Toll-like receptor expression patterns in the rat uterus during post partum involution
Emel Alan A and Narin Liman A B
+ Author Affiliations
- Author Affiliations
A Department of Histology and Embryology, Faculty of Veterinary Medicine, Erciyes University, Kayseri 38039, Turkey.
B Corresponding author. Email: narinliman@gmail.com
Reproduction, Fertility and Development 30(2) 330-348 https://doi.org/10.1071/RD16431
Submitted: 25 October 2016 Accepted: 12 June 2017 Published: 13 July 2017
Abstract
Toll-like receptors (TLRs) belong to a family of pathogen recognition receptors and play critical roles in detecting and responding to invading pathogens. TLR expression could be significant because, in the uterus, the reproductive tract is an important site of exposure to and infection by pathogens during the post partum involution period. To clarify the expression and localisation patterns of TLRs in the rat uterus on Days 1, 3, 5 and 10 post partum (PP1, PP3, PP5 and PP10 respectively), immunohistochemistry and western blotting were used to analyse TLR1–7, TLR9 and TLR10. The immunohistochemistry results indicated that TLR1–7, TLR9 and TLR10 were localised in both the cytoplasm and nuclei of luminal and glandular epithelium, stromal fibroblasts and myometrial cells in the rat uterus. In the luminal epithelium, TLR4–7 were also found in lateral membranes, whereas TLR10 was present in apical membranes. Western blot analysis revealed that the expression of TLR proteins increased with the number of days post partum, reaching a maximum on PP10, although levels did not differ significantly from those on PP1 (P > 0.05). These findings confirm that TLR1–7, TLR9 and TLR10 are constitutively expressed in uterine cells and that localisation pattern of TLRs in the endometrium varies with structural changes in the uterus on different days of involution. These results suggest that TLRs may play a role in uterine repair and remodelling during physiological involution.
Additional keywords: endometrium, immunohistochemistry, luminal and glandular epithelium, myometrium, pathogen recognition receptors, stromal cells, uterine repair and remodelling, western blotting.
References
Aflatoonian, R., Tuckerman, E., Elliott, S. L., Bruce, C., Aflatoonian, A., Li, T. C., and Fazeli, A. (2007). Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum. Reprod. 22, 586–593.| Menstrual cycle-dependent changes of Toll-like receptors in endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotFCrug%3D%3D&md5=e9cb47a92a14067ca701e9330d0b59a2CAS |
Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783–801.
| Pathogen recognition and innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Kltb8%3D&md5=49db6560fdbd0f2fd25cd8922cd1f628CAS |
Alan, E., and Liman, N. (2012). Immunohistochemical localization of beta defensins in the endometrium of rat uterus during the postpartum involution period. Vet. Res. Commun. 36, 173–185.
| Immunohistochemical localization of beta defensins in the endometrium of rat uterus during the postpartum involution period.Crossref | GoogleScholarGoogle Scholar |
Allhorn, S., Böing, C., Koch, A. A., Kimming, R., and Gashaw, I. (2008). TLR3 and TLR4 expression in healthy and diseased human endometrium. Reprod. Biol. Endocrinol. 6, 40.
| TLR3 and TLR4 expression in healthy and diseased human endometrium.Crossref | GoogleScholarGoogle Scholar |
Amjadi, F., Salehi, E., Mehdizadeh, M., and Aflatoonian, R. (2014). Role of the innate immunity in female reproductive tract. Adv. Biomed. Res. 3, 1.
| Role of the innate immunity in female reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Astakhova, N. M., Perelygin, A. A., Zharkikh, A. A., Lear, T. L., Coleman, S. J., MacLeod, J. N., and Brinton, M. A. (2009). Characterization of equine and other vertebrate TLR3, TLR7 and TLR8 genes. Immunogenetics 61, 529–539.
| Characterization of equine and other vertebrate TLR3, TLR7 and TLR8 genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotF2nurk%3D&md5=5510541bb7c2e8f67c21aab6b4bd84bdCAS |
Blackburn, S. T. (2007). ‘Maternal, Fetal, and Neonatal Physiology: A Clinical Perspective.’ (Saunders Elseiver: St. Louis.)
Chang, J. S., Russell, G. C., Jann, O., Glass, E. J., Werling, D., and Haig, D. M. (2009). Moleculer cloning and characterization of Toll-like receptors 1–10 in sheep. Vet. Immunol. Immunopathol. 127, 94–105.
| Moleculer cloning and characterization of Toll-like receptors 1–10 in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFChtbfL&md5=a41771380a67c29bfff9b706f849a320CAS |
Chapwanya, A., Meade, K. G., Doherty, M. L., Callanan, J. J., Mee, J. F., and O’Farrelly, C. (2009). Histopathological and molecular evaluation of Holstein–Friesian cows postpartum: toward an improved understanding of uterine innate immunity. Theriogenology 71, 1396–1407.
| Histopathological and molecular evaluation of Holstein–Friesian cows postpartum: toward an improved understanding of uterine innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltl2murw%3D&md5=fc1532b5d4f512f18ed83adbb62b0e0aCAS |
Chotimanukul, S., and Sirivaidyapong, S. (2011). Differential expression of Toll-like receptor 4 (TLR4) in healthy and infected canine endometrium. Theriogenology 76, 1152–1161.
| Differential expression of Toll-like receptor 4 (TLR4) in healthy and infected canine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFaitLrN&md5=27c1b24e38366d62891d09279f43d1dfCAS |
Davies, D., Meade, K. G., Herath, S., Eckersall, P. D., Gonzalez, D., White, J. O., Conlan, R. S., O’Farrelly, C., and Sheldon, I. M. (2008). Toll-like receptor and antimicrobial peptide expression in the bovine endometrium. Reprod. Biol. Endocrinol. 6, 53.
| Toll-like receptor and antimicrobial peptide expression in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar |
Faure, E., Equils, O., Sieling, P. A., Thomas, L., Zhang, F. X., Kirschning, C. J., Polentarutti, N., Muzio, M., and Arditi, M. (2000). Bacterial lipopolysaccharide activates NF-κB through Toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem. 275, 11058–11063.
| Bacterial lipopolysaccharide activates NF-κB through Toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislShtrk%3D&md5=0dc8929f967cd65e7c499baebc62adaeCAS |
Fazeli, A., Bruce, C., and Anumba, D. O. (2005). Characterization of Toll-like receptors in the female reproductive tract in humans. Hum. Reprod. 20, 1372–1378.
| Characterization of Toll-like receptors in the female reproductive tract in humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFOmtrY%3D&md5=133635931de6a1bbad47b16ef04c1ba6CAS |
Fitzner, N., Clauberg, S., Essmann, F., Liebmann, J., and Kolb-Bachofen, V. (2008). Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands. Clin. Vaccine Immunol. 15, 138–146.
| Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVGjurs%3D&md5=aa6b1dceec9f41328ce53e91b6ba56fdCAS |
Fonseca, B. M., Correia-da-Silva, G., and Teixeira, N. A. (2012). The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period. Reprod. Biol. 12, 97–118.
| The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period.Crossref | GoogleScholarGoogle Scholar |
Hart, K. M., Murphy, A. J., Barrett, K. T., Wira, C. R., Guyre, P. M., and Pioli, P. A. (2009). Fuctional expression of pattern recognition receptors in tissues of the human female reproductive tract. J. Reprod. Immunol. 80, 33–40.
| Fuctional expression of pattern recognition receptors in tissues of the human female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1Smsbw%3D&md5=38648a4de3c66f2947b593eb2f454c2aCAS |
Hasan, U. A., Trinchieri, G., and Vlach, J. (2005). Toll-like receptor signaling stimulates cell cycle entry and progression in fibroblasts. J. Biol. Chem. 280, 20620–20627.
| Toll-like receptor signaling stimulates cell cycle entry and progression in fibroblasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlClsL4%3D&md5=77f4cc1cafa0746abce3b82620549336CAS |
Hickey, D. K., Fahey, J. V., and Wira, C. R. (2013). Mouse estrous cycle regulation of vaginal versus uterine cytokines, chemokines, α-/β-defensins and TLRs. Innate Immun. 19, 121–131.
| Mouse estrous cycle regulation of vaginal versus uterine cytokines, chemokines, α-/β-defensins and TLRs.Crossref | GoogleScholarGoogle Scholar |
Hirata, T., Osuga, Y., Hamasaki, K., Hirota, Y., Nose, E., Morimoto, C., Harada, M., Takemura, Y., Koga, K., Yoshino, O., Tajima, T., Hasegawa, A., Yano, T., and Taketani, Y. (2007). Expression of toll-like receptors 2, 3, 4 and 9 genes in the human endometrium during the menstrual cycle. J. Reprod. Immunol. 74, 53–60.
| Expression of toll-like receptors 2, 3, 4 and 9 genes in the human endometrium during the menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFGgsbc%3D&md5=5fb09788bb4f32c46e6a8ee63e9799fdCAS |
Ignacio, G., Nordone, S., Howard, K. E., and Dean, G. A. (2005). Toll-like receptor expression in feline lymphoid tissues. Vet. Immunol. Immunopathol. 106, 229–237.
| Toll-like receptor expression in feline lymphoid tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1Ggsr0%3D&md5=73389a1a92a53adf4a274254a45d5482CAS |
Ioannou, S., and Voulgarelis, M. (2010). Toll-like receptors, tissue injury and tumourigenesis. Mediators Inflamm. 2010, 1–9.
| Toll-like receptors, tissue injury and tumourigenesis.Crossref | GoogleScholarGoogle Scholar |
Iqbal, M., Philbin, V. J., Withanage, G. S., Wigley, P., Beal, R. K., Goodchild, M. J., Barrow, P., McConnell, I., Maskell, D. J., Young, J., Bumstead, N., Boyd, Y., and Smith, A. L. (2005). Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar Typhimurium. Infect. Immun. 73, 2344–2350.
| Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar Typhimurium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFynsr8%3D&md5=cd197af893aa102a2b32b3a7ae4b96f0CAS |
Jiang, D., Liang, J., Fan, J., Yu, S., Chen, S., Luo, Y., Prestwich, G. D., Mascarenhas, M. M., Garg, H. G., Quinn, D. A., Homer, R. J., Goldstein, D. R., Bucala, R., Lee, P. J., Medzhitov, R., and Noble, P. W. (2005). Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11, 1173–1179.
| Regulation of lung injury and repair by Toll-like receptors and hyaluronan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOhsLvI&md5=499ba75744ca591608ff37ffa83d8016CAS |
Jiang, D., Liang, J., Li, Y., and Noble, P. W. (2006). The role of Toll-like receptors in non-infectious lung injury. Cell Res. 16, 693–701.
| The role of Toll-like receptors in non-infectious lung injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFKks7k%3D&md5=465f53128df897985916e2311a93a7b7CAS |
Jorgenson, R. L., Lesmeiter, M. J., and Misfeldt, M. L. (2005). Human endometrial epithelial cells cyclically express Toll-like receptor-3 (TLR3) and exhibit TLR3- dependent responses to dsRNA. Hum. Immunol. 66, 469–482.
| Human endometrial epithelial cells cyclically express Toll-like receptor-3 (TLR3) and exhibit TLR3- dependent responses to dsRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVeis7c%3D&md5=3f8c7b4adf5dd9be412436861e389087CAS |
Kannaki, T. R., Shanmugamb, M., and Vermaa, P. C. (2011). Toll like receptors and their role in animal reproduction. Anim. Reprod. Sci. 125, 1–12.
| Toll like receptors and their role in animal reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVyrtLY%3D&md5=a76975b1cf1ca903c2c760fdac724fa5CAS |
Koga, K., and Mor, G. (2008). Expression and function of Toll-like receptors at the maternal–fetal interface. Reprod. Sci. 15, 231–242.
| Expression and function of Toll-like receptors at the maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlShsbc%3D&md5=92fbcca39773c15e2bc8261314216d88CAS |
Lange, M. J. (2008). Hormonal regulation of innate immune responses and toll-like receptors in the human endometrium. Ph.D. Thesis, University of Missouri – Columbia, Missouri.
Li, J., Ma, Z., Tang, Z. L., Stevens, T., Pitt, B., and Li, S. (2004). CpG DNA-mediated immune response in pulmonary endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L552–L558.
| CpG DNA-mediated immune response in pulmonary endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVeitr8%3D&md5=0a1112a9cc81a9a7796b5c89d879122eCAS |
Li, X., Jiang, S., and Tapping, R. I. (2010). Toll-like receptor signaling in cell proliferation and survival. Cytokine 49, 1–9.
| Toll-like receptor signaling in cell proliferation and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyku7jK&md5=4cc69ea94f41ea7093ce947dc212aaacCAS |
Liman, N., Alan, E., Küçük Bayram, G., and Gürbulak, K. (2013). Expression of survivin, bcl-2 and bax proteins in the domestic cat (Felis catus) endometrium during the oestrus cycle. Reprod. Domest. Anim. 48, 33–45.
| Expression of survivin, bcl-2 and bax proteins in the domestic cat (Felis catus) endometrium during the oestrus cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktVOhtrk%3D&md5=e9d3756ed30ea40ac6ef0ee387f62320CAS |
Lin, Z., Xu, J., Jin, X., Zhang, X., and Ge, F. (2009). Modulation of expression of Toll-like receptors in the human endometrium. Am. J. Reprod. Immunol. 61, 338–345.
| Modulation of expression of Toll-like receptors in the human endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFOms74%3D&md5=c99cfb6812e4490f1dbaab997760713eCAS |
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
| 1:CAS:528:DyaG38XhsVyrsw%3D%3D&md5=543feb0ae4d03a840b0d5387fc0cd0f1CAS |
Martins, T. M., Paixão, T. A., Costa, É. A., Pires, A. C., Santos, R. L., and Borges, Á. M. (2011). Postpartum toll-like receptors and β-defensin 5 mRNA levels in the endometrium of Holstein cows. Vet. Immunol. Immunopathol. 139, 277–281.
| Postpartum toll-like receptors and β-defensin 5 mRNA levels in the endometrium of Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjslSmsw%3D%3D&md5=c048177d847610324c48c8e0247c703aCAS |
Nasu, K., and Narahara, H. (2010). Pattern recognition via the Toll-like receptor system in human female genital tract. Mediators Inflamm. 2010, 976024.
| Pattern recognition via the Toll-like receptor system in human female genital tract.Crossref | GoogleScholarGoogle Scholar |
Nilsen-Hamilton, M., Liu, Q., Ryon, J., Bendickson, L., Lepont, P., and Chang, Q. (2003). Tissue involution and the acute phase response. Ann. N. Y. Acad. Sci. 995, 94–108.
| Tissue involution and the acute phase response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVensrs%3D&md5=8218f550ff9c5d525847b9a0846f1e45CAS |
Paik, Y. H., Schwabe, R. F., Bataller, R., Russo, M. P., Jobin, C., and Brenner, D. A. (2003). Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 37, 1043–1055.
| Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVWns7Y%3D&md5=9fb12c3aba5f256f3320d62aa9e21571CAS |
Paik, Y. H., Lee, K. S., Lee, H. J., Yang, K. M., Lee, S. J., Lee, D. K., Han, K. H., Chon, C. Y., Lee, S. I., Moon, Y. M., and Brenner, D. A. (2006). Hepatic stellate cells primed with cytokines upregulate inflammation in response to peptidoglycan or lipoteichoic acid. Lab. Invest. 86, 676–686.
| Hepatic stellate cells primed with cytokines upregulate inflammation in response to peptidoglycan or lipoteichoic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xls1Kitb4%3D&md5=85176e076990199f25264f79afaa1b1eCAS |
Rakoff-Nahoum, S., and Medzhitov, R. (2008). Role of toll-like receptors in tissue repair and tumorigenesis. Biochemistry (Mosc.) 73, 555–561.
| Role of toll-like receptors in tissue repair and tumorigenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFKhurk%3D&md5=bbc10ca104e64072d84242dd58079e7dCAS |
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., and Medzhitov, R. (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229–241.
| Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlKntrg%3D&md5=cf5b35c430a9040349c091db097c46caCAS |
Ritter, N. (2007). Peripartal expression of endometrial Toll-like receptors and defensins in cattle. Ph.D. Thesis, University of Veterinary Medicine, Hannover.
Schaefer, T. M., Desouza, K., Fahey, J. V., Beagley, K. W., and Wira, C. R. (2004). Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 112, 428–436.
| Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFKgu70%3D&md5=fd83ee5c8c6dd252f217ba8351617a1eCAS |
Seki, E., de Minicis, S., Österreicher, C. H., Kluwe, J., Osawa, Y., Brenner, D. A., and Schwabe, R. F. (2007). TLR4 enhances TGF-β signaling and hepatic fibrosis. Nat. Med. 13, 1324–1332.
| TLR4 enhances TGF-β signaling and hepatic fibrosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Kmtr3O&md5=ea8ed1961e80bce548c00520dce42fddCAS |
Sheldon, I. M., Cronin, J., Goetze, L., Donofrio, G., and Schuberth, H. J. (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol. Reprod. 81, 1025–1032.
| Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vP&md5=e816f2d41f68f8e078c2f4907fbdcea5CAS |
Shinkai, H., Muneta, Y., Suzuki, K., Eguchi-Ogawa, T., Awata, T., and Uenishi, H. (2006). Porcine Toll-like receptor 1, 6 and 10 genes, complete sequencing of genomic region and expression analysis. Mol. Immunol. 43, 1474–1480.
| Porcine Toll-like receptor 1, 6 and 10 genes, complete sequencing of genomic region and expression analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslKjurc%3D&md5=8079ffd37f467a4b8e00fdcbdc56eac3CAS |
Silva, A. P., Costa, E. A., Macêdo, A. A., Martins Tda, M., Borges, A. M., Paixão, T. A., and Santos, R. L. (2012a). Transcription of pattern recognition receptors and abortive agents induced chemokines in the bovine pregnant uterus. Vet. Immunol. Immunopathol. 145, 248–256.
| Transcription of pattern recognition receptors and abortive agents induced chemokines in the bovine pregnant uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVertb0%3D&md5=fd543add949d8571666953b850dbdd72CAS |
Silva, E., Henriques, S., Brito, S., Ferreira-Dias, G., Lopes-da-Costa, L., and Mateus, L. (2012b). Oestrous cycle-related changes in production of Toll-like receptors and prostaglandins in the canine endometrium. J. Reprod. Immunol. 96, 45–57.
| Oestrous cycle-related changes in production of Toll-like receptors and prostaglandins in the canine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVSmsLrJ&md5=a4ca63d5925f6722dd52c8744a8a0a09CAS |
Soboll, G., Schaefer, T. M., and Wira, C. R. (2006). Effect of Toll-like receptor (TLR) agonists on TLR and microbicide expression in uterine and vaginal tissues of the mouse. Am. J. Reprod. Immunol. 55, 434–446.
| Effect of Toll-like receptor (TLR) agonists on TLR and microbicide expression in uterine and vaginal tissues of the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlKntb0%3D&md5=5d1b79a9b62ec885eb069cce578d978aCAS |
Swerdlow, M. P., Kennedy, D. R., Kennedy, J. S., Washabau, R. J., Henthorn, P. S., Moore, P. F., Carding, S. R., and Felsburg, P. J. (2006). Expression and function of TLR2, TLR4 and NOD2 in primary canine colonic epithelial cells. Vet. Immunol. Immunopathol. 114, 313–319.
| Expression and function of TLR2, TLR4 and NOD2 in primary canine colonic epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFequrnM&md5=29cb49c0a485c9a1b9184f9db07c253cCAS |
Takeda, K., Kaisho, T., and Akira, S. (2003). Toll-like receptors. Annu. Rev. Immunol. 21, 335–376.
| Toll-like receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtF2isrg%3D&md5=4fd4ccdb824dec326f62ce5bcb583541CAS |
Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805–820.
| Pattern recognition receptors and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVSgu74%3D&md5=465e0a134443214c63f296db5bb1a81cCAS |
Thota, C., Farmer, T., Garfield, R. E., Menon, R., and Al-Hendy, A. (2013). Vitamin D elicits anti-inflammatory response, inhibits contractile-associated proteins, and modulates Toll-like receptors in human myometrial cells. Reprod. Sci. 20, 463–475.
| Vitamin D elicits anti-inflammatory response, inhibits contractile-associated proteins, and modulates Toll-like receptors in human myometrial cells.Crossref | GoogleScholarGoogle Scholar |
Tirumurugaan, K. G., Dhanasekaran, S., Raj, G. D., Raja, A., Kumanan, K., and Ramaswamy, V. (2010). Differential expression of Toll-like receptor mRNA in selected tissues of goat. Vet. Immunol. Immunopathol. 133, 296–301.
| Differential expression of Toll-like receptor mRNA in selected tissues of goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Wns7vM&md5=9ebf146eb24c41f2e01a000686381d1bCAS |
Underhill, D. M. (2004). Toll-like receptors and microbes take aim at each other. Curr. Opin. Immunol. 16, 483–487.
| Toll-like receptors and microbes take aim at each other.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFyrtbw%3D&md5=1b5601c4b68df54f49cb95674749dc99CAS |
Vahanan, B. M., Raj, G. D., Pawar, R. M. C., Gopinath, V. P., Raja, A., and Thangavelu, A. (2008). Expression profile of Toll-like receptors in a range of water buffalo tissues (Bubalus bubalis). Vet. Immunol. Immunopathol. 126, 149–155.
| Expression profile of Toll-like receptors in a range of water buffalo tissues (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12gtL3J&md5=6e96a23ec7738bc3cd574517f8101be4CAS |
Warbrick, J. G. (1955). Postpartum changes in the uterus of rat. J. Embryol. Exp. Morphol. 3, 256–264.
Wira, C. R., and Fahey, J. V. (2004). The innate immune system, gatekeeper to the female reproductive tract. Immunology 111, 13–15.
| The innate immune system, gatekeeper to the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVykuw%3D%3D&md5=6146977778c0dbca2cd8f5db434dae0eCAS |
Yang, X., Coriolan, D., Murthy, V., Schultz, K., Golenbock, D. T., and Beasley, D. (2005). Proinflammatory phenotype of vascular smooth muscle cells, role of efficient Toll-like receptor 4 signaling. Am. J. Physiol. Heart Circ. Physiol. 289, H1069–H1076.
| 1:CAS:528:DC%2BD2MXhtVWktr%2FN&md5=17382c6a5b218350d6ab1dafda61966dCAS |
Yang, X., Murthy, V., Schultz, K., Tatro, J. B., Fitzgerald, K. A., and Beasley, D. (2006). Toll-like receptor 3 signaling evokes a proinflammatory and proliferative phenotype in human vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 291, H2334–H2343.
| 1:CAS:528:DC%2BD28Xht1Gnsb7P&md5=fbbc18b0b24443f11917103555346584CAS |
Young, S. L., Lyddon, T. D., Jorgenson, R. L., and Misfeldt, M. L. (2004). Expression of Toll-like receptors in human endometrial epithelial cells and cell lines. Am. J. Reprod. Immunol. 52, 67–73.
| Expression of Toll-like receptors in human endometrial epithelial cells and cell lines.Crossref | GoogleScholarGoogle Scholar |
Youssef, R. E., Ledingham, M. A., Bollapragada, S. S., O’Gorman, N., Jordan, F., Young, A., and Norman, J. E. (2009). The role of toll-like receptors (TLR-2 and -4) and triggering receptor expressed on myeloid cells 1 (TREM-1) in human term and preterm labor. Reprod. Sci. 16, 843–856.
| The role of toll-like receptors (TLR-2 and -4) and triggering receptor expressed on myeloid cells 1 (TREM-1) in human term and preterm labor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFagu7fO&md5=8e5a9093112bf75b4d26ca775c6890faCAS |
Zhang, Z., and Schluesener, H. J. (2006). Mammalian toll-like receptors, from endogenous ligands to tissue regeneration. Cell. Mol. Life Sci. 63, 2901–2907.
| Mammalian toll-like receptors, from endogenous ligands to tissue regeneration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1egtbw%3D&md5=e1893d43b9495feeaad7902d270aaa7bCAS |
Zheng, L.-H., Cai, F.-F., Ge, I., Biskup, E., and Cheng, Z.-P. (2014). Stromal fibroblast activation and their potential association with uterine fibroids. Oncol. Lett. 8, 479–486.
| 1:CAS:528:DC%2BC2cXhsFeltbnN&md5=f4e2cd7942d911ee2ac51752aa8a612cCAS |
