Skip to main content
Top
Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Glioblastoma | Research

Glycosylation spectral signatures for glioma grade discrimination using Raman spectroscopy

Authors: Agathe Quesnel, Nathan Coles, Claudio Angione, Priyanka Dey, Tuomo M. Polvikoski, Tiago F. Outeiro, Meez Islam, Ahmad A. Khundakar, Panagiota S. Filippou

Published in: BMC Cancer | Issue 1/2023

Login to get access

Abstract

Background

Gliomas are the most common brain tumours with the high-grade glioblastoma representing the most aggressive and lethal form. Currently, there is a lack of specific glioma biomarkers that would aid tumour subtyping and minimally invasive early diagnosis. Aberrant glycosylation is an important post-translational modification in cancer and is implicated in glioma progression. Raman spectroscopy (RS), a vibrational spectroscopic label-free technique, has already shown promise in cancer diagnostics.

Methods

RS was combined with machine learning to discriminate glioma grades. Raman spectral signatures of glycosylation patterns were used in serum samples and fixed tissue biopsy samples, as well as in single cells and spheroids.

Results

Glioma grades in fixed tissue patient samples and serum were discriminated with high accuracy. Discrimination between higher malignant glioma grades (III and IV) was achieved with high accuracy in tissue, serum, and cellular models using single cells and spheroids. Biomolecular changes were assigned to alterations in glycosylation corroborated by analysing glycan standards and other changes such as carotenoid antioxidant content.

Conclusion

RS combined with machine learning could pave the way for more objective and less invasive grading of glioma patients, serving as a useful tool to facilitate glioma diagnosis and delineate biomolecular glioma progression changes.
Appendix
Available only for authorised users
Literature
2.
go back to reference Davis ME, Glioblastoma. Overview of Disease and Treatment. Clin J Oncol Nurs. 2016;20(5 Suppl):2–8.CrossRef Davis ME, Glioblastoma. Overview of Disease and Treatment. Clin J Oncol Nurs. 2016;20(5 Suppl):2–8.CrossRef
3.
go back to reference Wesseling P, Capper D. WHO 2016 classification of gliomas. Neuropathol Appl Neurobiol. 2018;44(2):139–50.PubMedCrossRef Wesseling P, Capper D. WHO 2016 classification of gliomas. Neuropathol Appl Neurobiol. 2018;44(2):139–50.PubMedCrossRef
4.
go back to reference Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, et al. The 2021 WHO classification of tumors of the Central Nervous System: a summary. Neurooncology. 2021;23(8):1231–51. Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, et al. The 2021 WHO classification of tumors of the Central Nervous System: a summary. Neurooncology. 2021;23(8):1231–51.
6.
go back to reference Wood MD, Halfpenny AM, Moore SR. Applications of molecular neuro-oncology - a review of diffuse glioma integrated diagnosis and emerging molecular entities. Diagn Pathol. 2019;14(1):29.PubMedPubMedCentralCrossRef Wood MD, Halfpenny AM, Moore SR. Applications of molecular neuro-oncology - a review of diffuse glioma integrated diagnosis and emerging molecular entities. Diagn Pathol. 2019;14(1):29.PubMedPubMedCentralCrossRef
7.
go back to reference D’Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of Resection in Glioma-A Review of the cutting edge. World Neurosurg. 2017;103:538–49.PubMedCrossRef D’Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of Resection in Glioma-A Review of the cutting edge. World Neurosurg. 2017;103:538–49.PubMedCrossRef
8.
go back to reference Mamede AP, Santos IP, Batista de Carvalho ALM, Figueiredo P, Silva MC, Tavares MV, et al. A New look into Cancer-A Review on the contribution of vibrational spectroscopy on early diagnosis and surgery Guidance. Cancers (Basel). 2021;13:21.CrossRef Mamede AP, Santos IP, Batista de Carvalho ALM, Figueiredo P, Silva MC, Tavares MV, et al. A New look into Cancer-A Review on the contribution of vibrational spectroscopy on early diagnosis and surgery Guidance. Cancers (Basel). 2021;13:21.CrossRef
9.
go back to reference Auner GW, Koya SK, Huang C, Broadbent B, Trexler M, Auner Z, et al. Applications of Raman spectroscopy in cancer diagnosis. Cancer Metastasis Rev. 2018;37(4):691–717.PubMedPubMedCentralCrossRef Auner GW, Koya SK, Huang C, Broadbent B, Trexler M, Auner Z, et al. Applications of Raman spectroscopy in cancer diagnosis. Cancer Metastasis Rev. 2018;37(4):691–717.PubMedPubMedCentralCrossRef
10.
go back to reference Krafft C, Dietzek B, Schmitt M, Popp J. Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications.J Biomed Opt. 2012;17(4). Krafft C, Dietzek B, Schmitt M, Popp J. Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications.J Biomed Opt. 2012;17(4).
11.
go back to reference Crow P, Stone N, Kendall CA, Uff JS, Farmer JA, Barr H, et al. The use of Raman spectroscopy to identify and grade prostatic adenocarcinoma in vitro. Br J Cancer. 2003;89(1):106–8.PubMedPubMedCentralCrossRef Crow P, Stone N, Kendall CA, Uff JS, Farmer JA, Barr H, et al. The use of Raman spectroscopy to identify and grade prostatic adenocarcinoma in vitro. Br J Cancer. 2003;89(1):106–8.PubMedPubMedCentralCrossRef
12.
go back to reference Kopec M, Błaszczyk M, Radek M, Abramczyk H. Raman imaging and statistical methods for analysis various type of human brain tumors and breast cancers. Spectrochim Acta A Mol Biomol Spectrosc. 2021;262:120091.PubMedCrossRef Kopec M, Błaszczyk M, Radek M, Abramczyk H. Raman imaging and statistical methods for analysis various type of human brain tumors and breast cancers. Spectrochim Acta A Mol Biomol Spectrosc. 2021;262:120091.PubMedCrossRef
13.
go back to reference Chen C, Wu W, Chen C, Chen F, Dong X, Ma M, et al. Rapid diagnosis of lung cancer and glioma based on serum Raman spectroscopy combined with deep learning. J Raman Spectrosc. 2021;52(11):1798–809.CrossRef Chen C, Wu W, Chen C, Chen F, Dong X, Ma M, et al. Rapid diagnosis of lung cancer and glioma based on serum Raman spectroscopy combined with deep learning. J Raman Spectrosc. 2021;52(11):1798–809.CrossRef
14.
go back to reference Leng H, Chen C, Chen C, Chen F, Du Z, Chen J, et al. Raman spectroscopy and FTIR spectroscopy fusion technology combined with deep learning: a novel cancer prediction method. Spectrochim Acta Part A Mol Biomol Spectrosc. 2023;285:121839.CrossRef Leng H, Chen C, Chen C, Chen F, Du Z, Chen J, et al. Raman spectroscopy and FTIR spectroscopy fusion technology combined with deep learning: a novel cancer prediction method. Spectrochim Acta Part A Mol Biomol Spectrosc. 2023;285:121839.CrossRef
15.
go back to reference Qu H, Wu W, Chen C, Yan Z, Guo W, Meng C, et al. Application of serum mid-infrared spectroscopy combined with an ensemble learning method in rapid diagnosis of gliomas. Anal Methods. 2021;13(39):4642–51.PubMedCrossRef Qu H, Wu W, Chen C, Yan Z, Guo W, Meng C, et al. Application of serum mid-infrared spectroscopy combined with an ensemble learning method in rapid diagnosis of gliomas. Anal Methods. 2021;13(39):4642–51.PubMedCrossRef
16.
go back to reference Gajjar K, Heppenstall LD, Pang W, Ashton KM, Trevisan J, Patel II, et al. Diagnostic segregation of human brain tumours using Fourier-transform infrared and/or Raman spectroscopy coupled with discriminant analysis. Anal Methods. 2012;5:89–102.PubMedPubMedCentralCrossRef Gajjar K, Heppenstall LD, Pang W, Ashton KM, Trevisan J, Patel II, et al. Diagnostic segregation of human brain tumours using Fourier-transform infrared and/or Raman spectroscopy coupled with discriminant analysis. Anal Methods. 2012;5:89–102.PubMedPubMedCentralCrossRef
17.
go back to reference Chenxi Zhang YH, Bo S, Zhang W, Liu S, Liu J, Lv H, Zhang G, Kang X. Label-free serum detection based on Raman spectroscopy for the diagnosis and classification of glioma. J Raman Spectrosc. 2020;51(10):1977–85.CrossRef Chenxi Zhang YH, Bo S, Zhang W, Liu S, Liu J, Lv H, Zhang G, Kang X. Label-free serum detection based on Raman spectroscopy for the diagnosis and classification of glioma. J Raman Spectrosc. 2020;51(10):1977–85.CrossRef
18.
go back to reference Ma H, Han XX, Zhao B. Enhanced Raman spectroscopic analysis of protein post-translational modifications. TRAC Trends Anal Chem. 2020;131:116019.CrossRef Ma H, Han XX, Zhao B. Enhanced Raman spectroscopic analysis of protein post-translational modifications. TRAC Trends Anal Chem. 2020;131:116019.CrossRef
19.
go back to reference Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015;15(9):540–55.PubMedCrossRef Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015;15(9):540–55.PubMedCrossRef
20.
go back to reference Filippou PS, Ren AH, Korbakis D, Dimitrakopoulos L, Soosaipillai A, Barak V, et al. Exploring the potential of mucin 13 (MUC13) as a biomarker for carcinomas and other diseases. Clin Chem Lab Med (CCLM). 2018;56(11):1945–53.PubMedCrossRef Filippou PS, Ren AH, Korbakis D, Dimitrakopoulos L, Soosaipillai A, Barak V, et al. Exploring the potential of mucin 13 (MUC13) as a biomarker for carcinomas and other diseases. Clin Chem Lab Med (CCLM). 2018;56(11):1945–53.PubMedCrossRef
21.
go back to reference Wang G, Lipert RJ, Jain M, Kaur S, Chakraboty S, Torres MP, et al. Detection of the potential pancreatic cancer marker MUC4 in serum using surface-enhanced Raman scattering. Anal Chem. 2011;83(7):2554–61.PubMedPubMedCentralCrossRef Wang G, Lipert RJ, Jain M, Kaur S, Chakraboty S, Torres MP, et al. Detection of the potential pancreatic cancer marker MUC4 in serum using surface-enhanced Raman scattering. Anal Chem. 2011;83(7):2554–61.PubMedPubMedCentralCrossRef
22.
go back to reference Veillon L, Fakih C, Abou-El-Hassan H, Kobeissy F, Mechref Y. Glycosylation changes in Brain Cancer. ACS Chem Neurosci. 2018;9(1):51–72.PubMedCrossRef Veillon L, Fakih C, Abou-El-Hassan H, Kobeissy F, Mechref Y. Glycosylation changes in Brain Cancer. ACS Chem Neurosci. 2018;9(1):51–72.PubMedCrossRef
23.
go back to reference Faoláin EO, Hunter MB, Byrne JM, Kelehan P, Lambkin HA, Byrne HJ, et al. Raman spectroscopic evaluation of efficacy of current paraffin wax section dewaxing agents. J Histochem Cytochem. 2005;53(1):121–9.PubMedCrossRef Faoláin EO, Hunter MB, Byrne JM, Kelehan P, Lambkin HA, Byrne HJ, et al. Raman spectroscopic evaluation of efficacy of current paraffin wax section dewaxing agents. J Histochem Cytochem. 2005;53(1):121–9.PubMedCrossRef
24.
go back to reference Kalli M, Voutouri C, Minia A, Pliaka V, Fotis C, Alexopoulos LG, et al. Mechanical Compression regulates Brain Cancer Cell Migration through MEK1/Erk1 pathway activation and GDF15 expression. Front Oncol. 2019;9:992.PubMedPubMedCentralCrossRef Kalli M, Voutouri C, Minia A, Pliaka V, Fotis C, Alexopoulos LG, et al. Mechanical Compression regulates Brain Cancer Cell Migration through MEK1/Erk1 pathway activation and GDF15 expression. Front Oncol. 2019;9:992.PubMedPubMedCentralCrossRef
25.
go back to reference Chugh S, Gnanapragassam VS, Jain M, Rachagani S, Ponnusamy MP, Batra SK. Pathobiological implications of mucin glycans in cancer: Sweet poison and novel targets. Biochim Biophys Acta. 2015;1856(2):211–25.PubMedPubMedCentral Chugh S, Gnanapragassam VS, Jain M, Rachagani S, Ponnusamy MP, Batra SK. Pathobiological implications of mucin glycans in cancer: Sweet poison and novel targets. Biochim Biophys Acta. 2015;1856(2):211–25.PubMedPubMedCentral
26.
go back to reference Tondepu C, Karumbaiah L. Glycomaterials to investigate the functional role of aberrant glycosylation in Glioblastoma. Adv Healthc Mater. 2022;11(4):e2101956.PubMedCrossRef Tondepu C, Karumbaiah L. Glycomaterials to investigate the functional role of aberrant glycosylation in Glioblastoma. Adv Healthc Mater. 2022;11(4):e2101956.PubMedCrossRef
27.
go back to reference Arboleda PH, Loppnow GR. Raman spectroscopy as a discovery tool in carbohydrate chemistry. Anal Chem. 2000;72(9):2093–8.PubMedCrossRef Arboleda PH, Loppnow GR. Raman spectroscopy as a discovery tool in carbohydrate chemistry. Anal Chem. 2000;72(9):2093–8.PubMedCrossRef
28.
go back to reference Aubertin K, Trinh VQ, Jermyn M, Baksic P, Grosset AA, Desroches J, et al. Mesoscopic characterization of prostate cancer using Raman spectroscopy: potential for diagnostics and therapeutics. BJU Int. 2018;122(2):326–36.PubMedCrossRef Aubertin K, Trinh VQ, Jermyn M, Baksic P, Grosset AA, Desroches J, et al. Mesoscopic characterization of prostate cancer using Raman spectroscopy: potential for diagnostics and therapeutics. BJU Int. 2018;122(2):326–36.PubMedCrossRef
29.
go back to reference Riva M, Sciortino T, Secoli R, D’Amico E, Moccia S, Fernandes B et al. Glioma biopsies Classification Using Raman Spectroscopy and Machine Learning Models on Fresh Tissue Samples.Cancers (Basel). 2021;13(5). Riva M, Sciortino T, Secoli R, D’Amico E, Moccia S, Fernandes B et al. Glioma biopsies Classification Using Raman Spectroscopy and Machine Learning Models on Fresh Tissue Samples.Cancers (Basel). 2021;13(5).
30.
go back to reference Feng S, Chen R, Lin J, Pan J, Chen G, Li Y, et al. Nasopharyngeal cancer detection based on blood plasma surface-enhanced Raman spectroscopy and multivariate analysis. Biosens Bioelectron. 2010;25(11):2414–9.PubMedCrossRef Feng S, Chen R, Lin J, Pan J, Chen G, Li Y, et al. Nasopharyngeal cancer detection based on blood plasma surface-enhanced Raman spectroscopy and multivariate analysis. Biosens Bioelectron. 2010;25(11):2414–9.PubMedCrossRef
31.
go back to reference Lin D, Pan J, Huang H, Chen G, Qiu S, Shi H, et al. Label-free blood plasma test based on surface-enhanced Raman scattering for tumor stages detection in nasopharyngeal cancer. Sci Rep. 2014;4:4751.PubMedPubMedCentralCrossRef Lin D, Pan J, Huang H, Chen G, Qiu S, Shi H, et al. Label-free blood plasma test based on surface-enhanced Raman scattering for tumor stages detection in nasopharyngeal cancer. Sci Rep. 2014;4:4751.PubMedPubMedCentralCrossRef
32.
go back to reference Kast RE, Auner GW, Rosenblum ML, Mikkelsen T, Yurgelevic SM, Raghunathan A, et al. Raman molecular imaging of brain frozen tissue sections. J Neurooncol. 2014;120(1):55–62.PubMedCrossRef Kast RE, Auner GW, Rosenblum ML, Mikkelsen T, Yurgelevic SM, Raghunathan A, et al. Raman molecular imaging of brain frozen tissue sections. J Neurooncol. 2014;120(1):55–62.PubMedCrossRef
33.
go back to reference Galli R, Meinhardt M, Koch E, Schackert G, Steiner G, Kirsch M, et al. Rapid label-free analysis of Brain Tumor Biopsies by Near Infrared Raman and fluorescence Spectroscopy-A study of 209 patients. Front Oncol. 2019;9:1165.PubMedPubMedCentralCrossRef Galli R, Meinhardt M, Koch E, Schackert G, Steiner G, Kirsch M, et al. Rapid label-free analysis of Brain Tumor Biopsies by Near Infrared Raman and fluorescence Spectroscopy-A study of 209 patients. Front Oncol. 2019;9:1165.PubMedPubMedCentralCrossRef
34.
go back to reference Zhang C, Han Y, Sun B, Zhang W, Liu S, Liu J, et al. Label-free serum detection based on Raman spectroscopy for the diagnosis and classification of glioma. J Raman Spectrosc. 2020;51(10):1977–85.CrossRef Zhang C, Han Y, Sun B, Zhang W, Liu S, Liu J, et al. Label-free serum detection based on Raman spectroscopy for the diagnosis and classification of glioma. J Raman Spectrosc. 2020;51(10):1977–85.CrossRef
35.
go back to reference Abramczyk H, Imiela A. The biochemical, nanomechanical and chemometric signatures of brain cancer. Spectrochim Acta A Mol Biomol Spectrosc. 2018;188:8–19.PubMedCrossRef Abramczyk H, Imiela A. The biochemical, nanomechanical and chemometric signatures of brain cancer. Spectrochim Acta A Mol Biomol Spectrosc. 2018;188:8–19.PubMedCrossRef
36.
go back to reference Wiercigroch E, Szafraniec E, Czamara K, Pacia MZ, Majzner K, Kochan K, et al. Raman and infrared spectroscopy of carbohydrates: a review. Spectrochim Acta A Mol Biomol Spectrosc. 2017;185:317–35.PubMedCrossRef Wiercigroch E, Szafraniec E, Czamara K, Pacia MZ, Majzner K, Kochan K, et al. Raman and infrared spectroscopy of carbohydrates: a review. Spectrochim Acta A Mol Biomol Spectrosc. 2017;185:317–35.PubMedCrossRef
37.
go back to reference Ali SM, Bonnier F, Tfayli A, Lambkin H, Flynn K, McDonagh V, et al. Raman spectroscopic analysis of human skin tissue sections ex-vivo: evaluation of the effects of tissue processing and dewaxing. J Biomed Opt. 2013;18(6):061202.PubMedCrossRef Ali SM, Bonnier F, Tfayli A, Lambkin H, Flynn K, McDonagh V, et al. Raman spectroscopic analysis of human skin tissue sections ex-vivo: evaluation of the effects of tissue processing and dewaxing. J Biomed Opt. 2013;18(6):061202.PubMedCrossRef
38.
go back to reference Larkin P. Chapter 1 - introduction: Infrared and Raman Spectroscopy. In: Larkin P, editor. Infrared and Raman Spectroscopy. Oxford: Elsevier; 2011. pp. 1–5. Larkin P. Chapter 1 - introduction: Infrared and Raman Spectroscopy. In: Larkin P, editor. Infrared and Raman Spectroscopy. Oxford: Elsevier; 2011. pp. 1–5.
39.
go back to reference Larkin P. Chapter 2 - Basic Principles. In: Larkin P, editor. Infrared and Raman Spectroscopy. Oxford: Elsevier; 2011. pp. 7–25.CrossRef Larkin P. Chapter 2 - Basic Principles. In: Larkin P, editor. Infrared and Raman Spectroscopy. Oxford: Elsevier; 2011. pp. 7–25.CrossRef
40.
go back to reference Melhem JM, Detsky J, Lim-Fat MJ, Perry JR. Updates in IDH-Wildtype Glioblastoma. Neurotherapeutics. 2022. Melhem JM, Detsky J, Lim-Fat MJ, Perry JR. Updates in IDH-Wildtype Glioblastoma. Neurotherapeutics. 2022.
41.
go back to reference D’Alessio A, Proietti G, Sica G, Scicchitano BM. Pathological and molecular features of Glioblastoma and its Peritumoral tissue. Cancers. 2019;11(4):469.PubMedPubMedCentralCrossRef D’Alessio A, Proietti G, Sica G, Scicchitano BM. Pathological and molecular features of Glioblastoma and its Peritumoral tissue. Cancers. 2019;11(4):469.PubMedPubMedCentralCrossRef
42.
go back to reference Zhou Y, Liu CH, Sun Y, Pu Y, Boydston-White S, Liu Y, et al. Human brain cancer studied by resonance raman spectroscopy. J Biomed Opt. 2012;17(11):116021.PubMedPubMedCentralCrossRef Zhou Y, Liu CH, Sun Y, Pu Y, Boydston-White S, Liu Y, et al. Human brain cancer studied by resonance raman spectroscopy. J Biomed Opt. 2012;17(11):116021.PubMedPubMedCentralCrossRef
43.
go back to reference Payne LS, Huang PH. The pathobiology of collagens in glioma. Mol Cancer Res. 2013;11(10):1129–40.PubMedCrossRef Payne LS, Huang PH. The pathobiology of collagens in glioma. Mol Cancer Res. 2013;11(10):1129–40.PubMedCrossRef
44.
go back to reference Pointer KB, Clark PA, Schroeder AB, Salamat MS, Eliceiri KW, Kuo JS. Association of collagen architecture with glioblastoma patient survival. J Neurosurg. 2017;126(6):1812–21.PubMedCrossRef Pointer KB, Clark PA, Schroeder AB, Salamat MS, Eliceiri KW, Kuo JS. Association of collagen architecture with glioblastoma patient survival. J Neurosurg. 2017;126(6):1812–21.PubMedCrossRef
45.
go back to reference Banerjee HN, Banerji A, Banerjee AN, Riddick E, Petis J, Evans S, et al. Deciphering the Finger Prints of Brain Cancer Glioblastoma Multiforme from four different patients by using Near Infrared Raman Spectroscopy. J Cancer Sci Ther. 2015;7(2):44–7.PubMedPubMedCentralCrossRef Banerjee HN, Banerji A, Banerjee AN, Riddick E, Petis J, Evans S, et al. Deciphering the Finger Prints of Brain Cancer Glioblastoma Multiforme from four different patients by using Near Infrared Raman Spectroscopy. J Cancer Sci Ther. 2015;7(2):44–7.PubMedPubMedCentralCrossRef
46.
go back to reference Shrivastava A, Aggarwal LM, Murali Krishna C, Pradhan S, Mishra SP, Choudhary S, et al. Diagnostic and prognostic application of Raman spectroscopy in carcinoma cervix: a biomolecular approach. Spectrochim Acta Part A Mol Biomol Spectrosc. 2021;250:119356.CrossRef Shrivastava A, Aggarwal LM, Murali Krishna C, Pradhan S, Mishra SP, Choudhary S, et al. Diagnostic and prognostic application of Raman spectroscopy in carcinoma cervix: a biomolecular approach. Spectrochim Acta Part A Mol Biomol Spectrosc. 2021;250:119356.CrossRef
47.
go back to reference Mehta K, Atak A, Sahu A, Srivastava S, Chilakapati MK. An early investigative serum Raman spectroscopy study of meningioma.The Analyst. 2018;143. Mehta K, Atak A, Sahu A, Srivastava S, Chilakapati MK. An early investigative serum Raman spectroscopy study of meningioma.The Analyst. 2018;143.
48.
go back to reference Donczo B, Szigeti M, Ostoros G, Gacs A, Tovari J, Guttman A. N-Glycosylation analysis of formalin fixed paraffin embedded samples by capillary electrophoresis. Electrophoresis. 2016;37(17–18):2292–6.PubMedCrossRef Donczo B, Szigeti M, Ostoros G, Gacs A, Tovari J, Guttman A. N-Glycosylation analysis of formalin fixed paraffin embedded samples by capillary electrophoresis. Electrophoresis. 2016;37(17–18):2292–6.PubMedCrossRef
49.
go back to reference Furukawa J, Tsuda M, Okada K, Kimura T, Piao J, Tanaka S, et al. Comprehensive Glycomics of a Multistep Human Brain Tumor Model reveals specific glycosylation patterns related to Malignancy. PLoS ONE. 2015;10(7):e0128300.PubMedPubMedCentralCrossRef Furukawa J, Tsuda M, Okada K, Kimura T, Piao J, Tanaka S, et al. Comprehensive Glycomics of a Multistep Human Brain Tumor Model reveals specific glycosylation patterns related to Malignancy. PLoS ONE. 2015;10(7):e0128300.PubMedPubMedCentralCrossRef
50.
go back to reference Dusoswa SA, Verhoeff J, Abels E, Méndez-Huergo SP, Croci DO, Kuijper LH, et al. Glioblastomas exploit truncated O-linked glycans for local and distant immune modulation via the macrophage galactose-type lectin. Proc Natl Acad Sci U S A. 2020;117(7):3693–703.PubMedPubMedCentralCrossRef Dusoswa SA, Verhoeff J, Abels E, Méndez-Huergo SP, Croci DO, Kuijper LH, et al. Glioblastomas exploit truncated O-linked glycans for local and distant immune modulation via the macrophage galactose-type lectin. Proc Natl Acad Sci U S A. 2020;117(7):3693–703.PubMedPubMedCentralCrossRef
51.
go back to reference Peixoto A, Relvas-Santos M, Azevedo R, Santos LL, Ferreira JA. Protein glycosylation and tumor microenvironment alterations driving Cancer Hallmarks. Front Oncol. 2019;9:380.PubMedPubMedCentralCrossRef Peixoto A, Relvas-Santos M, Azevedo R, Santos LL, Ferreira JA. Protein glycosylation and tumor microenvironment alterations driving Cancer Hallmarks. Front Oncol. 2019;9:380.PubMedPubMedCentralCrossRef
52.
go back to reference Ferreira JA, Relvas-Santos M, Peixoto A, Lara Santos AMNS, Glycoproteogenomics L. Setting the course for next-generation Cancer Neoantigen Discovery for Cancer Vaccines. Genomics Proteom Bioinf. 2021;19(1):25–43.CrossRef Ferreira JA, Relvas-Santos M, Peixoto A, Lara Santos AMNS, Glycoproteogenomics L. Setting the course for next-generation Cancer Neoantigen Discovery for Cancer Vaccines. Genomics Proteom Bioinf. 2021;19(1):25–43.CrossRef
53.
go back to reference Eliassen AH, Hendrickson SJ, Brinton LA, Buring JE, Campos H, Dai Q, et al. Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst. 2012;104(24):1905–16.PubMedPubMedCentralCrossRef Eliassen AH, Hendrickson SJ, Brinton LA, Buring JE, Campos H, Dai Q, et al. Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst. 2012;104(24):1905–16.PubMedPubMedCentralCrossRef
54.
go back to reference Shrivastava A, Aggarwal L, Chilakapati MK, Pradhan S, Mishra S, Choudhary S, et al. Diagnostic and prognostic application of Raman Spectroscopy in Carcinoma Cervix: a Biomolecular Approach. Spectrochim Acta Part A Mol Biomol Spectrosc. 2020;250:119356.CrossRef Shrivastava A, Aggarwal L, Chilakapati MK, Pradhan S, Mishra S, Choudhary S, et al. Diagnostic and prognostic application of Raman Spectroscopy in Carcinoma Cervix: a Biomolecular Approach. Spectrochim Acta Part A Mol Biomol Spectrosc. 2020;250:119356.CrossRef
55.
go back to reference Kirwan A, Utratna M, O’Dwyer ME, Joshi L, Kilcoyne M. Glycosylation-based serum biomarkers for Cancer Diagnostics and Prognostics. Biomed Res Int. 2015;2015:490531.PubMedPubMedCentralCrossRef Kirwan A, Utratna M, O’Dwyer ME, Joshi L, Kilcoyne M. Glycosylation-based serum biomarkers for Cancer Diagnostics and Prognostics. Biomed Res Int. 2015;2015:490531.PubMedPubMedCentralCrossRef
56.
go back to reference Hanson RL, Hollingsworth MA. Functional consequences of Differential O-glycosylation of MUC1, MUC4, and MUC16 (downstream Effects on Signaling). Biomolecules. 2016;6(3):34.PubMedPubMedCentralCrossRef Hanson RL, Hollingsworth MA. Functional consequences of Differential O-glycosylation of MUC1, MUC4, and MUC16 (downstream Effects on Signaling). Biomolecules. 2016;6(3):34.PubMedPubMedCentralCrossRef
58.
go back to reference Singh R, Bandyopadhyay D. MUC1: a target molecule for cancer therapy. Cancer Biol Ther. 2007;6(4):481–6.PubMedCrossRef Singh R, Bandyopadhyay D. MUC1: a target molecule for cancer therapy. Cancer Biol Ther. 2007;6(4):481–6.PubMedCrossRef
60.
go back to reference Giamougiannis P, Martin-Hirsch PL, Martin FL. The evolving role of MUC16 (CA125) in the transformation of ovarian cells and the progression of neoplasia. Carcinogenesis. 2021;42(3):327–43.PubMedCrossRef Giamougiannis P, Martin-Hirsch PL, Martin FL. The evolving role of MUC16 (CA125) in the transformation of ovarian cells and the progression of neoplasia. Carcinogenesis. 2021;42(3):327–43.PubMedCrossRef
61.
go back to reference Radhakrishnan P, Dabelsteen S, Madsen FB, Francavilla C, Kopp KL, Steentoft C et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proceedings of the National Academy of Sciences. 2014;111(39):E4066-E75. Radhakrishnan P, Dabelsteen S, Madsen FB, Francavilla C, Kopp KL, Steentoft C et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proceedings of the National Academy of Sciences. 2014;111(39):E4066-E75.
62.
go back to reference Kudelka MR, Ju T, Heimburg-Molinaro J, Cummings RD. Simple sugars to complex disease–mucin-type O-glycans in cancer. Adv Cancer Res. 2015;126:53–135.PubMedPubMedCentralCrossRef Kudelka MR, Ju T, Heimburg-Molinaro J, Cummings RD. Simple sugars to complex disease–mucin-type O-glycans in cancer. Adv Cancer Res. 2015;126:53–135.PubMedPubMedCentralCrossRef
63.
go back to reference Vijayakumar S, Rahman PKSM, Angione C. A hybrid Flux Balance Analysis and Machine Learning Pipeline elucidates metabolic adaptation in Cyanobacteria. iScience. 2020;23(12):101818.PubMedPubMedCentralCrossRef Vijayakumar S, Rahman PKSM, Angione C. A hybrid Flux Balance Analysis and Machine Learning Pipeline elucidates metabolic adaptation in Cyanobacteria. iScience. 2020;23(12):101818.PubMedPubMedCentralCrossRef
64.
go back to reference Capper D, Jones DTW, Sill M, Hovestadt V, Schrimpf D, Sturm D, et al. DNA methylation-based classification of central nervous system tumours. Nature. 2018;555(7697):469–74.PubMedPubMedCentralCrossRef Capper D, Jones DTW, Sill M, Hovestadt V, Schrimpf D, Sturm D, et al. DNA methylation-based classification of central nervous system tumours. Nature. 2018;555(7697):469–74.PubMedPubMedCentralCrossRef
65.
go back to reference Krafft C, Sobottka SB, Schackert G, Salzer R. Near infrared Raman spectroscopic mapping of native brain tissue and intracranial tumors. Analyst. 2005;130(7):1070–7.PubMedCrossRef Krafft C, Sobottka SB, Schackert G, Salzer R. Near infrared Raman spectroscopic mapping of native brain tissue and intracranial tumors. Analyst. 2005;130(7):1070–7.PubMedCrossRef
66.
go back to reference Riva M, Sciortino T, Secoli R, D’Amico E, Moccia S, Fernandes B, et al. Glioma biopsies classification using Raman Spectroscopy and Machine Learning Models on Fresh tissue samples. Cancers. 2021;13(5):1073.PubMedPubMedCentralCrossRef Riva M, Sciortino T, Secoli R, D’Amico E, Moccia S, Fernandes B, et al. Glioma biopsies classification using Raman Spectroscopy and Machine Learning Models on Fresh tissue samples. Cancers. 2021;13(5):1073.PubMedPubMedCentralCrossRef
Metadata
Title
Glycosylation spectral signatures for glioma grade discrimination using Raman spectroscopy
Authors
Agathe Quesnel
Nathan Coles
Claudio Angione
Priyanka Dey
Tuomo M. Polvikoski
Tiago F. Outeiro
Meez Islam
Ahmad A. Khundakar
Panagiota S. Filippou
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-10588-w

Other articles of this Issue 1/2023

BMC Cancer 1/2023 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine