Putative Biomarkers for Malignant Pleural Mesothelioma Suggested by Proteomic Analysis of Cell Secretome

[en] BACKGROUND: Malignant pleural mesothelioma (MPM) a rare neoplasm linked to asbestos exposure is characterized by a poor prognosis. Soluble mesothelin is currently considered the most specific diagnostic biomarker. The aim of the study was to identify novel biomarkers by proteomic analysis of two MPM cell lines secretome. MATERIALS AND METHODS: The protein patterns of MPM cells secretome were examined and compared to a non-malignant mesothelial cell line using two-dimensional gel electrophoresis coupled to mass spectrometry. Serum levels of candidate biomarkers were determined in MPM patients and control subjects. RESULTS: Two up-regulated proteins involved in cancer biology, prosaposin and quiescin Q6 sulfhydryl oxidase 1, were considered candidate biomarkers. Serum levels of both proteins were significantly higher in MPM patients than control subjects. Combining the data of each receiver-operating characteristic analysis predicted a good diagnostic accuracy. CONCLUSION: A panel of the putative biomarkers represents a promising tool for MPM diagnosis. Copyright© 2020, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.

Disciplines :

Systèmes cardiovasculaire & respiratoire
Oncologie

Auteur, co-auteur :

Lacerenza, S.; Department of Pharmacy, University of Pisa, Pisa, Italy

Ciregia, Federica ; Université de Liège - ULiège > I3-Rheumatology

Giusti, L.; School of Pharmacy, University of Camerino, Camerino, Italy, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy

Bonotti, A.; Department of Translational Research and New Medical and Surgical Technologies, Occupational Medicine Unit, University-Hospital of Pisa, Pisa, Italy

Greco, V.; Institute of Biochemistry and Clinical Chemistry, Università Cattolica del Sacro Cuore, Rome, Italy, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy

Giannaccini, G.; Department of Pharmacy, University of Pisa, Pisa, Italy

D'Antongiovanni, V.; Department of Pharmacy, University of Pisa, Pisa, Italy

Fallahi, P.; Department of Translational Research and New Medical and Surgical Technologies, Occupational Medicine Unit, University-Hospital of Pisa, Pisa, Italy

Pieroni, L.; Proteomics and Metabonomics Unit, IRCCS-Fondazione Santa Lucia, Rome, Italy

Cristaudo, A.; Department of Translational Research and New Medical and Surgical Technologies, Occupational Medicine Unit, University-Hospital of Pisa, Pisa, Italy

Plus d'auteurs (3 en +)

Langue du document :

Anglais

Titre :

Putative Biomarkers for Malignant Pleural Mesothelioma Suggested by Proteomic Analysis of Cell Secretome

Date de publication/diffusion :

2020

Titre du périodique :

Cancer genomics & proteomics

ISSN :

1790-6245

Maison d'édition :

NLM (Medline)

Volume/Tome :

Fascicule/Saison :

Pagination :

225-236

Peer reviewed :

Peer reviewed

Disponible sur ORBi :

depuis le 17 juin 2021

Statistiques

Nombre de vues

99 (dont 2 ULiège)

Nombre de téléchargements

81 (dont 5 ULiège)

Voir plus de statistiques

citations Scopus^®

citations Scopus^®
sans auto-citations

OpenCitations

citations OpenAlex

Bibliographie

Zucali PA, Ceresoli GL, De Vincenzo F, Simonelli M, Lorenzi E, Gianoncelli L and Santoro A: Advances in the biology of malignant pleural mesothelioma. Cancer Treat Rev 37(7): 543-558, 2011. PMID: 21288646. DOI: 10.1016/j.ctrv.2011.01.001
van Zandwijk N, Clarke C, Henderson D, Musk AW, Fong K, Nowak A, Loneragan R, McCaughan B, Boyer M, Feigen M, Currow D, Schofield P, Nick Pavlakis BI, McLean J, Marshall H, Leong S, Keena V and Penman A: Guidelines for the diagnosis and treatment of malignant pleural mesothelioma. J Thorac Dis 5(6): E254-307, 2013. PMID: 24416529. DOI: 10.3978/j.issn.2072-1439.2013.11.28
Panou V, Vyberg M, Weinreich UM, Meristoudis C, Falkmer UG and Røe OD: The established and future biomarkers of malignant pleural mesothelioma. Cancer Treat Rev 41(6): 486-495, 2015. PMID: 25979846. DOI: 10.1016/j.ctrv.2015.05.001
Sun HH, Vaynblat A and Pass HI: Diagnosis and prognosis-review of biomarkers for mesothelioma. Ann Transl Med 5(11): 244, 2017. PMID: 28706912. DOI: 10.21037/atm. 2017.06.60
Lagniau S, Lamote K, van Meerbeeck JP and Vermaelen KY: Biomarkers for early diagnosis of malignant mesothelioma: Do we need another moonshot? Oncotarget 8(32): 53751-53762, 2017. PMID: 28881848. DOI: 10.18632/oncotarget.17910
Franceschini MC, Ferro P, Canessa PA, Battolla E, Dessanti P, Valentino A, Casolari L, Fontana V, Pezzi R, Fedeli F, Pistillo MP and Roncella S: Mesothelin in serum and pleural effusion in the diagnosis of malignant pleural mesothelioma with non-positive cytology. Anticancer Res 34(12): 7425-7429, 2014. PMID: 25503183.
Pass HI, Levin SM, Harbut MR, Melamed J, Chiriboga L, Donington J, Huflejt M, Carbone M, Chia D, Goodglick L, Goodman GE, Thornquist MD, Liu G, de Perrot M, Tsao MS and Goparaju C: Fibulin-3 as a blood and effusion biomarker for pleural mesothelioma. N Engl J Med 367(15): 1417-2147, 2012. PMID: 23050525. DOI: 10.1056/NEJMoa1115050
Creaney J, Dick IM, Meniawy TM, Leong SL, Leon JS, Demelker Y, Segal A, Musk AW, Lee YC, Skates SJ, Nowak AK and Robinson BW: Comparison of fibulin-3 and mesothelin as markers in malignant mesothelioma. Thorax 69(10): 895-902, 2014. PMID: 25037982. DOI: 10.1136/thoraxjnl-2014-205205
Battolla E, Canessa PA, Ferro P,Franceschini MC, Fontana V, Dessanti P, Pinelli V, Morabito A, Fedeli F, Pistillo MP and Roncella S: Comparison of the diagnostic performance of fibulin-3 and mesothelin in patients with pleural effusions from malignant mesothelioma. Anticancer Res 37(3): 1387-1391, 2017. PMID: 28314308.
Fontana V, Pistillo MP, Vigani A, Canessa PA, Berisso G, Giannoni U, Ferro P, Franceschini MC, Carosio R, Tonarelli M, Rossi C, Dessanti P and Roncella S: determination of mesothelin levels in pleural effusion does not help predict survival of patients with malignant pleural mesothelioma. Anticancer Res 39(9): 5219-5223, 2019. PMID: 31519636. DOI: 10.21873/anticanres.13719
Micolucci L, Akhtar MM, Olivieri F, Rippo MR and Procopio AD: Diagnostic value of microRNAs in asbestos exposure and malignant mesothelioma: systematic review and qualitative meta-analysis. Oncotarget 7(36): 58606-58637, 2016. PMID: 27259231. DOI: 10.18632/ oncotarget.9686
Greening DW, Ji H, Chen M, Robinson BW, Dick IM, Creaney J and Simpson RJ: Secreted primary human malignant mesothelioma exosome signature reflects oncogenic cargo. Sci Rep 6: 32643, 2016. PMID: 27605433. DOI: 10.1038/srep32643
Manfredi M, Martinotti S, Gosetti F, Ranzato E and Marengo E: The secretome signature of malignant mesothelioma cell lines. J Proteomics 145: 3-10, 2016. PMID: 26921831. DOI: 10.1016/j.jprot.2016.02.021
Creaney J, Dick IM, Leon JS and Robinson BW: A proteomic analysis of the malignant mesothelioma secretome using iTRAQ. Cancer Genomics Proteomics 14(2): 103-117, 2017. PMID: 28387650.
Fazzini A, D’Antongiovanni V, Giusti L, Da Valle Y, Ciregia F, Piano I, Caputo A, D’Ursi AM, Gargini C, Lucacchini A and Mazzoni MR: Altered protease-activated receptor-1 expression and signaling in a malignant pleural mesothelioma cellì line, NCI-H28, with homozygous deletion of the β-catenin gene. PLoS One 9(11): e111550, 2014. PMID: 25364818. DOI: 10.1371/ journal.pone.0111550
Kanaji N, Kita N, Kadowaki N and Bandoh S: fibronectin and hepatocyte growth factor produced by lung fibroblasts augment migration and invasion of malignant pleural mesothelioma cells. Anticancer Res 37(5): 2393-2400, 2017. PMID: 28476806. DOI: 10.21873/anticanres.11578
Ciregia F, Giusti L, Da Valle Y, Donadio E, Consensi A, Giacomelli C, Sernissi F, Scarpellini P, Maggi F, Lucacchini A and Bazzichi L: A multidisciplinary approach to study a couple of monozygotic twins discordant for the chronic fatigue syndrome: a focus on potential salivary biomarkers. J Transl Med 11: 243, 2013. PMID: 24088505. DOI: 10.1186/1479-5876-11-243
Giusti L, Baldini C, Bazzichi L, Ciregia F, Tonazzini I, Mascia G, Giannaccini G, Bombardieri S and Lucacchini A: Proteome analysis of whole saliva: a new tool for rheumatic diseases – the example of Sjögren’s syndrome. Proteomics 7(16): 1634-1643, 2007. PMID: 17436266. DOI: 10.1002/pmic.200600783
Giusti L, Iacconi P, Da Valle Y, Ciregia F, Ventroni T, Donadio E, Giannaccini G, Chiarugi M, Torregrossa L, Proietti A, Basolo F and Lucacchini A: A proteomic profile of washing fluid from the colorectal tract to search for potential biomarkers of colon cancer. Mol Biosyst 8(4): 1088-1099, 2012. PMID: 22294321. DOI: 10.1039/c2mb05394b
Aude-Garcia C, Collin-Faure V, Luche S and Rabilloud T: Improvements and simplifications in in-gel fluorescent detection of proteins using ruthenium II tris-(bathophenanthroline disulfonate): the poor man’s fluorescent detection method. Proteomics 11(2): 324-328, 2011. PMID: 21204259. DOI: 10.1002/pmic.201000370
Giusti L, Angeloni C, Barbalace MC, Lacerenza S, Ciregia F, Ronci M, Urbani A, Manera C, Digiacomo M, Macchia M, Mazzoni MR, Lucacchini A and Hrelia SA: Proteomic approach to uncover neuroprotective mechanisms of oleocanthal against oxidative stress. Int J Mol Sci 19(8): 2329, 2018. PMID: 30096819. DOI: 10.3390/ijms19082329
Soggiu A, Piras C, Greco V, Devoto P, Urbani A, Calzetta L, Bortolato M and Roncada P: Exploring the neural mechanisms of finasteride: a proteomic analysis in the nucleus accumbens. Psychoneuroendocrinology 74: 387-396, 2016. PMID: 27750143. DOI: 10.1016/j.psyneuen.2016.10.001
Piras C, Soggiu A, Greco V, Martino PA, Del Chierico F, Putignani L, Urbani A, Nally JE, Bonizzi L and Roncada P: Mechanisms of antibiotic resistance to enrofloxacin in uropathogenic Escherichia coli in dog. J Proteomics 127(pt8): 365-376, 2015. PMID: 26066767. DOI: 10.1016/j.jprot.2015.05.040
Ochiai T, Takenaka Y, Kuramoto Y, Kasuya M, Fukuda K, Kimura M, Shimeno H, Misasi R, Hiraiwa M and Soeda S: Molecular mechanism for neuro-protective effect of prosaposin against oxidative stress: its regulation of dimeric transcription factor formation. Biochim Biophys Acta 1780(12): 1441-1447, 2008. PMID: 18706485. DOI: 10.1016/j.bbagen.2008.07.010
Morel C, Adami P, Musard JF, Duval D, Radom J and Jouvenot M: Involvement of sulfhydryl oxidase QSOX1 in the protection of cells against oxidative stress-induced apoptosis. Exp Cell Res 313(19): 3971-3982, 2007. PMID: 17927979. DOI: 10.1016/ j.yexcr.2007.09.003
Kudryavtseva AV, Krasnov GS, Dmitriev AA, Alekseev BY, Kardymon OL, Sadritdinova AF, Fedorova MS, Pokrovsky AV, Melnikova NV, Kaprin AD, Moskalev AA and Snezhkina AV: Mitochondrial dysfunction and oxidative stress in aging and cancer. Oncotarget 7(29): 44879-44905, 2016. PMID: 27270647. DOI: 10.18632/oncotarget.9821
Benedetti S, Nuvoli B, Catalani S and Galati R: Reactive oxygen species a double-edged sword for mesothelioma. Oncotarget 6(18): 16848-16865, 2015. PMID: 26078352. DOI: 10.18632/ oncotarget.4253
Arnold DT and Maskell NA: Biomarkers in mesothelioma. Ann Clin Biochem 55(1): 49-58, 2018. PMID: 29058958. DOI: 10.1177/0004563217741145
Bonotti A, Foddis R, Landi S, Melaiu O, De Santi C, Giusti L, Donadio E,Ciregia F, Mazzoni MR, Lucacchini A, Bovenzi M, Comar M, Pantani E, Pistelli A and Cristaudo A: A novel panel of serum biomarkers for MPM diagnosis. Dis Markers 2017: 3510984, 2017. PMID: 28348450. DOI: 10.1155/2017/3510984
Meyer RC, Giddens MM, Coleman BM and Hall RA: The protective role of prosaposin and its receptors in the nervous system. Brain Res 1585: 1-12, 2014. PMID: 25130661. DOI: 10.1016/j.brainres.2014.08.022
O’Brien JS, Carson GS, Seo HC, Hiraiwa M and Kishimoto Y: Identification of prosaposin as a neurotrophic factor. Proc Natl Acad Sci USA 91(20): 9593-9596, 1994. PMID: 7937812. DOI: 10.1073/pnas.91.20.9593
Koochekpour S, Sartor O, Lee TJ, Zieske A, Patten DY, Hiraiwa M, Sandhoff K, Remmel N and Minokadeh A: Prosaptide TX14A stimulates growth, migration, and invasion and activates the Raf-MEK-ERK-RSK-Elk-1 signaling pathway in prostate cancer cells. Prostate 61(2): 114-123, 2004. PMID: 15305334. DOI: 10.1002/pros.20082
Koochekpour S, Zhuang YJ, Beroukhim R, Hsieh CL, Hofer MD, Zhau HE, Hiraiwa M, Pattan DY, Ware JL, Luftig RB, Sandhoff K, Sawyers CL, Pienta KJ, Rubin MA, Vessella RL, Sellers WR and Sartor O: Amplification and overexpression of prosaposin in prostate cancer. Genes Chromosomes Cancer 44(4): 351-364, 2005. PMID: 16080200. DOI: 10.1002/ gcc.20249
Koochekpour S, Lee TJ, Wang R, Culig Z, Delorme N, Caffey S, Marrero L and Aguirre J: Prosaposin upregulates AR and PSA expression and activity in prostate cancer cells (LNCaP). Prostate 67(2): 178-189, 2007. PMID: 17044040. DOI: 10.1002/pros.20513
Hu S, Delorme N, Liu Z, Liu T, Velasco-Gonzalez C, Garai J, Pullikuth A and Koochekpour S: Prosaposin down-modulation decreases metastatic prostate cancer cell adhesion, migration, and invasion. Mol Cancer 9: 30, 2010. PMID: 20132547. DOI: 10.1186/1476-4598-9-30
Kang SY, Halvorsen OJ, Gravdal K, Bhattacharya N, Lee JM, Liu NW, Johnston BT, Johnston AB, Haukaas SA, Aamodt K, Yoo S, Akslen LA and Watnick RS: Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1. Proc Natl Acad Sci USA 106(29): 12115-12120, 2009. PMID: 19581582. DOI: 10.1073/pnas.0903120106
Sahasrabuddhe NA, Barbhuiya MA, Bhunia S, Subbannayya T, Gowda H, Advani J, Shrivastav BR, Navani S, Leal P, Roa JC, Chaerkady R, Gupta S, Chatterjee A, Pandey A and Tiwari PK: Identification of prosaposin and transgelin as potential biomarkers for gallbladder cancer using quantitative proteomics. Biochem Biophys Res Commun 446(4): 863-869, 2014. PMID: 24657443. DOI: 10.1016/j.bbrc.2014.03.017
Yang S, Chen L, Chan DW, Li QK and Zhang H: Protein signatures of molecular pathways in non-small cell lung carcinoma (NSCLC): comparison of glycoproteomics and global proteomics. Clin Proteomics 14: 31, 2017. PMID: 28814946. DOI: 10.1186/s12014-017-9166-9
Lake DF and Faigel DO: The emerging role of QSOX1 in cancer. Antioxid Redox Signal 21(3): 485-496, 2014. PMID: 24359107. DOI: 10.1089/ars.2013.5572
Ilani T, Alon A, Grossman I, Horowitz B, Kartvelishvily E, Cohen SR and Fass D: A secreted disulfide catalyst controls extracellular matrix composition and function. Science 341(6141): 74-76, 2013. PMID: 23704371. DOI: 10.1126/science.1238279
Knutsvik G, Collett K, Arnes J, Akslen LA and Stefansson IM: QSOX1 expression is associated with aggressive tumor features and reduced survival in breast carcinomas. Mod Pathol 29(12): 1485-1491, 2016. PMID: 27562495. DOI: 10.1038/modpathol.2016.148
Antwi K, Hostetter G, Demeure MJ, Katchman BA, Decker GA, Ruiz Y, Sielaff TD, Koep LJ and Lake DF: Analysis of the plasma peptidome from pancreas cancer patients connects a peptide in plasma to overexpression of the parent protein in tumors. J Proteome Res 8(10): 4722-4731, 2009. PMID: 19795908. DOI: 10.1021/pr900414f
Sung HJ, Ahn JM, Yoon YH, Na SS, Choi YJ, Kim YI, Lee SY, Lee EB, Cho S and Cho JY: Quiescin sulfhydryl oxidase 1 (QSOX1) secreted by lung cancer cells promotes cancer metastasis. Int J Mol Sci 19(10): E3213, 2018. PMID: 30336636. DOI: 10.3390/ijms19103213
Valvona CJ, Fillmore HL, Nunn PB and Pilkington GJ: The regulation and function of lactate dehydrogenase A: therapeutic potential in brain tumor. Brain Pathol 26(1): 3-17, 2016. PMID: 26269128. DOI: 10.1111/bpa.12299
Petrelli F, Cabiddu M, Coinu A, Borgonovo K, Ghilardi M, Lonati V and Barni S: Prognostic role of lactate dehydrogenase in solid tumors: a systematic review and meta-analysis of 76 studies. Acta Oncol 54(7): 961-970, 2015. PMID: 25984930. DOI: 10.3109/0284186X.2015.1043026
Usami N, Sekido Y, Maeda O, Yamamoto K, Minna JD, Hasegawa Y, Yoshioka H, Imaizumi M, Ueda Y, Takahashi M and Shimokata K: Beta-catenin inhibits cell growth of a malignant mesothelioma cell line, NCI-H28, with a 3p21.3 homozygous deletion. Oncogene 22(39): 7923-7930, 2003. PMID: 12970740. DOI: 10.1038/sj.onc.1206533
Grigoriu BD, Scherpereel A, Devos P, Chahine B, Letourneux M, Lebailly P, Grégoire M, Porte H, Copin MC and Lassalle P: Utility of osteopontin and serum mesothelin in malignant pleural mesothelioma diagnosis and prognosis assessment. Clin Cancer Res 13(10): 2928-2935, 2007. PMID: 17504993. DOI: 10.1158/1078-0432.CCR-06-2144
Koochekpour S, Hu S, Vellasco-Gonzalez C, Bernardo R, Azabdaftari G, Zhu G, Zhau HE, Chung LW and Vessella RL: Serum prosaposin levels are increased in patients with advanced prostate cancer. Prostate 72(3): 253-269, 2012. PMID: 21630292. DOI: 10.1002/pros.21427