Login Register Cart 0
Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Comparative Analysis of Skeleton Muscle Proteome Profile between Yak and Cattle Provides Insight into High-Altitude Adaptation

Author(s): Jin-Wei Xin, Zhi-Xin Chai, Cheng-Fu Zhang, Yu-Mei Yang, Qiang Zhang, Yong Zhu, Han-Wen Cao, Cidan YangJi, Jin-Cheng Zhong and Qiu-Mei Ji *

Volume 18, Issue 1, 2021

Published on: 27 January, 2020

Page: [62 - 70] Pages: 9

DOI: 10.2174/1570164617666200127151931

Price: $65

Abstract

Background: Mechanisms underlying yak adaptation to high-altitude environments have been investigated at the levels of morphology, anatomy, physiology, genome and transcriptome, but have not been explored at the proteome level.

Objective: The protein profiles were compared between yak and cattle to explore molecular mechanisms underlying yak adaptation to high altitude conditions.

Methods: In the present study, an antibody microarray chip was developed, which included 6,500 mouse monoclonal antibodies. Immunoprecipitation and mass spectrometry were performed on 12 selected antibodies which showed that the chip was highly specific. Using this chip, muscle tissue proteome was compared between yak and cattle, and 12 significantly Differentially Expressed Proteins (DEPs) between yak and cattle were identified. Their expression levels were validated using Western blot.

Results: Compared with cattle, higher levels of Rieske Iron-Sulfur Protein (RISP), Cytochrome C oxidase subunit 4 isoform 1, mitochondrial (COX4I1), ATP synthase F1 subunit beta (ATP5F1B), Sarcoplasmic/ Endoplasmic Reticulum Calcium ATPase1 (SERCA1) and Adenosine Monophosphate Deaminase1 (AMPD1) in yak might improve oxygen utilization and energy metabolism. Pyruvate Dehydrogenase protein X component (PDHX) and Acetyltransferase component of pyruvate dehydrogenase complex (DLAT) showed higher expression levels and L-lactate dehydrogenase A chain (LDHA) showed lower expression level in yak, which might help yak reduce the accumulation of lactic acid. In addition, higher expression levels of Filamin C (FLNC) and low levels of AHNAK and Four and a half LIM domains 1 (FHL1) in yak might reduce the risks of pulmonary arteries vasoconstriction, remodeling and hypertension.

Conclusion: Overall, the present study reported the differences in protein profile between yak and cattle, which might be helpful to further understand molecular mechanisms underlying yak adaptation to high altitude environments.

Keywords: High altitude, proteomics, antibody microarray, energy metabolism, thermogenesis, yak.

« Previous Next »
Graphical Abstract

[1]
Wiener , G; Jianlin, H; Ruijun, L The Yakthe Regional Office for Asia and the Pacific Food and Agriculture Organization of the United Nations 2003.
[2]
Rendt, L. Wildlife of the Tibetan Steppes 2000.
[http://dx.doi.org/10.1093/jmammal/81.3.908]
[3]
Ishizaki, T.; Koizumi, T.; Ruan, Z.; Wang, Z.; Chen, Q.; Sakai, A. Nitric oxide inhibitor altitude-dependently elevates pulmonary arterial pressure in high-altitude adapted yaks. Respir. Physiol. Neurobiol., 2005, 146(2-3), 225-230.
[http://dx.doi.org/10.1016/j.resp.2004.12.002] [PMID: 15766910]
[4]
Durmowicz, A.G.; Hofmeister, S.; Kadyraliev, T.K.; Aldashev, A.A.; Stenmark, K.R. Functional and structural adaptation of the yak pulmonary circulation to residence at high altitude. J. Appl. Physiol., 1993, 74(5), 2276-2285.
[http://dx.doi.org/10.1152/jappl.1993.74.5.2276] [PMID: 8335557]
[5]
Qiu, Q.; Zhang, G.; Ma, T.; Qian, W.; Wang, J.; Ye, Z.; Cao, C.; Hu, Q.; Kim, J.; Larkin, D.M.; Auvil, L.; Capitanu, B.; Ma, J.; Lewin, H.A.; Qian, X.; Lang, Y.; Zhou, R.; Wang, L.; Wang, K.; Xia, J.; Liao, S.; Pan, S.; Lu, X.; Hou, H.; Wang, Y.; Zang, X.; Yin, Y.; Ma, H.; Zhang, J.; Wang, Z.; Zhang, Y.; Zhang, D.; Yonezawa, T.; Hasegawa, M.; Zhong, Y.; Liu, W.; Zhang, Y.; Huang, Z.; Zhang, S.; Long, R.; Yang, H.; Wang, J.; Lenstra, J.A.; Cooper, D.N.; Wu, Y.; Wang, J.; Shi, P.; Wang, J.; Liu, J. The yak genome and adaptation to life at high altitude. Nat. Genet., 2012, 44(8), 946-949.
[http://dx.doi.org/10.1038/ng.2343] [PMID: 22751099]
[6]
Lan, D.; Xiong, X.; Ji, W.; Li, J.; Mipam, T.D.; Ai, Y.; Chai, Z. Transcriptome profile and unique genetic evolution of positively selected genes in yak lungs. Genetica, 2018, 146(2), 151-160.
[http://dx.doi.org/10.1007/s10709-017-0005-8] [PMID: 29285685]
[7]
Wang, K.; Yang, Y.; Wang, L.; Ma, T.; Shang, H.; Ding, L.; Han, J.; Qiu, Q. Different gene expressions between cattle and yak provide insights into high-altitude adaptation. Anim. Genet., 2016, 47(1), 28-35.
[http://dx.doi.org/10.1111/age.12377] [PMID: 26538003]
[8]
Guan, J.; Long, K.; Ma, J.; Zhang, J.; He, D.; Jin, L.; Tang, Q.; Jiang, A.; Wang, X.; Hu, Y.; Tian, S.; Jiang, Z.; Li, M.; Luo, X. Comparative analysis of the microRNA transcriptome between yak and cattle provides insight into high-altitude adaptation. PeerJ, 2017, 5e3959
[http://dx.doi.org/10.7717/peerj.3959] [PMID: 29109913]
[9]
Poverennaya, E.V.; Ilgisonis, E.V.; Ponomarenko, E.A.; Kopylov, A.T.; Zgoda, V.G.; Radko, S.P.; Lisitsa, A.V.; Archakov, A.I. Why are the correlations between mRNA and protein levels so low among the 275 predicted protein-coding genes on human chromosome 18. J. Proteome Res., 2017, 16(12), 4311-4318.
[http://dx.doi.org/10.1021/acs.jproteome.7b00348] [PMID: 28956606]
[10]
Ahmad, Y.; Sharma, N.K.; Ahmad, M.F.; Sharma, M.; Garg, I.; Bhargava, K. Proteomic identification of novel differentiation plasma protein markers in hypobaric hypoxia-induced rat model. PLoS One, 2014, 9(5)e98027
[http://dx.doi.org/10.1371/journal.pone.0098027] [PMID: 24842778]
[11]
Hernández, R.; Blanco, S.; Peragón, J.; Pedrosa, J.A.; Peinado, M.A. Hypobaric hypoxia and reoxygenation induce proteomic profile changes in the rat brain cortex. Neuromolecular Med., 2013, 15(1), 82-94.
[http://dx.doi.org/10.1007/s12017-012-8197-7] [PMID: 22961459]
[12]
Du, X.; Zhang, R.; Ye, S.; Liu, F.; Jiang, P.; Yu, X.; Xu, J.; Ma, L.; Cao, H.; Shen, Y.; Lin, F.; Wang, Z.; Li, C. Alterations of human plasma proteome profile on adaptation to high-altitude hypobaric hypoxia. J. Proteome Res., 2019, 18(5), 2021-2031.
[http://dx.doi.org/10.1021/acs.jproteome.8b00911] [PMID: 30908922]
[13]
Borrebaeck, C.A.; Wingren, C. High-throughput proteomics using antibody microarrays: an update. Expert Rev. Mol. Diagn., 2007, 7(5), 673-686.
[http://dx.doi.org/10.1586/14737159.7.5.673] [PMID: 17892372]
[14]
Kaplan, R.S.; Pedersen, P.L. Determination of microgram quantities of protein in the presence of milligram levels of lipid with amido black 10B. Anal. Biochem., 1985, 150(1), 97-104.
[http://dx.doi.org/10.1016/0003-2697(85)90445-2] [PMID: 4083487]
[15]
Wettenhall, J.M.; Smyth, G.K. limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics, 2004, 20(18), 3705-3706.
[http://dx.doi.org/10.1093/bioinformatics/bth449] [PMID: 15297296]
[16]
Marcon, E.; Jain, H.; Bhattacharya, A.; Guo, H.; Phanse, S.; Pu, S.; Byram, G.; Collins, B.C.; Dowdell, E.; Fenner, M.; Guo, X.; Hutchinson, A.; Kennedy, J.J.; Krastins, B.; Larsen, B.; Lin, Z.Y.; Lopez, M.F.; Loppnau, P.; Miersch, S.; Nguyen, T.; Olsen, J.B.; Paduch, M.; Ravichandran, M.; Seitova, A.; Vadali, G.; Vogelsang, M.S.; Whiteaker, J.R.; Zhong, G.; Zhong, N.; Zhao, L.; Aebersold, R.; Arrowsmith, C.H.; Emili, A.; Frappier, L.; Gingras, A.C.; Gstaiger, M.; Paulovich, A.G.; Koide, S.; Kossiakoff, A.A.; Sidhu, S.S.; Wodak, S.J.; Gräslund, S.; Greenblatt, J.F.; Edwards, A.M. Assessment of a method to characterize antibody selectivity and specificity for use in immunoprecipitation. Nat. Methods, 2015, 12(8), 725-731.
[http://dx.doi.org/10.1038/nmeth.3472] [PMID: 26121405]
[17]
Zhang, Y.; Xu, Y.; Arellano, S.M.; Xiao, K.; Qian, P.Y. Comparative proteome and phosphoproteome analyses during cyprid development of the barnacle Balanus (Amphibalanus) amphitrite. J. Proteome Res., 2010, 9(6), 3146-3157.
[http://dx.doi.org/10.1021/pr1000384] [PMID: 20397722]
[18]
Xia, D.; Esser, L.; Yu, L.; Yu, C.A. Structural basis for the mechanism of electron bifurcation at the quinol oxidation site of the cytochrome bc1 complex. Photosynth. Res., 2007, 92(1), 17-34.
[http://dx.doi.org/10.1007/s11120-007-9155-3] [PMID: 17457691]
[19]
Babcock, G.T.; Wikström, M. Oxygen activation and the conservation of energy in cell respiration. Nature, 1992, 356(6367), 301-309.
[http://dx.doi.org/10.1038/356301a0] [PMID: 1312679]
[20]
Napiwotzki, J.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kadenbach, B. ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem., 1997, 378(9), 1013-1021.
[http://dx.doi.org/10.1515/bchm.1997.378.9.1013] [PMID: 9348111]
[21]
Arnold, S.; Kadenbach, B. The intramitochondrial ATP/ADP-ratio controls cytochrome C oxidase activity allosterically. FEBS Lett., 1999, 443(2), 105-108.
[http://dx.doi.org/10.1016/S0014-5793(98)01694-9 ] [PMID: 9989584]
[22]
Abrahams, J.P.; Leslie, A.G.; Lutter, R.; Walker, J.E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature, 1994, 370(6491), 621-628.
[http://dx.doi.org/10.1038/370621a0] [PMID: 8065448]
[23]
Futai, M.; Noumi, T.; Maeda, M. ATP synthase (H+-ATPase): Results by combined biochemical and molecular biological approaches. Annu. Rev. Biochem., 1989, 58, 111-136.
[http://dx.doi.org/10.1146/annurev.bi.58.070189.000551 ] [PMID: 2528322]
[24]
Lai-Zhang, J.; Mueller, D.M. Complementation of deletion mutants in the genes encoding the F1-ATPase by expression of the corresponding bovine subunits in yeast S. cerevisiae. Eur. J. Biochem., 2000, 267(8), 2409-2418.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01253.x ] [PMID: 10759867]
[25]
Patel, M.S.; Roche, T.E. Molecular biology and biochemistry of pyruvate dehydrogenase complexes. FASEB J., 1990, 4(14), 3224-3233.
[http://dx.doi.org/10.1096/fasebj.4.14.2227213] [PMID: 2227213]
[26]
Neagle, J.; De Marcucci, O.; Dunbar, B.; Lindsay, J.G. Component X of mammalian pyruvate dehydrogenase complex: Structural and functional relationship to the lipoate acetyltransferase (E2) component. FEBS Lett., 1989, 253(1-2), 11-15.
[http://dx.doi.org/10.1016/0014-5793(89)80919-6 ] [PMID: 2759236]
[27]
Rahmatullah, M.; Gopalakrishnan, S.; Radke, G.A.; Roche, T.E. Domain structures of the dihydrolipoyl transacetylase and the protein X components of mammalian pyruvate dehydrogenase complex. Selective cleavage by protease Arg C. J. Biol. Chem., 1989, 264(2), 1245-1251.
[PMID: 2642901]
[28]
Everse, J.; Kaplan, N.O. Lactate dehydrogenases: Structure and function. Adv. Enzymol. Relat. Areas Mol. Biol., 1973, 37, 61-133.
[PMID: 4144036]
[29]
Goebel, H.H.; Bardosi, A. Myoadenylate deaminase deficiency. Klin. Wochenschr., 1987, 65(21), 1023-1033.
[http://dx.doi.org/10.1007/BF01726321] [PMID: 3323644]
[30]
Matherne, G.P.; Headrick, J.P.; Berr, S.; Berne, R.M. Metabolic and functional responses of immature and mature rabbit hearts to hypoperfusion, ischemia, and reperfusion. Am. J. Physiol., 1993, 264(6 Pt 2), H2141-H2153.
[PMID: 8322945]
[31]
Marquetant, R.; Desai, N.M.; Sabina, R.L.; Holmes, E.W. Evidence for sequential expression of multiple AMP deaminase isoforms during skeletal muscle development. Proc. Natl. Acad. Sci. USA, 1987, 84(8), 2345-2349.
[http://dx.doi.org/10.1073/pnas.84.8.2345] [PMID: 3470799]
[32]
Dumonteil, E.; Barré, H.; Meissner, G. Sarcoplasmic reticulum Ca(2+)-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis. Am. J. Physiol., 1993, 265(2 Pt 1), C507-C513.
[http://dx.doi.org/10.1152/ajpcell.1993.265.2.C507] [PMID: 8018125]
[33]
Olesen, C.; Picard, M.; Winther, A.M.; Gyrup, C.; Morth, J.P.; Oxvig, C.; Møller, J.V.; Nissen, P. The structural basis of calcium transport by the calcium pump. Nature, 2007, 450(7172), 1036-1042.
[http://dx.doi.org/10.1038/nature06418] [PMID: 18075584]
[34]
Sørensen, T.L.; Møller, J.V.; Nissen, P. Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science, 2004, 304(5677), 1672-1675.
[http://dx.doi.org/10.1126/science.1099366] [PMID: 15192230]
[35]
Toyoshima, C. Structural aspects of ion pumping by Ca2+-ATPase of sarcoplasmic reticulum. Arch. Biochem. Biophys., 2008, 476(1), 3-11.
[http://dx.doi.org/10.1016/j.abb.2008.04.017] [PMID: 18455499]
[36]
Sacchetto, R.; Bertipaglia, I.; Giannetti, S.; Cendron, L.; Mascarello, F.; Damiani, E.; Carafoli, E.; Zanotti, G. Crystal structure of sarcoplasmic reticulum Ca2+-ATPase (SERCA) from bovine muscle. J. Struct. Biol., 2012, 178(1), 38-44.
[http://dx.doi.org/10.1016/j.jsb.2012.02.008] [PMID: 22387132]
[37]
Lytton, J.; Westlin, M.; Burk, S.E.; Shull, G.E.; MacLennan, D.H. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem., 1992, 267(20), 14483-14489.
[PMID: 1385815]
[38]
Arruda, A.P.; Da-Silva, W.S.; Carvalho, D.P.; De Meis, L. Hyperthyroidism increases the uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2+-ATPase. Biochem. J., 2003, 375(Pt 3), 753-760.
[http://dx.doi.org/10.1042/bj20031015] [PMID: 12887329]
[39]
de Meis, L. Uncoupled ATPase activity and heat production by the sarcoplasmic reticulum Ca2+-ATPase. Regulation by ADP. J. Biol. Chem., 2001, 276(27), 25078-25087.
[http://dx.doi.org/10.1074/jbc.M103318200] [PMID: 11342561]
[40]
Reis, M.; Farage, M.; de Meis, L. Thermogenesis and energy expenditure: control of heat production by the Ca(2+)-ATPase of fast and slow muscle. Mol. Membr. Biol., 2002, 19(4), 301-310.
[http://dx.doi.org/10.1080/09687680210166217 ] [PMID: 12512777]
[41]
Stossel, T.P.; Condeelis, J.; Cooley, L.; Hartwig, J.H.; Noegel, A.; Schleicher, M.; Shapiro, S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol., 2001, 2(2), 138-145.
[http://dx.doi.org/10.1038/35052082] [PMID: 11252955]
[42]
Zhou, A.X.; Hartwig, J.H.; Akyürek, L.M. Filamins in cell signaling, transcription and organ development. Trends Cell Biol., 2010, 20(2), 113-123.
[http://dx.doi.org/10.1016/j.tcb.2009.12.001] [PMID: 20061151]
[43]
Neethling, A.; Mouton, J.; Loos, B.; Corfield, V.; de Villiers, C.; Kinnear, C. Filamin C: a novel component of the KCNE2 interactome during hypoxia. Cardiovasc. J. Afr., 2016, 27(1), 4-11.
[http://dx.doi.org/10.5830/CVJA-2015-049] [PMID: 26956495]
[44]
Boraldi, F.; Annovi, G.; Carraro, F.; Naldini, A.; Tiozzo, R.; Sommer, P.; Quaglino, D. Hypoxia influences the cellular cross-talk of human dermal fibroblasts. A proteomic approach. Biochim. Biophys. Acta, 2007, 1774(11), 1402-1413.
[http://dx.doi.org/10.1016/j.bbapap.2007.08.011 ] [PMID: 17904921]
[45]
Hohaus, A.; Person, V.; Behlke, J.; Schaper, J.; Morano, I.; Haase, H. The carboxyl-terminal region of ahnak provides a link between cardiac L-type Ca2+ channels and the actin-based cytoskeleton. FASEB J., 2002, 16(10), 1205-1216.
[http://dx.doi.org/10.1096/fj.01-0855com] [PMID: 12153988]
[46]
Okagaki, T.; Weber, F.E.; Fischman, D.A.T.; Vaughan, K.T.; Mikawa, T.; Reinach, F.C. The major myosin-binding domain of skeletal muscle MyBP-C (C protein) resides in the COOH-terminal, immunoglobulin C2 motif. J. Cell Biol., 1993, 123(3), 619-626.
[http://dx.doi.org/10.1083/jcb.123.3.619] [PMID: 8227129]
[47]
Weber, F.E.; Vaughan, K.T.; Reinach, F.C.; Fischman, D.A. Complete sequence of human fast-type and slow-type muscle myosin-binding-protein C (MyBP-C). Differential expression, conserved domain structure and chromosome assignment. Eur. J. Biochem., 1993, 216(2), 661-669.
[http://dx.doi.org/10.1111/j.1432-1033.1993.tb18186.x ] [PMID: 8375400]
[48]
James, J.; Robbins, J. Signaling and myosin-binding protein C. J. Biol. Chem., 2011, 286(12), 9913-9919.
[http://dx.doi.org/10.1074/jbc.R110.171801] [PMID: 21257752]
[49]
Harris, S.P.; Rostkova, E.; Gautel, M.; Moss, R.L. Binding of myosin binding protein-C to myosin subfragment S2 affects contractility independent of a tether mechanism. Circ. Res., 2004, 95(9), 930-936.
[http://dx.doi.org/10.1161/01.RES.0000147312.02673.56 ] [PMID: 15472117]
[50]
Herron, T.J.; Rostkova, E.; Kunst, G.; Chaturvedi, R.; Gautel, M.; Kentish, J.C. Activation of myocardial contraction by the N-terminal domains of myosin binding protein-C. Circ. Res., 2006, 98(10), 1290-1298.
[http://dx.doi.org/10.1161/01.RES.0000222059.54917.ef ] [PMID: 16614305]
[51]
Sadayappan, S.; de Tombe, P.P. Cardiac myosin binding protein-C: redefining its structure and function. Biophys. Rev., 2012, 4(2), 93-106.
[http://dx.doi.org/10.1007/s12551-012-0067-x] [PMID: 22707987]
[52]
van Dijk, S.J.; Bezold, K.L.; Harris, S.P. Earning stripes: myosin binding protein-C interactions with actin. Pflugers Arch., 2014, 466(3), 445-450.
[http://dx.doi.org/10.1007/s00424-013-1432-8] [PMID: 24442149]
[53]
Chen , Z; Zhao, T.J; Li, J.; Gao, Y.S; Meng, F.G. ; Yan, Y.B; Zhou, H.M. Slow skeletal Muscle myosin-Binding Protein-C (MyBPC1) mediates recruitment of muscle-type Creatine Kinase (CK) to myosin. Biochem. J., 2011, 436(2), 437-445.
[http://dx.doi.org/10.1042/BJ20102007] [PMID: 21426302]

Rights & Permissions Print Cite
Article Metrics
17
© 2024 Bentham Science Publishers | Privacy Policy