Correlation of mucin 1 expression with prognosis and clinicopathologic characteristics in patients with colorectal cancer: a meta-analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

MA Fubin ^1,2 ,  YAO Nan ^1,2 , WANG Jun ² , JIANG Lei ² , MA Yuping ¹

1. The First Clinical Medical College of Lanzhou University, Lanzhou 730000, P. R. China;
2. Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding?author：

YAO Nan, Email: Pro_YaoNan@163.com

Keywords：

colorectal cancer; mucin 1; prognosis; meta-analysis

DOI：

10.7507/1007-9424.202101012

Video：

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Objective To systematically evaluate the effect of mucin 1 (MUC1) expression on the prognosis and clinicopathologic characteristics of patients with colorectal cancer.Methods The cohort studies on the relationship between MUC1 expression and the prognosis of colorectal cancer patients were retrieved from PubMed, Embase, Web of Science, Cochrane Library, CNKI, China Biology Medicine, WanFang, VIP, and other databases from the establishment of the database to December 2020. The two researchers screened the literatures according to the inclusion and exclusion criteria, extracted relevant data, and performed meta analysis using Stata 12.0 software.Results A total of 17 eligible studies comprising 2 516 patients with colorectal cancer were included. The results of meta-analysis showed that the overall survival (OS) of patients with high MUC1 expression was worse than that with low MUC1 expression [HR=1.51, 95%CI (1.33, 1.71), P<0.001], but not statistically significant with disease-free survival [HR=1.39, 95%CI (0.41, 4.68), P=0.565]. Subgroup analysis results showed the same results as the overall analysis regardless of analysis method (multivariate or survival curve), different ethnic groups (Asian or Caucasian), and different sample sizes (≥100 or <100). The results of clinicopathologic analysis showed that the high expression of MUC1 was correlated with lymph node metastasis, distant metastasis, depth of invasion, and TNM stage (P<0.05), but not correlated with gender, age, degree of tumor differentiation, and tumor location (P>0.05).Conclusions High expression of MUC1 is closely associated with poor prognosis, lymph node metastasis, distant metastasis, tumor invasion depth, and TNM stage in patients with colorectal cancer, which is expected to be an important reference indicator for disease monitoring and prognosis judgment of colorectal cancer.

Citation： MA Fubin, YAO Nan, WANG Jun, JIANG Lei, MA Yuping. Correlation of mucin 1 expression with prognosis and clinicopathologic characteristics in patients with colorectal cancer: a meta-analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(10): 1328-1333. doi: 10.7507/1007-9424.202101012 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2.	Miller KD, Nogueira L, Mariotto AB, et al. Cancer treatment and survivorship statistics, 2019. CA Cancer J Clin, 2019, 69(5): 363-385.
3.	Rubin G, Walter F, Emery J, et al. Reimagining the diagnostic pathway for gastrointestinal cancer. Nat Rev Gastroenterol Hepatol, 2018, 15(3): 181-188.
4.	Gao T, Cen Q, Lei H. A review on development of MUC1-based cancer vaccine. Biomed Pharmacother, 2020, 132: 110888.
5.	Jing X, Liang H, Hao C, et al. Overexpression of MUC1 predicts poor prognosis in patients with breast cancer. Oncol Rep, 2019, 41(2): 801-810.
6.	Heublein S, Friese K, Kost B, et al. TA-MUC1 as detected by the fully humanized, therapeutic antibody Gatipotzumab predicts poor prognosis in cervical cancer. J Cancer Res Clin Oncol, 2018, 144(10): 1899-1907.
7.	Nagai S, Takenaka K, Sonobe M, et al. A novel classification of MUC1 expression is correlated with tumor differentiation and postoperative prognosis in non-small cell lung cancer. J Thorac Oncol, 2006, 1(1): 46-51.
8.	Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007, 8: 16.
9.	Khanh do T, Mekata E, Mukaisho K, et al. Transmembrane mucin MUC1 overexpression and its association with CD10⁺myeloid cells, transforming growth factor-β1 expression, and tumor budding grade in colorectal cancer. Cancer Sci, 2013, 104(7): 958-964.
10.	Szlendak M, Sitarz R, Berbecka M, et al. Expression of cyclooxygenase-2 and mucin 1 in colorectal cancer. Mol Clin Oncol, 2020, 13(5): 52.
11.	王曉磊, 展鵬遠, 郭偉, 等. Gal-3和MUC1蛋白在結直腸癌中的表達及與預后的關系. 實用腫瘤雜志, 2016, 31(3): 250-254.
12.	魯明良, 何瑾, 葉衛東. MUC1聯合MUC2在結直腸腺瘤及結直腸癌中聯合表達與臨床病理的相關性研究. 結直腸肛門外科, 2014, 20(3): 158-163.
13.	Zhang W, Tang W, Inagaki Y, et al. Positive KL-6 mucin expression combined with decreased membranous beta-catenin expression indicates worse prognosis in colorectal carcinoma. Oncol Rep, 2008, 20(5): 1013-1019.
14.	Kasprzak A, Siod?a E, Andrzejewska M, et al. Differential expression of mucin 1 and mucin 2 in colorectal cancer. World J Gastroenterol, 2018, 24(36): 4164-4177.
15.	Sun Y, Wu X, Zhang Y, et al. Pathological complete response may underestimate distant metastasis in locally advanced rectal cancer following neoadjuvant chemoradiotherapy and radical surgery: Incidence, metastatic pattern, and risk factors. Eur J Surg Oncol, 2019, 45(7): 1225-1231.
16.	Baldus SE, Zirbes TK, Hanisch FG, et al. Thomsen-Friedenreich antigen presents as a prognostic factor in colorectal carcinoma: A clinicopathologic study of 264 patients. Cancer, 2000, 88(7): 1536-1543.
17.	Duncan TJ, Watson NF, Al-Attar AH, et al. The role of MUC1 and MUC3 in the biology and prognosis of colorectal cancer. World J Surg Oncol, 2007, 5: 31.
18.	Hiraga Y, Tanaka S, Haruma K, et al. Immunoreactive MUC1 expression at the deepest invasive portion correlates with prognosis of colorectal cancer. Oncology, 1998, 55(4): 307-319.
19.	Kimura T, Tanaka S, Haruma K, et al. Clinical significance of MUC1 and E-cadherin expression, cellular proliferation, and angiogenesis at the deepest invasive portion of colorectal cancer. Int J Oncol, 2000, 16(1): 55-64.
20.	Manne U, Weiss HL, Grizzle WE. Racial differences in the prognostic usefulness of MUC1 and MUC2 in colorectal adenocarcinomas. Clin Cancer Res, 2000, 6(10): 4017-4025.
21.	Perez RO, Bresciani BH, Bresciani C, et al. Mucinous colorectal adenocarcinoma: influence of mucin expression (Muc1, 2 and 5) on clinico-pathological features and prognosis. Int J Colorectal Dis, 2008, 23(8): 757-765.
22.	Baldus SE, M?nig SP, Hanisch FG, et al. Comparative evaluation of the prognostic value of MUC1, MUC2, sialyl-Lewis(a) and sialyl-Lewis(x) antigens in colorectal adenocarcinoma. Histopathology, 2002, 40(5): 440-449.
23.	Díaz Del Arco C, Garré P, Molina Roldán E, et al. MUC1 expression in colorectal carcinoma: Clinicopathological correlation and prognostic significance. Rev Esp Patol, 2018, 51(4): 204-209.
24.	You JF, Hsieh LL, Changchien CR, et al. Inverse effects of mucin on survival of matched hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer patients. Clin Cancer Res, 2006, 12(14 Pt 1): 4244-4250.
25.	于秀文, 榮瑋, 徐鳳琳, 等. 粘蛋白和上皮鈣粘附蛋白在結直腸腫瘤組織中的表達及其意義. 癌癥, 2007, 26(11): 1204-1210.
26.	Nath S, Mukherjee P. MUC1: a multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med, 2014, 20(6): 332-342.
27.	Sahraei M, Roy LD, Curry JM, et al. MUC1 regulates PDGFA expression during pancreatic cancer progression. Oncogene, 2012, 31(47): 4935-4945.
28.	Gao J, McConnell MJ, Yu B, et al. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol, 2009, 35(2): 337-345.
29.	Wang XT, Kong FB, Mai W, et al. MUC1 immunohistochemical expression as a prognostic factor in gastric cancer: meta-analysis. Dis Markers, 2016, 2016: 9421571.
30.	Lu H, Liang D, Zhu Y, et al. Prognostic and clinicopathological significance of MUC expression in head and neck cancer: a systematic review and meta-analysis. Oncotarget, 2017, 8(56): 96359-96372.
31.	Xu F, Liu F, Zhao H, et al. Prognostic significance of mucin antigen MUC1 in various human epithelial cancers: a meta-analysis. Medicine (Baltimore), 2015, 94(50): e2286.
32.	Zeng Y, Zhang Q, Zhang Y, et al. MUC1 predicts colorectal cancer metastasis: a systematic review and meta-analysis of case controlled studies. PLoS One, 2015, 10(9): e0138049.

1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2. Miller KD, Nogueira L, Mariotto AB, et al. Cancer treatment and survivorship statistics, 2019. CA Cancer J Clin, 2019, 69(5): 363-385.
3. Rubin G, Walter F, Emery J, et al. Reimagining the diagnostic pathway for gastrointestinal cancer. Nat Rev Gastroenterol Hepatol, 2018, 15(3): 181-188.
4. Gao T, Cen Q, Lei H. A review on development of MUC1-based cancer vaccine. Biomed Pharmacother, 2020, 132: 110888.
5. Jing X, Liang H, Hao C, et al. Overexpression of MUC1 predicts poor prognosis in patients with breast cancer. Oncol Rep, 2019, 41(2): 801-810.
6. Heublein S, Friese K, Kost B, et al. TA-MUC1 as detected by the fully humanized, therapeutic antibody Gatipotzumab predicts poor prognosis in cervical cancer. J Cancer Res Clin Oncol, 2018, 144(10): 1899-1907.
7. Nagai S, Takenaka K, Sonobe M, et al. A novel classification of MUC1 expression is correlated with tumor differentiation and postoperative prognosis in non-small cell lung cancer. J Thorac Oncol, 2006, 1(1): 46-51.
8. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007, 8: 16.
9. Khanh do T, Mekata E, Mukaisho K, et al. Transmembrane mucin MUC1 overexpression and its association with CD10⁺myeloid cells, transforming growth factor-β1 expression, and tumor budding grade in colorectal cancer. Cancer Sci, 2013, 104(7): 958-964.
10. Szlendak M, Sitarz R, Berbecka M, et al. Expression of cyclooxygenase-2 and mucin 1 in colorectal cancer. Mol Clin Oncol, 2020, 13(5): 52.
11. 王曉磊, 展鵬遠, 郭偉, 等. Gal-3和MUC1蛋白在結直腸癌中的表達及與預后的關系. 實用腫瘤雜志, 2016, 31(3): 250-254.
12. 魯明良, 何瑾, 葉衛東. MUC1聯合MUC2在結直腸腺瘤及結直腸癌中聯合表達與臨床病理的相關性研究. 結直腸肛門外科, 2014, 20(3): 158-163.
13. Zhang W, Tang W, Inagaki Y, et al. Positive KL-6 mucin expression combined with decreased membranous beta-catenin expression indicates worse prognosis in colorectal carcinoma. Oncol Rep, 2008, 20(5): 1013-1019.
14. Kasprzak A, Siod?a E, Andrzejewska M, et al. Differential expression of mucin 1 and mucin 2 in colorectal cancer. World J Gastroenterol, 2018, 24(36): 4164-4177.
15. Sun Y, Wu X, Zhang Y, et al. Pathological complete response may underestimate distant metastasis in locally advanced rectal cancer following neoadjuvant chemoradiotherapy and radical surgery: Incidence, metastatic pattern, and risk factors. Eur J Surg Oncol, 2019, 45(7): 1225-1231.
16. Baldus SE, Zirbes TK, Hanisch FG, et al. Thomsen-Friedenreich antigen presents as a prognostic factor in colorectal carcinoma: A clinicopathologic study of 264 patients. Cancer, 2000, 88(7): 1536-1543.
17. Duncan TJ, Watson NF, Al-Attar AH, et al. The role of MUC1 and MUC3 in the biology and prognosis of colorectal cancer. World J Surg Oncol, 2007, 5: 31.
18. Hiraga Y, Tanaka S, Haruma K, et al. Immunoreactive MUC1 expression at the deepest invasive portion correlates with prognosis of colorectal cancer. Oncology, 1998, 55(4): 307-319.
19. Kimura T, Tanaka S, Haruma K, et al. Clinical significance of MUC1 and E-cadherin expression, cellular proliferation, and angiogenesis at the deepest invasive portion of colorectal cancer. Int J Oncol, 2000, 16(1): 55-64.
20. Manne U, Weiss HL, Grizzle WE. Racial differences in the prognostic usefulness of MUC1 and MUC2 in colorectal adenocarcinomas. Clin Cancer Res, 2000, 6(10): 4017-4025.
21. Perez RO, Bresciani BH, Bresciani C, et al. Mucinous colorectal adenocarcinoma: influence of mucin expression (Muc1, 2 and 5) on clinico-pathological features and prognosis. Int J Colorectal Dis, 2008, 23(8): 757-765.
22. Baldus SE, M?nig SP, Hanisch FG, et al. Comparative evaluation of the prognostic value of MUC1, MUC2, sialyl-Lewis(a) and sialyl-Lewis(x) antigens in colorectal adenocarcinoma. Histopathology, 2002, 40(5): 440-449.
23. Díaz Del Arco C, Garré P, Molina Roldán E, et al. MUC1 expression in colorectal carcinoma: Clinicopathological correlation and prognostic significance. Rev Esp Patol, 2018, 51(4): 204-209.
24. You JF, Hsieh LL, Changchien CR, et al. Inverse effects of mucin on survival of matched hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer patients. Clin Cancer Res, 2006, 12(14 Pt 1): 4244-4250.
25. 于秀文, 榮瑋, 徐鳳琳, 等. 粘蛋白和上皮鈣粘附蛋白在結直腸腫瘤組織中的表達及其意義. 癌癥, 2007, 26(11): 1204-1210.
26. Nath S, Mukherjee P. MUC1: a multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med, 2014, 20(6): 332-342.
27. Sahraei M, Roy LD, Curry JM, et al. MUC1 regulates PDGFA expression during pancreatic cancer progression. Oncogene, 2012, 31(47): 4935-4945.
28. Gao J, McConnell MJ, Yu B, et al. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol, 2009, 35(2): 337-345.
29. Wang XT, Kong FB, Mai W, et al. MUC1 immunohistochemical expression as a prognostic factor in gastric cancer: meta-analysis. Dis Markers, 2016, 2016: 9421571.
30. Lu H, Liang D, Zhu Y, et al. Prognostic and clinicopathological significance of MUC expression in head and neck cancer: a systematic review and meta-analysis. Oncotarget, 2017, 8(56): 96359-96372.
31. Xu F, Liu F, Zhao H, et al. Prognostic significance of mucin antigen MUC1 in various human epithelial cancers: a meta-analysis. Medicine (Baltimore), 2015, 94(50): e2286.
32. Zeng Y, Zhang Q, Zhang Y, et al. MUC1 predicts colorectal cancer metastasis: a systematic review and meta-analysis of case controlled studies. PLoS One, 2015, 10(9): e0138049.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Correlation of mucin 1 expression with prognosis and clinicopathologic characteristics in patients with colorectal cancer: a meta-analysis

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