The pathophysiological role of Chemokines in the regulation of NK cell tissue homing

Critical Reviews in Oncogenesis

Volumn 19, Issue 1-2, 2014, Pages 77-90

  Bernardini, Giovanni ^a   Santoni, Angela ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Chemokines; Migration; NK cell; Tissue homing; Tumor

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; COMPLEMENTARY DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; MONOCLONAL ANTIBODY; NATURAL KILLER CELL RECEPTOR NKG2D;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BREAST CANCER; CELL DEATH; CELL MIGRATION; CELL THERAPY; CELL TYPE; GENE TRANSFER; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFECTION; INFLAMMATION; INNATE IMMUNITY; LEWIS CARCINOMA; LYMPH NODE METASTASIS; LYMPHOCYTE HOMING; MELANOMA; METASTASIS; MULTIPLE MYELOMA; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NEUROBLASTOMA; NONHUMAN; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR GROWTH;

CHEMOKINES; IMMUNITY, INNATE; KILLER CELLS, NATURAL; RECEPTORS, CHEMOKINE;

EID: 84899658350     PISSN: 08939675     EISSN: 21626448     Source Type: Journal    
DOI: 10.1615/CritRevOncog.2014010386     Document Type: Article

References (96)

1. Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187-376.
2. Lanier LL. NK cell recognition. Annu Rev Immunol. 2005; 23:225-274.
3. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med. 2002;195(3):327-33.
4. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med. 2002;195(3):335-41.
5. Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol.2008;8:259-268.
6. Bernardini G, Gismondi A, Santoni A. Chemokines and NK cells: regulators of development, trafcking and functions. Immunol Lett. 2012;145(1-2):39-46.
7. Gregoire C, Chasson L, Luci C, Tomasello E, Geissmann F, Vivier E, Walzer T. Te traf- fcking of natural killer cells. Immunol Rev. 2007;220:169-182.
8. Ponzetta A, Sciumè G, Benigni G, Antonangeli F, Morrone S, Santoni A, Bernardini G. CX3CR1 Regulates the Maintenance of KLRG1+ NK Cells into the bone marrow by promoting their entry into circulation. J Immunol. 2013;191(11):5684-5694.
9. Peng H, Jiang X, Chen Y, Sojka DK, Wei H, Gao X, Sun R, Yokoyama WM, Tian Z. Liver resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest. 2013;123(4):1444-1456.
10. Takeda K, Cretney E, Hayakawa Y, Ota T, Akiba H, Ogasawara K, Yagita H, Kinoshita K, Okumura K, Smyth MJ. TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood. 2005;105(5):2082-2089.
11. Vosshenrich CA, García-Ojeda ME, Samson-Villéger SI, Pasqualetto V, Enault L, Corcuf E, Guy-Grand D, Rocha B, Cumano A, Rogge L, Ezine S, Di Santo JP. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol. 2006;7(11):1217-24.
12. Hayakawa Y, Huntington ND, Nutt SL, Smyth MJ. Functional subsets of mouse natural killer cells. Immunol Rev. 2006;214:47-55.
13. Münz C. Non-cytotoxic protection by human NK cells in mucosal secondary lymphoid tissues. Eur J Immunol. 2008;38(11):2946-8.
14. Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW, von Andrian UH. Critical role for the chemo-kine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol. 2010;11(12):1127-35.
15. Doherty DG, O'Farrelly C. Innate and adaptive lymphoid cells in the human liver. Immunol Rev. 2000;174:5-20.
16. Clark EA, Brugge JS. Integrins and signal transduction pathways: the road taken. Science. 1995;268(5208):233-9.
17. Baggiolini M, Dewald B, Moser B. Human chemokines: an update. Annu Rev Immunol. 1997;15:675-705.
18. Mantovani A. Te chemokine system: redundancy for robust outputs. Immunol Today. 1999;20(6):254-7.
19. Wittamer V, Franssen JD, Vulcano M, Mirjolet JF, Le Poul E, Migeotte I, Brézillon S, Tyldesley R, Blanpain C, Detheux M, Mantovani A, Sozzani S, Vassart G, Parmentier M, Communi D. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human infammatory fuids. J Exp Med. 2003;198(7):977-85.
20. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, Brinkmann V, Allende ML, Proia RL, Cyster JG. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004;427(6972): 355-60.
21. Taub DD, Sayers TJ, Carter CR, Ortaldo JR. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol. 1995 Oct 15;155(8):3877-88.
22. Hedrick JA, Saylor V, Figueroa D, Mizoue L, Xu Y, Menon S, Abrams J, Handel T, Zlotnik A. Lymphotactin is produced by NK cells and attracts both NK cells and T cells in vivo. J Immunol. 1997;158(4):1533-40.
23. Allavena P, Bianchi G, Giardina P, Polentarutti N, Zhou D, Introna M, Sozzani S, Mantovani A. Migratory response of human NK cells to monocyte-chemotactic proteins. Methods. 1996;10(1):145-9.
24. Inngjerdingen M, Damaj B, Maghazachi AA. Expression and regulation of chemokine receptors in human natural killer cells. Blood. 2001;97(2):367-75.
25. Parolini S, Santoro A, Marcenaro E, Luini W, Massardi L, Facchetti F, Communi D, Parmentier M, Majorana A, Sironi M, Tabellini G, Moretta A, Sozzani S. Te role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood. 2007;109(9):3625-32.
26. Barlic J, Sechler JM, Murphy PM. IL-15 and IL-2 oppositely regulate expression of the chemokine receptor CX3CR1. Blood. 2003;102(10):3494-503.
27. Chung CY, Funamoto S, Firtel RA. Signaling pathways controlling cell polarity and chemo-taxis. Trends Biochem Sci. 2001;26(9):557-66.
28. Al-Aoukaty A, Schall TJ, Maghazachi AA. Diferential coupling of CC chemokine receptors to multiple heterotrimeric G proteins in human interleukin-2-activated natural killer cells. Blood. 1996;87(10):4255-60.
29. Arai H, Tsou CL, Charo IF. Chemotaxis in a lymphocyte cell line transfected with C-C chemokine receptor 2B: evidence that directed migration is mediated by betagamma dimers released by activation of Galphai-coupled receptors. Proc Natl Acad Sci U S A. 1997;94:14495-9.
30. Neptune ER, Bourne HR. Receptors induce chemotaxis by releasing the betagamma subunit of Gi, not by activating Gq or Gs. Proc Natl Acad Sci U S A. 1997;94(26):14489-94.
31. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol. 2005;5(7):546-59.
32. Svensson L, Stanley P, Willenbrock F, Hogg N. Te Gαq/11 proteins contribute to T lymphocyte migration by promoting turnover of integrin LFA-1 through recycling. PLoS One. 2012;7(6):e38517.
33. Curnock AP, Logan MK, Ward SG. Chemokine signalling: pivoting around multiple phosphoinositide 3-kinases. Immunology. 2002;105(2):125-36.
34. Bernardini G, Kim JY, Gismondi A, Butcher EC, Santoni A. Chemoattractant induces LFA-1 associated PI 3K activity and cell migration that are dependent on Fyn signaling. FASEB J. 2005;19(10):1305-7.
35. Hawkins P T, Anderson KE, Davidson K, Stephens LR. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans. 2006;34(Pt 5):647-62.
36. Al-Aoukaty A, Rolstad B, Maghazachi AA. Recruitment of pleckstrin and phosphoinosit-ide 3-kinase gamma into the cell membranes, and their association with G beta gamma after activation of NK cells with chemokines. J Immunol. 1999;162(6):3249-55.
37. Saudemont A, Garçon F, Yadi H, Roche-Molina M, Kim N, Segonds-Pichon A, Martín-Fontecha A, Okkenhaug K, Colucci F. p110gamma and p110delta isoforms of phosphoinositide 3-kinase differentially regulate natural killer cell migration in health and disease. Proc Natl Acad Sci U S A. 2009;106(14):5795-800.
38. Haddad E, Zugaza JL, Louache F, Debili N, Crouin C, Schwarz K, Fischer A, Vainchenker W, Bertoglio J. The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis. Blood. 2001;97(1):33-8.
39. Samstag Y, Eibert SM, Klemke M, Wabnitz GH. Actin cytoskeletal dynamics in T lymphocyte activation and migration. J Leukoc Biol. 2003;73(1):30-48.
40. Stabile H, Carlino C, Mazza C, Giliani S, Morrone S, Notarangelo LD, Notarangelo LD, Santoni A, Gismondi A. Impaired NK-cell migration in WAS/XLT patients: role of Cdc42/ WASp pathway in the control of chemokine-induced beta2 integrin high-affinity state. Blood. 2010;115(14):2818-26.
41. Dustin ML. Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr Opin Cell Biol. 2007;19(5):529-33.
42. Eriksson M, Leitz G, Fällman E, Axner O, Ryan JC, Nakamura MC, Sentman CL. Inhibitory receptors alter natural killer cell interactions with target cells yet allow simultaneous killing of susceptible targets. J Exp Med. 1999;190(7):1005-12.
43. Culley FJ, Johnson M, Evans JH, Kumar S, Crilly R, Casasbuenas J, Schnyder T, Mehrabi M, Deonarain MP, Ushakov DS, Braud V, Roth G, Brock R, Köhler K, Davis DM. Natural killer cell signal integration balances synapse symmetry and migration. PLoS Biol. 2009;7(7):e1000159.
44. Serrano-Pertierra E, Cernuda-Morollón E, López-Larrea C. Wiskott-Aldrich syndrome protein (WASp) and N-WASp are involved in the regulation of NK-cell migration upon NKG2D activation. Eur J Immunol. 2012;42(8):2142-51.
45. Salazar-Mather TP, Orange JS, Biron CA. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through mac-rophage infammatory protein 1alpha (MIP-1alpha)-dependent pathways. J Exp Med. 1998;187(1):1-14.
46. Salazar-Mather TP, Hamilton TA, Biron CA. A chemokine-to-cytokine-to-chemokine cascade critical in antiviral defense. J Clin Invest. 2000;105(7):985-93.
47. Hokeness KL, Kuziel WA, Biron CA, Salazar-Mather TP. Monocyte chemoattractant pro-tein-1 and CCR2 interactions are required for IFN-alpha/beta-induced inflammatory responses and antiviral defense in liver. J Immunol. 2005;174(3):1549-56.
48. Bernardini G, Sciumè G, Bosisio D, Morrone S, Sozzani S, Santoni A. CCL3 and CXCL12 regulate trafcking of mouse bone marrow NK cell subsets. Blood. 2008;111(7):3626-34.
49. Mayol K, Biajoux V, Marvel J, Balabanian K, Walzer T. Sequential desensitization of CXCR4 and S1P5 controls natural killer cell trafcking. Blood. 2011;118(18):4863-71.
50. Sciumè G, De Angelis G, Benigni G, Ponzetta A, Morrone S, Santoni A, Bernardini G. CX3CR1 expression defnes 2 KLRG1+ mouse NK-cell subsets with distinct functional properties and positioning in the bone marrow. Blood. 2011;117(17):4467-75.
51. Ochi M, Ohdan H, Mitsuta H, Onoe T, Tokita D, Hara H, Ishiyama K, Zhou W, Tanaka Y, Asahara T. Liver NK cells expressing TRAIL are toxic against self hepatocytes in mice. Hepatology. 2004;39(5):1321-31.
52. Dong Z, Wei H, Sun R, Tian Z. Te roles of innate immune cells in liver injury and regeneration. Cell Mol Immunol. 2007;4(4):241-52.
53. Perona-Wright G, Mohrs K, Szaba FM, Kummer LW, Madan R, Karp CL, Johnson LL, Smiley ST, Mohrs M. Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe. 2009;6(6):503-12.
54. Huang D, Shi FD, Jung S, Pien GC, Wang J, Salazar-Mather T P, He T T, Weaver JT, Ljunggren HG, Biron CA, Littman DR, Ransohoff RM. The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J. 2006;20(7):896-905.
55. Hammarberg H, Lidman O, Lundberg C, Eltayeb SY, Gielen AW, Muhallab S, Svenningsson A, Lindå H, van Der Meide PH, Cullheim S, Olsson T, Piehl F. Neuroprotection by encephalomyelitis: rescue of mechanically injured neurons and neurotrophin production by CNS-infltrating T and natural killer cells. J Neurosci. 2000;20(14):5283-91.
56. Hao J, Liu R, Piao W, Zhou Q, Vollmer TL, Campagnolo DI, Xiang R, La Cava A, Van Kaer L, Shi FD. Central nervous system (CNS)-resident natural killer cells suppress Th17 responses and CNS autoimmune pathology. J Exp Med. 2010;207(9):1907-21.
57. Zhang Z, Kaptanoglu L, Haddad W, Ivancic D, Alnadjim Z, Hurst S, Tishler D, Luster AD, Barrett TA, Fryer J. Donor T cell activation initiates small bowel allograft rejection through an IFN-gamma-inducible protein-10-dependent mechanism. J Immunol. 2002;168(7):3205-12.
58. Yoneda O, Imai T, Goda S, Inoue H, Yamauchi A, Okazaki T, Imai H, Yoshie O, Bloom ET, Domae N, Umehara H. Fractalkine-mediated endothelial cell injury by NK cells. J Immunol. 2000;164(8):4055-62.
59. Umehara H, Bloom E, Okazaki T, Domae N, Imai T. Fractalkine and vascular injury. Trends Immunol. 2001 Nov;22(11):602-7.
60. Ottaviani C, Nasorri F, Bedini C, de Pità O, Girolomoni G, Cavani A. CD56brightCD16(-) NK cells accumulate in psoriatic skin in response to CXCL10 and CCL5 and exacerbate skin inflammation. Eur J Immunol. 2006;36(1): 118-28.
61. Parolini S, Santoro A, Marcenaro E, Luini W, Massardi L, Facchetti F, Communi D, Parmentier M, Majorana A, Sironi M, Tabellini G, Moretta A, Sozzani S. Te role of chemerin in the colocalization of NK and dendritic cell subsets into infamed tissues. Blood. 2007 May 1;109(9):3625-32.
62. Skrzeczyńska-Moncznik J, Stefańska A, Zabel BA, Kapińska-Mrowiecka M, Butcher EC, Cichy J. Chemerin and the recruitment of NK cells to diseased skin. Acta Biochim Pol. 2009;56(2):355-60.
63. Huss RS, Huddleston JI, Goodman SB, Butcher EC, Zabel BA. Synovial tissue-infltrating natural killer cells in osteoarthritis and peri-prosthetic inflammation. Arthritis Rheum. 2010;62(12):3799-805.
64. Smyth MJ, Swann J, Cretney E, Zerafa N, Yokoyama WM, Hayakawa Y. NKG2D function protects the host from tumor initiation. J Exp Med. 2005; 202(5):583-8.
65. Chow MT, Sceneay J, Paget C, Wong CS, Duret H, Tschopp J, Möller A, Smyth MJ. NLRP3 suppresses NK cell-mediated responses to carcinogen-induced tumors and metastases. Cancer Res. 2012;72(22):5721-32.
66. Przewoznik M, Hömberg N, Naujoks M, Pötzl J, Münchmeier N, Brenner CD, Anz D, Bourquin C, Nelson PJ, Röcken M, Mocikat R. Recruitment of natural killer cells in advanced stages of endogenously arising B-cell lym-phoma: implications for therapeutic cell transfer. J Immunother. 2012;35(3):217-22.
67. Soria G, Yaal-Hahoshen N, Azenshtein E, Shina S, Leider-Trejo L, Ryvo L, Cohen-Hillel E, Shtabsky A, Ehrlich M, Meshel T, Keydar I, Ben-Baruch A. Concomitant expression of the chemokines RANTES and MCP-1 in human breast cancer:a basis for tumor-promoting interactions. Cytokine. 2008;44(1):191-200.
68. Conti I, Rollins BJ. CCL2 (monocyte chemoat-tractant protein-1) and cancer. Semin Cancer Biol. 2004;14(3):149-54.
69. Mantovani A, Allavena P, Sozzani S, Vecchi A, Locati M, Sica A. Chemokines in the recruitment and shaping of the leukocyte infltrate of tumors. Semin Cancer Biol. 2004;14:155-60.
70. Ben-Baruch A. Te tumor-promoting fow of cells into, within and out of the tumor site: regulation by the infammatory axis of TNFα and chemokines. Cancer Microenviron. 2012;5(2):151-64.
71. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10(9):942-9.
72. Ishida T, Ueda R. CCR4 as a novel molecular target for immunotherapy of cancer. Cancer Sci. 2006;97(11):1139-46.
73. Yang ZZ, Novak AJ, Stenson MJ, Witzig TE, Ansell SM. Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infltrating CD4+ T cells in B-cell non-Hodgkin lym-phoma. Blood. 2006 May 1;107(9):3639-46.
74. Mailloux AW, Young MR. NK-dependent increases in CCL22 secretion selectively recruits regulatory T cells to the tumor microenviron-ment. J Immunol. 2009;182(5):2753-65.
75. Mailloux AW, Clark AM, Young MR. NK depletion results in increased CCL22 secretion and Treg levels in Lewis lung carcinoma via the accumulation of CCL22-secreting CD11b+CD11c+ cells. Int J Cancer. 2010;127(11):2598-611.
76. Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, Möller A. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/ Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res. 2012;72(16):3906-11.
77. Olkhanud PB, Baatar D, Bodogai M, Hakim F, Gress R, Anderson RL, Deng J, Xu M, Briest S, Biragyn A. Breast cancer lung metastasis requires expression of chemokine receptor CCR4 and regulatory T cells. Cancer Res. 2009;69(14):5996-6004.
78. Ishida T, Joh T, Uike N, Yamamoto K, Utsunomiya A, Yoshida S, Saburi Y, Miyamoto T, Takemoto S, Suzushima H, Tsukasaki K, Nosaka K, Fujiwara H, Ishitsuka K, Inagaki H, Ogura M, Akinaga S, Tomonaga M, Tobinai K, Ueda R. Defucosylated anti-CCR4 monoclonal antibody (KW-0761) for relapsed adult T-cell leukemia-lymphoma: a multicenter phase II study. J Clin Oncol. 2012;30(8):837-42.
79. Ruggeri L, Capanni M, Casucci M, Volpi I, Tosti A, Perruccio K, Urbani E, Negrin RS, Martelli MF, Velardi A. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94(1):333-9.
80. Farag SS, Fehniger T, Ruggeri L, Velardi A, Caligiuri MA. Natural killer cells: biology and application in stem-cell transplantation. Cytotherapy. 2002;4(5):445-6.
81. Frohn C, Höppner M, Schlenke P, Kirchner H, Koritke P, Luhm J. Anti-myeloma activity of natural killer lymphocytes. Br J Haematol. 2002;119(3):660-4.
82. Locatelli F, Merli P, Rutella S. At the Bedside: Innate immunity as an immunotherapy tool for hematological malignancies. J Leukoc Biol. 2013;94(6):1141-57.
83. Alici E, Konstantinidis KV, Sutlu T, Aints A, Gahrton G, Ljunggren HG, Dilber MS. Anti-myeloma activity of endogenous and adoptively transferred activated natural killer cells in experimental multiple myeloma model. Exp Hematol. 2007;35(12):1839-46.
84. 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(6):2428-35.
85. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, Rimoldi M, Biswas SK, Allavena P, Mantovani A. Macrophage polarization in tumour progression. Semin Cancer Biol. 2008;18(5):349-355.
86. Mantovani A, Sica A Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010; 22:231-237.
87. Lode HN, Xiang R, Dreier T, Varki NM, Gillies SD, Reisfeld RA. Natural killer cell- mediated eradication of neuroblastoma metastases to bone marrow by targeted interleukin-2 therapy. Blood. 1998 Mar 1;91(5):1706-15.
88. Zeng Y, Huebener N, Fest S, Weixler S, Schroeder U, Gaedicke G, Xiang R, Schramm A, Eggert A, Reisfeld RA, Lode HN. Fractalkine (CX3CL1)- and interleukin-2-enriched neuroblastoma microenvironment induces eradication of metastases mediated by T cells and natural killer cells. Cancer Res. 2007;67(5):2331-8.
89. Pachynski RK, Zabel BA, Kohrt HE, Tejeda NM, Monnier J, Swanson CD, Holzer AK, Gentles AJ, Sperinde GV, Edalati A, Hadeiba HA, Alizadeh AA, Butcher EC. Te chemoat-tractant chemerin suppresses melanoma by recruiting natural killer cell antitumor defenses. J Exp Med. 2012;209(8):1427-35.
90. Keyser J, Schultz J, Ladell K, Elzaouk L, Heinzerling L, Pavlovic J, Moelling K. IP-10-encoding plasmid DNA therapy exhibits anti-tumor and anti-metastatic efciency. Exp Dermatol. 2004;13(6):380-90.
91. Tominaga M, Iwashita Y, Ohta M, Shibata K, Ishio T, Ohmori N, Goto T, Sato S, Kitano S. Antitumor efects of the MIG and IP-10 genes transferred with poly [D,L-2,4-diaminobutyric acid] on murine neuroblastoma. Cancer Gene Ter. 2007;14(8):696-705.
92. Zhang N, Yang Y, Cheng L, Zhang XM, Zhang S, Wang W, Liu SY, Wang SY, Wang RB, Xu WJ, Dai L, Yan N, Fan P, Dai LX, Tian HW, Liu L, Deng HX. Combination of Caspy2 and IP-10 gene therapy signifcantly improves therapeutic efcacy against murine malignant neoplasm growth and metastasis. Hum Gene Ter. 2012;23(8):837-46.
93. Fehniger TA, Shah MH, Turner MJ, VanDeusen JB, Whitman SP, Cooper MA, Suzuki K, Wechser M, Goodsaid F, Caligiuri MA. Diferential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol. 1999;162:4511-20.
94. Somersalo K, Carpen O, Saksela E. Stimulated natural killer cells secrete factors with chemo-tactic activity, including NAP-1/IL-8, which supports VLA-4- and VLA-5-mediated migration of T lymphocytes. Eur J Immunol. 1994;24:2957-65.
95. Roda JM, Parihar R, Magro C, Nuovo GJ, Tridandapani S, Carson WE. Natural killer cells produce T cell-recruiting chemokines in response to antibody-coated tumor cells. Cancer Res. 2006;66(1):517-26.
96. Roda JM, Joshi T, Butchar JP, McAlees JW, Lehman A, Tridandapani S, Carson WE. Te activation of natural killer cell efector functions by cetuximab coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines. Clin Cancer Res. 2007;13(21):6419-28.