[en] Cystic echinococcosis (CE) is a pandemic infectious disease caused by the tapeworm Echinococcus granulosus that forms cysts in different organs such as lungs and liver. Imaging examination and serological tests have some drawbacks such as low sensitivity. In this study, we used an up-to-date workflow of laser microdissection-based microproteomics and matrix-assisted laser desorption/ionization time-of-flight imaging mass spectrometry in order to depict the proteomic pattern of CE in the liver. This investigation revealed specific markers of a parasitic cyst in liver. This proteomic pattern could facilitate diagnosis of CE in the future.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Longuespée, Rémi; Proteopath GmbH, Trier, Max Planck Strasse 17, 54296 Trier, Germany, Institute of Pathology, University of Heidelberg, Im Neuenheimer Feld 224, 69120 Heidelberg, Germany. Electronic address: remi.longuespee@med.uni-heidelberg.de.
[1] Rinaldi, F., Brunetti, E., Neumayr, A., Maestri, M., Goblirsch, S., Tamarozzi, F., Cystic echinococcosis of the liver: a primer for hepatologists. World J. Hepatol. 6:5 (2014), 293–305.
[2] Pakala, T., Molina, M., Wu, G.Y., Hepatic echinococcal cysts: a review. J. clin. Transl. Hepatol. 4:1 (2016), 39–46.
[3] Group, W.H.O.I.W., International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Trop. 85:2 (2003), 253–261.
[4] Zhang, W., Wen, H., Li, J., Lin, R., McManus, D.P., Immunology and immunodiagnosis of cystic echinococcosis: an update. Clin. Dev. Immunol., 2012, 2012, 101895.
[5] Insabato, L., Marino, G., Fazioli, F., Iacono, V., Mascolo, M., Palombini, L., Primary intramuscular infestation of Echinococcus granulosus misdiagnosed as a soft tissue tumor: a case report. Acta Cytol. 51:4 (2007), 631–633.
[6] Secer, H.I., Anik, I., Celik, E., Daneyemez, M.K., Gonul, E., Spinal hydatid cyst mimicking arachnoid cyst on magnetic resonance imaging. J. Spinal Cord Med. 31:1 (2008), 106–108.
[7] Stojkovic, M., Mickan, C., Weber, T.F., Junghanss, T., Pitfalls in diagnosis and treatment of alveolar echinococcosis: a sentinel case series. BMJ Open Gastroenterol., 2(1), 2015, e000036.
[8] Cobanoglu, U., Sayir, F., Mergan, D., Diagnostic dilemma: analysis of 11 cases of hydatid disease. Turkiye parazitolojii dergisi/Turkiye Parazitoloji Dernegi = Acta parasitologica Turcica/Turkish Soc. Parasitol. 35:3 (2011), 164–168.
[9] Adas, G., Karatepe, O., Altiok, M., Battal, M., Bender, O., Ozcan, D., Karahan, S., Diagnostic problems with parasitic and non-parasitic splenic cysts. BMC Surg., 9, 2009, 9.
[10] Rostami, S., Shariat Torbaghan, S., Dabiri, S., Babaei, Z., Ali Mohammadi, M., Sharbatkhori, M., Fasihi Harandi, M., Genetic characterization of Echinococcus granulosus from a large number of formalin-fixed, paraffin-embedded tissue samples of human isolates in Iran. Am. J. Trop. Med. Hyg. 92:3 (2015), 588–594.
[11] Spotin, A., Mahami-Oskouei, M.F., Harandi, M., Baratchian, A., Bordbar, E., Ebrahimi, S., Genetic variability of Echinococcus granulosus complex in various geographical populations of Iran inferred by mitochondrial DNA sequences. Acta Trop. 165 (2017), 10–16.
[12] Dos Santos, G.B., Monteiro, K.M., da Silva, E.D., Battistella, M.E., Ferreira, H.B., Zaha, A., Excretory/secretory products in the Echinococcus granulosus metacestode: is the intermediate host complacent with infection caused by the larval form of the parasite?. Int. J. Parasitol. 46:13–14 (2016), 843–856.
[13] Hidalgo, C., Garcia, M.P., Stoore, C., Ramirez, J.P., Monteiro, K.M., Hellman, U., Zaha, A., Ferreira, H.B., Galanti, N., Landerer, E., Paredes, R., Proteomics analysis of Echinococcus granulosus protoscolex stage. Vet. Parasitol. 218 (2016), 43–45.
[14] Lorenzatto, K.R., Kim, K., Ntai, I., Paludo, G.P., Camargo de Lima, J., Thomas, P.M., Kelleher, N.L., Ferreira, H.B., Top down proteomics reveals mature proteoforms expressed in subcellular fractions of the echinococcus granulosus preadult stage. J. Proteome Res. 14:11 (2015), 4805–4814.
[15] Ahn, C.S., Han, X., Bae, Y.A., Ma, X., Kim, J.T., Cai, H., Yang, H.J., Kang, I., Wang, H., Kong, Y., Alteration of immunoproteome profile of Echinococcus granulosus hydatid fluid with progression of cystic echinococcosis. Parasites Vectors, 8, 2015, 10.
[16] Cui, S.J., Xu, L.L., Zhang, T., Xu, M., Yao, J., Fang, C.Y., Feng, Z., Yang, P.Y., Hu, W., Liu, F., Proteomic characterization of larval and adult developmental stages in Echinococcus granulosus reveals novel insight into host-parasite interactions. J. Proteom. 84 (2013), 158–175.
[17] Siracusano, A., Delunardo, F., Teggi, A., Ortona, E., Host-parasite relationship in cystic echinococcosis: an evolving story. Clin. Dev. Immunol., 2012, 2012, 639362.
[18] Aziz, A., Zhang, W., Li, J., Loukas, A., McManus, D.P., Mulvenna, J., Proteomic characterisation of Echinococcus granulosus hydatid cyst fluid from sheep, cattle and humans. J. Proteom. 74:9 (2011), 1560–1572.
[19] Monteiro, K.M., de Carvalho, M.O., Zaha, A., Ferreira, H.B., Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics 10:10 (2010), 1985–1999.
[20] Chemale, G., van Rossum, A.J., Jefferies, J.R., Barrett, J., Brophy, P.M., Ferreira, H.B., Zaha, A., Proteomic analysis of the larval stage of the parasite Echinococcus granulosus: causative agent of cystic hydatid disease. Proteomics 3:8 (2003), 1633–1636.
[21] Longuespee, R., Alberts, D., Pottier, C., Smargiasso, N., Mazzucchelli, G., Baiwir, D., Kriegsmann, M., Herfs, M., Kriegsmann, J., Delvenne, P., De Pauw, E., A laser microdissection-based workflow for FFPE tissue microproteomics: important considerations for small sample processing. Methods 104 (2016), 154–162.
[22] Kriegsmann, M., Casadonte, R., Kriegsmann, J., Dienemann, H., Schirmacher, P., Kobarg, J.H., Schwamborn, K., Stenzinger, A., Warth, A., Weichert, W., Reliable entity subtyping in non-small cell lung cancer by MALDI imaging mass spectrometry on formalin-fixed paraffin-embedded tissue specimens. Mol. Cell. Proteom. 15:10 (2016), 3081–3089.
[23] Longuespee, R., Gagnon, H., Boyon, C., Strupat, K., Dauly, C., Kerdraon, O., Ighodaro, A., Desmons, A., Dupuis, J., Wisztorski, M., Vinatier, D., Fournier, I., Day, R., Salzet, M., Proteomic analyses of serous and endometrioid epithelial ovarian cancers – cases studies – molecular insights of a possible histological etiology of serous ovarian cancer. Proteom. Clin. Appl. 7:5–6 (2013), 337–354.
[24] Casadonte, R., Caprioli, R.M., Proteomic analysis of formalin-fixed paraffin-embedded tissue by MALDI imaging mass spectrometry. Nat. Protoc. 6:11 (2011), 1695–1709.
[25] Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., Harris, M.A., Hill, D.P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J.C., Richardson, J.E., Ringwald, M., Rubin, G.M., Sherlock, G., Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25:1 (2000), 25–29.
[26] Brehm, K., Spiliotis, M., Zavala-Gongora, R., Konrad, C., Frosch, M., The molecular mechanisms of larval cestode development: first steps into an unknown world. Parasitol. Int.(55 Suppl), 2006, S15–21.
[27] Kriegsmann, J., Kriegsmann, M., Casadonte, R., MALDI TOF imaging mass spectrometry in clinical pathology: a valuable tool for cancer diagnostics (review). Int. J. Oncol. 46:3 (2015), 893–906.
[28] Sjostrom, M., Ice crystal growth in skeletal muscle fibres. J. Microsc. 105:1 (1975), 67–80.
[29] Christensen, A.K., Frozen thin sections of fresh tissue for electron microscopy, with a description of pancreas and liver. J. Cell Biol. 51:3 (1971), 772–804.
[30] Appleton, T.C., A cryostat approach to ultrathin dry frozen sections for electron microscopy: a morphological and x-ray analytical study. J. Microsc. 100:1 (1974), 49–74.
[31] Gustafsson, O.J., Arentz, G., Hoffmann, P., Proteomic developments in the analysis of formalin-fixed tissue. Biochim. Biophys. Acta 1854:6 (2015), 559–580.
[32] Chiquet-Ehrismann, R., Chiquet, M., Tenascins: regulation and putative functions during pathological stress. J. Pathol. 200:4 (2003), 488–499.
[33] Longuespee, R., Casadonte, R., Kriegsmann, M., Pottier, C., Picard de Muller, G., Delvenne, P., Kriegsmann, J., De Pauw, E., MALDI mass spectrometry imaging: a cutting-edge tool for fundamental and clinical histopathology. Proteom. Clin. Appl. 10:7 (2016), 701–719.
[34] Kriegsmann, M., Wandernoth, P., Lisenko, K., Casadonte, R., Longuespée, R., Arens, N., Kriegsmann, J., Detection of HPV subtypes by mass spectrometry in FFPE tissue specimens: a reliable tool for routine diagnostics. J. Clin. Pathol., 2016 in press.