Parental Social Isolation during Adolescence Alters Gut Microbiome in Rat Male Offspring

被引:2
作者
Siddi, Carlotta [1 ,5 ]
Cosentino, Sofia [2 ]
Tamburini, Elena [3 ]
Concas, Luca [1 ]
Pisano, Maria Barbara [2 ]
Ardu, Riccardo [3 ]
Deplano, Maura [2 ]
Follesa, Paolo [1 ]
Maciocco, Elisabetta [4 ]
Porcu, Patrizia [4 ]
Serra, Mariangela [1 ]
Pisu, Maria Giuseppina [4 ]
机构
[1] Univ Cagliari, Dept Life & Environm Sci, Sect Neurosci & Anthropol, I-09042 Monserrato, Cagliari, Italy
[2] Univ Cagliari, Dept Med Sci & Publ Hlth, I-09042 Monserrato, Cagliari, Italy
[3] Univ Cagliari, Dept Biomed Sci, I-09042 Monserrato, Cagliari, Italy
[4] Natl Res Council Italy CNR, Neurosci Inst, I-09042 Monserrato, Cagliari, Italy
[5] Univ Cagliari, Dept Biomed Sci, Div Neurosci & Clin Pharmacol, I-09042 Monserrato, Cagliari, Italy
关键词
social isolation; preconceptional stress; male rats offspring; gut microbiome; cytokines; corticosterone; CHAIN FATTY-ACIDS; PITUITARY-ADRENAL AXIS; MATERNAL-CARE; STRESS; DISORDER; DEFICITS;
D O I
10.3390/biom14020172
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Previous work from our laboratory demonstrated that parental stress, induced by social isolation starting at puberty, leads to behavioral, endocrine, and biochemical changes in the male, but not female, offspring (ISO-O) of Sprague-Dawley rats. Here, we report alterations in the gut microbiota composition of ISO-O vs. grouped-housed offspring (GH-O), although all animals received the same diet and were housed in the same conditions. Analysis of bacterial communities by next-generation sequencing (NGS) of 16S rRNA gene revealed alterations at family and order levels within the main phyla of Bacteroides, Proteobacteria, and Firmicutes, including an almost total deficit in Limosilactobacillus reuteri (formerly Lactobacillus reuteri) and a significant increase in Ligilactobacillus murinus (formerly Lactobacillus murinus). In addition, we found an increase in the relative abundance of Rhodospirillales and Clostridiales in the families of Lachnospiraceae and Ruminococcaceae, and Bacteroidales in the family of Prevotellaceae. Furthermore, we examined plasma levels of the proinflammatory cytokines interleukin-1-beta and tumor necrosis factor-alpha, which did not differ between the two groups, while corticosterone concentrations were significantly increased in ISO-O rats. Our findings suggest that adverse environmental conditions experienced by parents may have an impact on the likelihood of disease development in the subsequent generations.
引用
收藏
页数:15
相关论文
共 50 条
  • [1] The maternal gut microbiome during pregnancy and offspring allergy and asthma
    Gao, Yuan
    Nanan, Ralph
    Macia, Laurence
    Tan, Jian
    Sominsky, Luba
    Quinn, Thomas P.
    O'Hely, Martin
    Ponsonby, Anne-Louise
    Tang, Mimi L. K.
    Collier, Fiona
    Strickland, Deborah H.
    Dhar, Poshmaal
    Brix, Susanne
    Phipps, Simon
    Sly, Peter D.
    Ranganathan, Sarath
    Stokholm, Jakob
    Kristiansen, Karsten
    Gray, Lawrence E. K.
    Vuillermin, Peter
    JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY, 2021, 148 (03) : 669 - 678
  • [2] Periconceptional ethanol exposure alters the stress axis in adult female but not male rat offspring
    Burgess, Danielle J.
    Dorey, Emily S.
    Gardebjer, Emelie M.
    Bielefeldt-Ohmann, Helle
    Moritz, Karen M.
    Cuffe, James S. M.
    STRESS-THE INTERNATIONAL JOURNAL ON THE BIOLOGY OF STRESS, 2019, 22 (03): : 347 - 357
  • [3] Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats
    Hong, Suzie
    Flashner, Bess
    Chiu, Melissa
    Hoeve, Elizabeth Ver
    Luz, Sandra
    Bhatnagar, Seema
    PHYSIOLOGY & BEHAVIOR, 2012, 105 (02) : 269 - 275
  • [4] Peri-adolescence isolation rearing alters social behavior and nociception in rats
    Meng, Qingxuan
    Li, Nanxin
    Han, Xiao
    Shao, Feng
    Wang, Weiwen
    NEUROSCIENCE LETTERS, 2010, 480 (01) : 25 - 29
  • [5] Intergenerational effects of a paternal Western diet during adolescence on offspring gut microbiota, stress reactivity, and social behavior
    Bodden, Carina
    Pang, Terence Y.
    Feng, Yingshi
    Mridha, Faria
    Kong, Geraldine
    Li, Shanshan
    Watt, Matthew J.
    Reichelt, Amy C.
    Hannan, Anthony J.
    FASEB JOURNAL, 2022, 36 (01)
  • [6] Social isolation alters behavior, the gut-immune-brain axis, and neurochemical circuits in male and female prairie voles
    Donovan, Meghan
    Mackey, Calvin S.
    Platt, Grayson N.
    Rounds, Jacob
    Brown, Amber N.
    Trickey, Darryl J.
    Liu, Yan
    Jones, Kathryn M.
    Wang, Zuoxin
    NEUROBIOLOGY OF STRESS, 2020, 13
  • [7] Effect of the Nursing Mother on the Gut Microbiome of the Offspring During Early Mouse Development
    Treichel, Nicole Simone
    Prevorsek, Zala
    Mrak, Vesna
    Kostric, Matea
    Vestergaard, Gisle
    Foesel, Baerbel
    Pfeiffer, Stefan
    Stres, Blaz
    Schoeler, Anne
    Schloter, Michael
    MICROBIAL ECOLOGY, 2019, 78 (02) : 517 - 527
  • [8] Effect of the Nursing Mother on the Gut Microbiome of the Offspring During Early Mouse Development
    Nicole Simone Treichel
    Zala Prevoršek
    Vesna Mrak
    Matea Kostrić
    Gisle Vestergaard
    Bärbel Foesel
    Stefan Pfeiffer
    Blaž Stres
    Anne Schöler
    Michael Schloter
    Microbial Ecology, 2019, 78 : 517 - 527
  • [9] Excess Growth Hormone Alters the Male Mouse Gut Microbiome in an Age-dependent Manner
    Jensen, Elizabeth A.
    Young, Jonathan A.
    Jackson, Zachary
    Busken, Joshua
    Kuhn, Jaycie
    Onusko, Maria
    Carroll, Ronan K.
    List, Edward O.
    Brown, J. Mark
    Kopchick, John J.
    Murphy, Erin R.
    Berryman, Darlene E.
    ENDOCRINOLOGY, 2022, 163 (07)
  • [10] Stress during pregnancy alters the offspring hypothalamic, pituitary, adrenal, and testicular response to isolation on the day of weaning
    Williams, MT
    Davis, HN
    McCrea, AE
    Hennessy, MB
    NEUROTOXICOLOGY AND TERATOLOGY, 1999, 21 (06) : 653 - 659