Involvement of heat shock protein 47 in Schistosoma japonicum-induced hepatic fibrosis in mice

International Journal for Parasitology

Volumn 44, Issue 1, 2014, Pages 23-35

  Huang, Jia Quan ^a   Tao, Ran ^a   Li, Lan ^a   Ma, Ke ^a   Xu, Lei ^a   Ai, Guo ^a   Fan, Xiang Xue ^a   Jiao, Yun Tao ^a   Ning, Qin ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Cytokines; Heat shock protein 47; Hepatic fibrosis; Schistosomiasis japonica; Short hairpin RNA

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; GELATINASE B; HEAT SHOCK PROTEIN 47; INTERLEUKIN 13; INTERLEUKIN 17; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN COL1A1; PROTEIN COL3A1; SHORT HAIRPIN RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

GENE EXPRESSION; PARASITE; PROTEIN; RNA; SCHISTOSOMIASIS;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; ENZYME ACTIVITY; FEMALE; FETUS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PORTAL HYPERTENSION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; RNA INTERFERENCE; SCHISTOSOMIASIS JAPONICA; SPLEEN WEIGHT; SPLENOMEGALY; SURVIVAL RATE; SURVIVAL TIME;

JAPONICA; MURINAE; MUS; RODENTIA; SCHISTOSOMA; SCHISTOSOMA JAPONICUM; SCHISTOSOMATIDAE;

CYTOKINES; HEAT SHOCK PROTEIN 47; HEPATIC FIBROSIS; SCHISTOSOMIASIS JAPONICA; SHORT HAIRPIN RNA;

ADULT; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE SILENCING; HSP47 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER CIRRHOSIS; MALE; MICE; MIDDLE AGED; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA; SURVIVAL ANALYSIS;

EID: 84892370311     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.08.009     Document Type: Article

References (49)

1. Arthur M.J., Mann D.A., Iredale J.P. Tissue inhibitors of metalloproteinases, hepatic stellate cells and liver fibrosis. J. Gastroenterol. Hepatol. 1998, 13(Suppl.):33-38.
2. Andrade Z.A. Schistosomiasis and hepatic fibrosis regression. Acta Trop. 2008, 108:79-82.
3. Arnaud V., Li J., Wang Y., Fu X., Mengzhi S., Luo X., Hou X., Dessein H., Jie Z., Xin-Ling Y., He H., McManus D.P., Li Y., Dessein A. Regulatory role of interleukin-10 and interferon-gamma in severe hepatic central and peripheral fibrosis in humans infected with Schistosoma japonicum. J. Infect. Dis. 2008, 198:418-426.
4. Abdul-Ghani R.A., Hassan A.A. Murine schistosomiasis as a model for human schistosomiasis mansoni: similarities and discrepancies. Parasitol. Res. 2010, 107:1-8.
5. Anthony B.J., Ramm G.A., McManus D.P. Role of resident liver cells in the pathogenesis of schistosomiasis. Trends Parasitol. 2012, 12:531-580.
6. Biempica S.L., Wu C.H., Rojkind M. Liver collagen-type characterization in human schistosomiasis. A histological, ultrastructural, and immunocytochemical correlation. Am. J. Trop. Med. Hyg. 1983, 32:316-325.
7. Biempica L., Dunn M.A., Kamel I.A., Kamel R., Hait P.K., Fleischner C., Ming-Gang Chen Schistosoma japonicum and S. japonicum-like infections: epidemiology, clinical and pathological aspects. Human Schistosomiasis 1993, 237-270. CAB International, Wallingford. P. Jordan, G. Webbe, F.S. Sturrock (Eds.).
8. Breitkopf K., Haas S., Wiercinska E., Singer M.V., Dooley S. Anti-TGF-beta strategies for the treatment of chronic liver disease. Alcohol. Clin. Exp. Res. 2005, 29(Suppl.):121-131.
9. Bartley P.B., Ramm G.A., Jones M.K., Ruddell R.G., Li Y., McManus D.P. A contributory role for activated hepatic stellate cells in the dynamics of Schistosoma japonicum egg-induced fibrosis. Int. J. Parasitol. 2006, 36:993-1001.
10. Berhe N., Myrvang B., Gundersen S.G. Reversibility of schistosomal periportal thickening/fibrosis after praziquantel therapy: a twenty-six month follow-up study in Ethiopia. Am. J. Trop. Med. Hyg. 2008, 78:228-234.
11. Burke M.L., Jones M.K., Gobert G.N., Li Y.S., Ellis M.K., McManus D.P. Immunopathogenesis of human schistosomiasis. Parasite Immunol. 2009, 31:163-176.
12. Cheever A.W. Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bull. World Health Organ. 1968, 39:328-331.
13. Cortez-Pinto H., Baptista A., Camilo M.E., de Moura M.C. Hepatic stellate cell activation occurs in nonalcoholic steatohepatitis. Hepatogastroenterology 2001, 48:87-90.
14. Chu D., Luo Q., Li C., Gao Y., Yu L., Wei W., Wu Q., Shen J. Paeoniflorin inhibits TGF-beta1-mediated collagen production by Schistosoma japonicum soluble egg antigen in vitro. Parasitology 2007, 134:1611-1621.
15. Coutinho H.M., Acosta L.P., Wu H.W., McGarvey S.T., Su L., Langdon G.C., Jiz M.A., Jarilla B., Olveda R.M., Friedman J.F., Kurtis J.D. Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. J. Infect. Dis. 2007, 195:288-295.
16. Cheng K., Yang N., Mahato R.I. TGF-β1 gene silencing for treating liver fibrosis. Mol. Pharm. 2009, 6:772-779.
17. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-831.
18. Fichtner-Feigl S., Strober W., Kawakami K., Puri R.K., Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat. Med. 2006, 12:99-106.
19. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 2008, 88:125-172.
20. Friedman S.L. Evolving challenges in hepatic fibrosis. Nat. Rev. Gastroenterol. Hepatol. 2010, 7:425-436.
21. Griffiths G. Fine Structure Immunocytochemistry 1993, Springer, Berlin.
22. Gryseels B., Polman K., Clerinx J., Kestens L. Human schistosomiasis. Lancet 2006, 368:1106-1118.
23. Giannone F.A., Baldassarre M., Domenicali M., Zaccherini G., Trevisani F., Bernardi M., Caraceni P. Reversal of liver fibrosis by the antagonism of endocannabinoid CB1 receptor in a rat model of CCl(4)-induced advanced cirrhosis. Lab. Invest. 2012, 92:384-395.
24. Hagiwara S., Iwasaka H., Matsumoto S., Noguchi T. Introduction of antisense oligonueleotides to heat shock protein 47 prevents pulmonary fibrosis in lipopolysaeeharide-induced pneumopathy of the rat. Eur. J. Pharmacol. 2007, 564:174-180.
25. Hope M., Duke M., McManus D.P. A biological and immunological comparison of Chinese and Philippine Schistosoma japonicum. Int. J. Parasitol. 1996, 26:325-332.
26. Hu S., Wang Y., Lichtenstein L., Tao Y., Musch M.W., Jabri B., Antonopoulos D., Claud E.C., Chang E.B. Regional differences in colonic mucosa-associated microbiota determine the physiological expression of host heat shock proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:1266-1275.
27. Kawada N., Kuroki T., Kobayashi K., Inoue M., Nakatani K., Kaneda K., Nagata K. Expression of heat-shock protein 47 in mouse liver. Cell Tissue Res. 1996, 284:341-346.
28. Krizhanovsky V., Yon M., Dickins R.A., Hearn S., Simon J., Miething C., Yee H., Zender L., Lowe S.W. Senescence of activated stellate cells limits liver fibrosis. Cell 2008, 134:657-667.
29. Kovalenko E., Tacke F., Gressner O.A., Zimmermann H.W., Lahme B., Janetzko A., Wiederholt T., Berg T., Müller T., Trautwein C., Gressner A.M., Weiskirchen R. Validation of connective tissue growth factor (CTGF/CCN2) and its gene polymorphisms as noninvasive biomarkers for the assessment of liver fibrosis. J. Viral Hepat. 2009, 16:612-620.
30. Liang Y.J., Luo J., Yuan Q., Zheng D., Liu Y.P., Shi L., Zhou Y., Chen A.L., Ren Y.Y., Sun K.Y., Sun Y., Wang Y., Zhang Z.S. New insight into the antifibrotic effects of praziquantel on mice in infection with Schistosoma japonicum. PLoS ONE 2011, 6:e20247.
31. Lambeth L.S., Smith C.A. Short hairpin RNA-mediated gene silencing. Methods Mol. Biol. 2013, 942:205-232.
32. Liu P., Wang M., Lu X.D., Zhang S.J., Tang W.X. Schistosoma japonicum egg antigen up-regulates fibrogenesis and inhibits proliferation in primary hepatic stellate cells in a concentration-dependent manner. World J. Gastroenterol. 2013, 19:1230-1238.
33. Morcos S.H., Khayyal M.T., Mansour M.M., Saleh S., Ishak E.A. Reversal of hepatic fibrosis after praziquantel therapy of murine schistosomiasis. Am. J. Trop. Med. Hyg. 1985, 34:314-321.
34. Masuda H., Fukumoto M., Hirayoshi K., Nagata K. Coexpression of the collagen-binding stress protein HSP47 gene and the alpha 1(I) and alpha 1(III) collagen genes in carbon tetrachloride-induced rat liver fibrosis. J. Clin. Invest. 1994, 94:2481-2488.
35. McManus D.P., Loukas A. Current status of vaccines for schistosomiasis. Clin. Microbiol. Rev. 2008, 21:225-242.
36. McManus D.P., Gray D.J., Li Y., Feng Z., Williams G.M., Stewart D., Rey-Ladino J., Ross A.G. Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. Clin. Microbiol. Rev. 2010, 23:442-466.
37. Natsume T., Koide T., Yokota S., Hirayshi K., Nagata K. Interactions between collagen-binding stress protein HSP47 and collagen. Analysis of kinetic parameters by surface plasmon resonance biosensor. J. Biol. Chem. 1994, 269:31224-31228.
38. Nishikawa Y., Takahara Y., Asada S., Shigenaga A., Otaka A., Kitagawa K., Koide T. A structure-activity relationship study elucidating the mechanism of sequence-specific collagen recognition by the chaperone HSP47. Bioorg. Med. Chem. 2010, 18:3767-3775.
39. Roderfeld M., Hemmann S., Roeb E. Mechanisms of fibrinolysis in chronic liver injury (with special emphasis on MMPs and TIMPs). Z. Gastroenterol. 2007, 45:25-33.
40. Scheuer P.J. Evaluation of liver biopsies in chronic hepatitis. Orv. Hetil. 1994, 135:2309-2311.
41. Sunamoto M., Kuze K., Iehara N., Takeoka H., Nagata K., Kita T., Doi T. Expression of heat shock protein 47 is increased in remnant kidney and correlates with disease progression. Int. J. Exp. Pathol. 1998, 79:133-140.
42. Seki E., De Minicis S., Osterreicher C.H., Kluwe J., Osawa Y., Brenner D.A., Schwabe R.F. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 2007, 13:1324-1332.
43. Sato Y., Murase K., Kato J., Kobune M., Sato T., Kawano Y., Takimoto R., Takada K., Miyanishi K., Matsunaga T., Takayama T., Niitsu Y. Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone. Nat. Biotechnol. 2008, 26:431-442.
44. Takemura Y., Kikuchi S., Inaba Y. Epidemiologic study of the relationship between schistosomiasis due to Schistosoma japonicum and liver cancer/cirrhosis. Am. J. Trop. Med. Hyg. 1998, 59:551-556.
45. Tanaka K., Namba T., Arai Y., Fujimoto M., Adachi H., Sobue G., Takeuchi K., Nakai A., Mizushima T. Genetic evidence for a protective role for heat shock factor 1 and heat shock protein 70 against colitis. J. Biol. Chem. 2007, 282:23240-23252.
46. Tomanovic N.R., Boricic I.V., Brasanac D.C., Stojsic Z.M., Delic D.S., Brmbolic B.J. Activated liver stellate cells in chronic viral C hepatitis: histopathological and immunohistochemical study. J. Gastrointestin. Liver Dis. 2009, 18:163-167.
47. Ueno T., Sata M., Sakata R., Torimura T., Sakamoto M., Sugawara H., Tanikawa K. Hepatic stellate cells and intralobular innervation in human liver cirrhosis. Hum. Pathol. 1997, 28:953-959.
48. Wang Z., Li L. Adenovirus-mediated RNA interference against collagen-specific molecular chaperone 47-KD a heat shock protein suppresses scar formation on mouse wounds. Cell Biol. Int. 2008, 32:483-493.
49. WHO SCHISTOSOMIASIS progress report 2001-2011 Strategic Plan 2012-2020 2012, World Health Organization, Geneva, Switzerland.