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J Periodontal Res. 2021 Dec 19; doi: 10.1111/jre.12963. Epub 2021 Dec 19.

Distribution of neutrophil and monocyte/macrophage populations induced by the CXCR4 inhibitor AMD3100 in blood and periodontal tissue early after periodontitis induction.

Journal of periodontal research

Ae Ri Kim, Eun-Jung Bak, Yun-Jung Yoo

Affiliations

  1. Department of Oral Biology, Yonsei University College of Dentistry, Seoul, South Korea.
  2. Department of Applied Life Science, The Graduate School, Yonsei University, Seoul, South Korea.
  3. BK21 PLUS Project, Yonsei University College of Dentistry, Seoul, South Korea.

PMID: 34927238 DOI: 10.1111/jre.12963

Abstract

CXCR4, a CXCL12 receptor, is expressed on epithelial cells, fibroblasts, and inflammatory cells. The CXCR4-CXCL12 interaction is related to the migration of neutrophils and monocytes/macrophages. Periodontitis, an inflammatory disease mainly caused by gram-negative bacteria, is characterized by infiltration of circulating inflammatory cells and alveolar bone (AB) loss. To investigate whether CXCR4 is involved in the distribution of neutrophils and monocytes/macrophages early after periodontitis induction, we examined the effects of AMD3100 (AMD), a CXCR4 antagonist, in ligature-induced periodontitis mice and LPS-injected air pouch mice. The periodontitis study was accomplished in control (C), periodontitis (P), and P + AMD groups. Periodontitis was induced by ligation of the mandibular first molar. AMD was intraperitoneally administered daily beginning the day before ligation until sacrifice on the third day after ligation. The air pouch study was accomplished in C, lipopolysaccharide (LPS), and LPS + AMD groups. Air pouches on mice backs were formed by subcutaneous injection of sterilized air. AMD was administered and then LPS was injected into the air pouch. For the detection of neutrophils and monocytes/macrophages in blood and air pouch exudates, flow cytometry was performed with anti-Ly6G/anti-CD11b antibodies (Abs) and anti-CD115 Ab, respectively. In periodontal tissue, Ly6G

© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Keywords: CXCR4; macrophage; monocyte; neutrophil; periodontitis

References

  1. Pozzobon T, Goldoni G, Viola A, Molon B. CXCR4 signaling in health and disease. Immunol Lett. 2016;177:6-15. - PubMed
  2. Eash KJ, Means JM, White DW, Link DC. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood. 2009;113(19):4711-4719. - PubMed
  3. Hong CW. Current understanding in neutrophil differentiation and heterogeneity. Immune Netw. 2017;17(5):298-306. - PubMed
  4. Martin C, Burdon PC, Bridger G, Gutierrez-Ramos JC, Williams TJ, Rankin SM. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity. 2003;19(4):583-593. - PubMed
  5. Hampton HR, Bailey J, Tomura M, Brink R, Chtanova T. Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes. Nat Commun. 2015;6:7139. - PubMed
  6. Jung H, Mithal DS, Park JE, Miller RJ. Localized CCR2 activation in the bone marrow niche mobilizes monocytes by desensitizing CXCR4. PLoS One. 2015;10(6):e0128387. - PubMed
  7. Chong SZ, Evrard M, Devi S, et al. CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses. J Exp Med. 2016;213(11):2293-2314. - PubMed
  8. Meyle J, Dommisch H, Groeger S, Giacaman RA, Costalonga M, Herzberg M. The innate host response in caries and periodontitis. J Clin Periodontol. 2017;44(12):1215-1225. - PubMed
  9. Hajishengallis G. New developments in neutrophil biology and periodontitis. Periodontol. 2020;82(1):78-92. - PubMed
  10. Havens AM, Chiu E, Taba M, et al. Stromal-derived factor-1α (CXCL12) levels increase in periodontal disease. J Periodontol. 2008;79(5):845-853. - PubMed
  11. Sun J, Nemoto E, Hong G, Sasaki K. Modulation of stromal cell-derived factor 1 alpha (SDF-1α) and its receptor CXCR4 in Porphyromonas gingivalis-induced periodontal inflammation. BMC Oral Health. 2016;17(1):26. - PubMed
  12. Liu Q, Li Z, Gao JL, et al. CXCR4 antagonist AMD3100 redistributes leukocytes from primary immune organs to secondary immune organs, lung, and blood in mice. Eur J Immunol. 2015;45(6):1855-1867. - PubMed
  13. Swamydas M, Luo Y, Dorf ME, Lionakis MS. Isolation of mouse neutrophils. Curr Protoc Immunol. 2015;110(1):21-23. - PubMed
  14. Lee PY, Wang JX, Parisini E, Dascher CC, Nigrovic PA. Ly6 family proteins in neutrophil biology. J Leukoc Biol. 2013;94(4):585-594. - PubMed
  15. Breslin WL, Strohacker K, Carpenter KC, Haviland DL, McFarlin BK. Mouse blood monocytes: standardizing their identification and analysis using CD115. J Immunol Methods. 2013;390(1-2):1-8. - PubMed
  16. Lee DE, Kim JH, Choi SH, Cha JH, Bak EJ, Yoo YJ. Periodontitis mainly increases osteoclast formation via enhancing the differentiation of quiescent osteoclast precursors into osteoclasts. J Periodontal Res. 2015;50(2):256-264. - PubMed
  17. Kim JH, Lee DE, Cha JH, Bak EJ, Yoo YJ. Receptor activator of nuclear factor-κB ligand and sclerostin expression in osteocytes of alveolar bone in rats with ligature-induced periodontitis. J Periodontol. 2014;85(11):e370-e378. - PubMed
  18. Gaddale R, Mudda JA, Karthikeyan I, Desai SR, Shinde H, Deshpande P. Changes in cellular and molecular components of peripheral blood in patients with generalized aggressive periodontitis. J Investig Clin Dent. 2016;7(1):59-64. - PubMed
  19. Nagasawa T, Kobayashi H, Aramaki M, Kiji M, Oda S, Izumi Y. Expression of CD14, CD16 and CD45RA on monocytes from periodontitis patients. J Periodontal Res. 2004;39(1):72-78. - PubMed
  20. Zhang Z, Yuan W, Deng J, et al. Granulocyte colony stimulating factor (G-CSF) regulates neutrophils infiltration and periodontal tissue destruction in an experimental periodontitis. Mol Immunol. 2020;117:110-121. - PubMed
  21. O'Boyle C, Haley MJ, Lemarchand E, et al. Ligature-induced periodontitis induces systemic inflammation but does not alter acute outcome after stroke in mice. Int J Stroke. 2020;15(2):175-187. - PubMed
  22. Hajishengallis G, Chavakis T, Hajishengallis E, Lambris JD. Neutrophil homeostasis and inflammation: novel paradigms from studying periodontitis. J Leukoc Biol. 2015;98(4):539-548. - PubMed
  23. Younes R, Ghorra C, Khalife S, et al. Pertinent cell population to characterize periodontal disease. Tissue Cell. 2009;41(2):141-150. - PubMed
  24. Nagashima H, Shinoda M, Honda K, et al. CXCR4 signaling in macrophages contributes to periodontal mechanical hypersensitivity in Porphyromonas gingivalis-induced periodontitis in mice. Mol Pain. 2017;13:1744806916689269. - PubMed
  25. Hughes CE, Nibbs RJB. A guide to chemokines and their receptors. FEBS J. 2018;285(16):2944-2971. - PubMed
  26. Duarte DB, Vasko MR, Fehrenbacher JC. Models of inflammation: carrageenan air pouch. Curr Protoc Pharmacol. 2016;72(1):1-9. - PubMed
  27. Hajishengallis G, Wang M, Liang S, Triantafilou M, Triantafilou K. Pathogen induction of CXCR4/TLR2 cross-talk impairs host defense function. Proc Natl Acad Sci USA. 2008;105(36):13532-13537. - PubMed
  28. Nagashima H, Shinoda M, Honda K, et al. CXCR4 signaling contributes to alveolar bone resorption in Porphyromonas gingivalis-induced periodontitis in mice. J Oral Sci. 2017;59(4):571-577. - PubMed
  29. McIntosh ML, Hajishengallis G. Inhibition of Porphyromonas gingivalis-induced periodontal bone loss by CXCR4 antagonist treatment. Mol Oral Microbiol. 2012;27(6):449-457. - PubMed

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