Metabolic Reprogramming and Reliance in Human Skin Wound Healing

Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the sequential phases of inflammation, proliferation, and tissue remodeling. Although wound healing is a highly dynamic and energy-requiring process,...

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Published inJournal of Investigative Dermatology Vol. 143; no. 10; pp. 2039 - 2051.e10
Main Authors Manchanda, Mansi, Torres, Monica, Inuossa, Farydah, Bansal, Ritu, Kumar, Rahul, Hunt, Matthew, Wheelock, Craig E., Bachar-Wikstrom, Etty, Wikstrom, Jakob D.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.10.2023
Elsevier BV
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Online AccessGet full text
ISSN0022-202X
1523-1747
1523-1747
DOI10.1016/j.jid.2023.02.039

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Abstract Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the sequential phases of inflammation, proliferation, and tissue remodeling. Although wound healing is a highly dynamic and energy-requiring process, the role of metabolism remains largely unexplored. By combining transcriptomics and metabolomics of human skin biopsy samples, we mapped the core bioenergetic and metabolic changes in normal acute as well as chronic wounds in elderly subjects. We found upregulation of glycolysis, the tricarboxylic acid cycle, glutaminolysis, and β-oxidation in the later stages of acute wound healing and in chronic wounds. To ascertain the role of these metabolic pathways on wound healing, we targeted each pathway in a wound healing assay as well as in a human skin explant model using metabolic inhibitors and stimulants. Enhancement or inhibition of glycolysis and, to a lesser extent, glutaminolysis had a far greater impact on wound healing than similar manipulations of oxidative phosphorylation and fatty acid β-oxidation. These findings increase the understanding of wound metabolism and identify glycolysis and glutaminolysis as potential targets for therapeutic intervention.
AbstractList Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the sequential phases of inflammation, proliferation, and tissue remodeling. Although wound healing is a highly dynamic and energy-requiring process, the role of metabolism remains largely unexplored. By combining transcriptomics and metabolomics of human skin biopsy samples, we mapped the core bioenergetic and metabolic changes in normal acute as well as chronic wounds in elderly subjects. We found upregulation of glycolysis, the tricarboxylic acid cycle, glutaminolysis, and β-oxidation in the later stages of acute wound healing and in chronic wounds. To ascertain the role of these metabolic pathways on wound healing, we targeted each pathway in a wound healing assay as well as in a human skin explant model using metabolic inhibitors and stimulants. Enhancement or inhibition of glycolysis and, to a lesser extent, glutaminolysis had a far greater impact on wound healing than similar manipulations of oxidative phosphorylation and fatty acid β-oxidation. These findings increase the understanding of wound metabolism and identify glycolysis and glutaminolysis as potential targets for therapeutic intervention.
Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the sequential phases of inflammation, proliferation, and tissue remodeling. Although wound healing is a highly dynamic and energy-requiring process, the role of metabolism remains largely unexplored. By combining transcriptomics and metabolomics of human skin biopsy samples, we mapped the core bioenergetic and metabolic changes in normal acute as well as chronic wounds in elderly subjects. We found upregulation of glycolysis, the tricarboxylic acid cycle, glutaminolysis, and β-oxidation in the later stages of acute wound healing and in chronic wounds. To ascertain the role of these metabolic pathways on wound healing, we targeted each pathway in a wound healing assay as well as in a human skin explant model using metabolic inhibitors and stimulants. Enhancement or inhibition of glycolysis and, to a lesser extent, glutaminolysis had a far greater impact on wound healing than similar manipulations of oxidative phosphorylation and fatty acid β-oxidation. These findings increase the understanding of wound metabolism and identify glycolysis and glutaminolysis as potential targets for therapeutic intervention.Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the sequential phases of inflammation, proliferation, and tissue remodeling. Although wound healing is a highly dynamic and energy-requiring process, the role of metabolism remains largely unexplored. By combining transcriptomics and metabolomics of human skin biopsy samples, we mapped the core bioenergetic and metabolic changes in normal acute as well as chronic wounds in elderly subjects. We found upregulation of glycolysis, the tricarboxylic acid cycle, glutaminolysis, and β-oxidation in the later stages of acute wound healing and in chronic wounds. To ascertain the role of these metabolic pathways on wound healing, we targeted each pathway in a wound healing assay as well as in a human skin explant model using metabolic inhibitors and stimulants. Enhancement or inhibition of glycolysis and, to a lesser extent, glutaminolysis had a far greater impact on wound healing than similar manipulations of oxidative phosphorylation and fatty acid β-oxidation. These findings increase the understanding of wound metabolism and identify glycolysis and glutaminolysis as potential targets for therapeutic intervention.
Author Kumar, Rahul
Manchanda, Mansi
Hunt, Matthew
Wheelock, Craig E.
Torres, Monica
Bansal, Ritu
Wikstrom, Jakob D.
Bachar-Wikstrom, Etty
Inuossa, Farydah
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  orcidid: 0000-0002-8113-0653
  surname: Wheelock
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  organization: Research Division of Physiological Chemistry II, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
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  orcidid: 0000-0002-3283-6721
  surname: Bachar-Wikstrom
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  surname: Wikstrom
  fullname: Wikstrom, Jakob D.
  email: jakob.wikstrom@ki.se
  organization: Dermatology and Venereology Division, Department of Medicine (Solna), Karolinska Institutet, Stockholm, Sweden
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Cites_doi 10.1089/wound.2013.0520
10.1021/acs.jproteome.9b00460
10.1016/j.jdiacomp.2017.06.010
10.1111/jcmm.16013
10.1073/pnas.0805230105
10.1016/j.celrep.2020.02.091
10.1016/j.jpba.2017.01.018
10.1038/s41580-019-0123-5
10.1111/iwj.13525
10.1007/978-1-62703-505-7_14
10.1371/journal.pone.0121551
10.1111/iwj.12246
10.1016/0022-4804(70)90070-3
10.1007/s13671-016-0156-3
10.1074/jbc.RA117.000444
10.3791/56863-v
10.1371/journal.pone.0229545
10.1172/jci.insight.138949
10.3390/ijms21228435
10.3390/antiox7080098
10.1186/s12964-021-00717-y
10.1111/wrr.12688
10.1016/j.cels.2015.12.004
10.1016/j.jid.2018.05.029
10.1016/j.imbio.2010.06.007
10.1046/j.1524-475X.1996.40211.x
10.1126/scisignal.aav5918
10.1042/BJ20150645
10.1586/14737159.2014.927312
10.1194/jlr.M048207
10.1038/s41598-017-15876-7
10.1097/00003246-200004001-00007
10.1172/jci.insight.140598
10.1021/acs.analchem.9b04542
10.1073/pnas.1814097116
10.1126/science.aam7928
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References Bachar-Wikstrom, Manchanda, Bansal, Karlsson, Kelly-Pettersson, Sköldenberg (bib3) 2021; 18
Zhu, Thompson (bib38) 2019; 20
Liu, Du, St-Pierre, Bergholt, Autefage, Wang (bib20) 2020; 6
Cardoso, Favoreto, Oliveira, Vancim, Barban, Ferraz (bib7) 2011; 216
Eming, Wynn, Martin (bib9) 2017; 356
Guenin-Macé, Morel, Doisne, Schiavo, Boulet, Mayau (bib11) 2020; 5
Castellanos, Hernandez, Tomic-Canic, Jozic, Fernandez-Lima (bib8) 2020; 92
Hong, Hu, Esquivel, Liang, Rennert, McArdle (bib14) 2014; 3
Rodrigues, Obre, de Melo, Santos, Galina, Jasiulionis (bib26) 2016; 473
Alvarez, Castano-Tostado, Garcia-Gutierrez, Reynoso-Camacho, Elton-Puente, Barajas-Pozos (bib1) 2020; 15
Ashrafi, Xu, Muhamadali, White, Wilkinson, Hollywood (bib2) 2020; 15
Im, Hoopes (bib15) 1970; 10
Zhan, Yang, He, Wang, Tan, Zhou (bib36) 2015; 10
Soleimani, Hashemdokht, Bahmani, Taghizadeh, Memarzadeh, Asemi (bib27) 2017; 31
Bernard, Logsdon, Benavides, Sanders, Zhang, Darley-Usmar (bib4) 2018; 293
Henderson, Duffy, Stratton, Ford, O'Reilly (bib13) 2020; 24
Sumitra, Manikandan, Gayathri, Suguna (bib29) 2009; 2009
Wijesinghe, Brentnall, Mietla, Hoeferlin, Diegelmann, Boise (bib32) 2014; 55
Haensel, Jin, Sun, Cinco, Dragan, Nguyen (bib12) 2020; 30
Liberzon, Birger, Thorvaldsdóttir, Ghandi, Mesirov, Tamayo (bib18) 2015; 1
Goswami, Kandhare, Zanwar, Hegde, Bodhankar, Shinde (bib10) 2016; 13
Onida, Tan, Kafeza, Bergner, Shalhoub, Holmes (bib24) 2019; 18
Nasir, Paus, Ansell (bib23) 2019; 27
Botusan, Sunkari, Savu, Catrina, Grünler, Lindberg (bib5) 2008; 105
Trengove, Langton, Stacey (bib30) 1996; 4
Junka, Wojtowicz, Ząbek, Krasowski, Smutnicka, Bakalorz (bib17) 2017; 137
Lim, Rahim, Leo, Das, Lim, Uemura (bib19) 2018; 138
Ito, Ito, Ideta, Kanbe, Ninomiya, Shimizu (bib16) 2021; 19
MacKnight, Stephenson, Hoeferlin, Benusa, DeLigio, Maus (bib21) 2019; 12
Wijesinghe, Warncke, Diegelmann (bib33) 2016; 5
Zhang, Wang, Tracey (bib37) 2000; 28
Vinaik, Barayan, Auger, Abdullahi, Jeschke (bib31) 2020; 5
Yasukawa, Okuno, Yokomizo (bib34) 2020; 21
Mannello, Ligi, Canale, Raffetto (bib22) 2014; 14
Yu, Gao, Yang, Pei, Liu, Wang (bib35) 2017; 9
Cano Sanchez, Lancel, Boulanger, Neviere (bib6) 2018; 7
Raffetto, Ligi, Maniscalco, Khalil, Mannello (bib25) 2020; 10
Stojadinovic, Tomic-Canic (bib28) 2013; 1037
Alvarez (10.1016/j.jid.2023.02.039_bib1) 2020; 15
Ashrafi (10.1016/j.jid.2023.02.039_bib2) 2020; 15
Mannello (10.1016/j.jid.2023.02.039_bib22) 2014; 14
Goswami (10.1016/j.jid.2023.02.039_bib10) 2016; 13
Liberzon (10.1016/j.jid.2023.02.039_bib18) 2015; 1
Liu (10.1016/j.jid.2023.02.039_bib20) 2020; 6
Sumitra (10.1016/j.jid.2023.02.039_bib29) 2009; 2009
Nasir (10.1016/j.jid.2023.02.039_bib41) 2019; 27
Zhu (10.1016/j.jid.2023.02.039_bib38) 2019; 20
Bernard (10.1016/j.jid.2023.02.039_bib4) 2018; 293
Vinaik (10.1016/j.jid.2023.02.039_bib31) 2020; 5
MacKnight (10.1016/j.jid.2023.02.039_bib21) 2019; 12
Im (10.1016/j.jid.2023.02.039_bib15) 1970; 10
Botusan (10.1016/j.jid.2023.02.039_bib5) 2008; 105
Nasir (10.1016/j.jid.2023.02.039_bib23) 2019; 27
Johansen (10.1016/j.jid.2023.02.039_bib44) 2017
Stojadinovic (10.1016/j.jid.2023.02.039_bib28) 2013; 1037
Wijesinghe (10.1016/j.jid.2023.02.039_bib33) 2016; 5
Li (10.1016/j.jid.2023.02.039_bib43) 2019; 116
Henderson (10.1016/j.jid.2023.02.039_bib13) 2020; 24
Hong (10.1016/j.jid.2023.02.039_bib14) 2014; 3
Soleimani (10.1016/j.jid.2023.02.039_bib27) 2017; 31
Junka (10.1016/j.jid.2023.02.039_bib17) 2017; 137
Raffetto (10.1016/j.jid.2023.02.039_bib25) 2020; 10
Guenin-Macé (10.1016/j.jid.2023.02.039_bib11) 2020; 5
Cardoso (10.1016/j.jid.2023.02.039_bib7) 2011; 216
Trengove (10.1016/j.jid.2023.02.039_bib30) 1996; 4
Yeh (10.1016/j.jid.2023.02.039_bib45) 2017; 7
Zhan (10.1016/j.jid.2023.02.039_bib36) 2015; 10
Bachar-Wikstrom (10.1016/j.jid.2023.02.039_bib3) 2021; 18
Lim (10.1016/j.jid.2023.02.039_bib19) 2018; 138
Cano Sanchez (10.1016/j.jid.2023.02.039_bib6) 2018; 7
Haensel (10.1016/j.jid.2023.02.039_bib12) 2020; 30
Zhang (10.1016/j.jid.2023.02.039_bib37) 2000; 28
Yu (10.1016/j.jid.2023.02.039_bib35) 2017; 9
Onida (10.1016/j.jid.2023.02.039_bib24) 2019; 18
Castellanos (10.1016/j.jid.2023.02.039_bib8) 2020; 92
Ito (10.1016/j.jid.2023.02.039_bib16) 2021; 19
Wijesinghe (10.1016/j.jid.2023.02.039_bib32) 2014; 55
Takashima (10.1016/j.jid.2023.02.039_bib46) 2001
Bachar-Wikstrom (10.1016/j.jid.2023.02.039_bib39) 2021; 18
Stojadinovic (10.1016/j.jid.2023.02.039_bib42) 2013; 1037
Eming (10.1016/j.jid.2023.02.039_bib9) 2017; 356
Rodrigues (10.1016/j.jid.2023.02.039_bib26) 2016; 473
Liberzon (10.1016/j.jid.2023.02.039_bib40) 2015; 1
Yasukawa (10.1016/j.jid.2023.02.039_bib34) 2020; 21
References_xml – volume: 2009
  start-page: 1
  year: 2009
  end-page: 6
  ident: bib29
  article-title: Influence of honey on energy metabolism during wound healing in rats
  publication-title: Sch Res Exch
– volume: 18
  start-page: 49
  year: 2021
  end-page: 61
  ident: bib3
  article-title: Endoplasmic reticulum stress in human chronic wound healing: rescue by 4-phenylbutyrate
  publication-title: Int Wound J
– volume: 293
  start-page: 1218
  year: 2018
  end-page: 1228
  ident: bib4
  article-title: Glutaminolysis is required for transforming growth factor-beta1-induced myofibroblast differentiation and activation
  publication-title: J Biol Chem
– volume: 31
  start-page: 1394
  year: 2017
  end-page: 1400
  ident: bib27
  article-title: Clinical and metabolic response to flaxseed oil omega-3 fatty acids supplementation in patients with diabetic foot ulcer: A randomized, double-blind, placebo-controlled trial
  publication-title: J Diabetes Complications
– volume: 10
  year: 2015
  ident: bib36
  article-title: Nitric oxide enhances keratinocyte cell migration by regulating Rho GTPase via cGMP-PKG signalling
  publication-title: PLoS One
– volume: 27
  start-page: 126
  year: 2019
  end-page: 133
  ident: bib23
  article-title: Fluorescent cell tracer dye permits real-time assessment of re-epithelialization in a serum-free ex vivo human skin wound assay
  publication-title: Wound Repair Regen
– volume: 138
  start-page: 2653
  year: 2018
  end-page: 2665
  ident: bib19
  article-title: Polyamine regulator AMD1 promotes cell migration in epidermal wound healing
  publication-title: J Invest Dermatol
– volume: 137
  start-page: 13
  year: 2017
  end-page: 22
  ident: bib17
  article-title: Metabolic profiles of exudates from chronic leg ulcerations
  publication-title: J Pharm Biomed Anal
– volume: 9
  start-page: 4682
  year: 2017
  end-page: 4693
  ident: bib35
  article-title: Topical insulin accelerates cutaneous wound healing in insulin-resistant diabetic rats
  publication-title: Am J Transl Res
– volume: 14
  start-page: 737
  year: 2014
  end-page: 762
  ident: bib22
  article-title: Omics profiles in chronic venous ulcer wound fluid: innovative applications for translational medicine
  publication-title: Expert Rev Mol Diagn
– volume: 19
  start-page: 36
  year: 2021
  ident: bib16
  article-title: Systemic and topical administration of spermidine accelerates skin wound healing
  publication-title: Cell Commun Signal
– volume: 30
  start-page: 3932
  year: 2020
  end-page: 3947.e6
  ident: bib12
  article-title: Defining epidermal basal cell states during skin homeostasis and wound healing using single-cell transcriptomics
  publication-title: Cell Rep
– volume: 4
  start-page: 234
  year: 1996
  end-page: 239
  ident: bib30
  article-title: Biochemical analysis of wound fluid from nonhealing and healing chronic leg ulcers
  publication-title: Wound Repair Regen
– volume: 105
  start-page: 19426
  year: 2008
  end-page: 19431
  ident: bib5
  article-title: Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice
  publication-title: Proc Natl Acad Sci USA
– volume: 5
  year: 2020
  ident: bib31
  article-title: Regulation of glycolysis and the Warburg effect in wound healing
  publication-title: JCI Insight
– volume: 92
  start-page: 1386
  year: 2020
  end-page: 1394
  ident: bib8
  article-title: Multimodal, in situ imaging of ex vivo human skin reveals decrease of cholesterol sulfate in the neoepithelium during acute wound healing
  publication-title: Anal Chem
– volume: 356
  start-page: 1026
  year: 2017
  end-page: 1030
  ident: bib9
  article-title: Inflammation and metabolism in tissue repair and regeneration
  publication-title: Science
– volume: 15
  year: 2020
  ident: bib1
  article-title: Non-targeted metabolomic analysis reveals serum phospholipid alterations in patients with early stages of diabetic foot ulcer
  publication-title: Biomark Insights
– volume: 20
  start-page: 436
  year: 2019
  end-page: 450
  ident: bib38
  article-title: Metabolic regulation of cell growth and proliferation
  publication-title: Nat Rev Mol Cell Biol
– volume: 55
  start-page: 1298
  year: 2014
  end-page: 1309
  ident: bib32
  article-title: Ceramide kinase is required for a normal eicosanoid response and the subsequent orderly migration of fibroblasts
  publication-title: J Lipid Res
– volume: 15
  year: 2020
  ident: bib2
  article-title: A microbiome and metabolomic signature of phases of cutaneous healing identified by profiling sequential acute wounds of human skin: an exploratory study
  publication-title: PLoS One
– volume: 5
  year: 2020
  ident: bib11
  article-title: Dysregulation of tryptophan catabolism at the host-skin microbiota interface in hidradenitis suppurativa
  publication-title: JCI Insight
– volume: 13
  start-page: 116
  year: 2016
  end-page: 124
  ident: bib10
  article-title: Oral L-glutamine administration attenuated cutaneous wound healing in Wistar rats
  publication-title: Int Wound J
– volume: 12
  year: 2019
  ident: bib21
  article-title: The interaction of ceramide 1-phosphate with group IVA cytosolic phospholipase A2 coordinates acute wound healing and repair
  publication-title: Sci Signal
– volume: 21
  start-page: 8435
  year: 2020
  ident: bib34
  article-title: Eicosanoids in skin wound healing
  publication-title: Int J Mol Sci
– volume: 7
  start-page: 98
  year: 2018
  ident: bib6
  article-title: Targeting oxidative stress and mitochondrial dysfunction in the treatment of impaired wound healing: A systematic review
  publication-title: Antioxidants (Basel)
– volume: 473
  start-page: 703
  year: 2016
  end-page: 715
  ident: bib26
  article-title: Enhanced OXPHOS, glutaminolysis and beta-oxidation constitute the metastatic phenotype of melanoma cells
  publication-title: Biochem J
– volume: 3
  start-page: 390
  year: 2014
  end-page: 399
  ident: bib14
  article-title: The role of hypoxia-inducible factor in wound healing
  publication-title: Adv Wound Care (New Rochelle)
– volume: 10
  start-page: 29
  year: 2020
  ident: bib25
  article-title: Why venous leg ulcers have difficulty healing: overview on pathophysiology, clinical consequences, and treatment
  publication-title: J Clin Med
– volume: 5
  start-page: 244
  year: 2016
  end-page: 251
  ident: bib33
  article-title: Human as the ultimate wound healing model: strategies for studies investigating the dermal lipidome
  publication-title: Curr Dermatol Rep
– volume: 24
  start-page: 14026
  year: 2020
  end-page: 14038
  ident: bib13
  article-title: Metabolic reprogramming of glycolysis and glutamine metabolism are key events in myofibroblast transition in systemic sclerosis pathogenesis
  publication-title: J Cell Mol Med
– volume: 1
  start-page: 417
  year: 2015
  end-page: 425
  ident: bib18
  article-title: The Molecular Signatures Database (MSigDB) hallmark gene set collection
  publication-title: Cell Syst
– volume: 216
  start-page: 409
  year: 2011
  end-page: 415
  ident: bib7
  article-title: Oleic acid modulation of the immune response in wound healing: a new approach for skin repair
  publication-title: Immunobiology
– volume: 10
  start-page: 459
  year: 1970
  end-page: 464
  ident: bib15
  article-title: Energy metabolism in healing skin wounds
  publication-title: J Surg Res
– volume: 18
  start-page: 3809
  year: 2019
  end-page: 3820
  ident: bib24
  article-title: Metabolic phenotyping in venous disease: the need for standardization
  publication-title: J Proteome Res
– volume: 1037
  start-page: 255
  year: 2013
  end-page: 264
  ident: bib28
  article-title: Human ex vivo wound healing model
  publication-title: Methods Mol Biol
– volume: 28
  start-page: N60
  year: 2000
  end-page: N66
  ident: bib37
  article-title: Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story
  publication-title: Crit Care Med
– volume: 6
  year: 2020
  ident: bib20
  article-title: Bioenergetic-active materials enhance tissue regeneration by modulating cellular metabolic state
  publication-title: Sci Adv
– volume: 3
  start-page: 390
  year: 2014
  ident: 10.1016/j.jid.2023.02.039_bib14
  article-title: The role of hypoxia-inducible factor in wound healing
  publication-title: Adv Wound Care (New Rochelle)
  doi: 10.1089/wound.2013.0520
– volume: 18
  start-page: 3809
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib24
  article-title: Metabolic phenotyping in venous disease: the need for standardization
  publication-title: J Proteome Res
  doi: 10.1021/acs.jproteome.9b00460
– volume: 31
  start-page: 1394
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib27
  article-title: Clinical and metabolic response to flaxseed oil omega-3 fatty acids supplementation in patients with diabetic foot ulcer: A randomized, double-blind, placebo-controlled trial
  publication-title: J Diabetes Complications
  doi: 10.1016/j.jdiacomp.2017.06.010
– volume: 24
  start-page: 14026
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib13
  article-title: Metabolic reprogramming of glycolysis and glutamine metabolism are key events in myofibroblast transition in systemic sclerosis pathogenesis
  publication-title: J Cell Mol Med
  doi: 10.1111/jcmm.16013
– volume: 6
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib20
  article-title: Bioenergetic-active materials enhance tissue regeneration by modulating cellular metabolic state
  publication-title: Sci Adv
– volume: 105
  start-page: 19426
  year: 2008
  ident: 10.1016/j.jid.2023.02.039_bib5
  article-title: Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.0805230105
– volume: 30
  start-page: 3932
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib12
  article-title: Defining epidermal basal cell states during skin homeostasis and wound healing using single-cell transcriptomics
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2020.02.091
– volume: 137
  start-page: 13
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib17
  article-title: Metabolic profiles of exudates from chronic leg ulcerations
  publication-title: J Pharm Biomed Anal
  doi: 10.1016/j.jpba.2017.01.018
– volume: 20
  start-page: 436
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib38
  article-title: Metabolic regulation of cell growth and proliferation
  publication-title: Nat Rev Mol Cell Biol
  doi: 10.1038/s41580-019-0123-5
– volume: 18
  start-page: 49
  year: 2021
  ident: 10.1016/j.jid.2023.02.039_bib39
  article-title: Endoplasmic reticulum stress in human chronic wound healing: rescue by 4-phenylbutyrate
  publication-title: Int Wound J
  doi: 10.1111/iwj.13525
– volume: 1037
  start-page: 255
  year: 2013
  ident: 10.1016/j.jid.2023.02.039_bib28
  article-title: Human ex vivo wound healing model
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-62703-505-7_14
– volume: 10
  year: 2015
  ident: 10.1016/j.jid.2023.02.039_bib36
  article-title: Nitric oxide enhances keratinocyte cell migration by regulating Rho GTPase via cGMP-PKG signalling
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0121551
– volume: 15
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib1
  article-title: Non-targeted metabolomic analysis reveals serum phospholipid alterations in patients with early stages of diabetic foot ulcer
  publication-title: Biomark Insights
– volume: 13
  start-page: 116
  year: 2016
  ident: 10.1016/j.jid.2023.02.039_bib10
  article-title: Oral L-glutamine administration attenuated cutaneous wound healing in Wistar rats
  publication-title: Int Wound J
  doi: 10.1111/iwj.12246
– volume: 10
  start-page: 459
  year: 1970
  ident: 10.1016/j.jid.2023.02.039_bib15
  article-title: Energy metabolism in healing skin wounds
  publication-title: J Surg Res
  doi: 10.1016/0022-4804(70)90070-3
– volume: 5
  start-page: 244
  year: 2016
  ident: 10.1016/j.jid.2023.02.039_bib33
  article-title: Human as the ultimate wound healing model: strategies for studies investigating the dermal lipidome
  publication-title: Curr Dermatol Rep
  doi: 10.1007/s13671-016-0156-3
– volume: 293
  start-page: 1218
  year: 2018
  ident: 10.1016/j.jid.2023.02.039_bib4
  article-title: Glutaminolysis is required for transforming growth factor-beta1-induced myofibroblast differentiation and activation
  publication-title: J Biol Chem
  doi: 10.1074/jbc.RA117.000444
– issue: 130
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib44
  article-title: Generation and Culturing of Primary Human Keratinocytes from Adult Skin
  publication-title: J Vis Exp
  doi: 10.3791/56863-v
– volume: 1037
  start-page: 255
  year: 2013
  ident: 10.1016/j.jid.2023.02.039_bib42
  article-title: Human ex vivo wound healing model
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-62703-505-7_14
– volume: 15
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib2
  article-title: A microbiome and metabolomic signature of phases of cutaneous healing identified by profiling sequential acute wounds of human skin: an exploratory study
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0229545
– volume: 5
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib31
  article-title: Regulation of glycolysis and the Warburg effect in wound healing
  publication-title: JCI Insight
  doi: 10.1172/jci.insight.138949
– volume: 21
  start-page: 8435
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib34
  article-title: Eicosanoids in skin wound healing
  publication-title: Int J Mol Sci
  doi: 10.3390/ijms21228435
– volume: 7
  start-page: 98
  year: 2018
  ident: 10.1016/j.jid.2023.02.039_bib6
  article-title: Targeting oxidative stress and mitochondrial dysfunction in the treatment of impaired wound healing: A systematic review
  publication-title: Antioxidants (Basel)
  doi: 10.3390/antiox7080098
– volume: 19
  start-page: 36
  year: 2021
  ident: 10.1016/j.jid.2023.02.039_bib16
  article-title: Systemic and topical administration of spermidine accelerates skin wound healing
  publication-title: Cell Commun Signal
  doi: 10.1186/s12964-021-00717-y
– volume: 27
  start-page: 126
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib23
  article-title: Fluorescent cell tracer dye permits real-time assessment of re-epithelialization in a serum-free ex vivo human skin wound assay
  publication-title: Wound Repair Regen
  doi: 10.1111/wrr.12688
– volume: 1
  start-page: 417
  year: 2015
  ident: 10.1016/j.jid.2023.02.039_bib18
  article-title: The Molecular Signatures Database (MSigDB) hallmark gene set collection
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2015.12.004
– volume: 138
  start-page: 2653
  year: 2018
  ident: 10.1016/j.jid.2023.02.039_bib19
  article-title: Polyamine regulator AMD1 promotes cell migration in epidermal wound healing
  publication-title: J Invest Dermatol
  doi: 10.1016/j.jid.2018.05.029
– volume: 18
  start-page: 49
  year: 2021
  ident: 10.1016/j.jid.2023.02.039_bib3
  article-title: Endoplasmic reticulum stress in human chronic wound healing: rescue by 4-phenylbutyrate
  publication-title: Int Wound J
  doi: 10.1111/iwj.13525
– volume: 216
  start-page: 409
  year: 2011
  ident: 10.1016/j.jid.2023.02.039_bib7
  article-title: Oleic acid modulation of the immune response in wound healing: a new approach for skin repair
  publication-title: Immunobiology
  doi: 10.1016/j.imbio.2010.06.007
– year: 2001
  ident: 10.1016/j.jid.2023.02.039_bib46
  article-title: Establishment of fibroblast cultures
  publication-title: Curr Protoc Cell Biol
– volume: 4
  start-page: 234
  year: 1996
  ident: 10.1016/j.jid.2023.02.039_bib30
  article-title: Biochemical analysis of wound fluid from nonhealing and healing chronic leg ulcers
  publication-title: Wound Repair Regen
  doi: 10.1046/j.1524-475X.1996.40211.x
– volume: 12
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib21
  article-title: The interaction of ceramide 1-phosphate with group IVA cytosolic phospholipase A2 coordinates acute wound healing and repair
  publication-title: Sci Signal
  doi: 10.1126/scisignal.aav5918
– volume: 473
  start-page: 703
  year: 2016
  ident: 10.1016/j.jid.2023.02.039_bib26
  article-title: Enhanced OXPHOS, glutaminolysis and beta-oxidation constitute the metastatic phenotype of melanoma cells
  publication-title: Biochem J
  doi: 10.1042/BJ20150645
– volume: 27
  start-page: 126
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib41
  article-title: Fluorescent cell tracer dye permits real-time assessment of re-epithelialization in a serum-free ex vivo human skin wound assay
  publication-title: Wound Repair Regen
  doi: 10.1111/wrr.12688
– volume: 14
  start-page: 737
  year: 2014
  ident: 10.1016/j.jid.2023.02.039_bib22
  article-title: Omics profiles in chronic venous ulcer wound fluid: innovative applications for translational medicine
  publication-title: Expert Rev Mol Diagn
  doi: 10.1586/14737159.2014.927312
– volume: 55
  start-page: 1298
  year: 2014
  ident: 10.1016/j.jid.2023.02.039_bib32
  article-title: Ceramide kinase is required for a normal eicosanoid response and the subsequent orderly migration of fibroblasts
  publication-title: J Lipid Res
  doi: 10.1194/jlr.M048207
– volume: 7
  start-page: 15599
  issue: 1
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib45
  article-title: The effects of artocarpin on wound healing: in vitro and in vivo studies
  publication-title: Sci Rep
  doi: 10.1038/s41598-017-15876-7
– volume: 10
  start-page: 29
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib25
  article-title: Why venous leg ulcers have difficulty healing: overview on pathophysiology, clinical consequences, and treatment
  publication-title: J Clin Med
– volume: 28
  start-page: N60
  year: 2000
  ident: 10.1016/j.jid.2023.02.039_bib37
  article-title: Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story
  publication-title: Crit Care Med
  doi: 10.1097/00003246-200004001-00007
– volume: 5
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib11
  article-title: Dysregulation of tryptophan catabolism at the host-skin microbiota interface in hidradenitis suppurativa
  publication-title: JCI Insight
  doi: 10.1172/jci.insight.140598
– volume: 9
  start-page: 4682
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib35
  article-title: Topical insulin accelerates cutaneous wound healing in insulin-resistant diabetic rats
  publication-title: Am J Transl Res
– volume: 2009
  start-page: 1
  year: 2009
  ident: 10.1016/j.jid.2023.02.039_bib29
  article-title: Influence of honey on energy metabolism during wound healing in rats
  publication-title: Sch Res Exch
– volume: 92
  start-page: 1386
  year: 2020
  ident: 10.1016/j.jid.2023.02.039_bib8
  article-title: Multimodal, in situ imaging of ex vivo human skin reveals decrease of cholesterol sulfate in the neoepithelium during acute wound healing
  publication-title: Anal Chem
  doi: 10.1021/acs.analchem.9b04542
– volume: 1
  start-page: 417
  year: 2015
  ident: 10.1016/j.jid.2023.02.039_bib40
  article-title: The Molecular Signatures Database (MSigDB) hallmark gene set collection
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2015.12.004
– volume: 116
  start-page: 9443
  issue: 19
  year: 2019
  ident: 10.1016/j.jid.2023.02.039_bib43
  article-title: Human skin long noncoding RNA WAKMAR1 regulates wound healing by enhancing keratinocyte migration
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1814097116
– volume: 356
  start-page: 1026
  year: 2017
  ident: 10.1016/j.jid.2023.02.039_bib9
  article-title: Inflammation and metabolism in tissue repair and regeneration
  publication-title: Science
  doi: 10.1126/science.aam7928
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Snippet Impaired skin wound healing is a significant global health issue, especially among the elderly. Wound healing is a well-orchestrated process involving the...
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SubjectTerms Aged
Glycolysis
Humans
Metabolic Networks and Pathways
Metabolomics
Skin
Wound Healing
Title Metabolic Reprogramming and Reliance in Human Skin Wound Healing
URI https://dx.doi.org/10.1016/j.jid.2023.02.039
https://cir.nii.ac.jp/crid/1872835442494649344
https://www.ncbi.nlm.nih.gov/pubmed/37061123
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Volume 143
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