Perturbation of NK cell peripheral homeostasis accelerates prostate carcinoma metastasis

Journal of Clinical Investigation

Volumn 123, Issue 10, 2013, Pages 4410-4422

  Liu, Gang ^a   Lu, Shengjun ^b   Wang, Xuanjun ^a,c   Page, Stephanie T ^a   Higano, Celestia S ^a   Plymate, Stephen R ^a   Greenberg, Norman M ^d,e   Sun, Shaoli ^b   Li, Zihai ^b   Wu, Jennifer D ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c YUNNAN AGRICULTURAL UNIVERSITY   (China)

^d Fred Hutchinson Cancer Research Center   (United States)

^e MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D; HLA ANTIGEN CLASS 1; MICB ANTIGEN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INCIDENCE; CANCER PATIENT; CANCER SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; HISTOPATHOLOGY; HOMEOSTASIS; HUMAN; HUMAN CELL; MALE; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATE CARCINOMA; PROTEIN BLOOD LEVEL; TRANSGENIC MOUSE; TUMOR GROWTH; ANIMAL; BLOOD; BONE TUMOR; C57BL MOUSE; CANCER TRANSPLANTATION; CARCINOMA; CELL PROLIFERATION; IMMUNOLOGY; LIVER TUMOR; LUNG TUMOR; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; SECONDARY; TUMOR CELL LINE;

AGED; ANIMALS; BONE NEOPLASMS; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOMEOSTASIS; HUMANS; KILLER CELLS, NATURAL; LIVER NEOPLASMS; LUNG NEOPLASMS; LYMPHATIC METASTASIS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; NEOPLASM TRANSPLANTATION; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PROSTATIC NEOPLASMS;

EID: 84885080167     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69369     Document Type: Article

References (53)

1. Long EO. Versatile signaling through NKG2D. Nat Immunol. 2002;3(12):1119-1120.
2. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol. 2003;3(10):781-790.
3. Bauer S, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285(5428):727-729.
4. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol. 2001;2(3):255-260.
5. Wu J, Groh V, Spies T. T cell antigen receptor engagement and specificity in the recognition of stress-inducible MHC class I-related chains by human epithelial gamma delta T cells. J Immunol. 2002;169(3):1236-1240.
6. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature. 2001;413(6852):165-171.
7. Cerwenka A, Baron JL, Lanier LL. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci U S A. 2001;98(20):11521-11526.
8. 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):583-588.
9. Guerra N, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity. 2008;28(4):571-580.
10. Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene. 2008;27(45):5944-5958.
11. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A. 1999;96(12):6879-6884.
12. Coudert JD, et al. Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood. 2005;106(5):1711-1717.
13. Holdenrieder S, Stieber P, Peterfi A, Nagel D, Steinle A, Salih HR. Soluble MICB in malignant diseases: analysis of diagnostic significance and correlation with soluble MICA. Cancer Immunol Immunother. 2006;55(12):1584-1589.
14. Holdenrieder S, Stieber P, Peterfi A, Nagel D, Steinle A, Salih HR. Soluble MICA in malignant diseases. Int J Cancer. 2006;118(3):684-687.
15. Oppenheim DE, et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol. 2005;6(9):928-937.
16. Raffaghello L, et al. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia. 2004;6(5):558-568.
17. Salih HR, et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102(4):1389-1396.
18. Salih HR, Goehlsdorf D, Steinle A. Release of MICB molecules by tumor cells: mechanism and soluble MICB in sera of cancer patients. Hum Immunol. 2006;67(3):188-195.
19. Wiemann K, et al. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J Immunol. 2005;175(2):720-729.
20. McGilvray RW, Eagle RA, Rolland P, Jafferji I, Trowsdale J, Durrant LG. ULBP2 and RAET1E NKG2D ligands are independent predictors of poor prognosis in ovarian cancer patients. Int J Cancer. 2010;127(6):1412-1420.
21. Madjd Z, et al. Upregulation of MICA on highgrade invasive operable breast carcinoma. Cancer Immun. 2007;7:17.
22. Watson NF, et al. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int J Cancer. 2006;118(6):1445-1452.
23. McGilvray RW, et al. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res. 2009;15(22):6993-7002.
24. de Kruijf EM, et al. NKG2D ligand tumor expression and association with clinical outcome in early breast cancer patients: an observational study. BMC Cancer. 2012;12:24.
25. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 2002;419(6908):734-738.
26. Jinushi M, et al. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc Natl Acad Sci U S A. 2008;105(4):1285-1290.
27. Tamaki S, et al. Soluble MICB serum levels correlate with disease stage and survival rate in patients with oral squamous cell carcinoma. Anticancer Res. 2010;30(10):4097-4101.
28. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Invest. 2004;114(4):560-568.
29. Rebmann V, et al. Soluble MICA as an independent prognostic factor for the overall survival and progression-free survival of multiple myeloma patients. Clin Immunol. 2007;123(1):114-120.
30. Hayakawa Y. Targeting NKG2D in tumor surveillance. Expert Opin Ther Targets. 2012;16(6):587-599.
31. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev. 2010;235(1):267-285.
32. Friese MA, et al. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res. 2003;63(24):8996-9006.
33. Wu JD, Atteridge CL, Wang X, Seya T, Plymate SR. Obstructing shedding of the immunostimulatory MHC class I chain-related gene B prevents tumor formation. Clin Cancer Res. 2009;15(2):632-640.
34. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nature Immunol. 2000;1(2):119-126.
35. Greenberg NM, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A. 1995;92(8):3439-3443.
36. Wang X, Lundgren AD, Singh P, Goodlett DR, Plymate SR, Wu JD. An six-amino acid motif in the alpha3 domain of MICA is the cancer therapeutic target to inhibit shedding. Biochem Biophys Res Commun. 2009;387(3):476-481.
37. Gingrich JR, Barrios RJ, Foster BA, Greenberg NM. Pathologic progression of autochthonous prostate cancer in the TRAMP model. Prostate Cancer Prostatic Dis. 1999;2(2):70-75.
38. Kaplan-Lefko PJ, et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003;55(3):219-237.
39. Anderson MJ, Shafer-Weaver K, Greenberg NM, Hurwitz AA. Tolerization of tumor-specific T cells despite efficient initial priming in a primary murine model of prostate cancer. J Immunol. 2007;178(3):1268-1276.
40. Bai A, Higham E, Eisen HN, Wittrup KD, Chen J. Rapid tolerization of virus-activated tumor-specific CD8+ T cells in prostate tumors of TRAMP mice. Proc Natl Acad Sci U S A. 2008;105(35):13003-13008.
41. Ren C, et al. Cancer gene therapy using mesenchymal stem cells expressing interferon-beta in a mouse prostate cancer lung metastasis model. Gene Ther. 2008;15(21):1446-1453.
42. Varghese S, Rabkin SD, Liu R, Nielsen PG, Ipe T, Martuza RL. Enhanced therapeutic efficacy of IL-12, but not GM-CSF, expressing oncolytic herpes simplex virus for transgenic mouse derived prostate cancers. Cancer Gene Ther. 2006;13(3):253-265.
43. Holdenrieder S, et al. Soluble NKG2D ligands in hepatic autoimmune diseases and in benign diseases involved in marker metabolism. Anticancer Res. 2007;27(4A):2041-2045.
44. Doubrovina ES, et al. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol. 2003;171(12):6891-6899.
45. Suzuki Y, et al. MUC1 carrying core 2 O-glycans functions as a molecular shield against NK cell attack, promoting bladder tumor metastasis. Int J Oncol. 2012;40(6):1831-1838.
46. Galon J, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313(5795):1960-1964.
47. Gulubova M, Manolova I, Kyurkchiev D, Julianov A, Altunkova I. Decrease in intrahepatic CD56+ lymphocytes in gastric and colorectal cancer patients with liver metastases. APMIS. 2009;117(12):870-879.
48. Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L. Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol. 2012;12:239-252.
49. Salagianni M, Baxevanis CN, Papamichail M, Perez SA. New insights into the role of NK cells in cancer immunotherapy. Oncoimmunology. 2012;1(2):205-207.
50. Liu G, Atteridge CL, Wang X, Lundgren AD, Wu JD. The membrane type matrix metalloproteinase MMP14 mediates constitutive shedding of MHC class I chain-related molecule A independent of A disintegrin and metalloproteinases. J Immunol. 2010;184(7):3346-3350.
51. Waldhauer I, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68(15):6368-6376.
52. Perentes JY, et al. Cancer cell-associated MT1-MMP promotes blood vessel invasion and distant metastasis in triple-negative mammary tumors. Cancer Res. 2011;71(13):4527-4538.
53. Wu JD, Lin DW, Page ST, Lundgren AD, True LD, Plymate SR. Oxidative DNA damage in the prostate may predispose men to a higher risk of prostate cancer. Transl Oncol. 2009;2(1):39-45.