FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Vet Res / Transcriptomic analysis of equine chorioallantois reveals im...
Veterinary research2021; 52(1); 103; doi: 10.1186/s13567-021-00972-4

Transcriptomic analysis of equine chorioallantois reveals immune networks and molecular mechanisms involved in nocardioform placentitis.

Abstract: Nocardioform placentitis (NP) continues to result in episodic outbreaks of abortion and preterm birth in mares and remains a poorly understood disease. The objective of this study was to characterize the transcriptome of the chorioallantois (CA) of mares with NP. The CA were collected from mares with confirmed NP based upon histopathology, microbiological culture and PCR for Amycolatopsis spp. Samples were collected from the margin of the NP lesion (NPL, n = 4) and grossly normal region (NPN, n = 4). Additionally, CA samples were collected from normal postpartum mares (Control; CRL, n = 4). Transcriptome analysis identified 2892 differentially expressed genes (DEGs) in NPL vs. CRL and 2450 DEGs in NPL vs. NPN. Functional genomics analysis elucidated that inflammatory signaling, toll-like receptor signaling, inflammasome activation, chemotaxis, and apoptosis pathways are involved in NP. The increased leukocytic infiltration in NPL was associated with the upregulation of matrix metalloproteinase (MMP1, MMP3, and MMP8) and apoptosis-related genes, such as caspases (CASP3 and CASP7), which could explain placental separation associated with NP. Also, NP was associated with downregulation of several placenta-regulatory genes (ABCG2, GCM1, EPAS1, and NR3C1), angiogenesis-related genes (VEGFA, FLT1, KDR, and ANGPT2), and glucose transporter coding genes (GLUT1, GLUT10, and GLUT12), as well as upregulation of hypoxia-related genes (HIF1A and EGLN3), which could elucidate placental insufficiency accompanying NP. In conclusion, our findings revealed for the first time, the key regulators and mechanisms underlying placental inflammation, separation, and insufficiency during NP, which might lead to the development of efficacious therapies or diagnostic aids by targeting the key molecular pathways.
Get Full Text
Publication Date: 2021-07-08 PubMed ID: 34238364PubMed Central: PMC8268225DOI: 10.1186/s13567-021-00972-4Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article focuses on a comprehensive transcriptomic analysis of the equine chorioallantois in nocardioform placentitis, a disease responsible for abortions and preterm birth in mares. The study brings out the immune responses, key gene interactions, and molecular mechanisms involved in the disease, possibly directing the development of targeted therapeutic interventions.

Research Objective and Methodology

The core objective of the research was to understand the genetic aspects of nocardioform placentitis (NP) through the transcriptome analysis of the chorioallantois (CA), a crucial structure involved in gas and nutrient exchange during pregnancy. Chorioallantois samples were collected from mares diagnosed with NP (both from the lesion’s region and the grossly normal region). For comparison, similar samples were collected from normal post-birth mares.

Key Findings and Analysis

  • Transcriptome analysis revealed a total of 2892 and 2450 differentially expressed genes when compared between the NP lesion (NPL) and normal postpartum samples, and between NPL and the grossly normal region in NP (NPN) respectively.
  • Functional genomics pointed at key pathways like inflammatory signaling, toll-like receptor signaling, inflammasome activation, chemotaxis, and apoptosis being integral to NP pathogenesis.
  • An increase in leukocytic infiltration in NPL associated with the upregulation of certain genes like MMP1, MMP3, MMP8, and apoptosis-related genes (CASP3 and CASP7), providing a plausible explanation for placental separation correlated with NP.
  • The study also observed the downregulation of several placenta-regulatory genes, angiogenesis-related genes, and glucose transporter genes, and upregulation of hypoxia-related genes. These changes could decipher the origins of placental insufficiency seen in NP cases.

    • Conclusions and Significance

  • The research provides first-hand insight into molecular mechanisms, key regulators, and altered gene expressions involved in placental inflammation, separation, and insufficiency during NP.
  • These findings can act as a platform to develop effective therapies and diagnostic aids for NP, targeting the abnormalities in key molecular pathways.

    • Cite This Article

    APA
    El-Sheikh Ali H, Loux SC, Kennedy L, Scoggin KE, Dini P, Fedorka CE, Kalbfleisch TS, Esteller-Vico A, Horohov DW, Erol E, Carter CN, Smith JL, Ball BA. (2021). Transcriptomic analysis of equine chorioallantois reveals immune networks and molecular mechanisms involved in nocardioform placentitis. Vet Res, 52(1), 103. https://doi.org/10.1186/s13567-021-00972-4

    Publication

    Veterinary research
    ISSN: 1297-9716
    NlmUniqueID: 9309551
    Country: England
    Language: English
    Volume: 52
    Issue: 1
    Pages: 103
    PII: 103

    Researcher Affiliations

    El-Sheikh Ali, Hossam
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    • Theriogenology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura, 35516, Egypt.
    Loux, Shavahn C
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Kennedy, Laura
    • UK Veterinary Diagnostic Laboratory, University of Kentucky, Lexington, KY, 40546, USA.
    Scoggin, Kirsten E
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Dini, Pouya
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Fedorka, Carleigh E
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Kalbfleisch, Theodore S
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Esteller-Vico, Alejandro
    • Department of Biomedical and Diagnostic Sciences, University of Tennessee, Knoxville, USA.
    Horohov, David W
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
    Erol, Erdal
    • UK Veterinary Diagnostic Laboratory, University of Kentucky, Lexington, KY, 40546, USA.
    Carter, Craig N
    • UK Veterinary Diagnostic Laboratory, University of Kentucky, Lexington, KY, 40546, USA.
    Smith, Jackie L
    • UK Veterinary Diagnostic Laboratory, University of Kentucky, Lexington, KY, 40546, USA.
    Ball, Barry A
    • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA. b.a.ball@uky.edu.

    MeSH Terms

    • Actinobacteria / isolation & purification
    • Amycolatopsis / isolation & purification
    • Animals
    • Chorioamnionitis / immunology
    • Chorioamnionitis / microbiology
    • Chorioamnionitis / veterinary
    • Female
    • Gene Expression Profiling / veterinary
    • Gram-Positive Bacterial Infections / immunology
    • Gram-Positive Bacterial Infections / microbiology
    • Gram-Positive Bacterial Infections / veterinary
    • Horse Diseases / immunology
    • Horse Diseases / microbiology
    • Horses
    • Pregnancy
    • Transcriptome

    Conflict of Interest Statement

    The authors declare that they have no competing interests.

    References

    This article includes 75 references
    1. Donahue JM, Williams NM. Emergent causes of placentitis and abortion.. Vet Clin North Am Equine Pract 2000 Dec;16(3):443-56, viii.
      pubmed: 11219342doi: 10.1016/s0749-0739(17)30088-3google scholar: lookup
    2. Hong CB, Donahue JM, Giles RC Jr, Petrites-Murphy MB, Poonacha KB, Roberts AW, Smith BJ, Tramontin RR, Tuttle PA, Swerczek TW. Etiology and pathology of equine placentitis.. J Vet Diagn Invest 1993 Jan;5(1):56-63.
      doi: 10.1177/104063879300500113pubmed: 8466982google scholar: lookup
    3. Giles R, Hong C, Donahue J, Swerczek T, Poonacha K, Tuttle P, Tramontin R. Equine abortion caused by a gram-positive filamentous bacterium. In: Proceedings 37th Annual Meeting, American College of Veterinary Pathologists.
    4. Carter C, Erol E, Cohen N, Smith J. Diagnostic epidemiology of nocardioform placentitis and abortion in Kentucky, 1991–2015. J Equine Vet Sci 2016;39:S59–S60.
      doi: 10.1016/j.jevs.2016.02.129google scholar: lookup
    5. Christensen BW, Roberts JF, Pozor MA, Giguere S, Sells SF, Donahue JM. Nocardioform placentitis with isolation of Amycolatopsis spp in a Florida-bred mare.. J Am Vet Med Assoc 2006 Apr 15;228(8):1234-9.
      doi: 10.2460/javma.228.8.1234pubmed: 16618229google scholar: lookup
    6. Volkmann DH, Williams JH, Henton JH, Donahue JM, Williams NM. The first reported case of equine nocardioform placentitis in South Africa.. J S Afr Vet Assoc 2001 Dec;72(4):235-8.
      doi: 10.4102/jsava.v72i4.659pubmed: 12219921google scholar: lookup
    7. Cattoli G, Vascellari M, Corrò M, Capua I, Mutinelli F, Sells SF, Donahue JM. First case of equine nocardioform placentitis caused by Crossiella equi in Europe.. Vet Rec 2004 Jun 5;154(23):730-1.
      doi: 10.1136/vr.154.23.730pubmed: 15214520google scholar: lookup
    8. Hanlon DW, McLachlan AD, Gibson I. The first reported case of equine Nocardioform placentitis in New Zealand.. N Z Vet J 2016 May;64(3):198-9.
      doi: 10.1080/00480169.2015.1120166pubmed: 26584411google scholar: lookup
    9. Labeda DP, Price NP, Kroppenstedt RM, Donahue JM, Williams NM, Sells SF. Streptomyces atriruber sp. nov. and Streptomyces silaceus sp. nov., two novel species of equine origin.. Int J Syst Evol Microbiol 2009 Nov;59(Pt 11):2899-903.
      doi: 10.1099/ijs.0.008862-0pubmed: 19628594google scholar: lookup
    10. Erol E, Sells SF, Williams NM, Kennedy L, Locke SJ, Labeda DP, Donahue JM, Carter CN. An investigation of a recent outbreak of nocardioform placentitis caused abortions in horses.. Vet Microbiol 2012 Aug 17;158(3-4):425-30.
      doi: 10.1016/j.vetmic.2012.02.023pubmed: 22410309google scholar: lookup
    11. Canisso IF, Ball BA, Erol E, Claes A, Scoggin KE, McDowell KJ, Williams NM, Dorton AR, Wolfsdorf KE, Squires EL, Troedsson MH. Attempts to induce nocardioform placentitis (Crossiela equi) experimentally in mares.. Equine Vet J 2015 Jan;47(1):91-5.
      doi: 10.1111/evj.12249pubmed: 24612109google scholar: lookup
    12. El-Sheikh Ali H, Boakari YL, Loux SC, Dini P, Scoggin KE, Esteller-Vico A, Kalbfleisch T, Ball BA. Transcriptomic analysis reveals the key regulators and molecular mechanisms underlying myometrial activation during equine placentitis†.. Biol Reprod 2020 May 26;102(6):1306-1325.
      doi: 10.1093/biolre/ioaa020pubmed: 32065222google scholar: lookup
    13. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
      doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
    14. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks.. Nat Protoc 2012 Mar 1;7(3):562-78.
      doi: 10.1038/nprot.2012.016pmc: PMC3334321pubmed: 22383036google scholar: lookup
    15. Warnes MGR, Bolker B, Bonebakker L, Gentleman R. Package ‘gplots’. Various R Programming Tools for Plotting Data. .
    16. Langfelder P, Horvath S. The weighted gene co-expression network analysis (WGCNA) package. .
    17. Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis.. Stat Appl Genet Mol Biol 2005;4:Article17.
      pubmed: 16646834doi: 10.2202/1544-6115.1128google scholar: lookup
    18. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis.. BMC Bioinformatics 2008 Dec 29;9:559.
      doi: 10.1186/1471-2105-9-559pmc: PMC2631488pubmed: 19114008google scholar: lookup
    19. Abedi M, Gheisari Y. Nodes with high centrality in protein interaction networks are responsible for driving signaling pathways in diabetic nephropathy.. PeerJ 2015;3:e1284.
      doi: 10.7717/peerj.1284pmc: PMC4636410pubmed: 26557424google scholar: lookup
    20. Ramilowski JA, Goldberg T, Harshbarger J, Kloppmann E, Lizio M, Satagopam VP, Itoh M, Kawaji H, Carninci P, Rost B, Forrest AR. A draft network of ligand-receptor-mediated multicellular signalling in human.. Nat Commun 2015 Jul 22;6:7866.
      doi: 10.1038/ncomms8866pmc: PMC4525178pubmed: 26198319google scholar: lookup
    21. Andersen CL, Jensen JL, Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets.. Cancer Res 2004 Aug 1;64(15):5245-50.
      doi: 10.1158/0008-5472.CAN-04-0496pubmed: 15289330google scholar: lookup
    22. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data.. Nucleic Acids Res 2009 Apr;37(6):e45.
      doi: 10.1093/nar/gkp045pmc: PMC2665230pubmed: 19237396google scholar: lookup
    23. Ball BA, Scoggin KE, Troedsson MH, Squires EL. Characterization of prostaglandin E2 receptors (EP2, EP4) in the horse oviduct.. Anim Reprod Sci 2013 Nov 1;142(1-2):35-41.
      doi: 10.1016/j.anireprosci.2013.07.009pubmed: 24035156google scholar: lookup
    24. El-Sheikh Ali H, Dini P, Scoggin K, Loux S, Fedorka C, Boakari Y, Norris J, Esteller-Vico A, Kalbfleisch T, Ball B. Transcriptomic analysis of equine placenta reveals key regulators and pathways involved in ascending placentitis†.. Biol Reprod 2021 Mar 11;104(3):638-656.
      doi: 10.1093/biolre/ioaa209pubmed: 33345276google scholar: lookup
    25. LeBlanc MM, Giguère S, Lester GD, Brauer K, Paccamonti DL. Relationship between infection, inflammation and premature parturition in mares with experimentally induced placentitis.. Equine Vet J Suppl 2012 Feb;(41):8-14.
      doi: 10.1111/j.2042-3306.2011.00502.xpubmed: 22594019google scholar: lookup
    26. LeBlanc M. Premature delivery in ascending placentitis is associated with increased expression of placental cytokines and allantoic fluid prostaglandins E2 and F2α. Theriogenology 2002;58:841–844.
      doi: 10.1016/S0093-691X(02)00822-1google scholar: lookup
    27. Ackerman WE 4th, Buhimschi IA, Eidem HR, Rinker DC, Rokas A, Rood K, Zhao G, Summerfield TL, Landon MB, Buhimschi CS. Comprehensive RNA profiling of villous trophoblast and decidua basalis in pregnancies complicated by preterm birth following intra-amniotic infection.. Placenta 2016 Aug;44:23-33.
      doi: 10.1016/j.placenta.2016.05.010pubmed: 27452435google scholar: lookup
    28. Fedorka CE, Ball BA, Wynn MAA, McCormick ME, Scoggin KE, Esteller-Vico A, Curry TE, Kennedy LA, Squires EL, Troedsson MHT. Alterations of Circulating Biomarkers During Late Term Pregnancy Complications in the Horse Part II: Steroid Hormones and Alpha-Fetoprotein.. J Equine Vet Sci 2021 Apr;99:103395.
      doi: 10.1016/j.jevs.2021.103395pubmed: 33781417google scholar: lookup
    29. Fedorka CE, Ball BA, Walker OF, McCormick ME, Scoggin KE, Kennedy LA, Squires EL, Troedsson MHT. Alterations of Circulating Biomarkers During Late Term Pregnancy Complications in the Horse Part I: Cytokines.. J Equine Vet Sci 2021 Apr;99:103425.
      doi: 10.1016/j.jevs.2021.103425pubmed: 33781421google scholar: lookup
    30. Migale R, MacIntyre DA, Cacciatore S, Lee YS, Hagberg H, Herbert BR, Johnson MR, Peebles D, Waddington SN, Bennett PR. Modeling hormonal and inflammatory contributions to preterm and term labor using uterine temporal transcriptomics.. BMC Med 2016 Jun 13;14(1):86.
      doi: 10.1186/s12916-016-0632-4pmc: PMC4904357pubmed: 27291689google scholar: lookup
    31. Bollapragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix.. Am J Obstet Gynecol 2009 Jan;200(1):104.e1-11.
      pubmed: 19121663doi: 10.1016/j.ajog.2008.08.032google scholar: lookup
    32. Blank V, Hirsch E, Challis JR, Romero R, Lye SJ. Cytokine signaling, inflammation, innate immunity and preterm labour - a workshop report.. Placenta 2008 Mar;29 Suppl A:S102-4.
      doi: 10.1016/j.placenta.2007.10.011pubmed: 18082255google scholar: lookup
    33. Medzhitov R. Toll-like receptors and innate immunity.. Nat Rev Immunol 2001 Nov;1(2):135-45.
      doi: 10.1038/35100529pubmed: 11905821google scholar: lookup
    34. Waring GJ, Robson SC, Bulmer JN, Tyson-Capper AJ. Inflammatory Signalling in Fetal Membranes: Increased Expression Levels of TLR 1 in the Presence of Preterm Histological Chorioamnionitis.. PLoS One 2015;10(5):e0124298.
      doi: 10.1371/journal.pone.0124298pmc: PMC4429010pubmed: 25965269google scholar: lookup
    35. Adams Waldorf KM, Persing D, Novy MJ, Sadowsky DW, Gravett MG. Pretreatment with toll-like receptor 4 antagonist inhibits lipopolysaccharide-induced preterm uterine contractility, cytokines, and prostaglandins in rhesus monkeys.. Reprod Sci 2008 Feb;15(2):121-7.
      doi: 10.1177/1933719107310992pmc: PMC2774271pubmed: 18187405google scholar: lookup
    36. Robertson SA, Wahid HH, Chin PY, Hutchinson MR, Moldenhauer LM, Keelan JA. Toll-like Receptor-4: A New Target for Preterm Labour Pharmacotherapies?. Curr Pharm Des 2018;24(9):960-973.
      doi: 10.2174/1381612824666180130122450pubmed: 29384054google scholar: lookup
    37. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases.. Annu Rev Immunol 2011;29:707-35.
      doi: 10.1146/annurev-immunol-031210-101405pmc: PMC4067317pubmed: 21219188google scholar: lookup
    38. Gomez-Lopez N, Motomura K, Miller D, Garcia-Flores V, Galaz J, Romero R. Inflammasomes: Their Role in Normal and Complicated Pregnancies.. J Immunol 2019 Dec 1;203(11):2757-2769.
      doi: 10.4049/jimmunol.1900901pmc: PMC6871659pubmed: 31740550google scholar: lookup
    39. Gomez-Lopez N, Romero R, Garcia-Flores V, Leng Y, Miller D, Hassan SS, Hsu CD, Panaitescu B. Inhibition of the NLRP3 inflammasome can prevent sterile intra-amniotic inflammation, preterm labor/birth, and adverse neonatal outcomes†.. Biol Reprod 2019 May 1;100(5):1306-1318.
      doi: 10.1093/biolre/ioy264pmc: PMC6497524pubmed: 30596885google scholar: lookup
    40. Pereyra S, Sosa C, Bertoni B, Sapiro R. Transcriptomic analysis of fetal membranes reveals pathways involved in preterm birth.. BMC Med Genomics 2019 Apr 1;12(1):53.
      doi: 10.1186/s12920-019-0498-3pmc: PMC6444860pubmed: 30935390google scholar: lookup
    41. Arcuri F, Toti P, Buchwalder L, Casciaro A, Cintorino M, Schatz F, Rybalov B, Lockwood CJ. Mechanisms of leukocyte accumulation and activation in chorioamnionitis: interleukin 1 beta and tumor necrosis factor alpha enhance colony stimulating factor 2 expression in term decidua.. Reprod Sci 2009 May;16(5):453-61.
      doi: 10.1177/1933719108328609pmc: PMC3046766pubmed: 19164476google scholar: lookup
    42. Romero R, Chaemsaithong P, Korzeniewski SJ, Tarca AL, Bhatti G, Xu Z, Kusanovic JP, Dong Z, Docheva N, Martinez-Varea A, Yoon BH, Hassan SS, Chaiworapongsa T, Yeo L. Clinical chorioamnionitis at term II: the intra-amniotic inflammatory response.. J Perinat Med 2016 Jan;44(1):5-22.
      pmc: PMC5891100pubmed: 25938217doi: 10.1515/jpm-2015-0045google scholar: lookup
    43. Presicce P, Park CW, Senthamaraikannan P, Bhattacharyya S, Jackson C, Kong F, Rueda CM, DeFranco E, Miller LA, Hildeman DA, Salomonis N, Chougnet CA, Jobe AH, Kallapur SG. IL-1 signaling mediates intrauterine inflammation and chorio-decidua neutrophil recruitment and activation.. JCI Insight 2018 Mar 22;3(6).
      doi: 10.1172/jci.insight.98306pmc: PMC5926925pubmed: 29563340google scholar: lookup
    44. Sundrani DP, Chavan-Gautam PM, Pisal HR, Mehendale SS, Joshi SR. Matrix metalloproteinase-1 and -9 in human placenta during spontaneous vaginal delivery and caesarean sectioning in preterm pregnancy.. PLoS One 2012;7(1):e29855.
      doi: 10.1371/journal.pone.0029855pmc: PMC3257231pubmed: 22253805google scholar: lookup
    45. Takagi M, Yamamoto D, Ohtani M, Miyamoto A. Quantitative analysis of messenger RNA expression of matrix metalloproteinases (MMP-2 and MMP-9), tissue inhibitor-2 of matrix metalloproteinases (TIMP-2), and steroidogenic enzymes in bovine placentomes during gestation and postpartum.. Mol Reprod Dev 2007 Jul;74(7):801-7.
      doi: 10.1002/mrd.20637pubmed: 17154296google scholar: lookup
    46. Xu P, Alfaidy N, Challis JR. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in human placenta and fetal membranes in relation to preterm and term labor.. J Clin Endocrinol Metab 2002 Mar;87(3):1353-61.
      doi: 10.1210/jcem.87.3.8320pubmed: 11889208google scholar: lookup
    47. Riley SC, Webb CJ, Leask R, McCaig FM, Howe DC. Involvement of matrix metalloproteinases 2 and 9, tissue inhibitor of metalloproteinases and apoptosis in tissue remodelling in the sheep placenta.. J Reprod Fertil 2000 Jan;118(1):19-27.
      doi: 10.1530/jrf.0.1180019pubmed: 10793622google scholar: lookup
    48. Weiss A, Goldman S, Shalev E. The matrix metalloproteinases (MMPS) in the decidua and fetal membranes.. Front Biosci 2007 Jan 1;12:649-59.
      doi: 10.2741/2089pubmed: 17127325google scholar: lookup
    49. Tribe RM. Small Peptides with a Big Role: Antimicrobial Peptides in the Pregnant Female Reproductive Tract.. Am J Reprod Immunol 2015 Aug;74(2):123-5.
      doi: 10.1111/aji.12379pubmed: 25773319google scholar: lookup
    50. Ganz T. Defensins: antimicrobial peptides of innate immunity.. Nat Rev Immunol 2003 Sep;3(9):710-20.
      doi: 10.1038/nri1180pubmed: 12949495google scholar: lookup
    51. Bruhn O, Grötzinger J, Cascorbi I, Jung S. Antimicrobial peptides and proteins of the horse--insights into a well-armed organism.. Vet Res 2011 Sep 2;42(1):98.
      doi: 10.1186/1297-9716-42-98pmc: PMC3179947pubmed: 21888650google scholar: lookup
    52. Tambor V, Kacerovsky M, Lenco J, Bhat G, Menon R. Proteomics and bioinformatics analysis reveal underlying pathways of infection associated histologic chorioamnionitis in pPROM.. Placenta 2013 Feb;34(2):155-61.
      doi: 10.1016/j.placenta.2012.11.028pubmed: 23246098google scholar: lookup
    53. Espinoza J, Chaiworapongsa T, Romero R, Edwin S, Rathnasabapathy C, Gomez R, Bujold E, Camacho N, Kim YM, Hassan S, Blackwell S, Whitty J, Berman S, Redman M, Yoon BH, Sorokin Y. Antimicrobial peptides in amniotic fluid: defensins, calprotectin and bacterial/permeability-increasing protein in patients with microbial invasion of the amniotic cavity, intra-amniotic inflammation, preterm labor and premature rupture of membranes.. J Matern Fetal Neonatal Med 2003 Jan;13(1):2-21.
      doi: 10.1080/jmf.13.1.2.21pubmed: 12710851google scholar: lookup
    54. Lei J, Sun L, Huang S, Zhu C, Li P, He J, Mackey V, Coy DH, He Q. The antimicrobial peptides and their potential clinical applications.. Am J Transl Res 2019;11(7):3919-3931.
      pmc: PMC6684887pubmed: 31396309
    55. Pfalzgraff A, Brandenburg K, Weindl G. Antimicrobial Peptides and Their Therapeutic Potential for Bacterial Skin Infections and Wounds.. Front Pharmacol 2018;9:281.
      doi: 10.3389/fphar.2018.00281pmc: PMC5882822pubmed: 29643807google scholar: lookup
    56. Erlebacher A. Mechanisms of T cell tolerance towards the allogeneic fetus.. Nat Rev Immunol 2013 Jan;13(1):23-33.
      doi: 10.1038/nri3361pubmed: 23237963google scholar: lookup
    57. Figueiredo AS, Schumacher A. The T helper type 17/regulatory T cell paradigm in pregnancy.. Immunology 2016 May;148(1):13-21.
      doi: 10.1111/imm.12595pmc: PMC4819144pubmed: 26855005google scholar: lookup
    58. Cobo T, Kacerovsky M, Palacio M, Hornychova H, Hougaard DM, Skogstrand K, Jacobsson B. A prediction model of histological chorioamnionitis and funisitis in preterm prelabor rupture of membranes: analyses of multiple proteins in the amniotic fluid.. J Matern Fetal Neonatal Med 2012 Oct;25(10):1995-2001.
      doi: 10.3109/14767058.2012.666592pubmed: 22372866google scholar: lookup
    59. Rito DC, Viehl LT, Buchanan PM, Haridas S, Koenig JM. Augmented Th17-type immune responses in preterm neonates exposed to histologic chorioamnionitis.. Pediatr Res 2017 Apr;81(4):639-645.
      doi: 10.1038/pr.2016.254pmc: PMC5395318pubmed: 27870827google scholar: lookup
    60. Singh AM, Sherenian MG, Kim KY, Erickson KA, Yang A, Mestan K, Ernst LM, Kumar R. Fetal cord blood and tissue immune responses to chronic placental inflammation and chorioamnionitis.. Allergy Asthma Clin Immunol 2018;14:66.
      doi: 10.1186/s13223-018-0297-ypmc: PMC6240933pubmed: 30473713google scholar: lookup
    61. Guo Z, Xu Y, Zheng Q, Liu Y, Liu X. Analysis of chromosomes and the T helper 17 and regulatory T cell balance in patients with recurrent spontaneous abortion.. Exp Ther Med 2020 Apr;19(4):3159-3166.
      pmc: PMC7086275pubmed: 32256804doi: 10.3892/etm.2020.8537google scholar: lookup
    62. Zhao X, Jiang Y, Wang L, Li Z, Li Q, Feng X. Advances in Understanding the Immune Imbalance between T-Lymphocyte Subsets and NK Cells in Recurrent Spontaneous Abortion.. Geburtshilfe Frauenheilkd 2018 Jul;78(7):677-683.
      doi: 10.1055/a-0634-1813pmc: PMC6150770pubmed: 30258242google scholar: lookup
    63. Ito M, Nakashima A, Hidaka T, Okabe M, Bac ND, Ina S, Yoneda S, Shiozaki A, Sumi S, Tsuneyama K, Nikaido T, Saito S. A role for IL-17 in induction of an inflammation at the fetomaternal interface in preterm labour.. J Reprod Immunol 2010 Jan;84(1):75-85.
      doi: 10.1016/j.jri.2009.09.005pubmed: 19969371google scholar: lookup
    64. Zahran AM, Zharan KM, Hetta HF. Significant correlation between regulatory T cells and vitamin D status in term and preterm labor.. J Reprod Immunol 2018 Sep;129:15-22.
      doi: 10.1016/j.jri.2018.07.004pubmed: 30029057google scholar: lookup
    65. Eghbal-Fard S, Yousefi M, Heydarlou H, Ahmadi M, Taghavi S, Movasaghpour A, Jadidi-Niaragh F, Yousefi B, Dolati S, Hojjat-Farsangi M, Rikhtegar R, Nouri M, Aghebati-Maleki L. The imbalance of Th17/Treg axis involved in the pathogenesis of preeclampsia.. J Cell Physiol 2019 Apr;234(4):5106-5116.
      doi: 10.1002/jcp.27315pubmed: 30277561google scholar: lookup
    66. Fedorka CE, El-Sheikh Ali H, Walker OF, Scoggin KE, Dini P, Loux SC, Troedsson MHT, Ball BA. The imbalance of the Th17/Treg axis following equine ascending placental infection.. J Reprod Immunol 2021 Apr;144:103268.
      doi: 10.1016/j.jri.2020.103268pubmed: 33454392google scholar: lookup
    67. El-Sheikh Ali H, Scoggin K, Linhares Boakari Y, Dini P, Loux S, Fedorka C, Esteller-Vico A, Ball B. Kinetics of placenta-specific 8 (PLAC8) in equine placenta during pregnancy and placentitis.. Theriogenology 2021 Jan 15;160:81-89.
      doi: 10.1016/j.theriogenology.2020.10.041pubmed: 33189077google scholar: lookup
    68. Yakar S, Werner H, Rosen CJ. Insulin-like growth factors: actions on the skeleton.. J Mol Endocrinol 2018 Jul;61(1):T115-T137.
      doi: 10.1530/JME-17-0298pmc: PMC5966339pubmed: 29626053google scholar: lookup
    69. de Vrijer B, Davidsen ML, Wilkening RB, Anthony RV, Regnault TR. Altered placental and fetal expression of IGFs and IGF-binding proteins associated with intrauterine growth restriction in fetal sheep during early and mid-pregnancy.. Pediatr Res 2006 Nov;60(5):507-12.
      doi: 10.1203/01.PDR.0000242364.78002.71pubmed: 16966353google scholar: lookup
    70. Forbes K, Westwood M. The IGF axis and placental function. a mini review.. Horm Res 2008;69(3):129-37.
      pubmed: 18219215doi: 10.1159/000112585google scholar: lookup
    71. Walker N, Filis P, Soffientini U, Bellingham M, O'Shaughnessy PJ, Fowler PA. Placental transporter localization and expression in the Human: the importance of species, sex, and gestational age differences†.. Biol Reprod 2017 Apr 1;96(4):733-742.
      doi: 10.1093/biolre/iox012pmc: PMC5441296pubmed: 28339967google scholar: lookup
    72. Dini P, Carossino M, Loynachan AT, El-Sheikh Ali H, Wolfsdorf KE, Scoggin KE, Daels P, Ball BA. Equine hydrallantois is associated with impaired angiogenesis in the placenta.. Placenta 2020 Apr;93:101-112.
      doi: 10.1016/j.placenta.2020.03.001pubmed: 32250734google scholar: lookup
    73. Gravett MG, Thomas A, Schneider KA, Reddy AP, Dasari S, Jacob T, Lu X, Rodland M, Pereira L, Sadowsky DW, Roberts CT Jr, Novy MJ, Nagalla SR. Proteomic analysis of cervical-vaginal fluid: identification of novel biomarkers for detection of intra-amniotic infection.. J Proteome Res 2007 Jan;6(1):89-96.
      doi: 10.1021/pr060149vpmc: PMC2532920pubmed: 17203952google scholar: lookup
    74. Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokström H, Holst RM, Nikolaitchouk N, Wennerholm UB, Hagberg H. Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women with preterm prelabor rupture of membranes.. Acta Obstet Gynecol Scand 2003 May;82(5):423-31.
      doi: 10.1034/j.1600-0412.2003.00157.xpubmed: 12752072google scholar: lookup
    75. Martin NM, Cooke KM, Radford CC, Perley LE, Silasi M, Flannery CA. Time course analysis of RNA quality in placenta preserved by RNAlater or flash freezing.. Am J Reprod Immunol 2017 Apr;77(4).
      doi: 10.1111/aji.12637pmc: PMC5397349pubmed: 28138995google scholar: lookup

    Citations

    This article has been cited 2 times.
    1. Fedorka CE, Ali HE, Troedsson MHT. Galectins in Equine Placental Disease.. Vet Sci 2023 Mar 13;10(3).
      doi: 10.3390/vetsci10030218pubmed: 36977257google scholar: lookup
    2. Xia B, Zhang P, Lai Y, Cui S, Chen Z, Yu Q, Wu H, Zeng L, Xie B, Li J, Zhang H, Luo S, Gao J. Research on the Mechanism of Asperosaponin VI for Treating Recurrent Spontaneous Abortion by Bioinformatics Analysis and Experimental Validation.. Evid Based Complement Alternat Med 2022;2022:8099853.
      doi: 10.1155/2022/8099853pubmed: 35783512google scholar: lookup
    Subscribe to our newsletter
    Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.