Nonhematological mechanisms of improved sea-level performance after hypoxic exposure

Medicine and Science in Sports and Exercise

Volumn 39, Issue 9, 2007, Pages 1600-1609

  Gore, Christopher John ^a,b   Clark, Sally A ^a   Saunders, Philo U ^a  

^a AUSTRALIAN INSTITUTE OF SPORT   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

Author keywords

Efficiency; Erythropoiesis; Muscle buffering; Muscle pH

Indexed keywords

LACTIC ACID;

ANGIOGENESIS; ATHLETE; CONFERENCE PAPER; ENDURANCE; ERYTHROCYTE; ERYTHROPOIESIS; GLUCOSE TRANSPORT; GLYCOLYSIS; HEMATOCRIT; HUMAN; HYPOXIA; MITOCHONDRION; PERFORMANCE; PH; SEA LEVEL;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ALTITUDE; ANOXIA; ERYTHROCYTES; ERYTHROPOIESIS; HUMANS; MITOCHONDRIA; OXYGEN CONSUMPTION; PHYSICAL ENDURANCE; PHYSICAL FITNESS; SPORTS; TASK PERFORMANCE AND ANALYSIS;

EID: 34548391772     PISSN: 01959131     EISSN: 15300315     Source Type: Journal    
DOI: 10.1249/mss.0b013e3180de49d3     Document Type: Conference Paper

References (86)

1. ARNAUD, J., J. C. QUILICI, N. GUTIERREZ, J. BEARD, and H. VERGNES. Methaemoglobin and erythrocyte reducing systems in high-altitude natives. Ann. Hum. Biol. 6:585-592, 1979.
2. ASANO, M., K. KANEOKA, T. NOMURA, et al. Increase in serum vascular endothelial growth factor levels during altitude training. Acta Physiol. Scand. 162:455-459, 1998.
3. ASHENDEN, M. J., C. J. GORE, G. P. DOBSON, et al. Simulated moderate altitude elevates serum erythropoietin but does not increase reticulocyte production in well-trained runners. Eur. J. Appl. Physiol. 81:428-435, 2000.
4. ASHENDEN, M. J., C. J. GORE, G. P. DOBSON, and A. G. HAHN. "Live high, train low" does not change the total haemoglobin mass of male endurance athletes sleeping at a simulated altitude of 3000 m for 23 nights. Eur. J. Appl. Physiol. Occup. Physiol. 80: 479-484, 1999.
5. ASHENDEN, M. J., C. J. GORE, D. T. MARTIN, G. P. DOBSON, and A. G. HAHN. Effects of a 12-day "live high, train low" camp on reticulocyte production and haemoglobin mass in elite female road cyclists. Eur. J. Appl. Physiol. Occup. Physiol. 80:472-478, 1999.
6. AUGHEY, R. J., C. J. GORE, A. G. HAHN, et al. Chronic intermittent hypoxia and incremental cycling exercise independently depress muscle in vitro maximal Na+-K+-ATPase activity in well-trained athletes. J. Appl. Physiol. 98:186-192, 2005.
7. BAILEY, D. M., B. DAVIES, L. ROMER, L. CASTELL, E. NEWSHOLME, and G. GANDY. Implications of moderate altitude training for sea-level endurance in elite distance runners. Eur. J. Appl. Physiol. Occup. Physiol. 78:360-368, 1998.
8. BEALL, C. M. Tibetan and Andean patterns of adaptation to high-altitude hypoxia. Hum. Biol. 72:201-228, 2000.
9. BEALL, C. M., G. M. BRITTENHAM, K. P. STROHL, et al. Hemoglobin concentration of high-altitude Tibetans and Bolivian Aymara. Am. J. Phys. Anthropol. 106:385-400, 1998.
10. BEALL, C. M., M. J. DECKER, G. M. BRITTENHAM, I. KUSHNER, A. GEBREMEDHIN, and K. P. STROHL. An Ethiopian pattern of human adaptation to high-altitude hypoxia. Proc. Natl. Acad. Sci. U. S. A. 99:17215-17218, 2002.
11. BEALL, C. M., and A. B. REICHSMAN. Hemoglobin levels in a Himalayan high altitude population. Am. J. Phys. Anthropol. 63:301-306, 1984.
12. BEALL, C. M., K. P. STROHL, J. BLANGERO, et al. Ventilation and hypoxic ventilatory response of Tibetan and Aymara high altitude natives. Am. J. Phys. Anthropol. 104:427-447, 1997.
13. BEAVER, W. L., K. WASSERMAN, and B. J. WHIPP. Bicarbonate buffering of lactic acid generated during exercise. J. Appl. Physiol. 60:472-478, 1986.
14. BESARAB, A. Physiological and pharmacodynamic considerations for route of EPO administration. Semin. Nephrol. 20:364-374, 2000.
15. CHAPMAN, R. F., J. STRAY-GUNDERSEN, and B. D. LEVINE. Individual variation in response to altitude training. J. Appl. Physiol. 85: 1448-1456, 1998.
16. CLARK, S. A., R. J. AUGHEY, C. J. GORE, et al. Effects of live high, train low hypoxic exposure on lactate metabolism in trained humans. J. Appl. Physiol. 96:517-525, 2004.
17. CLINE, G. W., A. J. VIDAL-PUIG, S. DUFOUR, K. S. CADMAN, B. B. LOWELL, and G. I. SHULMAN. In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J. Biol. Chem. 276:20240-20244, 2001.
18. DI PRAMPERO, P. E. The energy cost of human locomotion on land and in water. Int. J. Sports Med. 7:55-72, 1986.
19. DUBOUCHAUD, H., G. E. BUTTERFIELD, E. E. WOLFEL, B. C. BERGMAN, and G. A. BROOKS. Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 278:E571-E579, 2000.
20. FAVIER, R., H. SPIELVOGEL, D. DESPLANCHES, et al. Training in hypoxia vs. training in normoxia in high-altitude natives. J. Appl. Physiol. 78:2286-2293, 1995.
21. GEERS, C., and G. GROS. Carbon dioxide transport and carbonic anhydrase in blood and muscle. Physiol. Rev. 80:681-715, 2000.
22. GORE, C. J., A. G. HAHN, R. J. AUGHEY, et al. Live high:train low increases muscle buffer capacity and submaximal cycling efficiency. Acta Physiol. Scand. 173:275-286, 2001.
23. GORE, C. J., F. A. RODRIGUEZ, M. J. TRUIJENS, N. E. TOWNSEND, J. STRAY-GUNDERSEN, and B. D. LEVINE. Increased serum erythropoietin but not red cell production after 4 wk of intermittent hypobaric hypoxia (4000-5500 m). J. Appl. Physiol. 101:1386-1393, 2006.
24. GRANNEMAN, J. G., Y. ZHAI, and K. N. LAHNERS. Selective upregulation of alpha1a-adrenergic receptor protein and mRNA in brown adipose tissue by neural and beta3-adrenergic stimulation. Mol. Pharmacol. 51:644-650, 1997.
25. GREEN, H. J., B. ROY, S. GRANT, et al. Increases in submaximal cycling efficiency mediated by altitude acclimatization. J. Appl. Physiol. 89:1189-1197, 2000.
26. GROVER, R. F., and P. BÄRTSCH. Blood. In: High Altitude. An Exploration of Human Adaptation, T. F. Hornbein and R. B. Schoene (Eds.). New York, NY: Dekkar, 2001, pp. 493-523.
27. HAHN, A. G., and C. J. GORE. The effect of altitude on cycling performance: a challenge to traditional concepts. Sports Med. 31:533-557, 2001.
28. HAHN, A. G., C. J. GORE, D. T. MARTIN, M. J. ASHENDEN, A. D. ROBERTS, and P. A. LOGAN. An evaluation of the concept of living at moderate altitude and training at sea level. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 128:777-789, 2001.
29. HANSEN, J. E., G. P. STELTER, and J. A. VOGEL. Arterial pyruvate, lactate, pH, and PCO2 during work at sea level and high altitude. J. Appl. Physiol. 23:523-530, 1967.
30. HOCHACHKA, P. W. Patterns of O2-dependence of metabolism. Adv. Exp. Med. Biol. 222:143-151, 1988.
31. HOCHACHKA, P. W., C. STANLEY, G. O. MATHESON, D. C. MCKENZIE, P. S. ALLEN, and W. S. PARKHOUSE. Metabolic and work efficiencies during exercise in Andean natives. J. Appl. Physiol. 70:1720-1730, 1991.
32. HOPKINS, W. G., and D. J. HEWSON. Variability of competitive performance of distance runners. Med. Sci. Sports Exerc. 33:1588-1592, 2001.
33. HUANG, L. E., J. GU, M. SCHAU, and H. F. BUNN. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 95:7987-7992, 1998.
34. JELKMANN, W. The enigma of the metabolic fate of circulating erythropoietin (Epo) in view of the pharmacokinetics of the recombinant drugs rhEpo and NESP. Eur. J. Haematol. 69:265-274, 2002.
35. JUEL, C., L. GRUNNET, M. HOLSE, S. KENWORTHY, V. SOMMER, and T. WULFF. Reversibility of exercise-induced translocation of Na+-K+ pump subunits to the plasma membrane in rat skeletal muscle. Pflugers Arch. 443:212-217, 2001.
36. JUEL, C., and A. P. HALESTRAP. Lactate transport in skeletal muscle - role and regulation of the monocarboxylate transporter. J. Physiol. 517:633-642, 1999.
37. JUEL, C., C. LUNDBY, M. SANDER, J. A. CALBET, and G. HALL. Human skeletal muscle and erythrocyte proteins involved in acid-base homeostasis: adaptations to chronic hypoxia. J. Physiol. 548:639-648, 2003.
38. JULIAN, C. G., C. J. GORE, R. L. WILBER, et al. Intermittent normobaric hypoxia does not alter performance or erythropoietic markers in highly trained distance runners. J. Appl. Physiol. 96:1800-1807, 2004.
39. KADENBACH, B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 1604:77-94, 2003.
40. KALLIO, P. J., W. J. WILSON, S. O'BRIEN, Y. MAKINO, and L. POELLINGER. Regulation of the hypoxiainducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 274:6519-6525, 1999.
41. KATAYAMA, K., M. MATSUO, K. ISHIDA, S. MORI, and M. MIYAMURA. Intermittent hypoxia improves endurance performance and submaximal efficiency. High Alt. Med. Biol. 4:291-304, 2003.
42. KATAYAMA, K., K. SATO, H. MATSUO, K. ISHIDA, K. I. IWASAKI, and M. MIYAMURA. Effect of intermittent hypoxia on oxygen uptake during submaximal exercise in endurance athletes. Eur. J. Appl. Physiol. 92:75-83, 2004.
43. KATZ, A. Modulation of glucose transport in skeletal muscle by reactive oxygen species. J. Appl. Physiol. 102:1671-1676, 2007.
44. KINSMAN, T. A., C. J. GORE, A. G. HAHN, et al. Sleep in athletes undertaking protocols of exposure to nocturnal simulated altitude at 2650 m. J. Sci. Med. Sport 8:222-232, 2005.
45. KNAUPP, W., S. KHILNANI, J. SHERWOOD, S. SCHARF, and H. STEINBERG. Erythropoietin response to acute normobaric hypoxia in humans. J. Appl. Physiol. 73:837-840, 1992.
46. LEVINE, B. D., and J. STRAY-GUNDERSEN. $Living high-training low": effect of moderate-altitude acclimatization with low-altitude training on performance. J. Appl. Physiol. 83:102-112, 1997.
47. LEVINE, B. D., J. STRAY-GUNDERSEN, C. J. GORE, and W. G. HOPKINS. Point:counterpoint: positive effects of intermittent hypoxia (live high:train low) on exercise are/are not mediated primarily by augmented red cell volume. J. Appl. Physiol. 99:2053-2055, 2005.
48. LIU, Y., J. M. STEINACKER, C. DEHNERT, et al. Effect of "living high-training low" on the cardiac functions at sea level. Int. J. Sports Med. 19:380-384, 1998.
49. LUKYANOVA, L. D. Molecular, metabolic and functional mechanisms of individual resistance to hypoxia. In: Adaptation Biology and Medicine, B. K. Sharma (Ed.). New Delhi, India: Narosa Publishing House, 1997, pp. 236-250.
50. LUNDBY, C., J. A. CALBET, M. SANDER, et al. Exercise economy does not change after acclimatization to moderate to very high altitude. Scand. J. Med. Sci. Sports. 17:281-291, 2007.
51. LUNDBY, C., J. J. THOMSEN, R. BOUSHEL, et al. Erythropoietin treatment elevates haemoglobin concentration by increasing red cell volume and depressing plasma volume. J. Physiol. 578:309-314, 2007.
52. MARCONI, C., M. MARZORATI, D. SCIUTO, A. FERRI, and P. CERRETELLI. Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia. J. Physiol. 569:667-675, 2005.
53. MATEO, J., M. GARCIA-LECEA, S. CADENAS, C. HERNANDEZ, and S. MONCADA. Regulation of hypoxia-inducible factor-1alpha by nitric oxide through mitochondria-dependent and -independent pathways. Biochem. J. 376:537-544, 2003.
54. MAZZEO, R. S. Altitude, exercise and immune function. Exerc. Immunol. Rev. 11:6-16, 2005.
55. MIZUNO, M., C. JUEL, T. BRO-RASMUSSEN, et al. Limb skeletal muscle adaptation in athletes after training at altitude. J. Appl. Physiol. 68:496-502, 1990.
56. MOGENSEN, M., M. BAGGER, P. K. PEDERSEN, M. FERNSTROM, and K. SAHLIN. Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency. J. Physiol. 571:669-681, 2006.
57. MOORE, L. G., L. CURRAN-EVERETT, T. S. DROMA, et al. Are Tibetans better adapted? Int. J. Sports Med. 13(Suppl. 1):S86-S88, 1992.
58. NEYA, M., T. ENOKI, Y. KUMAI, T. SUGOH, and T. KAWAHARA. The effects of nightly normobaric hypoxia and high intensity training under intermittent normobaric hypoxia on running economy and hemoglobin mass. J. Appl. Physiol. (in press).
59. PARISOTTO, R., C. J. GORE, K. R. EMSLIE, et al. A novel method utilising markers of altered erythropoiesis for the detection of recombinant human erythropoietin abuse in athletes. Haematologica 85:564-572, 2000.
60. PONSOT, E., S. P. DUFOUR, J. ZOLL, et al. Exercise training in normobaric hypoxia in endurance runners. II. Improvement of mitochondrial properties in skeletal muscle. J. Appl. Physiol. 100:1249-1257, 2006.
61. QIAN, Z. M., D. S. XIAO, P. L. TANG, F. Y. YAO, and Q. K. LIAO. Increased expression of transferrin receptor on membrane of erythroblasts in strenuously exercised rats. J. Appl. Physiol. 87:523-529, 1999.
62. REYNAFARJE, C., R. LOZANO, and J. VALDIVIESO. The polycythemia of high altitudes: iron metabolism and related aspects. Blood 14:433-455, 1959.
63. ROUSSET, S., M. C. ALVES-GUERRA, J. MOZO, et al. The biology of mitochondrial uncoupling proteins. Diabetes 53(Suppl. 1):S130-S135, 2004.
64. RUSKO, H. K., H. O. TIKKANEN, and J. E. PELTONEN. Altitude and endurance training. J. Sports Sci. 22:928-944, 2004.
65. RUSKO, H. R. New aspects of altitude training. Am. J. Sports Med. 24:S48-S52, 1996.
66. SALTIN, B. Exercise and the environment: focus on altitude. Res. Q. Exerc. Sport 67:S1-S10, 1996.
67. SALTIN, B., H. LARSEN, N. TERRADOS, et al. Aerobic exercise capacity at sea level and at altitude in Kenyan boys, junior and senior runners compared with Scandinavian runners. Scand. J. Med. Sci. Sports 5:209-221, 1995.
68. SASAKI, R., S. MASUDA, and M. NAGAO. Erythropoietin: multiple physiological functions and regulation of biosynthesis. Biosci. Biotechnol. Biochem. 64:1775-1793, 2000.
69. SAUNDERS, P. U., D. B. PYNE, R. D. TELFORD, and J. A. HAWLEY. Factors affecting running economy in trained distance runners. Sports Med. 34:465-485, 2004.
70. SAUNDERS, P. U., R. D. TELFORD, D. B. PYNE, et al. Improved running economy in elite runners after 20 days of simulated moderate-altitude exposure. J. Appl. Physiol. 96:931-937, 2004.
71. SCHMITT, L., G. MILLET, P. ROBACH, et al. Influence of "living high-training low" on aerobic performance and economy of work in elite athletes. Eur. J. Appl. Physiol. 97:627-636, 2006.
72. SEMENZA, G. L. O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J. Appl. Physiol. 96:1173-1177, 2004.
73. SIMON, T. L. Induced erythrocythemia and athletic performance. Semin. Hematol. 31:128-133, 1994.
74. STRAY-GUNDERSEN, J., R. F. CHAPMAN, and B. D. LEVINE. "Living high-training low" altitude training improves sea level performance in male and female elite runners. J. Appl. Physiol. 91:1113-1120, 2001.
75. SVEDENHAG, J., K. PIEHL-AULIN, C. SKOG, and B. SALTIN. Increased left ventricular muscle mass after long-term altitude training in athletes. Acta Physiol. Scand. 161:63-70, 1997.
76. TOWNSEND, N. E., C. J. GORE, A. G. HAHN, et al. Living high-training low increases hypoxic ventilatory response of well-trained endurance athletes. J. Appl. Physiol. 93:1498-1505, 2002.
77. VARLET-MARIE, E., A. GAUDARD, M. AUDRAN, R. GOMENI, and F. BRESSOLLE. Pharmacokinetic-pharmacodynamic modelling of recombinant human erythropoietin in athletes. Int. J. Sports Med. 24:252-257, 2003.
78. VILLAFUERTE, F. C., R. CARDENAS, and C. C. MONGE. Optimal hemoglobin concentration and high altitude: a theoretical approach for Andean men at rest. J. Appl. Physiol. 96:1581-1588, 2004.
79. VOGT, M., A. PUNTSCHART, J. GEISER, C. ZULEGER, R. BILLETER, and H. HOPPELER. Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J. Appl. Physiol. 91:173-182, 2001.
80. WANG, G. L., B. H. JIANG, E. A. RUE, and G. L. SEMENZA. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U. S. A. 92:5510-5514, 1995.
81. WEIL, J. V., G. JAMIESON, D.W. BROWN, and R. F. GROVER. The red cell mass-arterial oxygen relationship in normal man. Application to patients with chronic obstructive airway disease. J. Clin. Invest. 47:1627-1639, 1968.
82. WEST, J. B. Lactate during exercise at extreme altitude. Fed. Proc. 45:2953-2957, 1986.
83. WEST, J. B. Point: the lactate paradox does/does not occur during exercise at high altitude. J. Appl. Physiol. 102:2398-2399, 2007.
84. WU, T., and B. KAYSER. High altitude adaptation in Tibetans. High Alt. Med. Biol. 7:193-208, 2006.
85. ZHU, H., and H. F. BUNN. Oxygen sensing and signaling: impact on the regulation of physiologically important genes. Respir. Physiol. 115:239-247, 1999.
86. ZOLL, J., E. PONSOT, S. DUFOUR, et al. Exercise training in normobaric hypoxia in endurance runners. III. Muscular adjustments of selected gene transcripts. J. Appl. Physiol. 100:1258-1266, 2006.