Biological functions and clinical significance of exosomal proteins in pancreatic cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

PENG Bo ¹ , ZHANG Yanjun ¹ , LIU Xusheng ¹ , MOU Jiangwei ¹ ,  ZHU Kexiang ^1,2

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：

ZHU Kexiang, Email: flexzhu6910@163.com

Keywords：

Pancreatic cancer; exosomes; exosomal proteins; tumor progression; Clinical diagnosis and treatment; XXXXXXXXXX

DOI：

10.7507/1007-9424.202410122

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the role of exosomal proteins in the occurrence, development, and diagnosis and treatment of pancreatic cancer (PC), providing a reference for the exploration of biomarkers and therapeutic targets in this field. Method A systematic review of recent domestic and international literature on the mechanisms of exosomes and their proteins in pancreatic cancer was conducted. Result Proteins carried by tumor-derived exosomes, such as LGALS3BP, VSIG2, ZIP4, AEP, and GOT1, can effectively regulate the tumor microenvironment and influence cell behavior, playing an important role in the occurrence, progression, and metastasis of pancreatic cancer. Additionally, exosomal proteins can serve as potential biomarkers for the early diagnosis of pancreatic cancer. For example, exosomal membrane proteins GPC1 and DNAJB11 are highly expressed in pancreatic cancer tissues, indicating their potential. Conclusion Exosomal proteins are expected to become novel biomarkers and intervention targets for the early diagnosis and targeted therapy of pancreatic cancer, providing new ideas for improving the diagnosis and treatment of pancreatic cancer.

1.	姚一菲, 孙可欣, 郑荣寿. 《2022全球癌症统计报告》解读: 中国与全球对比. 中国普外基础与临床杂志, 2024, 31(7): 769-780.
2.	Halbrook CJ, Lyssiotis CA, Pasca di Magliano M, et al. Pancreatic cancer: Advances and challenges. Cell, 2023, 186(8): 1729-1754.
3.	Ariston Gabriel AN, Wang F, Jiao Q, et al. The involvement of exosomes in the diagnosis and treatment of pancreatic cancer. Mol Cancer, 2020, 19(1): 132. doi: 10.1186/s12943-020-01245-y.
4.	Yang J, Xu R, Wang C, et al. Early screening and diagnosis strategies of pancreatic cancer: a comprehensive review. Cancer Commun (Lond), 2021, 41(12): 1257-1274.
5.	Zhao Y, Tang J, Jiang K, et al. Liquid biopsy in pancreatic cancer—Current perspective and future outlook. Biochim Biophys Acta Rev Cancer, 2023, 1878(3): 188868. doi: 10.1016/j.bbcan.2023.188868.
6.	Mizrahi JD, Surana R, Valle JW, et al. Pancreatic cancer. Lancet, 2020, 395(10242): 2008-2020.
7.	Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol, 2014, 30: 255-289.
8.	Li XX, Yang LX, Wang C, et al. The roles of exosomal proteins: classification, function, and applications. Int J Mol Sci, 2023, 24(4): 3061. doi: 10.3390/ijms24043061.
9.	Hu C, Jiang W, Lv M, et al. Potentiality of exosomal proteins as novel cancer biomarkers for liquid biopsy. Front Immunol, 2022, 13: 792046. doi: 10.3389/fimmu.2022.792046.
10.	Gao P, Li X, Du X, et al. Diagnostic and therapeutic potential of exosomes in neurodegenerative diseases. Front Aging Neurosci, 2021, 13: 790863. doi: 10.3389/fnagi.2021.790863.
11.	Ghosh S, Rajendran RL, Mahajan AA, et al. Harnessing exosomes as cancer biomarkers in clinical oncology. Cancer Cell Int, 2024, 24(1): 278. doi: 10.1186/s12935-024-03464-5.
12.	Zhang Y, Bi J, Huang J, et al. Exosome: A review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomedicine, 2020, 15: 6917-6934.
13.	Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478): eaau6977. doi: 10.1126/science.aau6977.
14.	Zhang Y, Liu Y, Liu H, et al. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci, 2019, 9: 19. doi: 10.1186/s13578-019-0282-2.
15.	Dai J, Su Y, Zhong S, et al. Exosomes: Key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther, 2020, 5(1): 145. doi: 10.1038/s41392-020-00261-0.
16.	Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem, 2019, 88: 487-514.
17.	Du S, Guan Y, Xie A, et al. Extracellular vesicles: a rising star for therapeutics and drug delivery. J Nanobiotechnology, 2023, 21(1): 231. doi: 10.1186/s12951-023-01973-5.
18.	Fang X, Lan H, Jin K, et al. Pancreatic cancer and exosomes: role in progression, diagnosis, monitoring, and treatment. Front Oncol, 2023, 13: 1149551. doi: 10.3389/fonc.2023.1149551.
19.	Kok VC, Yu CC. Cancer-derived exosomes: Their role in cancer biology and biomarker development. Int J Nanomedicine, 2020, 15: 8019-8036.
20.	Casari I, Howard JA, Robless EE, et al. Exosomal integrins and their influence on pancreatic cancer progression and metastasis. Cancer Lett, 2021, 507: 124-134.
21.	Xu R, Rai A, Chen M, et al. Extracellular vesicles in cancer—implications for future improvements in cancer care. Nat Rev Clin Oncol, 2018, 15(10): 617-638.
22.	Xu J, Quan G, Huang W, et al. VSIG2 promotes malignant progression of pancreatic ductal adenocarcinoma by enhancing LAMTOR2-mediated mTOR activation. Cell Commun Signal, 2023, 21(1): 223. doi: 10.1186/s12964-023-01209-x.
23.	Jin H, Liu P, Wu Y, et al. Exosomal zinc transporter ZIP4 promotes cancer growth and is a novel diagnostic biomarker for pancreatic cancer. Cancer Sci, 2018, 109(9): 2946-2956.
24.	Yan Q, Yuan WB, Sun X, et al. Asparaginyl endopeptidase enhances pancreatic ductal adenocarcinoma cell invasion in an exosome-dependent manner and correlates with poor prognosis. Int J Oncol, 2018, 52(5): 1651-1660.
25.	Guo Y, Chen T, Liang X, et al. Tumor cell derived exosomal GOT1 suppresses tumor cell ferroptosis to accelerate pancreatic cancer progression by activating Nrf2/HO-1 axis via upregulating CCR2 expression. Cells, 2022, 11(23): 3893. doi: 10.3390/cells11233893.
26.	Yue S, Mu W, Erb U, et al. The tetraspanins CD151 and Tspan8 are essential exosome components for the crosstalk between cancer initiating cells and their surrounding. Oncotarget, 2015, 6(4): 2366-2384.
27.	Chen Y, Kleeff J, Sunami Y. Pancreatic cancer cell- and cancer-associated fibroblast-derived exosomes in disease progression, metastasis, and therapy. Discov Oncol, 2024, 15(1): 253. doi: 10.1007/s12672-024-01111-z.
28.	He Z, Li X, Chen S, et al. CD105⁺CAF-derived exosomes CircAMPK1 promotes pancreatic cancer progression by activating autophagy. Exp Hematol Oncol, 2024, 13(1): 79. doi: 10.1186/s40164-024-00533-3.
29.	Castillo J, Bernard V, San Lucas FA, et al. Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients. Ann Oncol, 2018, 29(1): 223-229.
30.	Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature, 2015, 527(7578): 329-335.
31.	Zhang H, Xing J, Dai Z, et al. Exosomes: The key of sophisticated cell-cell communication and targeted metastasis in pancreatic cancer. Cell Commun Signal, 2022, 20(1): 9. doi: 10.1186/s12964-021-00808-w.
32.	Xie Z, Gao Y, Ho C, et al. Exosome-delivered CD44v6/C1QBP complex drives pancreatic cancer liver metastasis by promoting fibrotic liver microenvironment. Gut, 2022, 71(3): 568-579.
33.	Ogawa K, Lin Q, Li L, et al. Prometastatic secretome trafficking via exosomes initiates pancreatic cancer pulmonary metastasis. Cancer Lett, 2020, 481: 63-75.
34.	Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest, 2009, 119(6): 1420-1428.
35.	Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl), 2013, 91(4): 431-437.
36.	Nakayama F, Miyoshi M, Kimoto A, et al. Pancreatic cancer cell-derived exosomes induce epithelial-mesenchymal transition in human pancreatic cancer cells themselves partially via transforming growth factor β1. Med Mol Morphol, 2022, 55(3): 227-235.
37.	Kruk L, Braun A, Cosset E, et al. Galectin functions in cancer-associated inflammation and thrombosis. Front Cardiovasc Med, 2023, 10: 1052959. doi: 10.3389/fcvm.2023.1052959.
38.	Toti A, Santi A, Pardella E, et al. Activated fibroblasts enhance cancer cell migration by microvesicles-mediated transfer of Galectin-1. J Cell Commun Signal, 2021, 15(3): 405-419.
39.	Wei Q, Wei L, Zhang J, et al. EphA2-enriched exosomes promote cell migration and are a potential diagnostic serum marker in pancreatic cancer. Mol Med Rep, 2020, 22(4): 2941-2947.
40.	Zhang YF, Zhou YZ, Zhang B, et al. Pancreatic cancer-derived exosomes promoted pancreatic stellate cells recruitment by pancreatic cancer. J Cancer, 2019, 10(18): 4397-4407.
41.	Qin C, Li T, Lin C, et al. The systematic role of pancreatic cancer exosomes: distant communication, liquid biopsy and future therapy. Cancer Cell Int, 2024, 24(1): 264. doi: 10.1186/s12935-024-03456-5.
42.	Luo Y, Li Z, Kong Y, et al. KRAS mutant-driven SUMOylation controls extracellular vesicle transmission to trigger lymphangiogenesis in pancreatic cancer. J Clin Invest, 2022, 132(14): e157644. doi: 10.1172/JCI157644.
43.	Linton SS, Abraham T, Liao J, et al. Tumor-promoting effects of pancreatic cancer cell exosomes on THP-1-derived macrophages. PLoS One, 2018, 13(11): e0206759. doi: 10.1371/journal.pone.0206759.
44.	Chang YT, Peng HY, Hu CM, et al. Pancreatic cancer-derived small extracellular vesical Ezrin regulates macrophage polarization and promotes metastasis. Am J Cancer Res, 2020, 10(1): 12-37.
45.	Vahabi M, Comandatore A, Centra C, et al. Thinking small to win big? A critical review on the potential application of extracellular vesicles for biomarker discovery and new therapeutic approaches in pancreatic cancer. Semin Cancer Biol, 2023, 97: 50-67.
46.	O’Neill RS, Stoita A. Biomarkers in the diagnosis of pancreatic cancer: Are we closer to finding the golden ticket?. World J Gastroenterol, 2021, 27(26): 4045-4087.
47.	Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature, 2015, 523(7559): 177-182.
48.	Nicoletti A, Negri M, Paratore M, et al. Diagnostic and prognostic role of extracellular vesicles in pancreatic cancer: Current evidence and future perspectives. Int J Mol Sci, 2023, 24(1): 885. doi: 10.3390/ijms24010885.
49.	Li H, Chiang CL, Kwak KJ, et al. Extracellular vesicular analysis of glypican 1 mRNA and protein for pancreatic cancer diagnosis and prognosis. Adv Sci (Weinh), 2024, 11(11): e2306373. doi: 10.1002/advs.202306373.
50.	Moutinho-Ribeiro P, Batista IA, Quintas ST, et al. Exosomal glypican-1 is elevated in pancreatic cancer precursors and can signal genetic predisposition in the absence of endoscopic ultrasound abnormalities. World J Gastroenterol, 2022, 28(31): 4310-4327.
51.	Liu P, Zu F, Chen H, et al. Exosomal DNAJB11 promotes the development of pancreatic cancer by modulating the EGFR/MAPK pathway. Cell Mol Biol Lett, 2022, 27(1): 87. doi: 10.1186/s11658-022-00390-0.
52.	Byeon S, McKay MJ, Molloy MP, et al. Novel serum protein biomarker panel for early diagnosis of pancreatic cancer. Int J Cancer, 2024, 155(2): 365-371.
53.	Yang J, Zhang Y, Gao X, et al. Plasma-derived exosomal ALIX as a novel biomarker for diagnosis and classification of pancreatic cancer. Front Oncol, 2021, 11: 628346. doi: 10.3389/fonc.2021.628346.
54.	He J, Long J, Zhai C, et al. Codetection of proteins and RNAs on extracellular vesicles for pancreatic cancer early diagnosis. Anal Chem, 2024, 96(17): 6618-6627.
55.	Hu ZI, O’Reilly EM. Therapeutic developments in pancreatic cancer. Nat Rev Gastroenterol Hepatol, 2024, 21(1): 7-24.
56.	Bauer MR, Bright EE, MacDonald JJ, et al. Quality of life in patients with pancreatic cancer and their caregivers: a systematic review. Pancreas, 2018, 47(4): 368-375.
57.	El-Tanani M, Nsairat H, Matalka II, et al. Impact of exosome therapy on pancreatic cancer and its progression. Med Oncol, 2023, 40(8): 225. doi: 10.1007/s12032-023-02101-x.
58.	Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature, 2017, 546(7659): 498-503.
59.	Luo J. KRAS mutation in pancreatic cancer. Semin Oncol, 2021, 48(1): 10-18.
60.	Choi H, Choi Y, Yim HY, et al. Biodistribution of exosomes and engineering strategies for targeted delivery of therapeutic exosomes. Tissue Eng Regen Med, 2021, 18(4): 499-511.
61.	Creeden JF, Sevier J, Zhang JT, et al. Smart exosomes enhance PDAC targeted therapy. J Control Release, 2024, 368: 413-429.
62.	Whiteside TL. Tumor-derived exosomes and their role in cancer progression. Adv Clin Chem, 2016, 74: 103-141.
63.	Qiu H, Liang J, Yang G, et al. Application of exosomes in tumor immunity: recent progresses. Front Cell Dev Biol, 2024, 12: 1372847. doi: 10.3389/fcell.2024.1372847.
64.	Que RS, Lin C, Ding GP, et al. Increasing the immune activity of exosomes: the effect of miRNA-depleted exosome proteins on activating dendritic cell/cytokine-induced killer cells against pancreatic cancer. J Zhejiang Univ Sci B, 2016, 17(5): 352-360.
65.	Guo M, Sun C, LiuR, et al. A drug delivery platform using engineered MUC1‐targeting exosomes enhances chemosensitivity and immunogenic cell death in pancreatic ductal adenocarcinoma. SmartMat, 2024, 5(5): e1279. doi: 10.1002/SMM2.1279.
66.	Chen L, Wang L, Zhu L, et al. Exosomes as drug carriers in anti-cancer therapy. Front Cell Dev Biol, 2022, 10: 728616. doi: 10.3389/fcell.2022.728616.
67.	Al Faruque H, Choi ES, Kim JH, et al. Enhanced effect of autologous EVs delivering paclitaxel in pancreatic cancer. J Control Release, 2022, 347: 330-346.
68.	Chiang CL, Ma Y, Hou YC, et al. Dual targeted extracellular vesicles regulate oncogenic genes in advanced pancreatic cancer. Nat Commun, 2023, 14(1): 6692. doi: 10.1038/s41467-023-42402-3.

1. 姚一菲, 孙可欣, 郑荣寿. 《2022全球癌症统计报告》解读: 中国与全球对比. 中国普外基础与临床杂志, 2024, 31(7): 769-780.
2. Halbrook CJ, Lyssiotis CA, Pasca di Magliano M, et al. Pancreatic cancer: Advances and challenges. Cell, 2023, 186(8): 1729-1754.
3. Ariston Gabriel AN, Wang F, Jiao Q, et al. The involvement of exosomes in the diagnosis and treatment of pancreatic cancer. Mol Cancer, 2020, 19(1): 132. doi: 10.1186/s12943-020-01245-y.
4. Yang J, Xu R, Wang C, et al. Early screening and diagnosis strategies of pancreatic cancer: a comprehensive review. Cancer Commun (Lond), 2021, 41(12): 1257-1274.
5. Zhao Y, Tang J, Jiang K, et al. Liquid biopsy in pancreatic cancer—Current perspective and future outlook. Biochim Biophys Acta Rev Cancer, 2023, 1878(3): 188868. doi: 10.1016/j.bbcan.2023.188868.
6. Mizrahi JD, Surana R, Valle JW, et al. Pancreatic cancer. Lancet, 2020, 395(10242): 2008-2020.
7. Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol, 2014, 30: 255-289.
8. Li XX, Yang LX, Wang C, et al. The roles of exosomal proteins: classification, function, and applications. Int J Mol Sci, 2023, 24(4): 3061. doi: 10.3390/ijms24043061.
9. Hu C, Jiang W, Lv M, et al. Potentiality of exosomal proteins as novel cancer biomarkers for liquid biopsy. Front Immunol, 2022, 13: 792046. doi: 10.3389/fimmu.2022.792046.
10. Gao P, Li X, Du X, et al. Diagnostic and therapeutic potential of exosomes in neurodegenerative diseases. Front Aging Neurosci, 2021, 13: 790863. doi: 10.3389/fnagi.2021.790863.
11. Ghosh S, Rajendran RL, Mahajan AA, et al. Harnessing exosomes as cancer biomarkers in clinical oncology. Cancer Cell Int, 2024, 24(1): 278. doi: 10.1186/s12935-024-03464-5.
12. Zhang Y, Bi J, Huang J, et al. Exosome: A review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomedicine, 2020, 15: 6917-6934.
13. Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478): eaau6977. doi: 10.1126/science.aau6977.
14. Zhang Y, Liu Y, Liu H, et al. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci, 2019, 9: 19. doi: 10.1186/s13578-019-0282-2.
15. Dai J, Su Y, Zhong S, et al. Exosomes: Key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther, 2020, 5(1): 145. doi: 10.1038/s41392-020-00261-0.
16. Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem, 2019, 88: 487-514.
17. Du S, Guan Y, Xie A, et al. Extracellular vesicles: a rising star for therapeutics and drug delivery. J Nanobiotechnology, 2023, 21(1): 231. doi: 10.1186/s12951-023-01973-5.
18. Fang X, Lan H, Jin K, et al. Pancreatic cancer and exosomes: role in progression, diagnosis, monitoring, and treatment. Front Oncol, 2023, 13: 1149551. doi: 10.3389/fonc.2023.1149551.
19. Kok VC, Yu CC. Cancer-derived exosomes: Their role in cancer biology and biomarker development. Int J Nanomedicine, 2020, 15: 8019-8036.
20. Casari I, Howard JA, Robless EE, et al. Exosomal integrins and their influence on pancreatic cancer progression and metastasis. Cancer Lett, 2021, 507: 124-134.
21. Xu R, Rai A, Chen M, et al. Extracellular vesicles in cancer—implications for future improvements in cancer care. Nat Rev Clin Oncol, 2018, 15(10): 617-638.
22. Xu J, Quan G, Huang W, et al. VSIG2 promotes malignant progression of pancreatic ductal adenocarcinoma by enhancing LAMTOR2-mediated mTOR activation. Cell Commun Signal, 2023, 21(1): 223. doi: 10.1186/s12964-023-01209-x.
23. Jin H, Liu P, Wu Y, et al. Exosomal zinc transporter ZIP4 promotes cancer growth and is a novel diagnostic biomarker for pancreatic cancer. Cancer Sci, 2018, 109(9): 2946-2956.
24. Yan Q, Yuan WB, Sun X, et al. Asparaginyl endopeptidase enhances pancreatic ductal adenocarcinoma cell invasion in an exosome-dependent manner and correlates with poor prognosis. Int J Oncol, 2018, 52(5): 1651-1660.
25. Guo Y, Chen T, Liang X, et al. Tumor cell derived exosomal GOT1 suppresses tumor cell ferroptosis to accelerate pancreatic cancer progression by activating Nrf2/HO-1 axis via upregulating CCR2 expression. Cells, 2022, 11(23): 3893. doi: 10.3390/cells11233893.
26. Yue S, Mu W, Erb U, et al. The tetraspanins CD151 and Tspan8 are essential exosome components for the crosstalk between cancer initiating cells and their surrounding. Oncotarget, 2015, 6(4): 2366-2384.
27. Chen Y, Kleeff J, Sunami Y. Pancreatic cancer cell- and cancer-associated fibroblast-derived exosomes in disease progression, metastasis, and therapy. Discov Oncol, 2024, 15(1): 253. doi: 10.1007/s12672-024-01111-z.
28. He Z, Li X, Chen S, et al. CD105⁺CAF-derived exosomes CircAMPK1 promotes pancreatic cancer progression by activating autophagy. Exp Hematol Oncol, 2024, 13(1): 79. doi: 10.1186/s40164-024-00533-3.
29. Castillo J, Bernard V, San Lucas FA, et al. Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients. Ann Oncol, 2018, 29(1): 223-229.
30. Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature, 2015, 527(7578): 329-335.
31. Zhang H, Xing J, Dai Z, et al. Exosomes: The key of sophisticated cell-cell communication and targeted metastasis in pancreatic cancer. Cell Commun Signal, 2022, 20(1): 9. doi: 10.1186/s12964-021-00808-w.
32. Xie Z, Gao Y, Ho C, et al. Exosome-delivered CD44v6/C1QBP complex drives pancreatic cancer liver metastasis by promoting fibrotic liver microenvironment. Gut, 2022, 71(3): 568-579.
33. Ogawa K, Lin Q, Li L, et al. Prometastatic secretome trafficking via exosomes initiates pancreatic cancer pulmonary metastasis. Cancer Lett, 2020, 481: 63-75.
34. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest, 2009, 119(6): 1420-1428.
35. Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl), 2013, 91(4): 431-437.
36. Nakayama F, Miyoshi M, Kimoto A, et al. Pancreatic cancer cell-derived exosomes induce epithelial-mesenchymal transition in human pancreatic cancer cells themselves partially via transforming growth factor β1. Med Mol Morphol, 2022, 55(3): 227-235.
37. Kruk L, Braun A, Cosset E, et al. Galectin functions in cancer-associated inflammation and thrombosis. Front Cardiovasc Med, 2023, 10: 1052959. doi: 10.3389/fcvm.2023.1052959.
38. Toti A, Santi A, Pardella E, et al. Activated fibroblasts enhance cancer cell migration by microvesicles-mediated transfer of Galectin-1. J Cell Commun Signal, 2021, 15(3): 405-419.
39. Wei Q, Wei L, Zhang J, et al. EphA2-enriched exosomes promote cell migration and are a potential diagnostic serum marker in pancreatic cancer. Mol Med Rep, 2020, 22(4): 2941-2947.
40. Zhang YF, Zhou YZ, Zhang B, et al. Pancreatic cancer-derived exosomes promoted pancreatic stellate cells recruitment by pancreatic cancer. J Cancer, 2019, 10(18): 4397-4407.
41. Qin C, Li T, Lin C, et al. The systematic role of pancreatic cancer exosomes: distant communication, liquid biopsy and future therapy. Cancer Cell Int, 2024, 24(1): 264. doi: 10.1186/s12935-024-03456-5.
42. Luo Y, Li Z, Kong Y, et al. KRAS mutant-driven SUMOylation controls extracellular vesicle transmission to trigger lymphangiogenesis in pancreatic cancer. J Clin Invest, 2022, 132(14): e157644. doi: 10.1172/JCI157644.
43. Linton SS, Abraham T, Liao J, et al. Tumor-promoting effects of pancreatic cancer cell exosomes on THP-1-derived macrophages. PLoS One, 2018, 13(11): e0206759. doi: 10.1371/journal.pone.0206759.
44. Chang YT, Peng HY, Hu CM, et al. Pancreatic cancer-derived small extracellular vesical Ezrin regulates macrophage polarization and promotes metastasis. Am J Cancer Res, 2020, 10(1): 12-37.
45. Vahabi M, Comandatore A, Centra C, et al. Thinking small to win big? A critical review on the potential application of extracellular vesicles for biomarker discovery and new therapeutic approaches in pancreatic cancer. Semin Cancer Biol, 2023, 97: 50-67.
46. O’Neill RS, Stoita A. Biomarkers in the diagnosis of pancreatic cancer: Are we closer to finding the golden ticket?. World J Gastroenterol, 2021, 27(26): 4045-4087.
47. Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature, 2015, 523(7559): 177-182.
48. Nicoletti A, Negri M, Paratore M, et al. Diagnostic and prognostic role of extracellular vesicles in pancreatic cancer: Current evidence and future perspectives. Int J Mol Sci, 2023, 24(1): 885. doi: 10.3390/ijms24010885.
49. Li H, Chiang CL, Kwak KJ, et al. Extracellular vesicular analysis of glypican 1 mRNA and protein for pancreatic cancer diagnosis and prognosis. Adv Sci (Weinh), 2024, 11(11): e2306373. doi: 10.1002/advs.202306373.
50. Moutinho-Ribeiro P, Batista IA, Quintas ST, et al. Exosomal glypican-1 is elevated in pancreatic cancer precursors and can signal genetic predisposition in the absence of endoscopic ultrasound abnormalities. World J Gastroenterol, 2022, 28(31): 4310-4327.
51. Liu P, Zu F, Chen H, et al. Exosomal DNAJB11 promotes the development of pancreatic cancer by modulating the EGFR/MAPK pathway. Cell Mol Biol Lett, 2022, 27(1): 87. doi: 10.1186/s11658-022-00390-0.
52. Byeon S, McKay MJ, Molloy MP, et al. Novel serum protein biomarker panel for early diagnosis of pancreatic cancer. Int J Cancer, 2024, 155(2): 365-371.
53. Yang J, Zhang Y, Gao X, et al. Plasma-derived exosomal ALIX as a novel biomarker for diagnosis and classification of pancreatic cancer. Front Oncol, 2021, 11: 628346. doi: 10.3389/fonc.2021.628346.
54. He J, Long J, Zhai C, et al. Codetection of proteins and RNAs on extracellular vesicles for pancreatic cancer early diagnosis. Anal Chem, 2024, 96(17): 6618-6627.
55. Hu ZI, O’Reilly EM. Therapeutic developments in pancreatic cancer. Nat Rev Gastroenterol Hepatol, 2024, 21(1): 7-24.
56. Bauer MR, Bright EE, MacDonald JJ, et al. Quality of life in patients with pancreatic cancer and their caregivers: a systematic review. Pancreas, 2018, 47(4): 368-375.
57. El-Tanani M, Nsairat H, Matalka II, et al. Impact of exosome therapy on pancreatic cancer and its progression. Med Oncol, 2023, 40(8): 225. doi: 10.1007/s12032-023-02101-x.
58. Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature, 2017, 546(7659): 498-503.
59. Luo J. KRAS mutation in pancreatic cancer. Semin Oncol, 2021, 48(1): 10-18.
60. Choi H, Choi Y, Yim HY, et al. Biodistribution of exosomes and engineering strategies for targeted delivery of therapeutic exosomes. Tissue Eng Regen Med, 2021, 18(4): 499-511.
61. Creeden JF, Sevier J, Zhang JT, et al. Smart exosomes enhance PDAC targeted therapy. J Control Release, 2024, 368: 413-429.
62. Whiteside TL. Tumor-derived exosomes and their role in cancer progression. Adv Clin Chem, 2016, 74: 103-141.
63. Qiu H, Liang J, Yang G, et al. Application of exosomes in tumor immunity: recent progresses. Front Cell Dev Biol, 2024, 12: 1372847. doi: 10.3389/fcell.2024.1372847.
64. Que RS, Lin C, Ding GP, et al. Increasing the immune activity of exosomes: the effect of miRNA-depleted exosome proteins on activating dendritic cell/cytokine-induced killer cells against pancreatic cancer. J Zhejiang Univ Sci B, 2016, 17(5): 352-360.
65. Guo M, Sun C, LiuR, et al. A drug delivery platform using engineered MUC1‐targeting exosomes enhances chemosensitivity and immunogenic cell death in pancreatic ductal adenocarcinoma. SmartMat, 2024, 5(5): e1279. doi: 10.1002/SMM2.1279.
66. Chen L, Wang L, Zhu L, et al. Exosomes as drug carriers in anti-cancer therapy. Front Cell Dev Biol, 2022, 10: 728616. doi: 10.3389/fcell.2022.728616.
67. Al Faruque H, Choi ES, Kim JH, et al. Enhanced effect of autologous EVs delivering paclitaxel in pancreatic cancer. J Control Release, 2022, 347: 330-346.
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