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Review Article

The relativity analysis of hypoxia inducible factor-1α in pulmonary arterial hypertension (ascites syndrome) in broilers: a review

, , , , , , , , , , , & show all
Received 27 Dec 2023, Accepted 17 May 2024, Published online: 18 Jun 2024

References

  • Aldred, M.A., Comhair, S.A., Varella-Garcia, M., Asosingh, K., Xu, W., Noon, G.P., Thistlethwaite, P.A., Tuder, R.M., Erzurum, S.C., Geraci, M.W. & Coldren, C.D. (2010). Somatic chromosome abnormalities in the lungs of patients with pulmonary arterial hypertension. American Journal of Respiratory and Critical Care Medicine, 182, 1153–1160.
  • Alexander, C., Li, T., Hattori, Y., Chiu, D., Frost, G.R., Liu, J.L., Anderson, C., Wong, C.J., Park, E., Iadecola, L., Li, C. & M, Y. (2022). Hypoxia Inducible Factor-1α binds and activates γ-secretase for Aβ production under hypoxia and cerebral hypoperfusion. Molecular Psychiatry, 27, 4264–4273.
  • Asosingh, K., Comhair, S., Mavrakis, L., Xu, W., Horton, D., Taylor, I., Tkachenko, S., Hu, B. & Erzurum, S. (2021). Single-cell transcriptomic profile of human pulmonary artery endothelial cells in health and pulmonary arterial hypertension. Scientific Reports, 11, 14714.
  • Ball, M.K., Waypa, G.B., Mungai, P.T., Nielsen, J.M., Czech, L., Dudley, V.J., Beussink, L., Dettman, R.W., Berkelhamer, S.K., Steinhorn, R.H., Shah, S.J. & Schumacker, P.T. (2014). Regulation of hypoxia-induced pulmonary hypertension by vascular smooth muscle hypoxia-inducible factor-1α. American Journal of Respiratory and Critical Care Medicine, 189, 314–324.
  • Baumann, J., Tsao, C.C., Huang, S.F., Gassmann, M. & Ogunshola, O.O. (2021). Astrocyte-specific hypoxia-inducible factor 1 (HIF-1) does not disrupt the endothelial barrier during hypoxia in vitro. Fluids and Barriers of the CNS, 18, 13.
  • Baysal, B.E. (2006). A phenotypic perspective on mammalian oxygen sensor candidates. Annals of the New York Academy of Sciences, 1073, 221–233.
  • Bordan, Z., Batori, R., Chen, F., Li, X., Meadows, M.L., Haigh, S., Sellers, H., Su, Y., Barman, S. & Fulton, D. (2022). PDZ-binding kinase drives pulmonary artery smooth muscle proliferation and vascular remodeling in pulmonary arterial hypertension. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 36.
  • Brusselmans, K., Compernolle, V., Tjwa, M., Wiesener, M.S., Maxwell, P.H., Collen, D. & Carmeliet, P. (2003). Heterozygous deficiency of hypoxia-inducible factor-2alpha protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia. The Journal of Clinical Investigation, 111, 1519–1527.
  • Cabaj, A., Moszyńska, A., Charzyńska, A., Bartoszewski, R. & Dąbrowski, M. (2022). Functional and HRE motifs count analysis of induction of selected hypoxia-responsive genes by HIF-1 and HIF-2 in human umbilical endothelial cells. Cellular Signalling, 90, 110209.
  • Chen, J., Sysol, J.R., Singla, S., Zhao, S., Yamamura, A., Valdez-Jasso, D., Abbasi, T., Shioura, K.M., Sahni, S., Reddy, V., Sridhar, A., Gao, H., Torres, J., Camp, S.M., Tang, H., Ye, S.Q., Comhair, S., Dweik, R., Hassoun, P., Yuan, J.X. & Garcia, J.G.N. (2017). Nicotinamide phosphoribosyl transferase promotes pulmonary vascular remodeling and is a therapeutic target in pulmonary arterial hypertension. Circulation, 135, 1532–1546.
  • Cheng, S., Liu, X., Liu, P., Li, G., Guo, X., Hu, G., Li, L., Wu, C., Xu, Z., Zhou, Q., Jiang, J., Luo, S., Huang, H. & Liu, P. (2021). Dysregulated expression of mRNA and SNP in pulmonary artery remodeling in ascites syndrome in broilers. Poultry Science, 100, 100877.
  • Choudhry, H. & Harris, A.L. (2018). Advances in hypoxia-inducible factor biology. Cell Metabolism, 27, 281–298.
  • Closter, A.M., van As, P., Groenen, M.A., Vereijken, A.L., van Arendonk, J.A. & Bovenhuis, H. (2009). Genetic and phenotypic relationships between blood gas parameters and ascites-related traits in broilers. Poultry Science, 88, 483–490.
  • Cui, H., Liu, J., Xu, G., Ren, X., Li, Z., Li, Y. & Ning, Z. (2019). Altered expression of zinc transporter ZIP12 in broilers of ascites syndrome induced by intravenous cellulose microparticle injection. Biochemical Genetics, 57, 159–169.
  • Davies, P. & Reid, L. (1991). Hypoxic remodeling of the rat pulmonary arterial microcirculation assessed by microdissection. Journal of Applied Physiology, 71, 1886–1891.
  • Dey, S., Parveen, A., Tarrant, K.J., Licknack, T., Kong, B.C., Anthony, N.B. & Rhoads, D.D. (2018). Whole genome resequencing identifies the CPQ gene as a determinant of ascites syndrome in broilers. PLoS One, 13, e0189544.
  • Eyries, M., Montani, D., Girerd, B., Perret, C., Leroy, A., Lonjou, C., Chelghoum, N., Coulet, F., Bonnet, D., Dorfmüller, P., Fadel, E., Sitbon, O., Simonneau, G., Tregouët, D.A., Humbert, M. & Soubrier, F. (2014). EIF2AK4 mutations cause pulmonary veno-occlusive disease, a recessive form of pulmonary hypertension. Nature Genetics, 46, 65–69.
  • Fuhrmann, D.C. & Brüne, B. (2022). A graphical journey through iron metabolism, microRNAs, and hypoxia in ferroptosis. Redox Biology, 54, 102365.
  • Gibbons, G.H. & Dzau, V.J. (1994). The emerging concept of vascular remodeling. The New England Journal of Medicine, 330, 1431–1438.
  • Graham, A.M. & Barreto, F.S. (2020). Independent losses of the hypoxia-inducible factor (HIF) pathway within crustacea. Molecular Biology and Evolution, 37, 1342–1349.
  • Guo, L., Qiu, Z., Wei, L., Yu, X., Gao, X., Jiang, S., Tian, H., Jiang, C. & Zhu, D. (2012). The microRNA-328 regulates hypoxic pulmonary hypertension by targeting at insulin growth factor 1 receptor and L-type calcium channel-α1C. Hypertension, 59, 1006–1013.
  • Hadinnapola, C., Bleda, M., Haimel, M., Screaton, N., Swift, A., Dorfmüller, P., Preston, S.D., Southwood, M., Hernandez-Sanchez, J., Martin, J., Treacy, C., Yates, K., Bogaard, H., Church, C., Coghlan, G., Condliffe, R., Corris, P.A., Gibbs, S., Girerd, B., Holden, S. & Humbert, M. (2017). Phenotypic characterization of EIF2AK4 mutation carriers in a large cohort of patients diagnosed clinically with pulmonary arterial hypertension. Circulation, 136, 2022–2033.
  • Hassanzadeh, M., Maddadi, M.S., Mirzaie, S., Assasie, K. & Moayyedian, H. (2010). Partial pressure of carbon dioxide in the venous blood of young birds as a predictor of ascites susceptibility in broiler chickens. Acta Veterinaria Hungarica, 58, 221–230.
  • He, M., Ma, S., Cai, Q., Wu, Y., Shao, C., Kong, H., Wang, H., Zeng, X. & Xie, W. (2018). Hypoxia induces the dysfunction of human endothelial colony-forming cells via HIF-1α signaling. Respiratory Physiology & Neurobiology, 247, 87–95.
  • He, S., Ma, C., Zhang, L., Bai, J., Wang, X., Zheng, X., Zhang, J., Xin, W., Li, Y., Jiang, Y., Wang, S. & Zhu, D. (2020). GLI1-mediated pulmonary artery smooth muscle cell pyroptosis contributes to hypoxia-induced pulmonary hypertension. American Journal of Physiology. Lung Cellular and Molecular Physiology, 318, L472–L482.
  • Iyer, N.V., Kotch, L.E., Agani, F., Leung, S.W., Laughner, E., Wenger, R.H., Gassmann, M., Gearhart, J.D., Lawler, A.M., Yu, A.Y. & Semenza, G.L. (1998). Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes & Development, 12, 149–162.
  • Jiang, B.H., Rue, E., Wang, G.L., Roe, R. & Semenza, G.L. (1996). Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. The Journal of Biological Chemistry, 271, 17771–17778.
  • Jiang, D.T., Tuo, L., Bai, X., Bing, W.D., Qu, Q.X., Zhao, X., Song, G.M., Bi, Y.W. & Sun, W.Y. (2022). Prostaglandin E1 reduces apoptosis and improves the homing of mesenchymal stem cells in pulmonary arterial hypertension by regulating hypoxia-inducible factor 1 alpha. Stem Cell Research & Therapy, 13, 316.
  • Jiang, Y., Zhou, Y., Peng, G., Liu, N., Tian, H., Pan, D., Liu, L., Yang, X., Li, C., Li, W., Chen, L., Ran, P. & Dai, A. (2018). Topotecan prevents hypoxia-induced pulmonary arterial hypertension and inhibits hypoxia-inducible factor-1α and TRPC channels. The International Journal of Biochemistry & Cell Biology, 104, 161–170.
  • Julian, R.J. (2000). Physiological, management and environmental triggers of the ascites syndrome: a review. Avian Pathology, 29, 519–527.
  • Kelly, B.D., Hackett, S.F., Hirota, K., Oshima, Y., Cai, Z., Berg-Dixon, S., Rowan, A., Yan, Z., Campochiaro, P.A. & Semenza, G.L. (2003). Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circulation Research, 93, 1074–1081.
  • Kojima, H., Tokunou, T., Takahara, Y., Sunagawa, K., Hirooka, Y., Ichiki, T. & Tsutsui, H. (2019). Hypoxia-inducible factor-1 α deletion in myeloid lineage attenuates hypoxia-induced pulmonary hypertension. Physiological Reports, 7, e14025.
  • Kouvaras, E., Christoni, Z., Siasios, I., Malizos, K., Koukoulis, G.K. & Ioannou, M. (2019). Hypoxia-inducible factor 1-alpha and vascular endothelial growth factor in cartilage tumors. Biotechnic & Histochemistry, 94, 283–289.
  • Li, Q.F. & Dai, A.G. (2004). Hypoxia-inducible factor-1 alpha regulates the role of vascular endothelial growth factor on pulmonary arteries of rats with hypoxia-induced pulmonary hypertension. Chinese Medical Journal, 117, 1023–1028.
  • Li, S., Ran, Y., Zhang, D., Chen, J., Li, S. & Zhu, D. (2013). MicroRNA-138 plays a role in hypoxic pulmonary vascular remodelling by targeting Mst1. The Biochemical Journal, 452, 281–291.
  • Li, S.S., Ran, Y.J., Zhang, D.D., SZ, L. & Zhu, D. (2014). MicroRNA-190 regulates hypoxic pulmonary vasoconstriction by targeting a voltage-gated K channel in arterial smooth muscle cells. Journal of Cellular Biochemistry, 115, 1196–1205.
  • Lok, C.N. & Ponka, P. (1999). Identification of a hypoxia response element in the transferrin receptor gene. The Journal of Biological Chemistry, 274, 24147–24152.
  • Luo, Y., Teng, X., Zhang, L., Chen, J., Liu, Z., Chen, X., Zhao, S., Yang, S., Feng, J. & Yan, X. (2019). CD146-HIF-1α hypoxic reprogramming drives vascular remodeling and pulmonary arterial hypertension. Nature Communications, 10, 3551.
  • Ma, C., Wang, X., He, S., Zhang, L., Bai, J., Qu, L., Qi, J., Zheng, X., Zhu, X., Mei, J., Guan, X., Yuan, H. & Zhu, D. (2022). Ubiquitinated AIF is a major mediator of hypoxia-induced mitochondrial dysfunction and pulmonary artery smooth muscle cell proliferation. Cell & Bioscience, 12, 9.
  • Madan, E., Parker, T.M., Pelham, C.J., Palma, A.M., Peixoto, M.L., Nagane, M., Chandaria, A., Tomás, A.R., Canas-Marques, R., Henriques, V., Galzerano, A., Cabral-Teixeira, J., Selvendiran, K., Kuppusamy, P., Carvalho, C., Beltran, A., Moreno, E., Pati, U.K. & Gogna, R. (2019). HIF-transcribed p53 chaperones HIF-1α. Nucleic Acids Research, 47, 10212–10234.
  • Manalo, D.J., Rowan, A., Lavoie, T., Natarajan, L., Kelly, B.D., Ye, S.Q., Garcia, J.G. & Semenza, G.L. (2005). Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood, 105, 659–669.
  • Masri, F.A., Xu, W., Comhair, S.A., Asosingh, K., Koo, M., Vasanji, A., Drazba, J., Anand-Apte, B. & Erzurum, S.C. (2007). Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. American Journal of Physiology. Lung Cellular and Molecular Physiology, 293, L548–L554.
  • Montani, D., Girerd, B., Jaïs, X., Levy, M., Amar, D., Savale, L., Dorfmüller, P., Seferian, A., Lau, E.M., Eyries, M., Le Pavec, J., Parent, F., Bonnet, D., Soubrier, F., Fadel, E., Sitbon, O., Simonneau, G. & Humbert, M. (2017). Clinical phenotypes and outcomes of heritable and sporadic pulmonary veno-occlusive disease: a population-based study. The Lancet. Respiratory Medicine, 5, 125–134.
  • Morin, P. & Storey, K.B. (2005). Cloning and expression of hypoxia-inducible factor 1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochimica et Biophysica Acta, 1729, 32–40.
  • Mukhopadhyay, C.K., Mazumder, B. & Fox, P.L. (2000). Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. The Journal of Biological Chemistry, 275, 21048–21054.
  • Ohh, M., Taber, C.C., Ferens, F.G. & Tarade, D. (2022). Hypoxia-inducible factor underlies von Hippel-Lindau disease stigmata. eLife, 11.
  • Okazaki, S., Boku, S., Watanabe, Y., Otsuka, I., Horai, T., Morikawa, R., Kimura, A., Shimmyo, N., Tanifuji, T., Someya, T. & Hishimoto, A. (2022). Polymorphisms in the hypoxia inducible factor binding site of the macrophage migration inhibitory factor gene promoter in schizophrenia. PLoS One, 17, e0265738.
  • Ozer, A. & Bruick, R.K. (2005). Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell cycle, 4, 1153–1156.
  • Ozer, A., Wu, L.C. & Bruick, R.K. (2005). The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proceedings of the National Academy of Sciences of the United States of America, 102, 7481–7486.
  • Paddenberg, R., Stieger, P., von Lilien, A.L., Faulhammer, P., Goldenberg, A., Tillmanns, H.H., Kummer, W. & Braun-Dullaeus, R.C. (2007). Rapamycin attenuates hypoxia-induced pulmonary vascular remodeling and right ventricular hypertrophy in mice. Respiratory Research, 8, 15.
  • Pan, S.Y., Tsai, P.Z., Chou, Y.H., Chang, Y.T., Chang, F.C., Chiu, Y.L., Chiang, W.C., Hsu, T., Chen, Y.M., TS, C. & Lin, S.L. (2021). Kidney pericyte hypoxia-inducible factor regulates erythropoiesis but not kidney fibrosis. Kidney International, 99, 1354–1368.
  • Parveen, A., Jackson, C.D., Dey, S., Tarrant, K., Anthony, N. & Rhoads, D.D. (2020). Identification and validation of quantitative trait loci for ascites syndrome in broiler chickens using whole genome resequencing. BMC Genetics, 21, 54.
  • Pugh, C.W. & Ratcliffe, P.J. (2003). Regulation of angiogenesis by hypoxia: role of the HIF system. Nature Medicine, 9, 677–684.
  • Pullamsetti, S.S., Mamazhakypov, A., Weissmann, N., Seeger, W. & Savai, R. (2020). Hypoxia-inducible factor signaling in pulmonary hypertension. The Journal of Clinical Investigation, 130, 5638–5651.
  • Rolfs, A., Kvietikova, I., Gassmann, M. & Wenger, R.H. (1997). Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. The Journal of Biological Chemistry, 272, 20055–20062.
  • Sawai, S., Wong, P.F. & Ramasamy, T.S. (2022). Hypoxia-regulated microRNAs: the molecular drivers of tumor progression. Critical Reviews in Biochemistry and Molecular Biology, 57, 351–376.
  • Semenza, G.L. (1998). Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Current Opinion in Genetics & Development, 8, 588–594.
  • Semenza, G.L. (2000). HIF-1 and human disease: one highly involved factor. Genes & Development, 14, 1983–1991.
  • Semenza, G.L. (2001). Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends in Molecular Medicine, 7, 345–350.
  • Semenza, G.L. (2003). Targeting HIF-1 for cancer therapy. Nature Reviews. Cancer, 3, 721–732.
  • Semenza, G.L. (2022). Regulation of erythropoiesis by the hypoxia-inducible factor pathway: effects of genetic and pharmacological perturbations. Annual Review of Medicine, null.
  • Semenza, G.L., Nejfelt, M.K., SM, C. & Antonarakis, S.E. (1991). Hypoxia-inducible nuclear factors bind to an enhancer element located 3’ to the human erythropoietin gene. Proceedings of the National Academy of Sciences of the United States of America, 88, 5680–5684.
  • Shah, Y.M. & Xie, L. (2014). Hypoxia-inducible factors link iron homeostasis and erythropoiesis. Gastroenterology, 146, 630–642.
  • Shih, H.M., Pan, S.Y., Wu, C.J., Chou, Y.H., Chen, C.Y., Chang, F.C., Chen, Y.T., Chiang, W.C., Tsai, H.C., Chen, Y.M. & Lin, S.L. (2021). Transforming growth factor-β1 decreases erythropoietin production through repressing hypoxia-inducible factor 2α in erythropoietin-producing cells. Journal of Biomedical Science, 28, 73.
  • Sun, Y., Wen, F., Yan, C., Su, L., Luo, J., Chi, W. & Zhang, S. (2021). Mitophagy protects the retina against anti-vascular endothelial growth factor therapy-driven hypoxia via hypoxia-inducible factor-1α signaling. Frontiers in Cell and Developmental Biology, 9, 727822.
  • Tanaka, H., Yamamoto, M., Hashimoto, N., Miyakoshi, M., Tamakawa, S., Yoshie, M., Tokusashi, Y., Yokoyama, K., Yaginuma, Y. & Ogawa, K. (2006). Hypoxia-independent overexpression of hypoxia-inducible factor 1alpha as an early change in mouse hepatocarcinogenesis. Cancer Research, 66, 11263–11270.
  • Taraseviciene-Stewart, L., Kasahara, Y., Alger, L., Hirth, P., McMahon, G., Waltenberger, J., Voelkel, N.F. & Tuder, R.M. (2001). Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 15, 427–438.
  • Thévenod, F., Schreiber, T. & Lee, W.K. (2022). Renal hypoxia-HIF-PHD-EPO signaling in transition metal nephrotoxicity: friend or foe? Archives of Toxicology, 96, 1573–1607.
  • Thompson, A.A.R. & Lawrie, A. (2017). Targeting vascular remodeling to treat pulmonary arterial hypertension. Trends in Molecular Medicine, 23, 31–45.
  • Tzouvelekis, A., Harokopos, V., Paparountas, T., Oikonomou, N., Chatziioannou, A., Vilaras, G., Tsiambas, E., Karameris, A., Bouros, D. & Aidinis, V. (2007). Comparative expression profiling in pulmonary fibrosis suggests a role of hypoxia-inducible factor-1alpha in disease pathogenesis. American Journal of Respiratory and Critical Care Medicine, 176, 1108–1119.
  • Tzouvelekis, A., Ntolios, P., Karameris, A., Koutsopoulos, A., Boglou, P., Koulelidis, A., Archontogeorgis, K., Zacharis, G., Drakopanagiotakis, F., Steiropoulos, P., Anevlavis, S., Polychronopoulos, V., Mikroulis, D. & Bouros, D. (2012). Expression of hypoxia-inducible factor (HIF)-1a-vascular endothelial growth factor (VEGF)-inhibitory growth factor (ING)-4- axis in sarcoidosis patients. BMC Research Notes, 5, 654.
  • Urick, M.E., Giles, J.R. & Johnson, P.A. (2008). VEGF expression and the effect of NSAIDs on ascites cell proliferation in the hen model of ovarian cancer. Gynecologic Oncology, 110, 418–424.
  • Veith, C., Schermuly, R.T., Brandes, R.P. & Weissmann, N. (2016). Molecular mechanisms of hypoxia-inducible factor-induced pulmonary arterial smooth muscle cell alterations in pulmonary hypertension. The Journal of Physiology, 594, 1167–1177.
  • Veith, C., Zakrzewicz, D., Dahal, B.K., Bálint, Z., Murmann, K., Wygrecka, M., Seeger, W., Schermuly, R.T., Weissmann, N. & Kwapiszewska, G. (2014). Hypoxia- or PDGF-BB-dependent paxillin tyrosine phosphorylation in pulmonary hypertension is reversed by HIF-1α depletion or imatinib treatment. Thrombosis and Haemostasis, 112, 1288–1303.
  • Wang, G., Tao, X. & Peng, L. (2022). miR-155-5p regulates hypoxia-induced pulmonary artery smooth muscle cell function by targeting PYGL. Bioengineered, 13, 12985–12997.
  • Wang, L., Guo, L., Zhu, L., Sun, Y., Zhang, M. & Xu, Z. (2020). Characteristics of pulmonary vascular remodeling in a porcine model of shunt-associated pulmonary arterial hypertension. Pediatric Cardiology, 41, 669–676.
  • Wang, L.L., Zhu, X.L., Han, S.H. & Xu, L. (2021). Hypoxia upregulates NOTCH3 signaling pathway to promote endothelial-mesenchymal transition in pulmonary artery endothelial cells. Evidence-based Complementary and Alternative Medicine, 2021, 1525619.
  • Wenger, R.H. (2002). Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB journal, 16, 1151–1162.
  • Wenger, R.H., Stiehl, D.P. & Camenisch, G. (2005). Integration of oxygen signaling at the consensus HRE. Science’s STKE: Signal Transduction Knowledge Environment, 2005, re12.
  • Wideman, R.F., Rhoads, D.D., Erf, G.F. & Anthony, N.B. (2013). Pulmonary arterial hypertension (ascites syndrome) in broilers: a review. Poultry Science, 92, 64–83.
  • Wood, S.M., Gleadle, J.M., Pugh, C.W., Hankinson, O. & Ratcliffe, P.J. (1996). The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNT-deficient cells. The Journal of Biological Chemistry, 271, 15117–15123.
  • Xing, Y., Zheng, X., Li, G., Liao, L., Cao, W., Xing, H., Shen, T., Sun, L., Yang, B. & Zhu, D. (2015). MicroRNA-30c contributes to the development of hypoxia pulmonary hypertension by inhibiting platelet-derived growth factor receptor β expression. The International Journal of Biochemistry & Cell Biology, 64, 155–166.
  • Xu, W., Comhair, S.A.A., Chen, R., Hu, B., Hou, Y., Zhou, Y., Mavrakis, L.A., Janocha, A.J., Li, L., Zhang, D., Willard, B.B., Asosingh, K., Cheng, F. & Erzurum, S.C. (2019). Integrative proteomics and phosphoproteomics in pulmonary arterial hypertension. Scientific Reports, 9, 18623.
  • Xu, W. & Erzurum, S.C. (2011). Endothelial cell energy metabolism, proliferation, and apoptosis in pulmonary hypertension. Comprehensive Physiology, 1, 357–372.
  • Xu, W., Koeck, T., Lara, A.R., Neumann, D., DiFilippo, F.P., Koo, M., Janocha, A.J., Masri, F.A., Arroliga, A.C., Jennings, C., Dweik, R.A., Tuder, R.M., Stuehr, D.J. & Erzurum, S.C. (2007). Alterations of cellular bioenergetics in pulmonary artery endothelial cells. Proceedings of the National Academy of Sciences of the United States of America, 104, 1342–1347.
  • Yang, F., Cao, H., Xiao, Q., Guo, X., Zhuang, Y., Zhang, C., Wang, T., Lin, H., Song, Y., Hu, G. & Liu, P. (2016). Transcriptome analysis and gene identification in the pulmonary artery of broilers with ascites syndrome. PLoS One, 11, e0156045.
  • Yang, Y., Qiao, J., Wu, Z., Chen, Y., Gao, M., Ou, D. & Wang, H. (2005). Endothelin-1 receptor antagonist BQ123 prevents pulmonary artery hypertension induced by low ambient temperature in broilers. Biological & Pharmaceutical Bulletin, 28, 2201–2205.
  • You, L., Wu, W., Wang, X., Fang, L., Adam, V., Nepovimova, E., Wu, Q. & Kuca, K. (2021). The role of hypoxia-inducible factor 1 in tumor immune evasion. Medicinal Research Reviews, 41, 1622–1643.
  • Yu, A.Y., Frid, M.G., Shimoda, L.A., Wiener, C.M., Stenmark, K. & Semenza, G.L. (1998). Temporal, spatial, and oxygen-regulated expression of hypoxia-inducible factor-1 in the lung. The American Journal of Physiology, 275, L818–L826.
  • Yu, A.Y., Shimoda, L.A., Iyer, N.V., Huso, D.L., Sun, X., McWilliams, R., Beaty, T., Sham, J.S., Wiener, C.M., Sylvester, J.T. & Semenza, G.L. (1999). Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1alpha. The Journal of Clinical Investigation, 103, 691–696.
  • Zeidan, E.M., Hossain, M.A., El-Daly, M., Abourehab, M.A.S., Khalifa, M.M.A. & Taye, A. (2022). Mitochondrial regulation of the hypoxia-inducible factor in the development of pulmonary hypertension. Journal of Clinical Medicine, 11.
  • Zhang, J., Feng, X., Zhao, L., Wang, W., Gao, M., Wu, B. & Qiao, J. (2013). Expression of hypoxia-inducible factor 1α mRNA in hearts and lungs of broiler chickens with ascites syndrome induced by excess salt in drinking water. Poultry Science, 92, 2044–2052.
  • Zhang, Y., Hernandez, M., Gower, J., Winicki, N., Morataya, X., Alvarez, S., Yuan, J.X., Shyy, J. & Thistlethwaite, P.A. (2022). JAGGED-NOTCH3 signaling in vascular remodeling in pulmonary arterial hypertension. Science Translational Medicine, 14, eabl5471.
  • Zhu, J., Zhao, L., Hu, Y., Cui, G., Luo, A., Bao, C., Han, Y., Zhou, T., Lu, W., Wang, J., Black, S.M. & Tang, H. (2021). Hypoxia-inducible Factor 2-alpha mediated gene sets differentiate pulmonary arterial hypertension. Frontiers in Cell and Developmental Biology, 9, 701247.

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