Mucin 1 gene (MUC1) and gastric-cancer susceptibility

International Journal of Molecular Sciences

Volumn 15, Issue 5, 2014, Pages 7958-7973

  Saeki, Norihisa ^a   Sakamoto, Hiromi ^a   Yoshida, Teruhiko ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

Cancer susceptibility gene; Gastric cancer; Genome wide association study; Helicobacter pylori; Mucin 1; Single nucleotide polymorphism

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; KRUPPEL LIKE FACTOR 4; MUCIN 1; PROSTATE STEM CELL ANTIGEN; PROTEIN P53;

CANCER SUSCEPTIBILITY; CARCINOGENESIS; CHROMOSOME; CHROMOSOME 1Q22; DOWN REGULATION; GENE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; HELICOBACTER INFECTION; HUMAN; IMMUNOHISTOCHEMISTRY; MUCIN 1 GENE; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STOMACH CANCER; ANIMAL; COMPLICATION; GENE SILENCING; GENETICS; HELICOBACTER; IMMUNOLOGY; INFLAMMATION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY; STOMACH; STOMACH TUMOR;

ANIMALS; GENE KNOCKDOWN TECHNIQUES; GENOME-WIDE ASSOCIATION STUDY; HELICOBACTER; HELICOBACTER INFECTIONS; HUMANS; INFLAMMATION; MICE; MUCIN-1; POLYMORPHISM, SINGLE NUCLEOTIDE; STOMACH; STOMACH NEOPLASMS;

EID: 84899973932     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15057958     Document Type: Review

References (79)

1. Brenner, H., Rothenbacher, D., Arndt, V. Epidemiology of gastric cancer. In Methods of Molecular Biology, Cancer Epidemiology, Verma, M., Ed., Humana Press: Totowa, NJ, USA, 2009, Volume 472, p. 467.
2. Yasui, W., Sentani, K., Motoshita, J., Nakayama, H. Molecular pathobiology of gastric cancer. Scand. J. Surg. 2006, 95, 225-231.
3. Peek, R.M., Jr., Blaser, M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2002, 2, 28-37.
4. Ricci, V., Romano, M., Boquet, P. Molecular cross-talk between Helicobacter pylori and human gastric mucosa. World J. Gastroenterol. 2011, 17, 1383-1399.
5. Forman, D. Helicobacter pylori and gastric cancer. Scand. J. Gastroenterol. Suppl. 1996, 220, 23-26.
6. Pilpilidis, I., Kountouras, J., Zavos, C., Katsinelos, P. Upper gastrointestinal carcinogenesis: H. pylori and stem cell cross-talk. J. Surg. Res. 2011, 166, 255-264.
7. Fock, K.M., Ang, T.L. Epidemiology of Helicobacter pylori infection and gastric cancer in Asia. J. Gastroenterol. Hepatol. 2010, 25, 479-486.
8. Sakamoto, H., Yoshimura, K., Saeki, N., Katai, H., Shimoda, T., Matsuno, Y., Saito, D., Sugimura, H., Tanioka, F., Kato S., et al. Genetic variation in PSCA is associated with susceptibility to diffuse-type gastric cancer. Nat. Genet. 2008, 40, 730-740.
9. Saeki, N., Saito, A., Choi, I.J., Matsuo, K., Ohnami, S., Totsuka, H., Chiku, S., Kuchiba, A., Lee, Y.S., Yoon, K.A., et al. A functional single nucleotide polymorphism in mucin 1, at chromosome 1q22, determines susceptibility to diffuse-type gastric cancer. Gastroenterology 2011, 140, 892-902.
10. Shi, Y., Hu, Z., Wu, C., Dai, J., Li, H., Dong, J., Wang, M., Miao, X., Zhou, Y., Lu, F., et al. A genome-wide association study identifies new susceptibility loci for non-cardia gastric cancer at 3q13.31 and 5p13.1. Nat. Genet. 2011, 43, 1215-1218.
11. Abnet, C.C., Freedman, N.D., Hu, N., Wang, Z., Yu, K., Shu, X.O., Yuan, J.M., Zheng, W., Dawsey, S.M., Dong, L.M., et al. A shared susceptibility locus in PLCE1 at 10q23 for gastric adenocarcinoma and esophageal squamous cell carcinoma. Nat. Genet. 2010, 42, 764-767.
12. Gibson, G. Rare and common variants: Twenty arguments. Nat. Rev. Genet. 2012, 13, 135-145.
13. Palmer, L.J., Cardon, L.R. Shaking the tree: Mapping complex disease genes with linkage disequilibrium. Lancet 2005, 366, 1223-1234.
14. Hirakawa, M., Tanaka, T., Hashimoto, Y., Kuroda, M., Takagi, T., Nakamura, Y. JSNP: A database of common gene variations in the Japanese population. Nucleic Acids Res. 2002, 30, 158-162.
15. Yoshida, T., Ono, H., Kuchiba, A., Saeki, N., Sakamoto, H. Genome-wide germline analyses on cancer susceptibility and GeMDBJ database: Gastric cancer as an example. Cancer Sci. 2010, 101, 1582-1589.
16. Miki, D., Kubo, M., Takahashi, A., Yoon, K.A., Kim, J., Lee, G.K., Zo, J.I., Lee, J.S., Hosono, N., Morizono, T., et al. Variation in TP63 is associated with lung adenocarcinoma susceptibility in Japanese and Korean populations. Nat. Genet. 2010, 42, 893-896.
17. Aoki, A., Ozaki, K., Sato, H., Takahashi, A., Kubo, M., Sakata, Y., Onouchi, Y., Kawaguchi, T., Lin, T.H., Takano, H., et al. SNPs on chromosome 5p15.3 associated with myocardial infarction in Japanese population. J. Hum. Genet. 2011, 56, 47-51.
18. Hirota, T., Takahashi, A., Kubo, M., Tsunoda, T., Tomita, K., Doi, S., Fujita, K., Miyatake, A., Enomoto, T., Miyagawa, T., et al. Genome-wide association study identifies three new susceptibility loci for adult asthma in the Japanese population. Nat. Genet. 2011, 43, 893-896.
19. Low, S.K., Takahashi, A., Cha, P.C., Zembutsu, H., Kamatani, N., Kubo, M., Nakamura, Y. Genome-wide association study for intracranial aneurysm in the Japanese population identifies three candidate susceptible loci and a functional genetic variant at EDNRA. Hum. Mol. Genet. 2012, 21, 2102-2110.
20. Onouchi, Y., Ozaki, K., Burns, J.C., Shimizu, C., Terai, M., Hamada, H., Honda, T., Suzuki, H., Suenaga, T., Takeuchi, T., et al. A genome-wide association study identifies three new risk loci for Kawasaki disease. Nat. Genet. 2012, 44, 517-521.
21. Wu, C., Wang, G., Yang, M., Huang, L., Yu, D., Tan, W., Lin, D. Two genetic variants in prostate stem cell antigen and gastric cancer susceptibility in a Chinese population. Mol. Carcinog. 2009, 48, 1131-1138.
22. Matsuo, K., Tajima, K., Suzuki, T., Kawase, T., Watanabe, M., Shitara, K., Misawa, K., Ito, S., Sawaki, A., Muro, K., et al. Association of prostate stem cell antigen gene polymorphisms with the risk of stomach cancer in Japanese. Int. J. Cancer 2009, 125, 1961-1964.
23. Lu, Y., Chen, J., Ding, Y., Jin, G., Wu, J., Huang, H., Deng, B., Hua, Z., Zhou, Y., Shu, Y., et al. Genetic variation of PSCA gene is associated with the risk of both diffuse- and intestinal-type gastric cancer in a Chinese population. Int. J. Cancer 2010, 127, 2183-2189.
24. Ou, J., Li, K., Ren, H., Bai, H., Zeng, D., Zhang, C. Association and haplotype analysis of prostate stem cell antigen with gastric cancer in Tibetans. DNA Cell Biol. 2010, 29, 319-323.
25. Lochhead, P., Frank, B., Hold, G.L., Rabkin, C.S., Ng, M.T., Vaughan, T.L., Risch, H.A., Gammon, M.D., Lissowska, J., Weck, M.N., et al. Genetic variation in the prostate stem cell antigen gene and upper gastrointestinal cancer in white individuals. Gastroenterology 2011, 140, 435-441.
26. Zeng, Z., Wu, X., Chen, F., Yu, J., Xue, L., Hao, Y., Wang, Y., Chen, M., Sung, J.J., Hu, P. Polymorphisms in prostate stem cell antigen gene rs2294008 increase gastric cancer risk in Chinese. Mol. Carcinog. 2011, 50, 353-358.
27. Song, H.R., Kim, H.N., Piao, J.M., Kweon, S.S., Choi, J.S., Bae, W.K., Chung, I.J., Park, Y.K., Kim, S.H., Choi, Y.D., et al. Association of a common genetic variant in prostate stem-cell antigen with gastric cancer susceptibility in a Korean population. Mol. Carcinog. 2011, 50, 871-875.
28. Sala, N., Muñoz, X., Travier, N., Agudo, A., Duell, E.J., Moreno, V., Overvad, K., Tjonneland, A., Boutron-Ruault, M.C. Clavel-Chapelon, F., et al. Prostate stem-cell antigen gene is associated with diffuse and intestinal gastric cancer in Caucasians: Results from the EPIC-EURGAST study. Int. J. Cancer 2011, 130, 2417-2427.
29. Ng, W., Loh, A.X., Teixeira, A.S., Pereira, S.P., Swallow, D.M. Genetic regulation of MUC1 alternative splicing in human tissues. Br. J. Cancer 2008, 99, 978-985.
30. Song, H.R., Kim, H.N., Kweon, S.S., Choi, J.S., Shim, H.J., Cho, S.H., Chung, I.J., Park, Y.K., Kim, S.H., Choi, Y.D., et al. Common genetic variants at 1q22 and 10q23 and gastric cancer susceptibility in a Korean population. Tumour Biol. 2014, 35, 3133-3137.
31. Xu, Q., Yuan, Y., Sun, L.P., Gong, Y.H., Xu, Y., Yu, X.W., Dong, N.N., Lin, G.D., Smith, P.N., Li, R.W. Risk of gastric cancer is associated with the MUC1 568 A/G polymorphism. Int. J. Oncol. 2009, 35, 1313-1320.
32. Li, F., Zhong, M.Z., Li, J.H., Liu, W., Li, B. Case-control study of single nucleotide polymorphisms of PSCA and MUC1 genes with gastric cancer in a Chinese. Asian Pac. J. Cancer Prev. 2012, 13, 2593-2596.
33. Jia, Y., Persson, C., Hou, L., Zheng, Z., Yeager, M., Lissowska, J., Chanock, S.J., Chow, W.H., Ye, W. A comprehensive analysis of common genetic variation in MUC1, MUC5AC, MUC6 genes and risk of stomach cancer. Cancer Causes Control 2010, 21, 313-321.
34. Palmer, A.J., Lochhead, P., Hold, G.L., Rabkin, C.S., Chow, W.H., Lissowska, J., Vaughan, T.L., Berry, S., Gammon, M., Risch, H., et al. Genetic variation in C20orf54, PLCE1 and MUC1 and the risk of upper gastrointestinal cancers in Caucasian populations. Eur. J. Cancer Prev. 2013, 21, 541-544.
35. Zheng, L., Zhu, C., Gu, J., Xi, P., Du, J., Jin, G. Functional polymorphism rs4072037 in MUC1 gene contributes to the susceptibility to gastric cancer: evidence from pooled 6580 cases and 10,324 controls. Mol. Biol. Rep. 2013, 40, 5791-5796.
36. Carvalho, F., Seruca, R., David, L., Amorim, A., Seixas, M., Bennett, E., Clausen, H., Sobrinho-Simões, M. MUC1 gene polymorphism and gastric cancer-An epidemiological study. Glycoconj. J. 1997, 14, 107-111.
37. Ho, S.B., Niehans, G.A., Lyftogt, C., Yan, P.S., Cherwitz, D.L., Gum, E.T., Dahiya, R., Kim, Y.S. Heterogeneity of mucin gene expression in normal and neoplastic tissues. Cancer Res. 1993, 53, 641-651.
38. Ho, S.B., Shekels, L.L., Toribara, N.W., Kim, Y.S., Lyftogt, C., Cherwitz, D.L., Niehans, G.A. Mucin gene expression in normal, preneoplastic, and neoplastic human gastric epithelium. Cancer Res. 1995, 55, 2681-2690.
39. Utsunomiya, T., Yonezawa, S., Sakamoto, H., Kitamura, H., Hokita, S., Aiko, T., Tanaka, S., Irimura, T., Kim, Y.S., Sato, E. Expression of MUC1 and MUC2 mucins in gastric carcinomas: its relationship with the prognosis of the patients. Clin. Cancer Res. 1998, 4, 2605-2614.
40. Reis, C.A., David, L., Seixas, M., Burchell, J., Sobrinho-Simões, M. Expression of fully and under-glycosylated forms of MUC1 mucin in gastric carcinoma. Int. J. Cancer 1998, 79, 402-410.
41. Lee, H.S., Lee, H.K., Kim, H.S., Yang, H.K., Kim, Y.I., Kim, W.H. MUC1, MUC2, MUC5AC, and MUC6 expressions in gastric carcinomas: Their roles as prognostic indicators. Cancer 2001, 92, 1427-1434.
42. Wang, R.Q., Fang, D.C. Alterations of MUC1 and MUC3 expression in gastric carcinoma: Relevance to patient clinicopathological features. J. Clin. Pathol. 2003, 56, 378-384.
43. Wang, J.Y., Chang, C.T., Hsieh, J.S., Lee, L.W., Huang, T.J., Chai, C.Y., Lin, S.R. Role of MUC1 and MUC5AC expressions as prognostic indicators in gastric carcinomas. J. Surg. Oncol. 2003, 83, 253-260.
44. Barresi, V., Vitarelli, E., Grosso, M., Tuccari, G., Barresi, G. Relationship between immunoexpression of mucin peptide cores MUC1 and MUC2 and Lauren's histologic subtypes of gastric carcinomas. Eur. J. Histochem. 2006, 50, 301-309.
45. Kocer, B., Soran, A., Kiyak, G., Erdogan, S., Eroglu, A., Bozkurt, B., Solak, C., Cengiz, O. Prognostic significance of mucin expression in gastric carcinoma. Dig. Dis. Sci. 2004, 49, 954-964.
46. Terada, T. An immunohistochemical study of primary signet-ring cell carcinoma of the stomach and colorectum: II. Expression of MUC1, MUC2, MUC5AC, and MUC6 in normal mucosa and in 42 cases. Int. J. Clin. Exp. Pathol. 2013, 6, 613-621.
47. Tanaka, M., Kitajima, Y., Sato, S., Miyazaki, K. Combined evaluation of mucin antigen and E-cadherin expression may help select patients with gastric cancer suitable for minimally invasive therapy. Br. J. Surg. 2003, 90, 95-101.
48. Ohno, T., Aihara, R., Kamiyama, Y., Mochiki, E., Asao, T., Kuwano, H. Prognostic significance of combined expression of MUC1 and adhesion molecules in advanced gastric cancer. Eur. J. Cancer 2006, 42, 256-263.
49. Owen, D.A. Stomach. In Histology for Pathologists, Mills, S.E., Ed., Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2007, p. 589.
50. Reis, C.A., David, L., Correa, P., Carneiro, F., de Bolós, C., Garcia, E., Mandel, U., Clausen, H, Sobrinho-Simões, M. Intestinal metaplasia of human stomach displays distinct patterns of mucin (MUC1, MUC2, MUC5AC, and MUC6) expression. Cancer Res. 1999, 59, 1003-1007.
51. Vernygorodskyi, S. Immunohistochemical evaluation of mucin expression in precancerous tissue of stomach. Exp. Oncol. 2013, 35, 114-117.
52. Jonckheere, N, van Seuningen, I. The membrane-bound mucins: From cell signalling to transcriptional regulation and expression in epithelial cancers. Biochimie 2010, 92, 1-11.
53. Bafna, S., Kaur, S., Batra, S.K. Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 2010, 29, 2893-2904.
54. Kufe, D.W. Mucins in cancer: Function, prognosis and therapy. Nat. Rev. Cancer 2009, 9, 874-885.
55. Gendler, S.J. MUC1, the renaissance molecule. Mammary Gland Biol. Neoplasia 2001, 6, 339-353.
56. McAuley, J.L., Linden, S.K., Png, C.W., King, R.M., Pennington, H.L., Gendler, S.J., Florin, T.H., Hill, G.R., Korolik, V., McGuckin, M.A. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J. Clin. Investig. 2007, 117, 2313-2324.
57. Lindén, S.K., Sheng, Y.H., Every, A.L., Miles, K.M., Skoog, E.C., Florin, T.H., Sutton, P., McGuckin, M.A. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog. 2009, 5, e1000617.
58. McGuckin, M.A., Every, A.L., Skene, C.D., Linden, S.K., Chionh, Y.T., Swierczak, A., McAuley, J., Harbour, S., Kaparakis, M., Ferrero, R., et al. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis. Gastroenterology 2007, 133, 1210-1218.
59. Vinall, L.E., King, M., Novelli, M., Green, C.A., Daniels, G., Hilkens, J., Sarner, M., Swallow, D.M. Altered expression and allelic association of the hypervariable membrane mucin MUC1 in Helicobacter pylori gastritis. Gastroenterology 2002, 123, 41-49.
60. Li, M., Huang, L., Qiu, H., Fu, Q., Li, W., Yu, Q., Sun, L., Zhang, L., Hu, G., Hu, J., et al. Helicobacter pylori infection synergizes with three inflammation-related genetic variants in the GWASs to increase risk of gastric cancer in a Chinese population. PLoS One 2013, 8, e74976.
61. Carson, D.D. The cytoplasmic tail of MUC1: A very busy place. Sci. Signal. 2008, 1, doi:10.1126/scisignal.127pe35.
62. Behrens, M.E., Grandgenett, P.M., Bailey, J.M., Singh, P.K., Yi, C.H., Yu, F., Hollingsworth, M.A. The reactive tumor microenvironment: MUC1 signaling directly reprograms transcription of CTGF. Oncogene 2010, 29, 5667-5677.
63. Masckauchán, T.N., Shawber, C.J., Funahashi, Y., Li, C.M., Kitajewski, J. Wnt/beta-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells. Angiogenesis 2005, 8, 43-51.
64. Murata-Kamiya, N., Kurashima, Y., Teishikata, Y., Yamahashi, Y., Saito, Y., Higashi, H., Aburatani, H., Akiyama, T., Peek, R.M., Jr., Azuma, T., et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene 2007, 26, 4617-4626.
65. Lévy, L., Neuveut, C., Renard, C.A., Charneau, P., Branchereau, S., Gauthier, F., van Nhieu, J.T., Cherqui, D., Petit-Bertron, A.F., Mathieu, D., et al. Transcriptional activation of interleukin-8 by β-catenin-Tcf4. J. Biol. Chem. 2002, 277, 42386-42393.
66. Guang, W., Twaddell, W.S., Lillehoj, E.P. Molecular Interactions between MUC1 Epithelial Mucin, β-Catenin, and CagA Proteins. Front. Immunol. 2012, 3, doi:10.3389/fimmu.2012.00105.
67. Park, Y.S., Guang, W., Blanchard, T.G., Kim, K.C., Lillehoj, E.P. Suppression of IL-8 production in gastric epithelial cells by MUC1 mucin and peroxisome proliferator-associated receptor-γ. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303, G765-G774.
68. Guang, W., Czinn, S.J., Blanchard, T.G., Kim, K.C., Lillehoj, E.P. Genetic regulation of MUC1 expression by Helicobacter pylori in gastric cancer cells. Biochem. Biophys. Res. Commun. 2014, 445, 145-150.
69. Perrais, M., Rousseaux, C., Ducourouble, M.P., Courcol, R., Vincent, P., Jonckheere, N., van Seuningen, I. Helicobacter pylori urease and flagellin alter mucin gene expression in human gastric cancer cells. Gastric Cancer 2014, 17, 235-246.
70. Navabi, N., Johansson, M.E., Raghavan, S., Lindén, S.K. Helicobacter pylori infection impairs the mucin production rate and turnover in the murine gastric mucosa. Infect. Immun. 2013, 81, 829-837.
71. Wei, X., Xu, H., Kufe, D. Human mucin 1 oncoprotein represses transcription of the p53 tumor suppressor gene. Cancer Res. 2007, 67, 1853-1858.
72. Weinberg, R.A. The Biology of Cancer, Garland Science: New York, NY, USA, 2007.
73. Raina, D., Kharbanda, S., Kufe, D. The MUC1 oncoprotein activates the anti-apoptotic phosphoinositide 3-kinase/Akt and Bcl-xL pathways in rat 3Y1 fibroblasts. J. Biol. Chem. 2004, 279, 20607-20612.
74. Raina, D., Ahmad, R., Kumar, S., Ren, J., Yoshida, K., Kharbanda, S., Kufe, D. MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J. 2006, 25, 3774-3783.
75. Rahn, J.J., Chow, J.W., Horne, G.J., Mah, B.K., Emerman, J.T., Hoffman, P., Hugh, J.C. MUC1 mediates transendothelial migration in vitro by ligating endothelial cell ICAM-1. Clin. Exp. Metastasis 2005, 22, 475-483.
76. Hikita, S.T., Kosik, K.S., Clegg, D.O., Bamdad, C. MUC1* mediates the growth of human pluripotent stem cells. PLoS One 2008, 3, e3312.
77. Stroopinsky, D., Rosenblatt, J., Ito, K., Mills, H., Yin, L., Rajabi, H., Vasir, B., Kufe, T., Luptakova, K., Arnason, J., et al. MUC1 is a potential target for the treatment of acute myeloid leukemia stem cells. Cancer Res. 2013, 73, 5569-5579.
78. Mehla, K., Singh, P.K. MUC1: A novel metabolic master regulator. Biochim. Biophys. Acta 2014, 1845, 126-135.
79. Saeki, N., Ono, H., Sakamoto, H., Yoshida, T. Genetic factors related to gastric cancer susceptibility identified using a genome-wide association study. Cancer Sci. 2013, 104, 1-8.