Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation

Journal of Clinical Investigation

Volumn 121, Issue 7, 2011, Pages 2794-2807

  Mauti, Laetitia A ^a   Le Bitoux, Marie Aude ^a   Baumer, Karine ^a   Stehle, Jean Christophe ^a   Golshayan, Dela ^b   Provero, Paolo ^c   Stamenkovic, Ivan ^a  

^a UNIVERSITY INSTITUTE OF PATHOLOGY   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL GROWTH; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; LIVER; LUNG; MELANOMA CELL; METASTASIS; METASTASIS POTENTIAL; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PRIORITY JOURNAL; TUMOR CELL; TUMOR GROWTH;

ANIMALS; CELL LINE, TUMOR; FEMALE; IMMUNE TOLERANCE; IMMUNOSUPPRESSION; KILLER CELLS, NATURAL; LIVER NEOPLASMS; LUNG NEOPLASMS; MELANOMA; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MYELOID CELLS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; PREGNANCY; PREGNANCY COMPLICATIONS, NEOPLASTIC;

EID: 79959684874     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI41936     Document Type: Article

References (53)

1. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127(4):679-695. (Pubitemid 44781029)
2. Weiss L. Metastatic inefficiency. Adv Cancer Res. 1990;54:159-211. (Pubitemid 20088338)
3. Luzzi KJ, et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol. 1998;153(3):865-873. (Pubitemid 28419039)
4. Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999;59(6):1295-1300. (Pubitemid 29136261)
5. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer. 2007;7(11):834-846. (Pubitemid 350006258)
6. Teng MW, Swann JB, Koebel CM, Schreiber RD, Smyth MJ. Immune-mediated dormancy: an equilibrium with cancer. J Leukoc Biol. 2008;84(4):988-993.
7. Khatami M. Inflammation, aging, and cancer: tumoricidal versus tumorigenesis of immunity: a common denominator mapping chronic diseases. Cell Biochem Biophys. 2009;55(2):55-79.
8. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009;9(4):285-293.
9. Kaplan RN, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438(7069):820-827. (Pubitemid 41753060)
10. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 2006;8(12):1369-1375. (Pubitemid 44835111)
11. Hiratsuka S, et al. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10(11):1349-1355.
12. Erler JT, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell. 2009;15(1):35-44.
13. Taranova AG, et al. Allergic pulmonary inflammation promotes the recruitment of circulating tumor cells to the lung. Cancer Res. 2008;68(20):8582-8589.
14. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137-148. (Pubitemid 39094044)
15. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol. 2009;182(8):4499-4506.
16. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162-174.
17. Sargent IL, Borzychowski AM, Redman CW. NK cells and human pregnancy - an inflammatory view. Trends Immunol. 2006;27(9):399-404. (Pubitemid 44216188)
18. Trowsdale J, Betz AG. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat Immunol. 2006;7(3):241-246.
19. Schedin P. Pregnancy-associated breast cancer and metastasis. Nat Rev Cancer. 2006;6(4):281-291.
20. Shakhar K, Valdimarsdottir HB, Bovbjerg DH. Heightened risk of breast cancer following pregnancy: could lasting systemic immune alterations contribute? Cancer Epidemiol Biomarkers Prev. 2007;16(6):1082-1086. (Pubitemid 46984942)
21. Tanaka H, et al. Increased experimental pulmonary metastasis in pregnant mice. Int J Cancer. 1995;62(3):314-318.
22. Hanna N. Role of natural killer cells in control of cancer metastasis. Cancer Metastasis Rev. 1982;1(1):45-64.
23. Hoechst B, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009;50(3):799-807.
24. Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol. 2009;182(1):240-249.
25. Liu C, et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumorbearing host. Blood. 2007;109(10):4336-4342. (Pubitemid 46743401)
26. Kuhnert M, Strohmeier R, Stegmuller M, Halberstadt E. Changes in lymphocyte subsets during normal pregnancy. Eur J Obstet Gynecol Reprod Biol. 1998;76(2):147-151. (Pubitemid 28031902)
27. Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 2006;16(1):53-65. (Pubitemid 43139709)
28. Yamamoto M, et al. TSU68 prevents liver metastasis of colon cancer xenografts by modulating the premetastatic niche. Cancer Res. 2008;68(23):9754-9762.
29. Raponi M, et al. Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung. Cancer Res. 2006;66(15):7466- 7472. (Pubitemid 44289200)
30. Russo J, Moral R, Balogh GA, Mailo D, Russo IH. The protective role of pregnancy in breast cancer. Breast Cancer Res. 2005;7(3):131-142. (Pubitemid 40704134)
31. Lyons TR, Schedin PJ, Borges VF. Pregnancy and breast cancer: when they collide. J Mammary Gland Biol Neoplasia. 2009;14(2):87-98.
32. McDaniel SM, et al. Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathol. 2006;168(2):608-620. (Pubitemid 43271158)
33. Mousa SA, Linhardt R, Francis JL, Amirkhosravi A. Anti-metastatic effect of a non-anticoagulant low-molecular-weight heparin versus the standard low-molecular-weight heparin, enoxaparin. Thromb Haemost. 2006;96(6):816-821. (Pubitemid 44883824)
34. Furukawa K, Itoh K, Okamura K, Kumagai K, Suzuki M. Changes in NK cell activity during the estrous cycle and pregnancy in mice. J Reprod Immunol. 1984;6(6):353-363. (Pubitemid 15187861)
35. Baley JE, Schacter BZ. Mechanisms of diminished natural killer cell activity in pregnant women and neonates. J Immunol. 1985;134(5):3042-3048. (Pubitemid 15249819)
36. Gabrilovac J, Zadjelovic J, Osmak M, Suchanek E, Zupanovic Z, Boranic M. NK cell activity and estrogen hormone levels during normal human pregnancy. Gynecol Obstet Invest. 1988;25(3):165-172.
37. Gregory CD, Shah LP, Lee H, Scott IV, Golding PR. Cytotoxic reactivity of human natural killer (NK) cells during normal pregnancy: a longitudinal study. J Clin Lab Immunol. 1985;18(4):175-181. (Pubitemid 16211797)
38. Hanna N, Schneider M. Enhancement of tumor metastasis and suppression of natural killer cell activity by beta-estradiol treatment. J Immunol. 1983;130(2):974-980. (Pubitemid 13186338)
39. Hedlund M, et al. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function. J Immunol. 2009;183(1):340-351.
40. Mincheva-Nilsson L, et al. Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol. 2006;176(6):3585-3592. (Pubitemid 43364006)
41. Erler JT, et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature. 2006;440(7088):1222-1226.
42. Kaplan RN, Psaila B, Lyden D. Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Cancer Metastasis Rev. 2006;25(4):521-529.
43. Corzo CA, et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol. 2009;182(9):5693- 5701.
44. Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol. 2008;181(7):4666-4675.
45. Cheng P, et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med. 2008;205(10):2235-2249.
46. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin- cyclophosphamide chemotherapy. Cancer Immunol Immunother. 2009;58(1):49-59.
47. Bacac M, Provero P, Mayran N, Stehle JC, Fusco C, Stamenkovic I. A mouse stromal response to tumor invasion predicts prostate and breast cancer patient survival. PLoS One. 2006;1:e32.
48. Ferretti C, Bruni L, Dangles-Marie V, Pecking AP, Bellet D. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum Reprod Update. 2007;13(2):121-141. (Pubitemid 46323191)
49. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003;31(4):e15.
50. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20(3):307-315. (Pubitemid 38262761)
51. Gentleman RC, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5(10):R80.
52. Breitling R, Armengaud P, Amtmann A, Herzyk P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 2004;573(1-3):83-92. (Pubitemid 39141040)
53. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics. 2006;22(22):2825-2827. (Pubitemid 44742407)