SMO Expression in Colorectal Cancer: Associations with Clinical, Pathological, and Molecular Features

Annals of Surgical Oncology

Volumn 21, Issue 13, 2014, Pages 4164-4173

  Li, Tingting ^a,b   Liao, Xiaoyun ^a   Lochhead, Paul ^a   Morikawa, Teppei ^c   Yamauchi, Mai ^a   Nishihara, Reiko ^a,d   Inamura, Kentaro ^a,e   Kim, Sun A ^a   Mima, Kosuke ^a   Sukawa, Yasutaka ^a   Kuchiba, Aya ^a,d   Imamura, Yu ^a   Baba, Yoshifumi ^f   Shima, Kaori ^g   Meyerhardt, Jeffrey A ^a   Chan, Andrew T ^h   Fuchs, Charles S ^a,i   Ogino, Shuji ^a,d,i   Qian, Zhi Rong ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c UNIVERSITY OF TOKYO HOSPITAL   (Japan)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f KUMAMOTO UNIVERSITY   (Japan)

^g KAGOSHIMA UNIVERSITY   (Japan)

^h MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁱ BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; BETA CATENIN; DNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; WNT PROTEIN; BRAF PROTEIN, HUMAN; CTNNB1 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; KRAS PROTEIN, HUMAN; ONCOPROTEIN; PIK3CA PROTEIN, HUMAN; RAS PROTEIN; SMO PROTEIN, HUMAN; TUMOR MARKER;

AGED; ARTICLE; B RAF KINASE GENE; CANCER PROGNOSIS; CANCER SPECIFIC SURVIVAL; COLORECTAL CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME PHOSPHORYLATION; FEMALE; FOLLOW UP; GENE EXPRESSION; GENE MUTATION; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; ONCOGENE; ONCOGENE K RAS; OVERALL SURVIVAL; PIK3CA GENE; SURVIVAL RATE; SURVIVAL TIME; WILD TYPE; CLINICAL TRIAL; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; MULTICENTER STUDY; MUTATION; PATHOLOGY; PHENOTYPE; PROGNOSIS; PROSPECTIVE STUDY; SIGNAL TRANSDUCTION; UNITED STATES;

AGED; BETA CATENIN; BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MUTATION; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; PROGNOSIS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-AKT; RAS PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; UNITED STATES;

EID: 84911484541     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-014-3888-y     Document Type: Article

References (69)

1. Ogino S, Fuchs CS, Giovannucci E. How many molecular subtypes? Implications of the unique tumor principle in personalized medicine. Expert Rev Mol Diagn. 2012;12:621–8.
2. Funkhouser WK Jr, Lubin IM, Monzon FA, et al. Relevance, pathogenesis, and testing algorithm for mismatch repair-defective colorectal carcinomas: a report of the association for molecular pathology. J Mol Diagn. 2012;14:91–103.
3. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci. 2013;14:16365–85.
4. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers. 2013;5:676–713.
5. Kim JH, Kang GH. Molecular and prognostic heterogeneity of microsatellite-unstable colorectal cancer. World J Gastroenterol. 2014;20:4230–43.
6. Berman DM, Karhadkar SS, Maitra A, et al. Widespread requirement for hedgehog ligand stimulation in growth of digestive tract tumours. Nature. 2003;425:846–51.
7. Kolterud A, Grosse AS, Zacharias WJ, et al. Paracrine hedgehog signaling in stomach and intestine: new roles for hedgehog in gastrointestinal patterning. Gastroenterology. 2009;137:618–28.
8. Fendrich V, Oh E, Bang S, et al. Ectopic overexpression of sonic hedgehog (Shh) induces stromal expansion and metaplasia in the adult murine pancreas. Neoplasia. 2011;13:923–30.
9. Ng JM, Curran T. The hedgehog’s tale: developing strategies for targeting cancer. Nat Rev Cancer. 2011;11:493–501.
10. Teglund S, Toftgard R. Hedgehog beyond medulloblastoma and basal cell carcinoma. Biochim Biophys Acta. 2010;1805:181–208.
11. Michael LE, Westerman BA, Ermilov AN, et al. Bmi1 is required for hedgehog pathway-driven medulloblastoma expansion. Neoplasia. 2008;10:1343–9.
12. Zhang Y, Laterra J, Pomper MG. Hedgehog pathway inhibitor HhAntag691 is a potent inhibitor of ABCG2/BCRP and ABCB1/Pgp. Neoplasia. 2009;11:96–101.
13. Chatel G, Ganeff C, Boussif N, et al. Hedgehog signaling pathway is inactive in colorectal cancer cell lines. Int J Cancer. 2007;121:2622–7.
14. Oniscu A, James RM, Morris RG, Bader S, Malcomson RD, Harrison DJ. Expression of sonic hedgehog pathway genes is altered in colonic neoplasia. J Pathol. 2004;203:909–17.
15. Qualtrough D, Buda A, Gaffield W, Williams AC, Paraskeva C. Hedgehog signalling in colorectal tumour cells: induction of apoptosis with cyclopamine treatment. Int J Cancer. 2004;110:831–7.
16. Alinger B, Kiesslich T, Datz C, et al. Hedgehog signaling is involved in differentiation of normal colonic tissue rather than in tumor proliferation. Virchows Arch. 2009;454:369–79.
17. Mazumdar T, DeVecchio J, Shi T, Jones J, Agyeman A, Houghton JA. Hedgehog signaling drives cellular survival in human colon carcinoma cells. Cancer Res. 2011;71:1092–102.
18. Varnat F, Duquet A, Malerba M, et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med. 2009;1:338–51.
19. Saqui-Salces M, Merchant JL. Hedgehog signaling and gastrointestinal cancer. Biochim Biophys Acta. 2010;1803:786–95.
20. Akiyoshi T, Nakamura M, Koga K, et al. Gli1, downregulated in colorectal cancers, inhibits proliferation of colon cancer cells involving Wnt signalling activation. Gut. 2006;55:991–9.
21. Ding YL, Wang QS, Zhao WM, Xiang L. Expression of smoothened protein in colon cancer and its prognostic value for postoperative liver metastasis. Asian Pac J Cancer Prev. 2012;13:4001–5.
22. Arimura S, Matsunaga A, Kitamura T, Aoki K, Aoki M, Taketo MM. Reduced level of smoothened suppresses intestinal tumorigenesis by down-regulation of Wnt signaling. Gastroenterology. 2009;137:629–38.
23. Morris JPT, Wang SC, Hebrok M. KRAS, hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat Rev Cancer. 2010;10:683–95.
24. Riobo NA, Lu K, Ai X, Haines GM, Emerson CP Jr. Phosphoinositide 3-kinase and Akt are essential for sonic hedgehog signaling. Proc Natl Acad Sci USA. 2006;103:4505–10.
25. Madhala-Levy D, Williams VC, Hughes SM, Reshef R, Halevy O. Cooperation between Shh and IGF-I in promoting myogenic proliferation and differentiation via the MAPK/ERK and PI3K/Akt pathways requires Smo activity. J Cell Physiol. 2012;227:1455–64.
26. Yoo YA, Kang MH, Lee HJ, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res. 2011;71:7061–70.
27. Ogino S, Stampfer M. Lifestyle factors and microsatellite instability in colorectal cancer: the evolving field of molecular pathological epidemiology. J Natl Cancer Inst. 2010;102:365–7.
28. Ogino S, Chan AT, Fuchs CS, Giovannucci E. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut. 2011;60:397–411.
29. Liao X, Lochhead P, Nishihara R, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012;367:1596–606.
30. Yamauchi M, Morikawa T, Kuchiba A, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 2012;61:847–54.
31. Chan AT, Ogino S, Fuchs CS. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med. 2007;356:2131–42.
32. Kawasaki T, Nosho K, Ohnishi M, et al. IGFBP3 promoter methylation in colorectal cancer: relationship with microsatellite instability, CpG island methylator phenotype, and p53. Neoplasia. 2007;9:1091–8.
33. Baba Y, Nosho K, Shima K, et al. Phosphorylated AKT expression is associated with PIK3CA mutation, low stage, and favorable outcome in 717 colorectal cancers. Cancer. 2011;117:1399–408.
34. Morikawa T, Kuchiba A, Yamauchi M, et al. Association of CTNNB1 (beta-catenin) alterations, body mass index, and physical activity with survival in patients with colorectal cancer. JAMA. 2011;305:1685–94.
35. Dierks C, Grbic J, Zirlik K, et al. Essential role of stromally induced hedgehog signaling in B-cell malignancies. Nat Med. 2007;13:944–51.
36. Riobo NA, Saucy B, Dilizio C, Manning DR. Activation of heterotrimeric G proteins by smoothened. Proc Natl Acad Sci USA. 2006;103:12607–12.
37. Gerber AN, Wilson CW, Li YJ, Chuang PT. The hedgehog regulated oncogenes Gli1 and Gli2 block myoblast differentiation by inhibiting MyoD-mediated transcriptional activation. Oncogene. 2007;26:1122–36.
38. Liao X, Siu MK, Au CW, et al. Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis. 2009;30:131–40.
39. Imamura Y, Morikawa T, Liao X, et al. Specific mutations in KRAS codons 12 and 13, and patient prognosis in 1075 BRAF wild-type colorectal cancers. Clin Cancer Res. 2012;18:4753–63.
40. Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J Mol Diagn. 2006;8:582–8.
41. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009;58:90–6.
42. Liao X, Morikawa T, Lochhead P, et al. Prognostic role of PIK3CA mutation in colorectal cancer: cohort study and literature review. Clin Cancer Res. 2012;18:2257–68.
43. Hinoue T, Weisenberger DJ, Lange CP, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012;22:271–82.
44. Ogino S, Kawasaki T, Brahmandam M, et al. Precision and performance characteristics of bisulfite conversion and real-time PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagn. 2006;8:209–17.
45. Ogino S, Kawasaki T, Nosho K, et al. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 2008;122:2767–73.
46. Ogino S, Nosho K, Kirkner GJ, et al. A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst. 2008;100:1734–8.
47. Ogino S, Goel A. Molecular classification and correlates in colorectal cancer. J Mol Diagn. 2008;10:13–27.
48. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330–7.
49. Wang D, Xia D, Dubois RN. The crosstalk of PTGS2 and EGF signaling pathways in colorectal cancer. Cancers. 2011;3:3894–908.
50. Bertrand FE, Angus CW, Partis WJ, Sigounas G. Developmental pathways in colon cancer: crosstalk between WNT, BMP, hedgehog and Notch. Cell Cycle. 2012;11:4344–51.
51. Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology. 2010;138:2088–100.
52. Rosty C, Hewett DG, Brown IS, Leggett BA, Whitehall VL. Serrated polyps of the large intestine: current understanding of diagnosis, pathogenesis, and clinical management. J Gastroenterol. 2013;48:287–302.
53. Domingo E, Ramamoorthy R, Oukrif D, et al. Use of multivariate analysis to suggest a new molecular classification of colorectal cancer. J Pathol. 2013;229:441–8.
54. Hayashi Y, Molina JR, Hamilton SR, Georgescu MM. NHERF1/EBP50 is a new marker in colorectal cancer. Neoplasia. 2010;12:1013–22.
55. Soerjomataram I, Thong MS, Korfage IJ, et al. Excess weight among colorectal cancer survivors: target for intervention. J Gastroenterol. 2012;47:999–1005.
56. Wu KL, Huang EY, Jhu EW, et al. Overexpression of galectin-3 enhances migration of colon cancer cells related to activation of the K-Ras-Raf-Erk1/2 pathway. J Gastroenterol. 2013;48:350–9.
57. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer. 2009;9:550–62.
58. van den Brink GR, Bleuming SA, Hardwick JC, et al. Indian hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet. 2004;36:277–82.
59. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA. 1999;96:8681–6.
60. Beggs AD, Jones A, El-Bahrawy M, Abulafi M, Hodgson SV, Tomlinson IP. Whole-genome methylation analysis of benign and malignant colorectal tumours. J Pathol. 2013;229:697–704.
61. Yang Q, Dong Y, Wu W, et al. Detection and differential diagnosis of colon cancer by a cumulative analysis of promoter methylation. Nat Commun. 2012;3:1206.
62. Dahlin AM, Palmqvist R, Henriksson ML, et al. The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status. Clin Cancer Res. 2010;16:1845–55.
63. Zlobec I, Bihl M, Foerster A, Rufle A, Lugli A. Comprehensive analysis of CpG island methylator phenotype (CIMP)-high, -low, and -negative colorectal cancers based on protein marker expression and molecular features. J Pathol. 2011;225:336–43.
64. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol. 2011;8:686–700.
65. Hughes LA, Bakker CA, Smits KM, et al. The CpG island methylator phenotype in colorectal cancer: progress and problems. Biochim Biophys Acta. 2012;1825:77–85.
66. Price TJ, Hardingham JE, Lee CK, et al. Impact of KRAS and BRAF gene mutation status on outcomes from the phase III AGITG MAX trial of capecitabine alone or in combination with bevacizumab and mitomycin in advanced colorectal cancer. J Clin Oncol. 2011;29:2675–82.
67. Ogino S, Shima K, Meyerhardt JA, et al. Predictive and prognostic roles of BRAF mutation in stage III colon cancer: results from intergroup trial CALGB 89803. Clin Cancer Res. 2012;18:890–900.
68. Samowitz WS, Sweeney C, Herrick J, et al. Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res. 2005;65:6063–9.
69. Lochhead P, Kuchiba A, Imamura Y, et al. Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. J Natl Cancer Inst. 2013;105:1151–6.