Commensal microbe regulation of skin cells in disease.

Yuyang Gan, Jiarui Zhang, Fangfang Qi, Zhiqi Hu, Evan Sweren, Sashank K Reddy, Lu Chen, Xinyi Feng, Elizabeth A Grice, Luis A Garza, Gaofeng Wang
Author Information
  1. Yuyang Gan: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  2. Jiarui Zhang: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  3. Fangfang Qi: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  4. Zhiqi Hu: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  5. Evan Sweren: University of Michigan Medical School, Ann Arbor, MI 48109, USA.
  6. Sashank K Reddy: Department of Dermatology, Johns Hopkins University School of Medicine, Baltimore, MD 21210, USA; Department of Plastic and Reconstructive Surgery, Johns Hopkins School of Medicine, Baltimore, MD 21287, USA.
  7. Lu Chen: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  8. Xinyi Feng: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China.
  9. Elizabeth A Grice: Department of Dermatology and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: egrice@upenn.edu.
  10. Luis A Garza: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China; Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21210, USA; Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, MD 21210, USA. Electronic address: lag@jhmi.edu.
  11. Gaofeng Wang: Department of Plastic and Aesthetic Surgery, Nanfang Hospital of Southern Medical University, Guangzhou, Guangdong Province 510515, China; Department of Dermatology, Johns Hopkins University School of Medicine, Baltimore, MD 21210, USA. Electronic address: gwang45@jhmi.edu.

Abstract

Human skin is the host to various commensal microbes that constitute a substantial microbial community. The reciprocal communication between these microbial inhabitants and host cells upholds both the morphological and functional attributes of the skin layers, contributing indispensably to microenvironmental and tissue homeostasis. Thus, disruption of the skin barrier or imbalances in the microbial communities can exert profound effects on the behavior of host cells. This influence, mediated by the microbes themselves or their metabolites, manifests in diverse outcomes. In this review, we examine existing knowledge to provide insight into the nuanced behavior exhibited by the microbiota on skin cells in health and disease states. These interactions provide insight into potential cellular targets for future microbiota-based therapies to prevent and treat skin disease.

References

  1. Theranostics. 2022 Oct 17;12(17):7319-7334 [PMID: 36438501]
  2. J Cell Biochem. 2018 Nov;119(11):9141-9153 [PMID: 30105859]
  3. Microbiome. 2019 Jun 24;7(1):95 [PMID: 31234928]
  4. Microbiol Spectr. 2022 Aug 31;10(4):e0065722 [PMID: 35730951]
  5. Exp Dermatol. 2020 Mar;29(3):286-294 [PMID: 30974503]
  6. Int J Mol Sci. 2021 Dec 09;22(24): [PMID: 34948051]
  7. Parasite Immunol. 2023 Feb;45(2):e12948 [PMID: 36047038]
  8. J Allergy Clin Immunol. 2014 Feb;133(2):448-60 [PMID: 24373353]
  9. Immunity. 2023 Apr 11;56(4):829-846.e8 [PMID: 36822206]
  10. Nat Rev Microbiol. 2018 Mar;16(3):143-155 [PMID: 29332945]
  11. Am J Respir Crit Care Med. 2017 Jul 15;196(2):208-219 [PMID: 28157391]
  12. Sci Transl Med. 2014 Dec 3;6(265):265sr6 [PMID: 25473038]
  13. Nat Rev Microbiol. 2022 Feb;20(2):95-108 [PMID: 34522050]
  14. Nat Rev Gastroenterol Hepatol. 2022 Mar;19(3):169-184 [PMID: 34876680]
  15. Science. 2019 Jan 4;363(6422): [PMID: 30523076]
  16. Commun Biol. 2020 Jun 1;3(1):277 [PMID: 32483173]
  17. Front Cell Infect Microbiol. 2020 Nov 16;10:575164 [PMID: 33330124]
  18. Microbiol Spectr. 2024 Feb 6;12(2):e0283823 [PMID: 38197658]
  19. Allergy. 2019 Mar;74(3):560-571 [PMID: 30269350]
  20. Allergy. 2011 Jul;66(7):845-52 [PMID: 21261663]
  21. Gastroenterology. 2019 Sep;157(3):793-806.e14 [PMID: 31170413]
  22. BMC Microbiol. 2011 Jun 21;11:143 [PMID: 21693040]
  23. Nat Med. 2014 Sep;20(9):1043-9 [PMID: 25129481]
  24. Methods Enzymol. 2010;470:833-55 [PMID: 20946837]
  25. Am J Respir Crit Care Med. 2019 May 1;199(9):1127-1138 [PMID: 30789747]
  26. Fish Shellfish Immunol. 2023 Jun;137:108777 [PMID: 37105423]
  27. Cell Host Microbe. 2017 Nov 8;22(5):653-666.e5 [PMID: 29120743]
  28. J Pediatr Gastroenterol Nutr. 2019 Jan;68(1):130-143 [PMID: 30540704]
  29. J Clin Med. 2019 Jul 07;8(7): [PMID: 31284694]
  30. Nutrients. 2024 Mar 11;16(6): [PMID: 38542701]
  31. J Extracell Vesicles. 2020 Jul 17;9(1):1793514 [PMID: 32944181]
  32. Acta Biomater. 2024 Aug;184:296-312 [PMID: 38871203]
  33. Exp Dermatol. 2011 Jan;20(1):48-52 [PMID: 20955203]
  34. Annu Rev Virol. 2021 Sep 29;8(1):415-435 [PMID: 34014761]
  35. J Allergy Clin Immunol. 2022 Feb;149(2):624-639 [PMID: 34363841]
  36. J Eur Acad Dermatol Venereol. 2019 Dec;33(12):2340-2348 [PMID: 31299116]
  37. Cell. 2018 Feb 8;172(4):784-796.e18 [PMID: 29358051]
  38. J Allergy Clin Immunol. 2018 Dec;142(6):1867-1883.e12 [PMID: 29522844]
  39. Nature. 2015 Apr 2;520(7545):104-8 [PMID: 25539086]
  40. Infect Immun. 1989 Dec;57(12):3783-7 [PMID: 2509368]
  41. J Invest Dermatol. 2019 Jan;139(1):146-156 [PMID: 30120937]
  42. Exp Dermatol. 2011 Feb;20(2):157-8 [PMID: 21255097]
  43. Nat Immunol. 2023 Jan;24(1):110-122 [PMID: 36550321]
  44. Sci Transl Med. 2022 Feb 2;14(630):eabj0324 [PMID: 35108061]
  45. Trends Microbiol. 2024 Apr;32(4):342-354 [PMID: 37802660]
  46. Clin Exp Allergy. 2017 Jan;47(1):85-96 [PMID: 27910159]
  47. Nat Cell Biol. 2017 Sep;19(9):1017-1026 [PMID: 28812580]
  48. Cell Host Microbe. 2019 May 8;25(5):641-655.e5 [PMID: 31006638]
  49. Immunity. 2015 Apr 21;42(4):756-66 [PMID: 25902485]
  50. J Allergy Clin Immunol. 2014 Apr;133(4):1184-94 [PMID: 24388011]
  51. Immunity. 2021 Oct 12;54(10):2321-2337.e10 [PMID: 34582748]
  52. Cell. 2018 Oct 4;175(2):372-386.e17 [PMID: 30270042]
  53. J Exp Med. 2018 Mar 5;215(3):785-799 [PMID: 29382696]
  54. Adv Wound Care (New Rochelle). 2020 Jan 1;9(1):16-27 [PMID: 31871827]
  55. Evid Based Complement Alternat Med. 2022 Sep 17;2022:4731675 [PMID: 36164402]
  56. J Clin Invest. 2022 Sep 1;132(17): [PMID: 35834333]
  57. Nature. 2022 Oct;610(7933):737-743 [PMID: 36071167]
  58. Redox Biol. 2023 Jul;63:102765 [PMID: 37269686]
  59. Cell. 2016 May 5;165(4):854-66 [PMID: 27153496]
  60. PLoS One. 2014 May 15;9(5):e94260 [PMID: 24832234]
  61. Cell Host Microbe. 2020 Aug 12;28(2):190-200 [PMID: 32791112]
  62. Science. 2022 Feb 25;375(6583):859-863 [PMID: 35201883]
  63. Int J Mol Sci. 2021 Jan 27;22(3): [PMID: 33513946]
  64. FASEB J. 2020 Apr;34(4):5282-5298 [PMID: 32067273]
  65. iScience. 2023 Oct 19;26(11):108279 [PMID: 38026194]
  66. Appl Microbiol Biotechnol. 2014 Jan;98(1):411-24 [PMID: 24265031]
  67. Nature. 2019 Nov;575(7783):519-522 [PMID: 31666702]
  68. mBio. 2015 Oct 20;6(5):e01578-15 [PMID: 26489866]
  69. Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):15061-6 [PMID: 23980152]
  70. JCI Insight. 2018 May 3;3(9): [PMID: 29720571]
  71. Front Immunol. 2021 Sep 28;12:740540 [PMID: 34650562]
  72. J Invest Dermatol. 2016 Mar;136(3):621-630 [PMID: 26739093]
  73. Arch Dermatol Res. 2009 Jun;301(5):347-55 [PMID: 18820941]
  74. Sci Total Environ. 2020 Nov 25;745:141049 [PMID: 32758727]
  75. Cell Death Dis. 2021 Mar 1;12(3):226 [PMID: 33649312]
  76. Allergy. 2023 May;78(5):1292-1306 [PMID: 36609802]
  77. Cell. 2021 Apr 15;184(8):2151-2166.e16 [PMID: 33765440]
  78. PLoS One. 2019 Apr 11;14(4):e0215206 [PMID: 30973913]
  79. Cell Rep. 2023 Oct 31;42(10):113148 [PMID: 37733587]
  80. Nat Med. 2009 Dec;15(12):1377-82 [PMID: 19966777]
  81. Sci Transl Med. 2022 Feb 16;14(632):eabh1478 [PMID: 35171653]
  82. Cell Rep Med. 2022 Feb 15;3(2):100521 [PMID: 35243421]
  83. Front Microbiol. 2016 Aug 17;7:1230 [PMID: 27582729]
  84. J Clin Invest. 2020 Jan 2;130(1):466-479 [PMID: 31815742]
  85. Cell Mol Life Sci. 2021 Feb;78(3):935-947 [PMID: 32409862]
  86. J Invest Dermatol. 2023 Aug;143(8):1613-1617.e5 [PMID: 36889664]
  87. Pharmaceutics. 2023 Oct 03;15(10): [PMID: 37896176]
  88. Cell Host Microbe. 2021 Aug 11;29(8):1235-1248.e8 [PMID: 34214492]
  89. Cell. 2021 Jul 8;184(14):3794-3811.e19 [PMID: 34166614]
  90. Allergol Int. 2022 Jul;71(3):265-277 [PMID: 35624035]
  91. Front Immunol. 2018 Feb 05;9:165 [PMID: 29459871]
  92. Nat Immunol. 2020 Sep;21(9):1034-1045 [PMID: 32661363]
  93. Adv Sci (Weinh). 2023 Nov;10(33):e2303369 [PMID: 37867255]
  94. Front Cardiovasc Med. 2022 Jun 02;9:910323 [PMID: 35722100]
  95. J Pathol. 2013 Jan;229(2):157-67 [PMID: 23023641]
  96. J Invest Dermatol. 2018 Feb;138(2):251-253 [PMID: 29389326]
  97. PLoS One. 2015 Oct 28;10(10):e0141067 [PMID: 26510097]
  98. Int J Mol Sci. 2023 Jan 31;24(3): [PMID: 36769020]
  99. Cold Spring Harb Perspect Med. 2013 Dec 01;3(12):a015362 [PMID: 24296350]
  100. Curr Biol. 2022 Aug 22;32(16):3584-3592.e4 [PMID: 35835122]
  101. Sci Adv. 2023 Jan 4;9(1):eabo7555 [PMID: 36598999]
  102. Nat Commun. 2016 Apr 21;7:11394 [PMID: 27099134]
  103. Br J Dermatol. 2019 Oct;181(4):691-699 [PMID: 31342510]
  104. Cardiovasc Res. 2014 May 1;102(2):258-69 [PMID: 24728497]
  105. Science. 2023 Apr 14;380(6641):203-210 [PMID: 37053311]
  106. Nat Immunol. 2022 Sep;23(9):1317-1323 [PMID: 35999393]
  107. Int J Biol Sci. 2022 Jun 27;18(10):4219-4232 [PMID: 35844801]
  108. Dermatoendocrinol. 2009 Mar;1(2):96-9 [PMID: 20224691]
  109. J Am Acad Dermatol. 2019 Jul;81(1):1-21 [PMID: 30502418]
  110. Clin Exp Dermatol. 2014 Mar;39(2):162-7 [PMID: 24524558]
  111. Microbiome. 2018 Sep 5;6(1):154 [PMID: 30185226]
  112. Arch Dermatol Res. 2010 Dec;302(10):745-56 [PMID: 20697725]
  113. Wound Repair Regen. 2012 Mar-Apr;20(2):253-61 [PMID: 22332802]
  114. J Invest Dermatol. 2016 Mar;136(3):559-560 [PMID: 26902125]
  115. J Invest Dermatol. 2023 Mar 11;: [PMID: 36907322]
  116. Immunity. 2019 Apr 16;50(4):892-906 [PMID: 30995505]
  117. JCI Insight. 2024 Feb 6;9(6): [PMID: 38319737]
  118. Br J Dermatol. 1994 Apr;130(4):405-14 [PMID: 7910477]
  119. J Invest Dermatol. 2017 Apr;137(4):941-950 [PMID: 28017830]
  120. Nature. 2013 Nov 21;503(7476):397-401 [PMID: 24172897]
  121. Lancet. 2012 Jan 28;379(9813):361-72 [PMID: 21880356]
  122. J Am Acad Dermatol. 2020 Apr;82(4):955-961 [PMID: 31228520]
  123. Annu Rev Virol. 2021 Sep 29;8(1):95-113 [PMID: 34255542]
  124. J Allergy Clin Immunol. 2023 Mar;151(3):737-746.e6 [PMID: 36410530]
  125. Nat Biotechnol. 2024 Jan 9;: [PMID: 38195987]
  126. PLoS One. 2012;7(7):e41480 [PMID: 22859988]
  127. Cell Host Microbe. 2022 Mar 9;30(3):301-313.e9 [PMID: 35123653]
  128. Arch Dermatol Res. 1984;276(5):333-4 [PMID: 6548356]
  129. Immunity. 2016 Mar 15;44(3):450-462 [PMID: 26982353]
  130. Metabolites. 2023 Aug 17;13(8): [PMID: 37623895]
  131. Immunity. 2024 Feb 13;57(2):319-332.e6 [PMID: 38295798]
  132. Front Cell Infect Microbiol. 2022 Mar 07;12:834135 [PMID: 35321316]
  133. J Eur Acad Dermatol Venereol. 2014 Mar;28(3):271-8 [PMID: 23905540]
  134. Sci Transl Med. 2020 Nov 18;12(570): [PMID: 33208503]
  135. Cell. 2023 Feb 2;186(3):607-620.e17 [PMID: 36640762]
  136. Curr Opin Microbiol. 2022 Dec;70:102235 [PMID: 36372041]
  137. J Allergy Clin Immunol. 2021 Jun;147(6):2305-2315.e3 [PMID: 33316284]
  138. Br J Dermatol. 2016 Mar;174(3):514-21 [PMID: 26436522]
  139. Wound Repair Regen. 2007 Jan-Feb;15(1):71-9 [PMID: 17244322]
  140. Science. 2018 Nov 23;362(6417): [PMID: 30467144]
  141. Cell Host Microbe. 2021 May 12;29(5):777-791.e6 [PMID: 33798492]
  142. Nat Med. 2021 Apr;27(4):700-709 [PMID: 33619370]
  143. Antimicrob Agents Chemother. 2012 May;56(5):2459-64 [PMID: 22290957]

Grants

  1. R01 AR074846/NIAMS NIH HHS
  2. R56 AR082660/NIAMS NIH HHS

MeSH Term

Humans
Skin
Microbiota
Symbiosis
Skin Diseases
Animals
Homeostasis
Host Microbial Interactions
Bacteria

Word Cloud

Created with Highcharts 10.0.0skincellshostmicrobialdiseasemicrobesbehaviorprovideinsightHumanvariouscommensalconstitutesubstantialcommunityreciprocalcommunicationinhabitantsupholdsmorphologicalfunctionalattributeslayerscontributingindispensablymicroenvironmentaltissuehomeostasisThusdisruptionbarrierimbalancescommunitiescanexertprofoundeffectsinfluencemediatedmetabolitesmanifestsdiverseoutcomesreviewexamineexistingknowledgenuancedexhibitedmicrobiotahealthstatesinteractionspotentialcellulartargetsfuturemicrobiota-basedtherapiespreventtreatCommensalmicroberegulation

Similar Articles

Cited By