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PubMed1998

Cloning of the presenilin 2 cDNA and its distribution in brain of the primate, Microcebus murinus: coexpression with betaAPP and Tau proteins.

A 1340-bp cDNA fragment encoding the lemurian presenilin 2 protein (PS2) was isolated from a Microcebus murinus brain cDNA library by PCR using oligonucleotide primers based on the nucleotide sequence of the human gene. Analysis of five isolated clones showed that the sequence encoded a 448-amino-acid open reading frame, 95.5% identical to the human and 93.5% identical to the mouse presenilin 2 sequences. However, neither the localization of the 2 positions in PS2 nor that of the 43 positions in PS1 associated with early onset Alzheimer's disease were changed. Expression of the presenilin 2 was detected by RT-PCR and compared with that of presenilin 1 and betaAPP in the brain and in peripheral tissues (liver, kidney, and spleen). Immunohistochemistry with a specific polyclonal antiserum raised against a synthetic peptide from the N-terminal part of the human PS2 showed that the protein is distributed throughout the microcebe brain, in vascular and nerve structures. In cortical and in subcortical areas, PS2 labeling was weak and granular in appearance and was scattered throughout the cytoplasm of many neurones, extending into neurites. The gene expression of PS2 increased with age but was not affected by the presence of numerous amyloid plaques. Double labeling immunocytochemistry detected very few neurones with combined immunoreactivity PS2 and APP, or PS2 and Tau.

Amino Acid Sequence↗
PubMed2000

Immunohistochemical analysis of cerebral cortical and vascular lesions in the primate Microcebus murinus reveal distinct amyloid beta1-42 and beta1-40 immunoreactivity profiles.

Recent reports have shown that amyloid beta deposits in the brains of Alzheimer's disease patients consist mainly of two distinct species of amyloid beta protein (Abeta) with different C-termini, Abeta1-42 (Abeta42) and Abeta1-40 (Abeta40). The nature of the Abeta species in Microcebus murinus brain was investigated immunocytochemically using polyclonal antibodies with clear specificity for the Abeta42 and Abeta40 C-termini. The cortical vascular deposits were immunopositive for both Abeta42 and Abeta40. However, most of the diffuse plaques were strongly positive for Abeta42 whereas only a subset of deposits were positive for Abeta40. Numerous cortical plaques were Abeta42-immunopositive but tested negative for Abeta40. This suggests that Abeta42 is probably associated with early stages of plaque maturation. This neuropathological feature reminiscent of that observed in brains affected by Alzheimer's disease further supports the idea that M. murinus could be used as a potential model of the early stages of this neurological disease.

Amyloid beta-Peptides↗
PubMed1994

Mouse lemur microscopic MRI brain atlas.

We present a three-dimensional (3D) digital atlas of a mouse lemur head at 60-micron cubic voxel isotropic resolution. It was constructed from a 3D proton magnetic resonance image (MRI) acquired at 500 MHz. It shows views of 3D volume-rendering and movies of contiguous 2D plane cuts in three orthogonal directions. This MR data set was acquired using a spin-echo pulse sequence under conditions of strong T2 and significant diffusion weighting. Experimental parameters were optimized to provide strong intrinsic contrast between gray and white matter. Familiar anatomical structures are clearly identifiable. Fine fiber tracts, laminations of cortices, details of the inner ears, and layering in the lateral geniculate nuclei are all visible. Anatomical identifications of structures in representative slices selected from the atlas are presented. We also describe some difficulties and trade-offs encountered in microscopic resolution MRI. We note that this type of atlas does not suffer from the spatial distortions and slice registration problems introduced by standard histological techniques. Future in vivo longitudinal studies will provide atlases describing in detail the development of the primate brain.

Animals↗
PubMed1995

Effects of aging upon recent memory in Microcebus murinus.

Four young (2 to 4-year-old) and four aged (9 to 10-year-old) grey mouse lemurs (Microcebus murinus) were given a simple visual discrimination task, and a delayed response visual discrimination task with variable retention delay. The response to the test is a motor one, that consists of choosing one out of four corridors of an apparatus based upon the degree of illumination. The aged animals did not show any learning deficiency, and were capable of memorizing the task for several months. However, they were more sensitive to the length of the delay in the delayed response task than the young animals. It is, therefore, possible to argue that the memory for recent stimulus events is affected during aging. These results corroborate those obtained in other primates, and demonstrate the usefulness of the grey mouse lemur as a new animal model for analyzing aging.

Aging↗
PubMed2002

White adipose tissue composition in the free-ranging fat-tailed dwarf lemur (Cheirogaleus medius; Primates), a tropical hibernator.

In temperate species, hibernation is enhanced by high levels of essential fatty acids in white adipose tissue. Essential fatty acids cannot be synthesized by mammals, thus nutritional ecology should play a key role in physiological adaptations to hibernation. Tropical hibernators are exposed to different physiological demands than hibernators in temperate regions and are expected to be subject to different constraints. The aims of this study were to assess whether or not the tropical hibernator Cheirogaleus medius shows biochemical changes in its white adipose tissue before and during hibernation. A capture-recapture study was combined with feeding observations in western Madagascar. Before and after hibernation, 77 samples of white adipose tissue from 57 individuals of C. medius, as well as dietary items eaten during pre-hibernation fattening, were sampled and analyzed for their fatty acid composition. In contrast to temperate hibernators, C. medius exhibits extremely low essential fatty acid concentrations in its white adipose tissue (2.5%) prior to hibernation. The fatty acid pattern of the white adipose tissue did not change during pre-hibernation fattening and did not reflect dietary fatty acid composition. During hibernation, fat stores showed only minor but significant compositional changes. Because of its prevalence, the main fuel during hibernation was the monounsaturated oleic acid, which seemed to be preferentially synthesized from dietary carbohydrates. Results suggest that essential fatty acids do not represent an ecological limitation for hibernation in the tropics, at least not in the fat-tailed dwarf lemur.

Adipose Tissue↗
PubMed2004

Factors affecting the daily rhythm of body temperature of captive mouse lemurs (Microcebus murinus).

Microcebus murinus, a small nocturnal Malagasy primate, exhibits adaptive energy-saving strategies such as daily hypothermia and gregarious patterns during diurnal rest. To determine whether ambient temperature (T(a)), food restriction and nest sharing can modify the daily body temperature (T(b)) rhythm, T(b) was recorded by telemetry during winter in six males exposed to different ambient temperatures (T(a) = 25, 20, 15 degrees C) and/or to a total food restriction for 3 days depending on social condition (isolated versus pair-grouped). At 25 degrees C, the daily rhythm of T(b) was characterized by high T(b) values during the night and lower values during the day. Exposure to cold significantly decreased minimal T(b) values and lengthened the daily hypothermia. Under food restriction, minimal T(b) values were also markedly lowered. The combination of food restriction and cold induced further increases in duration and depth of torpor bouts, minimal T(b) reaching a level just above T(a). Although it influenced daily hypothermia less than environmental factors, nest sharing modified effects of cold and food restriction previously observed by lengthening duration of torpor but without increasing its depth. In response to external conditions, mouse lemurs may thus adjust their energy expenditures through daily modifications of both the duration and the depth of torpor.

Adaptation, Physiological↗
PubMed2005

Hibernation in the tropics: lessons from a primate.

The Malagasy primate Cheirogaleus medius hibernates in tree holes for 7 months, although ambient temperatures during hibernation rise above 30 degrees C in their natural environment. In a field study we show that during hibernation the body temperature of most lemurs fluctuates between about 10 degrees C and 30 degrees C, closely tracking the diurnal fluctuations of ambient temperature passively. These lemurs do not interrupt hibernation by spontaneous arousals, previously thought to be obligatory for all mammalian hibernators. However, some lemurs hibernate in large trees, which provide better thermal insulation. Their body temperature fluctuates only little around 25 degrees C, but they show regular arousals, as known from temperate and arctic hibernators. The results from this study demonstrate that maximum body temperature is a key factor necessitating the occurrence of arousals. Furthermore, we show that hibernation is not necessarily coupled to low body temperature and, therefore, low body temperature should no longer be included in the definition of hibernation.

Animals↗
PubMed2000

Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor.

We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (Tsk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (Ta) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7-8.9 h with a daily mean of 3.4 h, and their Tsk s fell to a minimum of 18.8 degrees C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 +/- 65.4 kJ x day(-1)) was about the same of that of normothermic mouse lemurs in the dry season (115.5 +/- 27.3 kJ x day(-1)). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 +/- 32.7 kJ x day(-1) which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between Tsk and Ta (r2 = 0.37) and with torpor bout length (r2 = 0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 +/- 4.1 ml x day(-1)) was significantly lower than that of mouse lemurs remaining normothermic (19.4 +/- 3.8 ml x day(-1)), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus demonstrates that torpor may not only reflect its impact on the daily energy demands, but involve wider adaptive implications such as water requirements.

Animals↗
PubMed1998

Thermoregulatory responses to variations of photoperiod and ambient temperature in the male lesser mouse lemur: a primitive or an advanced adaptive character?

The lesser mouse lemur, a small Malagasy primate, is exposed to strong seasonal variations in ambient temperature and food availability in its natural habitat. To face these environmental constraints, this nocturnal primate exhibits biological seasonal rhythms that are photoperiodically driven. To determine the role of daylength on thermoregulatory responses to changes in ambient temperature, evaporative water loss (EWL), body temperature (Tb) and oxygen consumption, measured as resting metabolic rate (RMR), were measured in response to ambient temperatures ranging from 5 degrees C to 35 degrees C, in eight males exposed to either short (10L:14D) or long (14L:10D) daylengths in controlled captive conditions. In both photoperiods, EWL, Tb and RMR were significantly modified by ambient temperatures. Exposure to ambient temperatures below 25 degrees C was associated with a decrease in Tb and an increase in RMR, whereas EWL remained constant. Heat exposure caused an increase in Tb and heat loss through evaporative pathways. Thermoregulatory responses to changes in ambient temperature significantly differed according to daylength. Daily variations in Tb and EWL were characterized by high values during the night. During the diurnal rest, lower values were found and a phase of heterothermia occurred in the early morning followed by a spontaneous rewarming. The amplitude of Tb decrease with or without the occurrence of torpor (Tb < 33 degrees C) was dependent on both ambient temperature and photoperiod. This would support the hypothesis of advanced thermoregulatory processes in mouse lemurs in response to selective environmental pressure, the major external cue being photoperiodic variations.

Adaptation, Physiological↗
PubMed1997

Quantitative analysis of tau protein-immunoreactive accumulations and beta amyloid protein deposits in the cerebral cortex of the mouse lemur, Microcebus murinus.

Recent studies have revealed the presence of tau protein-immunoreactive accumulations and beta amyloid protein (A beta) deposits in the cerebral cortex of the aged mouse lemur, Microcebus murinus. To examine the age-related evolution of these changes and compare their regional distribution to that reported for humans and nonhuman primates with Alzheimer's disease lesions, we performed a quantitative analysis of a large series of mouse lemurs aged from 1 to 13 years. The prevalence and density of tau protein-immunoreactive accumulations in the neocortex of this prosimian increased steadily with age. Neocortical areas were frequently affected even in young mouse lemurs, whereas the subiculum and entorhinal cortex were only involved occasionally in animals older than 8 years. As in anthropoid primates, diffuse A beta deposits were often observed in the cerebral cortex and amygdala of old mouse lemurs. Although all animals with diffuse A beta deposits had tau protein-immunoreactive accumulations in the neocortex, no correlation was found between the densities of these lesions in each area and among the areas studied. The age-dependent progression of tau protein-immunoreactive accumulations indicates that this prosimian may represent a valuable model for the study of the biochemical mechanisms of brain aging, while the relative sparing of hippocampus in mouse lemurs contrasts sharply with previous reports on neurofibrillary tangle formation in humans, and suggests that this animal may also be useful to investigate the biological characteristics of neuroprotection in this area. Furthermore, the present data indicate that A beta deposition in mouse lemurs is not age dependent, but occurs in a few vulnerable old animals.

Age Factors↗
PubMed1998

Astroglial interlaminar processes in the cerebral cortex of prosimians and Old World monkeys.

Previous observations have shown that astrocytes with interlaminar processes are present in the cerebral cortex of humans and New and Old World monkeys, but not in the rodent. The present report furthers the analysis of possible evolutionary aspects regarding the expression of such astroglial features. A comparison between young and adult Microcebus murinus, a prosimian, and Old World monkeys (Macaca mulatta and Papio hamadryas) is presented. Brain samples were processed for glial fibrillary acidic protein (GFAP), vimentin, MAP2 and SMI 311 immunocytochemistry, using different procedures. The cerebral cortex of adult Microcebus showed the presence of long astroglial processes, albeit reduced in number and length with respect to those observed in Old World monkeys. Macaca and Papio showed dense packing of such processes extending in most cortical regions to a depth of approximately 700 micrometers. Based on double immunolabelling for GFAP and MAP 2 antigens, the location and extent of these processes was shown to overlap with areas traversed by bundles and individual apical dendrites. Aged Old World specimens depicted an increased thickness of terminal portions of interlaminar processes, with increased morphological alterations. Comparisons made between the average thickness of the "brush" composed of interlaminar processes and the thickness of lamina I among the species analyzed disclosed an absence of relationship between them. This suggests that interlaminar processes do not represent cellular adaptations to the increase in thickness in superficial cortical laminae, but rather to some other evolutionary pressure. Since astroglial interlaminar processes are already present in a prosimian, although in a comparatively reduced manner, it is suggested that such processes underwent an early expression within the primate order, with increasing presence in more recent primate species.

Animals↗
PubMed2003

Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur ( Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur ( Microcebus rufus) in Eastern Madagascar.

To investigate for the first time the relationship between contrasting patterns of seasonal changes of the environment and activity, body mass and reproduction for small nocturnal primates in nature, we compared a population of golden brown mouse lemur ( Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar and of the brown mouse lemur ( Microcebus rufus) in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions. Golden brown mouse lemurs (GBML) were active during the whole period (May to December) irrespective of changing environmental conditions. In contrast, a part of the population of brown mouse lemurs (BML) showed prolonged seasonal torpor, related to body mass during periods of short day length and low ambient temperatures. Differences between species might be due to differences in ambient temperature and food supply. Body weight and tail thickness (adipose tissue reserve) did not show prominent differences between short and long photoperiods in GBML, whereas both differ significantly in BML, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species showed a seasonal reproduction. The rate of growth and size of the testes were similar and preceded estrous onset in both species suggesting a photoperiodic control of reproduction in males. The estrous onset in females occurred earlier in GBML than in BML. Estrous females were observed over at least 4 months in the former, but in only 1 month in the latter species. Intraspecific variation of estrous onset in GBML may be explained by body mass. Interspecific variation of female reproduction indicates species-specific differences in the control of reproduction. Thus, environmentally related differences in annual rhythms between closely related small nocturnal lemurs emerged that allow them to cope with contrasting patterns of seasonal changes in their habitats.

Animals↗
PubMed2006

Non-invasive blood sampling from primates using laboratory-bred blood-sucking bugs (Dipetalogaster maximus; Reduviidae, Heteroptera).

Primates are easily stressed by the conventional veterinary blood sampling routine and consequently, measured blood parameters may be biased. In this study, we tested blood-sucking bugs (Dipetalogaster maximus) on one lemur and two ape species (Microcebus murinus, Pongo abelii, Pan paniscus) as an alternative, non-invasive technique for bleeding primates. Within time periods of between 6 and 62 min we obtained blood volumes of 0.01-2.4 ml in 11 out of 12 trials from all three species. Therefore, we conclude that these bugs represent a new, gentle and effective tool for bleeding captive primates without stress.

Animals↗
PubMed1995

Morphology and morphometrics of three oxyurids parasitic in primates with a description of Lemuricola microcebi n. sp.

Classical and morphometric analyses were conducted on several samples of oxyurid nematodes parasitic in strepsirrhine primates: Cheirogaleus major, Galago senegalensis, and Microcebus murinus. A diagnosis of Lemuricola contagiosus Chabaud & Petter, 1959 from C. major is given using syntypes, from which a lectotype is selected. The rest of the specimens were compared to L. contagiosus. From measurements taken from each sex, an initial Principal Component Analysis (PCA) was performed on log-transformed data and a second PCA was performed on log-shape ratios after elimination of the isometric differences. The parasites collected from M. murinus, which can be differentiated from the closely related L. contagiosus by both standard morphological characters and morphometric variables, are described as Lemuricola microcebi n. sp. The parasites collected from Galago are morphologically very similar to L. microcebi n. sp. The most probable explanation for this resemblance is considered to be a transfer from Microcebus to Galago but, due to the small numbers of individuals in our samples, it is impossible to eliminate the possibility that the parasites of Galago belong to an undescribed species. Until more material or information can be obtained, it is proposed to refer to the parasites from Galago as Lemuricola sp.

Animals↗
PubMed1995

Sexual responses to urinary chemosignals depend on photoperiod in a male primate.

In male lesser mouse lemurs, testicular size and plasma testosterone levels are controlled by photoperiodic variations but can be modified by urinary cues from conspecifics. To test whether urinary cues may have differential effects on testicular size and testosterone levels depending on the photoperiodic state of the receiver, isolated males were exposed for 4 wk to urinary cues from oestrous females or dominant males:--at the beginning of the breeding season induced by long photoperiod (LD),--during refractoriness to LD leading to spontaneous sexual regression and during sexual quiescence exhibited by males kept in short photoperiod (SD). Urinary chemosignals from females were always stimulatory producing significant increases in testosterone levels. By contrast, urinary cues from dominant males produced significant differential effects on reproductive function. They depressed sexual function only at the beginning of the breeding season. During SD or during refractoriness to LD, chemosignals were stimulatory leading to increases in testosterone levels and full development of testes. These results demonstrate that the same chemosignal may have opposite effect on sexual function of the receiver depending on endocrine mechanisms set up by photoperiod.

Animals↗
PubMed1996

Castration affects the emission of an ultrasonic vocalization in a nocturnal primate, the grey mouse lemur (Microcebus murinus).

Male primates have evolved particular displays to advertise male fitness. In nocturnal prosimians it was assumed that such displays (vocal advertisement, marking behaviour) are hormonally dependent and influenced by olfactory cues of a receptive female. To test this assumption mouse lemur males of different gonadal status (males castrated as adults, normal males), or of varying olfactory input (males vomeronasalectomized or bulbectomized as adults) were paired with intact "stimulus" preoestrous females and vocalization, vocal rates, and marking behaviours were monitored. The vocal rate of only one particular vocalization, the "trill" advertisement call, was sexually dimorphic and changed depending on gonadal status. Vocalization rate declined significantly in sexually experienced, castrated males as did their marking behaviour. There was however no significant correlation between either calling rate or marking behaviour and plasma testosterone levels in gonadally intact males. Neither vomeronasalectomy nor bulbectomy had a significant effect on trill calling rate or marking behaviour. Results imply that testicular hormones have a greater impact on advertisement calling and marking motivation than olfactory information of preoestrous females. In contrast to rodents, ultrasonic calling rate seems to be not only dependent on gonadal status, but also on social experience.

Animals↗
PubMedDate not supplied

Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus.

In some aged Microcebus brains (8- to 11-year-old animals) dramatic atrophy is found, particularly of the cortex, the hippocampus, the basal ganglia, the brainstem and the cerebellum, associated with a conspicuous increase in the size of the cerebral ventricles. These morphological changes are accompanied by certain histological profiles indicative of pathology. In the cortex, these histological changes consist of 1) a large number of senile plaques composed of degenerated neurites sometimes surrounding an amyloid plaque, 2) amyloid deposits in the vascular walls and 3) dense bundles of argyrophilic filaments in numerous pyramidal neurons. All these lesions resemble changes associated with Alzheimer's disease in man. The degenerative changes observed in the Microcebus brain are accompanied by behavioral changes. At the moment these preliminary studies, carried out on the smallest of all primates, do not prove that the degeneration is of the Alzheimer type, but do indicate that Microcebus murinus may well be a good model for the study of cerebral aging, providing a comparison with cerebral ageing in humans. The size, life span and cost of the animal provide further advantages when compared with other nonhuman primates.

Amyloid↗