Changes and effects of lymphatic vessels and lymphatic endothelial cells in lymph node metastasis of esophageal cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

GUO Jiayi ^1,2 , ALIMUJIANG·Muming ^1,2 ,  EDRIS·Awut ^1,2 , ZHANG Haiping ^1,2 , ZHAGN Liwei ^1,2

1. Department of Thoracic Surgery, The First Affiliated Hospital of Xinjiang Medical University, Urumqi, 830054, P. R. China;
2. State Key Laboratory of Xinjiang Medical University, Urumqi, 830054, P. R. China;

Corresponding?author：

EDRIS·Awut, Email: 15999180777@qq.com

Keywords：

Esophageal cancer; lymphatic metastasis; lymphatic endothelial cell; tumor-related lymph vessels; review

DOI：

10.7507/1007-4848.202207054

Video：

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Abstract Full text Figures/Tables Video References Cited by

The lymphatic system is the main way of tumor metastasis and diffusion. Esophageal cancer is one of the typical cancers that are prone to metastasis through the lymphatic system. At present, an increasing number of studies show that the interaction between tumor cells and lymphatic endothelial cells is the first step in tumor lymphatic metastasis, but the underlying molecular mechanism is unclear. This article reviews the role and changes of tumor-related lymphatic vessels and lymphatic endothelial cells in the process of tumor lymphatic metastasis, which lays a foundation for further study of the specific molecular mechanism of esophageal cancer lymphatic metastasis and provides a new treatment direction for esophageal cancer patients.

Citation： GUO Jiayi, ALIMUJIANG·Muming, EDRIS·Awut, ZHANG Haiping, ZHAGN Liwei. Changes and effects of lymphatic vessels and lymphatic endothelial cells in lymph node metastasis of esophageal cancer. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(5): 766-772. doi: 10.7507/1007-4848.202207054 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Akutsu Y, Matsubara H. The significance of lymph node status as a prognostic factor for esophageal cancer. Surg Today, 2011, 41(9): 1190-1195.
3.	Tachimori Y, Nagai Y, Kanamori N, et al. Pattern of lymph node metastases of esophageal squamous cell carcinoma based on the anatomical lymphatic drainage system. Dis Esophagus, 2011, 24(1): 33-38.
4.	Nafteux P, Depypere L, Van Veer H, et al. Principles of esophageal cancer surgery, including surgical approaches and optimal node dissection (2- vs. 3-field). Ann Cardiothorac Surg, 2017, 6(2): 152-158.
5.	Wang F, Zheng Y, Wang Z, et al. Nodal skip metastasis in esophageal squamous cell carcinoma patients undergoing three-field lymphadenectomy. Ann Thorac Surg, 2017, 104(4): 1187-1193.
6.	Oliver G, Kipnis J, Randolph GJ, et al. The lymphatic vasculature in the 21st century: Novel functional roles in homeostasis and disease. Cell, 2020, 182(2): 270-296.
7.	Valastyan S, Weinberg RA. Tumor metastasis: Molecular insights and evolving paradigms. Cell, 2011, 147(2): 275-292.
8.	Lee BS, Jang JY, Seo C, et al. Crosstalk between head and neck cancer cells and lymphatic endothelial cells promotes tumor metastasis via CXCL5-CXCR2 signaling. FASEB J, 2021, 35(1): e21181.
9.	Ferris RL, Lotze MT, Leong SP, et al. Lymphatics, lymph nodes and the immune system: Barriers and gateways for cancer spread. Clin Exp Metastasis, 2012, 29(7): 729-736.
10.	Liu ZY, Qiu HO, Yuan XJ, et al. Suppression of lymphangiogenesis in human lymphatic endothelial cells by simultaneously blocking VEGF-C and VEGF-D/VEGFR-3 with norcantharidin. Int J Oncol, 2012, 41(5): 1762-1772.
11.	Rebhun RB, Langley RR, Yokoi K, et al. Targeting receptor tyrosine kinase on lymphatic endothelial cells for the therapy of colon cancer lymph node metastasis. Neoplasia, 2006, 8(9): 747-757.
12.	于亮, 龐作良, 張煜. 胸段食管癌腹腔淋巴結轉移的臨床分析. 新疆醫科大學學報, 2007, 12: 1390-1392.
13.	Kuge K, Murakami G, Mizobuchi S, et al. Submucosal territory of the direct lymphatic drainage system to the thoracic duct in the human esophagus. J Thorac Cardiovasc Surg, 2003, 125(6): 1343-1349.
14.	Saito H, Sato T, Miyazaki M. Extramural lymphatic drainage from the thoracic esophagus based on minute cadaveric dissections: Fundamentals for the sentinel node navigation surgery for the thoracic esophageal cancers. Surg Radiol Anat, 2007, 29(7): 531-542.
15.	陳遠岷, 劉德森, 潘琪, 等. 胸段食管癌重點清掃淋巴結的臨床病理特點及預后分析. 中華臨床醫師雜志(電子版), 2014, 8(13): 2403-2407.
16.	徐成勝, 王鵬. 胸段食管鱗狀細胞癌淋巴結轉移規律研究. 中國實驗診斷學, 2022, 26(2): 190-193.
17.	Kim HE, Yang YH, Park BJ, et al. Skeletonizing en bloc esophagectomy revisited: Oncologic outcome in association with the presence of thoracic duct lymph nodes. Ann Surg Oncol, 2022, 29(8): 4909-4917.
18.	Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
19.	Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅡandⅢ. Esophagus, 2017, 14(1): 37-65.
20.	Dong Y, Guan H, Huang W, et al. Precise delineation of clinical target volume for crossing-segments thoracic esophageal squamous cell carcinoma based on the pattern of lymph node metastases. J Thorac Dis, 2015, 7(12): 2313-2320.
21.	Hagens ERC, van Berge Henegouwen MI, Gisbertz SS. Distribution of lymph node metastases in esophageal carcinoma patients undergoing upfront surgery: A systematic review. Cancers (Basel), 2020, 12(6): 1592.
22.	Lund AW. Rethinking lymphatic vessels and antitumor immunity. Trends Cancer, 2016, 2(10): 548-551.
23.	Shields JD, Kourtis IC, Tomei AA, et al. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science, 2010, 328(5979): 749-752.
24.	Takeda A, Hollmén M, Dermadi D, et al. Single-cell survey of human lymphatics unveils marked endothelial cell heterogeneity and mechanisms of homing for neutrophils. Immunity, 2019, 51(3): 561-572.
25.	Zhang F, Zarkada G, Yi S, et al. Lymphatic endothelial cell junctions: Molecular regulation in physiology and diseases. Front Physiol, 2020, 11: 509.
26.	樊天斐, 高冉, 郭文鈞, 等. 淋巴管內皮細胞在淋巴管生成異常相關疾病中的研究進展. 生理科學進展, 2021, 52(4): 253-258.
27.	Jalkanen S, Salmi M. Lymphatic endothelial cells of the lymph node. Nat Rev Immunol, 2020, 20(9): 566-578.
28.	Park SM, Angel CE, McIntosh JD, et al. Mapping the distinctive populations of lymphatic endothelial cells in different zones of human lymph nodes. PLoS One, 2014, 9(4): e94781.
29.	Kerjaschki D. The lymphatic vasculature revisited. J Clin Invest, 2014, 124(3): 877.
30.	Lucas ED, Tamburini BAJ. Lymph node lymphatic endothelial cell expansion and contraction and the programming of the immune response. Front Immunol, 2019, 10: 36.
31.	Testa U, Pelosi E, Castelli G. Endothelial progenitors in the tumor microenvironment. Adv Exp Med Biol, 2020, 1263: 85-115.
32.	Ran S, Volk-Draper L. Lymphatic endothelial cell progenitors in the tumor microenvironment. Adv Exp Med Biol, 2020, 1234: 87-105.
33.	Al-Rawi MA, Jiang WG. Lymphangiogenesis and cancer metastasis. Front Biosci (Landmark Ed), 2011, 16(2): 723-739.
34.	Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science, 2002, 296(5574): 1883-1886.
35.	Wong SY, Haack H, Crowley D, et al. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res, 2005, 65(21): 9789-9798.
36.	Tammela T, Alitalo K. Lymphangiogenesis: Molecular mechanisms and future promise. Cell, 2010, 140(4): 460-476.
37.	Timoshenko AV, Chakraborty C, Wagner GF, et al. COX-2-mediated stimulation of the lymphangiogenic factor VEGF-C in human breast cancer. Br J Cancer, 2006, 94(8): 1154-1163.
38.	Hirakawa S, Brown LF, Kodama S, et al. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood, 2007, 109(3): 1010-1017.
39.	Zheng W, Tammela T, Yamamoto M, et al. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood, 2011, 118(4): 1154-1162.
40.	Fujimoto N, He Y, D'Addio M, et al. Single-cell mapping reveals new markers and functions of lymphatic endothelial cells in lymph nodes. PLoS Biol, 2020, 18(4): e3000704.
41.	Cao R, Ji H, Feng N, et al. Collaborative interplay between FGF-2 and VEGF-C promotes lymphangiogenesis and metastasis. Proc Natl Acad Sci U S A, 2012, 109(39): 15894-15899.
42.	Bracher A, Cardona AS, Tauber S, et al. Epidermal growth factor facilitates melanoma lymph node metastasis by influencing tumor lymphangiogenesis. J Invest Dermatol, 2013, 133(1): 230-238.
43.	Karpinich NO, Kechele DO, Espenschied ST, et al. Adrenomedullin gene dosage correlates with tumor and lymph node lymphangiogenesis. FASEB J, 2013, 27(2): 590-600.
44.	Kesler CT, Liao S, Munn LL, et al. Lymphatic vessels in health and disease. Wiley Interdiscip Rev Syst Biol Med, 2013, 5(1): 111-124.
45.	Coso S, Bovay E, Petrova TV. Pressing the right buttons: Signaling in lymphangiogenesis. Blood, 2014, 123(17): 2614-2624.
46.	Tamburini BA, Burchill MA, Kedl RM. Antigen capture and archiving by lymphatic endothelial cells following vaccination or viral infection. Nat Commun, 2014, 5: 3989.
47.	Padera TP, Meijer EF, Munn LL. The lymphatic system in disease processes and cancer progression. Annu Rev Biomed Eng, 2016, 18: 125-158.
48.	Wang J, Huang Y, Zhang J, et al. NRP-2 in tumor lymphangiogenesis and lymphatic metastasis. Cancer Lett, 2018, 418: 176-184.
49.	Rudzińska M, Mikula M, Arczewska KD, et al. Transcription factor prospero homeobox 1 (PROX1) as a potential angiogenic regulator of follicular thyroid cancer dissemination. Int J Mol Sci, 2019, 20(22): 5619.
50.	Rudzińska M, Czarnocka B. The impact of transcription factor prospero homeobox 1 on the regulation of thyroid cancer malignancy. Int J Mol Sci, 2020, 21(9): 3220.
51.	Baluk P, McDonald DM. Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci, 2008, 1131: 1-12.
52.	Wu R, Sarkar J, Tokumaru Y, et al. Intratumoral lymphatic endothelial cell infiltration reflecting lymphangiogenesis is counterbalanced by immune responses and better cancer biology in the breast cancer tumor microenvironment. Ame J Cancer res, 2022, 12: 504-520.
53.	Obulkasim H, Shi X, Wang J, et al. Podoplanin is an important stromal prognostic marker in perihilar cholangiocarcinoma. Oncol Lett, 2018, 15(1): 137-146.
54.	Pan Y, Xia L. Emerging roles of podoplanin in vascular development and homeostasis. Front Med, 2015, 9(4): 421-430.
55.	Chen JM, Luo B, Ma R, et al. Lymphatic endothelial markers and tumor lymphangiogenesis assessment in human breast cancer. Diagnostics (Basel), 2021, 12(1): 4.
56.	Liu P, Zhou J, Zhu H, et al. VEGF-C promotes the development of esophageal cancer via regulating CNTN-1 expression. Cytokine, 2011, 55(1): 8-17.
57.	隋萍. 趨化因子受體CXCR-2在食管癌組織中的表達及與淋巴結轉移對指導預后的臨床意義. 山東大學, 2014.
58.	郭晶, 盧春來, 古杰, 等. 趨化因子受體7 (CXCR7) 在食管鱗形細胞癌組織中的表達及其臨床意義. 復旦學報(醫學版), 2013, 40(1): 26-30, 43.
59.	Guo J, Tong CY, Shi JG, et al. C-X-C motif chemokine ligand 12 (CXCL12)/C-X-C motif chemokine receptor 7(CXCR7) regulates epithelial-mesenchymal transition process and promotes the metastasis of esophageal cancer by activating signal transducer and activator of transcription 3 (STAT3) pathway. Bioengineered, 2022, 13(3): 7425-7438.
60.	李嘉, 王飛云, 郭石平. CCL20及其受體CCR6在食管鱗癌組織中的表達及意義. 中國藥物與臨床, 2014, 14(6): 748-749.
61.	Lian J, Liu S, Yue Y, et al. Eomes promotes esophageal carcinoma progression by recruiting Treg cells through the CCL20-CCR6 pathway. Cancer Sci, 2021, 112(1): 144-154.
62.	Xu X, Tang Y, Zhu J, et al. Endoplasmic reticulum stress-related four-biomarker risk classifier for survival evaluation in esophageal cancer. J Oncol, 2022, 2022: 5860671.
63.	宋永明. Ⅰ型膠原蛋白和TGF-β1在食管鱗癌中生物學意義的研究. 山東大學, 2014.
64.	Nakayama H, Ohuchida K, Yonenaga A, et al. S100P regulates the collective invasion of pancreatic cancer cells into the lymphatic endothelial monolayer. Int J Oncol, 2019, 55(1): 211-222.
65.	Kerjaschki D, Bago-Horvath Z, Rudas M, et al. Lipoxygenase mediates invasion of intrametastatic lymphatic vessels and propagates lymph node metastasis of human mammary carcinoma xenografts in mouse. J Clin Invest, 2011, 121(5): 2000-2012.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Akutsu Y, Matsubara H. The significance of lymph node status as a prognostic factor for esophageal cancer. Surg Today, 2011, 41(9): 1190-1195.
3. Tachimori Y, Nagai Y, Kanamori N, et al. Pattern of lymph node metastases of esophageal squamous cell carcinoma based on the anatomical lymphatic drainage system. Dis Esophagus, 2011, 24(1): 33-38.
4. Nafteux P, Depypere L, Van Veer H, et al. Principles of esophageal cancer surgery, including surgical approaches and optimal node dissection (2- vs. 3-field). Ann Cardiothorac Surg, 2017, 6(2): 152-158.
5. Wang F, Zheng Y, Wang Z, et al. Nodal skip metastasis in esophageal squamous cell carcinoma patients undergoing three-field lymphadenectomy. Ann Thorac Surg, 2017, 104(4): 1187-1193.
6. Oliver G, Kipnis J, Randolph GJ, et al. The lymphatic vasculature in the 21st century: Novel functional roles in homeostasis and disease. Cell, 2020, 182(2): 270-296.
7. Valastyan S, Weinberg RA. Tumor metastasis: Molecular insights and evolving paradigms. Cell, 2011, 147(2): 275-292.
8. Lee BS, Jang JY, Seo C, et al. Crosstalk between head and neck cancer cells and lymphatic endothelial cells promotes tumor metastasis via CXCL5-CXCR2 signaling. FASEB J, 2021, 35(1): e21181.
9. Ferris RL, Lotze MT, Leong SP, et al. Lymphatics, lymph nodes and the immune system: Barriers and gateways for cancer spread. Clin Exp Metastasis, 2012, 29(7): 729-736.
10. Liu ZY, Qiu HO, Yuan XJ, et al. Suppression of lymphangiogenesis in human lymphatic endothelial cells by simultaneously blocking VEGF-C and VEGF-D/VEGFR-3 with norcantharidin. Int J Oncol, 2012, 41(5): 1762-1772.
11. Rebhun RB, Langley RR, Yokoi K, et al. Targeting receptor tyrosine kinase on lymphatic endothelial cells for the therapy of colon cancer lymph node metastasis. Neoplasia, 2006, 8(9): 747-757.
12. 于亮, 龐作良, 張煜. 胸段食管癌腹腔淋巴結轉移的臨床分析. 新疆醫科大學學報, 2007, 12: 1390-1392.
13. Kuge K, Murakami G, Mizobuchi S, et al. Submucosal territory of the direct lymphatic drainage system to the thoracic duct in the human esophagus. J Thorac Cardiovasc Surg, 2003, 125(6): 1343-1349.
14. Saito H, Sato T, Miyazaki M. Extramural lymphatic drainage from the thoracic esophagus based on minute cadaveric dissections: Fundamentals for the sentinel node navigation surgery for the thoracic esophageal cancers. Surg Radiol Anat, 2007, 29(7): 531-542.
15. 陳遠岷, 劉德森, 潘琪, 等. 胸段食管癌重點清掃淋巴結的臨床病理特點及預后分析. 中華臨床醫師雜志(電子版), 2014, 8(13): 2403-2407.
16. 徐成勝, 王鵬. 胸段食管鱗狀細胞癌淋巴結轉移規律研究. 中國實驗診斷學, 2022, 26(2): 190-193.
17. Kim HE, Yang YH, Park BJ, et al. Skeletonizing en bloc esophagectomy revisited: Oncologic outcome in association with the presence of thoracic duct lymph nodes. Ann Surg Oncol, 2022, 29(8): 4909-4917.
18. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
19. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅡandⅢ. Esophagus, 2017, 14(1): 37-65.
20. Dong Y, Guan H, Huang W, et al. Precise delineation of clinical target volume for crossing-segments thoracic esophageal squamous cell carcinoma based on the pattern of lymph node metastases. J Thorac Dis, 2015, 7(12): 2313-2320.
21. Hagens ERC, van Berge Henegouwen MI, Gisbertz SS. Distribution of lymph node metastases in esophageal carcinoma patients undergoing upfront surgery: A systematic review. Cancers (Basel), 2020, 12(6): 1592.
22. Lund AW. Rethinking lymphatic vessels and antitumor immunity. Trends Cancer, 2016, 2(10): 548-551.
23. Shields JD, Kourtis IC, Tomei AA, et al. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science, 2010, 328(5979): 749-752.
24. Takeda A, Hollmén M, Dermadi D, et al. Single-cell survey of human lymphatics unveils marked endothelial cell heterogeneity and mechanisms of homing for neutrophils. Immunity, 2019, 51(3): 561-572.
25. Zhang F, Zarkada G, Yi S, et al. Lymphatic endothelial cell junctions: Molecular regulation in physiology and diseases. Front Physiol, 2020, 11: 509.
26. 樊天斐, 高冉, 郭文鈞, 等. 淋巴管內皮細胞在淋巴管生成異常相關疾病中的研究進展. 生理科學進展, 2021, 52(4): 253-258.
27. Jalkanen S, Salmi M. Lymphatic endothelial cells of the lymph node. Nat Rev Immunol, 2020, 20(9): 566-578.
28. Park SM, Angel CE, McIntosh JD, et al. Mapping the distinctive populations of lymphatic endothelial cells in different zones of human lymph nodes. PLoS One, 2014, 9(4): e94781.
29. Kerjaschki D. The lymphatic vasculature revisited. J Clin Invest, 2014, 124(3): 877.
30. Lucas ED, Tamburini BAJ. Lymph node lymphatic endothelial cell expansion and contraction and the programming of the immune response. Front Immunol, 2019, 10: 36.
31. Testa U, Pelosi E, Castelli G. Endothelial progenitors in the tumor microenvironment. Adv Exp Med Biol, 2020, 1263: 85-115.
32. Ran S, Volk-Draper L. Lymphatic endothelial cell progenitors in the tumor microenvironment. Adv Exp Med Biol, 2020, 1234: 87-105.
33. Al-Rawi MA, Jiang WG. Lymphangiogenesis and cancer metastasis. Front Biosci (Landmark Ed), 2011, 16(2): 723-739.
34. Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science, 2002, 296(5574): 1883-1886.
35. Wong SY, Haack H, Crowley D, et al. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res, 2005, 65(21): 9789-9798.
36. Tammela T, Alitalo K. Lymphangiogenesis: Molecular mechanisms and future promise. Cell, 2010, 140(4): 460-476.
37. Timoshenko AV, Chakraborty C, Wagner GF, et al. COX-2-mediated stimulation of the lymphangiogenic factor VEGF-C in human breast cancer. Br J Cancer, 2006, 94(8): 1154-1163.
38. Hirakawa S, Brown LF, Kodama S, et al. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood, 2007, 109(3): 1010-1017.
39. Zheng W, Tammela T, Yamamoto M, et al. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood, 2011, 118(4): 1154-1162.
40. Fujimoto N, He Y, D'Addio M, et al. Single-cell mapping reveals new markers and functions of lymphatic endothelial cells in lymph nodes. PLoS Biol, 2020, 18(4): e3000704.
41. Cao R, Ji H, Feng N, et al. Collaborative interplay between FGF-2 and VEGF-C promotes lymphangiogenesis and metastasis. Proc Natl Acad Sci U S A, 2012, 109(39): 15894-15899.
42. Bracher A, Cardona AS, Tauber S, et al. Epidermal growth factor facilitates melanoma lymph node metastasis by influencing tumor lymphangiogenesis. J Invest Dermatol, 2013, 133(1): 230-238.
43. Karpinich NO, Kechele DO, Espenschied ST, et al. Adrenomedullin gene dosage correlates with tumor and lymph node lymphangiogenesis. FASEB J, 2013, 27(2): 590-600.
44. Kesler CT, Liao S, Munn LL, et al. Lymphatic vessels in health and disease. Wiley Interdiscip Rev Syst Biol Med, 2013, 5(1): 111-124.
45. Coso S, Bovay E, Petrova TV. Pressing the right buttons: Signaling in lymphangiogenesis. Blood, 2014, 123(17): 2614-2624.
46. Tamburini BA, Burchill MA, Kedl RM. Antigen capture and archiving by lymphatic endothelial cells following vaccination or viral infection. Nat Commun, 2014, 5: 3989.
47. Padera TP, Meijer EF, Munn LL. The lymphatic system in disease processes and cancer progression. Annu Rev Biomed Eng, 2016, 18: 125-158.
48. Wang J, Huang Y, Zhang J, et al. NRP-2 in tumor lymphangiogenesis and lymphatic metastasis. Cancer Lett, 2018, 418: 176-184.
49. Rudzińska M, Mikula M, Arczewska KD, et al. Transcription factor prospero homeobox 1 (PROX1) as a potential angiogenic regulator of follicular thyroid cancer dissemination. Int J Mol Sci, 2019, 20(22): 5619.
50. Rudzińska M, Czarnocka B. The impact of transcription factor prospero homeobox 1 on the regulation of thyroid cancer malignancy. Int J Mol Sci, 2020, 21(9): 3220.
51. Baluk P, McDonald DM. Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci, 2008, 1131: 1-12.
52. Wu R, Sarkar J, Tokumaru Y, et al. Intratumoral lymphatic endothelial cell infiltration reflecting lymphangiogenesis is counterbalanced by immune responses and better cancer biology in the breast cancer tumor microenvironment. Ame J Cancer res, 2022, 12: 504-520.
53. Obulkasim H, Shi X, Wang J, et al. Podoplanin is an important stromal prognostic marker in perihilar cholangiocarcinoma. Oncol Lett, 2018, 15(1): 137-146.
54. Pan Y, Xia L. Emerging roles of podoplanin in vascular development and homeostasis. Front Med, 2015, 9(4): 421-430.
55. Chen JM, Luo B, Ma R, et al. Lymphatic endothelial markers and tumor lymphangiogenesis assessment in human breast cancer. Diagnostics (Basel), 2021, 12(1): 4.
56. Liu P, Zhou J, Zhu H, et al. VEGF-C promotes the development of esophageal cancer via regulating CNTN-1 expression. Cytokine, 2011, 55(1): 8-17.
57. 隋萍. 趨化因子受體CXCR-2在食管癌組織中的表達及與淋巴結轉移對指導預后的臨床意義. 山東大學, 2014.
58. 郭晶, 盧春來, 古杰, 等. 趨化因子受體7 (CXCR7) 在食管鱗形細胞癌組織中的表達及其臨床意義. 復旦學報(醫學版), 2013, 40(1): 26-30, 43.
59. Guo J, Tong CY, Shi JG, et al. C-X-C motif chemokine ligand 12 (CXCL12)/C-X-C motif chemokine receptor 7(CXCR7) regulates epithelial-mesenchymal transition process and promotes the metastasis of esophageal cancer by activating signal transducer and activator of transcription 3 (STAT3) pathway. Bioengineered, 2022, 13(3): 7425-7438.
60. 李嘉, 王飛云, 郭石平. CCL20及其受體CCR6在食管鱗癌組織中的表達及意義. 中國藥物與臨床, 2014, 14(6): 748-749.
61. Lian J, Liu S, Yue Y, et al. Eomes promotes esophageal carcinoma progression by recruiting Treg cells through the CCL20-CCR6 pathway. Cancer Sci, 2021, 112(1): 144-154.
62. Xu X, Tang Y, Zhu J, et al. Endoplasmic reticulum stress-related four-biomarker risk classifier for survival evaluation in esophageal cancer. J Oncol, 2022, 2022: 5860671.
63. 宋永明. Ⅰ型膠原蛋白和TGF-β1在食管鱗癌中生物學意義的研究. 山東大學, 2014.
64. Nakayama H, Ohuchida K, Yonenaga A, et al. S100P regulates the collective invasion of pancreatic cancer cells into the lymphatic endothelial monolayer. Int J Oncol, 2019, 55(1): 211-222.
65. Kerjaschki D, Bago-Horvath Z, Rudas M, et al. Lipoxygenase mediates invasion of intrametastatic lymphatic vessels and propagates lymph node metastasis of human mammary carcinoma xenografts in mouse. J Clin Invest, 2011, 121(5): 2000-2012.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Changes and effects of lymphatic vessels and lymphatic endothelial cells in lymph node metastasis of esophageal cancer

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