P53 in the Myeloid Lineage Modulates an Inflammatory Microenvironment Limiting Initiation and Invasion of Intestinal Tumors

Cell Reports

Volumn 13, Issue 5, 2015, Pages 888-897

  He, Xue Yan ^a   Xiang, Cong ^a   Zhang, Chen Xi ^a   Xie, Yin Yin ^a   Chen, Lai ^a   Zhang, Guo Xin ^a   Lu, Yi ^a   Liu, Geng ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL POLARITY; CHRONIC INFLAMMATION; COLITIS; COLORECTAL TUMOR; CONTROLLED STUDY; DOWN REGULATION; INTESTINE TUMOR; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; ADENOMA; ANIMAL; C57BL MOUSE; CELL LINEAGE; CYTOLOGY; GENETICS; MACROPHAGE; METABOLISM; MYELOID PROGENITOR CELL; PATHOLOGY; STEM CELL NICHE;

ADENOMA; ANIMALS; CELL LINEAGE; INTESTINAL NEOPLASMS; MACROPHAGES; MICE; MICE, INBRED C57BL; MYELOID PROGENITOR CELLS; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-MYC; STEM CELL NICHE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84947436258     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.045     Document Type: Article

References (49)

1. Ahn B., Ohshima H. Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res. 2001, 61:8357-8360.
2. Balkwill F., Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 2001, 357:539-545.
3. Bar J., Moskovits N., Oren M. Involvement of stromal p53 in tumor-stroma interactions. Semin. Cell Dev. Biol. 2010, 21:47-54.
4. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
5. Bollrath J., Greten F.R. IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. EMBO Rep. 2009, 10:1314-1319.
6. Brentnall T.A., Crispin D.A., Rabinovitch P.S., Haggitt R.C., Rubin C.E., Stevens A.C., Burmer G.C. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology 1994, 107:369-378.
7. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Förster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265-277.
8. Cooks T., Pateras I.S., Tarcic O., Solomon H., Schetter A.J., Wilder S., Lozano G., Pikarsky E., Forshew T., Rosenfeld N., et al. Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell 2013, 23:634-646.
9. Cooks T., Harris C.C., Oren M. Caught in the cross fire: p53 in inflammation. Carcinogenesis 2014, 35:1680-1690.
10. Cooper H.S., Everley L., Chang W.-C., Pfeiffer G., Lee B., Murthy S., Clapper M.L. The role of mutant Apc in the development of dysplasia and cancer in the mouse model of dextran sulfate sodium-induced colitis. Gastroenterology 2001, 121:1407-1416.
11. Erreni M., Mantovani A., Allavena P. Tumor-associated Macrophages (TAM) and Inflammation in Colorectal Cancer. Cancer Microenviron. 2011, 4:141-154.
12. Forrester K., Ambs S., Lupold S.E., Kapust R.B., Spillare E.A., Weinberg W.C., Felley-Bosco E., Wang X.W., Geller D.A., Tzeng E., et al. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc. Natl. Acad. Sci. USA 1996, 93:2442-2447.
13. Ghosh S., Mendoza T., Ortiz L.A., Hoyle G.W., Fermin C.D., Brody A.R., Friedman M., Morris G.F. Bleomycin sensitivity of mice expressing dominant-negative p53 in the lung epithelium. Am. J. Respir. Crit. Care Med. 2002, 166:890-897.
14. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., Kagnoff M.F., Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296.
15. Grier J.D., Xiong S., Elizondo-Fraire A.C., Parant J.M., Lozano G. Tissue-specific differences of p53 inhibition by Mdm2 and Mdm4. Mol. Cell. Biol. 2006, 26:192-198.
16. Grivennikov S.I., Wang K., Mucida D., Stewart C.A., Schnabl B., Jauch D., Taniguchi K., Yu G.Y., Osterreicher C.H., Hung K.E., et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012, 491:254-258.
17. Hagemann T., Lawrence T., McNeish I., Charles K.A., Kulbe H., Thompson R.G., Robinson S.C., Balkwill F.R. "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J. Exp. Med. 2008, 205:1261-1268.
18. Hill R., Song Y., Cardiff R.D., Van Dyke T. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell 2005, 123:1001-1011.
19. Hofseth L.J., Saito S., Hussain S.P., Espey M.G., Miranda K.M., Araki Y., Jhappan C., Higashimoto Y., He P., Linke S.P., et al. Nitric oxide-induced cellular stress and p53 activation in chronic inflammation. Proc. Natl. Acad. Sci. USA 2003, 100:143-148.
20. Hussain S.P., Amstad P., Raja K., Ambs S., Nagashima M., Bennett W.P., Shields P.G., Ham A.J., Swenberg J.A., Marrogi A.J., Harris C.C. Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease. Cancer Res. 2000, 60:3333-3337.
21. Hussain S.P., Hofseth L.J., Harris C.C. Radical causes of cancer. Nat. Rev. Cancer 2003, 3:276-285.
22. Jonkers J., Meuwissen R., van der Gulden H., Peterse H., van der Valk M., Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 2001, 29:418-425.
23. Kang S.Y., Halvorsen O.J., Gravdal K., Bhattacharya N., Lee J.M., Liu N.W., Johnston B.T., Johnston A.B., Haukaas S.A., Aamodt K., et al. Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1. Proc. Natl. Acad. Sci. USA 2009, 106:12115-12120.
24. Kiaris H., Chatzistamou I., Trimis G., Frangou-Plemmenou M., Pafiti-Kondi A., Kalofoutis A. Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer Res. 2005, 65:1627-1630.
25. Lane D.P., Cheok C.F., Lain S. p53-based cancer therapy. Cold Spring Harb. Perspect. Biol. 2010, 2:a001222.
26. Li L., Ng D.S., Mah W.C., Almeida F.F., Rahmat S.A., Rao V.K., Leow S.C., Laudisi F., Peh M.T., Goh A.M., et al. A unique role for p53 in the regulation of M2 macrophage polarization. Cell Death Differ. 2015, 22:1081-1093.
27. Lozano G. The oncogenic roles of p53 mutants in mouse models. Curr. Opin. Genet. Dev. 2007, 17:66-70.
28. Lujambio A., Akkari L., Simon J., Grace D., Tschaharganeh D.F., Bolden J.E., Zhao Z., Thapar V., Joyce J.A., Krizhanovsky V., Lowe S.W. Non-cell-autonomous tumor suppression by p53. Cell 2013, 153:449-460.
29. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
30. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014, 6:13.
31. Moser A.R., Pitot H.C., Dove W.F. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990, 247:322-324.
32. Moskovits N., Kalinkovich A., Bar J., Lapidot T., Oren M. p53 Attenuates cancer cell migration and invasion through repression of SDF-1/CXCL12 expression in stromal fibroblasts. Cancer Res. 2006, 66:10671-10676.
33. Nishizaki M., Fujiwara T., Tanida T., Hizuta A., Nishimori H., Tokino T., Nakamura Y., Bouvet M., Roth J.A., Tanaka N. Recombinant adenovirus expressing wild-type p53 is antiangiogenic: a proposed mechanism for bystander effect. Clin. Cancer Res. 1999, 5:1015-1023.
34. Pello O.M., De Pizzol M., Mirolo M., Soucek L., Zammataro L., Amabile A., Doni A., Nebuloni M., Swigart L.B., Evan G.I., et al. Role of c-MYC in alternative activation of human macrophages and tumor-associated macrophage biology. Blood 2012, 119:411-421.
35. Ruffell B., Coussens L.M. Macrophages and therapeutic resistance in cancer. Cancer Cell 2015, 27:462-472.
36. Sablina A.A., Budanov A.V., Ilyinskaya G.V., Agapova L.S., Kravchenko J.E., Chumakov P.M. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005, 11:1306-1313.
37. Schauer I.G., Zhang J., Xing Z., Guo X., Mercado-Uribe I., Sood A.K., Huang P., Liu J. Interleukin-1β promotes ovarian tumorigenesis through a p53/NF-κB-mediated inflammatory response in stromal fibroblasts. Neoplasia 2013, 15:409-420.
38. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., Canli O., Heijmans J., Huels D.J., Moreaux G., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152:25-38.
39. Schwitalla S., Ziegler P.K., Horst D., Becker V., Kerle I., Begus-Nahrmann Y., Lechel A., Rudolph K.L., Langer R., Slotta-Huspenina J., et al. Loss of p53 in enterocytes generates an inflammatory microenvironment enabling invasion and lymph node metastasis of carcinogen-induced colorectal tumors. Cancer Cell 2013, 23:93-106.
40. Shaked H., Hofseth L.J., Chumanevich A., Chumanevich A.A., Wang J., Wang Y., Taniguchi K., Guma M., Shenouda S., Clevers H., et al. Chronic epithelial NF-κB activation accelerates APC loss and intestinal tumor initiation through iNOS up-regulation. Proc. Natl. Acad. Sci. USA 2012, 109:14007-14012.
41. Tanaka T., Kohno H., Suzuki R., Hata K., Sugie S., Niho N., Sakano K., Takahashi M., Wakabayashi K. Dextran sodium sulfate strongly promotes colorectal carcinogenesis in Apc(Min/+) mice: inflammatory stimuli by dextran sodium sulfate results in development of multiple colonic neoplasms. Int. J. Cancer 2006, 118:25-34.
42. Terzian T., Wang Y., Van Pelt C.S., Box N.F., Travis E.L., Lozano G. Haploinsufficiency of Mdm2 and Mdm4 in tumorigenesis and development. Mol. Cell. Biol. 2007, 27:5479-5485.
43. Terzić J., Grivennikov S., Karin E., Karin M. Inflammation and colon cancer. Gastroenterology 2010, 138:2101-2114.e5.
44. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., Kong N., Kammlott U., Lukacs C., Klein C., et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004, 303:844-848.
45. Vousden K.H., Prives C. Blinded by the Light: The Growing Complexity of p53. Cell 2009, 137:413-431.
46. Xiong S., Van Pelt C.S., Elizondo-Fraire A.C., Liu G., Lozano G. Synergistic roles of Mdm2 and Mdm4 for p53 inhibition in central nervous system development. Proc. Natl. Acad. Sci. USA 2006, 103:3226-3231.
47. Yamanishi Y., Boyle D.L., Pinkoski M.J., Mahboubi A., Lin T., Han Z., Zvaifler N.J., Green D.R., Firestein G.S. Regulation of joint destruction and inflammation by p53 in collagen-induced arthritis. Am. J. Pathol. 2002, 160:123-130.
48. Zhang Q., He X., Chen L., Zhang C., Gao X., Yang Z., Liu G. Synergistic regulation of p53 by Mdm2 and Mdm4 is critical in cardiac endocardial cushion morphogenesis during heart development. J. Pathol. 2012, 228:416-428.
49. Zheng S.J., Lamhamedi-Cherradi S.E., Wang P., Xu L., Chen Y.H. Tumor suppressor p53 inhibits autoimmune inflammation and macrophage function. Diabetes 2005, 54:1423-1428.