Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor

2004 ◽  
Vol 287 (2) ◽  
pp. R349-R353 ◽  
Author(s):  
Frank van Breukelen ◽  
Nahum Sonenberg ◽  
Sandra L. Martin
Keyword(s):  
Ground Squirrel ◽  
Ground Squirrels ◽  
Translational Initiation ◽  
Spermophilus Lateralis ◽  
Initiation Factors ◽  
Eukaryotic Initiation Factors ◽  
State Dependent ◽  
Initiation Of Translation ◽  
Significant Locus ◽  
Mammalian Hibernation

Mammalian hibernation involves cessation of energetically costly processes typical of homeostatic regulation including protein synthesis. To further elucidate the mechanisms employed in depressing translation, we surveyed key eukaryotic initiation factors [eIF2, eIF4B, eIF4E, eIF4GI and -II, and 4E-binding protein-1 (4E-BP1), -2, and -3] for their availability and phosphorylation status in the livers of golden-mantled ground squirrels (Spermophilus lateralis) across the hibernation cycle. Western blot analyses indicated only one significant locus for regulation of translational initiation in ground squirrel liver: control of eIF4E. We found seasonal variation in a potent regulator of eIF4E activity, 4E-BP1. Summer squirrels lack 4E-BP1 and apparently control eIF4E activity through direct phosphorylation. In winter, eIF4E is regulated through binding with 4E-BP1. During the euthermic periods that separate bouts of torpor (interbout arousal), 4E-BP1 is hyperphosphorylated to promote initiation. However, during torpor, 4E-BP1 is hypophosphorylated and cap-dependent initiation of translation is restricted. The regulation of cap-dependent initiation of translation may allow for the differential expression of proteins directed toward enhancing survivorship.

scholarly journals Preference of IRES-mediated initiation of translation during hibernation in golden-mantled ground squirrels, Spermophilus lateralis

2011 ◽  
Vol 301 (2) ◽  
pp. R370-R377 ◽  
Author(s):  
Peipei Pan ◽  
Frank van Breukelen
Keyword(s):  
Gene Expression ◽  
Internal Ribosome Entry Site ◽  
Stress Proteins ◽  
Ground Squirrels ◽  
Entry Site ◽  
Internal Ribosome Entry ◽  
Spermophilus Lateralis ◽  
Preference Index ◽  
Initiation Of Translation ◽  
Mammalian Hibernation

Mammalian hibernation involves virtual cessation of energetically consumptive processes normally vital to homeostasis, including gene transcription and protein synthesis. As animals enter torpor, the bulk of initiation of translation is blocked at a body temperature of 18°C in golden-mantled ground squirrels [ Spermophilus (Callospermophilus) lateralis ]. Previous data demonstrated regulation of cap-dependent initiation of translation during torpor. We asked what happens to cap-independent, specifically, internal ribosome entry site (IRES)-mediated initiation of translation during hibernation. We analyzed polysome fractions for mRNAs that are known to contain or not to contain IRES elements. Here, we show that mRNAs harboring IRES elements preferentially associate with ribosomes as a torpor bout progresses. Squirrels allowed to naturally complete a torpor cycle have a higher IRES preference index than those animals that are prematurely aroused from torpor. Data indicate that this change in preference is not associated with gene expression, i.e., change is due to change in mRNA association with ribosomes as opposed to mRNA abundance. Thus, although processes like transcription and translation are virtually arrested during torpor, ribosomes are preferentially loaded with IRES-containing transcripts when squirrels arouse from torpor and translation resumes. Differential translation of preexisting mRNAs may allow for the preferential production of key stress proteins critical for survival of physiological insults that are lethal to other mammals.

Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation

2001 ◽  
Vol 281 (5) ◽  
pp. R1374-R1379 ◽  
Author(s):  
Frank van Breukelen ◽  
Sandra L. Martin
Keyword(s):  
Protein Synthesis ◽  
Protein Biosynthesis ◽  
Distribution Patterns ◽  
Reaction Rates ◽  
Ground Squirrels ◽  
Translational Initiation ◽  
Spermophilus Lateralis ◽  
Complete Restoration ◽  
New Protein ◽  
Mammalian Hibernation

Cellular and organismal homeostasis must be maintained across a body temperature (Tb) range of 0 to 37°C during mammalian hibernation. Hibernators depress biosynthetic activities including protein synthesis, concordant with limited energy availability and temperature effects on reaction rates. We used polysome analysis to show that initiation of protein synthesis ceases during entrance into torpor in golden-mantled ground squirrels ( Spermophilus lateralis) when Tb reaches 18°C. Elongation of preinitiated polypeptides continues slowly throughout the torpor bout. As Tb begins to rise, initiation resumes even at temperatures below 18°C, although the euthermic polysome pattern is not reestablished. At precisely 18°C, there is a large increase in initiation events and a complete restoration of euthermic polysome distribution patterns. These data indicate a role for both passive and active depression of translation during torpor and are consistent with a requirement for new protein biosynthesis during each interbout arousal.

Growth and its relationship to the initial annual cycle of the golden-mantled ground squirrel, Spermophilus lateralis

1981 ◽  
Vol 59 (6) ◽  
pp. 865-871 ◽  
Author(s):  
John A. Phillips
Keyword(s):  
Litter Size ◽  
Annual Cycle ◽  
Ground Squirrel ◽  
Growth And Development ◽  
Reproductive Effort ◽  
Ground Squirrels ◽  
Active Season ◽  
Spermophilus Lateralis ◽  
Significant Difference ◽  
Two Populations

Thirty-eight litters of golden-mantled ground squirrels (Spermophilus lateralis), from two populations that experienced different lengths of active season, were born and raised in the laboratory. Growth and development in young were inversely related to litter size. Offspring from smaller litters were both able to attain their prehibernation peak of body mass sooner and hibernate after fewer days of homeothermy than squirrels from larger litters. Young that remained homeothermic throughout the initial overwintering period were always from large litters and among the slowest growing littermates. Fecundity was lower in females from the temporally compressed environment. There was no significant difference between populations in the nutrition provided by mothers to their litters. The results suggest that reproductive effort is more conservative in populations of ground squirrels that experience short seasons of activity, yet this conservatism allows the offspring of those populations to reach independence and attain the prehibernation state of preparedness at an earlier age than their counterparts from populations of more moderate climates.

Temperature dependence of in vitro androgen production in testes from hibernating ground squirrels, Spermophilus lateralis

1987 ◽  
Vol 65 (12) ◽  
pp. 3020-3023 ◽  
Author(s):  
Brian M. Barnes ◽  
Paul Licht ◽  
Irving Zucker
Keyword(s):  
Ground Squirrel ◽  
Temperature Compensation ◽  
Laboratory Mouse ◽  
Ground Squirrels ◽  
The Body ◽  
Effect Of Temperature ◽  
Dependent Manner ◽  
Spermophilus Lateralis ◽  
Dose Dependent

The effect of temperature on the in vitro androgen secretion of testes from hibernating ground squirrels was measured in response to stimulation by luteinizing hormone (LH). We wished to determine whether hibernating ground squirrels can maintain responsiveness of gonads while at the low body temperatures of torpor. In gonads incubated at 32 °C, secretion of testosterone increased in a dose-dependent manner in response to ovine-LH or ground squirrel pituitary homogenate. This responsiveness was reduced at 20 and 9 °C and absent at 5 °C, the temperature that most closely approximates the body temperature of torpid ground squirrels. This temperature sensitivity was similar to that in the nonhibernating laboratory mouse. Superfusion of ground squirrel testes revealed a lag of testosterone secretion in response to LH and, additionally, an ability of testes to secrete testosterone after being only briefly exposed to ovine-LH while at 5 °C. These results provide evidence against a hypothesis of temperature compensation that would allow continued testis function during torpor, and support a previous study which indicated that gonadal growth is restricted to intervals of normothermy during and after the hibernation season.

scholarly journals Hibernation-associated gene regulation of plasma proteins with a collagen-like domain in mammalian hibernators.

1993 ◽  
Vol 13 (3) ◽  
pp. 1516-1521 ◽  
Author(s):  
N Takamatsu ◽  
K Ohba ◽  
J Kondo ◽  
N Kondo ◽  
T Shiba
Keyword(s):  
Gene Regulation ◽  
Ground Squirrel ◽  
Plasma Proteins ◽  
Molecular Mechanisms ◽  
Ground Squirrels ◽  
First Line ◽  
N Terminus ◽  
Tree Squirrel ◽  
Related Proteins ◽  
Mammalian Hibernation

In mammals, hibernation is expressed by only a limited number of species, and the molecular mechanisms underlying hibernation are not well understood. Recently, we have found plasma proteins which disappear from blood specifically during hibernation in a mammalian hibernator, the chipmunk. Here, we report the cDNA cloning of these chipmunk hibernation-related proteins, HP-20, -25, and -27, and analyses of their expression. All three proteins contain a collagen-like domain near the N terminus and are highly homologous to each other. Their mRNAs were detected only in liver in nonhibernating chipmunks, and in hibernating chipmunks, the amounts were reduced to less than 1/10 of those in nonhibernating chipmunks, indicating that HP-20, -25, and -27 mRNA expression is regulated similarly in association with hibernation. Southern blot analyses of the squirrel family with each of chipmunk HP-20, -25, and -27 cDNA revealed that a nonhibernating species (tree squirrel) as well as another hibernating species (ground squirrel) retained the corresponding genes. However, their transcripts were detected only with the hibernating species, and in hibernating ground squirrels, their levels were greatly reduced compared with those in nonhibernating animals, as were the cases with the chipmunk. These observations are the first line of evidence for occurrence of hibernation-associated gene regulation. The results would indicate the commitment of HP-20, -25, and -27 to hibernation and support the idea that genetic controls are involved in mammalian hibernation.

Hibernation-associated gene regulation of plasma proteins with a collagen-like domain in mammalian hibernators

1993 ◽  
Vol 13 (3) ◽  
pp. 1516-1521
Author(s):  
N Takamatsu ◽  
K Ohba ◽  
J Kondo ◽  
N Kondo ◽  
T Shiba
Keyword(s):  
Gene Regulation ◽  
Ground Squirrel ◽  
Plasma Proteins ◽  
Molecular Mechanisms ◽  
Ground Squirrels ◽  
First Line ◽  
N Terminus ◽  
Tree Squirrel ◽  
Related Proteins ◽  
Mammalian Hibernation

In mammals, hibernation is expressed by only a limited number of species, and the molecular mechanisms underlying hibernation are not well understood. Recently, we have found plasma proteins which disappear from blood specifically during hibernation in a mammalian hibernator, the chipmunk. Here, we report the cDNA cloning of these chipmunk hibernation-related proteins, HP-20, -25, and -27, and analyses of their expression. All three proteins contain a collagen-like domain near the N terminus and are highly homologous to each other. Their mRNAs were detected only in liver in nonhibernating chipmunks, and in hibernating chipmunks, the amounts were reduced to less than 1/10 of those in nonhibernating chipmunks, indicating that HP-20, -25, and -27 mRNA expression is regulated similarly in association with hibernation. Southern blot analyses of the squirrel family with each of chipmunk HP-20, -25, and -27 cDNA revealed that a nonhibernating species (tree squirrel) as well as another hibernating species (ground squirrel) retained the corresponding genes. However, their transcripts were detected only with the hibernating species, and in hibernating ground squirrels, their levels were greatly reduced compared with those in nonhibernating animals, as were the cases with the chipmunk. These observations are the first line of evidence for occurrence of hibernation-associated gene regulation. The results would indicate the commitment of HP-20, -25, and -27 to hibernation and support the idea that genetic controls are involved in mammalian hibernation.

Social behaviour of the golden-mantled ground squirrel (Spermophilus lateralis)

1985 ◽  
Vol 63 (11) ◽  
pp. 2529-2533 ◽  
Author(s):  
Jean Ferron
Keyword(s):  
Social Interactions ◽  
Rocky Mountains ◽  
Ground Squirrel ◽  
Ground Squirrels ◽  
Agonistic Interactions ◽  
Natural Conditions ◽  
Spermophilus Lateralis ◽  
The Social ◽  
Age And Sex

The social interactions of golden-mantled ground squirrels (Spermophilus lateralis) observed during a 2-year study in the Rocky Mountains of Alberta under natural conditions are described and quantitatively analyzed. Agonistic interactions were common for all age and sex groups, except among littermates before dispersal. Among adults, cohesive and recognitive behaviours were restricted almost exclusively to male–female interactions. For young, cohesive and recognitive behaviours occurred with other young (mainly littermates) and with the mother. This species can be categorized as "asocial" according to G. R. Michener's classification of social organization in ground squirrels.

scholarly journals Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis)

2010 ◽  
Vol 12 (1) ◽  
pp. 285-296 ◽  
Author(s):  
Mary Brooke McEachern ◽  
Dirk H. Van Vuren ◽  
Chris H. Floyd ◽  
Bernie May ◽  
John M. Eadie
Keyword(s):  
Ground Squirrels ◽  
Spermophilus Lateralis
Sign in / Sign up

Export Citation Format

Share Document