Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Ver. Summary Created by Modification Content Size Created at Operation
1
Christine A. Jansen
 + 2151 word(s) 2151 2021-11-23 03:59:30 |
2 format correct
Conner Chen
 Meta information modification 2151 2021-12-23 02:34:10 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Jansen, C.A. Innate Immune Cells in the Chicken Intestine. Encyclopedia. Available online: https://encyclopedia.pub/entry/17444 (accessed on 11 December 2023).
Jansen CA. Innate Immune Cells in the Chicken Intestine. Encyclopedia. Available at: https://encyclopedia.pub/entry/17444. Accessed December 11, 2023.
Jansen, Christine A.. "Innate Immune Cells in the Chicken Intestine" Encyclopedia, https://encyclopedia.pub/entry/17444 (accessed December 11, 2023).
Jansen, C.A.(2021, December 22). Innate Immune Cells in the Chicken Intestine. In Encyclopedia. https://encyclopedia.pub/entry/17444
Jansen, Christine A.. "Innate Immune Cells in the Chicken Intestine." Encyclopedia. Web. 22 December, 2021.
Innate Immune Cells in the Chicken Intestine
Edit
This entry is adapted from the peer-reviewed paper 10.3390/pathogens10111512

The chicken intestinal epithelium is a monolayer consisting of various cell types. Intercellular junctional complexes, tight junctions, present between the intestinal epithelial cells maintain the gut barrier integrity. Tight junctions hold the intestinal epithelial cells together to prevent the entry of enteric pathogens and thus maintain gut homeostasis. In addition to the gut microbiota, also intestinal epithelial cells inhibit the entry of pathogens for example by producing a mucus layer. In addtion to this physical barreier, also soluble factors suc a antimicrobial compunds play a role in the defence against pathogens. When all these defense mechanism are not sufficient in protecting the host, the cells of the intestinal innate immune system are activated. Properties and function of these cells are the subject of this entry.

innate immune cells intestine

1. Natural Killer (NK) Cells of the Intestinal Immune System

NK cells are involved in the innate defense, they are scavenger cells and their primary function is to recognize the virally infected, transformed, and neoplastic host cells and kill them [1][2]. NK cells originate in the bone marrow and migrate towards blood and organs like the spleen, lungs, and intestine [3]. In the chicken intestine NK cells are embedded between the enterocytes as intraepithelial lymphocytes along the length of the gut. In intestinal intraepithelial lymphocytes NK cells comprise even higher numbers than CD8+ T cells and γδ T cells [4][5] suggesting an important role in the intestinal innate immune system [6].
Chicken NK cells are described as a population of cells that lack surface expression of CD3 or Ig [5] that is able to kill the NK susceptible cell line (LSCC-RP9) [4]. Based on these characteristics, many studies have reported the presence of NK cells in various tissues like spleen, lungs and intestine of chickens [7][8][9][10][11]. NK cells are also present in large numbers in the embryonic spleen and duodenum of chickens [4][8][11][12] indicating that they are indeed important in early life innate defense.
The induction of NK cell activation is mediated by an array of activating and inhibitory receptors which are present on their surface [13]. Also, in the chicken genome NK cell receptors have been reported to be present. The leucocyte receptor complex on chromosome 31 encodes for chicken Ig-like receptors (CHIR) [14]. Chromosome 1 harbors the NK gene complex which encodes NKG2/CD94 and syntenic to the mammalian NK complex region [14][15][16].
Upon crosslinking, activation receptors on NK cells signal via immunoreceptor tyrosine-based activation motifs (ITAMs) which initiates downstream signaling, while inhibitory receptors signal via immunoreceptor tyrosine-based inhibitory motifs (ITIMs). The delicate balance between activating and inhibitory signals received by NK cell receptors activates NK cells [17][18][19].
Once activated, NK cells release lytic granules that contain perforin and granzyme to lyse target cells [20][21]. The degranulation of NK cells upon activation can be detected using the CD107 assay [8], since enhanced surface expression of CD107a, the lysosomal-associated membrane protein-1 (LAMP-1), is associated with NK cell activation [7]. In chickens, enhanced CD107 surface expression was reported on CD3 negative cells that express surface markers such as 28-4, 20E5, CD11b/c, and 7C1 suggesting that these are markers of cells with NK cell function.
NK cells that express 28-4 (the chicken IL-2Ra orthologue) are mostly present in the duodenum of layer chickens and have been shown to able to kill susceptible target cells (LSCC-RP9) [4][22]. In other organs such as spleen, blood, and lung of layer chickens NK cells expressing 28-4 are less dominant, here the major populations express 5C7 and 20E5 [4][8][22][23].
In the intestine, the majority of NK cells express 28-4, while lower expression of NK cell markers 20E5 and 5C7 was observed. The number of 28-4 expressing NK cells was higher at day 1 post-hatch compared to levels at embryonic day 14 and 18, and remained stable throughout the life. Conversely, the number of 20E5+ and 5C7+ cells was lower in 1 day-old chickens compared to embryonic day 14 and 18 and increased until day 21 post-hatch. Among intestinal NK cells, surface expression of CD107 was also higher in the 28-4+ subset as compared to intestinal 20E5+ cells suggesting that this population may play a role in the intestinal innate immune response [11].
Upon activation NK cells may also secrete the cytokine interferon-γ, which recruits and activates immune cells from peripheral blood and nearby lymphoid tissues to amplify the innate immune response against bacteria and/or viruses and to initiate adaptive immune response [24][25].

2. Heterophils of the Intestinal Immune System

Heterophils are the avian analogues of mammalian neutrophils and immediately appear at the site of infection to eliminate invasive pathogens [26][27]. Heterophils use multiple strategies such as phagocytosis, degranulation, and oxidative burst to kill the pathogens. In chickens, heterophils are the predominant granulocytes in circulating blood and the gut [28][29][30][31][32][33]. Heterophils are comparatively higher in number in young chickens as compared to the older ones [34]. However, in young birds heterophils are functionally less active as indicated by decreased phagocytosis, degranulation, oxidative burst and, subsequently, killing of bacteria.
In the chicken intestine, pro-inflammatory cytokines produced as a result of microorganism invasion attract heterophils to the site of infection [35]. Upon contact with pathogens, heterophils are activated through the interaction of TLRs with bacterial ligands such as LPS, peptidoglycan, flagellin, and lipoteichoic acid [36][37]. This activation of heterophils results in a sequence of events including phagocytosis, oxidative burst, degranulation, and cytokine (IL1β, IL6) and chemokine (CXCLi2) production through the NF-κB pathway [36][38]. Heterophils also become activated via avian triggering receptor expressed on myeloid cells-1 (TREM-A1), which modulates TLR signaling and causes phagocytosis [39].
Phagocytosis is the process by which heterophils internalize the pathogens. Following internalization, microorganisms are entrapped in a vacuole called the phagosome, which then immediately fuses with cytoplasmic granules leading to killing of entrapped pathogens by release of anti-microbicidal peptides and proteolytic enzymes from intracellular granules [40].
Degranulation is another host defense strategy used by heterophils to kill pathogens. Upon microbial agonist stimulation, heterophils release their cytoplasmic granules at the site of infection into the external environment to kill pathogens. Another important event closely linked with extracellular degranulation is the production of heterophil extracellular traps (HET) to trap pathogens. The HET is similar to the neutrophil extracellular trap [41]. This process allows heterophils to entrap and kill bacteria extracellularly. The HET mechanism is initiated by the formation of thin extracellular fibers (5–17 nm) between pathogens and heterophils [42]. This meshwork of fibers acts as a death trap and prevent the dissemination of pathogens in the tissues. Moreover, HET also destroy pathogens by highly concentrated microbicidal substances. Finally, phagocytes also use oxidative burst to produce reactive oxygen species for microbial killing. However, unlike neutrophils, avian heterophils are mostly dependent on non-oxidative killing of pathogens as they don’t generate strong oxidative burst as compared to their mammalian analogues [43][44].

3. Dendritic Cells (DCs) of the Intestinal Immune System

DCs act as an immunological bridge between innate and adaptive immunity since these cells are the key player of antigen presentation. The intestinal DCs take up and process antigens, and present these to adaptive immune cells, which initiates a pathogen-specific immune response [45]. In mice DCs are present underneath the intestinal epithelium together with macrophages [46]. Monocytes, macrophage progenitors, and DCs express colony stimulating factor 1 receptor [47]. The intestinal DCs in human and mice can be differentiated from intestinal monocyte-derived macrophages using CD64 expression [48].
Avian DCs are less well characterized compared to human and mice DCs in which the ontogeny and heterogenous nature is extensively explored [49][50][51]. Avian DCs are defined by the expression of several markers such as CD83, CD11c, DEC205, and MHC II [52][53][54][55]. In chickens, DCs expressing CD83 and DEC205 markers are particularly abundant in the spleen, cecal tonsils, thymus, and bursa of fabricius [54]. In the chicken intestine, DCs have been described in the clusters of the GALT. Follicular DCs are located in the germinal center of the cecal tonsil, and pyloric tonsils [56][57][58]. Follicular and interdigitating DCs have also been described in the PP [59].
Immature avian DCs are equipped with a variety of TLRs to recognize invading pathogen [60]. DCs also express the CCR6 chemokine receptor. Binding of of CCR6 to this receptor induces infiltration of the DCs at the infection site to encounter antigens, due to which immature DCs transform into the mature phenotype that presents antigens to T cells. Stimulation of chicken bone marrow derived DCs with LPS results into maturation of chicken DCs, which parallels increased expression of co-stimulatory molecules CD40, CD83, CD86, and a decrease in phagocytic activity [53][61]. DCs interact with LPS of the Gram-negative bacteria through TLR4, which activates CD14 dependent endocytosis of TLR4 [62]. In addition to antigen presentation, DCs also produce cytokines such as IL1β, IL6, 1L10, IL12p35, and TNFα, and CXCL chemokines to attract other immune cells and to enhance inflammatory processes [63][64].

4. Macrophages of the Intestinal Immune System

Macrophages are a type of innate immune cells, which can be involved in the defense against bacterial infections [65]. Macrophages actively recognize, phagocytize, and kill microbes by producing microbicidal substances like nitric oxide, reactive oxygen species, proteolytic enzymes, and lysozyme [66][67][68][69][70]. Upon contact with a pathogen, macrophages become activated and transform into either M1 or M2 phenotype [71][72][73]. The polarization of the macrophages into M1 or M2 phenotypes depends upon the activation pathway and the type of cytokines they are exposed to. Exposure of macrophages to intracellular bacteria and T helper cell type 1 (Th1) cytokines (interferon and TNFα) leads to M1 polarization [74], while T helper cell type 2 (Th2) cytokines (IL4, and 13) transform macrophages into the M2 phenotype [75][76][77].
Whether this polarization also occurs in chicken macrophages is currently not clear. It has been shown, in vitro, that cultured avian macrophages can have a more M1 like phenotype as described by Peng et al. [78] for monocyte-derived macrophages, while an IL4 induced polarization towards a more M2 phenotype has also been described [79]. However, evidence for the presence of M1 and M2 macrophages in vivo is still missing.
Chicken macrophages recognize pathogens by their phagocytic receptors [80], that may be opsonic (complement receptors, Fc receptors) or non-opsonic (TLRs, mannose receptors) [81][82][83][84]. Chicken intestinal macrophages possess a range of TLRs, and hence respond accordingly to a variety of bacterial ligands such as LPS, CpG oligonucleotides, and flagellin [85][86][87][88].
Upon pathogen recognition, macrophages activate intracellular signals (mitogen activated protein kinase p38) orchestrate the innate immune response by production of cytokines (TNFα, IL1, IL10), chemokines, and nitric oxide (NO) which has antibacterial properties [89][90][91][92][93][94][95][96]. In a recent study it has been shown that HD11 cells, a macrophage-like cell line, when stimulated with inactivated poultry vaccines, showed an increase in Fc-receptor driven phagocytosis as well as NO production when activated with TLR agonists [97]. In another study, HD11 cells stimulated with inactivated Avibacterium paragallinarium, led to NO production and express pro-inflammatory cytokines TNFα, IL1β, and IL12p40, as well as chemokines CXCLi1 and CXCLi2 [98].
In the chicken intestine, macrophages play a vital role in antigen presentation along with DCs, as well as act as regulators and effectors of immunity. Macrophages are present in the intestinal lamina propria in chickens and reach the invasion site after IFNγ production [99]. It has been shown that IFNγ stimulation increases the antiviral and phagocytic activity of macrophages and also induces IL12 and IL18 production which drives Th1 adaptive response [100][101].

5. γδ T Cells of the Intestinal Immune System

γδ T cells are unconventional CD3+ T cells having a unique T cell receptor (TCR) that consists of a γ chain and a δ chain. The number of γδ T cells in blood varies between 0.5 to 10% in humans, dogs, mice and monkeys [102][103], while in chickens, cattle and pigs γδ T cells ranges from 20–50% of the total circulating T cells in blood [104][105][106][107]. Apart from blood, γδ T cells have also been reported in, for example, the intestine and spleen and their frequency depends on age, sex, and strain of chickens [108][109].
The majority of the avian γδ T cells is activated in a MHC unrestricted way unlike αβ T cells [110]. Although toll-like receptors (TLR3 and 4) are present on chicken γδ T cells along with the scavenger receptor superfamily, their role in TCR independent activation of γδ T cells in chickens is still unclear [109][111]. Recently, Karunakaran et al. showed the TCR dependent activation of human γδ T cells. After stimulating γδ T cells with phospho-antigens, molecules present inside the infected cells, γδ T cells get activated to kill the target cell [112]. Activated γδ T cells also produce IL17 and IFNγ cytokines to attract other innate immune cells [113].
The primary function of γδ T cells is to recognize stressed, transformed, and tumor cells, and their killing by perforins and granzymes [114][115]. The mode of action of γδ T cells in chickens is still unclear, but a recent study demonstrated that γδ T cells show killing of LSCC-RP9 cells [109].
γδ T cells are abundantly present in the chicken intestine. It has been shown that the percentage of γδ T cells among IEL population in the ileum of the chicken intestine remained the same during late embryonic days and early post-hatch days but started to increase from day 14 to day 21 post-hatch. As compared to other T cell subsets in the chicken intestine such as CD8αα and CD8αβ T cells, the presence of γδ T cells is lower in chickens younger than 7 days of age, but from day 14 onwards their number becomes similar to CD8αα and CD8αβ T cells [11].

References

  1. Morvan, M.G.; Lanier, L.L. NK cells and cancer: You can teach innate cells new tricks. Nat. Rev. Cancer 2016, 16, 7–19.
  2. Lodoen, M.B.; Lanier, L.L. Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 2006, 18, 391–398.
  3. Bonanni, V.; Sciumè, G.; Santoni, A.; Bernardini, G. Bone marrow NK cells: Origin, distinctive features, and requirements for tissue localization. Front. Immunol. 2019, 10, 1569.
  4. Göbel, T.W.; Kaspers, B.; Stangassinger, M. NK and T cells constitute two major, functionally distinct intestinal epithelial lymphocyte subsets in the chicken. Int. Immunol. 2001, 13, 757–762.
  5. Göbel, T.W.; Chen, C.L.H.; Shrimpf, J.; Grossi, C.E.; Bernot, A.; Bucy, R.P.; Auffray, C.; Cooper, M.D. Characterization of avian natural killer cells and their intracellular CD3 protein complex. Eur. J. Immunol. 1994, 24, 1685–1691.
  6. Chai, J.; Lillehoj, H. Isolation and functional characterization of chicken intestinal intra-epithelial lymphocytes showing natural killer cell activity against tumour target cells. Immunology 1988, 63, 111.
  7. Alter, G.; Malenfant, J.M.; Altfeld, M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 2004, 294, 15–22.
  8. Jansen, C.A.; van de Haar, P.M.; van Haarlem, D.; van Kooten, P.; de Wit, S.; van Eden, W.; Viertlböck, B.C.; Göbel, T.W.; Vervelde, L. Identification of new populations of chicken natural killer (NK) cells. Dev. Comp. Immunol. 2010, 34, 759–767.
  9. Jansen, C.A.; De Geus, E.D.; Van Haarlem, D.A.; Van De Haar, P.M.; Löndt, B.Z.; Graham, S.P.; Göbel, T.W.; Van Eden, W.; Brookes, S.M.; Vervelde, L. Differential lung NK cell responses in avian influenza virus infected chickens correlate with pathogenicity. Sci. Rep. 2013, 3, 2478.
  10. Vervelde, L.; Matthijs, M.; Van Haarlem, D.; de Wit, J.; Jansen, C. Rapid NK-cell activation in chicken after infection with infectious bronchitis virus M41. Vet. Immunol. Immunopathol. 2013, 151, 337–341.
  11. Meijerink, N.; van Haarlem, D.A.; Velkers, F.C.; Stegeman, A.J.; Rutten, V.P.; Jansen, C.A. Analysis of chicken intestinal natural killer cells, a major IEL subset during embryonic and early life. Dev. Comp. Immunol. 2021, 114, 103857.
  12. Zhang, L.; Katselis, G.S.; Moore, R.E.; Lekpor, K.; Goto, R.M.; Hunt, H.D.; Lee, T.D.; Miller, M.M. MHC class I target recognition, immunophenotypes and proteomic profiles of natural killer cells within the spleens of day-14 chick embryos. Dev. Comp. Immunol. 2012, 37, 446–456.
  13. Sivori, S.; Vacca, P.; Del Zotto, G.; Munari, E.; Mingari, M.C.; Moretta, L. Human NK cells: Surface receptors, inhibitory checkpoints, and translational applications. Cell. Mol. Immunol. 2019, 16, 430–441.
  14. Viertlboeck, B.C.; Habermann, F.A.; Schmitt, R.; Groenen, M.A.; Du Pasquier, L.; Göbel, T.W. The chicken leukocyte receptor complex: A highly diverse multigene family encoding at least six structurally distinct receptor types. J. Immunol. 2005, 175, 385–393.
  15. Chiang, H.-I.; Zhou, H.; Raudsepp, T.; Jesudhasan, P.R.; Zhu, J.J. Chicken CD69 and CD94/NKG2-like genes in a chromosomal region syntenic to mammalian natural killer gene complex. Immunogenetics 2007, 59, 603–611.
  16. Viertlboeck, B.C.; Göbel, T.W. The chicken leukocyte receptor cluster. Vet. Immunol. Immunopathol. 2011, 144, 1–10.
  17. Biassoni, R. Natural killer cell receptors. In Multichain Immune Recognition Receptor Signaling; Springer: New York, NY, USA, 2008; pp. 35–52.
  18. Luci, C.; Reynders, A.; Ivanov, I.I.; Cognet, C.; Chiche, L.; Chasson, L.; Hardwigsen, J.; Anguiano, E.; Banchereau, J.; Chaussabel, D. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 2009, 10, 75–82.
  19. Mayassi, T.; Jabri, B. Human intraepithelial lymphocytes. Mucosal Immunol. 2018, 11, 1281–1289.
  20. Orange, J.S. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 2008, 8, 713–725.
  21. Solana, R.; Tarazona, R.; Gayoso, I.; Lesur, O.; Dupuis, G.; Fulop, T. Innate immunosenescence: Effect of aging on cells and receptors of the innate immune system in humans. In Seminars in Immunology; Academic Press: Cambridge, MA, USA, 2012; Volume 24, pp. 331–341.
  22. Jahromi, M.Z.; Bello, M.B.; Abdolmaleki, M.; Yeap, S.K.; Hair-Bejo, M.; Omar, A.R. Differential activation of intraepithelial lymphocyte-natural killer cells in chickens infected with very virulent and vaccine strains of infectious bursal disease virus. Dev. Comp. Immunol. 2018, 87, 116–123.
  23. Deeg, C.A.; Degroote, R.L.; Giese, I.M.; Hirmer, S.; Amann, B.; Weigand, M.; Wiedemann, C.; Hauck, S.M. CD11d is a novel antigen on chicken leukocytes. J. Proteom. 2020, 225, 103876.
  24. Bertzbach, L.D.; van Haarlem, D.A.; Härtle, S.; Kaufer, B.B.; Jansen, C.A. Marek’s disease virus infection of natural killer cells. Microorganisms 2019, 7, 588.
  25. Poggi, A.; Benelli, R.; Venè, R.; Costa, D.; Ferrari, N.; Tosetti, F.; Zocchi, M.R. Human gut-associated natural killer cells in health and disease. Front. Immunol. 2019, 10, 961.
  26. Wolfe, S.A.; Tracey, D.E.; Henney, C.S. Induction of “natural killer” cells by BCG. Nature 1976, 262, 584–586.
  27. Baron, E.J.; Proctor, R.A. Inefficient in vitro killing of virulent or nonvirulent Salmonella typhimurium by murine polymorphonuclear neutrophils. Can. J. Microbiol. 1984, 30, 1264–1270.
  28. Maxwell, M.; Robertson, G. The avian heterophil leucocyte: A review. World’s Poult. Sci. J. 1998, 54, 155–178.
  29. Kogut, M.; McGruder, E.; Hargis, B.; Corrier, D.; DeLoach, J. Dynamics of avian inflammatory response to Salmonella-immune lymphokines. Inflammation 1994, 18, 373–388.
  30. Kogut, M.H.; McGruder, E.D.; Hargis, B.M.; Corner, D.E.; DeLoach, J.R. In vivo activation of heterophil function in chickens following injection with Salmonella enteritidis-immune lymphokines. J. Leukoc. Biol. 1995, 57, 56–62.
  31. Kogut, M.H.; Mcgruder, E.D.; Hargis, B.M.; Corrier, D.E.; Deloach, J.R. Characterization of the pattern of inflammatory cell influx in chicks following the intraperitoneal administration of live Salmonella enteritidis and Salmonella enteritidis-immune lymphokines. Poult. Sci. 1995, 74, 8–17.
  32. Kogut, M.; Holtzapple, C.; Lowry, V.; Genovese, K.; Stanker, L. Functional responses of neonatal chicken and turkey heterophils following stimulation by inflammatory agonists. Am. J. Vet. Res. 1998, 59, 1404–1408.
  33. Stabler, J.; McCormick, T.; Powell, K.; Kogut, M. Avian heterophils and monocytes: Phagocytic and bactericidal activities against Salmonella enteritidis. Vet. Microbiol. 1994, 38, 293–305.
  34. Bar-Shira, E.; Friedman, A. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev. Comp. Immunol. 2006, 30, 930–941.
  35. Matulova, M.; Varmuzova, K.; Sisak, F.; Havlickova, H.; Babak, V.; Stejskal, K.; Zdrahal, Z.; Rychlik, I. Chicken innate immune response to oral infection with Salmonella enterica serovar Enteritidis. Vet. Res. 2013, 44, 1–11.
  36. Kogut, M.H.; Iqbal, M.; He, H.; Philbin, V.; Kaiser, P.; Smith, A. Expression and function of Toll-like receptors in chicken heterophils. Dev. Comp. Immunol. 2005, 29, 791–807.
  37. Kogut, M.H.; Rothwell, L.; Kaiser, P. IFN-γ priming of chicken heterophils upregulates the expression of proinflammatory and Th1 cytokine mRNA following receptor-mediated phagocytosis of Salmonella enterica serovar enteritidis. J. Interferon Cytokine Res. 2005, 25, 73–81.
  38. Kogut, M.H.; Swaggerty, C.; He, H.; Pevzner, I.; Kaiser, P. Toll-like receptor agonists stimulate differential functional activation and cytokine and chemokine gene expression in heterophils isolated from chickens with differential innate responses. Microbes Infect. 2006, 8, 1866–1874.
  39. Radsak, M.P.; Salih, H.R.; Rammensee, H.-G.; Schild, H. Triggering receptor expressed on myeloid cells-1 in neutrophil inflammatory responses: Differential regulation of activation and survival. J. Immunol. 2004, 172, 4956–4963.
  40. Genovese, K.J.; He, H.; Swaggerty, C.L.; Kogut, M.H. The avian heterophil. Dev. Comp. Immunol. 2013, 41, 334–340.
  41. Chuammitri, P.; Ostojić, J.; Andreasen, C.B.; Redmond, S.B.; Lamont, S.J.; Palić, D. Chicken heterophil extracellular traps (HETs): Novel defense mechanism of chicken heterophils. Vet. Immunol. Immunopathol. 2009, 129, 126–131.
  42. Guimaraes-Costa, A.B.; Nascimento, M.T.; Wardini, A.B.; Pinto-da-Silva, L.H.; Saraiva, E.M. ETosis: A microbicidal mechanism beyond cell death. J. Parasitol. Res. 2012, 2012.
  43. Wells, L.L.; Lowry, V.K.; Deloach, J.R.; Kogut, M.H. Age-dependent phagocytosis and bactericidal activities of the chicken heterophil. Dev. Comp. Immunol. 1998, 22, 103–109.
  44. Daimon, T.; Caxton-Martins, A. Electron microscopic and enzyme cytochemical studies on granules of mature chicken granular leucocytes. J. Anat. 1977, 123, 553.
  45. Banchereau, J.; Steinman, R.M. Dendritic cells and the control of immunity. Nature 1998, 392, 245–252.
  46. Farache, J.; Zigmond, E.; Shakhar, G.; Jung, S. Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol. Cell Biol. 2013, 91, 232–239.
  47. Garceau, V.; Smith, J.; Paton, I.R.; Davey, M.; Fares, M.A.; Sester, D.P.; Burt, D.W.; Hume, D.A. Pivotal Advance: Avian colony-stimulating factor 1 (CSF-1), interleukin-34 (IL-34), and CSF-1 receptor genes and gene products. J. Leukoc. Biol. 2010, 87, 753–764.
  48. Tamoutounour, S.; Henri, S.; Lelouard, H.; de Bovis, B.; de Haar, C.; van der Woude, C.J.; Woltman, A.M.; Reyal, Y.; Bonnet, D.; Sichien, D. CD 64 distinguishes macrophages from dendritic cells in the gut and reveals the T h1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 2012, 42, 3150–3166.
  49. Solano-Gálvez, S.G.; Tovar-Torres, S.M.; Tron-Gómez, M.S.; Weiser-Smeke, A.E.; Álvarez-Hernández, D.A.; Franyuti-Kelly, G.A.; Tapia-Moreno, M.; Ibarra, A.; Gutiérrez-Kobeh, L.; Vázquez-López, R. Human dendritic cells: Ontogeny and their subsets in health and disease. Med Sci. 2018, 6, 88.
  50. Merad, M.; Sathe, P.; Helft, J.; Miller, J.; Mortha, A. The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 2013, 31, 563–604.
  51. Nagy, N.; Bódi, I.; Oláh, I. Avian dendritic cells: Phenotype and ontogeny in lymphoid organs. Dev. Comp. Immunol. 2016, 58, 47–59.
  52. Hansell, C.; Zhu, X.W.; Brooks, H.; Sheppard, M.; Withanage, S.; Maskell, D.; McConnell, I. Unique features and distribution of the chicken CD83+ cell. J. Immunol. 2007, 179, 5117–5125.
  53. Wu, Z.; Rothwell, L.; Young, J.R.; Kaufman, J.; Butter, C.; Kaiser, P. Generation and characterization of chicken bone marrow-derived dendritic cells. Immunology 2010, 129, 133–145.
  54. Staines, K.; Young, J.R.; Butter, C. Expression of chicken DEC205 reflects the unique structure and function of the avian immune system. PLoS ONE 2013, 8, e51799.
  55. Manh, T.-P.V.; Marty, H.; Sibille, P.; Le Vern, Y.; Kaspers, B.; Dalod, M.; Schwartz-Cornil, I.; Quéré, P. Existence of conventional dendritic cells in Gallus gallus revealed by comparative gene expression profiling. J. Immunol. 2014, 192, 4510–4517.
  56. Jeurissen, S.; Janse, E.; Lehrbach, P.; Haddad, E.; Avakian, A.; Whitfill, C. The working mechanism of an immune complex vaccine that protects chickens against infectious bursal disease. Immunology 1998, 95, 494.
  57. Olah, I.; Glick, B. Structure of the germinal centers in the chicken caecal tonsil: Light and electron microscopic and autoradiographic studies. Poult. Sci. 1979, 58, 195–210.
  58. Nagy, N.; Oláh, I. Pyloric tonsil as a novel gut-associated lymphoepithelial organ of the chicken. J. Anat. 2007, 211, 407–411.
  59. Gallego, M.; Del Cacho, E.; Bascuas, J. Antigen-binding cells in the cecal tonsil and Peyer’s patches of the chicken after bovine serum albumin administration. Poult. Sci. 1995, 74, 472–479.
  60. Abasht, B.; Kaiser, M.; Lamont, S. Toll-like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enterica serovar Enteritidis. Vet. Immunol. Immunopathol. 2008, 123, 314–323.
  61. Van den Biggelaar, R.H.; Arkesteijn, G.J.; Rutten, V.P.; van Eden, W.; Jansen, C.A. In vitro chicken bone marrow-derived dendritic cells comprise subsets at different states of maturation. Front. Immunol. 2020, 11, 141.
  62. Zanoni, I.; Ostuni, R.; Marek, L.R.; Barresi, S.; Barbalat, R.; Barton, G.M.; Granucci, F.; Kagan, J.C. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 2011, 147, 868–880.
  63. Yitbarek, A.; Echeverry, H.; Brady, J.; Hernandez-Doria, J.; Camelo-Jaimes, G.; Sharif, S.; Guenter, W.; House, J.; Rodriguez-Lecompte, J. Innate immune response to yeast-derived carbohydrates in broiler chickens fed organic diets and challenged with Clostridium perfringens. Poult. Sci. 2012, 91, 1105–1112.
  64. Singh, D.; Singh, M.; Chander, V.; Sharma, G.K.; Mahawar, M.; Teeli, A.S.; Goswami, T.K. Differential responses of chicken monocyte-derived dendritic cells infected with Salmonella Gallinarum and Salmonella Typhimurium. Sci. Rep. 2021, 11, 17214.
  65. Rehman, M.U.; Yoshihisa, Y.; Miyamoto, Y.; Shimizu, T. The anti-inflammatory effects of platinum nanoparticles on the lipopolysaccharide-induced inflammatory response in RAW 264.7 macrophages. Inflamm. Res. 2012, 61, 1177–1185.
  66. Okamura, M.; Lillehoj, H.S.; Raybourne, R.B.; Babu, U.S.; Heckert, R.A.; Tani, H.; Sasai, K.; Baba, E.; Lillehoj, E.P. Differential responses of macrophages to Salmonella enterica serovars Enteritidis and Typhimurium. Vet. Immunol. Immunopathol. 2005, 107, 327–335.
  67. Withanage, G.; Mastroeni, P.; Brooks, H.; Maskell, D.; McConnell, I. Oxidative and nitrosative responses of the chicken macrophage cell line MQ-NCSU to experimental Salmonella infection. Br. Poult. Sci. 2005, 46, 261–267.
  68. Babu, U.S.; Gaines, D.W.; Lillehoj, H.; Raybourne, R.B. Differential reactive oxygen and nitrogen production and clearance of Salmonella serovars by chicken and mouse macrophages. Dev. Comp. Immunol. 2006, 30, 942–953.
  69. He, H.; Genovese, K.J.; Nisbet, D.J.; Kogut, M.H. Profile of Toll-like receptor expressions and induction of nitric oxide synthesis by Toll-like receptor agonists in chicken monocytes. Mol. Immunol. 2006, 43, 783–789.
  70. He, H.; MacKinnon, K.M.; Genovese, K.J.; Kogut, M.H. CpG oligodeoxynucleotide and double-stranded RNA synergize to enhance nitric oxide production and mRNA expression of inducible nitric oxide synthase, pro-inflammatory cytokines and chemokines in chicken monocytes. Innate Immun. 2011, 17, 137–144.
  71. Martinez, F.O.; Gordon, S. The M1 and M2 paradigm of macrophage activation: Time for reassessment. F1000prime Rep. 2014, 6, 6–13.
  72. Novak, M.L.; Koh, T.J. Macrophage phenotypes during tissue repair. J. Leukoc. Biol. 2013, 93, 875–881.
  73. Sica, A.; Mantovani, A. Macrophage plasticity and polarization: In vivo veritas. J. Clin. Investig. 2012, 122, 787–795.
  74. Ma, J.; Chen, T.; Mandelin, J.; Ceponis, A.; Miller, N.; Hukkanen, M.; Ma, G.; Konttinen, Y. Regulation of macrophage activation. Cell. Mol. Life Sci. 2003, 60, 2334–2346.
  75. Gordon, S.; Martinez, F.O. Alternative activation of macrophages: Mechanism and functions. Immunity 2010, 32, 593–604.
  76. Luzina, I.G.; Keegan, A.D.; Heller, N.M.; Rook, G.A.; Shea-Donohue, T.; Atamas, S.P. Regulation of inflammation by interleukin-4: A review of “alternatives”. J. Leukoc. Biol. 2012, 92, 753–764.
  77. Rőszer, T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediat. Inflamm. 2015, 2015.
  78. Peng, L.; van den Biggelaar, R.H.; Jansen, C.A.; Haagsman, H.P.; Veldhuizen, E.J. A method to differentiate chicken monocytes into macrophages with proinflammatory properties. Immunobiology 2020, 225, 152004.
  79. Chaudhari, A.A.; Kim, W.H.; Lillehoj, H.S. Interleukin-4 (IL-4) may regulate alternative activation of macrophage-like cells in chickens: A sequential study using novel and specific neutralizing monoclonal antibodies against chicken IL-4. Vet. Immunol. Immunopathol. 2018, 205, 72–82.
  80. Gordon, S. Pattern recognition receptors: Doubling up for the innate immune response. Cell 2002, 111, 927–930.
  81. Wright, A.E.; Douglas, S.R. An experimental investigation of the role of the blood fluids in connection with phagocytosis. Proc. R. Soc. Lond. 1904, 72, 357–370.
  82. Janeway, C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 1989, 54, 1–13.
  83. Janeway, C.A., Jr.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197–216.
  84. Stuart, L.M.; Ezekowitz, R.A.B. Phagocytosis: Elegant complexity. Immunity 2005, 22, 539–550.
  85. Akira, S.; Yamamoto, M.; Takeda, K. Toll-like receptor family: Receptors essential for microbial recognition and immune responses. Arthritis Res Ther 2003, 5, 1–54.
  86. He, H.; Genovese, K.J.; Nisbet, D.J.; Kogut, M.H. Synergy of CpG oligodeoxynucleotide and double-stranded RNA (poly I: C) on nitric oxide induction in chicken peripheral blood monocytes. Mol. Immunol. 2007, 44, 3234–3242.
  87. Hartley, C.; Salisbury, A.-M.; Wigley, P. CpG oligonucleotides and recombinant interferon-γ in combination improve protection in chickens to Salmonella enterica serovar Enteritidis challenge as an adjuvant component, but have no effect in reducing Salmonella carriage in infected chickens. Avian Pathol. 2012, 41, 77–82.
  88. Zhang, S.; Lillehoj, H.; Kim, C.-H.; Keeler, C., Jr.; Babu, U.; Zhang, M. Transcriptional response of chicken macrophages to Salmonella enterica serovar enteritidis infection. In Animal Genomics for Animal Health; Karger Publishers: Berlin, Germany, 2008; Volume 132, pp. 141–151.
  89. Kim, Y.-J.; Shin, Y.; Lee, K.H.; Kim, T.-J. Anethum graveloens flower extracts inhibited a lipopolysaccharide-induced inflammatory response by blocking iNOS expression and NF-κB activity in macrophages. Biosci. Biotechnol. Biochem. 2012, 76, 1122–1127.
  90. Gao, J.; Scheenstra, M.R.; van Dijk, A.; Veldhuizen, E.J.; Haagsman, H.P. A new and efficient culture method for porcine bone marrow-derived M1-and M2-polarized macrophages. Vet. Immunol. Immunopathol. 2018, 200, 7–15.
  91. Djeraba, A.; Musset, E.; van Rooijen, N.; Quéré, P. Resistance and susceptibility to Marek’s disease: Nitric oxide synthase/arginase activity balance. Vet. Microbiol. 2002, 86, 229–244.
  92. He, H.; Kogut, M.H. CpG-ODN-induced nitric oxide production is mediated through clathrin-dependent endocytosis, endosomal maturation, and activation of PKC, MEK1/2 and p38 MAPK, and NF-κB pathways in avian macrophage cells (HD11). Cell. Signal. 2003, 15, 911–917.
  93. Khatri, M.; Palmquist, J.M.; Cha, R.M.; Sharma, J.M. Infection and activation of bursal macrophages by virulent infectious bursal disease virus. Virus Res. 2005, 113, 44–50.
  94. Lillehoj, H.S.; Li, G. Nitric oxide production by macrophages stimulated with coccidia sporozoites, lipopolysaccharide, or interferon-γ, and its dynamic changes in SC and TK strains of chickens infected with Eimeria tenella. Avian Dis. 2004, 48, 244–253.
  95. Qureshi, M. Avian macrophage and immune response: An overview. Poult. Sci. 2003, 82, 691–698.
  96. Smith, C.K.; Kaiser, P.; Rothwell, L.; Humphrey, T.; Barrow, P.A.; Jones, M.A. Campylobacter jejuni-induced cytokine responses in avian cells. Infect. Immun. 2005, 73, 2094–2100.
  97. Van den Biggelaar, R.H.; Van Eden, W.; Rutten, V.P.; Jansen, C.A. Nitric oxide production and Fc receptor-mediated phagocytosis as functional readouts of macrophage activity upon stimulation with inactivated poultry vaccines in vitro. Vaccines 2020, 8, 332.
  98. Van den Biggelaar, R.H.; van Eden, W.; Rutten, V.P.; Jansen, C.A. Macrophage Activation Assays to Evaluate the Immunostimulatory Capacity of Avibacterium paragallinarum in A Multivalent Poultry Vaccine. Vaccines 2020, 8, 671.
  99. Lillehoj, H.S.; Trout, J.M. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Microbiol. Rev. 1996, 9, 349–360.
  100. Wigley, P.; Hulme, S.; Rothwell, L.; Bumstead, N.; Kaiser, P.; Barrow, P. Macrophages isolated from chickens genetically resistant or susceptible to systemic salmonellosis show magnitudinal and temporal differential expression of cytokines and chemokines following Salmonella enterica challenge. Infect. Immun. 2006, 74, 1425–1430.
  101. He, H.; Genovese, K.J.; Kogut, M.H. Modulation of chicken macrophage effector function by TH1/TH2 cytokines. Cytokine 2011, 53, 363–369.
  102. Malkovsky, M.; Bartz, S.R.; Mackenzie, D.; Radtke, B.E.; Wallace, M.; Manning, J.; Pauza, C.D.; Fisch, P. Are γδ T cells important for the elimination of virus-infected cells? J. Med Primatol. 1992, 21, 113–118.
  103. Hayday, A.C. γδ cells: A right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 2000, 18, 975–1026.
  104. Sowder, J.T.; Chen, C.; Ager, L.L.; Chan, M.M.; Cooper, M. A large subpopulation of avian T cells express a homologue of the mammalian T gamma/delta receptor. J. Exp. Med. 1988, 167, 315–322.
  105. Mackay, C.R.; Hein, W.R. A large proportion of bovine T cells express the γδ T cell receptor and show a distinct tissue distribution and surface phenotype. Int. Immunol. 1989, 1, 540–545.
  106. Yang, H.; Parkhouse, R. Phenotypic classification of porcine lymphocyte subpopulations in blood and lymphoid tissues. Immunology 1996, 89, 76–83.
  107. Kubota, T.; Wang, J.-y.; Göbel, T.W.; Hockett, R.D.; Cooper, M.D.; Chen-lo, H.C. Characterization of an avian (Gallus gallus domesticus) TCR αδ gene locus. J. Immunol. 1999, 163, 3858–3866.
  108. Pieper, J.; Methner, U.; Berndt, A. Heterogeneity of avian γδ T cells. Vet. Immunol. Immunopathol. 2008, 124, 241–252.
  109. Fenzl, L.; Göbel, T.W.; Neulen, M.-L. γδ T cells represent a major spontaneously cytotoxic cell population in the chicken. Dev. Comp. Immunol. 2017, 73, 175–183.
  110. Holderness, J.; Hedges, J.F.; Ramstead, A.; Jutila, M.A. Comparative biology of γδ T cell function in humans, mice, and domestic animals. Annu. Rev. Anim. Biosci. 2013, 1, 99–124.
  111. Baldwin, C.L.; Yirsaw, A.; Gillespie, A.; Le Page, L.; Zhang, F.; Damani-Yokota, P.; Telfer, J.C. γδ T cells in livestock: Responses to pathogens and vaccine potential. Transbound. Emerg. Dis. 2020, 67, 119–128.
  112. Karunakaran, M.M.; Willcox, C.R.; Salim, M.; Paletta, D.; Fichtner, A.S.; Noll, A.; Starick, L.; Nöhren, A.; Begley, C.R.; Berwick, K.A. Butyrophilin-2A1 directly binds germline-encoded regions of the Vγ9Vδ2 TCR and is essential for phosphoantigen sensing. Immunity 2020, 52, 487–498.e486.
  113. Shibata, K.; Yamada, H.; Nakamura, M.; Hatano, S.; Katsuragi, Y.; Kominami, R.; Yoshikai, Y. IFN-γ–Producing and IL-17–Producing γδ T Cells Differentiate at Distinct Developmental Stages in Murine Fetal Thymus. J. Immunol. 2014, 192, 2210–2218.
  114. Price, S.J.; Sopp, P.; Howard, C.J.; Hope, J.C. Workshop cluster 1+ γδ T-cell receptor+ T cells from calves express high levels of interferon-γ in response to stimulation with interleukin-12 and-18. Immunology 2007, 120, 57–65.
  115. Alvarez, A.; Endsley, J.; Werling, D.; Mark Estes, D. WC1+ γδ T Cells Indirectly Regulate Chemokine Production During Mycobacterium bovis Infection in SCID-bo Mice. Transbound. Emerg. Dis. 2009, 56, 275–284.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY)license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Agriculture, Dairy & Animal Science
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Christine A. Jansen
View Times: 335
Revisions: 2 times (View History)
Update Date: 23 Dec 2021
Table of Contents
    1000/1000
    Hot Most Recent
    Feedback