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Published in: BMC Immunology 1/2021

01-12-2021 | Helminths | Research

The role of β2 integrin in dendritic cell migration during infection

Authors: Tarfa Altorki, Werner Muller, Andrew Brass, Sheena Cruickshank

Published in: BMC Immunology | Issue 1/2021

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Abstract

Background

Dendritic cells (DCs) play a key role in shaping T cell responses. To do this, DCs must be able to migrate to the site of the infection and the lymph nodes to prime T cells and initiate the appropriate immune response. Integrins such as β2 integrin play a key role in leukocyte adhesion, migration, and cell activation. However, the role of β2 integrin in DC migration and function in the context of infection-induced inflammation in the gut is not well understood. This study looked at the role of β2 integrin in DC migration and function during infection with the nematode worm Trichuris muris. Itgb2tm1Bay mice lacking functional β2 integrin and WT littermate controls were infected with T. muris and the response to infection and kinetics of the DC response was assessed.

Results

In infection, the lack of functional β2 integrin significantly reduced DC migration to the site of infection but not the lymph nodes. The lack of functional β2 integrin did not negatively impact T cell activation in response to T. muris infection.

Conclusions

This data suggests that β2 integrins are important in DC recruitment to the infection site potentially impacting the initiation of innate immunity but is dispensible for DC migration to lymph nodes and T cell priming in the context of T. muris infection.
Appendix
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Literature
1.
go back to reference Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009;31(3):502–12.PubMedCrossRef Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009;31(3):502–12.PubMedCrossRef
2.
go back to reference Vicente-Manzanares M, Choi CK, Horwitz AR. Integrins in cell migration--the actin connection. J Cell Sci. 2009;122(Pt 2):199–206.PubMedCrossRef Vicente-Manzanares M, Choi CK, Horwitz AR. Integrins in cell migration--the actin connection. J Cell Sci. 2009;122(Pt 2):199–206.PubMedCrossRef
3.
go back to reference Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, et al. Integrins in immunity. J Cell Sci. 2009;122(Pt 2):215–25.PubMedCrossRef Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, et al. Integrins in immunity. J Cell Sci. 2009;122(Pt 2):215–25.PubMedCrossRef
6.
go back to reference Solovjov DA, Pluskota E, Plow EF. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem. 2005;280(2):1336–45.PubMedCrossRef Solovjov DA, Pluskota E, Plow EF. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem. 2005;280(2):1336–45.PubMedCrossRef
8.
go back to reference Morrison VL, James MJ, Grzes K, Cook P, Glass DG, Savinko T, et al. Loss of beta2-integrin-mediated cytoskeletal linkage reprogrammes dendritic cells to a mature migratory phenotype. Nat Commun. 2014;5:5359.PubMedCrossRef Morrison VL, James MJ, Grzes K, Cook P, Glass DG, Savinko T, et al. Loss of beta2-integrin-mediated cytoskeletal linkage reprogrammes dendritic cells to a mature migratory phenotype. Nat Commun. 2014;5:5359.PubMedCrossRef
9.
go back to reference von Andrian UH, Chambers JD, McEvoy LM, Bargatze RF, Arfors KE, Butcher EC. Two-step model of leukocyte-endothelial cell interaction in inflammation: distinct roles for LECAM-1 and the leukocyte beta 2 integrins in vivo. Proc Natl Acad Sci U S A. 1991;88(17):7538–42.CrossRef von Andrian UH, Chambers JD, McEvoy LM, Bargatze RF, Arfors KE, Butcher EC. Two-step model of leukocyte-endothelial cell interaction in inflammation: distinct roles for LECAM-1 and the leukocyte beta 2 integrins in vivo. Proc Natl Acad Sci U S A. 1991;88(17):7538–42.CrossRef
10.
11.
go back to reference Yakubenko VP, Belevych N, Mishchuk D, Schurin A, Lam SC, Ugarova TP. The role of integrin alpha D beta2 (CD11d/CD18) in monocyte/macrophage migration. Exp Cell Res. 2008;314(14):2569–78.PubMedPubMedCentralCrossRef Yakubenko VP, Belevych N, Mishchuk D, Schurin A, Lam SC, Ugarova TP. The role of integrin alpha D beta2 (CD11d/CD18) in monocyte/macrophage migration. Exp Cell Res. 2008;314(14):2569–78.PubMedPubMedCentralCrossRef
12.
go back to reference Hogg N, Stewart MP, Scarth SL, Newton R, Shaw JM, Law SK, et al. A novel leukocyte adhesion deficiency caused by expressed but nonfunctional beta2 integrins mac-1 and LFA-1. J Clin Invest. 1999;103(1):97–106.PubMedPubMedCentralCrossRef Hogg N, Stewart MP, Scarth SL, Newton R, Shaw JM, Law SK, et al. A novel leukocyte adhesion deficiency caused by expressed but nonfunctional beta2 integrins mac-1 and LFA-1. J Clin Invest. 1999;103(1):97–106.PubMedPubMedCentralCrossRef
13.
go back to reference Marski M, Kandula S, Turner JR, Abraham C. CD18 is required for optimal development and function of CD4(+) CD25(+) T regulatory cells. J Immunol. 2005;175(12):7889–97.PubMedCrossRef Marski M, Kandula S, Turner JR, Abraham C. CD18 is required for optimal development and function of CD4(+) CD25(+) T regulatory cells. J Immunol. 2005;175(12):7889–97.PubMedCrossRef
14.
go back to reference Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 2008;453(7191):51–5.PubMedCrossRef Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 2008;453(7191):51–5.PubMedCrossRef
15.
go back to reference Jang MH, Sougawa N, Tanaka T, Hirata T, Hiroi T, Tohya K, et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol. 2006;176(2):803–10.PubMedCrossRef Jang MH, Sougawa N, Tanaka T, Hirata T, Hiroi T, Tohya K, et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol. 2006;176(2):803–10.PubMedCrossRef
16.
go back to reference Cruickshank SM, Deschoolmeester ML, Svensson M, Howell G, Bazakou A, Logunova L, et al. Rapid dendritic cell mobilization to the large intestinal epithelium is associated with resistance to Trichuris muris infection. J Immunol (Baltimore, Md : 1950). 2009;182(5):3055–62.CrossRef Cruickshank SM, Deschoolmeester ML, Svensson M, Howell G, Bazakou A, Logunova L, et al. Rapid dendritic cell mobilization to the large intestinal epithelium is associated with resistance to Trichuris muris infection. J Immunol (Baltimore, Md : 1950). 2009;182(5):3055–62.CrossRef
17.
go back to reference Bowcutt R, Bramhall M, Logunova L, Wilson J, Booth C, Carding SR, et al. A role for the pattern recognition receptor Nod2 in promoting recruitment of CD103+ dendritic cells to the colon in response to Trichuris muris infection. Mucosal Immunol. 2014;7(5):1094–105.PubMedPubMedCentralCrossRef Bowcutt R, Bramhall M, Logunova L, Wilson J, Booth C, Carding SR, et al. A role for the pattern recognition receptor Nod2 in promoting recruitment of CD103+ dendritic cells to the colon in response to Trichuris muris infection. Mucosal Immunol. 2014;7(5):1094–105.PubMedPubMedCentralCrossRef
18.
go back to reference Huang SW, Walker C, Pennock J, Else K, Muller W, Daniels MJ, et al. P2X7 receptor-dependent tuning of gut epithelial responses to infection. Immunol Cell Biol. 2017;95(2):178–88.PubMedCrossRef Huang SW, Walker C, Pennock J, Else K, Muller W, Daniels MJ, et al. P2X7 receptor-dependent tuning of gut epithelial responses to infection. Immunol Cell Biol. 2017;95(2):178–88.PubMedCrossRef
19.
go back to reference Gawden-Bone C, West MA, Morrison VL, Edgar AJ, McMillan SJ, Dill BD, et al. A crucial role for beta2 integrins in podosome formation, dynamics and toll-like-receptor-signaled disassembly in dendritic cells. J Cell Sci. 2014;127(Pt 19):4213–24.PubMedPubMedCentralCrossRef Gawden-Bone C, West MA, Morrison VL, Edgar AJ, McMillan SJ, Dill BD, et al. A crucial role for beta2 integrins in podosome formation, dynamics and toll-like-receptor-signaled disassembly in dendritic cells. J Cell Sci. 2014;127(Pt 19):4213–24.PubMedPubMedCentralCrossRef
20.
go back to reference Bancroft AJ, Else KJ, Grencis RK. Low-level infection with Trichuris-Muris significantly affects the polarization of the Cd4 response. Eur J Immunol. 1994;24(12):3113–8.PubMedCrossRef Bancroft AJ, Else KJ, Grencis RK. Low-level infection with Trichuris-Muris significantly affects the polarization of the Cd4 response. Eur J Immunol. 1994;24(12):3113–8.PubMedCrossRef
21.
go back to reference Bancroft AJ, Else KJ, Humphreys NE, Grencis RK. The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. Int J Parasitol. 2001;31(14):1627–37.PubMedCrossRef Bancroft AJ, Else KJ, Humphreys NE, Grencis RK. The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. Int J Parasitol. 2001;31(14):1627–37.PubMedCrossRef
22.
go back to reference Bowcutt R, Forman R, Glymenaki M, Carding SR, Else KJ, Cruickshank SM. Heterogeneity across the murine small and large intestine. World J Gastroenterol. 2014;20(41):15216–32.PubMedPubMedCentralCrossRef Bowcutt R, Forman R, Glymenaki M, Carding SR, Else KJ, Cruickshank SM. Heterogeneity across the murine small and large intestine. World J Gastroenterol. 2014;20(41):15216–32.PubMedPubMedCentralCrossRef
23.
24.
go back to reference Hasnain SZ, McGuckin MA, Grencis RK, Thornton DJ. Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier. PLoS Negl Trop Dis. 2012;6(10):e1856.PubMedPubMedCentralCrossRef Hasnain SZ, McGuckin MA, Grencis RK, Thornton DJ. Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier. PLoS Negl Trop Dis. 2012;6(10):e1856.PubMedPubMedCentralCrossRef
25.
go back to reference Hasnain SZ, Thornton DJ, Grencis RK. Changes in the mucosal barrier during acute and chronic Trichuris muris infection. Parasite Immunol. 2011;33(1):45–55.PubMedPubMedCentralCrossRef Hasnain SZ, Thornton DJ, Grencis RK. Changes in the mucosal barrier during acute and chronic Trichuris muris infection. Parasite Immunol. 2011;33(1):45–55.PubMedPubMedCentralCrossRef
26.
go back to reference Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 2004;21(2):279–88.PubMedCrossRef Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 2004;21(2):279–88.PubMedCrossRef
27.
go back to reference Diao J, Winter E, Chen W, Cantin C, Cattral MS. Characterization of distinct conventional and plasmacytoid dendritic cell-committed precursors in murine bone marrow. J Immunol. 2004;173(3):1826–33.PubMedCrossRef Diao J, Winter E, Chen W, Cantin C, Cattral MS. Characterization of distinct conventional and plasmacytoid dendritic cell-committed precursors in murine bone marrow. J Immunol. 2004;173(3):1826–33.PubMedCrossRef
28.
go back to reference Bogunovic M, Ginhoux F, Helft J, Shang LM, Hashimoto D, Greter M, et al. Origin of the Lamina Propria dendritic cell network. Immunity. 2009;31(3):513–25.PubMedPubMedCentralCrossRef Bogunovic M, Ginhoux F, Helft J, Shang LM, Hashimoto D, Greter M, et al. Origin of the Lamina Propria dendritic cell network. Immunity. 2009;31(3):513–25.PubMedPubMedCentralCrossRef
29.
go back to reference Persson EK, Scott CL, Mowat AM, Agace WW. Dendritic cell subsets in the intestinal lamina propria: ontogeny and function. Eur J Immunol. 2013;43(12):3098–107.PubMedPubMedCentralCrossRef Persson EK, Scott CL, Mowat AM, Agace WW. Dendritic cell subsets in the intestinal lamina propria: ontogeny and function. Eur J Immunol. 2013;43(12):3098–107.PubMedPubMedCentralCrossRef
30.
go back to reference Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, et al. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med. 2007;204(1):171–80.PubMedPubMedCentralCrossRef Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, et al. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med. 2007;204(1):171–80.PubMedPubMedCentralCrossRef
32.
go back to reference Souza COS, Espindola MS, Fontanari C, Prado MKB, Frantz FG, Rodrigues V, et al. CD18 regulates monocyte hematopoiesis and promotes resistance to experimental Schistosomiasis. Front Immunol. 2018;9:1970.PubMedPubMedCentralCrossRef Souza COS, Espindola MS, Fontanari C, Prado MKB, Frantz FG, Rodrigues V, et al. CD18 regulates monocyte hematopoiesis and promotes resistance to experimental Schistosomiasis. Front Immunol. 2018;9:1970.PubMedPubMedCentralCrossRef
33.
go back to reference Semmrich M, Plantinga M, Svensson-Frej M, Uronen-Hansson H, Gustafsson T, Mowat AM, et al. Directed antigen targeting in vivo identifies a role for CD103+ dendritic cells in both tolerogenic and immunogenic T-cell responses. Mucosal Immunol. 2012;5(2):150–60.PubMedCrossRef Semmrich M, Plantinga M, Svensson-Frej M, Uronen-Hansson H, Gustafsson T, Mowat AM, et al. Directed antigen targeting in vivo identifies a role for CD103+ dendritic cells in both tolerogenic and immunogenic T-cell responses. Mucosal Immunol. 2012;5(2):150–60.PubMedCrossRef
34.
go back to reference Everts B, Tussiwand R, Dreesen L, Fairfax KC, Huang SC, Smith AM, et al. Migratory CD103+ dendritic cells suppress helminth-driven type 2 immunity through constitutive expression of IL-12. J Exp Med. 2016;213(1):35–51.PubMedPubMedCentralCrossRef Everts B, Tussiwand R, Dreesen L, Fairfax KC, Huang SC, Smith AM, et al. Migratory CD103+ dendritic cells suppress helminth-driven type 2 immunity through constitutive expression of IL-12. J Exp Med. 2016;213(1):35–51.PubMedPubMedCentralCrossRef
35.
go back to reference Cerovic V, Houston SA, Scott CL, Aumeunier A, Yrlid U, Mowat AM, et al. Intestinal CD103(−) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 2013;6(1):104–13.PubMedCrossRef Cerovic V, Houston SA, Scott CL, Aumeunier A, Yrlid U, Mowat AM, et al. Intestinal CD103(−) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 2013;6(1):104–13.PubMedCrossRef
36.
go back to reference Fujimoto K, Karuppuchamy T, Takemura N, Shimohigoshi M, Machida T, Haseda Y, et al. A new subset of CD103(+)CD8 alpha(+) dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol. 2011;186(11):6287–95.PubMedCrossRef Fujimoto K, Karuppuchamy T, Takemura N, Shimohigoshi M, Machida T, Haseda Y, et al. A new subset of CD103(+)CD8 alpha(+) dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol. 2011;186(11):6287–95.PubMedCrossRef
37.
go back to reference Tang H, Cao WP, Kasturi SP, Ravindran R, Nakaya HI, Kundu K, et al. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat Immunol. 2010;11(7):608–U80.PubMedPubMedCentralCrossRef Tang H, Cao WP, Kasturi SP, Ravindran R, Nakaya HI, Kundu K, et al. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat Immunol. 2010;11(7):608–U80.PubMedPubMedCentralCrossRef
38.
go back to reference Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH, Brewer JM, et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic Helminth expulsion. Immunity. 2014;41(2):283–95.PubMedPubMedCentralCrossRef Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH, Brewer JM, et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic Helminth expulsion. Immunity. 2014;41(2):283–95.PubMedPubMedCentralCrossRef
39.
go back to reference Nakanishi K. Basophils as APC in Th2 response in allergic inflammation and parasite infection. Curr Opin Immunol. 2010;22(6):814–20.PubMedCrossRef Nakanishi K. Basophils as APC in Th2 response in allergic inflammation and parasite infection. Curr Opin Immunol. 2010;22(6):814–20.PubMedCrossRef
41.
42.
go back to reference Travis MA, Reizis B, Melton AC, Masteller E, Tang Q, Proctor JM, et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature. 2007;449(7160):361–5.PubMedPubMedCentralCrossRef Travis MA, Reizis B, Melton AC, Masteller E, Tang Q, Proctor JM, et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature. 2007;449(7160):361–5.PubMedPubMedCentralCrossRef
43.
go back to reference Savinko TS, Morrison VL, Uotila LM, Wolff CHJ, Alenius HT, Fagerholm SC. Functional Beta2-Integrins restrict skin inflammation in vivo. J Invest Dermatol. 2015;135(9):2249–57.PubMedCrossRef Savinko TS, Morrison VL, Uotila LM, Wolff CHJ, Alenius HT, Fagerholm SC. Functional Beta2-Integrins restrict skin inflammation in vivo. J Invest Dermatol. 2015;135(9):2249–57.PubMedCrossRef
45.
go back to reference Grabbe S, Varga G, Beissert S, Steinert M, Pendl G, Seeliger S, et al. Beta2 integrins are required for skin homing of primed T cells but not for priming naive T cells. J Clin Invest. 2002;109(2):183–92.PubMedPubMedCentralCrossRef Grabbe S, Varga G, Beissert S, Steinert M, Pendl G, Seeliger S, et al. Beta2 integrins are required for skin homing of primed T cells but not for priming naive T cells. J Clin Invest. 2002;109(2):183–92.PubMedPubMedCentralCrossRef
46.
go back to reference Morrison VL, MacPherson M, Savinko T, Lek HS, Prescott A, Fagerholm SC. The beta2 integrin-kindlin-3 interaction is essential for T-cell homing but dispensable for T-cell activation in vivo. Blood. 2013;122(8):1428–36.PubMedPubMedCentralCrossRef Morrison VL, MacPherson M, Savinko T, Lek HS, Prescott A, Fagerholm SC. The beta2 integrin-kindlin-3 interaction is essential for T-cell homing but dispensable for T-cell activation in vivo. Blood. 2013;122(8):1428–36.PubMedPubMedCentralCrossRef
47.
go back to reference Varga G, Balkow S, Wild MK, Stadtbaeumer A, Krummen M, Rothoeft T, et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood. 2007;109(2):661–9.PubMedCrossRef Varga G, Balkow S, Wild MK, Stadtbaeumer A, Krummen M, Rothoeft T, et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood. 2007;109(2):661–9.PubMedCrossRef
48.
go back to reference Haasken S, Auger JL, Binstadt BA. Absence of beta (2) Integrins impairs regulatory T cells and exacerbates CD4(+) T cell-dependent autoimmune Carditis. J Immunol. 2011;187(5):2702–10.PubMedCrossRef Haasken S, Auger JL, Binstadt BA. Absence of beta (2) Integrins impairs regulatory T cells and exacerbates CD4(+) T cell-dependent autoimmune Carditis. J Immunol. 2011;187(5):2702–10.PubMedCrossRef
49.
go back to reference Ehirchiou D, Xiong Y, Xu GW, Chen WJ, Shi YF, Zhang L. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J Exp Med. 2007;204(7):1519–24.PubMedPubMedCentralCrossRef Ehirchiou D, Xiong Y, Xu GW, Chen WJ, Shi YF, Zhang L. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J Exp Med. 2007;204(7):1519–24.PubMedPubMedCentralCrossRef
50.
go back to reference Moutsopoulos NM, Konkel J, Sarmadi M, Eskan MA, Wild T, Dutzan N, et al. Defective neutrophil recruitment in leukocyte adhesion deficiency type I disease causes local IL-17-driven inflammatory bone loss. Sci Transl Med. 2014;6(229):229ra40.PubMedPubMedCentralCrossRef Moutsopoulos NM, Konkel J, Sarmadi M, Eskan MA, Wild T, Dutzan N, et al. Defective neutrophil recruitment in leukocyte adhesion deficiency type I disease causes local IL-17-driven inflammatory bone loss. Sci Transl Med. 2014;6(229):229ra40.PubMedPubMedCentralCrossRef
51.
go back to reference Cliffe LJ, Grencis RK. The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv Parasitol. 2004;57:255–307.PubMedCrossRef Cliffe LJ, Grencis RK. The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv Parasitol. 2004;57:255–307.PubMedCrossRef
52.
go back to reference Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005;308(5727):1463–5.PubMedCrossRef Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005;308(5727):1463–5.PubMedCrossRef
53.
go back to reference Faulkner H, Renauld JC, Van Snick J, Grencis RK. Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect Immun. 1998;66(8):3832–40.PubMedPubMedCentralCrossRef Faulkner H, Renauld JC, Van Snick J, Grencis RK. Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect Immun. 1998;66(8):3832–40.PubMedPubMedCentralCrossRef
55.
go back to reference McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature. 2012;483(7389):345–9.PubMedPubMedCentralCrossRef McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature. 2012;483(7389):345–9.PubMedPubMedCentralCrossRef
56.
go back to reference Else KJ, Wakelin D, Wassom DL, Hauda KM. The influence of genes mapping within the major histocompatibility complex on resistance to Trichuris muris infections in mice. Parasitology. 1990;101(Pt 1):61–7.PubMedCrossRef Else KJ, Wakelin D, Wassom DL, Hauda KM. The influence of genes mapping within the major histocompatibility complex on resistance to Trichuris muris infections in mice. Parasitology. 1990;101(Pt 1):61–7.PubMedCrossRef
57.
go back to reference Bowcutt R, Bell LV, Little M, Wilson J, Booth C, Murray PJ, et al. Arginase-1-expressing macrophages are dispensable for resistance to infection with the gastrointestinal helminth Trichuris muris. Parasite Immunol. 2011;33(7):411–20.PubMedPubMedCentralCrossRef Bowcutt R, Bell LV, Little M, Wilson J, Booth C, Murray PJ, et al. Arginase-1-expressing macrophages are dispensable for resistance to infection with the gastrointestinal helminth Trichuris muris. Parasite Immunol. 2011;33(7):411–20.PubMedPubMedCentralCrossRef
58.
go back to reference Else KJ, Grencis RK. Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology. 1991;72(4):508–13.PubMedPubMedCentral Else KJ, Grencis RK. Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology. 1991;72(4):508–13.PubMedPubMedCentral
59.
go back to reference Hansson GC, Johansson ME. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes. 2010;1(1):51–4. Hansson GC, Johansson ME. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes. 2010;1(1):51–4.
Metadata
Title
The role of β2 integrin in dendritic cell migration during infection
Authors
Tarfa Altorki
Werner Muller
Andrew Brass
Sheena Cruickshank
Publication date
01-12-2021
Publisher
BioMed Central
Keyword
Helminths
Published in
BMC Immunology / Issue 1/2021
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-020-00394-5

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