Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment

William Q. Nguyen; Lauren P. Chrisman; Gail L. Enriquez; Madeline J. Hooper; Teresa L. Griffin; Merjaan Ahmad; Sophia Rahman; Stefan J. Green; Patrick C. Seed; Joan Guitart; Michael B. Burns; Xiaolong A. Zhou

doi:10.3389/fimmu.2023.1280205

Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment

William Q. Nguyen, Lauren P. Chrisman, Gail L. Enriquez, Madeline J. Hooper, Teresa L. Griffin, Merjaan Ahmad, Sophia Rahman, Stefan J. Green, Patrick C. Seed, Joan Guitart, Michael B. Burns, Xiaolong A. Zhou^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

4 Scopus citations

Abstract

Recent studies have shown a close relationship between cutaneous T-cell lymphoma (CTCL) and its microbiome. CTCL disease progression is associated with gut dysbiosis and alterations in bacterial taxa parallel those observed in immunologically similar atopic dermatitis. Moreover, the microbial profile of lesional skin may predict response to narrowband ultraviolet B (nbUVB), a common skin-directed therapy. However, the relationship between the gut microbiome, an immunologically vital niche, and nbUVB remains unexplored in CTCL. Herein, we performed 16S rRNA sequencing and PICRUSt2 predictive metagenomics on DNA extracted from stool swabs of 13 CTCL patients treated with nbUVB, 8 non-treated patients, and 13 healthy controls. Disease response was assessed with modified Severity Weighted Assessment Tool (mSWAT); of nbUVB-treated patients, 6 improved (decreased mSWAT), 2 remained stable, and 5 worsened (increased mSWAT). Protective commensal bacteria including Lactobacillaceae and Erysipelatoclostridiaceae were significantly less abundant in CTCL patients compared to controls. With treatment, the CTCL gut microbiome exhibited decreased phylogenetic diversity and lower relative abundance of pro-inflammatory Sutterellaceae. Sutterellaceae was also significantly more abundant in patients who worsened, and Eggerthellaceae and Erysipelotrichaceae trended higher in patients who improved. Finally, PICRUSt2 functional predictions based on shifts in abundance of bacterial sequences repeatedly identified alterations in inositol degradation, which plays a key role in host immunomodulation, including inositol phospholipid signaling relevant to T-cell survival and proliferation. Our results bolster the paradigm of gut dysbiosis in CTCL and its functional implications in disease pathogenesis, and further delineate bacterial taxa associated with nbUVB response and with nbUVB treatment itself.

Original language	English (US)
Article number	1280205
Journal	Frontiers in immunology
Volume	14
DOIs	https://doi.org/10.3389/fimmu.2023.1280205
State	Published - 2023

Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. XZ is supported in part by a career development award from the Dermatology Foundation, a Cutaneous Lymphoma Foundation Catalyst Research Grant, American Cancer Society Institutional Research Grant, and an institutional grant from Northwestern University Clinical and Translational Sciences Institute and National Institute of Health (5KL2TR001424). These grants helped support the research contained in this article. Acknowledgments

Keywords

cancer
cutaneous T cell lymphoma
gut dysbiosis
inositol
lymphoma
microbiome
phototherapy
skin cancer

ASJC Scopus subject areas

Immunology and Allergy
Immunology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3389/fimmu.2023.1280205

Cite this

Nguyen, W. Q., Chrisman, L. P., Enriquez, G. L., Hooper, M. J., Griffin, T. L., Ahmad, M., Rahman, S., Green, S. J., Seed, P. C., Guitart, J., Burns, M. B., & Zhou, X. A. (2023). Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment. Frontiers in immunology, 14, Article 1280205. https://doi.org/10.3389/fimmu.2023.1280205

@article{68bd60d34f7649978026cbdb211ae4d6,

title = "Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment",

abstract = "Recent studies have shown a close relationship between cutaneous T-cell lymphoma (CTCL) and its microbiome. CTCL disease progression is associated with gut dysbiosis and alterations in bacterial taxa parallel those observed in immunologically similar atopic dermatitis. Moreover, the microbial profile of lesional skin may predict response to narrowband ultraviolet B (nbUVB), a common skin-directed therapy. However, the relationship between the gut microbiome, an immunologically vital niche, and nbUVB remains unexplored in CTCL. Herein, we performed 16S rRNA sequencing and PICRUSt2 predictive metagenomics on DNA extracted from stool swabs of 13 CTCL patients treated with nbUVB, 8 non-treated patients, and 13 healthy controls. Disease response was assessed with modified Severity Weighted Assessment Tool (mSWAT); of nbUVB-treated patients, 6 improved (decreased mSWAT), 2 remained stable, and 5 worsened (increased mSWAT). Protective commensal bacteria including Lactobacillaceae and Erysipelatoclostridiaceae were significantly less abundant in CTCL patients compared to controls. With treatment, the CTCL gut microbiome exhibited decreased phylogenetic diversity and lower relative abundance of pro-inflammatory Sutterellaceae. Sutterellaceae was also significantly more abundant in patients who worsened, and Eggerthellaceae and Erysipelotrichaceae trended higher in patients who improved. Finally, PICRUSt2 functional predictions based on shifts in abundance of bacterial sequences repeatedly identified alterations in inositol degradation, which plays a key role in host immunomodulation, including inositol phospholipid signaling relevant to T-cell survival and proliferation. Our results bolster the paradigm of gut dysbiosis in CTCL and its functional implications in disease pathogenesis, and further delineate bacterial taxa associated with nbUVB response and with nbUVB treatment itself.",

keywords = "cancer, cutaneous T cell lymphoma, gut dysbiosis, inositol, lymphoma, microbiome, phototherapy, skin cancer",

author = "Nguyen, {William Q.} and Chrisman, {Lauren P.} and Enriquez, {Gail L.} and Hooper, {Madeline J.} and Griffin, {Teresa L.} and Merjaan Ahmad and Sophia Rahman and Green, {Stefan J.} and Seed, {Patrick C.} and Joan Guitart and Burns, {Michael B.} and Zhou, {Xiaolong A.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2024 Nguyen, Chrisman, Enriquez, Hooper, Griffin, Ahmad, Rahman, Green, Seed, Guitart, Burns and Zhou.",

year = "2023",

doi = "10.3389/fimmu.2023.1280205",

language = "English (US)",

volume = "14",

journal = "Frontiers in immunology",

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Nguyen, WQ, Chrisman, LP, Enriquez, GL, Hooper, MJ, Griffin, TL, Ahmad, M, Rahman, S, Green, SJ, Seed, PC , Guitart, J, Burns, MB & Zhou, XA 2023, 'Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment', Frontiers in immunology, vol. 14, 1280205. https://doi.org/10.3389/fimmu.2023.1280205

TY - JOUR

T1 - Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment

AU - Nguyen, William Q.

AU - Chrisman, Lauren P.

AU - Enriquez, Gail L.

AU - Hooper, Madeline J.

AU - Griffin, Teresa L.

AU - Ahmad, Merjaan

AU - Rahman, Sophia

AU - Green, Stefan J.

AU - Seed, Patrick C.

AU - Guitart, Joan

AU - Burns, Michael B.

AU - Zhou, Xiaolong A.

PY - 2023

Y1 - 2023

N2 - Recent studies have shown a close relationship between cutaneous T-cell lymphoma (CTCL) and its microbiome. CTCL disease progression is associated with gut dysbiosis and alterations in bacterial taxa parallel those observed in immunologically similar atopic dermatitis. Moreover, the microbial profile of lesional skin may predict response to narrowband ultraviolet B (nbUVB), a common skin-directed therapy. However, the relationship between the gut microbiome, an immunologically vital niche, and nbUVB remains unexplored in CTCL. Herein, we performed 16S rRNA sequencing and PICRUSt2 predictive metagenomics on DNA extracted from stool swabs of 13 CTCL patients treated with nbUVB, 8 non-treated patients, and 13 healthy controls. Disease response was assessed with modified Severity Weighted Assessment Tool (mSWAT); of nbUVB-treated patients, 6 improved (decreased mSWAT), 2 remained stable, and 5 worsened (increased mSWAT). Protective commensal bacteria including Lactobacillaceae and Erysipelatoclostridiaceae were significantly less abundant in CTCL patients compared to controls. With treatment, the CTCL gut microbiome exhibited decreased phylogenetic diversity and lower relative abundance of pro-inflammatory Sutterellaceae. Sutterellaceae was also significantly more abundant in patients who worsened, and Eggerthellaceae and Erysipelotrichaceae trended higher in patients who improved. Finally, PICRUSt2 functional predictions based on shifts in abundance of bacterial sequences repeatedly identified alterations in inositol degradation, which plays a key role in host immunomodulation, including inositol phospholipid signaling relevant to T-cell survival and proliferation. Our results bolster the paradigm of gut dysbiosis in CTCL and its functional implications in disease pathogenesis, and further delineate bacterial taxa associated with nbUVB response and with nbUVB treatment itself.

AB - Recent studies have shown a close relationship between cutaneous T-cell lymphoma (CTCL) and its microbiome. CTCL disease progression is associated with gut dysbiosis and alterations in bacterial taxa parallel those observed in immunologically similar atopic dermatitis. Moreover, the microbial profile of lesional skin may predict response to narrowband ultraviolet B (nbUVB), a common skin-directed therapy. However, the relationship between the gut microbiome, an immunologically vital niche, and nbUVB remains unexplored in CTCL. Herein, we performed 16S rRNA sequencing and PICRUSt2 predictive metagenomics on DNA extracted from stool swabs of 13 CTCL patients treated with nbUVB, 8 non-treated patients, and 13 healthy controls. Disease response was assessed with modified Severity Weighted Assessment Tool (mSWAT); of nbUVB-treated patients, 6 improved (decreased mSWAT), 2 remained stable, and 5 worsened (increased mSWAT). Protective commensal bacteria including Lactobacillaceae and Erysipelatoclostridiaceae were significantly less abundant in CTCL patients compared to controls. With treatment, the CTCL gut microbiome exhibited decreased phylogenetic diversity and lower relative abundance of pro-inflammatory Sutterellaceae. Sutterellaceae was also significantly more abundant in patients who worsened, and Eggerthellaceae and Erysipelotrichaceae trended higher in patients who improved. Finally, PICRUSt2 functional predictions based on shifts in abundance of bacterial sequences repeatedly identified alterations in inositol degradation, which plays a key role in host immunomodulation, including inositol phospholipid signaling relevant to T-cell survival and proliferation. Our results bolster the paradigm of gut dysbiosis in CTCL and its functional implications in disease pathogenesis, and further delineate bacterial taxa associated with nbUVB response and with nbUVB treatment itself.

KW - cancer

KW - cutaneous T cell lymphoma

KW - gut dysbiosis

KW - inositol

KW - lymphoma

KW - microbiome

KW - phototherapy

KW - skin cancer

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Gut microbiota analyses of cutaneous T-cell lymphoma patients undergoing narrowband ultraviolet B therapy reveal alterations associated with disease treatment

Abstract

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

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