Review Article

Tumor Markers Involved in Invasion of Pancreatic Cancer

Abstract

Pancreatic cancer is still one of the most lethal malignancies across the world, and hence exploring new biomarkers related to the progression and invasive nature of this cancer is important to overcome its resistance to various types of treatments through the design of new therapeutic strategies. Several markers have been shown to play a role in pancreatic cancer invasion, but CA19-9, CA125, and noncoding RNAs, including microRNAs, long noncoding RNAs, and circular RNAs, are the most common ones. In the current review, the role of these markers in pancreatic cancer progression, invasion, and metastasis, as well as related mechanisms, has been provided, and their potential to be utilized in pancreatic cancer diagnosis and treatment has been discussed.

1. Mizrahi JD, Surana R, Valle JW, Shroff RT. Pancreatic cancer. Lancet. 2020;395(10242):2008-20.
2. Huang J, Lok V, Ngai CH, Zhang L, Yuan J, Lao XQ, et al. Worldwide Burden of, Risk Factors for, and Trends in Pancreatic Cancer. Gastroenterology. 2021;160(3):744-54.
3. Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74(11):2913-21.
4. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7-33.
5. Arnold M, Abnet CC, Neale RE, Vignat J, Giovannucci EL, McGlynn KA, et al. Global Burden of 5 Major Types of Gastrointestinal Cancer. Gastroenterology. 2020;159(1):335-49.e15.
6. Costello E, Greenhalf W, Neoptolemos JP. New biomarkers and targets in pancreatic cancer and their application to treatment. Nat Rev Gastroenterol Hepatol. 2012;9(8):435-44.
7. DiMagno EP, Reber HA, Tempero MA. AGA technical review on the epidemiology, diagnosis, and treatment of pancreatic ductal adenocarcinoma. American Gastroenterological Association. Gastroenterology. 1999;117(6):1464-84.
8. Keleg S, Büchler P, Ludwig R, Büchler MW, Friess H. Invasion and metastasis in pancreatic cancer. Mol Cancer. 2003;2:14-.
9. Sotiriou C, Lothaire P, Dequanter D, Cardoso F, Awada A. Molecular profiling of head and neck tumors. Curr Opin Oncol. 2004;16(3):211-4.
10. Nagpal M, Singh S, Singh P, Chauhan P, Zaidi MA. Tumor markers: A diagnostic tool. Natl J Maxillofac Surg. 2016;7(1):17-20.
11. Herreros-Villanueva M, Gironella M, Castells A, Bujanda L. Molecular markers in pancreatic cancer diagnosis. Clin Chim Acta. 2013;418:22-9.
12. Ge L, Pan B, Song F, Ma J, Zeraatkar D, Zhou J, et al. Comparing the diagnostic accuracy of five common tumour biomarkers and CA19-9 for pancreatic cancer: a protocol for a network meta-analysis of diagnostic test accuracy. BMJ Open. 2017;7(12):e018175-e.
13. Rückert F, Pilarsky C, Grützmann R. Serum tumor markers in pancreatic cancer-recent discoveries. Cancers (Basel). 2010;2(2):1107-24.
14. Wang PH, Song N, Shi LB, Zhang QH, Chen ZY. The relationship between multiple clinicopathological features and nerve invasion in pancreatic cancer. Hepatobiliary Pancreat Dis Int. 2013;12(5):546-51.
15. Sharma GG, Okada Y, Von Hoff D, Goel A. Non-coding RNA biomarkers in pancreatic ductal adenocarcinoma. Semin Cancer Biol. 2021;75:153-68.
16. Ghafouri-Fard S, Fathi M, Zhai T, Taheri M, Dong P. LncRNAs: Novel Biomarkers for Pancreatic Cancer. Biomolecules. 2021;11(11):1665.
17. Sun J, Zhang Y. LncRNA XIST enhanced TGF-β2 expression by targeting miR-141-3p to promote pancreatic cancer cells invasion. Biosci Rep. 2019;39(7).
18. Lin C, Sun L, Huang S, Weng X, Wu Z. STC2 Is a Potential Prognostic Biomarker for Pancreatic Cancer and Promotes Migration and Invasion by Inducing Epithelial-Mesenchymal Transition. Biomed Res Int. 2019;2019:8042489-.
19. Luo G, Jin K, Deng S, Cheng H, Fan Z, Gong Y, et al. Roles of CA19-9 in pancreatic cancer: Biomarker, predictor and promoter. Biochim Biophys Acta Rev Cancer. 2021;1875(2):188409.
20. Borenstein-Katz A, Warszawski S, Amon R, Eilon M, Cohen-Dvashi H, Leviatan Ben-Arye S, et al. Biomolecular Recognition of the Glycan Neoantigen CA19-9 by Distinct Antibodies. J Mol Biol. 2021;433(15):167099.
21. Scarà S, Bottoni P, Scatena R. CA 19-9: Biochemical and Clinical Aspects. Adv Exp Med Biol. 2015;867:247-60.
22. Silsirivanit A. Glycosylation markers in cancer. Adv Clin Chem. 2019;89:189-213.
23. Kannagi R. Carbohydrate antigen sialyl Lewis a--its pathophysiological significance and induction mechanism in cancer progression. Chang Gung Med J. 2007;30(3):189-209.
24. Thomas D, Rathinavel AK, Radhakrishnan P. Altered glycosylation in cancer: A promising target for biomarkers and therapeutics. Biochim Biophys Acta Rev Cancer. 2021;1875(1):188464.
25. Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015;15(9):540-55.
26. Läubli H, Borsig L. Altered Cell Adhesion and Glycosylation Promote Cancer Immune Suppression and Metastasis. Front Immunol. 2019;10:2120.
27. Engle DD, Tiriac H, Rivera KD, Pommier A, Whalen S, Oni TE, et al. The glycan CA19-9 promotes pancreatitis and pancreatic cancer in mice. Science. 2019;364(6446):1156-62.
28. Xu J, Lyu S, Zhao Y, Zhang X, Liu Z, Zhao X, et al. Ratio of CA19-9 Level to Total Tumor Volume as a Prognostic Predictor of Pancreatic Carcinoma After Curative Resection. Technol Cancer Res Treat. 2022;21:15330338221078438.
29. Abdel-Misih SR, Hatzaras I, Schmidt C, Saab TB, Klemanski D, Muscarella P, et al. Failure of normalization of CA19-9 following resection for pancreatic cancer is tantamount to metastatic disease. Ann Surg Oncol. 2011;18(4):1116-21.
30. Zhao Y, Wang C. Clinicopathological Features, Recurrence Patterns, and Prognosis of Pancreatic Adenocarcinoma with Normal Serum CA19-9. A Consecutive Series of 154 Cases from a Single Institute. J Gastrointest Surg. 2020;24(4):855-65.
31. Kowalchuk RO, Lester SC, Graham RP, Harmsen WS, Zhang L, Halfdanarson TR, et al. Predicting Adverse Pathologic Features and Clinical Outcomes of Resectable Pancreas Cancer With Preoperative CA 19-9. Front Oncol. 2021;11:651119.
32. Felder M, Kapur A, Gonzalez-Bosquet J, Horibata S, Heintz J, Albrecht R, et al. MUC16 (CA125): tumor biomarker to cancer therapy, a work in progress. Mol Cancer. 2014;13:129.
33. Gandhi T, Bhatt H. Cancer Antigen 125. StatPearls. Treasure Island (FL): StatPearls Publishing Copyright © 2022, StatPearls Publishing LLC.; 2022.
34. Liu L, Xu HX, Wang WQ, Wu CT, Xiang JF, Liu C, et al. Serum CA125 is a novel predictive marker for pancreatic cancer metastasis and correlates with the metastasis-associated burden. Oncotarget. 2016;7(5):5943-56.
35. Chen SH, Hung WC, Wang P, Paul C, Konstantopoulos K. Mesothelin binding to CA125/MUC16 promotes pancreatic cancer cell motility and invasion via MMP-7 activation. Sci Rep. 2013;3:1870.
36. Shimizu A, Hirono S, Tani M, Kawai M, Okada K, Miyazawa M, et al. Coexpression of MUC16 and mesothelin is related to the invasion process in pancreatic ductal adenocarcinoma. Cancer Sci. 2012;103(4):739-46.
37. He B, Zhao Z, Cai Q, Zhang Y, Zhang P, Shi S, et al. miRNA-based biomarkers, therapies, and resistance in Cancer. Int J Biol Sci. 2020;16(14):2628-47.
38. Daoud AZ, Mulholland EJ, Cole G, McCarthy HO. MicroRNAs in Pancreatic Cancer: biomarkers, prognostic, and therapeutic modulators. BMC Cancer. 2019;19(1):1130.
39. Gheytanchi E, Tajik F, Razmi M, Babashah S, Cho WCS, Tanha K, et al. Circulating exosomal microRNAs as potential prognostic biomarkers in gastrointestinal cancers: a systematic review and meta-analysis. Cancer Cell International. 2023;23(1):10.
40. Pengcheng Z, Peng G, Haowen F, Xida L, Yuhua L, Yao W, et al. MiR-573 suppresses cell proliferation, migration and invasion via regulation of E2F3 in pancreatic cancer. J Cancer. 2021;12(10):3033-44.
41. Lei S, Zeng Z, He Z, Cao W. miRNA‑7515 suppresses pancreatic cancer cell proliferation, migration and invasion via downregulating IGF‑1 expression. Oncol Rep. 2021;46(3).
42. Xue Y, Wu T, Sheng Y, Zhong Y, Hu B, Bao C. MicroRNA-1252-5p, regulated by Myb, inhibits invasion and epithelial-mesenchymal transition of pancreatic cancer cells by targeting NEDD9. Aging (Albany NY). 2021;13(14):18924-45.
43. Fu XF, Zhao HC, Yang CL, Chen CZ, Wang K, Gao F, et al. MicroRNA-203-3p inhibits the proliferation, invasion and migration of pancreatic cancer cells by downregulating fibroblast growth factor 2. Oncol Lett. 2021;22(2):626.
44. Liu J, Zhu C, Zhang L, Lu H, Wang Z, Lv J, et al. MicroRNA-1469-5p promotes the invasion and proliferation of pancreatic cancer cells via direct regulating the NDRG1/NF-κB/E-cadherin axis. Hum Cell. 2020;33(4):1176-85.
45. Hu H, Zhang Q, Chen W, Wu T, Liu S, Li X, et al. MicroRNA-301a promotes pancreatic cancer invasion and metastasis through the JAK/STAT3 signaling pathway by targeting SOCS5. Carcinogenesis. 2020;41(4):502-14.
46. Shen Y, Chen G, Gao H, Li Y, Zhuang L, Meng Z, et al. miR-939-5p Contributes to the Migration and Invasion of Pancreatic Cancer by Targeting ARHGAP4. Onco Targets Ther. 2020;13:389-99.
47. Ma J, Cao T, Cui Y, Zhang F, Shi Y, Xia J, et al. miR-223 Regulates Cell Proliferation and Invasion via Targeting PDS5B in Pancreatic Cancer Cells. Mol Ther Nucleic Acids. 2019;14:583-92.
48. Yuan Q, Zhang Y, Li J, Cao G, Yang W. High expression of microRNA-4295 contributes to cell proliferation and invasion of pancreatic ductal adenocarcinoma by the down-regulation of Glypican-5. Biochem Biophys Res Commun. 2018;497(1):73-9.
49. Zhu J, Zhou L, Wei B, Qian Z, Wang J, Hui H, et al. miR‑142‑5p inhibits pancreatic cancer cell migration and invasion by targeting PIK3CA. Mol Med Rep. 2020;22(3):2085-92.
50. Xu C, Qi X. MiR-10b inhibits migration and invasion of pancreatic ductal adenocarcinoma via regulating E2F7. J Clin Lab Anal. 2020;34(10):e23442.
51. Dai C, Zhang Y, Xu Z, Jin M. MicroRNA-122-5p inhibits cell proliferation, migration and invasion by targeting CCNG1 in pancreatic ductal adenocarcinoma. Cancer Cell Int. 2020;20:98.
52. Xue L, Shen Y, Zhai Z, Zheng S. miR‑539 suppresses the proliferation, migration, invasion and epithelial mesenchymal transition of pancreatic cancer cells through targeting SP1. Int J Mol Med. 2020;45(6):1771-82.
53. Zhu JH, De Mello RA, Yan QL, Wang JW, Chen Y, Ye QH, et al. MiR-139-5p/SLC7A11 inhibits the proliferation, invasion and metastasis of pancreatic carcinoma via PI3K/Akt signaling pathway. Biochim Biophys Acta Mol Basis Dis. 2020;1866(6):165747.
54. Zhou ZG, Xu C, Dong Z, Wang YP, Duan JY, Yan CQ. MiR-497 inhibits cell proliferation and invasion ability by targeting HMGA2 in pancreatic ductal adenocarcinoma. Eur Rev Med Pharmacol Sci. 2020;24(1):122-9.
55. Zhou L, Jiao X, Peng X, Yao X, Liu L, Zhang L. MicroRNA-628-5p inhibits invasion and migration of human pancreatic ductal adenocarcinoma via suppression of the AKT/NF-kappa B pathway. J Cell Physiol. 2020;235(11):8141-54.
56. Yang Y, Sun KK, Shen XJ, Wu XY, Li DC. miR-557 inhibits the proliferation and invasion of pancreatic cancer cells by targeting EGFR. Int J Clin Exp Pathol. 2019;12(4):1333-41.
57. Yu Z, Zhao S, Wang L, Wang J, Zhou J. miRNA-339-5p Plays an Important Role in Invasion and Migration of Pancreatic Cancer Cells. Med Sci Monit. 2019;25:7509-17.
58. Sun Y, Zhu Q, Zhou M, Yang W, Shi H, Shan Y, et al. Restoration of miRNA-148a in pancreatic cancer reduces invasion and metastasis by inhibiting the Wnt/β-catenin signaling pathway via downregulating maternally expressed gene-3. Exp Ther Med. 2019;17(1):639-48.
59. Wang J, Wang B, Ren H, Chen W. miR-9-5p inhibits pancreatic cancer cell proliferation, invasion and glutamine metabolism by targeting GOT1. Biochem Biophys Res Commun. 2019;509(1):241-8.
60. Cao TH, Ling X, Chen C, Tang W, Hu DM, Yin GJ. Role of miR-214-5p in the migration and invasion of pancreatic cancer cells. Eur Rev Med Pharmacol Sci. 2018;22(21):7214-21.
61. Chen G, Hu M, Qu X, Wang K, Qu Y. MicroRNA‑584 directly targets CCND1 and inhibits cell proliferation and invasion in pancreatic cancer. Mol Med Rep. 2019;19(1):719-26.
62. Zhang H, Li M, Xu X. MicroRNA-204 attenuates the migration and invasion of pancreatic cancer cells by targeting ZEB1/EMT axis. Int J Clin Exp Pathol. 2018;11(7):3802-11.
63. Zhu L, Chen Y, Nie K, Xiao Y, Yu H. MiR-101 inhibits cell proliferation and invasion of pancreatic cancer through targeting STMN1. Cancer Biomark. 2018;23(2):301-9.
64. Yang Y, Tao X, Li CB, Wang CM. MicroRNA-494 acts as a tumor suppressor in pancreatic cancer, inhibiting epithelial-mesenchymal transition, migration and invasion by binding to SDC1. Int J Oncol. 2018;53(3):1204-14.
65. Lin C, Hu Z, Yuan G, Su H, Zeng Y, Guo Z, et al. MicroRNA-1179 inhibits the proliferation, migration and invasion of human pancreatic cancer cells by targeting E2F5. Chem Biol Interact. 2018;291:65-71.
66. Bolha L, Ravnik-Glavač M, Glavač D. Long Noncoding RNAs as Biomarkers in Cancer. Dis Markers. 2017;2017:7243968.
67. Zhang X, Wang W, Zhu W, Dong J, Cheng Y, Yin Z, et al. Mechanisms and Functions of Long Non-Coding RNAs at Multiple Regulatory Levels. Int J Mol Sci. 2019;20(22).
68. Chi Y, Wang D, Wang J, Yu W, Yang J. Long Non-Coding RNA in the Pathogenesis of Cancers. Cells. 2019;8(9).
69. Mahabady MK, Mirzaei S, Saebfar H, Gholami MH, Zabolian A, Hushmandi K, et al. Noncoding RNAs and their therapeutics in paclitaxel chemotherapy: Mechanisms of initiation, progression, and drug sensitivity. J Cell Physiol. 2022;237(5):2309-44.
70. Zhao J, Wu F, Yang J. A novel long non-coding RNA TTN-AS1/microRNA-589-5p/FOXP1 positive feedback loop increases the proliferation, migration and invasion of pancreatic cancer cell lines. Oncol Lett. 2021;22(5):794.
71. Jiang P, Yin Y, Wu Y, Sun Z. Silencing of long non-coding RNA SNHG15 suppresses proliferation, migration and invasion of pancreatic cancer cells by regulating the microRNA-345-5p/RAB27B axis. Exp Ther Med. 2021;22(5):1273.
72. Li P, Wang H, Tang Y, Sun S, Ma Y, Xu Y, et al. Knockdown of LINC00657 inhibits the viability, migration and invasion of pancreatic cancer cells by regulating the miR-520h/CKS1B axis. Exp Ther Med. 2021;22(4):1142.
73. Cheng J, Lou Y, Jiang K. Downregulation of long non-coding RNA LINC00460 inhibits the proliferation, migration and invasion, and promotes apoptosis of pancreatic cancer cells via modulation of the miR-320b/ARF1 axis. Bioengineered. 2021;12(1):96-107.
74. Wang W, Li X, Guan C, Hu Z, Zhao Y, Li W, et al. LncRNA PCAT6 promotes the proliferation, migration and invasion of pancreatic ductal adenocarcinoma via regulating miR-185-5p/CBX2 axis. Pathol Res Pract. 2020;216(9):153074.
75. Hu S, Zheng Q, Xiong J, Wu H, Wang W, Zhou W. Long non-coding RNA MVIH promotes cell proliferation, migration, invasion through regulating multiple cancer-related pathways, and correlates with worse prognosis in pancreatic ductal adenocarcinomas. Am J Transl Res. 2020;12(5):2118-35.
76. Yuan ZJ, Yu C, Hu XF, He Y, Chen P, Ouyang SX. LINC00152 promotes pancreatic cancer cell proliferation, migration and invasion via targeting miR-150. Am J Transl Res. 2020;12(5):2241-56.
77. Liu S, Zhang J, Yin L, Wang X, Zheng Y, Zhang Y, et al. The lncRNA RUNX1-IT1 regulates C-FOS transcription by interacting with RUNX1 in the process of pancreatic cancer proliferation, migration and invasion. Cell Death Dis. 2020;11(6):412.
78. Cao W, Zhou G. LncRNA SNHG12 contributes proliferation, invasion and epithelial-mesenchymal transition of pancreatic cancer cells by absorbing miRNA-320b. Biosci Rep. 2020;40(6).
79. Lu H, Ye J, Zhang L, Li M, Lu S, Yang D, et al. Downregulation of LINC01638 lncRNA inhibits migration and invasion of pancreatic ductal adenocarcinoma cells by reducing TGF‑β signaling. Mol Med Rep. 2019;20(5):4533-9.
80. Chen W, Wang H, Liu Y, Xu W, Ling C, Li Y, et al. Linc-RoR promotes proliferation, migration, and invasion via the Hippo/YAP pathway in pancreatic cancer cells. J Cell Biochem. 2020;121(1):632-41.
81. Jin X, Ye L, Lin M, Gu B, Wang J, He Y, et al. lncRNA-CCHE1 is involved in migration and invasion but not in proliferation of pancreatic adenocarcinoma cells possibly by interacting with ROCK1. Oncol Lett. 2019;18(2):1218-24.
82. Tang Y, Cao G, Zhao G, Wang C, Qin Q. LncRNA differentiation antagonizing non-protein coding RNA promotes proliferation and invasion through regulating miR-135a/NLRP37 axis in pancreatic cancer. Invest New Drugs. 2020;38(3):714-21.
83. Cui XP, Wang CX, Wang ZY, Li J, Tan YW, Gu ST, et al. LncRNA TP73-AS1 sponges miR-141-3p to promote the migration and invasion of pancreatic cancer cells through the up-regulation of BDH2. Biosci Rep. 2019;39(3).
84. Ye Z, Yang Y, Wei Y, Li L, Wang X, Zhang J. Long Noncoding RNA FOXD2-AS1 Promotes Pancreas Adenocarcinoma Cell Invasion and Migration by Sponging miR-30a-3p to Upregulate COX-2. Crit Rev Eukaryot Gene Expr. 2022;32(1):25-33.
85. Liu Y, Chen S, Cai K, Zheng D, Zhu C, Li L, et al. Hypoxia-induced long noncoding RNA NR2F1-AS1 maintains pancreatic cancer proliferation, migration, and invasion by activating the NR2F1/AKT/mTOR axis. Cell Death Dis. 2022;13(3):232.
86. Wang Y, Zhang XF, Wang DY, Zhu Y, Chen L, Zhang JJ. Long noncoding RNA SOX2OT promotes pancreatic cancer cell migration and invasion through destabilizing FUS protein via ubiquitination. Cell Death Discov. 2021;7(1):261.
87. Li JR, Liu L, Luo H, Chen ZG, Wang JH, Li NF. Long Noncoding RNA DUXAP8 Promotes Pancreatic Carcinoma Cell Migration and Invasion Via Pathway by miR-448/WTAP/Fak Signaling Axis. Pancreas. 2021;50(3):317-26.
88. Xie F, Huang Q, Wang C, Chen S, Liu C, Lin X, et al. Downregulation of long noncoding RNA SNHG14 suppresses cell proliferation and invasion by regulating EZH2 in pancreatic ductal adenocarcinoma (PDAC). Cancer Biomark. 2020;27(3):357-64.
89. Ou ZL, Zhang M, Ji LD, Luo Z, Han T, Lu YB, et al. Long noncoding RNA FEZF1-AS1 predicts poor prognosis and modulates pancreatic cancer cell proliferation and invasion through miR-142/HIF-1α and miR-133a/EGFR upon hypoxia/normoxia. J Cell Physiol. 2019.
90. Cui K, Jin S, Du Y, Yu J, Feng H, Fan Q, et al. Long noncoding RNA DIO3OS interacts with miR-122 to promote proliferation and invasion of pancreatic cancer cells through upregulating ALDOA. Cancer Cell Int. 2019;19:202.
91. Lu Y, Tang L, Zhang Z, Li S, Liang S, Ji L, et al. Long Noncoding RNA TUG1/miR-29c Axis Affects Cell Proliferation, Invasion, and Migration in Human Pancreatic Cancer. Dis Markers. 2018;2018:6857042.
92. Cui L, Dong Y, Wang X, Zhao X, Kong C, Liu Y, et al. Downregulation of long noncoding RNA SNHG1 inhibits cell proliferation, metastasis, and invasion by suppressing the Notch-1 signaling pathway in pancreatic cancer. J Cell Biochem. 2019;120(4):6106-12.
93. Tian C, Jin Y, Shi S. Long non-coding RNA SUMO1P3 may promote cell proliferation, migration, and invasion of pancreatic cancer via EMT signaling pathway. Oncol Lett. 2018;16(5):6109-15.
94. An Y, Chen XM, Yang Y, Mo F, Jiang Y, Sun DL, et al. LncRNA DLX6-AS1 promoted cancer cell proliferation and invasion by attenuating the endogenous function of miR-181b in pancreatic cancer. Cancer Cell Int. 2018;18:143.
95. Gao H, Gong N, Ma Z, Miao X, Chen J, Cao Y, et al. LncRNA ZEB2-AS1 promotes pancreatic cancer cell growth and invasion through regulating the miR-204/HMGB1 axis. Int J Biol Macromol. 2018;116:545-51.
96. Zhang M, Zhao Y, Zhang Y, Wang D, Gu S, Feng W, et al. LncRNA UCA1 promotes migration and invasion in pancreatic cancer cells via the Hippo pathway. Biochim Biophys Acta Mol Basis Dis. 2018;1864(5 Pt A):1770-82.
97. Guo W, Zhong K, Wei H, Nie C, Yuan Z. Long non-coding RNA SPRY4-IT1 promotes cell proliferation and invasion by regulation of Cdc20 in pancreatic cancer cells. PLoS One. 2018;13(2):e0193483.
98. Lian Y, Xiao C, Yan C, Chen D, Huang Q, Fan Y, et al. Knockdown of pseudogene derived from lncRNA DUXAP10 inhibits cell proliferation, migration, invasion, and promotes apoptosis in pancreatic cancer. J Cell Biochem. 2018;119(4):3671-82.
99. Zheng S, Chen H, Wang Y, Gao W, Fu Z, Zhou Q, et al. Long non-coding RNA LOC389641 promotes progression of pancreatic ductal adenocarcinoma and increases cell invasion by regulating E-cadherin in a TNFRSF10A-related manner. Cancer Lett. 2016;371(2):354-65.
100. Jiao F, Hu H, Yuan C, Wang L, Jiang W, Jin Z, et al. Elevated expression level of long noncoding RNA MALAT-1 facilitates cell growth, migration and invasion in pancreatic cancer. Oncol Rep. 2014;32(6):2485-92.
101. Hu H, Wang Y, Ding X, He Y, Lu Z, Wu P, et al. Long non-coding RNA XLOC_000647 suppresses progression of pancreatic cancer and decreases epithelial-mesenchymal transition-induced cell invasion by down-regulating NLRP3. Mol Cancer. 2018;17(1):18.
102. Sun YW, Chen YF, Li J, Huo YM, Liu DJ, Hua R, et al. A novel long non-coding RNA ENST00000480739 suppresses tumour cell invasion by regulating OS-9 and HIF-1α in pancreatic ductal adenocarcinoma. Br J Cancer. 2014;111(11):2131-41.
103. Bach DH, Lee SK, Sood AK. Circular RNAs in Cancer. Mol Ther Nucleic Acids. 2019;16:118-29.
104. Song H, Liu Q, Liao Q. Circular RNA and tumor microenvironment. Cancer Cell Int. 2020;20:211.
105. Chen Q, Li J, Shen P, Yuan H, Yin J, Ge W, et al. Biological functions, mechanisms, and clinical significance of circular RNA in pancreatic cancer: a promising rising star. Cell Biosci. 2022;12(1):97.
106. Li Z, Yanfang W, Li J, Jiang P, Peng T, Chen K, et al. Tumor-released exosomal circular RNA PDE8A promotes invasive growth via the miR-338/MACC1/MET pathway in pancreatic cancer. Cancer Lett. 2018;432:237-50.
107. Huang L, Han J, Yu H, Liu J, Gui L, Wu Z, et al. CircRNA_000864 Upregulates B-cell Translocation Gene 2 Expression and Represses Migration and Invasion in Pancreatic Cancer Cells by Binding to miR-361-3p. Front Oncol. 2020;10:547942.
108. Qu S, Hao X, Song W, Niu K, Yang X, Zhang X, et al. Circular RNA circRHOT1 is upregulated and promotes cell proliferation and invasion in pancreatic cancer. Epigenomics. 2019;11(1):53-63.
109. Yao X, Mao Y, Wu D, Zhu Y, Lu J, Huang Y, et al. Exosomal circ_0030167 derived from BM-MSCs inhibits the invasion, migration, proliferation and stemness of pancreatic cancer cells by sponging miR-338-5p and targeting the Wif1/Wnt8/β-catenin axis. Cancer Lett. 2021;512:38-50.
110. Hao L, Rong W, Bai L, Cui H, Zhang S, Li Y, et al. Upregulated circular RNA circ_0007534 indicates an unfavorable prognosis in pancreatic ductal adenocarcinoma and regulates cell proliferation, apoptosis, and invasion by sponging miR-625 and miR-892b. J Cell Biochem. 2019;120(3):3780-9.
111. Guo W, Zhao L, Wei G, Liu P, Zhang Y, Fu L. Blocking circ_0013912 Suppressed Cell Growth, Migration and Invasion of Pancreatic Ductal Adenocarcinoma Cells in vitro and in vivo Partially Through Sponging miR-7-5p. Cancer Manag Res. 2020;12:7291-303.
112. Zhang X, Tan P, Zhuang Y, Du L. hsa_circRNA_001587 upregulates SLC4A4 expression to inhibit migration, invasion, and angiogenesis of pancreatic cancer cells via binding to microRNA-223. Am J Physiol Gastrointest Liver Physiol. 2020;319(6):G703-g17.
113. Joshi AD. New Insights Into Physiological and Pathophysiological Functions of Stanniocalcin 2. Front Endocrinol (Lausanne). 2020;11:172.
114. Li S, Huang Q, Li D, Lv L, Li Y, Wu Z. The significance of Stanniocalcin 2 in malignancies and mechanisms. Bioengineered. 2021;12(1):7276-85.
115. Lin C, Sun L, Huang S, Weng X, Wu Z. STC2 Is a Potential Prognostic Biomarker for Pancreatic Cancer and Promotes Migration and Invasion by Inducing Epithelial-Mesenchymal Transition. Biomed Res Int. 2019;2019:8042489.
IssueVol 8, No 3 (2025) QRcode
SectionReview Article
DOI https://doi.org/10.18502/igj.v8i3.18208
Keywords
Pancreatic Cancer (PC) Invasion microRNAs Long Noncoding RNAs Circular RNAs CA19-9 CA125

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Tajik F, Kamali Zonouzi S, Razi S. Tumor Markers Involved in Invasion of Pancreatic Cancer. Immunol Genet J. 2025;8(3).