Critical role of VGLL4 in the regulation of chronic normobaric hypoxia-induced pulmonary hypertension in mice.
Animals
Cell Proliferation
Cells, Cultured
Chronic Disease
Hypertension, Pulmonary
/ metabolism
Lung
/ metabolism
Male
Mice
Mice, Inbred C57BL
Muscle, Smooth, Vascular
/ metabolism
Myocytes, Smooth Muscle
Pulmonary Artery
/ metabolism
STAT3 Transcription Factor
/ metabolism
Transcription Factors
/ physiology
Vascular Remodeling
STAT3
VGLL4
hypoxia
pulmonary hypertension
vascular remodeling
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
12
07
2021
received:
04
12
2020
accepted:
15
07
2021
entrez:
27
7
2021
pubmed:
28
7
2021
medline:
5
8
2021
Statut:
ppublish
Résumé
Pulmonary hypertension (PH), a rare but deadly cardiopulmonary disorder, is characterized by extensive remodeling of pulmonary arteries resulting from enhancement of pulmonary artery smooth muscle cell proliferation and suppressed apoptosis; however, the underlying pathophysiological mechanisms remain largely unknown. Recently, epigenetics has gained increasing prominence in the development of PH. We aimed to investigate the role of vestigial-like family member 4 (VGLL4) in chronic normobaric hypoxia (CNH)-induced PH and to address whether it is associated with epigenetic regulation. The rodent model of PH was established by CNH treatment (10% O
Identifiants
pubmed: 34314061
doi: 10.1096/fj.202002650RR
doi:
Substances chimiques
STAT3 Transcription Factor
0
Stat3 protein, mouse
0
Transcription Factors
0
VGLL4 protein, mouse
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21822Subventions
Organisme : Zhejiang Provincial Natural Science Foundation of China
ID : LY20H010001
Organisme : Zhejiang Provincial Natural Science Foundation of China
ID : LY18H010007
Organisme : Zhejiang Provincial Natural Science Foundation of China
ID : LY17H010007
Organisme : National Natural Science Foundation of China
ID : 81900403
Organisme : National Natural Science Foundation of China
ID : 31900685
Informations de copyright
© 2021 Federation of American Societies for Experimental Biology.
Références
Badesch DB, Champion HC, Sanchez MA, et al. Diagnosis and assessment of pulmonary arterial hypertension. J Am Coll Cardiol. 2009;54:S55-S66.
Morrell NW, Adnot S, Archer SL, et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol. 2009;54:S20-S31.
Stenmark KR, Frid MG, Graham BB, Tuder RM. Dynamic and diverse changes in the functional properties of vascular smooth muscle cells in pulmonary hypertension. Cardiovasc Res. 2018;114:551-564.
Gamen E, Seeger W, Pullamsetti SS. The emerging role of epigenetics in pulmonary hypertension. Eur Respir J. 2016;48:903-917.
Chelladurai P, Boucherat O, Stenmark K, et al. Targeting histone acetylation in pulmonary hypertension and right ventricular hypertrophy. Br J Pharmacol. 2021;178:54-71.
Zhao L, Chen CN, Hajji N, et al. Histone deacetylation inhibition in pulmonary hypertension: therapeutic potential of valproic acid and suberoylanilide hydroxamic acid. Circulation. 2012;126:455-467.
Chen F, Li X, Aquadro E, et al. Inhibition of histone deacetylase reduces transcription of NADPH oxidases and ROS production and ameliorates pulmonary arterial hypertension. Free Radic Biol Med. 2016;99:167-178.
Wang Y, Huang X, Leng D, et al. DNA methylation signatures of pulmonary arterial smooth muscle cells in chronic thromboembolic pulmonary hypertension. Physiol Genomics. 2018;50:313-322.
Shen H, Zhang J, Wang C, et al. MDM2-mediated ubiquitination of angiotensin-converting enzyme 2 contributes to the development of pulmonary arterial hypertension. Circulation. 2020;142:1190-1204.
Ghosh S, Gupta M, Xu W, et al. Phosphorylation inactivation of endothelial nitric oxide synthesis in pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol. 2016;310:L1199-L1205.
Samanta S, Rajasingh S, Cao T, Dawn B, Rajasingh J. Epigenetic dysfunctional diseases and therapy for infection and inflammation. Biochim Biophys Acta Mol Basis Dis. 2017;1863:518-528.
Totaro A, Panciera T, Piccolo S. YAP/TAZ upstream signals and downstream responses. Nat Cell Biol. 2018;20:888-899.
Kim J, Kim YH, Kim J, et al. YAP/TAZ regulates sprouting angiogenesis and vascular barrier maturation. J Clin Invest. 2017;127:3441-3461.
Neto F, Klaus-Bergmann A, Ong YT, et al. YAP and TAZ regulate adherens junction dynamics and endothelial cell distribution during vascular development. Elife. 2018;7:e31037.
Fang L, Teng H, Wang Y, et al. SET1A-mediated mono-methylation at K342 regulates YAP activation by blocking its nuclear export and promotes tumorigenesis. Cancer Cell. 2018;34(103-118):e109.
Yuan WC, Pepe-Mooney B, Galli GG, et al. NUAK2 is a critical YAP target in liver cancer. Nat Commun. 2018;9:4834.
Dieffenbach PB, Haeger CM, Coronata AMF, et al. Arterial stiffness induces remodeling phenotypes in pulmonary artery smooth muscle cells via YAP/TAZ-mediated repression of cyclooxygenase-2. Am J Physiol Lung Cell Mol Physiol. 2017;313:L628-L647.
Bertero T, Oldham WM, Cottrill KA, et al. Vascular stiffness mechanoactivates YAP/TAZ-dependent glutaminolysis to drive pulmonary hypertension. J Clin Invest. 2016;126:3313-3335.
Bertero T, Cottrill K, Lu YU, et al. Matrix remodeling promotes pulmonary hypertension through feedback mechanoactivation of the YAP/TAZ-miR-130/301 circuit. Cell Rep. 2015;13:1016-1032.
He J, Bao Q, Yan M, et al. The role of Hippo/yes-associated protein signalling in vascular remodelling associated with cardiovascular disease. Br J Pharmacol. 2018;175:1354-1361.
Wu A, Wu Q, Deng Y, et al. Loss of VGLL4 suppresses tumor PD-L1 expression and immune evasion. EMBO J. 2019;38:e99506.
Jiao S, Li C, Hao Q, et al. VGLL4 targets a TCF4-TEAD4 complex to coregulate Wnt and Hippo signalling in colorectal cancer. Nat Commun. 2017;8:14058.
Zhang W, Gao Y, Li P, et al. VGLL4 functions as a new tumor suppressor in lung cancer by negatively regulating the YAP-TEAD transcriptional complex. Cell Res. 2014;24:331-343.
Lin Z, Guo H, Cao Y, et al. Acetylation of VGLL4 regulates Hippo-YAP signaling and postnatal cardiac growth. Dev Cell. 2016;39:466-479.
Yu W, Ma X, Xu J, et al. VGLL4 plays a critical role in heart valve development and homeostasis. PLoS Genet. 2019;15:e1007977.
Li N, Yu N, Wang J, et al. miR-222/VGLL4/YAP-TEAD1 regulatory loop promotes proliferation and invasion of gastric cancer cells. Am J Cancer Res. 2015;5:1158-1168.
Zhang E, Shen B, Mu X, et al. Ubiquitin-specific protease 11 (USP11) functions as a tumor suppressor through deubiquitinating and stabilizing VGLL4 protein. Am J Cancer Res. 2016;6:2901-2909.
Rai PR, Cool CD, King JA, et al. The cancer paradigm of severe pulmonary arterial hypertension. Am J Respir Crit Care Med. 2008;178:558-564.
Guignabert C, Tu L, Le Hiress M, et al. Pathogenesis of pulmonary arterial hypertension: lessons from cancer. Eur Respir Rev. 2013;22:543-551.
Boucherat O, Vitry G, Trinh I, Paulin R, Provencher S, Bonnet S. The cancer theory of pulmonary arterial hypertension. Pulm Circ. 2017;7:285-299.
Fan J, Fan X, Guang H, et al. Upregulation of miR-335-3p by NF-kappaB transcriptional regulation contributes to the induction of pulmonary arterial hypertension via APJ during hypoxia. Int J Biol Sci. 2020;16:515-528.
Fan J, Guang H, Zhang H, et al. SIRT1 mediates Apelin-13 in ameliorating chronic normobaric hypoxia-induced anxiety-like behavior by suppressing NF-kappaB pathway in mice hippocampus. Neuroscience. 2018;381:22-34.
Fan J, Fan X, Li Y, et al. Chronic normobaric hypoxia induces pulmonary hypertension in rats: role of NF-kappaB. High Alt Med Biol. 2016;17:43-49.
Mao SZ, Fan XF, Xue F, et al. Intermedin modulates hypoxic pulmonary vascular remodeling by inhibiting pulmonary artery smooth muscle cell proliferation. Pulm Pharmacol Ther. 2014;27:1-9.
Tian Q, Fan X, Ma J, et al. Resveratrol ameliorates lipopolysaccharide-induced anxiety-like behavior by attenuating YAP-mediated neuro-inflammation and promoting hippocampal autophagy in mice. Toxicol Appl Pharmacol. 2020;408:115261.
Chen J, Zhou Y, Mueller-Steiner S, et al. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J Biol Chem. 2005;280:40364-40374.
Zhang F, Wang S, Gan L, et al. Protective effects and mechanisms of sirtuins in the nervous system. Prog Neurogibol. 2011;95:373-395.
Yao H, Chung S, Hwang JW, et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest. 2012;122:2032-2045.
Mao B, Hu F, Cheng J, et al. SIRT1 regulates YAP2-mediated cell proliferation and chemoresistance in hepatocellular carcinoma. Oncogene. 2014;33:1468-1474.
Ding M, Lei J, Qu Y, et al. Calorie restriction attenuates monocrotaline-induced pulmonary arterial hypertension in rats. J Cardiovasc Pharmacol. 2015;65:562-570.
Zurlo G, Piquereau J, Moulin M, et al. Sirtuin 1 regulates pulmonary artery smooth muscle cell proliferation: role in pulmonary arterial hypertension. J Hypertens. 2018;36:1164-1177.
Csiszar A, Labinskyy N, Olson S, et al. Resveratrol prevents monocrotaline-induced pulmonary hypertension in rats. Hypertension. 2009;54:668-675.
Paffett ML, Lucas SN, Campen MJ. Resveratrol reverses monocrotaline-induced pulmonary vascular and cardiac dysfunction: a potential role for atrogin-1 in smooth muscle. Vasc Pharmacol. 2012;56:64-73.
Chen B, Xue J, Meng X, Slutzky JL, Calvert AE, Chicoine LG. Resveratrol prevents hypoxia-induced arginase II expression and proliferation of human pulmonary artery smooth muscle cells via Akt-dependent signaling. Am J Physiol Lung Cell Mol Physiol. 2014;307:L317-L325.
Noman MZ, Buart S, Van Pelt J, et al. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol. 2009;182:3510-3521.
Cai Z, Li J, Zhuang Q, et al. MiR-125a-5p ameliorates monocrotaline-induced pulmonary arterial hypertension by targeting the TGF-beta1 and IL-6/STAT3 signaling pathways. Exp Mol Med. 2018;50:45.
Courboulin A, Paulin R, Giguere NJ, et al. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med. 2011;208:535-548.
Paulin R, Courboulin A, Meloche J, et al. Signal transducers and activators of transcription-3/pim1 axis plays a critical role in the pathogenesis of human pulmonary arterial hypertension. Circulation. 2011;123:1205-1215.
Courboulin A, Barrier M, Perreault T, et al. Plumbagin reverses proliferation and resistance to apoptosis in experimental PAH. Eur Respir J. 2012;40:618-629.
Song H, Luo Q, Deng X, et al. VGLL4 interacts with STAT3 to function as a tumor suppressor in triple-negative breast cancer. Exp Mol Med. 2019;51:1-13.