Year 2024 / Volume 116 / Number 3
Review
Prognostic analysis of Yes-associated protein 1 in patients with colorectal cancer. A systematic review and meta-analysis

148-156

DOI: 10.17235/reed.2022.8472/2021

Hui Zhang, Mengqi Yin, Yu Hu, Mingming Jiang, Mingliang Lu, Yajuan Wu,

Abstract
Background: colorectal cancer (CRC) is the most common carcinoma worldwide, but a lack of effective prognostic markers limits clinical diagnosis and treatment. Yes-associated protein 1 (YAP1) is an effector of the HIPPO-pathway, which plays a critical role in cancer development and prognosis, including CRC. However, previous reports have suggested that it plays a dual role in CRC. Methods: a meta-analysis using RevMan 5.4 and Stata 14.0 was performed to evaluate the relationship between YAP1 and clinical outcomes of CRC, after searching for eligible studies in the PubMed, Web of Science and Embase databases. Online datasets GEPIA and LOGpc were also used to calculate survival results and for comparison with the meta-analysis results. Besides, “DESeq” packages were used for the expression analysis of YAP1 from the TCGA dataset. Results: YAP1 was overexpressed in the cancer tissues when compared to normal tissues in patients with CRC from the TCGA database (p = 0.000164) and GEPIA database. A total of 10 studies involving 2305 patients from the literature were selected. Pooled HR indicated that overexpression of YAP1 was associated with poor clinical outcomes (HR = 1.70, 95 % CI: 1.28-2.26, p = 0.0003). Subgroup analysis showed a clear correlation between overexpression of YAP1 and worse survival rate in Chinese patients (HR = 1.94, 95 % CI: 1.40-2.69, p = 0.0001), nuclear YAP1 overexpression (HR = 2.07, 95 % CI: 1.29-3.31, p = 0.003), 60 months of follow-up (HR = 1.89, 95 % CI: 1.30-2.73, p = 0.0008), IHC test (HR = 1.65, 95 % CI: 1.17-2.33, p = 0.005), IHC combined with other tests (HR = 1.77, 95 % CI: 1.13-2.77, p = 0.01) and multivariate analysis (HR = 1.70, 95 % CI: 1.24-2.31, p = 0.0009). Nevertheless, disease-free survival (DFS) showed no significant results in the patients with CRC in our meta-analysis (HR = 1.38, 95 % CI: 0.51-3.75, p = 0.52) as well as in the GEPIA and LOGpc databases. Meanwhile, YAP1 overexpression was also significantly associated with worse overall survival (OS) in GSE17536, GSE40967, GSE29623 and GSE71187. Conclusion: YAP1 overexpression is common in CRC tissues. Overexpression of YAP1 in CRC patients, particularly in the nucleus, might be related to shorter OS, maybe in the early stages. YAP1 could serve as a potential predictor of poor prognosis in CRC.
Share Button
New comment
Comments
No comments for this article
References
1. Read, B. and P. Sylla, Aggressive Colorectal Cancer in the Young. Clin Colon Rectal Surg, 2020. 33(5): p. 298-304.
2. Recio-Boiles, A. and B. Cagir, Colon Cancer, in StatPearls. 2021: Treasure Island (FL).
3. Dekker, E., et al., Colorectal cancer. Lancet, 2019. 394(10207): p. 1467-1480.
4. Gu, M. and S. Thapa, Colorectal cancer in the United States and a review of its heterogeneity among Asian American subgroups. Asia Pac J Clin Oncol, 2020. 16(4): p. 193-200.
5. Fisher, K.W., et al., Precision medicine in colorectal cancer: evolving genomic landscape and emerging consensus. Future Oncol, 2015. 11(19): p. 2711-2719.
6. Hardingham, J.E., et al., Detection and Clinical Significance of Circulating Tumor Cells in Colorectal Cancer--20 Years of Progress. Mol Med, 2015. 21 Suppl 1: p. S25-31.
7. Edgar, B.A., From cell structure to transcription: Hippo forges a new path. Cell, 2006. 124(2): p. 267-73.
8. Hong, A.W., Z. Meng, and K.L. Guan, The Hippo pathway in intestinal regeneration and disease. Nat Rev Gastroenterol Hepatol, 2016. 13(6): p. 324-37.
9. Meng, Z., T. Moroishi, and K.L. Guan, Mechanisms of Hippo pathway regulation. Genes Dev, 2016. 30(1): p. 1-17.
10. Moroishi, T., C.G. Hansen, and K.L. Guan, The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer, 2015. 15(2): p. 73-79.
11. Matallanas, D., et al., RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol Cell, 2007. 27(6): p. 962-75.
12. Murakami, S., et al., Yes-associated protein mediates immune reprogramming in pancreatic ductal adenocarcinoma. Oncogene, 2017. 36(9): p. 1232-1244.
13. Wu, H., et al., Clinicopathological and prognostic significance of Yes-associated protein expression in hepatocellular carcinoma and hepatic cholangiocarcinoma. Tumour Biol, 2016. 37(10): p. 13499-13508.
14. Liu, J.Y., et al., Overexpression of YAP 1 contributes to progressive features and poor prognosis of human urothelial carcinoma of the bladder. BMC Cancer, 2013. 13: p. 349.
15. Wang, Y., et al., Overexpression of yes-associated protein contributes to progression and poor prognosis of non-small-cell lung cancer. Cancer Sci, 2010. 101(5): p. 1279-85.
16. Yan, H., et al., Yap regulates gastric cancer survival and migration via SIRT1/Mfn2/mitophagy. Oncol Rep, 2018. 39(4): p. 1671-1681.
17. Konsavage, W.M., Jr., et al., Wnt/beta-catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells. J Biol Chem, 2012. 287(15): p. 11730-9.
18. Yuan, M., et al., Yes-associated protein (YAP) functions as a tumor suppressor in breast. Cell Death Differ, 2008. 15(11): p. 1752-9.
19. Barry, E.R., et al., Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature, 2013. 493(7430): p. 106-10.
20. Cottini, F., et al., Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers. Nat Med, 2014. 20(6): p. 599-606.
21. Xu, Z., et al., YAP Levels Combined with Plasma CEA Levels Are Prognostic Biomarkers for Early-Clinical-Stage Patients of Colorectal Cancer. Biomed Res Int, 2019. 2019: p. 2170830.
22. Li, H.L., et al., A review: hippo signaling pathway promotes tumor invasion and metastasis by regulating target gene expression. J Cancer Res Clin Oncol, 2021. 147(6): p. 1569-1585.
23. Dong, T., et al., High cytoplasmic YAP1 expression predicts a poor prognosis in patients with colorectal cancer. PeerJ, 2020. 8.
24. Wang, Y., et al., Clinical and prognostic significance of Yes-associated protein in colorectal cancer. Tumour Biol, 2013. 34(4): p. 2169-74.
25. Yang, R., et al., Tumour YAP1 and PTEN expression correlates with tumour-associated myeloid suppressor cell expansion and reduced survival in colorectal cancer. Immunology, 2018. 155(2): p. 263-272.
26. Wang, L., et al., Overexpression of YAP and TAZ is an independent predictor of prognosis in colorectal cancer and related to the proliferation and metastasis of colon cancer cells. PLoS One, 2013. 8(6): p. e65539.
27. Zhang, S., et al., Loss of Yes-associated Protein Represents an Aggressive Subtype of Colorectal Cancer. J Cancer, 2019. 10(3): p. 689-696.
28. Tierney, J.F., et al., Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007. 8: p. 16.
29. Kim, J.Y., et al., VGLL4 with low YAP expression is associated with favorable prognosis in colorectal cancer. Apmis, 2020. 128(10): p. 543-551.
30. Ou, C., et al., MiR-590-5p, a density-sensitive microRNA, inhibits tumorigenesis by targeting YAP1 in colorectal cancer. Cancer Letters, 2017. 399: p. 53-63.
31. Sun, Z., et al., YAP1-induced MALAT1 promotes epithelial-mesenchymal transition and angiogenesis by sponging miR-126-5p in colorectal cancer. Oncogene, 2019. 38(14): p. 2627-2644.
32. Kim, D.H., et al., Differential expression of Yes-associated protein and phosphorylated Yes-associated protein is correlated with expression of Ki-67 and phospho-ERK in colorectal adenocarcinoma. Histol Histopathol, 2013. 28(11): p. 1483-90.
33. Weinstein, P.S., et al., Acute-phase proteins or tumour markers: the role of SAA, SAP, CRP and CEA as indicators of metastasis in a broad spectrum of neoplastic diseases. Scand J Immunol, 1984. 19(3): p. 193-8.
34. Duffy, M.J., et al., Tumour markers in colorectal cancer: European Group on Tumour Markers (EGTM) guidelines for clinical use. Eur J Cancer, 2007. 43(9): p. 1348-60.
35. Zhou, D., et al., Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci U S A, 2011. 108(49): p. E1312-20.
36. Steinhardt, A.A., et al., Expression of Yes-associated protein in common solid tumors. Hum Pathol, 2008. 39(11): p. 1582-9.
1. READ B, SYLLA P. Aggressive Colorectal Cancer in the Young[J]. Clin Colon Rectal Surg, 2020,33(5):298-304.
2. RECIO-BOILES A, CAGIR B. Colon Cancer. StatPearls. Treasure Island (FL)2021.
3. DEKKER E, TANIS P J, VLEUGELS J L A, et al. Colorectal cancer[J]. Lancet, 2019,394(10207):1467-1480.
4. GU M, THAPA S. Colorectal cancer in the United States and a review of its heterogeneity among Asian American subgroups[J]. Asia Pac J Clin Oncol, 2020,16(4):193-200.
5. FISHER K W, LOPEZ-BELTRAN A, MONTIRONI R, et al. Precision medicine in colorectal cancer: evolving genomic landscape and emerging consensus[J]. Future Oncol, 2015,11(19):2711-2719.
6. HARDINGHAM J E, GROVER P, WINTER M, et al. Detection and Clinical Significance of Circulating Tumor Cells in Colorectal Cancer--20 Years of Progress[J]. Mol Med, 2015,21 Suppl 1:S25-31.
7. EDGAR B A. From cell structure to transcription: Hippo forges a new path[J]. Cell, 2006,124(2):267-273.
8. HONG A W, MENG Z, GUAN K L. The Hippo pathway in intestinal regeneration and disease[J]. Nat Rev Gastroenterol Hepatol, 2016,13(6):324-337.
9. MENG Z, MOROISHI T, GUAN K L. Mechanisms of Hippo pathway regulation[J]. Genes Dev, 2016,30(1):1-17.
10. MOROISHI T, HANSEN C G, GUAN K L. The emerging roles of YAP and TAZ in cancer[J]. Nat Rev Cancer, 2015,15(2):73-79.
11. MATALLANAS D, ROMANO D, YEE K, et al. RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein[J]. Mol Cell, 2007,27(6):962-975.
12. MURAKAMI S, SHAHBAZIAN D, SURANA R, et al. Yes-associated protein mediates immune reprogramming in pancreatic ductal adenocarcinoma[J]. Oncogene, 2017,36(9):1232-1244.
13. WU H, LIU Y, JIANG X W, et al. Clinicopathological and prognostic significance of Yes-associated protein expression in hepatocellular carcinoma and hepatic cholangiocarcinoma[J]. Tumour Biol, 2016,37(10):13499-13508.
14. LIU J Y, LI Y H, LIN H X, et al. Overexpression of YAP 1 contributes to progressive features and poor prognosis of human urothelial carcinoma of the bladder[J]. BMC Cancer, 2013,13:349.
15. WANG Y, DONG Q, ZHANG Q, et al. Overexpression of yes-associated protein contributes to progression and poor prognosis of non-small-cell lung cancer[J]. Cancer Sci, 2010,101(5):1279-1285.
16. YAN H, QIU C, SUN W, et al. Yap regulates gastric cancer survival and migration via SIRT1/Mfn2/mitophagy[J]. Oncol Rep, 2018,39(4):1671-1681.
17. KONSAVAGE W M, JR., KYLER S L, RENNOLL S A, et al. Wnt/beta-catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells[J]. J Biol Chem, 2012,287(15):11730-11739.
18. YUAN M, TOMLINSON V, LARA R, et al. Yes-associated protein (YAP) functions as a tumor suppressor in breast[J]. Cell Death Differ, 2008,15(11):1752-1759.
19. BARRY E R, MORIKAWA T, BUTLER B L, et al. Restriction of intestinal stem cell expansion and the regenerative response by YAP[J]. Nature, 2013,493(7430):106-110.
20. COTTINI F, HIDESHIMA T, XU C, et al. Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers[J]. Nat Med, 2014,20(6):599-606.
21. XU Z, WANG H, GAO L, et al. YAP Levels Combined with Plasma CEA Levels Are Prognostic Biomarkers for Early-Clinical-Stage Patients of Colorectal Cancer[J]. Biomed Res Int, 2019,2019:2170830.
22. LI H L, LI Q Y, JIN M J, et al. A review: hippo signaling pathway promotes tumor invasion and metastasis by regulating target gene expression[J]. J Cancer Res Clin Oncol, 2021,147(6):1569-1585.
23. DONG T, YUAN Y, XIANG X, et al. High cytoplasmic YAP1 expression predicts a poor prognosis in patients with colorectal cancer[J]. PeerJ, 2020,8.
24. WANG Y, XIE C, LI Q, et al. Clinical and prognostic significance of Yes-associated protein in colorectal cancer[J]. Tumour Biol, 2013,34(4):2169-2174.
25. YANG R, CAI T-T, WU X-J, et al. Tumour YAP1 and PTEN expression correlates with tumour-associated myeloid suppressor cell expansion and reduced survival in colorectal cancer[J]. Immunology, 2018,155(2):263-272.
26. WANG L, SHI S, GUO Z, et al. Overexpression of YAP and TAZ is an independent predictor of prognosis in colorectal cancer and related to the proliferation and metastasis of colon cancer cells[J]. PLoS One, 2013,8(6):e65539.
27. ZHANG S, WEI Q, YANG Y, et al. Loss of Yes-associated Protein Represents an Aggressive Subtype of Colorectal Cancer[J]. J Cancer, 2019,10(3):689-696.
28. TIERNEY J F, STEWART L A, GHERSI D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis[J]. Trials, 2007,8:16.
29. KIM J Y, KIM E K, LEE W M, et al. VGLL4 with low YAP expression is associated with favorable prognosis in colorectal cancer[J]. Apmis, 2020,128(10):543-551.
30. OU C, SUN Z, PENG Q, et al. MiR-590-5p, a density-sensitive microRNA, inhibits tumorigenesis by targeting YAP1 in colorectal cancer[J]. Cancer Letters, 2017,399:53-63.
31. SUN Z, OU C, LIU J, et al. YAP1-induced MALAT1 promotes epithelial-mesenchymal transition and angiogenesis by sponging miR-126-5p in colorectal cancer[J]. Oncogene, 2019,38(14):2627-2644.
32. KIM D H, KIM S H, LEE O J, et al. Differential expression of Yes-associated protein and phosphorylated Yes-associated protein is correlated with expression of Ki-67 and phospho-ERK in colorectal adenocarcinoma[J]. Histol Histopathol, 2013,28(11):1483-1490.
33. WEINSTEIN P S, SKINNER M, SIPE J D, et al. Acute-phase proteins or tumour markers: the role of SAA, SAP, CRP and CEA as indicators of metastasis in a broad spectrum of neoplastic diseases[J]. Scand J Immunol, 1984,19(3):193-198.
34. DUFFY M J, VAN DALEN A, HAGLUND C, et al. Tumour markers in colorectal cancer: European Group on Tumour Markers (EGTM) guidelines for clinical use[J]. Eur J Cancer, 2007,43(9):1348-1360.
35. ZHOU D, ZHANG Y, WU H, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance[J]. Proc Natl Acad Sci U S A, 2011,108(49):E1312-1320.
36. STEINHARDT A A, GAYYED M F, KLEIN A P, et al. Expression of Yes-associated protein in common solid tumors[J]. Hum Pathol, 2008,39(11):1582-1589.
Related articles

Letter

Vaginal lesion as first manifestation of colorectal disease

DOI: 10.17235/reed.2022.9270/2022

Review

Inflammatory bowel disease and solid organ transplantation

DOI: 10.17235/reed.2020.7361/2020

Original

Can we optimize CEA as a response marker in rectal cancer?

DOI: 10.17235/reed.2020.7321/2020

Review

New non-invasive biomarkers for colorectal cancer screening

DOI: 10.17235/reed.2020.7233/2020

Letter

Medullary colorectal carcinoma. Do we really know it?

DOI: 10.17235/reed.2020.6728/2019

Letter

The rectosigmoid junction: are limits important?

DOI: 10.17235/reed.2019.5983/2018

Editorial

Colorectal cancer screening and survival

DOI: 10.17235/reed.2018.5870/2018

Editorial

The right colon challenge

DOI: 10.17235/reed.2018.5544/2018

Letter to the Editor

Neuroendocrine tumors of the pancreas: keys issues in dealing with heterogeneity

DOI: 10.17235/reed.2017.4997/2017

Letter to the Editor

Pancreatic neuroendocrine tumors. Prognostic factors

DOI: 10.17235/reed.2017.5109/2017

Editorial

Pancreas neuroendocrine tumors - not so rare or benign

DOI: 10.17235/reed.2016.4672/2016

Letter to the Editor

Liver metastasis from colorectal cancer 12 years after liver transplantation

DOI: 10.17235/reed.2017.4507/2016

Review

Serrated lesions and serrated polyposis syndrome

DOI: 10.17235/reed.2017.4065/2015

Letter to the Editor

Endobronchial metastases of colorectal cancer

DOI: 10.17235/reed.2016.4080/2015

Citation tools
Zhang H, Yin M, Hu Y, Jiang M, Lu M, Wu Y, et all. Prognostic analysis of Yes-associated protein 1 in patients with colorectal cancer. A systematic review and meta-analysis. 8472/2021


Download to a citation manager

Download the citation for this article by clicking on one of the following citation managers:

Metrics
This article has received 220 visits.
This article has been downloaded 27 times.

Statistics from Dimensions


Statistics from Plum Analytics

Publication history

Received: 26/11/2021

Accepted: 21/09/2022

Online First: 30/09/2022

Published: 04/03/2024

Article revision time: 295 days

Article Online First time: 308 days

Article editing time: 829 days


Share
This article hasn't been rated yet.
Reader rating:
Valora este artículo:




Asociación Española de Ecografía Digestiva Sociedad Española de Endoscopia Digestiva Sociedad Española de Patología Digestiva
The Spanish Journal of Gastroenterology is the official organ of the Sociedad Española de Patología Digestiva, the Sociedad Española de Endoscopia Digestiva and the Asociación Española de Ecografía Digestiva
Cookie policy Privacy Policy Legal Notice © Copyright 2023 y Creative Commons. The Spanish Journal of Gastroenterology