Personalized Microbial Fingerprint Associated with Differential Glycemic Effects of a Whole Grain Rye Intervention on Chinese Adults.

bacteroides bile acid glycemic effect gut microbiota short‐chain fatty acids whole grain rye

Journal

Molecular nutrition & food research
ISSN: 1613-4133
Titre abrégé: Mol Nutr Food Res
Pays: Germany
ID NLM: 101231818

Informations de publication

Date de publication:
01 Aug 2024
Historique:
revised: 13 07 2024
received: 14 04 2024
medline: 2 8 2024
pubmed: 2 8 2024
entrez: 2 8 2024
Statut: aheadofprint

Résumé

This study aims to identify the gut enterotypes that explain differential responses to intervention with whole grain rye by proposing an "enterotype - metabolic" model. A 12-week randomized controlled trial is conducted in Chinese adults, with 79 subjects consuming whole grain products with fermented rye bran (FRB) and 77 consuming refined wheat products in this exploratory post-hoc analysis. Responders or non-responders are identified according to whether blood glucose decreased by more than 10% after rye intervention. Compared to non-responders, responders in FRB have higher baseline Bacteroides (p < 0.001), associated with reduced blood glucose (p < 0.001), increased Faecalibacterium (p = 0.020) and Erysipelotrichaceae_UCG.003 (p = 0.022), as well as deceased 7β-hydroxysteroid dehydrogenase (p = 0.033) after intervention. The differentiated gut microbiota and metabolites between responders and non-responders after intervention are enriched in aminoacyl-tRNA biosynthesis. The work confirms the previously suggested importance of microbial enterotypes in differential responses to whole grain interventions and supports taking enterotypes into consideration for improved efficacy of whole grain intervention for preventing type 2 diabetes. Altered short-chain fatty acids and bile acid metabolism might be a potential mediator for the beneficial effects of whole grain rye on glucose metabolism.

Identifiants

pubmed: 39091068
doi: 10.1002/mnfr.202400274
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2400274

Subventions

Organisme : National Natural Science Foundation of China
ID : 82373555
Organisme : National Natural Science Foundation of China
ID : 81861138007
Organisme : Shanghai Pujiang Program
ID : 21PJD005
Organisme : VINNOVA
Organisme : Swedish Research Council
ID : 2017-05840

Informations de copyright

© 2024 Wiley‐VCH GmbH.

Références

E. Ahmad, S. Lim, R. Lamptey, D. R. Webb, M. J. Davies, Lancet 2022, 400, 1803.
L. Qi, Y. Chen, J. Clin. Endocrinol. Metab. 2023, 108, 251.
A. Reynolds, J. Mann, J. Cummings, N. Winter, E. Mete, L. Te Morenga, Lancet 2019, 393, 434.
K. Jonsson, R. Andersson, K. E. Bach Knudsen, G. Hallmans, K. Hanhineva, K. Katina, M. Kolehmainen, C. Kyrø, M. Langton, E. Nordlund, H. N. Lærke, A. Olsen, K. Poutanen, A. Tjønneland, R. Landberg, Trends Food Sci. Technol. 2018, 79, 78.
K. Musa‐Veloso, T. Poon, L. S. Harkness, M. O'shea, Y. Chu, Am. J. Clin. Nutr. 2018, 108, 759.
S. Åberg, J. Mann, S. Neumann, A. B. Ross, A. N. Reynolds, Diabetes Care 2020, 43, 1717.
H. M. Roager, J. K. Vogt, M. Kristensen, L. B. S. Hansen, S. Ibrügger, R. B. Mærkedahl, M. I. Bahl, M. V. Lind, R. L. Nielsen, H. Frøkiær, R. J. Gøbel, R. Landberg, A. B. Ross, S. Brix, J. Holck, A. S. Meyer, M. H. Sparholt, A. F. Christensen, V. Carvalho, B. Hartmann, J. J. Holst, J. J. Rumessen, A. Linneberg, T. Sicheritz‐Pontén, M. D. Dalgaard, A. Blennow, H. L. Frandsen, S. Villas‐Bôas, K. Kristiansen, H. Vestergaard, et al., Gut 2019, 68, 83.
R. Gao, X. Meng, Y. Xue, M. Mao, Y. Liu, X. Tian, B. Sui, X. Li, P. Zhang, Front. Pharmacol. 2022, 13, 1027212.
A. Koh, F. De Vadder, P. Kovatcheva‐Datchary, F. Backhed, Cell 2016, 165, 1332.
M. F. Hjorth, A. Astrup, Am. J. Clin. Nutr. 2020, 111, 242.
M. S. A. Palmnas‐Bedard, G. Costabile, C. Vetrani, S. Aberg, Y. Hjalmarsson, J. Dicksved, G. Riccardi, R. Landberg, Am. J. Clin. Nutr. 2022, 116, 862.
K. A. Krautkramer, J. Fan, F. Backhed, Nat. Rev. Microbiol. 2021, 19, 77.
R. Cheng, L. Wang, S. Le, Y. Yang, C. Zhao, X. Zhang, X. Yang, T. Xu, L. Xu, P. Wiklund, J. Ge, D. Lu, C. Zhang, L. Chen, S. Cheng, Nat. Commun. 2022, 13, 2555.
P. I. Costea, F. Hildebrand, M. Arumugam, F. Backhed, M. J. Blaser, F. D. Bushman, W. M. De Vos, S. D. Ehrlich, C. M. Fraser, M. Hattori, C. Huttenhower, I. B. Jeffery, D. Knights, J. D. Lewis, R. E. Ley, H. Ochman, P. W. O'toole, C. Quince, D. A. Relman, F. Shanahan, S. Sunagawa, J. Wang, G. M. Weinstock, G. D. Wu, G. Zeller, L. Zhao, J. Raes, R. Knight, P. Bork, Nat. Microbiol. 2018, 3, 8.
M. Arumugam, J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D. R. Mende, G. R. Fernandes, J. Tap, T. Bruls, J. M. Batto, M. Bertalan, N. Borruel, F. Casellas, L. Fernandez, L. Gautier, T. Hansen, M. Hattori, T. Hayashi, M. Kleerebezem, K. Kurokawa, M. Leclerc, F. Levenez, C. Manichanh, H. B. Nielsen, T. Nielsen, N. Pons, J. Poulain, J. Qin, T. Sicheritz‐Ponten, S. Tims, et al., Nature 2011, 473, 174.
I. Garcia‐Mantrana, M. Selma‐Royo, S. Gonzalez, A. Parra‐Llorca, C. Martinez‐Costa, M. C. Collado, Gut Microbes 2020, 11, 962.
E. J. Song, J. H. Shin, J. Microbiol. Biotechnol. 2022, 32, 1497.
J. Wang, W. Li, C. Wang, L. Wang, T. He, H. Hu, J. Song, C. Cui, J. Qiao, L. Qing, L. Li, N. Zang, K. Wang, C. Wu, L. Qi, A. Ma, H. Zheng, X. Hou, F. Liu, L. Chen, J. Diabetes Res. 2020, 2020, 6047145.
A. C. De Moraes, G. R. Fernandes, I. T. Da Silva, B. Almeida‐Pititto, E. P. Gomes, A. D. Pereira, S. R. Ferreira, Front. Cell Infect. Microbiol. 2017, 7, 47.
M. F. Hjorth, H. M. Roager, T. M. Larsen, S. K. Poulsen, T. R. Licht, M. I. Bahl, Y. Zohar, A. Astrup, Int. J. Obes. (Lond.) 2018, 42, 284.
P. Kovatcheva‐Datchary, A. Nilsson, R. Akrami, Y. S. Lee, F. De Vadder, T. Arora, A. Hallen, E. Martens, I. Bjorck, F. Backhed, Cell Metab. 2015, 22, 971.
L. Christensen, S. Vuholm, H. M. Roager, D. S. Nielsen, L. Krych, M. Kristensen, A. Astrup, M. F. Hjorth, J. Nutr. 2019, 149, 2174.
L. Christensen, H. M. Roager, A. Astrup, M. F. Hjorth, Am. J. Clin. Nutr. 2018, 108, 645.
J. L. Sonnenburg, F. Backhed, Nature 2016, 535, 56.
T. Yntema, D. P. Y. Koonen, F. Kuipers, Nutrients 2023, 15, 1850.
W. Jia, G. Xie, W. Jia, Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 111.
R. G. Pushpass, S. Alzoufairi, K. G. Jackson, J. A. Lovegrove, Nutr. Res. Rev. 2022, 35, 161.
X. Wu, S. Yin, C. Cheng, C. Xu, J. Peng, Front. Vet. Sci. 2021, 8, 756910.
K. Makki, H. Brolin, N. Petersen, M. Henricsson, D. P. Christensen, M. T. Khan, A. Wahlstrom, P. O. Bergh, V. Tremaroli, K. Schoonjans, H. U. Marschall, F. Backhed, Gut 2023, 72, 314.
D. Xing, Q. Zhou, Y. Wang, J. Xu, Biol. Trace Elem. Res. 2023, 201, 1205.
P. Portincasa, L. Bonfrate, M. Vacca, M. De Angelis, I. Farella, E. Lanza, M. Khalil, D. Q. Wang, M. Sperandio, A. Di Ciaula, Int. J. Mol. Sci. 2022, 23, 1105.
D. Salamone, A. A. Rivellese, C. Vetrani, Acta Diabetol. 2021, 58, 1131.
K. Xue, Y. Liu, K. N. Iversen, M. Mazidi, Z. Qu, C. Dong, T. Jin, G. Hallmans, P. Aman, A. Johansson, G. He, R. Landberg, Front. Nutr. 2020, 7, 608623.
Y. Liu, K. Xue, K. N. Iversen, Z. Qu, C. Dong, T. Jin, G. Hallmans, P. Aman, A. Johansson, G. He, R. Landberg, Food Funct. 2021, 12, 9141.
G. Kakiyama, A. Muto, H. Takei, H. Nittono, T. Murai, T. Kurosawa, A. F. Hofmann, W. M. Pandak, J. S. Bajaj, J. Lipid Res. 2014, 55, 978.
C. Thomas, R. Pellicciari, M. Pruzanski, J. Auwerx, K. Schoonjans, Nat. Rev. Drug Discov. 2008, 7, 678.
F. Rohart, B. Gautier, A. Singh, K. A. Le Cao, PLoS Comput. Biol. 2017, 13, e1005752.
A. Singh, C. P. Shannon, B. Gautier, F. Rohart, M. Vacher, S. J. Tebbutt, K. A. Le Cao, Bioinformatics 2019, 35, 3055.
J. Bajerska, S. Mildner‐Szkudlarz, J. Walkowiak, J. Med. Food 2015, 18, 698.
J. Lappi, H. Mykkanen, K. E. Bach Knudsen, P. Kirjavainen, K. Katina, J. Pihlajamaki, K. Poutanen, M. Kolehmainen, Nutr. J. 2014, 13, 104.
K. S. Leinonen, K. S. Poutanen, H. M. Mykkanen, J. Nutr. 2000, 130, 164.
M. Lankinen, U. Schwab, P. V. Gopalacharyulu, T. Seppanen‐Laakso, L. Yetukuri, M. Sysi‐Aho, P. Kallio, T. Suortti, D. E. Laaksonen, H. Gylling, K. Poutanen, M. Kolehmainen, M. Oresic, Nutr. Metab. Cardiovasc Dis. 2010, 20, 249.
O. Prykhodko, J. Sandberg, S. Burleigh, I. Björck, A. Nilsson, F. Fåk Hållenius, Front. Nutr. 2018, 5, 45.
M. Candela, E. Biagi, M. Soverini, C. Consolandi, S. Quercia, M. Severgnini, C. Peano, S. Turroni, S. Rampelli, P. Pozzilli, M. Pianesi, F. Fallucca, P. Brigidi, Br. J. Nutr. 2016, 116, 80.
M. Gurung, Z. Li, H. You, R. Rodrigues, D. B. Jump, A. Morgun, N. Shulzhenko, EBioMedicine 2020, 51, 102590.
J. Y. Yang, Y. S. Lee, Y. Kim, S. H. Lee, S. Ryu, S. Fukuda, K. Hase, C. S. Yang, H. S. Lim, M. S. Kim, H. M. Kim, S. H. Ahn, B. E. Kwon, H. J. Ko, M. N. Kweon, Mucosal Immunol. 2017, 10, 104.
P. Gauffin Cano, A. Santacruz, A. Moya, Y. Sanz, PLoS One 2012, 7, e41079.
M. Federici, X. Zhang, D. Shen, Z. Fang, Z. Jie, X. Qiu, C. Zhang, Y. Chen, L. Ji, PLoS One 2013, 8, e71108.
H. G. Peach, N. E. Barnett, J. Clin. Pathol. 2001, 54, 466.
H. M. Roager, T. R. Licht, S. K. Poulsen, T. M. Larsen, M. I. Bahl, Appl. Environ. Microbiol. 2014, 80, 1142.
G. Den Besten, K. Van Eunen, A. K. Groen, K. Venema, D. J. Reijngoud, B. M. Bakker, J. Lipid Res. 2013, 54, 2325.
A. Mayorga‐Ramos, C. Barba‐Ostria, D. Simancas‐Racines, L. P. Guaman, Front. Nutr. 2022, 9, 1067647.
T. Arora, V. Tremaroli, Front. Endocrinol. (Lausanne) 2021, 12, 761834.
S. Coppola, C. Avagliano, A. Calignano, R. Berni Canani, Molecules 2021, 26, 682.
N. H. Kwon, P. L. Fox, S. Kim, Nat. Rev. Drug Discov. 2019, 18, 629.
Y. Yu, P. Zhao, S. Zhai, Aquac. Rep. 2022, 26, 101283.
G. Calderon, A. Mcrae, J. Rievaj, J. Davis, I. Zandvakili, S. Linker‐Nord, D. Burton, G. Roberts, F. Reimann, B. Gedulin, A. Vella, N. F. Larusso, M. Camilleri, F. M. Gribble, A. Acosta, EBioMedicine 2020, 55, 102759.
G. C. Manrique, J. Davis, A. N. Bonis, D. Khemani, B. Gedulin, A. Vella, M. Camilleri, A. Acosta, Diabetes 2018, 67, 128.
J. Y. Lee, H. Arai, Y. Nakamura, S. Fukiya, M. Wada, A. Yokota, J. Lipid Res. 2013, 54, 3062.
T. Dos Reis Araujo, M. Roberta Rodrigues Muniz, B. Lourenconi Alves, L. Monali Barreto Dos Santos, M. Fernandes Bonfim, J. Alves Da Silva Junior, J. Franciesco Vettorazzi, C. Cesar Zoppi, E. Magalhaes Carneiro, Food Res. Int. 2022, 156, 111331.
X. Liu, Y. Wang, H. Ji, K. Aihara, L. Chen, Nucleic Acids Res. 2016, 44, e164.
J. Friedman, E. J. Alm, PLoS Comput. Biol. 2012, 8, e1002687.

Auteurs

Wenyun Li (W)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Huiru Tang (H)

State Key Laboratory of Genetic Engineering, Zhongshan Hospital and School of Life Sciences, Laboratory of Metabonomics and Systems Biology, Human Phenome Institute, Fudan University, Shanghai, 200032, China.

Kun Xue (K)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Tao Ying (T)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Min Wu (M)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Zheng Qu (Z)

Department of Gastroenterology, Zhongye Hospital, Shanghai, 200003, China.

Chenglin Dong (C)

Department of Clinical Laboratory, Zhongye Hospital, Shanghai, 200003, China.

Taiyi Jin (T)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Carl Brunius (C)

Department of Life Sciences, Chalmers University of Technology, Gothenburg, 412 96, Sweden.

Göran Hallmans (G)

Department of Public Health and Clinical Medicine, Umeå University, Umeå, 901 87, Sweden.

Per Åman (P)

Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala, 750 07, Sweden.

Anders Johansson (A)

Department of Public Health and Clinical Medicine, Umeå University, Umeå, 901 87, Sweden.
Department of Odontology, Section of Molecular Periodontology, Umeå University, Umeå, 901 87, Sweden.

Rikard Landberg (R)

Department of Life Sciences, Chalmers University of Technology, Gothenburg, 412 96, Sweden.

Yuwei Liu (Y)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Gengsheng He (G)

School of Public Health, Fudan University/Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, 200032, China.

Classifications MeSH