Expression of a chimeric retroviral-lipase mRNA confers enhanced lipolysis in a hibernating mammal

Bauer, Vernon W.; Squire, Teresa L.; Lowe, Mark E.; Andrews, Matthew T.

doi:10.1152/ajpregu.2001.281.4.r1186

Cited by 35 publications

(57 citation statements)

References 32 publications

(21 reference statements)

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“…Pancreatic lipase mRNA and protein activity are also induced in white adipose tissue of hibernators, although it appears to be a distinct gene from the one induced in heart (4). The mRNA for hormone-sensitive lipase is differentially regulated in hibernators (4,96), again consistent with an enhanced role for fatty acid metabolism during hibernation. Other reports of upregulated mRNAs in hibernators include uncoupling protein 2 (UCP2) in white adipose tissue and UCP3 in muscle (12), NADH-ubiquinone oxidoreductase subunit 2 and ventricular myosin light chain 1 in heart (24), and glyceraldehyde-3-phosphate dehydrogenase in liver (77).…”

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confidence: 53%

Invited Review: Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?

Breukelen

Martin

2002

Journal of Applied Physiology

117

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are unique among mammals in their ability to attain, withstand, and reverse low body temperatures. Hibernators repeatedly cycle between body temperatures near zero during torpor and 37°C during euthermy. How do these mammals maintain cardiac function, cell integrity, blood fluidity, and energetic balance during their prolonged periods at low body temperature and avoid damage when they rewarm? Hibernation is often considered an example of a unique adaptation for low-temperature function in mammals. Although such adaptation is apparent at the level of whole animal physiology, it is surprisingly difficult to demonstrate clear examples of adaptations at the cellular and biochemical levels that improve function in the cold and are unique to hibernators. Instead of adaptation for improved function in the cold, the key molecular adaptations of hibernation may be to exploit the cold to depress most aspects of biochemical function and then rewarm without damage to restore optimal function of all systems. These capabilities are likely due to novel regulation of biochemical pathways shared by all mammals, including humans. torpor; hypothermia; differential gene expression WHEN A HUMAN IS EXPOSED TO low environmental temperatures and body temperature begins to fall, hypothermia ensues: the shivering response fails at a body temperature of 30-32°C, the heart fibrillates at 27-29°C, and ventilation ceases at 23-27°C, leading to death (reviewed in Refs. 47 and 48). However, a myriad of mammals avoid the damage associated with hypothermia by evoking controlled excursions to reduced body temperatures called torpor. In contrast to hypothermia, the reduction of body temperature in hibernators is not a patholological state (56). Deep hibernators are the masters of this adaptive hypothermia because they can maintain body temperatures below 0°C for up to 3 wk (2, 26, 34). Key characteristics of torpor include a profound reduction of metabolism (up to 1/100th of basal metabolic rate), reduced heart rate, and extremely low body temperature (reviewed in Ref. 90). The physiological consequences associated with hibernation provide a natural model for the study of ischemia, muscle and bone disuse atrophy, hypothermia, ketosis, organ transplant therapy, obesity, kidney failure, and cardiac arrhythmogenesis (e.g., Refs. 18,28,70,93,95).Ground-dwelling sciurid rodents have become the favorite model organisms for recent laboratory studies to explore the molecular bases of mammalian hibernation. In nature, these species exhibit a strict circannual rhythm of reproduction, fattening, and hibernation (for review, see Ref. 49). The cycle begins in the spring with mating, gestation, and birth. The seasons' young are

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confidence: 53%

Invited Review: Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?

Breukelen

Martin

2002

Journal of Applied Physiology

117

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“…(35) The significance of this insertion is that it may play a role in the hibernation-specific activation of the PTL gene in non-pancreatic tissues. (35) Novel expression of PTL in heart (8) and white adipose tissue (36) provides continuous low-temperature lipolysis unaffected by hormonal fluctuations that normally influence the activity of the standard mammalian lipase found in these tissues, hormone-sensitive lipase (HSL). (36) PTL has 75-fold greater activity than HSL and offers an example of a common gastrointestinal (GI) enzyme that is seasonally activated in novel locations to provide a steady stream of fatty acids at low body temperatures.…”

Section: Metabolic Oscillationsmentioning

confidence: 99%

Advances in molecular biology of hibernation in mammals

2007

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Mammalian hibernation is characterized by profound reductions in metabolism, oxygen consumption and heart rate. As a result, the animal enters a state of suspended animation where core body temperatures can plummet as low as -2.9 degrees C. Not only can hibernating mammals survive these physiological extremes, but they also return to a normothermic state of activity without reperfusion injury or other ill effects. This review examines recent findings on the genes, proteins and small molecules that control the induction and maintenance of hibernation in mammals. The molecular events involved with remodeling metabolism, inducing hypothermia and maintaining organ function are discussed and considered with respect to analogous processes in non-hibernating mammals such as mice and humans. The advent of sequenced genomes from three distantly related hibernators, a bat, hedgehog and ground squirrel, provides additional opportunities for molecular biologists to explore the mechanistic aspects of this biological adaptation in greater detail.

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“…The expression of a given retrovirus in such tissue should impart a benefit to the progeny of those individuals in which integration into their germ lineage occurred. Such are the cases, 8 for the gene encoding an enzyme that enhances lipolysis in hibernating mammal and for that encoding one of the two receptors that mediate the effects of endothelin. On the contrary, aberrant expression of the same retroviruses in other tissues would be detrimental.…”

Section: Introductionmentioning

confidence: 99%

Characterization of the human CD5 endogenous retrovirus-E in B lymphocytes

Renaudineau¹,

Vallet²,

Dantec³

et al. 2005

Genes Immun

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All T lymphocytes and some B lymphocytes express CD5. This coreceptor is encoded by one gene that consists of 11 exons. We have previously described a B cell-specific alternative exon 1, leading to the synthesis of a protein, devoid of leader peptide, and, therefore, retained in the cytoplasm. The novel exon 1 originates from a human endogenous retrovirus (HERV) at a time interval between the divergence of New World monkeys from Old World monkeys, and prior to the divergence of humans from Old World monkeys. Based on sequence similarity to g-retroviruses, it was categorized as class I: based on the specificity of its primer binding site, it was allotted to the subclass E, and based on its location within the cd5 gene, named HERV-E.CD5. Alternative transcripts were detected in lymphoid organs including fetal liver (not adult liver), more particularly in CD5-negative cell surface B-1b than in CD5-positive cell surface B-1a, and not at all in B-2 cells. By alignment of 5 0 long terminal repeats, HERV-E.CD5 was distinguished from similar proviruses. This could be central to the regulation of membrane expression of CD5 in human B lymphocytes, and, thereby, to the strength of the B-cell antigen receptor signaling.

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Expression of a chimeric retroviral-lipase mRNA confers enhanced lipolysis in a hibernating mammal

Cited by 35 publications

References 32 publications

Invited Review: Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?

Invited Review: Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?

Advances in molecular biology of hibernation in mammals

Characterization of the human CD5 endogenous retrovirus-E in B lymphocytes

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