Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T08:58:11.677Z Has data issue: false hasContentIssue false

In vitro influence of Theileria annulata on the functions of bovine dendritic cells for stimulation of T lymphocyte proliferation

Published online by Cambridge University Press:  10 September 2019

Muhammad Rashid
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Junlong Liu*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Guiquan Guan
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Jinming Wang
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Zhi Li
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Muhammad Adeel Hassan
Affiliation:
Department of Parasitology, Cholistan University of Veterinary and Animal Sciences, Bahawalpur63100, Pakistan
Muhammad Imran Rashid
Affiliation:
Department of Parasitology, University of Veterinary and Animal Sciences, Lahore54200, Pakistan
Muhammad Uzair Mukhtar
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Jianxun Luo
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China
Hong Yin*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu730046, People's Republic of China Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Disease and Zoonose, Yangzhou University, Yangzhou225009, People's Republic of China
*
Author for correspondence: Junlon Liu, E-mail: liujunlong@caas.cn and Hong Yin, E-mail: yinhong@caas.cn
Author for correspondence: Junlon Liu, E-mail: liujunlong@caas.cn and Hong Yin, E-mail: yinhong@caas.cn

Abstract

The present study was performed on antigen-presenting cells (APCs) of Theileria annulata transformed dendritic cells (TaDCs) and monocyte-derived dendritic cells (MoDCs) to compare differences in antigen presentation and stimulation of T lymphocyte proliferation. Antigen presentation for T lymphocyte proliferation was analysed by flow cytometry. Additionally, the level of mRNA transcription of small GTPases of the Rab family expressed in the TaDC cell line was analysed by quantitative real-time polymerase chain reaction (Q-RT-PCR). The endocytosis rate of TaDCs was significantly (P < 0.01) lower than in MoDCs. In contrast, when T lymphocytes were co-cultured with TaDC-APCs T cell proliferation was similar, while co-culture with MoDC-APC stimulated proliferation of CD4+ cells to a greater degree than CD8+ cells. However, the efficacy of TaDC-APCs to stimulate T lymphocytes dropped as the number of passages of TaDC-APC increased. Likewise, the transcription level of Rab family genes also significantly (P > 0.001) declined with progressive passages (>50) of the TaDC cell line. We conclude that initially the TaDC cell line efficiently presents antigen to stimulate T lymphocyte proliferation to produce a cellular immune response against the presented antigen.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019

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

Bull, M, Lee, D, Stucky, J, Chiu, Y-L, Rubin, A, Horton, H and McElrath, MJ (2007) Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. Journal of Immunological Methods 322, 5769.CrossRefGoogle ScholarPubMed
Cebrian, I, Croce, C, Guerrero, NA, Blanchard, N and Mayorga, LS (2016) Rab22a controls MHC-I intracellular trafficking and antigen cross-presentation by dendritic cells. EMBO Reports 17, 17531756.CrossRefGoogle ScholarPubMed
Chiang, SC, Theorell, J, Entesarian, M, Meeths, M, Mastafa, M, Al-Herz, W, Frisk, P, Gilmour, KC, Ifversen, M and Langenskiöld, C (2013) Comparison of primary human cytotoxic T cell and natural killer cell responses reveal similar molecular requirements for lytic granule exocytosis but differences in cytokine production. Blood 121, 13451356.CrossRefGoogle ScholarPubMed
Coussens, PM, Verman, N, Coussens, MA, Elftman, MD and McNulty, AM (2004) Cytokine gene expression in peripheral blood mononuclear cells and tissues of cattle infected with Mycobacterium avium subsp. paratuberculosis: evidence for an inherent proinflammatory gene expression pattern. Infection and Immunity 72, 14091422.CrossRefGoogle ScholarPubMed
Hart, J, MacHugh, ND and Morrison, WI (2011) Theileria annulata-transformed cell lines are efficient antigen-presenting cells for in vitro analysis of CD8 T cell responses to bovine herpesvirus-1. Veterinary Research 42, 119.CrossRefGoogle ScholarPubMed
Hassan, MA, Liu, J, Sajid, MS, Mahmood, A, Zhao, SY, Abbas, Q, Guan, G, Yin, H and Luo, J (2018) Molecular detection of Theileria annulata in cattle from different regions of Punjab, Pakistan using recombinase polymerase amplification and PCR. Journal of Parasitology 104, 196201.CrossRefGoogle Scholar
Hayashida, K, Hara, Y, Abe, T, Yamasaki, C, Toyoda, A, Kosuge, T, Suzuki, Y, Sato, Y, Kawashima, S and Katayama, T (2012) Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation. MBio 3, e00204e00212.CrossRefGoogle ScholarPubMed
Huppa, JB, Axmann, M, Mörtelmaier, MA, Lillemeier, BF, Newell, EW, Brameshuber, M, Klein, LO, Schütz, GJ and Davis, MM (2010) TCR–peptide–MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463, 963.CrossRefGoogle ScholarPubMed
Imai, T, Kato, Y, Kajiwara, C, Mizukami, S, Ishige, I, Ichiyanagi, T, Hikida, M, Wang, J-Y and Udono, H (2011) Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proceedings of the National Academy of Sciences 108, 1636316368.CrossRefGoogle ScholarPubMed
Inaba, K, Metlay, JP, Crowley, MT and Steinman, RM (1990) Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. Journal of Experimental Medicine 172, 631640.CrossRefGoogle Scholar
Jancic, C, Savina, A, Wasmeier, C, Tolmachova, T, El-Benna, J, Dang, PM-C, Pascolo, S, Gougerot-Pocidalo, M-A, Raposo, G and Seabra, MC (2007) Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nature Cell Biology 9, 367.CrossRefGoogle ScholarPubMed
Kamphorst, AO, Guermonprez, P, Dudziak, D and Nussenzweig, MC (2010) Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. The Journal of Immunology 185, 34263435.CrossRefGoogle ScholarPubMed
Karamitros, D, Kotantaki, P, Lygerou, Z, Kioussis, D and Taraviras, S (2011) T cell proliferation and homeostasis: an emerging role for the cell cycle inhibitor geminin. Critical Reviews in Immunology 31, 209231.CrossRefGoogle ScholarPubMed
Kennedy, R, Undale, AH, Kieper, WC, Block, MS, Pease, LR and Celis, E (2005) Direct cross-priming by Th lymphocytes generates memory cytotoxic T cell responses. The Journal of Immunology 174, 39673977.CrossRefGoogle ScholarPubMed
Kikuchi, K, Yanagawa, Y and Onoé, K (2005) CCR7 ligand-enhanced phagocytosis of various antigens in mature dendritic cells – time course and antigen distribution different from phagocytosis in immature dendritic cells. Microbiology and Immunology 49, 535544.CrossRefGoogle ScholarPubMed
Kim, SH, Visser, A, Cruijsen, C, van der Velden, AW and Boes, M (2008) Recruitment of Rab27a to phagosomes controls microbial antigen cross-presentation by dendritic cells. Infection and Immunity 76, 53735380.CrossRefGoogle ScholarPubMed
Liu, Q and Gao, B (2008) Manipulation of MHC-I/TCR interaction for immune therapy. Cellular & Molecular Immunology 5, 171.CrossRefGoogle ScholarPubMed
Mahnke, K, Guo, M, Lee, S, Sepulveda, H, Swain, SL, Nussenzweig, M and Steinman, RM (2000) The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II–positive lysosomal compartments. The Journal of Cell Biology 151, 673684.CrossRefGoogle ScholarPubMed
Mannering, SI, Zhong, J and Cheers, C (2002) T-cell activation, proliferation and apoptosis in primary Listeria monocytogenes infection. Immunology 106, 8795.CrossRefGoogle ScholarPubMed
Mayorga, LS and Cebrian, I (2018) Rab22a: a novel regulator of immune functions. Molecular Immunology 15, 246259.Google Scholar
Monrad, SU, Rea, K, Thacker, S and Kaplan, MJ (2008) Myeloid dendritic cells display downregulation of C-type lectin receptors and aberrant lectin uptake in systemic lupus erythematosus. Arthritis Research & Therapy 10, R114.CrossRefGoogle ScholarPubMed
Moreau, M-F, Thibaud, J-L, Miled, LB, Chaussepied, M, Baumgartner, M, Davis, WC, Minoprio, P and Langsley, G (1999) Theileria annulata in CD5+ macrophages and B1 B cells. Infection and Immunity 67, 66786682.Google ScholarPubMed
Nierkens, S, Tel, J, Janssen, E and Adema, GJ (2013) Antigen cross-presentation by dendritic cell subsets: one general or all sergeants? Trends in Immunology 34, 361370.CrossRefGoogle ScholarPubMed
Obermaier, B, Dauer, M, Herten, J, Schad, K, Endres, S and Eigler, A (2003) Development of a new protocol for 2-day generation of mature dendritic cells from human monocytes. Biological Procedures Online 5, 197203.CrossRefGoogle ScholarPubMed
Obst, R, van Santen, H-M, Melamed, R, Kamphorst, AO, Benoist, C and Mathis, D (2007) Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proceedings of the National Academy of Sciences 104, 1546015465.CrossRefGoogle ScholarPubMed
Rao, X, Huang, X, Zhou, Z and Lin, X (2013) An improvement of the 2^(–delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostatistics, Bioinformatics and Biomathematics 3, 7185.Google ScholarPubMed
Rashid, M, Akbar, H, Rashid, I, Saeed, K, Ahmad, L, Ahmad, AS, Shehzad, W, Islam, S and Farooqi, S (2018) Economic significance of tropical theileriosis on a Holstein Friesian dairy farm in Pakistan. The Journal of Parasitology 104, 310312.CrossRefGoogle ScholarPubMed
Rashid, M, Guan, G, Luo, J, Zhao, S, Wang, X, Rashid, MI, Hassan, MA, Mukhtar, MU, Liu, J and Yin, H (2019a) Establishment and expression of cytokines in a Theileria annulata-infected bovine B cell line. Genes 10, 329.CrossRefGoogle Scholar
Rashid, M, Rashid, MI, Akbar, H, Ahmad, L, Hassan, MA, Ashraf, K, Saeed, K and Gharbi, M (2019b) A systematic review on modelling approaches for economic losses studies caused by parasites and their associated diseases in cattle. Parasitology 146, 129141.CrossRefGoogle Scholar
Rio, DC, Ares, M, Hannon, GJ and Nilsen, TW (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harbor Protocols 2010, pdb. prot5439.CrossRefGoogle Scholar
Sager, H, Brunschwiler, C and Jungi, TW (1998) Interferon production by Theileria annulata-transformed cell lines is restricted to the beta family. Parasite Immunology 20, 175182.CrossRefGoogle ScholarPubMed
Sager, H, Davis, WC and Jungi, TW (1999) Bovine monocytoid cells transformed to proliferate cease to exhibit lineage-specific functions. Veterinary Immunology and Immunopathology 68, 113130.CrossRefGoogle ScholarPubMed
Sallusto, F, Cella, M, Danieli, C and Lanzavecchia, A (1995) Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. Journal of Experimental Medicine 182, 389400.CrossRefGoogle ScholarPubMed
Savina, A and Amigorena, S (2007) Phagocytosis and antigen presentation in dendritic cells. Immunological Reviews 219, 143156.CrossRefGoogle ScholarPubMed
Savina, A, Jancic, C, Hugues, S, Guermonprez, P, Vargas, P, Moura, IC, Lennon-Duménil, A-M, Seabra, MC, Raposo, G and Amigorena, S (2006) NOX2 controls phagosomal pH to regulate antigen processing during cross-presentation by dendritic cells. Cell 126, 205218.CrossRefGoogle Scholar
Schoenberger, SP, Toes, RE, van der Voort, EI, Offringa, R and Melief, CJ (1998) T-cell help for cytotoxic T lymphocytes is mediated by CD40–CD40L interactions. Nature 393, 480483.CrossRefGoogle ScholarPubMed
Stephens, S and Howard, C (2002) Infection and transformation of dendritic cells from bovine afferent lymph by Theileria annulata. Parasitology 124, 485493.CrossRefGoogle ScholarPubMed
Tretina, K, Gotia, HT, Mann, DJ and Silva, JC (2015) Theileria-transformed bovine leukocytes have cancer hallmarks. Trends in Parasitology 31, 306314.CrossRefGoogle ScholarPubMed
Umeshappa, CS, Huang, H, Xie, Y, Wei, Y, Mulligan, SJ, Deng, Y and Xiang, J (2009) CD4+ Th-APC with acquired peptide/MHC class I and II complexes stimulate type 1 helper CD4+ and central memory CD8+ T cell responses. The Journal of Immunology 182, 193206.CrossRefGoogle Scholar
Wang, C, Liu, Z and Huang, X (2012) Rab32 is important for autophagy and lipid storage in Drosophila. PLoS One 7, e32086.CrossRefGoogle ScholarPubMed
Weimershaus, M, Maschalidi, S, Sepulveda, F, Manoury, B, van Endert, P and Saveanu, L (2012) Conventional dendritic cells require IRAP-Rab14 endosomes for efficient cross-presentation. The Journal of Immunology 188, 18401846.CrossRefGoogle ScholarPubMed
Wong, NK, Shenoi, RA, Abbina, S, Chafeeva, I, Kizhakkedathu, JN and Khan, MK (2017) Nontransformed and cancer cells can utilize different endocytic pathways to internalize dendritic nanoparticle variants: implications on nanocarrier design. Biomacromolecules 18, 24272438.CrossRefGoogle ScholarPubMed
Wu, L-G, Hamid, E, Shin, W and Chiang, H-C (2014) Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annual Review of Physiology 76, 301331.CrossRefGoogle ScholarPubMed
Wykes, M, Pombo, A, Jenkins, C and MacPherson, GG (1998) Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. The Journal of Immunology 161, 13131319.Google Scholar
Zehner, M, Marschall, AL, Bos, E, Schloetel, J-G, Kreer, C, Fehrenschild, D, Limmer, A, Ossendorp, F, Lang, T and Koster, AJ (2015) The translocon protein Sec61 mediates antigen transport from endosomes in the cytosol for cross-presentation to CD8+ T cells. Immunity 42, 850863.CrossRefGoogle ScholarPubMed
Zhao, S, Guan, G, Liu, J, Liu, A, Li, Y, Yin, H and Luo, J (2017) Screening and identification of host proteins interacting with Theileria annulata cysteine proteinase (TaCP) by yeast-two-hybrid system. Parasites & Vectors 10, 536.CrossRefGoogle ScholarPubMed
Zhao, S, Liu, J, Guan, G, Liu, A, Li, Y, Yin, H and Luo, J (2018) Theileria annulata Cyclophilin1 (TaCyp1) interacts with host cell MED21. Frontiers in Microbiology 9, 2973.CrossRefGoogle ScholarPubMed
Zhou, Y, Wu, J, Liu, C, Guo, X, Zhu, X, Yao, Y, Jiao, Y, He, P, Han, J and Wu, L (2016) P38α has an important role in antigen cross-presentation by dendritic cells. Cellular & Molecular Immunology 15, 246259.CrossRefGoogle ScholarPubMed
Zou, L, Zhou, J, Zhang, J, Li, J, Liu, N, Chai, L, Li, N, Liu, T, Li, L and Xie, Z (2009) The GTPase Rab3b/3c-positive recycling vesicles are involved in cross-presentation in dendritic cells. Proceedings of the National Academy of Sciences 106, 1580115806.CrossRefGoogle ScholarPubMed
Supplementary material: File

Rashid et al. supplementary material

Rashid et al. supplementary material

Download Rashid et al. supplementary material(File)
File 293.6 KB