Hostname: page-component-7479d7b7d-m9pkr Total loading time: 0 Render date: 2024-07-10T16:56:43.327Z Has data issue: false hasContentIssue false
  • English
  • Français

LPS- and LTA-Induced Expression of TLR4, MyD88, and TNF-α in Lymph Nodes of the Akkaraman and Romanov Lambs

Published online by Cambridge University Press:  05 September 2022

Aydın Alan ,
Emel Alan Open the ORCID record for Emel Alan [Opens in a new window] ,
Korhan Arslan Open the ORCID record for Korhan Arslan [Opens in a new window] ,
Fadime Daldaban ,
Esma Gamze Aksel ,
Mehmet Ulaş Çınar  and
Bilal Akyüz
Aydın Alan
Affiliation:
Department of Anatomy, Faculty of Veterinary Medicine, Erciyes University, 38030 Kayseri, Turkey
Emel Alan
Affiliation:
Department of Histology and Embryology, Faculty of Veterinary Medicine, Erciyes University, 38030 Kayseri, Turkey
Korhan Arslan*
Affiliation:
Department of Genetics, Faculty of Veterinary Medicine, University of Erciyes, 38030 Kayseri, Turkey
Fadime Daldaban
Affiliation:
Department of Genetics, Faculty of Veterinary Medicine, University of Erciyes, 38030 Kayseri, Turkey
Esma Gamze Aksel
Affiliation:
Department of Genetics, Faculty of Veterinary Medicine, University of Erciyes, 38030 Kayseri, Turkey
Mehmet Ulaş Çınar
Affiliation:
Department of Animal Science, Faculty of Agriculture, University of Erciyes, 38030 Kayseri, Turkey Department of Veterinary Microbiology & Pathology, Washington State University, Pullman, WA 99164, USA
Bilal Akyüz
Affiliation:
Department of Genetics, Faculty of Veterinary Medicine, University of Erciyes, 38030 Kayseri, Turkey
*
*Corresponding author: Korhan Arslan, E-mail: korhanarslan@erciyes.edu.tr
Get access

Abstract

Toll-like receptor (TLR)-mediated inflammatory processes play a critical role in the innate immune response during the initial interaction between the infecting microorganism and immune cells. This study aimed to investigate the possible microanatomical and histological differences in mandibular and bronchial lymph nodes in Akkaraman and Romanov lambs induced by lipopolysaccharide (LPS) and lipoteichoic acid (LTA) and study the gene, protein, and immunoexpression levels of TLR4, myeloid differentiation factor 88 (MyD88), and tumor necrosis factor-α (TNF-α) that are involved in the immune system. Microanatomical examinations demonstrated more intense lymphocyte infiltration in the bronchial lymph nodes of Akkaraman lambs in the LPS and LTA groups compared to Romanov lambs. TLR4, MyD88, and TNF-α immunoreactivities were more intense in the experimental groups of both breeds. Expression levels of MyD88 and TNF-α genes in the bronchial lymph node of Akkaraman lambs were found to increase statistically significantly in the LTA group. TLR4 gene expression level in the mandibular lymph node was found to be statistically significantly higher in the LTA + LPS group. In conclusion, dynamic changes in the immune cell populations involved in response to antigens such as LTA and LPS in the lymph nodes of both breeds can be associated with the difference in the expression level of the TLR4/MyD88/TNF-α genes.

Keywords

gene expressionimmunohistochemistrylamblymph nodescanning electron microscopy (SEM)
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 28 , Issue 6 , December 2022 , pp. 2078 - 2092
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akira, S, Uematsu, S & Takeuchi, O (2006). Pathogen recognition and innate immunity. Cell 124, 783–801.CrossRefGoogle ScholarPubMed
Aksel, EG & Akyüz, B (2021). Effect of LPS and LTA stimulation on the expression of TLR-pathway genes in PBMCs of Akkaraman lambs in vivo. Trop Anim Health Prod 53, 1–9.CrossRefGoogle ScholarPubMed
Alan, E & Kulak, Y (2021). The immunoexpression patterns of fibroblast growth factors in the pregnant and postpartum rat ovary. Reprod Fertil Dev 33, 817–830.CrossRefGoogle ScholarPubMed
Atanasova, K, Van Gucht, S, Barbé, F, Duchateau, L & Van Reeth, K (2011). Lipoteichoic acid from Staphylococcus aureus exacerbates respiratory disease in porcine respiratory coronavirus-infected pigs. Vet J 188, 210–215.CrossRefGoogle ScholarPubMed
Bachwich, PR, Chensue, SW, Larrick, JW & Kunkel, SL (1986). Tumor necrosis factor stimulates interleukin-1 and prostaglandin E2 production in resting macrophages. Biochem Biophys Res Commun 136, 94–101.CrossRefGoogle ScholarPubMed
Breyne, K, Steenbrugge, J, Demeyere, K, Vanden Berghe, T & Meyer, E (2017). Preconditioning with lipopolysaccharide or lipoteichoic acid protects against Staphylococcus aureus mammary infection in mice. Front Immunol 8, 833.CrossRefGoogle ScholarPubMed
Buettner, M & Bode, U (2012). Lymph node dissection–understanding the immunological function of lymph nodes. Clin Exp Immunol 169, 205–212.CrossRefGoogle ScholarPubMed
Bulgari, O, Dong, X, Roca, AL, Caroli, AM & Loor, JJ (2017). Innate immune responses induced by lipopolysaccharide and lipoteichoic acid in primary goat mammary epithelial cells. J Anim Sci Biotechnol 8, 1–10.CrossRefGoogle ScholarPubMed
Caminero, A, Comabella, M & Montalban, X (2011). Tumor necrosis factor alpha (TNF-α), anti-TNF-α and demyelination revisited: An ongoing story. J Neuroimmunol 234, 1–6.CrossRefGoogle Scholar
Chakraborty, S, Zawieja, SD, Wang, W, Lee, Y, Wang, YJ, von der Weid, P-Y, Zawieja, DC & Muthuchamy, M (2015). Lipopolysaccharide modulates neutrophil recruitment and macrophage polarization on lymphatic vessels and impairs lymphatic function in rat mesentery. Am J Physiol Heart Circ Physiol 309, H2042–H2057.CrossRefGoogle ScholarPubMed
Chang, J-S, Russell, GC, Jann, O, Glass, EJ, Werling, D & Haig, DM (2009). Molecular cloning and characterization of toll-like receptors 1-10 in sheep. Vet Immunol Immunopathol 127, 94–105.CrossRefGoogle ScholarPubMed
Crossmon, G (1937). A modification of mallory's connective tissue stain with a discussion of the principles involved. Anat Rec 69, 33–38.CrossRefGoogle Scholar
Deng, S, Wu, Q, Yu, K, Zhang, Y, Yao, Y, Li, W, Deng, Z, Liu, G, Li, W & Lian, Z (2012). Changes in the relative inflammatory responses in sheep cells overexpressing of toll-like receptor 4 when stimulated with LPS. PLoS One 7, 1–11.CrossRefGoogle ScholarPubMed
Detre, S, Saclani Jotti, G & Dowsett, M (1995). A “quickscore” method for immunohistochemical semiquantitation: Validation for oestrogen receptor in breast carcinomas. J Clin Pathol 48, 876–878.CrossRefGoogle ScholarPubMed
Dunne, A & O'Neill, LAJ (2005). Adaptor usage and toll-like receptor signaling specificity. FEBS Lett 579, 3330–3335.CrossRefGoogle ScholarPubMed
Elazar, S, Gonen, E, Livneh-Kol, A, Rosenshine, I & Shpigel, NY (2010). Neutrophil recruitment in endotoxin-induced murine mastitis is strictly dependent on mammary alveolar macrophages. Vet Res 41, 1–14.CrossRefGoogle ScholarPubMed
Enkhbaatar, P, Nelson, C, Salsbury, JR, Carmical, JR, Torres, KEO, Herndon, D, Prough, DS, Luan, L & Sherwood, ER (2015). Comparison of gene expression by sheep and human blood stimulated with the TLR4 agonists lipopolysaccharide and monophosphoryl lipid A. PLoS One 10, e0144345.CrossRefGoogle ScholarPubMed
Finney, SJ, Leaver, SK, Evans, TW & Burke-Gaffney, A (2012). Differences in lipopolysaccharide- and lipoteichoic acid-induced cytokine/chemokine expression. Intensive Care Med 38, 324–332.CrossRefGoogle ScholarPubMed
Firmal, P, Shah, VK & Chattopadhyay, S (2020). Insight into TLR4-mediated immunomodulation in normal pregnancy and related disorders. Front Immunol 11, 807.CrossRefGoogle ScholarPubMed
Fu, Y, Liu, B, Feng, X, Liu, Z, Liang, D, Li, F, Li, D, Cao, Y, Feng, S & Zhang, X (2013). Lipopolysaccharide increases toll-like receptor 4 and downstream toll-like receptor signaling molecules expression in bovine endometrial epithelial cells. Vet Immunol Immunopathol 151, 20–27.CrossRefGoogle ScholarPubMed
Ginsburg, I (2002). Role of lipoteichoic acid in infection and inflammation. Lancet Infect Dis 2, 171–179.CrossRefGoogle ScholarPubMed
Grunfeld, C, Marshall, M, Shigenaga, JK, Moser, AH, Tobias, P & Feingold, KR (1999). Lipoproteins inhibit macrophage activation by lipoteichoic acid. J Lipid Res 40, 245–252.CrossRefGoogle ScholarPubMed
Guo, Y, Zhao, G, Tanaka, S & Yamaguchi, T (2009). Differential responses between monocytes and monocyte-derived macrophages for lipopolysaccharide stimulation of calves. Cell Mol Immunol 6, 223–229.CrossRefGoogle ScholarPubMed
Haligur, A, Ozkadif, S & Alan, A (2019). Light and scanning electron microscopic study of lingual papillae in the wolf (Canis lupus). Microsc Res Tech 82, 501–506.CrossRefGoogle Scholar
Hillman, NH, Moss, TJM, Nitsos, I, Kramer, BW, Bachurski, CJ, Ikegami, M, Jobe, AH & Kallapur, SG (2008). Toll-like receptors and agonist responses in the developing fetal sheep lung. Pediatr Res 63, 388–393.CrossRefGoogle ScholarPubMed
Ibeagha-Awemu, EM, Lee, J-W, Ibeagha, AE, Bannerman, DD, Paape, MJ & Zhao, X (2008). Bacterial lipopolysaccharide induces increased expression of toll-like receptor (TLR) 4 and downstream TLR signaling molecules in bovine mammary epithelial cells. Vet Res 39, 1–12.CrossRefGoogle ScholarPubMed
Kawai, T, Adachi, O, Ogawa, T, Takeda, K & Akira, S (1999). Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11, 115–122.CrossRefGoogle ScholarPubMed
Kawakami, M, Ishibashi, S, Ogawa, H, Murase, T, Takaku, F & Shibata, S (1986). Cachectin/TNF as well as interleukin-1 induces prostacyclin synthesis in cultured vascular endothelial cells. Biochem Biophys Res Commun 141, 482–487.CrossRefGoogle ScholarPubMed
Kim, HG, Kim, N-R, Gim, MG, Lee, JM, Lee, SY, Ko, MY, Kim, JY, Han, SH & Chung, DK (2008). Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-α production in THP-1 cells and endotoxin shock in mice. J Immunol Res 180, 2553–2561.Google ScholarPubMed
Kozak, W, Zheng, H, Conn, CA, Soszynski, D, Van der Ploeg, LH & Kluger, MJ (1995). Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1 beta-deficient mice. Am J Physiol Regul Integr Comp Physiol 269, R969–R977.CrossRefGoogle ScholarPubMed
Lorentz, A, Baumann, A, Vitte, J & Blank, U (2012). The SNARE machinery in mast cell secretion. Front Physiol 3, 143.Google ScholarPubMed
Nijland, R, Hofland, T & Van Strijp, JAG (2014). Recognition of LPS by TLR4: Potential for anti-inflammatory therapies. Mar Drugs 12, 4260–4273.CrossRefGoogle ScholarPubMed
Percy, MG & Gründling, A (2014). Lipoteichoic acid synthesis and function in gram-positive bacteria. Annu Rev Microbiol 68, 81–100.CrossRefGoogle ScholarPubMed
Pérez-Rodríguez, MJ, Ibarra-Sánchez, A, Román-Figueroa, A, Pérez-Severiano, F & González-Espinosa, C (2020). Mutant huntingtin affects toll-like receptor 4 intracellular trafficking and cytokine production in mast cells. J Neuroinflammation 17, 1–18.CrossRefGoogle ScholarPubMed
Pfeffer, K (2003). Biological functions of tumor necrosis factor cytokines and their receptors. Cytokine Growth Factor Rev 14, 185–191.CrossRefGoogle ScholarPubMed
Rashidi, N, Mirahmadian, M, Jeddi-Tehrani, M, Rezania, S, Ghasemi, J, Kazemnejad, S, Mirzadegan, E, Vafaei, S, Kashanian, M & Rasoulzadeh, Z (2015). Lipopolysaccharide- and lipoteichoic acid-mediated pro-inflammatory cytokine production and modulation of TLR2, TLR4 and MyD88 expression in human endometrial cells. J Reprod Infertil 16, 72.Google ScholarPubMed
Rifkin, IR, Leadbetter, EA, Busconi, L, Viglianti, G & Marshak-Rothstein, A (2005). Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 204, 27–42.CrossRefGoogle ScholarPubMed
Sánchez-Tarjuelo, R, Cortegano, I, Manosalva, J, Rodríguez, M, Ruíz, C, Alía, M, Prado, MC, Cano, EM, Ferrándiz, MJ & de la Campa, AG (2020). The TLR4-MyD88 signaling axis regulates lung monocyte differentiation pathways in response to streptococcus pneumoniae. Front Immunol 11, 2120.CrossRefGoogle ScholarPubMed
Schaefer, TM, Desouza, K, Fahey, JV, Beagley, KW & Wira, CR (2004). Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 112, 428–436.CrossRefGoogle ScholarPubMed
Schmittgen, TD & Livak, KJ (2008). Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3, 1101–1108.CrossRefGoogle Scholar
Schwandner, R, Dziarski, R, Wesche, H, Rothe, M & Kirschning, CJ (1999). Peptidoglycan-and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem 274, 17406–17409.CrossRefGoogle ScholarPubMed
Strandberg, Y, Gray, C, Vuocolo, T, Donaldson, L, Broadway, M & Tellam, R (2005). Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in bovine mammary epithelial cells. Cytokine 31, 72–86.CrossRefGoogle ScholarPubMed
Su, X, Sykes, JB, Ao, L, Raeburn, CD, Fullerton, DA & Meng, X (2010). Extracellular heat shock cognate protein 70 induces cardiac functional tolerance to endotoxin: Differential effect on TNF-α and ICAM-1 levels in heart tissue. Cytokine 51, 60–66.CrossRefGoogle ScholarPubMed
Takeda, K, Kaisho, T & Akira, S (2003). Toll-like receptors. Annu Rev Immunol 21, 335–376.CrossRefGoogle ScholarPubMed
Van Gucht, S, Labarque, G & Van Reeth, K (2004). The combination of PRRS virus and bacterial endotoxin as a model for multifactorial respiratory disease in pigs. Vet Immunol Immunopathol 102, 165–178.CrossRefGoogle ScholarPubMed
Vijay, K (2018). Toll-like receptors in immunity and inflammatory diseases: Past, present, and future. Int Immunopharmacol 59, 391–412.CrossRefGoogle ScholarPubMed
Wei, S, Yang, D, Yang, J, Zhang, X, Zhang, J, Fu, J, Zhou, G, Liu, H, Lian, Z & Han, H (2019). Overexpression of toll-like receptor 4 enhances LPS-induced inflammatory response and inhibits Salmonella Typhimurium growth in ovine macrophages. Eur J Cell Biol 98, 36–50.CrossRefGoogle ScholarPubMed
Wu, H, Wang, H, Xiong, W, Chen, S, Tang, H & Han, D (2008). Expression patterns and functions of toll-like receptors in mouse sertoli cells. Endocrinology 149, 4402–4412.CrossRefGoogle ScholarPubMed
Wyns, H, Plessers, E, De Backer, P, Meyer, E & Croubels, S (2015). In vivo porcine lipopolysaccharide inflammation models to study immunomodulation of drugs. Vet Immunol Immunopathol 166, 58–69.CrossRefGoogle ScholarPubMed
Zhu, M & Fu, Y (2011). The role of core TNF/LIGHT family members in lymph node homeostasis and remodeling. Immunol Rev 244, 75–84.CrossRefGoogle ScholarPubMed