Effect of perinatal asphyxia on tuberomammillary nucleus neuronal density and object recognition memory: A possible role for histamine?

Flores-Balter, Gabriela; Cordova-Jadue, Héctor; Chiti-Morales, Alessandra; Lespay, Carolyne; Espina-Marchant, Pablo; Falcon, Romina; Grinspun, Noemí; Sánchez, J. E.; Bustamante, Diego; Morales, Paola; Herrera‐Marschitz, Mario; Valdés, José Luís

doi:10.1016/j.bbr.2016.07.026

Cited by 6 publications

(6 citation statements)

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“…Exploratory behavior was monitored at P30 with a video camera, with the animals placed in a square arena (open field) in a noise-free room as previously described [ 38 , 62 ]. When monitoring rats at P7, the rat was placed in the center of a square arena (21 × 29 cm, with a continuous wall 15 cm high) to freely explore for 5 min, monitoring the total traveled distance (cm) (locomotor activity).…”

Section: Methodsmentioning

confidence: 99%

“…The novel object recognition test was used to evaluate recognition memory, assessed at P30 as previously described [ 38 , 62 ]. Briefly, the animals were first habituated to a box and then exposed to two identical plastic objects for 5 min, letting the animals freely explore and get familiar with the objects.…”

Section: Methodsmentioning

confidence: 99%

“…Pro-inflammatory cytokines released by reactive glial cells also produce cytotoxic effects on oligodendrocytes [ 33 ], inducing premature maturation of oligodendrocyte progenitor cells and aberrant myelination, thereby contributing to hypomyelination in the developing brain [ 34 ], and to delays in neurobehavioral development [ 35 , 36 ], and cognitive impairments [ 2 , 37 ], including deficit in recognition memory [ 35 , 38 ], social skills [ 39 ], and increased anxiety [ 6 , 35 ], as well as deficits in motor coordination [ 6 , 35 ].…”

Section: Introductionmentioning

confidence: 99%

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Intranasal Administration of Mesenchymal Stem Cell Secretome Reduces Hippocampal Oxidative Stress, Neuroinflammation and Cell Death, Improving the Behavioral Outcome Following Perinatal Asphyxia

Farfan

Carril

Redel

et al. 2020

IJMS

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Perinatal Asphyxia (PA) is a leading cause of motor and neuropsychiatric disability associated with sustained oxidative stress, neuroinflammation, and cell death, affecting brain development. Based on a rat model of global PA, we investigated the neuroprotective effect of intranasally administered secretome, derived from human adipose mesenchymal stem cells (MSC-S), preconditioned with either deferoxamine (an hypoxia-mimetic) or TNF-α+IFN-γ (pro-inflammatory cytokines). PA was generated by immersing fetus-containing uterine horns in a water bath at 37 °C for 21 min. Thereafter, 16 μL of MSC-S (containing 6 μg of protein derived from 2 × 105 preconditioned-MSC), or vehicle, were intranasally administered 2 h after birth to asphyxia-exposed and control rats, evaluated at postnatal day (P) 7. Alternatively, pups received a dose of either preconditioned MSC-S or vehicle, both at 2 h and P7, and were evaluated at P14, P30, and P60. The preconditioned MSC-S treatment (i) reversed asphyxia-induced oxidative stress in the hippocampus (oxidized/reduced glutathione); (ii) increased antioxidative Nuclear Erythroid 2-Related Factor 2 (NRF2) translocation; (iii) increased NQO1 antioxidant protein; (iv) reduced neuroinflammation (decreasing nuclearNF-κB/p65 levels and microglial reactivity); (v) decreased cleaved-caspase-3 cell-death; (vi) improved righting reflex, negative geotaxis, cliff aversion, locomotor activity, anxiety, motor coordination, and recognition memory. Overall, the study demonstrates that intranasal administration of preconditioned MSC-S is a novel therapeutic strategy that prevents the long-term effects of perinatal asphyxia.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Intranasal Administration of Mesenchymal Stem Cell Secretome Reduces Hippocampal Oxidative Stress, Neuroinflammation and Cell Death, Improving the Behavioral Outcome Following Perinatal Asphyxia

Farfan

Carril

Redel

et al. 2020

IJMS

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“…Interestingly, asphyxia‐exposed rats exhibited an impaired performance in the object recognition test, which was correlated with a decreased number of ventral TMN neurons and marked reduction of histidine decarboxylase expression in the hypothalamus. Acute treatment with the H 3 R antagonist thioperamide dose‐dependently reverted perinatal asphyxia‐induced recognition memory impairment in adulthood (Flores‐Balter et al ., 2016).…”

Section: Different Types Of Memory and Memory Modulation By Histaminementioning

confidence: 99%

Brain histamine modulates recognition memory: possible implications in major cognitive disorders

Provensi

Costa

Izquierdo

et al. 2018

British J Pharmacology

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Several behavioural tests have been developed to study and measure emotionally charged or emotionally neutral memories and how these may be affected by pharmacological, dietary or environmental manipulations. In this review, we describe the experimental paradigms used in preclinical studies to unravel the brain circuits involved in the recognition and memorization of environmentally salient stimuli devoid of strong emotional value. In particular, we focus on the modulatory role of the brain histaminergic system in the elaboration of recognition memory that is based on the judgement of the prior occurrence of an event, and it is believed to be a critical component of human declarative memory. The review also addresses questions that may help improve the treatment of impaired declarative memory described in several affective and neuropsychiatric disorders such as ADHD, Alzheimer's disease and major neurocognitive disorder.

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“…In humans, PA is a risk factor for several psychiatric disorders, including learning deficits and schizophrenia. Conversely, in rodents, PA is associated with delayed cell death, dopamine and histamine transmission deficits and behavioural impairments assessed at adulthood, affecting learning, spatial, and non-spatial memory and anxiety (Simola et al 2008 ; Morales et al 2010 ; Galeano et al 2011 , 2015 ; Flores-Balter et al 2016 ; Tapia-Bustos et al 2017 ). The idea of progressive dysfunction and “first” and successive hit sequences, triggering and perpetuating pathophysiological conditions and/or diseases, has recently been discussed (Marriott et al 2017 ; Israel et al 2017 ).…”

Section: Vulnerability To Recurrent Metabolic Insultsmentioning

confidence: 99%

Targeting Sentinel Proteins and Extrasynaptic Glutamate Receptors: a Therapeutic Strategy for Preventing the Effects Elicited by Perinatal Asphyxia?

et al. 2017

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Perinatal asphyxia (PA) is a relevant cause of death at the time of labour, and when survival is stabilised, associated with short- and long-term developmental disabilities, requiring inordinate care by health systems and families. Its prevalence is high (1 to 10/1000 live births) worldwide. At present, there are few therapeutic options, apart from hypothermia, that regrettably provides only limited protection if applied shortly after the insult.PA implies a primary and a secondary insult. The primary insult relates to the lack of oxygen, and the secondary one to the oxidative stress triggered by re-oxygenation, formation of reactive oxygen (ROS) and reactive nitrogen (RNS) species, and overactivation of glutamate receptors and mitochondrial deficiencies. PA induces overactivation of a number of sentinel proteins, including hypoxia-induced factor-1α (HIF-1α) and the genome-protecting poly(ADP-ribose) polymerase-1 (PARP-1). Upon activation, PARP-1 consumes high amounts of ATP at a time when this metabolite is scarce, worsening in turn the energy crisis elicited by asphyxia. The energy crisis also impairs ATP-dependent transport, including glutamate re-uptake by astroglia. Nicotinamide, a PARP-1 inhibitor, protects against the metabolic cascade elicited by the primary stage, avoiding NAD+ exhaustion and the energetic crisis. Upon re-oxygenation, however, oxidative stress leads to nuclear translocation of the NF-κB subunit p65, overexpression of the pro-inflammatory cytokines IL-1β and TNF-α, and glutamate-excitotoxicity, due to impairment of glial-glutamate transport, extracellular glutamate overflow, and overactivation of NMDA receptors, mainly of the extrasynaptic type. This leads to calcium influx, mitochondrial impairment, and inactivation of antioxidant enzymes, increasing further the activity of pro-oxidant enzymes, thereby making the surviving neonate vulnerable to recurrent metabolic insults whenever oxidative stress is involved. Here, we discuss evidence showing that (i) inhibition of PARP-1 overactivation by nicotinamide and (ii) inhibition of extrasynaptic NMDA receptor overactivation by memantine can prevent the short- and long-term consequences of PA. These hypotheses have been evaluated in a rat preclinical model of PA, aiming to identify the metabolic cascades responsible for the long-term consequences induced by the insult, also assessing postnatal vulnerability to recurrent oxidative insults. Thus, we present and discuss evidence demonstrating that PA induces long-term changes in metabolic pathways related to energy and oxidative stress, priming vulnerability of cells with both the neuronal and the glial phenotype. The effects induced by PA are region dependent, the substantia nigra being particularly prone to cell death. The issue of short- and long-term consequences of PA provides a framework for addressing a fundamental issue referred to plasticity of the CNS, since the perinatal insult triggers a domino-like sequence of events making the developing individual vulnerable to recurrent adverse con...

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Effect of perinatal asphyxia on tuberomammillary nucleus neuronal density and object recognition memory: A possible role for histamine?

Cited by 6 publications

References 37 publications

Intranasal Administration of Mesenchymal Stem Cell Secretome Reduces Hippocampal Oxidative Stress, Neuroinflammation and Cell Death, Improving the Behavioral Outcome Following Perinatal Asphyxia

Intranasal Administration of Mesenchymal Stem Cell Secretome Reduces Hippocampal Oxidative Stress, Neuroinflammation and Cell Death, Improving the Behavioral Outcome Following Perinatal Asphyxia

Brain histamine modulates recognition memory: possible implications in major cognitive disorders

Targeting Sentinel Proteins and Extrasynaptic Glutamate Receptors: a Therapeutic Strategy for Preventing the Effects Elicited by Perinatal Asphyxia?

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