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Published in: BMC Endocrine Disorders 1/2019

Open Access 01-12-2019 | Pituitary Adenoma | Research article

Endothelial cell-specific molecule-1 as an invasiveness marker for pituitary null cell adenoma

Authors: Shousen Wang, Zhifeng Wu, Liangfeng Wei, Jianhe Zhang

Published in: BMC Endocrine Disorders | Issue 1/2019

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Abstract

Background

Endothelial cell-specific molecule-1 (ESM-1) is a biomarker associated with tumor progression in pituitary adenoma. We specifically focused on one type of pituitary adenoma, namely null cell adenoma (NCA) and evaluated the relationship between invasion and ESM-1 expression in both vascular endothelial and adenoma tissues.

Methods

Tissue samples from 94 patients with pituitary NCA were obtained through microscopic transsphenoidal resection. Tumor size and invasion were determined through preoperative magnetic resonance imaging. Immunohistochemical staining was performed to detect ESM-1 expression. ESM-1 index of ≥3 was defined as high expression.

Results

Signs of invasion were observed in 46 (47.9%) of the 94 patients. Significant differences were observed in the invasion state and maximum tumor diameter between high and low expression of ESM-1 in vascular endothelial tissues (both P < 0.05). Significant positive associations were noted between ESM-1 expression in vascular endothelial tissues and tumor invasion (P = 0.002) and tumor size (P = 0.020). However, only tumor size was associated with ESM-1 expression in adenoma tissues (P = 0.016).

Conclusion

In NCA, a significant positive association between tumor invasion and ESM-1 expression was observed only in vascular endothelial tissues, suggesting that tumor progression occurs mainly through ESM-1-associated mechanism.
Literature
1.
go back to reference Ho M, Yang E, Matcuk G, Deng D, Sampas N, Tsalenko A, Tabibiazar R, Zhang Y, Chen M, Talbi S, et al. Identification of endothelial cell genes by combined database mining and microarray analysis. Physiol Genomics. 2003;13(3):249–62.CrossRef Ho M, Yang E, Matcuk G, Deng D, Sampas N, Tsalenko A, Tabibiazar R, Zhang Y, Chen M, Talbi S, et al. Identification of endothelial cell genes by combined database mining and microarray analysis. Physiol Genomics. 2003;13(3):249–62.CrossRef
2.
go back to reference Bechard D, Gentina T, Delehedde M, Scherpereel A, Lyon M, Aumercier M, Vazeux R, Richet C, Degand P, Jude B, et al. Endocan is a novel chondroitin sulfate/dermatan sulfate proteoglycan that promotes hepatocyte growth factor/scatter factor mitogenic activity. J Biol Chem. 2001;276(51):48341–9.CrossRef Bechard D, Gentina T, Delehedde M, Scherpereel A, Lyon M, Aumercier M, Vazeux R, Richet C, Degand P, Jude B, et al. Endocan is a novel chondroitin sulfate/dermatan sulfate proteoglycan that promotes hepatocyte growth factor/scatter factor mitogenic activity. J Biol Chem. 2001;276(51):48341–9.CrossRef
3.
go back to reference Maurage CA, Adam E, Mineo JF, Sarrazin S, Debunne M, Siminski RM, Baroncini M, Lassalle P, Blond S, Delehedde M. Endocan expression and localization in human glioblastomas. J Neuropathol Exp Neurol. 2009;68(6):633–41.CrossRef Maurage CA, Adam E, Mineo JF, Sarrazin S, Debunne M, Siminski RM, Baroncini M, Lassalle P, Blond S, Delehedde M. Endocan expression and localization in human glioblastomas. J Neuropathol Exp Neurol. 2009;68(6):633–41.CrossRef
4.
go back to reference Rennel E, Mellberg S, Dimberg A, Petersson L, Botling J, Ameur A, Westholm JO, Komorowski J, Lassalle P, Cross MJ, et al. Endocan is a VEGF-A and PI3K regulated gene with increased expression in human renal cancer. Exp Cell Res. 2007;313(7):1285–94.CrossRef Rennel E, Mellberg S, Dimberg A, Petersson L, Botling J, Ameur A, Westholm JO, Komorowski J, Lassalle P, Cross MJ, et al. Endocan is a VEGF-A and PI3K regulated gene with increased expression in human renal cancer. Exp Cell Res. 2007;313(7):1285–94.CrossRef
5.
go back to reference Roudnicky F, Poyet C, Wild P, Krampitz S, Negrini F, Huggenberger R, Rogler A, Stohr R, Hartmann A, Provenzano M, et al. Endocan is upregulated on tumor vessels in invasive bladder cancer where it mediates VEGF-A-induced angiogenesis. Cancer Res. 2013;73(3):1097–106.CrossRef Roudnicky F, Poyet C, Wild P, Krampitz S, Negrini F, Huggenberger R, Rogler A, Stohr R, Hartmann A, Provenzano M, et al. Endocan is upregulated on tumor vessels in invasive bladder cancer where it mediates VEGF-A-induced angiogenesis. Cancer Res. 2013;73(3):1097–106.CrossRef
6.
go back to reference Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–6.CrossRef Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–6.CrossRef
7.
go back to reference Grigoriu BD, Depontieu F, Scherpereel A, Gourcerol D, Devos P, Ouatas T, Lafitte JJ, Copin MC, Tonnel AB, Lassalle P. Endocan expression and relationship with survival in human non-small cell lung cancer. Clin Cancer Res. 2006;12(15):4575–82.CrossRef Grigoriu BD, Depontieu F, Scherpereel A, Gourcerol D, Devos P, Ouatas T, Lafitte JJ, Copin MC, Tonnel AB, Lassalle P. Endocan expression and relationship with survival in human non-small cell lung cancer. Clin Cancer Res. 2006;12(15):4575–82.CrossRef
8.
go back to reference Chen LY, Liu X, Wang SL, Qin CY. Over-expression of the Endocan gene in endothelial cells from hepatocellular carcinoma is associated with angiogenesis and tumour invasion. J Int Med Res. 2010;38(2):498–510.CrossRef Chen LY, Liu X, Wang SL, Qin CY. Over-expression of the Endocan gene in endothelial cells from hepatocellular carcinoma is associated with angiogenesis and tumour invasion. J Int Med Res. 2010;38(2):498–510.CrossRef
9.
go back to reference Huang GW, Tao YM, Ding X. Endocan expression correlated with poor survival in human hepatocellular carcinoma. Dig Dis Sci. 2009;54(2):389–94.CrossRef Huang GW, Tao YM, Ding X. Endocan expression correlated with poor survival in human hepatocellular carcinoma. Dig Dis Sci. 2009;54(2):389–94.CrossRef
10.
go back to reference Leroy X, Aubert S, Zini L, Franquet H, Kervoaze G, Villers A, Delehedde M, Copin MC, Lassalle P. Vascular endocan (ESM-1) is markedly overexpressed in clear cell renal cell carcinoma. Histopathology. 2010;56(2):180–7.CrossRef Leroy X, Aubert S, Zini L, Franquet H, Kervoaze G, Villers A, Delehedde M, Copin MC, Lassalle P. Vascular endocan (ESM-1) is markedly overexpressed in clear cell renal cell carcinoma. Histopathology. 2010;56(2):180–7.CrossRef
11.
go back to reference Liu N, Zhang LH, Du H, Hu Y, Zhang GG, Wang XH, Li JY, Ji JF. Overexpression of endothelial cell specific molecule-1 (ESM-1) in gastric cancer. Ann Surg Oncol. 2010;17(10):2628–39.CrossRef Liu N, Zhang LH, Du H, Hu Y, Zhang GG, Wang XH, Li JY, Ji JF. Overexpression of endothelial cell specific molecule-1 (ESM-1) in gastric cancer. Ann Surg Oncol. 2010;17(10):2628–39.CrossRef
12.
go back to reference Niveiro M, Aranda FI, Peiro G, Alenda C, Pico A. Immunohistochemical analysis of tumor angiogenic factors in human pituitary adenomas. Hum Pathol. 2005;36(10):1090–5.CrossRef Niveiro M, Aranda FI, Peiro G, Alenda C, Pico A. Immunohistochemical analysis of tumor angiogenic factors in human pituitary adenomas. Hum Pathol. 2005;36(10):1090–5.CrossRef
13.
go back to reference Sanchez-Ortiga R, Sanchez-Tejada L, Moreno-Perez O, Riesgo P, Niveiro M, Pico Alfonso AM. Over-expression of vascular endothelial growth factor in pituitary adenomas is associated with extrasellar growth and recurrence. Pituitary. 2013;16(3):370–7.CrossRef Sanchez-Ortiga R, Sanchez-Tejada L, Moreno-Perez O, Riesgo P, Niveiro M, Pico Alfonso AM. Over-expression of vascular endothelial growth factor in pituitary adenomas is associated with extrasellar growth and recurrence. Pituitary. 2013;16(3):370–7.CrossRef
14.
go back to reference Miao Y, Zong M, Jiang T, Yuan X, Guan S, Wang Y, Zhou D. A comparative analysis of ESM-1 and vascular endothelial cell marker (CD34/CD105) expression on pituitary adenoma invasion. Pituitary. 2016;19(2):194–201.CrossRef Miao Y, Zong M, Jiang T, Yuan X, Guan S, Wang Y, Zhou D. A comparative analysis of ESM-1 and vascular endothelial cell marker (CD34/CD105) expression on pituitary adenoma invasion. Pituitary. 2016;19(2):194–201.CrossRef
15.
go back to reference Di Ieva A, Weckman A, Di Michele J, Rotondo F, Grizzi F, Kovacs K, Cusimano MD. Microvascular morphometrics of the hypophysis and pituitary tumors: from bench to operating theatre. Microvasc Res. 2013;89:7–14.CrossRef Di Ieva A, Weckman A, Di Michele J, Rotondo F, Grizzi F, Kovacs K, Cusimano MD. Microvascular morphometrics of the hypophysis and pituitary tumors: from bench to operating theatre. Microvasc Res. 2013;89:7–14.CrossRef
16.
go back to reference Lloyd RV, Vidal S, Horvath E, Kovacs K, Scheithauer B. Angiogenesis in normal and neoplastic pituitary tissues. Microsc Res Tech. 2003;60(2):244–50.CrossRef Lloyd RV, Vidal S, Horvath E, Kovacs K, Scheithauer B. Angiogenesis in normal and neoplastic pituitary tissues. Microsc Res Tech. 2003;60(2):244–50.CrossRef
17.
go back to reference Turner HE, Nagy Z, Gatter KC, Esiri MM, Harris AL, Wass JA. Angiogenesis in pituitary adenomas and the normal pituitary gland. J Clin Endocrinol Metab. 2000;85(3):1159–62.CrossRef Turner HE, Nagy Z, Gatter KC, Esiri MM, Harris AL, Wass JA. Angiogenesis in pituitary adenomas and the normal pituitary gland. J Clin Endocrinol Metab. 2000;85(3):1159–62.CrossRef
18.
go back to reference Cornelius A, Cortet-Rudelli C, Assaker R, Kerdraon O, Gevaert MH, Prevot V, Lassalle P, Trouillas J, Delehedde M, Maurage CA. Endothelial expression of endocan is strongly associated with tumor progression in pituitary adenoma. Brain Pathol (Zurich, Switzerland). 2012;22(6):757–64.CrossRef Cornelius A, Cortet-Rudelli C, Assaker R, Kerdraon O, Gevaert MH, Prevot V, Lassalle P, Trouillas J, Delehedde M, Maurage CA. Endothelial expression of endocan is strongly associated with tumor progression in pituitary adenoma. Brain Pathol (Zurich, Switzerland). 2012;22(6):757–64.CrossRef
19.
go back to reference Matano F, Yoshida D, Ishii Y, Tahara S, Teramoto A, Morita A. Endocan, a new invasion and angiogenesis marker of pituitary adenomas. J Neurooncol. 2014;117(3):485–91.CrossRef Matano F, Yoshida D, Ishii Y, Tahara S, Teramoto A, Morita A. Endocan, a new invasion and angiogenesis marker of pituitary adenomas. J Neurooncol. 2014;117(3):485–91.CrossRef
20.
go back to reference Delellis RA, Lloyd RV, Heitz PU, Eng C. World Health Organization classification of tumours: Tumours of endocrine organs. Lyons: IARC; 2004. Delellis RA, Lloyd RV, Heitz PU, Eng C. World Health Organization classification of tumours: Tumours of endocrine organs. Lyons: IARC; 2004.
21.
go back to reference Knosp E, Steiner E, Kitz K, Matula C. Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery. 1993;33(4):610–7 discussion 617-618. Knosp E, Steiner E, Kitz K, Matula C. Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery. 1993;33(4):610–7 discussion 617-618.
22.
go back to reference Wilson CB. A decade of pituitary microsurgery. The Herbert Olivecrona lecture. J Neurosurg. 1984;61(5):814–33.CrossRef Wilson CB. A decade of pituitary microsurgery. The Herbert Olivecrona lecture. J Neurosurg. 1984;61(5):814–33.CrossRef
23.
go back to reference Asa SL, Kovacs K. Clinically non-functioning human pituitary adenomas. Can J Neurol Sci. 1992;19(2):228–35.CrossRef Asa SL, Kovacs K. Clinically non-functioning human pituitary adenomas. Can J Neurol Sci. 1992;19(2):228–35.CrossRef
24.
go back to reference Moreno CS, Evans CO, Zhan X, Okor M, Desiderio DM, Oyesiku NM. Novel molecular signaling and classification of human clinically nonfunctional pituitary adenomas identified by gene expression profiling and proteomic analyses. Cancer Res. 2005;65(22):10214–22.CrossRef Moreno CS, Evans CO, Zhan X, Okor M, Desiderio DM, Oyesiku NM. Novel molecular signaling and classification of human clinically nonfunctional pituitary adenomas identified by gene expression profiling and proteomic analyses. Cancer Res. 2005;65(22):10214–22.CrossRef
25.
go back to reference Lopes MBS. The 2017 World Health Organization classification of tumors of the pituitary gland: a summary. Acta Neuropathol. 2017;134(4):521–35.CrossRef Lopes MBS. The 2017 World Health Organization classification of tumors of the pituitary gland: a summary. Acta Neuropathol. 2017;134(4):521–35.CrossRef
26.
go back to reference Thapar K, Kovacs K, Scheithauer BW, Stefaneanu L, Horvath E, Pernicone PJ, Murray D, Laws ER Jr. Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody. Neurosurgery. 1996;38(1):99–106; discussion 106-107.CrossRef Thapar K, Kovacs K, Scheithauer BW, Stefaneanu L, Horvath E, Pernicone PJ, Murray D, Laws ER Jr. Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody. Neurosurgery. 1996;38(1):99–106; discussion 106-107.CrossRef
27.
go back to reference Scheithauer BW, Kovacs KT, Laws ER Jr, Randall RV. Pathology of invasive pituitary tumors with special reference to functional classification. J Neurosurg. 1986;65(6):733–44.CrossRef Scheithauer BW, Kovacs KT, Laws ER Jr, Randall RV. Pathology of invasive pituitary tumors with special reference to functional classification. J Neurosurg. 1986;65(6):733–44.CrossRef
28.
go back to reference Losa M, Mortini P, Barzaghi R, Ribotto P, Terreni MR, Marzoli SB, Pieralli S, Giovanelli M. Early results of surgery in patients with nonfunctioning pituitary adenoma and analysis of the risk of tumor recurrence. J Neurosurg. 2008;108(3):525–32.CrossRef Losa M, Mortini P, Barzaghi R, Ribotto P, Terreni MR, Marzoli SB, Pieralli S, Giovanelli M. Early results of surgery in patients with nonfunctioning pituitary adenoma and analysis of the risk of tumor recurrence. J Neurosurg. 2008;108(3):525–32.CrossRef
29.
go back to reference Berkmann S, Schlaffer S, Buchfelder M. Tumor shrinkage after transsphenoidal surgery for nonfunctioning pituitary adenoma. J Neurosurg. 2013;119(6):1447–52.CrossRef Berkmann S, Schlaffer S, Buchfelder M. Tumor shrinkage after transsphenoidal surgery for nonfunctioning pituitary adenoma. J Neurosurg. 2013;119(6):1447–52.CrossRef
30.
go back to reference Ito M, Kuge A, Matsuda KI, Sato S, Kayama T, Sonoda Y. The likelihood of remnant nonfunctioning pituitary adenomas shrinking is associated with the Lesion's blood supply pattern. World Neurosurg. 2017;107:137–41.CrossRef Ito M, Kuge A, Matsuda KI, Sato S, Kayama T, Sonoda Y. The likelihood of remnant nonfunctioning pituitary adenomas shrinking is associated with the Lesion's blood supply pattern. World Neurosurg. 2017;107:137–41.CrossRef
31.
go back to reference Dekkers OM, Biermasz NR, Pereira AM, Romijn JA, Vandenbroucke JP. Mortality in acromegaly: a metaanalysis. J Clin Endocrinol Metab. 2008;93(1):61–7.CrossRef Dekkers OM, Biermasz NR, Pereira AM, Romijn JA, Vandenbroucke JP. Mortality in acromegaly: a metaanalysis. J Clin Endocrinol Metab. 2008;93(1):61–7.CrossRef
32.
go back to reference Thapar K, Yamada Y, Scheithauer B, Kovacs K, Yamada S, Stefaneanu L. Assessment of mitotic activity in pituitary adenomas and carcinomas. Endocr Pathol. 1996;7(3):215–21.CrossRef Thapar K, Yamada Y, Scheithauer B, Kovacs K, Yamada S, Stefaneanu L. Assessment of mitotic activity in pituitary adenomas and carcinomas. Endocr Pathol. 1996;7(3):215–21.CrossRef
Metadata
Title
Endothelial cell-specific molecule-1 as an invasiveness marker for pituitary null cell adenoma
Authors
Shousen Wang
Zhifeng Wu
Liangfeng Wei
Jianhe Zhang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2019
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-019-0418-8

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