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1. Genes, inflammatory response, tolerance, and resistance to virus infections in migratory birds, bats, and rodents

Author

Patrick Douglas Corrêa Pereira, Daniel Guerreiro Diniz, Emanuel Ramos da Costa, Nara Gyzely de Morais Magalhães, Anderson de Jesus Falcão da Silva, Jéssica Gizele Sousa Leite, Natan Ibraim Pires Almeida, Kelle de Nazaré Cunha, Mauro André Damasceno de Melo, Pedro Fernando da Costa Vasconcelos, José Antonio Picanço Diniz, Dora Brites, Daniel Clive Anthony, Cristovam Wanderley Picanço Diniz, and Cristovam Guerreiro-Diniz

Subjects
virome, disease tolerance, resistance, inflammatory response, sickness behavior, Immunologic diseases. Allergy, RC581-607
Abstract

Normally, the host immunological response to viral infection is coordinated to restore homeostasis and protect the individual from possible tissue damage. The two major approaches are adopted by the host to deal with the pathogen: resistance or tolerance. The nature of the responses often differs between species and between individuals of the same species. Resistance includes innate and adaptive immune responses to control virus replication. Disease tolerance relies on the immune response allowing the coexistence of infections in the host with minimal or no clinical signs, while maintaining sufficient viral replication for transmission. Here, we compared the virome of bats, rodents and migratory birds and the molecular mechanisms underlying symptomatic and asymptomatic disease progression. We also explore the influence of the host physiology and environmental influences on RNA virus expression and how it impacts on the whole brain transcriptome of seemingly healthy semipalmated sandpiper (Calidris pusilla) and spotted sandpiper (Actitis macularius). Three time points throughout the year were selected to understand the importance of longitudinal surveys in the characterization of the virome. We finally revisited evidence that upstream and downstream regulation of the inflammatory response is, respectively, associated with resistance and tolerance to viral infections.

Published
2023
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2. Molecular Changes in the Brain of the Wintering Calidris pusilla in the Mangroves of the Amazon River Estuary

Author

Patrick Douglas Corrêa Pereira, Ediely Pereira Henrique, Emanuel Ramos da Costa, Anderson de Jesus Falcão, Mauro André Damasceno de Melo, Maria Paula Cruz Schneider, Rommel Mario Rodriguez Burbano, Daniel Guerreiro Diniz, Nara Gyzely de Morais Magalhães, David Francis Sherry, Cristovam Wanderley Picanço Diniz, and Cristovam Guerreiro-Diniz

Subjects
brain transcriptome, migratory birds, spring migration, wintering, Calidris pusilla, Biology (General), QH301-705.5, Chemistry, QD1-999
Abstract

Migrant birds prepare differently to fly north for breeding in the spring and for the flight to lower latitudes during autumn, avoiding the cold and food shortages of the Northern Hemisphere’s harsh winter. The molecular events associated with these fundamental stages in the life history of migrants include the differential gene expression in different tissues. Semipalmated sandpipers (Calidris pusilla) are Arctic-breeding shorebirds that migrate to the coast of South America during the non-breeding season. In a previous study, we demonstrated that between the beginning and the end of the wintering period, substantial glial changes and neurogenesis occur in the brain of C. pusilla. These changes follow the epic journey of the autumn migration when a 5-day non-stop transatlantic flight towards the coast of South America and the subsequent preparation for the long-distance flight of the spring migration takes place. Here, we tested the hypothesis that the differential gene expressions observed in the brains of individuals captured in the autumn and spring windows are consistent with the previously described cellular changes. We searched for differential gene expressions in the brain of the semipalmated sandpiper, of recently arrived birds (RA) from the autumnal migration, and that of individuals in the premigratory period (PM) in the spring. All individuals were collected in the tropical coastal of northern Brazil in the mangrove region of the Amazon River estuary. We generated a de novo neurotranscriptome for C. pusilla individuals and compared the gene expressions across libraries. To that end, we mapped an RNA-Seq that reads to the C. pusilla neurotranscriptome in four brain samples of each group and found that the differential gene expressions in newly arrived and premigratory birds were related with neurogenesis, metabolic pathways (ketone body biosynthetic and the catabolic and lipid biosynthetic processes), and glial changes (astrocyte-dopaminergic neuron signaling, astrocyte differentiation, astrocyte cell migration, and astrocyte activation involved in immune response), as well as genes related to the immune response to virus infections (Type I Interferons), inflammatory cytokines (IL-6, IL-1β, TNF, and NF-κB), NLRP3 inflammasome, anti-inflammatory cytokines (IL-10), and cell death pathways (pyroptosis- and caspase-related changes).

Published
2023
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3. Microglial Morphology Across Distantly Related Species: Phylogenetic, Environmental and Age Influences on Microglia Reactivity and Surveillance States

Author

Dario Carvalho-Paulo, João Bento Torres Neto, Carlos Santos Filho, Thais Cristina Galdino de Oliveira, Aline Andrade de Sousa, Renata Rodrigues dos Reis, Zaire Alves dos Santos, Camila Mendes de Lima, Marcus Augusto de Oliveira, Nivin Mazen Said, Sinara Franco Freitas, Marcia Consentino Kronka Sosthenes, Giovanni Freitas Gomes, Ediely Pereira Henrique, Patrick Douglas Côrrea Pereira, Lucas Silva de Siqueira, Mauro André Damasceno de Melo, Cristovam Guerreiro Diniz, Nara Gyzely de Morais Magalhães, José Antonio Picanço Diniz, Pedro Fernando da Costa Vasconcelos, Daniel Guerreiro Diniz, Daniel Clive Anthony, David Francis Sherry, Dora Brites, and Cristovam Wanderley Picanço Diniz

Subjects
age and environment influence on microglia alteration, brain size and microglia response cognitive performances, Felsenstein’s independent phylogenetic contrast, microglia, mouse, bat, Immunologic diseases. Allergy, RC581-607
Abstract

Microglial immunosurveillance of the brain parenchyma to detect local perturbations in homeostasis, in all species, results in the adoption of a spectrum of morphological changes that reflect functional adaptations. Here, we review the contribution of these changes in microglia morphology in distantly related species, in homeostatic and non-homeostatic conditions, with three principal goals (1): to review the phylogenetic influences on the morphological diversity of microglia during homeostasis (2); to explore the impact of homeostatic perturbations (Dengue virus challenge) in distantly related species (Mus musculus and Callithrix penicillata) as a proxy for the differential immune response in small and large brains; and (3) to examine the influences of environmental enrichment and aging on the plasticity of the microglial morphological response following an immunological challenge (neurotropic arbovirus infection). Our findings reveal that the differences in microglia morphology across distantly related species under homeostatic condition cannot be attributed to the phylogenetic origin of the species. However, large and small brains, under similar non-homeostatic conditions, display differential microglial morphological responses, and we argue that age and environment interact to affect the microglia morphology after an immunological challenge; in particular, mice living in an enriched environment exhibit a more efficient immune response to the virus resulting in earlier removal of the virus and earlier return to the homeostatic morphological phenotype of microglia than it is observed in sedentary mice.

Published
2021
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4. Environmental Enrichment Improved Learning and Memory, Increased Telencephalic Cell Proliferation, and Induced Differential Gene Expression in Colossoma macropomum

Author

Patrick Douglas Corrêa Pereira, Ediely Pereira Henrique, Danillo Monteiro Porfírio, Caio César de Sousa Crispim, Maitê Thaís Barros Campos, Renata Melo de Oliveira, Isabella Mesquita Sfair Silva, Luma Cristina Ferreira Guerreiro, Tiago Werley Pires da Silva, Anderson de Jesus Falcão da Silva, João Batista da Silva Rosa, Dmitre Leonardo Ferreira de Azevedo, Cecília Gabriella Coutinho Lima, Cintya Castro de Abreu, Carlos Santos Filho, Domingos Luiz Wanderley Picanço Diniz, Nara Gyzely de Morais Magalhães, Cristovam Guerreiro-Diniz, Cristovam Wanderley Picanço Diniz, and Daniel Guerreiro Diniz

Subjects
environmental enrichment, spatial learning, and memory, object recognition, telencephalic and tectal cell count, neurotranscriptomics, Therapeutics. Pharmacology, RM1-950
Abstract

Fish use spatial cognition based on allocentric cues to navigate, but little is known about how environmental enrichment (EE) affects learning and memory in correlation with hematological changes or gene expression in the fish brain. Here we investigated these questions in Colossoma macropomum (Teleostei). Fish were housed for 192 days in either EE or in an impoverished environment (IE) aquarium. EE contained toys, natural plants, and a 12-h/day water stream for voluntary exercise, whereas IE had no toys, plants, or water stream. A third plus maze aquarium was used for spatial and object recognition tests. Compared with IE, the EE fish showed greater learning rates, body length, and body weight. After behavioral tests, whole brain tissue was taken, stored in RNA-later, and then homogenized for DNA sequencing after conversion of isolated RNA. To compare read mapping and gene expression profiles across libraries for neurotranscriptome differential expression, we mapped back RNA-seq reads to the C. macropomum de novo assembled transcriptome. The results showed significant differential behavior, cell counts and gene expression in EE and IE individuals. As compared with IE, we found a greater number of cells in the telencephalon of individuals maintained in EE but no significant difference in the tectum opticum, suggesting differential plasticity in these areas. A total of 107,669 transcripts were found that ultimately yielded 64 differentially expressed transcripts between IE and EE brains. Another group of adult fish growing in aquaculture conditions were either subjected to exercise using running water flow or maintained sedentary. Flow cytometry analysis of peripheral blood showed a significantly higher density of lymphocytes, and platelets but no significant differences in erythrocytes and granulocytes. Thus, under the influence of contrasting environments, our findings showed differential changes at the behavioral, cellular, and molecular levels. We propose that the differential expression of selected transcripts, number of telencephalic cell counts, learning and memory performance, and selective hematological cell changes may be part of Teleostei adaptive physiological responses triggered by EE visuospatial and somatomotor stimulation. Our findings suggest abundant differential gene expression changes depending on environment and provide a basis for exploring gene regulation mechanisms under EE in C. macropomum.

Published
2020
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5. Differential Change in Hippocampal Radial Astrocytes and Neurogenesis in Shorebirds With Contrasting Migratory Routes

Author

Camila Mendes de Lima, Patrick Douglas Corrêa Pereira, Ediely Pereira Henrique, Marcus Augusto de Oliveira, Dario Carvalho Paulo, Lucas Silva de Siqueira, Daniel Guerreiro Diniz, Diego Almeida Miranda, Mauro André Damasceno de Melo, Nara Gyzely de Morais Magalhães, David Francis Sherry, Cristovam Wanderley Picanço Diniz, and Cristovam Guerreiro Diniz

Subjects
radial astrocytes, morphometry, hippocampus, neurogenesis, shorebirds, Calidris pusilla, Neurosciences. Biological psychiatry. Neuropsychiatry, RC321-571, Human anatomy, QM1-695
Abstract

Little is known about environmental influences on radial glia-like (RGL) α cells (radial astrocytes) and their relation to neurogenesis. Because radial glia is involved in adult neurogenesis and astrogenesis, we investigated this association in two migratory shorebird species that complete their autumnal migration using contrasting strategies. Before their flights to South America, the birds stop over at the Bay of Fundy in Canada. From there, the semipalmated sandpiper (Calidris pusilla) crosses the Atlantic Ocean in a non-stop 5-day flight, whereas the semipalmated plover (Charadrius semipalmatus) flies primarily overland with stopovers for rest and feeding. From the hierarchical cluster analysis of multimodal morphometric features, followed by the discriminant analysis, the radial astrocytes were classified into two main morphotypes, Type I and Type II. After migration, we detected differential changes in the morphology of these cells that were more intense in Type I than in Type II in both species. We also compared the number of doublecortin (DCX)-immunolabeled neurons with morphometric features of radial glial–like α cells in the hippocampal V region between C. pusilla and C. semipalmatus before and after autumn migration. Compared to migrating birds, the convex hull surface area of radial astrocytes increased significantly in wintering individuals in both C. semipalmatus and C. pusilla. Although to a different extent we found a strong correlation between the increase in the convex hull surface area and the increase in the total number of DCX immunostained neurons in both species. Despite phylogenetic differences, it is of interest to note that the increased morphological complexity of radial astrocytes in C. semipalmatus coincides with the fact that during the migratory process over the continent, the visuospatial environment changes more intensely than that associated with migration over Atlantic. The migratory flight of the semipalmated plover, with stopovers for feeding and rest, vs. the non-stop flight of the semipalmated sandpiper may differentially affect radial astrocyte morphology and neurogenesis.

Published
2019
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6. Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla).

Author

Nara Gyzely de Morais Magalhães, Cristovam Guerreiro Diniz, Daniel Guerreiro Diniz, Ediely Pereira Henrique, Patrick Douglas Corrêa Pereira, Isis Ananda Matos Moraes, Mauro André Damasceno de Melo, David Francis Sherry, and Cristovam Wanderley Picanço Diniz

Subjects
Medicine, Science
Abstract

Long distance migratory birds find their way by sensing and integrating information from a large number of cues in their environment. These cues are essential to navigate over thousands of kilometers and reach the same breeding, stopover, and wintering sites every year. The semipalmated sandpiper (Calidris pusilla) is a long-distance migrant that breeds in the arctic tundra of Canada and Alaska and winters on the northeast coast of South America. Its fall migration includes a 5,300-kilometer nonstop flight over the Atlantic Ocean. The avian hippocampus has been proposed to play a central role in the integration of multisensory spatial information for navigation. Hippocampal neurogenesis may contribute to hippocampal function and a variety of factors including cognitive activity, exercise, enrichment, diet and stress influence neurogenesis in the hippocampus. We quantified hippocampal neurogenesis and volume in adult migrating and wintering semipalmated sandpipers using stereological counts of doublecortin (DCX) immunolabeled immature neurons. We found that birds captured in the coastal region of Bragança, Brazil during the wintering period had more DCX positive neurons and larger volume in the hippocampus than individuals captured in the Bay of Fundy, Canada during fall migration. We also estimate the number of NeuN immunolabeled cells in migrating and wintering birds and found no significant differences between them. These findings suggest that, at this time window, neurogenesis just replaced neurons that might be lost during the transatlantic flight. Our findings also show that in active fall migrating birds, a lower level of adult hippocampal neurogenesis is associated with a smaller hippocampal formation. High levels of adult hippocampal neurogenesis and a larger hippocampal formation found in wintering birds may be late occurring effects of long distance migratory flight or the result of conditions the birds experienced while wintering.

Published
2017
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7. Plasticity in the hippocampal formation of shorebirds during the wintering period: Stereological analysis of parvalbumin neurons in Actitis macularius

Author

Emanuel Ramos da Costa, Nara Gyzely de Morais Magalhães, Cintya Castro de Abreu, Cristovam Wanderley Picanço Diniz, Patrick Douglas Corrêa Pereira, João Batista da Silva Rosa, Daniel Guerreiro Diniz, Ediely Pereira Henrique, Cristovam Guerreiro-Diniz, Taiany Nogueira Fernandes, Anderson de Jesus Falcão da Silva, and Luma Cristina Ferreira Guerreiro

Subjects
Sandpiper, Cognitive Neuroscience, Period (gene), Zoology, Experimental and Cognitive Psychology, Hippocampal formation, Inhibitory postsynaptic potential, Hippocampus, Birds, Behavioral Neuroscience, Charadriiformes, medicine, Actitis, Parvalbuminas / an?lise, Hipocampo, Animals, Migra??o Animal, Aves / anatomia & histologia, Mammals, Neurons, biology, Voo Animal, ?rea Pr?-Tectal, biology.organism_classification, medicine.anatomical_structure, Parvalbumins, nervous system, biology.protein, Neuron, Sistema Nervoso / anatomia & histologia, Psychology, Nucleus, Parvalbumin
Abstract

This research was supported by: Coordena??o de Aperfei?oamento de Pessoal de N?vel Superior (CAPES); Programa Ci?ncias do Mar II; The Canadian Bureau for International Education (CBIE); the Brazilian Research Council (CNPq) Edital Universal Grant number 440722/2014-4; Funda??o Amaz?nia Paraense de Amparo ? Pesquisa (FAPESPA); Programa de Apoio a N?cleos Emergentes and Financiadora de Estudos e Projetos (FINEP); Instituto Brasileiro de Neuroci?ncias (IBNnet); and the Natural Sciences and Engineering Research Council of Canada (NSERC). Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brasil. Instituto Federal de Educa??o, Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brasil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brasil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brasil / Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Laborat?rio de Microscopia. Ananindeua, PA, Brasil. The number of parvalbumin neurons can be modified by social, multisensory, and cognitive stimuli in both mammals and birds, but nothing is known about their plasticity in long-distance migratory shorebirds. Here, in the spotted sandpiper (Actitis macularius), we investigated the plasticity of parvalbumin neurons of two brain areas during this species' wintering period at a lower latitude. We compared individuals in a nonmigratory rest period (November-January) and premigration (May-July) period. We used parvalbumin as a marker for counting a subpopulation of inhibitory neurons in the hippocampal formation (HF), with the magnocellular nucleus of the tectal isthmus (IMC) as a control area. Because the HF is involved in learning and memory and social interaction and the IMC is essential for control of head, neck, and eye movements, we hypothesized that parvalbumin neurons would increase in the HF and remain unchanged in the IMC. We used an optical fractionator to estimate cell numbers. Compared with the nonmigratory rest birds, parvalbumin neuron count estimates in the premigration birds increased significantly in the HF but remained unchanged in IMC. We suggest that the greater number of parvalbuminergic neurons in the HF of A. macularius in the premigration period represents adaptive circuitry changes involved in the migration back to reproductive niches in the northern hemisphere.

Published
2021

8. Author response for 'Contrasting migratory journeys and changes in hippocampal astrocyte morphology in shorebirds'

Author

Nara Gyzely de Morais Magalhães, Péricles Sena do Rêgo, Diego de Almeida Miranda, Juliana Araripe, Cristovam Guerreiro Diniz, David F. Sherry, Camila Mendes de Lima, Cleyssian Dias, Patrick Douglas Corrêa Pereira, Ediely Pereira Henrique, Dario Carvalho Paulo, Lucas Silva de Siqueira, Mauro André Damasceno de Melo, Marcus Augusto de Oliveira, Daniel Guerreiro Diniz, and Cristovam Wanderley Picanço Diniz

Subjects
medicine.anatomical_structure, medicine, Morphology (biology), Hippocampal formation, Biology, Neuroscience, Astrocyte
Published
2020

9. Changes in hippocampal astrocyte morphology of Ruddy turnstone (Arenaria interpres) during the wintering period at the mangroves of Amazon

Author

Cintya Castro de Abreu, Nara Gyzely de Morais Magalhães, Daniel Guerreiro Diniz, Anderson de Jesus Falcão da Silva, Cristovam Wanderley Picanço Diniz, Taiany Nogueira Fernandes, Cristovam Guerreiro Diniz, Emanuel Ramos da Costa, Ediely Pereira Henrique, Patrick Douglas Corrêa Pereira, João Batista da Silva, and Luma Cristina Ferreira Guerreiro

Subjects
0301 basic medicine, food.ingredient, Period (gene), Zoology, Hippocampal formation, Hippocampus, Arenaria interpres, Charadriiformes, 03 medical and health sciences, Cellular and Molecular Neuroscience, Astr?citos / citologia, 0302 clinical medicine, food, Turnstone, Animals, Cell Shape, geography, geography.geographical_feature_category, biology, Amazon rainforest, Voo Animal, Estuary, Hipocampo / citologia, biology.organism_classification, Calidris, 030104 developmental biology, Astrocytes, Ruddy turnstone (Arenaria interpres), Animal Migration, Sistema Nervoso / an?lise, Mangrove, Estuaries, Aves, 030217 neurology & neurosurgery, Charadriiformes / anatomia & histologia
Abstract

Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Instituto Federal de Educa??o. Ci?ncia e Tecnologia do Par?. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil / Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Laborat?rio de Microscopia Eletr?nica. Bel?m, PA, Brasil. Astrocytes are essential for lipid neuronal metabolism in long-distance uninterrupted migratory flights, when glucose is not available as the main source of energy. We previously demonstrated in Calidris pusilla that after uninterrupted 5 days transatlantic flight, astrocytes shrink and reduce its number in the hippocampal formation. Here we shifted our attention to the wintering period and tested the hypothesis that hippocampal astrocyte morphology of A interpres will change as the wintering period progresses towards the premigration window. To that end we used Arenaria interpres, which also crosses the Atlantic Ocean and reaches the mangroves of the Amazon River estuary for wintering. Birds were captured in September/October (closer to the arrival in the coast of Bragan?a, Para, Brazil for wintering) and in April/May (closer to the departure towards the breeding sites) and had their brains processed for selective GFAP-astrocyte immunolabeling. Three-dimensional reconstructions of the immunostained astrocytes were performed and morphological classification was done based on hierarchical cluster and discriminant analysis of multimodal morphometric features. We found two morphological phenotypes of astrocytes in the newcomers which differentially increased its morphological complexities as wintering period progresses towards the pre-migration window. Taken together, our findings demonstrate that the long-distance non-stop flight and wintering period differentially affected the two astrocytes morphotypes, suggesting distinct physiological roles for these cells. We suggest that morphological changes during the wintering period, may be part of the adaptive plasticity of the local hippocampal circuits of A. interpres in preparation for the long journey back to their breeding sites in the north hemisphere.

Published
2020

10. Contrasting migratory journeys and changes in hippocampal astrocyte morphology in shorebirds

Author

Nara Gyzely de Morais Magalhães, Juliana Araripe, Ediely Pereira Henrique, Marcus Augusto de Oliveira, Diego de Almeida Miranda, Daniel Guerreiro Diniz, Camila Mendes de Lima, Péricles Sena do Rêgo, Lucas Silva de Siqueira, Dario Carvalho Paulo, David F. Sherry, Cleyssian Dias, Patrick Douglas Corrêa Pereira, Cristovam Wanderley Picanço Diniz, Mauro André Damasceno de Melo, and Cristovam Guerreiro Diniz

Subjects
Canada, food.ingredient, Sandpiper, hippocampus, Zoology, Biology, Hippocampal formation, migration, Hippocampus, 03 medical and health sciences, Charadriiformes, Astr?citos / citologia, 0302 clinical medicine, food, transatlantic flight, medicine, semipalmated plover, Animals, Humans, Calidris pusilla, Charadrius semipalmatus, Southern Hemisphere, Phylogeny, Migra??o Animal, 030304 developmental biology, Aves / anatomia & histologia, 0303 health sciences, Phylogenetic tree, General Neuroscience, Plover, Voo Animal, semipalmated sandpiper, Hipocampo / citologia, Nearctic birds, biology.organism_classification, Charadrius, non-stop flight, Calidris, medicine.anatomical_structure, Astrocytes, astrocyte morphology, shorebird, Sistema Nervoso / anatomia & histologia, 030217 neurology & neurosurgery, Astrocyte
Abstract

Edital Universal Grant number 440722/2014-4/Brazilian Research Council (CNPq) Programa de Apoio a N?cleos Emergentes - Centro de Piscicultura do IFPA Campus Bragan?a/Funda??o Amaz?nia Paraense de Amparo ? Pesquisa (FAPESPA) Canada-Brazil Awards - Joint Research Projects (/The Canadian Bureau for International Education (CBIE) Instituto Brasileiro de Neuroci?ncias (IBNnet)/Financiadora de Estudos e Projetos (FINEP) Natural Sciences and Engineering Research Council of Canada Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Museu Paraense Em?lio Goeldi. Curso de P?s-Gradua??o em Zoologia. Bel?m, PA, Brazil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Estudos Costeiros. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Estudos Costeiros. Bragan?a, PA, Brazil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil / Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Laborat?rio de Miscroscopia Eletr?nica. Ananindeua, PA, Brasil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. University of Western Ontario. Department of Psychology, Advanced Facility for Avian Research. London, ON, Canada. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Instituto Federal de Educa??o Ci?ncia e Tecnologia do Par? - Campus Bragan?a. Laborat?rio de Biologia Molecular e Neuroecologia. Bragan?a, PA, Brazil. Semipalmated sandpiper (Calidris pusilla) migration to the Southern Hemisphere includes a 5-day non-stop flight over the Atlantic Ocean, whereas semipalmated plover (Charadrius semipalmatus) migration, to the same area, is largely over land, with stopovers for feeding and rest. We compared the number and 3D morphology of hippocampal astrocytes of Ch. semipalmatus before and after autumnal migration with those of C. pusilla to test the hypothesis that the contrasting migratory flights of these species could differentially shape hippocampal astrocyte number and morphology. We captured individuals from both species in the Bay of Fundy (Canada) and in the coastal region of Bragan?a (Brazil) and processed their brains for selective GFAP immunolabeling of astrocytes. Hierarchical cluster analysis of astrocyte morphological features distinguished two families of morphological phenotypes, named type I and type II, which were differentially affected after migratory flights. Stereological counts of hippocampal astrocytes demonstrated that the number of astrocytes decreased significantly in C. pusilla, but did not change in Ch. semipalmatus. In addition, C. pusilla and Ch. semipalmatus hippocampal astrocyte morphological features were differentially affected after autumnal migration. We evaluated whether astrocyte morphometric variables were influenced by phylogenetic differences between C. pusilla and Ch. semipalmatus, using phylogenetically independent contrast approach, and phylogenetic trees generated by nuclear and mitochondrial markers. Our findings suggest that phylogenetic differences do not explain the results and that contrasting long-distance migratory flights shape plasticity of type I and type II astrocytes in different ways, which may imply distinct physiological roles for these cells.

Published
2020

11. Cães domésticos predadores de ninho de batuíra bicuda (Charadrius wilsonia) no nordeste brasileiro

Author

Cristovam Guerreiro Diniz, Nara Gyzely de Morais Magalhães, Daniel Guerreiro Diniz, Patrick Douglas Corrêa Pereira, Dario Carvalho Paulo, Fabio Renato Rendeiro, David Francis Sherry, and Cristovam Wanderley Picanço Diniz

Subjects
0106 biological sciences, Geography, 010604 marine biology & hydrobiology, General Medicine, 010603 evolutionary biology, 01 natural sciences
Published
2016

12. Small-scale environmental enrichment and exercise enhance learning and spatial memory of Carassius auratus, and increase cell proliferation in the telencephalon: an exploratory study

Author

Nara Gyzely de Morais Magalhães, Daniel Guerreiro Diniz, Cristovam W. Picanço-Diniz, Cristovam Guerreiro-Diniz, Mauro André Damasceno de Melo, F.R.R. Oliveira, S.B. Marques, Taiany Nogueira Fernandes, Ediely Pereira Henrique, Cintya Castro de Abreu, S.L.S. Herdeiro, Patrick Douglas Corrêa Pereira, and Daniel C. Anthony

Subjects
0301 basic medicine, Male, Telencephalon, Physiology, Stereology, Immunology, Biophysics, Spatial Learning, Ocean Engineering, Cell Count, Carassius auratus, Biology, Biochemistry, 03 medical and health sciences, 0302 clinical medicine, Behavioral study, Physical Conditioning, Animal, medicine, Animals, Spatial learning and memory, General Pharmacology, Toxicology and Pharmaceutics, lcsh:QH301-705.5, Cell Proliferation, Spatial Memory, lcsh:R5-920, Environmental enrichment, Behavior, Animal, Cerebrum, General Neuroscience, Fishes, Cell Biology, General Medicine, Water stream, Object recognition, 030104 developmental biology, medicine.anatomical_structure, lcsh:Biology (General), Turnover, 030220 oncology & carcinogenesis, Spatial learning, %22">Fish , Female, lcsh:Medicine (General)
Abstract

Carassius auratus is a teleost fish that has been largely used in behavioral studies. However, little is known about potential environmental influences on its performance of learning and memory tasks. Here, we investigated this question in C. auratus, and searched for potential correlation between exercise and visuospatial enrichment with the total number of telencephalic glia and neurons. To that end, males and females were housed for 183 days in either an enriched (EE) or impoverished environment (IE) aquarium. EE contained toys, natural plants, and a 12-hour/day water stream for voluntary exercise, whereas the IE had none of the above. A third plus-maze aquarium was used for spatial and object recognition tests. Different visual clues in 2 of its 4 arms were used to guide fish to reach the criteria to complete the task. The test consisted of 30 sessions and was concluded when each animal performed three consecutive correct choices or seven alternated, each ten trials. Learning rates revealed significant differences between EE and IE fish. The optical fractionator was used to estimate the total number of telencephalic cells that were stained with cresyl violet. On average, the total number of cells in the subjects from EE was higher than those from subjects maintained in IE (P=0.0202). We suggest that environmental enrichment significantly influenced goldfish spatial learning and memory abilities, and this may be associated with an increase in the total number of telencephalic cells.

Published
2018

13. Seqs-Extractor: Automated sequences extraction to reduce tedious manual corrections of large datasets

Author

Nara Gyzely de Morais Magalhães, Cristovam Guerreiro Diniz, Mauro André Damasceno de Melo, Cleyssian Dias, Patrick Douglas Corrêa Pereira, and Cristovam Wanderley Picanço Diniz

Subjects
Engineering, Focus (computing), Sequence, Interface (Java), business.industry, Sequence analysis, Shell script, computer.software_genre, Extractor, Reduction (complexity), Identification (information), Data mining, business, computer, computer.programming_language
Abstract

The analysis of large numbers of sequences requires the reduction of ambiguities during the analytical work to ensure that the effort will focus only on confirmed sequences. Performing this work automatically may help to minimize potential errors associated with tedious manual correction, allowing more effective results. Basic local alignment search tool (BLAST) seems to be the most widely used sequence analysis program. It is free, but commercial parties enhanced BLAST applications and charge a fee for their uses. There are some tools of public domain that can perform the search of microsatellites in the next generation sequencing (NGS) data, as the microsatellite identification tool (MISA), which has some features to discover microsatellites in large datasets. Here, we developed a basic shell script (BASH script) to be ran under Linux environment that can be used to extract from a sequence dataset only confirmed (BLASTed) sequences from both nucleotide (BLASTN) and protein (BLASTX) databases and extract sequences that contains microsatellites using MISA tool, using a friendly interface and no fees charged. Seqs-Extractor is a helpful tool that may enhance the analysis of large datasets in BLAST+ and MISA by minimizing the time of management, reducing potential errors caused by manipulating data and no fees charged. Seqs-Extractor is available at https://github.com/patrick-douglas/Seqs-Extractor/wiki .

Published
2017

14. NeuN Immunohistochemistry Protocol v2

Author

Nara Gyzely de Morais Magalhães

Abstract

Protocol for Immunohistochemistry free-floating sections with anti-NeuN antibody for avian tissue.

Published
2017

15. DCX Immunohistochemistry Protocol v2

Author

Nara Gyzely de Morais Magalhães

Subjects
Protocol (science), Pathology, medicine.medical_specialty, business.industry, medicine, Immunohistochemistry, business
Abstract

Protocol for Immunohistochemistry free-floating sections with anti-doublecortin antibody for avian tissue.

Published
2017

16. DCX Immunohistochemistry rotocol v1

Author

Nara Gyzely de Morais Magalhães

Subjects
Pathology, medicine.medical_specialty, medicine, Immunohistochemistry, Biology
Abstract

Protocol Immunohistochemistry free-floating sections with anti-doublecortin antibody for avian tissue.

Published
2017

17. Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla)

Author

Ediely Pereira Henrique, Daniel Guerreiro Diniz, Isis Ananda Matos Moraes, Nara Gyzely de Morais Magalhães, Mauro André Damasceno de Melo, Patrick Douglas Corrêa Pereira, David F. Sherry, Cristovam Wanderley Picanço Diniz, and Cristovam Guerreiro Diniz

Subjects
0301 basic medicine, Physiology, lcsh:Medicine, Hippocampus, Hippocampal formation, Breeding, Charadriiformes, 0302 clinical medicine, Ornithology, Animal Cells, Bird Flight, Hippocampal Neurogenesis, Medicine and Health Sciences, Psychology, lcsh:Science, Atlantic Ocean, Neurons, Multidisciplinary, biology, Animal Behavior, Ecology, Neurogenesis, Brain, Calidris, Cell Motility, Bird flight, Seasons, Cellular Types, Anatomy, Flight (Biology), Brazil, Research Article, Canada, food.ingredient, Sandpiper, Cell Migration, 03 medical and health sciences, food, Developmental Neuroscience, Animals, 14. Life underwater, Neuron Migration, Behavior, Biological Locomotion, lcsh:R, Hippocampal Formation, Neurosciences, Biology and Life Sciences, Cell Biology, Feeding Behavior, biology.organism_classification, Doublecortin, 030104 developmental biology, Cellular Neuroscience, biology.protein, lcsh:Q, Animal Migration, Zoology, 030217 neurology & neurosurgery, Alaska, Neuroscience, Developmental Biology
Abstract

Long distance migratory birds find their way by sensing and integrating information from a large number of cues in their environment. These cues are essential to navigate over thousands of kilometers and reach the same breeding, stopover, and wintering sites every year. The semipalmated sandpiper (Calidris pusilla) is a long-distance migrant that breeds in the arctic tundra of Canada and Alaska and winters on the northeast coast of South America. Its fall migration includes a 5,300-kilometer nonstop flight over the Atlantic Ocean. The avian hippocampus has been proposed to play a central role in the integration of multisensory spatial information for navigation. Hippocampal neurogenesis may contribute to hippocampal function and a variety of factors including cognitive activity, exercise, enrichment, diet and stress influence neurogenesis in the hippocampus. We quantified hippocampal neurogenesis and volume in adult migrating and wintering semipalmated sandpipers using stereological counts of doublecortin (DCX) immunolabeled immature neurons. We found that birds captured in the coastal region of Bragança, Brazil during the wintering period had more DCX positive neurons and larger volume in the hippocampus than individuals captured in the Bay of Fundy, Canada during fall migration. We also estimate the number of NeuN immunolabeled cells in migrating and wintering birds and found no significant differences between them. These findings suggest that, at this time window, neurogenesis just replaced neurons that might be lost during the transatlantic flight. Our findings also show that in active fall migrating birds, a lower level of adult hippocampal neurogenesis is associated with a smaller hippocampal formation. High levels of adult hippocampal neurogenesis and a larger hippocampal formation found in wintering birds may be late occurring effects of long distance migratory flight or the result of conditions the birds experienced while wintering.

Published
2017

18. Microglia and neurons in the hippocampus of migratory sandpipers

Author

Cristovam W. Picanço-Diniz, Patrick Douglas Corrêa Pereira, Nara Gyzely de Morais Magalhães, Camila Mendes de Lima, Dario Carvalho Paulo, Aline Andrade de Sousa, Daniel Guerreiro Diniz, David F. Sherry, Cristovam Guerreiro Diniz, C. Santos Filho, and Marcus Augusto de Oliveira

Subjects
Photomicrography, Telencephalon, 0301 basic medicine, Medicine (General), Physiology, Stereology, Shorebirds, Hippocampus, Breeding, Hippocampal formation, Biochemistry, Charadriiformes, 0302 clinical medicine, Actitis, Psychology, Biology (General), General Pharmacology, Toxicology and Pharmaceutics, lcsh:QH301-705.5, Phylogeny, Neurons, lcsh:R5-920, biology, Ecology, General Neuroscience, Organ Size, General Medicine, Immunohistochemistry, Calidris, Hippocampal volume, Microglia, lcsh:Medicine (General), geographic locations, Spatial Navigation, food.ingredient, Sandpiper, QH301-705.5, Immunology, Biophysics, Ocean Engineering, 03 medical and health sciences, R5-920, food, Species Specificity, Orientation, Animals, Morphometry, Neurosciences, Biomedical Sciences, Cell Biology, biology.organism_classification, Tundra, 030104 developmental biology, lcsh:Biology (General), Animal Migration, 030217 neurology & neurosurgery
Abstract

The semipalmated sandpiper Calidris pusilla and the spotted sandpiper Actitis macularia are long- and short-distance migrants, respectively. C. pusilla breeds in the sub-arctic and mid-arctic tundra of Canada and Alaska and winters on the north and east coasts of South America. A. macularia breeds in a broad distribution across most of North America from the treeline to the southern United States. It winters in the southern United States, and Central and South America. The autumn migration route of C. pusilla includes a non-stop flight over the Atlantic Ocean, whereas autumn route of A. macularia is largely over land. Because of this difference in their migratory paths and the visuo-spatial recognition tasks involved, we hypothesized that hippocampal volume and neuronal and glial numbers would differ between these two species. A. macularia did not differ from C. pusilla in the total number of hippocampal neurons, but the species had a larger hippocampal formation and more hippocampal microglia. It remains to be investigated whether these differences indicate interspecies differences or neural specializations associated with different strategies of orientation and navigation.

Published
2016

19. Visuospatial learning and memory in the Cebus apella and microglial morphology in the molecular layer of the dentate gyrus and CA1 lacunosum molecular layer

Author

Pedro Fernando da Costa Vasconcelos, Daniel Guerreiro Diniz, Cesar Augusto Raiol Foro, Camila Mendes de Lima, Carlos Santos-Filho, Nara Gyzely de Morais Magalhães, Cristovam Guerreiro-Diniz, Cristovam Wanderley Picanço Diniz, and Marcus Augusto de Oliveira

Subjects
Male, Primatas, Spatial Learning, Hippocampal formation, Cellular and Molecular Neuroscience, Imaging, Three-Dimensional, Memory, medicine, Animals, Cebus, Cluster Analysis, CA1 Region, Hippocampal, Microglia, Dentate gyrus, Immunohistochemistry, Phenotype, medicine.anatomical_structure, Aprendizagem, nervous system, Dentate Gyrus, Spatial learning, Female, Giro Denteado, Psychology, Neuroscience, Microglia / citologia
Abstract

Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Universidade Federal do Par? - Instituto de Ci?ncias Biol?gicas - Hospital Universit?rio Jo?o de Barros Barreto - Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o, Bel?m, PA, Brazil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Ananindeua, PA, Brasil. Universidade Federal do Par?. Instituto de Ci?ncias Biol?gicas. Hospital Universit?rio Jo?o de Barros Barreto. Laborat?rio de Investiga??es em Neurodegenera??o e Infec??o. Bel?m, PA, Brazil. We investigated whether the morphology of microglia in the molecular layer of the dentate gyrus (DG-Mol) or in the lacunosum molecular layer of CA1 (CA1-LMol) was correlated with spatial learning and memory in the capuchin monkey (Cebus apella). Learning and memory was tested in 4 monkeys with visuo-spatial, paired associated learning (PAL) tasks from the Cambridge battery of neuropsychological tests. After testing, monkeys were sacrificed, and hippocampi were sectioned. We specifically immunolabeled microglia with an antibody against the adapter binding, ionized calcium protein. Microglia were selected from the middle and outer thirds of the DG-Mol (n = 268) and the CA1-LMol (n = 185) for three-dimensional reconstructions created with Neurolucida and Neuroexplorer software. Cluster and discriminant analyses, based on microglial morphometric parameters, identified two major morphological microglia phenotypes (types I and II) found in both the CA1-LMol and DG-Mol of all individuals. Compared to type II, type I microglia were significantly smaller, thinner, more tortuous and ramified, and less complex (lower fractal dimensions). PAL performance was both linearly and nonlinearly correlated with type Imicroglial morphological features from the rostral and caudal DG-Mol, but not with microglia from the CA1-LMol. These differences in microglial morphology and correlations with PAL performance were consistent with previous proposals of hippocampal regional contributions for spatial learning and memory. Our results suggested that at least two morphological microglial phenotypes provided distinct physiological roles to learning-associated activity in the rostral and caudal DG-Mol of the monkey brain.

Published
2014

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