Migratory activity of CD105+ pancreatic cancer cells is strongly enhanced by pancreatic stellate cells

Pancreas

Volumn 42, Issue 8, 2013, Pages 1283-1290

  Fujiwara, Kenji ^a,b   Ohuchida, Kenoki ^a,b   Ohtsuka, Takao ^a,c   Mizumoto, Kazuhiro ^a   Shindo, Koji ^a,d,e   Ikenaga, Naoki ^a   Cui, Lin ^a   Takahata, Shunichi ^a   Aishima, Shinichi ^a   Tanaka, Masao ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c KYUSHU UNIVERSITY HOSPITAL   (Japan)

^d Japan Soc for Promotion of Science   (Japan)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CD105; endoglin; epithelial mesenchymal transition; pancreatic cancer; pancreatic stellate cells; tumor microenvironment

Indexed keywords

ENDOGLIN; MESSENGER RNA; UVOMORULIN; VIMENTIN;

ADULT; AGED; ARTICLE; CANCER CELL; CELL MIGRATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPH VESSEL; MALE; MICROENVIRONMENT; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREAS DUCT; PANCREATIC STELLATE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; BLOTTING, WESTERN; CADHERINS; CELL LINE, TUMOR; CELL MIGRATION ASSAYS; CELL MOVEMENT; COCULTURE TECHNIQUES; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; PROGNOSIS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIMENTIN;

EID: 84887317473     PISSN: 08853177     EISSN: 15364828     Source Type: Journal    
DOI: 10.1097/MPA.0b013e318293e7bd     Document Type: Article

References (36)

1. Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet. 2011;378:607Y620.
2. Hirata K, Egawa S, Kimura Y, et al. Current status of surgery for pancreatic cancer. Dig Surg. 2007;24:137Y147.
3. Corsini MM, Miller RC, Haddock MG, et al. Adjuvant radiotherapy and chemotherapy for pancreatic carcinoma: the Mayo Clinic experience (1975-2005). J Clin Oncol. 2008;26:3511Y3516.
4. Keedy VL, Berlin J. Adjuvant and neoadjuvant approaches to treat surgically resectable pancreatic cancer. Curr Treat Options Oncol. 2006;7:381Y388.
5. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105Y111.
6. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030Y1037.
7. O'Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106Y110.
8. Todaro M, Alea MP, Di Stefano AB, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1:389Y402.
9. Moriyama T, Ohuchida K, Mizumoto K, et al. Enhanced cell migration and invasion of CD133+ pancreatic cancer cells cocultured with pancreatic stromal cells. Cancer. 2010;116:3357Y3368.
10. Mahadevan D, Von Hoff DD. Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol Cancer Ther. 2007;6:1186Y1197.
11. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta. 2008;1782:197Y228.
12. Bernabeu C, Conley BA, Vary CP. Novel biochemical pathways of endoglin in vascular cell physiology. J Cell Biochem. 2007;102:1375Y1388.
13. Fonsatti E, Nicolay HJ, Altomonte M, et al. Targeting cancer vasculature via endoglin/CD105: a novel antibody-based diagnostic and therapeutic strategy in solid tumours. Cardiovasc Res. 2010;86:12Y19.
14. Perez-Gomez E, Del Castillo G, Juan Francisco S, et al. The role of the TGF-beta coreceptor endoglin in cancer. ScientificWorldJournal. 2010;10:2367Y2384.
15. Grange C, Tapparo M, Collino F, et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011;71:5346Y5356.
16. Bussolati B, Bruno S, Grange C, et al. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 2008;22:3696Y3705.
17. Liu Y, Jovanovic B, Pins M, et al. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene. 2002;21:8272Y8281.
18. Wong VC, Chan PL, Bernabeu C, et al. Identification of an invasion and tumor-suppressing gene, Endoglin (ENG), silenced by both epigenetic inactivation and allelic loss in esophageal squamous cell carcinoma. Int J Cancer. 2008;123:2816Y2823.
19. Henry LA, Johnson DA, Sarrio D, et al. Endoglin expression in breast tumor cells suppresses invasion and metastasis and correlates with improved clinical outcome. Oncogene. 2011;30:1046Y1058.
20. Bachem MG, Schneider E, Gross H, et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology. 1998;115:421Y432.
21. Apte MV, Park S, Phillips PA, et al. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas. 2004;29:179Y187.
22. Hwang RF, Moore T, Arumugam T, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008;68:918Y926.
23. Bachem MG, Schunemann M, Ramadani M, et al. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology. 2005;128:907Y921.
24. Ohuchida K, Mizumoto K, Murakami M, et al. Radiation to stromal fibroblasts increases invasiveness of pancreatic cancer cells through tumor-stromal interactions. Cancer Res. 2004;64:3215Y3222.
25. Fujita H, Ohuchida K, Mizumoto K, et al. Tumor-stromal interactions with direct cell contacts enhance proliferation of human pancreatic carcinoma cells. Cancer Sci. 2009;100:2309Y2317.
26. Zhang L, Mizumoto K, Sato N, et al. Quantitative determination of apoptotic death in cultured human pancreatic cancer cells by propidium iodide and digitonin. Cancer Lett. 1999;142:129Y137.
27. Yoshitomi H, Kobayashi S, Ohtsuka M, et al. Specific expression of endoglin (CD105) in endothelial cells of intratumoral blood and lymphatic vessels in pancreatic cancer. Pancreas. 2008;37:275Y281.
28. Saad RS, El-Gohary Y, Memari E, et al. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in esophageal adenocarcinoma. Hum Pathol. 2005;36:955Y961.
29. Yao Y, Pan Y, Chen J, et al. Endoglin (CD105) expression in angiogenesis of primary hepatocellular carcinomas: analysis using tissue microarrays and comparisons with CD34 and VEGF. Ann Clin Lab Sci. 2007;37:39Y48.
30. El-Gohary YM, Silverman JF, Olson PR, et al. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in prostatic adenocarcinoma. Am J Clin Pathol. 2007;127:572Y579.
31. Pardali E, van der Schaft DW, Wiercinska E, et al. Critical role of endoglin in tumor cell plasticity of Ewing sarcoma and melanoma. Oncogene. 2011;30:334Y345.
32. Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871Y890.
33. Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118:277Y279.
34. Zeng Q, Li W, Lu D, et al. CD146, an epithelial-mesenchymal transition inducer, is associated with triple-negative breast cancer. Proc Natl Acad Sci U S A. 2012;109:1127Y1132.
35. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265Y273.
36. Vonlaufen A, Joshi S, Qu C, et al. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res. 2008;68:2085Y2093.