target effects. We previously ... ...

Abstract	Engineering pathogens is a useful method for discovering new details of microbial pathogenesis and host defense. However, engineering can result in off-target effects. We previously engineered
MeSH term(s)	Animals ; Mice ; Salmonella typhimurium ; Virulence ; Type III Secretion Systems/genetics ; Virulence Factors/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism
Chemical Substances	Type III Secretion Systems ; Virulence Factors ; Bacterial Proteins
Language	English
Publishing date	2023-12-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	218698-6
ISSN	1098-5522 ; 0019-9567
ISSN (online)	1098-5522
ISSN	0019-9567
DOI	10.1128/iai.00329-23
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Article: Apoptotic signaling clears engineered

Abele, Taylor J / Billman, Zachary P / Li, Lupeng / Harvest, Carissa K / Bryan, Alexia K / Magalski, Gabrielle R / Lopez, Joseph P / Larson, Heather N / Yin, Xiao-Ming / Miao, Edward A

bioRxiv : the preprint server for biology

2023

Abstract: Pyroptosis and apoptosis are two forms of regulated cell death that can defend against intracellular infection. Although pyroptosis and apoptosis have distinct signaling pathways, when a cell fails to complete pyroptosis, backup pathways will initiate ... ...

Abstract	Pyroptosis and apoptosis are two forms of regulated cell death that can defend against intracellular infection. Although pyroptosis and apoptosis have distinct signaling pathways, when a cell fails to complete pyroptosis, backup pathways will initiate apoptosis. Here, we investigated the utility of apoptosis compared to pyroptosis in defense against an intracellular bacterial infection. We previously engineered
Language	English
Publishing date	2023-08-19
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.06.539681
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Article ; Online: Apoptotic signaling clears engineered

Abele, Taylor J / Billman, Zachary P / Li, Lupeng / Harvest, Carissa K / Bryan, Alexia K / Magalski, Gabrielle R / Lopez, Joseph P / Larson, Heather N / Yin, Xiao-Ming / Miao, Edward A

eLife

2023 Volume 12

Abstract: Pyroptosis and apoptosis are two forms of regulated cell death that can defend against intracellular infection. When a cell fails to complete pyroptosis, backup pathways will initiate apoptosis. Here, we investigated the utility of apoptosis compared to ... ...

Abstract	Pyroptosis and apoptosis are two forms of regulated cell death that can defend against intracellular infection. When a cell fails to complete pyroptosis, backup pathways will initiate apoptosis. Here, we investigated the utility of apoptosis compared to pyroptosis in defense against an intracellular bacterial infection. We previously engineered
MeSH term(s)	Animals ; Mice ; Flagellin ; Apoptosis ; Cell Death ; Caspase 1/metabolism ; Salmonella typhimurium/genetics ; Salmonella typhimurium/metabolism ; Pyroptosis ; Inflammasomes/metabolism
Chemical Substances	Flagellin (12777-81-0) ; Caspase 1 (EC 3.4.22.36) ; Inflammasomes
Language	English
Publishing date	2023-12-06
Publishing country	England
Document type	Journal Article
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.89210
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Article ; Online: Purification of Plasmodium Sporozoites Enhances Parasite-Specific CD8+ T Cell Responses.

Billman, Zachary P / Seilie, Annette M / Murphy, Sean C

Infection and immunity

2016 Volume 84, Issue 8, Page(s) 2233–2242

Abstract: Malaria infection caused by Plasmodium parasites continues to cause enormous morbidity and mortality in areas where it is endemic, and there is no licensed vaccine capable of inducing sterile protection. Hyperimmunization with attenuated whole ... ...

Abstract	Malaria infection caused by Plasmodium parasites continues to cause enormous morbidity and mortality in areas where it is endemic, and there is no licensed vaccine capable of inducing sterile protection. Hyperimmunization with attenuated whole sporozoites can induce sterile protective immune responses targeting preerythrocytic antigens. Most animal models of hyperimmunization rely on sporozoites dissected from mosquito salivary glands and injected without further purification. In BALB/c mice, repeated small doses of P. yoelii sporozoites progressively expand the population of sporozoite-specific CD8(+) T cells. In this study, large secondary doses of unpurified sporozoites unexpectedly led to contraction of sporozoite-specific CD8(+) T cell responses in sporozoite-primed mice. While sporozoite-primed CD8(+) T cells alternatively can be expanded by secondary exposure to Listeria monocytogenes expressing recombinant Plasmodium antigens, such expansion was potently inhibited by coinjection of large doses of unpurified sporozoites and by uninfected salivary glands alone. Purification of sporozoites away from mosquito salivary gland debris by density gradient centrifugation eliminated salivary gland-associated inhibition. Thus, the inhibitory effect appears to be due to exposure to uninfected mosquito salivary glands rather than sporozoites. To further assess the effect of salivary gland exposure on later sporozoite vaccinations, mice were immunized with uninfected salivary glands from a single mosquito. Compared to naive mice, salivary gland presensitization reduced subsequent liver burdens by 71%. These data show that a component(s) in mosquito salivary glands reduces liver infection, thereby limiting antigen dose and contributing to lower-magnitude T cell responses. These findings suggest that sporozoite immunogenicity studies be performed using purified sporozoites whenever feasible.
MeSH term(s)	Animals ; CD8-Positive T-Lymphocytes/immunology ; Disease Models, Animal ; Epitopes, T-Lymphocyte/immunology ; Female ; Immunization ; Malaria/immunology ; Malaria/parasitology ; Malaria Vaccines/immunology ; Mice ; Plasmodium/immunology ; Sporozoites/immunology
Chemical Substances	Epitopes, T-Lymphocyte ; Malaria Vaccines
Language	English
Publishing date	2016-07-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	218698-6
ISSN	1098-5522 ; 0019-9567
ISSN (online)	1098-5522
ISSN	0019-9567
DOI	10.1128/IAI.01439-15
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Article ; Online: An innate granuloma eradicates an environmental pathogen using Gsdmd and Nos2.

Harvest, Carissa K / Abele, Taylor J / Yu, Chen / Beatty, Cole J / Amason, Megan E / Billman, Zachary P / DePrizio, Morgan A / Souza, Fernando W / Lacey, Carolyn A / Maltez, Vivien I / Larson, Heather N / McGlaughon, Benjamin D / Saban, Daniel R / Montgomery, Stephanie A / Miao, Edward A

Nature communications

2023 Volume 14, Issue 1, Page(s) 6686

Abstract: Granulomas often form around pathogens that cause chronic infections. Here, we discover an innate granuloma model in mice with an environmental bacterium called Chromobacterium violaceum. Granuloma formation not only successfully walls off, but also ... ...

Abstract	Granulomas often form around pathogens that cause chronic infections. Here, we discover an innate granuloma model in mice with an environmental bacterium called Chromobacterium violaceum. Granuloma formation not only successfully walls off, but also clears, the infection. The infected lesion can arise from a single bacterium that replicates despite the presence of a neutrophil swarm. Bacterial replication ceases when macrophages organize around the infection and form a granuloma. This granuloma response is accomplished independently of adaptive immunity that is typically required to organize granulomas. The C. violaceum-induced granuloma requires at least two separate defense pathways, gasdermin D and iNOS, to maintain the integrity of the granuloma architecture. This innate granuloma successfully eradicates C. violaceum infection. Therefore, this C. violaceum-induced granuloma model demonstrates that innate immune cells successfully organize a granuloma and thereby resolve infection by an environmental pathogen.
MeSH term(s)	Animals ; Mice ; Granuloma ; Macrophages/metabolism ; Neutrophils ; Nitric Oxide Synthase Type II/metabolism
Chemical Substances	Nitric Oxide Synthase Type II (EC 1.14.13.39) ; Nos2 protein, mouse (EC 1.14.13.39) ; Gsdmd protein, mouse
Language	English
Publishing date	2023-10-21
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-42218-1
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Article ; Online: More time to kill: A longer liver stage increases T cell-mediated protection against pre-erythrocytic malaria.

Yadav, Naveen / Parthiban, Chaitra / Billman, Zachary P / Stone, Brad C / Watson, Felicia N / Zhou, Kevin / Olsen, Tayla M / Cruz Talavera, Irene / Seilie, Annette Mariko / Kalata, Anya C / Matsubara, Jokichi / Shears, Melanie J / Reynolds, Rebekah A / Murphy, Sean C

iScience

2023 Volume 26, Issue 12, Page(s) 108489

Abstract: Liver stage (LS) Plasmodia mature in 2-2.5 days in rodents compared to 5-6 days in humans. ...

Abstract	Liver stage (LS) Plasmodia mature in 2-2.5 days in rodents compared to 5-6 days in humans.
Language	English
Publishing date	2023-11-20
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2023.108489
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Article: An innate granuloma eradicates an environmental pathogen using

Harvest, Carissa K / Abele, Taylor J / Yu, Chen / Beatty, Cole J / Amason, Megan E / Billman, Zachary P / DePrizio, Morgan A / Lacey, Carolyn A / Maltez, Vivien I / Larson, Heather N / McGlaughon, Benjamin D / Saban, Daniel R / Montgomery, Stephanie A / Miao, Edward A

bioRxiv : the preprint server for biology

2023

Abstract: Granulomas often form around pathogens that cause chronic infections. Here, we discover a novel granuloma model in mice. ...

Abstract	Granulomas often form around pathogens that cause chronic infections. Here, we discover a novel granuloma model in mice.
Language	English
Publishing date	2023-03-09
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.07.531568
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Article ; Online: Defining rules of CD8(+) T cell expansion against pre-erythrocytic Plasmodium antigens in sporozoite-immunized mice.

Billman, Zachary P / Kas, Arnold / Stone, Brad C / Murphy, Sean C

Malaria journal

2016 Volume 15, Page(s) 238

Abstract: Background: Whole Plasmodium sporozoites serve as both experimental tools and potentially as deployable vaccines in the fight against malaria infection. Live sporozoites infect hepatocytes and induce a diverse repertoire of CD8(+) T cell responses, some ...

Abstract	Background: Whole Plasmodium sporozoites serve as both experimental tools and potentially as deployable vaccines in the fight against malaria infection. Live sporozoites infect hepatocytes and induce a diverse repertoire of CD8(+) T cell responses, some of which are capable of killing Plasmodium-infected hepatocytes. Previous studies in Plasmodium yoelii-immunized BALB/c mice showed that some CD8(+) T cell responses expanded with repeated parasite exposure, whereas other responses did not. Results: Here, similar outcomes were observed using known Plasmodium berghei epitopes in C57BL/6 mice. With the exception of the response to PbTRAP, IFNγ-producing T cell responses to most studied antigens, such as PbGAP50, failed to re-expand in mice immunized with two doses of irradiated P. berghei sporozoites. In an effort to boost secondary CD8(+) T cell responses, heterologous cross-species immunizations were performed. Alignment of P. yoelii 17XNL and P. berghei ANKA proteins revealed that >60 % of the amino acids in syntenic orthologous proteins are continuously homologous in fragments ≥8-amino acids long, suggesting that cross-species immunization could potentially trigger responses to a large number of common Class I epitopes. Heterologous immunization resulted in a larger liver burden than homologous immunization. Amongst seven tested antigen-specific responses, only CSP- and TRAP-specific CD8(+) T cell responses were expanded by secondary homologous sporozoite immunization and only those to the L3 ribosomal protein and S20 could be re-expanded by heterologous immunization. In general, heterologous late-arresting, genetically attenuated sporozoites were better at secondarily expanding L3-specific responses than were irradiated sporozoites. GAP50 and several other antigens shared between P. berghei and P. yoelii induced a large number of IFNγ-positive T cells during primary immunization, yet these responses could not be re-expanded by either homologous or heterologous secondary immunization. Conclusions: These studies highlight how responses to different sporozoite antigens can markedly differ in recall following repeated sporozoite vaccinations. Cross-species immunization broadens the secondary response to sporozoites and may represent a novel strategy for candidate antigen discovery.
MeSH term(s)	Animals ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/parasitology ; Enzyme-Linked Immunosorbent Assay ; Epitopes/immunology ; Female ; Malaria Vaccines/immunology ; Mice ; Mice, Inbred C57BL ; Plasmodium berghei/immunology ; Plasmodium yoelii/immunology ; Protozoan Proteins/immunology ; Protozoan Proteins/metabolism ; Sequence Analysis, DNA ; Sporozoites/immunology
Chemical Substances	Epitopes ; Malaria Vaccines ; Protozoan Proteins ; circumsporozoite protein, Protozoan
Language	English
Publishing date	2016-04-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1475-2875
ISSN (online)	1475-2875
DOI	10.1186/s12936-016-1295-5
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Plasmodium vivax

Flannery, Erika L / Kangwanrangsan, Niwat / Chuenchob, Vorada / Roobsoong, Wanlapa / Fishbaugher, Matthew / Zhou, Kevin / Billman, Zachary P / Martinson, Thomas / Olsen, Tayla M / Schäfer, Carola / Campo, Brice / Murphy, Sean C / Mikolajczak, Sebastian A / Kappe, Stefan H I / Sattabongkot, Jetsumon

Molecular therapy. Methods & clinical development

2022 Volume 26, Page(s) 427–440

Abstract: Plasmodium ... ...

Abstract	Plasmodium vivax
Language	English
Publishing date	2022-08-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	2872938-9
ISSN	2329-0501 ; 2329-0501
ISSN (online)	2329-0501
ISSN	2329-0501
DOI	10.1016/j.omtm.2022.07.016
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