Alternative polyadenylation events in epithelial cells sense endometritis progression in dairy cows

doi:10.1016/j.jia.2022.11.009

Journal of Integrative Agriculture ›› 2023, Vol. 22 ›› Issue (6): 1820-1832.DOI: 10.1016/j.jia.2022.11.009

收稿日期:2022-08-15 修回日期:2022-11-24 接受日期:2022-10-24 出版日期:2023-06-20 发布日期:2022-10-24

Alternative polyadenylation events in epithelial cells sense endometritis progression in dairy cows

Meagan J. STOTTS¹, Yangzi ZHANG¹, Shuwen ZHANG¹, Jennifer J. MICHAL¹, Juan VELEZ², Bothe HANS², Martin MAQUIVAR^1#, Zhihua JIANG^1#

¹Department of Animal Sciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164-7620, USA
²Aurora Organic Farms, Platteville, CO 80651, USA

Received:2022-08-15 Revised:2022-11-24 Accepted:2022-10-24 Online:2023-06-20 Published:2022-10-24
About author:#Correspondence Zhihua JIANG, E-mail: jiangz@wsu.edu; Martin MAQUIVAR, E-mail: martin.maquivar@wsu.edu
Supported by:
This work was supported by the National Institute of Food and Agriculture, United States Department of Agriculture (2016-67015-24470, 2018-67015-27500 (sub-contract), 2020-67015-31733 and 2022-51300-38058) and by funds provided for medical and biological research by the State of Washington Initiative Measure, USA (No. 171) and the Washington State University Agricultural Experiment Station (Hatch funds 1014918) received from the National Institutes for Food and Agriculture, United States Department of Agriculture.

摘要/Abstract

Abstract:

Endometritis (inflammation of the endometrial lining) is one of the most devastating reproductive diseases in dairy cattle, resulting in substantial production loss and causing more than $650 million in lost revenue annually in the USA. We hypothesize that alternative polyadenylation (APA) sites serve as decisive sensors for endometrium health and disease in dairy cows. Endometrial cells collected from 18 cows with purulent vaginal discharge scored 0 to 2 were used for APA profiling with our whole transcriptome termini site sequencing (WTTS-seq) method. Overall, pathogens trigger hosts to use more differentially expressed APA (DE-APA), more intronic DE-APA, more DE-APA sites per gene and more DE-genes associated with inflammation. Host CD59 molecule (CD59), Fc fragment of IgG receptor IIa (FCGR2A), lymphocyte antigen 75 (LY75) and plasminogen (PLG) may serve as initial contacts or combats with pathogens on cell surface, followed by activation of nuclear receptor subfamily 1 group H member 4 (NR1H4) to regulate AXL receptor tyrosine kinase (AXL), FGR proto-oncogene, Src family tyrosine kinase (FGR), HCK proto-oncogene, Src family tyrosine kinase (HCK) and integrin subunit beta 2 (ITGB2) for anti-inflammation. This study is the first to show significance of cilium pathways in endometrium health and animal reproduction. MIR21 and MIR30A would be perfect antagonistic biomarkers for diagnosis of either inflammation or anti-inflammation. These novel findings will set precedent for future genomic studies to aid the dairy industry develop new strategies to reduce endometritis incidence and improve fertility.

Key words: organic dairy , endometritis , alternative polyadenylation , infection progression , antagonistic biomarkers

Meagan J. STOTTS, Yangzi ZHANG, Shuwen ZHANG, Jennifer J. MICHAL, Juan VELEZ, Bothe HANS, Martin MAQUIVAR, Zhihua JIANG. [J]. Journal of Integrative Agriculture, 2023, 22(6): 1820-1832.

Meagan J. STOTTS, Yangzi ZHANG, Shuwen ZHANG, Jennifer J. MICHAL, Juan VELEZ, Bothe HANS, Martin MAQUIVAR, Zhihua JIANG.

Alternative polyadenylation events in epithelial cells sense endometritis progression in dairy cows [J]. Journal of Integrative Agriculture, 2023, 22(6): 1820-1832.

参考文献

Afonso-Grunz F. 2015. Putative alternative polyadenylation (APA) events in the early interaction of Salmonella enterica Typhimurium and human host cells. Genomics Data, 6, 222–227.

Barlund C S, Carruthers T D, Waldner C L, Palmer C W. 2008. A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology, 69, 714–723.

Brutman J N, Zhou X, Zhang Y, Michal J, Stark B, Jiang Z, Davis J F. 2018. Mapping diet-induced alternative polyadenylation of hypothalamic transcripts in the obese rat. Physiology & Behavior, 188, 173–180.

Chapwanya A, Meade K G, Narciandi F, Stanley P, Mee J F, Doherty M L, Callanan J J, O’Farrelly C. 2010. Endometrial biopsy: A valuable clinical and research tool in bovine reproduction. Theriogenology, 73, 988–994.

Cheng Y, Chen G, Hu M, Huang J, Li B, Zhou L, Hong L. 2015. Has-miR-30a regulates autophagic activity in cervical cancer upon hydroxycamptothecin exposure. Biomedicine & Pharmacotherapy, 75, 67–74.

Chomczynski P. 1993. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques, 15, 532–534.

Crozat K, Eidenschenk C, Jaeger B N, Krebs P, Guia S, Beutler B, Vivier E, Ugolini S. 2011. Impact of β2 integrin deficiency on mouse natural killer cell development and function. Blood, 117, 2874–2882.

Demolli S, Doebele C, Doddaballapur A, Lang V, Fisslthaler B, Chavakis E, Vinciguerra M, Sciacca S, Henschler R, Hecker M, Savant S, Augustin H G, Kaluza D, Dimmeler S, Boon R A. 2015. MicroRNA-30 mediates anti-inflammatory effects of shear stress and KLF2 via repression of angiopoietin 2. Journal of Molecular and Cellular Cardiology, 88, 111–119.

Dubuc J, Duffield T F, Leslie K E, Walton J S, LeBlanc S J. 2011. Randomized clinical trial of antibiotic and prostaglandin treatments for uterine health and reproductive performance in dairy cows. Journal of Dairy Science, 94, 1325–1338.

Enuka Y, Hanukoglu I, Edelheit O, Vaknine H, Hanukoglu A. 2012. Epithelial sodium channels (EnaC) are uniformly distributed on motile cilia in the oviduct and the respiratory airways. Histochemistry and Cell Biology, 137, 339–353.

Faddaoui A, Bachvarova M, Plante M, Gregoire J, Renaud M C, Sebastianelli A, Gobeil S, Morin C, Macdonald E, Vanderhyden B, Bachvarov D. 2016. The mannose receptor LY75 (DEC205/CD205) modulates cellular phenotype and metastatic potential of ovarian cancer cells. Oncotarget, 7, 14125–14142.

Foley C, Chapwanya A, Callanan J J, Whiston R, Miranda-CasoLuengo R, Lu J, Meijer W G, Lynn D J, O’Farrelly C, Meade K G. 2015. Integrated analysis of the local and systemic changes preceding the development of post-partum cytological endometritis. BMC Genomics, 16, 811.

Fumagalli L, Zhang H, Baruzzi A, Lowell C A, Berton G. 2007. The Src family kinases Hck and Fgr regulate neutrophil responses to N-formyl-methionyl-leucyl-phenylalanine. Journal of Immunology, 178, 3874–3885.

Hagiwara H, Ohwada N, Aoki T, Takata K. 2000. Ciliogenesis and ciliary abnormalities. Medical Electron Microscopy, 33, 109–114.

Heppelmann M, Weinert M, Ulbrich S E, Brommling A, Piechotta M, Merbach S, Schoon H A, Hoedemaker M, Bollwein H. 2016. The effect of puerperal uterine disease on histopathologic findings and mRNA expression of proinflammatory cytokines of the endometrium in dairy cows. Theriogenology, 85, 1348–1356.

Honke N, Shaabani N, Hardt C, Krings C, Häussinger D, Lang P A, Lang KS, Keitel V. 2017. Farnesoid X receptor in mice prevents severe liver immunopathology during lymphocytic choriomeningitis virus infection. Cellular Physiology and Biochemistry, 41, 323–338.

Jiang Z, Zhou X, Li R, Michal J J, Zhang S, Dodson M V, Zhang Z, Harland R M. 2015. Whole transcriptome analysis with sequencing: Methods, challenges and potential solutions. Cellular and Molecular Life Sciences, 72, 3425–3439.

Kaczorowski C C, Stodola T J, Hoffmann B R, Prisco A R, Liu P Y, Didier D N, Karcher J R, Liang M, Jacob H J, Greene A S. 2013. Targeting the endothelial progenitor cell surface proteome to identify novel mechanisms that mediate angiogenic efficacy in a rodent model of vascular disease. Physiological Genomics, 45, 999–1011.

LeBlanc S J, Duffield T F, Leslie K E, Bateman K G, Keefe G P, Walton J S, Johnson W H. 2002. Defining and diagnosing postpartum clinical endometritis and its impact on reproductive performance in dairy cows. Journal of Dairy Science, 85, 2223–2236.

Li J, He L, Zhang Y, Xue C, Cao Y. 2017. A novel method for genome-wide profiling of dynamic host-pathogen interactions using 3´ end enriched RNA-seq. Scientific Reports, 7, 8681.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Maquivar M G, Barragan A A, Velez J S, Bothe H, Schuenemann G M. 2015. Effect of intrauterine dextrose on reproductive performance of lactating dairy cows diagnosed with purulent vaginal discharge under certified organic management. Journal of Dairy Science, 98, 3876–3886.

van der Meer J H, van der Poll T, van´t Veer C. 2014. TAM receptors, Gas6, and protein S: Roles in inflammation and hemostasis. Blood, 123, 2460–2469.

Mido S, Murata N, Rawy M S, Kitahara G, Osawa T. 2016. Effects of intrauterine infusion of poviodine-iodine on endometrial cytology and bacteriology in dairy cows with clinical endometritis. The Journal of Veterinary Medical Science, 78, 551–556.

Moiani A, Paleari Y, Sartori D, Mezzadra R, Miccio A, Cattoglio C, Cocchiarella F, Lidonnici M R, Ferrari G, Mavilio F. 2012. Lentiviral vector integration in the human genome induces alternative splicing and generates aberrant transcripts. The Journal of Clinical Investigation, 122, 1653–1666.

NRC (National Research Council). 2001. Nutrient Requirements of Dairy Cattle. 7th ed. The National Academies Press, Washington, D.C.

Park Y R, Kim S L, Lee M R, Seo S Y, Lee J H, Kim S H, Kim I H, Lee S O, Lee S T, Kim S W. 2017. MicroRNA-30a-5p (miR-30a) regulates cell motility and EMT by directly targeting oncogenic TM4SF1 in colorectal cancer. Journal of Cancer Research and Clinical Oncology, 143, 1915–1927.

Pascottini O B, Dini P, Hostens M, Ducatelle R, Opsomer G. 2015. A novel cytologic sampling technique to diagnose subclinical endometritis and comparison of staining methods for endometrial cytology samples in dairy cows. Theriogenology, 84, 1438–1446.

Prabowo A S, van Scheppingen J, Iyer A M, Anink J J, Spliet W G, van Rijen P C, Schouten-van Meeteren A Y, Aronica E. 2015. Differential expression and clinical significance of three inflammation-related microRNAs in gangliogliomas. Journal of Neuroinflammation, 12, 97.

Salilew-Wondim D, Ibrahim S, Gebremedhn S, Tesfaye D, Heppelmann M, Bollwein H, Pfarrer C, Tholen E, Neuhoff C, Schellander K, Hoelker M. 2016. Clinical and subclinical endometritis induced alterations in bovine endometrial transcriptome and miRNome profile. BMC Genomics, 17, 218.

Shannon P, Markiel A, Ozier O, Baliga N S, Wang J T, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498–2504.

Sheldon I M, Cronin J, Goetze L, Donofrio G, Schuberth H J. 2009. Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction, 81, 1025–1032.

Sheldon I M, Cronin J G, Pospiech M, Turner M L. 2018. Symposium review: Mechanisms linking metabolic stress with innate immunity in the endometrium. Journal of Dairy Science, 101, 3655–3664.

Sheldon I M, Lewis G S, LeBlanc S, Gilbert R O. 2006. Defining postpartum uterine disease in cattle. Theriogenology, 65, 1516–1530.

Stefanová I, Horejsí V. 1991. Association of the CD59 and CD55 cell surface glycoproteins with other membrane molecules. Journal of Immunology, 147, 1587–1592.

Sumitomo T, Nakata M, Higashino M, Yamaguchi M, Kawabata S. 2016. Group A Streptococcus exploits human plasminogen for bacterial translocation across epithelial barrier via tricellular tight junctions. Scientific Reports, 7, 20069.

Szklarczyk D, Morris J H, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva N T, Roth A, Bork P, Jensen L J, Mering C. 2017. The STRING database in 2017: Quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Research, 45, D362–D368.

Tripathi S, Pohl M O, Zhou Y, Rodriguez-Frandsen A, Wang G, Stein D A, Moulton H M, DeJesus P, Che J, Mulder L C, Yanguez E, Andenmatten D, Pache L, Manicassamy B, Albrecht R A, Gonzalez M G, Nguyen Q, Brass A, Elledges S, White M, et al. 2015. Meta- and orthogonal integration of influenza “OMICs” data defines a role for UBR4 in virus budding. Cell Host & Microbe, 18, 723–735.

Wang R, Nambiar R, Zheng D, Tian B. 2018. PolyA_DB 3 catalogs cleavage and polyadenylation sites identified by deep sequencing in multiple genomes. Nucleic Acids Research, 46, D315–D319.

Wang S, Burton J C, Behringer R R, Larina I V. 2015. In vivo micro-scale tomography of ciliary behavior in the mammalian oviduct. Scientific Reports, 5, 13216.

Williams E J, Fischer D P, Pfeiffer D U, England G C W, Noakes D E, Dobson H, Sheldon I M. 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology, 63, 102–117.

Zhang R, Yan S, Wang J, Deng F, Guo Y, Li Y, Fan M, Song Q, Liu H, Weng Y, Shi Q. 2016. MiR-30a regulates the proliferation, migration, and invasion of human osteosarcoma by targeting Runx2. Tumour Biology, 37, 3479–3488.

Zhang S, Zhang Y, Zhou X, Fu X, Michal J J, Ji G, Du M, Davis J F, Jiang Z. 2018. Alternative polyadenylation drives genome-to-phenome information detours in the AMPKα1 and AMPKα2 knockout mice. Scientific Reports, 8, 6462.

Zhou X, Li R, Michal J J, Wu X L, Liu Z, Zhao H, Xia Y, Du W, Wildung M R, Pouchnik D J, Harland R M, Jiang Z. 2016. Accurate profiling of gene expression and alternative polyadenylation with whole transcriptome termini site sequencing (WTTS-Seq). Genetics, 203, 683–697.

Zhou X, Zhang Y, Michal J J, Qu L, Zhang S, Wildung M R, Du W, Pouchnik D J, Zhao H, Xia Y, Shi H, Ji G, Davis J F, Smith G D, Griswold M D, Harland R M, Jiang Z. 2019. Alternative polyadenylation coordinates embryonic development, sexual dimorphism and longitudinal growth in Xenopus tropicalis. Cellular and Molecular Life Sciences, 76, 2185–2198.

Alternative polyadenylation events in epithelial cells sense endometritis progression in dairy cows

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics