Metabolic Characteristics and Response to High Altitude in Phrynocephalus erythrurus (Lacertilia: Agamidae), a Lizard Dwell at Altitudes Higher Than Any Other Living Lizards in the World

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Tang, Xiaolong ^a   Xin, Ying ^a   Wang, Huihui ^a   Li, Weixin ^a   Zhang, Yang ^a   Liang, Shiwei ^a   He, Jianzheng ^a   Wang, Ningbo ^a   Ma, Ming ^a   Chen, Qiang ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CITRATE SYNTHASE; LACTATE DEHYDROGENASE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ALTITUDE ACCLIMATIZATION; ANAEROBIC METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; LIZARD; MALE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN TENSION; PHRYNOCEPHALUS ERYTHRURUS; PHRYNOCEPHALUS PRZEWALSKII; PROTEIN EXPRESSION; SPECIES COMPARISON;

ACCLIMATIZATION; ALTITUDE; ANIMALS; ATRACTYLOSIDE; CITRATE (SI)-SYNTHASE; ENERGY METABOLISM; GENE EXPRESSION; GUANOSINE DIPHOSPHATE; L-LACTATE DEHYDROGENASE; LIVER; LIZARDS; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; PPAR GAMMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84881350983     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071976     Document Type: Article

References (48)

1. Storz JF, Scott GR, Cheviron ZA, (2010) Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol 213: 4125-4136. doi:10.1242/jeb.048181. PubMed: 21112992.
2. Beall CM, (2007) Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104: 8655-8660. doi:10.1073/pnas.0701985104. PubMed: 17494744.
3. León-Velarde F, Sanchez J, Bigard AX, Brunet A, Lesty C, et al. (1993) High altitude tissue adaptation in Andean coots: capillarity, fibre area, fibre type and enzymatic activities of skeletal muscle. J Comp Physiol B Biochem Syst Environ Physiol 163: 52-58. doi:10.1007/BF00309665. PubMed: 8459054.
4. Qiu Q, Zhang G, Ma T, Qian W, Wang J, et al. (2012) The yak genome and adaptation to life at high altitude. Nat Genet 44: 946-949. doi:10.1038/ng.2343. PubMed: 22751099.
5. Hoppeler H, Vogt M, Weibel ER, Flück M, (2003) Response of skeletal muscle mitochondria to hypoxia. Exp Physiol 88: 109-119. doi:10.1113/eph8802513. PubMed: 12525860.
6. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, et al. (2004) Developmental plasticity and human health. Nat 430: 419-421. doi:10.1038/nature02725. PubMed: 15269759.
7. Feala JD, Coquin L, Zhou D, Haddad GG, Paternostro G, et al. (2009) Metabolism as means for hypoxia adaptation: metabolic profiling and flux balance analysis. BMC Syst Biol 3: 91. doi:10.1186/1752-0509-3-91. PubMed: 19740440.
8. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC, (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3: 187-197. doi:10.1016/j.cmet.2006.01.012. PubMed: 16517406.
9. St-Pierre J, Tattersall GJ, Boutilier RG, (2000) Metabolic depression and enhanced O2 affinity of mitochondria in hypoxic hypometabolism. Am J Physiolreg I279:: 1205-1214.
10. Muleme HM, Walpole AC, Staples JF, (2006) Mitochondrial Metabolism in Hibernation: Metabolic Suppression, Temperature Effects, and Substrate Preferences. Physiol Biochem Zool 79: 474-483. doi:10.1086/501053. PubMed: 16691514.
11. Boutilier RG, (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204: 3171-3181. PubMed: 11581331.
12. St-Pierre J, Brand MD, Boutilier RG, (2000) The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203: 1469-1476. PubMed: 10751162.
13. Boutilier RG, St-Pierre J, (2002) Adaptive plasticity of skeletal muscle energetics in hibernating frogs: mitochondrial proton leak during metabolic depression. J Exp Biol 205: 2287-2296. PubMed: 12110662.
14. Rolfe DFS, Newman JMB, Buckingham JA, Clark MG, Brand MD, (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiolcell Ph 276: C692-C699. PubMed: 10069997.
15. Pierce VA, Crawford DL, (1997) Phylogenetic analysis of glycolytic enzyme expression. Sci 276: 256-259. doi:10.1126/science.276.5310.256. PubMed: 9092475.
16. Kennedy SL, Stanley WC, Panchal AR, Mazzeo RS, (2001) Alterations in enzymes involved in fat metabolism after acute and chronic altitude exposure. J Appl Physiol 90: 17-22. PubMed: 11133888.
17. J St-Pierre, G Boutilier R (2001) Aerobic Capacity of Frog Skeletal Muscle during Hibernation. Physiol Biochem Zool 74: 390-397.
18. He J, Xiu M, Tang X, Yue F, Wang N, et al. (2013) The Different Mechanisms of Hypoxic Acclimatization and Adaptation in Lizard Phrynocephalus vlangalii Living on Qinghai-Tibet Plateau. J Exp Zool A. 319: 117-123. doi:10.1002/jez.1776. PubMed: 23319459.
19. He J, Xiu M, Tang X, Wang N, Xin Y, et al. (2013) Thermoregulatory and metabolic responses to hypoxia in the oviparous lizard, Phrynocephalus przewalskii. Comp Biochem Physiol A Mol Integr Physiol 165: 207-213. doi:10.1016/j.cbpa.2013.03.007. PubMed: 23500623.
20. Scarpulla RC, (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. BBA-Mol. Cell Res 1813: 1269-1278.
21. Storey KB, (2003) Mammalian hibernation. Transcriptional and translational controls. Adv Exp Med Biol 543: 21-38. doi:10.1007/978-1-4419-8997-0_3. PubMed: 14713112.
22. Puigserver P, Wu Z, Park CW, Graves R, Wright M, et al. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839. doi:10.1016/S0092-8674(00)81410-5. PubMed: 9529258.
23. Pearson OP, (1954) Habits of the Lizard Liolaemus multiformis multiformis at High Altitudes in Southern Peru. Copeia: pp. 1954: 111-116.
24. Bennett AF, Ruben J, (1975) High altitude adaptation and anaerobiosis in sceloporine lizards. Comp Biochem Physiol A Physiol 50: 105-108. doi:10.1016/S0010-406X(75)80209-X. PubMed: 234037.
25. Pearson OP, Bradford DF, (1976) Thermoregulation of Lizards and Toads at High Altitudes in Peru. Copeia: pp. 1976: 155-170.
26. Wood SC, Gonzales R, (1996) Hypothermia in hypoxic animals: mechanisms, mediators, and functional significance. Comp Biochem Physiol B Biochem Mol Biol 113: 37-43. doi:10.1016/0305-0491(95)02045-4. PubMed: 8936041.
27. Zhao E, Adler K, (1993) Herpetology of China.
28. Jin Y-T, Liu N-F, (2010) Phylogeography of Phrynocephalus erythrurus from the Qiangtang Plateau of the Tibetan Plateau. Mol Phylogenet Evol 54: 933-940. doi:10.1016/j.ympev.2009.11.003. PubMed: 19900565.
29. Rey B, Sibille B, Romestaing C, Belouze M, Letexier D, et al. (2008) Reptilian uncoupling protein: functionality and expression in sub-zero temperatures. J Exp Biol 211: 1456-1462. doi:10.1242/jeb.012328. PubMed: 18424679.
30. Guderley H, Seebacher F, (2010) Thermal acclimation, mitochondrial capacities and organ metabolic profiles in a reptile (Alligator mississippiensis). J Comp Physiol B 181(1):: 53-64. PubMed: 20680297.
31. Seebacher F, Guderley H, Elsey RM, Trosclair PL, (2003) Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J Exp Biol 206: 1193-1200. doi:10.1242/jeb.00223. PubMed: 12604579.
32. John-Alder HB, Joos B, (1991) Interactive effects of thyroxine and experimental location on running endurance, tissue masses, and enzyme activities in captive versus field-active lizards (Sceloporus undulatus). Gen Comp Endocrinol 81: 120-132. doi:10.1016/0016-6480(91)90132-P. PubMed: 2026310.
33. Livak KJ, Schmittgen TD, (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 < sup>- ΔΔCT Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
34. Hulbert AJ, Else PL, Manolis SC, Brand MD, (2002) Proton leak in hepatocytes and liver mitochondria from archosaurs (crocodiles) and allometric relationships for ectotherms. J Comp Physiol B 172: 387-397. doi:10.1007/s00360-002-0264-1. PubMed: 12122455.
35. Glanville EJ, Seebacher F, (2006) Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J Exp Biol 209: 4869-4877. doi:10.1242/jeb.02585. PubMed: 17142675.
36. Solaini G, Baracca A, Lenaz G, Sgarbi G, (2010) Hypoxia and mitochondrial oxidative metabolism. BBA-Bioenergetics 1797: 1171-1177.
37. de Souza SCR, de Carvalho JE, Abe AS, Bicudo JEPW, Bianconcini MSC, (2004) Seasonal metabolic depression, substrate utilisation and changes in scaling patterns during the first year cycle of tegu lizards (Tupinambis merianae). J Exp Biol 207: 307-318. doi:10.1242/jeb.00756. PubMed: 14668314.
38. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ, (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275: 81-86. PubMed: 1850242.
39. Rolfe DFS, Brand MD, (1997) The Physiological Significance of Mitochondrial Proton Leak in Animal Cells and Tissues. Biosci Rep 17: 9-16. PubMed: 9171916.
40. Rolfe DF, Brand MD, (1996) Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiolcell Ph 271: C1380-C1389. PubMed: 8897845.
41. Sheafor BA, (2003) Metabolic enzyme activities across an altitudinal gradient: an examination of pikas (genus Ochotona). J Exp Biol 206: 1241-1249. doi:10.1242/jeb.00226. PubMed: 12604584.
42. Hochachka PW, (1998) Mechanism and evolution of hypoxia-tolerance in humans. J Exp Biol 201: 1243-1254. PubMed: 9510535.
43. Hoppeler H, Vogt M, (2001) Muscle tissue adaptations to hypoxia. J Exp Biol 204: 3133-3139. PubMed: 11581327.
44. Kuang L, Zheng Y, Lin Y, Xu Y, Jin S, et al. (2010) High-Altitude Adaptation of Yak Based on Genetic Variants and Activity of Lactate Dehydrogenase-1. Biochem Genet 48: 418-427. doi:10.1007/s10528-009-9322-7. PubMed: 20047072.
45. Hochachka PW, Stanley C, Merkt J, Sumar-Kalinowski J, (1983) Metabolic meaning of elevated levels of oxidative enzymes in high altitude adapted animals: an interpretive hypothesis. Respir Physiol 52: 303-313. doi:10.1016/0034-5687(83)90087-7. PubMed: 6612104.
46. Barnard RJ, Peter JB, (1969) Effect of training and exhaustion on hexokinase activity of skeletal muscle. J Appl Physiol 27: 691-695. PubMed: 5360446.
47. Staudte HW, Exner GU, Pette D, (1973) Effects of short-term, high intensity (sprint) training on some contractile and metabolic characteristics of fast and slow muscle of the rat. Pflug Arch Eur J Phy 344: 159-168. doi:10.1007/BF00586549. PubMed: 4797950.
48. Storey KB, (1996) Metabolic adaptations supporting anoxia tolerance in reptiles: Recent advances. Comp Biochem Physiol B Biochem Mol Biol 113: 23-35. doi:10.1016/0305-0491(95)02043-8. PubMed: 8936040.