Sex-dependent alterations in motor and anxiety-like behavior of aged bacterial peptidoglycan sensing molecule 2 knockout mice
Open accessAbstract
Peptidoglycan recognition proteins (PGRPs) are key sensing-molecules of the innate immune system that specifically detect bacterial peptidoglycan (PGN) and its derivates. PGRPs have recently emerged as potential key regulators of normal brain development and behavior. To test the hypothesis that PGRPs play a role in motor control and anxiety-like behavior in later life, we used 15-month old male and female peptidoglycan recognition protein 2 (Pglyrp2) knockout (KO) mice. Pglyrp2 is an N-acetylmuramyl-l-alanine amidase that hydrolyzes PGN between the sugar backbone and the peptide chain (which is unique among the mammalian PGRPs). Using a battery of behavioral tests, we demonstrate that Pglyrp2 KO male mice display decreased levels of anxiety-like behavior compared with wild type (WT) males. In contrast, Pglyrp2 KO female mice show reduced rearing activity and increased anxiety-like behavior compared to WT females. In the accelerated rotarod test, however, Pglyrp2 KO female mice performed better compared to WT females (i.e., they had longer latency to fall off the rotarod). Further, Pglyrp2 KO male mice exhibited decreased expression levels of synaptophysin, gephyrin, and brain-derived neurotrophic factor in the frontal cortex, but not in the amygdala. Pglyrp2 KO female mice exhibited increased expression levels of spinophilin and alpha-synuclein in the frontal cortex, while exhibiting decreased expression levels of synaptophysin, gephyrin and spinophilin in the amygdala. Our findings suggest a novel role for Pglyrp2asa key regulator of motor and anxiety-like behavior in late life.
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Some studies involving GF Swiss Webster mice show decreased anxiety-like behavior whereas the opposite has been found in male GF BALB/c mice.
“For example, some studies involving GF Swiss Webster mice show a decreased anxiety-like behavior (Arentsen et al., 2018;Clarke et al., 2013;Neufeld et al., 2011) whereas the opposite has been found in male GF BALB/c mice (Chen et al., 2017b;Nishino et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Arentsen et al., 2018
The Discussion (section 4; page unavailable) says germ-free animal studies show that gut microbiota affect anxiety-like behavior, but it does not identify Swiss Webster mice or state the direction of that effect in them. Its reported decrease in anxiety-like behavior concerns male Pglyrp2 knockout mice, not germ-free mice. The BALB/c clause is attached to other citations and is not assessed here. (LLM, conf=0.83)
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Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.77 · Cited by 1,893 · see citing works
The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior
Arentsen, T., Qian, Y., Gkotzis, S., Femenia, T., Wang, T., Udekwu, K., Forssberg, H., & Diaz Heijtz, R. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.182 · Cited by 280 · see citing works
Self-citationNakajima, M., Görlich, A., & Heintz, N. (2014) · Cell · doi:10.1016/j.cell.2014.09.020 · Cited by 262 · see citing works
A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
Li, K., Nakajima, M., Ibañez-Tallon, I., & Heintz, N. (2016) · Cell · doi:10.1016/j.cell.2016.08.067 · Cited by 234 · see citing works
PirB regulates a structural substrate for cortical plasticity.
Djurisic, M., Vidal, G. S., Mann, M., Aharon, A., Kim, T., Ferrao Santos, A., Zuo, Y., Hübener, M., & Shatz, C. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321092110 · Cited by 79 · see citing works
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Research works printed but not linked: 5
- Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Bjorkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., Pettersson, S., 2011. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. U.S.A. 108, 3047-3052.
- Dziarski, R., Gupta, D., 2010. Review: mammalian peptidoglycan recognition proteins (PGRPs) in innate immunity. Innate Immun. 16, 168-174.
- Neufeld, K.M., Kang, N., Bienenstock, J., Foster, J.A., 2011. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23 (255-264), e119.
- Okun, E., Griffioen, K., Barak, B., Roberts, N.J., Castro, K., Pita, M.A., Cheng, A., Mughal, M.R., Wan, R., Ashery, U., Mattson, M.P., 2010a. Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 107, 15625-15630.
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Bacterial Peptidoglycans from Microbiota in Neurodevelopment and Behavior
Gonzalez-Santana, A., & Diaz Heijtz, R. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.05.003 · Cited by 118 · see citing works
Self-citation
- Authors
- Arentsen, T., Khalid, R., Qian, Y., & Diaz Heijtz, R.
- Affiliations
- Karolinska Institutet (SE)
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2018-01
- Volume
- 67
- Pages
- 345-354
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2757298064
- Cited by
- 42
- References
- 5
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 9 · 2022: 8 · 2021: 3 · 2020: 3 · 2019: 6 · 2018: 3
- FWCI
- 1.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain Behavior and Immunity (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Olle Engkvist Byggmästare Foundation
- Swedish Research Council (K2015-62X-22745-01-4)
- Swedish Brain Foundation
- Knut and Alice Wallenberg Foundation
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- peptidoglycan sensing, innate immunity, aging, sex differences, anxiety-like behavior, motor behavior, rotarod performance, synaptophysin, gephyrin, spinophilin, alpha-synuclein, brain-derived neurotrophic factor, frontal cortex, amygdala, knockout mice
- MeSH terms
- Amygdala, Animals, Anxiety, Behavior, Animal, Female, Frontal Lobe, Male, Mice, Inbred C57BL, Motor Activity, N-Acetylmuramoyl-L-alanine Amidase, Neuronal Plasticity, Sex Characteristics, Mice, Knockout, Rotarod Performance Test
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