皮肤微生物与皮肤肿瘤相关性的研究进展

doi:10.35541/cjd.20230241

Abstract

Abstract: 【Abstract】 In recent years, the incidence of skin tumors has been increasing, and patients are becoming younger, posing a great threat to human health. However, their pathogenesis and etiology are not yet fully elucidated. Multiple studies have shown that skin microbiome is closely related to the occurrence and development of skin tumors. This review summarizes microecological disorders in skin tumors, their effects on the skin barrier and skin immune system,

Key words: Skin neoplasms, Microbial consortia, Biota, Staphylococcal skin infections, Staphylococcus aureus, Immune system, Prebiotics, Skin barrier

Liu Yingying, Deng Danqi. Correlations between skin microbiome and skin tumors[J]. Chinese Journal of Dermatology,2024,e20230241. doi:10.35541/cjd.20230241

References ［49］

［1］	Richardson BN, Lin J, Buchwald ZS, et al. Skin microbiome and treatment⁃related skin toxicities in patients with cancer: a mini⁃review［J］. Front Oncol, 2022,12:924849. doi: 10.3389/fonc. 2022.924849.
［2］	Kapoor B, Gulati M, Rani P, et al. Psoriasis: interplay between dysbiosis and host immune system［J］. Autoimmun Rev, 2022,21（11）:103169. doi: 10.1016/j.autrev.2022.103169.
［3］	Schneider AM, Nolan ZT, Banerjee K, et al. Evolution of the facial skin microbiome during puberty in normal and acne skin［J］. J Eur Acad Dermatol Venereol, 2023,37（1）:166⁃175. doi: 10.1111/jdv.18616.
［4］	Gao YW, Yao X, Yang XY. Application of bioengineered bacteria in allergic diseases［J］. Int J Dermatol Venerol, 2023,6（1）:43⁃48. doi: 10.1097/JD9.0000000000000242.
［5］	Łyko M, Jankowska⁃Konsur A. The skin microbiome in cutaneous T⁃cell lymphomas （CTCL）⁃a narrative review［J］. Pathogens, 2022,11（8）:935. doi: 10.3390/pathogens11080935.
［6］	Jost M, Wehkamp U. The skin microbiome and influencing elements in cutaneous T⁃cell lymphomas［J］. Cancers （Basel）, 2022,14（5）:1324. doi: 10.3390/cancers14051324.
［7］	郑娜娜, 曾荣, 陶盈凯, 等. 环状RNA与皮肤肿瘤相关性研究进展［J］. 中华皮肤科杂志, 2023,e20210893. doi: 10.35541/cjd.20210893.
［8］	Squarzanti DF, Zavattaro E, Pizzimenti S, et al. Non⁃melanoma skin cancer: news from microbiota research［J］. Crit Rev Microbiol, 2020,46（4）:433⁃449. doi: 10.1080/1040841X.2020. 1794792.
［9］	Parida S, Sharma D. The microbiome and cancer: creating friendly neighborhoods and removing the foes within［J］. Cancer Res, 2021,81（4）:790⁃800. doi: 10.1158/0008⁃5472.CAN⁃20⁃2629.
［10］	Kennedy MS, Chang EB. The microbiome: composition and locations［J］. Prog Mol Biol Transl Sci, 2020,176:1⁃42. doi: 10. 1016/bs.pmbts.2020.08.013.
［11］	Luna PC. Skin microbiome as years go by［J］. Am J Clin Dermatol, 2020,21（Suppl 1）:12⁃17. doi: 10.1007/s40257⁃020⁃00549⁃5.
［12］	Byrd AL, Belkaid Y, Segre JA. The human skin microbiome［J］. Nat Rev Microbiol, 2018,16（3）:143⁃155. doi: 10.1038/nrmicro. 2017.157.
［13］	闫慧敏, 姜薇. 人类皮肤微生物群和皮肤疾病［J］. 中国皮肤性病学杂志, 2015,29（12）:1292⁃1294. doi: 10.13735/j.cjdv. 1001⁃7089.201412052.
［14］	Wood D, Lachner N, Tan JM, et al. A natural history of actinic keratosis and cutaneous squamous cell carcinoma microbiomes［J］. mBio, 2018,9（5）:e01432⁃18. doi: 10.1128/mBio.01432⁃18.
［15］	Blümel E, Munir Ahmad S, Nastasi C, et al. Staphylococcus aureus alpha⁃toxin inhibits CD8+ T cell⁃mediated killing of cancer cells in cutaneous T⁃cell lymphoma［J］. Oncoimmunology, 2020,9（1）:1751561. doi: 10.1080/2162402X.2020.1751561.
［16］	Nakatsuji T, Chen TH, Butcher AM, et al. A commensal strain of Staphylococcus epidermidis protects against skin neoplasia［J］. Sci Adv, 2018,4（2）:eaao4502. doi: 10.1126/sciadv.aao4502.
［17］	Mizuhashi S, Kajihara I, Sawamura S, et al. Skin microbiome in acral melanoma: Corynebacterium is associated with advanced melanoma［J］. J Dermatol, 2021,48（1）:e15⁃e16. doi: 10.1111/1346⁃8138.15633.
［18］	Mrázek J, Mekadim C, Kučerová P, et al. Melanoma⁃related changes in skin microbiome［J］. Folia Microbiol （Praha）, 2019,64（3）:435⁃442. doi: 10.1007/s12223⁃018⁃00670⁃3.
［19］	Kumar P, Brazel D, DeRogatis J, et al. The cure from within? A review of the microbiome and diet in melanoma［J］. Cancer Metastasis Rev, 2022,41（2）:261⁃280. doi: 10.1007/s10555⁃022⁃10029⁃3.
［20］	Gluud M, Pallesen E, Buus TB, et al. Malignant T cells induce skin barrier defects through cytokine⁃mediated JAK/STAT signaling in cutaneous T⁃cell lymphoma［J］. Blood, 2023,141（2）:180⁃193. doi: 10.1182/blood.2022016690.
［21］	Edslev SM, Agner T, Andersen PS. Skin microbiome in atopic dermatitis［J］. Acta Derm Venereol, 2020,100（12）:adv00164. doi: 10.2340/00015555⁃3514.
［22］	Bosman ES, Albert AY, Lui H, et al. Skin exposure to narrow band ultraviolet （UVB） light modulates the human intestinal microbiome［J］. Front Microbiol, 2019,10:2410. doi: 10.3389/fmicb.2019.02410.
［23］	Wang X，Koffi PF，English OF，et al. Staphylococcus aureus extracellular vesicles: a story of toxicity and the stress of 2020 ［J］. Toxins （Basel）, 2021,13（2）:75. doi: 10.3390/toxins13020075.
［24］	Krueger A，Mohamed A，Kolka CM，et al. Skin cancer⁃associated S. aureus strains can induce DNA damage in human keratinocytes by downregulating DNA repair and promoting oxidative stress［J］. Cancers （Basel）, 2022,14（9）:2143. doi:10.3390/cancers14092143.
［25］	Quintero⁃Fabián S, Arreola R, Becerril⁃Villanueva E, et al. Role of matrix metalloproteinases in angiogenesis and cancer［J］. Front Oncol, 2019,9:1370. doi: 10.3389/fonc.2019.01370.
［26］	Nauroy P, Nyström A. Kallikreins: Essential epidermal messengers for regulation of the skin microenvironment during homeostasis, repair and disease［J］. Matrix Biol Plus, 2020,6⁃7:100019. doi: 10.1016/j.mbplus.2019.100019.
［27］	Krueger A, Zaugg J, Chisholm S, et al. Secreted toxins from Staphylococcus aureus strains isolated from keratinocyte skin cancers mediate pro⁃tumorigenic inflammatory responses in the skin［J］. Front Microbiol, 2021,12:789042. doi: 10.3389/fmicb. 2021.789042.
［28］	Duan T，Du Y，Xing C，et al. Toll⁃like receptor signaling and its role in cell⁃mediated immunity［J］. Front Immunol, 2022,13:812774. doi:10.3389/fimmu.2022.812774.
［29］	Blohm⁃Mangone K, Burkett NB, Tahsin S, et al. Pharmacological TLR4 antagonism using topical resatorvid blocks solar UV⁃induced skin tumorigenesis in SKH⁃1 mice［J］. Cancer Prev Res （Phila）, 2018,11（5）:265⁃278. doi: 10.1158/1940⁃6207.CAPR⁃17⁃0349.
［30］	Mann JE, Ludwig ML, Kulkarni A, et al. Microbe⁃mediated activation of Toll⁃like receptor 2 drives PDL1 expression in HNSCC［J］. Cancers （Basel）, 2021,13（19）:4782. doi: 10.3390/cancers13194782.
［31］	Kiatsurayanon C, Ogawa H, Niyonsaba F. The role of host defense peptide human β⁃defensins in the maintenance of skin barriers［J］. Curr Pharm Des, 2018,24（10）:1092⁃1099. doi: 10. 2174/1381612824666180327164445.
［32］	Madhusudhan N，Pausan MR，Halwachs B，et al. Molecular profiling of keratinocyte skin tumors links Staphylococcus aureus overabundance and increased human β⁃defensin⁃2 expression to growth promotion of squamous cell carcinoma ［J］. Cancers （Basel）, 2020,12（3）:541. doi: 10.3390/cancers12030541.
［33］	Nakagawa S, Matsumoto M, Katayama Y, et al. Staphylococcus aureus virulent PSMα peptides induce keratinocyte alarmin release to orchestrate IL⁃17⁃dependent skin inflammation［J］. Cell Host Microbe, 2017,22（5）:667⁃677.e5. doi: 10.1016/j.chom. 2017.10.008.
［34］	Ridaura VK, Bouladoux N, Claesen J, et al. Contextual control of skin immunity and inflammation by Corynebacterium［J］. J Exp Med, 2018,215（3）:785⁃799. doi: 10.1084/jem.20171079.
［35］	Sakamoto R, Kajihara I, Mijiddorj T, et al. Existence of Staphylococcus aureus correlates with the progression of extramammary Paget′s disease: potential involvement of interleukin⁃17 and M2⁃like macrophage polarization［J］. Eur J Dermatol, 2021,31（1）:48⁃54. doi: 10.1684/ejd.2021.3972.
［36］	Willerslev⁃Olsen A, Krejsgaard T, Lindahl LM, et al. Staphylococcal enterotoxin A （SEA） stimulates STAT3 activation and IL⁃17 expression in cutaneous T⁃cell lymphoma［J］. Blood, 2016,127（10）:1287⁃1296. doi: 10.1182/blood⁃2015⁃08⁃662353.
［37］	Willerslev⁃Olsen A, Gjerdrum L, Lindahl LM, et al. Staphylococcus aureus induces signal transducer and activator of transcription 5⁃dependent miR⁃155 expression in cutaneous T⁃cell lymphoma［J］. J Invest Dermatol, 2021,141（10）:2449⁃2458. doi: 10.1016/j.jid.2021.01.038.
［38］	Lindahl LM, Willerslev⁃Olsen A, Gjerdrum L, et al. Antibiotics inhibit tumor and disease activity in cutaneous T⁃cell lymphoma［J］. Blood, 2019,134（13）:1072⁃1083. doi: 10.1182/blood.2018 888107.
［39］	Blümel E, Willerslev⁃Olsen A, Gluud M, et al. Staphylococcal alpha⁃toxin tilts the balance between malignant and non⁃malignant CD4+ T cells in cutaneous T⁃cell lymphoma［J］. Oncoimmunology, 2019,8（11）:e1641387. doi: 10.1080/2162402X. 2019.1641387.
［40］	Glatthardt T，Campos JC de M，Chamon RC，et al. Small molecules produced by commensal Staphylococcus epidermidis disrupt formation of biofilms by staphylococcus aureus ［J］. Appl Environ Microbiol, 2020,86（5）:e02539⁃19. doi:10.1128/AEM. 02539⁃19.
［41］	Wang Z, Choi JE, Wu CC, et al. Skin commensal bacteria Staphylococcus epidermidis promote survival of melanocytes bearing UVB⁃induced DNA damage, while bacteria Propionibacterium acnes inhibit survival of melanocytes by increasing apoptosis［J］. Photodermatol Photoimmunol Photomed, 2018,34（6）:405⁃414. doi: 10.1111/phpp.12411.
［42］	Li H, Goh BN, Teh WK, et al. Skin commensal Malassezia globosa secreted protease attenuates Staphylococcus aureus biofilm formation［J］. J Invest Dermatol, 2018,138（5）:1137⁃1145. doi: 10.1016/j.jid.2017.11.034.
［43］	Wood DLA，Lachner N，Tan J⁃M，et al. A natural history of actinic keratosis and cutaneous squamous cell carcinoma microbiomes［J］. mBio, 2018,9（5）:e01432⁃18. doi: 10.1128/mBio.01432⁃18.
［44］	Sato Y, Fujimura T, Tanita K, et al. Malassezia⁃derived aryl hydrocarbon receptor ligands enhance the CCL20/Th17/soluble CD163 pathogenic axis in extra⁃mammary Paget′s disease［J］. Exp Dermatol, 2019,28（8）:933⁃939. doi: 10.1111/exd.13944.
［45］	Friedrich AD, Campo VE, Cela EM, et al. Oral administration of lipoteichoic acid from Lactobacillus rhamnosus GG overcomes UVB⁃induced immunosuppression and impairs skin tumor growth in mice［J］. Eur J Immunol, 2019,49（11）:2095⁃2102. doi: 10.1002/eji.201848024.
［46］	Kianmehr S, Jahani M, Moazzen N, et al. The potential of probiotics for treating skin disorders: a concise review［J］. Curr Pharm Biotechnol, 2022,23（15）:1851⁃1863. doi: 10.2174/138920 1023666220411090301.
［47］	Lizardo M，Magalhães RM，Tavaria FK. Probiotic adhesion to skin keratinocytes and underlying mechanisms ［J］. Biology （Basel）, 2022,11（9）:1372. doi:10.3390/biology11091372.
［48］	Petrov A, Ćorović M, Milivojević A, et al. Prebiotic effect of galacto⁃oligosaccharides on the skin microbiota and determination of their diffusion properties［J］. Int J Cosmet Sci, 2022,44（3）:309⁃319. doi: 10.1111/ics.12778.
［49］	Le Bourgot C, Meunier C, Gaio E, et al. Effects of short chain fructo⁃oligosaccharides on selected skin bacteria［J］. Sci Rep, 2022,12（1）:9702. doi: 10.1038/s41598⁃022⁃13093⁃5.

[1]	Combination of Traditional and Western Medicine Dermatology, Chinese Society of Dermatology, China Dermatologist Association. Expert consensus on reflectance confocal microscopic features of common non-melanocytic skin tumors （2025 edition） [J]. Chinese Journal of Dermatology, 2025, 58(1): 20-33.
[2]	Ai Fangting, Sun Zijun, Miao Guoying, Yao Chunxia. Role of calcium-sensing receptors in the pathophysiology of skin of the elderly [J]. Chinese Journal of Dermatology, 2025, 58(1): 76-79.
[3]	Zhang Jiaqi, Wu Fan, Han Yuqing, Liu Qi, Pan Yao. Application of multi-photon microscopy in dermatology [J]. Chinese Journal of Dermatology, 2024, 57(9): 857-862.
[4]	Hao Feng, Liu Guoyan. Application of optical coherence tomography in dermatology [J]. Chinese Journal of Dermatology, 2024, 57(9): 853-857.
[5]	Combination of Traditional and Western Medicine Dermatology, Chinese Society of Dermatology, China Dermatologist Association. Expert consensus on the application of reflectance confocal microscopy in common melanocytic skin tumors（2024） [J]. Chinese Journal of Dermatology, 2024, 57(9): 775-784.
[6]	Wang Yimeng, Wu Wenting, Zhang Qian, Zhang Chunlei, Li Weiwei. Clinical and pathological diagnoses of 389 patients with primary solid tumors localized in the perianal and external genitalia regions [J]. Chinese Journal of Dermatology, 2024, 57(4): 316-323.
[7]	Li Jiaqi, Liang Mengchen, Wu Xinyi, Zhang Qiujing, Li Sitong, Mo Xiaohui, Ju Qiang. Staphylococcus epidermidis phylotypes in hair follicles in skin lesions of patients with moderate acne vulgaris: a preliminary study [J]. Chinese Journal of Dermatology, 2024, 57(4): 295-301.
[8]	Ma Tongchuan, Deng Tingyue, Xiao Fengli. Associations between smoking and atopic dermatitis [J]. Chinese Journal of Dermatology, 2024, 0(3): 20220793-e20220793.
[9]	Enze LI Lu CHEN Chu-Qiao ZHANG Jiao qingqing JI Jiang. Correlations of gut microbiota and short-chain fatty acids with chronic spontaneous urticaria [J]. Chinese Journal of Dermatology, 2024, 0(3): 20230310-e20230310.
[10]	Hong Yongzhen, Wang Qian, Liang Junqin, . Application of next-generation sequencing in the field of non-hereditary dermatoses [J]. Chinese Journal of Dermatology, 2024, 0(3): 20220436-e20220436.
[11]	Sun Jiayi, Song Xiuzu. Role of transient receptor potential vanilloid type 4 channel in skin diseases [J]. Chinese Journal of Dermatology, 2024, 57(12): 1149-1152.
[12]	Li Chunying, Chen Jianru, Li Shuli. Metabolic reconfiguration in vitiligo: progress and future [J]. Chinese Journal of Dermatology, 2024, 57(1): 8-11.
[13]	Chen Chunli, Yan Siyu, Wang Dan, Gao Lihua, Tan Lina, Tang Siyuan, Liu Wei, Zeng Jinrong, Lu Jianyun, . Efficacy of acidified aliphatic ester in the treatment of atopic dermatitis in mouse models and preliminary exploration of its mechanisms of action [J]. Chinese Journal of Dermatology, 2023, 56(9): 822-831.
[14]	Yue Chao, Duan Mengying, Wang Tao, Zhang Manyu, Dai Yeqin, Peng Jianzhong, Song Xiuzu. Application of the upper eyelid orbicularis oculi myocutaneous island flap in repairing secondary defects after resection of eyelid and periorbital skin tumors: a retrospective analysis of 28 cases [J]. Chinese Journal of Dermatology, 2023, 56(9): 862-865.
[15]	China Dermatologist Association. Guidance on application of moisturizers and emollients: an expert consensus （2023） [J]. Chinese Journal of Dermatology, 2023, 56(8): 711-717.

Correlations between skin microbiome and skin tumors

PDF

PDF (Mobile)

Knowledge

Abstract

Cite this article

share this article

References ［49］

Related Articles 15

Metrics

Comments

Recommended 10