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Localization profiles of natriuretic peptides in hearts of pre-hibernating and hibernating Anatolian ground squirrels (Spermophilus xanthoprymnus)

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Abstract

The Anatolian ground squirrel (Spermophilus xanthoprymnus) is a typical example of true mammalian hibernators. In order to adapt to extreme external and internal environments during hibernation, they lower their body temperatures, heart rates and oxygen consumption; however, pathological events such as ischemia and ventricular fibrillation do not occur in their cardiovascular systems. During the hibernation, maintenance of cardiac function is very important for survival of ground squirrels. Natriuretic peptides (NPs) are key factors in the regulation of cardiovascular hemostasis. Since NPs’ role on the protection of heart during hibernation are less clear, the aim of this study was to investigate dynamic changes in NPs content in the cardiac chambers and to reveal the possible role of NPs on establishing cardiac function in ground squirrel during hibernation using immunohistochemistry. The immunohistochemical results indicate that cardiac NP expressions in atrial and ventricular cardiomyocytes were different from each other and were sex-independent. ANP and BNP were expressed in a chamber-dependent manner in female and male squirrel hearts. Furthermore, cardiac NPs expression levels in hibernation period were lower than those at the pre-hibernation period. During prehibernation period, ANP, BNP and CNP were expressed in the white and beige adipocytes of epicardial adipose tissue (EAT); while during hibernation period, the brown adipocytes of EAT were positive for BNP and CNP. These data suggest that the hibernation-dependent reduction in levels of NPs, particularly ANP, in cardiac chambers and EAT may be associated with low heart rate and oxygen consumption during hibernation. However, further studies are needed to better delineate the roles of NPs during the hibernation.

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References

  • Abrosimov DA, Yakovleva EI, Bugrova ML (2015) Quantitative assay of brain natriuretic peptide in rat cardiomyocytes in the early postreperfusion period. Cell and Tissue Biol 9:336-339

  • Addario C, Milanesi G, Vaccarone R, Barni S, Gerzeli G, Fenoglio C (2004) Expression of atrial natriuretic peptide in the heart of active and hibernating frog. Ital J Zool 71:69-72

  • Aldiss P, Davies G, Woods R, Budge H, Sacks HS, Symonds ME (2017) ‘Browning’ the cardiac and peri-vascular adipose tissues to modulate cardiovascular risk. Int J Cardiol 228:265–274

    Article  PubMed  PubMed Central  Google Scholar 

  • Aoki CA, Maldonado CA, Forssmann WG (1989) Seasonal changes of the endocrine heart. In: Forssmann WG, Scheuermann DW and Alt J (ed) Functional Morphology of the Endocrine Heart, Springer-Verlag, New York, pp 61-68

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

    Article  CAS  PubMed  Google Scholar 

  • Arjamaa O (2014) Physiology of natriuretic peptides: the volume overload hypothesis revisited. World J Cardiol 6:4–7

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballinger MA, Andrews MT (2018) Nature’s fat-burning machine: brown adipose tissue in a hibernating mammal. J Exp Biol 221:jeb162586

    Article  PubMed  Google Scholar 

  • Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, Giacobino JP, De Matteis R, Cinti S (2010) The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab 298:1244–1253

    Article  CAS  Google Scholar 

  • Biondo AW, Ehrhart EJ, Sisson DD, Bulmer BJ, De Morais HS, Solter PF (2003) Immunohistochemistry of atrial and brain natriuretic peptides in control cats and cats with hypertrophic cardiomyopathy. Vet Pathol 40:501–506

    Article  CAS  PubMed  Google Scholar 

  • Bonis A, Anderson L, Talhourne G et al (2018) Cardiovascular resistance to thrombosis in 13-lined ground squirrels. J Comp Physiol B 189:167–177. https://doi.org/10.1007/s00360-018-1186-x

    Article  CAS  PubMed  Google Scholar 

  • Bordicchia M, Liu D, Amri EZ, Ailhaud G, Dessi-Fulgheri P, Zhang C, Takahashi N, Sarzani R, Collins S (2012) Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest 122:1022–1036

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouma HR (2013) Immunological aspects of hibernation as leads in the prevention of acute organ injury. Dissertation, University of Groningen

  • Buck MJ, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Phys 279:255–262

    Google Scholar 

  • Cameron VA, Rademaker MT, Ellmers LJ, Espiner EA, Nicholls MG, Richards AM (2000) Atrial (ANP) and brain natriuretic peptide (BNP) expression after myocardial infarction in sheep: ANP is synthesized by fibroblasts infiltrating the infarct. Endocrinology 141:4690–4697

    Article  CAS  PubMed  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    Article  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

    Article  CAS  Google Scholar 

  • Chapeau C, Gutkowska J, Schiller PW, Milne RW, Thibault G, Garcia R, Genest J, Cantin M (1985) Localization of immunoreactive synthetic atrial natriuretic factor (ANF) in the heart of various animal species. J Histochem Cytochem 33:541–550

    Article  CAS  PubMed  Google Scholar 

  • Colbatzky F, Vollmar A, Monch U, Hermanns W (1993) Synthesis and distribution of atrial natriuretic peptide (ANP) in hearts from normal dogs and those with cardiac abnormalities. J Comp Pathol 108:149–163

    Article  CAS  PubMed  Google Scholar 

  • Collins S (2014) A heart-adipose tissue connection in the regulation of energy metabolism. Nat Rev Endocrinol 10:157–163

    Article  CAS  PubMed  Google Scholar 

  • Collins S, Bordicchia M (2013) Heart hormones fueling a fire in fat. Adipocyte 2:104–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Ry S, Cabiati M, Vozzi F, Battolla B, Caselli C, Forini F, Segnani C, Prescimone T, Giannessi D, Mattii L (2011) Expression of C-type natriuretic peptide and its receptor NPR-B in cardiomyocytes. Peptides 32:1713–1718

    Article  CAS  PubMed  Google Scholar 

  • Espiner EA, Richards AM, Yandle TG, Nicholls MG (1995) Natriuretic hormones. Endocrinol Metab Clin N Am 24:481–509

    Article  CAS  Google Scholar 

  • Federico C (2010) Natriuretic peptide system and cardiovascular disease. Heart Views 11:10–15

    PubMed  PubMed Central  Google Scholar 

  • Fedorov VV, Li L, Glukhov A, Shishkina I, Aliev RR, Mikheeva T, Nikolski VP, Rosenshtrukh LV, Efimov IR (2005) Hibernator Citellus undulatus maintains safe cardiac conduction and is protected against tachyarrhythmias during extreme hypothermia: possible role of Cx43 and Cx45 up-regulation. Heart Rhythm 2:966–975

    Article  PubMed  Google Scholar 

  • Fitzgibbons TP, Czech MP (2014) Epicardial and perivascular adipose tissues and their influence on cardiovascular disease: basic mechanisms and clinical associations. J Am Heart Assoc 3:e000582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleck CC, Carey HV (2005) Modulation of apoptotic pathways in intestinal mucosa during hibernation. Am J Phys Regul Integr Comp Phys 289:586–595

    Google Scholar 

  • Giralt M, Villarroya F (2013) White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154:2992–3000

    Article  CAS  PubMed  Google Scholar 

  • Green C (2000) Mammalian hibernation: lessons for organ preparation? Cryo Letters 21:91–98

    CAS  PubMed  Google Scholar 

  • Gür H (2010) Why do Anatolian ground squirrels exhibit a Bergmannian size pattern? A phylogenetic comparative analysis of geographic variation in body size. Biol J Linn Soc 100:695–710

    Article  Google Scholar 

  • Herinckx G, Hussain N, Opperdoes FR, Storey KB, Rider MH, Vertommen D (2017) Changes in the phosphoproteome of brown adipose tissue during hibernation in the ground squirrel, Ictidomys tridecemlineatus. Physiol Genomics 49:462–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Zhou PH, Zhang XB, Xu CG, Wang W (2015) Plasma concentrations of adrenomedullin and natriuretic peptides in patients with essential hypertension. Exp Ther Med 9:1901-1908

  • Hut RA, Barnes BM, Daan S (2002) Body temperature patterns before, during, and after semi- natural hibernation in the European ground squirrel. J Comp Physiol B 172:47–58

    Article  CAS  PubMed  Google Scholar 

  • Iacobellis G, Bianco AC (2011) Epicardial adipose tissue: emerging physiological, pathophysiological and clinical features. Trends Endocrinol Metab 22:450-457

  • Iacobellis G, Corradi D, Sharma AM (2005) Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med 2:536–543

    Article  PubMed  Google Scholar 

  • Ignat'ev DA, Sukhova GS, Sukhov VP (2001) Analysis of changes in heart rate and temperature of the ground squirrel Citellus undulatus in various physiological states. Zh Obshch Biol 62:66–77

    CAS  PubMed  Google Scholar 

  • Jensen EC (2013) Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec (Hoboken) 296:378–381

    Article  Google Scholar 

  • Johansson BW (1996) The hibernator heart: nature’s model of resistance to ventricular fibrillation. Cardiovasc Res 31:828–832

    Google Scholar 

  • Kimura H, Nagoshi T, Yoshii A, Kashiwagi Y, Tanaka Y, Ito K, Yoshino T, Tanaka TD, Yoshimura M (2017) The thermogenic actions of natriuretic peptide in brown adipocytes: the direct measurement of the intracellular temperature using a fuorescent thermoprobe. Sci Rep 7:12978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu Y, Nakao K, Itoh H, Suga S, Ogawa Y, Imura H (1992) Vascular natriuretic peptide. Lancet 340:622

    Article  CAS  PubMed  Google Scholar 

  • Kuehnl A, Pelisek J, Bruckmeier M, Safi W, Eckstein HH (2013) Comparative measurement of CNP and NT-proCNP in human blood samples: a methodological evaluation. J Negat Results Biomed 12:7

  • Lidell ME, Betz MJ, Enerbäck S (2014) Two types of brown adipose tissue in humans. Adipocyte 3:63–66

    Article  CAS  PubMed  Google Scholar 

  • Liman N (2017) Heat shock proteins (HSP)-60, −70, −90 and 105 display variable spatial and temporal immunolocalization patterns in the involuting rat uterus. Anim Reprod Sci 14:1072–1086

    Article  Google Scholar 

  • Logan SM, Storey KB (2017) Avoiding apoptosis during mammalian hibernation. Temperature 4:15–17

    Article  Google Scholar 

  • Lu J, Pan SS (2016) Elevated C-type natriuretic peptide elicits exercise preconditioning-induced cardioprotection against myocardial injury probably via the up-regulation of NPR-B. J Physiol Sci 67:475–487

    Article  CAS  PubMed  Google Scholar 

  • Luchner A, Stevens TL, Borgeson DD, Redfield M, Wei CM, Porter JG, Burnett JC Jr (1998) Differential atrial and ventricular expression of myocardial BNP during evolution of heart failure. Am J Phys 274:H1684–H1689

    CAS  Google Scholar 

  • Lumsden NG, Khambata RS, Hobbs AJ (2010) C-type natriuretic peptide (CNP): cardiovascular roles and potential as a therapeutic target. Curr Pharm Des 16:4080–4088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luu BE, Tessier SN, Duford DL, Storey KB (2015) The regulation of troponins I, C and ANP by GATA4 and Nkx2-5 in heart of hibernating thirteen-lined ground squirrels, Ictidomys tridecemlineatus. PLoS One 10:e0117747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyman C, Chatfield P (1955) Physiology of hibernation in mammals. Physiol Rev 35:403–425

    Article  CAS  PubMed  Google Scholar 

  • Melvin RG, Andrews MT (2009) Torpor induction in mammals: recent discoveries fueling new ideas. Trends Endocrinol Metab 20:490–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mifune H, Richter R, Forssmann WG (1995) Detection of immunoreactive atrial and brain natriuretic peptides in the equine atrium. Anat Embryol 192:117–121

    Article  CAS  PubMed  Google Scholar 

  • Mifune H, Suzuki S, Nokihara K, Noda Y (1996) Distribution of immunoreactive atrial and brain natriuretic peptides in the heart of the chicken, quail, snake and frog. Exp Anim 45:125-133

  • Mifune H, Honda J, Takamori S, Sugiyama F, Yagami K, Suzuki S (2004) A-type natriuretic peptide level in hypertensive transgenic mice. Exp Anim 53:9–11

    Article  Google Scholar 

  • Mifune Н, Nishi Y, Tajiri Y, Yabuki A (2012) Different A-type natriuretic peptide level in five strains of mice. J Vet Med Sci 74:499–502

    Article  PubMed  Google Scholar 

  • Milsom WK, Zimmer MB, Harris MB (1999) Regulation of cardiac rhythm in hibernating mammals. Comp Biochem Physiol A Physiol 124:383–391

    Article  CAS  Google Scholar 

  • Moe GW, Grima EA, Angus C, Wong NL, Hu DC, Howard RJ, Armstrong PW (1991) Response of atrial natriuretic factor to acute and chronic increases of atrial pressures in experimental heart failure in dogs. Role of changes in heart rate, atrial dimension, and cardiac tissue concentration. Circulation 83:1780–1787

    Article  CAS  PubMed  Google Scholar 

  • Moe GW, Grima EA, Wong NL, Howard RJ, Armstrong PW (1993) Dual natriuretic peptide system in experimental heart failure. J Am Coll Cardiol 22:891–898

    Article  CAS  PubMed  Google Scholar 

  • Moe GW, Grima EA, Wong NLY, Howard RJ, Armstrong PW (1996) Plasma and cardiac tissue atrial and brain natriuretic peptides in experimental heart failure. J Am Coll Cardiol 27:720–727

    Article  CAS  PubMed  Google Scholar 

  • Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, Shirakami G, Jougasaki M, Obata K, Yasue H (1991) Brain natriuretic peptide as a novel cardiac hormone in humans: evidence for an exquisite dual natriuretic peptide system, ANP and BNP. J Clin Invest 87:1402–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa M, Tanaka I, Suga S, Ogawa Y, Tamura N, Goto M, Sugawara A, Yoshimasa T, Itoh H, Mukoyama M, Nakao K (1995) Preparation of a monoclonal antibody against mouse brain natriuretic peptide (BNP) and tissue distribution of BNP in mice. Clin Exp Pharmacol Physiol Suppl 22:S186–S187

    Article  CAS  PubMed  Google Scholar 

  • Nazario B, Hu RM, Pedram A, Prins B, Levin ER (1995) Atrial and brain natriuretic peptides stimulate the production and secretion of C-type natriuretic peptide from bovine aortic endothelial cells. J Clin Invest 95:1151–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemer M, Lavigne JP, Drouin J, Thibault G, Gannon M, Antakly T (1986) Expression of atrial natriuretic factor gene in heart ventricular tissue. Peptides 7:1147–1152

    Article  CAS  PubMed  Google Scholar 

  • Nishikimi T, Maeda N, Matsuoka H (2006) The role of natriuretic peptides in cardioprotection. Cardiovasc Res 69:318–328

    Article  CAS  PubMed  Google Scholar 

  • Ogawa Y, Nakao K, Mukoyama M, Hosoda K, Shirakami G, Arai H, Saito Y, Suga S, Jougasaki M, Imura H (1991) Natriuretic peptides as cardiac hormones in normotensive and spontaneously hypertensive rats. The ventricle is a major site of synthesis and secretion of brain natriuretic peptide. Circ Res 69:491–500

    Article  CAS  PubMed  Google Scholar 

  • Olson ME, McCabe K (1986) Anesthesia in the Richardson’s ground squirrel: comparison of ketamine, ketamine and xylazine, droperidol and fentanyl, and sodium pentobarbital. J Am Vet Med Assoc 189:1035–1037

    CAS  PubMed  Google Scholar 

  • Osman AH, Yuge S, Hyodo S, Sato S, Maeda S, Marie H, Caceci T, Birukawa N, Urano A, Naruse K, Naruse M, Takei Y (2004) Molecular identification and immunohistochemical localization of atrial natriuretic peptide in the heart of the dromedary camel (Camelus dromedarius). Comp Biochem Physiol A Mol Integr Physiol 139:417–424

    Article  CAS  PubMed  Google Scholar 

  • Özbek M, Bozkurt MF, Beyaz F, Ergün E, Ergün L (2018) Expression profile of some neuronal and glial cell markers in the ovine ileal enteric nervous system during prenatal development. Acta Histochem 120:768–779

    Article  CAS  PubMed  Google Scholar 

  • Öztop M, Çınar K, Türk S (2018) Immunolocalization of natriuretic peptides and their receptors in goat (Capra hircus) heart. Biotech Histochem 93:389–404

    Article  CAS  PubMed  Google Scholar 

  • Payvar S, Spertus JA, Miller AB, Casscells SW, Pang PS, Zannad F, Swedberg K, Maggioni AP, Reid KJ, Gheorghiade M, for the Efficacy of Vasopressin Antagonism in Heart Failure Outcome Study with Tolvaptan (EVEREST) Investigators (2013) Association of low body temperature and poor outcomes in patients admitted with worsening heart failure: a substudy of the efficacy of vasopressin antagonism in heart failure outcome study with Tolvaptan (EVEREST) trial. Eur J Heart Fail 15:1382–1389

    Article  CAS  PubMed  Google Scholar 

  • Potter LR, Abbey-Hosch S, Dickey DM (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27:47–72

    Article  CAS  Google Scholar 

  • Prati F, Arbustini E, Labellarte A, Sommariva L, Pawlowski T, Manzoli A, Pagano A, Motolese M, Boccanelli A (2003) Eccentric atherosclerotic plaques with positive remodelling have a pericardial distribution: a permissive role of epicardial fat? A three-dimensional intravascular ultrasound study of left anterior descending artery lesions. Eur Heart J 24:329–336

    Article  CAS  PubMed  Google Scholar 

  • Rademaker MT, Richards AM (2005) Cardiac natriuretic peptides for cardiac health. Clin Sci (Lond) 108:23–36

    Article  CAS  Google Scholar 

  • Ratigan ED, McKay DB (2016) Exploring principles of hibernation for organ preservation. Transplant Rev (Orlando) 30:13-19

  • Sacks HS, Fain JN, Holman B, Cheema P, Chary A, Parks F, Karas J, Optican R, Bahouth SW, Garrett E, Wolf RY, Carter RA, Robbins T, Wolford D, Samaha J (2009) Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat. J Clin Endocrinol Metab 94:3611–3615

    Article  CAS  PubMed  Google Scholar 

  • Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H, Cinti S, Symonds ME (2013) Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab 98:1448–1455

    Article  CAS  Google Scholar 

  • Sagnella GA (1998) Measurement and significance of circulating natriuretic peptides in cardiovascular disease. Clin Sci (Lond) 95:519–529

    Article  CAS  Google Scholar 

  • Sandovici M, Henning R, Hut RA, Strijkstra AM, Epema AH, van Goor H, Deelman LE (2004) Differential regulation of glomerular and interstitial endothelial nitric oxide synthase expression in the kidney of hibernating ground squirrel. Nitric Oxide 11:194–200

    Article  CAS  PubMed  Google Scholar 

  • Satoh K, Masuda T, Hasegawa N, Marumo F, Kikawada R (1989) The concentration of atrial natriuretic peptide (ANP) in plasma and atrial tissue of canines with acute heart failure induced by reversible aortic or mitral regurgitation. Nihon Naibunpi Gakkai Zasshi 65:794-806

  • Sergeeva IA, Cristoffels VM (2013) Regulation of expression of atrial and brain natriuretic peptide, biomarkers for heart development and disease. Biochim Biophys Acta (BBA) - Mol Basis Dis 1832:2403–2413

    Article  CAS  Google Scholar 

  • Shabalina IG, Petrovic N, de Jong JM, Kalinovich AV, Cannon B, Nedergaard J (2013) UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep 5:1196–1203

    Article  CAS  PubMed  Google Scholar 

  • Sidossis L, Kajimura S (2015) Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest 125:478–486

    Article  PubMed  PubMed Central  Google Scholar 

  • Sirithunyanont C, Leowattana W, Sukumalchantra Y, Chaisupamonkollarp S, Watanawaroon S, Chivatanaporn B, Bhuriponyo K, Mahanonda N (2003) Role of the plasma brain natriuretic peptide in differentiating patients with congestive heart failure from other diseases. J Med Assoc Thail 86:87–95

    Google Scholar 

  • Storey KB, Storey JM (2010) Metabolic rate depression: the biochemistry of mammalian hibernation. Clin Chem 52:77–108

    Article  CAS  Google Scholar 

  • Sudoh T, Minamino N, Kangawa K, Matsuo H (1990) C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem Biophys Res Commun 168:863–870

    Article  CAS  PubMed  Google Scholar 

  • Suffee N, Moore-Morris T, Farahmand P et al (2017) Atrial natriuretic peptide regulates adipose tissue accumulation in adult atria. Proc Natl Acad Sci U S A 114(5):771–780

    Article  CAS  Google Scholar 

  • Talaei F, Hylkema MN, Bouma HR, Boerema AS, Strijkstra AM, Henning RH, Schmidt M (2011) Reversible remodelling of lung tissue during hibernation in the Syrian hamster. J Exp Biol 214:1276–1282

    Article  PubMed  Google Scholar 

  • Talman AH, Psaltis PJ, Cameron JD, Meredith IT, Seneviratne SK, Wong DT (2014) Epicardial adipose tissue: far more than a fat depot. Cardiovasc Diagn Ther 4:416–429

    PubMed  PubMed Central  Google Scholar 

  • Thibault G, Charbonneau C, Bilodeau J, Schiffrin EL, Garcia R (1992) Rat brain natriuretic peptide is localized in atrial granules and released into the circulation. Am J Phys 263:R301–R309

    CAS  Google Scholar 

  • Tøien Ø, Drew KL, Chao ML, Rice ME (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am J Phys Regul Integr Comp Phys 281:572–583

    Google Scholar 

  • Torres-Courchoud I, Chen HH (2016) B-type natriuretic peptide and acute heart failure: fluid homeostasis, biomarker and therapeutics. Rev Clin Esp 216:393–398

    Article  CAS  PubMed  Google Scholar 

  • Villar I, Panayiotou CM, Sheraz A, Madhani M, Scotland RS, Nobles M, Kemp-Harper B, Ahluwalia A, Hobbs AJ (2007) Definitive role for natriuretic peptide receptor-C in mediating the vasorelaxant activity of C-type natriuretic peptide and endothelium-derived hyperpolarising factor. Cardiovasc Res 74:515–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viscarra JA, Ortiz RM (2013) Cellular mechanisms regulating fuel metabolism in mammals: role of adipose tissue and lipids during prolonged food deprivation. Metabolism 62:889–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodard GE, Rosado JA (2008) Natriuretic peptides in vascular physiology and pathology. Int Rev Cell Mol Biol 268:59–93

    Article  CAS  PubMed  Google Scholar 

  • Woodard GE, Rosado JA, Brown J (2002) Expression and control of C-type natriuretic peptide in rat vascular smooth muscle cells. Am J Phys Regul Integr Comp Phys 282:156–165

    Google Scholar 

  • Yamaji T, Ishibashi M, Takaku F, Sato F, Kamoi K, Nakaoka H, Fujii J, Hasegawa K, Morii H (1987) Clinical significance of atrial natriuretic peptide in human blood. Jpn J Med 26:207–211

    Article  CAS  PubMed  Google Scholar 

  • Yamane T, Takemura N, Inoue H, Soeta S, Oishi M, Amasaki H (2011) Preliminary immunohistochemical study of natriuretic peptide receptor localization in canine and feline heart. J Vet Med Sci 73:375–378

    Article  CAS  PubMed  Google Scholar 

  • Yasue H, Yoshimura M, Sumida H, Kikuta K, Kugiyama K, Jougasaki M, Ogaw H, Okumura K, Mukoyama M, Nakao K (1994) Localization and mechanism of secretion of B-type natriuretic peptide in comparison with those of A-type natriuretic peptide in normal subjects and patients with heart failure. Circulation 90:195–203

    Article  CAS  PubMed  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 ischemia and reperfusion. Nephrol Dial Transplant 14:1982–1990

    Article  CAS  PubMed  Google Scholar 

  • Zatzman ML, Thornhill GV (1989) Plasma levels of atrial natriuretic factor in nonhibernating and hibernating marmots. Cryobiology 26:196–198

    Article  CAS  PubMed  Google Scholar 

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Conceived of and designed the experiments: MÖ1, MÖ, NL, FB. Performed the experiments: NL, FB. Analyzed the data: MÖ1, MÖ. Contributed reagents/materials/analysis tools: MÖ1, MÖ, NL, FB, EE, LE. Wrote the paper: MÖ1, NL.

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Correspondence to Mustafa Öztop.

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Öztop, M., Özbek, M., Liman, N. et al. Localization profiles of natriuretic peptides in hearts of pre-hibernating and hibernating Anatolian ground squirrels (Spermophilus xanthoprymnus). Vet Res Commun 43, 45–65 (2019). https://doi.org/10.1007/s11259-019-9745-5

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