Testis-Specific Lactate Dehydrogenase (LDH-C4) in Skeletal Muscle Enhances Apika’s Sprint-Running Capacity in Hypoxic Environment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animal Procedures
2.2. Enzyme and Inhibitor Preparation
2.3. Enzyme Kinetics of N-Propyl Oxamate and N-Isopropyl Oxamateon LDH Isozymes
2.4. Exercise Tolerance Experiments for Plateau Pikas
2.5. Activity of LDH, the Content of LD and ATP Assay
2.6. Data Analysis
3. Results
3.1. Enzyme Kinetic Properties of N-Propyl Oxamate and N-Isopropyl Oxamate on LDH Isozymes
3.2. Swimming Time and Biochemistry Assay after Exercise Tolerance Experiment
4. Discussion
5. Conclusions
Acknowledgements
Author Contributions
Conflicts of Interest
References
- Wu, T. High altitude adaptation in Tibetans. High. Alt. Med. Biol 2006, 7, 193–208. [Google Scholar] [CrossRef] [PubMed]
- Groves, B.M.; Droma, T.; Sutton, J.R.; McCullough, R.G.; McCullough, R.E.; Zhuang, J.; Rapmund, G.; Sun, S.; Janes, C.; Moore, L.G. Minimal hypoxic pulmonary hypertension in normal Tibetans at 3,658 m. J. Appl. Physiol. 1985, 74, 312–318. [Google Scholar]
- Beall, C.M.; Laskowski, D.; Strohl, K.P.; Soria, R.; Villena, M.; Vargas, E.; Alarcon, A.M.; Gonzales, C.; Erzurum, S.P. Pulmonary nitric oxide in mountain dwellers. Nature 2001, 414, 411–412. [Google Scholar] [CrossRef] [PubMed]
- Smith, A.T.; Foggin, J.M. The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau. Anim. Conserv. 1999, 2, 235–240. [Google Scholar] [CrossRef]
- Lai, C.H.; Smith, A.T. Keystone status of plateau pikas (Ochotona curzoniae): Effect of control on biodiversity of native birds. Biodivers. Conserv. 2003, 12, 1901–1912. [Google Scholar] [CrossRef]
- Yang, Y.Z.; Cao, Y.; Jin, G.E.; Bai, Z.Z.; Lan, M.L.; Yun, H.X.; Ge, R.L. Molecular cloning and characterization of hemoglobin α and β chains from plateau pika (Ochotona curzoniae) living at high altitude. Gene 2007, 403, 118–124. [Google Scholar]
- Wang, X.J.; Wei, D.B.; Wei, L.; Qi, X.Z.; Zhu, S.H. Characteristics of pulmonary acinus structure in the plateau zokor (Myospalax baileyi) and plateau pika (Ochotona curzoniae). J. Zool. 2008, 54, 531–539. [Google Scholar]
- Ge, R.L.; 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. Heart Circ. Physiol. 1998, 274, H1792–H1799. [Google Scholar]
- Wang, X.J.; Wei, D.B.; Wei, L.; Zhang, J.M.; Yu, H.Y. Physiological character of erythrocyte adapting to hypoxia in plateau zokor and plateau pika. Sichuan J. Zoo. 2008, 6, 38. (in Chinese). [Google Scholar]
- Ye, R.R.; Cao, Y.F.; Bai, Q.H. Blood indices of plateau pika and relationship with hypoxia adaptation. J. Zool. 1994, 2, 114–119. [Google Scholar]
- He, J.; Xu, C; Meng, X.; Li, H.; Wang, Y. Comparative analysis in transport and intake of oxygen between pikas (Ochotona curzoniae) and rats. J. Prevent Med. Chinese People's Liberation 1994, 12, 431–435. (in Chinese). [Google Scholar]
- Qi, X.Z.; Wang, X.J.; Zhu, S.H.; Rao, X.F.; Wei, L.; Wei, D.B. Hypoxic adaptation of the hearts of plateau zokor (Myospalax baileyi) and plateau pika (Ochotona curzoniae). J. Zool. 2008, 60, 348–354. [Google Scholar]
- Wei, D.B; Wei, L.; Zhang, J.M.; Yu, H.Y. Blood-gas properties of plateau zokor (Myospalax baileyi). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2006, 145, 372–375. [Google Scholar] [CrossRef] [PubMed]
- Zhu, S.H.; Qi, X.Z.; Wang, X.J.; Rao, X.F.; Wei, L.; Wei, D.B. Difference in oxygen uptake in skeletal muscles between plateau zokor (Myospalax rufescens baileyi) and plateau pika (Ochotona curzoniac). Acta Physiol. Sinica 2009, 61, 373–378. (in Chinese). [Google Scholar] [PubMed]
- Sun, S.Z.; Wei, L; Wei, D.B.; Wang, D.W.; Ma, B.Y. Differences of glycolysis in skeletal muscle and lactate metabolism in liver between plateau zokor (Myospalax baileyi) and plateau pika (Ochotona curzoniae). Acta Physiol. Sinica 2013, 65, 276–284. (in Chinese). [Google Scholar] [PubMed]
- Li, H.G.; Ren, Y.M.; Guo, S.C.; Cheng, L.; Wang, D.P.; Yang, J; Chang, Z.J.; Zhao, X.Q. The protein level of hypoxia-inducible factor-1α is increased in the plateau pika (Ochotona curzoniae) inhabiting high altitudes. J. Exp. Zool A Ecol. Genet. Physiol 2009, 311, 134–141. [Google Scholar] [CrossRef] [PubMed]
- Zhao, T.B.; Ning, H.X.; Zhu, S.S.; Sun, P.; Xu, S.X.; Chang, Z.J.; Zhao, X.Q. Cloning of hypoxia-inducible factor-1α cDNA from a high hypoxia tolerant mammal-plateau pika (Ochotona curzoniae). Biochem. Biophys. Res. Commun. 2004, 316, 565–572. [Google Scholar] [CrossRef] [PubMed]
- Li, H.G.; Guo, S.C.; Ren, Y.M.; Wang, D.P.; Yu, H.H.; Li, W.J.; Zhao, X.Q.; Chang, Z.J. VEGF189 expression is highly related to adaptation of the Plateau Pika (Ochotona curzoniae) Inhabiting High Altitudes. High. Alt. Med. Biol. 2013, 14, 395–404. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.N.; Zhu, R.J.; Wang, D.W.; Wei, L.; Wei, D.B. Gene coding and mRNA expression of vascular endothelial growth factor as well as microvessel density in brain of plateau zokor: comparison with other rodents. Acta Physiol. Sinica 2011, 63, 155–163. (in Chinese). [Google Scholar] [PubMed]
- Wang, D.W.; Wei, L.; Wei, D.B.; Rao, X.F.; Qi, X.Z.; Wang, X.J.; Ma, B.Y. Testis-specific lactate dehydrogenase is expressed in somatic tissues of plateau pikas. FEBS Open Bio 2013, 3, 118–123. [Google Scholar] [CrossRef] [PubMed]
- Luo, Y.J.; Gao, W.X.; Gao, Y.Q.; Tang, S.; Huang, Q.Y.; Tan, X.L.; Chen, J.; Huang, T.S. Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation. Mitochondrion 2008, 8, 352–357. [Google Scholar] [CrossRef] [PubMed]
- Pichon, A.; Zhenzhong, B.; Favret, F.; Jin, G.; Shufeng, H.; Marchant, D.; Richalet, J.P.; Ge, R.L. Long-term ventilatory adaptation and ventilatory response to hypoxia in plateau pika (Ochotona curzoniae): Role of nNOS and dopamine. Am. J. Physiol. Regul. Integr Comp. Physiol. 2009, 297, R978–R987. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Wang, Z.L.; Zhao, X.Q.; Xu, B.H.; Ren, Y.H.; Tian, H.F. Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress. PLoS ONE 2008, 3, e1472. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Zhao, X.Q.; Guo, S.C.; Li, H.G.; Qi, D.L.; Wang, D.P.; Cao, J.H. Leptin cDNA cloning and its mRNA expression in plateau pikas (Ochotona curzoniae) from different altitudes on Qinghai-Tibet Plateau. Biochem. Biophys. Res. Commun. 2006, 345, 1405–1413. [Google Scholar] [CrossRef] [PubMed]
- Everse, J.; Kaplan, N.O. Lactate dehydrogenases: Structure and function. Adv. Enzymol. Relat. Areas Mol. Biol. 1973, 37, 61–133. [Google Scholar] [PubMed]
- Li, S. Lactate dehydrogenase isoenzymes A (muscle), B (heart) and C (testis) of mammals and the genes coding for these enzymes. Biochem. Soc. Trans. 1989, 17, 304. [Google Scholar] [PubMed]
- Li, S.; O'brien, D.; Hou, E.; Versola, J.; Rockett, D.; Eddy, E. Differential activity and synthesis of lactate dehydrogenase isozymes A (muscle), B (heart), and C (testis) in mouse spermatogenic cells. Biol. Reprod. 1989, 40, 173–180. [Google Scholar] [CrossRef] [PubMed]
- Cahn, R.D.; Zwilling, E; Kaplan, N.O.; Levine, L. Nature and development of lactic dehydrogenases. Science 1962, 136, 962–969. [Google Scholar] [CrossRef] [PubMed]
- Fine, I.; Kaplan, N.; Kuftinec, D. Developmental changes of mammalian lactic dehydrogenases. Biochemistry 1963, 2, 116–121. [Google Scholar] [CrossRef]
- Goldberg, E. Reproductive implications of LDH-C4 and other testis-specific isozymes. Exp. Clin. Immunogenet. 1984, 2, 120–124. [Google Scholar]
- Coonrod, S.; Vitale, A.; Duan, C.; Bristol-Gould, S.; Herr, J.; Goldberg, E. Testis-Specific Lactate Dehydrogenase (LDH-C4; Ldh3) in Murine Oocytes and Preimplantation Embryos. J. Androl. 2006, 27, 502–509. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, E. Lactate dehydrogenase-X from mouse testes and spermatozoa. Methods Enzymol. 1975, 41, 318. [Google Scholar] [PubMed]
- Goldberg, E. Lactate dehydrogenases and malate dehydrogenases in sperm: studied by polyacrylamide gel electrophoresis. Ann. N. Y. Acad. Sci. 1964, 121, 560–570. [Google Scholar] [CrossRef] [PubMed]
- Odet, F.; Gabel, S.A.; Williams, J.; London, R.E.; Goldberg, E.; Eddy, E.M. Lactate dehydrogenase C and energy metabolism in mouse sperm. Biol. Reprod. 2011, 85, 556–564. [Google Scholar] [CrossRef] [PubMed]
- Coronel, C.E.; Burgos, C.; Gerez De Burgos, N.M.; Rovai, L.E.; Blanco, A. Catalytic properties of the sperm-specific lactate dehydrogenase (LDH X or C4) from different species. J. Exp. Zool. 1983, 225, 379–385. [Google Scholar] [CrossRef] [PubMed]
- Hawtrey, C.O.; Goldberg, E. Some kinetic aspects of sperm specific lactate dehydrogenase in mice. J. Exp. Zool. 1970, 174, 451–461. [Google Scholar] [CrossRef] [PubMed]
- Fleisher, G.; Kolb, E.; Larner, J. Isolation and characterization of bovine lactate dehydrogenase X. Biochemistry 1970, 9, 4372–4380. [Google Scholar] [CrossRef]
- Wong, C.; Rodrı́guez-Páez, L.; Nogueda, B.; Pérez, A.; Baeza, I. Selective inhibition of the sperm-specific lactate dehydrogenase isozyme-C4 by N-isopropyl oxamate. Biochim. Biophys. Acta. 1997, 1343, 16–22. [Google Scholar] [CrossRef]
- Rodríguez-Páez, L.; Chena-Taboada, M.A.; Cabrera-Hernández, A.; Cordero-Martínez, J.; Wong, C. Oxamic acid analogues as LDH-C4-specific competitive inhibitors. J. Enzyme Inhib Med. Chem. 2011, 26, 579–586. [Google Scholar] [CrossRef] [PubMed]
- Wong, C.; Yañez, R.; Brown, D.M.; Dickey, A.; Parks, M.E.; McKee, R.W. Isolation and properties of lactate dehydrogenase isozyme X from Swiss mice. Arch. Biochem. Biophys. 1971, 146, 454–460. [Google Scholar] [CrossRef]
- Allen, J.M. Multiple forms of lactic dehydrogenase in tissues of the mouse: their specificity, cellular localization, and response to altered physiological conditions. Ann. N. Y. Acad. Sci. 1961, 94, 937–951. [Google Scholar] [CrossRef] [PubMed]
- Zinkham, W.H.; Blanco, A.; Clowry, L.J. An unusual isozyme of lactate dehydrogenase in mature testes: localization, ontogeny, and kinetic properties. Ann. N. Y. Acad. Sci. 1964, 121, 571–588. [Google Scholar]
- Wilkinson, J.; Withycombe, W.A. Organ specificity and lactate-dehydrogenase activity. Some properties of human spermatozoal lactate dehydrogenase. Biochem. J. 1965, 97, 663–668. [Google Scholar] [PubMed]
- Blanco, A.; Zinkham, W.H.; Kupchyk, L. Genetic control and ontogeny of lactate dehydrogenase in pigeon testes. J. Exp. Zool. 1964, 156, 137–152. [Google Scholar] [CrossRef] [PubMed]
- Battellino, L.J.; Jaime, F.R.; Blanco, A. Kinetic properties of rabbit testicular lactate dehydrogenase isozyme. J. Biol. Chem. 1968, 243, 5185–5192. [Google Scholar] [PubMed]
- Schatz, L.; Segal, H.L. Reduction of α-ketoglutarate by homogeneous lactic dehydrogenase X of testicular tissue. J. Biol. Chem. 1969, 244, 4393–4397. [Google Scholar] [PubMed]
- Battellino, L.J.; Blanco, A. Catalytic properties of the lactate dehydrogenase isozyme “X” from mouse testis. J. Exp. Zool. 1970, 174, 173–186. [Google Scholar] [CrossRef] [PubMed]
- Blanco, A.; Burgos, C.; Gerez, B.N.M.; Montamat, E.E. Properties of the testicular lactate dehydrogenase isoenzyme. Biochem. J. 1976, 153, 165–172. [Google Scholar] [PubMed]
- Baker, B.R. Design of active-site-directed irreversible enzyme inhibitors; the organic chemistry of the enzymic active-site. Science 1968, 159, 1091. [Google Scholar]
- Elizondo, S.; Chena, M.A.; Rodríguez-Páez, L.; Nogueda, B.; Baeza, I.; Wong, C. Inhibition of Trypanosoma cruzi α-hydroxyacid dehydrogenase-isozyme II by N-isopropyl oxamate and its effect on intact epimastigotes. J. Enzyme Inhib. Med. Chem. 2003, 18, 265–271. [Google Scholar] [CrossRef] [PubMed]
- John, J.S. Determination of ATP in Chlorella with the luciferin-luciferase enzyme system. Anal. Biochem. 1970, 37, 409–416. [Google Scholar] [CrossRef]
- Blanco, A.; Zinkham, W.H. Lactate dehydrogenases in human testes. Science 1963, 139, 601–602. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, E. Lactic and malic dehydrogenases in human spermatozoa. Science 1963, 139, 602–603. [Google Scholar] [CrossRef] [PubMed]
- Clausen, J.; Ovlisen, B. Lactate dehydrogenase isoenzymes of human semen. Biochem. J. 1965, 97, 513–517. [Google Scholar] [PubMed]
- LeVan, K.M.; Goldberg, E. Properties of human testis-specific lactate dehydrogenase expressed from Escherichia coli. Biochem. J. 1991, 273, 587–592. [Google Scholar] [PubMed]
- Hereng, T.H.; Elgstøen, K.B.; Cederkvist, F.H.; Eide, L.; Jahnsen, T.; Skålhegg, B.S.; Rosendal, K.R. Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum. Reprod. 2011, 26, 3249–3263. [Google Scholar] [CrossRef] [PubMed]
- Odet, F.; Duan, C.; Willis, W.D.; Goulding, E.H.; Kung, A.; Eddy, E.M.; Goldberg, E. Expression of the gene for mouse lactate dehydrogenase C (Ldhc) is required for male fertility. Biol. Reprod. 2008, 79, 26–34. [Google Scholar] [CrossRef] [PubMed]
- Mukai, C.; Okuno, M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 2004, 71, 540–547. [Google Scholar] [CrossRef] [PubMed]
- Williams, A.C.; Ford, W.C.L. The role of glucose in supporting motility and capacitation in human spermatozoa. J. Androl. 2001, 22, 680–695. [Google Scholar] [PubMed]
- Belleau, B.; Lacasse, G. Aspects of the Chemical Mechanism of Complex Formation between Acetylcholinesterase and Acetylcholine-Related Compounds1a, b. J. Med. Chem. 1964, 7, 768–775. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, E. Amino acid composition and properties of crystalline lactate dehydrogenase X from mouse testes. J. Biol. Chem. 1972, 247, 2044–2048. [Google Scholar] [PubMed]
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Wang, Y.; Wei, L.; Wei, D.; Li, X.; Xu, L.; Wei, L. Testis-Specific Lactate Dehydrogenase (LDH-C4) in Skeletal Muscle Enhances Apika’s Sprint-Running Capacity in Hypoxic Environment. Int. J. Environ. Res. Public Health 2015, 12, 9218-9236. https://doi.org/10.3390/ijerph120809218
Wang Y, Wei L, Wei D, Li X, Xu L, Wei L. Testis-Specific Lactate Dehydrogenase (LDH-C4) in Skeletal Muscle Enhances Apika’s Sprint-Running Capacity in Hypoxic Environment. International Journal of Environmental Research and Public Health. 2015; 12(8):9218-9236. https://doi.org/10.3390/ijerph120809218
Chicago/Turabian StyleWang, Yang, Lian Wei, Dengbang Wei, Xiao Li, Lina Xu, and Linna Wei. 2015. "Testis-Specific Lactate Dehydrogenase (LDH-C4) in Skeletal Muscle Enhances Apika’s Sprint-Running Capacity in Hypoxic Environment" International Journal of Environmental Research and Public Health 12, no. 8: 9218-9236. https://doi.org/10.3390/ijerph120809218