A novel role of hematopoietic CCL5 in promoting triple-negative mammary tumor progression by regulating generation of myeloid-derived suppressor cells

Cell Research

Volumn 23, Issue 3, 2013, Pages 394-408

  Zhang, Yan ^a   Lv, Dandan ^b   Kim, Ha Jeong ^a   Kurt, Robert A ^c   Bu, Wen ^d   Li, Yi ^d   Ma, Xiaojing ^a,b,e  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c LAFAYETTE COLLEGE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; NEUTRALIZING ANTIBODY; RANTES;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CD8+ T LYMPHOCYTE; CELL CULTURE; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; DRUG ANTAGONISM; EXPERIMENTAL NEOPLASM; GENETICS; HUMAN; MALE; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD11B; BONE MARROW TRANSPLANTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHEMOKINE CCL5; DISEASE PROGRESSION; HUMANS; MALE; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MYELOID CELLS; T-LYMPHOCYTES, CYTOTOXIC;

MUS;

EID: 84874646861     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2012.178     Document Type: Article

References (56)

1. Appay V, Rowland-Jones SL. RANTES: a versatile and controversial chemokine. Trends Immunol 2001; 22:83-87.
2. Levy JA. The unexpected pleiotropic activities of RANTES. J Immunol 2009; 182:3945-3946.
3. Pakianathan DR, Kuta EG, Artis DR, Skelton NJ, Hebert CA. Distinct but overlapping epitopes for the interaction of a CCchemokine with CCR1, CCR3 and CCR5. Biochemistry 1997; 36:9642-9648.
4. Movahedi K, Guilliams M, Van den Bossche J, et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233-4244.
5. Yaal-Hahoshen N, Shina S, Leider-Trejo L, et al. The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients. Clin Cancer Res 2006; 12:4474-4480.
6. Niwa Y, Akamatsu H, Niwa H, Sumi H, Ozaki Y, Abe A. Correlation of tissue and plasma RANTES levels with disease course in patients with breast or cervical cancer. Clin Cancer Res 2001; 7:285-289.
7. Nouh MA, Eissa SA, Zaki SA, El-Maghraby SM, Kadry DY. Importance of Serum IL-18 and RANTES as Markers for Breast Carcinoma Progression. J Egypt Natl Canc Inst 2005; 17:51-55.
8. Bieche I, Lerebours F, Tozlu S, Espie M, Marty M, Lidereau R. Molecular profiling of inflammatory breast cancer: identification of a poor-prognosis gene expression signature. Clin Cancer Res 2004; 10:6789-6795.
9. Wigler N, Shina S, Kaplan O, et al. Breast carcinoma: a report on the potential usage of the CC chemokine RANTES as a marker for a progressive disease. Isr Med Assoc J 2002; 4:940-943.
10. Sauer G, Schneiderhan-Marra N, Kazmaier C, et al. Prediction of nodal involvement in breast cancer based on multiparametric protein analyses from preoperative core needle biopsies of the primary lesion. Clin Cancer Res 2008; 14:3345-3353.
11. Luboshits G, Shina S, Kaplan O, et al. Elevated expression of the CC chemokine regulated on activation, normal T cell expressed and secreted (RANTES) in advanced breast carcinoma. Cancer Res 1999; 59:4681-4687.
12. Adler EP, Lemken CA, Katchen NS, Kurt RA. A dual role for tumor-derived chemokine RANTES (CCL5). Immunol Lett 2003; 90:187-194.
13. Robinson SC, Scott KA, Wilson JL, Thompson RG, Proudfoot AE, Balkwill FR. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res 2003; 63:8360-8365.
14. Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett 2008; 267:271-285.
15. Jayasinghe MM, Golden JM, Nair P, O'Donnell CM, Werner MT, Kurt RA. Tumor-derived CCL5 does not contribute to breast cancer progression. Breast Cancer Res Treat 2008; 111:511-521.
16. Ostrand-Rosenberg S, Grusby MJ, Clements VK. Cutting edge: STAT6-deficient mice have enhanced tumor immunity to primary and metastatic mammary carcinoma. J Immunol 2000; 165:6015-6019.
17. Kelner GS, Kennedy J, Bacon KB, et al. Lymphotactin: a cytokine that represents a new class of chemokine. Science 1994; 266:1395-1399.
18. Dolcetti L, Peranzoni E, Ugel S, et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 2010; 40:22-35.
19. Sawanobori Y, Ueha S, Kurachi M, et al. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 2008; 111:5457-5466.
20. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-5802.
21. Zhu B, Bando Y, Xiao S, et al. CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J Immunol 2007; 179:5228-5237.
22. Melani C, Chiodoni C, Forni G, Colombo MP. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 2003; 102:2138-2145.
23. Ling V, Luxenberg D, Wang J, et al. Structural identification of the hematopoietic progenitor antigen ER-MP12 as the vascular endothelial adhesion molecule PECAM-1 (CD31). Eur J Immunol 1997; 27:509-514.
24. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162-174.
25. Katz BZ, Eshel R, Sagi-Assif O, Witz IP. An association between high Ly-6A/E expression on tumor cells and a highly malignant phenotype. Int J Cancer 1994; 59:684-691.
26. Trottier MD, Newsted MM, King LE, Fraker PJ. Natural glucocorticoids induce expansion of all developmental stages of murine bone marrow granulocytes without inhibiting function. Proc Natl Acad Sci USA 2008; 105:2028-2033.
27. de Bruijn MF, Slieker WA, van der Loo JC, Voerman JS, van Ewijk W, Leenen PJ. Distinct mouse bone marrow macrophage precursors identified by differential expression of ER-MP12 and ER-MP20 antigens. Eur J Immunol 1994; 24:2279-2284.
28. Shojaei F, Wu X, Qu X, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci USA 2009; 106:6742-6747.
29. Shojaei F, Wu X, Zhong C, et al. Bv8 regulates myeloid-celldependent tumour angiogenesis. Nature 2007; 450:825-831.
30. Kusmartsev S, Cheng F, Yu B, et al. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res 2003; 63:4441-4449.
31. Li Y, Hively WP, Varmus HE. Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 2000; 19:1002-1009.
32. Lechner MG, Liebertz DJ, Epstein AL. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 2010; 185:2273-2284.
33. Seung LP, Rowley DA, Dubey P, Schreiber H. Synergy between T-cell immunity and inhibition of paracrine stimulation causes tumor rejection. Proc Natl Acad Sci USA 1995; 92:6254-6258.
34. Bronte V, Chappell DB, Apolloni E, et al. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J Immunol 1999; 162:5728-5737.
35. Salvadori S, Martinelli G, Zier K. Resection of solid tumors reverses T cell defects and restores protective immunity. J Immunol 2000; 164:2214-2220.
36. Terabe M, Matsui S, Park JM, et al. Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence. J Exp Med 2003; 198:1741-1752.
37. Danna EA, Sinha P, Gilbert M, Clements VK, Pulaski BA, Ostrand-Rosenberg S. Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res 2004; 64:2205-2211.
38. Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 2006; 16:53-65.
39. Hock H, Hamblen MJ, Rooke HM, et al. Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity 2003; 18:109-120.
40. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12:253-268.
41. Pan PY, Ma G, Weber KJ, et al. Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer. Cancer Res 2010; 70:99-108.
42. Serafini P, Mgebroff S, Noonan K, Borrello I. Myeloidderived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 2008; 68:5439-5449.
43. Hoechst B, Gamrekelashvili J, Manns MP, Greten TF, Korangy F. Plasticity of human Th17 cells and iTregs is orchestrated by different subsets of myeloid cells. Blood 2011; 117:6532-6541.
44. Chang LY, Lin YC, Mahalingam J, et al. Tumor-derived chemokine CCL5 enhances TGF-beta-mediated killing of CD8(+) T cells in colon cancer by T-regulatory cells. Cancer Res 2012; 72:1092-1102.
45. Broxmeyer HE, Sherry B, Lu L, et al. Enhancing and suppressing effects of recombinant murine macrophage inflammatory proteins on colony formation in vitro by bone marrow myeloid progenitor cells. Blood 1990; 76:1110-1116.
46. Broxmeyer HE, Sherry B, Cooper S, et al. Macrophage inflammatory protein (MIP)-1 beta abrogates the capacity of MIP-1 alpha to suppress myeloid progenitor cell growth. J Immunol 1991; 147:2586-2594.
47. Dahl R, Walsh JC, Lancki D, et al. Regulation of macrophage and neutrophil cell fates by the PU.1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nat Immunol 2003; 4:1029-1036.
48. Laslo P, Spooner CJ, Warmflash A, et al. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006; 126:755-766.
49. Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449:557-563.
50. Mi Z, Bhattacharya SD, Kim VM, Guo H, Talbot LJ, Kuo PC. Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis 2011; 32:477-487.
51. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992; 12:954-961.
52. Wareing MD, Lyon AB, Lu B, Gerard C, Sarawar SR. Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J Leukoc Biol 2004; 76:886-895.
53. Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 1988; 55:619-625.
54. Poh TW, Bradley JM, Mukherjee P, Gendler SJ. Lack of Muc1-regulated beta-catenin stability results in aberrant expansion of CD11b+Gr1+ myeloid-derived suppressor cells from the bone marrow. Cancer Res 2009; 69:3554-3562.
55. Novak EK, Reddington M, Zhen L, et al. Inherited thrombocytopenia caused by reduced platelet production in mice with the gunmetal pigment gene mutation. Blood 1995; 85:1781-1789.
56. Karsunky H, Zeng H, Schmidt T, et al. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat Genet 2002; 30:295-300.