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Published in: BMC Cancer 1/2018

Open Access 01-12-2018 | Research article

Evaluation of Endoglin (CD105) expression in pediatric rhabdomyosarcoma

Authors: Virginia Di Paolo, Ida Russo, Renata Boldrini, Lucilla Ravà, Marco Pezzullo, Maria Chiara Benedetti, Angela Galardi, Marta Colletti, Rossella Rota, Domenico Orlando, Alessandro Crocoli, Hector Peinado, Giuseppe Maria Milano, Angela Di Giannatale

Published in: BMC Cancer | Issue 1/2018

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Abstract

Background

The Intratumoral Microvessel Density (IMVD) is commonly used to quantify tumoral vascularization and is usually assessed by pan-endothelial markers, such as CD31. Endoglin (CD105) is a protein predominantly expressed in proliferating endothelium and the IMVD determined by this marker measures specifically the neovascularization. In this study, we investigated the CD105 expression in pediatric rhabdomyosarcoma and assessed the neovascularization by using the angiogenic ratio IMVD-CD105 to IMVD-CD31.

Methods

Paraffin-embedded archival tumor specimens were selected from 65 pediatric patients affected by rhabdomyosarcoma. The expression levels of CD105, CD31 and Vascular Endothelial Growth Factor (VEGF) were investigated in 30 cases (18 embryonal and 12 alveolar) available for this study. The IMVD-CD105 to IMVD-CD31 expression ratio was correlated with clinical and pathologic features of these patients.

Results

We found a specific expression of endoglin (CD105) in endothelial cells of all the rhabdomyosarcoma specimens analyzed. We observed a significant positive correlation between the IMVD individually measured by CD105 and CD31. The CD105/CD31 expression ratio was significantly higher in patients with lower survival and embryonal histology. Indeed, patients with a CD105/CD31 expression ratio < 1.3 had a significantly increased OS (88%, 95%CI, 60%–97%) compared to patients with higher values (40%, 95%CI, 12%–67%). We did not find any statistical correlation among VEGF and EFS, OS and CD105/CD31 expression ratio.

Conclusion

CD105 is expressed on endothelial cells of rhabdomyosarcoma and represent a useful tool to quantify neovascularization in this tumor. If confirmed by further studies, these results will indicate that CD105 is a potential target for combined therapies in rhabdomyosarcoma.
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Literature
1.
go back to reference Gurney JG, Young JL Jr, Roffers SD, Smith MA, Bunin GR. Soft tissue sarcomas. In: LAG R, Smith MA, Gurney JG, et al., editors. Cancer incidence and survival among children and adolescents: United States SEER program 1975–1995. Bethesda: National Cancer Institute, SEER Program; 1999. p. 111–23. NIH Pub. No. 99-4649. Gurney JG, Young JL Jr, Roffers SD, Smith MA, Bunin GR. Soft tissue sarcomas. In: LAG R, Smith MA, Gurney JG, et al., editors. Cancer incidence and survival among children and adolescents: United States SEER program 1975–1995. Bethesda: National Cancer Institute, SEER Program; 1999. p. 111–23. NIH Pub. No. 99-4649.
2.
go back to reference Sorensen PH, Lynch JC, Qualman SJ, et al. PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children’s oncology group. J Clin Oncol. 2002;20:2672–9.CrossRefPubMed Sorensen PH, Lynch JC, Qualman SJ, et al. PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children’s oncology group. J Clin Oncol. 2002;20:2672–9.CrossRefPubMed
3.
go back to reference McDowell HP, Foot AB, Ellershaw C, Machin D, Giraud C, Bergeron C. Outcomes in paediatric metastatic rhabdomyosarcoma: results of the International Society of Paediatric Oncology (SIOP) study MMT-98. Eur J Cancer. 2010;46(9):1588–95.CrossRefPubMed McDowell HP, Foot AB, Ellershaw C, Machin D, Giraud C, Bergeron C. Outcomes in paediatric metastatic rhabdomyosarcoma: results of the International Society of Paediatric Oncology (SIOP) study MMT-98. Eur J Cancer. 2010;46(9):1588–95.CrossRefPubMed
4.
go back to reference de Castro JG, Puglisi F, de Azambuja E, El Saghir NS, Awada A. Angiogenesis and cancer: a cross-talk between basic science and clinical trials (the “do ut des” paradigm). Crit Rev Oncol Hematol. 2006;59(1):40–50.CrossRef de Castro JG, Puglisi F, de Azambuja E, El Saghir NS, Awada A. Angiogenesis and cancer: a cross-talk between basic science and clinical trials (the “do ut des” paradigm). Crit Rev Oncol Hematol. 2006;59(1):40–50.CrossRef
5.
go back to reference Maris JM, Courtright J, Houghton PJ, Morton CL, Kolb EA, Lock R, Tajbakhsh M, Reynolds CP, Keir ST, Wu J, Smith MA. Initial testing (stage 1) of sunitinib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2008;51(1):42–8.CrossRefPubMed Maris JM, Courtright J, Houghton PJ, Morton CL, Kolb EA, Lock R, Tajbakhsh M, Reynolds CP, Keir ST, Wu J, Smith MA. Initial testing (stage 1) of sunitinib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2008;51(1):42–8.CrossRefPubMed
6.
go back to reference Kumar S, Mokhtari RB, Sheikh R, Wu B, Zhang L, Xu P, Man S, Oliveira ID, Yeger H, Kerbel RS, Baruchel S. Metronomic oral topotecan with pazopanib is an active antiangiogenic regimen in mouse models of aggressive pediatric solid tumor. Clin Cancer Res. 2011;17(17):5656–67.CrossRefPubMedPubMedCentral Kumar S, Mokhtari RB, Sheikh R, Wu B, Zhang L, Xu P, Man S, Oliveira ID, Yeger H, Kerbel RS, Baruchel S. Metronomic oral topotecan with pazopanib is an active antiangiogenic regimen in mouse models of aggressive pediatric solid tumor. Clin Cancer Res. 2011;17(17):5656–67.CrossRefPubMedPubMedCentral
7.
go back to reference Keir ST, Morton CL, Wu J, Kurmasheva RT, Houghton PJ, Smith MA. Initial testing of the multitargeted kinase inhibitor pazopanib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2012;59(3):586–8.CrossRefPubMed Keir ST, Morton CL, Wu J, Kurmasheva RT, Houghton PJ, Smith MA. Initial testing of the multitargeted kinase inhibitor pazopanib by the pediatric preclinical testing program. Pediatr Blood Cancer. 2012;59(3):586–8.CrossRefPubMed
8.
go back to reference Navid F, Baker SD, McCarville MB, Stewart CF, Billups CA, Wu J, Davidoff AM, Spunt SL, Furman WL, McGregor LM, Hu S, Panetta JC, Turner D, Fofana D, Reddick WE, Leung W, Santana VM. Phase I and clinical pharmacology study of bevacizumab, sorafenib, and low-dose cyclophosphamide in children and young adults with refractory/recurrent solid tumors. Clin Cancer Res. 2013;19(1):236–46.CrossRefPubMed Navid F, Baker SD, McCarville MB, Stewart CF, Billups CA, Wu J, Davidoff AM, Spunt SL, Furman WL, McGregor LM, Hu S, Panetta JC, Turner D, Fofana D, Reddick WE, Leung W, Santana VM. Phase I and clinical pharmacology study of bevacizumab, sorafenib, and low-dose cyclophosphamide in children and young adults with refractory/recurrent solid tumors. Clin Cancer Res. 2013;19(1):236–46.CrossRefPubMed
9.
go back to reference Glade Bender JL, Lee A, Reid JM, Baruchel S, Roberts T, Voss SD, Wu B, Ahern CH, Ingle AM, Harris P, Weigel BJ, Blaney SM. Phase I pharmacokinetic and pharmacodynamic study of pazopanib in children with soft tissue sarcoma and other refractory solid tumors: a children's oncology group phase I consortium report. J Clin Oncol. 2013;31(24):3034–43.CrossRefPubMedPubMedCentral Glade Bender JL, Lee A, Reid JM, Baruchel S, Roberts T, Voss SD, Wu B, Ahern CH, Ingle AM, Harris P, Weigel BJ, Blaney SM. Phase I pharmacokinetic and pharmacodynamic study of pazopanib in children with soft tissue sarcoma and other refractory solid tumors: a children's oncology group phase I consortium report. J Clin Oncol. 2013;31(24):3034–43.CrossRefPubMedPubMedCentral
10.
go back to reference Giatromanolaki A, Koukourakis MI, Theodossiou D, Barbatis K, O'Byrne K, Harris AL, Gatter KC. Comparative evaluation of angiogenesis assessment with anti-factor-VIII and anti-CD31 immunostaining in non-small cell lung cancer. Clin Cancer Res. 1997;3(12 Pt 1):2485–92.PubMed Giatromanolaki A, Koukourakis MI, Theodossiou D, Barbatis K, O'Byrne K, Harris AL, Gatter KC. Comparative evaluation of angiogenesis assessment with anti-factor-VIII and anti-CD31 immunostaining in non-small cell lung cancer. Clin Cancer Res. 1997;3(12 Pt 1):2485–92.PubMed
11.
go back to reference Weidner N. Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat. 1995;36(2):169–80. ReviewCrossRefPubMed Weidner N. Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat. 1995;36(2):169–80. ReviewCrossRefPubMed
12.
go back to reference Offersen BV, Pfeiffer P, Hamilton-Dutoit S, Overgaard J. Patterns of angiogenesis in nonsmall-cell lung carcinoma. Cancer. 2001;91(8):1500–9.CrossRefPubMed Offersen BV, Pfeiffer P, Hamilton-Dutoit S, Overgaard J. Patterns of angiogenesis in nonsmall-cell lung carcinoma. Cancer. 2001;91(8):1500–9.CrossRefPubMed
13.
go back to reference Tanaka F, Otake Y, Yanagihara K, Kawano Y, Miyahara R, Li M, Yamada T, Hanaoka N, Inui K, Wada H. Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res. 2001;7(11):3410–5.PubMed Tanaka F, Otake Y, Yanagihara K, Kawano Y, Miyahara R, Li M, Yamada T, Hanaoka N, Inui K, Wada H. Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res. 2001;7(11):3410–5.PubMed
14.
go back to reference de la Taille A, Katz AE, Bagiella E, et al. Microvessel density as a predictor of PSA recurrence after radical prostatectomy. A comparison of CD34 and CD31. Am. J Clin Pathol. 2000;113:555–62.CrossRef de la Taille A, Katz AE, Bagiella E, et al. Microvessel density as a predictor of PSA recurrence after radical prostatectomy. A comparison of CD34 and CD31. Am. J Clin Pathol. 2000;113:555–62.CrossRef
15.
go back to reference Tomisaki S, Ohno S, Ichiyoshi Y, Kuwano H, Machra Y, Sugimachi K. Microvessel quantification and its possible relation with liver metastasis in colorectal cancer. Cancer. 1996;77:1772–8.CrossRef Tomisaki S, Ohno S, Ichiyoshi Y, Kuwano H, Machra Y, Sugimachi K. Microvessel quantification and its possible relation with liver metastasis in colorectal cancer. Cancer. 1996;77:1772–8.CrossRef
16.
go back to reference Behrem S, Zarkovic K, Eskinja N, Jonjic N. Endoglin is a better marker than CD31 in evaluation f angiogenesis in glioblastoma. Croat Med J. 2005;46(3):417–22.PubMed Behrem S, Zarkovic K, Eskinja N, Jonjic N. Endoglin is a better marker than CD31 in evaluation f angiogenesis in glioblastoma. Croat Med J. 2005;46(3):417–22.PubMed
17.
go back to reference Yang LY, Lu WQ, Huang GW, Wang W. Correlation between CD105 expression and postoperative recurrence and metastasis of hepatocellular carcinoma. BMC Cancer. 2006;6:110.CrossRefPubMedPubMedCentral Yang LY, Lu WQ, Huang GW, Wang W. Correlation between CD105 expression and postoperative recurrence and metastasis of hepatocellular carcinoma. BMC Cancer. 2006;6:110.CrossRefPubMedPubMedCentral
18.
go back to reference Li SL, Gao DL, Zhao ZH, et al. Correlation of matrix metalloproteinase suppressor genes RECK, VEGF, and CD105 with angiogenesis and biological behavior in esophageal squamous cell carcinoma. World J Gastroenterol. 2007;13:6076–81.CrossRefPubMedPubMedCentral Li SL, Gao DL, Zhao ZH, et al. Correlation of matrix metalloproteinase suppressor genes RECK, VEGF, and CD105 with angiogenesis and biological behavior in esophageal squamous cell carcinoma. World J Gastroenterol. 2007;13:6076–81.CrossRefPubMedPubMedCentral
19.
go back to reference Miyata Y, Sagara Y, Watanabe S, et al. CD105 is a more appropriate marker for evaluating angiogenesis in urothelial cancer of the upper urinary tract than CD31 or CD34. Virchows Arch. 2013;46:673–9.CrossRef Miyata Y, Sagara Y, Watanabe S, et al. CD105 is a more appropriate marker for evaluating angiogenesis in urothelial cancer of the upper urinary tract than CD31 or CD34. Virchows Arch. 2013;46:673–9.CrossRef
20.
go back to reference Ding S, Li C, Lin S, Yang Y, Liu D, Han Y, Zhang Y, Li L, Zhou L, Kumar S. Comparative evaluation of microvessel density determined by CD34 or CD105 in benign and malignant gastric lesions. Hum Pathol. 2006;37(7):861–6.CrossRefPubMed Ding S, Li C, Lin S, Yang Y, Liu D, Han Y, Zhang Y, Li L, Zhou L, Kumar S. Comparative evaluation of microvessel density determined by CD34 or CD105 in benign and malignant gastric lesions. Hum Pathol. 2006;37(7):861–6.CrossRefPubMed
21.
go back to reference Basilio-de-Oliveira RP, Pannain VL. Prognostic angiogenic markers (endoglin, VEGF, CD31) and tumor cell proliferation (Ki67) for gastrointestinal stromal tumors. World J Gastroenterol. 2015;21(22):6924–30.CrossRefPubMedPubMedCentral Basilio-de-Oliveira RP, Pannain VL. Prognostic angiogenic markers (endoglin, VEGF, CD31) and tumor cell proliferation (Ki67) for gastrointestinal stromal tumors. World J Gastroenterol. 2015;21(22):6924–30.CrossRefPubMedPubMedCentral
22.
go back to reference Cavar S, Jelašic D, Seiwerth S, Miloševic M, Hutinec Z, Mišic M. Endoglin (CD 105) as a potential prognostic factor in neuroblastoma. Pediatr Blood Cancer. 2015;62(5):770–5.CrossRefPubMed Cavar S, Jelašic D, Seiwerth S, Miloševic M, Hutinec Z, Mišic M. Endoglin (CD 105) as a potential prognostic factor in neuroblastoma. Pediatr Blood Cancer. 2015;62(5):770–5.CrossRefPubMed
23.
go back to reference Sugita Y, Takase Y, Mori D, Tokunaga O, Nakashima A, Shigemori M. Endoglin (CD 105) is expressed on endothelial cells in the primary central nervous system lymphomas and correlates with survival. J Neuro-Oncol. 2007;82(3):249–56.CrossRef Sugita Y, Takase Y, Mori D, Tokunaga O, Nakashima A, Shigemori M. Endoglin (CD 105) is expressed on endothelial cells in the primary central nervous system lymphomas and correlates with survival. J Neuro-Oncol. 2007;82(3):249–56.CrossRef
24.
go back to reference Zhou D, Cheng SQ, Ji HF, Wang JS, Xu HT, Zhang GQ, Pang D. Evaluation of protein pigment epithelium-derived factor (PEDF) and microvessel density (MVD) as prognostic indicators in breast cancer. J Cancer Res Clin Oncol. 2010;136(11):1719–27.CrossRefPubMed Zhou D, Cheng SQ, Ji HF, Wang JS, Xu HT, Zhang GQ, Pang D. Evaluation of protein pigment epithelium-derived factor (PEDF) and microvessel density (MVD) as prognostic indicators in breast cancer. J Cancer Res Clin Oncol. 2010;136(11):1719–27.CrossRefPubMed
25.
go back to reference Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science. 1999;284(5419):1534–7.CrossRefPubMed Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science. 1999;284(5419):1534–7.CrossRefPubMed
26.
go back to reference Seon BK, Haba A, Matsuno F, Takahashi N, Tsujie M, She X, Harada N, Uneda S, Tsujie T, Toi H, Tsai H, Haruta Y. Endoglin-targeted cancer therapy. Curr Drug Deliv. 2011;8(1):135–43.CrossRefPubMedPubMedCentral Seon BK, Haba A, Matsuno F, Takahashi N, Tsujie M, She X, Harada N, Uneda S, Tsujie T, Toi H, Tsai H, Haruta Y. Endoglin-targeted cancer therapy. Curr Drug Deliv. 2011;8(1):135–43.CrossRefPubMedPubMedCentral
27.
go back to reference Bockhorn M, Tsuzuki Y, Xu L, Frilling A, Broelsch CE, Fukumura D. Differential vascular and transcriptional responses to anti-vascular endothelial growth factor antibody in orthotopic human pancreatic cancer xenografts. Clin Cancer Res. 2003;9(11):4221–6.PubMed Bockhorn M, Tsuzuki Y, Xu L, Frilling A, Broelsch CE, Fukumura D. Differential vascular and transcriptional responses to anti-vascular endothelial growth factor antibody in orthotopic human pancreatic cancer xenografts. Clin Cancer Res. 2003;9(11):4221–6.PubMed
28.
go back to reference Davis TW, O'Neal JM, Pagel MD, Zweifel BS, Mehta PP, Heuvelman DM, Masferrer JL. Synergy between celecoxib and radiotherapy results from inhibition of cyclooxygenase-2-derived prostaglandin E2, a survival factor for tumor and associated vasculature. Cancer Res. 2004;64(1):279–85.CrossRefPubMed Davis TW, O'Neal JM, Pagel MD, Zweifel BS, Mehta PP, Heuvelman DM, Masferrer JL. Synergy between celecoxib and radiotherapy results from inhibition of cyclooxygenase-2-derived prostaglandin E2, a survival factor for tumor and associated vasculature. Cancer Res. 2004;64(1):279–85.CrossRefPubMed
29.
go back to reference Anderberg C, Cunha SI, Zhai Z, Cortez E, Pardali E, Johnson JR, Franco M, Páez-Ribes M, Cordiner R, Fuxe J, Johansson BR, Goumans MJ, Casanovas O, ten Dijke P, Arthur HM, Pietras K. Deficiency for endoglin in tumor vasculature weakens the endothelial barrier to metastatic dissemination. J Exp Med. 2013;210(3):563–79.CrossRefPubMedPubMedCentral Anderberg C, Cunha SI, Zhai Z, Cortez E, Pardali E, Johnson JR, Franco M, Páez-Ribes M, Cordiner R, Fuxe J, Johansson BR, Goumans MJ, Casanovas O, ten Dijke P, Arthur HM, Pietras K. Deficiency for endoglin in tumor vasculature weakens the endothelial barrier to metastatic dissemination. J Exp Med. 2013;210(3):563–79.CrossRefPubMedPubMedCentral
30.
go back to reference Ciernik IF, Krayenbühl Ciernik BH, Cockerell CJ, Minna JD, Gazdar AF, Carbone DP. Expression of transforming growth factor beta and transforming growth factor beta receptors on AIDS-associated Kaposi's sarcoma. Clin Cancer Res. 1995;1(10):1119–24.PubMed Ciernik IF, Krayenbühl Ciernik BH, Cockerell CJ, Minna JD, Gazdar AF, Carbone DP. Expression of transforming growth factor beta and transforming growth factor beta receptors on AIDS-associated Kaposi's sarcoma. Clin Cancer Res. 1995;1(10):1119–24.PubMed
31.
go back to reference Hara H. Endoglin (CD105) and claudin-5 expression in cutaneous angiosarcoma. Am J Dermatopathol. 2012;34(7):779–82.CrossRefPubMed Hara H. Endoglin (CD105) and claudin-5 expression in cutaneous angiosarcoma. Am J Dermatopathol. 2012;34(7):779–82.CrossRefPubMed
32.
go back to reference Mitsui H, Shibata K, Mano Y, Suzuki S, Umezu T, Mizuno M, Yamamoto E, Kajiyama H, Kotani T, Senga T, Kikkawa F. The expression and characterization of endoglin in uterine leiomyosarcoma. Clin Exp Metastasis. 2013;30(6):731–40.CrossRefPubMed Mitsui H, Shibata K, Mano Y, Suzuki S, Umezu T, Mizuno M, Yamamoto E, Kajiyama H, Kotani T, Senga T, Kikkawa F. The expression and characterization of endoglin in uterine leiomyosarcoma. Clin Exp Metastasis. 2013;30(6):731–40.CrossRefPubMed
33.
go back to reference Boeuf S, Bovée JV, Lehner B, van den Akker B, van Ruler M, Cleton-Jansen AM, Richter W. BMP and TGFbeta pathways in human central chondrosarcoma: enhanced endoglin and Smad 1 signaling in high grade tumors. BMC Cancer. 2012;12:488.CrossRefPubMedPubMedCentral Boeuf S, Bovée JV, Lehner B, van den Akker B, van Ruler M, Cleton-Jansen AM, Richter W. BMP and TGFbeta pathways in human central chondrosarcoma: enhanced endoglin and Smad 1 signaling in high grade tumors. BMC Cancer. 2012;12:488.CrossRefPubMedPubMedCentral
34.
go back to reference Takase Y, Kai K, Masuda M, Akashi M, Tokunaga O. Endoglin (CD105) expression and angiogenesis status in small cell lung cancer. Pathol Res Pract. 2010;206(11):725–30.CrossRefPubMed Takase Y, Kai K, Masuda M, Akashi M, Tokunaga O. Endoglin (CD105) expression and angiogenesis status in small cell lung cancer. Pathol Res Pract. 2010;206(11):725–30.CrossRefPubMed
35.
go back to reference Bauman TM, Huang W, Lee MH, Abel EJ. Neovascularity as a prognostic marker in renal cell carcinoma. Hum Pathol. 2016;57:98–105.CrossRefPubMed Bauman TM, Huang W, Lee MH, Abel EJ. Neovascularity as a prognostic marker in renal cell carcinoma. Hum Pathol. 2016;57:98–105.CrossRefPubMed
36.
go back to reference Tachezy M, Reichelt U, Melenberg T, Gebauer F, Izbicki JR, Kaifi JT. Angiogenesis index CD105 (endoglin)/CD31 (PECAM-1) as a predictive factor for invasion and proliferation in intraductal papillary mucinous neoplasm (IPMN) of the pancreas. Histol Histopathol. 2010;25(10):1239–46.PubMed Tachezy M, Reichelt U, Melenberg T, Gebauer F, Izbicki JR, Kaifi JT. Angiogenesis index CD105 (endoglin)/CD31 (PECAM-1) as a predictive factor for invasion and proliferation in intraductal papillary mucinous neoplasm (IPMN) of the pancreas. Histol Histopathol. 2010;25(10):1239–46.PubMed
37.
go back to reference Malempati S, Hawkins DS. Rhabdomyosarcoma: review of the Children’s oncology group (COG) soft-tissue sarcoma committee experience and rationale for current COG studies. Pediatr Blood Cancer. 2012;59(1):5–10.CrossRefPubMedPubMedCentral Malempati S, Hawkins DS. Rhabdomyosarcoma: review of the Children’s oncology group (COG) soft-tissue sarcoma committee experience and rationale for current COG studies. Pediatr Blood Cancer. 2012;59(1):5–10.CrossRefPubMedPubMedCentral
38.
go back to reference Weidner N. Chapter 14. Measuring intratumoral microvessel density. Methods Enzymol. 2008;444:305–23.CrossRefPubMed Weidner N. Chapter 14. Measuring intratumoral microvessel density. Methods Enzymol. 2008;444:305–23.CrossRefPubMed
39.
go back to reference Miyoshi K, Kohashi K, Fushimi F, Yamamoto H, Kishimoto J, Taguchi T, Iwamoto Y, Oda Y. Close correlation between CXCR4 and VEGF expression and frequent CXCR7 expression in rhabdomyosarcoma. Hum Pathol. 2014;45(9):1900–9.CrossRefPubMed Miyoshi K, Kohashi K, Fushimi F, Yamamoto H, Kishimoto J, Taguchi T, Iwamoto Y, Oda Y. Close correlation between CXCR4 and VEGF expression and frequent CXCR7 expression in rhabdomyosarcoma. Hum Pathol. 2014;45(9):1900–9.CrossRefPubMed
40.
go back to reference Onisto M, Slongo ML, Gregnanin L, Gastaldi T, Carli M, Rosolen A. Expression and activity of vascular endothelial growth factor and metalloproteinases in alveolar and embryonal rhabdomyosarcoma cell lines. Int J Oncol. 2005;27(3):791–8.PubMed Onisto M, Slongo ML, Gregnanin L, Gastaldi T, Carli M, Rosolen A. Expression and activity of vascular endothelial growth factor and metalloproteinases in alveolar and embryonal rhabdomyosarcoma cell lines. Int J Oncol. 2005;27(3):791–8.PubMed
41.
go back to reference Gee MF, Tsuchida R, Eichler-Jonsson C, Das B, Baruchel S, Malkin D. Vascular endothelial growth factor acts in an autocrine manner in rhabdomyosarcoma cell lines and can be inhibited with all-trans-retinoic acid. Oncogene. 2005;24(54):8025–37.CrossRefPubMed Gee MF, Tsuchida R, Eichler-Jonsson C, Das B, Baruchel S, Malkin D. Vascular endothelial growth factor acts in an autocrine manner in rhabdomyosarcoma cell lines and can be inhibited with all-trans-retinoic acid. Oncogene. 2005;24(54):8025–37.CrossRefPubMed
42.
go back to reference Barber TD, Barber MC, Tomescu O, Barr FG, Ruben S, Friedman TB. Identification of target genes regulated by PAX3 and PAX3-FKHR in embryogenesis and alveolar rhabdomyosarcoma. Genomics. 2002;79(3):278–84.CrossRefPubMed Barber TD, Barber MC, Tomescu O, Barr FG, Ruben S, Friedman TB. Identification of target genes regulated by PAX3 and PAX3-FKHR in embryogenesis and alveolar rhabdomyosarcoma. Genomics. 2002;79(3):278–84.CrossRefPubMed
43.
go back to reference Wang W, Slevin M, Kumar S, Kumar P. The cooperative transforming effects of PAX3-FKHR and IGF-II on mouse myoblasts. Int J Oncol. 2005;27(4):1087–96.PubMed Wang W, Slevin M, Kumar S, Kumar P. The cooperative transforming effects of PAX3-FKHR and IGF-II on mouse myoblasts. Int J Oncol. 2005;27(4):1087–96.PubMed
44.
go back to reference Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature. 1989;339:58–61.CrossRefPubMed Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature. 1989;339:58–61.CrossRefPubMed
45.
go back to reference Liu CD, Tilch L, Kwan D, McFadden DW. Vascular endothelial growth factor is increased in ascites from metastatic pancreatic cancer. J Surg Res. 2002;102(1):31–4.CrossRefPubMed Liu CD, Tilch L, Kwan D, McFadden DW. Vascular endothelial growth factor is increased in ascites from metastatic pancreatic cancer. J Surg Res. 2002;102(1):31–4.CrossRefPubMed
46.
go back to reference Poon RT, Fan ST, Wong J. Clinical implications of circulating angiogenic factors in cancer patients. J Clin Oncol. 2001;19:1207–25.CrossRefPubMed Poon RT, Fan ST, Wong J. Clinical implications of circulating angiogenic factors in cancer patients. J Clin Oncol. 2001;19:1207–25.CrossRefPubMed
47.
go back to reference Chisholm JC., Merks JH., Casanova M., Bisogno G., Orbach D., Gentet JC., Thomassin Defachelles AS, Chastagner PB., Lowis S., Ronghe M., McHugh K., van Rijn R., Hilton M., Bachir J., Fürst-Recktenwald S., Geoerger B., Oberlin O.; BERNIE: Open-label, randomized, phase II study of bevacizumab plus chemotherapy in pediatric metastatic rhabdomyosarcoma (RMS) and non-rhabdomyosarcoma soft tissue sarcoma (NRSTS). J Clin Oncol, 2016; 34 (suppl; abstr 11054). Chisholm JC., Merks JH., Casanova M., Bisogno G., Orbach D., Gentet JC., Thomassin Defachelles AS, Chastagner PB., Lowis S., Ronghe M., McHugh K., van Rijn R., Hilton M., Bachir J., Fürst-Recktenwald S., Geoerger B., Oberlin O.; BERNIE: Open-label, randomized, phase II study of bevacizumab plus chemotherapy in pediatric metastatic rhabdomyosarcoma (RMS) and non-rhabdomyosarcoma soft tissue sarcoma (NRSTS). J Clin Oncol, 2016; 34 (suppl; abstr 11054).
48.
go back to reference Mascarenhas L, Meyers WH, Lyden E, Rodeberg DA. Randomized phase II trial of bevacizumab and temsirolimus in combination with vinorelbine (V) and cyclophosphamide (C) for first relapse/disease progression of rhabdomyosarcoma (RMS): a report from the Children’s Oncology Group (COG). J Clin Oncol. 2014; 32: 5s (suppl; abstract 10003). Mascarenhas L, Meyers WH, Lyden E, Rodeberg DA. Randomized phase II trial of bevacizumab and temsirolimus in combination with vinorelbine (V) and cyclophosphamide (C) for first relapse/disease progression of rhabdomyosarcoma (RMS): a report from the Children’s Oncology Group (COG). J Clin Oncol. 2014; 32: 5s (suppl; abstract 10003).
49.
go back to reference Gordon MS, Robert F, Matei D, Mendelson DS, Goldman JW, Chiorean EG, Strother RM, Seon BK, Figg WD, Peer CJ, Alvarez D, Adams BJ, Theuer CP, Rosen LS. An open-label phase Ib dose-escalation study of TRC105 (anti-endoglin antibody) with bevacizumab in patients with advanced cancer. Clin Cancer Res. 2014 Dec 1;20(23):5918–26.CrossRefPubMedPubMedCentral Gordon MS, Robert F, Matei D, Mendelson DS, Goldman JW, Chiorean EG, Strother RM, Seon BK, Figg WD, Peer CJ, Alvarez D, Adams BJ, Theuer CP, Rosen LS. An open-label phase Ib dose-escalation study of TRC105 (anti-endoglin antibody) with bevacizumab in patients with advanced cancer. Clin Cancer Res. 2014 Dec 1;20(23):5918–26.CrossRefPubMedPubMedCentral
50.
go back to reference Attia S, Kumar S, Riedel RF., Robinson SI, Conry RM, McKay Boland P, Barve MA, Fritchie K, Seon BK, Alvarez D, Adams BJ, Shazer RL, Theuer CP, Maki RG. A phase 1B/ phase 2A study of TRC105 (Endoglin Antibody) in combination with pazopanib (P) in patients (pts) with advanced soft tissue sarcoma (STS). J Clin Oncol. 2016;34 (suppl; abstr 11016). Attia S, Kumar S, Riedel RF., Robinson SI, Conry RM, McKay Boland P, Barve MA, Fritchie K, Seon BK, Alvarez D, Adams BJ, Shazer RL, Theuer CP, Maki RG. A phase 1B/ phase 2A study of TRC105 (Endoglin Antibody) in combination with pazopanib (P) in patients (pts) with advanced soft tissue sarcoma (STS). J Clin Oncol. 2016;34 (suppl; abstr 11016).
51.
go back to reference Afshar Moghaddam N, Mahsuni P, Taheri D. Evaluation of Endoglin as an angiogenesis marker in Glioblastoma. Iran J Pathol. 2015 Spring;10(2):89–96.PubMedPubMedCentral Afshar Moghaddam N, Mahsuni P, Taheri D. Evaluation of Endoglin as an angiogenesis marker in Glioblastoma. Iran J Pathol. 2015 Spring;10(2):89–96.PubMedPubMedCentral
52.
go back to reference Barresi V, Cerasoli S, Vitarelli E, Tuccari G. Density of microvessels positive for CD105 (endoglin) is related to prognosis in meningiomas. Acta Neuropathol. 2007;114(2):147–56. Epub 2007 Jun 27CrossRefPubMed Barresi V, Cerasoli S, Vitarelli E, Tuccari G. Density of microvessels positive for CD105 (endoglin) is related to prognosis in meningiomas. Acta Neuropathol. 2007;114(2):147–56. Epub 2007 Jun 27CrossRefPubMed
53.
go back to reference Wexler LH, Meyer WH, Helman LJ. Rhabdomyosarcoma. In: Pizzo PA, Poplack DG, editors. Principles and Practice of Pediatric Oncology, vol. 6. Philadelphia: Wolter Kluwer–Lippincott Williams & Wilkins. 2011. pp. 923–53. Wexler LH, Meyer WH, Helman LJ. Rhabdomyosarcoma. In: Pizzo PA, Poplack DG, editors. Principles and Practice of Pediatric Oncology, vol. 6. Philadelphia: Wolter Kluwer–Lippincott Williams & Wilkins. 2011. pp. 923–53.
54.
go back to reference 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.PubMed 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.PubMed
55.
go back to reference Yao Y, Pan Y, Chen J, Sun X, Qiu Y, Ding Y. Endoglin (CD105) expression in angiogenesis of primary hepatocellular carcinomas: analysis using tissue microarrays and comparisons with CD34 and VEGF. Ann Clin Lab Sci. 2007;37:39–48.PubMed Yao Y, Pan Y, Chen J, Sun X, Qiu Y, Ding Y. Endoglin (CD105) expression in angiogenesis of primary hepatocellular carcinomas: analysis using tissue microarrays and comparisons with CD34 and VEGF. Ann Clin Lab Sci. 2007;37:39–48.PubMed
56.
go back to reference Kuda M, Kohashi K, Yamada Y, Maekawa A, Kinoshita Y, Nakatsura T, Iwamoto Y, Taguchi T, Oda Y. FOXM1 expression in rhabdomyosarcoma: a novel prognostic factor and therapeutic target. Tumour Biol. 2016;37(4):5213–23.CrossRefPubMed Kuda M, Kohashi K, Yamada Y, Maekawa A, Kinoshita Y, Nakatsura T, Iwamoto Y, Taguchi T, Oda Y. FOXM1 expression in rhabdomyosarcoma: a novel prognostic factor and therapeutic target. Tumour Biol. 2016;37(4):5213–23.CrossRefPubMed
58.
go back to reference Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013;49(18):3914–23.CrossRefPubMed Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013;49(18):3914–23.CrossRefPubMed
59.
go back to reference Chen X, Maniotis AJ, Majumdar D, Pe'er J, Folberg R. Uveal melanoma cell staining for CD34 and assessment of tumor vascularity. Invest Ophthalmol Vis Sci. 2002;43(8):2533–9.PubMed Chen X, Maniotis AJ, Majumdar D, Pe'er J, Folberg R. Uveal melanoma cell staining for CD34 and assessment of tumor vascularity. Invest Ophthalmol Vis Sci. 2002;43(8):2533–9.PubMed
60.
go back to reference Chen L, He Y, Sun S, Sun B, Tang X. Vasculogenic mimicry is a major feature and novel predictor of poor prognosis in patients with orbital rhabdomyosarcoma. Oncol Lett. 2015;10(3):1635–41. Epub 2015 Jul 8PubMedPubMedCentral Chen L, He Y, Sun S, Sun B, Tang X. Vasculogenic mimicry is a major feature and novel predictor of poor prognosis in patients with orbital rhabdomyosarcoma. Oncol Lett. 2015;10(3):1635–41. Epub 2015 Jul 8PubMedPubMedCentral
61.
go back to reference Sun B, Zhang S, Zhao X, Zhang W, Hao X. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol. 2004;25(6):1609–14.PubMed Sun B, Zhang S, Zhao X, Zhang W, Hao X. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol. 2004;25(6):1609–14.PubMed
62.
go back to reference Yudoh K, Kanamori M, Ohmori K, Yasuda T, Aoki M, Kimura T. Concentration of vascular endothelial growth factor in the tumour tissue as a prognostic factor of soft tissue sarcomas. Br J Cancer. 2001;84(12):1610–5.CrossRefPubMedPubMedCentral Yudoh K, Kanamori M, Ohmori K, Yasuda T, Aoki M, Kimura T. Concentration of vascular endothelial growth factor in the tumour tissue as a prognostic factor of soft tissue sarcomas. Br J Cancer. 2001;84(12):1610–5.CrossRefPubMedPubMedCentral
63.
go back to reference Chao C, Al-Saleem T, Brooks JJ, Rogatko A, Kraybill WG, Eisenberg B. Vascular endothelial growth factor and soft tissue sarcomas: tumor expression correlates with grade. Ann Surg Oncol. 2001;8(3):260–7.CrossRefPubMed Chao C, Al-Saleem T, Brooks JJ, Rogatko A, Kraybill WG, Eisenberg B. Vascular endothelial growth factor and soft tissue sarcomas: tumor expression correlates with grade. Ann Surg Oncol. 2001;8(3):260–7.CrossRefPubMed
64.
go back to reference West CC, Brown NJ, Mangham DC, Grimer RJ, Reed MW. Microvessel density does not predict outcome in high grade soft tissue sarcoma. Eur J Surg Oncol. 2005;31(10):1198–205.CrossRefPubMed West CC, Brown NJ, Mangham DC, Grimer RJ, Reed MW. Microvessel density does not predict outcome in high grade soft tissue sarcoma. Eur J Surg Oncol. 2005;31(10):1198–205.CrossRefPubMed
Metadata
Title
Evaluation of Endoglin (CD105) expression in pediatric rhabdomyosarcoma
Authors
Virginia Di Paolo
Ida Russo
Renata Boldrini
Lucilla Ravà
Marco Pezzullo
Maria Chiara Benedetti
Angela Galardi
Marta Colletti
Rossella Rota
Domenico Orlando
Alessandro Crocoli
Hector Peinado
Giuseppe Maria Milano
Angela Di Giannatale
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2018
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-017-3947-4

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