Crucial Involvement of Tumor-Associated Neutrophils in the Regulation of Chronic Colitis-Associated Carcinogenesis in Mice

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Shang, Kun ^a   Bai, Yu Pan ^a   Wang, Chen ^a   Wang, Zhen ^a   Gu, Hong Yu ^a   Du, Xiang ^a   Zhou, Xiao Yan ^a   Zheng, Chun Lei ^a   Chi, Ya Yun ^a   Mukaida, Naofumi ^b   Li, Ying Yi ^a,b  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; CHEMOKINE RECEPTOR CXCR2; CXCL2 CHEMOKINE; DEXTRAN SULFATE; GELATINASE B; LEUKOCYTE ELASTASE; MESSENGER RNA; NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL PROLIFERATION; COLITIS; COLITIS ASSOCIATED COLON CANCER; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IN VITRO STUDY; LAMINA PROPRIA; MACROPHAGE; MACROPHAGE INFILTRATION; MALIGNANT TRANSFORMATION; MOUSE; MUCOSA INFLAMMATION; NEOVASCULARIZATION (PATHOLOGY); NEUTROPHIL CHEMOTAXIS; NONHUMAN; SUBMUCOSA; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, LY; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHEMOKINE CXCL2; CHRONIC DISEASE; COLITIS; COLITIS, ULCERATIVE; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; LEUKOCYTE ELASTASE; MATRIX METALLOPROTEINASE 9; MICE; NEOVASCULARIZATION, PATHOLOGIC; NEUTROPHIL INFILTRATION; NEUTROPHILS; PROLIFERATING CELL NUCLEAR ANTIGEN; RECEPTORS, INTERLEUKIN-8B;

MUS;

EID: 84871330172     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051848     Document Type: Article

References (57)

1. Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, et al. (2004) Cancer statistics, 2004. CA Cancer J Clin 54(1): 8-29.
2. Hussain SP, Harris CC, (2007) Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 121(11): 2373-2380.
3. Hanauer SB, (2006) Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis 12Suppl 1: S3-9.
4. Asquith M, Powrie F, (2010) An innately dangerous balancing act: intestinal homeostasis, inflammation, and colitis-associated cancer. J Exp Med 207(8): 1573-1577.
5. Ullman T, Crooq V, Harpaz N, Sachar D, Itzkowitz S, (2003) Progression of flat low-grade dysplasia to advanced neoplasia in patients with ulcerative colitis. Gastroenterology 125(5): 1311-1319.
6. Dobbins WR, (1984) Dysplasia and malignancy in inflammatory bowel disease. Annu Rev Med 35: 33-48.
7. Gupta RB, Harpaz N, Itzkowitz S, Hossain S, Matula S, et al. (2007) Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology 133(4): 1099-1105; quiz 1340-1341.
8. Bernstein CN, Blanchard JF, Kliewer E, Wajda A, (2001) Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 91(4): 854-862.
9. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, et al. (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142(1): 46-54.e42; quiz e30.
10. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inaqaki Y, et al. (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98(3): 694-702.
11. Okayasu I, Yamada M, Mikami T, Yoshida T, Kanno J, et al. (2002) Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J Gastroenterol Hepatol 17(10): 1078-1083.
12. Boivin GP, Washington K, Yang K, Ward JM, Pretlow TP, et al. (2003) Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 124(3): 762-777.
13. Okayasu I, Ohkusa T, Kaijiura K, Kanno J, Sakamoto S, (1996) Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 39(1): 87-92.
14. Stolfi C, Rizzo A, Franze E, Rotondi A, Fantini MC, et al. (2011) Involvement of interleukin-21 in the regulation of colitis-associated colon cancer. J Exp Med 208(11): 2279-2290.
15. Lowe EL, Crother TR, Rabizadeh S, Hu B, Wang H, et al. (2010) Toll-like receptor 2 signaling protects mice from tumor development in a mouse model of colitis-induced cancer. PLoS One 5(9): e13027.
16. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118(3): 285-296.
17. Popivanova BK, Kostadinova FI, Furuichi K, Shamekh MM, Kondo T, et al. (2009) Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice. Cancer Res 69(19): 7884-7892.
18. Houghton AM, (2010) The paradox of tumor-associated neutrophils: fueling tumor growth with cytotoxic substances. Cell Cycle 9(9): 1732-1737.
19. Pham CT, (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 6(7): 541-550.
20. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, et al. (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177: 195-203.
21. Baggiolini M, (1998) Chemokines and leukocyte traffic. Nature 392(6676): 565-568.
22. Strieter RM, Polverini PJ, Kunkel SL, Arenberg DA, Burdick MD, et al. (1995) The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J Biol Chem 270(45): 27348-27357.
23. Queen MM, Ryan RE, Holzer RG, Keller-Peck CR, Jorcyk CL, (2005) Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression. Cancer Res 65(19): 8896-8904.
24. Jensen HK, donskov F, Marcussen N, Nordsmark M, Lundbeck F, et al. (2009) Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol 27(28): 4709-4717.
25. Bellocq A, Antoine M, Flahault A, Philippe C, Crestani B, et al. (1998) Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am J Pathol 152(1): 83-92.
26. Michael M, Goldstein D, Clarke SJ, Milner AD, Beale P, et al. (2006) Prognostic factors predictive of response and survival to a modified FOLFOX regimen: importance of an increased neutrophil count. Clin Colorectal Cancer 6(4): 297-304.
27. Ding PR, An X, Zhang RX, Fang YJ, LI LR, et al. (2010) Elevated preoperative neutrophil to lymphocyte ratio predicts risk of recurrence following curative resection for stage IIA colon cancer. Int J Colorectal Dis 25(12): 1427-1433.
28. Paesmans M, Sculier JP, Lecomte J, Thiriaux J, Libert P, et al. (2000) Prognostic factors for patients with small cell lung carcinoma: analysis of a series of 763 patients included in 4 consecutive prospective trials with a minimum follow-up of 5 years. Cancer 89(3): 523-533.
29. Schmidt H, Suciu S, Punt CJ, Gore M, Kruit W, et al. (2007) Pretreatment levels of peripheral neutrophils and leukocytes as independent predictors of overall survival in patients with American Joint Committee on Cancer Stage IV Melanoma: results of the EORTC 18951 Biochemotherapy Trial. J Clin Oncol 25(12): 1562-1569.
30. Lu P, Li L, Kuno K, Wu Y, Baba T, et al. (2008) Protective roles of the fractalkine/CX3CL1-CX3CR1 interactions in alkali-induced corneal neovascularization through enhanced antiangiogenic factor expression. J Immunol 180(6): 4283-4291.
31. Nickkho-Amiry M, McVey R, Holland C, (2012) Peroxisome proliferator-activated receptors modulate proliferation and angiogenesis in human endometrial carcinoma. Mol Cancer Res 10(3): 441-453.
32. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, et al. (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2(10): 737-744.
33. Coussens LM, Tinkle CL, Hanahan D, Werb Z, (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103(3): 481-490.
34. Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, et al. (2008) Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 118(2): 560-570.
35. Kostadinova FI, Baba T, Ishida Y, Kondo T, Popivanova BK, et al. (2010) Crucial involvement of the CX3CR1-CX3CL1 axis in dextran sulfate sodium-mediated acute colitis in mice. J Leukoc Biol 88(1): 133-143.
36. Tanaka T, Kohno H, Suzuki R, Yamada Y, Sugie S, et al. (2003) A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 94(11): 965-973.
37. Fukata M, Chen A, Vamadevan AS, Cohen J, Breqlio K, et al. (2007) Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology 133(6): 1869-1881.
38. Mantovani A, Cassatella MA, Costantini C, Jaillon S, (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11(8): 519-531.
39. Donskov F, von der Maase H, (2006) Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 24(13): 1997-2005.
40. Kuang DM, Zhao Q, Wu Y, Peng C, Wang J, et al. (2011) Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J Hepatol 54(5): 948-955.
41. Trellakis S, Farjah H, Bruderek K, Dumitru CA, Hoffmann TK, et al. (2011) Peripheral blood neutrophil granulocytes from patients with head and neck squamous cell carcinoma functionally differ from their counterparts in healthy donors. Int J Immunopathol Pharmacol 24(3): 683-693.
42. Wislez M, Rabbe N, Marchal J, Milleron B, Crestani B, et al. (2003) Hepatocyte growth factor production by neutrophils infiltration bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death. Cancer Res 63(6): 1405-1412.
43. Fossati G, Ricevuti G, Edwards SW, Walker C, Dalton A, et al. (1999) Neutrophil infiltration into human gliomas. Acta Neuropathol 98(4): 349-354.
44. Reid MD, Basturk O, Thirabanjasak D, Hruban RH, Klimstra DS, et al. (2011) 24(12): 1612-1619.
45. Mukaida N, Baba T, (2012) Chemokines in tumor development and progression. Exp Cell Res 318(2): 95-102.
46. Hannelien V, Karel G, Jo VD, Sofie S, (2012) The role of CXC chemokines in the transition of chronic inflammation to esophageal and gastric cancer. Biochim Biophys Acta 1825(1): 117-129.
47. Vandercappellen J, Van Damme J, Struyf S, (2008) The role of CXC chemokines and their receptors in cancer. Cancer Lett 267(2): 226-244.
48. Wu Y, Wang S, Farooq SM, Castelvetere MP, Hou Y, et al. (2012) A chemokine receptor CXCR2 macromolecular complex regulates neutrophil functions in inflammatory diseases. J Biol Chem 287(8): 5744-5755.
49. Terkeltaub R, Baird S, Sears P, Santiaqo R, Boisvert W, (1998) The murine homolog of the interleukin-8 receptor CXCR-2 is essential for the occurrence of neutrophilic inflammation in the air pouch model of acute urate crystal-induced gouty synovitis. Arthritis Rheum 41(5): 900-909.
50. Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, et al. (1994) Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265(5172): 682-684.
51. Baggiolini M, Dewald B, Moser B, (1994) Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol 55: 97-179.
52. Sternlicht MD, Werb Z, (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463-516.
53. Nozawa H, Chiu C, Hanahan D, (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 103(33): 12493-12498.
54. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML, (2005) Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169(4): 681-691.
55. Lee WL, Downey GP, (2001) Leukocyte elastase: physiological functions and role in acute lung injury. Am J Respir Crit Care Med 164(5): 896-904.
56. Owen CA, Campbell MA, Boukedes SS, Stockley RA, Campbell EJ, (1994) A discrete subpopulation of human monocytes expresses a neutrophil-like proinflammatory (P) phenotype. Am J Physiol 267(6 Pt 1): L775-785.
57. Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, et al. (2010) Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 16(2): 219-223.