{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,16]],"date-time":"2026-01-16T09:27:48Z","timestamp":1768555668503,"version":"3.49.0"},"reference-count":36,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Polish Ministry of Science and Higher Education","award":["BST-162"],"award-info":[{"award-number":["BST-162"]}]},{"name":"Medical University of Bialystok","award":["BST-162"],"award-info":[{"award-number":["BST-162"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Brain glioma is one of the most common malignant tumors of brain tissue. It is characterized by rich vascularization, which indicates the significant participation of angiogenesis in its growth and development. In its first stages, the disease is very often asymptomatic, and late diagnosis significantly limits possibilities of treatment. Tumor angiogenesis, i.e., the formation of new vessels, requires the presence of angiogenic compounds that will enable tumor progression by creating a path for the supply of nutrients. The proangiogenic compounds involved in the development of glioma include hypoxia-inducible factor 1\u03b1 (HIF-1\u03b1), angiopoietin-2 (ANG-2), and interleukin-1\u03b2 (IL-1\u03b2). The aim of this study was to analyze changes in the levels of these proteins in plasma samples of patients diagnosed with brain glioma in stages G1 to G4, and in a control group, using SPRi biosensors. The results obtained in plasma were compared with the concentrations obtained during the analysis of tissue homogenates from patients with glioma in stages G2 to G4. A statistically significant difference in plasma concentrations was obtained between the patient group and the control group. The concentrations of the markers in tissue homogenate samples were statistically higher than in blood plasma. There was no significant effect of gender, diet, smoking, or the patient\u2019s general health condition (Karnofsky score) on the course of the disease. These factors do not directly increase the risk of developing brain glioma.<\/jats:p>","DOI":"10.3390\/ijms26104802","type":"journal-article","created":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T07:34:03Z","timestamp":1747640043000},"page":"4802","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["A Study on the Levels of Selected Proangiogenic Proteins in Human Tissues and Plasma in Relation to Brain Glioma"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8515-9840","authenticated-orcid":false,"given":"Zuzanna","family":"Zielinska","sequence":"first","affiliation":[{"name":"Doctoral School, Department of Physical Chemistry, Faculty of Chemistry, University of Bialystok, Ciolkowskiego 1K, 15-245 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julia","family":"Gie\u0142a\u017cyn","sequence":"additional","affiliation":[{"name":"Higher School of Social Psychology, SWPS University, 03-815 Warsaw, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5139-2321","authenticated-orcid":false,"given":"Zofia","family":"Dzieciol-Anikiej","sequence":"additional","affiliation":[{"name":"Biobank, Medical University of Bialystok, Waszyngtona 13, 15-269 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Janusz","family":"Dzieciol","sequence":"additional","affiliation":[{"name":"Biobank, Medical University of Bialystok, Waszyngtona 13, 15-269 Bialystok, Poland"},{"name":"Department of Medical Pathology, Medical University of Bialystok, Waszyngtona 13, 15-269 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9788-6957","authenticated-orcid":false,"given":"Piotr","family":"Mrozek","sequence":"additional","affiliation":[{"name":"Faculty of Mechanical Engineering, Bialystok University of Technology, Wiejska 45 C, 15-351 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanna","family":"Reszec-Gielazyn","sequence":"additional","affiliation":[{"name":"Biobank, Medical University of Bialystok, Waszyngtona 13, 15-269 Bialystok, Poland"},{"name":"Department of Medical Pathology, Medical University of Bialystok, Waszyngtona 13, 15-269 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ewa","family":"Gorodkiewicz","sequence":"additional","affiliation":[{"name":"Department of Physical Chemistry, Faculty of Chemistry, University of Bialystok, Ciolkowskiego 1K, 15-245 Bialystok, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e000069","DOI":"10.1136\/bmjno-2020-000069","article-title":"Potential biomarkers and challenges in glioma diagnosis, therapy and prognosis","volume":"2","author":"Kan","year":"2020","journal-title":"BMJ Neurol. Open"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Papadimitrakis, D., Perdikakis, M., Gargalionis, A.N., and Papavassiliou, A.G. (2024). Biomarkers in Cerebrospinal Fluid for the Diagnosis and Monitoring of Gliomas. Biomolecules, 14.","DOI":"10.3390\/biom14070801"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2461","DOI":"10.1007\/s12035-020-01892-8","article-title":"Tumor Development and Angiogenesis in Adult Brain Tumor: Glioblastoma","volume":"57","author":"Ahir","year":"2020","journal-title":"Mol. Neurobiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3109\/07357907.2011.630050","article-title":"Deregulated signaling pathways in glioblastoma multiforme: Molecular mechanisms and therapeutic targets","volume":"30","author":"Mao","year":"2012","journal-title":"Cancer Investig."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Sareen, H., Ma, Y., Becker, T.M., Roberts, T.L., de Souza, P., and Powter, B. (2022). Molecular Biomarkers in Glioblastoma: A Systematic Review and Meta-Analysis. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23168835"},{"key":"ref_6","unstructured":"US Department of Health and Human Services, National Institutes of Health, National Cancer Institute, and USA.gov (2025, April 08). Oligodendroglioma and Other IDH-Mutated Tumors: Diagnosis and Treatment, Available online: https:\/\/www.cancer.gov\/rare-brain-spine-tumor\/tumors\/oligodendroglioma."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"254","DOI":"10.18388\/pb.2021_495","article-title":"Genetyczne i molekularne pod\u0142o\u017ca rozwoju glejaka","volume":"69","author":"Panek","year":"2023","journal-title":"Post\u0119py Biochem."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1038\/nrd3455","article-title":"Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases","volume":"10","author":"Carmeliet","year":"2011","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.gde.2010.10.008","article-title":"Vessel abnormalization: Another hallmark of cancer? Molecular mechanisms and therapeutic implications","volume":"21","author":"Cauwenberghs","year":"2011","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1080\/07357907.2017.1364745","article-title":"Realizing the Potential of Vascular Targeted Therapy: The Rationale for Combining Vascular Disrupting Agents and Anti-Angiogenic Agents to Treat Cancer","volume":"35","author":"Siemann","year":"2017","journal-title":"Cancer Investig."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"176277","DOI":"10.1016\/j.ejphar.2023.176277","article-title":"Hypoxia-inducible factor-1: Regulatory mechanisms and drug therapy in myocardial infarction","volume":"963","author":"Pan","year":"2024","journal-title":"Eur. J. Pharmacol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1016\/j.tem.2017.02.009","article-title":"Role of AHR and HIF-1\u03b1 in Glioblastoma Metabolism","volume":"28","author":"Gabriely","year":"2017","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1378\/chest.06-2915","article-title":"Serum angiopoietin-2 as a clinical marker for lung cancer","volume":"132","author":"Park","year":"2007","journal-title":"Chest"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.canlet.2012.08.018","article-title":"Angiopoietins in angiogenesis","volume":"328","author":"Fagiani","year":"2013","journal-title":"Cancer Lett."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e1020","DOI":"10.1038\/cddis.2013.562","article-title":"Interleukin-1\u03b2 promotes hypoxia-induced apoptosis of glioblastoma cells by inhibiting hypoxia-inducible factor-1 mediated adrenomedullin production","volume":"5","author":"Sun","year":"2014","journal-title":"Cell Death Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3500","DOI":"10.4049\/jimmunol.1202769","article-title":"The Role of IL-1 in the Early Tumor Cell-Induced Angiogenic Response","volume":"190","author":"Carmi","year":"2013","journal-title":"J. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1039\/D1NR05400G","article-title":"Research advances on surface plasmon resonance biosensors","volume":"14","author":"Wang","year":"2022","journal-title":"Nanoscale"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1080\/10408347.2014.881250","article-title":"Surface Plasmon Resonance (SPR) Biosensors in Pharmaceutical Analysis","volume":"45","author":"Olaru","year":"2015","journal-title":"Crit. Rev. Anal. Chem."},{"key":"ref_19","first-page":"1478","article-title":"A suspected case of the electrical resonance of minute metal particles for light-waves. A new type of absorption","volume":"18","author":"Wood","year":"1902","journal-title":"Proc. Phys. Soc. Lond."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.cossms.2011.05.001","article-title":"Surface Plasmon Resonance Based Biosensors: From the Development of Different SPR Structures to Novel Surface Functionalization Strategies","volume":"15","author":"Wijaya","year":"2011","journal-title":"Curr. Opin. Solid State Mater. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Schasfoort, R.B.M. (2017). Handbook of Surface Plasmon Resonance, Royal Society of Chemistry. [2nd ed.].","DOI":"10.1039\/9781788010283"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Xu, J., Zhang, P., and Chen, Y. (2024). Surface Plasmon Resonance Biosensors: A Review of Molecular Imaging with High Spatial Resolution. Biosensors, 14.","DOI":"10.3390\/bios14020084"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1380","DOI":"10.1016\/j.bios.2010.07.056","article-title":"Surface plasmon resonance imaging (SPRi)-based sensing: A new approach in signal sampling and management","volume":"26","author":"Scarano","year":"2010","journal-title":"Biosens. Bioelectron."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"5966","DOI":"10.1021\/ja400951g","article-title":"Real-time evaluation of binding mechanisms in multivalent interactions: A surface plasmon resonance kinetic approach","volume":"135","author":"Munoz","year":"2013","journal-title":"J. Am. Chem. Soc."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.burns.2017.12.001","article-title":"Matrix metalloproteinase-2 and its correlation with basal membrane components laminin-5 and collagen type IV in paediatric burn patients measured with Surface Plasmon Resonance Imaging (SPRI) biosensors","volume":"44","author":"Weremijewicz","year":"2018","journal-title":"Burns"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Toliczenko-Bernatowicz, D., Matuszczak, E., Tylicka, M., Szyma\u0144ska, B., Komarowska, M., Gorodkiewicz, E., Debek, W., and Hermanowicz, A. (2018). Overexpression of ubiquitin carboxyl-terminal hydrolase 1 (UCHL1) in boys with cryptorchidism. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0191806"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Oldak, L., Le\u015bniewska, A., Zelazowska-Rutkowska, B., Latoch, E., Lukaszewski, Z., Krawczuk-Rybak, M., and Gorodkiewicz, E. (2022). An Array SPRi Biosensor for Simultaneous VEGF-A and FGF-2 Determination in Biological Samples. Appl. Sci., 12.","DOI":"10.3390\/app122412699"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.nurt.2009.04.001","article-title":"Biology of angiogenesis and invasion in glioma","volume":"6","author":"Tate","year":"2009","journal-title":"Neurotherapeutics"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"657","DOI":"10.3109\/00207454.2013.789874","article-title":"The expression of hypoxia-inducible factor-1 in primary brain tumors","volume":"123","author":"Reszec","year":"2013","journal-title":"Int. J. Neurosci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/j.1750-3639.2005.tb00116.x","article-title":"The Role of Angiopoietins During Angiogenesis in Gliomas","volume":"15","author":"Reiss","year":"2006","journal-title":"Brain Pathol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Tarassishin, L., Casper, D., and Lee, S.C. (2014). Aberrant Expression of Interleukin-1\u03b2 and Inflammasome Activation in Human Malignant Gliomas. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0103432"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5200","DOI":"10.4103\/jfmpc.jfmpc_640_19","article-title":"Effect of lifestyle and dietary factors in the development of brain tumors","volume":"9","author":"Bansal","year":"2020","journal-title":"J. Fam. Med. Prim. Care"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.autrev.2017.11.010","article-title":"Physical activity and autoimmune diseases: Get moving and manage the disease","volume":"17","author":"Sharif","year":"2018","journal-title":"Autoimmun. Rev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/s11060-005-9103-z","article-title":"Inhibition of hypoxia inducible factor-1\u03b1 (HIF-1\u03b1) decreases vascular endothelial growth factor (VEGF) secretion and tumor growth in malignant gliomas","volume":"78","author":"Jensen","year":"2006","journal-title":"J. Neurooncol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Saponaro, C., Malfettone, A., Ranieri, G., Danza, K., Simone, G., Paradiso, A., and Mangia, A. (2013). VEGF, HIF-1\u03b1 expression and MVD as an angiogenic network in familial breast cancer. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0053070"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Zielinska, Z., Oldak, L., Guszcz, T., Hermanowicz, A., and Gorodkiewicz, E. (2024). SPRi Biosensor for Simultaneous Determination of HIF-1\u03b1, Angiopoietin-2, and Interleukin-1\u03b2 in Blood Plasma. Sensors, 24.","DOI":"10.3390\/s24175481"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4802\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:34:17Z","timestamp":1760031257000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4802"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,16]]},"references-count":36,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ijms26104802"],"URL":"https:\/\/doi.org\/10.3390\/ijms26104802","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,16]]}}}