Hypometabolic induced state: a potential tool in biomedicine and space exploration

Malatesta, Manuela; Biggiogera, Marco; Zancanaro, Carlo

doi:10.1007/s11157-006-9101-4

Cited by 15 publications

(14 citation statements)

References 110 publications

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“…Because of their morphological appearance as well as to the presence of snRNPs and SMN protein (Malatesta et al, 2004), NADs strongly remind the interchromatin granule-associated zones (IGAZ), that is, nuclear domains occur close to IG clusters (Visa et al, 1993); however, IGAZs contain coilin (Puvion-Dutilleul et al, 1995) and cleavage factors (Cardinale et al, 2007), which are absent in NADs. Therefore, the NADs occurring in hazel dormice seem to represent nuclear structures typical of the hibernating state, like several nuclear bodies found in different tissues, which, similarly to NADs, form during lethargy and quickly disappear upon arousal [reviewed in Malatesta et al (2007)]. …”

Section: Discussionmentioning

confidence: 99%

“…Previous studies on several tissues of hibernating rodents revealed that the cell nucleus undergoes important structural reorganization during the hypometabolic period: RNA transcription and maturation factors redistribute among the nuclear constituents; various nuclear bodies, which contain splicing factors, do form during the lethargic period and disappear upon arousal; the nucleolus undergoes structural and molecular modifications (Malatesta et al, 2007(Malatesta et al, , 2008. In particular, during hibernation, the nucleolus is characterized by irregular shapes due to many nucleoplasmic invaginations, which sometimes contain weakly contrasted areas of unknown nature.…”

Section: Introductionmentioning

confidence: 99%

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Immunoelectron microscopic characterization of nucleolus‐associated domains during hibernation

Malatesta

Zancanaro

Biggiogera

2010

Microscopy Res & Technique

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The nucleolus represents a highly dynamic nuclear compartment involved in multiple functions and able to promptly respond to variations of metabolic needs. In the hibernator dormouse, which drastically modifies its metabolic activity during the seasonal cycle, the nucleolus undergoes structural and molecular changes during the torpor bouts; in particular, it shows many nucleoplasmic invaginations containing weakly contrasted areas of unknown nature. To analyze the molecular composition of these nucleolus-associated domains (NADs) and to understand their functional significance, the fine nucleolar composition has been investigated by means of ultrastructural immunocytochemistry in different tissues of euthermic, hibernating, and arousing hazel dormice (Muscardinus avellanarius): in particular, the intranucleolar location of several protein factors involved in the transcription and processing of either pre-rRNA or pre-mRNA has been considered. NADs proved to form during hibernation and disappear upon arousal and were found to contain m₃-G-capped snRNAs, snRNPs, hnRNPs, and the survival motor neuron protein; they were, on the contrary, devoid of the nucleolar factors tested (polymerase I, fibrillarin, nucleolin, and the ribosomal phosphoproteins P₀, P₁, and P₂). We hypothesize that NADs may represent a transient storage site for those molecules involved in the pre-mRNA splicing, which usually transit through the nucleolus; upon arousal, this would facilitate the resumption of RNA maturation by promoting the rapid reactivation of the molecular trafficking from the nucleolus.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Immunoelectron microscopic characterization of nucleolus‐associated domains during hibernation

Malatesta

Zancanaro

Biggiogera

2010

Microscopy Res & Technique

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“…Natural hypothermia occurs in the majority of mammalian families, suggesting that torpor may be possible for many, if not all, mammals (Heldmaier et al 2004). Torpor physiology has recently attracted increased attention for its potential therapeutic applications (Carey et al 2003), which include neuroprotection in cardiac-arrest patients, preservation of organs for transplantation, and the treatment of neurodegenerative diseases like Alzheimer's (Malatesta et al 2007).…”

Section: Introductionmentioning

confidence: 99%

Daily torpor in mice: high foraging costs trigger energy-saving hypothermia

et al. 2009

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Many animal species employ natural hypothermia in seasonal (hibernation) and daily (torpor) strategies to save energy. Facultative daily torpor is a typical response to fluctuations in food availability, but the relationship between environmental quality, foraging behaviour and torpor responses is poorly understood. We studied body temperature responses of outbred ICR (CD-1) mice exposed to different food reward schedules, simulating variation in habitat quality. Our main comparison was between female mice exposed to low foragingcost environments and high-cost environments. As controls, we pair-fed a group of inactive animals (no-cost treatment) the same amount of pellets as high-cost animals. Mice faced with high foraging costs were more likely to employ torpor than mice exposed to low foraging costs, or no-cost controls (100% versus 40% and 33% of animals, respectively). While resting-phase temperature showed a non-significant decrease in high-cost animals, torpor was not associated with depressions in active-phase body temperature. These results demonstrate (i) that mice show daily torpor in response to poor foraging conditions; (ii) that torpor incidence is not attributable to food restriction alone; and (iii) that high levels of nocturnal activity do not preclude the use of daily torpor as an energy-saving strategy. The finding that daily torpor is not restricted to conditions of severe starvation puts torpor in mice in a more fundamental ecological context.

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“…These animals are, in fact, able to drastically lower their body temperature and to reduce all metabolic and physiological activities, thus facilitating survival under adverse environmental conditions; however, as soon as the situation reverts to favorable conditions, they leave the depressed metabolic state restoring the euthermic functions in a short time (Lyman et al, 1982). Previous studies on several tissues of hibernating rodents revealed that the cell nucleus undergoes important structural reorganization during the hypometabolic period; various nuclear bodies containing transcription and splicing factors do form during the lethargic period and disappear upon arousal, and the nucleolus undergoes structural and molecular modifications as well (reviews in Malatesta et al, 2005Malatesta et al, , 2007. However, the nuclear structural constituents involved in pre-mRNA transcription and processing do not show evident morphological modifications during hibernation, despite the severe inhibition of the transcriptional activity (van Breukelen and Martin, 2002).…”

Section: Introductionmentioning

confidence: 99%

Hibernation as a far‐reaching program for the modulation of RNA transcription

Malatesta

Biggiogera

Baldelli

et al. 2008

Microscopy Res & Technique

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In eukaryotic cells, pre-mRNAs undergo several transformation steps to generate mature mRNAs ready to be exported to the cytoplasm. The molecular and structural apparatus for mRNA production is generally able to promptly respond to variations of metabolic demands. Hibernating mammals, which periodically enter a hypometabolic state, represent an interesting physiological model to investigate the adaptive morpho-functional modifications of the pre-mRNA transcriptional and processing machinery under extreme metabolic conditions. In this study, the subnuclear distribution of some transcriptional, splicing, and cleavage factors was investigated by ultrastructural immunocytochemistry in cell nuclei of the liver (a highly metabolizing organ involved in multiple regulatory functions) and the brown adipose tissue (responsible for nonshivering thermogenesis) from euthermic, hibernating, and arousing hazel dormice (Muscardinus avellanarius). Our observations demonstrate that, during hibernation, transcriptional activity significantly decreases and pre-mRNA processing factors undergo an intranuclear redistribution moving to domains usually devoid of such molecules; moreover, in hepatocytes, there is a preferential accumulation of pre-mRNAs at the splicing stage, whereas, in brown adipocytes, pre-mRNAs are mainly stored at the cleavage stage. Upon arousal, the pre-mRNAs at the cleavage stage are immediately utilized, while the maturation of pre-mRNAs at the splicing stage seems to be restored before transcription had taken place. Our data suggest a programmed intranuclear reorganization of the RNA maturation machinery aimed at efficiently and rapidly restoring the pre-mRNA processing, and, consequently, the specific cellular activities upon arousal. Once again natural hibernation appears as a highly programmed hypometabolic state rather than a simple fall of metabolic and physiological functions.

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Hypometabolic induced state: a potential tool in biomedicine and space exploration

Cited by 15 publications

References 110 publications

Immunoelectron microscopic characterization of nucleolus‐associated domains during hibernation

Immunoelectron microscopic characterization of nucleolus‐associated domains during hibernation

Daily torpor in mice: high foraging costs trigger energy-saving hypothermia

Hibernation as a far‐reaching program for the modulation of RNA transcription

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