Liquid plasma promotes angiogenesis through upregulation of endothelial nitric oxide synthase-induced extracellular matrix metabolism: potential applications of liquid plasma for vascular injuries.


Journal

Cell communication and signaling : CCS
ISSN: 1478-811X
Titre abrégé: Cell Commun Signal
Pays: England
ID NLM: 101170464

Informations de publication

Date de publication:
19 02 2024
Historique:
received: 04 07 2023
accepted: 25 11 2023
medline: 21 2 2024
pubmed: 20 2 2024
entrez: 19 2 2024
Statut: epublish

Résumé

Applications of nonthermal plasma have expanded beyond the biomedical field to include antibacterial, anti-inflammatory, wound healing, and tissue regeneration. Plasma enhances epithelial cell repair; however, the potential damage to deep tissues and vascular structures remains under investigation. This study assessed whether liquid plasma (LP) increased nitric oxide (NO) production in human umbilical vein endothelial cells by modulating endothelial NO synthase (eNOS) phosphorylation and potential signaling pathways. First, we developed a liquid plasma product and confirmed the angiogenic effect of LP using the Matrigel plug assay. We found that the NO content increased in plasma-treated water. NO in plasma-treated water promoted cell migration and angiogenesis in scratch and tube formation assays via vascular endothelial growth factor mRNA expression. In addition to endothelial cell proliferation and migration, LP influenced extracellular matrix metabolism and matrix metalloproteinase activity. These effects were abolished by treatment with NG-L-monomethyl arginine, a specific inhibitor of NO synthase. Furthermore, we investigated the signaling pathways mediating the phosphorylation and activation of eNOS in LP-treated cells and the role of LKB1-adenosine monophosphate-activated protein kinase in signaling. Downregulation of adenosine monophosphate-activated protein kinase by siRNA partially inhibited LP-induced eNOS phosphorylation, angiogenesis, and migration. The present study suggests that LP treatment may be a novel strategy for promoting angiogenesis in vascular damage. Video Abstract.

Sections du résumé

BACKGROUND
Applications of nonthermal plasma have expanded beyond the biomedical field to include antibacterial, anti-inflammatory, wound healing, and tissue regeneration. Plasma enhances epithelial cell repair; however, the potential damage to deep tissues and vascular structures remains under investigation.
RESULT
This study assessed whether liquid plasma (LP) increased nitric oxide (NO) production in human umbilical vein endothelial cells by modulating endothelial NO synthase (eNOS) phosphorylation and potential signaling pathways. First, we developed a liquid plasma product and confirmed the angiogenic effect of LP using the Matrigel plug assay. We found that the NO content increased in plasma-treated water. NO in plasma-treated water promoted cell migration and angiogenesis in scratch and tube formation assays via vascular endothelial growth factor mRNA expression. In addition to endothelial cell proliferation and migration, LP influenced extracellular matrix metabolism and matrix metalloproteinase activity. These effects were abolished by treatment with NG-L-monomethyl arginine, a specific inhibitor of NO synthase. Furthermore, we investigated the signaling pathways mediating the phosphorylation and activation of eNOS in LP-treated cells and the role of LKB1-adenosine monophosphate-activated protein kinase in signaling. Downregulation of adenosine monophosphate-activated protein kinase by siRNA partially inhibited LP-induced eNOS phosphorylation, angiogenesis, and migration.
CONCLUSION
The present study suggests that LP treatment may be a novel strategy for promoting angiogenesis in vascular damage. Video Abstract.

Identifiants

pubmed: 38374138
doi: 10.1186/s12964-023-01412-w
pii: 10.1186/s12964-023-01412-w
pmc: PMC10875778
doi:

Substances chimiques

Adenosine Monophosphate 415SHH325A
Nitric Oxide 31C4KY9ESH
Nitric Oxide Synthase EC 1.14.13.39
Nitric Oxide Synthase Type III EC 1.14.13.39
Protein Kinases EC 2.7.-
Vascular Endothelial Growth Factor A 0

Types de publication

Video-Audio Media Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

138

Informations de copyright

© 2024. The Author(s).

Références

Cardiovasc Res. 1993 Dec;27(12):2282-3
pubmed: 8141908
Kardiol Pol. 2020 Jan 24;78(1):51-58
pubmed: 31746314
Surgery. 2004 Apr;135(4):437-46
pubmed: 15041968
PLoS One. 2017 Nov 16;12(11):e0187978
pubmed: 29145520
Free Radic Biol Med. 2014 Feb;67:115-30
pubmed: 24216474
Chemosphere. 2020 Mar;243:125377
pubmed: 31760291
PLoS One. 2014 Mar 25;9(3):e92198
pubmed: 24667444
Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6448-53
pubmed: 8692835
Exp Biol Med (Maywood). 2019 Jul;244(10):824-833
pubmed: 31088117
Free Radic Biol Med. 2020 May 20;152:43-51
pubmed: 32151744
PLoS One. 2017 Jun 29;12(6):e0180183
pubmed: 28662202
Zhen Ci Yan Jiu. 2020 Feb 25;45(2):99-104
pubmed: 32144918
Oxid Med Cell Longev. 2020 Sep 7;2020:7151946
pubmed: 32963699
Dev Biol. 2007 Aug 15;308(2):474-84
pubmed: 17604018
J Cell Sci. 2013 Dec 15;126(Pt 24):5541-52
pubmed: 24046447
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):355-60
pubmed: 11134509
Am J Physiol Cell Physiol. 2010 Apr;298(4):C847-56
pubmed: 20089932
Am J Physiol Gastrointest Liver Physiol. 2001 Nov;281(5):G1151-7
pubmed: 11668023
Nat Rev Mol Cell Biol. 2023 Nov;24(11):816-834
pubmed: 37491579
Biochem Biophys Res Commun. 2000 Aug 11;274(3):689-96
pubmed: 10924337
Biol Reprod. 2006 Feb;74(2):375-82
pubmed: 16251502
Oxid Med Cell Longev. 2019 Oct 31;2019:8730816
pubmed: 31781355
Cell Death Dis. 2014 Feb 13;5:e1056
pubmed: 24525732
J Immunol. 1997 Mar 1;158(5):2375-81
pubmed: 9036987
Wounds. 2020 Jun;32(6):164-173
pubmed: 32804658
Nitric Oxide. 2016 May 1;55-56:45-53
pubmed: 26989010
Amino Acids. 2020 Apr;52(4):639-648
pubmed: 32303905
Proc Natl Acad Sci U S A. 2004 Jun 1;101(22):8497-502
pubmed: 15173604
Sci Rep. 2018 Feb 2;8(1):2277
pubmed: 29396442
Sci Rep. 2016 Jun 28;6:28829
pubmed: 27349181
Dev Cell. 2005 Aug;9(2):185-96
pubmed: 16054026
Circ Res. 2000 Feb 18;86(3):347-54
pubmed: 10679488
Arterioscler Thromb Vasc Biol. 1998 May;18(5):717-22
pubmed: 9598829
Cardiovasc Res. 2000 Oct;48(1):168-77
pubmed: 11033119
Biochem J. 2000 Sep 15;350 Pt 3:709-16
pubmed: 10970783
Mol Med Rep. 2017 Feb;15(2):908-914
pubmed: 28000882
Front Physiol. 2022 Aug 17;13:981161
pubmed: 36060683
J Surg Res. 1996 Jun;63(1):237-40
pubmed: 8661204
Sci Rep. 2016 Jul 29;6:30687
pubmed: 27469024
Biochim Biophys Acta. 2011 Feb;1813(2):322-31
pubmed: 21145922
Liver Transpl Surg. 1997 Jan;3(1):54-5
pubmed: 9377759
J Hum Hypertens. 2021 Apr;35(4):325-333
pubmed: 32382032
Immunol Rev. 2012 Sep;249(1):59-71
pubmed: 22889215
Nat Cell Biol. 2004 Feb;6(2):154-61
pubmed: 14743221
Basic Res Cardiol. 2015 May;110(3):21
pubmed: 25804308
Vascul Pharmacol. 2016 Dec;87:159-171
pubmed: 27634591
Diabet Med. 2010 Oct;27(10):1097-106
pubmed: 20854376
Australas Phys Eng Sci Med. 2018 Dec;41(4):905-917
pubmed: 30276627
Electromagn Biol Med. 2007;26(2):99-106
pubmed: 17613037
Sci Rep. 2018 Sep 13;8(1):13754
pubmed: 30213992
J Cell Biol. 2004 May 10;165(3):371-81
pubmed: 15138291
J Histochem Cytochem. 2006 Feb;54(2):151-9
pubmed: 16009963
Biomed Pharmacother. 2020 Nov;131:110750
pubmed: 32942160
Am J Physiol Gastrointest Liver Physiol. 2013 Jul 15;305(2):G163-71
pubmed: 23639812
Circulation. 1997 Jul 15;96(2):379-82
pubmed: 9244195
Curr Opin Clin Nutr Metab Care. 2000 May;3(3):197-204
pubmed: 10871235
Am J Physiol Heart Circ Physiol. 2001 Nov;281(5):H2226-32
pubmed: 11668087
Phytother Res. 2010 Jun;24(6):934-40
pubmed: 19960515
Clin Sci (Lond). 2009 Apr;116(8):607-20
pubmed: 19275766
Proc Natl Acad Sci U S A. 2019 Oct 1;116(40):20210-20217
pubmed: 31527268
Acta Pharmacol Sin. 2005 Mar;26(3):259-64
pubmed: 15715920
Front Pharmacol. 2021 May 12;12:671563
pubmed: 34054544
Ophthalmic Res. 2012;48(4):165-70
pubmed: 22710949
Exp Dermatol. 2017 Feb;26(2):163-170
pubmed: 27673439
Ann N Y Acad Sci. 2002 May;962:360-71
pubmed: 12076987
Biol Direct. 2023 Aug 28;18(1):52
pubmed: 37635249
Adv Wound Care (New Rochelle). 2014 Oct 1;3(10):647-661
pubmed: 25302139
Endocrinology. 2001 Oct;142(10):4288-94
pubmed: 11564686
Clin Sci (Lond). 2001 Apr;100(4):387-93
pubmed: 11256976
Atherosclerosis. 1999 May;144(1):49-57
pubmed: 10381277
Microsurgery. 2005;25(5):442-51
pubmed: 16044466

Auteurs

Sung Un Kang (SU)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Haeng Jun Kim (HJ)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Sukhwal Ma (S)

Medical Accelerator Research Team, Korea Institute of Radiological & Medical Sciences (KIRAMS), 75 Nowonro, Nowon-gu, Seoul, 01812, South Korea.

Doo-Yi Oh (DY)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Jeon Yeob Jang (JY)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Chorong Seo (C)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Yun Sang Lee (YS)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea.

Chul-Ho Kim (CH)

Department of Otolaryngology, Department of Molecular Science and Technology, Ajou University School of Medicine, 164, World cup-ro, Yeongtong-Gu, Suwon, 443-380, Republic of Korea. ostium@ajou.ac.kr.

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