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Review Articles

Non-Melanoma Skin Cancer: news from microbiota research

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Pages 433-449 | Received 09 Mar 2020, Accepted 17 Jun 2020, Published online: 21 Jul 2020

References

  • Abdallah F, Mijouin L, Pichon C. 2017. Skin immune landscape: inside and outside the organism. Mediators Inflamm. 2017:5095293.
  • Abel EL, Angel JM, Kiguchi K, DiGiovanni J. 2009. Multi-stage chemical carcinogenesis in mouse skin: fundamentals and applications. Nat Protoc. 4(9):1350–1362.
  • Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G. 2006. Inflammation and cancer: how hot is the link? Biochem Pharmacol. 72(11):1605–1621.
  • Altoparlak U, Koca O, Koca T. 2011. Incidence and risk factors of the secondary skin infections in patients with radiodermatitis. EAJM. 42(3):177–181.
  • Arck P, Handjiski B, Hagen E, Pincus M, Bruenahl C, Bienenstock J, Paus R. 2010. Is there a “gut-brain-skin axis”? Exp Dermatol. 19(5):401–405.
  • Azzimonti B, Dell'Oste V, Borgogna C, Mondini M, Gugliesi F, De Andrea M, Chiorino G, Scatolini M, Ghimenti C, Landolfo S, et al. 2009. The epithelial-mesenchymal transition induced by keratinocyte growth conditions is overcome by E6 and E7 from HPV16, but not HPV8 and HPV38: characterization of global transcription profiles. Virology. 388(2):260–269.
  • Balkwill F, Mantovani A. 2001. Inflammation and cancer: back to Virchow? Lancet. 357(9255):539–545.
  • Barré-Sinoussi F, Montagutelli X. 2015. Animal models are essential to biological research: issues and perspectives. Future Sci OA. 1(4):FSO63.
  • Barton V, Armeson K, Hampras S, Ferris LK, Visvanathan K, Rollison D, Alberg AJ. 2017. Nonmelanoma skin cancer and risk of all-cause and cancer-related mortality: a systematic review. Arch Dermatol Res. 309(4):243–251.
  • Bhatt AP, Redinbo MR, Bultman SJ. 2017. The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 67(4):326–344.
  • Borgogna C, Zavattaro E, De Andrea M, Griffin HM, Dell'Oste V, Azzimonti B, Landini MM, Peh WL, Pfister H, Doorbar J, et al. 2012. Characterization of beta papillomavirus E4 expression in tumours from Epidermodysplasia Verruciformis patients and in experimental models. Virology. 423(2):195–204.
  • Borkowski AW, Gallo RL. 2011. The coordinated response of the physical and antimicrobial peptide barriers of the skin. J Invest Dermatol. 131(2):285–287.
  • Bosman ES, Albert AY, Lui H, Dutz JP, Vallance BA. 2019. Skin exposure to narrow band Ultraviolet (UVB) light modulates the human intestinal microbiome. Front Microbiol. 10:410.
  • Bouilly-Gauthier D, Jeannes C, Maubert Y, Duteil L, Queille-Roussel C, Piccardi N, Montastier C, Manissier P, Piérard G, Ortonne J-P. 2010. Clinical evidence of benefits of a dietary supplement containing probiotic and carotenoids on ultraviolet-induced skin damage. Br J Dermatol. 163(3):536–543.
  • Boursi B, Mamtani R, Haynes K, Yang Y-X. 2015. Recurrent antibiotics exposure may promote cancer formation – another step in understanding the role of the human microbiota? Eur J Cancer. 51(17):2655–2664.
  • Bouslimani A, da Silva R, Kosciolek T, Janssen S, Callewaert C, Amir A, Dorrestein K, Melnik AV, Zaramela LS, Kim JM, et al. 2019. The impact of skin care products on skin chemistry and microbiome dynamics. BMC Biol. 17(1):47.
  • Brandwein M, Bentwich Z, Steinberg D. 2017. Endogenous antimicrobial peptide expression in response to bacterial epidermal colonization. Front Immunol. 8:1637.
  • Bultman SJ. 2014. Emerging roles of the microbiome in cancer. Carcinogenesis. 35(2):249–255.
  • Byrd AL, Belkaid Y, Segre JA. 2018. The human skin microbiome. Nat Rev Microbiol. 16(3):143–155.
  • Calzavara-Pinton P, Rossi MT, Sala R, Venturini M. 2012. Photodynamic antifungal chemotherapy. Photochem Photobiol. 88(3):512–522.
  • Candi E, Schmidt R, Melino G. 2005. The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol. 6(4):328–340.
  • Catalano E, Cochis A, Varoni E, Rimondini L, Azzimonti B. 2013. Tissue-engineered skin substitutes: an overview. J Artif Organs. 16(4):397–403.
  • Chang HW, Yan D, Singh R, Liu J, Lu X, Ucmak D, Lee K, Afifi L, Fadrosh D, Leech J, et al. 2018. Alteration of the cutaneous microbiome in psoriasis and potential role in Th17 polarization. Microbiome. 6(1):154.
  • Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, Boselli L, Routier E, Cassard L, Collins M, et al. 2019. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol. 30(12):2012.
  • Chen AC, Halliday GM, Damian DL. 2013. Non-melanoma skin cancer: carcinogenesis and chemoprevention. Pathology. 45(3):331–341.
  • Chen J, Domingue JC, Sears CL. 2017. Microbiota dysbiosis in select human cancers: evidence of association and causality. Semin Immunol. 32:25–34.
  • Chen Q, Li R, Zhao X, Liang B, Ma S, Li Z, Zhu H. 2016. Prevention of ultraviolet radiation-induced immunosuppression by sunscreen in Candida albicans-induced delayed-type hypersensitivity. Mol Med Rep. 14(1):202–208.
  • Chen X, Bode AM, Dong Z, Cao Y. 2016. The epithelial-mesenchymal transition (EMT) is regulated by oncoviruses in cancer. Faseb J. 30(9):3001–3010.
  • Chen YE, Fischbach MA, Belkaid Y. 2018. Skin microbiota-host interactions. Nature. 553(7689):427–436.
  • Chung LM, Liang JA, Lin CL, Sun LM, Kao CH. 2017. Cancer risk in patients with candidiasis: a nationwide population-based cohort study. Oncotarget. 8(38):63562–63573.
  • Cipolat S, Hoste E, Natsuga K, Quist SR, Watt FM. 2014. Epidermal barrier defects link atopic dermatitis with altered skin cancer susceptibility. Elife. 3:e01888.
  • Coates M, Blanchard S, MacLeod AS. 2018. Innate antimicrobial immunity in the skin: a protective barrier against bacteria, viruses, and fungi. PLoS Pathog. 14(12):e1007353.
  • Cogen AL, Yamasaki K, Sanchez KM, Dorschner RA, Lai Y, MacLeod DT, Torpey JW, Otto M, Nizet V, Kim JE, et al. 2010. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol. 130(1):192–200.
  • Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. 2009. Bacterial community variation in human body habitats across space and time. Science. 326(5960):1694–1697.
  • Cundell AM. 2018. Microbial ecology of the human skin. Microb Ecol. 76(1):113–120.
  • Cyprian FS, Al-Antary N, Al Moustafa AE. 2018. HER-2/Epstein-Barr virus crosstalk in human gastric carcinogenesis: a novel concept of oncogene/oncovirus interaction. Cell Adh Migr. 12(1):1–4.
  • Cyprian FS, Al-Farsi HF, Vranic S, Akhtar S, Al Moustafa AE. 2018. Epstein-barr virus and human papillomaviruses interactions and their roles in the initiation of epithelial-mesenchymal transition and cancer progression. Front Oncol. 8(111):111.
  • Dell'Oste V, Azzimonti B, Mondini M, De Andrea M, Borgogna C, Mesturini R, Accardi R, Tommasino M, Landolfo S, Dianzani U, et al. 2008. Altered expression of UVB-induced cytokines in human papillomavirus-immortalized epithelial cells. J Gen Virol. 89(Pt 10):2461–2466.
  • Diernaes J, Heje M, Pfeiffer-Jensen M, Lorentzen HF. 2019. Non-melanoma skin cancer as a possible adverse event due to anti-interleukin-6 treatment. Scand J Rheumatol. 48(1):82–84.
  • Dinulos JG, Mentele L, Fredericks LP, Dale BA, Darmstadt GL. 2003. Keratinocyte expression of human beta defensin 2 following bacterial infection: role in cutaneous host defense. Clin Diagn Lab Immunol. 10(1):161–166.
  • Dong M, Meng Z, Kuerban K, Qi F, Liu J, Wei Y, Wang Q, Jiang S, Feng M, Ye L. 2018. Diosgenin promotes antitumor immunity and PD-1 antibody efficacy against melanoma by regulating intestinal microbiota. Cell Death Dis. 9(10):1039.
  • Dréno B, Araviiskaia E, Berardesca E, Gontijo G, Sanchez Viera M, Xiang LF, Martin R, Bieber T. 2016. Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatol Venereol. 30(12):2038–2047.
  • Dréno B. 2019. The microbiome, a new target for ecobiology in dermatology. Eur J Dermatol. 29(S1):15–18.
  • Duarte AF, Sousa-Pinto B, Freitas A, Delgado L, Costa-Pereira A, Correia O. 2018. Skin cancer healthcare impact: a nation-wide assessment of an administrative database. Cancer Epidemiol. 56:154–160.
  • Egert M, Simmering R, Riedel CU. 2017. The association of the skin microbiota with health, immunity, and disease. Clin Pharmacol Ther. 102(1):62–69.
  • Fang W, Zhang J, Hong S, Zhan J, Chen N, Qin T, Tang Y, Zhang Y, Kang S, Zhou T, et al. 2014. EBV-driven LMP1 and IFN-γ up-regulate PD-L1 in nasopharyngeal carcinoma: implications for oncotargeted therapy. Oncotarget. 5(23):12189–12202.
  • Faries MB, Mozzillo N, Kashani-Sabet M, Thompson JF, Kelley MC, DeConti RC, Lee JE, Huth JF, Wagner J, Dalgleish A, MMAIT-IV Clinical Trial Group, et al. 2017. Long-term survival after complete surgical resection and adjuvant immunotherapy for distant melanoma metastases. Ann Surg Oncol. 24(13):3991–4000.
  • Findley K, Grice EA. 2014. The skin microbiome: a focus on pathogens and their association with skin disease. PLoS Pathog. 10(10):e1004436.
  • Friedrich AD, Campo VE, Cela EM, Morelli AE, Shufesky WJ, Tckacheva OA, Leoni J, Paz ML, Larregina AT, González Maglio DH. 2019. Oral administration of lipoteichoic acid from Lactobacillus rhamnosus GG overcomes UVB-induced immunosuppression and impairs skin tumor growth in mice. Eur J Immunol. 49(11):2095–2102.
  • Fyhrquist N, Salava A, Auvinen P, Lauerma A. 2016. Skin biomes. Curr Allergy Asthma Rep. 16(5):40.
  • Gaitanis G, Velegraki A, Magiatis P, Pappas P, Bassukas ID. 2011. Could Malassezia yeasts be implicated in skin carcinogenesis through the production of aryl-hydrocarbon receptor ligands? Med Hypotheses. 77(1):47–51.
  • Gallo RL, Nakatsuji T. 2011. Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol. 131(10):1974–1980.
  • Gallo RL. 2017. Human skin is the largest epithelial surface for interaction with microbes. J Invest Dermatol. 137(6):1213–1214.
  • Gilaberte Y, Aspiroz C, Alejandre C, Rezusta A. 2015. Malassezia growth on peritumoral skin after routine methyl-5-aminoluvulinate Photodynamic Therapy for actinic keratosis and Nonmelanoma Skin cancer. Actas Dermosifiliogr. 106(1):70–77.
  • Gong J, Chehrazi-Raffle A, Placencio-Hickok V, Guan M, Hendifar A, Salgia R. 2019. The gut microbiome and response to immune checkpoint inhibitors: preclinical and clinical strategies. Clin Transl Med. 8(1):9.
  • Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, Dantas G, Gordon JI. 2011. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci Usa. 108(15):6252–6257.
  • Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. 2018. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 359(6371):97–103.
  • Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Bouffard GG, Blakesley RW, Murray PR, Green ED, et al. 2009. Topographical and temporal diversity of the human skin microbiome. Science. 324(5931):1190–1192.
  • Grice EA, Kong HH, Renaud G, Young AC, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA, NISC Comparative Sequencing Program 2008. A diversity profile of the human skin microbiota. Genome Res. 18(7):1043–1050.
  • Grice EA, Segre JA. 2011. The skin microbiome. Nat Rev Microbiol. 9(4):244–253.
  • Guéniche A, Philippe D, Bastien P, Blum S, Buyukpamukcu E, Castiel-Higounenc I. 2009. Castiel-Higounenc, I. Probiotics for photoprotection. Dermatoendocrinol. 1(5):275–279.
  • Hara H, Shibata H, Nakano K, Abe T, Uosaki H, Ohnuki T, Hishikawa S, Kunita S, Watanabe M, Nureki O, et al. 2018. Production and rearing of germ-free X-SCID pigs. Exp Anim. 67(2):139–146.
  • Hennings H, Glick AB, Lowry DT, Krsmanovic LS, Sly LM, Yuspa SH. 1993. FVB/N mice: an inbred strain sensitive to the chemical induction of squamous cell carcinomas in the skin. Carcinogenesis. 14(11):2353–2358.
  • Hoste E, Arwert EN, Lal R, South AP, Salas-Alanis JC, Murrell DF, Donati G, Watt FM. 2015. Innate sensing of microbial products promotes wound-induced skin cancer. Nat Commun. 6:5932.
  • Howard MD, Su JC, Chong AH. 2018. Skin cancer following solid organ transplantation: a review of risk factors and models of care. Am J Clin Dermatol. 19(4):585–597.
  • Huang PY, Balmain A. 2014. Modeling cutaneous squamous carcinoma development in the mouse. Cold Spring Harb Perspect Med. 4(9):a013623.
  • Hugenholtz F, de Vos WM. 2018. Mouse models for human intestinal microbiota research: a critical evaluation. Cell Mol Life Sci. 75(1):149–160.
  • Humphries A, Daud A. 2018. The gut microbiota and immune checkpoint inhibitors. Hum Vaccin Immunother. 14(9):2178–2182.
  • Iannitti T, Palmieri B. 2010. Therapeutical use of probiotic formulations in clinical practice. Clin Nutr. 29(6):701–725.
  • Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, et al. 2013. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 342(6161):967–970.
  • Jo JH, Kennedy EA, Kong HH. 2017. Topographical and physiological differences of the skin mycobiome in health and disease. Virulence. 8(3):324–333.
  • Kennedy EA, Connolly J, Hourihane JO, Fallon PG, McLean WHI, Murray D, Jo JH, Segre JA, Kong HH, Irvine AD. 2017. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol. 139(1):166–172.
  • Keshari S, Balasubramaniam A, Myagmardoloonjin B, Herr DR, Negari IP, Huang CM. 2019. Butyric acid from probiotic Staphylococcus epidermidis in the skin microbiome down-regulates the ultraviolet-induced pro-inflammatory IL-6 cytokine via short-chain fatty acid receptor. IJMS. 20(18):4477.
  • Kim TH, Ananthaswamy HN, Kripke ML, Ullrich SE. 2003. Advantages of using hairless mice versus haired mice to test efficacy against photoimmune suppression. Photochem Photobiol. 78(1):37–42.
  • Knackstedt R, Knackstedt T, Gatherwright J. 2020. The role of topical probiotics in skin conditions: a systematic review of animal and human studies and implications for future therapies. Exp Dermatol. 29(1):15–21.
  • Kohorst JJ, Kimball AB, Davis MD. 2015. Systemic associations of hidradenitis suppurativa. J Am Acad Dermatol. 73(5 Suppl 1):S27–S35.
  • Krutmann J. 2012. Pre- and probiotics for human skin. Clin Plast Surg. 39(1):59–64.
  • Kullander J, Forslund O, Dillner J. 2009. Staphylococcus aureus and squamous cell carcinoma of the skin. Cancer Epidemiol Biomarkers Prev. 18(2):472–478.
  • Kumar S, Mahajan BB, Kamra N. 2014. Future perspective of probiotics in dermatology: an old wine in new bottle. Dermatol Online J. 20(9).
  • Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, Wu Z-R, Hooper LV, Schmidt RR, von Aulock S, et al. 2009. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 15(12):1377–1382.
  • Langan EA, Griffiths CEM, Solbach W, Knobloch JK, Zillikens D, Thaçi D. 2018. The role of the microbiome in psoriasis: moving from disease description to treatment selection? Br J Dermatol. 178(5):1020–1027.
  • Lee GR, Maarouf M, Hendricks AJ, Lee DE, Shi VY. 2019. Topical probiotics: the unknowns behind their rising popularity. Dermatol Online J. 25(5).
  • Lee JA, Ko JH, Jung BG, Kim TH, Hong JI, Park YS, Lee B. J. 2013. Fermented Prunus mume with probiotics inhibits 7,12-dimethylbenz[a]anthracene and 12-O-Tetradecanoyl phorbol-13-acetate induced skin carcinogenesis through alleviation of oxidative stress. Asian Pac J Cancer Prev. 14(5):2973–2978.
  • Lee YB, Byun EJ, Kim AHS. 2019. Potential role of the microbiome in acne: a comprehensive review. J Clin Med. 8(7):E987.
  • Li H, Goh BN, Teh WK, Jiang Z, Goh JPZ, Goh A, Wu G, Hoon SS, Raida M, Camattari A, et al. 2018. Skin commensal Malassezia globosa secreted protease attenuates Staphylococcus aureus biofilm formation. J Invest Dermatol. 138(5):1137–1145.
  • Li Y, Tinoco R, Elmén L, Segota I, Xian Y, Fujita Y, Sahu A, Zarecki R, Marie K, Feng Y, et al. 2019. Gut microbiota dependent anti-tumor immunity restricts melanoma growth in Rnf5-/- mice. Nat Commun. 10(1):1492.
  • Limon JJ, Skalski JH, Underhill DM. 2017. Commensal fungi in health and disease. Cell Host Microbe. 22(2):156–165.
  • Lomas A, Leonardi‐Bee J, Bath‐Hextall F. 2012. Bath-Hextall, F.A systematic review of worldwide incidence of nonmelanoma skin cancer. Br. J. Dermatol. 166(5):1069–1080.
  • Lotem M, Peretz T, Drize O, Gimmon Z, Ad El D, Weitzen R, Goldberg H, Ben David I, Prus D, Hamburger T, et al. 2002. Autologous cell vaccine as a postoperative adjuvant treatment for high-risk melanoma patients (AJCC stages III and IV). The new American Joint Committee on Cancer. Br J Cancer. 86(10):1534–1539.
  • Ma Y, Madupu R, Karaoz U, Nossa CW, Yang L, Yooseph S, Yachimski PS, Brodie EL, Nelson KE, Pei Z. 2014. Human Papillomavirus community in healthy persons, defined by metagenomics analysis of human microbiome projects shotgun sequencing data sets. J Virol. 88(9):4786–4797.
  • Macpherson AJ, McCoy KD. 2015. Standardised animal models of host microbial mutualism. Mucosal Immunol. 8(3):476–486.
  • Madhusudhan N, Pausan MR, Halwachs B, Durdević M, Windisch M, Kehrmann J, Patra VK, Wolf P, Boukamp P, Moissl-Eichinger C, et al. 2020. Molecular profiling of keratinocyte skin tumors links Staphylococcus aureus overabundance and increased human beta-defensin-2 expression to growth promotion of squamous cell carcinoma. Cancers (Basel). 12(3):541.
  • Maguire M, Maguire G. 2017. The role of microbiota, and probiotics and prebiotics in skin health. Arch Dermatol Res. 309(6):411–421.
  • Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. 2012. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 13(6):607–615.
  • Martín R, Bermúdez-Humarán LG, Langella P. 2016. Gnotobiotic rodents: an in vivo model for the study of microbe-microbe interactions. Front Microbiol. 7:409.
  • Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF. 2018. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 359(6371):104–108.
  • McQuade JL, Daniel CR, Helmink BA, Wargo JA. 2019. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol. 20(2):e77–e91.
  • Melancon E, Gomez De La Torre Canny S, Sichel S, Kelly M, Wiles TJ, Rawls JF, Eisen JS, Guillemin K. 2017. Best practices for germ-free derivation and gnotobiotic zebrafish husbandry. Methods Cell Biol. 138:61–100.
  • Moqbil S, Kurnatowski P. 2012. Secretion of hydrolytic enzymes by fungal strains, isolated from patients with malignant tumors of head and neck, before, during and after radiotherapy. Ann Parasitol. 58(1):27–35.
  • Mrázek J, Mekadim C, Kučerová P, Švejstil R, Salmonová H, Vlasáková J, Tarasová R, Čížková J, Červinková M. 2019. Melanoma-related changes in skin microbiome. Folia Microbiol (Praha)). 64(3):435–442.
  • Musthaq S, Mazuy A, Jakus J. 2018. The microbiome in dermatology. Clin Dermatol. 36(3):390–398.
  • Nakagawa S, Matsumoto M, Katayama Y, Oguma R, Wakabayashi S, Nygaard T, Saijo S, Inohara N, Otto M, Matsue H, et al. 2017. Staphylococcus aureus virulent PSMα peptides induce keratinocyte alarmin release to orchestrate IL-17-dependent skin inflammation. Cell Host Microbe. 22(5):667–677.e5.
  • Nakatsuji T, Chen TH, Butcher AM, Trzoss LL, Nam SJ, Shirakawa KT, Zhou W, Oh J, Otto M, Fenical W, et al. 2018. A commensal strain of Staphylococcus epidermidis protects against skin neoplasia. Sci Adv. 4(2):eaao4502.
  • Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL. 2013. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 4:1431.
  • Natsuga K, Cipolat S, Watt FM. 2016. Increased bacterial load and expression of antimicrobial peptides in skin of barrier-deficient mice with reduced cancer susceptibility. J Invest Dermatol. 136(1):99–106.
  • Nguyen TL, Vieira-Silva S, Liston A, Raes J. 2015. How informative is the mouse for human gut microbiota research? Dis Model Mech. 8(1):1–16.
  • Niehues H, Bouwstra JA, El Ghalbzouri A, Brandner JM, Zeeuwen PLJM, van den Bogaard EH. 2018. 3D skin models for 3R research: the potential of 3D reconstructed skin models to study skin barrier function. Exp Dermatol. 27(5):501–511.
  • Nishida S, Tsuboi A, Tanemura A, Ito T, Nakajima H, Shirakata T, Morimoto S, Fujiki F, Hosen N, Oji Y, et al. 2019. Immune adjuvant therapy using Bacillus Calmette-Guérin cell wall skeleton (BCG-CWS) in advanced malignancies: a phase 1 study of safety and immunogenicity assessments. Medicine (Baltimore)). 98(33):e16771.
  • Niyonsaba F, Ushio H, Nakano N, Ng W, Sayama K, Hashimoto K, Nagaoka I, Okumura K, Ogawa H. 2007. Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J Invest Dermatol. 127(3):594–604.
  • O'Neill CA, Monteleone G, McLaughlin JT, Paus R. 2016. The gut-skin axis in health and disease: a paradigm with therapeutic implications. Bioessays. 38(11):1167–1176.
  • Outh-Gauer S, Alt M, Le Tourneau C, Augustin J, Broudin C, Gasne C, Denize T, Mirghani H, Fabre E, Ménard M, et al. 2018. Immunotherapy in head and neck cancers: a new challenge for immunologists, pathologists and clinicians. Cancer Treat Rev. 65:54–64.
  • Peguet-Navarro J, Dezutter-Dambuyant C, Buetler T, Leclaire J, Smola H, Blum S, Bastien P, Breton L, Gueniche A. 2008. Supplementation with oral probiotic bacteria protects human cutaneous immune homeostasis after UV exposure-double blind, randomized, placebo controlled clinical trial. Eur J Dermatol. 18(5):504–511.
  • Perrins N, Gaudiano F, Bond R. 2007. Carriage of Malassetia spp.Yeasts in cats with diabetes mellitus, hyperthyroidism and neoplasia. Med Mycol. 45(6):541–546.
  • Rademacher F, Simanski M, Gläser R, Harder J. 2018. Skin microbiota and human 3D skin models. Exp Dermatol. 27(5):489–494.
  • Rahmati Roudsari M, Karimi R, Sohrabvandi S, Mortazavian AM. 2015. Health effects of probiotics on the skin. Crit Rev Food Sci Nutr. 55(9):1219–1240.
  • Randall MJ, Jüngel A, Rimann M, Wuertz-Kozak K. 2018. Advances in the biofabrication of 3D skin in vitro: healthy and pathological models. Front Bioeng Biotechnol. 6:154.
  • Rippke F, Berardesca E, Weber TM. 2018. pH and microbial infections. Curr Probl Dermatol. 54:87–94.
  • Rollison DE, Viarisio D, Amorrortu RP, Gheit T, Tommasino M. 2019. An emerging issue in oncogenic virology: the role of beta human papillomavirus types in the development of cutaneous squamous cell carcinoma. J Virol. 93(7):18.
  • Rossi G, Pezzuto A, Sini C, Tuzi A, Citarella F, McCusker MG, Nigro O, Tanda E, Russo A. 2019. Concomitant medications during immune checkpoint blockage in cancer patients: novel insights in this emerging clinical scenario. Crit Rev Oncol Hematol. 142:26–34.
  • Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al. 2018. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 359(6371):91–97.
  • Russell DA, Ross RP, Fitzgerald GF, Stanton C. 2011. Metabolic activities and probiotic potential of bifidobacteria. Int J Food Microbiol. 149(1):88–105.
  • Salava A, Lauerma A. 2014. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 4:33.
  • Samaras V, Rafailidis PI, Mourtzoukou EG, Peppas G, Falagas ME. 2010. Chronic bacterial and parasitic infections and cancer: a review. J Infect Dev Ctries. 4(5):267–281.
  • Sanford JA, Gallo RL. 2013. Functions of the skin microbiota in health and disease. Semin Immunol. 25(5):370–377.
  • Schellhammer PF, Ladaga LE, Fillion MB. 1986. Bacillus Calmette-Guerin for superficial transitional cell carcinoma of the bladder . J Urol. 135(2):261–264.
  • Sherwani MA, Tufail S, Muzaffar AF, Yusuf N. 2018. The skin microbiome and immune system: potential target for chemoprevention? Photodermatol Photoimmunol Photomed. 34(1):25–34.
  • Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre M-L, et al. 2015. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 350(6264):1084–1089.
  • Skalsky RL, Cullen BR. 2015. EBV noncoding RNAs. Curr Top Microbiol Immunol. 391:181–217.
  • Sloot S, Rashid OM, Sarnaik AA, Zager JS. 2016. Developments in intralesional therapy for metastatic melanoma. Cancer Control. 23(1):12–20.
  • Smibert OC, Guo CW, Khoo C, Thursky KA, Sandhu S, Slavin MA. 2019. Microbiome transplantation and modulation of immune related adverse events. EClinicalMedicine. 8:10–11.
  • Sohn E. 2018. Skin microbiota's community effort. Nature. 563(7732):S91–S93.
  • Squarzanti DF, Sorrentino R, Azzimonti B. 2019. High-risk HPVs, microbiota and epithelial carcinogenesis: state of the art and research contribution of in vitro 3D models. J. Cancer Metastasis Treat. 5:73.
  • Squarzanti DF, Sorrentino R, Landini MM, Chiesa A, Pinato S, Rocchio F, Mattii M, Penengo L, Azzimonti B. 2018. Human papillomavirus type 16 E6 and E7 oncoproteins interact with the nuclear p53-binding protein 1 in an in vitro reconstructed 3D epithelium: new insights for the virus-induced DNA damage response. Virol J. 15(1):176.
  • Strickley JD, Messerschmidt JL, Awad ME, Li T, Hasegawa T, Ha DT, Nabeta HW, Bevins PA, Ngo KH, Asgari MM, et al. 2019. Immunity to commensal papillomaviruses protects against skin cancer. Nature. 575(7783):519–522.
  • Sun Z, Huang S, Zhu P, Yue F, Zhao H, Yang M, Niu Y, Jing G, Su X, Li H, et al. 2019. A microbiome-based index for assessing skin health and treatment effects for atopic dermatitis in children. mSystems. 4(4):e00293.
  • Surdu S, Fitzgerald EF, Bloom MS, Boscoe FP, Carpenter DO, Haase RF, Gurzau E, Rudnai P, Koppova K, Févotte J, et al. 2013. Occupational exposure to ultraviolet radiation and risk of non-melanoma skin cancer in a multinational European study. PLoS One. 8(4):e62359.
  • Szántó M, Dózsa A, Antal D, Szabó K, Kemény L, Bai P. 2019. Targeting the gut-skin axis-Probiotics as new tools for skin disorder management? Exp Dermatol. 28(11):1210–1218.
  • Teoh F, Pavelka N. 2016. How chemotherapy increases the risk of systemic candidiasis in cancer patients: current paradigm and future direction. Pathogens. 5(1):6.
  • Thompson KG, Shuster M, Li BC, Antonescu C, Florea L, Chien AL, Kang S. 2020. Variability in skin microbiota between smokers, former smokers and non-smokers. J Am Acad Dermatol. S0190-9622(20)30126-2.
  • Todd JK. 2005. Staphylococcal infections. Pediatr Rev. 26(12):444–450.
  • Tommasino M. 2019. HPV and skin carcinogenesis. Papillomavirus Res. 7:129–131.
  • Triozzi PL, Tuthill RJ, Borden E. 2011. Re-inventing intratumoral immunotherapy for melanoma. Immunotherapy. 3(5):653–671.
  • Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al. 2015. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 350(6264):1079–1084.
  • Viarisio D, Mueller-Decker K, Kloz U, Aengeneyndt B, Kopp-Schneider A, Gröne HJ, Gheit T, Flechtenmacher C, Gissmann L, Tommasino M. 2011. E6 and E7 from beta HPV38 cooperate with ultraviolet light in the development of actinic keratosis-like lesions and squamous cell carcinoma in mice. PLoS Pathog. 7(7):e1002125.
  • Viarisio D, Müller-Decker K, Accardi R, Robitaille A, Dürst M, Beer K, Jansen L, Flechtenmacher C, Bozza M, Harbottle R, et al. 2018. Beta HPV38 oncoproteins act with a hit-and-run mechanism in ultraviolet radiation-induced skin carcinogenesis in mice. PLoS Pathog. 14(1):e1006783
  • Viarisio D, Müller-Decker K, Hassel JC, Alvarez JC, Flechtenmacher C, Pawlita M, Gissmann L, Tommasino M. 2017. The BRAF inhibitor vemurafenib enhances UV-induced skin carcinogenesis in beta HPV38 E6 and E7 transgenic mice. J Invest Dermatol. 137(1):261–264.
  • Von Hertzen LC, Joensuu H, Haahtela T. 2011. Microbial deprivation, inflammation and cancer. Cancer Metastasis Rev. 30(2):211–223.
  • Wang Y, Zhu W, Shu M, Jiang Y, Gallo RL, Liu YT, Huang CM. 2012. The response of human skin commensal bacteria as a reflection of UV radiation: UV-B decreases porphyrin production. Plos One. 7(10):e47798.
  • Wanke I, Steffen H, Christ C, Krismer B, Gotz F, Peschel A, Schaller M, Schittek B. 2011. Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J Invest Dermatol. 131(2):382–390.
  • Weill FS, Cela EM, Paz ML, Ferrari A, Leoni J, González Maglio DH. 2013. Lipoteichoic acid from Lactobacillus rhamnosus GG as an oral photoprotective agent against UV-induced carcinogenesis. Br J Nutr. 109(3):457–466.
  • Weinstock GM. 2012. Genomic approaches to studying the human microbiota. Nature. 489(7415):250–256.
  • Weyrich LS, Dixit S, Farrer AG, Cooper AJ, Cooper AJ. 2015. The skin microbiome: associations between altered microbial communities and disease. Australas J Dermatol. 56(4):268–274.
  • Wieërs G, Belkhir L, Enaud R, Leclercq S, Philippart de Foy J-M, Dequenne I, de Timary P, Cani PD. 2019. How probiotics affect the microbiota. Front Cell Infect Microbiol. 9:454.
  • Wood DLA, Lachner N, Tan J-M, Tang S, Angel N, Laino A, Linedale R, Lê Cao K-A, Morrison M, Frazer IH, et al. 2018. A natural history of actinic keratosis and cutaneous squamous cell carcinoma microbiomes. MBio. 9(5):18.
  • Wu L, Zeng T, Deligios M, Milanesi L, Langille MGI, Zinellu A, Rubino S, Carru C, Kelvin DJ. 2020. Age-related variation of bacterial and fungal communities in different body habitats across the young, elderly and centenarians in Sardinia. mSphere. 5(1):e00558.
  • Yan X, Zhang S, Deng Y, Wang P, Hou Q, Xu H. 2018. Prognostic factors for checkpoint inhibitor based immunotherapy: an update with new evidences. Front Pharmacol. 9:1050.
  • Yu Y, Champer J, Beynet D, Kim J, Friedman AJ. 2015. The role of the cutaneous microbiome in skin cancer: lessons learned from the gut. J Drugs Dermatol. 14(5):461–465.
  • Yu Y, Dunaway S, Champer J, Kim J, Alikhan A. 2020. Changing our microbiome: probiotics in dermatology. Br J Dermatol. 182(1):39–46.
  • Yuan X, Wang L, Meng D, Wu L, Wang X, Zhang D, Luo Z, Pang Y, Liu G. 2020. The impact of NBUVB on microbial community profiling in the lesional skin of vitiligo subjects. Microb Pathog. 140:103943.
  • Zavattaro E, Fava P, Veronese F, Cavaliere G, Ferrante D, Cantaluppi V, Ranghino A, Biancone L, Fierro MT, Savoia P. 2019. Identification of risk factors for multiple non-melanoma skin cancers in Italian kidney transplant recipients. Medicina (Kaunas). 55(6):279.
  • Zeeuwen PL, Boekhorst J, van den Bogaard EH, De Koning HD, van de Kerkhof PM, Saulnier DM, van Swam II, van Hijum SA, Kleerebezem M, Schalkwijk J, et al. 2012. Microbiome dynamics of human epidermis following skin barrier disruption. Genome Biol. 13(11):R101.
  • Zeeuwen PL, Kleerebezem M, Timmerman HM, Schalkwijk J. 2013. Microbiome and skin diseases. Curr Opin Allergy Clin Immunol. 13(5):514–520.
  • Zhou C, Tuong ZK, Frazer IH. 2019. Papillomavirus immune evasion strategies target the infected cell and the local immune system. Front Oncol. 9:682.

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