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Xiu-Juan Li, Cong-Cong Qiao, Bo-Jian Chen, Meng-Yang Li, Peng Chen, Mao-Lin Huang, Chun-Xiao Chen, Yan Liu, Han Cheng, Meng-Wan Jiang, Lu-Ye Shi, Zhen-Long Wang. Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia. Zoological Research, 2022, 43(4): 497-513. doi: 10.24272/j.issn.2095-8137.2022.011
Citation: Xiu-Juan Li, Cong-Cong Qiao, Bo-Jian Chen, Meng-Yang Li, Peng Chen, Mao-Lin Huang, Chun-Xiao Chen, Yan Liu, Han Cheng, Meng-Wan Jiang, Lu-Ye Shi, Zhen-Long Wang. Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia. Zoological Research, 2022, 43(4): 497-513. doi: 10.24272/j.issn.2095-8137.2022.011

Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia

doi: 10.24272/j.issn.2095-8137.2022.011
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (U2004152), Zhongyuan Science and Technology Innovation Leading Talent Project (224200510001), and China Postdoctoral Science Foundation (2020M672264)
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  • Corresponding author: E-mail: sly@zzu.edu.cnwzl@zzu.edu.cn
  • Received Date: 2022-03-07
  • Accepted Date: 2022-05-05
  • Published Online: 2022-05-11
  • Oxygen is essential for most life forms. Insufficient oxygen supply can disrupt homeostasis and compromise survival, and hypoxia-induced cardiovascular failure is fatal in many animals, including humans. However, certain species have adapted and evolved to cope with hypoxic environments and are therefore good models for studying the regulatory mechanisms underlying responses to hypoxia. Here, we explored the physiological and molecular responses of the cardiovascular system in two closely related hypoxia-adapted species with different life histories, namely, Qinghai voles (Neodon fuscus) and Brandt’s voles (Lasiopodomys brandtii), under hypoxic (10% O2 for 48 h) and normoxic (20.9% O2 for 48 h) exposure. Kunming mice (Mus musculus) were used for comparison. Qinghai voles live in plateau areas under hypoxic conditions, whereas Brandt’s voles only experience periodic hypoxia. Histological and hematological analyses indicated a strong tolerance to hypoxia in both species, but significant cardiac tissue damage and increased blood circulation resistance in mice exposed to hypoxia. Comparative transcriptome analysis revealed enhanced oxygen transport efficiency as a coping mechanism against hypoxia in both N. fuscus and L. brandtii, but with some differences. Specifically, N. fuscus showed up-regulated expression of genes related to accelerated cardiac contraction and angiogenesis, whereas L. brandtii showed significant up-regulation of erythropoiesis-related genes. Synchronized up-regulation of hemoglobin synthesis-related genes was observed in both species. In addition, differences in cardiometabolic strategies against hypoxia were observed in the rodents. Notably, M. musculus relied on adenosine triphosphate (ATP) generation via fatty acid oxidation, whereas N. fuscus shifted energy production to glucose oxidation under hypoxic conditions and L. brandtii employed a conservative strategy involving down-regulation of fatty acid and glucose oxidation and a bradycardia phenotype. In conclusion, the cardiovascular systems of N. fuscus and L. brandtii have evolved different adaptation strategies to enhance oxygen transport capacity and conserve energy under hypoxia. Our findings suggest that the coping mechanisms underlying hypoxia tolerance in these closely related species are context dependent.
  • #Authors contributed equally to this work
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  • [1]
    Abdurrachim D, Luiken JJFP, Nicolay K, Glatz JFC, Prompers JJ, Nabben M. 2015. Good and bad consequences of altered fatty acid metabolism in heart failure: evidence from mouse models. Cardiovascular Research, 106(2): 194−205. doi: 10.1093/cvr/cvv105
    [2]
    Abu-Farha M, Niles J, Willmore WG. 2005. Erythroid-specific 5-aminolevulinate synthase protein is stabilized by low oxygen and proteasomal inhibition. Biochemistry and Cell Biology, 83(5): 620−630. doi: 10.1139/o05-045
    [3]
    Arakawa T, Kobayashi-Yurugi T, Alguel Y, Iwanari H, Hatae H, Iwata M, et al. 2015. Crystal structure of the anion exchanger domain of human erythrocyte band 3. Science, 350(6261): 680−684. doi: 10.1126/science.aaa4335
    [4]
    Arieli R, Heth G, Nevo E, Zamir Y, Neutra O. 1986. Adaptive heart and breathing frequencies in 4 ecologically differentiating chromosomal species of mole rats in Israel. Experientia, 42(2): 131−133. doi: 10.1007/BF01952430
    [5]
    Bai J, Liu CB, Zhu PJ, Li Y. 2021. Novel insights into molecular mechanism of mitochondria in diabetic cardiomyopathy. Frontiers in Physiology, 11: 609157. doi: 10.3389/fphys.2020.609157
    [6]
    Barnett JM, McCollum GW, Penn JS. 2010. Role of cytosolic phospholipase A2 in retinal neovascularization. Investigative Ophthalmology & Visual Science, 51(2): 1136−1142.
    [7]
    Batista DS, Koehler AD, Romanel E, de Souza VC, Silva TD, Almeida MC, et al. 2019. De novo assembly and transcriptome of Pfaffia glomerata uncovers the role of photoautotrophy and the P450 family genes in 20-hydroxyecdysone production. Protoplasma, 256(3): 601−614. doi: 10.1007/s00709-018-1322-1
    [8]
    Bildyug N. 2019. Extracellular matrix in regulation of contractile system in cardiomyocytes. International Journal of Molecular Sciences, 20(20): 5054. doi: 10.3390/ijms20205054
    [9]
    Boosani CS, Sudhakar YA. 2011. Proteolytically derived endogenous angioinhibitors originating from the extracellular matrix. Pharmaceuticals, 4(12): 1551−1577. doi: 10.3390/ph4121551
    [10]
    Brennan CM, Mazzucca NQ, Mezoian T, Hunt TM, Keane ML, Leonard JN, et al. 2014. Reduced heme levels underlie the exponential growth defect of the Shewanella oneidensis hfq mutant. PLoS One, 9(10): e109879. doi: 10.1371/journal.pone.0109879
    [11]
    Brown N, Alkhayer K, Clements R, Singhal N, Gregory R, Azzam S, et al. 2016. Neuronal hemoglobin expression and its relevance to multiple sclerosis neuropathology. Journal of Molecular Neuroscience, 59(1): 1−17. doi: 10.1007/s12031-015-0711-6
    [12]
    Chen KY, Liu XJ, Bu PC, Lin CS, Rakhilin N, Locasale JW, et al. 2014. A metabolic signature of colon cancer initiating cells. In: Proceedings of 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Chicago: IEEE, 4759–4762.
    [13]
    Chen MC, Chang JP, Lin YS, Pan KL, Ho WC, Liu WH, et al. 2016. Deciphering the gene expression profile of peroxisome proliferator-activated receptor signaling pathway in the left atria of patients with mitral regurgitation. Journal of Translational Medicine, 14(1): 157. doi: 10.1186/s12967-016-0871-3
    [14]
    Chen SF, Zhou YQ, Chen YR, Gu J. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884−i890. doi: 10.1093/bioinformatics/bty560
    [15]
    Chen X, Zhang LB, Wang C. 2019. Prenatal hypoxia-induced epigenomic and transcriptomic reprogramming in rat fetal and adult offspring hearts. Scientific Data, 6(1): 238. doi: 10.1038/s41597-019-0253-9
    [16]
    Cheng Q, Huang CH, Cao H, Lin JL, Gong X, Li J, et al. 2019. A novel prognostic signature of transcription factors for the prediction in patients with GBM. Frontiers in Genetics, 10: 906. doi: 10.3389/fgene.2019.00906
    [17]
    Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18): 3674−3676. doi: 10.1093/bioinformatics/bti610
    [18]
    Cox B, Tsamou M, Vrijens K, Neven KY, Winckelmans E, de Kok TM, et al. 2019. A Co-expression analysis of the placental transcriptome in association with maternal pre-pregnancy BMI and newborn birth weight. Frontiers in Genetics, 10: 354. doi: 10.3389/fgene.2019.00354
    [19]
    Davidson NM, Oshlack A. 2014. Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biology, 15(7): 410.
    [20]
    Diessler S, Jan M, Emmenegger Y, Guex N, Middleton B, Skene DJ, et al. 2018. A systems genetics resource and analysis of sleep regulation in the mouse. PLoS Biology, 16(8): e2005750. doi: 10.1371/journal.pbio.2005750
    [21]
    Dong QQ, Shi LY, Li YW, Jiang MW, Sun H, Wang BS, et al. 2018. Differential responses of Lasiopodomys mandarinus and Lasiopodomys brandtii to chronic hypoxia: a cross-species brain transcriptome analysis. BMC Genomics, 19(1): 901. doi: 10.1186/s12864-018-5318-1
    [22]
    Duan MQ, Wang ZM, Guo XY, Wang KJ, Liu SY, Zhang B, et al. 2021. Integrated analysis of transcriptomic and proteomic analyses reveals different metabolic patterns in the livers of Tibetan and Yorkshire pigs. Animal Bioscience, 34(5): 922−930. doi: 10.5713/ajas.20.0342
    [23]
    Fan TJ, Sun GH, Sun XD, Zhao LJ, Zhong RG, Peng YZ. 2019. Tumor energy metabolism and potential of 3-bromopyruvate as an inhibitor of aerobic glycolysis: implications in tumor treatment. Cancers, 11(3): 317. doi: 10.3390/cancers11030317
    [24]
    Frade AF, Teixeira PC, Ianni BM, Pissetti CW, Saba B, Wang LHT, et al. 2013. Polymorphism in the alpha cardiac muscle actin 1 gene is associated to susceptibility to chronic inflammatory cardiomyopathy. PLoS One, 8(12): e83446. doi: 10.1371/journal.pone.0083446
    [25]
    Froese A, Breher SS, Waldeyer C, Schindler RFR, Nikolaev VO, Rinné S, et al. 2012. Popeye domain containing proteins are essential for stress-mediated modulation of cardiac pacemaking in mice. The Journal of Clinical Investigation, 122(3): 1119−1130. doi: 10.1172/JCI59410
    [26]
    Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7): 644−652. doi: 10.1038/nbt.1883
    [27]
    Grimes KM, Voorhees A, Chiao YA, Han HC, Lindsey ML, Buffenstein R. 2014. Cardiac function of the naked mole-rat: ecophysiological responses to working underground. American Journal of Physiology Heart and Circulatory Physiology, 306(5): H730−H737. doi: 10.1152/ajpheart.00831.2013
    [28]
    Grimes KM, Barefield DY, Kumar M, McNamara JW, Weintraub ST, de Tombe PP, et al. 2017. The naked mole-rat exhibits an unusual cardiac myofilament protein profile providing new insights into heart function of this naturally subterranean rodent. Pflügers Archiv-European Journal of Physiology, 469(12): 1603−1613.
    [29]
    Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8(8): 1494−1512. doi: 10.1038/nprot.2013.084
    [30]
    He JZ, Xiu MH, Tang XL, Yue F, Wang NB, Yang SB, et al. 2013. The different mechanisms of hypoxic acclimatization and adaptation in Lizard Phrynocephalus vlangalii living on Qinghai-Tibet Plateau. Journal of Experimental Zoology Part A:Ecological Genetics and Physiology, 319(3): 117−123. doi: 10.1002/jez.1776
    [31]
    He M, Cheng Y, Li W, Liu QS, Liu JX, Huang JH, et al. 2010. Vascular endothelial growth factor C promotes cervical cancer metastasis via up-regulation and activation of RhoA/ROCK-2/moesin cascade. BMC Cancer, 10: 170. doi: 10.1186/1471-2407-10-170
    [32]
    Hermes-Lima M, Zenteno-Savı́n T. 2002. Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 133(4): 537−556.
    [33]
    Hochachka PW, Clark CM, Holden JE, Stanley C, Ugurbil K, Menon RS. 1996. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proceedings of the National Academy of Sciences of the United States of America, 93(3): 1215−1220. doi: 10.1073/pnas.93.3.1215
    [34]
    Hofer T, Wenger RH, Kramer MF, Ferreira GC, Gassmann M. 2003. Hypoxic up-regulation of erythroid 5-aminolevulinate synthase. Blood, 101(1): 348−350. doi: 10.1182/blood-2002-03-0773
    [35]
    Hsiao YT, Shimizu I, Wakasugi T, Yoshida Y, Ikegami R, Hayashi Y, et al. 2021. Cardiac mitofusin-1 is reduced in non-responding patients with idiopathic dilated cardiomyopathy. Scientific Reports, 11(1): 6722. doi: 10.1038/s41598-021-86209-y
    [36]
    Huang H, Xie SW, Gu XL, Xiang B, Zhong ZF, Huang P, et al. 2021. Higher circulating miR-199a-5p indicates poor aerobic exercise capacity and associates with cardiovascular dysfunction during chronic exposure to high altitude. Frontiers in Physiology, 12: 587241. doi: 10.3389/fphys.2021.587241
    [37]
    Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. 2017. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Molecular Biology and Evolution, 34(8): 2115−2122. doi: 10.1093/molbev/msx148
    [38]
    Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. 2019. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47(D1): D309−D314. doi: 10.1093/nar/gky1085
    [39]
    Iacobas DA, Fan CH, Iacobas S. 2008. Integrated transcriptomic response to cardiac chronic hypoxia: translation regulators and response to stress in cell survival. Functional & Integrative Genomics, 8(3): 265−275.
    [40]
    Ilkovski B, Clement S, Sewry C, North KN, Cooper ST. 2005. Defining α-skeletal and α-cardiac actin expression in human heart and skeletal muscle explains the absence of cardiac involvement in ACTA1 nemaline myopathy. Neuromuscular Disorders, 15(12): 829−835. doi: 10.1016/j.nmd.2005.08.004
    [41]
    Ivy CM, Sprenger RJ, Bennett NC, van Jaarsveld B, Hart DW, Kirby AM, et al. 2020. The hypoxia tolerance of eight related African mole-rat species rivals that of naked mole-rats, despite divergent ventilatory and metabolic strategies in severe hypoxia. Acta Physiologica, 228(4): e13436.
    [42]
    Jeckel KM, Bouma GJ, Hess AM, Petrilli EB, Frye MA. 2014. Dietary fatty acids alter left ventricular myocardial gene expression in Wistar rats. Nutrition Research, 34(8): 694−706. doi: 10.1016/j.nutres.2014.07.011
    [43]
    Kashyap M, Yoshimura N, Smith PP, Chancellor M, Tyagi P. 2015. Characterization of the role of HCN channels in β3-adrenoceptor mediated rat bladder relaxation. Bladder, 2(2): e15. doi: 10.14440/bladder.2015.44
    [44]
    Katano W, Moriyama Y, Takeuchi JK, Koshiba-Takeuchi K. 2019. Cardiac septation in heart development and evolution. Development, Growth & Differentiation, 61(1): 114−123.
    [45]
    Khechaduri A, Bayeva M, Chang HC, Ardehali H. 2013. Heme levels are increased in human failing hearts. Journal of the American College of Cardiology, 61(18): 1884−1893. doi: 10.1016/j.jacc.2013.02.012
    [46]
    Khodaee M, Grothe HL, Seyfert JH, VanBaak K. 2016. Athletes at high altitude. Sports Health:A Multidisciplinary Approach, 8(2): 126−132. doi: 10.1177/1941738116630948
    [47]
    Kirby AM, Fairman GD, Pamenter ME. 2018. Atypical behavioural, metabolic and thermoregulatory responses to hypoxia in the naked mole rat (Heterocephalus glaber). Journal of Zoology, 305(2): 106−115. doi: 10.1111/jzo.12542
    [48]
    Koga T, Sasaki F, Saeki K, Tsuchiya S, Okuno T, Ohba M, et al. 2021. Expression of leukotriene B4 receptor 1 defines functionally distinct DCs that control allergic skin inflammation. Cellular & Molecular Immunology, 18(6): 1437−1449.
    [49]
    Kolwicz SC Jr, Olson DP, Marney LC, Garcia-Menendez L, Synovec RE, Tian R. 2012. Cardiac-specific deletion of acetyl CoA carboxylase 2 prevents metabolic remodeling during pressure-overload hypertrophy. Circulation Research, 111(6): 728−738. doi: 10.1161/CIRCRESAHA.112.268128
    [50]
    Kong XY, Dong XX, Yang SL, Qian JH, Yang JF, Jiang Q, et al. 2019. Natural selection on TMPRSS6 associated with the blunted erythropoiesis and improved blood viscosity in Tibetan pigs. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 233: 11−22. doi: 10.1016/j.cbpb.2019.03.003
    [51]
    Kryczek I, Lange A, Mottram P, Alvarez X, Cheng P, Hogan M, et al. 2005. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Research, 65(2): 465−472.
    [52]
    Kurniawan H, Soriano-Baguet L, Brenner D. 2020. Regulatory T cell metabolism at the intersection between autoimmune diseases and cancer. European Journal of Immunology, 50(11): 1626−1642. doi: 10.1002/eji.201948470
    [53]
    Lau GY, Arndt S, Murphy MP, Richards JG. 2019. Species- and tissue-specific differences in ROS metabolism during exposure to hypoxia and hyperoxia plus recovery in marine sculpins. Journal of Experimental Biology, 222(Pt 22): jeb206896.
    [54]
    Lavergne A, Tarifeño-Saldivia E, Pirson J, Reuter AS, Flasse L, Manfroid I, et al. 2020. Pancreatic and intestinal endocrine cells in zebrafish share common transcriptomic signatures and regulatory programmes. BMC Biology, 18(1): 109. doi: 10.1186/s12915-020-00840-1
    [55]
    Lawler J. 2002. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. Journal of Cellular and Molecular Medicine, 6(1): 1−12. doi: 10.1111/j.1582-4934.2002.tb00307.x
    [56]
    Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1): 323. doi: 10.1186/1471-2105-12-323
    [57]
    Li F, Xu RJ, Low BE, Lin CL, Garcia-Barros M, Schrandt J, et al. 2018. Alkaline ceramidase 2 is essential for the homeostasis of plasma sphingoid bases and their phosphates. The FASEB Journal, 32(6): 3058−3069. doi: 10.1096/fj.201700445RR
    [58]
    Li MK, Pan D, Sun H, Zhang L, Cheng H, Shao T, et al. 2021a. The hypoxia adaptation of small mammals to plateau and underground burrow conditions. Animal Models and Experimental Medicine, 4(4): 319−328. doi: 10.1002/ame2.12183
    [59]
    Li MY, Tian XY, Li XJ, Huang ML, Huang S, Wu Y, et al. 2021b. Diverse energy metabolism patterns in females in Neodon fuscus, Lasiopodomys brandtii, and Mus musculus revealed by comparative transcriptomics under hypoxic conditions. Science of the Total Environment, 783: 147130. doi: 10.1016/j.scitotenv.2021.147130
    [60]
    Li W, Dong YN, Dong QQ, Sun H, Zhang YF, Wang ZL. 2021c. The remarkable hypoxia tolerance in Brandt's voles (Lasiopodomys brandtii). European Journal of Neuroscience, 53(5): 1652−1660. doi: 10.1111/ejn.15012
    [61]
    Liu B, Wang ZL, Lu JQ. 2010. Response to chronic intermittent hypoxia in blood system of Mandarin vole (Lasiopodomys mandarinus). Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 156(4): 469−474.
    [62]
    Liu CC, Niu YL, Zhou XD, Xu X, Yang Y, Zhang Y, et al. 2015. Cell cycle control, DNA damage repair, and apoptosis-related pathways control pre-ameloblasts differentiation during tooth development. BMC Genomics, 16(1): 592. doi: 10.1186/s12864-015-1783-y
    [63]
    Liu J, Huang SL, Li GL, Zhao JD, Lu W, Zhang ZB. 2020. High housing density increases stress hormone- or disease-associated fecal microbiota in male Brandt's voles (Lasiopodomys brandtii). Hormones and Behavior, 126: 104838. doi: 10.1016/j.yhbeh.2020.104838
    [64]
    Long Y, Yan JJ, Song GL, Li XH, Li XX, Li Q, et al. 2015. Transcriptional events co-regulated by hypoxia and cold stresses in Zebrafish larvae. BMC Genomics, 16(1): 385. doi: 10.1186/s12864-015-1560-y
    [65]
    López-Barneo J, Pardal R, Ortega-Sáenz P. 2001. Cellular mechanism of oxygen sensing. Annual Review of Physiology, 63: 259−287. doi: 10.1146/annurev.physiol.63.1.259
    [66]
    Lorenzo O, Ramírez E, Picatoste B, Egido J, Tuñón J. 2013. Alteration of energy substrates and ROS production in diabetic cardiomyopathy. Mediators of Inflammation, 2013: 461967.
    [67]
    Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12): 550. doi: 10.1186/s13059-014-0550-8
    [68]
    Ludwig LS, Khajuria RK, Sankaran VG. 2016. Emerging cellular and gene therapies for congenital anemias. American Journal of Medical Genetics Part C:Seminars in Medical Genetics, 172(4): 332−348. doi: 10.1002/ajmg.c.31529
    [69]
    Lv L, Deng H, Li Y, Zhang C, Liu X, Liu Q, et al. 2014. The DNA methylation-regulated miR-193a-3p dictates the multi-chemoresistance of bladder cancer via repression of SRSF2/PLAU/HIC2 expression. Cell Death & Disease, 5(9): e1402.
    [70]
    Ma H, Yu S, Liu XJ, Zhang YG, Fakadej T, Liu ZQ, et al. 2019. Lin28a regulates pathological cardiac hypertrophic growth through Pck2-mediated enhancement of anabolic synthesis. Circulation, 139(14): 1725−1740. doi: 10.1161/CIRCULATIONAHA.118.037803
    [71]
    Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Molecular Cell, 40(2): 294−309. doi: 10.1016/j.molcel.2010.09.022
    [72]
    Martínez-Micaelo N, González-Abuín N, Terra X, Ardévol A, Pinent M, Petretto E, et al. 2016. Identification of a nutrient-sensing transcriptional network in monocytes by using inbred rat models on a cafeteria diet. Disease Models & Mechanisms, 9(10): 1231−1239.
    [73]
    Mehta V, Fields L, Evans IM, Yamaji M, Pellet-Many C, Jones T, et al. 2018. VEGF (vascular endothelial growth factor) induces NRP1 (neuropilin-1) cleavage via ADAMs (a disintegrin and metalloproteinase) 9 and 10 to generate novel carboxy-terminal NRP1 fragments that regulate angiogenic signaling. Arteriosclerosis, Thrombosis, and Vascular Biology, 38(8): 1845−1858. doi: 10.1161/ATVBAHA.118.311118
    [74]
    Milanesi R, Bucchi A, Baruscotti M. 2015. The genetic basis for inherited forms of sinoatrial dysfunction and atrioventricular node dysfunction. Journal of Interventional Cardiac Electrophysiology, 43(2): 121−134. doi: 10.1007/s10840-015-9998-z
    [75]
    Miller D, Hannon C, Ganetzky B. 2012. A mutation in Drosophila aldolase causes temperature-sensitive paralysis, shortened lifespan, and neurodegeneration. Journal of Neurogenetics, 26(3-4): 317−327. doi: 10.3109/01677063.2012.706346
    [76]
    Miyata S, Minobe W, Bristow MR, Leinwand LA. 2000. Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circulation Research, 86(4): 386−390. doi: 10.1161/01.RES.86.4.386
    [77]
    Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research, 35(S2): W182−W185.
    [78]
    Orso F, Balzac F, Marino M, Lembo A, Retta SF, Taverna D. 2013. miR-21 coordinates tumor growth and modulates KRIT1 levels. Biochemical and Biophysical Research Communications, 438(1): 90−96. doi: 10.1016/j.bbrc.2013.07.031
    [79]
    Pamenter ME, Lau GY, Richards JG, Milsom WK. 2018. Naked mole rat brain mitochondria electron transport system flux and H+ leak are reduced during acute hypoxia. Journal of Experimental Biology, 221(4): jeb171397.
    [80]
    Pamidimukkala NV, Leonard MK, Snyder D, McCorkle JR, Kaetzel DM. 2018. Metastasis suppressor NME1 directly activates transcription of the ALDOC gene in melanoma cells. Anticancer Research, 38(11): 6059−6068. doi: 10.21873/anticanres.12956
    [81]
    Paparde A, Plakane L, Circenis K, Aivars JI. 2015. Effect of acute systemic hypoxia on human cutaneous microcirculation and endothelial, sympathetic and myogenic activity. Microvascular Research, 102: 1−5. doi: 10.1016/j.mvr.2015.07.005
    [82]
    Paul DS, Grevengoed TJ, Pascual F, Ellis JM, Willis MS, Coleman RA. 2014. Deficiency of cardiac Acyl-CoA synthetase-1 induces diastolic dysfunction, but pathologic hypertrophy is reversed by rapamycin. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1841(6): 880–887.
    [83]
    Pell VR, Chouchani ET, Murphy MP, Brookes PS, Krieg T. 2016. Moving forwards by blocking back-flow: the Yin and Yang of MI therapy. Circulation Research, 118(5): 898−906. doi: 10.1161/CIRCRESAHA.115.306569
    [84]
    Peoples JN, Saraf A, Ghazal N, Pham TT, Kwong JQ. 2019. Mitochondrial dysfunction and oxidative stress in heart disease. Experimental & Molecular Medicine, 51(12): 1−13.
    [85]
    Pichon A, Bai ZZ, Marchant D, Jin GE, Voituron N, Yu HX, et al. 2013. Cardiac adaptation to high altitude in the plateau pika (Ochotona curzoniae). Physiological Reports, 1(2): e00032.
    [86]
    Potter JHT, Davies KTJ, Yohe LR, Sanchez MKR, Rengifo EM, Struebig M, et al. 2021. Dietary diversification and specialization in neotropical bats facilitated by early molecular evolution. Molecular Biology and Evolution, 38(9): 3864−3883. doi: 10.1093/molbev/msab028
    [87]
    Qu YL, Deng CH, Luo Q, Shang XY, Wu JX, Shi Y, et al. 2019. Arid1a regulates insulin sensitivity and lipid metabolism. eBioMedicine, 42: 481−493. doi: 10.1016/j.ebiom.2019.03.021
    [88]
    Roklicer R, Lakicevic N, Stajer V, Trivic T, Bianco A, Mani D, et al. 2020. The effects of rapid weight loss on skeletal muscle in judo athletes. Journal of Translational Medicine, 18(1): 142. doi: 10.1186/s12967-020-02315-x
    [89]
    Sawada N, Li YX, Liao JK. 2010. Novel aspects of the roles of Rac1 GTPase in the cardiovascular system. Current Opinion in Pharmacology, 10(2): 116−121. doi: 10.1016/j.coph.2009.11.004
    [90]
    Schindler RFR, Brand T. 2016. The Popeye domain containing protein family-A novel class of cAMP effectors with important functions in multiple tissues. Progress in Biophysics and Molecular Biology, 120(1-3): 28−36. doi: 10.1016/j.pbiomolbio.2016.01.001
    [91]
    Schippers MP, Ramirez O, Arana M, Pinedo-Bernal P, McClelland GB. 2012. Increase in carbohydrate utilization in high-altitude Andean mice. Current Biology, 22(24): 2350−2354. doi: 10.1016/j.cub.2012.10.043
    [92]
    Schneider AM, Duffield AS, Symer DE, Burns KH. 2009. Roles of retrotransposons in benign and malignant hematologic disease. Cellscience, 6(2): 121−145.
    [93]
    Scott GR, Hawkes LA, Frappell PB, Butler PJ, Bishop CM, Milsom WK. 2015. How bar-headed geese fly over the Himalayas. Physiology, 30(2): 107−115. doi: 10.1152/physiol.00050.2014
    [94]
    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11): 2498−2504. doi: 10.1101/gr.1239303
    [95]
    Shao X, Dong X, Cai J, Tang C, Xie KN, Yan ZD, et al. 2021. Oxygen enrichment ameliorates cardiorespiratory alterations induced by chronic high-altitude hypoxia in rats. Frontiers in Physiology, 11: 616145. doi: 10.3389/fphys.2020.616145
    [96]
    Shi LY, Liu LK, Li XJ, Wu Y, Tian XY, Shi YH, et al. 2021a. Phylogeny and evolution of Lasiopodomys in subfamily Arvivolinae based on mitochondrial genomics. PeerJ, 9: e10850. doi: 10.7717/peerj.10850
    [97]
    Shi LY, Jiang MW, Li MY, Shang XZ, Li XJ, Huang ML, et al. 2021b. Regulation of HIF-1α and p53 in stress responses in the subterranean rodents Lasiopodomys mandarinus and Lasiopodomys brandtii (Rodentia: Cricetidae). Zoologia, 38: e58607.
    [98]
    Shi LY, Chen BJ, Wang XR, Huang ML, Qiao CC, Wang JG, et al. 2021c. Antioxidant response to severe hypoxia in Brandt's vole Lasiopodomys brandtii. Integrative Zoology, 00: 1–15.
    [99]
    Shinzawa-Itoh K, Shimomura rt H, Yanagisawa S, Shimada S, Takahashi R, Oosaki M, et al. 2016. Purification of active respiratory supercomplex from bovine heamitochondria enables functional studies. Journal of Biological Chemistry, 291(8): 4178−4184. doi: 10.1074/jbc.M115.680553
    [100]
    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31(19): 3210−3212. doi: 10.1093/bioinformatics/btv351
    [101]
    Sindi HA, Russomanno G, Satta S, Abdul-Salam VB, Jo KB, Qazi-Chaudhry B, et al. 2020. Therapeutic potential of KLF2-induced exosomal microRNAs in pulmonary hypertension. Nature Communications, 11(1): 1185. doi: 10.1038/s41467-020-14966-x
    [102]
    Singh NK, Rao GN. 2019. Emerging role of 12/15-Lipoxygenase (ALOX15) in human pathologies. Progress in Lipid Research, 73: 28−45. doi: 10.1016/j.plipres.2018.11.001
    [103]
    Su ZH, Liu YW, Zhang H. 2021. Adaptive cardiac metabolism under chronic hypoxia: mechanism and clinical implications. Frontiers in Cell and Developmental Biology, 9: 625524. doi: 10.3389/fcell.2021.625524
    [104]
    Sun KQ, Zhang YJ, D’Alessandro A, Nemkov T, Song AR, Wu HY, et al. 2016. Sphingosine-1-phosphate promotes erythrocyte glycolysis and oxygen release for adaptation to high-altitude hypoxia. Nature Communications, 7(1): 12086. doi: 10.1038/ncomms12086
    [105]
    Sun W, Liu CX, Chen QH, Liu N, Yan YY, Liu B. 2018. SIRT3: a new regulator of cardiovascular diseases. Oxidative Medicine and Cellular Longevity, 2018: 7293861.
    [106]
    Suzuki TA, Martins FM, Nachman MW. 2019. Altitudinal variation of the gut microbiota in wild house mice. Molecular Ecology, 28(9): 2378−2390. doi: 10.1111/mec.14905
    [107]
    Thompson CB. 2016. Into thin air: how we sense and respond to hypoxia. Cell, 167(1): 9−11. doi: 10.1016/j.cell.2016.08.036
    [108]
    Toyono T, Usui T, Yokoo S, Taketani Y, Nakagawa S, Kuroda M, et al. 2015. Angiopoietin-like 7 is an anti-angiogenic protein required to prevent vascularization of the cornea. PLoS One, 10(1): e0116838. doi: 10.1371/journal.pone.0116838
    [109]
    Trindade A, Duarte A. 2020. Notch signaling function in the angiocrine regulation of tumor development. Cells, 9(11): 2467. doi: 10.3390/cells9112467
    [110]
    Verghese J. 2013. Slaying dementia dragons with blood, lungs, and guts. Journal of the American Geriatrics Society, 61(1): 155−157. doi: 10.1111/jgs.12064
    [111]
    Wang H, Zhong JC, Wang JK, Chai ZX, Zhang CF, Xin JW, et al. 2021. Whole-transcriptome analysis of yak and cattle heart tissues reveals regulatory pathways associated with high-altitude adaptation. Frontiers in Genetics, 12: 579800. doi: 10.3389/fgene.2021.579800
    [112]
    Wang L, Song LJ, Li C, Feng QL, Xu MP, Li ZQ, et al. 2018. Renal denervation improves cardiac function by attenuating myocardiocyte apoptosis in dogs after myocardial infarction. BMC Cardiovascular Disorders, 18(1): 86. doi: 10.1186/s12872-018-0828-y
    [113]
    Wang SF, Yu XP, Lin ZH, Zhang SQ, Xue LY, Xue QG, et al. 2017a. Hemoglobins likely function as peroxidase in blood clam Tegillarca granosa hemocytes. Journal of Immunology Research, 2017: 7125084.
    [114]
    Wang ZX, Shang P, Li QG, Wang LY, Chamba Y, Zhang B, et al. 2017b. iTRAQ-based proteomic analysis reveals key proteins affecting muscle growth and lipid deposition in pigs. Scientific Reports, 7: 46717. doi: 10.1038/srep46717
    [115]
    Wu Z, Jin FY, Wang LX, Zhao YF, Jiang Y, Li J, et al. 2019. Antioxidant effects of baoyuan decoction on dysfunctional erythrocytes in high-fat diet-induced hyperlipidemic ApoE-/- Mice. Oxidative Medicine and Cellular Longevity, 2019: 5172480.
    [116]
    Xu LL, Hao ZQ, Lin JY, Zhao Q, Zhang BJ, Li GL, et al. 2019. Transcriptome sequencing of Eospalax fontanierii to determine hypoxia regulation of cardiac fibrinogen. Molecular Biology Reports, 46(6): 5671−5683. doi: 10.1007/s11033-019-04690-1
    [117]
    Xu-Cai YO, Wu QY. 2010. Molecular forms of natriuretic peptides in heart failure and their implications. Heart, 96(6): 419−424. doi: 10.1136/hrt.2008.164145
    [118]
    Yan W, Wu FY, Morser J, Wu QY. 2000. Corin, a transmembrane cardiac serine protease, acts as a pro-atrial natriuretic peptide-converting enzyme. Proceedings of the National Academy of Sciences of the United States of America, 97(15): 8525−8529. doi: 10.1073/pnas.150149097
    [119]
    Yang X, Zhang H, Shang J, Liu G, Xia T, Zhao C, et al. 2018. Comparative analysis of the blood transcriptomes between wolves and dogs. Animal Genetics, 49(4): 291−302. doi: 10.1111/age.12675
    [120]
    Yčas JW, Horrow JC, Horne BD. 2015. Persistent increase in red cell size distribution width after acute diseases: a biomarker of hypoxemia. Clinica Chimica Acta, 448: 107−117. doi: 10.1016/j.cca.2015.05.021
    [121]
    Yin ZY, Ren J, Guo W. 2015. Sarcomeric protein isoform transitions in cardiac muscle: a journey to heart failure. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1852(1): 47–52.
    [122]
    Yoon HE, Kim SJ, Hwang HS, Chung S, Yang CW, Shin SJ. 2015. Progressive rise in red blood cell distribution width predicts mortality and cardiovascular events in end-stage renal disease patients. PLoS One, 10(5): e0126272. doi: 10.1371/journal.pone.0126272
    [123]
    Zeng CJ, Li WJ, Liao Q, Yan TT, Wang KS, Hu Y, et al. 2019. Comparative transcriptomics reveals the expression differences between four developmental stages of American cockroach (Periplaneta americana). DNA and Cell Biology, 38(10): 1078−1087. doi: 10.1089/dna.2018.4578
    [124]
    Zhang J, Malmirchegini GR, Clubb RT, Loo JA. 2015. Native top-down mass spectrometry for the structural characterization of human hemoglobin. European Journal of Mass Spectrometry, 21(3): 221−231. doi: 10.1255/ejms.1340
    [125]
    Zhang XX, Lou ZZ, Huang SY, Zhou DH, Jia WZ, Su CL, et al. 2013. Genetic characterization of Toxoplasma gondii from Qinghai vole, Plateau pika and Tibetan ground-tit on the Qinghai-Tibet Plateau, China. Parasites & Vectors, 6: 291.
    [126]
    Zhang XY, Jian YN, Li XP, Ma LQ, Karanis G, Karanis P. 2018. The first report of Cryptosporidium spp. in Microtus fuscus (Qinghai vole) and Ochotona curzoniae (wild plateau pika) in the Qinghai-Tibetan Plateau area, China. Parasitology Research, 117(5): 1401−1407. doi: 10.1007/s00436-018-5827-5
    [127]
    Zhang Y, Zhang HL, Zhang B, Ling Y, Zhang H. 2020. Identification of key HIF-1α target genes that regulate adaptation to hypoxic conditions in Tibetan chicken embryos. Gene, 729: 144321. doi: 10.1016/j.gene.2019.144321
    [128]
    Zheng XG, Chopp M, Lu Y, Buller B, Jiang F. 2013. MiR-15b and miR-152 reduce glioma cell invasion and angiogenesis via NRP-2 and MMP-3. Cancer Letters, 329(2): 146−154. doi: 10.1016/j.canlet.2012.10.026
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