CD11a regulates effector CD8 T cell differentiation and central memory development in response to infection with Listeria monocytogenes

Infection and Immunity

Volumn 81, Issue 4, 2013, Pages 1140-1151

  Bose, Tina O ^a   Pham, Quynh Mai ^a   Jellison, Evan R ^a   Mouries, Juliette ^a   Ballantyne, Christie M ^b   Lefrançois, Leo ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; GRANZYME B; INTERLEUKIN 7 RECEPTOR; L SELECTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL LOAD; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANTIGENS, CD11A; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNOLOGIC MEMORY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, KNOCKOUT;

EID: 84875481910     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00749-12     Document Type: Article

References (65)

1. McFarland HI, Nahill SR, Maciaszek JW, Welsh RM. 1992. CD11b(Mac-1): a marker forCD8+cytotoxicTcell activation and memory in virus infection. J. Immunol. 149:1326-1333.
2. Huleatt JW, Lefrançois L. 1995. Antigen-driven induction of CD11c on intestinal intraepithelial lymphocytes and CD8(+) T cells in vivo. J. Immunol. 154:5684-5693.
3. Hynes RO. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
4. Anderson DC, Springer TA. 1987. Leukocyte adhesion deficiency: an inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. Annu. Rev. Med. 38:175-194.
5. Hogg N, Bates PA. 2000. Genetic analysis of integrin function in man: LAD-1 and other syndromes. Matrix Biol. 19:211-222. 6. Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, Hogg N. 2009. Integrins in immunity. J. Cell Sci. 122:215-225.
6. Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, Hogg N. 2009. Integrins in immunity. J. Cell Sci. 122:215-225.
7. Scharffetter-Kochanek K, Lu H, Norman K, van Nood N, Munoz F, Grabbe S, McArthur M, Lorenzo I, Kaplan S, Ley K, Smith CW, Montgomery CA, Rich S, Beaudet AL. 1998. Spontaneous skin ulceration and defective T cell function in CD18 null mice. J. Exp. Med. 188: 119-131.
8. Liang Y, Liu C, Djeu JY, Zhong B, Peters T, Scharffetter-Kochanek K, Anasetti C, Yu XZ. 2008. α2 integrins separate graft-versus-host disease and graft-versus-leukemia effects. Blood 111:954-962.
9. Ren B, McCrory MA, Pass C, Bullard DC, Ballantyne CM, Xu Y, Briles DE, Szalai AJ. 2004. The virulence function of Streptococcus pneumoniae surface protein A involves inhibition of complement activation and impairment of complement receptor-mediated protection. J. Immunol. 173:7506-7512.
10. Ding ZM, Babensee JE, Simon SI, Lu H, Perrard JL, Bullard DC, Dai XY, Bromley SK, Dustin ML, Entman ML, Smith CW, Ballantyne CM. 1999. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. J. Immunol. 163:5029-5038.
11. Borjesson DL, Simon SI, Hodzic E, DeCock HE, Ballantyne CM, Barthold SW. 2003. Roles of neutrophil beta 2 integrins in kinetics of bacteremia, extravasation, and tick acquisition of Anaplasma phagocytophila in mice. Blood 101:3257-3264.
12. Borjesson DL, Simon SI, Hodzic E, Ballantyne CM, Barthold SW. 2002. Kinetics of CD11b/CD18 up-regulation during infection with the agent of human granulocytic ehrlichiosis in mice. Lab. Invest. 82:303-311.
13. Kadioglu A, De FK, Bangert M, Fernandes VE, Richards L, Jones K, Andrew PW, Hogg N. 2011. The integrins Mac-1 and β4α1 perform crucial roles in neutrophil and T cell recruitment to lungs during Streptococcus pneumoniae infection. J. Immunol. 186:5907-5915.
14. Allen SJ, Mott KR, Chentoufi AA, BenMohamed L, Wechsler SL, Ballantyne CM, Ghiasi H. 2011. CD11c controls herpes simplex virus 1 responses to limit virus replication during primary infection. J. Virol. 85:9945-9955.
15. Wu H, Rodgers JR, Perrard XY, Perrard JL, Prince JE, Abe Y, Davis BK, Dietsch G, Smith CW, Ballantyne CM. 2004. Deficiency of CD11b or CD11d results in reduced staphylococcal enterotoxin-induced T cell response and T cell phenotypic changes. J. Immunol. 173:297-306.
16. Dustin ML, Springer TA. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341:619-624.
17. van Seventer GA, Shimizu Y, Horgan KJ, Shaw S. 1990. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptormediated activation of resting T cells. J. Immunol. 144:4579-4586.
18. Bachmann MF, Kall-Faienza K, Schmits R, Bouchard D, Beach J, Speiser DE, Mak TW, Ohashi PS. 1997. Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation. Immunity 7:549-557.
19. Park EJ, Peixoto A, Imai Y, Goodarzi A, Cheng G, Carman CV, von Andrian UH, Shimaoka M. 2010. Distinct roles for LFA-1 affinity regulation during T-cell adhesion, diapedesis, and interstitial migration in lymph nodes. Blood 115:1572-1581.
20. Berlin-Rufenach C, Otto F, Mathies M, Westermann J, Owen MJ, Hamann A, Hogg N. 1999. Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J. Exp. Med. 189:1467-1478.
21. Schmits R, Kundig TM, Baker DM, Shumaker G, Simard JJL, Duncan G, Wakeman A, Shahinian A, van der Heiden A, Bachmann MF, Ohashi PS, Mak TW, Hickstein DD. 1996. LFA-1-deficient mice show normal CTL responses to virus but fail to reject immunogenic tumor. J. Exp. Med. 183:1415-1426.
22. Marski M, Ye AL, Abraham C. 2007. CD18 is required for intestinal T cell responses at multiple immune checkpoints. J. Immunol. 178:2104-2112.
23. Prince JE, Brayton CF, Fossett MC, Durand JA, Kaplan SL, Smith CW, Ballantyne CM. 2001. The differential roles of LFA-1 and Mac-1 in host defense against systemic infection with Streptococcus pneumoniae. J. Immunol. 166:7362-7369.
24. Ghosh S, Chackerian AA, Parker CM, Ballantyne CM, Behar SM. 2006. The LFA-1 adhesion molecule is required for protective immunity during pulmonary Mycobacterium tuberculosis infection. J. Immunol. 176:4914-4922.
25. Hamann A, Jablonski-Westrich D, Duijvestijn A, Butcher EC, Baisch H, Harder R, Thiele HG. 1988. Evidence for an accessory role of LFA-1 in lymphocyte-high endothelium interaction during homing. J. Immunol. 140:693-699.
26. Miyamoto M, Emoto M, Emoto Y, Brinkmann V, Yoshizawa I, Seiler P, Aichele P, Kita E, Kaufmann SH. 2003. Neutrophilia in LFA-1-deficient mice confers resistance to listeriosis: possible contribution of granulocytecolony- stimulating factor and IL-17. J. Immunol. 170:5228-5234.
27. Emoto M, Miyamoto M, Emoto Y, Yoshizawa I, Brinkmann V, van Rooijen N, Kaufmann SH. 2003. Highly biased type 1 immune responses in mice deficient in LFA-1 in Listeria monocytogenes infection are caused by elevated IL-12 production by granulocytes. J. Immunol. 171:3970-3976.
28. Wu H, Prince JE, Brayton CF, Shah C, Zeve D, Gregory SH, Smith CW, Ballantyne CM. 2003. Host resistance of CD18 knockout mice against systemic infection with Listeria monocytogenes. Infect. Immun. 71:5986-5993.
29. Shi C, Hohl TM, Leiner I, Equinda MJ, Fan X, Pamer EG. 2011. Ly6G+ neutrophils are dispensable for defense against systemic Listeria monocytogenes infection. J. Immunol. 187:5293-5298.
30. Carr KD, Sieve AN, Indramohan M, Break TJ, Lee S, Berg RE. 2011. Specific depletion reveals a novel role for neutrophil-mediated protection in the liver during Listeria monocytogenes infection. Eur. J. Immunol. 41:2666-2676.
31. Serbina NV, Shi C, Pamer EG. 2012. Monocyte-mediated immune defense against murine Listeria monocytogenes infection. Adv. Immunol. 113:119-134.
32. Coxon A, Rieu P, Barkalow FJ, Askari S, Sharpe AH, von Andrian UH, Arnaout MA, Mayadas TN. 1996. A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 5:653-666.
33. Pope C, Kim Marzo S-KA, Masopust D, Williams K, Jiang J, Shen H, Lefrançois L. 2001. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166:3402-3409.
34. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, Cleary PP, Jenkins MK. 2010. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11:83-89.
35. Khanna KM, McNamara JT, Lefrancois L. 2007. In situ imaging of the endogenous CD8 T cell response to infection. Science 318:116-120.
36. Turner MJ, Jellison ER, Lingenheld EG, Puddington L, Lefrancois L. 2008. Avidity maturation of memory CD8 T cells is limited by self-antigen expression. J. Exp. Med. 205:1859-1868.
37. Obar JJ, Khanna KM, Lefrancois L. 2008. Endogenous naive CD8+T cell precursor frequency regulates primary and memory responses to infection. Immunity 28:859-869.
38. Lin Y, Roberts TJ, Sriram V, Cho S, Brutkiewicz RR. 2003. Myeloid marker expression on antiviral CD8+ T cells following an acute virus infection. Eur. J. Immunol. 33:2736-2743.
39. Klonowski KD, Marzo AL, Williams KJ, Lee SJ, Pham QM, Lefrancois L. 2006. CD8 T cell recall responses are regulated by the tissue tropism of the memory cell and pathogen. J. Immunol. 177:6738-6746.
40. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. 2003. Selectiveexpressionoftheinterleukin7receptoridentifieseffectorCD8Tcellsthat give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198.
41. Obar JJ, Jellison ER, Sheridan BS, Blair DA, Pham QM, Zickovich JM, Lefrancois L. 2011. Pathogen-induced inflammatory environment controls effector and memory CD8+T cell differentiation. J. Immunol. 187:4967-4978.
42. Varga G, Nippe N, Balkow S, Peters T, Wild MK, Seeliger S, Beissert S, Krummen M, Roth J, Sunderkotter C, Grabbe S. 2010. LFA-1 contributes to signal I of T-cell activation and to the production of T(h)1 cytokines. J. Invest. Dermatol. 130:1005-1012.
43. Davignon D, Martz E, Reynolds T, Kurzinger K, Springer TA. 1981. Lymphocyte function-associated antigen 1 (LFA-1): a surface antigen distinct from Lyt-2,3 that participates in T lymphocyte-mediated killing. Proc. Natl. Acad. Sci. U. S. A. 78:4535-4539.
44. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M, Koup RA. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281:65-78.
45. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, Gapin L, Kaech SM. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
46. Cui W, Joshi NS, Jiang A, Kaech SM. 2009. Effects of Signal 3 during CD8 T cell priming: bystander production of IL-12 enhances effector T cell expansion but promotes terminal differentiation. Vaccine 27:2177-2187.
47. Obar JJ, Lefrancois L. 2010. Early signals during CD8 T cell priming regulate the generation of central memory cells. J. Immunol. 185:263-272. 48. Obar JJ, Lefrancois L. 2010. Early events governing memory CD8+T-cell differentiation. Int. Immunol. 22:619-625.
48. Obar JJ, Lefrancois L. 2010. Early events governing memory CD8+T-cell differentiation. Int. Immunol. 22:619-625.
49. Obar JJ, Molloy MJ, Jellison ER, Stoklasek TA, Zhang W, Usherwood EJ, Lefrancois L. 2010. CD4+ T cell regulation of CD25 expression controls development of short-lived effector CD8+ T cells in primary and secondary responses. Proc. Natl. Acad. Sci. U. S. A. 107:193-198.
50. Kohlmeier JE, Reiley WW, Perona-Wright G, Freeman ML, Yager EJ, Connor LM, Brincks EL, Cookenham T, Roberts AD, Burkum CE, Sell S, Winslow GM, Blackman MA, Mohrs M, Woodland DL. 2011. Inflammatory chemokine receptors regulate CD8+ T cell contraction and memory generation following infection. J. Exp. Med. 208:1621-1634.
51. Scholer A, Hugues S, Boissonnas A, Fetler L, Amigorena S. 2008. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 28:258-270.
52. Badovinac VP, Porter BB, Harty JT. 2004. CD8+ T cell contraction is controlled by early inflammation. Nat. Immunol. 5:809-817.
53. Sarkar S, Teichgraber V, Kalia V, Polley A, Masopust D, Harrington LE, Ahmed R, Wherry EJ. 2007. Strength of stimulus and clonal competition impact the rate of memory CD8 T cell differentiation. J. Immunol. 179:6704-6714.
54. Blair DA, Turner DL, Bose TO, Pham QM, Bouchard KR, Williams KJ, McAleer JP, Cauley LS, Vella AT, Lefrancois L. 2011. Duration of antigen availability influences the expansion and memory differentiation of T cells. J. Immunol. 187:2310-2321.
55. Mempel TR, Henrickson SE, von Andrian UH. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154-159.
56. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. 1998. Threedimensional segregation of supramolecular activation clusters in T cells. Nature 395:82-86.
57. Parameswaran N, Suresh R, Bal V, Rath S, George A. 2005. Lack of ICAM-1 on APCs during T cell priming leads to poor generation of central memory cells. J. Immunol. 175:2201-2211.
58. Huleatt JW, Lefrançois L. 1996. α2-integrins and ICAM-1 are involved in establishment of the mucosal T cell compartment. Immunity 5:263-273. 59. Sims TN, Dustin ML. 2002. The immunological synapse: integrins take the stage. Immunol. Rev. 186:100-117.
59. Sims TN, Dustin ML. 2002. The immunological synapse: integrins take the stage. Immunol. Rev. 186:100-117.
60. Li D, Molldrem JJ, Ma Q. 2009. LFA-1 regulates CD8+ T cell activation via T cell receptor-mediated and LFA-1-mediated Erk1/2 signal pathways. J. Biol. Chem. 284:21001-21010.
61. Beinke S, Phee H, Clingan JM, Schlessinger J, Matloubian M, Weiss A. 2010. Proline-rich tyrosine kinase-2 is critical for CD8 T-cell short-lived effector fate. Proc. Natl. Acad. Sci. U. S. A. 107:16234-16239.
62. Chao CC, Jensen R, Dailey MO. 1997. Mechanisms of L-selectin regulation by activated T cells. J. Immunol. 159:1686-1694.
63. Smalley DM, Ley K. 2005. L-selectin: mechanisms and physiological significance of ectodomain cleavage. J. Cell. Mol. Med. 9:255-266.
64. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian UH, Ahmed R. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4:225-234.
65. Marzo AL, Klonowski KD, Le Bon A, Borrow P, Tough DF, Lefrancois L. 2005. Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nat. Immunol. 6:793-799.