The Human Microbiome and Obesity: Moving beyond Associations

Cell Host and Microbe

Volumn 22, Issue 5, 2017, Pages 589-599

  Maruvada, Padma ^a   Leone, Vanessa ^b   Kaplan, Lee M ^c   Chang, Eugene B ^b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

animal models; diet induced obesity; DIO; energy balance; energy expenditure; energy intake; microbial metabolites; microbiome; microbiota; microbiota targeted therapies; MTT; obesity

Indexed keywords

CLINICAL RESEARCH; EXPERIMENTAL MODEL; HOST; HUMAN; INTESTINE FLORA; MEDICAL INFORMATICS; MEDICAL TECHNOLOGY; METABOLIC DISORDER; METABOLISM; MICROBIOME; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; TRANSLATIONAL RESEARCH; ANIMAL; ANIMAL MODEL; CALORIC INTAKE; COMPLICATION; DIET; DYSBIOSIS; ENERGY METABOLISM; GASTROINTESTINAL TRACT; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

ANIMALS; DIET; DYSBIOSIS; ENERGY INTAKE; ENERGY METABOLISM; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; MICROBIOTA; MODELS, ANIMAL; OBESITY;

EID: 85032732514     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.10.005     Document Type: Review

References (89)

1. Al-Asmakh, M., Zadjali, F., Use of germ-free animal models in microbiota-related research. J. Microbiol. Biotechnol. 25 (2015), 1583–1588.
2. Alhassan, S., Kim, S., Bersamin, A., King, A.C., Gardner, C.D., Dietary adherence and weight loss success among overweight women: results from the A TO Z weight loss study. Int. J. Obes. 32 (2008), 985–991.
3. Anhê F.F., Roy, D., Pilon, G., Dudonné S., Matamoros, S., Varin, T.V., Garofalo, C., Moine, Q., Desjardins, Y., Levy, E., Marette, A., A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 64 (2015), 872–883.
4. Arnold, J.W., Roach, J., Azcarate-Peril, M.A., Emerging technologies for gut microbiome research. Trends Microbiol. 24 (2016), 887–901.
5. Arora, T., Wegmann, U., Bobhate, A., Lee, Y.S., Greiner, T.U., Drucker, D.J., Narbad, A., Bäckhed, F., Microbially produced glucagon-like peptide 1 improves glucose tolerance in mice. Mol. Metab. 5 (2016), 725–730.
6. Bartfeld, S., Clevers, H., Stem cell-derived organoids and their application for medical research and patient treatment. J. Mol. Med. (Berl.) 95 (2017), 729–738.
7. Bass, J., Circadian topology of metabolism. Nature 491 (2012), 348–356.
8. Bauer, P.V., Hamr, S.C., Duca, F.A., Regulation of energy balance by a gut-brain axis and involvement of the gut microbiota. Cell. Mol. Life Sci. 73 (2016), 737–755.
9. Bennett, B.J., de Aguiar Vallim, T.Q., Wang, Z., Shih, D.M., Meng, Y., Gregory, J., Allayee, H., Lee, R., Graham, M., Crooke, R., et al. Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 17 (2013), 49–60.
10. Blanton, L.V., Charbonneau, M.R., Salih, T., Barratt, M.J., Venkatesh, S., Ilkaveya, O., Subramanian, S., Manary, M.J., Trehan, I., Jorgensen, J.M., et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351 (2016), 1–10.
11. Blundell, J.E., Caudwell, P., Gibbons, C., Hopkins, M., Näslund, E., King, N.A., Finlayson, G., Body composition and appetite: fat-free mass (but not fat mass or BMI) is positively associated with self-determined meal size and daily energy intake in humans. Br. J. Nutr. 107 (2012), 445–449.
12. Buxton, O.M., Cain, S.W., O'Connor, S.P., Porter, J.H., Duffy, J.F., Wang, W., Czeisler, C.A., Shea, S.A., Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci. Transl. Med., 4, 2012, 129ra43.
13. Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P.D., Bäckhed, F., Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab. 22 (2015), 658–668.
14. Carmody, R.N., Gerber, G.K., Luevano, J.M. Jr., Gatti, D.M., Somes, L., Svenson, K.L., Turnbaugh, P.J., Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17 (2015), 72–84.
15. Carneiro, I.P., Elliott, S.A., Siervo, M., Padwal, R., Bertoli, S., Battezzati, A., Prado, C.M., Is obesity associated with altered energy expenditure?. Adv. Nutr. 7 (2016), 476–487.
16. Chassaing, B., Ley, R.E., Gewirtz, A.T., Intestinal epithelial cell toll-like receptor 5 regulates the intestinal microbiota to prevent low-grade inflammation and metabolic syndrome in mice. Gastroenterology 147 (2014), 1363–1377.e17.
17. Chassaing, B., Koren, O., Goodrich, J.K., Poole, A.C., Srinivasan, S., Ley, R.E., Gewirtz, A.T., Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519 (2015), 92–96.
18. Cox, L.M., Blaser, M.J., Antibiotics in early life and obesity. Nat. Rev. Endocrinol. 11 (2015), 182–190.
19. Dao, M.C., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E.O., Kayser, B.D., Levenez, F., Chilloux, J., Hoyles, L., et al., MICRO-Obes Consortium. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65 (2016), 426–436.
20. David, L.A., Materna, A.C., Friedman, J., Campos-Baptista, M.I., Blackburn, M.C., Perrotta, A., Erdman, S.E., Alm, E.J., Host lifestyle affects human microbiota on daily timescales. Genome Biol., 15, 2014, R89.
21. Debelius, J.W., Vázquez-Baeza, Y., McDonald, D., Xu, Z., Wolfe, E., Knight, R., Turning participatory microbiome research into usable data: lessons from the American Gut Project. J. Microbiol. Biol. Educ. 17 (2016), 46–50.
22. Depner, C.M., Stothard, E.R., Wright, K.P. Jr., Metabolic consequences of sleep and circadian disorders. Curr. Diab. Rep., 14, 2014, 507.
23. Dibner, C., Schibler, U., Albrecht, U., The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72 (2010), 517–549.
24. Donia, M.S., Fischbach, M.A., HUMAN MICROBIOTA. Small molecules from the human microbiota. Science, 349, 2015, 1254766.
25. Dotz, V., Rudloff, S., Blank, D., Lochnit, G., Geyer, R., Kunz, C., 13C-labeled oligosaccharides in breastfed infants’ urine: individual-, structure- and time-dependent differences in the excretion. Glycobiology 24 (2014), 185–194.
26. Earle, K.A., Billings, G., Sigal, M., Lichtman, J.S., Hansson, G.C., Elias, J.E., Amieva, M.R., Huang, K.C., Sonnenburg, J.L., Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18 (2015), 478–488.
27. Embree, M., Liu, J.K., Al-Bassam, M.M., Zengler, K., Networks of energetic and metabolic interactions define dynamics in microbial communities. Proc. Natl. Acad. Sci. USA 112 (2015), 15450–15455.
28. Eren, A.M., Maignien, L., Sul, W.J., Murphy, L.G., Grim, S.L., Morrison, H.G., Sogin, M.L., Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol. Evol. 4 (2013), 1111–1119.
29. Eren, A.M., Morrison, H.G., Lescault, P.J., Reveillaud, J., Vineis, J.H., Sogin, M.L., Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 9 (2015), 968–979.
30. Eren, A.M., Esen, Ö.C., Quince, C., Vineis, J.H., Morrison, H.G., Sogin, M.L., Delmont, T.O., Anvi'o: an advanced analysis and visualization platform for ‘omics data. PeerJ, 3, 2015, e1319.
31. Geisler, C., Braun, W., Pourhassan, M., Schweitzer, L., Glüer, C.-C., Bosy-Westphal, A., Müller, M.J., Age-dependent changes in resting energy expenditure (REE): insights from detailed body composition analysis in normal and overweight healthy caucasians. Nutrients, 8, 2016, E322.
32. Goodrich, J.K., Davenport, E.R., Beaumont, M., Jackson, M.A., Knight, R., Ober, C., Spector, T.D., Bell, J.T., Clark, A.G., Ley, R.E., Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19 (2016), 731–743.
33. Greiner, T.U., Bäckhed, F., Microbial regulation of GLP-1 and L-cell biology. Mol. Metab. 5 (2016), 753–758.
34. Guo, C.-J., Chang, F.-Y., Wyche, T.P., Backus, K.M., Acker, T.M., Funabashi, M., Taketani, M., Donia, M.S., Nayfach, S., Pollard, K.S., et al. Discovery of reactive microbiota-derived metabolites that inhibit host proteases. Cell 168 (2017), 517–526.e18.
35. Hao, Z., Mumphrey, M.B., Townsend, R.L., Morrison, C.D., Münzberg, H., Ye, J., Berthoud, H.-R., Reprogramming of defended body weight after Roux-En-Y gastric bypass surgery in diet-induced obese mice. Obesity (Silver Spring) 24 (2016), 654–660.
36. Hartstra, A.V., Bouter, K.E.C., Bäckhed, F., Nieuwdorp, M., Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care 38 (2015), 159–165.
37. Huch, M., Dorrell, C., Boj, S.F., van Es, J.H., Li, V.S.W., van de Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M.J., et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 494 (2013), 247–250.
38. Jones, M.L., Martoni, C.J., Ganopolsky, J.G., Labbé A., Prakash, S., The human microbiome and bile acid metabolism: dysbiosis, dysmetabolism, disease and intervention. Expert Opin. Biol. Ther. 14 (2014), 467–482.
39. Joyce, S.A., Gahan, C.G.M., Bile acid modifications at the microbe-host interface: potential for nutraceutical and pharmaceutical interventions in host health. Annu. Rev. Food Sci. Technol. 7 (2016), 313–333.
40. Khan, M.T., Nieuwdorp, M., Bäckhed, F., Microbial modulation of insulin sensitivity. Cell Metab. 20 (2014), 753–760.
41. Khoruts, A., Sadowsky, M.J., Understanding the mechanisms of faecal microbiota transplantation. Nat. Rev. Gastroenterol. Hepatol. 13 (2016), 508–516.
42. Kim, H.J., Ingber, D.E., Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr. Biol. 5 (2013), 1130–1140.
43. Kohsaka, A., Laposky, A.D., Ramsey, K.M., Estrada, C., Joshu, C., Kobayashi, Y., Turek, F.W., Bass, J., High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6 (2007), 414–421.
44. Kotula, J.W., Kerns, S.J., Shaket, L.A., Siraj, L., Collins, J.J., Way, J.C., Silver, P.A., Programmable bacteria detect and record an environmental signal in the mammalian gut. Proc. Natl. Acad. Sci. USA 111 (2014), 4838–4843.
45. Lakoff, A., Fazili, Z., Aufreiter, S., Pfeiffer, C.M., Connolly, B., Gregory, J.F. 3rd, Pencharz, P.B., O'Connor, D.L., Folate is absorbed across the human colon: evidence by using enteric-coated caplets containing 13C-labeled [6S]-5-formyltetrahydrofolate. Am. J. Clin. Nutr. 100 (2014), 1278–1286.
46. Leone, V., Gibbons, S.M., Martinez, K., Hutchison, A.L., Huang, E.Y., Cham, C.M., Pierre, J.F., Heneghan, A.F., Nadimpalli, A., Hubert, N., et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17 (2015), 681–689.
47. Leslie, J.L., Huang, S., Opp, J.S., Nagy, M.S., Kobayashi, M., Young, V.B., Spence, J.R., Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect. Immun. 83 (2015), 138–145.
48. Liang, X., Bushman, F.D., FitzGerald, G.A., Rhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock. Proc. Natl. Acad. Sci. USA 112 (2015), 10479–10484.
49. Liou, A.P., Paziuk, M., Luevano, J.-M. Jr., Machineni, S., Turnbaugh, P.J., Kaplan, L.M., Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med., 5, 2013, 178ra41.
50. Lytle, C.A., Fuller, M.E., Gan, Y.M., Peacock, A., DeFlaun, M.F., Onstott, T.C., White, D.C., Utility of high performance liquid chromatography/electrospray/mass spectrometry of polar lipids in specifically Per-13C labeled Gram-negative bacteria DA001 as a tracer for acceleration of bioremediation in the subsurface. J. Microbiol. Methods 44 (2001), 271–281.
51. Ma, J., Prince, A.L., Bader, D., Hu, M., Ganu, R., Baquero, K., Blundell, P., Alan Harris, R., Frias, A.E., Grove, K.L., Aagaard, K.M., High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat. Commun., 5, 2014, 3889.
52. Ma, L., Kim, J., Hatzenpichler, R., Karymov, M.A., Hubert, N., Hanan, I.M., Chang, E.B., Ismagilov, R.F., Gene-targeted microfluidic cultivation validated by isolation of a gut bacterium listed in Human Microbiome Project's Most Wanted taxa. Proc. Natl. Acad. Sci. USA 111 (2014), 9768–9773.
53. Martinez, K.B., Leone, V., Chang, E.B., Western diets, gut dysbiosis, and metabolic diseases: are they linked?. Gut Microbes 8 (2017), 130–142.
54. Melancon, E., Gomez De La Torre Canny, S., Sichel, S., Kelly, M., Wiles, T.J., Rawls, J.F., Eisen, J.S., Guillemin, K., Best practices for germ-free derivation and gnotobiotic zebrafish husbandry. Methods Cell Biol. 138 (2017), 61–100.
55. Mukherji, A., Kobiita, A., Ye, T., Chambon, P., Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153 (2013), 812–827.
56. Müller, M.J., Bosy-Westphal, A., Adaptive thermogenesis with weight loss in humans. Obesity (Silver Spring) 21 (2013), 218–228.
57. Müller, M.J., Enderle, J., Pourhassan, M., Braun, W., Eggeling, B., Lagerpusch, M., Glüer, C.-C., Kehayias, J.J., Kiosz, D., Bosy-Westphal, A., Metabolic adaptation to caloric restriction and subsequent refeeding: the Minnesota Starvation Experiment revisited. Am. J. Clin. Nutr. 102 (2015), 807–819.
58. Müller, M.J., Enderle, J., Bosy-Westphal, A., Changes in energy expenditure with weight gain and weight loss in humans. Curr. Obes. Rep. 5 (2016), 413–423.
59. Murakami, M., Tognini, P., Liu, Y., Eckel-Mahan, K.L., Baldi, P., Sassone-Corsi, P., Gut microbiota directs PPARγ-driven reprogramming of the liver circadian clock by nutritional challenge. EMBO Rep. 17 (2016), 1292–1303.
60. Ohigashi, S., Sudo, K., Kobayashi, D., Takahashi, T., Nomoto, K., Onodera, H., Significant changes in the intestinal environment after surgery in patients with colorectal cancer. J. Gastrointest. Surg. 17 (2013), 1657–1664.
61. Ohta, H., Izumi, S., Yoshimoto, M., A more acceptable endoluminal implantation for remotely monitoring ingestible sensors anchored to the stomach wall. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2015 (2015), 4089–4092.
62. Palleja, A., Kashani, A., Allin, K.H., Nielsen, T., Zhang, C., Li, Y., Brach, T., Liang, S., Feng, Q., Jørgensen, N.B., et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med., 8, 2016, 67.
63. Parséus, A., Sommer, N., Sommer, F., Caesar, R., Molinaro, A., Ståhlman, M., Greiner, T.U., Perkins, R., Bäckhed, F., Microbiota-induced obesity requires farnesoid X receptor. Gut 66 (2017), 429–437.
64. Penney, N.C., Kinross, J., Newton, R.C., Purkayastha, S., The role of bile acids in reducing the metabolic complications of obesity after bariatric surgery: a systematic review. Int. J. Obes. 39 (2015), 1565–1574.
65. Roopchand, D.E., Carmody, R.N., Kuhn, P., Moskal, K., Rojas-Silva, P., Turnbaugh, P.J., Raskin, I., Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes 64 (2015), 2847–2858.
66. Rosenbaum, M., Leibel, R.L., 20 years of leptin: role of leptin in energy homeostasis in humans. J. Endocrinol. 223 (2014), T83–T96.
67. Rosenbaum, M., Goldsmith, R., Bloomfield, D., Magnano, A., Weimer, L., Heymsfield, S., Gallagher, D., Mayer, L., Murphy, E., Leibel, R.L., Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J. Clin. Invest. 115 (2005), 3579–3586.
68. Rosenbaum, M., Knight, R., Leibel, R.L., The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol. Metab. 26 (2015), 493–501.
69. Ryan, K.K., Tremaroli, V., Clemmensen, C., Kovatcheva-Datchary, P., Myronovych, A., Karns, R., Wilson-Pérez, H.E., Sandoval, D.A., Kohli, R., Bäckhed, F., Seeley, R.J., FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 509 (2014), 183–188.
70. Sachs, N., Tsukamoto, Y., Kujala, P., Peters, P.J., Clevers, H., Intestinal epithelial organoids fuse to form self-organizing tubes in floating collagen gels. Development 144 (2017), 1107–1112.
71. Schweitzer, L., Geisler, C., Pourhassan, M., Braun, W., Glüer, C.C., Bosy-Westphal, A., Müller, M.J., Estimation of skeletal muscle mass and visceral adipose tissue volume by a single magnetic resonance imaging slice in healthy elderly adults. J. Nutr. 146 (2016), 2143–2148.
72. Sonnenburg, J.L., Bäckhed, F., Diet-microbiota interactions as moderators of human metabolism. Nature 535 (2016), 56–64.
73. Sonnenburg, E.D., Smits, S.A., Tikhonov, M., Higginbottom, S.K., Wingreen, N.S., Sonnenburg, J.L., Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 (2016), 212–215.
74. Stefater, M.A., Pérez-Tilve, D., Chambers, A.P., Wilson-Pérez, H.E., Sandoval, D.A., Berger, J., Toure, M., Tschöp, M., Woods, S.C., Seeley, R.J., Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 138 (2010), 2426–2436, 2436.e1–2436.e3.
75. Thaiss, C.A., Zeevi, D., Levy, M., Zilberman-Schapira, G., Suez, J., Tengeler, A.C., Abramson, L., Katz, M.N., Korem, T., Zmora, N., et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159 (2014), 514–529.
76. Thaiss, C.A., Levy, M., Korem, T., Dohnalová L., Shapiro, H., Jaitin, D.A., David, E., Winter, D.R., Gury-BenAri, M., Tatirovsky, E., et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell 167 (2016), 1495–1510.e12.
77. Trinh, I., Boulianne, G.L., Modeling obesity and its associated disorders in Drosophila. Physiology (Bethesda) 28 (2013), 117–124.
78. Turnbaugh, P.J., Gordon, J.I., The core gut microbiome, energy balance and obesity. J. Physiol. 587 (2009), 4153–4158.
79. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., et al. A core gut microbiome in obese and lean twins. Nature 457 (2009), 480–484.
80. Ussar, S., Griffin, N.W., Bezy, O., Fujisaka, S., Vienberg, S., Softic, S., Deng, L., Bry, L., Gordon, J.I., Kahn, C.R., Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metab. 22 (2015), 516–530.
81. Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R.S., Bartelsman, J.F.W.M., Dallinga-Thie, G.M., Ackermans, M.T., Serlie, M.J., Oozeer, R., et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143 (2012), 913–916.e7.
82. Wang, Y., Kuang, Z., Yu, X., Ruhn, K.A., Kubo, M., Hooper, L.V., The intestinal microbiota regulates body composition through NFIL3 and the circadian clock. Science 357 (2017), 912–916.
83. Wichmann, A., Allahyar, A., Greiner, T.U., Plovier, H., Lundén, G.Ö., Larsson, T., Drucker, D.J., Delzenne, N.M., Cani, P.D., Bäckhed, F., Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host Microbe 14 (2013), 582–590.
84. Wu, G.D., Compher, C., Chen, E.Z., Smith, S.A., Shah, R.D., Bittinger, K., Chehoud, C., Albenberg, L.G., Nessel, L., Gilroy, E., et al. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut 65 (2016), 63–72.
85. Yu, H., Hasan, N.M., In, J.G., Estes, M.K., Kovbasnjuk, O., Zachos, N.C., Donowitz, M., The contributions of human mini-intestines to the study of intestinal physiology and pathophysiology. Annu. Rev. Physiol. 79 (2017), 291–312.
86. Zarrinpar, A., Chaix, A., Yooseph, S., Panda, S., Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 20 (2014), 1006–1017.
87. Zeevi, D., Korem, T., Zmora, N., Israeli, D., Rothschild, D., Weinberger, A., Ben-Yacov, O., Lador, D., Avnit-Sagi, T., Lotan-Pompan, M., et al. Personalized nutrition by prediction of glycemic responses. Cell 163 (2015), 1079–1094.
88. Zheng, J., Greenway, F.L., Caenorhabditis elegans as a model for obesity research. Int. J. Obes. 36 (2012), 186–194.
89. Ziętak, M., Kovatcheva-Datchary, P., Markiewicz, L.H., Ståhlman, M., Kozak, L.P., Bäckhed, F., Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab. 23 (2016), 1216–1223.