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Published in: Dermatology and Therapy 7/2022

Open Access 25-06-2022 | Skin Aging | Review

Estrogen Action and Gut Microbiome Metabolism in Dermal Health

Authors: Edwin D. Lephart, Frederick Naftolin

Published in: Dermatology and Therapy | Issue 7/2022

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Abstract

Emerging scientific advances in microbial research linking estrogens and the gut-skin microbiome in reference to dermal health are featured in this narrative review of journal reports and reviews from January 2018 through February 2022. Background information on advances in microbial research along with defining the microbiota and microbiome is presented in brief. The development of and factors that influence the gut microbiome in health and disease as well as the intrinsic and extrinsic factors influencing the skin microbiome and skin aging are summarized. New information on the development and changes of organ microbiomes have exposed similarities between skin and gut structure/function, microbial components/diversity/taxonomy and how they impact the immune response for combating disease and enhancing wellness. Estrogens promote health and support homeostasis in general and directly impact dermal health. Moreover, the gut, based upon the level of the microbial enzyme β-glucuronidase, which regulates estrogen’s enterohepatic recirculation, constitutes a gut-skin microbial axis. This axis revolves around the systemically available estrogen to support immune function, counteract inflammation and oxidative stress, and decrease the risk of hormone-dependent skin cancers. These data support the direct effect of estrogens on skin health and the interaction of diet on dermal health via effects on the gut microflora. Finally, the potential for bioactive botanicals containing phytoestrogens or selective estrogen receptor modulators (SERMs) to evade the effects of gut β-glucuronidase expressing flora is proposed that may have a positive impact on skin.
Literature
1.
go back to reference Jo H-Y, Kennedy EA, Kong HH. Research techniques make sample: Bacterial 16S Ribosomal RNA gene sequencing in cutaneous research. J Invest Dermatol. 2016;136:e23–7.PubMedPubMedCentralCrossRef Jo H-Y, Kennedy EA, Kong HH. Research techniques make sample: Bacterial 16S Ribosomal RNA gene sequencing in cutaneous research. J Invest Dermatol. 2016;136:e23–7.PubMedPubMedCentralCrossRef
6.
go back to reference Mazur M, Tomczak H, Lodyga M, et al. The microbiome of the human skin and its variability in psoriasis and atopic dermatitis. Adv Dermatol Allergol. 2021;38:205–9.CrossRef Mazur M, Tomczak H, Lodyga M, et al. The microbiome of the human skin and its variability in psoriasis and atopic dermatitis. Adv Dermatol Allergol. 2021;38:205–9.CrossRef
7.
go back to reference Sinha S, Lin G, Ferenczi K. The skin microbiome and the gut-skin axis. Clin Dermatol. 2021;39:829–39.PubMedCrossRef Sinha S, Lin G, Ferenczi K. The skin microbiome and the gut-skin axis. Clin Dermatol. 2021;39:829–39.PubMedCrossRef
10.
go back to reference Ervin SM, Li H, Lim L, et al. Gut microbial β-glucuronidases reactive estrogens as components of the estrobolome that reactivate estrogens. J Biol Chem. 2019;294:18586–99.PubMedPubMedCentralCrossRef Ervin SM, Li H, Lim L, et al. Gut microbial β-glucuronidases reactive estrogens as components of the estrobolome that reactivate estrogens. J Biol Chem. 2019;294:18586–99.PubMedPubMedCentralCrossRef
17.
go back to reference Sekirov I, Russell SL, Antunes CM, Finlay BB. Gut microbiome in health and disease. Physiol Rev. 2010;90:859–904.PubMedCrossRef Sekirov I, Russell SL, Antunes CM, Finlay BB. Gut microbiome in health and disease. Physiol Rev. 2010;90:859–904.PubMedCrossRef
18.
go back to reference National Academies of Sciences, Engineering, and Medicine: Division of Earth and Life Sciences; Board on Life Sciences; Board on Environmental Studies and Toxicology. Committee on advancing understanding of the implications of: environmental chemicals, the human microbiome, and health risk: a research strategy. Washington: National Academies Press; 2017. https://doi.org/10.17226/24960.CrossRef National Academies of Sciences, Engineering, and Medicine: Division of Earth and Life Sciences; Board on Life Sciences; Board on Environmental Studies and Toxicology. Committee on advancing understanding of the implications of: environmental chemicals, the human microbiome, and health risk: a research strategy. Washington: National Academies Press; 2017. https://​doi.​org/​10.​17226/​24960.CrossRef
22.
go back to reference Fuhrman BJ, Feigelson HS, Flores R, Gail MH, Xu X, Ravel J, Goedert JJ. Associations of the fecal microbiome with urinary estrogens and estrogens metabolites in postmenopausal women. J Clin Endocrinol Metab. 2014;99:4632–40.PubMedPubMedCentralCrossRef Fuhrman BJ, Feigelson HS, Flores R, Gail MH, Xu X, Ravel J, Goedert JJ. Associations of the fecal microbiome with urinary estrogens and estrogens metabolites in postmenopausal women. J Clin Endocrinol Metab. 2014;99:4632–40.PubMedPubMedCentralCrossRef
23.
go back to reference David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.PubMedCrossRef David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.PubMedCrossRef
24.
go back to reference Hoashi M, Meche L, Mahal LK, Bakacs E, Nardella D, Naftolin F, Bar-Yam N, Dominguez-Bello MG. Human milk bacterial and glycosylation patterns differ by delivery mode. Reproductive Sci. 2016;23:902–7.CrossRef Hoashi M, Meche L, Mahal LK, Bakacs E, Nardella D, Naftolin F, Bar-Yam N, Dominguez-Bello MG. Human milk bacterial and glycosylation patterns differ by delivery mode. Reproductive Sci. 2016;23:902–7.CrossRef
25.
go back to reference Wu GD, Compher C, Chen EZ, Smith SA, Shah RD, Bittinger K, Chehoud C, Albenberg LG, Nessel L, Gilroy E, Star J, Weljie AM, Flint HJ, Metz DC, Bennett MJ, Li H, Bushman FD, Lewis JD. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut. 2016;65:63–72.PubMedCrossRef Wu GD, Compher C, Chen EZ, Smith SA, Shah RD, Bittinger K, Chehoud C, Albenberg LG, Nessel L, Gilroy E, Star J, Weljie AM, Flint HJ, Metz DC, Bennett MJ, Li H, Bushman FD, Lewis JD. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut. 2016;65:63–72.PubMedCrossRef
26.
go back to reference Khanna S, Pardi DS. Clinical implications of antibiotic impact on gastrointestinal microbiota and Clostridium difficile infection. Expert Rev Gastroenterol Hepatol. 2016;10:1145–52.PubMedCrossRef Khanna S, Pardi DS. Clinical implications of antibiotic impact on gastrointestinal microbiota and Clostridium difficile infection. Expert Rev Gastroenterol Hepatol. 2016;10:1145–52.PubMedCrossRef
29.
go back to reference Shin J-H, Park Y-H, Sim M, Kim S-A, Joung H, Shin D-M. Serum level of sex steroid hormones is associated with diversity and profiles of human gut microbiome. Res Microbiol. 2019;170:192–201.PubMedCrossRef Shin J-H, Park Y-H, Sim M, Kim S-A, Joung H, Shin D-M. Serum level of sex steroid hormones is associated with diversity and profiles of human gut microbiome. Res Microbiol. 2019;170:192–201.PubMedCrossRef
33.
go back to reference Ju W. The gut microbiome and its impact on the brain. 4.1 pressbooks, neuroscience: Canadian 1st edition open textbook. Toronto: University of Toronto; 2020. Ju W. The gut microbiome and its impact on the brain. 4.1 pressbooks, neuroscience: Canadian 1st edition open textbook. Toronto: University of Toronto; 2020.
36.
go back to reference Tanes C, Bittinger K, Gao Y, Friedman ES, Nessel L, Paladhi UR, Chau L, Panfen E, Fischbach MA, Braun J, Xavier RJ, Clish CB, Li H, Bushman FD, Lewis JD, Wu GD. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021;29:394–407.PubMedPubMedCentralCrossRef Tanes C, Bittinger K, Gao Y, Friedman ES, Nessel L, Paladhi UR, Chau L, Panfen E, Fischbach MA, Braun J, Xavier RJ, Clish CB, Li H, Bushman FD, Lewis JD, Wu GD. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021;29:394–407.PubMedPubMedCentralCrossRef
37.
go back to reference van der Merwe M. Gut microbiome changes induced by a diet rich in fruits and vegetables. Internat J Food Sci Nutr. 2012;72:665–9.CrossRef van der Merwe M. Gut microbiome changes induced by a diet rich in fruits and vegetables. Internat J Food Sci Nutr. 2012;72:665–9.CrossRef
38.
go back to reference Sprockett D, Fukami T, Relman DA. Role of priority effects in the early-life assembly of the gut microbiota. Nat Rev Gastroenterol Hepatol. 2018;15:197–205.PubMedPubMedCentralCrossRef Sprockett D, Fukami T, Relman DA. Role of priority effects in the early-life assembly of the gut microbiota. Nat Rev Gastroenterol Hepatol. 2018;15:197–205.PubMedPubMedCentralCrossRef
41.
go back to reference Hussain T, Murtaza G, Kalhoro DH, et al. Relationship between the gut microbiome and host-metabolism: Emphasis on hormones related to reproductive function. Animal Nutr. 2021;7:1–10.CrossRef Hussain T, Murtaza G, Kalhoro DH, et al. Relationship between the gut microbiome and host-metabolism: Emphasis on hormones related to reproductive function. Animal Nutr. 2021;7:1–10.CrossRef
42.
go back to reference Jiang C, Li G, Huang P, Liu Z, Zhao B. The gut microbiota and Alzheimer’s disease. J Alzheimer’s Dis. 2017;58:1–15.CrossRef Jiang C, Li G, Huang P, Liu Z, Zhao B. The gut microbiota and Alzheimer’s disease. J Alzheimer’s Dis. 2017;58:1–15.CrossRef
44.
go back to reference Zhang F, Yue L, Fang X, et al. Altered gut microbiota in Parkinson’s disease patients/healthy spouses and its association with clinical features. Parkinsonism Related Dis. 2020;18:84–8.CrossRef Zhang F, Yue L, Fang X, et al. Altered gut microbiota in Parkinson’s disease patients/healthy spouses and its association with clinical features. Parkinsonism Related Dis. 2020;18:84–8.CrossRef
46.
51.
go back to reference Lephart E, Naftolin F. Menopause and the skin: old favorites and new innovation in cosmeceuticals for estrogen-deficient skin. Dermatol Ther (Heidelb). 2021;11:53–69.CrossRef Lephart E, Naftolin F. Menopause and the skin: old favorites and new innovation in cosmeceuticals for estrogen-deficient skin. Dermatol Ther (Heidelb). 2021;11:53–69.CrossRef
52.
go back to reference Bonté F, Girard D, Archambault J-C, et al. Chapter 10, skin changes during aging. In: Harris JR, Korolchuk VI, editors., et al., Biochemistry and cell biology of aging: part II clinical sciences, subcellular biochemistry. Singapore: Springer Nature; 2019. p. 249–80. Bonté F, Girard D, Archambault J-C, et al. Chapter 10, skin changes during aging. In: Harris JR, Korolchuk VI, editors., et al., Biochemistry and cell biology of aging: part II clinical sciences, subcellular biochemistry. Singapore: Springer Nature; 2019. p. 249–80.
53.
go back to reference Lephart ED. Skin aging and oxidative stress: equol’s anti-aging effects via biochemical and molecular mechanisms. Ageing Res Rev. 2016;31:36–54.PubMedCrossRef Lephart ED. Skin aging and oxidative stress: equol’s anti-aging effects via biochemical and molecular mechanisms. Ageing Res Rev. 2016;31:36–54.PubMedCrossRef
54.
go back to reference Zhang S, Duan E. Fighting against skin aging: the way from bench to bedside. Cell Transpl. 2018;27:729–38.CrossRef Zhang S, Duan E. Fighting against skin aging: the way from bench to bedside. Cell Transpl. 2018;27:729–38.CrossRef
55.
go back to reference Lephart ED. A review of the role of estrogen in dermal aging and facial attractiveness in women. J Cosmet Dermatol. 2018;17:282–8.PubMedCrossRef Lephart ED. A review of the role of estrogen in dermal aging and facial attractiveness in women. J Cosmet Dermatol. 2018;17:282–8.PubMedCrossRef
56.
go back to reference Huang AH, Chien AL. Photoaging: a review of the current literature. Current Dermatol Rep. 2020;9:22–9.CrossRef Huang AH, Chien AL. Photoaging: a review of the current literature. Current Dermatol Rep. 2020;9:22–9.CrossRef
57.
go back to reference Dyer JM, Miller RA. Chronic skin fragility of aging: current concepts in pathogenesis, recognition, and management of dermatoporosis. J Clin Aesthet Dermatol. 2018;11:13–8.PubMedPubMedCentral Dyer JM, Miller RA. Chronic skin fragility of aging: current concepts in pathogenesis, recognition, and management of dermatoporosis. J Clin Aesthet Dermatol. 2018;11:13–8.PubMedPubMedCentral
62.
go back to reference Dimitriu PA, Iker B, Malik K, Leung H, Mohn WW, Hillebrand GG. New insights into the intrinsic and extrinsic factors that shape the human skin microbiome. MBio. 2019;10(4):e00839-e919.PubMedPubMedCentralCrossRef Dimitriu PA, Iker B, Malik K, Leung H, Mohn WW, Hillebrand GG. New insights into the intrinsic and extrinsic factors that shape the human skin microbiome. MBio. 2019;10(4):e00839-e919.PubMedPubMedCentralCrossRef
65.
go back to reference Lambers H, Piessens S, Bloem A, et al. Natural skin surface pH is on average below 5, which is beneficial for its resident flora. Internat J Cosmet Sci. 2006;28:359–70.CrossRef Lambers H, Piessens S, Bloem A, et al. Natural skin surface pH is on average below 5, which is beneficial for its resident flora. Internat J Cosmet Sci. 2006;28:359–70.CrossRef
68.
go back to reference Blakemore J, Naftolin F. Aromatase: contributions to physiology and disease in women and men. Physiology (Bethesda). 2016;31:258–69. Blakemore J, Naftolin F. Aromatase: contributions to physiology and disease in women and men. Physiology (Bethesda). 2016;31:258–69.
69.
go back to reference Santen RJ, Simpson E. History of estrogen: Its purification, structure, synthesis, biological actions, and clinical implications. Endocrinol. 2019;160:605–25.CrossRef Santen RJ, Simpson E. History of estrogen: Its purification, structure, synthesis, biological actions, and clinical implications. Endocrinol. 2019;160:605–25.CrossRef
70.
go back to reference Ceccarelli I, Bioletti L, Peparini S, et al. Estrogens and phytoestrogens in body functions. Neurosci Biobehav Rev. 2022;132:648–63.PubMedCrossRef Ceccarelli I, Bioletti L, Peparini S, et al. Estrogens and phytoestrogens in body functions. Neurosci Biobehav Rev. 2022;132:648–63.PubMedCrossRef
72.
go back to reference Chen G, Chen Z, Fan X, et al. Gut-brain-skin axis in psoriasis: a review. Dermatol Ther (Heidelb). 2021;11:25–38.CrossRef Chen G, Chen Z, Fan X, et al. Gut-brain-skin axis in psoriasis: a review. Dermatol Ther (Heidelb). 2021;11:25–38.CrossRef
74.
go back to reference Adercreutz H. Studies on oestrogen excretion in human bile. Acta Endocrinol. 1962;42:1–220. Adercreutz H. Studies on oestrogen excretion in human bile. Acta Endocrinol. 1962;42:1–220.
75.
go back to reference Adlercreutz H, Jarvenpaa P. Assay of oestrogens in human feces. J Steroid Biochem. 1982;17:639–45.PubMedCrossRef Adlercreutz H, Jarvenpaa P. Assay of oestrogens in human feces. J Steroid Biochem. 1982;17:639–45.PubMedCrossRef
79.
go back to reference Kim Y-S, Kim T-H, Park ES, Fadiel A, Naftolin F. Ezrin expression and activation in hypertrophic and keloid scar. Gynecol Reprod Endocrinol Metab. 2020;1:29–36. Kim Y-S, Kim T-H, Park ES, Fadiel A, Naftolin F. Ezrin expression and activation in hypertrophic and keloid scar. Gynecol Reprod Endocrinol Metab. 2020;1:29–36.
80.
go back to reference Naftolin F. Prevention during the menopause is critical for good health: skin studies support protracted hormone therapy. Fertil Steril. 2005;84:293–4.PubMedCrossRef Naftolin F. Prevention during the menopause is critical for good health: skin studies support protracted hormone therapy. Fertil Steril. 2005;84:293–4.PubMedCrossRef
87.
go back to reference Espin JC, Gonzales-Sarrias A, Tomas-Barberan FA. The gut microbiome: a key factor in the therapeutic effects of (ploy)phenols. Biochem Pharma. 2017;139:82–93.CrossRef Espin JC, Gonzales-Sarrias A, Tomas-Barberan FA. The gut microbiome: a key factor in the therapeutic effects of (ploy)phenols. Biochem Pharma. 2017;139:82–93.CrossRef
89.
go back to reference Anna Addor FA. Beyond photoaging: additional factors involved in the process of skin aging. Clin Cosmet Invest Dermatol. 2018;11:437–43.CrossRef Anna Addor FA. Beyond photoaging: additional factors involved in the process of skin aging. Clin Cosmet Invest Dermatol. 2018;11:437–43.CrossRef
98.
go back to reference Muzmdar S, Ferenczi K. Nutrition and youthful skin. Clin Dermatol. 2021;39:796–808.CrossRef Muzmdar S, Ferenczi K. Nutrition and youthful skin. Clin Dermatol. 2021;39:796–808.CrossRef
100.
go back to reference Rowe IJ, Baber RJ. The effects of phytoestrogens on postmenopausal health. Climacteric. 2021;24:57–63.PubMedCrossRef Rowe IJ, Baber RJ. The effects of phytoestrogens on postmenopausal health. Climacteric. 2021;24:57–63.PubMedCrossRef
102.
go back to reference Naftolin F, Friedenthal J, Nachtigall R, Nachtigall L. Cardiovascular health and the menopausal woman: the role of estrogen and when to begin and end hormone treatment. Faculty of 1000 Res. F1000Res. 2019;8:F1000.PubMedPubMedCentralCrossRef Naftolin F, Friedenthal J, Nachtigall R, Nachtigall L. Cardiovascular health and the menopausal woman: the role of estrogen and when to begin and end hormone treatment. Faculty of 1000 Res. F1000Res. 2019;8:F1000.PubMedPubMedCentralCrossRef
Metadata
Title
Estrogen Action and Gut Microbiome Metabolism in Dermal Health
Authors
Edwin D. Lephart
Frederick Naftolin
Publication date
25-06-2022
Publisher
Springer Healthcare
Published in
Dermatology and Therapy / Issue 7/2022
Print ISSN: 2193-8210
Electronic ISSN: 2190-9172
DOI
https://doi.org/10.1007/s13555-022-00759-1

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