Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice
Angela B. Javurek A B , William G. Spollen A C , Sarah A. Johnson A B D , Nathan J. Bivens E , Karen H. Bromert E , Scott A. Givan A C F and Cheryl S. Rosenfeld A B G H I
+ Author Affiliations
- Author Affiliations
A Department of Bond Life Sciences Center, University of Missouri, 1201 E. Rollins Road, Columbia, MO 65211, USA.
B Department of Biomedical Sciences, University of Missouri, 1201 E. Rollins Road, Columbia, MO 65211, USA.
C Department of Informatics Research Core Facility, University of Missouri, 1201 E. Rollins Road, Columbia, MO 65211, USA.
D Department of Animal Sciences, University of Missouri, 920 E. Campus Drive, Columbia, MO 65211, USA.
E DNA Core Facility, University of Missouri, 1201 E. Rollins Road, Columbia, MO 65211, USA.
F Department of Molecular Microbiology and Immunology, University of Missouri, 1201 E. Rollins Road, Columbia, MO 65211, USA.
G Genetics Area Program, University of Missouri, Columbia, MO 65211, USA.
H Thompson Center for Autism and Neurobehavioral Disorders, University of Missouri, 205 Portland Street, Columbia, MO 65211, USA.
I Corresponding author. Email: rosenfeldc@missouri.edu
Reproduction, Fertility and Development 29(8) 1602-1612 https://doi.org/10.1071/RD16119
Submitted: 15 March 2016 Accepted: 29 July 2016 Published: 29 August 2016
Abstract
Our prior work showed that a novel microbiome resides in the seminal vesicles of wild-type and oestrogen receptor α (Esr1) knock-out mice and is impacted by the presence of functional Esr1 genes. The seminal fluid microbiome (SFM) may influence the health and reproductive status of the male, along with that of his partner and offspring. A high-fat diet (HFD) alters metabolites and other factors within seminal fluid and might affect the SFM. Adult (~15 weeks old) male mice were placed for 4 weeks on a control or high-fat diet and seminal fluid and fecal samples were collected, bacterial DNA isolated and subjected to 16s rRNA sequencing. Corynebacterium spp. were elevated in the seminal fluid of HFD males; however, Acinetobacter johnsonii, Streptophyta, Ammoniphilus spp., Bacillus spp. and Propionibacterium acnes were increased in control males. Rikenellaceae was more abundant in the fecal samples from HFD males. However, Bacteroides ovatus and another Bacteroides species, Bilophila, Sutterella spp., Parabacteroides, Bifidobacterium longum, Akkermansia muciniphila and Desulfovibrio spp. were greater in control males. Thus, short-term consumption of a HFD influences the seminal fluid and fecal microbiomes, which may have important health consequence for males and developmental origins of health and disease effects in resulting offspring.
Additional keywords: bacteria, DOHaD, metabolic pathway, microbiota, prostate cancer, reproductive tract, semen.
References
Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., and Versalovic, J. (2014). The placenta harbors a unique microbiome. Sci. Transl. Med. 6, 237ra65.| The placenta harbors a unique microbiome.Crossref | GoogleScholarGoogle Scholar | 24848255PubMed |
Ait-Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., Houdeau, E., Theodorou, V., and Tompkins, T. (2014). Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol. Motil. 26, 510–520.
| Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2czgsFKrug%3D%3D&md5=b0c584d3bea5d6aa3a452c20c784b47bCAS | 24372793PubMed |
Baka, S. (2014). Microbiota of the seminal fluid. Fertil. Steril. 101, e27.
| Microbiota of the seminal fluid.Crossref | GoogleScholarGoogle Scholar | 24589522PubMed |
Bakos, H. W., Mitchell, M., Setchell, B. P., and Lane, M. (2011). The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402–410.
| The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOlu7fP&md5=07814560ba0e86335682456285678fc1CAS | 20649934PubMed |
Barouki, R., Gluckman, P. D., Grandjean, P., Hanson, M., and Heindel, J. J. (2012). Developmental origins of non-communicable disease: implications for research and public health. Environ. Health 11, 42.
| Developmental origins of non-communicable disease: implications for research and public health.Crossref | GoogleScholarGoogle Scholar | 22715989PubMed |
Binder, N. K., Hannan, N. J., and Gardner, D. K. (2012a). Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 7, e52304.
| Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFGhsA%3D%3D&md5=fb51dc52fc7c8c5e756afa35945fb90fCAS | 23300638PubMed |
Binder, N. K., Mitchell, M., and Gardner, D. K. (2012b). Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod. Fertil. Dev. 24, 804–812.
| Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFKls7c%3D&md5=47a3b7cd35d1d36c45e702e3f5085d59CAS | 22781931PubMed |
Binder, N. K., Beard, S. A., Kaitu’u-Lino, T. J., Tong, S., Hannan, N. J., and Gardner, D. (2015a). Paternal obesity in a rodent model affects placental gene expression in a sex-specific manner. Reproduction 149, 435–444.
| Paternal obesity in a rodent model affects placental gene expression in a sex-specific manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVCkur7K&md5=28b8612b6166515251842eafdf25a6d0CAS | 25725082PubMed |
Binder, N. K., Sheedy, J. R., Hannan, N. J., and Gardner, D. K. (2015b). Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model. Mol. Hum. Reprod. 21, 424–434.
| Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model.Crossref | GoogleScholarGoogle Scholar | 25731709PubMed |
Borovkova, N., Korrovits, P., Ausmees, K., Turk, S., Joers, K., Punab, M., and Mandar, R. (2011). Influence of sexual intercourse on genital tract microbiota in infertile couples. Anaerobe 17, 414–418.
| Influence of sexual intercourse on genital tract microbiota in infertile couples.Crossref | GoogleScholarGoogle Scholar | 21549210PubMed |
Bromfield, J. J. (2014). Seminal fluid and reproduction: much more than previously thought. J. Assist. Reprod. Genet. 31, 627–636.
| Seminal fluid and reproduction: much more than previously thought.Crossref | GoogleScholarGoogle Scholar | 24830788PubMed |
Bromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J., and Robertson, S. A. (2014). Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc. Natl. Acad. Sci. USA 111, 2200–2205.
| Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFOqtLc%3D&md5=69e682c77a9e6512483ccaa5541f94f6CAS | 24469827PubMed |
Busolo, F., Zanchetta, R., Lanzone, E., and Cusinato, R. (1984). Microbial flora in semen of asymptomatic infertile men. Andrologia 16, 269–275.
| Microbial flora in semen of asymptomatic infertile men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3nvVersg%3D%3D&md5=f91f76e4e94acc011a731f361b2d4957CAS | 6465553PubMed |
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336.
| QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFalurg%3D&md5=301fd189b5ac95faa4885f3dd2db8b10CAS | 20383131PubMed |
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., Fierer, N., and Knight, R. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 108, 4516–4522.
| Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVCktL0%3D&md5=a5de46f5894b537e5fb739c731f2f76bCAS | 20534432PubMed |
Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G. H., Peng, H., Zhang, X., Zhang, Y., Qian, J., Duan, E., Zhai, Q., and Zhou, Q. (2016). Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351, 397–400.
| Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtValsb4%3D&md5=129dcb42950d7353d16c214b3ed4a595CAS | 26721680PubMed |
Daniel, H., Moghaddas Gholami, A., Berry, D., Desmarchelier, C., Hahne, H., Loh, G., Mondot, S., Lepage, P., Rothballer, M., Walker, A., Böhm, C., Wenning, M., Wagner, M., Blaut, M., Schmitt-Kopplin, P., Kuster, B., Haller, D., and Clavel, T. (2014). High-fat diet alters gut microbiota physiology in mice. ISME J. 8, 295–308.
| High-fat diet alters gut microbiota physiology in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Cjsb8%3D&md5=f19bd31b32baace8ab63a291f5b72418CAS | 24030595PubMed |
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G. L. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072.
| Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVaqtLg%3D&md5=c8e73426d1f572cad2735e4c266a26caCAS | 16820507PubMed |
Devkota, S., and Chang, E. B. (2015). Interactions between diet, bile acid metabolism, gut microbiota, and inflammatory bowel diseases. Dig. Dis. 33, 351–356.
| Interactions between diet, bile acid metabolism, gut microbiota, and inflammatory bowel diseases.Crossref | GoogleScholarGoogle Scholar | 26045269PubMed |
Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
| Search and clustering orders of magnitude faster than BLAST.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WhtbzM&md5=423df971fc2a177aad8368ea272e7364CAS | 20709691PubMed |
Faure, C., Dupont, C., Chavatte-Palmer, P., Gautier, B., and Levy, R. (2015). Are semen parameters related to birth weight? Fertil. Steril. 103, 6–10.
| Are semen parameters related to birth weight?Crossref | GoogleScholarGoogle Scholar | 25552408PubMed |
Fullston, T., Palmer, N. O., Owens, J. A., Mitchell, M., Bakos, H. W., and Lane, M. (2012). Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27, 1391–1400.
| Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vjvFGhsQ%3D%3D&md5=f16c775543dd06738682e8d22e08599dCAS | 22357767PubMed |
Fullston, T., Ohlsson Teague, E. M., Palmer, N. O., DeBlasio, M. J., Mitchell, M., Corbett, M., Print, C. G., Owens, J. A., and Lane, M. (2013). Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 27, 4226–4243.
| Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SqtLzN&md5=5c943a95c532f2df1f973540ea786836CAS | 23845863PubMed |
Fullston, T., McPherson, N. O., Owens, J. A., Kang, W. X., Sandeman, L. Y., and Lane, M. (2015a). Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet. Physiol. Rep. 3, e12336.
| Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet.Crossref | GoogleScholarGoogle Scholar | 25804263PubMed |
Fullston, T., Shehadeh, H., Sandeman, L. Y., Kang, W. X., Wu, L. L., Robker, R. L., McPherson, N. O., and Lane, M. (2015b). Female offspring sired by diet-induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells. J. Assist. Reprod. Genet. 32, 725–735.
| Female offspring sired by diet-induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 25854657PubMed |
Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., and Mansuy, I. M. (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17, 667–669.
| Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtlWgsrg%3D&md5=017cba8a74cfabffff2cce80fa70f808CAS | 24728267PubMed |
Grandjean, V., Fourre, S., De Abreu, D. A., Derieppe, M. A., Remy, J. J., and Rassoulzadegan, M. (2015). RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep. 5, 18193.
| RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVWqsbbI&md5=37442df2412a00a4a936ef9a6b7ac21fCAS | 26658372PubMed |
Hanson, M. (2015). The birth and future health of DOHaD. J. Dev. Orig. Health Dis. 6, 434–437.
| The birth and future health of DOHaD.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MfmslyrtQ%3D%3D&md5=63918907e1dde3d3b8d0d973a9cb318bCAS | 26004094PubMed |
Hanson, M. A., and Gluckman, P. D. (2014). Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol. Rev. 94, 1027–1076.
| Early developmental conditioning of later health and disease: physiology or pathophysiology?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFansbnO&md5=aec0e1847aeb682fe1f4c3eafd1fd65fCAS | 25287859PubMed |
Hanson, M., Godfrey, K. M., Lillycrop, K. A., Burdge, G. C., and Gluckman, P. D. (2011). Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms. Prog. Biophys. Mol. Biol. 106, 272–280.
| Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms.Crossref | GoogleScholarGoogle Scholar | 21219925PubMed |
Heine, P. A., Taylor, J. A., Iwamoto, G. A., Lubahn, D. B., and Cooke, P. S. (2000). Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc. Natl. Acad. Sci. USA 97, 12729–12734.
| Increased adipose tissue in male and female estrogen receptor-alpha knockout mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFyntrk%3D&md5=cca437d8b1b51d8d489c3f15ca3d5d36CAS | 11070086PubMed |
Hou, D., Zhou, X., Zhong, X., Settles, M. L., Herring, J., Wang, L., Abdo, Z., Forney, L. J., and Xu, C. (2013). Microbiota of the seminal fluid from healthy and infertile men. Fertil. Steril. 100, 1261–1269.e3.
| Microbiota of the seminal fluid from healthy and infertile men.Crossref | GoogleScholarGoogle Scholar | 23993888PubMed |
Howe, A., Ringus, D. L., Williams, R. J., Choo, Z. N., Greenwald, S. M., Owens, S. M., Coleman, M. L., Meyer, F., and Chang, E. B. (2016). Divergent responses of viral and bacterial communities in the gut microbiome to dietary disturbances in mice. ISME J. 10, 1217–1227.
| Divergent responses of viral and bacterial communities in the gut microbiome to dietary disturbances in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xmsl2qu7s%3D&md5=a3ef582a2231f3744d3dbbd1f170b7e3CAS | 26473721PubMed |
Ivanov, I. B., Kuzmin, M. D., and Gritsenko, V. A. (2009). Microflora of the seminal fluid of healthy men and men suffering from chronic prostatitis syndrome. Int. J. Androl. 32, 462–467.
| Microflora of the seminal fluid of healthy men and men suffering from chronic prostatitis syndrome.Crossref | GoogleScholarGoogle Scholar | 18328042PubMed |
Javurek, A. B., Spollen, W. G., Ali, A. M., Johnson, S. A., Lubahn, D. B., Bivens, N. J., Bromert, K. H., Ellersieck, M. R., Givan, S. A., and Rosenfeld, C. S. (2016). Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status. Sci. Rep. 6, 23027.
| Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktFKis7o%3D&md5=40646f789f0499095bfc76d8f5061769CAS | 26971397PubMed |
Kwon, S. K., Kwak, M. J., Seo, J. G., Chung, M. J., and Kim, J. F. (2015). Complete genome sequence of Bifidobacterium longum KCTC 12200BP, a probiotic strain promoting the intestinal health. J. Biotechnol. 214, 169–170.
| Complete genome sequence of Bifidobacterium longum KCTC 12200BP, a probiotic strain promoting the intestinal health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Chur3P&md5=ebc563789993996ec313554cb0a30e3bCAS | 26439427PubMed |
Lam, Y. Y., Ha, C. W., Hoffmann, J. M., Oscarsson, J., Dinudom, A., Mather, T. J., Cook, D. I., Hunt, N. H., Caterson, I. D., Holmes, A. J., and Storlien, L. H. (2015). Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice. Obesity (Silver Spring) 23, 1429–1439.
| Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVOms7vF&md5=278f5ea511355de766d8c609a99d2a79CAS | 26053244PubMed |
Langille, M. G., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., Beiko, R. G., and Huttenhower, C. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821.
| Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWku7fJ&md5=31889057b6a69f295b594d5dde2e4669CAS | 23975157PubMed |
Le, T. K., Hosaka, T., Le, T. T., Nguyen, T. G., Tran, Q. B., Le, T. H., and Pham, X. D. (2014). Oral administration of Bifidobacterium spp. improves insulin resistance, induces adiponectin, and prevents inflammatory adipokine expressions. Biomed. Res. 35, 303–310.
| Oral administration of Bifidobacterium spp. improves insulin resistance, induces adiponectin, and prevents inflammatory adipokine expressions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWqsLzJ&md5=849ddbebe4a865914888a9f61acb2583CAS | 25355437PubMed |
Liu, C. M., Hungate, B. A., Tobian, A. A., Ravel, J., Prodger, J. L., Serwadda, D., Kigozi, G., Galiwango, R. M., Nalugoda, F., Keim, P., Wawer, M. J., Price, L. B., and Gray, R. H. (2015). Penile microbiota and female partner bacterial vaginosis in Rakai, Uganda. MBio 6, e00589-15.
| Penile microbiota and female partner bacterial vaginosis in Rakai, Uganda.Crossref | GoogleScholarGoogle Scholar | 26081632PubMed |
Loy, A., Maixner, F., Wagner, M., and Horn, M. (2007). probeBase – an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res. 35, D800–D804.
| probeBase – an online resource for rRNA-targeted oligonucleotide probes: new features 2007.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivFGruw%3D%3D&md5=34165fafd458ee1d1f87bd650ad4e7b7CAS | 17099228PubMed |
Ma, J., Prince, A. L., Bader, D., Hu, M., Ganu, R., Baquero, K., Blundell, P., Alan Harris, R., Frias, A. E., Grove, K. L., and Aagaard, K. M. (2014). High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat. Commun. 5, 3889.
| High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXksVektro%3D&md5=87f5b68bc409c51e4a58d479eafea1a0CAS | 24846660PubMed |
Magnusson, K. R., Hauck, L., Jeffrey, B. M., Elias, V., Humphrey, A., Nath, R., Perrone, A., and Bermudez, L. E. (2015). Relationships between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience 300, 128–140.
| Relationships between diet-related changes in the gut microbiome and cognitive flexibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXos1egtrs%3D&md5=ecc46ebf8908308ccdf560011df7bab7CAS | 25982560PubMed |
Magoč, T., and Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.
| FLASH: fast length adjustment of short reads to improve genome assemblies.Crossref | GoogleScholarGoogle Scholar | 21903629PubMed |
Mändar, R., Punab, M., Borovkova, N., Lapp, E., Kiiker, R., Korrovits, P., Metspalu, A., Krjutškov, K., Nõlvak, H., Preem, J. K., Oopkaup, K., Salumets, A., and Truu, J. (2015). Complementary seminovaginal microbiome in couples. Res. Microbiol. 166, 440–447.
| Complementary seminovaginal microbiome in couples.Crossref | GoogleScholarGoogle Scholar | 25869222PubMed |
McMurdie, P. J., and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217.
| phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVWht7w%3D&md5=8ed709284f63569a90b6fd8ae273f883CAS | 23630581PubMed |
Messaoudi, M., Violle, N., Bisson, J. F., Desor, D., Javelot, H., and Rougeot, C. (2011). Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2, 256–261.
| Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers.Crossref | GoogleScholarGoogle Scholar | 21983070PubMed |
Mitchell, M., Bakos, H. W., and Lane, M. (2011). Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95, 1349–1353.
| Paternal diet-induced obesity impairs embryo development and implantation in the mouse.Crossref | GoogleScholarGoogle Scholar | 21047633PubMed |
Murphy, E. A., Velazquez, K. T., and Herbert, K. M. (2015). Influence of high-fat diet on gut microbiota: a driving force for chronic disease risk. Curr. Opin. Clin. Nutr. Metab. Care 18, 515–520.
| Influence of high-fat diet on gut microbiota: a driving force for chronic disease risk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlWiu7rN&md5=e5f599bb3bcc9eb5872527e6438f27edCAS | 26154278PubMed |
Ng, S. F., Lin, R. C., Laybutt, D. R., Barres, R., Owens, J. A., and Morris, M. J. (2010). Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963–966.
| Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlWlsr%2FF&md5=8940bfed5c3b7960c11c11b53a458c97CAS | 20962845PubMed |
Ng, S. F., Lin, R. C., Maloney, C. A., Youngson, N. A., Owens, J. A., and Morris, M. J. (2014). Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring. FASEB J. 28, 1830–1841.
| Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVGrsb4%3D&md5=666a88cbb9e5c825b10f9f34a9fc51fcCAS | 24421403PubMed |
Paulson, J. N., Stine, O. C., Bravo, H. C., and Pop, M. (2013). Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200–1202.
| Differential abundance analysis for microbial marker-gene surveys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFaksbvP&md5=c67dbba7e6a4e6c61e8e46cdd4345717CAS | 24076764PubMed |
Rando, O. J. (2012). Daddy issues: paternal effects on phenotype. Cell 151, 702–708.
| Daddy issues: paternal effects on phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kjsr%2FJ&md5=f63e64b32dcad884c6dce71768a78fbaCAS | 23141533PubMed |
Rando, O. J., and Simmons, R. A. (2015). I’m eating for two: parental dietary effects on offspring metabolism. Cell 161, 93–105.
| I’m eating for two: parental dietary effects on offspring metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXls1agsro%3D&md5=0a3d87fe7d3cdd0ba11fc148465cd1a5CAS | 25815988PubMed |
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., and Bale, T. L. (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33, 9003–9012.
| Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXoslyktbY%3D&md5=e34aad2cee0aad1c2db476e1477e2126CAS | 23699511PubMed |
Rodgers, A. B., Morgan, C. P., Leu, N. A., and Bale, T. L. (2015). Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. USA 112, 13699–13704.
| Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1yksbfM&md5=e7518914b36b20dc1e162e497e2820faCAS | 26483456PubMed |
Rodin, D. M., Larone, D., and Goldstein, M. (2003). Relationship between semen cultures, leukospermia, and semen analysis in men undergoing fertility evaluation. Fertil. Steril. 79, 1555–1558.
| Relationship between semen cultures, leukospermia, and semen analysis in men undergoing fertility evaluation.Crossref | GoogleScholarGoogle Scholar | 12801559PubMed |
Schneeberger, M., Everard, A., Gomez-Valades, A. G., Matamoros, S., Ramirez, S., Delzenne, N. M., Gomis, R., Claret, M., and Cani, P. D. (2015). Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 5, 16643.
| Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVOru7vM&md5=36c56b0f651b721b37426360d2b44c99CAS | 26563823PubMed |
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., and Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60.
| Metagenomic biomarker discovery and explanation.Crossref | GoogleScholarGoogle Scholar | 21702898PubMed |
Shannon, B. A., Garrett, K. L., and Cohen, R. J. (2006). Links between Propionibacterium acnes and prostate cancer. Future Oncol. 2, 225–232.
| Links between Propionibacterium acnes and prostate cancer.Crossref | GoogleScholarGoogle Scholar | 16563091PubMed |
Sharma, U., and Rando, O. J. (2014). Father–son chats: inheriting stress through sperm RNA. Cell Metab. 19, 894–895.
| Father–son chats: inheriting stress through sperm RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpslCrsro%3D&md5=cc99f52fb83ace33f3f517a20aad5c11CAS | 24896534PubMed |
Sharma, U., Conine, C. C., Shea, J. M., Boskovic, A., Derr, A. G., Bing, X. Y., Belleannee, C., Kucukural, A., Serra, R. W., Sun, F., Song, L., Carone, B. R., Ricci, E. P., Li, X. Z., Fauquier, L., Moore, M. J., Sullivan, R., Mello, C. C., Garber, M., and Rando, O. J. (2016). Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351, 391–396.
| Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtValsLk%3D&md5=f717e3acc40c6340251337c74f4c2bd2CAS | 26721685PubMed |
Shinohara, D. B., Vaghasia, A. M., Yu, S. H., Mak, T. N., Bruggemann, H., Nelson, W. G., De Marzo, A. M., Yegnasubramanian, S., and Sfanos, K. S. (2013). A mouse model of chronic prostatic inflammation using a human prostate cancer-derived isolate of Propionibacterium acnes. Prostate 73, 1007–1015.
| A mouse model of chronic prostatic inflammation using a human prostate cancer-derived isolate of Propionibacterium acnes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFehtbk%3D&md5=8e0967a442a7d794848aaccf0807ee33CAS | 23389852PubMed |
Swenson, C. E., Toth, A., Toth, C., Wolfgruber, L., and O’Leary, W. M. (1980). Asymptomatic bacteriospermia in infertile men. Andrologia 12, 7–11.
| Asymptomatic bacteriospermia in infertile men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c7ps1ersQ%3D%3D&md5=6c0de7e5e35bb3c373acb3acf3f4f43bCAS | 6990832PubMed |
Terashima, M., Barbour, S., Ren, J., Yu, W., Han, Y., and Muegge, K. (2015). Effect of high-fat diet on paternal sperm histone distribution and male offspring liver gene expression. Epigenetics 10, 861–871.
| Effect of high-fat diet on paternal sperm histone distribution and male offspring liver gene expression.Crossref | GoogleScholarGoogle Scholar | 26252449PubMed |
Thorburn, A. N., McKenzie, C. I., and Shen, S. (2015). Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat. Commun. 6, 7320.
| Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtF2ktrjK&md5=4fccfc21b212f77b3fbdb68f853b7ebcCAS | 26102221PubMed |
Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., and Gordon, J. I. (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1, 6ra14.
| The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.Crossref | GoogleScholarGoogle Scholar | 20368178PubMed |
Virecoulon, F., Wallet, F., Fruchart-Flamenbaum, A., Rigot, J. M., Peers, M. C., Mitchell, V., and Courcol, R. J. (2005). Bacterial flora of the low male genital tract in patients consulting for infertility. Andrologia 37, 160–165.
| Bacterial flora of the low male genital tract in patients consulting for infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MroslGnug%3D%3D&md5=409c48a25e6dedf5fa01486e4ce830e0CAS | 16266393PubMed |
Walker, A., Pfitzner, B., Neschen, S., Kahle, M., Harir, M., Lucio, M., Moritz, F., Tziotis, D., Witting, M., Rothballer, M., Engel, M., Schmid, M., Endesfelder, D., Klingenspor, M., Rattei, T., Castell, W. Z., de Angelis, M. H., Hartmann, A., and Schmitt-Kopplin, P. (2014). Distinct signatures of host-microbial meta-metabolome and gut microbiome in two C57BL/6 strains under high-fat diet. ISME J. 8, 2380–2396.
| Distinct signatures of host-microbial meta-metabolome and gut microbiome in two C57BL/6 strains under high-fat diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFKntbfJ&md5=b9f538899d6e86c4988755dfbad8e2a8CAS | 24906017PubMed |
Walters, W. A., Caporaso, J. G., Lauber, C. L., Berg-Lyons, D., Fierer, N., and Knight, R. (2011). PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics 27, 1159–1161.
| PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFKltLk%3D&md5=47e4d3974d9f382f8134677218b75cc3CAS | 21349862PubMed |
Youngson, N. A., Lecomte, V., Maloney, C. A., Leung, P., Liu, J., Hesson, L. B., Luciani, F., Krause, L., and Morris, M. J. (2015). Obesity-induced sperm DNA methylation changes at satellite repeats are reprogrammed in rat offspring. Asian J. Androl. , .
| Obesity-induced sperm DNA methylation changes at satellite repeats are reprogrammed in rat offspring.Crossref | GoogleScholarGoogle Scholar | 26608942PubMed |
Zozaya, M., Ferris, M. J., Siren, J. D., Lillis, R., Myers, L., Nsuami, M. J., Eren, A. M., Brown, J., Taylor, C. M., and Martin, D. H. (2016). Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis. Microbiome 4, 16.
| Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis.Crossref | GoogleScholarGoogle Scholar | 27090518PubMed |
