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Avian Research 2021, 12(1): 44 https://doi.org/10.1186/s40657-021-00279-0
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Coping with extremes: lowered myocardial phosphofructokinase activities and glucose content but increased fatty acids content in highland Eurasian Tree Sparrows

Show Author's Information Boyang Ding1,  Yuliang Zhao1,  Yanfeng Sun1,2,  Qian Zhang1,  Mo Li1,3,  Ghulam Nabi1,  Yuefeng Wu1,  Chuan Jiang1( ),  Dongming Li1( )
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050010, China
Ocean College, Hebei Agricultural University, 066003, Qinhuangdao, China
College of Life Science, Cangzhou Normal University, 061001, Cangzhou, China
Keywords:
Energy utilization, Eurasian Tree Sparrow, Metabolic enzyme, Myocardium, The Qinghai-Tibet Plateau
Cite this article:
Ding B, Zhao Y, Sun Y, et al. Coping with extremes: lowered myocardial phosphofructokinase activities and glucose content but increased fatty acids content in highland Eurasian Tree Sparrows. Avian Research, 2021, 12(1): 44. https://doi.org/10.1186/s40657-021-00279-0
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Abstract Full text About this article
Background

Efficient and selective utilization of metabolic substrates is one of the key strategies in high-altitude animals to cope with hypoxia and hypothermia. Previous findings have shown that the energy substrate utilization of highland animals varies with evolutionary history and phylogeny. The heart is a proxy for the cardiopulmonary system, and the metabolic substrate utilization in the myocardium is also under the strong selective pressure of chronically hypoxic and hypothermic environments. However, little information is available on the physiological adjustments in relation to metabolic substrate utilization in the myocardium for coping with high-altitude environments.

Methods

We compared the metabolic enzyme activities, including hexokinase (HK), phosphofructokinase (PFK), pyruvate kinase (PK), citrate synthase (CS), carnitine palmitoyl transferase 1 (CPT-1), lactic dehydrogenase (LDH), and creatine kinase (CK), and metabolic substrate contents including glucose (Glu), triglyceride (TG), and free fatty acid (FFA) in the myocardium of a typical human commensal species, Eurasian Tree Sparrows (Passer montanus) between the Qinghai-Tibet Plateau (the QTP, 3230 m) and low altitude population (Shijiazhuang, 80 m), and between sexes.

Results

Among the seven metabolic enzymes and three substrates investigated, we identified no significant differences in PK, CPT-1, HK, CS, LDH, and CK activities and TG content of the myocardium between high and low altitude populations. However, the QTP sparrows had significantly lower Glu content and PFK activities but higher FFA content relative to their lowland counterparts. In addition, male sparrows had higher myocardial HK and CS activities relative to females, independent of altitude.

Conclusions

Our results showed that the QTP sparrows elevated fatty acid utilization rather than glucose preference in the myocardium relative to lowland counterpart, which contributes to uncovering both the physiological adjustments for adapting to the extreme conditions of the QTP, intraspecifically.


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About this article

Coping with extremes: lowered myocardial phosphofructokinase activities and glucose content but increased fatty acids content in highland Eurasian Tree Sparrows

Show Author's information Boyang Ding1, Yuliang Zhao1, Yanfeng Sun1,2, Qian Zhang1, Mo Li1,3, Ghulam Nabi1, Yuefeng Wu1, Chuan Jiang1( ), Dongming Li1( )
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050010, China
Ocean College, Hebei Agricultural University, 066003, Qinhuangdao, China
College of Life Science, Cangzhou Normal University, 061001, Cangzhou, China

Abstract

Background

Efficient and selective utilization of metabolic substrates is one of the key strategies in high-altitude animals to cope with hypoxia and hypothermia. Previous findings have shown that the energy substrate utilization of highland animals varies with evolutionary history and phylogeny. The heart is a proxy for the cardiopulmonary system, and the metabolic substrate utilization in the myocardium is also under the strong selective pressure of chronically hypoxic and hypothermic environments. However, little information is available on the physiological adjustments in relation to metabolic substrate utilization in the myocardium for coping with high-altitude environments.

Methods

We compared the metabolic enzyme activities, including hexokinase (HK), phosphofructokinase (PFK), pyruvate kinase (PK), citrate synthase (CS), carnitine palmitoyl transferase 1 (CPT-1), lactic dehydrogenase (LDH), and creatine kinase (CK), and metabolic substrate contents including glucose (Glu), triglyceride (TG), and free fatty acid (FFA) in the myocardium of a typical human commensal species, Eurasian Tree Sparrows (Passer montanus) between the Qinghai-Tibet Plateau (the QTP, 3230 m) and low altitude population (Shijiazhuang, 80 m), and between sexes.

Results

Among the seven metabolic enzymes and three substrates investigated, we identified no significant differences in PK, CPT-1, HK, CS, LDH, and CK activities and TG content of the myocardium between high and low altitude populations. However, the QTP sparrows had significantly lower Glu content and PFK activities but higher FFA content relative to their lowland counterparts. In addition, male sparrows had higher myocardial HK and CS activities relative to females, independent of altitude.

Conclusions

Our results showed that the QTP sparrows elevated fatty acid utilization rather than glucose preference in the myocardium relative to lowland counterpart, which contributes to uncovering both the physiological adjustments for adapting to the extreme conditions of the QTP, intraspecifically.

Keywords: Energy utilization, Eurasian Tree Sparrow, Metabolic enzyme, Myocardium, The Qinghai-Tibet Plateau

References(75)

Azevedo JL Jr, Carey JO, Pories WJ, Morris PG, Dohm GL. Hypoxia stimulates glucose transport in insulin-resistant human skeletal muscle. Diabetes. 1995;44: 695–8.
DOI Google Scholar

Bagger JP, Thomassen A, Nielsen TT. Cardiac energy metabolism in patients with chest pain and normal coronary angiograms. Am J Cardiol. 2000;85: 315–20.
DOI Google Scholar
Belitz HD, Grosch W, Schieberle P. Food chemistry. 4th ed. Berlin: Springer; 2009.

Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology. 1995;20: 117–34.
DOI Google Scholar

Brooks GA, Butterfield GE, Wolfe RR, Groves BM, Mazzeo RS, Sutton JR, et al. Increased dependence on blood glucose after acclimatization to 4, 300 m. J Appl Physiol. 1991;70: 919–27.
DOI Google Scholar

Brooks GA, Wolfel EE, Groves BM, Bender PR, Butterfield GE, Cymerman A, et al. Muscle accounts for glucose disposal but not blood lactate appearance during exercise after acclimatization to 4, 300 m. J Appl Physiol. 1992;72: 2435–45.
DOI Google Scholar

Burggren WW, Cameron JN. Anaerobic metabolism, gas exchange, and acid–base balance during hypoxic exposure in the channel catfish Ictalurus punctatus. J Exp Zool. 1980;213: 405–16.
DOI Google Scholar
Burggren WW, Farrell AP, Lillywhite HB. Vertebrate cardiovascular systems. In: Terjung R, editor. Comprehensive physiology, Suppl. 30. Handbook of physiology, comparative physiology. Hoboken, NJ: Wiley-Blackwell; 2011.

Calder WA. Respiratory and heart rates of birds at rest. Condor. 1968;70: 358–65.
DOI Google Scholar

Camici PG, Marraccini P, Lorenzoni R, Buzzigoli G, Pecori N, Perissinotto A, et al. Coronary hemodynamics and myocardial metabolism in patients with syndrome X: response to pacing stress. J Am Coll Cardiol. 1991;17: 1461–70.
DOI Google Scholar

Cartee GD, Douen AG, Ramlal T, Klip A, Holloszy JO. Stimulation of glucose transport in skeletal muscle by hypoxia. J Appl Physiol. 1991;70: 1593–600.
DOI Google Scholar
Casiday R, Frey R. Blood, sweat, and buffers: pH regulation during exercise, acid–base equilibria experiment. St. Louis: Washington University; 2012.

Cheviron ZA, Bachman GC, Connaty AD, McClelland GB, Storz JF. Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice. Proc Natl Acad Sci USA. 2012;109: 8635–40.
DOI Google Scholar

Cheviron ZA, Natarajan C, Projecto-Garcia J, Eddy DK, Jones J, Carling MD, et al. Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean sparrow, Zonotrichia capensis. Mol Biol Evol. 2014;31: 2948–62.
DOI Google Scholar

Durmowicz AG, Hofmeister S, Kadyraliev TK, Aldashev AA, Stenmark KR. Functional and structural adaptation of the yak pulmonary circulation to residence at high altitude. J Appl Physiol. 1993;74: 2276–85.
DOI Google Scholar

Faraci FM, Kilgore DL Jr, Fedde MR. Attenuated pulmonary pressor response to hypoxia in bar-headed geese. Am J Physiol. 1984;247: R402–3.
DOI Google Scholar

Fuxe K, Cintra A, Andbjer B, Anggård E, Goldstein M, Agnati LF. Centrally administered endothelin-1 produces lesions in the brain of the male rat. Acta Physiol Scand. 1989;137: 155–6.
DOI Google Scholar

Ge RL, Kubo K, Kobayashi T, Sekiguchi M, Honda T. Blunted hypoxic pulmonary vasoconstrictive response in the rodent Ochotona curzoniae (pika) at high altitude. Am J Physiol. 1998;274: H1792–9.
DOI Google Scholar

Ge RL, Simonson TS, Cooksey RC, Tanna U, Qin G, Huff CD, et al. Metabolic insight into mechanisms of high-altitude adaptation in Tibetans. Mol Genet Metab. 2012;106: 244–7.
DOI Google Scholar

Gertz EW, Wisneski JA, Stanley WC, Neese RA. Myocardial substrate utilization during exercise in humans. Dual carbon-labeled carbohydrate isotope experiments. J Clin Invest. 1988;82: 2017–25.
DOI Google Scholar

Green HJ, Sutton JR, Cymerman A, Young PM, Houston CS. Operation Everest Ⅱ: adaptations in human skeletal muscle. J Appl Physiol. 1989;66: 2454–61.
DOI Google Scholar

Groves BM, Droma T, Sutton JR, McCullough RG, McCullough RE, Zhuang J, et al. Minimal hypoxic pulmonary hypertension in normal Tibetans at 3, 658 m. J Appl Physiol. 1985;1993(74): 312–8.
DOI Google Scholar

Grubb BR. Allometric relations of cardiovascular function in birds. Am J Physiol. 1983;245: H567–72.
DOI Google Scholar

Hao Y, Xiong Y, Cheng Y, Song G, Jia C, Qu Y, et al. Comparative transcriptomics of 3 high-altitude passerine birds and their low-altitude relatives. Proc Natl Acad Sci USA. 2019;116: 11851–6.
DOI Google Scholar

Hayward CS, Webb CM, Collins P. Effect of sex hormones on cardiac mass. Lancet. 2001;357: 1354–6.
DOI Google Scholar

Hebisz R, Hebisz P, Borkowski J, Zatoń M. Differences in physiological responses to interval training in cyclists with and without interval training experience. J Hum Kinet. 2016;50: 93–101.
DOI Google Scholar
Hochachka PW, Somero GN. Biochemical adaptation. Mechanism and process in physiological evolution. New York: Oxford University Press; 2002.

Holden JE, Stone CK, Clark CM, Brown WD, Nickles RJ, Stanley C, et al. Enhanced cardiac metabolism of plasma glucose in high-altitude natives: adaptation against chronic hypoxia. J Appl Physiol. 1995;79: 222–8.
DOI Google Scholar

Horscroft JA, Kotwica AO, Laner V, West JA, Hennis PJ, Levett DZH, et al. Metabolic basis to Sherpa altitude adaptation. Proc Natl Acad Sci USA. 2017;114: 6382–7.
DOI Google Scholar

Ingwall JS, Kramer MF, Fifer MA, Lorell BH, Shemin R, Grossman W, et al. The creatine kinase system in normal and diseased human myocardium. N Engl J Med. 1985;313: 1050–4.
DOI Google Scholar

Ivy CM, Scott GR. Control of breathing and the circulation in high-altitude mammals and birds. Comp Biochem Phys A. 2015;186: 66–74.
DOI Google Scholar

Jing XP, Wang WJ, Degen AA, Guo YM, Kang JP, Liu PP, et al. Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep. Animal. 2021;15: 100162.
DOI Google Scholar

Kaur H, Parikh V, Sharma A, Singh M. Effect of amiloride a Na+/H+ exchange inhibitor on cardioprotective effect of ischaemic preconditioning: possible involvement of resident cardiac mast cells. Pharmacol Res. 1997;36: 95–102.
DOI Google Scholar

Kodde IF, van der Stok J, Smolenski RT, de Jong JW. Metabolic and genetic regulation of cardiac energy substrate preference. Comp Biochem Phys A. 2007;146: 26–39.
DOI Google Scholar

Kolar F, Ostadal B. Sex differences in cardiovascular function. Acta Physiol. 2013;207: 584–7.
DOI Google Scholar
Koolhaas JM, Meerlo P, de Boer SF, Strubbe JH, Bohus B. Social stress in rats: an animal model of depression? Acta Neuropsychiatr. 1995;7: 27–9.https://doi.org/10.1017/S0924270800037479
DOI

Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E. Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res. 2010;106: 1681–91.
DOI Google Scholar

Li D, Wu J, Zhang X, Ma X, Wingfield JC, Lei F, et al. Comparison of adrenocortical responses to acute stress in lowland and highland Eurasian Tree Sparrows (Passer montanus): similar patterns during the breeding, but different during the prebasic molt. J Exp Zool A Ecol Genet Physiol. 2011;315: 512–9.
DOI Google Scholar

Lopaschuk GD, Ussher JR, Folmes CDL, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90: 207–58.
DOI Google Scholar

Martinez M, Calvo-Torrent A, Pico-Alfonso MA. Social defeat and subordination as models of social stress in laboratory rodents: a review. Aggressive Behav. 1998;24: 241–56.
DOI

Milerová M, Drahota Z, Chytilová A, Tauchmannová K, Houštěk J, Ošťádal B. Sex difference in the sensitivity of cardiac mitochondrial permeability transition pore to calcium load. Mol Cell Biochem. 2016;412: 147–54.
DOI Google Scholar

Mónus F, Szabó K, Lózsa A, Pénzes Z, Barta Z. Intersexual size and plumage differences in tree sparrows (Passer montanus)—a morphologicals study based on molecular sex determination. Acta Zool Acad Sci H. 2011;57: 269–77.
Google Scholar

Murphy E. Estrogen signaling and cardiovascular disease. Circ Res. 2011;109: 687–96.
DOI Google Scholar

Neglia D, de Caterina A, Marraccini P, Natali A, Ciardetti M, Vecoli C, et al. Impaired myocardial metabolic reserve and substrate selection flexibility during stress in patients with idiopathic dilated cardiomyopathy. Am J Physiol Heart Circ Physiol. 2007;293: H3270–8.
DOI Google Scholar

Pilarski JQ, Solomon IC, Kilgore DL Jr, Hempleman SC. Effects of aerobic and anaerobic metabolic inhibitors on avian intrapulmonary chemoreceptors. Am J Physiol Regul Integr Comp Physiol. 2009;296: R1576–84.
DOI Google Scholar

Pulinilkunnil T, Rodrigues B. Cardiac lipoprotein lipase: metabolic basis for diabetic heart disease. Cardiovasc Res. 2006;69: 329–40.
DOI Google Scholar

Qiu Q, Zhang G, Ma T, Qian W, Wang J, Ye Z, et al. The yak genome and adaptation to life at high altitude. Nat Genet. 2012;44: 946–9.
DOI Google Scholar

Qu Y, Zhao H, Han N, Zhou G, Song G, Gao B, et al. Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan plateau. Nat Commun. 2013;4: 2071.
DOI Google Scholar

Qu Y, Tian S, Han N, Zhao H, Gao B, Fu J, et al. Genetic responses to seasonal variation in altitudinal stress: whole-genome resequencing of great tit in eastern Himalayas. Sci Rep. 2015;5: 14256.
DOI Google Scholar

Qu Y, Chen C, Xiong Y, She H, Zhang YE, Cheng Y, et al. Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in Eurasian Tree Sparrows. Natl Sci Rev. 2020;7: 113–27.
DOI Google Scholar

Roberts AC, Butterfield GE, Cymerman A, Reeves JT, Wolfel EE, Brooks GA. Acclimatization to 4, 300-m altitude decreases reliance on fat as a substrate. J Appl Physiol. 1996a;81: 1762–71.
DOI Google Scholar

Roberts AC, Reeves JT, Butterfield GE, Mazzeo RS, Sutton JR, Wolfel EE, et al. Altitude and beta-blockade augment glucose utilization during submaximal exercise. J Appl Physiol. 1996b;80: 605–15.
DOI Google Scholar

Sakai A, Matsumoto T, Saitoh M, Matsuzaki T, Koizumi T, Ishizaki T, et al. Cardiopulmonary hemodynamics of blue-sheep, Pseudois nayaur, as high-altitude adapted mammals. Jpn J Physiol. 2003;53: 377–84.
DOI Google Scholar

Samaja M, Mariani C, Prestini A, Cerretelli P. Acid–base balance and O2 transport at high altitude. Acta Physiol Scand. 1997;159: 249–56.
DOI Google Scholar
Scott GR, Milsom WK. Control of breathing and adaptation to high altitude in the bar-headed goose. Am J Physiol-Reg. 2007;I(293): R379–91.https://doi.org/10.1152/ajpregu.00161.2007
DOI

Scott GR, Schulte PM, Egginton S, Scott AL, Richards JG, Milsom WK. Molecular evolution of cytochrome C oxidase underlies high-altitude adaptation in the bar-headed goose. Mol Biol Evol. 2011;28: 351–63.
DOI Google Scholar

Sears MW, Hayes JP, O'Connor CS, Geluso K, Sedinger JS. Individual variation in thermogenic capacity affects above-ground activity of high-altitude Deer Mice. Funct Ecol. 2006;20: 97–104.
DOI Google Scholar

Shao Y, Li JX, Ge RL, Zhong L, Irwin DM, Murphy RW, et al. Genetic adaptations of the plateau zokor in high-elevation burrows. Sci Rep. 2015;5: 17262.
DOI Google Scholar

Storz JF, Moriyama H. Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Alt Med Biol. 2008;9: 148–57.
DOI Google Scholar

Storz JF, Scott GR, Cheviron ZA. Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol. 2010;213: 4125–36.
DOI Google Scholar
Summers-Smith D. Eurasian tree sparrow (Passer montanus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E, editors. Handbook of the birds of the world alive. Barcelona: Lynx Edicions; 2018. p. 217–44.

Sun YF, Ren ZP, Wu YF, Lei FM, Dudley R, Li DM. Flying high: limits to flight performance by sparrows on the Qinghai-Tibet Plateau. J Exp Biol. 2016;219: 3642–8.
Google Scholar

Sun YF, Li M, Song G, Lei FM, Li DM, Wu YF. The role of climate factors in geographic variation in body mass and wing length in a passerine bird. Avian Res. 2017;8: 1.
DOI Google Scholar

Sutton JR, Jones NL, Griffith L, Pugh CE. Exercise at altitude. Annu Rev Physiol. 1983;45: 427–37.
DOI Google Scholar

Tate KB, Ivy CM, Velotta JP, Storz JF, McClelland GB, Cheviron ZA, et al. Circulatory mechanisms underlying adaptive increases in thermogenic capacity in high-altitude deer mice. J Exp Biol. 2017;220: 3616–20.
Google Scholar

Thompson LG, Yao T, Mosley-Thompson E, Davis ME, Henderson KA, Lin P-N. A high-resolution millennial record of the south Asian monsoon from Himalayan ice cores. Science. 2000;289: 1916–9.
DOI Google Scholar

Vaillancourt E, Haman F, Weber JM. Fuel selection in Wistar rats exposed to cold: shivering thermogenesis diverts fatty acids from re-esterification to oxidation. J Physiol. 2009;587: 4349–59.
DOI Google Scholar

van der Vusse GJ, Glatz JF, Stam HC, Reneman RS. Fatty acid homeostasis in the normoxic and ischemic heart. Physiol Rev. 1992;72: 881–940.
DOI Google Scholar

Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol. 2004;555: 1–13.
DOI Google Scholar

Vinet A, Mandigout S, Nottin S, Nguyen LD, Lecoq AM, Courteix D, et al. Influence of body composition, hemoglobin concentration, and cardiac size and function of gender differences in maximal oxygen uptake in prepubertal children. Chest. 2003;124: 1494–9.
DOI Google Scholar

Wang X, Hole DG, da Costa TH, Evans RD. Alterations in myocardial lipid metabolism during lactation in the rat. Am J Physiol. 1998;275: E265–71.
DOI Google Scholar

Weber JM. Metabolic fuels: regulating fluxes to select mix. J Exp Biol. 2011;214: 286–94.
DOI Google Scholar

Young AJ, Evans WJ, Cymerman A, Pandolf KB, Knapik JJ, Maher JT. Sparing effect of chronic high-altitude exposure on muscle glycogen utilization. J Appl Physiol. 1982;52: 857–62.
DOI Google Scholar

Zhu X, Guan Y, Signore AV, Natarajan C, DuBay SG, Cheng Y, et al. Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA. 2018;115: 1865–70.
DOI Google Scholar

Zinker BA, Namdaran K, Wilson R, Lacy DB, Wasserman DH. Acute adaptation of carbohydrate metabolism to decreased arterial PO2. Am J Physiol. 1994;266: E921–9.
DOI Google Scholar
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Publication history

Received: 19 April 2021
Accepted: 01 September 2021
Published: 09 September 2021
Issue date: January 2021

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© The Author(s) 2021.

Acknowledgements

Acknowledgements

We thank Zhipeng Ren, Yinchao Hao, Simeng Yu, and Haiqing He for theirassistance with sample collection in the field.

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