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Post-translational modifications in Chagas Disease biological processes and diagnostics: novel methodological approaches and biological applications

Abstract

Chagas Disease, caused by the protozoan parasite T. cruzi, is a neglected disease, which can lead to Cardiomyopathy, neurological complications and megaviscera. Over 100 years after its description, this disease affects 8 million people and most of them do not know that they are infected. Although endemic in the South America, it has been recognized a worldwide public health problem due to global population migration. Despite the great efforts to control T. cruzi transmission and introduce novel therapeutic options, one of the unmet needs is the development of novel sensitive and specific diagnostic markers for treatment response and disease progression. Moreover, a better understanding of the T. cruzi-host interaction will aid in prioritize novel therapeutic targets. This project is divided in three parts: 1) analytical method development for post-translational modifications (PTMs); 2) elucidation of the role of protein glycosylation and arginylation in the T. cruzi-host interaction and 3) biomarker discovery for Chagas Disease. The development of novel analytical methods for PTMs analysis will offer the possibility to detect protein modifications in complex biological systems with high accuracy and sensitivity. In particular, the identification of protein glycosylation of different T. cruzi strains belonging to the seven DTUs will be evaluated and associated to the expression of specific glycosyltransferases. The large-scale analysis of the cell surface glycoproteome and glycome combined with functional assays will be used as a molecular determinant to link the T. cruzi glycosylation enzymes expression and phenotype. The characterization of protein arginylation in T. cruzi and the Tc-Ate1 enzyme involved in this process will allow us to understand the role of this poorly explored PTM in Chagas Disease biology. The third part of the project will be focused on implementing a diagnostic platform for urinary protein biomarker discovery in Chagas Disease. (AU)

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Scientific publications (27)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
KAWAHARA, REBECA; CHERNYKH, ANASTASIA; ALAGESAN, KATHIRVEL; BERN, MARSHALL; CAO, WEIQIAN; CHALKLEY, ROBERT J.; CHENG, KAI; CHOO, MATTHEW S.; EDWARDS, NATHAN; GOLDMAN, RADOSLAV; HOFFMANN, MARCUS; HU, YINGWEI; HUANG, YIFAN; KIM, JIN YOUNG; KLETTER, DORON; LIQUET, BENOIT; LIU, MINGQI; MECHREF, YEHIA; MENG, BO; NEELAMEGHAM, SRIRAM; NGUYEN-KHUONG, TERRY; NILSSON, JONAS; PAP, ADAM; PARK, GUN WOOK; PARKER, BENJAMIN L.; PEGG, CASSANDRA L.; PENNINGER, JOSEF M.; PHUNG, TOAN K.; PIOCH, MARKUS; RAPP, ERDMANN; SAKALLI, ENES; SANDA, MILOSLAV; SCHULZ, BENJAMIN L.; SCOTT, NICHOLLAS E.; SOFRONOV, GEORGY; STADLMANN, JOHANNES; VAKHRUSHEV, SERGEY Y.; WOO, CHRISTINA M.; WU, HUNG-YI; YANG, PENGYUAN; YING, WANTAO; ZHANG, HUI; ZHANG, YONG; ZHAO, JINGFU; ZAIA, JOSEPH; HASLAM, STUART M.; PALMISANO, GIUSEPPE; YOO, JONG SHIN; LARSON, GORAN; KHOO, KAI-HOOI; MEDZIHRADSZKY, KATALIN F.; KOLARICH, DANIEL; PACKER, NICOLLE H.; THAYSEN-ANDERSEN, MORTEN. Community evaluation of glycoproteomics informatics solutions reveals high-performance search strategies for serum glycopeptide analysis. NATURE METHODS, v. 18, n. 11, p. 1304+, NOV 2021. Web of Science Citations: 2.
SOUZA JUNIOR, DOUGLAS RICARDO; MARTINS SILVA, AMANDA RIBEIRO; ROSA-FERNANDES, LIVIA; REIS, LORENNA ROCHA; ALEXANDRIA, GABRIELLY; BHOSALE, SANTOSH D.; GHILARDI, FABIO DE ROSE; DALCOQUIO, TALIA FALCAO; BERTOLIN, ADRIADNE JUSTI; NICOLAU, JOSE CARLOS; MARINHO, CLAUDIO R. F.; WRENGER, CARSTEN; LARSEN, MARTIN R.; SICILIANO, RINALDO FOCACCIA; DI MASCIO, PAOLO; PALMISANO, GIUSEPPE; RONSEIN, GRAZIELLA ELIZA. HDL proteome remodeling associates with COVID-19 severity. JOURNAL OF CLINICAL LIPIDOLOGY, v. 15, n. 6, p. 796-804, NOV-DEC 2021. Web of Science Citations: 0.
COUTINHO, JOAO V. P.; ROSA-FERNANDES, LIVIA; MULE, SIMON NGAO; DE OLIVEIRA, GILBERTO SANTOS; MANCHOLA, NUBIA CAROLINA; SANTIAGO, VERONICA FEIJOLI; COLLI, WALTER; WRENGER, CARSTEN; MANSO ALVES, MARIA JULIA; PALMISANO, GIUSEPPE. The thermal proteome stability profile of Trypanosoma cruzi in epimastigote and trypomastigote life stages. JOURNAL OF PROTEOMICS, v. 248, SEP 30 2021. Web of Science Citations: 0.
MULE, SIMON NGAO; ROSA-FERNANDES, LIVIA; COUTINHO, JOAO V. P.; GOMES, VINICIUS DE MORAIS; MACEDO-DA-SILVA, JANAINA; SANTIAGO, VERONICA FEIJOLI; QUINA, DANIEL; DE OLIVEIRA, GILBERTO SANTOS; THAYSEN-ANDERSEN, MORTEN; LARSEN, MARTIN R.; LABRIOLA, LETICIA; PALMISANO, GIUSEPPE. Systems-wide analysis of glycoprotein conformational changes by limited deglycosylation assay. JOURNAL OF PROTEOMICS, v. 248, SEP 30 2021. Web of Science Citations: 0.
MULE, SIMON NGAO; GOMES, VINICIUS DE MORAIS; WAILEMANN, ROSANGELA A. M.; MACEDO-DA-SILVA, JANAINA; ROSA-FERNANDES, LIVIA; LARSEN, MARTIN R.; LABRIOLA, LETICIA; PALMISANO, GIUSEPPE. HSPB1 influences mitochondrial respiration in ER-stressed beta cells. BIOCHIMICA ET BIOPHYSICA ACTA-PROTEINS AND PROTEOMICS, v. 1869, n. 9 SEP 2021. Web of Science Citations: 0.
LAZARI, LUCAS CARDOSO; GHILARDI, FABIO DE ROSE; ROSA-FERNANDES, LIVIA; ASSIS, DIEGO M.; NICOLAU, JOSE CARLOS; SANTIAGO, VERONICA FEIJOLI; DALCOQUIO, TALIA FALCAO; ANGELI, CLAUDIA B.; BERTOLIN, ADRIADNE JUSTI; MARINHO, CLAUDIO R. F.; WRENGER, CARSTEN; DURIGON, EDISON LUIZ; SICILIANO, RINALDO FOCACCIA; PALMISANO, GIUSEPPE. Prognostic accuracy of MALDI-TOF mass spectrometric analysis of plasma in COVID-19. LIFE SCIENCE ALLIANCE, v. 4, n. 8 AUG 2021. Web of Science Citations: 2.
CARNEIRO, ANDREIA; VIANA-GOMES, DIEGO; MACEDO-DA-SILVA, JANAINA; OLIVEIRA LIMA, GISCARD HUMBERTO; MITRI, SIMONE; ALVES, SERGIO RABELLO; KOLLIARI-TURNER, ALEXANDER; ZANOTELI, EDMAR; DE AQUINO NETO, FRANCISCO RADLER; PALMISANO, GIUSEPPE; PESQUERO, JOAO BOSCO; MOREIRA, JOSINO COSTA; PEREIRA, MARCOS DIAS. Risk factors and future directions for preventing and diagnosing exertional rhabdomyolysis. Neuromuscular Disorders, v. 31, n. 7, p. 583-595, JUL 2021. Web of Science Citations: 0.
MACEDO-DA-SILVA, JANAINA; SANTIAGO, VERONICA F.; ROSA-FERNANDES, LIVIA; MARINHO, CLAUDIO R. F.; PALMISANO, GIUSEPPE. Protein glycosylation in extracellular vesicles: Structural characterization and biological functions. Molecular Immunology, v. 135, p. 226-246, JUL 2021. Web of Science Citations: 0.
SUMAM DE OLIVEIRA, DAFFINY; KRONENBERGER, THALES; PALMISANO, GIUSEPPE; WRENGER, CARSTEN; DE SOUZA, EDMARCIA ELISA. Targeting SUMOylation in Plasmodium as a Potential Target for Malaria Therapy. FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY, v. 11, JUN 10 2021. Web of Science Citations: 0.
CAVALCANTE, TAINA; MEDEIROS, MARIANA MEDINA; MULE, SIMON NGAO; PALMISANO, GIUSEPPE; STOLF, BEATRIZ SIMONSEN. The Role of Sialic Acids in the Establishment of Infections by Pathogens, With Special Focus on Leishmania. FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY, v. 11, MAY 13 2021. Web of Science Citations: 1.
DOMBROWSKI, JAMILLE GREGORIO; BARATEIRO, ANDRE; MACHADO PEIXOTO, ERIKA PAULA; CLAUDIO DA SILVA BARROS, ANDRE BOLER; DE SOUZA, RODRIGO MEDEIROS; CLARK, TAANE GREGORY; CAMPINO, SUSANA; WRENGER, CARSTEN; WUNDERLICH, GERHARD; PALMISANO, GIUSEPPE; EPIPHANIO, SABRINA; GONCALVES, LIGIA ANTUNES; FARIAS MARINHO, CLAUDIO ROMERO. Adverse pregnancy outcomes are associated with Plasmodium vivax malaria in a prospective cohort of women from the Brazilian Amazon. PLoS Neglected Tropical Diseases, v. 15, n. 4 APR 2021. Web of Science Citations: 0.
MULE, SIMON NGAO; COSTA-MARTINS, ANDRE GUILHERME; ROSA-FERNANDES, LIVIA; DE OLIVEIRA, GILBERTO SANTOS; RODRIGUES, CARLA MONADELI F.; QUINA, DANIEL; ROSEIN, GRAZIELLA E.; GERALDES TEIXEIRA, MARTA MARIA; PALMISANO, GIUSEPPE. PhyloQuant approach provides insights into Trypanosoma cruzi evolution using a systems-wide mass spectrometry-based quantitative protein profile. COMMUNICATIONS BIOLOGY, v. 4, n. 1 MAR 11 2021. Web of Science Citations: 0.
LATROFA, MARIA STEFANIA; PALMISANO, GIUSEPPE; ANNOSCIA, GIADA; PIERRI, CIRO LEONARDO; CHANDRASHEKAR, RAMASWAMY; OTRANTO, DOMENICO. Major antigen and paramyosin proteins as candidate biomarkers for serodiagnosis of canine infection by zoonotic Onchocerca lupi. PLoS Neglected Tropical Diseases, v. 15, n. 2 FEB 2021. Web of Science Citations: 1.
MULE, S. N.; MANCHOLA, N. C.; DE OLIVEIRA, G. S.; PEREIRA, M.; MAGALHAES, R. D. M.; TEIXEIRA, A. A.; COLLI, W.; ALVES, M. J. M.; PALMISANO, G. Proteome-wide modulation of S-nitrosylation in Trypanosoma cruzi trypomastigotes upon interaction with the host extracellular matrix. JOURNAL OF PROTEOMICS, v. 231, JAN 16 2021. Web of Science Citations: 0.
GOMES, LAURA CORDEIRO; SANSON, MARINA CORDEIRO GOMES; BRAININ, PHILIP; DE MELO, MARIA DA CONCEICAO VIEIRA; DE SOUZA, RODRIGO MEDEIROS; MAZARO, JANAINA; LIMA, KARINE OLIVEIRA; RESENDE, JUNIA SILVA; VIEIRA, ISABELLE VICTORIA MARTINS; MESQUITA, EDINILSON DA SILVA; MATOS, LUAN OLIVEIRA; DUTRA, ISABELLE CAROLINE SILVA; PALMISANO, GIUSEPPE; WRENGER, CARSTEN; MARINHO, CLAUDIO ROMERO FARIAS; DA SILVA, RITA DO SOCORRO UCHOA. Levels of hepatitis B antibody titers are affected by age and doses gap time in children from a high endemic area of the western Amazon. PLoS One, v. 16, n. 7 2021. Web of Science Citations: 0.
KAWAHARA, REBECA; RECUERO, SAULO; SROUGI, MIGUEL; LEITE, KATIA R. M.; THAYSEN-ANDERSEN, MORTEN; PALMISANO, GIUSEPPE. The Complexity and Dynamics of the Tissue Glycoproteome Associated With Prostate Cancer Progression. MOLECULAR & CELLULAR PROTEOMICS, v. 20, 2021. Web of Science Citations: 3.
MARTINS, LARISSA ALMEIDA; PALMISANO, GIUSEPPE; CORTEZ, MAURO; KAWAHARA, REBECA; DE FREITAS BALANCO, JOSE MARIO; FUJITA, ANDRE; ALONSO, BEATRIZ IGLESIAS; BARROS-BATTESTI, DARCI MORAES; BRAZ, GLORIA REGINA CARDOSO; TIRLONI, LUCAS; ESTEVES, ELIANE; DAFFRE, SIRLEI; FOGACA, ANDREA CRISTINA. The intracellular bacterium Rickettsia rickettsii exerts an inhibitory effect on the apoptosis of tick cells. PARASITES & VECTORS, v. 13, n. 1 DEC 1 2020. Web of Science Citations: 0.
RODRIGUES, MARIANE A. D.; PIMENTA, MARCELA V.; COSTA, IRIS M.; ZENATTI, PRISCILA P.; MIGITA, NATACHA A.; YUNES, JOSE A.; RANGEL-YAGUI, CARLOTA O.; DE SA, MATHEUS M.; PESSOA, ADALBERTO; COSTA-SILVA, TALES A.; TOYAMA, MARCOS H.; BREYER, CARLOS A.; DE OLIVEIRA, MARCOS A.; SANTIAGO, VERONICA F.; PALMISANO, GIUSEPPE; BARBOSA, CHRISTIANO M. V.; HEBEDA, CRISTINA B.; FARSKY, SANDRA H. P.; MONTEIRO, GISELE. Influence of lysosomal protease sensitivity in the immunogenicity of the antitumor biopharmaceutical asparaginase. Biochemical Pharmacology, v. 182, DEC 2020. Web of Science Citations: 0.
ROSA-FERNANDES, LIVIA; BARBOSA, RAQUEL HORA; DOS SANTOS, MARIA LUIZA B.; ANGELI, CLAUDIA B.; SILVA, THIAGO P.; MELO, ROSSANA C. N.; DE OLIVEIRA, GILBERTO SANTOS; LEMOS, BERNARDO; VAN EYK, JENNIFER E.; LARSEN, MARTIN R.; CARDOSO, CLAUDETE ARAUJO; PALMISANO, GIUSEPPE. Cellular Imprinting Proteomics Assay: A Novel Method for Detection of Neural and Ocular Disorders Applied to Congenital Zika Virus Syndrome. JOURNAL OF PROTEOME RESEARCH, v. 19, n. 11, p. 4496-4515, NOV 6 2020. Web of Science Citations: 1.
MULE, SIMON NGAO; SAAD, JOYCE SILVA; FERNANDES, LIVIA ROSA; STOLF, BEATRIZ S.; CORTEZ, MAURO; PALMISANO, GIUSEPPE. Protein glycosylation inLeishmaniaspp.. MOLECULAR OMICS, v. 16, n. 5, p. 407-424, OCT 1 2020. Web of Science Citations: 0.
GAVINHO, BRUNO; SABATKE, BRUNA; FEIJOLI, VERONICA; ROSSI, IZADORA VOLPATO; DA SILVA, JANAINA MACEDO; EVANS-OSSES, INGRID; PALMISANO, GIUSEPPE; LANGE, SIGRUN; RAMIREZ, MARCEL IVAN. Peptidylarginine Deiminase Inhibition Abolishes the Production of Large Extracellular Vesicles FromGiardia intestinalis, Affecting Host-Pathogen Interactions by Hindering Adhesion to Host Cells. FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY, v. 10, SEP 23 2020. Web of Science Citations: 1.
MISERANI MAGALHAES, RUBENS DANIEL; MATTOS, ELICIANE CEVOLANI; ROZANSKI, ANDREI; FAVORETTO GALANTE, PEDRO ALEXANDRE; PALMISANO, GIUSEPPE; CRUZ, ANGELA KAYSEL; COLLI, WALTER; CAMARGO, ANAMARIA ARANHA; MANSO ALVES, MARIA JULIA. Global changes in nitration levels and DNA binding profile of Trypanosoma cruzi histones induced by incubation with host extracellular matrix. PLoS Neglected Tropical Diseases, v. 14, n. 5 MAY 2020. Web of Science Citations: 1.
LIMA, GUILHERME MEIRA; EFFER, BRIAN; BIASOTO, HENRIQUE PELLIN; FEIJOLI, VERONICA; PESSOA, ADALBERTO; PALMISANO, GIUSEPPE; MONTEIRO, GISELE. Glycosylation of L-asparaginase from E. coli through yeast expression and site-directed mutagenesis. Biochemical Engineering Journal, v. 156, APR 15 2020. Web of Science Citations: 0.
MOREIRA, RAFAEL J.; CASTRO, ERIQUE; OLIVEIRA, TIAGO E.; BELCHIOR, THIAGO; PEIXOTO, ALBERT S.; CHAVES-FILHO, ADRIANO B.; MORENO, MAYARA F.; LIMA, JANAYNA D.; YOSHINAGA, MARCOS; MIYAMOTO, SAYURI; MORAIS, MYCHEL R. P. T.; ZORN, TELMA M. T.; COGLIATI, BRUNO; IWAI, LEO K.; PALMISANO, GIUSEPPE; CABRAL, FERNANDA J.; FESTUCCIA, WILLIAM. Lipoatrophy-Associated Insulin Resistance and Hepatic Steatosis are Attenuated by Intake of Diet Rich in Omega 3 Fatty Acids. MOLECULAR NUTRITION & FOOD RESEARCH, v. 64, n. 7 FEB 2020. Web of Science Citations: 1.
CHATTERJEE, SAYANTANI; LEE, LING Y.; KAWAHARA, REBECA; ABRAHAMS, JODIE L.; ADAMCZYK, BARBARA; ANUGRAHAM, MERRINA; ASHWOOD, CHRISTOPHER; SUMER-BAYRAKTAR, ZEYNEP; BRIGGS, MATTHEW T.; CHIK, JENNY H. L.; EVEREST-DASS, ARUN; FOERSTER, SARAH; HINNEBURG, HANNES; LEITE, KATIA R. M.; LOKE, IAN; MOGINGER, UWE; MOH, EDWARD S. X.; NAKANO, MIYAKO; RECUERO, SAULO; SETHI, MANVEEN K.; SROUGI, MIGUEL; STAVENHAGEN, KATHRIN; VENKATAKRISHNAN, VIGNESH; WONGTRAKUL-KISH, KATHERINE; DIESTEL, SIMONE; HOFFMANN, PETER; KARLSSON, NICLAS G.; KOLARICH, DANIEL; MOLLOY, MARK P.; MUDERS, MICHAEL H.; OEHLER, MARTIN K.; PACKER, NICOLLE H.; PALMISANO, GIUSEPPE; THAYSEN-ANDERSEN, MORTEN. Protein Paucimannosylation Is an Enriched N-Glycosylation Signature of Human Cancers. PROTEOMICS, v. 19, n. 21-22, SI NOV 2019. Web of Science Citations: 2.
KAWAHARA, REBECA; RECUERO, SAULO; NOGUEIRA, FABIO C. S.; DOMONT, GILBERTO B.; LEITE, KATIA R. M.; SROUGI, MIGUEL; THAYSEN-ANDERSEN, MORTEN; PALMISANO, GIUSEPPE. Tissue Proteome Signatures Associated with Five Grades of Prostate Cancer and Benign Prostatic Hyperplasia. PROTEOMICS, v. 19, n. 21-22, SI NOV 2019. Web of Science Citations: 0.
CAPELLI-PEIXOTO, JANAINA; MULE, SIMON NGAO; TANO, FABIA TOMIE; PALMISANO, GIUSEPPE; STOLF, BEATRIZ SIMONSEN. Proteomics and Leishmaniasis: Potential Clinical Applications. PROTEOMICS CLINICAL APPLICATIONS, v. 13, n. 6 AUG 2019. Web of Science Citations: 0.

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