Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing
Preparations from Arabian Gulf catfish (Arius bilineatus, Val) epidermal gel secretion (PCEGS) effectively heal chronic wounds in diabetic patients. However, specific lipid components of PCEGS that are responsible for various aspects of wound healing are unknown. Here, we report for the first time t...
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-06-01
|
| Series: | Frontiers in Pharmacology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fphar.2020.00899/full |
| _version_ | 1819054452351434752 |
|---|---|
| author | Jassim M. Al-Hassan Aleksander Hinek Waleed M. Renno Yanting Wang Yuan Fang Liu Rui Guan Xiao-Yen Wen Xiao-Yen Wen Michael L. Litvack Andras Lindenmaier Mohammad Afzal Bincy Paul Sosamma Oommen Divya Nair Jijin Kumar Meraj A. Khan Nades Palaniyar Nades Palaniyar Cecil Pace-Asciak Cecil Pace-Asciak |
| author_facet | Jassim M. Al-Hassan Aleksander Hinek Waleed M. Renno Yanting Wang Yuan Fang Liu Rui Guan Xiao-Yen Wen Xiao-Yen Wen Michael L. Litvack Andras Lindenmaier Mohammad Afzal Bincy Paul Sosamma Oommen Divya Nair Jijin Kumar Meraj A. Khan Nades Palaniyar Nades Palaniyar Cecil Pace-Asciak Cecil Pace-Asciak |
| author_sort | Jassim M. Al-Hassan |
| collection | DOAJ |
| description | Preparations from Arabian Gulf catfish (Arius bilineatus, Val) epidermal gel secretion (PCEGS) effectively heal chronic wounds in diabetic patients. However, specific lipid components of PCEGS that are responsible for various aspects of wound healing are unknown. Here, we report for the first time that, i) a unique preparation containing only proteins and lipids (Fraction B, FB), derived from the PCEGS accelerated the healing of experimental dermal wounds in female rats (transdermal punch biopsy) in vivo. Histological analyses showed that topical treatment of these wounds with FB promoted the migration of fibroblasts, facilitated the production of extracellular matrix (collagen, fibronectin), induced capillary formation and recruitment of immune cells, and accelerated overall wound healing by day 4 (tested at 1, 2, 3, 4, and 10 days; n=15 for vehicle; n=15 for FB treatment), ii) the lipids responsible for different stages of wound healing were separated into a protein-free bioactive lipid fraction, Ft, which contained a few common long-chain fatty acids, a unique furan fatty acid (F6) and a cholesterol metabolite, cholesta-3,5-diene (S5). Ft (the partially purified lipid fraction of PCEGS), and F6 and S5 present in Ft, proved to be bioactive for wound healing in human dermal fibroblasts. Ft increased the production and extracellular deposition of collagen and fibronectin, ex vivo, iii) Ft and its subcomponents, pure F6 and S5, also promoted human dermal fibroblast migration into the scratch wound gaps, ex vivo, iv) Ft, F6, and S5 promoted the recruitment of neutrophils (Green fluorescence protein labeled) to the site of injury in the transected tailfins of transgenic zebrafish, in vivo, v) Ft, but not F6 or S5, promoted the regeneration of tissues at the wound site in the transgenic zebrafish tailfin, in vivo. Therefore, we conclude that lipid fraction Ft from PCEGS contains the components necessary to promote complete wound healing, and F6 and S5 are responsible for promoting fibroblast and neutrophil recruitment to the site of wounds. |
| first_indexed | 2024-12-21T12:51:51Z |
| format | Article |
| id | doaj.art-ed44f2fdb2e64b20abd35777021e3371 |
| institution | Directory Open Access Journal |
| issn | 1663-9812 |
| language | English |
| last_indexed | 2024-12-21T12:51:51Z |
| publishDate | 2020-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Pharmacology |
| spelling | doaj.art-ed44f2fdb2e64b20abd35777021e33712022-12-21T19:03:28ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122020-06-011110.3389/fphar.2020.00899536775Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound HealingJassim M. Al-Hassan0Aleksander Hinek1Waleed M. Renno2Yanting Wang3Yuan Fang Liu4Rui Guan5Xiao-Yen Wen6Xiao-Yen Wen7Michael L. Litvack8Andras Lindenmaier9Mohammad Afzal10Bincy Paul11Sosamma Oommen12Divya Nair13Jijin Kumar14Meraj A. Khan15Nades Palaniyar16Nades Palaniyar17Cecil Pace-Asciak18Cecil Pace-Asciak19Department of Biological Sciences, Faculty of Science, Kuwait University, Kuwait City, KuwaitProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaDepartment of Anatomy, Faculty of Medicine, Kuwait University, Kuwait City, KuwaitProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaDepartments of Lab Medicine and Pathobiology, and Institute of Medical Sciences, Faculty of Medicine, University of Toronto, Toronto, ON, CanadaZebrafish Centre for Advanced Drug Discovery & Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael’s Hospital, Unity Health Toronto, Toronto, ON, CanadaDepartments of Lab Medicine and Pathobiology, and Institute of Medical Sciences, Faculty of Medicine, University of Toronto, Toronto, ON, CanadaProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaDepartment of Biological Sciences, Faculty of Science, Kuwait University, Kuwait City, KuwaitDepartment of Biological Sciences, Faculty of Science, Kuwait University, Kuwait City, KuwaitDepartment of Zoology, CMS College, Kottayam, IndiaDepartment of Biological Sciences, Faculty of Science, Kuwait University, Kuwait City, KuwaitDepartment of Anatomy, Faculty of Medicine, Kuwait University, Kuwait City, KuwaitProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaDepartments of Lab Medicine and Pathobiology, and Institute of Medical Sciences, Faculty of Medicine, University of Toronto, Toronto, ON, CanadaProgram in Translational Medicine, Peter Gilgan Centre for Research and Learning (PGCRL), The Hospital for Sick Children, Toronto, ON, CanadaDepartment of Pharmacology, University of Toronto, Toronto, ON, CanadaPreparations from Arabian Gulf catfish (Arius bilineatus, Val) epidermal gel secretion (PCEGS) effectively heal chronic wounds in diabetic patients. However, specific lipid components of PCEGS that are responsible for various aspects of wound healing are unknown. Here, we report for the first time that, i) a unique preparation containing only proteins and lipids (Fraction B, FB), derived from the PCEGS accelerated the healing of experimental dermal wounds in female rats (transdermal punch biopsy) in vivo. Histological analyses showed that topical treatment of these wounds with FB promoted the migration of fibroblasts, facilitated the production of extracellular matrix (collagen, fibronectin), induced capillary formation and recruitment of immune cells, and accelerated overall wound healing by day 4 (tested at 1, 2, 3, 4, and 10 days; n=15 for vehicle; n=15 for FB treatment), ii) the lipids responsible for different stages of wound healing were separated into a protein-free bioactive lipid fraction, Ft, which contained a few common long-chain fatty acids, a unique furan fatty acid (F6) and a cholesterol metabolite, cholesta-3,5-diene (S5). Ft (the partially purified lipid fraction of PCEGS), and F6 and S5 present in Ft, proved to be bioactive for wound healing in human dermal fibroblasts. Ft increased the production and extracellular deposition of collagen and fibronectin, ex vivo, iii) Ft and its subcomponents, pure F6 and S5, also promoted human dermal fibroblast migration into the scratch wound gaps, ex vivo, iv) Ft, F6, and S5 promoted the recruitment of neutrophils (Green fluorescence protein labeled) to the site of injury in the transected tailfins of transgenic zebrafish, in vivo, v) Ft, but not F6 or S5, promoted the regeneration of tissues at the wound site in the transgenic zebrafish tailfin, in vivo. Therefore, we conclude that lipid fraction Ft from PCEGS contains the components necessary to promote complete wound healing, and F6 and S5 are responsible for promoting fibroblast and neutrophil recruitment to the site of wounds.https://www.frontiersin.org/article/10.3389/fphar.2020.00899/fullfuran F-acidcholesta-3,5-dieneFraction-BGulf catfish lipidswound healinghistology |
| spellingShingle | Jassim M. Al-Hassan Aleksander Hinek Waleed M. Renno Yanting Wang Yuan Fang Liu Rui Guan Xiao-Yen Wen Xiao-Yen Wen Michael L. Litvack Andras Lindenmaier Mohammad Afzal Bincy Paul Sosamma Oommen Divya Nair Jijin Kumar Meraj A. Khan Nades Palaniyar Nades Palaniyar Cecil Pace-Asciak Cecil Pace-Asciak Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing Frontiers in Pharmacology furan F-acid cholesta-3,5-diene Fraction-B Gulf catfish lipids wound healing histology |
| title | Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing |
| title_full | Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing |
| title_fullStr | Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing |
| title_full_unstemmed | Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing |
| title_short | Potential Mechanism of Dermal Wound Treatment With Preparations From the Skin Gel of Arabian Gulf Catfish: A Unique Furan Fatty Acid (F6) and Cholesta-3,5-Diene (S5) Recruit Neutrophils and Fibroblasts to Promote Wound Healing |
| title_sort | potential mechanism of dermal wound treatment with preparations from the skin gel of arabian gulf catfish a unique furan fatty acid f6 and cholesta 3 5 diene s5 recruit neutrophils and fibroblasts to promote wound healing |
| topic | furan F-acid cholesta-3,5-diene Fraction-B Gulf catfish lipids wound healing histology |
| url | https://www.frontiersin.org/article/10.3389/fphar.2020.00899/full |
| work_keys_str_mv | AT jassimmalhassan potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT aleksanderhinek potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT waleedmrenno potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT yantingwang potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT yuanfangliu potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT ruiguan potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT xiaoyenwen potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT xiaoyenwen potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT michaelllitvack potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT andraslindenmaier potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT mohammadafzal potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT bincypaul potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT sosammaoommen potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT divyanair potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT jijinkumar potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT merajakhan potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT nadespalaniyar potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT nadespalaniyar potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT cecilpaceasciak potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing AT cecilpaceasciak potentialmechanismofdermalwoundtreatmentwithpreparationsfromtheskingelofarabiangulfcatfishauniquefuranfattyacidf6andcholesta35dienes5recruitneutrophilsandfibroblaststopromotewoundhealing |