Topical estrogen application to wounds promotes delayed cutaneous wound healing in 80-week-old female mice
Autoři:
Kanae Mukai aff001; Yukari Nakajima aff001; Kimi Asano aff002; Toshio Nakatani aff001
Působiště autorů:
Faculty of Health Sciences, Institute of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan
aff001; Department of Clinical Nursing, Graduate Course of Nursing Science, Division of Health Sciences, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225880
Souhrn
Topical estrogen application to wounds is effective in promoting cutaneous wound healing. However, whether it promotes cutaneous wound healing in delayed cutaneous wound healing associated with advanced age remains to be elucidated. This study aimed to evaluate the effect of topical estrogen application to wounds in cutaneous wound healing in 80-week-old female mice. C57BL/6J female mice aged 82–85 and 12 weeks old were submitted to two full-thickness wounds. Mice were divided into four groups: aged group, topical estrogen wound treatment aged group (aged-E), vehicle wound treatment aged group (aged-vehicle), and young group. Wound healing was observed until day 14. In the aged group, wound area ratio (wound area / initial wound area) was significantly higher on days 3–14, ratio of re-epithelialization was significantly lower on day 3 and tended to be lower on day 14, and neutrophil number was significantly higher on day 7 compared with the young group. In contrast, in the aged-E group, wound area ratio was significantly smaller on days 1–14, re-epithelialization ratio was significantly higher on days 3–14, and neutrophil and macrophage number was significantly lower on days 3 and 7 compared with the aged group. These results demonstrate that topical estrogen application to wounds in 80-week-old female mice promoted cutaneous wound healing by reducing wound area and inflammatory response and promoting re-epithelialization.
Klíčová slova:
Inflammation – Fibroblasts – Macrophages – Neutrophils – Wound healing – Oils – Estrogens – Estrogen replacement therapy
Zdroje
1. He W, Goodkind D, Kowal P. An Aging World: 2015. International Population Reports. U.S. Government Printing Office, Washington DC.2016:1–165.
2. Montagna W, Carlisle K. Structural changes in ageing skin. Br J Dermatol. 1990;122 Suppl: 61–70.
3. Fenske NA, Lober CW. Structural and functional changes of normal aging skin. J Am Acad Dermatol. 1986;15:571–585. doi: 10.1016/s0190-9622(86)70208-9 3534008
4. Kurban RS, Bhawan J. Histologic changes in skin associated with aging. J Dermatol Surg Oncol. 1990;16: 908–914. doi: 10.1111/j.1524-4725.1990.tb01554.x 2229632
5. Richard S, Querleux B, Bittoun J, Jolivet O, Idy-Peretti I, de Lacharriere O, et al. Characterization of the skin in vivo by high resolution magnetic resonance imaging: water behavior and age-related effects. J Invest Dermatol. 1993;100: 705–709. doi: 10.1111/1523-1747.ep12472356 8388010
6. Ashcroft GS, Mills SJ, Ashworth JJ. Ageing and wound healing. Biogerontology. 2002; 337–345. doi: 10.1023/a:1021399228395 12510172
7. Kenyon CJ. The genetics of ageing. Nature. 2010;464: 504–512. doi: 10.1038/nature08980 20336132
8. Velarde MC, Demaria M, Melov S, Campisi J. Pleiotropic age-dependent effects of mitochondrial dysfunction on epidermal stem cells. Proc Natl Acad Sci USA. 2015;112: 10407–10412. doi: 10.1073/pnas.1505675112 26240345
9. Ashcroft GS, Horan M a, Ferguson MW. The effects of ageing on cutaneous wound healing in mammals. J Anat. 1995;187 (Pt 1): 1–26.
10. Shaw TJ, Martin P. Wound repair at a glance. J Cell Sci. 2009;122: 3209–3213. doi: 10.1242/jcs.031187 19726630
11. Sgonc R, Gruber J. Age-related aspects of cutaneous wound healing: A mini-review. Gerontology. 2013;59: 159–164. doi: 10.1159/000342344 23108154
12. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson FM. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-β1 levels. Nat Med. 1997;3: 1209–1215. 9359694
13. Ashcroft GS, Greenwell-Wild T, Horan MA, Wahl SM, Ferguson MW. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol. 1999;155: 1137–1146. doi: 10.1016/S0002-9440(10)65217-0 10514397
14. Hardman MJ, Ashcroft GS. Estrogen, not intrinsic aging, is the major regulator of delayed human wound healing in the elderly. Genome Biol. 2008;9. doi: 10.1186/gb-2008-9-5-r80 18477406
15. Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, et al. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest. 2003;111: 1309–1318. doi: 10.1172/JCI16288 12727922
16. Emmerson E, Campbell L, Ashcroft GS, Hardman MJ. The phytoestrogen genistein promotes wound healing by multiple independent mechanisms. Mol Cell Endocrinol. 2010;321: 184–193. doi: 10.1016/j.mce.2010.02.026 20193736
17. Hardman MJ, Emmerson E, Campbell L, Ashcroft GS. Selective estrogen receptor modulators accelerate cutaneous wound healing in ovariectomized female mice. Endocrinology. 2008;149: 551–557. doi: 10.1210/en.2007-1042 17974625
18. Routley CE, Ashcroft GS. Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen. 2009;17: 42–50. doi: 10.1111/j.1524-475X.2008.00440.x 19152650
19. Brufani M, Ceccacci F, Filocamo L, Garofalo B, Joudioux R, Bella A La, et al. Novel locally active estrogens accelerate cutaneous wound healing. A preliminary study. Mol Pharm. 2009;6: 543–556. doi: 10.1021/mp800206b 19718805
20. Emmerson E, Campbell L, Ashcroft GS, Hardman MJ. Unique and synergistic roles for 17β-estradiol and macrophage migration inhibitory factor during cutaneous wound closure are cell type specific. Endocrinology. 2009;150: 2749–2757. doi: 10.1210/en.2008-1569 19196797
21. Mukai K, Urai T, Asano K, Nakajima Y, Nakatani T. Evaluation of effects of topical estradiol benzoate application on cutaneous wound healing in ovariectomized female mice. PLoS One. 2016;11:e0163560. doi: 10.1371/journal.pone.0163560 27658263
22. Gilliver SC, Ruckshanthi JPD, Hardman MJ, Nakayama T, Ashcroft GS. Sex dimorphism in wound healing: The roles of sex steroids and macrophage migration inhibitory factor. Endocrinology. 2008;149: 5747–5757. doi: 10.1210/en.2008-0355 18653719
23. Campbell L, Emmerson E, Davies F, Gilliver SC, Krust A, Chambon P, et al. Estrogen promotes cutaneous wound healing via estrogen receptor β independent of its antiinflammatory activities. J Exp Med. 2010;207: 1825–1833. doi: 10.1084/jem.20100500 20733032
24. Gilliver SC, Emmerson E, Chambon P, Hardman MJ, Ashcroft GS. 17B-Estradiol Inhibits Wound Healing in Male Mice Via Estrogen Receptor-A. Am J Pathol. 2010;176: 2707–2721. doi: 10.2353/ajpath.2010.090432 20448060
25. Mukai K, Nakatani T, Sugama J, Komatsu E, Nakajima Y, Nasruddin, et al. The Effect of 17β-Estradiol on Cutaneous Wound Healing in Protein-Malnourished Ovariectomized Female Mouse Model. PLoS One. 2014;9: e115564. doi: 10.1371/journal.pone.0115564 25518000
26. Hozzein WN, Badr G, Al Ghamdi AA, Sayed A, Al-Waili NS, Garraud O. Topical application of propolis enhances cutaneous wound healing by promoting TGF-beta/Smad-mediated collagen production in a streptozotocin-induced type I diabetic mouse model. Cell Physiol Biochem. 2015;37: 940–954. doi: 10.1159/000430221 26381245
27. Naraginti S, Kumari PL, Das RK, Sivakumar A, Patil SH, Andhalkar VV. Amelioration of excision wounds by topical application of green synthesized, formulated silver and gold nanoparticles in albino Wistar rats. Mater Sci Eng C Mater Biol Appl. 2016;62: 293–300. doi: 10.1016/j.msec.2016.01.069 26952426
28. Ahn J, Kim SG, Kim MK, Kim DW, Lee JH, Seok H, et al. Topical delivery of 4-hexylresorcinol promotes wound healing via tumor necrosis factor-α suppression. Burns. 2016;42: 1534–1541. doi: 10.1016/j.burns.2016.04.016 27198070
29. Farzadinia P, Jofreh N, Khatamsaz S, Movahed A, Akbarzadeh S, Mohammadi M, et al. Anti-inflammatory and Wound Healing Activities of Aloe vera, Honey and Milk Ointment on Second-Degree Burns in Rats. Int J Low Extrem Wounds. 2016;15: 241–247. doi: 10.1177/1534734616645031 27217089
30. Mukai K, Nakajima Y, Urai T, Komatsu E, Takata K, Miyasaka Y, et al. The Effect of 17β-Estradiol on Cutaneous Wound Healing in 24-Week Ovariectomized Female Mice. J Horm. 2014; Article ID 234632, 8 pages. doi: 10.1371/journal.pone.0115564 25518000
31. Mukai K, Nakajima Y, Urai T, Komatsu E, Nasruddin, Sugama J, et al. 17B-Estradiol Administration Promotes Delayed Cutaneous Wound Healing in 40-Week Ovariectomised Female Mice. Int Wound J. 2016;13: 636–644. doi: 10.1111/iwj.12336 25132513
32. Keyes BE, Liu S, Asare A, Naik S, Levorse J, Polak L, et al. Impaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin. Cell. 2016;167: 1323–1338.e14. doi: 10.1016/j.cell.2016.10.052 27863246
33. Ashcroft GS, Horan MA, Ferguson MWJ. Aging Is Associated with Reduced Deposition of Specific Extracellular Matrix Components, an Upregulation of Angiogenesis, and an Altered Inflammatory Response in a Murine Incisional Wound Healing Model. J Invest Dermatol. 1997;108: 430–437. doi: 10.1111/1523-1747.ep12289705 9077470
34. Felicio LS, Nelson JF, Finch CE. Spontaneous pituitary tumorigenesis and plasma oestradiol in ageing female C57BL/6J mice. Exp Gerontol. 1980;15: 139–143. doi: 10.1016/0531-5565(80)90085-6 7190097
35. Campbell L, Emmerson E, Williams H, Saville CR, Krust A, Chambon P et al. Estrogen receptor-alpha promotes alternative macrophage activation during cutaneous repair. J Invest Dermatol. 2014;134(9): 2447–2457. doi: 10.1038/jid.2014.175 24769859
36. Abbott RE, Corral CJ, MacIvor DM, Lin X, Ley TJ, Mustoe TA. Augmented inflammatory responses and altered wound healing in cathepsin G-deficient mice. Arch Surg. 1998;133: 1002–1006. doi: 10.1001/archsurg.133.9.1002 9749856
37. Hübner G, Brauchle M, Smola H, Madlener M, Fässler R, Werner S. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine. 1996;8: 548–556. doi: 10.1006/cyto.1996.0074 8891436
38. Mercado AM, Quan N, Padgett DA, Sheridan JF, Marucha PT. Restraint stress alters the expression of interleukin-1 and keratinocyte growth factor at the wound site: an in situ hybridization study. J Neuroimmunol. 2002;129(1–2):74–83. doi: 10.1016/s0165-5728(02)00174-1 12161023
39. Delgado A V, Mcmanus AT, Chambers JP. Production of Tumor Necrosis Factor-alpha, Interleukin 1-beta, Interleukin 2, and Interleukin 6 by rat leukocyte subpopulations after exposure to Substance P. Neuropeptides. 2003;37(6):355–361. doi: 10.1016/j.npep.2003.09.005 14698678
40. Feldmann M, Williams RO, Paleolog E. What have we learnt from targeted anti-TNF therapy? Ann Rheum Dis. 2010;69: i97–i99. doi: 10.1136/ard.2009.117143 19995756
41. Chan JMK, Villarreal G, Jin WW, Stepan T, Burstein H, Wahl SM. Intraarticular Gene Transfer of TNFR:Fc Suppresses Experimental Arthritis with Reduced Systemic Distribution of the Gene Product. Mol Ther. 2002;6(6): 727–736. doi: 10.1006/mthe.2002.0808 12498769
42. Ashcroft GS, Horan MA, Ferguson MW. Aging alters the inflammatory and endothelial cell adhesion molecule profiles during human cutaneous wound healing. Lab Invest. 1998;78: 47–58. 9461121
43. Lipschitz DA, Udupa KB. Influence of aging and protein deficiency on neutrophil function. J Gerontol. 1986;41: 690–694. doi: 10.1093/geronj/41.6.690 3021843
44. Wenisch C, Patruta S, Daxböck F, Krause R, Hörl W. Effect of age on human neutrophil function. J Leukoc Biol. 2000;67: 40–45. doi: 10.1002/jlb.67.1.40 10647996
45. Butcher SK, Chahal H, Nayak L, Sinclair A, Henriquez N V, Sapey E, et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J Leukoc Biol. 2001;70: 881–886. 11739550
46. Song XY, Zeng L, Jin W, Thompson J, Mizel DE, Lei KJ, et al. Secretory Leukocyte Protease Inhibitor Suppresses the Inflammation and Joint Damage of Bacterial Cell Wall-induced Arthritis. J Exp Med. 1999;190: 535–542. doi: 10.1084/jem.190.4.535 10449524
47. Brüünsgaard H, Pedersen BK. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am. 2003;23: 15–39. doi: 10.1016/s0889-8561(02)00056-5 12645876
48. Bruunsgaard H. Effects of tumor necrosis factor-alpha and interleukin-6 in elderly populations. Eur Cytokine Netw. 2002;13: 389–91. 12517724
49. Kojima H, Inoue T, Kunimoto H, Nakajima K. IL-6-STAT3 signaling and premature senescence. JAK-STAT. 2013;2(4):e25763. doi: 10.4161/jkst.25763 24416650
50. Franceschi C, Campisi J. Chronic Inflammation (Inflammaging) and Its Potential Contribution to Age-Associated Diseases. Biol Sci Cite J as J Gerontol A Biol Sci Med Sci. 2014;69. doi: 10.1093/gerona/glu057 24833586
51. Valacchi G, Lim Y, Belmonte G, Miracco C, Zanardi I, Bocci V, et al. Ozonated sesame oil enhances cutaneous wound healing in SKH1 mice. Wound Repair Regen. 2011;19: 107–115. doi: 10.1111/j.1524-475X.2010.00649.x 21134039
52. Donato-Trancoso A, Monte-Alto-Costa A, Romana-Souza B. Olive oil-induced reduction of oxidative damage and inflammation promotes wound healing of pressure ulcers in mice. J Dermatol Sci. 2016;83: 60–69. doi: 10.1016/j.jdermsci.2016.03.012 27091748
53. Ishak WMW, Katas H, Yuen NP, Abdullah MA, Zulfakar MH. Topical application of omega-3-, omega-6-, and omega-9-rich oil emulsions for cutaneous wound healing in rats. Drug Deliv Transl Res. 2019;9: 418–433. doi: 10.1007/s13346-018-0522-8 29667150
54. Schanuel FS, Saguie BO, Monte-Alto-Costa A. Olive oil promotes wound healing of mice pressure injuries through NOS-2 and Nrf2. Appl Physiol Nutr Metab. 2019 [Epup ahed of print]. doi: 10.1139/apnm-2018-0845 30901524
Článok vyšiel v časopise
PLOS One
2019 Číslo 11
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Dlouhodobá recidiva a komplikace spojené s elektivní operací břišní kýly
Najčítanejšie v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF