Calreticulin promotes migration and invasion of esophageal cancer cells by upregulating neuropilin-1 expression via STAT5A

Clinical Cancer Research

Volumn 20, Issue 23, 2014, Pages 6153-6162

  Shi, Feng ^a   Shang, Li ^a   Pan, Bei Qing ^a   Wang, Xiao Min ^a   Jiang, Yan Yi ^a   Hao, Jia Jie ^a   Zhang, Yu ^a   Cai, Yan ^a   Xu, Xin ^a   Zhan, Qi Min ^a   Wang, Ming Rong ^a  

^a CANCER HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALRETICULIN; FOCAL ADHESION KINASE; GELATINASE A; NEUROPILIN 1; SHORT HAIRPIN RNA; STAT5A PROTEIN; STAT5 PROTEIN; STAT5A PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; CALRETICULIN GENE; CARCINOMA CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME REGULATION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; GENE FUNCTION; GENE SILENCING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PHENOTYPE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REPORTER GENE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL MOTION; DISEASE MODEL; ESOPHAGUS TUMOR; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CALRETICULIN; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE MODELS, ANIMAL; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; LYMPHATIC METASTASIS; MICE; NEUROPILIN-1; STAT5 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84918576886     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0583     Document Type: Article

References (36)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90.
2. Enzinger PC, Mayer RJ Esophageal cancer. N Engl J Med 2003; 349: 2241-52.
3. Du XL, Hu H, Lin D.C., Xia SH, Shen XM, Zhang Y, et al Proteomic profiling of proteins dysregulated in Chinese esophageal squamous cell carcinoma. J Mol Med 2007; 85:863-75.
4. Michalak M, Groenendyk J, Szabo E., Gold LI, Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic retic-ulum. Biochem J 2009; 417:651-66.
5. Chen CN, Chang CC, Su T.E., Hsu WM, Jeng YM, Ho MC, et al Identification of calreticulin as a prognosis marker and angio-genic regulator in human gastric cancer. Ann Surg Oncol 2009; 16: 524-33.
6. Lu YC, Chen CN, Wang B, Hsu WM, Chen ST, Chang KJ, et al. Changes in tumor growth and metastatic capacities of J82 human bladder cancer cells suppressed by down-regulation of calreticulin expression. Am J Pathol 2011; 179:1425-33.
7. Eric A, Juranic Z, Milovanovic Z., Markovic I, Inic M, Stanojevic-Bakic N, et al. Effects of humoral immunity and calreticulin over-expression on postoperative course in breast cancer. Pathol Oncol Res 2009; 15:89-90.
8. Eric-Nikolic A., Milovanovic Z, Sanchez D., Pekarikova A, Dzodic R, Matic I.Z., et al. Overexpression of calreticulin in malignant and benign breast tumors: relationship with humoral immunity. Oncology 2012; 82:48-55.
9. Wang WA, Groenendyk J, Michalak M. Calreticulin signaling in health and disease. Int J Biochem Cell Biol 2012; 44:842-6.
10. Wang XM, Shang L, Zhang Y., Hao JJ, Shi F, Luo W, et al PTP1B contributes to calreticulin-induced metastatic phenotypes in esophageal squamous cell carcinoma. Mol Cancer Res 2013; 11: 986-94.
11. Pellet-Many C., Frankel P, Jia H., Zachary I. Neuropilins: structure, function and role in disease. Biochem J 2008; 411:211-26.
12. Horowitz A, Seerapu HR Regulation of VEGF signaling by membrane traffic. Cell Signal 2012; 24:1810-20.
13. Rizzolio S, Rabinowicz N, Rainero E., Lanzetti L, Serini G, Norman J., et al. Neuropilin-1-Dependent Regulation of EGF-Receptor Signaling. Cancer Res 2012; 72:5801-11.
14. Guttmann-Raviv N., Kessler O, Shraga-Heled N, Lange T., Herzog Y, Neufeld G. The neuropilins and their role in tumorigenesis and tumor progression. Cancer Lett 2006; 231:1-11.
15. Du XL, Yang H, Liu S.G., Luo ML, Hao JJ, Zhang Y, et al Calreticulin promotes cell motility and enhances resistance to anoikis through STAT3-CTTN-Akt pathway in esophageal squamous cell carcinoma. Oncogene 2009; 28:3714-22.
16. Shen WD, Ji Y, Liu P.F., Xiang B., Chen GQ, Huang B, et al. Correlation of E-cadherin and CD44v6 expression with clinical pathology in esoph-ageal carcinoma. Mol Med Rep 2012; 5:817-21.
17. Lv J, Cao XF, Ji L, Zhu B., Wang DD, Tao L, et al. Association of beta-catenin, Wnt1, Smad4, Hoxa9, and Bmi-1 with the prognosis of esophageal squamous cell carcinoma. Med Oncol 2012; 29: 151-60.
18. Cai HX, Yang LC, Song X.H., Liu ZR, Chen YB, Dong GK. Expression of paxillin and FAK mRNA and the related clinical significance in esophageal carcinoma. Mol Med Rep 2012; 5: 469-72.
19. Shen YG, Xu YJ, Shi Z.L., Han HL, Sun DQ, Zhang X. Effects of RNAi-mediated matrix metalloproteinase-2 gene silencing on the invasive-ness and adhesion of esophageal carcinoma cells, KYSE150. Dig Dis Sci 2012; 57:32-7.
20. Gu ZD, Chen KN, Li M, Gu J., Li JY. Clinical significance of matrix metalloproteinase-9 expression in esophageal squamous cell carcinoma. World J Gastroenterol 2005; 11:871-4.
21. Si J, Collins SJ Activated Ca2+/calmodulin-dependent protein kinase IIgamma is a critical regulator of myeloid leukemia cell proliferation. Cancer Res 2008; 68:3733-42.
22. Hanahan D, Weinberg RA Hallmarks of cancer: the next generation. Cell 2011; 144:646-74.
23. Ellis LM. The role of neuropilins in cancer. Mol Cancer Ther 2006; 5:1099-107.
24. Ochiumi T, Kitadai Y, Tanaka S., Akagi M, Yoshihara M, Chayama K. Neuropilin-1 is involved in regulation of apoptosis and migration of human colon cancer. Int J Oncol 2006; 29: 105-16.
25. Xu Y, Li P, Zhang X., Wang J, Gu D, Wang Y. Prognostic implication of neuropilin-1 upregulation in human nasopharyngeal carcinoma. Diagn Pathol 2013; 8:155.
26. Hansel DE, Wilentz RE, Yeo C.J., Schulick RD, Montgomery E, Maitra A. Expression of neuropilin-1 in high-grade dysplasia, invasive cancer, and metastases of the human gastrointestinal tract. Am J Surg Pathol 2004; 28:347-56.
27. Cao Y, Wang L, Nandy D, Zhang Y, Basu A, Radisky D, et al. Neuropilin-1 upholds dedifferentiation and propagation phenotypes of renal cell carcinoma cells by activating Akt and sonic hedgehog axes. Cancer Res 2008; 68:8667-72.
28. Matsushita A, Gotze T, Korc M. Hepatocyte growth factor-mediated cell invasion in pancreatic cancer cells is dependent on neuropilin-1. Cancer Res 2007; 67:10309-16.
29. Gray MJ, Wey JS, Belcheva A, McCarty M.F., Trevino JG, Evans DB, et al. Neuropilin-1 suppresses tumorigenic properties in a human pancreatic adenocarcinoma cell line lacking neuropilin-1 coreceptors. Cancer Res 2005; 65:3664-70.
30. Wan L, Pantel K, Kang Y. Tumor metastasis: moving new biological insights into the clinic. Nat Med 2013; 19:1450-64.
31. Nasarre P, Kusy S, Constantin B., Castellani V, Drabkin HA, Bagnard D, et al Semaphorin SEMA3F has a repulsing activity on breast cancer cells and inhibits E-cadherin-mediated cell adhesion. Neoplasia 2005; 7:180-9.
32. Papp S, Szabo E, Kim H., McCulloch CA, Opas M. Kinase-dependent adhesion to fibronectin: regulation by calreticulin. Exp Cell Res 2008; 314:1313-26.
33. Okutani Y, Kitanaka A, Tanaka T., Kamano H, Ohnishi H, Kubota Y., et al. Src directly tyrosine-phosphorylates STAT5 on its activation site and is involved in erythropoietin-induced signaling pathway. Oncogene 2001; 20:6643-50.
34. Hong TM, Chen YL, Wu Y.Y., Yuan A., Chao YC, Chung YC, et al. Targeting neuropilin 1 as an antitumor strategy in lung cancer. Clin Cancer Res 2007; 13:4759-68.
35. Snuderl M, Batista A, Kirkpatrick ND, RuizdeAlmodovar C, Riedemann L, Walsh EC, et al. Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell 2013; 152:1065-76.
36. Lee E, Koskimaki JE, Pandey N.B., Popel AS. Inhibition of lymphangio-genesis and angiogenesis in breast tumor xenografts and lymph nodes by a peptide derived from transmembrane protein 45A. Neoplasia 2013; 15:112-24.