[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4014/jmb.2111.11048

Vascular Endothelial Growth Factor May Be Involved in the Behavioral Changes of Progeny Rats after Exposure to Ceftriaxone Sodium during Pregnancy

Yang, Xin (Department of Primary Child Health Care, Children's Hospital of Chongqing Medical University)
Tang, Ting (Department of Primary Child Health Care, Children's Hospital of Chongqing Medical University)
Li, Mengchun (Department of Pediatrics, Daping Hospital, Army Medical University)
Chen, Jie (Department of Pediatrics, Daping Hospital, Army Medical University)
Li, Tingyu (Department of Primary Child Health Care, Children's Hospital of Chongqing Medical University)
Dai, Ying (Department of Primary Child Health Care, Children's Hospital of Chongqing Medical University)
Cheng, Qian (Department of Primary Child Health Care, Children's Hospital of Chongqing Medical University)

Publication Information

Journal of Microbiology and Biotechnology / v.32, no.6, 2022 , pp. 699-708 More about this Journal

Abstract

Antibiotic exposure during pregnancy have an adversely effects on offspring behavior and development. However, its mechanism is still poorly understood. To uncover this, we added ceftriaxone sodium to the drinking water of rats during pregnancy and conducted three-chamber sociability test, open-field test, and Morris water maze test in 3- and 6-week-old offspring. The antibiotic group offspring showed lower sociability and spatial learning and memory than control. To determine the role of the gut microbiota and their metabolites in the changes in offspring behavior, fecal samples of 6-week-old offspring rats were sequenced. The composition of dominant gut microbial taxa differed between the control and antibiotic groups. KEGG pathway analysis showed that S24-7 exerted its effects through the metabolic pathways including mineral absorption, protein digestion and absorption, Valine, leucine, and isoleucine biosynthesis. Correlation analysis showed that S24-7 abundance was negatively correlated with the level of VEGF, and metabolites associated with S24-7-including 3-aminobutanoic acid, dacarbazine, L-leucine, 3-ketosphinganine, 1-methylnicotinamide, and N-acetyl-L-glutamate-were also significantly correlated with VEGF levels. The findings suggest that antibiotic exposure during pregnancy, specifically ceftriaxone sodium, will adversely affects the behavior of offspring rats due to the imbalance of gut microbiota, especially S24-7, via VEGF and various metabolic pathways.

Keywords

Ceftriaxone sodium; S24-7; vascular endothelial growth factor;

Citations & Related Records

Reference

1	Tsuneyoshi Y, Sato M, Tomonaga S, Yamane H, Morishita K, Denbow DM, et al. 2009. Oral administration of Excitin-1 (beta-alanyl-L-leucine) alters behavior and brain monoamine and amino acid concentrations in rats. Nutr. Neurosci. 12: 175-182. DOI
2	Jiang HY, Zhou YY, Zhou GL, Li Y-C. Yuan J, Li A-H, et al. 2018. Gut microbiota profiles in treatment-naive children with attention deficit hyperactivity disorder. Behav. Brain Res. 347: 408-413. DOI
3	Griveau A, Seano G, Shelton SJ, Kupp R, Jahagiri A, Obernier K, et al. 2018. A glial signature and Wnt7 signaling regulate glioma-vascular interactions and tumor microenvironment. Cancer Cell 33: 874-889.e7. DOI
4	Zhang A, Fang H, Chen J, He L, Chen Y. 2020. Role of VEGF-A and LRG1 in abnormal angiogenesis associated with diabetic nephropathy. Front. Physiol. 11: 1064.
5	Krischak MK, Rosett HA, Sachdeva S, Weaver KE, Robert Phillips Heine, Anna E Denoble, et al. 2020. Beyond expert opinion: a comparison of antibiotic regimens for infectious urinary tract pathology in pregnancy. AJP Rep. 10: e352-e356. DOI
6	Dotters-Katz S. 2020. Antibiotics for prophylaxis in the setting of preterm prelabor rupture of membranes. Obstet. Gynecol. Clin. North Am. 47: 595-603. DOI
7	Lammert CR, Frost EL, Bolte AC, Pysour MJ, Shaw ME, Bellinger CE, et al. 2018. Cutting edge: critical roles for microbiota-mediated regulation of the immune system in a prenatal immune activation model of autism. J. Immunol. 201: 845-850. DOI
8	Gonzalez-Perez G, Hicks AL, Tekieli TM, Raden CM, Williams BL, Lamouse-Smith ESN. 2016. Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J. Immunol. 196: 3768-3779. DOI
9	Liu Y, Du DM, Li XF. 2010. Establishment of mice model for dysbiosis of intestinal flora. Chinese J. Microecol. 22: 293-295.
10	Bookstaver PB, Bland CM, Griffin B, Stover KR, Eliand LS, McLaughlin M. 2015. A review of antibiotic use in pregnancy. Pharmacotherapy 35: 1052-1062. DOI
11	Degroote S, Hunting DJ, Baccarelli AA, Takser L. 2016. Maternal gut and fetal brain connection: increased anxiety and reduced social interactions in Wistar rat offspring following peri-conceptional antibiotic exposure. Prog. Neuropsychopharmacol. Biol. Psychiatry 71: 76-82. DOI
12	Vuong HE, Pronovost GN, Williams DW, Coley EJL, Siegler EL, Qiu A, et al. 2020. The maternal microbiome modulates fetal neurodevelopment in mice. Nature 586: 281-286. DOI
13	Azami M, Jaafari Z, Masoumi M, Masoumi M, Shohani M, Badfar G, et al. 2019. The etiology and prevalence of urinary tract infection and asymptomatic bacteriuria in pregnant women in Iran: a systematic review and Meta-analysis. BMC Urol. 19: 43. DOI
14	Hamad AF, Alessi-Severini S, Mahmud S. Brownell M, Kuo IF. 2020. Prenatal antibiotic exposure and risk of attention-deficit/hyperactivity disorder: a population-based cohort study. CMAJ 192: E527-E535. DOI
15	Atladottir HO, Henriksen TB, Schendel DE, Partner ET. 2012. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics 130: e1447-54. DOI
16	Pingping Jiang, Alessia Trimigno, Jan Stanstrup, Bekzod Khakimov, Nanna Viereck, Soren Balling Engelsen, et al. 2017. Antibiotic treatment preventing necrotising enterocolitis alters urinary and plasma metabolomes in preterm pigs. J. Proteome Res. 16: 3547-3557. DOI
17	Luo X, Zheng Y, Wen R, Deng X, Zhou L, Liao H. 2016. Effects of ceftriaxone induced intestinal dysbacteriosis on lym- phocytes in different tissues in mice. Immunobiology 221: 994-1000. DOI
18	Cho SW, Lee JS, Choi SH. 2004. Enhanced oral bioavailability of poorly absorbed drugs. I. Screening of absorption carrier for the ceftriaxone complex. J. Pharm. Sci. 93: 612-620. DOI
19	Haas DM, Marsh DJ, Dang DT, Baker CB, Wing DA, Simhan HN, et al. 2018. Prescription and other medication use in pregnancy. Obstet. Gynecol. 131: 789-798. DOI
20	Yang X, Tang T, Wen J, Li M, Chen J, Li T, et al. 2021. Effects of S24-7 on the weight of progeny rats after exposure to ceftriaxone sodium during pregnancy. BMC Microbiol. 21: 166. DOI
21	Gao X, Jia R, Xie L, Kuang L, Feng L, Wan C. 2018. A study of the correlation between obesity and intestinal flora in school-age children. Sci. Rep. 8: 14511. DOI
22	Yu M, Jia HM, Zhou C, Yang Y, Sun L-L, Zou Z-M. 2017.Urinary and fecal metabonomics study of the protective effect of Chaihu-Shu-Gan-San on antibiotic-induced gut microbiota dysbiosis in rats. Sci. Rep. 7: 46551. DOI
23	Ikuo Kimura, Junki Miyamoto, Ryuji Ohue-Kitano, Keita Watanabe, Takahiro Yamada, Masayoshi Onuki , et al. 2020. Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science 367: eaaw8429. DOI
24	Kim S, Kim H, Yim YS, Ha S, Atarashi K, Tan TG, et al. 2017. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature 549: 528-532. DOI
25	Wang X, Yang J, Zhang H, Zhang H, Yu J, Yao Z. 2019. Oral probiotic administration during pregnancy prevents autism-related behaviors in offspring induced by maternal immune activation via anti-inflammation in mice. Autism Res. 12: 576-588. DOI
26	Aarts E, Ederveen THA, Naaijen J, Zwiers MP, Boekhorst J, Timmerman HM, et al. 2017.Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS One 12: e0183509. DOI
27	Strati F, Cavalieri D, Albanese D, De Delice C, Donati C, Hayek J, et al. 2017. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5: 24. DOI
28	Chen K, Fu Y, Wang Y, Liao L, Xu H, Zhang A, et al. 2020. Therapeutic effects of the in vitro cultured human gut microbiota as transplants on altering gut microbiota and improving symptoms associated with autism spectrum disorder. Microb. Ecol. 80: 475-486. DOI
29	Nie C, He T, Zhang W, Zhang G. 2018. Branched chain amino acids: beyond nutrition metabolism. Int. J. Mol. Sci. 19: 954. DOI
30	Wexler HM. 2007. Bacteroides: the good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20: 593-621. DOI
31	Buffington SA, Di Prisco GV, Auchtung TA, Ajami N, Petrosino JF, Costa-Mattioli M. 2016. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165: 1762-1775. DOI
32	Chen R, Wang J, Zhan R, Zhang L, Wang X. 2019. Fecal metabonomics combined with 16S rRNA gene sequencing to analyze the changes of gut microbiota in rats with kidney-yang deficiency syndrome and the intervention effect of You-gui pill. J. Ethnopharmacol. 244: 112139. DOI
33	Sideromenos S, Lindtner C, Zambon A, Horvath O, Berger A, Pollak DD. 2020. VEGF treatment ameliorates depression-like behavior in adult offspring after maternal immune activation. Cells 9: 1048. DOI
34	Walker AK, Wing EE, Banks WA, Dantzer R. 2019. Leucine competes with kynurenine for blood-to-brain transport and prevents lipopolysaccharide-induced depression-like behavior in mice. Mol. Psychiatry 24: 1523-1532. DOI
35	Da Silva KDL, Fernandes FEM, de Lima Pessoa T, Lima SIVC, Oliveira AG, Martins RR. 2019. Prevalence and profile of adverse drug reactions in high-risk pregnancy: a cohort study. BMC Pregnancy Childbirth 19: 199. DOI
36	Theis V, Theiss C. 2018. VEGF - A stimulus for neuronal development and regeneration in the CNS and PNS. Curr. Protein Pept. Sci. 19: 589-597. DOI
37	Yudkoff M. 2017. Interactions in the metabolism of glutamate and the branched-chain amino acids and ketoacids in the CNS. Neurochem. Res. 42: 10-18. DOI
38	Benakis C, Poon C, Lane D, Brea D, Sita G, Moore J, et al. 2020. Distinct commensal bacterial signature in the gut is associated with acute and long-term protection from ischemic stroke. Stroke 51: 1844-1854. DOI
39	Kim YM, Snijders AM, Brislawn CJ, Stratton KG, Zink EM, Fansler SJ, et al. 2019. Light-stress influences the composition of the murine gut microbiome, memory function, and plasma metabolome. Front. Mol. Biosci. 6: 108. DOI
40	Bourdon AK, Spano GM, Marshall W, Bellesi M, Tononi G, Serra PA, et al. 2018. Metabolomic analysis of mouse prefrontal cortex reveals upregulated analytes during wakefulness compared to sleep. Sci. Rep. 8: 11225. DOI
41	Chanyachukul T, Yoovathaworn K, Thongsaard W, Chongthammakun S, Navasumrit P, Satayavivad J. 2004. Attenuation of paraquat-induced motor behavior and neurochemical disturbances by L-valine in vivo. Toxicol. Lett. 150: 259-269. DOI
42	Sanguinetti E, Collado MC, Marrachelli VG, Monleon D, Selma-Royo M, Pardo-Tendero M, et al. 2018. Microbiome-metabolome signatures in mice genetically prone to develop dementia, fed a normal or fatty diet. Sci. Rep. 8: 4907. DOI
43	Ameratunga M, Pavlakis N, Wheeler H, Grant R, Simes J, Khasraw M, et al. 2018. Anti-angiogenic therapy for high-grade glioma. Cochrane Database Syst. Rev. 11: CD008218.