Tumor progression stage and anatomical site regulate tumor-associated macrophage and bone marrow-derived monocyte polarization

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2972-2985

  Redente, Elizabeth F ^a   Dwyer Nield, Lori D ^a   Merrick, Daniel T ^b   Raina, Komal ^a   Agarwal, Rajesh ^a   Pao, William ^c   Rice, Pamela L ^d   Shroyer, Kenneth R ^e   Malkinson, Alvin M ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; INOSINATE DEHYDROGENASE; K RAS PROTEIN; GAMMA INTERFERON; INTERLEUKIN 4;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW; CANCER MODEL; CANCER PREVENTION; CARCINOGENESIS; CLINICAL ARTICLE; COLON CANCER; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; LUNG ALVEOLUS MACROPHAGE; LUNG CANCER; MONOCYTE; MOUSE; NEOPLASMS SUBDIVIDED BY ANATOMICAL SITE; NONHUMAN; ONCOGENE K RAS; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROSTATE CANCER; TRANSGENE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; CELL POLARITY; CHEMISTRY; CYTOLOGY; DISEASE COURSE; DISEASE MODEL; FEMALE; INBRED MOUSE STRAIN; LUNG LAVAGE; MALE; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL POLARITY; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-4; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED STRAINS; MONOCYTES; NEOPLASMS;

EID: 77953183233     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090879     Document Type: Article

References (60)

1. Nathan C: Points of control in inflammation. Nature 2002, 420: 846-852
2. Coussens LM, Werb Z: Inflammation and cancer. Nature 2002, 420:860-867
3. Geissmann F, Jung S, Littman DR: Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82
4. Malkinson AM: Role of inflammation in mouse lung tumorigenesis: a review. Exp Lung Res 2005, 31:57-82
5. Balkwill F, Mantovani A: Inflammation and cancer: back to Virchow? Lancet 2001, 357:539-545
6. Williams CS, Goldman AP, Sheng H, Morrow JD, Dubois RN: Sulindac sulfide, but not sulindac sulfone, inhibits colorectal cancer growth. Neoplasia 1999, 1:170-176
7. Bauer AK, Malkinson AM, Kleeberger SR: Susceptibility to neoplastic and non-neoplastic pulmonary diseases in mice: genetic similarities. Am J Physiol Lung Cell Mol Physiol 2004, 287:L685-L703
8. Engels EA, Wu X, Gu J, Dong Q, Liu J, Spitz MR: Systematic evaluation of genetic variants in the inflammation pathway and risk of lung cancer. Cancer Res 2007, 67:6520-6527 (Pubitemid 47037538)
9. Keith RL, Miller YE, Hoshikawa Y, Moore MD, Gesell TL, Gao B, Malkinson AM, Golpon HA, Nemenoff RA, Geraci MW: Manipulation of pulmonary prostacyclin synthase expression prevents murine lung cancer. Cancer Res 2002, 62:734-740 (Pubitemid 34126948)
10. Bernert H, Sekikawa K, Radcliffe RA, Iraqi F, You M, Malkinson AM: Tnfa and Il-10 deficiencies have contrasting effects on lung tumor susceptibility: gender-dependent modulation of IL-10 haploinsufficiency. Mol Carcinog 2003, 38:117-123
11. Clark JC, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT, Whitsett JA: FGF-10 disrupts lung morphogenesis and causes pulmonary adenomas in vivo. Am J Physiol Lung Cell Mol Physiol 2001, 280:L705-L715 (Pubitemid 33776137)
12. Gordon S: Alternative activation of macrophages. Nat Rev Immunol 2003, 3:23-35
13. Takanami I, Takeuchi K, Kodaira S: Tumor-associated macrophage infiltration in pulmonary adenocarcinoma: association with angiogenesis and poor prognosis. Oncology 1999, 57:138-142
14. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J, Condeelis J: A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 2004, 64:7022-7029
15. Terabe M, Berzofsky JA: Immunoregulatory T cells in tumor immunity. Curr Opin Immunol 2004, 16:157-162
16. Sica A, Bronte V: Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007, 117:1155-1166
17. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM: M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 2000, 164:6166-6173
18. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J: Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol 2005, 175:342-349 (Pubitemid 40884337)
19. Kotowicz K, Callard RE, Friedrich K, Matthews DJ, Klein N: Biological activity of IL-4 and IL-13 on human endothelial cells: functional evidence that both cytokines act through the same receptor. Int Immunol 1996, 8:1915-1925
20. Munder M, Eichmann K, Moran JM, Centeno F, Soler G, Modolell M: Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J Immunol 1999, 163:3771-3777 (Pubitemid 29450901)
21. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004, 25:677-686
22. Montaner LJ, da Silva RP, Sun J, Sutterwala S, Hollinshead M, Vaux D, Gordon S: Type 1 and type 2 cytokine regulation of macrophage endocytosis: differential activation by IL-4/IL-13 as opposed to IFN-gamma or IL-10. J Immunol 1999, 162:4606-4613 (Pubitemid 29314860)
23. Nair MG, Cochrane DW, Allen JE: Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol Lett 2003, 85:173-180
24. Morris SM Jr, Kepka-Lenhart D, Chen LC: Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol 1998, 275:E740-E747 (Pubitemid 28536311)
25. Luo Y, Zhou H, Krueger J, Kaplan C, Lee SH, Dolman C, Markowitz D, Wu W, Liu C, Reisfeld RA, Xiang R: Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest 2006, 116:2132-2141
26. Huang M, Wang J, Lee P, Sharma S, Mao JT, Meissner H, Uyemura K, Modlin R, Wollman J, Dubinett SM: Human non-small cell lung cancer cells express a type 2 cytokine pattern. Cancer Res 1995, 55:3847-3853
27. Robinson-Smith TM, Isaacsohn I, Mercer CA, Zhou M, Van RN, Husseinzadeh N, Farland-Mancini MM, Drew AF: Macrophages mediate inflammation-enhanced metastasis of ovarian tumors in mice. Cancer Res 2007, 67:5708-5716
28. Hagemann T, Wilson J, Burke F, Kulbe H, Li NF, Pluddemann A, Charles K, Gordon S, Balkwill FR: Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype. J Immunol 2006, 176:5023-5032
29. Redente EF, Orlicky DJ, Bouchard RJ, Malkinson AM: Tumor signaling to the bone marrow changes the phenotype of monocytes and pulmonary macrophages during urethane-induced primary lung tumorigenesis in A/J mice. Am J Pathol 2007, 170:693-708
30. Malkinson AM: Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung. Lung Cancer 2001, 32:265-279
31. Malkinson AM, Beer DS: Major effect on susceptibility to urethan-induced pulmonary adenoma by a single gene in BALB/cBy mice. J Natl Cancer Inst 1983, 70:931-936
32. Bauer AK, Dwyer-Nield LD, Keil K, Koski K, Malkinson AM: Butylated hydroxytoluene (BHT) induction of pulmonary inflammation: a role in tumor promotion. Exp Lung Res 2001, 27:197-216 (Pubitemid 32239293)
33. Malkinson AM, Koski KM, Evans WA, Festing MF: Butylated hydroxytoluene exposure is necessary to induce lung tumors in BALB mice treated with 3-methylcholanthrene. Cancer Res 1997, 57:2832-2834
34. Bauer AK, Dwyer-Nield LD, Hankin JA, Murphy RC, Malkinson AM: The lung tumor promoter, butylated hydroxytoluene (BHT), causes chronic inflammation in promotion-sensitive BALB/cByJ mice but not in promotion- resistant CXB4 mice. Toxicology 2001, 169:1-15
35. Gingrich JR, Barrios RJ, Foster BA, Greenberg NM: Pathologic progression of autochthonous prostate cancer in the TRAMP model. Prostate Cancer Prostatic Dis 1999, 2:70-75
36. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ, Rosen JM: Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 1995, 92:3439-3443
37. Greenberg NM, DeMayo FJ, Sheppard PC, Barrios R, Lebovitz R, Finegold M, Angelopoulou R, Dodd JG, Duckworth ML, Rosen JM: The rat probasin gene promoter directs hormonally and developmentally regulated expression of a heterologous gene specifically to the prostate in transgenic mice. Mol Endocrinol 1994, 8:230-239
38. Raina K, Singh RP, Agarwal R, Agarwal C: Oral grape seed extract inhibits prostate tumor growth and progression in TRAMP mice. Cancer Res 2007, 67:5976-5982
39. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, Whitsett JA, Koretsky A, Varmus HE: Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 2001, 15:3249-3262
40. Mitchell BS, Horny HP, Schumacher U: Immunophenotyping of human HT29 colon cancer cell primary tumours and their metastases in severe combined immunodeficient mice. Histochem J 1997, 29: 393-399
41. Jojovic M, Schumacher U: Quantitative assessment of spontaneous lung metastases of human HT29 colon cancer cells transplanted into SCID mice. Cancer Lett 2000, 152:151-156
42. Raes G, Brys L, Dahal BK, Brandt J, Grooten J, Brombacher F, Vanham G, Noel W, Bogaert P, Boonefaes T, Kindt A, Van den BR, Leenen PJ, De BP, Ghassabeh GH: Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J Leukoc Biol 2005, 77:321-327
43. Rotondo R, Barisione G, Mastracci L, Grossi F, Orengo AM, Costa R, Truini M, Fabbi M, Ferrini S, Barbieri O: IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer 2009, 125:887-893
44. Martinez FO, Gordon S, Locati M, Mantovani A: Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006, 177:7303-7311 (Pubitemid 44715100)
45. Miller YE, Dwyer-Nield LD, Keith RL, Le M, Franklin WA, Malkinson AM: Induction of a high incidence of lung tumors in C57BL/6 mice with multiple ethyl carbamate injections. Cancer Lett 2003, 198: 139-144
46. Forkert PG, Jackson AC, Parkinson A, Chen S: Diminished expression of CYP1A1 in urethane-induced lung tumors in strain A/J mice: analysis by in situ hybridization and immunohistochemical methods. Am J Respir Cell Mol Biol 1996, 14:444-453 (Pubitemid 126440513)
47. O'Donnell EP, Zerbe LK, Dwyer-Nield LD, Kisley LR, Malkinson AM: Quantitative analysis of early chemically-induced pulmonary lesions in mice of varying susceptibilities to lung tumorigenesis. Cancer Lett 2006, 241:197-202
48. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC, Kaufman MH, Linnoila RI, Maronpot RR, Rabson AS, Reddick RL, Rehm S, Rozengurt N, Schuller HM, Shmidt EN, Travis WD, Ward JM, Jacks T: Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004, 64:2307-2316
49. Dinapoli MR, Calderon CL, Lopez DM: The altered tumoricidal capacity of macrophages isolated from tumor-bearing mice is related to reduce expression of the inducible nitric oxide synthase gene. J Exp Med 1996, 183:1323-1329 (Pubitemid 126613318)
50. Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O'Neill A, Mier J, Ochoa AC: Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 2005, 65:3044-3048
51. Chang CI, Liao JC, Kuo L: Macrophage arginase promotes tumor cell growth and suppresses nitric oxide-mediated tumor cytotoxicity. Cancer Res 2001, 61:1100-1106
52. Biswas SK, Sica A, Lewis CE: Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J Immunol 2008, 180:2011-2017
53. Boraschi D, Meltzer MS: Defective tumoricidal capacity of macrophages from A/J mice. I. Characterization of the macrophage cytotoxic defect after in vivo and in vitro activation stimuli. J Immunol 1979, 122:1587-1591
54. Boraschi D, Meltzer MS: Defective tumoricidal capacity of macrophages from A/J mice. II. Comparison of the macrophage cytotoxic defect of A/J mice with that of lipid A-unresponsive C3H/HeJ mice. J Immunol 1979, 122:1592-1597 (Pubitemid 9181538)
55. Boraschi D, Meltzer MS: Defective tumoricidal capacity of macrophages from A/J mice. III. Genetic analysis of the macrophage defect. J Immunol 1980, 124:1050-1053 (Pubitemid 10139235)
56. Meyer AM, Dwyer-Nield LD, Hurteau G, Keith RL, Ouyang Y, Freed BM, Kisley LR, Geraci MW, Bonventre JV, Nemenoff RA, Malkinson AM: Attenuation of the pulmonary inflammatory response following butylated hydroxytoluene treatment of cytosolic phospholipase A2 null mice. Am J Physiol Lung Cell Mol Physiol 2006, 290:L1260-L1266
57. Watkins SK, Egilmez NK, Suttles J, Stout RD: IL-12 rapidly alters the functional profile of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo. J Immunol 2007, 178:1357-1362 (Pubitemid 46154605)
58. Mills CD, Shearer J, Evans R, Caldwell MD: Macrophage arginine metabolism and the inhibition or stimulation of cancer. J Immunol 1992, 149:2709-2714
59. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A: Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002, 23:549-555
60. Swann JB, Smyth MJ: Immune surveillance of tumors. J Clin Invest 2007, 117:1137-1146