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Home / Equine Research Bank / Equine Vet J / Transcriptomic analysis of the chorioallantois in equine pre...
Equine veterinary journal2022; 55(3); 405-418; doi: 10.1111/evj.13602

Transcriptomic analysis of the chorioallantois in equine premature placental separation.

Abstract: Equine premature placental separation (PPS) is poorly understood and represents an important risk factor for fetal/neonatal hypoxia. Objective: To examine transcriptomic changes in the chorioallantois (CA) from mares with clinical PPS compared with the CA from normal foaling mares. Differential gene expression was determined and gene ontology as well as molecular pathways related to PPS were characterised. Methods: Retrospective case: control study. Methods: CA were collected from Thoroughbred mares with a clinical history of PPS (n = 33) and from control Thoroughbred mares (n = 4) with normal parturition for examination of transcriptional changes in the placenta associated with PPS. Transcriptomic changes in the villous CA near the cervical star were determined by Illumina® sequencing and subsequent bioinformatic analysis. PPS samples were divided by k-means clustering, and differentially expressed genes (DEGs) in each PPS cluster were identified by comparing to controls. Shared DEGs between PPS clusters were used for gene ontology analysis and pathway analysis. Results: A total of 1204 DEGs were identified between PPS and control. Gene ontology revealed extracellular matrix (ECM) and cell adhesion, and pathway analysis revealed fatty acid, p-53, hypoxia and inflammation. Eleven key regulator genes of PPS including growth factors (IGF1, TGFB2, TGFB3), transcription factors (HIF1A, JUNB, SMAD3), and transmembrane receptors (FGFR1, TNFRSF1A, TYROBP) were also identified. Conclusions: The use of clinical history of PPS, in the absence of other criteria, may have led to misidentification of some cases as PPS. Conclusions: Transcriptomic analysis indicated that changes in ECM and cell adhesion were important factors in equine PPS. Key predicted upstream events include genes associated with hypoxia, inflammation and growth factors related to the pathogenesis of equine PPS.
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Publication Date: 2022-06-13 PubMed ID: 35622344DOI: 10.1111/evj.13602Google Scholar: Lookup
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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.

This research investigates the genetic changes in the chorioallantois (a part of the placenta) of horses that experience premature placental separation (PPS), a condition that can cause risks for fetal or neonatal horses. The study discovered 1,204 genes with different expression levels in PPS compared to normal conditions, highlighting changes in them associated with inflammation, lack of oxygen, and growth factors.

Objective and Methods

  • The main goal of this study was to examine transcriptomic changes (changes in gene expression) in the chorioallantois (CA) from horses (mares) with clinical PPS compared with CA from mares who had normal foaling.
  • Researchers collected CA samples from Thoroughbred mares with a clinical history of PPS and from control Thoroughbred mares with normal parturition.
  • Transcriptomic changes in the villous CA near the cervical star were determined by using Illumina® sequencing and subsequent bioinformatic analysis.
  • The PPS samples were grouped into clusters using k-means clustering, and differentially expressed genes (DEGs) in each PPS cluster were identified by comparing to controls. These DEGs were used for gene ontology analysis and pathway analysis.

Results

  • A total of 1204 DEGs were identified between PPS and control.
  • Gene ontology indicated changes in extracellular matrix (ECM) and cell adhesion, highlighting structural changes in the cellular environment in cases of PPS.
  • Pathway analysis revealed alterations in fatty acid metabolism, the p-53 regulatory pathway, hypoxia (low oxygen levels), and inflammation associated with PPS.
  • Eleven key regulator genes of PPS, including growth factors (IGF1, TGFB2, TGFB3), transcription factors (HIF1A, JUNB, SMAD3), and transmembrane receptors (FGFR1, TNFRSF1A, TYROBP), were also identified. These genes are involved in vital biological processes and seemed significantly altered in PPS cases.

Conclusions

  • Researchers suggest that the use of clinical history of PPS, without other criteria, may have caused misidentification of some cases as PPS.
  • The transcriptomic analysis indicated that changes in the extracellular matrix (ECM) and cell adhesion were important factors in equine PPS. This suggests that PPS might involve substantial changes in tissue structure and integrity.
  • The study identified key upstream events that predict PPS, which include changes in genes associated with low oxygen, inflammation, and growth factors. This deepens our understanding of the pathogenesis of equine PPS, potentially providing targets for treatment or preventative strategies.

Cite This Article

APA
Murase H, El-Sheikh Ali H, Ruby RE, Scoggin KE, Ball BA. (2022). Transcriptomic analysis of the chorioallantois in equine premature placental separation. Equine Vet J, 55(3), 405-418. https://doi.org/10.1111/evj.13602

Publication

Equine veterinary journal
ISSN: 2042-3306
NlmUniqueID: 0173320
Country: United States
Language: English
Volume: 55
Issue: 3
Pages: 405-418

Researcher Affiliations

Murase, Harutaka
  • Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
  • Equine Science Division, Hidaka Training and Research Center, Japan Racing Association, Hokkaido, Japan.
El-Sheikh Ali, Hossam
  • Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
  • Faculty of Veterinary Medicine, Mansoura University, Mansoura, Egypt.
Ruby, Rebecca E
  • Veterinary Diagnostic Laboratory, University of Kentucky, Lexington, Kentucky, USA.
Scoggin, Kirsten E
  • Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.
Ball, Barry A
  • Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, USA.

MeSH Terms

  • Animals
  • Pregnancy
  • Horses / genetics
  • Female
  • Placenta
  • Transcriptome
  • Retrospective Studies
  • Inflammation / metabolism
  • Inflammation / veterinary
  • Horse Diseases / etiology

Grant Funding

  • University of Kentucy
  • Albert G. Clay Endowment
  • Japan Racing Association

References

This article includes 75 references
  1. McCue PM, Ferris RA. Parturition, dystocia and foal survival: a retrospective study of 1047 births.. Equine Vet J 2012;44(Suppl 41):22-5.
    doi: 10.1111/j.2042-3306.2011.00476.xgoogle scholar: lookup
  2. Laugier C, Foucher N, Sevin C, Leon A, Tapprest J. A 24-year retrospective study of equine abortion in Normandy (France).. J Equine Vet Sci 2011;31(3):116-23.
    doi: 10.1016/j.jevs.2010.12.012google scholar: lookup
  3. Hong CB, Donahue JM, Giles RC Jr, Petrites-Murphy MB, Poonacha KB, Roberts AW. Equine abortion and stillbirth in central Kentucky during 1988 and 1989 foaling seasons.. J Vet Diagn Invest 1993;5(4):560-6.
    doi: 10.1177/104063879300500410google scholar: lookup
  4. Cohen ND, Carey VJ, Donahue JG, Seahorn JL, Harrison LR. Descriptive epidemiology of late-term abortions associated with the mare reproductive loss syndrome in Central Kentucky.. J Vet Diagn Invest 2003;15(3):295-7.
    doi: 10.1177/104063870301500315google scholar: lookup
  5. Putnam MR, Bransby DI, Schumacher J, Boosinger TR, Bush L, Shelby RA. Effects of the fungal endophyte Acremonium coenophialum in fescue on pregnant mares and foal viability.. Am J Vet Res 1991;52(12):2071-4.
  6. Smith KC, Whitwell KE, Blunden AS, Bestbier ME, Scase TJ, Geraghty RJ. Equine herpesvirus-1 abortion: atypical cases with lesions largely or wholly restricted to the placenta.. Equine Vet J 2004;36(1):79-82.
    doi: 10.2746/0425164044864732google scholar: lookup
  7. Canisso I, Ball BA, Squires EL, Troedsson MHT. Comprehensive review on equine Placentitis.. Proc Am Assoc Equine Pract 2015;61:490-509.
  8. Canisso IF, Ball BA, Scoggin KE, Squires EL, Williams NM, Troedsson MH. Alpha-fetoprotein is present in the fetal fluids and is increased in plasma of mares with experimentally induced ascending placentitis.. Anim Reprod Sci 2015;154:48-55.
    doi: 10.1016/j.anireprosci.2014.12.019google scholar: lookup
  9. Njaa B. Kirkbride's diagnosis of abortion and neonatal loss in animals.. Diagnosis of abortion and neonatal loss in animals 4th ed. West Sussex, UK: Wiley-Blackwell; 2012.
  10. Novakovic P, Detmer SE, Suleman M, Malgarin CM, MacPhee DJ, Harding JCS. Histologic changes associated with placental separation in gilts infected with porcine reproductive and respiratory syndrome virus.. Vet Pathol 2018;55(4):521-30.
    doi: 10.1177/0300985818765067google scholar: lookup
  11. Downes KL, Grantz KL, Shenassa ED. Maternal, labor, delivery, and perinatal outcomes associated with placental abruption: a systematic review.. Am J Perinatol 2017;34(10):935-57.
    doi: 10.1055/s-0037-1599149google scholar: lookup
  12. Ananth CV, Lavery JA, Vintzileos AM, Skupski DW, Varner M, Saade G. Severe placental abruption: clinical definition and associations with maternal complications.. Am J Obstet Gynecol 2016;214(2):272.e1-9.
    doi: 10.1016/j.ajog.2015.09.069google scholar: lookup
  13. Shah SG, Rashid M, Verma T, Ludbe M, Khade B, Gera PB. Establishing a correlation between RIN and A260/280 along with the multivariate evaluation of factors affecting the quality of RNA in cryopreserved cancer bio-specimen.. Cell Tissue Bank 2019;20(4):489-99.
    doi: 10.1007/s10561-019-09782-7google scholar: lookup
  14. Udvardi MK, Czechowski T, Scheible W-R. Eleven golden rules of quantitative RT-PCR.. Plant Cell 2008;20(7):1736-7.
    doi: 10.1105/tpc.108.061143google scholar: lookup
  15. Bayega A, Wang YC, Oikonomopoulos S, Djambazian H, Fahiminiya S, Ragoussis J. Transcript profiling using long-read sequencing technologies.. Gene expression analysis: methods and protocols 2018. New York: Springer; p. 121-47.
  16. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.. Nat Protoc 2009;4(1):44-57.
    doi: 10.1038/nprot.2008.211google scholar: lookup
  17. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists.. Nucleic Acids Res 2009;37(1):1-13.
    doi: 10.1093/nar/gkn923google scholar: lookup
  18. Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000;28(1):27-30.
    doi: 10.1093/nar/28.1.27google scholar: lookup
  19. Mi H, Muruganujan A, Huang X, Ebert D, Mills C, Guo X. Protocol update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0).. Nat Protoc 2019;14(3):703-21.
    doi: 10.1038/s41596-019-0128-8google scholar: lookup
  20. Kramer A, Green J, Pollard J Jr, Tugendreich S. Causal analysis approaches in ingenuity pathway analysis.. Bioinformatics 2014;30(4):523-30.
    doi: 10.1093/bioinformatics/btt703google scholar: lookup
  21. El-Sheikh Ali H, Scoggin KE, Ruby R, Loynachan A, Boakari Y, Fernandes C. Equine cervical remodeling during placentitis and the prepartum period: a transcriptomic approach.. Reproduction 2021;161(6):603-21.
    doi: 10.1530/rep-21-0008google scholar: lookup
  22. El-Sheikh Ali H, Loux SC, Kennedy L, Scoggin KE, Dini P, Fedorka CE. Transcriptomic analysis of equine chorioallantois reveals immune networks and molecular mechanisms involved in nocardioform placentitis.. Vet Res 2021;52(1):103.
    doi: 10.1186/s13567-021-00972-4google 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;142(1-2):35-41.
    doi: 10.1016/j.anireprosci.2013.07.009google scholar: lookup
  24. Harburger DS, Calderwood DA. Integrin signalling at a glance.. J Cell Sci 2009;122(Pt 2):159-63.
    doi: 10.1242/jcs.018093google scholar: lookup
  25. Jarvelainen H, Sainio A, Koulu M, Wight TN, Penttinen R. Extracellular matrix molecules: potential targets in pharmacotherapy.. Pharmacol Rev 2009;61(2):198-223.
    doi: 10.1124/pr.109.001289google scholar: lookup
  26. Boos A, Stelljes A, Kohtes J. Collagen types I, III and IV in the placentome and interplacentomal maternal and fetal tissues in normal cows and in cattle with retention of fetal membranes.. Cells Tissues Organs 2003;174(4):170-83.
    doi: 10.1159/000072720google scholar: lookup
  27. Attupuram NM, Kumaresan A, Narayanan K, Kumar H. Cellular and molecular mechanisms involved in placental separation in the bovine: a review.. Mol Reprod Dev 2016;83(4):287-97.
    doi: 10.1002/mrd.22635google scholar: lookup
  28. Hampson V, Liu D, Billett E, Kirk S. Amniotic membrane collagen content and type distribution in women with preterm premature rupture of the membranes in pregnancy.. BJOG 1997;104(9):1087-91.
    doi: 10.1111/j.1471-0528.1997.tb12073.xgoogle scholar: lookup
  29. 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;87(3):1353-61.
    doi: 10.1210/jcem.87.3.8320google scholar: lookup
  30. Moore RM, Mansour JM, Redline RW, Mercer BM, Moore JJ. The physiology of fetal membrane rupture: insight gained from the determination of physical properties.. Placenta 2006;27(11-12):1037-51.
    doi: 10.1016/j.placenta.2006.01.002google scholar: lookup
  31. Strauss JF 3rd. Extracellular matrix dynamics and fetal membrane rupture.. Reprod Sci 2013;20(2):140-53.
    doi: 10.1177/1933719111424454google scholar: lookup
  32. Franczyk M, Lopucki M, Stachowicz N, Morawska D, Kankofer M. Extracellular matrix proteins in healthy and retained placentas, comparing hemochorial and synepitheliochorial placentas.. Placenta 2017;50:19-24.
    doi: 10.1016/j.placenta.2016.12.014google scholar: lookup
  33. Shoulders MD, Raines RT. Collagen structure and stability.. Annu Rev Biochem 2009;78:929-58.
    doi: 10.1146/annurev.biochem.77.032207.120833google scholar: lookup
  34. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Okscold P, Mardinoglu A. Proteomics. Tissue-based map of the human proteome.. Science 2015;347(6220):1260419.
    doi: 10.1126/science.1260419google scholar: lookup
  35. Mecham R, Mecham RP, SpringerLink. The Extracellular Matrix: An Overview.. 1st ed. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011.
  36. Meinert M, Malmström A, Tufvesson E, Westergren-Thorsson G, Petersen AC, Laurent C. Labour induces increased concentrations of biglycan and hyaluronan in human fetal membranes.. Placenta 2007;28(5-6):482-6.
    doi: 10.1016/j.placenta.2006.09.006google scholar: lookup
  37. Swan BC, Murthi P, Rajaraman G, Pathirage NA, Said JM, Ignjatovic V. Decorin expression is decreased in human idiopathic fetal growth restriction.. Reprod Fertil Dev 2010;22(6):949-55.
    doi: 10.1071/rd09240google scholar: lookup
  38. Murthi P, Faisal FA, Rajaraman G, Stevenson J, Ignjatovic V, Monagle PT. Placental biglycan expression is decreased in human idiopathic fetal growth restriction.. Placenta 2010;31(8):712-7.
    doi: 10.1016/j.placenta.2010.05.009google scholar: lookup
  39. Calmus ML, Macksoud EE, Tucker R, Iozzo RV, Lechner BE. A mouse model of spontaneous preterm birth based on the genetic ablation of biglycan and decorin.. Reproduction 2011;142(1):183-94.
    doi: 10.1530/rep-10-0387google scholar: lookup
  40. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry.. Circ Res 2003;92(8):827-39.
    doi: 10.1161/01.res.0000070112.80711.3dgoogle scholar: lookup
  41. Dilly M, Hambruch N, Shenavai S, Schuler G, Froehlich R, Haeger J-D. Expression of matrix metalloproteinase (MMP)-2, MMP-14 and tissue inhibitor of matrix metalloproteinase (TIMP)-2 during bovine placentation and at term with or without placental retention.. Theriogenology 2011;75(6):1104-14.
    doi: 10.1016/j.theriogenology.2010.11.019google scholar: lookup
  42. Timpl R. Structure and biological activity of basement membrane proteins.. Eur J Biochem 1989;180(3):487-502.
    doi: 10.1111/j.1432-1033.1989.tb14673.xgoogle scholar: lookup
  43. Poppenga RH, Mostrom MS, Haschek WM, Lock TF, Buck WB, Beasley VR. Mare agalactia, placental thickening, and high foal mortality associated with the grazing of tall fescue: a case report.. Proc Am Assoc of Vet Lab Diagn 1984;27:325-36.
  44. Laderoute KR. The interaction between HIF-1 and AP-1 transcription factors in response to low oxygen.. Semin Cell Dev Biol 2005;16(4-5):502-13.
    doi: 10.1016/j.semcdb.2005.03.005google scholar: lookup
  45. Moslehi R, Ambroggio X, Nagarajan V, Kumar A, Dzutsev A. Nucleotide excision repair/transcription gene defects in the fetus and impaired TFIIH-mediated function in transcription in placenta leading to preeclampsia.. BMC Genomics 2014;15:373.
    doi: 10.1186/1471-2164-15-373google scholar: lookup
  46. Mata-Greenwood E, Liao WX, Wang W, Zheng J, Chen DB. Activation of AP-1 transcription factors differentiates FGF2 and vascular endothelial growth factor regulation of endothelial nitric-oxide synthase expression in placental artery endothelial cells.. J Biol Chem 2010;285(23):17348-58.
    doi: 10.1074/jbc.m109.092791google scholar: lookup
  47. Verrecchia F, Vindevoghel L, Lechleider RJ, Uitto J, Roberts AB, Mauviel A. Smad3/AP-1 interactions control transcriptional responses to TGF-beta in a promoter-specific manner.. Oncogene 2001;20(26):3332-40.
    doi: 10.1038/sj.onc.1204448google scholar: lookup
  48. Ignotz RA, Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix.. J Biol Chem 1986;261(9):4337-45.
  49. Nikitovic D, Zafiropoulos A, Katonis P, Tsatsakis A, Theocharis AD, Karamanos NK. Transforming growth factor-beta as a key molecule triggering the expression of versican isoforms v0 and v1, hyaluronan synthase-2 and synthesis of hyaluronan in malignant osteosarcoma cells.. IUBMB Life 2006;58(1):47-53.
    doi: 10.1080/15216540500531713google scholar: lookup
  50. Verrecchia F, Chu ML, Mauviel A. Identification of novel TGF-beta /Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach.. J Biol Chem 2001;276(20):17058-62.
    doi: 10.1074/jbc.m100754200google scholar: lookup
  51. Nishi H, Nakada T, Hokamura M, Osakabe Y, Itokazu O, Huang LE. Hypoxia-inducible factor-1 transactivates transforming growth factor-beta3 in trophoblast.. Endocrinology 2004;145(9):4113-8.
    doi: 10.1210/en.2003-1639google scholar: lookup
  52. Schäffer L, Scheid A, Spielmann P, Breymann C, Zimmermann R, Meuli M. Oxygen-regulated expression of TGF-β3, a growth factor involved in trophoblast differentiation.. Placenta 2003;24(10):941-50.
    doi: 10.1016/s0143-4004(03)00166-8google scholar: lookup
  53. Patel J, Landers K, Mortimer RH, Richard K. Regulation of hypoxia inducible factors (HIF) in hypoxia and normoxia during placental development.. Placenta 2010;31(11):951-7.
    doi: 10.1016/j.placenta.2010.08.008google scholar: lookup
  54. Caniggia I, Winter J, Lye SJ, Post M. Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia.. Placenta 2000;21(Suppl A):S25-30.
    doi: 10.1053/plac.1999.0522google scholar: lookup
  55. Asplund A, Stillemark-Billton P, Larsson E, Rydberg EK, Moses J, Hultén LM. Hypoxic regulation of secreted proteoglycans in macrophages.. Glycobiology 2010;20(1):33-40.
    doi: 10.1093/glycob/cwp139google scholar: lookup
  56. Massague J. The transforming growth factor-beta family.. Annu Rev Cell Biol 1990;6:597-641.
    doi: 10.1146/annurev.cb.06.110190.003121google scholar: lookup
  57. Ali LE, Salih MM, Elhassan EM, Mohmmed AA, Adam I. Placental growth factor, vascular endothelial growth factor, and hypoxia-inducible factor-1alpha in the placentas of women with pre-eclampsia.. J Matern Fetal Neonatal Med 2019;32(16):2628-32.
    doi: 10.1080/14767058.2018.1443066google scholar: lookup
  58. Korkes HA, De Oliveira L, Sass N, Salahuddin S, Karumanchi SA, Rajakumar A. Relationship between hypoxia and downstream pathogenic pathways in preeclampsia.. Hypertens Pregnancy 2017;36(2):145-50.
    doi: 10.1080/10641955.2016.1259627google scholar: lookup
  59. van Uitert M, Moerland PD, Enquobahrie DA, Laivuori H, van der Post JAM, Ris-Stalpers C. Meta-analysis of placental transcriptome data identifies a novel molecular pathway related to preeclampsia.. PLoS One 2015;10(7):e0132468.
    doi: 10.1371/journal.pone.0132468google scholar: lookup
  60. Galbiati S, Inversetti A, Causarano V, Stenirri S, Soriani N, Ambrosi A. HIF1A and MIF as potential predictive mRNA biomarkers of pre-eclampsia: a longitudinal prospective study in high risk population.. Clin Chem Lab Med 2015;53(9):1339-47.
    doi: 10.1515/cclm-2014-0745google scholar: lookup
  61. Tal R. The role of hypoxia and hypoxia-inducible factor-1alpha in preeclampsia pathogenesis.. Biol Reprod 2012;87(6):134.
    doi: 10.1095/biolreprod.112.102723google scholar: lookup
  62. Stubert J, Schattenberg F, Richter DU, Dieterich M, Briese V. Trophoblastic progranulin expression is upregulated in cases of fetal growth restriction and preeclampsia.. J Perinat Med 2012;40(5):475-81.
    doi: 10.1515/jpm-2011-0277google scholar: lookup
  63. Devisme L, Merlot B, Ego A, Houfflin-Debarge V, Deruelle P, Subtil D. A case-control study of placental lesions associated with pre-eclampsia.. Int J Gynaecol Obstet 2013;120(2):165-8.
    doi: 10.1016/j.ijgo.2012.08.023google scholar: lookup
  64. Ducray JF, Naicker T, Moodley J. Pilot study of comparative placental morphometry in pre-eclamptic and normotensive pregnancies suggests possible maladaptations of the fetal component of the placenta.. Eur J Obstet Gynecol Reprod Biol 2011;156(1):29-34.
    doi: 10.1016/j.ejogrb.2010.12.038google scholar: lookup
  65. Kim YH, O'Neill HM, Whitehead JP. Carboxypeptidase X-1 (CPX-1) is a secreted collagen-binding glycoprotein.. Biochem Biophys Res Commun 2015;468(4):894-9.
    doi: 10.1016/j.bbrc.2015.11.053google scholar: lookup
  66. Weiner CP, Mason CW, Dong Y, Buhimschi IA, Swaan PW, Buhimschi CS. Human effector/initiator gene sets that regulate myometrial contractility during term and preterm labor.. Am J Obstet Gynecol 2010;202(5):474 e1-20.
    doi: 10.1016/j.ajog.2010.02.034google scholar: lookup
  67. Bouchon A, Dietrich J, Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes.. J Immunol 2000;164(10):4991-5.
    doi: 10.4049/jimmunol.164.10.4991google scholar: lookup
  68. Schorpp-Kistner M, Wang ZQ, Angel P, Wagner EF. JunB is essential for mammalian placentation.. EMBO J 1999;18(4):934-48.
    doi: 10.1093/emboj/18.4.934google scholar: lookup
  69. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions.. Endocr Rev 1995;16(1):3-34.
    doi: 10.1210/edrv-16-1-3google scholar: lookup
  70. Fowden A. The insulin-like growth factors and feto-placental growth.. Placenta 2003;24(8-9):803-12.
    doi: 10.1016/s0143-4004(03)00080-8google scholar: lookup
  71. Vadillo-Ortega F, Gonzalez-Avila G, Furth EE, Lei H, Muschel RJ, Stetler-Stevenson WG. 92-kd type IV collagenase (matrix metalloproteinase-9) activity in human amniochorion increases with labor.. Am J Pathol 1995;146(1):148-56.
  72. Fortunato SJ, Menon R, Lombardi SJ. Collagenolytic enzymes (gelatinases) and their inhibitors in human amniochorionic membrane.. Am J Obstet Gynecol 1997;177(4):731-41.
    doi: 10.1016/s0002-9378(97)70260-6google scholar: lookup
  73. Maymon E, Romero R, Pacora P, Gervasi MT, Gomez R, Edwin SS. Evidence of in vivo differential bioavailability of the active forms of matrix metalloproteinases 9 and 2 in parturition, spontaneous rupture of membranes, and intra-amniotic infection.. Am J Obstet Gynecol 2000;183(4):887-94.
    doi: 10.1067/mob.2000.108878google scholar: lookup
  74. Streyl D, Kenngott R, Herbach N, Wanke R, Blum H, Sinowatz F. Gene expression profiling of bovine peripartal placentomes: detection of molecular pathways potentially involved in the release of foetal membranes.. Reproduction 2012;143(1):85-105.
    doi: 10.1530/rep-11-0204google scholar: lookup
  75. Dilly M, Hambruch N, Haeger JD, Pfarrer C. Epidermal growth factor (EGF) induces motility and upregulates MMP-9 and TIMP-1 in bovine trophoblast cells.. Mol Reprod Dev 2010;77(7):622-9.
    doi: 10.1002/mrd.21197google scholar: lookup

Citations

This article has been cited 2 times.
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  2. Scoggin KE, Rakha SI, Abdellatif AM, Adlan F, Helmy YA, Ruby R, Ball B, Boakari Y, Ali HE. Activation of the S100A8/A9 Alarmin Amplifies Inflammatory Pathways in Equine Ascending Placentitis. Int J Mol Sci 2026 Feb 4;27(3).
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