Source: UNIV OF CONNECTICUT submitted to NRP
IDENTIFICATION OF SMALL MOLECULES TO PREVENT PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS (PRRSV)
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1028276
Grant No.
2022-67016-37126
Cumulative Award Amt.
$642,000.00
Proposal No.
2021-07035
Multistate No.
(N/A)
Project Start Date
Jun 1, 2022
Project End Date
May 31, 2026
Grant Year
2022
Program Code
[A1221]- Animal Health and Production and Animal Products: Animal Health and Disease
Recipient Organization
UNIV OF CONNECTICUT
438 WHITNEY RD EXTENSION UNIT 1133
STORRS,CT 06269
Performing Department
Animal Science
Non Technical Summary
Porcine reproductive and respiratory syndrome (PRRS), caused by PRRS virus (PRRSV), is the most economically devastating disease affecting swine industry worldwide. The sows with PRRS exhibit reproductive problems such as abortion, premature birth, and stillbirth. All PRRSV infected pigs develop symptoms such as coughing, difficulty breathing, inappetence, poor weight gain, with distress complicated by secondary infections provoking more serious diseases and mortality. Because of the high genetic heterogeneities of PRRSV, currentlyno broadly effective vaccine is availableagainst PRRS. Based on our recent studies, we plan 1) to evaluate the inhibitory effect on PRRSV infection in pigs by a natural compound (and its herb form) that can downregulate the PRRSV specific receptor expression in pig cells to inhibit PRRSV-infection, and to evaluate the derivatives and analogues of this compound to inhibit PRRSV-infectionin vitro; 2) to develop a lead compound from the derivatives/analogues of another small moleculethat blocks the interaction of PRRSV with its receptor and therefore PRRSV infection, and evaluate thein vivotoxicity and efficacy of this lead compound on inhibiting PRRSV infection in pigs; and 3) to perform high-throughput screening to identify additional compounds that block PRRSV binding to its receptor and therefore the viral infection. The data generated from this project will identify novel veterinary medications to block PRRSV infection in pigs. This study will also generatenew knowledge on the PRRSV specific receptor expression and its interaction with PRRSV,to facilitate the identification and test of new therapeutics to curtail the PRRS panzootic.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3113510103010%
3113510104010%
3113510110120%
3113510115020%
3113510116020%
3113510102010%
3117010110110%
Goals / Objectives
Thegoal of this project is to identify phytoceuticals or synthetic compounds for prophylactic or therapeutic use (either alone or as adjunct to vaccination programs) for porcine reproductive and respiratory syndrome (PRRS) in pigs.Theoverall objectives are1)to determine the inhibitory effect of a specific natural compoundand as a more cost-effective approach, its herb formon PRRSV infectionin vivo, and identify additional lead compounds from the derivatives/analogues of this compoundon PRRSV infection ofporcine alveolar macrophages (PAMs);2)to develop a lead compound from a specific synthetic compoundand its derivatives/analogues and characterize this compound for toxicity and efficacy on inhibiting PRRSV infectionin vivo; and3)to perform high-throughput (HTP) screening on a small chemical library of 150,000 compounds, to identify additional compounds that block the PRRSV-CD163 interaction and PRRSV infection of PAMsin vitro.
Project Methods
For objective 1, we will (A) Determine theIn VivoInhibitory Effects of the Specific Natural Compound and Its Herb Form on CD163 Expression and PRRSV Infection inPigs. This will be done in 3 to 4-week old cross-bred male and female PRRSV-free piglets divided in 4 groups. Group 1 will be non-infected, non-treated control. For other groups, pigs will be inoculated on day 0 with PRRSV strain VR-2332 by oronasal inoculation. Group 2 will serve as the infection control and will be treated orally with 225 mL vehicle once daily for 7 days following PRRSV inoculation. Groups 3 and 4 will be treated for 7 days with the natural compound suspended in vehicle, with a low and high daily oral dosage, respectively. Groups 5 and 6 will be treated daily for 7 days with the herb powderin vehicleat low and high dose, respectively. Thepigs will be evaluated for 2 weeks after viral inoculation, based on their clinical response. Blood viremia will be measured by quantitative reverse transcription PCR (qRT-PCR). Plasma serial diluents will be co-cultured with MARC-145 cells to monitor cytopathogenic effect forPRRSV titration. The compound plasma concentration will be measured using Liquid Chromatography-Mass Spectrometry (LC-MS). On day 14, pigs will be euthanized and post-mortem examinations performed. The lungs will be examined macroscopically for signs of inflammation and PRRSV infection, weighted, and bronchoalveolar lavage performed. Alveolar macrophages will be subject to RNA extraction for qRT-PCR detection of CD163 expression and PRRSV RNA level. Tissue samples will be collected from eachlung lobe(7 plus 2 additional sections from the large lobes), tracheobronchiallymph nodes, spleen, andinguinal lymph nodes, and will be frozen or fixed in 10% neutral bufferedformalin. Fixed tissues will be sectioned, and stained withhematoxylinandeosinfor histologic evaluation.The lungs will be scored microscopically on 9 sections per pig for lesions. Viral loads will be measured in frozen tissues by qRT-PCR. To evaluate any potential toxic effect by the treatment, we will also examine the pig brain, lung, heart, kidney and liver sections microscopically. Whole blood cell count and complete blood chemistry panel will be analyzed. We will also (B) Collect Primary PAMs and Determining the PRRSV-Susceptibility forIn VitroAssay, and Identify Additional Lead Compounds from the Derivatives/Analogues of the Natural Compound that Potently Inhibiting CD163 Expression and PRRSV InfectionIn Vitro. Atomwise, Inc. will support our effort to identify any derivatives that may exhibit superior potency and bioavailability than this natural compound. They will perform SAR-optimization to design and produce derivatives to further improve the solubility, bioavailability and potency. We will then evaluate all these compounds for their aqueous solubility, cytotoxicity, and inhibitory effects on CD163 expression in PAMs. We will further determine the inhibitory effect of these derivatives/analogues for PRRSV-susceptibility in PAMs. Up to 3 derivative/derivatives with superior solubility and CD163 inhibitory potency will be selected based on the LC50and IC50values. LV and VR-2332 strains of PRRSV (MOI = 0.1-1) will be used for PRRSV infection separately. The PRRSV-susceptibility of treated PAMs will be evaluated by qRT-PCR, immunostaining/FACS, and plaque assay for viral RNA and protein expression, and viral production. We will identify the lead compounds with the greatest potency to inhibit PRRSV-infection. For objective 2, we will (A) Identify A Lead Compound from the Specific Synthetic Compound and Its Analogues/Derivatives with the Most Potent Inhibition on PRRSV-Infection of PAMsIn Vitro. We will 1) determine the maximum aqueous (saline) solubility of this compound and any lead compounds identified below. 2) Based on the compound structure, we have found five additional commercially available analogues from the NCBI PubChem database. Also, Atomwise Inc. will provide ~20 additional analogues for us to test. 3) Atomwise Inc. will perform SAR-optimization based on the compound structure and the 3-D protein structure of CD163-SRCR5, to generate new derivatives for further improvement of compound solubility, bioavailability and potency. We will determine the solubility, LC50, and IC50for all analogues/derivatives. Using the bimolecular fluorescence complementation (BiFC) and PRRSV-infection assays developed by us, we will compare the potency of these compounds for PRRSV inhibition, and identify the lead compound with superior aqueous solubility and potency forin vivostudies. We will then (B) Evaluate the Toxicity of the Lead Compound in Pigs. We will first perform a 7-day pilot study in 4-week old piglets via intramuscular (IM) injection to evaluate the acute toxicity of the selected lead compound and determine the appropriate dosage in pigs for efficacy studies. We will observe clinical symptoms, collect data, and will examine the pig brain, lung, heart, kidney and liver sections microscopically after euthanasian. Whole blood cell count and complete blood chemistry panel will also be analyzed. We will then (C) Evaluate the Inhibition of PRRSV Infection in Pigs by the Lead Compound. The maximum non-toxic dose of the lead compound as determined above will be chosen to evaluate thein vivoinhibition of PRRSV infection. The compound will beIMadministered after PRRSV inoculation. The experiment duration and methodology for evaluation of compound efficacy against PRRSV challenge will be similar as described in objective 1 (A). For objective 3, we will conduct high throughput (HTP) screening using the BiFC assays in 384-well-plate format. We will utilize an in-house pre-selected small chemical library with 150,000 diverse chemotypes and pharmacophores (ChemBridge) maintained at the UConn HTP Facility. For BiFC assay signal detection, the 293T cells will be fixed at 24 h after compound treatment with formaldehyde (4%) and counterstained with Hoechst 33342 in PBS. Bright field, Hoechst nuclear stain, and fluorescence images of cells in each well will be acquired under a scanning microscope capable of automated imaging of 96 to 384-well-plates. The positive inhibition will be identified by fluorescent intensity analysis, and confirmed by examining the fluorescent images. Up to 20 positive compounds identified here with the most significant inhibitory effects will be further evaluated, by testing the cytotoxicity of these compounds in PAMs, and determining theirin vitroinhibitory effects on PRRSV infection of PAMs similarly as described in objectives 1 and 2.

Progress 06/01/24 to 05/31/25

Outputs
Target Audience:Scientists and researchers working in the field of porcine disease control and prevention. Graduate and undergraduate students learning about safety in animal husbandry and animal production. Pig farmers, government regulatory agencies for animal diseases. Pharmaceutical companies producing drugs for livestock. Human medical professionals treating zoonotic diseases. Animal scientists and veterinarians in general who are interested in using the small molecule model to treat diseases.General public who care about food safety andanimal welfare, and journalists who report on food safety, animal health and animalresearch. Changes/Problems:We added the viral mutation study upon long-term drug selection as well as bioavailability determination of the nanopackaged B7. Both were suggestions from stakeholders. What opportunities for training and professional development has the project provided?A PhD student (Dr. Jiaqi Zhu) was supported and trained throughout this project and obtained her PhD in 2024. Another PhD student is currently working full time in this project, together with a research associate and another PhD student helping her when needed. We also involved a number of undergraduate students in the project and one of them became a co-author of the publication reported here. Recently, we participated in BRAD (Biomedical Research Awareness Day) at the University of Connecticut and spoke about our project to undergraduate students and fellow scientists. How have the results been disseminated to communities of interest?Yes, we published a scientific paper (reported here). We also spoke to the community on our research project. However, our mainfocuswas to speakto stakeholders of the pig production industry, including farmers, animal health professionals. We aim to learnwhat aspects they want us todevelop the lead compound so it becomes an effective treatment in the pig production. The next group of people we speak to are potential collaborators such as drug delivery researchers to find the best way to administer the compound. What do you plan to do during the next reporting period to accomplish the goals?We plan to conduct Objective 3 of the project by screening more small molecules to increase the potency of the drug for a lower treatment cost. We will also conduct the proof-of-principlein vivo efficacy testing and pharmacokinetics determinationin weaned piglets.

Impacts
What was accomplished under these goals? The lead compound, B7, has very low solubility in PBS, we then used nanopackaging and increased its solubility and efficacy. We also conducted plasma, lung and lysosome release studies to determine the bioavailability of the nanopackaged B7. We found high bioavailability.When speaking to industry stakeholders, we were asked to conduct a "drug selection" mutation study on the PRRSV. We found that the drug did not change the viral DNA sequence in the region that interacts with CD163. Additionally, stakeholders asked us to include more contemporary and virulent strains of PRRSV. We obtained such a PRRSV-2 strained and completed the efficacy study in vitro. We are in the process of obtaining a PRRSV-1 strain from Spain.

Publications

  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Zhu J, Lai Y, Cheng M, Dash RC, Guo S, Guo J, Su Y, Wolek A, Issacs B, Liu Z, Li Q, Mishra N, Garmendia A, Hadden MK, Tian XC, He X, Tang Y. 2024. Journal of Virology. Discovery of small molecules against porcine reproductive and respiratory syndrome virus replication by targeting NendoU activity


Progress 06/01/23 to 05/31/24

Outputs
Target Audience:Scientists and researchers working in the field of porcine disease control and prevention.Graduate and undergraduate students learning about safety in animal husandry and animal production. Pig farmers, government regulatory agencies for animal diseases. Pharmaceutical companies producing drugs for livestock. Human medical professionals treating zootic diseases. General public who care about food safety, and journalists who report on food safety and zoonotic diseases. Changes/Problems:The changes are to develop nanoparticles for packaging of the compounds and testing for their safety. What opportunities for training and professional development has the project provided?A second new Ph.D. student has been extensively trained by a prior project personnel in pig macrophage isolation, functional evaluation, PRRSV production and titration, and evaluation of compounds to block PRRSV infection. This project has helped the PI to develop acollaborations on the application of nanotechnology indrugformulation to increase solubility of the small molecules and another collaboration on bioinformatics. The project also allowed the PI and project personnel to interact with the producers of the porcine industry as well as scientists of the pharmacedutical industry. How have the results been disseminated to communities of interest?The PD and the research group have presented the research results to scientists and staff at UConn Technology Commercialization Services. The Technology Commercialization Services have reached out to pharmaceutical companies and porcine production companiesforpotential licensing after signing CDAs. Amanuscript was submitted to PLoS Pathogen and is under major revision to provide additional data. What do you plan to do during the next reporting period to accomplish the goals?The low solubility problem of the small molecules have been solved by packaging in nanoparticles, which have been shown to be equally effective as unpackaged molecules dissolved in 100% organic solvants. We are in the process of testing the safety of the nanoparticles and the release of the molecules from the nanopackaging. The mechanism of nanoparticles such as endosomal escape may be studied.

Impacts
What was accomplished under these goals? We evaluated commercially available inhibitors of STAT3, which mediates expression of CD163, the scavenger receptor important for PRRSV entry to target cells. From the 45 compounds screened, we identified 6 that consistently inhibited CD163 expression in Porcine Alveolar Macrophages (PAMs). Following an assessment of their cytotoxicity on PAMs, we selected two promising candidates, ML116 and Niclosamide, for further investigation in viral infection assays. Notably, neither of these compounds exhibited cytotoxicity on PAMs up to 50 μM. ML116, however, showed limited effectiveness which only reduced viral titers by less than onelog at concentrations between 5 to 20 μM. Conversely, Niclosamide demonstrated a robust antiviral activity, significantly decreasing viral titers by threeand 1.5 logs in two viral strains, Lelystad (type 1) and VR-2332 (type 2), respectively, at an effective dose as low as 1 μM. Furthermore, we confirmed that Niclosamide effectively inhibits the mRNA levels of CD163 and SOCS3, a downstream target gene of STAT3 activation, during PRRSV infection. This elucidates the mechanism underlying Niclosamide's potent antiviral properties, positioning it as a promising anti-PRRSV agent. We also screened analogs of small molecules that were effective in inhibiting PRRSV entry into PAMS cells. One of them, F9, was found as effective and safe as the original small molecule of B7. Both molecules, however, have low solubility. We developed nanopackaging (up to 30 mg/ml) for both and found them equally effective as unpackaged compounds.

Publications

  • Type: Journal Articles Status: Other Year Published: 2024 Citation: Zhu J, He X, Dash RC, Su Y, Shen J, Wolek A, Liu J, Issacs B, Mishra N, Tian XC, Garmendia A, Hadden MK, Tang Y. 2024. Discovery of Broad-Spectrum Small Molecules Against Nidovirus. (submitted to PloS Pathogen) Replication by Targeting NendoU Activity.


Progress 06/01/22 to 05/31/23

Outputs
Target Audience:Scientists and researchers working in the field of porcine disease control and prevention. Graduate and undergraduate students learning about safety in animal husbandry and animal production. Pig farmers, government regulatory agencies for animal diseases, pharmaceutical companies producing drugs for livestock. Human medical professionals treating zootic diseases, general public who care about food safety, andjournalists who report onfood safety and zoonotic diseases. Changes/Problems:We willexplore nanopackaging of the small molecules to increase solubility and effectiveness. What opportunities for training and professional development has the project provided?A new Ph.D. studenthasbeen extensively trained by a senior Ph.D. student in pig macrophage isolation, functional evaluation, PRRSV production and titration, studying signaling pathways that regulate CD163 expression, BiFC assay development to investigate PRRSV-CD163 interaction, and evaluation of compounds to block PRRSV infection. One Ph.D. student has graduated and will be moving on to workas apostdoc with Dr. A. Garmendia in the Department of Pathobiology, UConn. This project has helped the PI to develop 2 collaborations on the application of nanotechnology to the drug formulation to increase effectiveness of the small molecules. How have the results been disseminated to communities of interest?The PD and the research group havepresented the research results to scientists and staff at UConn Technology Commercialization Services. The Technology Commercialization Services have reached out to pharmaceutical companies for potential licensing after signing CDAs. OnePh.D. studentpresented herresearch data at the UConn Animal Science Department seminar series. One full scientific article has been published. What do you plan to do during the next reporting period to accomplish the goals?The small molecules have low solubility, and high amounts are needed for effectiveness.We will continue to search for improved formulations to increase solubility and effectiveness through nanoparticle packaging and endosomal escape.

Impacts
What was accomplished under these goals? The porcine reproductive and respiratory syndrome viruses (PRRSV) led toa global panzootic and huge economical losses to the pork industry. PRRSV targets thescavenger receptor CD163 for productive infection. However, currently no effective treatmentis available to control the spread of this disease. Using bimolecular fluorescencecomplementation (BiFC) assays, we screened a set of small molecules potentially targetingthe scavenger receptor cysteine-rich domain 5 (SRCR5) of CD163. We found that theassay examining protein-protein interactions (PPI) between PRRSV glycoprotein 4 (GP4)and the CD163-SRCR5 domain mainly identifies compounds that potently inhibit PRRSVinfection, while examining the PPI between PRRSV-GP2a and the SRCR5 domain maximizedthe identification of positive compounds, including additional ones with variousantiviral capabilities. These positive compounds significantly inhibited both types 1 and 2 PRRSV infection of porcine alveolar macrophages. We confirmed that the highly activecompounds physically bind to the CD163-SRCR5 protein, with dissociation constant (KD)values ranging from 28 to 39 mM. Structure-activity-relationship (SAR) analysis revealedthat although both the 3-(morpholinosulfonyl)anilino and benzenesulfonamide moietiesin these compounds are critical for the potency to inhibit PRRSV infection, the morpholinosulfonylgroup can be replaced by chlorine substituents without significant loss ofantiviral potency. Our study established a system for throughput screening of natural orsynthetic compounds highly effective on blocking of PRRSV infection and shed light onfurther SAR modification of these compounds.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Zhu J, He X, Bernard, D, Shen J, Su Y, Wolek, A, Issacs B, Mishra N, *Tian, X, *Garmendia A, *Tang, Y. 2023. Identification of New Compounds against PRRSV Infection by Directly Targeting CD163. Journal of Virology eooo5423, published on May 3, 2023, doi: 10.1128/jvi.00054-23