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PMID: 27294158 Published · ppublish English Journal Article Review

NK Cells, Tumor Cell Transition, and Tumor Progression in Solid Malignancies: New Hints for NK-Based Immunotherapy?

Journal of immunology research ·Vol. 2016 ·2016-00-00 ·Pages 4684268

Cantoni C, Huergo-Zapico L, Parodi M, Pedrazzi M, Mingari MC, Moretta A, Sparatore B, Gonzalez S, Olive D, Bottino C, Castriconi R, Vitale M

Abstract

Several evidences suggest that NK cells can patrol the body and eliminate tumors in their initial phases but may hardly control established solid tumors. Multiple factors, including the transition of tumor cells towards a proinvasive/prometastatic phenotype, the immunosuppressive effect of the tumor microenvironment, and the tumor structure complexity, may account for limited NK cell efficacy. Several putative mechanisms of NK cell suppression have been defined in these last years; conversely, the cross talk between NK cells and tumor cells undergoing different transitional phases remains poorly explored. Nevertheless, recent in vitro studies and immunohistochemical analyses on tumor biopsies suggest that NK cells could not only kill tumor cells but also influence their evolution. Indeed, NK cells may induce tumor cells to change the expression of HLA-I, PD-L1, or NKG2D-L and modulate their susceptibility to the immune response. Moreover, NK cells may be preferentially located in the borders of tumor masses, where, indeed, tumor cells can undergo Epithelial-to-Mesenchymal Transition (EMT) acquiring prometastatic phenotype. Finally, the recently highlighted role of HMGB1 both in EMT and in amplifying the recruitment of NK cells provides further hints on a possible effect of NK cells on tumor progression and fosters new studies on this issue.

MeSH Terms
Animals B7-H1 Antigen/metabolism Cytotoxicity, Immunologic Disease Progression Epithelial-Mesenchymal Transition/immunology HLA Antigens/metabolism HMGB1 Protein/physiology Humans Immune Tolerance Immunotherapy Killer Cells, Natural/chemistry,immunology NK Cell Lectin-Like Receptor Subfamily K/metabolism Neoplasm Metastasis/prevention & control Neoplasms/immunology,physiopathology,therapy Tumor Microenvironment/immunology
Chemicals
B7-H1 Antigen CD274 protein, human HLA Antigens HMGB1 Protein HMGB1 protein, human KLRK1 protein, human NK Cell Lectin-Like Receptor Subfamily K
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Cantoni Claudia ORCID
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Center of Excellence for Biomedical Research (CEBR), University of Genoa, 16132 Genova, Italy; Istituto Giannina Gaslini, 16147 Genova, Italy.
Huergo-Zapico Leticia
IRCCS AOU San Martino-IST, 16132 Genova, Italy.
Parodi Monica
IRCCS AOU San Martino-IST, 16132 Genova, Italy.
Pedrazzi Marco
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy.
Mingari Maria Cristina
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Center of Excellence for Biomedical Research (CEBR), University of Genoa, 16132 Genova, Italy; IRCCS AOU San Martino-IST, 16132 Genova, Italy.
Moretta Alessandro ORCID
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Center of Excellence for Biomedical Research (CEBR), University of Genoa, 16132 Genova, Italy.
Sparatore Bianca
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Center of Excellence for Biomedical Research (CEBR), University of Genoa, 16132 Genova, Italy.
Gonzalez Segundo
Department of Functional Biology, IUOPA, University of Oviedo, 33006 Oviedo, Spain.
Olive Daniel
U1068, CRCM, Immunity and Cancer, INSERM, 1312 Marseille, France.
Bottino Cristina
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Istituto Giannina Gaslini, 16147 Genova, Italy.
Castriconi Roberta ORCID
Department of Experimental Medicine (DIMES), University of Genoa, 16132 Genova, Italy; Center of Excellence for Biomedical Research (CEBR), University of Genoa, 16132 Genova, Italy.
Vitale Massimo ORCID
IRCCS AOU San Martino-IST, 16132 Genova, Italy.
References (163)
163 references, click to expand
  1. Interferon-γ-induced activation of JAK1 and JAK2 suppresses tumor cell susceptibility to NK cells through upregulation of PD-L1 expression.
    Oncoimmunology. 2015 Mar 2;4(6):e1008824 PMID: 26155422
  2. Regulatory networks defining EMT during cancer initiation and progression.
    Nat Rev Cancer. 2013 Feb;13(2):97-110 PMID: 23344542
  3. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion.
    EMBO J. 2003 Oct 15;22(20):5551-60 PMID: 14532127
  4. Overexpression of high-mobility group box 1 correlates with tumor progression and poor prognosis in human colorectal carcinoma.
    J Cancer Res Clin Oncol. 2010 May;136(5):677-84 PMID: 19898867
  5. TGF-β and EGF induced HLA-I downregulation is associated with epithelial-mesenchymal transition (EMT) through upregulation of snail in prostate cancer cells.
    Mol Immunol. 2015 May;65(1):34-42 PMID: 25618241
  6. Role of chemokines in the biology of natural killer cells.
    J Leukoc Biol. 2002 Feb;71(2):173-83 PMID: 11818437
  7. Human NK Cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism.
    J Immunol. 2012 Feb 15;188(4):1668-74 PMID: 22231698
  8. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire.
    J Immunol. 2001 Jun 1;166(11):6477-82 PMID: 11359797
  9. Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1).
    Mol Med. 2012 Mar 30;18:250-9 PMID: 22105604
  10. Low natural cytotoxicity of peripheral blood mononuclear cells in individuals with high familial incidences of cancer.
    Cancer Res. 1984 Jan;44(1):370-4 PMID: 6690050
  11. The chemoattractant chemerin suppresses melanoma by recruiting natural killer cell antitumor defenses.
    J Exp Med. 2012 Jul 30;209(8):1427-35 PMID: 22753924
  12. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues.
    Blood. 2007 May 1;109(9):3625-32 PMID: 17202316
  13. Natural killer cells and neuroblastoma: tumor recognition, escape mechanisms, and possible novel immunotherapeutic approaches.
    Front Immunol. 2014 Feb 12;5:56 PMID: 24575100
  14. Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages.
    J Immunol. 2008 Oct 1;181(7):5015-23 PMID: 18802105
  15. Natural killer cells are scarce in colorectal carcinoma tissue despite high levels of chemokines and cytokines.
    Clin Cancer Res. 2011 Feb 15;17(4):678-89 PMID: 21325295
  16. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education.
    Blood. 2010 Nov 11;116(19):3853-64 PMID: 20696944
  17. Immunoediting of cancers may lead to epithelial to mesenchymal transition.
    J Immunol. 2006 Aug 1;177(3):1526-33 PMID: 16849459
  18. High-mobility group box 1 activates caspase-1 and promotes hepatocellular carcinoma invasiveness and metastases.
    Hepatology. 2012 Jun;55(6):1863-75 PMID: 22234969
  19. M2-polarized tumor-associated macrophages promoted epithelial-mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway.
    Lab Invest. 2013 Jul;93(7):844-54 PMID: 23752129
  20. TLR activation of tumor-associated macrophages from ovarian cancer patients triggers cytolytic activity of NK cells.
    Eur J Immunol. 2014 Jun;44(6):1814-22 PMID: 24510590
  21. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands.
    Cancer Res. 2008 Oct 15;68(20):8437-45 PMID: 18922917
  22. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin.
    J Leukoc Biol. 2007 Jan;81(1):59-66 PMID: 16966386
  23. Natural killer cells infiltrating colorectal cancer and MHC class I expression.
    Mol Immunol. 2005 Feb;42(4):541-6 PMID: 15607811
  24. Inherent and Tumor-Driven Immune Tolerance in the Prostate Microenvironment Impairs Natural Killer Cell Antitumor Activity.
    Cancer Res. 2016 Apr 15;76(8):2153-65 PMID: 27197252
  25. NMDA receptors in immune competent cells.
    Biochemistry (Mosc). 2012 Feb;77(2):128-34 PMID: 22348471
  26. Evaluation of in vitro properties of predicted kinases that phosphorylate serine residues within nuclear localization signal 1 of high mobility group box 1.
    J Pept Sci. 2014 Aug;20(8):613-7 PMID: 24863048
  27. Epithelial-mesenchymal plasticity in carcinoma metastasis.
    Genes Dev. 2013 Oct 15;27(20):2192-206 PMID: 24142872
  28. The SLUG zinc-finger protein represses E-cadherin in breast cancer.
    Cancer Res. 2002 Mar 15;62(6):1613-8 PMID: 11912130
  29. TLR/NCR/KIR: Which One to Use and When?
    Front Immunol. 2014 Mar 19;5:105 PMID: 24678311
  30. IL-2 and IL-12 alter NK cell responsiveness to IFN-gamma-inducible protein 10 by down-regulating CXCR3 expression.
    J Immunol. 2002 Jun 15;168(12):6090-8 PMID: 12055219
  31. Myeloid-derived suppressor cells in the tumor microenvironment: expect the unexpected.
    J Clin Invest. 2015 Sep;125(9):3356-64 PMID: 26168215
  32. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells.
    Cancer Cell. 2009 Mar 3;15(3):195-206 PMID: 19249678
  33. Cutting edge: extracellular high mobility group box-1 protein is a proangiogenic cytokine.
    J Immunol. 2006 Jan 1;176(1):12-5 PMID: 16365390
  34. High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts.
    Arthritis Res Ther. 2011 Aug 26;13(4):R136 PMID: 21871094
  35. Development of human natural killer cells and other innate lymphoid cells.
    Semin Immunol. 2014 Apr;26(2):107-13 PMID: 24559836
  36. Poly(ADP-ribosyl)ation of high mobility group box 1 (HMGB1) protein enhances inhibition of efferocytosis.
    Mol Med. 2012 May 09;18:359-69 PMID: 22204001
  37. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits.
    Nat Rev Cancer. 2009 Apr;9(4):265-73 PMID: 19262571
  38. Role of HMGB1 in apoptosis-mediated sepsis lethality.
    J Exp Med. 2006 Jul 10;203(7):1637-42 PMID: 16818669
  39. Tumour heterogeneity and cancer cell plasticity.
    Nature. 2013 Sep 19;501(7467):328-37 PMID: 24048065
  40. The effect of HMGB1, a damage-associated molecular pattern molecule, on polymorphonuclear neutrophil migration depends on its concentration.
    J Innate Immun. 2012;4(1):41-58 PMID: 21860212
  41. Epithelial-mesenchymal transitions in development and disease.
    Cell. 2009 Nov 25;139(5):871-90 PMID: 19945376
  42. Regulation of cutaneous malignancy by gammadelta T cells.
    Science. 2001 Oct 19;294(5542):605-9 PMID: 11567106
  43. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis.
    Cell. 2004 Jun 25;117(7):927-39 PMID: 15210113
  44. Natural Killer (NK)/melanoma cell interaction induces NK-mediated release of chemotactic High Mobility Group Box-1 (HMGB1) capable of amplifying NK cell recruitment.
    Oncoimmunology. 2015 May 29;4(12):e1052353 PMID: 26587323
  45. Natural killer cell memory in infection, inflammation and cancer.
    Nat Rev Immunol. 2016 Feb;16(2):112-23 PMID: 26806484
  46. Chemokines and NK cells: regulators of development, trafficking and functions.
    Immunol Lett. 2012 Jul 30;145(1-2):39-46 PMID: 22698182
  47. In vivo natural killer cell activities revealed by natural killer cell-deficient mice.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2731-6 PMID: 10694580
  48. Regulation of HMGB1 release by autophagy.
    Autophagy. 2009 Feb;5(2):247-9 PMID: 19098461
  49. Natural killer cells and solid tumors.
    J Innate Immun. 2011;3(4):355-64 PMID: 21502747
  50. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma.
    Int Immunol. 2001 Apr;13(4):459-63 PMID: 11282985
  51. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1.
    Nat Immunol. 2012 Sep;13(9):832-42 PMID: 22842346
  52. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells.
    Oncogene. 2010 Sep 23;29(38):5299-310 PMID: 20622903
  53. Potentiation of NMDA receptor-dependent cell responses by extracellular high mobility group box 1 protein.
    PLoS One. 2012;7(8):e44518 PMID: 22952988
  54. MED12 controls the response to multiple cancer drugs through regulation of TGF-β receptor signaling.
    Cell. 2012 Nov 21;151(5):937-50 PMID: 23178117
  55. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity.
    J Clin Invest. 2011 Sep;121(9):3609-22 PMID: 21841316
  56. The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression.
    Immunol Rev. 2006 Dec;214:229-38 PMID: 17100888
  57. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset.
    Blood. 2010 Nov 11;116(19):3865-74 PMID: 20733159
  58. Early liaisons between cells of the innate immune system in inflamed peripheral tissues.
    Trends Immunol. 2005 Dec;26(12):668-75 PMID: 16198147
  59. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity.
    Cancer Res. 2012 Mar 15;72(6):1407-15 PMID: 22258454
  60. HMG1 and 2, and related 'architectural' DNA-binding proteins.
    Trends Biochem Sci. 2001 Mar;26(3):167-74 PMID: 11246022
  61. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release.
    Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11942-7 PMID: 20547845
  62. Gelatinase A (MMP-2), collagenase-2 (MMP-8), and laminin-5 gamma2-chain expression in murine inflammatory bowel disease (ulcerative colitis).
    Dig Dis Sci. 2003 Jan;48(1):93-8 PMID: 12645796
  63. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release.
    J Exp Med. 2012 Aug 27;209(9):1519-28 PMID: 22869893
  64. Interaction between uric acid and HMGB1 translocation and release from endothelial cells.
    Am J Physiol Renal Physiol. 2012 Mar 15;302(6):F730-41 PMID: 22189943
  65. Epithelial-mesenchymal transition induces an antitumor immune response mediated by NKG2D receptor.
    J Immunol. 2013 Apr 15;190(8):4408-19 PMID: 23509364
  66. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity.
    Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20847-52 PMID: 19934056
  67. Post-translational methylation of high mobility group box 1 (HMGB1) causes its cytoplasmic localization in neutrophils.
    J Biol Chem. 2007 Jun 1;282(22):16336-44 PMID: 17403684
  68. High mobility group box-1 is phosphorylated by protein kinase C zeta and secreted in colon cancer cells.
    Biochem Biophys Res Commun. 2012 Jul 27;424(2):321-6 PMID: 22750245
  69. NK cells and the tumour microenvironment: implications for NK-cell function and anti-tumour activity.
    Trends Immunol. 2003 Nov;24(11):603-9 PMID: 14596885
  70. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor.
    Hepatology. 2009 Sep;50(3):799-807 PMID: 19551844
  71. High-mobility group box 1-mediated matrix metalloproteinase-9 expression in non-small cell lung cancer contributes to tumor cell invasiveness.
    Am J Respir Cell Mol Biol. 2010 Nov;43(5):530-8 PMID: 19933377
  72. DNA alkylating therapy induces tumor regression through an HMGB1-mediated activation of innate immunity.
    J Immunol. 2011 Mar 15;186(6):3517-26 PMID: 21300822
  73. Neutrophil Granulocytes in Ovarian Cancer - Induction of Epithelial-To-Mesenchymal-Transition and Tumor Cell Migration.
    J Cancer. 2016 Mar 10;7(5):546-54 PMID: 27053953
  74. Analysis of nuclear high mobility group box 1 (HMGB1)-binding proteins in colon cancer cells: clustering with proteins involved in secretion and extranuclear function.
    J Proteome Res. 2010 Sep 3;9(9):4661-70 PMID: 20812762
  75. IL-18-induced CD83+CCR7+ NK helper cells.
    J Exp Med. 2005 Oct 3;202(7):941-53 PMID: 16203865
  76. NK cells infiltrating a MHC class I-deficient lung adenocarcinoma display impaired cytotoxic activity toward autologous tumor cells associated with altered NK cell-triggering receptors.
    J Immunol. 2005 Nov 1;175(9):5790-8 PMID: 16237071
  77. New views on natural killer cell-based immunotherapy for melanoma treatment.
    Trends Immunol. 2010 Sep;31(9):339-45 PMID: 20655806
  78. High-mobility group box 1: a novel inducer of the epithelial-mesenchymal transition in colorectal carcinoma.
    Cancer Lett. 2015 Feb 28;357(2):527-34 PMID: 25511739
  79. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression.
    Nat Cell Biol. 2000 Feb;2(2):76-83 PMID: 10655586
  80. Mature cytotoxic CD56(bright)/CD16(+) natural killer cells can infiltrate lymph nodes adjacent to metastatic melanoma.
    Cancer Res. 2014 Jan 1;74(1):81-92 PMID: 24225017
  81. PD-L1 expression in metastatic neuroblastoma as an additional mechanism for limiting immune surveillance.
    Oncoimmunology. 2015 Jul 15;5(1):e1064578 PMID: 26942080
  82. The blockade of immune checkpoints in cancer immunotherapy.
    Nat Rev Cancer. 2012 Mar 22;12(4):252-64 PMID: 22437870
  83. Differential Expression of Immune-Regulatory Genes Associated with PD-L1 Display in Melanoma: Implications for PD-1 Pathway Blockade.
    Clin Cancer Res. 2015 Sep 1;21(17):3969-76 PMID: 25944800
  84. Molecular Bases for the Regulation of NKG2D Ligands in Cancer.
    Front Immunol. 2014 Mar 21;5:106 PMID: 24711808
  85. Human innate lymphoid cells.
    Immunol Lett. 2016 Nov;179:2-8 PMID: 26844414
  86. Directed phenotype switching as an effective antimelanoma strategy.
    Cancer Cell. 2013 Jul 8;24(1):105-19 PMID: 23792190
  87. Epithelial-to-mesenchymal transition (EMT) induced by inflammatory priming elicits mesenchymal stromal cell-like immune-modulatory properties in cancer cells.
    Br J Cancer. 2015 Mar 17;112(6):1067-75 PMID: 25668006
  88. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4.
    J Exp Med. 2012 Mar 12;209(3):551-63 PMID: 22370717
  89. Innate or adaptive immunity? The example of natural killer cells.
    Science. 2011 Jan 7;331(6013):44-9 PMID: 21212348
  90. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors.
    Cancer Res. 2013 Jun 15;73(12):3499-510 PMID: 23592754
  91. Phenotype switching: tumor cell plasticity as a resistance mechanism and target for therapy.
    Cancer Res. 2014 Nov 1;74(21):5937-41 PMID: 25320006
  92. The IKKα-dependent NF-κB p52/RelB noncanonical pathway is essential to sustain a CXCL12 autocrine loop in cells migrating in response to HMGB1.
    J Immunol. 2012 Mar 1;188(5):2380-6 PMID: 22287708
  93. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4120-5 PMID: 12646700
  94. Melanoma cells become resistant to NK-cell-mediated killing when exposed to NK-cell numbers compatible with NK-cell infiltration in the tumor.
    Eur J Immunol. 2012 Jul;42(7):1833-42 PMID: 22585684
  95. High-throughput proteomics reveal alarmins as amplifiers of tissue pathology and inflammation after spinal cord injury.
    Sci Rep. 2016 Feb 22;6:21607 PMID: 26899371
  96. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation.
    J Leukoc Biol. 2009 Sep;86(3):655-62 PMID: 19564572
  97. Inhibition of interleukin-8 (CXCL8/IL-8) responses by repertaxin, a new inhibitor of the chemokine receptors CXCR1 and CXCR2.
    Biochem Pharmacol. 2005 Feb 1;69(3):385-94 PMID: 15652230
  98. High mobility group box protein 1 (HMGB1)-partner molecule complexes enhance cytokine production by signaling through the partner molecule receptor.
    Mol Med. 2012 Mar 27;18:224-30 PMID: 22076468
  99. HMGB1 attenuates anti-metastatic defense of the lymph nodes in colorectal cancer.
    Pathobiology. 2010;77(1):17-23 PMID: 20185963
  100. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein.
    Immunity. 2008 Jul 18;29(1):21-32 PMID: 18631454
  101. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population.
    Lancet. 2000 Nov 25;356(9244):1795-9 PMID: 11117911
  102. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo.
    J Clin Invest. 2009 May;119(5):1251-63 PMID: 19349689
  103. Metalloprotease-mediated tumor cell shedding of B7-H6, the ligand of the natural killer cell-activating receptor NKp30.
    Cancer Res. 2014 Jul 1;74(13):3429-40 PMID: 24780758
  104. Hypoxia downregulates the expression of activating receptors involved in NK-cell-mediated target cell killing without affecting ADCC.
    Eur J Immunol. 2013 Oct;43(10 ):2756-64 PMID: 23913266
  105. Increased expression of HMGB1 is associated with poor prognosis in human bladder cancer.
    J Surg Oncol. 2012 Jul 1;106(1):57-61 PMID: 22237993
  106. Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor.
    PLoS Biol. 2011 Sep;9(9):e1001162 PMID: 21980263
  107. Sorafenib perpetuates cellular anticancer effector functions by modulating the crosstalk between macrophages and natural killer cells.
    Hepatology. 2013 Jun;57(6):2358-68 PMID: 23424039
  108. HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism.
    J Immunol. 2009 May 1;182(9):5800-9 PMID: 19380828
  109. Expression and regulation of chemokine receptors in human natural killer cells.
    Blood. 2001 Jan 15;97(2):367-75 PMID: 11154210
  110. The association of HMGB1 expression with clinicopathological significance and prognosis in hepatocellular carcinoma: a meta-analysis and literature review.
    PLoS One. 2014 Oct 30;9(10):e110626 PMID: 25356587
  111. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10116-21 PMID: 15218108
  112. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma.
    Int Immunol. 2008 Apr;20(4):631 PMID: 18334503
  113. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation.
    Proc Natl Acad Sci U S A. 2014 Feb 25;111(8):3068-73 PMID: 24469805
  114. Prognostic value of HMGB1 overexpression in resectable gastric adenocarcinomas.
    World J Surg Oncol. 2010 Jun 26;8:52 PMID: 20579387
  115. Effect of tumor cells and tumor microenvironment on NK-cell function.
    Eur J Immunol. 2014 Jun;44(6):1582-92 PMID: 24777896
  116. Dissecting CD56dim human NK cells.
    Blood. 2010 Nov 11;116(19):3689-91 PMID: 21071612
  117. Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells.
    EMBO J. 2008 Jun 18;27(12 ):1671-81 PMID: 18511911
  118. HMGB1 in cancer: good, bad, or both?
    Clin Cancer Res. 2013 Aug 1;19(15):4046-57 PMID: 23723299
  119. Altered phenotype in peripheral blood and tumor-associated NK cells from colorectal cancer patients.
    Innate Immun. 2013 Feb;19(1):76-85 PMID: 22781631
  120. Dysregulated Tim-3 expression on natural killer cells is associated with increased Galectin-9 levels in HIV-1 infection.
    Retrovirology. 2013 Jul 18;10 :74 PMID: 23866914
  121. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph.
    J Immunol. 2014 Apr 15;192(8):3805-15 PMID: 24646734
  122. miR-200b mediates post-transcriptional repression of ZFHX1B.
    RNA. 2007 Aug;13(8):1172-8 PMID: 17585049
  123. Murine B16 melanomas expressing high levels of the chemokine stromal-derived factor-1/CXCL12 induce tumor-specific T cell chemorepulsion and escape from immune control.
    J Immunol. 2006 Mar 1;176(5):2902-14 PMID: 16493048
  124. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1.
    Nat Cell Biol. 2008 May;10 (5):593-601 PMID: 18376396
  125. HMG-1 as a late mediator of endotoxin lethality in mice.
    Science. 1999 Jul 9;285(5425):248-51 PMID: 10398600
  126. The biology of human natural killer-cell subsets.
    Trends Immunol. 2001 Nov;22(11):633-40 PMID: 11698225
  127. Expression of stress-induced MHC class I related chain molecules on human melanoma.
    J Invest Dermatol. 2002 Apr;118(4):600-5 PMID: 11918705
  128. Innate lymphoid cells--a proposal for uniform nomenclature.
    Nat Rev Immunol. 2013 Feb;13(2):145-9 PMID: 23348417
  129. Complex networks orchestrate epithelial-mesenchymal transitions.
    Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42 PMID: 16493418
  130. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors.
    Nat Med. 2011 Jun;17(6):700-7 PMID: 21552268
  131. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors.
    J Cell Sci. 2003 Feb 1;116(Pt 3):499-511 PMID: 12508111
  132. Regulation of human NK-cell cytokine and chemokine production by target cell recognition.
    Blood. 2010 Mar 18;115(11):2167-76 PMID: 19965656
  133. Neuroblastoma-derived TGF-β1 modulates the chemokine receptor repertoire of human resting NK cells.
    J Immunol. 2013 May 15;190(10):5321-8 PMID: 23576682
  134. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion.
    Mol Cell. 2001 Jun;7(6):1267-78 PMID: 11430829
  135. Enrichment of CD56(dim)KIR + CD57 + highly cytotoxic NK cells in tumour-infiltrated lymph nodes of melanoma patients.
    Nat Commun. 2014 Dec 04;5:5639 PMID: 25472612
  136. The three Es of cancer immunoediting.
    Annu Rev Immunol. 2004;22:329-60 PMID: 15032581
  137. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma.
    Cancer Res. 2011 Aug 15;71(16):5412-22 PMID: 21708957
  138. HMGB1: The Central Cytokine for All Lymphoid Cells.
    Front Immunol. 2013 Mar 20;4:68 PMID: 23519706
  139. IL-15 and IL-2 oppositely regulate expression of the chemokine receptor CX3CR1.
    Blood. 2003 Nov 15;102(10):3494-503 PMID: 12881312
  140. Matrix metalloproteinase-7-catalyzed release of HB-EGF mediates deoxycholyltaurine-induced proliferation of a human colon cancer cell line.
    Biochem Pharmacol. 2007 Apr 1;73(7):1001-12 PMID: 17222808
  141. Different checkpoints in human NK-cell activation.
    Trends Immunol. 2004 Dec;25(12):670-6 PMID: 15530838
  142. Neuroblastoma: developmental biology, cancer genomics and immunotherapy.
    Nat Rev Cancer. 2013 Jun;13(6):397-411 PMID: 23702928
  143. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape.
    Sci Transl Med. 2012 Mar 28;4(127):127ra37 PMID: 22461641
  144. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity.
    Immunol Rev. 2007 Dec;220:60-81 PMID: 17979840
  145. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells.
    Cancer. 2008 Feb 15;112(4):863-75 PMID: 18203207
  146. Phenotype switching in melanoma: implications for progression and therapy.
    Front Oncol. 2015 Feb 13;5:31 PMID: 25763355
  147. HER-2/neu antigen loss and relapse of mammary carcinoma are actively induced by T cell-mediated anti-tumor immune responses.
    Eur J Immunol. 2007 Mar;37(3):675-85 PMID: 17304628
  148. HMGB1 is overexpressed in tumor cells and promotes activity of regulatory T cells in patients with head and neck cancer.
    Oral Oncol. 2012 May;48(5):409-16 PMID: 22265157
  149. The speed of change: towards a discontinuity theory of immunity?
    Nat Rev Immunol. 2013 Oct;13(10 ):764-9 PMID: 23995627
  150. Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression.
    Nat Commun. 2014 Oct 28;5:5241 PMID: 25348003
  151. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin.
    Clin Cancer Res. 2013 Aug 1;19(15):4079-91 PMID: 23785047
  152. Overexpression of HMGB1 in melanoma predicts patient survival and suppression of HMGB1 induces cell cycle arrest and senescence in association with p21 (Waf1/Cip1) up-regulation via a p53-independent, Sp1-dependent pathway.
    Oncotarget. 2014 Aug 15;5(15):6387-403 PMID: 25051367
  153. In vivo switching of human melanoma cells between proliferative and invasive states.
    Cancer Res. 2008 Feb 1;68(3):650-6 PMID: 18245463
  154. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma.
    Cancer Res. 2012 Mar 1;72(5):1070-80 PMID: 22266112
  155. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming.
    Nat Immunol. 2004 Dec;5(12):1260-5 PMID: 15531883
  156. Human gingival fibroblasts release high-mobility group box-1 protein through active and passive pathways.
    Oral Microbiol Immunol. 2009 Aug;24(4):292-8 PMID: 19572890
  157. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function.
    Blood. 2006 Dec 15;108(13):4118-25 PMID: 16902152
  158. Tumor angiogenesis is enforced by autocrine regulation of high-mobility group box 1.
    Oncogene. 2013 Jan 17;32(3):363-74 PMID: 22391561
  159. Accessories to the crime: functions of cells recruited to the tumor microenvironment.
    Cancer Cell. 2012 Mar 20;21(3):309-22 PMID: 22439926
  160. Co-expression of RAGE and HMGB1 is associated with cancer progression and poor patient outcome of prostate cancer.
    Am J Cancer Res. 2014 Jul 16;4(4):369-77 PMID: 25057439
  161. Malignant and non-malignant lung tissue areas are differentially populated by natural killer cells and regulatory T cells in non-small cell lung cancer.
    Lung Cancer. 2008 Jan;59(1):32-40 PMID: 17825949
  162. Melanoma cells inhibit NK cell functions.
    Cancer Res. 2012 Oct 15;72(20):5428-9; author reply 5430 PMID: 23047870
  163. Laminin-5 with transforming growth factor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma.
    Gastroenterology. 2005 Nov;129(5):1375-83 PMID: 16285938
Article Info
Journal
Journal of immunology research
Abbr.
J Immunol Res
ISSN
2314-7156
DOI
10.1155/2016/4684268
Published
2016-00-00
Epub
2016-00-12
Pages
4684268
Language
English
Region
Egypt
NLM ID
101627166
PMCID
PMC4880686
Subset
IM
External Links
PubMed source DOI: 10.1155/2016/4684268 PMC Full Text View journal details
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