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Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte

Year 2022, Volume: 6 Issue: 1, 9 - 14, 29.03.2022
https://doi.org/10.47748/tjvr.1037041

Abstract

Objective: In this study, it was aimed to evaluate the levels of interleukins such as IL-1β, IL-6, IL-10 and IL-12β in Jaagsiekte sheep by immunohistochemical methods. In this way, it will be revealed whether interleukins are effective in the progression of Jaagsiekte and how useful they are in the diagnosis of the disease.
Material-Method: The material of current study consisted of lung tissues of 26 sheep (Control, n=6 and Jaagsiekte, n=20) brought to Department of Pathology for routine histopathological diagnosis. Tissue samples taken were fixed in 10% buffered formaldehyde solution. 5 µm-thick sections were taken from the paraffin blocks prepared after routine tissue follow-up procedures. Hematoxylin & Eosin staining was applied to the sections in order to detect histopathological changes. Sections were examined and photographed under a light microscope. The routine streptavidin–biotin peroxidase complex method was used.
Results: In sheep with Jaagsiekte, tumoral foci with large and small acinar or papillary growths were observed in the alveolar and bronchiole lumens. The control group was negative for IL-1β, IL-6, IL-10 and IL-12β immunoreactivity. IL 1β-6-10 and 12β levels were dramatically increased in the Jaagsiekte group compared to the control group.
Conclusion: It was determined that interleukins were produced from tumoral cells and tumor microenvironment elements, and these interleukins showed pro-inflammatory effects, except for IL-10. Data from the current study show that interleukins are very useful markers for the diagnosis of Jaagsiekte.

References

  • Referans1Airoldi I, Di Carlo E, Cocco C, Caci E, Cilli M, Sorrentino C, et al. IL-12 can Target Human Lung Adenocarcinoma Cells and Normal Bronchial Epithelial Cells Surrounding Tumor Lesions. PLoS One. 2009; 4(7): e6119.
  • Referans2Arango Duque G, Descoteaux A. Macrophage Cytokines: Involvement in Immunity and Infectious Diseases. Front Immunol. 2014; 5: 491.
  • Referans3Belalmi NEH, Sid N, Bennoune O, Ouhida S, Heras ML, Leroux C. Evidence of Jaagsiekte Sheep Retrovirus-induced Pulmonary Adenocarcinoma in Ouled Djellal Breed Sheep in Algeria. Vet Res Forum. 2020; 11(1): 93-95.
  • Referans4Bhat IA, Naykoo NA, Qasim I, Ganie FA, Yousuf Q, Bhat BA, et al. Association of Interleukin 1 Beta (IL-1β) Polymorphism with mRNA Expression and Risk of Non Small Cell Lung Cancer. Meta Gene. 2014; 2: 123-133.
  • Referans5Bugalho A, Martins C, Silva Z, Nunes G, Mendes AS, Ferreira I, et al. Immature Myeloid Cells and Tolerogenic Cytokine Profile in Lung Adenocarcinoma Metastatic Lymph Nodes Assessed by Endobronchial Ultrasound. Tumour Biol. 2016; 37(1): 953-961.
  • Referans6Ding X, Zhang J, Shi M, Liu D, Zhang L, Zhang R, et al. High Expression Level of Interleukin-1β is Correlated with Poor Prognosis and PD-1 Expression in Patients with Lung Adenocarcinoma. Clin Transl Oncol. 2021; 23(1): 35-42.
  • Referans7Dutkowska A, Szmyd B, Kaszkowiak M, Domańska-Senderowska D, Pastuszak-Lewandoska D, Brzeziańska-Lasota E, et al. Expression of Inflammatory Interleukins and Selected miRNAs in Non-Small Cell Lung Cancer. Sci Rep. 2021; 11(1): 5092.
  • Referans8D’Amico L, Ruffini E, Ferracini R, Roato I. Low Dose of IL-12 Stimulates T Cell Response in Cultures of PBMCs Derived from Non Small Cell Lung Cancer Patients. J Cancer Ther. 2012; 3(4): 337-342.
  • Referans9Gao Y, Lu J, Zeng C, Yang J, Huang B, Zhang N, et al. IL-10 suppresses IFN-γ-mediated signaling in lung adenocarcinoma. Clin Exp Med. 2020; 20(3): 449-459.
  • Referans10Gomes M, Archer F, Girard N, Gineys B, Dolmazon C, Bobet Erny A, et al. Blocked Expression of Key Genes of the Angiogenic Pathway in JSRV-induced Pulmonary Adenocarcinomas. Vet Res. 2017; 48(1): 76.
  • Referans11Hsu TI, Wang YC, Hung CY, Yu CH, Su WC, Chang WC, et al. Positive Feedback Regulation Between IL10 and EGFR Promotes Lung Cancer Formation. Oncotarget. 2016; 7(15): 20840-20854.
  • Referans12Hu X, Gu Y, Zhao S, Hua S, Jiang Y. Increased IL-10+CD206+CD14+M2-like Macrophages in Alveolar Lavage Fluid of Patients with Small Cell Lung Cancer. Cancer Immunol Immunother. 2020; 69(12): 2547-2560.
  • Referans13Islas-Vazquez L, Aguilar-Cazares D, Galicia-Velasco M, Rumbo-Nava U, Meneses-Flores M, Luna-Rivero C, et al. IL-6, NLR, and SII Markers and Their Relation with Alterations in CD8+ T-Lymphocyte Subpopulations in Patients Treated for Lung Adenocarcinoma. Biology (Basel). 2020; 9(11): 376.
  • Referans14Karagianni AE, Vasoya D, Finlayson J, Martineau HM, Wood AR, Cousens C, et al. Transcriptional Response of Ovine Lung to Infection with Jaagsiekte Sheep Retrovirus. J Virol. 2019; 93(21): e00876-19.
  • Referans15Ke W, Zhang L, Dai Y. The Role of IL-6 in Immunotherapy of Non-small Cell Lung Cancer (NSCLC) with Immune-related Adverse Events (irAEs). Thorac Cancer 2020; 11(4): 835-839.
  • Referans16Kim JW, Koh Y, Kim DW, Ahn YO, Kim TM, Han SW, et al. Clinical Implications of VEGF, TGF-β1, and IL-1β in Patients with Advanced Non-small Cell Lung Cancer. Cancer Res Treat. 2013; 45(4): 325-333.
  • Referans17Kiss E, Abdelwahab EHMM, Steib A, Papp E, Torok Z, Jakab L, et al. Cisplatin Treatment Induced Interleukin 6 and 8 Production Alters Lung Adenocarcinoma Cell Migration in an Oncogenic Mutation Dependent Manner. Respir Res. 2020; 21(1): 120.
  • Referans18Larruskain A, Esparza-Baquer A, Minguijón E, Juste RA, Jugo BM. SNPs in Candidate Genes MX Dynamin-like GTPase and Chemokine (C-C motif) Receptor-5 are Associated with Ovine Pulmonary Adenocarcinoma Progression in Latxa Sheep. Anim Genet 2015; 46 (6): 666-675.
  • Referans19Larruskain A, Jugo BM. Retroviral Infections in Sheep and Goats: Small Ruminant Lentiviruses and Host Interaction. Viruses. 2013; 5(8): 2043-2061.
  • Referans20Larruskain A, Minguijón E, Arostegui I, Moreno B, Juste RA, Jugo BM. Microsatellites in Immune-relevant Regions and Their Associations with Maedi-Visna and Ovine Pulmonary Adenocarcinoma Viral Diseases. Vet Immunol Immunopathol. 2012; 145(1-2): 438-446.
  • Referans21Lee AM, Wolfe A, Cassidy JP, McV Messam LL, Moriarty JP, O'Neill R, et al. First Confirmation by PCR of Jaagsiekte Sheep Retrovirus in Ireland and Prevalence of Ovine Pulmonary Adenocarcinoma in Adult Sheep at Slaughter. Ir Vet J. 2017; 70: 33.
  • Referans22Li L, Li D, Chen Y. miRNA-26a Blocks Interleukin-2-mediated Migration and Proliferation of Non-small Cell Lung Cancer Cells via Vascular Cell Adhesion Molecule-1. Transl Cancer Res. 2020; 9 (3): 1768-1778.
  • Referans23Li R, Ong SL, Tran LM, Jing Z, Liu B, Park SJ, et al. Author Correction: Chronic IL-1β-induced Inflammation Regulates Epithelial-to-mesenchymal Transition Memory Phenotypes via Epigenetic Modifications in Non-small Cell Lung Cancer. Sci Rep. 2020; 10(1): 4386. Erratum for: Sci Rep. 2020; 10(1): 377.
  • Referans24Pan T, Zhang F, Li F, Gao X, Li Z, Li X, et al. Shikonin Blocks Human Lung Adenocarcinoma Cell Migration and Invasion in the Inflammatory Microenvironment via the IL‑6/STAT3 Signaling Pathway. Oncol Rep. 2020; 44(3): 1049-1063.
  • Referans25Pang L, Han S, Jiao Y, Jiang S, He X, Li P. Bu Fei Decoction Attenuates the Tumor Associated Macrophage Stimulated Proliferation, Migration, Invasion and Immunosuppression of Non-small Cell Lung Cancer, Partially via IL-10 and PD-L1 Regulation. Int J Oncol. 2017; 51(1): 25-38.
  • Referans26Petrella BL, Armstrong DA, Vincenti MP. Interleukin-1 Beta and Transforming Growth Factor-beta 3 Cooperate to Activate Matrix Metalloproteinase Expression and Invasiveness in A549 Lung Adenocarcinoma Cells. Cancer Letters 2012; 325(2): 220-226.
  • Referans27Scott PR, Dagleish MP, Cousens C. Development of Superficial Lung Lesions Monitored on Farm by Serial Ultrasonographic Examination in Sheep with Lesions Confirmed as Ovine Pulmonary Adenocarcinoma at Necropsy. Ir Vet J. 2018; 71: 23.
  • Referans28Su XH, Zhu YR, Hou YJ, Li K, Dong NH. PVT1 Induces NSCLC Cell Migration and Invasion by Regulating IL-6 via Sponging miR-760. Molecular and Cellular Probes 2020; 54: 101652.
  • Referans29Tekpli X, Landvik NE, Anmarkud KH, Skaug V, Haugen A, Zienolddiny S. DNA Methylation at Promoter Regions of Interleukin 1B, Interleukin 6, and Interleukin 8 in Non-small Cell Lung Cancer. Cancer Immunol Immunother. 20131; 62(2): 337-345.
  • Referans30Toma C, Bâlteanu VA, Tripon S, Trifa A, Rema A, Amorim I, et al. Exogenous Jaagsiekte Sheep Retrovirus Type 2 (exJSRV2) Related to Ovine Pulmonary Adenocarcinoma (OPA) in Romania: Prevalence, Anatomical Forms, Pathological Description, Immunophenotyping and Virus Identification. BMC Vet Res. 2020; 16(1): 296.
  • Referans31Turner MD, Nedjai B, Hurst T, Pennington DJ. Cytokines and Chemokines: At the Crossroads of Cell Signalling and Inflammatory Disease. Biochim Biophys Acta. 2014; 1843(11): 2563-2582.
  • Referans32Vahl JM, Friedrich J, Mittler S, Trump S, Heim L, Kachler K, et al. Interleukin-10-Regulated Tumour Tolerance in Non-small Cell Lung Cancer. Br J Cancer. 2017; 117(11): 1644-1655.
  • Referans33Yang L, Dong Y, Li Y, Wang D, Liu S, Wang D, et al. IL-10 Derived From M2 Macrophage Promotes Cancer Stemness via JAK1/STAT1/NF-κB/Notch1 Pathway in Non-small Cell Lung Cancer. Int J Cancer. 2019; 145(4): 1099-1110.
  • Referans34Yue T, Zheng X, Dou Y, Zheng X, Sun R, Tian Z, et al. Interleukin 12 Shows a Better Curative Effect on Lung Cancer than Paclitaxel and Cisplatin Doublet Chemotherapy. BMC Cancer. 2016; 16(1): 665.
Year 2022, Volume: 6 Issue: 1, 9 - 14, 29.03.2022
https://doi.org/10.47748/tjvr.1037041

Abstract

References

  • Referans1Airoldi I, Di Carlo E, Cocco C, Caci E, Cilli M, Sorrentino C, et al. IL-12 can Target Human Lung Adenocarcinoma Cells and Normal Bronchial Epithelial Cells Surrounding Tumor Lesions. PLoS One. 2009; 4(7): e6119.
  • Referans2Arango Duque G, Descoteaux A. Macrophage Cytokines: Involvement in Immunity and Infectious Diseases. Front Immunol. 2014; 5: 491.
  • Referans3Belalmi NEH, Sid N, Bennoune O, Ouhida S, Heras ML, Leroux C. Evidence of Jaagsiekte Sheep Retrovirus-induced Pulmonary Adenocarcinoma in Ouled Djellal Breed Sheep in Algeria. Vet Res Forum. 2020; 11(1): 93-95.
  • Referans4Bhat IA, Naykoo NA, Qasim I, Ganie FA, Yousuf Q, Bhat BA, et al. Association of Interleukin 1 Beta (IL-1β) Polymorphism with mRNA Expression and Risk of Non Small Cell Lung Cancer. Meta Gene. 2014; 2: 123-133.
  • Referans5Bugalho A, Martins C, Silva Z, Nunes G, Mendes AS, Ferreira I, et al. Immature Myeloid Cells and Tolerogenic Cytokine Profile in Lung Adenocarcinoma Metastatic Lymph Nodes Assessed by Endobronchial Ultrasound. Tumour Biol. 2016; 37(1): 953-961.
  • Referans6Ding X, Zhang J, Shi M, Liu D, Zhang L, Zhang R, et al. High Expression Level of Interleukin-1β is Correlated with Poor Prognosis and PD-1 Expression in Patients with Lung Adenocarcinoma. Clin Transl Oncol. 2021; 23(1): 35-42.
  • Referans7Dutkowska A, Szmyd B, Kaszkowiak M, Domańska-Senderowska D, Pastuszak-Lewandoska D, Brzeziańska-Lasota E, et al. Expression of Inflammatory Interleukins and Selected miRNAs in Non-Small Cell Lung Cancer. Sci Rep. 2021; 11(1): 5092.
  • Referans8D’Amico L, Ruffini E, Ferracini R, Roato I. Low Dose of IL-12 Stimulates T Cell Response in Cultures of PBMCs Derived from Non Small Cell Lung Cancer Patients. J Cancer Ther. 2012; 3(4): 337-342.
  • Referans9Gao Y, Lu J, Zeng C, Yang J, Huang B, Zhang N, et al. IL-10 suppresses IFN-γ-mediated signaling in lung adenocarcinoma. Clin Exp Med. 2020; 20(3): 449-459.
  • Referans10Gomes M, Archer F, Girard N, Gineys B, Dolmazon C, Bobet Erny A, et al. Blocked Expression of Key Genes of the Angiogenic Pathway in JSRV-induced Pulmonary Adenocarcinomas. Vet Res. 2017; 48(1): 76.
  • Referans11Hsu TI, Wang YC, Hung CY, Yu CH, Su WC, Chang WC, et al. Positive Feedback Regulation Between IL10 and EGFR Promotes Lung Cancer Formation. Oncotarget. 2016; 7(15): 20840-20854.
  • Referans12Hu X, Gu Y, Zhao S, Hua S, Jiang Y. Increased IL-10+CD206+CD14+M2-like Macrophages in Alveolar Lavage Fluid of Patients with Small Cell Lung Cancer. Cancer Immunol Immunother. 2020; 69(12): 2547-2560.
  • Referans13Islas-Vazquez L, Aguilar-Cazares D, Galicia-Velasco M, Rumbo-Nava U, Meneses-Flores M, Luna-Rivero C, et al. IL-6, NLR, and SII Markers and Their Relation with Alterations in CD8+ T-Lymphocyte Subpopulations in Patients Treated for Lung Adenocarcinoma. Biology (Basel). 2020; 9(11): 376.
  • Referans14Karagianni AE, Vasoya D, Finlayson J, Martineau HM, Wood AR, Cousens C, et al. Transcriptional Response of Ovine Lung to Infection with Jaagsiekte Sheep Retrovirus. J Virol. 2019; 93(21): e00876-19.
  • Referans15Ke W, Zhang L, Dai Y. The Role of IL-6 in Immunotherapy of Non-small Cell Lung Cancer (NSCLC) with Immune-related Adverse Events (irAEs). Thorac Cancer 2020; 11(4): 835-839.
  • Referans16Kim JW, Koh Y, Kim DW, Ahn YO, Kim TM, Han SW, et al. Clinical Implications of VEGF, TGF-β1, and IL-1β in Patients with Advanced Non-small Cell Lung Cancer. Cancer Res Treat. 2013; 45(4): 325-333.
  • Referans17Kiss E, Abdelwahab EHMM, Steib A, Papp E, Torok Z, Jakab L, et al. Cisplatin Treatment Induced Interleukin 6 and 8 Production Alters Lung Adenocarcinoma Cell Migration in an Oncogenic Mutation Dependent Manner. Respir Res. 2020; 21(1): 120.
  • Referans18Larruskain A, Esparza-Baquer A, Minguijón E, Juste RA, Jugo BM. SNPs in Candidate Genes MX Dynamin-like GTPase and Chemokine (C-C motif) Receptor-5 are Associated with Ovine Pulmonary Adenocarcinoma Progression in Latxa Sheep. Anim Genet 2015; 46 (6): 666-675.
  • Referans19Larruskain A, Jugo BM. Retroviral Infections in Sheep and Goats: Small Ruminant Lentiviruses and Host Interaction. Viruses. 2013; 5(8): 2043-2061.
  • Referans20Larruskain A, Minguijón E, Arostegui I, Moreno B, Juste RA, Jugo BM. Microsatellites in Immune-relevant Regions and Their Associations with Maedi-Visna and Ovine Pulmonary Adenocarcinoma Viral Diseases. Vet Immunol Immunopathol. 2012; 145(1-2): 438-446.
  • Referans21Lee AM, Wolfe A, Cassidy JP, McV Messam LL, Moriarty JP, O'Neill R, et al. First Confirmation by PCR of Jaagsiekte Sheep Retrovirus in Ireland and Prevalence of Ovine Pulmonary Adenocarcinoma in Adult Sheep at Slaughter. Ir Vet J. 2017; 70: 33.
  • Referans22Li L, Li D, Chen Y. miRNA-26a Blocks Interleukin-2-mediated Migration and Proliferation of Non-small Cell Lung Cancer Cells via Vascular Cell Adhesion Molecule-1. Transl Cancer Res. 2020; 9 (3): 1768-1778.
  • Referans23Li R, Ong SL, Tran LM, Jing Z, Liu B, Park SJ, et al. Author Correction: Chronic IL-1β-induced Inflammation Regulates Epithelial-to-mesenchymal Transition Memory Phenotypes via Epigenetic Modifications in Non-small Cell Lung Cancer. Sci Rep. 2020; 10(1): 4386. Erratum for: Sci Rep. 2020; 10(1): 377.
  • Referans24Pan T, Zhang F, Li F, Gao X, Li Z, Li X, et al. Shikonin Blocks Human Lung Adenocarcinoma Cell Migration and Invasion in the Inflammatory Microenvironment via the IL‑6/STAT3 Signaling Pathway. Oncol Rep. 2020; 44(3): 1049-1063.
  • Referans25Pang L, Han S, Jiao Y, Jiang S, He X, Li P. Bu Fei Decoction Attenuates the Tumor Associated Macrophage Stimulated Proliferation, Migration, Invasion and Immunosuppression of Non-small Cell Lung Cancer, Partially via IL-10 and PD-L1 Regulation. Int J Oncol. 2017; 51(1): 25-38.
  • Referans26Petrella BL, Armstrong DA, Vincenti MP. Interleukin-1 Beta and Transforming Growth Factor-beta 3 Cooperate to Activate Matrix Metalloproteinase Expression and Invasiveness in A549 Lung Adenocarcinoma Cells. Cancer Letters 2012; 325(2): 220-226.
  • Referans27Scott PR, Dagleish MP, Cousens C. Development of Superficial Lung Lesions Monitored on Farm by Serial Ultrasonographic Examination in Sheep with Lesions Confirmed as Ovine Pulmonary Adenocarcinoma at Necropsy. Ir Vet J. 2018; 71: 23.
  • Referans28Su XH, Zhu YR, Hou YJ, Li K, Dong NH. PVT1 Induces NSCLC Cell Migration and Invasion by Regulating IL-6 via Sponging miR-760. Molecular and Cellular Probes 2020; 54: 101652.
  • Referans29Tekpli X, Landvik NE, Anmarkud KH, Skaug V, Haugen A, Zienolddiny S. DNA Methylation at Promoter Regions of Interleukin 1B, Interleukin 6, and Interleukin 8 in Non-small Cell Lung Cancer. Cancer Immunol Immunother. 20131; 62(2): 337-345.
  • Referans30Toma C, Bâlteanu VA, Tripon S, Trifa A, Rema A, Amorim I, et al. Exogenous Jaagsiekte Sheep Retrovirus Type 2 (exJSRV2) Related to Ovine Pulmonary Adenocarcinoma (OPA) in Romania: Prevalence, Anatomical Forms, Pathological Description, Immunophenotyping and Virus Identification. BMC Vet Res. 2020; 16(1): 296.
  • Referans31Turner MD, Nedjai B, Hurst T, Pennington DJ. Cytokines and Chemokines: At the Crossroads of Cell Signalling and Inflammatory Disease. Biochim Biophys Acta. 2014; 1843(11): 2563-2582.
  • Referans32Vahl JM, Friedrich J, Mittler S, Trump S, Heim L, Kachler K, et al. Interleukin-10-Regulated Tumour Tolerance in Non-small Cell Lung Cancer. Br J Cancer. 2017; 117(11): 1644-1655.
  • Referans33Yang L, Dong Y, Li Y, Wang D, Liu S, Wang D, et al. IL-10 Derived From M2 Macrophage Promotes Cancer Stemness via JAK1/STAT1/NF-κB/Notch1 Pathway in Non-small Cell Lung Cancer. Int J Cancer. 2019; 145(4): 1099-1110.
  • Referans34Yue T, Zheng X, Dou Y, Zheng X, Sun R, Tian Z, et al. Interleukin 12 Shows a Better Curative Effect on Lung Cancer than Paclitaxel and Cisplatin Doublet Chemotherapy. BMC Cancer. 2016; 16(1): 665.
There are 34 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section 2022 Volume 6 Number 1
Authors

Emin Karakurt 0000-0003-2019-3690

Enver Beytut 0000-0003-3360-2940

Serpil Dağ 0000-0001-7667-689X

Hilmi Nuhoğlu 0000-0003-2530-2542

Ayfer Yıldız 0000-0002-6569-5435

Emre Kurtbaş 0000-0002-9752-194X

Early Pub Date March 26, 2022
Publication Date March 29, 2022
Submission Date December 15, 2021
Published in Issue Year 2022 Volume: 6 Issue: 1

Cite

APA Karakurt, E., Beytut, E., Dağ, S., Nuhoğlu, H., et al. (2022). Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte. Turkish Journal of Veterinary Research, 6(1), 9-14. https://doi.org/10.47748/tjvr.1037041
AMA Karakurt E, Beytut E, Dağ S, Nuhoğlu H, Yıldız A, Kurtbaş E. Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte. TJVR. March 2022;6(1):9-14. doi:10.47748/tjvr.1037041
Chicago Karakurt, Emin, Enver Beytut, Serpil Dağ, Hilmi Nuhoğlu, Ayfer Yıldız, and Emre Kurtbaş. “Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep With Jaagsiekte”. Turkish Journal of Veterinary Research 6, no. 1 (March 2022): 9-14. https://doi.org/10.47748/tjvr.1037041.
EndNote Karakurt E, Beytut E, Dağ S, Nuhoğlu H, Yıldız A, Kurtbaş E (March 1, 2022) Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte. Turkish Journal of Veterinary Research 6 1 9–14.
IEEE E. Karakurt, E. Beytut, S. Dağ, H. Nuhoğlu, A. Yıldız, and E. Kurtbaş, “Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte”, TJVR, vol. 6, no. 1, pp. 9–14, 2022, doi: 10.47748/tjvr.1037041.
ISNAD Karakurt, Emin et al. “Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep With Jaagsiekte”. Turkish Journal of Veterinary Research 6/1 (March 2022), 9-14. https://doi.org/10.47748/tjvr.1037041.
JAMA Karakurt E, Beytut E, Dağ S, Nuhoğlu H, Yıldız A, Kurtbaş E. Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte. TJVR. 2022;6:9–14.
MLA Karakurt, Emin et al. “Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep With Jaagsiekte”. Turkish Journal of Veterinary Research, vol. 6, no. 1, 2022, pp. 9-14, doi:10.47748/tjvr.1037041.
Vancouver Karakurt E, Beytut E, Dağ S, Nuhoğlu H, Yıldız A, Kurtbaş E. Immunohistochemical Detection of Pro-Inflammatory and Anti-Inflammatory Interleukins in the Lungs of Sheep with Jaagsiekte. TJVR. 2022;6(1):9-14.