Dysregulation of the MiR-324-5p-CUEDC2 Axis Leads to Macrophage Dysfunction and Is Associated with Colon Cancer

Cell Reports

Volumn 7, Issue 6, 2014, Pages 1982-1993

  Chen, Yuan ^a   Wang, Shao Xin ^a,b   Mu, Rui ^a   Luo, Xue ^a   Liu, Zhao Shan ^a   Liang, Bing ^a   Zhuo, Hai Long ^c   Hao, Xiao Peng ^c   Wang, Qiong ^a   Fang, Di Feng ^a   Bai, Zhao Fang ^a   Wang, Qian Yi ^a   Wang, He Mei ^d   Jin, Bao Feng ^a   Gong, Wei Li ^a   Zhou, Tao ^a   Zhang, Xue Min ^a   Xia, Qing ^a   Li, Tao ^a  

^a NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

^b NAVY GENERAL HOSPITAL   (China)

^c BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^d BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CUEDC2 PROTEIN; DEXTRAN SULFATE; INTERLEUKIN 4; MICRORNA; MICRORNA 324 5P; PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CUEDC2 PROTEIN, HUMAN; CUEDC2 PROTEIN, MOUSE; MEMBRANE PROTEIN; REPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INFILTRATION; CELL TRANSPLANTATION; COLITIS; COLON CANCER; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; GENETIC REGULATION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MACROPHAGE; MACROPHAGE FUNCTION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; COLON TUMOR; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MUS;

ANIMALS; CARRIER PROTEINS; COLITIS; COLONIC NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICRORNAS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84903478165     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.05.007     Document Type: Article

References (53)

1. Allen I.C., Wilson J.E., Schneider M., Lich J.D., Roberts R.A., Arthur J.C., Woodford R.M., Davis B.K., Uronis J.M., Herfarth H.H., et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity 2012, 36:742-754.
2. Anand P.K., Malireddi R.K.S., Lukens J.R., Vogel P., Bertin J., Lamkanfi M., Kanneganti T.-D. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature 2012, 488:389-393.
3. Arranz A., Doxaki C., Vergadi E., Martinez de la Torre Y., Vaporidi K., Lagoudaki E.D., Ieronymaki E., Androulidaki A., Venihaki M., Margioris A.N., et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. USA 2012, 109:9517-9522.
4. Bai Z., Tai Y., Li W., Zhen C., Gu W., Jian Z., Wang Q., Lin J.E., Zhao Q., Gong W., et al. Gankyrin activates IL-8 to promote hepatic metastasis of colorectal cancer. Cancer Res. 2013, 73:4548-4558.
5. Baltimore D. NF-κB is 25. Nat. Immunol. 2011, 12:683-685.
6. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
7. Biswas S.K., Sica A., Lewis C.E. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J.Immunol. 2008, 180:2011-2017.
8. Bouma G., Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 2003, 3:521-533.
9. Deng L., Zhou J.F., Sellers R.S., Li J.F., Nguyen A.V., Wang Y., Orlofsky A., Liu Q., Hume D.A., Pollard J.W., et al. A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis. Am. J. Pathol. 2010, 176:952-967.
10. Di Leva G., Garofalo M., Croce C.M. MicroRNAs in cancer. Annu. Rev. Pathol. 2014, 9:287-314.
11. Fabian M.R., Sonenberg N., Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 2010, 79:351-379.
12. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 1998, 115:182-205.
13. Gao Y.-F., Li T., Chang Y., Wang Y.-B., Zhang W.-N., Li W.-H., He K., Mu R., Zhen C., Man J.-H., et al. Cdk1-phosphorylated CUEDC2 promotes spindle checkpoint inactivation and chromosomal instability. Nat. Cell Biol. 2011, 13:924-933.
14. Garofalo M., Croce C.M. microRNAs: Master regulators as potential therapeutics in cancer. Annu. Rev. Pharmacol. Toxicol. 2011, 51:25-43.
15. Gibbings D.J., Ciaudo C., Erhardt M., Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 2009, 11:1143-1149.
16. Gocheva V., Wang H.W., Gadea B.B., Shree T., Hunter K.E., Garfall A.L., Berman T., Joyce J.A. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010, 24:241-255.
17. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
18. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5:953-964.
19. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.-Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
20. Karnevi E., Andersson R., Rosendahl A.H. Tumour-educated macrophages display a mixed polarisation and enhance pancreatic cancer cell invasion. Immunol. Cell Biol. 2014.
21. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annu. Rev. Immunol. 2010, 28:573-621.
22. Kim S.W., Kim H.M., Yang K.M., Kim S.-A., Kim S.-K., An M.J., Park J.J., Lee S.K., Kim T.I., Kim W.H., Cheon J.H. Bifidobacterium lactis inhibits NF-kappaB in intestinal epithelial cells and prevents acute colitis and colitis-associated colon cancer in mice. Inflamm. Bowel Dis. 2010, 16:1514-1525.
23. Krausgruber T., Blazek K., Smallie T., Alzabin S., Lockstone H., Sahgal N., Hussell T., Feldmann M., Udalova I.A. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 2011, 12:231-238.
24. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb. Perspect. Biol. 2009, 1. a001651-a001651.
25. Lawrence T., Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 2011, 11:750-761.
26. Lawrence T., Bebien M., Liu G.Y., Nizet V., Karin M. IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 2005, 434:1138-1143.
27. Lee Y.S., Dutta A. MicroRNAs in cancer. Annu. Rev. Pathol. 2009, 4:199-227.
28. Li H.-Y., Liu H., Wang C.-H., Zhang J.-Y., Man J.-H., Gao Y.-F., Zhang P.-J., Li W.-H., Zhao J., Pan X., et al. Deactivation of the kinase IKK by CUEDC2 through recruitment of the phosphatase PP1. Nat. Immunol. 2008, 9:533-541.
29. Li Z., Jiang J., Wang Z., Zhang J., Xiao M., Wang C., Lu Y., Qin Z. Endogenous interleukin-4 promotes tumor development by increasing tumor cell resistance to apoptosis. Cancer Res. 2008, 68:8687-8694.
30. Li T., Morgan M.J., Choksi S., Zhang Y., Kim Y.-S., Liu Z.G. MicroRNAs modulate the noncanonical transcription factor NF-kappaB pathway by regulating expression of the kinase IKKalpha during macrophage differentiation. Nat. Immunol. 2010, 11:799-805.
31. Liu Z., Lee J., Krummey S., Lu W., Cai H., Lenardo M.J. The kinase LRRK2 is a regulator of the transcription factor NFAT that modulates the severity of inflammatory bowel disease. Nat. Immunol. 2011, 12:1063-1070.
32. Maeda S., Hsu L.C., Liu H., Bankston L.A., Iimura M., Kagnoff M.F., Eckmann L., Karin M. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 2005, 307:734-738.
33. Munitz A., Cole E.T., Beichler A., Groschwitz K., Ahrens R., Steinbrecher K., Willson T., Han X., Denson L., Rothenberg M.E., Hogan S.P. Paired immunoglobulin-like receptor B (PIR-B) negatively regulates macrophage activation in experimental colitis. Gastroenterology 2010, 139:530-541.
34. Murdoch C., Muthana M., Coffelt S.B., Lewis C.E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 2008, 8:618-631.
35. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11:723-737.
36. Neufert C., Becker C., Neurath M.F. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat. Protoc. 2007, 2:1998-2004.
37. 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.
38. Qian B.-Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
39. Rehwinkel J., Behm-Ansmant I., Gatfield D., Izaurralde E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 2005, 11:1640-1647.
40. Saleh M., Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat. Rev. Immunol. 2011, 11:9-20.
41. Satoh T., Takeuchi O., Vandenbon A., Yasuda K., Tanaka Y., Kumagai Y., Miyake T., Matsushita K., Okazaki T., Saitoh T., et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 2010, 11:936-944.
42. Schetter A.J., Okayama H., Harris C.C. The role of microRNAs in colorectal cancer. Cancer J. 2012, 18:244-252.
43. Sica A., Mantovani A. Macrophage plasticity and polarization: invivo veritas. J.Clin. Invest. 2012, 122:787-795.
44. Terzic J., Grivennikov S., Karin E., Karin M. Inflammation and colon cancer. Gastroenterology 2010, 138:2101-2114.
45. Todaro M., Alea M.P., Di Stefano A.B., Cammareri P., Vermeulen L., Iovino F., Tripodo C., Russo A., Gulotta G., Medema J.P., Stassi G. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1:389-402.
46. Todaro M., Lombardo Y., Francipane M.G., Alea M.P., Cammareri P., Iovino F., Di Stefano A.B., Di Bernardo C., Agrusa A., Condorelli G., et al. Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4. Cell Death Differ. 2008, 15:762-772.
47. Valencia-Sanchez M.A., Liu J., Hannon G.J., Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006, 20:515-524.
48. Vallabhapurapu S., Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 2009, 27:693-733.
49. Wirtz S., Neufert C., Weigmann B., Neurath M.F. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2007, 2:541-546.
50. Zaki M.H., Boyd K.L., Vogel P., Kastan M.B., Lamkanfi M., Kanneganti T.-D. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 2010, 32:379-391.
51. Zaki M.H., Vogel P., Malireddi R.K.S., Body-Malapel M., Anand P.K., Bertin J., Green D.R., Lamkanfi M., Kanneganti T.D. The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell 2011, 20:649-660.
52. Zhang J., Stirling B., Temmerman S.T., Ma C.A., Fuss I.J., Derry J.M.J., Jain A. Impaired regulation of NF-kappaB and increased susceptibility to colitis-associated tumorigenesis in CYLD-deficient mice. J.Clin. Invest. 2006, 116:3042-3049.
53. Zhang Y., Morgan M.J., Chen K., Choksi S., Liu Z.G. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood 2012, 119:2895-2905.