SAES-422 Multistate Research Activity Accomplishments Report

Sections

Status: Approved

Basic Information

Participants

• In-person (n = 37): Raghavendra Amachawadi, Jennifer Auchtung, Menuka Bhandari, Yung-Fu Chang, Morgan Farnell, Yuhua Farnell, Aradhya Gourapura, Dylan Harris, Scott Kenney, Saroj Khatiwada, Gizem Levent, Wenli Li, Yu Li, Jun Lin, George Liu, Jing Liu, Melha Mellata, Melissa Monson, Shafeekh Muyyarikkandy, TG Nagaraja, Xiaoyu Niu, Gireesh Rajashekara, Sheela Ramamoorthy, Orhan Sahin, Linda Saif, Milena Saqui-Salces, Elizabeth Shepherd, Xiaolun Sun, Anusree Thenissery, Isabel Tobin, Qiuhong Wang, Carmen Wickware, Melanie Whitmore, Kush Kumar Yadav, Qijing Zhang, Glenn Zhang, Weiping Zhang • Remote (n = 3): Michelle Colby, Torey Looft, Peixin Fan • These investigators came from at least 20 different universities and institutions including Cornell U, Iowa State U, Kansas State U, Mississippi State U, North Carolina Agricultural and Technical State U, North Dakota State U, Ohio State U, Oklahoma State U, South Dakota State U, Texas A&M, Texas Tech, U of Arkansas, U of Illinois Urbana-Champaign, U of Minnesota, U of Nebraska-Lincoln, U of Tennessee, USDA ARS, USDA NIFA, U.S. Dairy Forage Research Center, and USDA National Animal Disease Center.

  • Welcome: Drs. Orhan Sahin (Chair) and Glenn Zhang (Secretary)
  • Opening remarks: Dr. Milena Saqui-Salces, NC1202 Administrative Advisor
  • Self-introductions among onsite and remote attendees
  • Business Meeting: Discussed budget and student awards; appointed Dr. Glenn Zhang as new chair; elected Dr. Scott Kenney as new secretary for a 2-year term; discussed the ways to strengthen collaborations within the group.
  • USDA-NIFA updates: Dr. Michelle Colby, National Program Leader for Animal Biosecurity, provided an update on the USDA funding perspectives remotely.
  • Progress reports and presentations: Dr. Linda Saif gave a keynote presentation, followed by another seven progress reports, with each 25 min presentation plus 5 min Q&A.

Accomplishments

  1. Optimized the porcine epidemic diarrhea virus (PEDV) recombination-resistant platform for live attenuated vaccine development.
  2. Elucidated how vitamin A status modulates maternal/lactogenic immunity and the gut-mammary gland-secretory IgA(sIgA) axis in sows.
  3. Characterized extraintestinal infection of porcine deltacoronavirus (PDCoV) by demonstrating that PDCoV RNA could be detected in low to moderate quantities in multiple organs or extraintestinal fluids, such as bronchoalveolar lavage and bile.
  4. Isolated and characterized current bovine coronavirus (BCoV) strains from dairy cows, dairy calves, and beef cattle for infectious clone establishment to study BCoV gene functions, tissue tropisms, and attenuated vaccine development.
  5. Constructed broadly immunogenic multivalent antigens for broad immunity and cross-protection against pig post-weaning diarrhea and moderate-to-severe diarrhea in humans using a novel multiepitope-fusion-antigen (MEFA) vaccinology platform.
  6. Identified three inhibitors of Cryptosporidium parvum glycolytic enzymes to be efficacious in treating cryptosporidiosis in infected bovine neonatal calves.
  7. Demonstrated that clathrin is involved in the endocytosis of Lawsonia intracellularis.
  8. Characterized two novel regulatory mechanisms that play a critical role in polymyxin resistance in Gram-negative pathogens and revealed novel targets for combating polymyxin resistance, a significant issue in animal health and food safety.
  9. Demonstrated that small molecules, GI-7 and QSI-5, possess a higher anti-APEC efficacy than sulfadimethoxine without a negative impact on growth performance of chickens.
  10. Revealed that Clostridium perfringens virulence was reduced by secondary bile acid deoxycholic acid (DCA) and isoallolithocholic acid (isoalloLCA).
  11. Developed a microbiota-based treatment that significantly altered the host gut innate immune response and provided protection to Enterobacteriaceae and Salmonella in chickens.
  12. Deciphered the association between Campylobacter jejuni colonization and gut microbiota composition of commercial broilers, and demonstrated fecal microbiota transplantation reduced cecal Campylobacter colonization significantly in broilers.
  13. Established avian and porcine organoid models for studying host-pathogen interactions.
  14. Validated digital PCR for monitoring priority antibiotic resistance genes in wastewater plants representing municipalities of different sizes in Wyoming.
  15. Collaborated with the USDA-APHIS to conduct in-depth molecular characterization of SARS-CoV-2 in white-tail deer and seroprevalence over the course of several years.

Impacts

  1. Coronaviruses such as PEDV, PDCoV, and BCoV are responsible for respiratory and gastrointestinal illnesses in pigs, cattle, and humans. The progresses from three groups have led to a better understanding of the influence of Vitamin A on the gut-mammary gland-secretory IgA axis during pregnancy, as well as the pathogenesis of PDCoV and BCoV. These findings will facilitate the development of more effective vaccines.
  2. ETEC bacteria are a leading cause of diarrhea in newly-weaned pigs, children in developing countries, and international travelers. A newly-improved vaccine demonstrates superior efficacy in protecting piglets from post-weaning diarrhea, potentially saving hundreds of millions of dollars annually for US swine producers. By incorporating an additional antigen into MecVax to target second-tier ETEC strains, protection of the vaccine will be broadened against children’s and travelers’ diarrhea.
  3. Zoonotic and foodborne pathogens like Campylobacter, Salmonella, APEC, Clostridium perfringens, and C. difficile pose serious risks to animal and human health. Several groups have developed novel vaccines, small-molecule compounds, and microbiome-based approaches to reduce their colonization in animals and the risk of transmission to humans.
  4. L. intracellularis is an economically significant pathogen causing hemorrhagic enteritis in pigs. A significant progress has been made in understanding its cellular entry mechanism. Clathrin has been identified for the first time to play a crucial role in the bacteria's endocytosis, potentially paving the way for novel treatment approaches.
  5. Poultry and swine organoids have been developed by two groups, serving as invaluable tools for studying host-pathogen interactions and the pathogenesis of enteric diseases.
  6. Several groups have developed and validated tools for monitoring antimicrobial resistance at the population level and SARS-CoV-2 prevalence in wildlife, contributing to characterizing and quantifying the magnitude of these public health challenges.

Publications

Grants and Contracts (Names in bold denote the NC1202 participants) 

  1. Zhao L (PI), Wang Q, Bielke L, Nazmi A (co-PIs). USDA-NIFA. Abate poultry disease and heat stress by climate-smart housing and environment control intervention for sustainable cage-free egg production. #2023-68014-39720. 6/1/2023 – 5/31/2027. $1,000,000.
  2. Yoo DW (PI), Wang Q (co-PI). USDA-NIFA. Recombination-negative, immune-enhanced, and clinically attenuated PRRSV as a vaccine. #2023-67015-39710. 4/15/2023-4/14/2027. $650,000.
  3. Vlasova A (PI), Saif L (Co-PI). NIH-NIAID. rotavirus reverse genetics system to study viral pathogenesis and receptor interactions. #1R21AI173880-01A1. 7/10/2023-6/30/2025. $393,750.
  4. Labbe N, Rajan K, Lin J (Co-PI), D’Souza D. USDA-NIFA. production and valorization of hemicellulosic biorefining streams as functional feed ingredients for the poultry industry. #2023-67021-39644. 01/01/2023 – 12/31/2025. $626,713.
  5. Sang Y (PI). USDA-NIFA. Whole-transcriptomic profiling of non-coding RNAs for antiviral regulation in porcine alveolar macrophages. #TENX-2132-GFSHAP. 09/30/2023-09/29/2026. $123,000
  6. Mellata M (PI), Kogut M (Co-PI). USDA-NIFA. A novel probiotic to increase chicken gut integrity and maturation at early life to improve health and disease resistance. #2023-67015-39078. 02/01/2023-01/31/2027. $635,000.
  7. Sibley D (PI), Witola WH (Co-PI). NIH-NIAID. Genetic basis of host infectivity by Cryptosporidium. #1R01AI175150-01. 12/2023-02/2028. $3,396,385.
  8. Zhang W (PI), Silvera P, Sack DA. NIH-NIAID. Development of MecVax, a cross-protective subunit vaccine for ETEC. #R01AI177144-01. 6/1/2023–5/30/2028. $5,643,881.
  9. Sack DA, Zhang W (Co-PI). NIH-NIAID. A cross-protective multivalent vaccine for Shigella and ETEC #R01AI175214-01. 3/6/2023 – 2/29/2028. $3,921,648.
  10. Piepnbrink KH (PI). structural mechanisms of bacterial extracellular DNA-recognition. #2310647. 07/2023 – 07/2026. $630,746.
  11. Farnell YF (PI). USDA-ARS. Establishment and characterization of liver organoids from layer chickens. # 5070-31320-001-011-S. 7/1/2023 -6/30/2026. $112,611.
  12. Farnell, MB (PI). USDA-APHIS. Evaluation and identification of psycho-socio-demographic factors impacting the implementation of and compliance to biosecurity plans for relevant infectious diseases in poultry farmers in Texas. #TX04.22. $306,042.
  13. Bisha B (PI). USDA-APHIS. Laboratory capacity for wildlife-focused diagnostics. #AP23WSNWRC00C038. 05/24/2023 - 05/23/2026. $6,000,000.
  14. Bisha B (PI). USDA-APHIS. Development, validation, and implementation of diagnostic tests for SARS-CoV-2 and other pathogenic microorganisms of wildlife. #AP23WSNWRC00C036. 05/15/2023 - 05/14/2026. $6,276,250.
  15. Bisha B (PI). USDA-APHIS. Spillover of SARS-CoV-2 into wildlife from wastewater treatment plants in the U.S. #AP23WSNWRC00C028. 06/01/2023 – 06/01/2025. $1,362,664.
  16. Zhang G (PI). USDA-NIFA. Epigenetic regulatory mechanism of host defense peptide synthesis. # 2023-67015-39095. 01/15/2023 – 01/14/2027. $650,000.

Publications (Names in bold denote the NC1202 participants) 

  1. Su CM, Du Y, Rowland RRR, Wang Q, Yoo D. Reprogramming viral immune evasion for a rational design of next-generation vaccines for RNA viruses. Front Immunol. 2023; 14: 1172000.
  2. Niu X, Liu M, Yang S, Xu J, Hou YJ, Liu D, Tang Q, Zhu H, Wang Q. A recombination-resistant genome for live attenuated and stable PEDV vaccines by engineering the transcriptional regulatory sequences. J Virol. 2023; 97: e0119323.
  3. Chepngeno J, Amimo JO, Michael H, Raev SA. Jung K, Lee MV, Damtie D, Omwando A, Vlasova AN, Saif LJ. Vitamin A deficiency and vitamin A supplementation affect innate and T cell immune responses to rotavirus A infection in a conventional sow model. Front Immunol. 2023; 14: 1188757.
  4. Bedsted AE, Jung K, Saif LJ. Detection of porcine deltacoronavirus RNA in the upper and lower respiratory tract and biliary fluid and the effect of infection on serum cholesterol levels and blood T cell population frequencies in gnotobiotic Vet Sci. 2023; 10: 117.
  5. Raev SA, Raque M, Kick MK, Saif LJ, Vlasova AN. Differential transcriptome response following infection of porcine ileal enteroids with species A and C rotaviruses. Virol J. 2023; 20: 238.
  6. Raque M, Raev SA, Guo Y, Kick MK, Saif LJ, Vlasova AN. Host cell response to rotavirus infection with emphasis on virus-glycan interactions, cholesterol metabolism, and innate immunity. Viruses 2023; 15: 1406.
  7. Yadav KK, Kenney SP. Animal Models for Studying Congenital Transmission of Hepatitis E Virus. Microorganisms. 2023; 11: 618.
  8. Bhandari M, Poelstra JW, Kauffman M, Varghese B, Helmy YA, Scaria J, Rajashekara G. Genomic diversity, antimicrobial resistance, plasmidome, and virulence profiles of Salmonella isolated from small specialty crop farms revealed by whole-genome sequencing. Antibiotics 2023; 12: 1637.
  9. Deblais L, Jang H, Kauffman M, Gangiredla J, Sawyer M, Basa S, Poelstra JW, Babu US, Harrison LM, Hiett KL, Balan KV, Rajashekara G. Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio. Front Microbiol. 2023; 14: 1074548.
  10. Deblais L, Ranjit S, Vrisman C, Antony L, Scaria J, Miller SA, Rajashekara G. Role of stress-induced proteins RpoS and YicC in the persistence of Salmonella enterica enterica Serotype Typhimurium in tomato plants. Mol Plant Microbe Interact. 2023; 36: 109.
  11. Helmy YA, Kathayat D, Closs G Jr, Galgozy K, Fuchs JR, Rajashekara G. Efficacy of quorum sensing and growth inhibitors alone and in combination against avian pathogenic Escherichia coli infection in chickens. Poult Sci. 2023; 102: 102543.
  12. Deblais L, Ojeda A, Brhane M, Mummed B, Hassen KA, Ahmedo BU, Weldesenbet YD, Amin JK, Ahmed IA, Usmane IA, Yusuf EA, Seran AJ, Abrahim FI, Game HT, Mummed BA, Usmail MM, Umer KA, Dawid MM, Gebreyes W, French N, Hassen JY, Roba KT, Mohammed A, Yimer G, Saleem C, Chen D, Singh N, Manary MJ, McKune SL, Havelaar AH, Rajashekara G. Prevalence and load of the Campylobacter genus in infants and associated household contacts in rural eastern Ethiopia: a longitudinal study from the campylobacter genomics and environmental enteric dysfunction (CAGED) project. Appl Environ Microbiol. 2023; 89: e0042423.
  13. Nguyen, X.D., Y. Zhao Lin, J. L. Purswell, T. Tabler, B. Voy, S. Hawkins, J.D. Evans. Modeling long-distance airborne transmission of highly pathogenic avian influenza carried by dust particles. Sci Rep..2023; 13: 16255.
  14. Wang, H., C.M. Logue, L.K. Nolan, Lin. Assessment of an enterobactin conjugate vaccine in layers to protect the offspring from colibacillosis. Pathogens 2023; 12: 1002.
  15. Kumar, V., J. Boorman, W.J. Greenlee, X. Zeng, Lin, F. van den Akker. Exploring the inhibition of the soluble lytic transglycosylase Cj0843c of Campylobacter jejuni via targeting different sites and different scaffolds. Prot Sci. 2023; 32: e4683.
  16. Zeng, X., J. Vidlund, B. Gillespie, L. Cao, G. Agga, Lin, O. Kerro Dego. Evaluation of immunogenicity of enterobactin conjugate vaccine for the control of E. coli mastitis in dairy cows. J Dairy Sci. 2023; 106: 7147-7163.
  17. Cao, L., X. Zeng, Lin. Generation of polystyrene-specific antibodies for developing efficient immunoassays to analyze microplastics. Chem Eng J. 2023; 465: 142843.
  18. Wang, H., Q. Zhong, Lin. Egg yolk antibody for passive immunization: status, challenges, and prospects. J. Agric Food Chem. 2023; 71: 5053-5061.
  19. Dmitry, S. K., S. L Long, X. Zeng, F. Xu, K. Lal, L. Cao, K. Hayoun, Lin, S. A. Joyce, I., Tikhonova. Characterization of the mechanism of bile salt hydrolase substrate specificity by experimental and computational analyses. Structure 2023; 31: 629-638.
  20. Zeng, X., A. Hinenoya, Z. Guan, F. Xu, Lin. Critical role of the RpoE stress response pathway in polymyxin resistance of Escherichia coli. J Antimicrob Chemother. 2023; 78: 732-746.
  21. Wang, H., L. Cao, C.M. Logue, N. L. Barbieri, L.K. Nolan, Lin. Evaluation of immunogenicity and efficacy of the enterobactin conjugate vaccine in protecting chickens from colibacillosis. Vaccine. 2023; 41: 930-937.
  22. Li, P.X., Y.F. Cui, F.F. Guo, J.H.Guo, X.Y. Cao, Lin, B. Ding, F. Xu. Campylobacter jejuni infection induces dynamic expression of avian host defense peptides in vitro and in vivo. Vet Microbiol. 2023; 277: 109631.
  23. Sarlo Davila KM, Nelli RK, Phadke KS, Ruden RM, Sang Y, Bellaire B, Gimenez-Lirola LG, Miller LC. How do deer respiratory epithelial cells weather the initial storm of SARS-CoV-2? Microbiol Spec. 2023; 12: e02524-232.
  24. Dimitrakopoulou D, Khwatenge CN; James-Zorn C, Paiola M, Bellin EW, Tian Y, Sundararajm N, Grayfer L, Barnard D, Ohta Y, Horb M, Sang Y, Robert J Advances in the xenopus immunome: diversification, expansion, and contraction. Dev Comp Immunol. 2023; 145: 104734.
  25. Adeyemi OD, Khwatenge CN, Tian Y, Grayfer L, Sang Y. Molecular diversity and functional implication of amphibian interferon complex: remarking immune adaptation in vertebrate evolution. Dev Comp Immunol. 2023; 140: 104624.
  26. Pereira CER, Resende TP, Vannucci FA, Gebhart C, Guedes RMC. Evaluation of the role of clathrin and bacterial viability in the endocytosis of Lawsonia intracellularis. Front Vet Sci. 2023; 10: 1005676.
  27. Hada A, Li L, Kandel A, Jin Y, Xiao Z. Characterization of bovine intraepithelial T lymphocytes in the gut. Pathogens 2023; 12: 1173.
  28. Meinen-Jochum J, Ott LC, Mellata M. Segmented filamentous bacteria-based treatment to elicit protection against Enterobacteriaceae in layer chickens. Front Microbiol. 2023; 14: 1231837.
  29. Pang J, Looft T, Zhang Q, Sahin O. Deciphering the association between Campylobacter colonization and microbiota composition in the intestine of commercial broilers. Microorganisms 2023; 11: 1724.
  30. Pang J, Beyi AF, Looft T, Zhang Q, Sahin O. Fecal microbiota transplantation reduces Campylobacter jejuni colonization in young broiler chickens challenged by oral gavage but not by seeder birds. Antibiotics 2023; 12: 1503.
  31. Lewis GL, Fenton RJ, Moriyama EN, Loy JD, Moxley RA. Association of ISVsa3 with multidrug resistance in Salmonella enterica isolates from cattle (Bos taurus). Microorganisms 2023; 11: 631.
  32. Xu R, Beatty WL, Greigert V, Witola WH, Sibley LD. Multiple pathways for glucose phosphate transport and utilization support growth of Cryptosporidium parvum. Nat Commun. 2023; 15: 380.
  33. Greigert V, Saraav I, Son J, Dayao D, Antia A, Tzipori S, Witola WH, Stappenbeck TS, Ding S, Sibley LD Cryptosporidium infection of human small intestinal epithelial cells induces type III interferon and impairs infectivity of Rotavirus. Gut Microbes 2023; 16: 2297897.
  34. Khan SM, Bajwa MR, Witola WH. Combination of two glycolytic enzymes protrays high synergistic efficacy against Cryptosporidium parvum. Antimicrob Agents Chemother. 2023; 67: e0056923.
  35. Stec J, Witola WH. Alternatives to piperidine in Knoevenagel condensation of 2-cyanoacetamide with benzaldehydes. Results Chem. 2023; 6: 101212.
  36. Liu M, Xia N, Witola WH, Li K. Editorial: Advances in molecular biology, pathogenesis, diagnosis, vaccines, and treatment of diseases caused by apicomplexan parasites. Front Cell Infect Microbiol. 2023; 13: 1205563.
  37. Khan SM, Witola WH. Past, current, and potential treatments for cryptosporidiosis in humans and farm animals: A comprehensive review. Front Cell Infect Microbiol. 2023; 13: 1115522.
  38. Khan SM, Hernandez AG, Allaie IM, Grooms GM, Li K, Witola WH, Stec J. Activity of (1-benzyl-4-triazolyl)-indole-2-carboxamides against Toxoplasma gondii and Cryptosporidium parvum. Int J Parasitol Drugs Drug Resist. 2022; 19: 6-20.
  39. Khan SM, Zhang X, Witola WH. Cryptosporidium parvum pyruvate kinase inhibitors with in vivo anti-cryptosporidial efficacy. Front Microbiol. 2022; 12: 800293.
  40. Upadhyay I, SM Parvej, Y. Shen, S Li, KL Lauder, C. Zhang, Zhang. Protein-based vaccine candidate MecVax broadly protects against intestinal colonization of ETEC strains expressing different adhesins (CS1 – CS6) in a rabbit model. Infect Immun. 2023; 91: e0027223.
  41. Li S, S Anvari, G Ptacek, I Upadhyay, RW Kaminiski, DA Sack, W Zhang. A broadly immunogenic polyvalent Shigella multiepitope fusion antigen (MEFA) protein protects against sonnei and S. flexneri lethal pulmonary challenges in mice. Infect Immun. 2023; 91: e0031623.
  42. Li S, H Seo, I Upadhyay, W Zhang. A polyvalent adhesin-toxoid multiepitope-fusion-antigen (MEFA-IIb) induced functional antibodies against five enterotoxigenic Escherichia coli adhesins (CS7, CS12, CS14, CS17, and CS21) but not enterotoxins (LT and STa). Microorganisms 2023; 11: 11102473.
  43. Upadhyay I, Parvej SM, S Li, KL Lauder, Y Shen, W Zhang. Polyvalent protein adhesin MEFA-II induces functional antibodies against enterotoxigenic Escherichia coli (ETEC) adhesins CS7, CS12, CS14, CS17, and CS21 and heat-stable toxin (STa). Appl Environ Microbiol. 2023; 89: e0068323.
  44. Alenezi T, Fu Y, Alrubaye B, Alanazi T, Almansour A, Wang H, Sun X. Potent bile acid microbial metabolites modulate Clostridium perfringens Pathogens 2023; 12: 1202.
  45. Dal Pont GC, Lee A, Bortoluzzi C, Farnell YZ, Gougoulias C, Kogut MH. Bacitracin supplementation as a growth promoter down-regulates innate and adaptive cytokines in broilers’ intestines. 2023; 2: 411-417.
  46. Cardoso Dal Pont G, Lee A, Bortoluzzi C, Farnell YZ, Gougoulias C, Kogut MH. Novel model for chronic intestinal inflammation in chickens: (2) Immunologic mechanism behind the inflammatory response. Dev Comp Immunol. 2023; 138: 104524.
  47. Osman M, Daaboul D, Tajani AG, El Omari K, Bisha B, Hassan J, Cazer CL, Fiorella KJ, Karah N, Abbara A, Hamze M, Cummings KJ, Naas T, Kassem II. Multidrug-resistant pathogens contaminate river water used in irrigation in disenfranchised communities: multidrug-resistant pathogens in irrigation waters. J Glob Antimicrob Res. 2023; 36: 175-180.
  48. Lai M, Cao Y, Wulff SS, Robinson TJ, McGuire A, Bisha B. A time series-based machine learning strategy for wastewater-based forecasting and nowcasting of COVID-19 dynamics. Sci Total Environ. 2023; 897: 165105.
  49. Liu J, Robinson K, Lyu W, Yang Q, Wang J, Christensen KD, Zhang G. Anaerobutyricum and Subdoligranulum are differentially enriched in broilers with disparate weight gains. Animals 2023; 13: 1834.
  50. Tobin I, Zhang G. Regulation of host defense peptide synthesis by polyphenols. Antibiotics 2023; 12: 660.
  51. Lyu W, Deng Z, Zhang G. High-throughput screening for epigenetic compounds that induce human β-defensin 1 synthesis. Antibiotics 2023; 12: 186.
  52. Pi Y, Wu Y, Lu D, Han D, Zhao J, Zheng X, Zhang S, Ye H, Lian S, Bai Y, Wang Z, Tao S, Ni D, Zou X, Jia W, Zhang G, Li D, and Wang J. Gut microbiota-derived ursodeoxycholic acid alleviates low birth weight-induced colonic inflammation by enhancing M2 macrophage polarization. Microbiome 2023; 11: 19.
  53. Arango M, Forga A, Liu J, Zhang G, Gray L, Moore R, Coles M, Atencio A, Trujillo C, Latorre JD, Tellez-Isaias M, Hargis B, Graham D. Characterizing the impact of Enterococcus cecorum infection during late embryogenesis on disease progression, cecal microbiome composition, and early performance in broiler chickens. Poult Sci. 2023; 102: 103059.
  54. Han D, Wu Y, Lu D, Pang J, Hu J, Zhang X, Wang Z, Zhang G, and Wang J. Polyphenol-rich diet mediates interplay between macrophage-neutrophil and gut microbiota to alleviate intestinal inflammation. Cell Death Dis. 2023; 14: 656.
  55. Hu J, Wu, Y, Kang L, Liu Y, Ye H, Wang R, Zhao J, Zhang G, Li X, Wang J, Han D. Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli. NPJ Biofilms Microbiomes 2023; 9: 79.
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