Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response

Christine N. Spencer; Jennifer L. McQuade; Vancheswaran Gopalakrishnan; John A. McCulloch; Marie Vetizou; Alexandria P. Cogdill; Md A. Wadud Khan; Xiaotao Zhang; Michael G. White; Christine B. Peterson; Matthew C. Wong; Golnaz Morad; Theresa Rodgers; Jonathan H. Badger; Beth A. Helmink; Miles C. Andrews; Richard R. Rodrigues; Andrey Morgun; Young S. Kim; Jason Roszik; Kristi L. Hoffman; Jiali Zheng; Yifan Zhou; Yusra B. Medik; Laura M. Kahn; Sarah Johnson; Courtney W. Hudgens; Khalida Wani; Pierre Olivier Gaudreau; Angela L. Harris; Mohamed A. Jamal; Erez N. Baruch; Eva Perez-Guijarro; Chi Ping Day; Glenn Merlino; Barbara Pazdrak; Brooke S. Lochmann; Robert A. Szczepaniak-Sloane; Reetakshi Arora; Jaime Anderson; Chrystia M. Zobniw; Eliza Posada; Elizabeth Sirmans; Julie Simon; Lauren E. Haydu; Elizabeth M. Burton; Linghua Wang; Minghao Dang; Karen Clise-Dwyer; Sarah Schneider; Thomas Chapman; Nana Ama A.S. Anang; Sheila Duncan; Joseph Toker; Jared C. Malke; Isabella C. Glitza; Rodabe N. Amaria; Hussein A. Tawbi; Adi Diab; Michael K. Wong; Sapna P. Patel; Scott E. Woodman; Michael A. Davies; Merrick I. Ross; Jeffrey E. Gershenwald; Jeffrey E. Lee; Patrick Hwu; Vanessa Jensen; Yardena Samuels; Ravid Straussman; Nadim J. Ajami; Kelly C. Nelson; Luigi Nezi; Joseph F. Petrosino; P. Andrew Futreal; Alexander J. Lazar; Jianhua Hu; Robert R. Jenq; Michael T. Tetzlaff; Yan Yan; Wendy S. Garrett; Curtis Huttenhower; Padmanee Sharma; Stephanie S. Watowich; James P. Allison; Lorenzo Cohen; Giorgio Trinchieri; Carrie R. Daniel; Jennifer A. Wargo

doi:10.1126/science.aaz7015

Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response

Christine N. Spencer, Jennifer L. McQuade, Vancheswaran Gopalakrishnan, John A. McCulloch, Marie Vetizou, Alexandria P. Cogdill, Md A. Wadud Khan, Xiaotao Zhang, Michael G. White, Christine B. Peterson, Matthew C. Wong, Golnaz Morad, Theresa Rodgers, Jonathan H. Badger, Beth A. Helmink, Miles C. Andrews, Richard R. Rodrigues, Andrey Morgun, Young S. Kim, Jason RoszikKristi L. Hoffman, Jiali Zheng, Yifan Zhou, Yusra B. Medik, Laura M. Kahn, Sarah Johnson, Courtney W. Hudgens, Khalida Wani, Pierre Olivier Gaudreau, Angela L. Harris, Mohamed A. Jamal, Erez N. Baruch, Eva Perez-Guijarro, Chi Ping Day, Glenn Merlino, Barbara Pazdrak, Brooke S. Lochmann, Robert A. Szczepaniak-Sloane, Reetakshi Arora, Jaime Anderson, Chrystia M. Zobniw, Eliza Posada, Elizabeth Sirmans, Julie Simon, Lauren E. Haydu, Elizabeth M. Burton, Linghua Wang, Minghao Dang, Karen Clise-Dwyer, Sarah Schneider, Thomas Chapman, Nana Ama A.S. Anang, Sheila Duncan, Joseph Toker, Jared C. Malke, Isabella C. Glitza, Rodabe N. Amaria, Hussein A. Tawbi, Adi Diab, Michael K. Wong, Sapna P. Patel, Scott E. Woodman, Michael A. Davies, Merrick I. Ross, Jeffrey E. Gershenwald, Jeffrey E. Lee, Patrick Hwu, Vanessa Jensen, Yardena Samuels, Ravid Straussman, Nadim J. Ajami, Kelly C. Nelson, Luigi Nezi, Joseph F. Petrosino, P. Andrew Futreal, Alexander J. Lazar, Jianhua Hu, Robert R. Jenq, Michael T. Tetzlaff, Yan Yan, Wendy S. Garrett, Curtis Huttenhower, Padmanee Sharma, Stephanie S. Watowich, James P. Allison, Lorenzo Cohen, Giorgio Trinchieri, Carrie R. Daniel, Jennifer A. Wargo

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Abstract

Gut bacteria modulate the response to immune checkpoint blockade (ICB) treatment in cancer, but the effect of diet and supplements on this interaction is not well studied. We assessed fecal microbiota profiles, dietary habits, and commercially available probiotic supplement use in melanoma patients and performed parallel preclinical studies. Higher dietary fiber was associated with significantly improved progression-free survival in 128 patients on ICB, with the most pronounced benefit observed in patients with sufficient dietary fiber intake and no probiotic use. Findings were recapitulated in preclinical models, which demonstrated impaired treatment response to anti-programmed cell death 1 (anti-PD-1)-based therapy in mice receiving a low-fiber diet or probiotics, with a lower frequency of interferon-g-positive cytotoxic T cells in the tumor microenvironment. Together, these data have clinical implications for patients receiving ICB for cancer.

Original language	English
Pages (from-to)	1632-1640
Number of pages	9
Journal	Science
Volume	374
Issue number	6575
DOIs	https://doi.org/10.1126/science.aaz7015
State	Published - Dec 24 2021

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10.1126/science.aaz7015

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Spencer, C. N., McQuade, J. L., Gopalakrishnan, V., McCulloch, J. A., Vetizou, M., Cogdill, A. P., Wadud Khan, M. A., Zhang, X., White, M. G., Peterson, C. B., Wong, M. C., Morad, G., Rodgers, T., Badger, J. H., Helmink, B. A., Andrews, M. C., Rodrigues, R. R., Morgun, A., Kim, Y. S., ... Wargo, J. A. (2021). Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science, 374(6575), 1632-1640. https://doi.org/10.1126/science.aaz7015

@article{53149597a09443e3876631633b6bbb42,

title = "Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response",

abstract = "Gut bacteria modulate the response to immune checkpoint blockade (ICB) treatment in cancer, but the effect of diet and supplements on this interaction is not well studied. We assessed fecal microbiota profiles, dietary habits, and commercially available probiotic supplement use in melanoma patients and performed parallel preclinical studies. Higher dietary fiber was associated with significantly improved progression-free survival in 128 patients on ICB, with the most pronounced benefit observed in patients with sufficient dietary fiber intake and no probiotic use. Findings were recapitulated in preclinical models, which demonstrated impaired treatment response to anti-programmed cell death 1 (anti-PD-1)-based therapy in mice receiving a low-fiber diet or probiotics, with a lower frequency of interferon-g-positive cytotoxic T cells in the tumor microenvironment. Together, these data have clinical implications for patients receiving ICB for cancer.",

author = "Spencer, {Christine N.} and McQuade, {Jennifer L.} and Vancheswaran Gopalakrishnan and McCulloch, {John A.} and Marie Vetizou and Cogdill, {Alexandria P.} and {Wadud Khan}, {Md A.} and Xiaotao Zhang and White, {Michael G.} and Peterson, {Christine B.} and Wong, {Matthew C.} and Golnaz Morad and Theresa Rodgers and Badger, {Jonathan H.} and Helmink, {Beth A.} and Andrews, {Miles C.} and Rodrigues, {Richard R.} and Andrey Morgun and Kim, {Young S.} and Jason Roszik and Hoffman, {Kristi L.} and Jiali Zheng and Yifan Zhou and Medik, {Yusra B.} and Kahn, {Laura M.} and Sarah Johnson and Hudgens, {Courtney W.} and Khalida Wani and Gaudreau, {Pierre Olivier} and Harris, {Angela L.} and Jamal, {Mohamed A.} and Baruch, {Erez N.} and Eva Perez-Guijarro and Day, {Chi Ping} and Glenn Merlino and Barbara Pazdrak and Lochmann, {Brooke S.} and Szczepaniak-Sloane, {Robert A.} and Reetakshi Arora and Jaime Anderson and Zobniw, {Chrystia M.} and Eliza Posada and Elizabeth Sirmans and Julie Simon and Haydu, {Lauren E.} and Burton, {Elizabeth M.} and Linghua Wang and Minghao Dang and Karen Clise-Dwyer and Sarah Schneider and Thomas Chapman and Anang, {Nana Ama A.S.} and Sheila Duncan and Joseph Toker and Malke, {Jared C.} and Glitza, {Isabella C.} and Amaria, {Rodabe N.} and Tawbi, {Hussein A.} and Adi Diab and Wong, {Michael K.} and Patel, {Sapna P.} and Woodman, {Scott E.} and Davies, {Michael A.} and Ross, {Merrick I.} and Gershenwald, {Jeffrey E.} and Lee, {Jeffrey E.} and Patrick Hwu and Vanessa Jensen and Yardena Samuels and Ravid Straussman and Ajami, {Nadim J.} and Nelson, {Kelly C.} and Luigi Nezi and Petrosino, {Joseph F.} and {Andrew Futreal}, P. and Lazar, {Alexander J.} and Jianhua Hu and Jenq, {Robert R.} and Tetzlaff, {Michael T.} and Yan Yan and Garrett, {Wendy S.} and Curtis Huttenhower and Padmanee Sharma and Watowich, {Stephanie S.} and Allison, {James P.} and Lorenzo Cohen and Giorgio Trinchieri and Daniel, {Carrie R.} and Wargo, {Jennifer A.}",

year = "2021",

month = dec,

day = "24",

doi = "10.1126/science.aaz7015",

language = "English",

volume = "374",

pages = "1632--1640",

journal = "Science",

issn = "0036-8075",

number = "6575",

}

Spencer, CN, McQuade, JL, Gopalakrishnan, V, McCulloch, JA, Vetizou, M, Cogdill, AP, Wadud Khan, MA, Zhang, X, White, MG, Peterson, CB, Wong, MC, Morad, G, Rodgers, T, Badger, JH, Helmink, BA, Andrews, MC, Rodrigues, RR, Morgun, A, Kim, YS, Roszik, J, Hoffman, KL, Zheng, J, Zhou, Y, Medik, YB, Kahn, LM, Johnson, S, Hudgens, CW, Wani, K, Gaudreau, PO, Harris, AL, Jamal, MA, Baruch, EN, Perez-Guijarro, E, Day, CP, Merlino, G, Pazdrak, B, Lochmann, BS, Szczepaniak-Sloane, RA, Arora, R, Anderson, J, Zobniw, CM, Posada, E, Sirmans, E, Simon, J, Haydu, LE, Burton, EM, Wang, L, Dang, M, Clise-Dwyer, K, Schneider, S, Chapman, T, Anang, NAAS, Duncan, S, Toker, J, Malke, JC, Glitza, IC, Amaria, RN, Tawbi, HA, Diab, A, Wong, MK, Patel, SP, Woodman, SE, Davies, MA, Ross, MI, Gershenwald, JE, Lee, JE, Hwu, P, Jensen, V, Samuels, Y, Straussman, R, Ajami, NJ, Nelson, KC, Nezi, L, Petrosino, JF, Andrew Futreal, P, Lazar, AJ, Hu, J, Jenq, RR, Tetzlaff, MT, Yan, Y, Garrett, WS, Huttenhower, C, Sharma, P, Watowich, SS, Allison, JP, Cohen, L, Trinchieri, G, Daniel, CR & Wargo, JA 2021, 'Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response', Science, vol. 374, no. 6575, pp. 1632-1640. https://doi.org/10.1126/science.aaz7015

TY - JOUR

T1 - Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response

AU - Spencer, Christine N.

AU - McQuade, Jennifer L.

AU - Gopalakrishnan, Vancheswaran

AU - McCulloch, John A.

AU - Vetizou, Marie

AU - Cogdill, Alexandria P.

AU - Wadud Khan, Md A.

AU - Zhang, Xiaotao

AU - White, Michael G.

AU - Peterson, Christine B.

AU - Wong, Matthew C.

AU - Morad, Golnaz

AU - Rodgers, Theresa

AU - Badger, Jonathan H.

AU - Helmink, Beth A.

AU - Andrews, Miles C.

AU - Rodrigues, Richard R.

AU - Morgun, Andrey

AU - Kim, Young S.

AU - Roszik, Jason

AU - Hoffman, Kristi L.

AU - Zheng, Jiali

AU - Zhou, Yifan

AU - Medik, Yusra B.

AU - Kahn, Laura M.

AU - Johnson, Sarah

AU - Hudgens, Courtney W.

AU - Wani, Khalida

AU - Gaudreau, Pierre Olivier

AU - Harris, Angela L.

AU - Jamal, Mohamed A.

AU - Baruch, Erez N.

AU - Perez-Guijarro, Eva

AU - Day, Chi Ping

AU - Merlino, Glenn

AU - Pazdrak, Barbara

AU - Lochmann, Brooke S.

AU - Szczepaniak-Sloane, Robert A.

AU - Arora, Reetakshi

AU - Anderson, Jaime

AU - Zobniw, Chrystia M.

AU - Posada, Eliza

AU - Sirmans, Elizabeth

AU - Simon, Julie

AU - Haydu, Lauren E.

AU - Burton, Elizabeth M.

AU - Wang, Linghua

AU - Dang, Minghao

AU - Clise-Dwyer, Karen

AU - Schneider, Sarah

AU - Chapman, Thomas

AU - Anang, Nana Ama A.S.

AU - Duncan, Sheila

AU - Toker, Joseph

AU - Malke, Jared C.

AU - Glitza, Isabella C.

AU - Amaria, Rodabe N.

AU - Tawbi, Hussein A.

AU - Diab, Adi

AU - Wong, Michael K.

AU - Patel, Sapna P.

AU - Woodman, Scott E.

AU - Davies, Michael A.

AU - Ross, Merrick I.

AU - Gershenwald, Jeffrey E.

AU - Lee, Jeffrey E.

AU - Hwu, Patrick

AU - Jensen, Vanessa

AU - Samuels, Yardena

AU - Straussman, Ravid

AU - Ajami, Nadim J.

AU - Nelson, Kelly C.

AU - Nezi, Luigi

AU - Petrosino, Joseph F.

AU - Andrew Futreal, P.

AU - Lazar, Alexander J.

AU - Hu, Jianhua

AU - Jenq, Robert R.

AU - Tetzlaff, Michael T.

AU - Yan, Yan

AU - Garrett, Wendy S.

AU - Huttenhower, Curtis

AU - Sharma, Padmanee

AU - Watowich, Stephanie S.

AU - Allison, James P.

AU - Cohen, Lorenzo

AU - Trinchieri, Giorgio

AU - Daniel, Carrie R.

AU - Wargo, Jennifer A.

PY - 2021/12/24

Y1 - 2021/12/24

N2 - Gut bacteria modulate the response to immune checkpoint blockade (ICB) treatment in cancer, but the effect of diet and supplements on this interaction is not well studied. We assessed fecal microbiota profiles, dietary habits, and commercially available probiotic supplement use in melanoma patients and performed parallel preclinical studies. Higher dietary fiber was associated with significantly improved progression-free survival in 128 patients on ICB, with the most pronounced benefit observed in patients with sufficient dietary fiber intake and no probiotic use. Findings were recapitulated in preclinical models, which demonstrated impaired treatment response to anti-programmed cell death 1 (anti-PD-1)-based therapy in mice receiving a low-fiber diet or probiotics, with a lower frequency of interferon-g-positive cytotoxic T cells in the tumor microenvironment. Together, these data have clinical implications for patients receiving ICB for cancer.

AB - Gut bacteria modulate the response to immune checkpoint blockade (ICB) treatment in cancer, but the effect of diet and supplements on this interaction is not well studied. We assessed fecal microbiota profiles, dietary habits, and commercially available probiotic supplement use in melanoma patients and performed parallel preclinical studies. Higher dietary fiber was associated with significantly improved progression-free survival in 128 patients on ICB, with the most pronounced benefit observed in patients with sufficient dietary fiber intake and no probiotic use. Findings were recapitulated in preclinical models, which demonstrated impaired treatment response to anti-programmed cell death 1 (anti-PD-1)-based therapy in mice receiving a low-fiber diet or probiotics, with a lower frequency of interferon-g-positive cytotoxic T cells in the tumor microenvironment. Together, these data have clinical implications for patients receiving ICB for cancer.

UR - http://www.scopus.com/inward/record.url?scp=85122906876&partnerID=8YFLogxK

U2 - 10.1126/science.aaz7015

DO - 10.1126/science.aaz7015

M3 - Article

C2 - 34941392

AN - SCOPUS:85122906876

SN - 0036-8075

VL - 374

SP - 1632

EP - 1640

JO - Science

JF - Science

IS - 6575

ER -

Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response

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