Transforming growth factor-β binding receptor endoglin (CD105) expression in esophageal cancer and in adjacent nontumorous esophagus as prognostic predictor of recurrence

Annals of Surgical Oncology

Volumn 14, Issue 11, 2007, Pages 3232-3242

  Bellone, Graziella ^a   Solerio, Dino ^a   Chiusa, Luigi ^a   Brondino, Gabriele ^a   Carbone, Anna ^a,b   Prati, Adriana ^a   Scirelli, Tiziana ^a   Camandona, Michele ^a   Palestro, Giorgio ^a   Dei Poli, Marcello ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b MOLINETTE HOSPITAL   (Italy)

Author keywords

CD34; Endoglin; Esophageal cancer; Microvessel density; Tumor angiogenesis

Indexed keywords

ENDOGLIN; MESSENGER RNA;

ADENOCARCINOMA; ADULT; AGED; ARTICLE; BARRETT ESOPHAGUS; CANCER RECURRENCE; CANCER SURVIVAL; CLINICAL ARTICLE; CORRELATION ANALYSIS; DISEASE FREE SURVIVAL; ENDOTHELIUM CELL; ESOPHAGUS; ESOPHAGUS CANCER; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; PROGNOSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VASCULAR ENDOTHELIUM;

ADENOCARCINOMA; ADULT; AGED; ANTIGENS, CD; BARRETT ESOPHAGUS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; ESOPHAGEAL NEOPLASMS; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHATIC METASTASIS; MALE; MICROCIRCULATION; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; PROGNOSIS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 35348907869     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-007-9528-z     Document Type: Article

References (65)

1. Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 1990;82:4-6
2. Auguste P, Lemiere S, Larrieu-Lahargue F, Bikfalvi A. Molecular mechanisms of tumor vascularization. Crit Rev Oncol Hematol 2005;54:53-61
3. Hobson B, Denekamp J. Endothelial proliferation in tumours and normal tissues: continuous labelling studies. Br J Cancer 1984;49:405-13
4. Herlyn M. Endothelial cells as targets for tumor therapy. J Immunother 1999;22:185
5. Nagy JA, Brown LF, Senger DR, Lanir N, Van de Water L, Dvorak AM, Dvorak HF. Pathogenesis of tumor stroma generation: a critical role for leaky blood vessels and fibrin deposition. Biochim Biophys Acta 1989;948:305-26
6. American Cancer Society. Cancer facts and figures 2006. Atlanta: American Cancer Society, 2006 Accessed online April 24, 2006, at http://www.cancer.org
7. Blot WJ, McLaughlin JK. The changing epidemiology of esophageal cancer. Semin Oncol 1999;26:2-8
8. Tanigawa N, Matsumura M, Amaya H, et al. Tumor vascularity correlates with the prognosis of patients with esophageal squamous cell carcinoma. Cancer 1997;79:220-5
9. Shimada H, Hoshino T, Okazumi S, et al. Expression of angiogenic factors predicts response to chemoradiotherapy and prognosis of oesophageal squamous cell carcinoma. Br J Cancer 2002;86:552-7
10. Kitadai Y, Amioka T, Haruma K, et al. Clinicopathological significance of vascular endothelial growth factor (VEGF)-C in human esophageal squamous cell carcinomas. Int J Cancer 2001;93:662-6
11. Lord RV, Park JM, Wickramasinghe K, et al. Vascular endothelial growth factor and basic fibroblast growth factor expression in esophageal adenocarcinoma and Barrett esophagus. J Thorac Cardiovasc Surg 2003;125:246-53
12. Torres C, Wang H, Turner J, Shahsafaei A, Odze RD. Prognostic significance and effect of chemoradiotherapy on microvessel density (angiogenesis) in esophageal Barrett's esophagus-associated adenocarcinoma and squamous cell carcinoma. Hum Pathol 1999;30:753-8
13. Barbara NP, Wrana JL, Letarte M. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-β superfamily. J Biol Chem 1999;274:584-94
14. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M. Endoglin is a component of the transforming growth factor-β receptor system in human endothelial cells. J Biol Chem 1992;267:19027-30
15. Lastres P, Letamendia A, Zhang H, et al. Endoglin modulates cellular response to TGF-β1. J Cell Biol 1996;133:1109-21
16. Letamendia A, Lastres P, Botella LM, et al. Role of endoglin in cellular responses to transforming growth factor-β. J Biol Chem 1998;273:33011-9
17. Miller DW, Graulich W, Karges B, et al. Elevated expression of endoglin, a component of the TGF-β-receptor complex, correlates with proliferation of tumor endothelial cells. Int J Cancer 1999;81:568-72
18. Saad RS, Liu YL, Nathan G, Celebrezze J, Medich D, Silverman JF. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in colorectal cancer. Mod Pathol 2004;17:197-203
19. Akagi K, Ikeda Y, Sumiyoshi Y, Kimura Y, Kinoshita J, Miyazaki M, Abe T. Estimation of angiogenesis with anti-CD105 immunostaining in the process of colorectal cancer development. Surgery 2002;131:S109-13
20. Yu JX, Zhang XT, Liao YQ, Zhang QY, Chen H, Lin M, Kumar S. Relationship between expression of CD105 and growth factors in malignant tumors of gastrointestinal tract and its significance. World J Gastroenterol 2003;9:2866-9
21. Dales JP, Garcia S, Andrac L, et al. Prognostic significance of angiogenesis evaluated by CD105 expression compared to CD31 in 905 breast carcinomas: correlation with long-term patient outcome. Int J Oncol 2004;24:1197-204
22. Dales JP, Garcia S, Bonnier P, et al. CD105 expression is a marker of high metastatic risk and poor outcome in breast carcinomas. Correlations between immunohistochemical analysis and long-term follow-up in a series of 929 patients. Am J Clin Pathol 2003;119:374-80
23. Behrem S, Zarkovic K, Eskinja N, Jonjic N. Endoglin is a better marker than CD31 in evaluation of angiogenesis in glioblastoma. Croat Med J 2005;46:417-22
24. Bodey B, Bodey B Jr, Siegel SE, Kaiser HE. Upregulation of endoglin (CD105) expression during childhood brain tumor-related angiogenesis. Anti-angiogenic therapy. Anticancer Res 1998;18:1485-500
25. Tanaka F, Otake Y, Yanagihara K, et al. Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res 2001;7:3410-5
26. Wikstrom P, Lissbrant IF, Stattin P, Egevad L, Bergh A. Endoglin (CD105) is expressed on immature blood vessels and is a marker for survival in prostate cancer. Prostate 2002;51:268-75
27. Brewer CA, Setterdahl JJ, Li MJ, Johnston JM, Mann JL, McAsey ME. Endoglin expression as a measure of microvessel density in cervical cancer. Obstet Gynecol 2000;96:224-8
28. Kumar S, Ghellal A, Li C, Byrne G, Haboubi N, Wang JM, Bundred N. Breast carcinoma: vascular density determined using CD105 antibody correlates with tumor prognosis. Cancer Res 1999;59:856-61
29. Schimming R, Marme D. Endoglin (CD105) expression in squamous cell carcinoma of the oral cavity. Head Neck 2002;24:151-6
30. Martone T, Rosso P, Albera R, et al. Prognostic relevance of CD105+ microvessel density in HNSCC patient outcome. Oral Oncol 2005;41:147-55
31. Yagasaki H, Kawata N, Takimoto Y, Nemoto N. Histopathological analysis of angiogenic factors in renal cell carcinoma. Int J Urol 2003;10:220-7
32. Japanese Society for Esophageal Diseases. Guide lines for the clinical and pathologic studies of the esophagus. 9th ed. Tokyo, Japan: Kanehara, 1999
33. Lastres P, Bellon T, Cabanas C, et al. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur J Immunol 1992;22:393-7
34. Bernabeu C, Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 2003;339:62-6
35. Rasmussen R. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, (eds). Rapid Cycle Real-time PCR, Methods and Applications. Heidelberg: Springer, 2001:21-34
36. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002;30:e36
37. Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis correlation in invasive breast carcinoma. N Engl J Med 1991;324:1-8
38. Nakagawa S, Kitoh T. Measurement of KIT ligand/stem cell factor: clinical and biochemical significance. Curr Opin Hematol 2000;7:133-42
39. Abdalla SA, Behzad F, Bsharah S, Kumar S, Amini SK, O'Dwyer ST, Habaubi NY. Prognostic relevance of microvessel density in colorectal tumours. Oncol Rep 1999;6:839-42
40. Vermeulen PB, Van den Eynden GG, Huget P, et al. Prospective study of intratumoral microvessel density, p53 expression and survival in colorectal cancer. Br J Cancer 1999;79:316-22
41. Arakawa A, Soh S, Chakraborty S, Scardino PT, Wheeler TM. Prognostic significance of angiogenesis in clinically localized prostate cancer (staining for factor VIII-related antigen and CD34 antigen). Prostate Cancer Prostatic Dis 1997;1:32-8
42. Prall F, Gringmuth U, Nizze H, Barten M. Microvessel densities and microvascular architecture in colorectal carcinomas and their liver metastases: Significant correlation of high microvessel densities with better survival. Histopathology 2003;42:482-91
43. Dekel Y, Koren R, Kugel V, Livne PM, Gal R. Significance of angiogenesis and microvascular invasion in renal cell carcinoma. Pathol Oncol Res 2002;8:129-32
44. Pruneri G, Ponzoni M, Ferreri AJ, et al. Microvessel density, a surrogate marker of angiogenesis, is significantly related to survival in multiple myeloma patients. Br J Haematol 2002;118:817-20
45. Fonsatti E, Altomonte M, Nicotra MR, Natali PG, Maio M. Endoglin (CD105): a powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003;22:6557-63
46. Wang JM, Kumar S, Pye D, van Agthoven AJ, Krupinski J, Hunter RD. A monoclonal antibody detects heterogeneity in vascular endothelium of tumours and normal tissues. Int J Cancer 1993;54:363-70
47. Bodey B, Bodey B Jr, Siegel SE, Kaiser HE. Upregulation of endoglin (CD105) expression during childhood brain tumor-related angiogenesis. Anti-angiogenic therapy. Anticancer Res 1998;18:1485-500
48. Dales JP, Garcia S, Carpentier S, et al. Long-term prognostic significance of neoangiogenesis in breast carcinomas: comparison of Tie-2/Tek, CD105, and CD 31 immunocytochemical expression. Hum Pathol 2004;35:176-83
49. Minhajat R, Mori D, Yamasaki F, Sugita Y, Satoh T, Tokunaga O. Endoglin (CD 105) expression in angiogenesis of colon cancer; analysis using tissue microarrays and comparison with other endothelial markers. Vichows Arch 2005;22:1-8
50. Santos L, Costa C, Pereira S, et al. Neovascularisation is a prognostic factor of early recurrence in T1/G2 urothelial bladder tumours. Ann Oncol 2003;14:1419-24
51. Yao Y, Kubota T, Takeuchi H, Sato K. Prognostic significance of microvessel density determined by an anti-CD105/endoglin monoclonal antibody in astrocytic tumors: comparison with an anti-CD31 monoclonal antibody. Neuropathology 2005;25:201-6
52. Williams LJ, Guernsey DL, Casson AG. Biomarkers in the molecular pathogenesis of esophageal (Barrett) adenocarcinoma. Curr Oncol. 2006; 13:33-43
53. Fidler IJ, DeVita VT, Hellman S Jr, et al. (eds). Molecular biology of cancer: invasion and metastasis. Cancer: Principles and Practice of Oncology. 5th ed. Philadelphia: Lippincott-Raven, 1997:135-52
54. Zetter BR. Angiogenesis and tumor metastasis. Annu Rev Med 1998;49:407-24
55. Duff SE, Li C, Garland JM, Kumar S. CD105 is important for angiogenesis: evidence and potential applications. FASEB J 2003;17:984-92
56. Furstenberger G, von Moos R, Lucas R, Thurlimann B, Senn HJ, Hamacher J, Boneberg EM. Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy of primary breast cancer. Br J Cancer 2006;94:524-31
57. Folkman J. Tumor angiogenesis. Adv Cancer Res 1985;43:175-203
58. Li C, Guo B, Wilson PB, Stewart A, Byrne G, Bundred N, Kumar S. Plasma levels of soluble CD105 correlate with metastasis in patients with breast cancer. Int J Cancer 2000;89:122-6
59. Takahashi N, Kawanishi-Tabata R, Haba A, Tabata M, Haruta Y, Tsai H, Seon BK. Association of serum endoglin with metastasis in patients with colorectal, breast, and other solid tumors, and suppressive effect of chemotherapy on the serum endoglin. Clin Cancer Res 2001;7:524-732
60. McKian KP, Miller RC, Cassivi SD, Jatoi A. Curing patients with locally advanced esophageal cancer: an update on multimodality therapy. Dis Esophagus 2006;19:448-53
61. Roder JD, Busch R, Stein HJ, Fink U, Siewert JR. Ratio of invaded to removed lymph nodes as a predictor of survival in squamous cell carcinoma of the oesophagus. Br J Surg 1994;81:410-3
62. Aklilu M, Ilson DH. Targeted agents and esophageal cancer-the next step? Semin Radiat Oncol 2007;17:62-9
63. Bourdeau A, Dumont DJ, Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 1999;104:1343-51
64. Seon BK, Matsuno F, Haruta Y, Kondo M, Barcos M. Long-lasting complete inhibition of human solid tumors in SCID mice by targeting endothelial cells of tumor vasculature with antihuman endoglin immunotoxin. Clin Cancer Res 1997;3:1031-44
65. Matsuno F, Haruta Y, Kondo M, Tsai H, Barcos M, Seon BK. Induction of lasting complete regression of preformed distinct solid tumors by targeting the tumor vasculature using two new anti-endoglin monoclonal antibodies. Clin Cancer Res 1999;5:371-82