CBMA

Fungi have many precious talents: they decompose organic matter, are the source of antibiotics and play importante roles in the production of bread and beer, are vital symbiosis partners, and are exploited in many biotechnological applications. But there’s also a dark side: they are responsible for many devastating infections, not only in crop plants but also in animals, including humans. Candida yeasts are among the major fungal pathogens in humans.

My main research areas are:

1-   fungal diagnosis and identification: applying and developing new molecular techniques for the identification of human fungal pathogens and epidemiology studies.

Were developed new microsatellite markers for differentiation of C. albicans and C. parapsilosis isolates (Sampaio et al. 2003, 2005, Sabino el al. 2010) and the differentiation of Sporothrix spp species (Oliveira et al. 2012). These and other markers have been used in the study of fungal epidemiology in Portugal (Correia et al. 2004, Sabino et al. 2010). From these studies we have identified and described a new fungal species, Candida bracarensis (Correia et al. 2006).

Since Candida and Aspergillus species are the most frequently isolated fungal pathogens in Europe we have developed a new multiplex diagnostic method for the identification of the most clinically important species: C. albicans, C. parapsilosis, C. glabrata, C. krusei, C. tropicalis, A. fumigatus, A. flavus, A. terreus and A. niger.

2-   microbial pathogenesis and host response: using in vitro cell cultures and in vivo of models to identify and study virulence factors and molecular mechanisms involved in host-fungus interaction.

Microorganisms evolved mechanisms for increasing genetic variations in loci that are involved in critical interaction with the host. In Candida albicans one of those genes is CaRLM1. The role of CaRLM1, a putative transcription factor, was evaluated and we showed that CaRLM1 is required for C. albicans cell wall biogenesis and virulence (Delgado-Silva et al. 2014). Currently, we are determining the effect of different carbon sources in the expression of these genes and the consequent cell surface changes.

In vivo and in vitro studies showed that adaptation not always involve trough increasing the virulence status. We showed a virulence decrease phenotype in Candida albicans variants of the same strain isolated from an immunocompromised patient with recurrent blood stream infection (Sampaio et al. 2010). Sequencing of these isolates are underway to evaluate genetic and genomic changes that may be associated with phenotypic heterogeneity responsible for the decreased virulence.

3-    developing of a liposomal nanocarrier as a delivery system for immunoprotective strategies against Candida albicans infections

More recently, we developed and Characterized a delivery systems based on cationic liposomes loaded with C. albicans cell wall surface antigenic proteins (Carneiro et al. 2015). We showed that Immunization of BALB/c mice with these DODAB:MO liposomes have a potent adjuvant effect and induced  antibody and T lymphocyte responses towards associated antigens that protected mice against a lethal systemic infection (Carneiro et al. 2016). Heterologous expression of the proteins that induced protection is underway to develop a more efficient vaccine against Candida albicans as well as the determination if this system may also induce convergent immunity, conferring protection towards a non-target organism.

• Carneiro C; Correia A; Lima T; Vilanova M; Pais C; Gomes AC; M. Real Oliveira CDE; Sampaio P. 2016. Protective effect of antigen delivery using monoolein-based liposomes in experimental hematogenously disseminated candidiasis. Acta Biomaterialia DOI 10.1016/j.actbio.2016.05.001.

• Carneiro C, Correia A, Collins T, Vilanova M, Pais C, Gomes AC, Real Oliveira ME, Sampaio P. 2015. DODAB:monoolein liposomes containing Candida albicans cell wall surface proteins: a novel adjuvant and delivery system. Eur J Pharm Biopharm. 89:190-200. doi: 10.1016/j.ejpb.2014.11.028.

• Carneiro C, Vaz C, Carvalho-Pereira J, Pais C, Sampaio P. 2014. A new method for yeast phagocytosis analysis by flow cytometry. J Microbiol Methods 101:56-62.
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• Correia A, Sampaio P, James S, and Pais C. 2006. Candida bracarensis sp. nov. a novel anamorphic yeast species phenotypically similar to Candida glabrata. International Journal of Systematic and Evolutionary Microbiology 56:313-317.
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• Correia A., Sampaio P., Almeida J. and Pais C. 2004. Identification of Candida clinical isolates by PCR fingerprinting: a contribution to the study of molecular epidemiology of candidiasis in Portugal. Journal of Clinical Microbiology Microbiology 42: 5899-5903.
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• Delgado-Silva Y, Vaz C, Carvalho-Pereira J, Carneiro C, Nogueira E, Correia A, Carreto L, Silva S, Faustino A, Pais C, Oliveira R, Sampaio P. 2014. Participation of Candida albicans Transcription Factor RLM1 in Cell Wall Biogenesis and Virulence. PLoS One 23;9(1):e86270.
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• Oliveira MM, Sampaio P, Almeida-Paes RD, Pais C, Zancope-Oliveira RM. 2012. Rapid identification of Sporothrix species by T3B PCR fingerprinting. J Clin Microbiol. 50:2159-62.
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• Sabino R, Sampaio P, Rosado L, Graça M, Stevens D, and Pais C. 2010 New microsatellite markers for molecular genotyping of Candida parapsilosis sensu stricto. Journal of Clinical Microbiology 48:1677-1682.
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• Sabino R, Verissimo C, Brandao J, Alves C, Parada H, Rosado L, Paixao E, Videira Z, Tendeiro T, Sampaio P, and Pais C. 2010. Epidemiology of candidemia in oncology patients: a 6-year survey in a Portuguese central hospital. Med Mycol 5:1-10.
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• Sampaio P, Gusmão L, Correia A, Alves C, Rodrigues AG, Pina-Vaz C, Amorim A, and Pais C. 2005. New microsatellite multiplex PCR for Candida albicans strain typing reveals microevolutionary changes. Journal of Clinical Microbiology 43: 3869-3875.
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• Sampaio P, Santos M, Correia A, Amaral FE, Chavéz-Galarza J, Costa-de-Oliveira S, Castro AG, Pedrosa J, and Pais C. 2010. Virulence attenuation of Candida albicans genetic variants isolated from a patient with a recurrent bloodstream infection. PLOS One 5(4): e10155.
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• Sampaio P., Gusmão L., Alves C., Pina-Vaz C, Amorim A. and Pais C. 2003. Highly polymorphic microsatellite for identification of Candida albicans strains. Journal of Clinical Microbiology 41:552-557.
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• Vaz C, Sampaio P, Clemons KV, Huang Yc, Stevens DA and Pais C. 2011. Microsatellite multilocus genotyping clarifies the relationship of Candida parapsilosis strains involved in a neonatal intensive care unit outbreak. Diagn Microbiol Infect Dis. 71:159-162.

“Biowaste derived volatile fatty acid platform for biopolymers, bioactive compounds and chemical building blocks – VOLATILE. H2020-NMBP-BIO-2016. Project number: 720777.

Innovative green products and processes to promote Agri-Food BioEconomy - EcoAgriFood. N2020- NORTE-01-0145-FEDER-000009 

Cetaceans as marine ecosystem health sentinels – CETSENSI (RECI/AAG-GLO/0470/2012).  FCT financed project. Coordination: Catarina Eira, Universidade de Aveiro. Coordinator at the Universidade do Minho.

Biotransformation of by-products from fruit and vegetable processing industry into valuable bioproducts – TRANSBIO (Grant agreement no: 289603).Financed in the scope of  the 7th framework programme EU, started on December  2011. Includes 16 participants, including laboratories, research centres and companies, from Spain, Portugal, Germany, Belgium, Italy, Romania, Argentina, Costa Rica and Mexico. Coordination: Thomas Dietrich from Fundacion Tecnalia Research & Innovation, Spain. Principal investigator of the portuguese team. 

Mechanisms of Candida glabrata biofilms tolerance to antifungal agents (PTDC/SAU-MIC/119069/2010). Projeto financiado pela FCT, com início em 2012. Coordenação de Mariana Rangel Henriques, Universidade do Minho. Integra a equipa de investigação.

Implementation of a Nacional Facility for DNA Microarrays: Phase II (PTDC/BIA-BCM/64745/2006).

Rede iberoamericana de diagnóstico molecular de las micosis sistémicas y oportunistas. (Red 208RT0347 da CYTED).

Immunobiological studies of Candida albicans recombinant secreted aspartic proteinases and their use as target antigens for vaccination against systemic candidiasis (POCI/SAU-IMI/58014/2004).

Carneiro C, Correia A, Collins T, Vilanova M, Pais C, Gomes AC, Real Oliveira ME, Sampaio P. 2015. DODAB:monoolein liposomes containing Candida albicans cell wall surface proteins: a novel adjuvant and delivery system. Eur J Pharm Biopharm. 89:190-200. doi: 10.1016/j.ejpb.2014.11.028.

V. Chillemi · C. Lo Passo · A. D. van Diepeningen · S. Rharmitt · D. Delfino · A. Cascio · N. E. Nnadi · B. D. Cilo · P. Sampaio · H.-J. Tietz · J. Pemán · G. Criseo · O. Romeo · F. Scordino. 2016. Multilocus microsatellite analysis of European and African Candida glabrata isolates. European Journal of Clinical. DOI 10.1007/s10096-016-2610-3.

J. Borges, D. Costa, E. Antunes, C. Lopes, M.S. Rodrigues, M. Apreutesei, E. Alves, N.P. Barradas, P. Pedrosa, C. Moura, L. Cunha, T. Polcar, F. Vaz, P. Sampaio. 2015.Biological behaviour of thin films consisting of Au nanoparticles dispersed in a TiO2 dielectric matrix. DOI:10.1016/j.vacuum.2015.03.036

Sabino R, Sampaio P, Rosado L, Videira Z, Grenouillet F, Pais C. 2015. Analysis of clinical and environmental Candida parapsilosis isolates by microsatellite genotyping-a tool for hospital infection surveillance. Clin Microbiol Infect. 21(10) doi: 10.1016/j.cmi.2015.06.001.

Sandra Mota · Rosana Alves · Catarina Carneiro · Sónia Silva · Alistair J Brown · Fabian Istel · Karl Kuchler · Paula Sampaio · Margarida Casal · Mariana Henriques · Sandra Paiva 2015· Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate. Frontiers in Microbiology. 6:919

Irinyi et al. 2015. International Society of Human and Animal Mycology (ISHAM)-ITS reference DNA barcoding database - the quality controlled standard tool for routine identification of human and animal pathogenic fungi. Med Mycol. 53:313-37

Oliveira, Manoel; Franco-Duarte, Ricardo; Romeo, Orazio; Pais, Célia; Criseo, Giuseppe; Sampaio, Paula; Zancope-Oliveira, Rosely. 2015. Evaluation of T3B fingerprinting for identification of clinical and environmental Sporothrix species. FEMS Microbiol Lett. 362(6).

Joana Carvalho-Pereira, Catarina Vaz, Catarina Carneiro, Célia Pais, Paula Sampaio. 2015. Genetic Variability of Candida albicans Sap8 Propeptide in Isolates from Different Types of Infection. BioMed Research International 01/2015; 2015:1-8. DOI: 10.1155/2015/148343

Carneiro C, Correia A, Collins T, Vilanova M, Pais C, Gomes AC, Real Oliveira ME, Sampaio P. 2015. DODAB:monoolein liposomes containing Candida albicans cell wall surface proteins: a novel adjuvant and delivery system. Eur J Pharm Biopharm. 89:190-200, doi: 10.1016/j.ejpb.2014.11.028.

Barbedo LS, Vaz C, Pais C, Figueiredo-Carvalho MH, Muniz Mde M, Zancope-Oliveira RM, and Sampaio P. 2014. Different scenarios for Candida parapsilosis fungemia reveal high numbers of mixed C. parapsilosis and C. orthopsilosis infections. J Med Microbiol. 64:7-17, doi: 10.1099/jmm.0.080655-0.

Catarina Carneiro, Catarina Vaz, Joana Carvalho-Pereira, Célia Pais, and Paula Sampaio. A new method for yeast phagocytosis analysis by flow cytometry. Journal of Microbiological Methods 101: 56-61

Yolanda Delgado-Silva, Eugénia Nogueira, Catarina Vaz, Catarina Carneiro, Joana Carvalho-Pereira, Alexandra Correia, Laura Carreto, Sónia Silva, Augusto Faustino, Célia Pais, Rui Oliveira and Paula Sampaio.2014. Participation of Candida albicans transcription factor RLM1 in cell wall biogenesis and virulence. PLoS ONE 9(1): e86270. doi:10.1371/journal.pone.0086270

Manoel Marques Evangelista de Oliveira, Cristina Veríssimo, Raquel Sabino, Rosely Maria Zancopé-Oliveira, Paula Sampaio and Célia Pais. 2014. First autochthone case of sporotrichosis by Sporothrix globosa in Portugal. Diagnostic Microbiology & Infectious Disease 78:388-390.

Reginaldo Lima-Neto, Cledir Santos, Nelson Lima, Paula Sampaio, Célia Pais and Rejane P. Neves 2013. Application of MALDI-TOF MS for requalification of a Candida clinical isolates culture collection. Brazilian Journal of Microbiology (Accepted)

Puinhas A, Sampaio P, Castanheira EM, Real Oliveira ME, Lira M. 2013. Comparison of IgA, TNF-a and surface tension of the tear film in two different times of the day. Cont Lens Anterior Eye. 36:140-145.

Manoel Marques Evangelista de Oliveira; Paula Sampaio, Rodrigo de Almeida-Paes; Célia Pais and Rosely Maria Zancope-Oliveira. 2012. Rapid identification of Sporothrix species by T3B PCR fingerprinting. J Clin Microbiol 50:2159-2162. 

SABINO R, SAMPAIO P, CARNEIRO C, ROSADO L, PAIS C. 2011. Isolates from hospital environments are the most virulent of the Candida parapsilosis complex. BMC Microbiology. 11:180-190. 

SANTOS C, LIMA N; SAMPAIO P, PAIS C. 2011. Matrix-assisted laser desorption/ionization time-of-flight intact cell mass spectrometry (MALDI-TOF-ICMS) to detect emerging pathogenic Candida species. Diagn Microbiol Infect Dis. 71:304-308. 

VAZ C, SAMPAIO P, CLEMONS KV, HUANG YC, STEVENS DA and PAIS C.2011. Microsatellite multilocus genotyping clarifies the relationship of Candida parapsilosis strains involved in a neonatal intensive care unit outbreak. Diagn Microbiol Infect Dis. 71:159-162. 

FERREIRA SA; PEREIRA P; SAMPAIO P, COUTINHO JP and GAMA FM. 2011 Supramolecular assembled nanogel made of mannan. J Colloid Interface Sci. 361:97-108

Costa-de-Oliveira S, Sousa I, Correia A, Sampaio P, Pais C, Gonçalves Rodrigues A, Pina-Vaz C. 2010. Genetic relatedness and antifungal susceptibility profile of Candida albicans isolates from fungaemia patients. Med Mycol. Aug 25

Correia A, Lermann U, Teixeira L, Cerca F, Botelho S, Gil da Costa RM, Sampaio P, Gartner F, Morschhaeuser J, Vilanova M, and Pais C. 2010. Limited role of secreted aspartyl proteinase Sap 1-6 in Candida albicans virulence and host immune response in murine hematogenously disseminated candidiasis Infection and Immunity 78:4839-4849.

Garcia-Hermoso, D., D.M. Maccallum, T.J. Lott, P. Sampaio, M.J. Buitrago Serna, F. Grenouillet, C.H. Klaassen, and S. Bretagne. 2010. A Multicenter Collaborative Study for the Standardization of Candida albicans Genotyping using a Polymorphic Microsatellite Marker. J Clin Microbiol. 8:2578-2581

CHAVÉZ-GALARZA J, PAIS C, AND SAMPAIO P. 2010. Microsatellite typing identifies the major clades of the human pathogen Candida albicans. Infection, Genetics and Evolution. 10:697-702.

Sabino R, Sampaio P, Rosado L, Graça M, Stevens D and Pais C. 2010 New microsatellite markers for molecular genotyping of Candida parapsilosis sensu strictum. Journal of Clinical Microbiology, 48:1677-1682.

Sampaio P, Santos M, Correia A, F. Amaral FE, Chavéz-Galarza J, Costa-de-Oliveira S, Castro AG, Pedrosa J and Pais C. 2010. Virulence attenuation of Candida albicans genetic variants isolated from a patient with a recurrent bloodstream infection.. PLoS One. 5(4): e10155.

Sabino R, Verissimo C, Brandao J, Alves C, Parada H, Rosado L, Paixao E, Videira Z, Tendeiro T, Sampaio P, Pais C. 2010. Epidemiology of candidemia in oncology patients: a 6-year survey in a Portuguese central hospital. Med Mycol 5:1-10.

Sampaio P, E. Nogueira, A. Sá Loureiro, Y. Delgado-Silva, A. Correia and C. Pais 2009. Increased number of glutamine repeats in the C- terminal of Candida albicans Rlm1p enhances the resistance to stress agents. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology. 96:395-404


CORREIA A., SAMPAIO P., JAMES S. and PAIS C. 2006. Candida bracarensis sp. nov. a novel anamorphic yeast species phenotypically similar to Candida glabrata. International Journal of Systematic and Evolutionary Microbiology 56:313-317.

SAMPAIO P., GUSMÃO L., CORREIA, A., ALVES C., RODRIGUES, A. G., PINA-VAZ C, AMORIM A. and PAIS C. 2005. New microsatellite multiplex PCR for Candida albicans strain typing reveals microevolutionary changes. Journal of Clinical Microbiology 43: 3869-3875.

CORREIA A., P. SAMPAIO P., and C. PAIS, 2004 Identification of Candida clinical isolates by PCR fingerprinting: a contribution to the study of molecular epidemiology of candidiasis in Portugal. Journal of Clinical Microbiology 42:5899-5903.

SAMPAIO P., GUSMÃO L., ALVES C., PINA-VAZ C, AMORIM A. and PAIS C. 2003. A highly polymorphic microsatellite for the identification of Candida albicans strains. Journal of Clinical Microbiology 41: 552-557. 

Carneiro C, Correia A, Lima T, Vilanova M, Pais C, Gomes AC, Real Oliveira MECD, Sampaio P. DODAB: Monolein based liposomes as novel nanocarriers for vaccine design against Candida albicans infections. MEDICINE: 95 Nº10. Two Commerce Sq, 2001 Market st, Philadelphia, pa 19103 usa: Lippincott Williams & Wilkins, 2016.

Sabino R, Rosado L, Sampaio P, and Pais C. 2009. Response to macrophage infection by Candida parapsilosis sensu stricto isolates with different multilocus genotypes. Mycoses; 52 (Suppl. 1): 106-107.

Sabino R, Veríssimo C, Brandão J, Alves C, Alves P, Parada H, Rosado L, Videira Z, Tendeiro T, Sampaio P, and Pais C. 2007. Candida bloodstream infections in oncological patients: a 2-year survey in a Portuguese central hospital. Journal of Chemotherapy 19: 85.

Santos M, Sampaio P, Correia A, Castro G, Pedrosa J, and Pais C. 2007. Recurrent Candida albicans infections: is the reinfecting strain presenting loss of heterozygocity less virulent? Journal of Chemotherapy 19: 96.

SAMPAIO P., GUSMÃO L., ALVES C., PINA-VAZ C, AMORIM A. and PAIS C. 2003. Highly polymorphic new microsatellites for molecular typing of Candida albicans strains. Infection, genetics and Evolution. 85: 87. 

 Alexandra Correia, Paula Sampaio, Manuel Vilanova, Célia Pais. 2016. Candida albicans: Clinical Relevance, Pathogenesis, and Host Immunity. Human Emerging and Re-emerging Infections: Viral and Parasitic Infections, Volume II. Pag. 929-952. John Wiley & Sons, Inc.

C Pais, R Franco-Duarte, P Sampaio, J Wildner, A Carolas, D Figueira, BS Ferreira. 2016 Production of Dicarboxylic Acid Platform Chemicals Using Yeasts: Focus on Succinic Acid- In: Biotransformation of Agricultural Waste and By-Products: The Food, Feed, Fibre, Fuel (4F) Economy (2016) Elsevier pp 237-269.

Célia Pais and Paula Sampaio. 2014. Epidemiology of Invasive Candidiasis and Challenges for the Mycology Laboratory: Specificities of Candida glabrata. Current Clinical Microbiology Reports. Volume 1, Issue 1-2, pp 1-9.

 PhD

Joana Pereira com o tema "Development of a new antifungal strategy based on encapsulated antimicrobial peptides: evaluation of the mechanism of action and in vivo efficiency on Candida systemic infections" Bolseira FCT desde 2016. 

Catarina Carneiro sob o tema “Cationic Liposomes as antigenic delivery systems: development of an immunoprotective strategy against fungal infections”. Bolseira FCT. Terminou 2015

Co-supervisor of Manoel Marques Evangelista de Oliveira with the thesis title “Desenvolvimento de ferramentas moleculares para a diferenciação de espécies do complexo Sporothrix”. (finished 2013). PhD grant from CAPES, Brasil. Now he is a senior investigator at the Institute of Clinical Research Evandro Chagas, Fundação Oswaldo Cruz, Brasil.Terminou em 2014.

Yolanda Bedsabé Delgado Silva sob o tema “Involvement of CaRLM1 in Candida albicans virulence”. Bolseira ALBAN terminou 2013.

 MCs

Augusto Alexandre Costa Barbosa “Development of a novel recombinant subunit antigen as a vaccination target against candidiasis: Cht3 and Sap2 from Candida albicans”

João Pacheco "The impact of carbon source in Candida albicans virulence: participation of RLM1 in pathogen host interaction" (Finished  2015)

Catarina Vaz sob o tema “Characterization of Liposomes as Antigenic Delivery Systems: Evaluation of its Candidacidal Ability. (Finished  2012)

Joana Pereira with the thesis title “Desenvolvimento de Biomarcadores para o Diagnóstico de Espécies Patogénicas de Candida spp” (finished 2012)

Moisés Tavares with the thesis title "O papel do ar e água ambientais como veículos de transmissão de infecções fúngicas no Hospital Agostinho Neto, Cidade da Praia, Cabo Verde" (finished 2012). 

Ana Filipa Vale with the thesis title “Diversidade fúngica do guano em Portugal” (finished 2012)

Julio César Chávez Galarza sob o tema “Phylogenetic Relationship of the most Common Pathogenic Candida Species Inferred by Sequence Analysis of Nuclear Genes”. Terminou 2009.

Eugénia Sofia da Costa Nogueira sob o tema “Estudo da função do factor de transcrição rlm1 em Candida albicans”. Terminou em 2008.

Marlene Elisabete Moreira dos Santos sob o tema “Virulence studies of Candida albicans recurrent isolates in a mouse model of disseminated infection”. Terminou 2008.

Inês Cátia Dinis de Sousa sob o tema “Description and characterization of a microsatellite in Candida albicans IFF8 gene”. Terminou em 2007.