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Article ; Online: Gene editing as applied to prevention of reproductive porcine reproductive and respiratory syndrome.

Whitworth, Kristin M / Prather, Randall S

2017 Volume 84, Issue 9, Page(s) 926–933

Abstract: Porcine Reproductive and Respiratory Syndrome (PRRS) causes severe reproductive failure in sows as well as transplacental transfer of PRRS virus (PRRSV) to late-gestation fetuses, resulting in abortions, early farrowing, increased number of stillborn ... ...

Abstract	Porcine Reproductive and Respiratory Syndrome (PRRS) causes severe reproductive failure in sows as well as transplacental transfer of PRRS virus (PRRSV) to late-gestation fetuses, resulting in abortions, early farrowing, increased number of stillborn piglets, and weak neonatal piglets. PRRSV-infected boars present with anorexia and lethargy, and have decreased sperm quality. The gene for the cellular receptor that the PRRSV uses, Cluster of differentiation 163 (CD163), was edited using Clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 gene-editing technology to create biallelic DNA edits to the CD163 gene in 100% of the offspring. CD163-null pigs challenged with virus were completely resistant to both Type 1 and Type 2 PRRSV isolates, as measured by clinical signs, viremia, antibody response, and lung histopathology. In vitro studies showed that CD163-null alveolar macrophages were also not permissive to infection by a panel of six Type 1 and nine Type 2 viral isolates. Thus, DNA editing of the CD163 gene prevented PRRSV infection and reproductive losses associated with infection.
Language	English
Publishing date	2017-09
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	20321-x
ISSN	1098-2795 ; 1040-452X
ISSN (online)	1098-2795
ISSN	1040-452X
DOI	10.1002/mrd.22811
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Article: Gene editing of pigs to control influenza A virus infections.

Kwon, Taeyong / Artiaga, Bianca L / McDowell, Chester D / Whitworth, Kristin M / Wells, Kevin D / Prather, Randall S / Delhon, Gustavo / Cigan, Mark / White, Stephen N / Retallick, Jamie / Gaudreault, Natasha N / Morozov, Igor / Richt, Juergen A

bioRxiv : the preprint server for biology

2024

Abstract: Proteolytic activation of the hemagglutinin (HA) glycoprotein by host cellular proteases is pivotal for influenza A virus (IAV) infectivity. Highly pathogenic avian influenza viruses possess the multibasic cleavage site of the HA which is cleaved by ... ...

Abstract	Proteolytic activation of the hemagglutinin (HA) glycoprotein by host cellular proteases is pivotal for influenza A virus (IAV) infectivity. Highly pathogenic avian influenza viruses possess the multibasic cleavage site of the HA which is cleaved by ubiquitous proteases, such as furin; in contrast, the monobasic HA motif is recognized and activated by trypsin-like proteases, such as the transmembrane serine protease 2 (TMPRSS2). Here, we aimed to determine the effects of TMPRSS2 on the replication of pandemic H1N1 and H3N2 subtype IAVs in the natural host, the pig. The use of the CRISPR/Cas 9 system led to the establishment of homozygous gene edited (GE)
Language	English
Publishing date	2024-01-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.15.575771
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Article ; Online: Improvements in pig agriculture through gene editing.

Whitworth, Kristin M / Green, Jonathan A / Redel, Bethany K / Geisert, Rodney D / Lee, Kiho / Telugu, Bhanu P / Wells, Kevin D / Prather, Randall S

CABI agriculture and bioscience

2022 Volume 3, Issue 1, Page(s) 41

Abstract: Genetic modification of animals via selective breeding is the basis for modern agriculture. The current breeding paradigm however has limitations, chief among them is the requirement for the beneficial trait to exist within the population. Desirable ... ...

Abstract	Genetic modification of animals via selective breeding is the basis for modern agriculture. The current breeding paradigm however has limitations, chief among them is the requirement for the beneficial trait to exist within the population. Desirable alleles in geographically isolated breeds, or breeds selected for a different conformation and commercial application, and more importantly animals from different genera or species cannot be introgressed into the population via selective breeding. Additionally, linkage disequilibrium results in low heritability and necessitates breeding over successive generations to fix a beneficial trait within a population. Given the need to sustainably improve animal production to feed an anticipated 9 billion global population by 2030 against a backdrop of infectious diseases and a looming threat from climate change, there is a pressing need for responsive, precise, and agile breeding strategies. The availability of genome editing tools that allow for the introduction of precise genetic modification at a single nucleotide resolution, while also facilitating large transgene integration in the target population, offers a solution. Concordant with the developments in genomic sequencing approaches, progress among germline editing efforts is expected to reach feverish pace. The current manuscript reviews past and current developments in germline engineering in pigs, and the many advantages they confer for advancing animal agriculture.
Language	English
Publishing date	2022-06-21
Publishing country	United States
Document type	Journal Article ; Review
ISSN	2662-4044
ISSN (online)	2662-4044
DOI	10.1186/s43170-022-00111-9
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Article ; Online: Genetic engineering alveolar macrophages for host resistance to PRRSV.

Prather, Randall S / Whitworth, Kristin M / Schommer, Susan K / Wells, Kevin D

Veterinary microbiology

2017 Volume 209, Page(s) 124–129

Abstract: Standard strategies for control of porcine reproductive and respiratory syndrome virus (PRRSV) have not been effective, as vaccines have not reduced the prevalence of disease and many producers depopulate after an outbreak. Another method of control ... ...

Abstract	Standard strategies for control of porcine reproductive and respiratory syndrome virus (PRRSV) have not been effective, as vaccines have not reduced the prevalence of disease and many producers depopulate after an outbreak. Another method of control would be to prevent the virus from infecting the pig. The virus was thought to infect alveolar macrophages by interaction with a variety of cell surface molecules. One popular model had PRRSV first interacting with heparin sulfate followed by binding to sialoadhesin and then being internalized into an endosome. Within the endosome, PRRSV was thought to interact with CD163 to uncoat the virus so the viral genome could be released into the cytosol and infect the cell. Other candidate receptors have included vimentin, CD151 and CD209. By using genetic engineering, it is possible to test the importance of individual entry mediators by knocking them out. Pigs engineered by knockout of sialoadhesin were still susceptible to infection, while CD163 knockout resulted in pigs that were resistant to infection. Genetic engineering is not only a valuable tool to determine the role of specific proteins in infection by PRRSV (in this case), but also provides a means to create animals resistant to disease. Genetic engineering of alveolar macrophages can also illuminate the role of other proteins in response to infection. We suggest that strategies to prevent infection be pursued to reduce the reservoir of virus.
Language	English
Publishing date	2017-09
Publishing country	Netherlands
Document type	Journal Article ; Review
ZDB-ID	753154-0
ISSN	1873-2542 ; 0378-1135
ISSN (online)	1873-2542
ISSN	0378-1135
DOI	10.1016/j.vetmic.2017.01.036
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Article ; Online: Chloride channel accessory 1 gene deficiency causes selective loss of mucus production in a new pig model.

Keeler, Shamus P / Yantis, Jennifer / Gerovac, Benjamin J / Youkilis, Samuel L / Podgorny, Stephanie / Mao, Dailing / Zhang, Yong / Whitworth, Kristin M / Redel, Bethany / Samuel, Melissa S / Wells, Kevin D / Prather, Randall S / Holtzman, Michael J

American journal of physiology. Lung cellular and molecular physiology

2022 Volume 322, Issue 6, Page(s) L842–L852

Abstract: Morbidity and mortality of respiratory diseases are linked to airway obstruction by mucus but there are still no specific, safe, and effective drugs to correct this phenotype. The need for better treatment requires a new understanding of the basis for ... ...

Abstract	Morbidity and mortality of respiratory diseases are linked to airway obstruction by mucus but there are still no specific, safe, and effective drugs to correct this phenotype. The need for better treatment requires a new understanding of the basis for mucus production. In that regard, studies of human airway epithelial cells in primary culture show that a mucin granule constituent known as chloride channel accessory 1 (CLCA1) is required for inducible expression of the inflammatory mucin MUC5AC in response to potent type 2 cytokines. However, it remained uncertain whether CLCLA1 is necessary for mucus production in vivo. Conventional approaches to functional biology using targeted gene knockout were difficult due to the functional redundancy of additional
MeSH term(s)	Animals ; Chloride Channels/genetics ; Chloride Channels/metabolism ; Epithelial Cells/metabolism ; Goblet Cells/metabolism ; Lung/metabolism ; Mice ; Mucin 5AC/genetics ; Mucin 5AC/metabolism ; Mucus/metabolism ; Respiratory Mucosa/metabolism ; Swine
Chemical Substances	Chloride Channels ; Mucin 5AC
Language	English
Publishing date	2022-04-19
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1013184-x
ISSN	1522-1504 ; 1040-0605
ISSN (online)	1522-1504
ISSN	1040-0605
DOI	10.1152/ajplung.00443.2021
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Article ; Online: Profiling development of abdominal organs in the pig.

Gabriel, George C / Devine, William A / Redel, Bethany K / Whitworth, Kristin M / Samuel, Melissa / Spate, Lee D / Cecil, Raissa F / Prather, Randall S / Wu, Yijen L / Wells, Kevin D / Lo, Cecilia W

Scientific reports

2022 Volume 12, Issue 1, Page(s) 16245

Abstract: The pig is an ideal model system for studying human development and disease due to its similarities to human anatomy, physiology, size, and genome. Further, advances in CRISPR gene editing have made genetically engineered pigs viable models for the study ...

Abstract	The pig is an ideal model system for studying human development and disease due to its similarities to human anatomy, physiology, size, and genome. Further, advances in CRISPR gene editing have made genetically engineered pigs viable models for the study of human pathologies and congenital anomalies. However, a detailed atlas illustrating pig development is necessary for identifying and modeling developmental defects. Here we describe normal development of the pig abdominal system and show examples of congenital defects that can arise in CRISPR gene edited SAP130 mutant pigs. Normal pigs at different gestational ages from day 20 (D20) to term were examined and the configuration of the abdominal organs was studied using 3D histological reconstructions with episcopic confocal microscopy, magnetic resonance imaging (MRI) and necropsy. This revealed prominent mesonephros, a transient embryonic organ present only during embryogenesis, at D20, while the developing metanephros that will form the permanent kidney are noted at D26. By D64 the mesonephroi are absent and only the metanephroi remain. The formation of the liver and pancreas was observed by D20 and complete by D30 and D35 respectively. The spleen and adrenal glands are first identified at D26 and completed by D42. The developing bowel and the gonads are identified at D20. The bowel appears completely rotated by D42, and testes in the male were descended at D64. This atlas and the methods used are excellent tools for identifying developmental pathologies of the abdominal organs in the pig at different stages of development.
MeSH term(s)	Abdomen/diagnostic imaging ; Animals ; Clustered Regularly Interspaced Short Palindromic Repeats ; Gene Editing/methods ; Genetic Engineering ; Humans ; Kidney ; Male ; Swine
Language	English
Publishing date	2022-09-28
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-022-19960-5
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Article ; Online: Somatic cell nuclear transfer efficiency: how can it be improved through nuclear remodeling and reprogramming?

Whitworth, Kristin M / Prather, Randall S

Molecular reproduction and development

2010 Volume 77, Issue 12, Page(s) 1001–1015

Abstract: Fertile offspring from somatic cell nuclear transfer (SCNT) is the goal of most cloning laboratories. For this process to be successful, a number of events must occur correctly. First the donor nucleus must be in a state that is amenable to remodeling ... ...

Abstract	Fertile offspring from somatic cell nuclear transfer (SCNT) is the goal of most cloning laboratories. For this process to be successful, a number of events must occur correctly. First the donor nucleus must be in a state that is amenable to remodeling and subsequent genomic reprogramming. The nucleus must be introduced into an oocyte cytoplasm that is capable of facilitating the nuclear remodeling. The oocyte must then be adequately stimulated to initiate development. Finally the resulting embryo must be cultured in an environment that is compatible with the development of that particular embryo. Much has been learned about the incredible changes that occur to a nucleus after it is placed in the cytoplasm of an oocyte. While we think that we are gaining an understanding of the reorganization that occurs to proteins in the donor nucleus, the process of cloning is still very inefficient. Below we will introduce the procedures for SCNT, discuss nuclear remodeling and reprogramming, and review techniques that may improve reprogramming. Finally we will briefly touch on other aspects of SCNT that may improve the development of cloned embryos.
MeSH term(s)	Animals ; Cell Nucleus/physiology ; Cell Physiological Phenomena/physiology ; Humans ; Mice ; Nuclear Transfer Techniques
Language	English
Publishing date	2010-10-07
Publishing country	United States
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	20321-x
ISSN	1098-2795 ; 1040-452X
ISSN (online)	1098-2795
ISSN	1040-452X
DOI	10.1002/mrd.21242
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Article ; Online: Cardiovascular Development and Congenital Heart Disease Modeling in the Pig.

Gabriel, George C / Devine, William / Redel, Bethany K / Whitworth, Kristin M / Samuel, Melissa / Spate, Lee D / Cecil, Raissa F / Prather, Randall S / Wu, Yijen / Wells, Kevin D / Lo, Cecilia W

Journal of the American Heart Association

2021 Volume 10, Issue 14, Page(s) e021631

Abstract: Background Modeling cardiovascular diseases in mice has provided invaluable insights into the cause of congenital heart disease. However, the small size of the mouse heart has precluded translational studies. Given current high-efficiency gene editing, ... ...

Abstract	Background Modeling cardiovascular diseases in mice has provided invaluable insights into the cause of congenital heart disease. However, the small size of the mouse heart has precluded translational studies. Given current high-efficiency gene editing, congenital heart disease modeling in other species is possible. The pig is advantageous given its cardiac anatomy, physiology, and size are similar to human infants. We profiled pig cardiovascular development and generated genetically edited pigs with congenital heart defects. Methods and Results Pig conceptuses and fetuses were collected spanning 7 stages (day 20 to birth at day 115), with at least 3 embryos analyzed per stage. A combination of magnetic resonance imaging and 3-dimensional histological reconstructions with episcopic confocal microscopy were conducted. Gross dissections were performed in late-stage or term fetuses by using sequential segmental analysis of the atrial, ventricular, and arterial segments. At day 20, the heart has looped, forming a common atria and ventricle and an undivided outflow tract. Cardiac morphogenesis progressed rapidly, with atrial and outflow septation evident by day 26 and ventricular septation completed by day 30. The outflow and atrioventricular cushions seen at day 20 undergo remodeling to form mature valves, a process continuing beyond day 42. Genetically edited pigs generated with mutation in chromatin modifier
MeSH term(s)	Animals ; Disease Models, Animal ; Heart/embryology ; Heart Defects, Congenital/embryology ; Magnetic Resonance Imaging, Cine/methods ; Microscopy, Confocal ; Organogenesis/physiology ; Swine
Language	English
Publishing date	2021-07-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2653953-6
ISSN	2047-9980 ; 2047-9980
ISSN (online)	2047-9980
ISSN	2047-9980
DOI	10.1161/JAHA.121.021631
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Article ; Online: Genomic profiling to improve embryogenesis in the pig.

Prather, Randall S / Redel, Bethany K / Whitworth, Kristin M / Zhao, Ming-Tao

Animal reproduction science

2014 Volume 149, Issue 1-2, Page(s) 39–45

Abstract: Over the past decade the technology to characterize transcription during embryogenesis has progressed from estimating a single transcript to a reliable description of the entire transcriptome. Northern blots were followed by sequencing ESTs, quantitative ...

Abstract	Over the past decade the technology to characterize transcription during embryogenesis has progressed from estimating a single transcript to a reliable description of the entire transcriptome. Northern blots were followed by sequencing ESTs, quantitative real time PCR, cDNA arrays, custom oligo arrays, and more recently, deep sequencing. The amount of information that can be generated is overwhelming. The challenge now is how to glean information from these vast data sets that can be used to understand development and to improve methods for creating and culturing embryos in vitro, and for reducing reproductive loss. The use of ESTs permitted the identification of SPP1 as an oviductal component that could reduce polyspermy. Microarrays identified LDL and NMDA as components to replace BSA in embryo culture media. Deep sequencing implicated arginine, glycine, and folate as components that should be adjusted in our current culture system, and identified a characteristic of embryo metabolism that is similar to cancer and stem cells. Not only will these characterizations aid in improving in vitro production of embryos, but will also be useful for identifying, or creating conditions for donor cells that will be more likely to result in normal development of cloned embryos. The easily found targets have been identified, and now more sophisticated methods are being employed to advance our understanding of embryogenesis. Here the technology to study the global transcriptome is reviewed followed by specific examples of how the technology has been used to understand and improve porcine embryogenesis both in vitro and in vivo.
MeSH term(s)	Animals ; Embryonic Development/physiology ; Gene Expression Regulation, Developmental/physiology ; Genomics ; Swine/embryology ; Transcriptome/physiology
Language	English
Publishing date	2014-09
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	429674-6
ISSN	1873-2232 ; 0378-4320
ISSN (online)	1873-2232
ISSN	0378-4320
DOI	10.1016/j.anireprosci.2014.04.017
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Article ; Online: Glycine supplementation in vitro enhances porcine preimplantation embryo cell number and decreases apoptosis but does not lead to live births.

Redel, Bethany K / Spate, Lee D / Lee, Kiho / Mao, Jiude / Whitworth, Kristin M / Prather, Randall S

Molecular reproduction and development

2016 Volume 83, Issue 3, Page(s) 246–258

Abstract: Most in vitro culture conditions are less-than-optimal for embryo development. Here, we used a transcriptional-profiling database to identify culture-induced differences in gene expression in porcine blastocysts compared to in vivo-produced counterparts. ...

Abstract	Most in vitro culture conditions are less-than-optimal for embryo development. Here, we used a transcriptional-profiling database to identify culture-induced differences in gene expression in porcine blastocysts compared to in vivo-produced counterparts. Genes involved in glycine transport (SLC6A9), glycine metabolism (GLDC, GCSH, DLD, and AMT), and serine metabolism (PSAT1, PSPH, and PHGDH) were differentially expressed. Addition of 10 mM glycine to the culture medium (currently containing 0.1 mM) reduced the abundance of SLC6A9 transcript and increased total cell number, primarily in the trophectoderm lineage (P = 0.003); this was likely by decreasing the percentage of apoptotic nuclei. As serine and glycine can be reversibly metabolized by serine hydroxymethyltransferase 2 (SHMT2), we assessed the abundance of SHMT2 transcript as well as its functional role by inhibiting it with aminomethylphosphonic acid (AMPA), a glycine analog, during in vitro culture. Both AMPA supplementation and elevated glycine decreased the mRNA abundance of SHMT2 and tumor protein p53 (TP53), which is activated in response to cellular stress, compared to controls (P ≤ 0.02). On the other hand, mitochondrial activity of blastocysts, mtDNA copy number, and abundance of mitochondria-related transcripts did not differ between control and 10 mM glycine culture conditions. Despite improvements to these metrics of blastocyst quality, transfer of embryos cultured in 10 mM glycine did not result in pregnancy whereas the transfer of in vitro-produced embryos cultured in control medium yielded live births. Mol. Reprod. Dev. 83: 246-258, 2016. © 2016 The Authors.
MeSH term(s)	Animals ; Biological Transport, Active/drug effects ; Blastocyst/metabolism ; Embryo Transfer ; Female ; Gene Expression Regulation, Developmental/drug effects ; Glycine/pharmacology ; Pregnancy ; Swine
Chemical Substances	Glycine (TE7660XO1C)
Language	English
Publishing date	2016-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	20321-x
ISSN	1098-2795 ; 1040-452X
ISSN (online)	1098-2795
ISSN	1040-452X
DOI	10.1002/mrd.22618
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