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A dramatic blood plasticity in hibernating and 14-day hindlimb unloading Daurian ground squirrels (Spermophilus dauricus)

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Abstract

We compared the effects of hibernation inactivity and 14-day hindlimb unloading in non-hibernating period on biochemical, rheological, and hematological parameters of blood in Daurian ground squirrels (Spermophilus dauricus). Twenty-four squirrels were randomly divided into four groups: control (CON), hibernation (HIB), post-hibernation (POST), and 14-day hindlimb unloading (HU). The results showed that serum enzymes (l-lactate dehydrogenase, alanine aminotransferase, and aspartate aminotransferase) activities decreased in HIB, POST, and HU squirrels compared with CON. Total protein (including albumin and globulin) maintained in HIB but decreased in HU compared with CON. Total cholesterol and high-density lipoprotein–cholesterol increased in HIB but maintained in HU and POST compared with CON. Meanwhile, serum creatinine decreased and urea increased in HU compared with CON. All blood ions concentrations were unchanged in HIB, POST, and HU squirrels compared with CON except calcium which increased in HIB compared with CON, and phosphorus which increased in HIB and POST compared with CON. Most of detected serum biochemical analytes in POST recovered to the CON level. Blood viscosity, which was unchanged in all shear rates in HU, increased in HIB and recovered in POST in lower shear rates compared with CON. Erythrocyte and corpuscular volume decreased in HIB and HU but maintained in POST compared with CON. All the routine hematological parameters recovered in POST as compared with CON except platelet, which decreased in HIB and POST but maintained in HU compared with CON. In conclusion, our results suggested a remarkable ability to maintain blood homeostasis in hibernating squirrels.

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References

  • Alexandre C, Vico L, Pilonchery G, Chapuy MC, Delmas PD, Chappard D (1988) Effects of weightlessness on phospho-calcium metabolism and its hormonal regulation in man during the 51 G Franco-American space flight. Pathol Biol (Paris) 36(2):144–148

    CAS  Google Scholar 

  • Alfrey CP, Udden MM, Leach-Huntoon C, Driscoll T, Pickett MH (1996) Control of red blood cell mass in spaceflight. J Appl Physiol (1985) 81(1):98–104

    CAS  Google Scholar 

  • Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20(4):470–475

    CAS  PubMed  Google Scholar 

  • Andersen NA, Larsen CM, Mandrup-Poulsen T (2000) TNFalpha and IFNgamma potentiate IL-1beta induced mitogen activated protein kinase activity in rat pancreatic islets of Langerhans. Diabetologia 43(11):1389–1396

    Article  CAS  PubMed  Google Scholar 

  • Begum SJ, Reddy MM, Ramakrishna O, Indira K, Swami KS (1986) Skeletal muscle protein metabolism under denervation atrophy in dog, Canis domesticus. Indian J Physiol Pharmacol 30(4):341–346

    CAS  PubMed  Google Scholar 

  • Bodine SC (2013a) Disuse-induced muscle wasting. Int J Biochem Cell Biol 45(10):2200–2208. doi:10.1016/j.biocel.2013.06.011

    Article  CAS  PubMed  Google Scholar 

  • Bodine SC (2013b) Hibernation: the search for treatments to prevent disuse-induced skeletal muscle atrophy. Exp Neurol 248:129–135. doi:10.1016/j.expneurol.2013.06.003

    Article  PubMed  Google Scholar 

  • Booth FW (1982) Effect of limb immobilization on skeletal muscle. J Appl Physiol Respir Environ Exerc Physiol 52(5):1113–1118

    CAS  PubMed  Google Scholar 

  • Bouma HR, Strijkstra AM, Boerema AS, Deelman LE, Epema AH, Hut RA, Kroese FG, Henning RH (2010) Blood cell dynamics during hibernation in the European Ground Squirrel. Vet Immunol Immunopathol 136(3–4):319–323. doi:10.1016/j.vetimm.2010.03.016

    Article  CAS  PubMed  Google Scholar 

  • Broucek J, Gajdosik D, Kovalcik K, Brestensky V (1984) The effect of prolonged movement restriction of dairy cows on biochemical parameters. Vet Med (Praha) 29(12):705–712

    CAS  Google Scholar 

  • Burlington RF, Klain GJ (1967) Gluconeogenesis during hibernation and arousal from hibernation. Comp Biochem Physiol 22(3):701–708

    Article  CAS  PubMed  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83(4):1153–1181. doi:10.1152/physrev.00008.2003

    Article  CAS  PubMed  Google Scholar 

  • Chauhan V, Sheikh A, Chauhan A, Tsiouris J, Malik M, Vaughan M (2002) Changes during hibernation in different phospholipid and free and esterified cholesterol serum levels in black bears. Biochimie 84(10):1031–1034

    Article  CAS  PubMed  Google Scholar 

  • Cohen I, Bogin E, Chechick A, Rzetelny V (1999) Biochemical alterations secondary to disuse atrophy in the rat’s serum and limb tissues. Arch Orthop Trauma Surg 119(7–8):410–417

    Article  CAS  PubMed  Google Scholar 

  • Cooper ST, Richters KE, Melin TE, Liu ZJ, Hordyk PJ, Benrud RR, Geiser LR, Cash SE, Simon Shelley C, Howard DR, Ereth MH, Sola-Visner MC (2012) The hibernating 13-lined ground squirrel as a model organism for potential cold storage of platelets. Am J Physiol Regul Integr Comp Physiol 302(10):R1202–R1208. doi:10.1152/ajpregu.00018.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cotton CJ (2016) Skeletal muscle mass and composition during mammalian hibernation. J Exp Biol 219(Pt 2):226–234. doi:10.1242/jeb.125401

    Google Scholar 

  • Dang K, Feng B, Gao YF, Hu N, Jiang S, Fu W, Hinghofer-Szalkay HG (2016) Muscle protection during hibernation: role of atrogin-1 and MuRF1, and fiber type transition in Daurian ground squirrels. Can J Zool 94:619–629. doi:10.1139/cjz-2015-0242

    Article  CAS  Google Scholar 

  • De Santo NG, Cirillo M, Kirsch KA, Correale G, Drummer C, Frassl W, Perna AF, Di Stazio E, Bellini L, Gunga HC (2005) Anemia and erythropoietin in space flights. Semin Nephrol 25(6):379–387. doi:10.1016/j.semnephrol.2005.05.006

    Article  PubMed  Google Scholar 

  • Doumas BT (1975) Standards for total serum protein assays—a collaborative study. Clin Chem 21(8):1159–1166

    CAS  PubMed  Google Scholar 

  • Doumas BT, Watson WA, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chim Acta 31(1):87–96

    Article  CAS  PubMed  Google Scholar 

  • Fitts RH, Riley DR, Widrick JJ (2001) Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204(Pt 18):3201–3208

    CAS  PubMed  Google Scholar 

  • Fu W, Hu H, Dang K, Chang H, Du B, Wu X, Gao Y (2016) Remarkable preservation of Ca2+ homeostasis and inhibition of apoptosis contribute to anti-muscle atrophy effect in hibernating Daurian ground squirrels. Sci Rep 6:27020. doi:10.1038/srep27020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao YF, Wang J, Wang HP, Feng B, Dang K, Wang Q, Hinghofer-Szalkay HG (2012) Skeletal muscle is protected from disuse in hibernating dauria ground squirrels. Comp Biochem Physiol A Mol Integr Physiol 161(3):296–300. doi:10.1016/j.cbpa.2011.11.009

    Article  CAS  PubMed  Google Scholar 

  • Graesli AR, Evans AL, Fahlman A, Bertelsen MF, Blanc S, Arnemo JM (2015) Seasonal variation in haematological and biochemical variables in free-ranging subadult brown bears (Ursus arctos) in Sweden. BMC Vet Res 11:301. doi:10.1186/s12917-015-0615-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Haggag G, Raheem A, Khalil F (1966) Hibernation in reptiles. II. Changes in blood glucose, haemoglobin, red blood cell count, protein and non-protein nitrogen. Comp Biochem Physiol 17(1):335–339

    Article  CAS  PubMed  Google Scholar 

  • Harlow HJ, Seal US (1981) Changes in hematology and metabolites in the serum and urine of the badger, Taxidea taxus, during food deprivation. Can J Zool 59(11):2123–2128

    Article  CAS  Google Scholar 

  • Hellgren EC, Lochmiller RL, Amoss MS Jr, Grant WE (1985) Endocrine and metabolic responses of the collared peccary (Tayassu tajacu) to immobilization with ketamine hydrochloride. J Wildl Dis 21(4):417–425

    Article  CAS  PubMed  Google Scholar 

  • Kaperonis AA, Michelsen CB, Askanazi J, Kinney JM, Chien S (1988) Effects of total hip replacement and bed rest on blood rheology and red cell metabolism. J Trauma 28(4):453–457

    Article  CAS  PubMed  Google Scholar 

  • Koenig W, Sund M, Ernst E, Mraz W, Hombach V, Keil U (1992) Association between rheology and components of lipoproteins in human blood. Results from the MONICA project. Circulation 85(6):2197–2204

    Article  CAS  PubMed  Google Scholar 

  • Larkin EC, Simmonds RC, Ulvedal F, Williams WT (1972) Responses of some hematologic parameters of active and hibernating squirrels (Spermophilus mexicanus) upon exposure to hypobaric and isobaric hyperoxia. Comp Biochem Physiol A Comp Physiol 43(4):757–770

    Article  CAS  PubMed  Google Scholar 

  • Lechler E, Penick GD (1963) Blood clotting defect in hibernating ground squirrels (Citellus tridecemlineatus). Am J Physiol 205(5):985–988

    CAS  PubMed  Google Scholar 

  • Lee SR, Ko TH, Kim HK, Marquez J, Ko KS, Rhee BD, Han J (2015) Influence of starvation on heart contractility and corticosterone level in rats. Pflug Arch Eur J Physiol 467(11):2351–2360. doi:10.1007/s00424-015-1701-9

    Article  CAS  Google Scholar 

  • Lohuis TD, Harlow HJ, Beck TD (2007) Hibernating black bears (Ursus americanus) experience skeletal muscle protein balance during winter anorexia. Comp Biochem Physiol Part B Biochem Mol Biol 147(1):20–28. doi:10.1016/j.cbpb.2006.12.020

    Article  CAS  Google Scholar 

  • Martin DG, Convertino VA, Goldwater D, Ferguson EW, Schoomaker EB (1986) Plasma viscosity elevations with simulated weightlessness. Aviat Space Environ Med 57(5):426–431

    CAS  PubMed  Google Scholar 

  • McGee-Lawrence ME, Carey HV, Donahue SW (2008) Mammalian hibernation as a model of disuse osteoporosis: the effects of physical inactivity on bone metabolism, structure, and strength. Am J Physiol Regul Integr Comp Physiol 295(6):R1999–R2014. doi:10.1152/ajpregu.90648.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGee-Lawrence M, Buckendahl P, Carpenter C, Henriksen K, Vaughan M, Donahue S (2015) Suppressed bone remodeling in black bears conserves energy and bone mass during hibernation. J Exp Biol 218(Pt 13):2067–2074. doi:10.1242/jeb.120725

    Google Scholar 

  • Merrill EW (1969) Rheology of blood. Physiol Rev 49:863–888

    Google Scholar 

  • Morey-Holton ER, Globus RK, Morey-Holton ER (2002) Hindlimb unloading rodent model: technical aspects. J Appl Physiol (Bethesda, Md, 1985) 92(4):1367–1377

    Article  Google Scholar 

  • Nansel D, Knoche L (1972) Blood changes in torpid and non-torpid columbian ground squirrels, Spermophilus columbianus. Comp Biochem Physiol A Comp Physiol 41(1):175–179

    Article  CAS  PubMed  Google Scholar 

  • Otis JP, Sahoo D, Drover VA, Yen CL, Carey HV (2011) Cholesterol and lipoprotein dynamics in a hibernating mammal. PLoS One 6(12):e29111. doi:10.1371/journal.pone.0029111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poliakov VV, Ivanova SM, Noskov VB, Labetskaia OI, Iarlykova Iu V, Karashtin VV, Legen’kov VI, Sarycheva TG, Shishkanova ZG, Kozinets GI (1998) Hematological investigations in conditions of long-term space flights. Aviakosm Ekolog Med 32(2):9–18

    CAS  PubMed  Google Scholar 

  • Popova IA, Vetrova EG, Rustam’ian LA, Nosova EA (1991) Carbohydrate and lipid metabolites and blood serum enzymes in humans during graded exercise test in long-term anti-orthostatic hypokinesia. Kosm Biol Aviakosm Med 25(2):50–54

    CAS  PubMed  Google Scholar 

  • Russom JM, Guba GR, Sanchez D, Tam CF, Lopez GA, Garcia RE (1992) Plasma lipoprotein cholesterol concentrations in the golden-mantled ground squirrel (Spermophilus lateralis): a comparison between pre-hibernators and hibernators. Comp Biochem Physiol Part B Biochem Mol Biol 102(3):573–578

    Article  CAS  Google Scholar 

  • Salazar Vazquez BY, Martini J, Chavez Negrete A, Tsai AG, Forconi S, Cabrales P, Johnson PC, Intaglietta M (2010) Cardiovascular benefits in moderate increases of blood and plasma viscosity surpass those associated with lowering viscosity: experimental and clinical evidence. Clin Hemorheol Microcirc 44(2):75–85. doi:10.3233/CH-2010-1261

    CAS  PubMed  Google Scholar 

  • Santos-Junior FF, Pires Ade F, Ribeiro NM, Mendonca VA, Alves JO, Soares PM, Ceccatto VM, Assreuy AM (2015) Sensorial, structural and functional response of rats subjected to hind limb immobilization. Life Sci 137:158–163. doi:10.1016/j.lfs.2015.07.020

    Article  CAS  PubMed  Google Scholar 

  • Saunders DK, Roberts AC, Aldrich KJ, Cuthbertson B (2002) Hematological and blood viscosity changes in tail-suspended rats. Aviat Space Environ Med 73(7):647–653

    PubMed  Google Scholar 

  • Savolainen J (1987) Acid and alkaline proteolytic activities of cast-immobilized rat hind-limb muscles after electric stimulation. Arch Phys Med Rehabil 68(8):481–485

    CAS  PubMed  Google Scholar 

  • Schmitt O (1978) The influence of the electromagnetic field on the activity of alkaline phosphatase in immobilised children (author’s transl). Arch Orthop Trauma Surg 93(1):21–24

    Article  CAS  PubMed  Google Scholar 

  • South FE, 2nd, Jeffay H (1958) Alterations in serum proteins of hibernating hamsters. In: Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine (New York, NY) 98(4):885–887

  • Spurrier WA, Dawe AR (1973) Several blood and circulatory changes in the hibernation of the 13-lined ground squirrel, Citellus tridecemlineatus. Comp Biochem Physiol A Comp Physiol 44(2):267–282

    Article  CAS  PubMed  Google Scholar 

  • Steffen JM, Koebel DA, Musacchia XJ, Milsom WK (1991) Morphometric and metabolic indices of disuse in muscles of hibernating ground squirrels. Comp Biochem Physiol Part B Biochem Mol Biol 99(4):815–819

    Article  CAS  Google Scholar 

  • Szilagyi JE, Senturia JB (1972) A comparison of bone marrow leukocytes in hibernating and nonhibernating woodchucks and ground squirrels. Cryobiology 9(4):257–261

    Article  CAS  PubMed  Google Scholar 

  • van der Wiel HE, Lips P, Nauta J, Netelenbos JC, Hazenberg GJ (1991) Biochemical parameters of bone turnover during ten days of bed rest and subsequent mobilization. Bone Miner 13(2):123–129

    Article  PubMed  Google Scholar 

  • Vestergaard P, Stoen OG, Swenson JE, Mosekilde L, Heickendorff L, Frobert O (2011) Vitamin D status and bone and connective tissue turnover in brown bears (Ursus arctos) during hibernation and the active state. PLoS One 6(6):e21483. doi:10.1371/journal.pone.0021483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Gao Y F, Fan X (2007) Effects of tail suspension upon the morphology and myosin ATPase activities of the soleus muscle of the Dauria ground squirrel Spermophilus dauricus. Acta Zool Sin 53(1):116–122. doi:10.3969/j.issn.1674-5507.2007.01.013

    CAS  Google Scholar 

  • Wells Jr RE, Merrill EW, Gabelnick H (1962) Shear-rate dependence of viscosity of blood: interaction of red cells and plasma proteins. Trans Soc Rheol (1957–1977) 6(1):19–24

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (31270455), the International Scientific and Technological Cooperation Projects in Shaanxi Province of China (2013KW26-01), the Postdoctoral Science Foundation of China (No. 2015M580869), and the Shaanxi Province Natural Science Basic Research Program (2016JQ3014). The authors thank Yasir Arfat for language revision.

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    Authors and Affiliations

    1. Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), Ministry of Education, Xi’an, China

      Huan-Xin Hu, Fang-Ying Du, Wei-Wei Fu, Shan-Feng Jiang, Jin Cao, Shen-Hui Xu, Hui-Ping Wang, Hui Chang & Yun-Fang Gao

    2. Department of Genetics and Molecular Biology, School of Medicine, Xi’an Jiaotong University, Xi’an, China

      Fang-Ying Du

    3. Gravitational Physiology and Medicine Research Unit, Institute of Physiology, Center of Physiological Medicine, Medical University Graz, Graz, Austria

      Nandu Goswami

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    1. Huan-Xin Hu
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    Communicated by F. van Breukelen.

    Yun-Fang Gao is the first corresponding author.

    Huan-Xin Hu and Fang-Ying Du contributed equally to the study.

    This manuscript is part of the special issue Hibernation—Guest Editors: Frank van Breukelen and Jenifer C. Utz.

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    Hu, HX., Du, FY., Fu, WW. et al. A dramatic blood plasticity in hibernating and 14-day hindlimb unloading Daurian ground squirrels (Spermophilus dauricus). J Comp Physiol B 187, 869–879 (2017). https://doi.org/10.1007/s00360-017-1092-7

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