Chemokines and NK cells: regulators of development, trafficking and functions

Giovanni Bernardini, Angela Gismondi, Angela Santoni, Giovanni Bernardini, Angela Gismondi, Angela Santoni

Abstract

NK cells are innate lymphocytes capable of killing malignant or infected cells and to produce a wide array of cytokines and chemokines following activation. Chemokines, play critical roles in the regulation of NK cell tissue distribution in normal conditions as well as their rapid recruitment to the parenchyma of injured organs during inflammation, which is critical for NK cell ability to promote protective responses. In this regard, differences in chemokine receptor expression have been reported on specialized NK cell subsets with distinct effector functions and tissue distribution. Besides their role in the regulation of NK cell trafficking, chemotactic molecules can also affect NK cell effector functions by regulating their priming and their ability to kill and secrete cytokines.

Copyright © 2012 Elsevier B.V. All rights reserved.

Figures

Fig. 1
Fig. 1
Hypothetical model of CXCR4 role on NK cell development during NK cell interaction with stromal cells. During development, high expression levels of CXCR4 on immature NK cells may potentiate their response to IL-15, directly favoring their proliferation and differentiation, while CXCR4/CXCL12-mediated retention may influence stromal cell-promoted differentiation in later differentiation stages. Down-modulation of CXCR4 coincides with NK cell subset exclusion from BM-parenchyma and enrichment in sinusoids and is likely to allow responsiveness to other chemoattractant including S1P and CCL3, allowing egress from BM.
Fig. 2
Fig. 2
Chemokines regulate NK cell cross-talk with other immune cells in lymphoid and non lymphoid tissues. NK cells functional interaction with DC, monocytes or tissue resident machrophages can be facilitated by tissue expression of chemokines that promote simultaneous recruitment of cells from circulation facilitating their communication in vivo. In addition, several in vitro studies have evidenced the role of chemokines produced by NK cells and other immune cells, including CCR5, CXCR3 and XCL1 ligands for reciprocal attraction.

References

    1. Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187–376.
    1. Lanier L.L. NK cell recognition. Annu Rev Immunol. 2005;23:225–274.
    1. Di Santo J.P. Natural killer cell developmental pathways: a question of balance. Annu Rev Immunol. 2006;24:257–286.
    1. Freud A.G., Caligiuri M.A. Human natural killer cell development. Immunol Rev. 2006;214:56–72.
    1. Kennedy M.K., Glaccum M., Brown S.N., Butz E.A., Viney J.L., Embers M. Reversible defects in natural killer and memory CD8T cell lineages in interleukin 15-deficient mice. J Exp Med. 2000;191:771–780.
    1. Vosshenrich C.A., Samson-Villeger S.I., Di Santo J.P. Distinguishing features of developing natural killer cells. Curr Opin Immunol. 2005;17:151–158.
    1. Srour E.F., Brandt J.E., Briddell R.A., Leemhuis T., van Besien K., Hoffman R. Human CD34+ HLA-DR- bone marrow cells contain progenitor cells capable of self-renewal, multilineage differentiation, and long-term in vitro hematopoiesis. Blood Cells. 1991;17:287–295.
    1. Miller J.S., Verfaillie C., McGlave P. The generation of human natural killer cells from CD34+/DR− primitive progenitors in long-term bone marrow culture. Blood. 1992;80:2182–2187.
    1. Caligiuri M.A. Human natural killer cells. Blood. 2008;112:461–469.
    1. Chiossone L., Chaix J., Fuseri N., Roth C., Vivier E., Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood. 2009;113:5488–5496.
    1. Huntington N.D., Tabarias H., Fairfax K., Brady J., Hayakawa Y., Degli-Esposti M.A. NK cell maturation and peripheral axis is associated with KLRG1 up-regulation. J Immunol. 2007;178:4764–4770.
    1. Vosshenrich C.A., García-Ojeda M.E., Samson-Villéger S.I., Pasqualetto V., Enault L., Richard-Le Goff O. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol. 2006;7:1217–1224.
    1. Santoni A., Zingoni A., Cerboni C., Gismondi A. Natural killer (NK) cells from killers to regulators: distinct features between peripheral blood and decidual NK cells. Am J Reprod Immunol. 2007;58:280–288.
    1. Salazar-Mather T.P., Ishikawa R., Biron C.A. NK cell trafficking and cytokine expression in splenic compartments after IFN induction and viral infection. J Immunol. 1996;157:3054–3064.
    1. Dokun A.O., Chu D.T., Yang L., Bendelac A.S., Yokoyama W.M. Analysis of in situ NK cell responses during viral infection. J Immunol. 2001;167:5286–5293.
    1. Gregoire C., Cognet C., Chasson L., Coupet C.A., Dalod M., Reboldi A. Intrasplenic trafficking of natural killer cells is redirected by chemokines upon inflammation. Eur J Immunol. 2008;38:2076–2084.
    1. Sciumè G., De Angelis G., Benigni G., Ponzetta A., Morrone S., Santoni A. CX3CR1 expression defines 2 KLRG1+ mouse NK-cell subsets with distinct functional properties and positioning in the bone marrow. Blood. 2011;117:4467–4475.
    1. Bajénoff M., Breart B., Huang A.Y., Qi H., Cazareth J., Braud V.M. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med. 2006;203:619–631.
    1. Whitelaw P.F., Croy B.A. Granulated lymphocytes of pregnancy. Placenta. 1996;17:533–543.
    1. Doherty D.G., O’Farrelly C. Innate and adaptive lymphoid cells in the human liver. Immunol Rev. 2000;174:5–20.
    1. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature. 2009;457:722–725.
    1. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity. 2008;29:958–970.
    1. Luci C., Reynders A., Ivanov I.I., Cognet C., Chiche L., Chasson L. Influence of the transcription factor RORgamma on the development of NKp46+ cell populations in gut and skin. Nat Immunol. 2009;10:75–82.
    1. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C. RORgamma and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol. 2009;10:83–91.
    1. Spits H., Di Santo J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat Immunol. 2011;12:21–27.
    1. Colonna M. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity. Immunity. 2009;31:15–23.
    1. Gregoire C., Chasson L., Luci C., Tomasello E., Geissmann F., Vivier E. The trafficking of natural killer cells. Immunol Rev. 2007;220:169–182.
    1. Hayakawa Y., Huntington N.D., Nutt S.L., Smyth M.J. Functional subsets of mouse natural killer cells. Immunol Rev. 2006;214:47–55.
    1. Robertson M.J. Role of chemokines in the biology of natural killer cells. J Leukoc Biol. 2002;71:173–183.
    1. Chuntharapai A., Lee J., Hebert C.A., Kim K. Monoclonal antibodies detect different distribution patterns of IL-8 receptor A and IL-8 receptor B on human peripheral blood leukocytes. J Immunol. 1994;153:5682–5688.
    1. Morohashi H., Miyawaki T., Nomura H., Kuno K., Murakami S., Matsushima K. Expression of both types of human interleukin-8 receptors on mature neutrophils, monocytes, and natural killer cells. J Leukoc Biol. 1995;57:180–187.
    1. Casilli F., Bianchini A., Gloaguen I., Biordi L., Alesse E., Festuccia C. Inhibition of interleukin-8 (CXCL8/IL-8) responses by repertaxin, a new inhibitor of the chemokine receptors CXCR1 and CXCR2. Biochem Pharmacol. 2005;69:385–394.
    1. Yoneda O., Imai T., Goda S., Inoue H., Yamauchi A., Okazaki T. Fractalkine-mediated endothelial cell injury by NK cells. J Immunol. 2000;164:4055–4062.
    1. Campbell J.J., Qin S., Unutmaz D., Soler D., Murphy K.E., Hodge M.R. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol. 2001;166:6477–6482.
    1. Taub D.D., Sayers T.J., Carter C.R., Ortaldo J.R. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol. 1995;155:3877–3888.
    1. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004;427:355–360.
    1. Maghazachi A.A. G protein-coupled receptors in natural killer cells. J Leukoc Biol. 2003;74:16–24.
    1. Walzer T., Chiossone L., Chaix J., Calver A., Carozzo C., Garrigue-Antar L. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat Immunol. 2007;8:1337–1344.
    1. Marquardt N., Wilk E., Pokoyski C., Schmidt R.E., Jacobs R. Murine CXCR3+ CD27bright NK cells resemble the human CD56bright NK-cell population. Eur J Immunol. 2010;40:1428–1439.
    1. Paust S., Gill H.S., Wang B.Z., Flynn M.P., Moseman E.A., Senman B. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol. 2010;11:1127–1135.
    1. Hodge D.L., Schill W.B., Wang J.M., Blanca I., Reynolds D.A., Ortaldo J.R. IL-2 and IL-12 alter NK cell responsiveness to IFN-gamma-inducible protein 10 by down-regulating CXCR3 expression. J Immunol. 2002;168:6090–6098.
    1. Inngjerdingen M., Damaj B., Maghazachi A.A. Expression and regulation of chemokine receptors in human natural killer cells. Blood. 2001;97:367–375.
    1. Parolini S., Santoro A., Marcenaro E., Luini W., Massardi L., Facchetti F. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood. 2007;109:3625–3632.
    1. Barlic J., Sechler J.M., Murphy P.M. IL-15 and IL-2 oppositely regulate expression of the chemokine receptor CX3CR1. Blood. 2003;102:3494–3503.
    1. Mailliard R.B., Alber S.M., Shen H., Watkins S.C., Kirkwood J.M., Herberman R.B. IL-18-induced CD83+ CCR7+ NK helper cells. J Exp Med. 2005;202:941–953.
    1. Taub D.D., Ortaldo J.R., Turcovski-Corrales S.M., Key M.L., Longo D.L., Murphy W.J. Beta chemokines costimulate lymphocyte cytolysis, proliferation, and lymphokine production. J Leukoc Biol. 1996;59:81–89.
    1. Guo J., Chen T., Wang B., Zhang M., An H., Guo Z. Chemoattraction, adhesion and activation of natural killer cells are involved in the antitumor immune response induced by fractalkine/CX3CL1. Immunol Lett. 2003;89:1–7.
    1. Yoneda O., Imai T., Nishimura M., Miyaji M., Mimori T., Okazaki T. Membrane-bound form of fractalkine induces IFN-gamma production by NK cells. Eur J Immunol. 2003;33:53–58.
    1. Maghazachi A.A., Al-Aoukaty A., Schall T.J. CC chemokines induce the generation of killer cells from CD56+ cells. Eur J Immunol. 1996;26:315–319.
    1. Nieto M., Navarro F., Perez-Villar J.J., del Pozo M.A., Gonzalez-Amaro R., Mellado M. Roles of chemokines and receptor polarization in NK-target cell interactions. J Immunol. 1998;161:3330–3339.
    1. Pallandre J.R., Krzewski K., Bedel R., Ryffel B., Caignard A., Rohrlich P.S. Dendritic cell and natural killer cell cross-talk: a pivotal role of CX3CL1 in NK cytoskeleton organization and activation. Blood. 2008
    1. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA. 1998;95:9448–9453.
    1. Dar A., Kollet O., Lapidot T. Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp Hematol. 2006;34:967–975.
    1. Broxmeyer H.E., Orschell C.M., Clapp D.W., Hangoc G., Cooper S., Plett P.A. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD-3100, a CXCR4 antagonist. J Exp Med. 2005;201:1307–1318.
    1. Broxmeyer H.E. Chemokines in hematopoiesis. Curr Opin Hematol. 2008;15:49–58.
    1. Egawa T., Kawabata K., Kawamoto H., Amada K., Okamoto R., Fujii N. The earliest stages of B cell development require a chemokine stromal cell-derived factor/pre-B cell growth-stimulating factor. Immunity. 2001;15:323–334.
    1. Foudi A., Jarrier P., Zhang Y., Wittner M., Geay J.F., Lecluse Y. Reduced retention of radioprotective hematopoietic cells within the bone marrow microenvironment in CXCR4−/− chimeric mice. Blood. 2006;107:2243–2251.
    1. Tokoyoda K., Egawa T., Sugiyama T., Choi B.I., Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity. 2004;20:707–718.
    1. Plotkin J., Prockop S.E., Lepique A., Petrie H.T. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. J Immunol. 2003;171:4521–4527.
    1. Bernardini G., Sciumè G., Bosisio D., Morrone S., Sozzani S., Santoni A. CCL3 and CXCL12 regulate trafficking of mouse bone marrow NK cell subsets. Blood. 2008;111:3626–3634.
    1. Noda M., Omatsu Y., Sugiyama T., Oishi S., Fujii N., Nagasawa T. CXCL12-CXCR4 chemokine signaling is essential for NK-cell development in adult mice. Blood. 2011;117:451–458.
    1. Weiss I.D., Shoham H., Wald O., Wald H., Beider K., Abraham M. Ccr5 deficiency regulates the proliferation and trafficking of natural killer cells under physiological conditions. Cytokine. 2011;54:249–257.
    1. Yu Y.R., Fong A.M., Combadiere C., Gao J.L., Murphy P.M., Patel D.D. Defective antitumor responses in CX3CR1-deficient mice. Int J Cancer. 2007;121:316–322.
    1. Salazar-Mather T.P., Orange J.S., Biron C.A. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein 1alpha (MIP-1alpha)-dependent pathways. J Exp Med. 1998;187:1–14.
    1. Hokeness K.L., Kuziel W.A., Biron C.A., Salazar-Mather T.P. Monocyte chemoattractant protein-1 and CCR2 interactions are required for IFN-alpha/beta-induced inflammatory responses and antiviral defense in liver. J Immunol. 2005;174:1549–1556.
    1. Wald O., Weiss I.D., Wald H., Shoham H., Bar-Shavit Y., Beider K. IFN-gamma acts on T cells to induce NK cell mobilization and accumulation in target organs. J Immunol. 2006;176:4716–4729.
    1. Zeng X., Moore T.A., Newstead M.W., Hernandez-Alcoceba R., Tsai W.C., Standiford T.J. Intrapulmonary expression of macrophage inflammatory protein 1alpha (CCL3) induces neutrophil and NK cell accumulation and stimulates innate immunity in murine bacterial pneumonia. Infect Immun. 2003;71:1306–1315.
    1. Shang X., Qiu B., Frait K.A., Hu J.S., Sonstein J., Curtis J.L. Chemokine receptor 1 knockout abrogates natural killer cell recruitment and impairs type-1 cytokines in lymphoid tissue during pulmonary granuloma formation. Am J Pathol. 2000;157:2055–2063.
    1. Morrison B.E., Park S.J., Mooney J.M., Mehrad B. Chemokine-mediated recruitment of NK cells is a critical host defense mechanism in invasive aspergillosis. J Clin Invest. 2003;112:1862–1870.
    1. Robinson L.A., Nataraj C., Thomas D.W., Cosby J.M., Griffiths R., Bautch V. The chemokine CX3CL1 regulates NK cell activity in vivo. Cell Immunol. 2003;225:122–130.
    1. Widney D.P., Hu Y., Foreman-Wykert A.K., Bui K.C., Nguyen T.T., Lu B. CXCR3 and its ligands participate in the host response to Bordetella bronchiseptica infection of the mouse respiratory tract but are not required for clearance of bacteria from the lung. Infect Immun. 2005;73:485–493.
    1. Trifilo M.J., Montalto-Morrison C., Stiles L.N., Hurst K.R., Hardison J.L., Manning J.E. CXC chemokine ligand 10 controls viral infection in the central nervous system: evidence for a role in innate immune response through recruitment and activation of natural killer cells. J Virol. 2004;78:585–594.
    1. Thapa M., Kuziel W.A., Carr D.J. Susceptibility of CCR5-deficient mice to genital herpes simplex virus type 2 is linked to NK cell mobilization. J Virol. 2007;81:3704–3713.
    1. Hao J., Liu R., Piao W., Zhou Q., Vollmer T.L., Campagnolo D.I. Central nervous system (CNS)-resident natural killer cells suppress Th17 responses and CNS autoimmune pathology. J Exp Med. 2010;207:1907–1921.
    1. Saudemont A., Jouy N., Hetuin D., Quesnel B. NK cells that are activated by CXCL10 can kill dormant tumor cells that resist CTL-mediated lysis and can express B7-H1 that stimulates T cells. Blood. 2005;105:2428–2435.
    1. Wendel M., Galani I.E., Suri-Payer E., Cerwenka A. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res. 2008;68:8437–8445.
    1. Martin-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol. 2004;5:1260–1265.
    1. Lucas M., Schachterle W., Oberle K., Aichele P., Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity. 2007;26:503–517.
    1. Van Elssen C.H., Vanderlocht J., Frings P.W., Senden-Gijsbers B.L., Schnijderberg M.C., van Gelder M. Klebsiella pneumoniae-triggered DC recruit human NK cells in a CCR5-dependent manner leading to increased CCL19-responsiveness and activation of NK cells. Eur J Immunol. 2010;40:3138–3149.
    1. Andrews D.M., Scalzo A.A., Yokoyama W.M., Smyth M.J., Degli-Esposti M.A. Functional interactions between dendritic cells and NK cells during viral infection. Nat Immunol. 2003 Feb;4(2):175–181.
    1. Auffray C., Fogg D.K., Narni-Mancinelli E., Senechal B., Trouillet C., Saederup N. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med. 2009;206:595–606.
    1. Kang S.J., Liang H.E., Reizis B., Locksley R.M. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity. 2008;29:819–833.
    1. Soderquest K., Powell N., Luci C., van Rooijen N., Hidalgo A., Geissmann F. Monocytes control natural killer cell differentiation to effector phenotypes. Blood. 2011;117:4511–4518.
    1. Beuneu H., Deguine J., Breart B., Mandelboim O., Di Santo J.P., Bousso P. Dynamic behavior of NK cells during activation in lymph nodes. Blood. 2009;114:3227–3234.
    1. Costantini C., Cassatella M.A. The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol. 2011;89:221–233.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться