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BioMed Research International
Volume 2014, Article ID 357062, 9 pages
http://dx.doi.org/10.1155/2014/357062
Research Article

The Association of Toll-Like Receptor 4 Polymorphism with Hepatitis C Virus Infection in Saudi Arabian Patients

1Department of Infection and Immunity, Research Center, King Faisal Specialist Hospital & Research Center, Riyadh 11211, Saudi Arabia
2Department of Microbiology and Immunology, Alfaisal University School of Medicine, Riyadh, Saudi Arabia
3Liver Disease Research Center, King Saud University, Riyadh, Saudi Arabia
4Molecular BioMedicine Program, Research Center, King Faisal Specialist Hospital & Research Center, Riyadh, Saudi Arabia
5Department of Medicine, College of Medicine, King Saud University, Riyadh, Saudi Arabia
6Division of Gastroenterology, Department of Medicine, King Abdulaziz Medical City, Jeddah, Saudi Arabia
7Department of Medicine, King Faisal Specialist Hospital & Research Center, Riyadh, Saudi Arabia
8Department of Gastroenterology & Hepatology, Prince Sultan Military Medical City, Riyadh, Saudi Arabia
9Department of Pathology and Laboratory Medicine, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia

Received 1 June 2014; Accepted 9 July 2014; Published 10 August 2014

Academic Editor: Masayuki Kurosaki

Copyright © 2014 Ahmed A. Al-Qahtani et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. J. Gane, “The natural history of recurrent hepatitis C and what influences this,” Liver Transplantation, vol. 14, supplement 2, pp. S36–S44, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. V. Svitkin, A. Pause, M. Lopez-Lastra, S. Perreault, and N. Sonenberg, “Complete translation of the hepatitis C virus genome in vitro: membranes play a critical role in the maturation of all virus proteins except for NS3,” Journal of Virology, vol. 79, no. 11, pp. 6868–6881, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Simmonds, J. Bukh, C. Combet et al., “Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes,” Hepatology, vol. 42, no. 4, pp. 962–973, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. L. B. Seeff, “Natural history of chronic hepatitis C,” Hepatology, vol. 36, supplement 1, no. 5, pp. S35–S46, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Thursz, L. Yee, and S. Khakoo, “Understanding the host genetics of chronic hepatitis B and C,” Seminars in Liver Disease, vol. 31, no. 2, pp. 115–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Tanaka, N. Nishida, M. Sugiyama et al., “Genome-wide association of IL28B with response to pegylated interferon-α and ribavirin therapy for chronic hepatitis C,” Nature Genetics, vol. 41, no. 10, pp. 1105–1109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. D. L. Thomas, C. L. Thio, M. P. Martin et al., “Genetic variation in IL28B and spontaneous clearance of hepatitis C virus,” Nature, vol. 461, no. 7265, pp. 798–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Abe, H. Ochi, T. Maekawa et al., “Common variation of IL28 affects gamma-GTP levels and inflammation of the liver in chronically infected hepatitis C virus patients,” Journal of Hepatology, vol. 53, no. 3, pp. 439–443, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Eurich, S. Boas-Knoop, M. Bahra et al., “Role of IL28B polymorphism in the development of hepatitis C virus-induced hepatocellular carcinoma, graft fibrosis, and posttransplant antiviral therapy,” Transplantation, vol. 93, no. 6, pp. 644–649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. B. P. Doehle and M. Gale Jr., “evasion strategies of HCV and HIV: common themes for chronic viral infection,” in Nucleic Acid Sensors and Antiviral Immunity, S. Sambhara and T. Fujita, Eds., Landes Bioscience, 2012. View at Google Scholar
  11. E. Thomas, V. D. Gonzalez, Q. Li et al., “HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons,” Gastroenterology, vol. 142, no. 4, pp. 978–988, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Ferwerda, M. B. B. McCall, K. Verheijen et al., “Functional consequences of Toll-like receptor 4 polymorphisms,” Molecular Medicine, vol. 14, no. 5-6, pp. 346–352, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. U. Düesberg, A. von Dem Bussche, C. J. Kirschning, K. Miyake, T. Sauerbruch, and U. Spengler, “Cell activation by synthetic lipopeptides of the hepatitis C virus (HCV)–core protein is mediated by toll like receptors (TLRs) 2 and 4,” Immunology Letters, vol. 84, no. 2, pp. 89–95, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Chang, A. Dolganiuc, and G. Szabo, “Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins,” Journal of Leukocyte Biology, vol. 82, no. 3, pp. 479–487, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Dolganiuc, S. Oak, K. Kodys et al., “Hepatitis C core and nonstructural 3 proteins trigger toll-like receptor 2-mediated pathways and inflammatory activation,” Gastroenterology, vol. 127, no. 5, pp. 1513–1524, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Ait-Goughoulte, A. Banerjee, K. Meyer, B. Mazumdar, K. Saito, and R. B. Ray, “Hepatitis C virus core protein interacts with fibrinogen-β and attenuates cytokine stimulated acute-phase response,” Hepatology, vol. 51, no. 5, pp. 1505–1513, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Arnaud, S. Dabo, D. Akazawa et al., “Hepatitis C virus reveals a novel early control in acute immune response,” PLoS Pathogens, vol. 7, no. 10, Article ID e1002289, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. S. J. Polyak, K. S. A. Khabar, D. M. Paschal et al., “Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response,” Journal of Virology, vol. 75, no. 13, pp. 6095–6106, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. E. A. Kurt-Jones, L. Popova, L. Kwinn et al., “Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus,” Nature Immunology, vol. 1, no. 5, pp. 398–401, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. J. C. Rassa, J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross, “Murine retroviruses activate B cells via interaction with Toll-like receptor 4,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2281–2286, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Howell, P. Angus, P. Gow, and K. Visvanathan, “Toll-like receptors in hepatitis C infection: implications for pathogenesis and treatment,” Journal of Gastroenterology and Hepatology, vol. 28, no. 5, pp. 766–776, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Machida, K. T. H. Cheng, V. M. Sung, A. M. Levine, S. Foung, and M. M. C. Lai, “Hepatitis C virus induces toll-like receptor 4 expression, leading to enhanced production of beta interferon and interleukin-6,” Journal of Virology, vol. 80, no. 2, pp. 866–874, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Huang, M. L. Shiffman, S. Friedman et al., “A 7 gene signature identifies the risk of developing cirrhosis in patients with chronic hepatitis C,” Hepatology, vol. 46, no. 2, pp. 297–306, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Li, M. Chang, O. Abar et al., “Multiple variants in toll-like receptor 4 gene modulate risk of liver fibrosis in Caucasians with chronic hepatitis C infection,” Journal of Hepatology, vol. 51, no. 4, pp. 750–757, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Guo, J. Loke, F. Zheng et al., “Functional linkage of cirrhosis-predictive single nucleotide polymorphisms of Toll-like receptor 4 to hepatic stellate cell responses,” Hepatology, vol. 49, no. 3, pp. 960–968, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. A. A. Abdo, H. A. A. Karim, T. Al Fuhaid et al., “Saudi gastroenterology association guidelines for the diagnosis and management of hepatocellular carcinoma: summary of recommendations,” Annals of Saudi Medicine, vol. 26, no. 4, pp. 261–265, 2006. View at Google Scholar · View at Scopus
  27. R. Bataller, K. E. North, and D. A. Brenner, “Genetic polymorphisms and the progression of liver fibrosis: a critical appraisal,” Hepatology, vol. 37, no. 3, pp. 493–503, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. K. C. Chang, Y. Y. Wu, C. H. Hung et al., “Clinical-guide risk prediction of hepatocellular carcinoma development in chronic hepatitis C patients after interferon-based therapy,” The British Journal of Cancer, vol. 109, no. 9, pp. 2481–2488, 2013. View at Google Scholar
  29. A. Mallat, C. Hezode, and S. Lotersztajn, “Environmental factors as disease accelerators during chronic hepatitis C,” Journal of Hepatology, vol. 48, no. 4, pp. 657–665, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. S. J. Chapman and A. V. S. Hill, “Human genetic susceptibility to infectious disease,” Nature Reviews Genetics, vol. 13, no. 3, pp. 175–188, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. P. J. Clark and A. J. Thompson, “Host genomics and HCV treatment response,” Journal of Gastroenterology and Hepatology, vol. 27, no. 2, pp. 212–222, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. V. Kumar, N. Kato, Y. Urabe et al., “Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma,” Nature Genetics, vol. 43, no. 5, pp. 455–458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Yang, C. Luo, R. Feng, and S. Bi, “The TNF-α, IL-1B and IL-10 polymorphisms and risk for hepatocellular carcinoma: a meta-analysis,” Journal of Cancer Research and Clinical Oncology, vol. 137, no. 6, pp. 947–952, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Promrat, D. H. McDermott, C. M. Gonzalez et al., “Associations of chemokine system polymorphisms with clinical outcomes and treatment responses of chronic hepatitis C,” Gastroenterology, vol. 124, no. 2, pp. 352–360, 2003. View at Google Scholar
  35. D. Miki, H. Ochi, C. N. Hayes et al., “Variation in the DEPDC5 locus is associated with progression to hepatocellular carcinoma in chronic hepatitis C virus carriers,” Nature Genetics, vol. 43, no. 8, pp. 797–800, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Akira and K. Takeda, “Toll-like receptor signalling,” Nature Reviews Immunology, vol. 4, no. 7, pp. 499–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. L. A. J. O'Neill, C. E. Bryant, and S. L. Doyle, “Therapeutic targeting of toll-like receptors for infectious and inflammatory diseases and cancer,” Pharmacological Reviews, vol. 61, no. 2, pp. 177–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Beutler, “Innate immune responses to microbial poisons: discovery and function of the Toll-like receptors,” Annual Review of Pharmacology and Toxicology, vol. 43, pp. 609–628, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. B. S. Park, D. H. Song, H. M. Kim, B. Choi, H. Lee, and J. Lee, “The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex,” Nature, vol. 458, no. 7242, pp. 1191–1195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Resman, J. Vašl, A. Oblak et al., “Essential roles of hydrophobic residues in both MD-2 and toll-like receptor 4 in activation by endotoxin,” The Journal of Biological Chemistry, vol. 284, no. 22, pp. 15052–15060, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Kawai and S. Akira, “TLR signaling,” Cell Death and Differentiation, vol. 13, no. 5, pp. 816–825, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. A. G. Testro and K. Visvanathan, “Toll-like receptors and their role in gastrointestinal disease,” Journal of Gastroenterology and Hepatology, vol. 24, no. 6, pp. 943–954, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Faber, C. U. Meyer, C. Gemmer et al., “Human toll-like receptor 4 mutations are associated with susceptibility to invasive meningococcal disease in infancy,” Pediatric Infectious Disease Journal, vol. 25, no. 1, pp. 80–81, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. B. D. Taylor, T. Darville, R. E. Ferrell, C. M. Kammerer, R. B. Ness, and C. L. Haggerty, “Variants in toll-like receptor 1 and 4 genes are associated with chlamydia trachomatis among women with pelvic inflammatory disease,” Journal of Infectious Diseases, vol. 205, no. 4, pp. 603–609, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Tietze, A. Dalpke, S. Morath, R. Mutters, K. Heeg, and C. Nonnenmacher, “Differences in innate immune responses upon stimulation with gram-positive and gram-negative bacteria,” Journal of Periodontal Research, vol. 41, no. 5, pp. 447–454, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. A. A. Awomoyi, P. Rallabhandi, T. I. Pollin et al., “Association of TLR4 polymorphisms with symptomatic respiratory syncytial virus infection in high-risk infants and young children,” Journal of Immunology, vol. 179, no. 5, pp. 3171–3177, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J. F. Wu, C. Chen, Y. Ni et al., “Toll-like receptor and hepatitis B virus clearance in chronic infected patients: a long-term prospective cohort study in Taiwan,” Journal of Infectious Diseases, vol. 206, no. 5, pp. 662–668, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Bali, S. Pradhan, D. Sharma, and T. Adak, “Toll like receptor 2 and 4 polymorphisms in malaria endemic populations of India,” Human Immunology, vol. 74, no. 2, pp. 223–229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Basu, A. K. Maji, A. Chakraborty et al., “Genetic association of Toll-like-receptor 4 and tumor necrosis factor-α polymorphisms with Plasmodium falciparum blood infection levels,” Infection, Genetics and Evolution, vol. 10, no. 5, pp. 686–696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. F. P. Mockenhaupt, J. P. Cramer, L. Hamann et al., “Toll-like receptor (TLR) polymorphisms in African children: Common TLR-4 variants predispose to severe malaria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 1, pp. 177–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. J. A. Agúndez, E. García-Martín, M. J. Devesa et al., “Polymorphism of the TLR4 gene reduces the risk of hepatitis C virus-induced hepatocellular carcinoma,” Oncology, vol. 82, no. 1, pp. 35–40, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Rudofsky Jr., P. Reismann, S. Witte et al., “Asp299Gly and Thr399Ile genotypes of the TLR4 gene are associated with a reduced prevalence of diabetic neuropathy in patients with type 2 diabetes,” Diabetes Care, vol. 27, no. 1, pp. 179–183, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Kiechl, E. Lorenz, M. Reindl et al., “Toll-like receptor 4 polymorphisms and atherogenesis,” The New England Journal of Medicine, vol. 347, no. 3, pp. 185–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. T. R. D. J. Radstake, B. Franke, S. Hanssen et al., “The Toll-like receptor 4 Asp299Gly functional variant is associated with decreased rheumatoid arthritis disease susceptibility but does not influence disease severity and/or outcome,” Arthritis and Rheumatism, vol. 50, no. 3, pp. 999–1001, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. K. S. Crider, N. Whitehead, and R. M. Buus, “Genetic variation associated with preterm birth: a HuGE review,” Genetics in Medicine, vol. 7, no. 9, pp. 593–604, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Oblak and R. Jerala, “Toll-like receptor 4 activation in cancer progression and therapy,” Clinical and Developmental Immunology, vol. 2011, Article ID 609579, 12 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Machida, H. Tsukamoto, H. Mkrtchyan et al., “Toll-like receptor 4 mediates synergism between alcohol and HCV in hepatic oncogenesis involving stem cell marker Nanog,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 5, pp. 1548–1553, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. M. J. Citores, I. Baños, A. Noblejas, S. Rosado, R. Castejon, and V. Cuervas-Mons, “Toll-like receptor 3 L412F polymorphism may protect against acute graft rejection in adult patients undergoing liver transplantation for hepatitis C-related cirrhosis,” Transplantation Proceedings, vol. 43, no. 6, pp. 2224–2226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Nakamura, T. Kanda, S. Nakamoto et al., “No correlation between PNPLA3 rs738409 genotype and fatty liver and hepatic cirrhosis in Japanese patients with HCV,” PLoS ONE, vol. 8, no. 12, Article ID e81312, 2013. View at Google Scholar
  60. R. Tamura, T. Kanda, F. Imazeki et al., “Hepatitis C virus nonstructural 5A protein inhibits lipopolysaccharide-mediated apoptosis of hepatocytes by decreasing expression of toll-like receptor 4,” Journal of Infectious Diseases, vol. 204, no. 5, pp. 793–801, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. U. Ohto, N. Yamakawa, S. Akashi-Takamura, K. Miyake, and T. Shimizu, “Structural analyses of human toll-like receptor 4 polymorphisms D299G and T399I,” The Journal of Biological Chemistry, vol. 287, no. 48, pp. 40611–40617, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. N. Yamakawa, U. Ohto, S. Akashi-Takamura et al., “Human TLR4 polymorphism D299G/T399I alters TLR4/MD-2 conformation and response to a weak ligand monophosphoryl lipid A,” International Immunology, vol. 25, no. 1, pp. 45–52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. N. C. Arbour, E. Lorenz, B. C. Schutte et al., “TLR4 mutations are associated with endotoxin hyporesponsiveness in humans,” Nature Genetics, vol. 25, no. 2, pp. 187–191, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Figueroa, Y. Xiong, C. Song, W. Piao, S. N. Vogel, and A. E. Medvedev, “The Asp 299Gly polymorphism alters TLR4 signaling by interfering with recruitment of MyD88 and TRIF,” Journal of Immunology, vol. 188, no. 9, pp. 4506–4515, 2012. View at Publisher · View at Google Scholar · View at Scopus