A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes

ABSTRACT Cutaneous squamous cell carcinoma (SCC) is the second-most-common cancer in Australia. The majority of SCCs progress from premalignant actinic keratosis (AK) lesions that form on chronically sun-exposed skin. The role of skin microbiota in this progression is not well understood; therefore,...

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Autores principales:	David L. A. Wood, Nancy Lachner, Jean-Marie Tan, Stephanie Tang, Nicola Angel, Antonia Laino, Richard Linedale, Kim-Anh Lê Cao, Mark Morrison, Ian H. Frazer, H. Peter Soyer, Philip Hugenholtz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	16S RNA actinic keratosis Malassezia microbiome skin squamous cell carcinoma Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fc69b3fabd5a431896934efc73fd9aaf
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spelling	oai:doaj.org-article:fc69b3fabd5a431896934efc73fd9aaf2021-11-15T15:58:20ZA Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes10.1128/mBio.01432-182150-7511https://doaj.org/article/fc69b3fabd5a431896934efc73fd9aaf2018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01432-18https://doaj.org/toc/2150-7511ABSTRACT Cutaneous squamous cell carcinoma (SCC) is the second-most-common cancer in Australia. The majority of SCCs progress from premalignant actinic keratosis (AK) lesions that form on chronically sun-exposed skin. The role of skin microbiota in this progression is not well understood; therefore, we performed a longitudinal microbiome analysis of AKs and SCCs using a cohort of 13 SCC-prone immunocompetent men. The majority of variability in microbial profiles was attributable to subject, followed by time and lesion type. Propionibacterium and Malassezia organisms were relatively more abundant in nonlesional photodamaged skin than in AKs and SCCs. Staphylococcus was most commonly associated with lesional skin, in particular, sequences most closely related to Staphylococcus aureus. Of 11 S. aureus-like operational taxonomic units (OTUs), six were significantly associated with SCC lesions across seven subjects, suggesting their specific involvement with AK-to-SCC progression. If a causative link exists between certain S. aureus-like OTUs and SCC etiology, therapeutic approaches specifically targeting these bacteria could be used to reduce SCC. IMPORTANCE Actinic keratosis (AK) and cutaneous squamous cell carcinoma (SCC) are two of the most common dermatologic conditions in Western countries and cause substantial morbidity worldwide. The role of human papillomaviruses under these conditions has been well studied yet remains inconclusive. One PCR-based study has investigated bacteria in the etiology of these conditions; however, no study has investigated the microbiomes of AK and SCC more broadly. We longitudinally profiled the microbiomes of 112 AK lesions, profiled cross sections of 32 spontaneously arising SCC lesions, and compared these to matching nonlesional photodamaged control skin sites. We identified commonly occurring strains of Propionibacterium and Malassezia at higher relative abundances on nonlesional skin than in AK and SCC lesions, and strains of Staphylococcus aureus were relatively more abundant in lesional than nonlesional skin. These findings may aid in the prevention of SCC.David L. A. WoodNancy LachnerJean-Marie TanStephanie TangNicola AngelAntonia LainoRichard LinedaleKim-Anh Lê CaoMark MorrisonIan H. FrazerH. Peter SoyerPhilip HugenholtzAmerican Society for Microbiologyarticle16S RNAactinic keratosisMalasseziamicrobiomeskinsquamous cell carcinomaMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	16S RNA actinic keratosis Malassezia microbiome skin squamous cell carcinoma Microbiology QR1-502
spellingShingle	16S RNA actinic keratosis Malassezia microbiome skin squamous cell carcinoma Microbiology QR1-502 David L. A. Wood Nancy Lachner Jean-Marie Tan Stephanie Tang Nicola Angel Antonia Laino Richard Linedale Kim-Anh Lê Cao Mark Morrison Ian H. Frazer H. Peter Soyer Philip Hugenholtz A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
description	ABSTRACT Cutaneous squamous cell carcinoma (SCC) is the second-most-common cancer in Australia. The majority of SCCs progress from premalignant actinic keratosis (AK) lesions that form on chronically sun-exposed skin. The role of skin microbiota in this progression is not well understood; therefore, we performed a longitudinal microbiome analysis of AKs and SCCs using a cohort of 13 SCC-prone immunocompetent men. The majority of variability in microbial profiles was attributable to subject, followed by time and lesion type. Propionibacterium and Malassezia organisms were relatively more abundant in nonlesional photodamaged skin than in AKs and SCCs. Staphylococcus was most commonly associated with lesional skin, in particular, sequences most closely related to Staphylococcus aureus. Of 11 S. aureus-like operational taxonomic units (OTUs), six were significantly associated with SCC lesions across seven subjects, suggesting their specific involvement with AK-to-SCC progression. If a causative link exists between certain S. aureus-like OTUs and SCC etiology, therapeutic approaches specifically targeting these bacteria could be used to reduce SCC. IMPORTANCE Actinic keratosis (AK) and cutaneous squamous cell carcinoma (SCC) are two of the most common dermatologic conditions in Western countries and cause substantial morbidity worldwide. The role of human papillomaviruses under these conditions has been well studied yet remains inconclusive. One PCR-based study has investigated bacteria in the etiology of these conditions; however, no study has investigated the microbiomes of AK and SCC more broadly. We longitudinally profiled the microbiomes of 112 AK lesions, profiled cross sections of 32 spontaneously arising SCC lesions, and compared these to matching nonlesional photodamaged control skin sites. We identified commonly occurring strains of Propionibacterium and Malassezia at higher relative abundances on nonlesional skin than in AK and SCC lesions, and strains of Staphylococcus aureus were relatively more abundant in lesional than nonlesional skin. These findings may aid in the prevention of SCC.
format	article
author	David L. A. Wood Nancy Lachner Jean-Marie Tan Stephanie Tang Nicola Angel Antonia Laino Richard Linedale Kim-Anh Lê Cao Mark Morrison Ian H. Frazer H. Peter Soyer Philip Hugenholtz
author_facet	David L. A. Wood Nancy Lachner Jean-Marie Tan Stephanie Tang Nicola Angel Antonia Laino Richard Linedale Kim-Anh Lê Cao Mark Morrison Ian H. Frazer H. Peter Soyer Philip Hugenholtz
author_sort	David L. A. Wood
title	A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
title_short	A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
title_full	A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
title_fullStr	A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
title_full_unstemmed	A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes
title_sort	natural history of actinic keratosis and cutaneous squamous cell carcinoma microbiomes
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/fc69b3fabd5a431896934efc73fd9aaf
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A Natural History of Actinic Keratosis and Cutaneous Squamous Cell Carcinoma Microbiomes

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