Acidic extracellular ph promotes epithelial mesenchymal transition in lewis lung carcinoma model

Cancer Cell International

Volumn 14, Issue 1, 2014, Pages

  Suzuki, Atsuko ^a   Maeda, Toyonobu ^a   Baba, Yuh ^a   Shimamura, Kazuhiro ^a   Kato, Yasumasa ^a  

^a OHU UNIVERSITY   (Japan)

Author keywords

Acidic extracellular pH; EMT; Invasion; Lewis lung carcinoma; MMP 9

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE 14; REPRESSOR PROTEIN; STROMELYSIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; TWIST1 PROTEIN; TWIST2 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; ZEB2 PROTEIN;

ACIDITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; COBBLE STONE; DISEASE MODEL; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLASTIC; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; LEWIS CARCINOMA; METASTASIS POTENTIAL; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 84988530132     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/s12935-014-0129-1     Document Type: Article

References (43)

1. Gheldof A, Berx G: Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci 2013, 116:317-336.
2. Fujimoto J, Ichigo S, Hirose R, Sakaguchi H, Tamaya T: Suppression of E-cadherin and a-and ß-catenin mRNA expression in the metastatic lesions of gynecological cancers. Eur J Gynaecol Oncol 1997, 18:484-487.
3. Warburg O, Posener K, Negelein E: über den Stoffwechsel der Tumoren (On metabolism of tumors). Biochem Z 1924, 152:319-344.
4. Rofstad EK, Mathiesen B, Kindem K, Galappathi K: Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 2006, 66:6699-6707.
5. Kato Y, Ozawa S, Miyamoto C, Maehata Y, Suzuki A, Maeda T, Baba Y: Acidic extracellular microenvironment and cancer. Cancer Cell Int 2013, 13:89.
6. Kato Y, Nakayama Y, Umeda M, Miyazaki K: Induction of 103-kDa gelatinase/ type IV collagenase by acidic culture conditions in mouse metastatic melanoma cell lines. J Biol Chem 1992, 267:11424-11430.
7. Peppicelli S, Bianchini F, Torre E, Calorini L: Contribution of acidic melanoma cells undergoing epithelial-to-mesenchymal transition to aggressiveness of non-acidic melanoma cells. Clin Exp Metastasis 2014, 31:423-433.
8. Kim JE, Leung E, Baguley BC, Finlay GJ: Heterogeneity of expression of epithelial-mesenchymal transition markers in melanocytes and melanoma cell lines. Front Genet 2013, 4:97.
9. Martínez-Zaguilán R, Seftor EA, Seftor RE, Chu YW, Gillies RJ, Hendrix MJ: Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis 1996, 14:176-186.
10. Chen X, Xiao W, Wang W, Luo L, Ye S, Liu Y: The complex interplay between ERK1/2, TGFß/Smad, and Jagged/Notch signaling pathways in the regulation of epithelial-mesenchymal transition in retinal pigment epithelium cells. PLoS One 2014, 9:e96365.
11. Islam SS, Mokhtari RB, El Hout Y, Azadi MA, Alauddin M, Yeger H, Farhat WA: TGF-ß1 induces EMT reprogramming of porcine bladder urothelial cells into collagen producing fibroblasts-like cells in a Smad2/Smad3-dependent manner. J Cell Commun Signal 2014, 8:39-58.
12. Liu LC, Tsao TC, Hsu SR, Wang HC, Tsai TC, Kao JY, Way TD: EGCG inhibits transforming growth factor-ß-mediated epithelial-to-mesenchymal transition via the inhibition of Smad2 and Erk1/2 signaling pathways in nonsmall cell lung cancer cells. J Agric Food Chem 2012, 60:9863-9873.
13. Kumar M, Allison DF, Baranova NN, Wamsley JJ, Katz AJ, Bekiranov S, Jones DR, Mayo MW: NF-κB regulates mesenchymal transition for the induction of non-small cell lung cancer initiating cells. PLoS One 2013, 8:e68597.
14. Wu Y, Deng J, Rychahou PG, Qiu S, Evers BM, Zhou BP: Stabilization of snail by NF-κB is required for inflammation-induced cell migration and invasion. Cancer Cell 2009, 15:416-428.
15. Wang F, He W, Fanghui P, Wang L, Fan Q: NF-κBP65 promotes invasion and metastasis of oesophageal squamous cell cancer by regulating matrix metalloproteinase-9 and epithelial-to-mesenchymal transition. Cell Biol Int 2013, 37:780-788.
16. Wang Y, Yue B, Yu X, Wang Z, Wang M: SLUG is activated by nuclear factor kappa B and confers human alveolar epithelial A549 cells resistance to tumor necrosis factor-alpha-induced apoptosis. World J Surg Oncol 2013, 11:12.
17. Kawashima A, Nakanishi I, Tsuchiya H, Roessner A, Obata K, Okada Y: Expression of matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) induced by tumour necrosis factor alpha correlates with metastatic ability in a human osteosarcoma cell line. Virchows Arch 1994, 424:547-552.
18. Kato Y, Lambert CA, Colige AC, Mineur P, Noël A, Frankenne F, Foidart JM, Baba M, Hata RI, Miyazaki K, Tsukuda M: Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J Biol Chem 2005, 280:10938-10944.
19. Kato Y, Ozawa S, Tsukuda M, Kubota E, Miyazaki K, St-Pierre Y, Hata R: Acidic extracellular pH increases calcium influx-triggered phospholipase D activity along with acidic sphingomyelinase activation to induce matrix metalloproteinase-9 expression in mouse metastatic melanoma. FEBS J 2007, 274:3171-3183.
20. Qiao B, Johnson NW, Gao J: Epithelial-mesenchymal transition in oral squamous cell carcinoma triggered by transforming growth factor-ß1 is Snail family-dependent and correlates with matrix metalloproteinase-2 and -9 expressions. Int J Oncol 2010, 37:663-668.
21. Yu M, Sato H, Seiki M, Spiegel S, Thompson EW: Calcium influx inhibits MT1-MMP processing and blocks MMP-2 activation. FEBS Lett 1997, 412:568-572.
22. Symowicz J, Adley BP, Gleason KJ, Johnson JJ, Ghosh S, Fishman DA, Hudson LG, Stack MS: Engagement of collagen-binding integrins promotes matrix metalloproteinase-9-dependent E-cadherin ectodomain shedding in ovarian carcinoma cells. Cancer Res 2007, 67:2030-2039.
23. Zuo JH, Zhu W, Li MY, Li XH, Yi H, Zeng GQ, Wan XX, He QY, Li JH, Qu JQ, Chen Y, Xiao ZQ: Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin. J Cell Biochem 2011, 112:2508-2517.
24. Richter P, Umbreit C, Franz M, Berndt A, Grimm S, Uecker A, Bohmer FD, Kosmehl H, Berndt A: EGF/TGFß1 co-stimulation of oral squamous cell carcinoma cells causes an epithelial-mesenchymal transition cell phenotype expressing laminin 332. J Oral Pathol Med 2011, 40:46-54.
25. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, Morita I, Miyazono K, Saitoh M: TGF-ß regulates isoform switching of FGF receptors and epithelial-mesenchymal transition. EMBO J 2011, 30:783-795.
26. Helmlinger G, Sckell A, Dellian M, Forbes NS, Jain RK: Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res 2002, 8:1284-1291.
27. Salnikov AV, Liu L, Platen M, Gladkich J, Salnikova O, Ryschich E, Mattern J, Moldenhauer G, Werner J, Schemmer P, Buchler MW, Herr I: Hypoxia induces EMT in low and highly aggressive pancreatic tumor cells but only cells with cancer stem cell characteristics acquire pronounced migratory potential. PLoS One 2012, 7:e46391.
28. Kato Y, Ozono S, Shuin T, Miyazaki K: Slow induction of gelatinase B mRNA by acidic culture conditions in mouse metastatic melanoma cells. Cell Biol Int 1996, 20:375-377.
29. Fukumura D, Xu L, Chen Y, Gohongi T, Seed B, Jain RK: Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res 2001, 61:6020-6024.
30. Shi Q, Le X, Wang B, Abbruzzese JL, Xiong Q, He Y, Xie K: Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 2001, 20:3751-3756.
31. Xu L, Fukumura D, Jain RK: Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J Biol Chem 2002, 277:11368-11374.
32. Peppicelli S, Bianchini F, Contena C, Tombaccini D, Calorini L: Acidic pH via NF-κB favours VEGF-C expression in human melanoma cells. Clin Exp Metastasis 2013, 30:957-967.
33. Shi Q, Abbruzzese JL, Huang S, Fidler IJ, Xiong Q, Xie K: Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic. Clin Cancer Res 1999, 5:3711-3721.
34. Shi Q, Le X, Wang B, Xiong Q, Abbruzzese JL, Xie K: Regulation of interleukin-8 expression by cellular pH in human pancreatic adenocarcinoma cells. J Interferon Cytokine Res 2000, 20:1023-1028.
35. Xu L, Fidler IJ: Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells. Cancer Res 2000, 60:4610-4616.
36. Bellocq A, Suberville S, Philippe C, Bertrand F, Perez J, Fouqueray B, Cherqui G, Baud L: Low environmental pH is responsible for the induction of nitric-oxide synthase in macrophages. Evidence for involvement of nuclear factor-κB activation. J Biol Chem 1998, 273:5086-5092.
37. Griffiths L, Dachs GU, Bicknell R, Harris AL, Stratford IJ: The influence of oxygen tension and pH on the expression of platelet-derived endothelial cell growth factor/thymidine phosphorylase in human breast tumor cells grown in vitro and in vivo. Cancer Res 1997, 57:570-572.
38. Garcia-Sanz M, Simón-Marín R, Hilario E: Morphological characterization of Lewis lung carcinoma (3LL). A light and electron microscopic study. Tumori 1989, 75:23-27.
39. Sharma S, Zhu L, Yang SC, Zhang L, Lin J, Hillinger S, Gardner B, Reckamp K, Strieter RM, Huang M, Batra RK, Dubinett SM: Cyclooxygenase 2 inhibition promotes IFN-γ-dependent enhancement of antitumor responses. J Immunol 2005, 175:813-819.
40. Liu R, Khullar OV, Griset AP, Wade JE, Zubris KA, Grinstaff MW, Colson YL: Paclitaxel-loaded expansile nanoparticles delay local recurrence in a heterotopic murine non-small cell lung cancer model. Ann Thorac Surg 2011, 91:1077-1083. discussion 1083-1074.
41. Fidler IJ: Selection of successive tumour lines for metastasis. Nat New Biol 1973, 242:148-149.
42. Baba Y, Kato Y, Mochimatsu I, Nagashima Y, Kurihara M, Kawano T, Taguchi T, Hata R, Tsukuda M: Inostamycin suppresses vascular endothelial growth factor-stimulated growth and migration of human umbilical vein endothelial cells. Clin Exp Metastasis 2004, 21:419-425.
43. Baba Y, Tsukuda M, Mochimatsu I, Furukawa S, Kagata H, Nagashima Y, Sakai N, Koshika S, Imoto M, Kato Y: Inostamycin, an inhibitor of cytidine 5'-diphosphate 1,2-diacyl-sn-glycerol (CDP-DG): inositol transferase, suppresses invasion ability by reducing productions of matrix metalloproteinase-2 and -9 and cell motility in HSC-4 tongue carcinoma cell line. Clin Exp Metastasis 2000, 18:273-279.