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Article ; Online: Expression of sex-specific molecular markers by Babesia bovis gametes.

Hussein, Hala E / Johnson, Wendell C / Taus, Naomi S / Ueti, Massaro W

2024 Volume 17, Issue 1, Page(s) 75

Abstract: Background: Bovine babesiosis caused by Babesia bovis is one of the most important tick-borne diseases of cattle in tropical and subtropical regions. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and ... ...

Abstract	Background: Bovine babesiosis caused by Babesia bovis is one of the most important tick-borne diseases of cattle in tropical and subtropical regions. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. In the tick midgut, extracellular Babesia parasites transform into gametes that fuse to form zygotes. To date, little is known about genes and proteins expressed by male gametes. Methods and results: We developed a method to separate male gametes from in vitro induced B. bovis culture. Separation enabled the validation of sex-specific markers. Collected male gametocytes were observed by Giemsa-stained smear and live-cell fluorescence microscopy. Babesia male gametes were used to confirm sex-specific markers by quantitative real-time PCR. Some genes were found to be male gamete specific genes including pka, hap2, α-tubulin II and znfp2. However, α-tubulin I and ABC transporter, trap2-4 and ccp1-3 genes were found to be upregulated in culture depleted of male gametes (female-enriched). Live immunofluorescence analysis using polyclonal antibodies confirmed surface expression of HAP2 by male and TRAP2-4 by female gametes. These results revealed strong markers to distinguish between B. bovis male and female gametes. Conclusions: Herein, we describe the identification of sex-specific molecular markers essential for B. bovis sexual reproduction. These tools will enhance our understanding of the biology of sexual stages and, consequently, the development of additional strategies to control bovine babesiosis.
MeSH term(s)	Cattle ; Female ; Male ; Animals ; Babesia bovis/genetics ; Babesiosis/parasitology ; Tubulin ; Babesia/genetics ; Ticks/parasitology ; Biomarkers ; Germ Cells ; Cattle Diseases/diagnosis ; Cattle Diseases/parasitology ; Mammals
Chemical Substances	Tubulin ; Biomarkers
Language	English
Publishing date	2024-02-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2409480-8
ISSN	1756-3305 ; 1756-3305
ISSN (online)	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-024-06185-w
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Identification of novel immune correlates of protection against acute bovine babesiosis by superinfecting cattle with

Bastos, Reginaldo G / Laughery, Jacob M / Ozubek, Sezayi / Alzan, Heba F / Taus, Naomi S / Ueti, Massaro W / Suarez, Carlos E

Frontiers in immunology

2022 Volume 13, Page(s) 1045608

Abstract: The apicomplexan tickborne ... ...

Abstract	The apicomplexan tickborne parasites
MeSH term(s)	Cattle ; Animals ; Babesia bovis ; Babesiosis/prevention & control ; Vaccination ; Cytokines ; Neutropenia ; Blood Group Antigens
Chemical Substances	Cytokines ; Blood Group Antigens
Language	English
Publishing date	2022-11-18
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.1045608
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Article: A Transfected

Johnson, Wendell C / Hussein, Hala E / Capelli-Peixoto, Janaina / Laughery, Jacob M / Taus, Naomi S / Suarez, Carlos E / Ueti, Massaro W

Pathogens (Basel, Switzerland)

2022 Volume 11, Issue 6

Abstract: Bovine babesiosis is caused by apicomplexan pathogens of the ... ...

Abstract	Bovine babesiosis is caused by apicomplexan pathogens of the genus
Language	English
Publishing date	2022-05-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens11060623
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Article: A Transfected Babesia bovis Parasite Line Expressing eGFP Is Able to Complete the Full Life Cycle of the Parasite in Mammalian and Tick Hosts

Johnson, Wendell C. / Hussein, Hala E. / Capelli-Peixoto, Janaina / Laughery, Jacob M. / Taus, Naomi S. / Suarez, Carlos E. / Ueti, Massaro W.

Pathogens. 2022 May 27, v. 11, no. 6

2022

Abstract: Bovine babesiosis is caused by apicomplexan pathogens of the genus Babesia, including B. bovis. This protozoan parasite has a complex life cycle involving dynamic changes to its transcriptome during the transition between the invertebrate and vertebrate ... ...

Abstract	Bovine babesiosis is caused by apicomplexan pathogens of the genus Babesia, including B. bovis. This protozoan parasite has a complex life cycle involving dynamic changes to its transcriptome during the transition between the invertebrate and vertebrate hosts. Studying the role of genes upregulated by tick stage parasites has been hindered by the lack of appropriate tools to study parasite gene products in the invertebrate host. Herein, we present tfBbo5480, a transfected B. bovis cell line, constitutively expressing enhanced green fluorescent protein (eGFP) created by a whole gene replacement transfection strategy, that was capable of completing the parasite’s entire life cycle in both the vertebrate and invertebrate hosts. tfBbo5480 was demonstrated to respond to in vitro sexual stage induction and upon acquisition by the female tick vector, Rhipicephalus microplus, the tick specific kinete stage of tfBbo5480 was detected in tick hemolymph. Larvae from tfBbo5480 exposed R. microplus female ticks successfully transmitted the transfected parasite to a naïve calf. The development of the whole gene replacement strategy will permit a deeper understanding of the biology of parasite-host-vector triad interactions and facilitate the evaluation of upregulated genes during the parasite’s journey through the tick vector leading to new intervention strategies for the control of bovine babesiosis.
Keywords	Babesia bovis ; Protozoa ; Rhipicephalus microplus ; babesiosis ; calves ; cell lines ; females ; genes ; green fluorescent protein ; hemolymph ; ticks ; transcriptome ; transfection
Language	English
Dates of publication	2022-0527
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens11060623
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Article ; Online: Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages.

Hussein, Hala E / Johnson, Wendell C / Taus, Naomi S / Capelli-Peixoto, Janaina / Suarez, Carlos E / Mousel, Michelle R / Ueti, Massaro W

Parasites & vectors

2021 Volume 14, Issue 1, Page(s) 395

Abstract: Background: Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental ...

Abstract	Background: Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental forms that differ in morphology and metabolism. Differentiation between these forms is highly regulated in response to changes in the parasite's environment. Understanding the mechanisms by which Babesia parasites respond to environmental changes and the transmission cycle through the biological vector is critically important for developing bovine babesiosis control strategies. Results: In this study, we induced B. bovis sexual stages in vitro using xanthurenic acid and documented changes in morphology and gene expression. In vitro induced B. bovis sexual stages displayed distinctive protrusive structures and surface ruffles. We also demonstrated the upregulation of B. bovis calcium-dependent protein kinase 4 (cdpk4), tubulin-tyrosine ligase (ttl), and methyltransferase (mt) genes by in vitro induced sexual stages and during parasite development within tick midguts. Conclusions: Similar to other apicomplexan parasites, it is likely that B. bovis upregulated genes play a vital role in sexual reproduction and parasite transmission. Herein, we document the upregulation of cdpk4, ttl, and mt genes by both B. bovis in vitro induced sexual stages and parasites developing in the tick vector. Understanding the parasite's biology and identifying target genes essential for sexual reproduction will enable the production of non-transmissible live vaccines to control bovine babesiosis.
MeSH term(s)	Animals ; Babesia bovis/drug effects ; Babesia bovis/genetics ; Babesiosis/parasitology ; Babesiosis/transmission ; Cattle ; Cattle Diseases/parasitology ; Female ; Gene Expression ; Life Cycle Stages/drug effects ; Life Cycle Stages/genetics ; Male ; Methyltransferases/genetics ; Peptide Synthases/genetics ; Protein Kinases/genetics ; Ticks/parasitology ; Xanthurenates/pharmacology
Chemical Substances	Xanthurenates ; xanthurenic acid (58LAB1BG8J) ; Methyltransferases (EC 2.1.1.-) ; Protein Kinases (EC 2.7.-) ; calcium-dependent protein kinase (EC 2.7.1.-) ; Peptide Synthases (EC 6.3.2.-) ; tyrosyltubulin ligase (EC 6.3.2.-)
Language	English
Publishing date	2021-08-10
Publishing country	England
Document type	Journal Article
ZDB-ID	2409480-8
ISSN	1756-3305 ; 1756-3305
ISSN (online)	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-021-04902-3
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Article: Immunization against a Conserved Surface Polysaccharide Stimulates Bovine Antibodies with Opsonic Killing Activity but Does Not Protect against

Taus, Naomi S / Cywes-Bentley, Colette / Johnson, Wendell C / Pier, Gerald B / Fry, Lindsay M / Mousel, Michelle R / Ueti, Massaro W

Pathogens (Basel, Switzerland)

2021 Volume 10, Issue 12

Abstract: Arthropod-borne apicomplexan pathogens remain a great concern and challenge for disease control in animals and humans. In order to ... ...

Abstract	Arthropod-borne apicomplexan pathogens remain a great concern and challenge for disease control in animals and humans. In order to prevent
Language	English
Publishing date	2021-12-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens10121598
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Article ; Online: Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Hussein, Hala E. / Johnson, Wendell C. / Taus, Naomi S. / Capelli-Peixoto, Janaina / Suarez, Carlos E. / Mousel, Michelle R. / Ueti, Massaro W.

Parasites & vectors. 2021 Dec., v. 14, no. 1 p.395-395

2021

Abstract: BACKGROUND: Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental ... ...

Abstract	BACKGROUND: Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental forms that differ in morphology and metabolism. Differentiation between these forms is highly regulated in response to changes in the parasite’s environment. Understanding the mechanisms by which Babesia parasites respond to environmental changes and the transmission cycle through the biological vector is critically important for developing bovine babesiosis control strategies. RESULTS: In this study, we induced B. bovis sexual stages in vitro using xanthurenic acid and documented changes in morphology and gene expression. In vitro induced B. bovis sexual stages displayed distinctive protrusive structures and surface ruffles. We also demonstrated the upregulation of B. bovis calcium-dependent protein kinase 4 (cdpk4), tubulin-tyrosine ligase (ttl), and methyltransferase (mt) genes by in vitro induced sexual stages and during parasite development within tick midguts. CONCLUSIONS: Similar to other apicomplexan parasites, it is likely that B. bovis upregulated genes play a vital role in sexual reproduction and parasite transmission. Herein, we document the upregulation of cdpk4, ttl, and mt genes by both B. bovis in vitro induced sexual stages and parasites developing in the tick vector. Understanding the parasite's biology and identifying target genes essential for sexual reproduction will enable the production of non-transmissible live vaccines to control bovine babesiosis.
Keywords	Babesia bovis ; acid-amino-acid ligases ; babesiosis ; calcium-calmodulin-dependent protein kinase ; developmental stages ; disease vectors ; gene expression ; gene expression regulation ; in vitro studies ; methyltransferases ; midgut ; parasitism ; ticks ; xanthurenic acid
Language	English
Dates of publication	2021-12
Size	p. 395.
Publishing place	BioMed Central
Document type	Article ; Online
ZDB-ID	2409480-8
ISSN	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-021-04902-3
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Article: Silencing expression of the Rhipicephalus microplus vitellogenin receptor gene blocks Babesia bovis transmission and interferes with oocyte maturation

Hussein, Hala E / Johnson, Wendell C / Taus, Naomi S / Suarez, Carlos E / Scoles, Glen A / Ueti, Massaro W

Parasites & vectors. 2019 Dec., v. 12, no. 1

2019

Abstract: BACKGROUND: Rhipicephalus microplus is an efficient biological vector of Babesia bovis, a causative agent of bovine babesiosis. Babesia bovis is passed transovarially to the next generation of ticks, which then transmit the parasite to naïve animals. Due ...

Abstract	BACKGROUND: Rhipicephalus microplus is an efficient biological vector of Babesia bovis, a causative agent of bovine babesiosis. Babesia bovis is passed transovarially to the next generation of ticks, which then transmit the parasite to naïve animals. Due to the importance of the R. microplus ovary for tick reproduction and transmission of B. bovis, we investigated the hypothesis that silencing vitellogenin receptor gene expression in the ovary during tick feeding on B. bovis-infected cattle would affect parasite transmission to the next generation of ticks. RESULTS: Silencing expression of the vitellogenin receptor in the ovary by RNA interference, resulted in reduced tick fertility. We observed reduced egg production (i.e. reduced weight of eggs), a lower rate of embryonic development, and a reduction in hatching. Analysis of individual larvae by PCR confirmed that RNAi mediated downregulation of the R. microplus vitellogenin receptor and also interfered with transovarial transmission of B. bovis. None of the larvae (0/58) from the RmVgR dsRNA-injected group were PCR-positive, whereas 12% (7/58) and 17% (10/58) of larvae from the non-injected and buffer-injected control groups, respectively, were infected with B. bovis. CONCLUSIONS: The combined effects of reduced fecundity and reduced infection in surviving larvae resulting from silencing indicate that vitellogenin receptor is essential for tick reproduction and may play a vital role in B. bovis transmission.
Keywords	Babesia bovis ; RNA interference ; Rhipicephalus microplus ; animal ovaries ; babesiosis ; cattle ; egg production ; eggs ; embryogenesis ; fecundity ; gene expression ; genes ; hatching ; larvae ; oocytes ; polymerase chain reaction ; receptors ; ticks ; transovarial transmission ; vitellogenin
Language	English
Dates of publication	2019-12
Size	p. 7.
Publishing place	BioMed Central
Document type	Article
ZDB-ID	2409480-8
ISSN	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-018-3270-1
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Article: Thrombospondin-Related Anonymous Protein (TRAP) Family Expression by

Masterson, Hayley E / Taus, Naomi S / Johnson, Wendell C / Kappmeyer, Lowell / Capelli-Peixoto, Janaina / Hussein, Hala E / Mousel, Michelle R / Hernandez-Silva, Diego J / Laughery, Jacob M / Mosqueda, Juan / Ueti, Massaro W

Microorganisms

2022 Volume 10, Issue 11

Abstract: The tick-transmitted disease bovine babesiosis causes significant economic losses in many countries around the world. Current control methods include modified live-attenuated vaccines that have limited efficacy. Recombinant proteins could provide ... ...

Abstract	The tick-transmitted disease bovine babesiosis causes significant economic losses in many countries around the world. Current control methods include modified live-attenuated vaccines that have limited efficacy. Recombinant proteins could provide effective, safe, and low-cost alternative vaccines. We compared the expression of the
Language	English
Publishing date	2022-11-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms10112173
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Article ; Online: Anaplasma marginale

Vimonish, Rubikah / Capelli-Peixoto, Janaina / Johnson, Wendell C / Hussein, Hala E / Taus, Naomi S / Brayton, Kelly A / Munderloh, Ulrike G / Noh, Susan M / Ueti, Massaro W

Frontiers in cellular and infection microbiology

2022 Volume 12, Page(s) 877525

Abstract: Tick midgut is the primary infection site required by tick-borne pathogens to initiate their development for transmission. Despite the biological significance of this organ, cell cultures derived exclusively from tick midgut tissues are unavailable and ... ...

Abstract	Tick midgut is the primary infection site required by tick-borne pathogens to initiate their development for transmission. Despite the biological significance of this organ, cell cultures derived exclusively from tick midgut tissues are unavailable and protocols for generating primary midgut cell cultures have not been described. To study the mechanism of
MeSH term(s)	Anaplasma ; Anaplasma marginale/genetics ; Anaplasmosis ; Animals ; Cell Culture Techniques ; Dermacentor/metabolism ; Polysaccharides/metabolism
Chemical Substances	Polysaccharides
Language	English
Publishing date	2022-05-31
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2619676-1
ISSN	2235-2988 ; 2235-2988
ISSN (online)	2235-2988
ISSN	2235-2988
DOI	10.3389/fcimb.2022.877525
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