Relative expression of hormone receptors by endothelial and smooth muscle cells in proliferative and non-proliferative areas of congenital arteriovenous malformations

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Abstract

Background

Episodic growth due to microvascular proliferations (MVP) has been reported in congenital arteriovenous malformations (AVM), which are normally quiescent lesions composed of mature malformed vessels. Since AVM also may worsen under conditions of hormonal dysregulation, we hypothesized that hormonal influences may stimulate this process of vasoproliferative growth through potential interactions with hormone receptors (HR).

Methods

13 Cases of AVM tissue with histologically documented vasoproliferative growth were analyzed quantitatively for the presence and tissue localization of estrogen receptor (ER), progesterone receptor (PGR), growth hormone receptor (GHR) and follicle-stimulating hormone receptor (FSHR) in relation to resident cells of interest (endothelial cells (EC), smooth muscle cells (SMC) and mast cells (MC)) by applying multiplex immunohistochemistry (IHC) staining. Expression patterns in lesions with MVP and mature vessels were quantified and compared. Available fresh frozen tissues of 3 AVM samples were used to confirm the presence of HR using Reverse-Transcriptase quantitative Polymerase Chain Reaction (RT-qPCR).

Results

All four HR studied were expressed in all cases within EC and SMC in areas of MVP and mature vessels, but not in normal skin tissue. ER, GHR, and FSHR showed more expression in EC of MVP and in SMC of mature vessels. RT-qPCR confirmed presence of all 4 HR in both areas.

Conclusion

Expression of ER, PGR, GHR, and FSHR in vasoproliferative areas of congenital AVM could explain onset of sudden symptomatic growth, as has observed in a subpopulation of patients. These findings may have implications for eventual anti-hormonal targeted therapy in the lesions involved.

Supplementary Information

The online version contains supplementary material available at 10.1186/s40001-023-01436-5.

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Most cited references 51

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Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data

J. M. Ruijter, C. Ramakers, W. M. H. Hoogaars … (2009)

Despite the central role of quantitative PCR (qPCR) in the quantification of mRNA transcripts, most analyses of qPCR data are still delegated to the software that comes with the qPCR apparatus. This is especially true for the handling of the fluorescence baseline. This article shows that baseline estimation errors are directly reflected in the observed PCR efficiency values and are thus propagated exponentially in the estimated starting concentrations as well as ‘fold-difference’ results. Because of the unknown origin and kinetics of the baseline fluorescence, the fluorescence values monitored in the initial cycles of the PCR reaction cannot be used to estimate a useful baseline value. An algorithm that estimates the baseline by reconstructing the log-linear phase downward from the early plateau phase of the PCR reaction was developed and shown to lead to very reproducible PCR efficiency values. PCR efficiency values were determined per sample by fitting a regression line to a subset of data points in the log-linear phase. The variability, as well as the bias, in qPCR results was significantly reduced when the mean of these PCR efficiencies per amplicon was used in the calculation of an estimate of the starting concentration per sample.

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Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.

Christian Ramakers, Jan Ruijter, Ronald Deprez … (2003)

Quantification of mRNAs using real-time polymerase chain reaction (PCR) by monitoring the product formation with the fluorescent dye SYBR Green I is being extensively used in neurosciences, developmental biology, and medical diagnostics. Most PCR data analysis procedures assume that the PCR efficiency for the amplicon of interest is constant or even, in the case of the comparative C(t) method, equal to 2. The latter method already leads to a 4-fold error when the PCR efficiencies vary over just a 0.04 range. PCR efficiencies of amplicons are usually calculated from standard curves based on either known RNA inputs or on dilution series of a reference cDNA sample. In this paper we show that the first approach can lead to PCR efficiencies that vary over a 0.2 range, whereas the second approach may be off by 0.26. Therefore, we propose linear regression on the Log(fluorescence) per cycle number data as an assumption-free method to calculate starting concentrations of mRNAs and PCR efficiencies for each sample. A computer program to perform this calculation is available on request (e-mail: bioinfo@amc.uva.nl; subject: LinRegPCR).

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Hypoxia-induced angiogenesis: good and evil.

Bryan Krock, Nicolas Skuli, M. Celeste Simon (2011)

The vascular network delivers oxygen (O(2)) and nutrients to all cells within the body. It is therefore not surprising that O(2) availability serves as a primary regulator of this complex organ. Most transcriptional responses to low O(2) are mediated by hypoxia-inducible factors (HIFs), highly conserved transcription factors that control the expression of numerous angiogenic, metabolic, and cell cycle genes. Accordingly, the HIF pathway is currently viewed as a master regulator of angiogenesis. HIF modulation could provide therapeutic benefit for a wide array of pathologies, including cancer, ischemic heart disease, peripheral artery disease, wound healing, and neovascular eye diseases. Hypoxia promotes vessel growth by upregulating multiple pro-angiogenic pathways that mediate key aspects of endothelial, stromal, and vascular support cell biology. Interestingly, recent studies show that hypoxia influences additional aspects of angiogenesis, including vessel patterning, maturation, and function. Through extensive research, the integral role of hypoxia and HIF signaling in human disease is becoming increasingly clear. Consequently, a thorough understanding of how hypoxia regulates angiogenesis through an ever-expanding number of pathways in multiple cell types will be essential for the identification of new therapeutic targets and modalities.

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Author and article information

Contributors

A. M. Utami:

ORCID: http://orcid.org/0000-0002-7399-1867

amalia.m.utami@gmail.com

J. B. G. Halfwerk: j.b.halfwerk@amsterdamumc.nl

O. J. de Boer: o.j.deboer@amsterdamumc.nl

C. Mackaaij: c.mackaaij@umcutrecht.nl

D. R. Pabittei: d.pabittei@gmail.com

C. M. A. M. van der Horst: c.m.vanderhorst@amsterdamumc.nl

L. B. Meijer-Jorna: l.b.meijer-jorna@nwz.nl

A. C. van der Wal: a.c.vanderwal@amsterdamumc.nl

Journal

Journal ID (nlm-ta): Eur J Med Res

Journal ID (iso-abbrev): Eur J Med Res

Title: European Journal of Medical Research

Publisher: BioMed Central (London )

ISSN (Print): 0949-2321

ISSN (Electronic): 2047-783X

Publication date (Electronic): 20 October 2023

Publication date PMC-release: 20 October 2023

Publication date Collection: 2023

Volume: 28

Electronic Location Identifier: 449

Affiliations

[1 ]GRID grid.7177.6, ISNI 0000000084992262, Department of Pathology, , Amsterdam University Medical Center-Location AMC, University of Amsterdam, ; Amsterdam, The Netherlands

[2 ]Department of Anatomical Pathology, Faculty of Medicine, Hasanuddin University, ( https://ror.org/00da1gf19) Makassar, Indonesia

[3 ]GRID grid.7177.6, ISNI 0000000084992262, Department of Plastic Surgery, , Amsterdam University Medical Center-Location AMC, University of Amsterdam, ; Amsterdam, The Netherlands

[4 ]Department of Physiology, Faculty of Medicine, Hasanuddin University, ( https://ror.org/00da1gf19) Makassar, Indonesia

[5 ]Symbiant Pathology Expert Center, NWZ- Noordwest Ziekenhuisgroep, ( https://ror.org/00bc64s87) Alkmaar, The Netherlands

[6 ]Department of Anatomy, University Medical Center Utrecht, ( https://ror.org/0575yy874) Utrecht, The Netherlands

Author information

A. M. Utami http://orcid.org/0000-0002-7399-1867

Article

Publisher ID: 1436

DOI: 10.1186/s40001-023-01436-5

PMC ID: 10588228

PubMed ID: 37864259

SO-VID: 0999042c-aa5a-403b-bfa6-671fa3c1e1e7

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 19 October 2022

Date accepted : 7 October 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100014538, Lembaga Pengelola Dana Pendidikan;

Award ID: 20161122049713

Award Recipient : A. M. Utami

Custom metadata

ScienceOpen disciplines: Medicine

Keywords: arteriovenous malformations,hormone receptor,microvascular proliferation,vascular malformations

Data availability:

ScienceOpen disciplines: Medicine

Keywords: arteriovenous malformations, hormone receptor, microvascular proliferation, vascular malformations

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Relative expression of hormone receptors by endothelial and smooth muscle cells in proliferative and non-proliferative areas of congenital arteriovenous malformations

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Supplementary Information

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Journal of Medical Education Research

Most cited references 51

Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data

Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.

Hypoxia-induced angiogenesis: good and evil.

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