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Article

Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages

  • Authors:
    • Xiu-Ying Li
    • Chun Wang
    • Xue-Rong Xiang
    • Fang-Chun Chen
    • Cong-Ming Yang
    • Jing  Wu
  • View Affiliations / Copyright

    Affiliations: Department of Pharmacy, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P.R. China, Department of Periodontology, The Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing 401147, P.R. China
  • Pages: 1329-1336
    |
    Published online on: July 8, 2013
       https://doi.org/10.3892/or.2013.2600
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Abstract

Porphyromonas gingivalis lipopolysaccharide (P. gingivalis LPS) promotes macrophage-derived foam cell formation, however, the mechanisms are not well established. In macrophages, lipid uptake is mediated by scavenger receptors including SR-A and CD36, while the cholesterol efflux is mediated by ATP-binding cassette transporter G1 (ABCG1), ABCA1 and SR-BI. We further investigated the mechanisms underlying the dysregulation by P. gingivalis LPS of these regulators resulting in the promotion of lipid accumulation in THP-1-derived macrophages. Our results showed that P. gingivalis LPS exacerbated lipid accumulation in oxidized low-density lipoprotein (oxLDL)-treated macrophages. However, cholesterol efflux was inhibited by P. gingivalis LPS in THP-1-derived macrophages. In oxLDL-untreated macrophages, P. gingivalis LPS treatment caused an increase in CD36 mRNA and protein levels, and a decrease in ABCA1 mRNA and protein levels, while having no effect on SR-A, SR-BI or ABCG1 expression. Upregulation of CD36 by P. gingivalis LPS resulted from activation of c-Jun/AP-1, and this was confirmed by the inhibition of increased CD36 expression after AP-1 inhibition using SP600125. However, the decreased protein stability of ABCA1 by P. gingivalis LPS was a result of increased calpain activity. Moreover, small hairpin RNA (shRNA) targeting heme oxygenase-1 (HO-1) augmented the P. gingivalis LPS-induced atherogenic effects on the expression of c-Jun/AP-1, CD36, ABCA1 and calpain activity. Accordingly, P. gingivalis LPS-regulated promotion of lipid accumulation in foam cells was also exacerbated by HO-1 shRNA. These results indicate that P. gingivalis LPS confers a exacerbation effect on the formation of foam cells by a novel HO-1-dependent mediation of cholesterol efflux and lipid accumulation in macrophages.
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1 

Xue JH, Yuan Z, Wu Y, et al: High glucose promotes intracellular lipid accumulation in vascular smooth muscle cells by impairing cholesterol influx and efflux balance. Cardiovasc Res. 86:141–150. 2010. View Article : Google Scholar : PubMed/NCBI

2 

Li AC and Glass CK: The macrophage foam cell as a target for therapeutic intervention. Nat Med. 8:1235–1242. 2002. View Article : Google Scholar : PubMed/NCBI

3 

Kleemann R, Zadelaar S and Kooistra T: Cytokines and atherosclerosis: a comprehensive review of studies in mice. Cardiovasc Res. 79:360–376. 2008. View Article : Google Scholar : PubMed/NCBI

4 

Lin CY, Lee TS, Chen CC, Chang CA, Lin YJ, Hsu YP and Ho LT: Endothelin-1 exacerbates lipid accumulation by increasing the protein degradation of the ATP-binding cassette transporter G1 in macrophages. J Cell Physiol. 226:2198–2205. 2011. View Article : Google Scholar : PubMed/NCBI

5 

Cheng LC, Su KH, Kou YR, Shyue SK, et al: α-Lipoic acid ameliorates foam cell formation via liver X receptor α-dependent upregulation of ATP-binding cassette transporters A1 and G1. Free Radic Biol Med. 50:47–54. 2011.

6 

Park YM, Kashyap SR, Major J and Silverstein RL: Insulin promotes macrophage foam cell formation: potential implications in diabetes-related atherosclerosis. Lab Invest. 92:1171–1180. 2012. View Article : Google Scholar : PubMed/NCBI

7 

Morimoto Y, Kikuchi K, Ito T, et al: MK615 attenuates Porphyromonas gingivalis lipopolysaccharide-induced pro-inflammatory cytokine release via MAPK inactivation in murine macrophage-like RAW264.7 cells. Biochem Biophys Res Commun. 389:90–94. 2009.

8 

Triantafilou M, Gamper FG, Lepper PM, et al: Lipopolysaccharides from atherosclerosis-associated bacteria antagonize TLR4, induce formation of TLR2/1/CD36 complexes in lipid rafts and trigger TLR2-induced inflammatory responses in human vascular endothelial cells. Cell Microbiol. 9:2030–2039. 2007. View Article : Google Scholar

9 

Nakamura N, Yoshida M, Umeda M, et al: Extended exposure of lipopolysaccharide fraction from Porphyromonas gingivalis facilitates mononuclear cell adhesion to vascular endothelium via Toll-like receptor-2 dependent mechanism. Atherosclerosis. 196:59–67. 2008.PubMed/NCBI

10 

Kiechl S, Egger G, Mayr M, et al: Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation. 103:1064–1070. 2001. View Article : Google Scholar : PubMed/NCBI

11 

Gitlin JM and Loftin CD: Cyclooxygenase-2 inhibition increases lipopolysaccharide-induced atherosclerosis in mice. Cardiovasc Res. 81:400–407. 2009. View Article : Google Scholar : PubMed/NCBI

12 

Lei L, Li H, Yan F, Li Y and Xiao Y: Porphyromonas gingivalis lipopolysaccharide alters atherosclerotic-related gene expression in oxidized low-density-lipoprotein-induced macrophages and foam cells. J Periodontal Res. 46:427–437. 2011. View Article : Google Scholar

13 

Pussinen PJ and Mattila K: Periodontal infections and atherosclerosis: mere associations? Curr Opin Lipidol. 15:583–588. 2004. View Article : Google Scholar : PubMed/NCBI

14 

Qi M, Miyakawa H and Kuramitsu HK: Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog. 35:259–267. 2003. View Article : Google Scholar

15 

Kuramitsu HK, Kang IC and Qi M: Interactions of Porphyromonas gingivalis with host cells: implications for cardiovascular diseases. J Periodontol. 74:85–89. 2003.

16 

Kuramitsu HK, Qi M, Kang IC and Chen W: Role for periodontal bacteria in cardiovascular diseases. Ann Periodontol. 6:41–47. 2001. View Article : Google Scholar : PubMed/NCBI

17 

Kuramitsu HK, Miyakawa H, Qi M and Kang IC: Cellular responses to oral pathogens. Ann Periodontol. 7:90–94. 2002. View Article : Google Scholar : PubMed/NCBI

18 

Katayama I, Hotokezaka Y, Matsuyama T, Sumi T and Nakamura T: Ionizing radiation induces macrophage foam cell formation and aggregation through JNK-dependent activation of CD36 scavenger receptors. Int J Radiat Oncol Biol Phys. 70:835–846. 2008. View Article : Google Scholar : PubMed/NCBI

19 

Li XY, Kong LX, Li J, He HX and Zhou YD: Kaempferol suppresses lipid accumulation in macrophages through the downregulation of cluster of differentiation 36 and the upregulation of scavenger receptor class B type I and ATP-binding cassette transporters A1 and G1. Int J Mol Med. 31:331–338. 2013.

20 

Tsai JY, Su KH, Shyue SK, et al: EGb761 ameliorates the formation of foam cells by regulating the expression of SR-A and ABCA1: role of haem oxygenase-1. Cardiovasc Res. 88:415–423. 2010. View Article : Google Scholar : PubMed/NCBI

21 

Feng B and Tabas I: ABCA1-mediated cholesterol efflux is defective in free cholesterol-loaded macrophages. Mechanism involves enhanced ABCA1 degradation in a process requiring full NPC1 activity. J Biol Chem. 277:43271–43280. 2002. View Article : Google Scholar

22 

Wang Y and Oram JF: Unsaturated fatty acids inhibit cholesterol efflux from macrophages by increasing degradation of ATP-binding cassette transporter A1. J Biol Chem. 277:5692–5697. 2002. View Article : Google Scholar : PubMed/NCBI

23 

Kim HS, Park SY, Kim EK, Ryu EY, Kim YH, Park G and Lee SJ: Acanthopanax senticosus has a heme oxygenase-1 signaling-dependent effect on Porphyromonas gingivalis lipopolysaccharide-stimulated macrophages. J Ethnopharmacol. 142:819–828. 2012. View Article : Google Scholar

24 

de Winther MP and Hofker MH: Scavenging new insights into atherogenesis. J Clin Invest. 105:1039–1041. 2000.PubMed/NCBI

25 

Kunjathoor VV, Febbraio M, Podrez EA, et al: Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem. 277:49982–49988. 2002. View Article : Google Scholar

26 

Ortiz-Masià D, Díez I, Calatayud S, et al: Induction of CD36 and thrombospondin-1 in macrophages by hypoxia-inducible factor 1 and its relevance in the inflammatory process. PLoS One. 7:e485352012.PubMed/NCBI

27 

Brooks-Wilson A, Marcil M, Clee SM, et al: Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet. 22:336–345. 1999. View Article : Google Scholar : PubMed/NCBI

28 

Maekawa T, Takahashi N, Tabeta K, et al: Chronic oral infection with Porphyromonas gingivalis accelerates atheroma formation by shifting the lipid profile. PLoS One. 6:e202402011.

29 

Oram JF and Heinecke JW: ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev. 85:1343–1372. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Yin K, Liao DF and Tang CK: ATP-binding membrane cassette transporter A1 (ABCA1): a possible link between inflammation and reverse cholesterol transport. Mol Med. 16:438–449. 2010.PubMed/NCBI

31 

Martinez LO, Agerholm-Larsen B, Wang N, Chen W and Tall AR: Phosphorylation of a pest sequence in ABCA1 promotes calpain degradation and is reversed by ApoA-I. J Biol Chem. 278:37368–37374. 2003. View Article : Google Scholar : PubMed/NCBI

32 

Arakawa R and Yokoyama S: Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J Biol Chem. 277:22426–22429. 2002. View Article : Google Scholar

33 

Liu XY, Lu Q, Ouyang XP, et al: Apelin-13 increases expression of ATP-binding cassette transporter A1 via activating protein kinase C α signaling in THP-1 macrophage-derived foam cells. Atherosclerosis. 226:398–407. 2013.PubMed/NCBI

34 

Orozco LD, Kapturczak MH, Barajas B, et al: Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res. 100:1703–1711. 2007. View Article : Google Scholar : PubMed/NCBI

35 

Idriss NK, Blann AD and Lip GY: Hemoxygenase-1 in cardiovascular disease. J Am Coll Cardiol. 52:971–978. 2008. View Article : Google Scholar

36 

Ishikawa K, Sugawara D, Wang Xp, Suzuki K, Itabe H, Maruyama Y and Lusis AJ: Heme oxygenase-1 inhibits atherosclerotic lesion formation in ldl-receptor knockout mice. Circ Res. 88:506–512. 2001. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Li X, Wang C, Xiang X, Chen F, Yang C and Wu J: Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages. Oncol Rep 30: 1329-1336, 2013.
APA
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., & Wu, J. (2013). Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages. Oncology Reports, 30, 1329-1336. https://doi.org/10.3892/or.2013.2600
MLA
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., Wu, J."Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages". Oncology Reports 30.3 (2013): 1329-1336.
Chicago
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., Wu, J."Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages". Oncology Reports 30, no. 3 (2013): 1329-1336. https://doi.org/10.3892/or.2013.2600
Copy and paste a formatted citation
x
Spandidos Publications style
Li X, Wang C, Xiang X, Chen F, Yang C and Wu J: Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages. Oncol Rep 30: 1329-1336, 2013.
APA
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., & Wu, J. (2013). Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages. Oncology Reports, 30, 1329-1336. https://doi.org/10.3892/or.2013.2600
MLA
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., Wu, J."Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages". Oncology Reports 30.3 (2013): 1329-1336.
Chicago
Li, X., Wang, C., Xiang, X., Chen, F., Yang, C., Wu, J."Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages". Oncology Reports 30, no. 3 (2013): 1329-1336. https://doi.org/10.3892/or.2013.2600
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