Skip to main content
SpringerLink
Log in

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

  • Review Paper
  • Chapter
  • First Online:
Life in Extreme Environments

  • 2307 Accesses

Abstract

This paper will first review the issue of hypometabolism in mammals with a focus on the strategies these animals evolved to cope with life challenge in hostile environments (e.g., cold weather and/or shortage of food). The different types of natural hypometabolism (hibernation, torpor, winter sleep) will be briefly described as well as major adaptations in body temperature, and energy and cell metabolism. In the second part of this review the issue of inducing a hypometabolic state in mammals will be afforded with special attention paid to changes in body temperature and metabolism, regulation of gene expression and the possible role of hibernation inducing factors. Finally, an overview of the potential of inducing a hypometabolic state in the human as related to the broad field of biomedicine will be given.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ahonen J, Salmenpera M (2004) Brain injury after adult cardiac surgery. Acta Anaesthesiol Scand 48:4–19

    Article  PubMed  CAS  Google Scholar 

  • Alam HB, Bowyer MW, Koustova E, Gushchin V, Anderson D, Stanton K, Kreishman P, Cryer CM, Hancock T, Rhee P (2002) Learning and memory is preserved after induced asanguineous hyperkalemic hypothermic arrest in a swine model of traumatic exsanguination. Surgery 132:278–288

    Article  PubMed  Google Scholar 

  • Andrews MT, Squire TL, Bowen CM, Rollins MB (1998) Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc Natl Acad Sci USA 95:8392–8397

    Article  PubMed  CAS  Google Scholar 

  • Arendt T, Stieler J, Strijkstra AM, Hut RA, Rudiger J, Van der Zee EA, Harkany T, Holzer M, Hartig W (2003) Reversible paired helical filament-like phosphotylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 23:6972–6981

    PubMed  CAS  Google Scholar 

  • Ayre M, Zancanaro C, Malatesta M (2004) Morpheus-hypometabolic stasis for long-term spaceflight. J Brit Interplan Soc 57:325–339

    Google Scholar 

  • Baldelli B, Vecchio L, Biggiogera M, Vittoria E, Muzzonigro G, Gazzanelli G, Malatesta M (2004) Ultrastructural and immunocytochemical analyses of opioid treatment effects on PC3 prostatic cancer cells. Microsc Res Tech 64:243–249

    Article  PubMed  CAS  Google Scholar 

  • Baldelli B, Vecchio L, Bottone MG, Muzzonigro G, Biggiogera M, Malatesta M (2006) The effect of the enkephalin DADLE on transcription does not depend on opioid receptors. Histochem Cell Biol. In press

    Google Scholar 

  • Barger JL, Brand MD, Barnes BM, Boyer BB (2003) Tissue-specific depression of mitochondrial proton leak and substrate oxidation in hibernating arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 284:R1306–R1313

    PubMed  CAS  Google Scholar 

  • Baumber J, South FE, Ferren L, Zatznan ML (1971) A possible basis for periodic arousals during hibernation: accumulation of ketone bodies. Life Sci 10:462–467

    Article  Google Scholar 

  • Benedict PE, Benedict MB, Su TP, Bolling SF (1999) Opiate drugs and delta-receptor-mediated myocardial protection. Circulation 100:357–360

    CAS  Google Scholar 

  • Biggiogera M, Fabene P, Zancanaro C (2006) DADLE: a cue to human hibernation? J Brit Interplan Soc 59:115–118

    Google Scholar 

  • Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518

    Article  PubMed  CAS  Google Scholar 

  • Bolling K, Kronon M, Allen BS, Wang T, Ramon S, Feinberg H (1997a) Myocardial protection in normal and hypoxically stressed neonatal hearts: the superiority of blood versus crystalloid cardioplegia. J Thorac Cardiovasc Surg 113:994–1003

    Article  CAS  Google Scholar 

  • Bolling K, Halldorsson A, Allen BS, Rahman S, Wang T, Kronon M, Feinberg H (1997b) Prevention of the hypoxic reoxygenation injury with the use of a leukocyte-depleting filter. J Thorac Cardiovasc Surg 113:1081–1089

    Article  CAS  Google Scholar 

  • Bolling SF, Benedict MB, Tramontini NL, Kilgore KS, Harlow HH, Su TP, Oeltgen PR (1998) Hibernation triggers and myocardial protection. Circulation 98:220–223

    Google Scholar 

  • Boswell T, Richardson RD, Schwartz MW, D’Alessio DA, Woods SC, Sipols AJ, Baskin DG, Kenagy GJ (1993) NPY and galanin in a hibernator: hypothalamic gene expression and effects on feeding. Brain Res Bull 32:379–384

    Article  PubMed  CAS  Google Scholar 

  • Boutilier RG (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171–3181

    PubMed  CAS  Google Scholar 

  • Bronnikov GE, Vinogradova SO, Chernyak BV (1990) Regulation of ATP hydrolysis in liver mitochondria from ground squirrel. FEBS 266:8386

    Article  Google Scholar 

  • Buck CL, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol Regul Integr Comp Physiol 279:R255–R262

    PubMed  CAS  Google Scholar 

  • Burks TF (1991) Opioid and opioid receptors in thermoregulation. In: Thermoregulation:pathology, pharmacology, biosynthesis and analysis. Pergamon Press, NY, pp 489–508

    Google Scholar 

  • Carey HV, Frank CL, Seifert JP (2000) Hibernation induces oxidative stress and activation of NK-kappaB in ground squirrel intestine. J Comp Physiol 170B:551–559

    CAS  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    PubMed  CAS  Google Scholar 

  • Chen Z, Chen H, Rhee P, Koustova E, Ayuste EC, Honma K, Nadel A, Alam HB (2005) Induction of profound hypothermia modulates the immune/inflammatory response in a swine model of lethal hemorrhage. Resuscitation 66:209–216

    Article  PubMed  Google Scholar 

  • Chien SF, Oeltgen PR, Diana JN, Salley RK, Su TP (1994) Extension of tissuesurvival time in multiorgan block preparation using a delta opioid DADLE. J Thorac Cardiovasc Surg 107:964–967

    PubMed  CAS  Google Scholar 

  • Clifton GL, Miller ER, Choi SC, Levin HS, McCauley S, Smith KR Jr, Muizelaar JP, Wagner FC Jr, Marion DW, Luerssen TG, Chesnut RM, Schwartz M (2001) Lack of effect of induction of hypothermia after acute brain injury. N Engl J Med 344:556–563

    Article  PubMed  CAS  Google Scholar 

  • Collins DL (2003) Psychological issues relevant to astronaut selection for long-duration space flight: a review of the literature. Hum Perf Extrem Environ Spring 7:43–67

    Google Scholar 

  • Cooper KE (2002) Molecular biology of thermoregulation – some historical perspectives on thermoregulation. J Appl Physiol 92:1717–1724

    PubMed  CAS  Google Scholar 

  • Cui Y, Lee TF, Wang LCH (1996) State-dependent changes of brain endogenous opioids in mammalian hibernation. Brain Res Bull 40:129–133

    Article  PubMed  CAS  Google Scholar 

  • D’Alecy LG, Lundy EF, Kluger MJ, Harker CT, LeMay DR, Shlafer M (1990) Beta-hydroxybutyrate and response to hypoxia in the ground squirrel, Spermophilus tridecimlineatus. Comp Biochem Physiol 96B:189–193

    Article  CAS  Google Scholar 

  • Daan S, Bernes BM, Strijkstra AM (1991) Warming up for sleep? Ground squirrels sleep during arousal from hibernation. Neurosci Lett 128:265–268

    Article  PubMed  CAS  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826

    Article  PubMed  CAS  Google Scholar 

  • Di Carli MF, Prcevski P, Singh TP, Janisse J, Ager J, Muzik O, Vander Heide R (2000) Myocardial blood flow, function, and metabolism in repetitive stunning. J Nucl Med 41:1227–1234

    PubMed  Google Scholar 

  • Donahue SW, McGee ME, Harvey KB, Vaughan MR, Robbins CT (2005) Hibernating bears as a model for preventing disuse osteoporosis. J Biomech doi:10.1016/j.jbiomech.2005.03.030

    Google Scholar 

  • Drew KL, Rice ME, Kuhn TB, Smith MA (2001) Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases. Free Radic Biol Med 31:563–573

    Article  PubMed  CAS  Google Scholar 

  • Eddy SF, Storey KB (2003) Differential expression of Akt, PPARgamma, and PGC-1 during hibernation in bats. Biochem Cell Biol 81:269–274

    Article  PubMed  CAS  Google Scholar 

  • Fitts RH, Riley DR, Widrick JJ (2001) Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204:3201–3208

    PubMed  CAS  Google Scholar 

  • French AR (1988) The patterns of mammalian hibernation. Am Sci 76:569–575

    Google Scholar 

  • Galster W, Morrison PR (1975) Gluconeogenesis in arctic squirrels between periods of hibernation. Am J Physiol 228:325–330

    PubMed  CAS  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  PubMed  CAS  Google Scholar 

  • Geiser F, McAllan BM, Kenagy GJ (1994) The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J Comp Physiol 164:299–305

    CAS  Google Scholar 

  • Gertsberger R (1999) Nitric oxide and body temperature control. News Physiol Sci 14:30–36

    Google Scholar 

  • Giesbrecht GG, Goheen MS, Johnston CE, Kenny GP, Bristow GK, Hayward JS (1997) Inhibition of shivering increases core temperature afterdrop and attenuates rewarming in hypothermic humans. J Appl Physiol 83:1630–1634

    PubMed  CAS  Google Scholar 

  • Giacometti S, Scherini E, Bernocchi G (1989) Seasonal changes in the nucleoli of Purkinje cells of the hedgehog cerebellum. Brain Res 488:365–368

    Article  PubMed  CAS  Google Scholar 

  • Heldmaier G, Steinlechner S, Ruf T, Wiesinger H, Klingenspor M (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhytms 4:251–265

    CAS  Google Scholar 

  • Heldmaier G, Klingenspor M, Werneyer M, Lampi BJ, Brooks SP, Storey KB (1999) Metabolic adjustements during daily torpor in the Djungarian hamster. Am J Physiol 276:E896–E906

    PubMed  CAS  Google Scholar 

  • Heller HC (1979) Hibernation: neural aspects. Annu Rev Physiol 41:305–321

    Article  PubMed  CAS  Google Scholar 

  • Himms-Hagen J (1986) Brown adipose tissue and cold acclimatation. In: Trayhurn P, Nicholls DG (eds) Brown adipose tissue. Edward Arnold, London, pp 214–268

    Google Scholar 

  • Hittel DS, Storey KB (2002) The translation state of differentially expressed mRNAs in the hibernating 13-lined ground squirrel (Spermophilus tridecemlineatus). Arch Biochem Biophys 401:244–254

    Article  PubMed  CAS  Google Scholar 

  • Hochachka PW, Buck L, Doll C, Laand S (1996) Unifying theory of hypoxia tolerance: defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493–9498

    Article  PubMed  CAS  Google Scholar 

  • Hong J, Sigg DC, Coles JA Jr, Oeltgen PR, Harlow HJ, Soule CL, Iaizzo PA (2005) Hibernation induction trigger reduces hypoxic damage of swine skeletal muscle. Muscle Nerve 32:200–207

    Article  PubMed  Google Scholar 

  • Horwitz BA, Hamilton JS, Kott KS (1985) GDP binding to hamster brown fat mitochondria is reduced during hibernation. Am J Physiol 249:R689–R693

    PubMed  CAS  Google Scholar 

  • Hu H, Miyauchi S, Bridges CC, Smith SB, Ganapathy V (2003) Identification of a novel Na+-and Cl−-coupled transport system for endogenous opioid peptides in retinal pigment epithelium and induction of the transport system by HIV-1 Tat. Biochem J 375:17–22

    Article  PubMed  CAS  Google Scholar 

  • Hypothermia after Cardiac Arrest Study Group (2002) Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 346:549–56. Erratum in: N Engl J Med 2002 346:1756

    Google Scholar 

  • Johansson BW (1996) The hibernator heart – nature’s model of resistance to ventricular fibrillation. Cardiov Res 31:826–832

    Article  CAS  Google Scholar 

  • Kabine M, Clemencet MC, Bride J, El Kebbaj M-S, Latruffe N, Cherkaoui-Malki M (2003) Changes of peroxisomal fatty acid metabolism during cold acclimatization in hibernating jerboa (Jaculus orientalis). Biochimie 85:707–714

    Article  PubMed  CAS  Google Scholar 

  • Kampa M, Bakogeorgou E, Hatzoglou A, Damianaki A, Martin P-M, Castanas E (1997) Opioid alkaloids and casomorphin peptides decrease the proliferation of prostatic cancer cell lines (LNCaP, PC3 and DU145) through a partial interaction with opioid receptors. Eur J Pharmacol 335:255–265

    Article  PubMed  CAS  Google Scholar 

  • Knight JE, Narus EN, Martin SL, Jacobson A, Barnes BM, Boyer BB (2000) mRNA stability and polysome loss in hibernating Arctic ground squirrels (Spermophilus parryii). Mol Cell Biol 20:6374–6379

    Article  PubMed  CAS  Google Scholar 

  • Kolaeva SG, Kramarova LI, Ilyasova EN, Ilyasova FE (1980) The kinetics and metabolism of the cells of hibernating animals during hibernation. Int Rev Cytol 66:148–169

    Google Scholar 

  • Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T (2006) Circannual control of hibernation by HP complex in the brain. Cell 125:161–172

    Article  PubMed  CAS  Google Scholar 

  • Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–109

    Article  PubMed  Google Scholar 

  • Kunos G, Mosqueda-Garcia R, Mastrianni JA (1988) Endophinergic neurons in the brainstem and the control of blood pressure and heart rate. In: Illes P, Farsang C (eds) Regulatory roles of opioid peptides. VCH, Weinheim, pp 460–470

    Google Scholar 

  • Lee RE Jr, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annu Rev Physiol 60:55–72

    Article  PubMed  CAS  Google Scholar 

  • Lee TF, Westly J, Wang LCH (2000) Effects of hetastarch and mannitol on prolonging survival in stable hypothermia in rats. Am J Physiol Reg Integr Comp Physiol 278:R1040–R1047

    CAS  Google Scholar 

  • Lindell SL, Klahn SL, Piazza TM, Mangino MJ, Torrealba JR Southard JH, Carey HV (2005) Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288:G473–G480

    Article  PubMed  CAS  Google Scholar 

  • Liu XT, Li QS, Lin QF, Sun RY (2001) Uncoupling protein 1 mRNA, mitochondrial GTP-binding, and T4 5′-deiodinase of brown adipose tissue in euthermic Daurian ground squirrel during cold exposure. Comp Biochem Physiol A Mol Integr Physiol 128:827–835

    Article  PubMed  CAS  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and topor in mammals and birds. Accademic Press, New York

    Google Scholar 

  • MacDonald JA, Storey KB (1999) Regulation of ground squirrel Na+K+-ATPase activity by reversible phosphorylation during hibernation. Biochem Biophys Res Commun 254:424–429

    Article  PubMed  CAS  Google Scholar 

  • Malan A, Mioskowski E, Calgari C (1988) Time-course of blood acid-base state during arousal from hibernation in the European hamster. J Comp Physiol 158B:495–500

    Google Scholar 

  • Malatesta M, Zancanaro C, Martin TE, Chan EKL, Amalric F, Lührmann R, Vogel P, Fakan S (1994a) Is the coiled body involved in nucleolar functions? Exp Cell Res 211:415–419

    Article  CAS  Google Scholar 

  • Malatesta M, Zancanaro C, Martin TE, Chan EKL, Amalric F, Lührmann R, Vogel P, Fakan S (1994b) Cytochemical and immunocytochemical characterization of nuclear bodies during hibernation. Eur J Cell Biol 65:82–93

    CAS  Google Scholar 

  • Malatesta M, Zancanaro C, Tamburini M, Martin TE, Fu X-D, Vogel P, Fakan S (1995) Novel nuclear ribonucleoprotein structural components in the dormouse adrenal cortex during hibernation. Chromosoma 104:121–128

    PubMed  CAS  Google Scholar 

  • Malatesta M, Zancanaro C, Marcheggiani F, Cardinali A, Rocchi MBL, Capizzi D, Vogel P, Fakan S, Gazzanelli G (1998) Ultrastructural, morphometrical and immunocytochemical analyses of the exocrine pancreas in a hibernating dormouse. Cell Tissue Res 292:531–541

    Article  PubMed  CAS  Google Scholar 

  • Malatesta M, Cardinali A, Battistelli S, Zancanaro C, Martin TE, Fakan S, Gazzanelli G (1999) Nuclear bodies are usual constituents in tissues of hibernating dormice. Anat Rec 254:389–395

    Article  PubMed  CAS  Google Scholar 

  • Malatesta M, Gazzanelli G, Marcheggiani F, Zancanaro C, Rocchi MBL (2001) Ultrastructural characterisation of periinsular pancreatic acinar cells in the hibernating dormouse Muscardinus avellanarius. It J Zool 68:101–106

    Google Scholar 

  • Malatesta M, Zancanaro C, Baldelli B, Gazzanelli G (2002) Quantitative ultrastructural changes of hepatocyte constituents in euthermic, hibernating and arousing dormice (Muscardinus avellanarius). Tissue Cell 34:397–405

    Article  PubMed  CAS  Google Scholar 

  • Malatesta M, Baldelli B, Rossi L, Serafini S, Gazzanelli G (2003) Fine distribution of clock protein in hepatocytes of hibernating dormice. Eur J Histochem 47:233–240

    PubMed  CAS  Google Scholar 

  • Martin SL, Maniero GD, Carey C, Hand SC (1999) Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72:255–264

    Article  PubMed  CAS  Google Scholar 

  • Mayfield KP, D’Alecy LG (1994) Delta 1 opioid receptor dependence of acute hypoxic adaptation. J Pharmacol Exp Ther 268:74–77

    PubMed  CAS  Google Scholar 

  • Mostafa N, Everett DC, Chou SC, Kong PA, Florant GL, Coleman RA (1993) Seasonal changes in critical enzymes of lipogenesis and triacylglycerol syntesis in the marmot (Marmota flaviventris). Comp Physiol 163:463–469

    CAS  Google Scholar 

  • Mrosovsky N, Fisher KC (1970) Sliding set points for body weight in ground squirrels during the hibernation season. Can J Zool 48:241–247

    PubMed  CAS  Google Scholar 

  • Nizielski SE, Levine AS, Morley GE, Hall KA, Gosnell BA (1986) Seasonal variation in opioid modulation of feeding in the 13-lined ground squirrel. Physiol Behav 37: 5–9

    Article  PubMed  CAS  Google Scholar 

  • Nozari A, Safar P, Wu X, Stezoski WS, Henchir J, Kochanek P, Klain M, Radovsky A, Tisherman SA (2004) Suspended animation can allow survival without brain damage after traumatic exsanguination cardiac arrest of 60 minutes in dogs. J Trauma 57:1266–1275

    PubMed  Google Scholar 

  • Nurnberger F (1995) The neuroendocrine system in hibernating mammals: present knowledge and open questions. Cell Tissue Res 281:391–412

    PubMed  CAS  Google Scholar 

  • O’Hara BF, Watson FL, Srere HK, Kumar H, Wiler SW, Welch SK, Bitting L, Heller HC, Kilduff TS (1999) Gene expression in the brain across the hibernation cycle. Neuroscience 19:3781–3790

    PubMed  CAS  Google Scholar 

  • Oganov VS (2004) Modern analysis of bone loss mechanisms in microgravity. J Gravit Physiol 11:P143–146

    PubMed  CAS  Google Scholar 

  • Oeltgen PR, Nuchols PA, Nilekani WA, Spurrier WA, Su TP (1988) Further studies on opioids and hibernation: delta opioid receptor ligand selectively induced hibernation in summer active ground squirrels. Life Sci 43:1565–1574

    Article  PubMed  CAS  Google Scholar 

  • Oeltgen PR, Horton ND, Bolling SF, Su TP (1996) Extended lung preservation with the use of hibernation trigger factors. Ann Thorac Surg 61:1488–1493

    Article  PubMed  CAS  Google Scholar 

  • Ohtsuki T, Jaffe H, Brenner M, Azzam R, Frerichs KU, Hallenbeck JM (1998) Stimulation of tyrosine phosphporylation of a brain protein by hibernation. Cereb Blood Flow Metab 18:1040–1045

    Article  CAS  Google Scholar 

  • Ortmann S, Heldmaier G (2000) Regulation of body temperature and energy requirements of hibernating Alpine marmots (Marmota marmota). Am J Physiol Regul Integr Comp Physiol 278:R689–R704

    Google Scholar 

  • Pakotin PL, Pakotina ID, Belusov AB (1993) The study of brain slices from hibernating mammals in vitro and some approaches to the analysis of hibernation problems in vivo. Progr Neurobiol 40:123–161

    Article  Google Scholar 

  • Palinkas LA (2001) Psychosocial issues in long-term space flight: overview. Gravit Space Biol Bull 14:25–33

    PubMed  CAS  Google Scholar 

  • Peters SJ, Harris RA, Wu P, Pehleman TL, Heigenhauser GJ, Spriet LL (2001) Human skeletal muscle PDH kinase activity and isoform expression during a 3-day high-fat/low-carbohydrate diet. Am J Physiol Endocrinol Metab 281:E1151–E1158

    PubMed  CAS  Google Scholar 

  • Postnikova GB, Tselikova SV, Kolaeva SG, Solomonov NG (1999) Myoglobin content in skeletal muscles of hibernating ground squirrels rises in autumn and winter. Comp Biochem Physiol A Mol Integr Physiol 124:35–37

    Article  PubMed  CAS  Google Scholar 

  • Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initation of immune responses in ground squirrels. Am J Physiol Regul Integr Comp Physiol 282:R1054–R1062

    PubMed  CAS  Google Scholar 

  • Rousseau K, Archa Z, Loudon AS (2003) Leptin and seasonal mammals. Neuroendocrinol 15:409–414

    Article  CAS  Google Scholar 

  • Srere HK, Wang LCH, Martin SL (1992) Central role for differential gene expression in mammalian hibernation. Proc Natl Acad Sci USA 89:7119–7123

    Article  PubMed  CAS  Google Scholar 

  • Srere HK, Belke D, Wang LC, Martin SL (1995) α2-Macroglobulin gene expression during hibernation in ground squirrel (Citellus tridecemlineatus). Am J Physiol 268:R1507–R1512

    PubMed  CAS  Google Scholar 

  • Stephens TW, Caro JF (1998) To be lean or not to be lean: is leptin the answer? Exp Clin Endocrinol Diabetes 106:1–15

    Article  PubMed  CAS  Google Scholar 

  • Storey KB (2004) Cold ischemic organ preservation: lessons from natural systems. J Invest Med 52:315–322

    CAS  Google Scholar 

  • Strijkstra AM, Daan S (1997) Ambient temperature during torpor affects NREM sleep EEG during arousal episodes in hibernating European ground squirrels. Neurosci Lett 221:177–180

    Article  PubMed  CAS  Google Scholar 

  • Su TP (2000) Delta opioid peptide[D-Ala(2),D-Leu(5)]enkephalin promotes cell survival. J Biomed Sci 7:195–199

    PubMed  CAS  Google Scholar 

  • Tamburini M, Malatesta M, Zancanaro C, Martin TE, Fu XD, Vogel P, Fakan S (1996) Dense granular bodies: a novel nucleoplasmic structure in hibernating dormice. Histochem Cell Biol 106:581–586

    PubMed  CAS  Google Scholar 

  • Tinker DB, Harlow HJ, Beck TD (1998) Protein use and muscle-fiber changes in free-ranging, hibernating black bears. Physiol Zool 71:414–424

    Article  PubMed  CAS  Google Scholar 

  • Tsao LI, Su TP (2001) Hibernation-induction peptide and cell death: [D-Ala2,D-Leu5]enkephalin blocks Bax-related apoptotic processes. Eur J Pharmacol 428:149–151

    Article  PubMed  CAS  Google Scholar 

  • van Breukelen F, Martin SL (2001) Translational initiation is uncoupled from elongation at 18 degrees C during mammalian hibernation. Am J Physiol Regul Integr Comp Physiol 281:R1374–R1379

    PubMed  Google Scholar 

  • van Breukelen F, Carey V (2002) Ubiquitin conjugate dynamics in the gut and liver of hibernating ground squirrels. J Comp Physiol 172B:269–273

    Google Scholar 

  • van Breukelen F, Martin SL (2002a) Invited review: molecular adaptations in mammalian hibernators: unique adaptations or generalized responses? J Appl Physiol 92:2640–2647

    PubMed  Google Scholar 

  • van Breukelen F, Martin SL (2002b) Reversible depression of transcription during hibernation. J Comp Physiol 172B:R1374–R1379

    Google Scholar 

  • Vecchio L, Soldani C, Bottone MG, Malatesta M, Martin TE, Rothblum LI, Pellicciari C Biggiogera M (2006) DADLE induces a reversible hibernation-like state in HeLa cells. Histochem Cell Biol 125:193–201

    Article  PubMed  CAS  Google Scholar 

  • Vybiral S, Jansky L ((1997) Hibernation triggers and cryogens: do they play a role in hibernation? Comp Biochem Physiol A Physiol 118:1125–1133

    Article  PubMed  CAS  Google Scholar 

  • Wang LCH (1993) Is endogenous oipoid involved in hibernation? In: Cynthia C et al. (eds) Life in the cold: Ecological, physiological, and molecular mechanisms. Westview Press, Colorado, pp 297–304

    Google Scholar 

  • Wang SQ, Lakatta EG, Cheng H, Zhou ZQ (2002) Adaptive mechanisms of intracellular calcium homeostasis in mammalian hibernators. J Exp Biol 205:2957–2962

    PubMed  CAS  Google Scholar 

  • Wu G, Zhang F, Salley RK, Diana JN, Su TP, Chien S (1996) delta Opioid extends hypothermic preservation time of the lung. J Thorac Cardiovasc Surg 111:259–267

    Article  PubMed  CAS  Google Scholar 

  • Yeadon M, Kitchen I (1989) Opioids and respiration. Progr Neurobiol 33:1–16

    Article  CAS  Google Scholar 

  • Zancanaro C, Malatesta M, Mannello F, Vogel P, Fakan S (1999) The kidney during hibernation and arousal from hibernation A natural model of organ preservation during cold ischaemia and reperfusion. Nephrol Dial Transpl 14:1982–1990

    Article  CAS  Google Scholar 

  • Zancanaro C, Malatesta M, Vogel P, Fakan S (1997) Ultrastructure of the adrenal cortex of hibernating, arousing and euthermic dormouse, Muscardinus avellanarius. Anat Rec 249:359–364

    Article  PubMed  CAS  Google Scholar 

  • Zancanaro C, Malatesta M, Vogel P, Osculati F, Fakan S (1993) Ultrastructural and morphometrical analyses of the brown adipocyte nucleus in a hibernating dormouse. Biol Cell 79:55–61

    Article  PubMed  CAS  Google Scholar 

  • Zatzman ML (1984) Renal and cardiovascular effect of hibernation. Cryobiology 21:593–614

    Article  PubMed  CAS  Google Scholar 

  • Zhang YY, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Istituto di Istologia e Analisi di Laboratorio, Università di Urbino, Urbino, Italy

    Manuela Malatesta

  2. Dipartimento di Biologia Animale, Università di Pavia, Pavia, Italy

    Marco Biggiogera

  3. Anatomy & Histology Section, Dipartimento di Scienze Morfologico-Biomediche, Università di Verona, Strada Le Grazie, 8, I-37134, Verona, Italy

    Carlo Zancanaro

Authors
  1. Manuela Malatesta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Biggiogera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlo Zancanaro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlo Zancanaro .

Editor information

Editors and Affiliations

  1. Universidad Autónoma de Madrid, Centro de Biología Molecular del CSIC, Madrid, Spain

    Ricardo Amils

  2. British Antarctic Survey, Cambridge, United Kingdom

    Cynan Ellis-Evans

  3. Institute of Physiology, Medical University, Graz, Austria

    Helmut Hinghofer-Szalkay

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Malatesta, M., Biggiogera, M., Zancanaro, C. (2006). Hypometabolic induced state: a potential tool in biomedicine and space exploration. In: Amils, R., Ellis-Evans, C., Hinghofer-Szalkay, H. (eds) Life in Extreme Environments. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6285-8_26

Download citation

Publish with us

Policies and ethics

Search

Navigation