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Increased Intestinal Epithelial Cell Turnover and Intestinal Motility in Gymnophalloides seoi-Infected C57BL/6 Mice

  • Lee, Sang Hyub (Department of Internal Medicine and Liver research Institute, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Jung, Bong-Kwang (Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine) ;
  • Park, Jae-Hwan (Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine) ;
  • Shin, Eun-Hee (Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine) ;
  • Chai, Jong-Yil (Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine)
  • Received : 2014.01.29
  • Accepted : 2014.04.16
  • Published : 2014.06.30

Abstract

The changing patterns of goblet cell hyperplasia, intestinal epithelial cell turnover, and intestinal motility were studied in ICR and C57BL/6 mice infected with Gymnophalloides seoi (Digenea: Gymnophallidae). Whereas ICR mice retained G. seoi worms until day 7 post-infection (PI), C57BL/6 mice showed a rapid worm expulsion within day 3 PI. Immunosuppression with Depo-Medrol significantly delayed the worm expulsion in C57BL/6 mice. Goblet cell counts were increased in both strains of mice, peaking at day 1 PI in C57BL/6 mice and slowly increasing until day 7 PI in ICR mice. In C57BL/6 mice infected with G. seoi, newly proliferating intestinal epithelial cells were remarkably increased in the crypt, and the increase was the highest at day 1 PI. However, in ICR mice, newly proliferating intestinal epithelial cells increased slowly from day 1 to day 7 PI. Intestinal motility was increased in G. seoi-infected mice, and its chronological pattern was highly correlated with the worm load in both strains of mice. Meanwhile, immunosuppression of C57BL/6 mice abrogated the goblet cell proliferation, reduced the epithelial cell proliferation, and suppressed the intestinal motility. Goblet cell hyperplasia, increased intestinal epithelial cell turnover, and increased intestinal motility should be important mucosal defense mechanisms in G. seoi-infected C57BL/6 mice.

Keywords

References

  1. Lee SH, Chai JY, Hong ST. Gymnophalloides seoi n. sp. (Digenea: Gymnophallidae), the first report of human infection by a gymnophallid. J Parasitol 1993; 79: 677-680. https://doi.org/10.2307/3283602
  2. Chai JY, Choi MH, Yu JR, Lee SH. Gymnophalloides seoi: a new human intestinal trematode. Trends Parasitol 2003; 19: 109-112. https://doi.org/10.1016/S1471-4922(02)00068-5
  3. Lee SH, Chai JY, Lee HJ, Hong ST, Yu JR, Sohn WM, Kho WG, Choi MH, Lim YJ. High prevalence of Gymnophalloides seoi infection in a village on a southwestern island of the Republic of Korea. Am J Trop Med Hyg 1994; 51: 281-285. https://doi.org/10.4269/ajtmh.1994.51.281
  4. Chai JY, Park JH, Han ET, Shin EH, Kim JL, Hong KS, Rim HJ, Lee SH. A nationwide survey of the prevalence of human Gymnophalloides seoi infection on western and southern coastal islands in the Republic of Korea. Korean J Parasitol 2001; 39: 23-30. https://doi.org/10.3347/kjp.2001.39.1.23
  5. Guk SM, Park JH, Shin EH, Kim JL, Lin A, Chai JY. Prevalence of Gymnophalloides seoi infection in coastal villages of Haenam-gun and Yeongam-gun, Republic of Korea. Korean J Parasitol 2006; 44: 1-5. https://doi.org/10.3347/kjp.2006.44.1.1
  6. Lee SH, Chai JY. A review of Gymnophalloides seoi (Digenea: Gymnophallidae) and human infections in the Republic of Korea. Korean J Parasitol 2001; 39: 85-118. https://doi.org/10.3347/kjp.2001.39.2.85
  7. Forman RA, deSchoolmeester ML, Hurst RJM, Wright SH, Pemberton AD, Else KJ. The goblet cell is the cellular source of the anti-microbial angiotensin 4 in the large intestine post Trichuris muris infection. PLoS One 2012; 7: e42248. https://doi.org/10.1371/journal.pone.0042248
  8. Hasnain SZ, Gallagher AL, Grencis RK, Thornton DJ. A new role for mucins in immunity: insights from gastrointestinal nematodes. Int J Biochem Cell Biol 2012; 45: 367-374.
  9. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 2005; 308, 1463-1465. https://doi.org/10.1126/science.1108661
  10. Klementovicz JE, Travis MA, Grencis RK. Trichuris muris: a model of gastrointestinal parasitic infection. Sem Immunopathol 2012; 34: 815-828. https://doi.org/10.1007/s00281-012-0348-2
  11. Akiho H, Blennerhassett P, Deng Y, Collins SM. Role of IL-4, IL- 13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 2002; 282: 226-232. https://doi.org/10.1152/ajpgi.2002.282.2.G226
  12. Zhao A, Mcdermott J, Urban JF Jr, Gause W, Madden KB, Yeung KA , Morris SC, Finkelman FD, Shea-Donohue T. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J Immunol 2003; 171, 948-954. https://doi.org/10.4049/jimmunol.171.2.948
  13. Finkelman FD, Shea-donohue T, Morris SC, Gilea L, Strait R, Madden KB, Schope L, Urban JF, JR. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol Rev 2004; 201: 139-155. https://doi.org/10.1111/j.0105-2896.2004.00192.x
  14. Fujino T, Fried B, Ichikawa H, Tada I. Rapid expulsion of the intestinal trematodes Echinostoma trivolvis and E. caproni from C3H mice by trapping with increased goblet cell mucins. Int J Parasitol 1996; 26: 319-324. https://doi.org/10.1016/0020-7519(95)00125-5
  15. Fujino T, Ichikawa H, Fukuda K, Fried B. The expulsion of Echinostoma trivolvis caused by goblet cell hyperplasia in severe combined immunodeficient (SCID) mice. Parasite 1998; 5: 219-222. https://doi.org/10.1051/parasite/1998053219
  16. Chai JY, Kim TH, Kho WG, Chung SW, Hung SW, Hong ST, Lee SH. Mucosal mast cell responses to experimental Metagonimus yokogawai infection in rats. Korean J Parasitol 1993; 31: 129-134. https://doi.org/10.3347/kjp.1993.31.2.129
  17. Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002; 51: 129-154. https://doi.org/10.1016/S1383-5769(02)00008-9
  18. Kim I, Im JA, Lee KJ, Ryang YS. Mucosal mast cell responses in the small intestine of rats infected with Echinostoma hortense. Korean J Parasitol 2000; 38: 139-143. https://doi.org/10.3347/kjp.2000.38.3.139
  19. Chai JY, Kim TK, Cho WH, Seo M, Kook J, Guk SM, LEE SH. Intestinal mastocytosis and goblet cell hyperplasia in BALB/c and C3H mice infected with Neodiplostomum seoulense. Korean J Parasitol 1998; 36: 109-119. https://doi.org/10.3347/kjp.1998.36.2.109
  20. Shin EH, Kim TH, Hong SJ, Park JH, Guk SM, Chai JY. Effects of anti-allergic drugs on intestinal mastocytosis and worm expulsion of rats infected with Neodiplostomum seoulense. Korean J Parasitol 2003; 41: 81-87. https://doi.org/10.3347/kjp.2003.41.2.81
  21. Lee SH, Park SK, Seo M, Guk SM, Choi MH, Chai JY. Susceptibility of various species of animals and strains of mice to Gymnophalloides seoi infection and the effects of immunosuppression in C3H/HeN mice. J Parasitol 1997; 83: 883-886. https://doi.org/10.2307/3284283
  22. Chai JY, Chung WJ, Hung WJ, Kook J, Seo M, Park YK, Guk SM, Choi MH, Lee SH. Growth and development of Gymnophalloides seoi in immunocompetent and immunosuppressed C3H/HeN mice. Korean J Parasitol 1999; 37: 21-26. https://doi.org/10.3347/kjp.1999.37.1.21
  23. Seo M, Guk SM, Han ET, Chai JY. Role of intestinal goblet cells in the expulsion of Gymnophalloides seoi from mice. J Parasitol 2003; 89: 1080-1082. https://doi.org/10.1645/GE-3182RN
  24. Guk SM, Lee JH, Kim HJ, Kim WH, Shin EH, Chai JY. $CD4^+$ T-cell-dependent goblet cell proliferation and expulsion of Gymnophalloides seoi from the intestine of C57BL/6 mice. J Parasitol 2009; 95: 581-590. https://doi.org/10.1645/GE-1807.1
  25. Lee JJ, Kim D, Pyo KH, Kim MK, Kim HJ, Chai JY, Shin EH. STAT6 expression and IL-13 production in association with goblet cell hyperplasia and worm expulsion of Gymnophalloides seoi from C57BL/6 mice. Korean J Parasitol 2013; 51: 589-594. https://doi.org/10.3347/kjp.2013.51.5.589
  26. Lee KD, Guk SM, Chai JY. Toll-like receptor 2 and MUC2 expression on human intestinal epithelial cells by Gymnophalloides seoi adult antigen. J Parasitol 2010; 96: 58-66. https://doi.org/10.1645/GE-2195.1
  27. Kook J, Nawa Y, Lee SH, Chai JY. Pathogenicity and lethality of a minute intestinal fluke, Neodiplostomum seoulense, to various strains of mice. J Parasitol 1998; 84: 1178-1183. https://doi.org/10.2307/3284669
  28. Brunet LR, Joseph S, Dunne DW, Fried B. Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni. Parasitology 2000; 120: 565-571. https://doi.org/10.1017/S0031182099006009
  29. Artis D, Wang ML, Keilbaugh SA, He W, Brenes M, Swain GP, Knight PA, Donaldson DD, Lazar MA, Miller HR, Schad GA, Scott P, Wu GD. RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc Natl Acad Sci U S A 2004; 101: 13596-13600. https://doi.org/10.1073/pnas.0404034101
  30. Hasnain SZ, Wang H, Ghia JE, Haq N, Deng Y, Velcich A, Grencis RK, Thornton, DJ, Khan WI. Mucin gene deficiency in miceimpairs host resistance to an enteric parasitic infection. Gastroenterology 2010; 138: 1763-1771. https://doi.org/10.1053/j.gastro.2010.01.045
  31. Potten CS. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 1998; 353: 821-830. https://doi.org/10.1098/rstb.1998.0246
  32. Sasaki S, Yoneyama H, Suzuki K, Suriki H, Aiba T, Watanabe S, Kaqauchi Y, Kawachi H, Shimizu F, Matsushima K, Asakura H, Narumi S. Blockade of CXCL10 protects mice from acute colitis and enhances crypt cell survival. Eur J Immunol 2002; 32: 3197-3205. https://doi.org/10.1002/1521-4141(200211)32:11<3197::AID-IMMU3197>3.0.CO;2-1
  33. Artis D, Potten CS, Else KJ, Finkelman FD, Grencis RK. Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma. Exp Parasitol 1999; 92: 144-153. https://doi.org/10.1006/expr.1999.4407
  34. Khan WI, Blennerhasset P, Ma C, Matthaei KI, Collins SM. Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunol 2001; 23, 39-42. https://doi.org/10.1046/j.1365-3024.2001.00353.x
  35. Khan WI, Richard M, Akiho H, Blennerhasset PA, Humphreys NE, Grencis RK, Snick JV, Collins SM. Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections. Infect Immun 2003; 71: 2430-2438. https://doi.org/10.1128/IAI.71.5.2430-2438.2003
  36. Mckenzie AN. Regulation of T helper type 2 cell immunity by interleukin-4 and interleukin-13. Pharmacol Ther 2000; 88: 143-151. https://doi.org/10.1016/S0163-7258(00)00088-7
  37. Khan WI, Vallance BA, Blennerhassett PA, Deng Y, Verdu EF, Matthaei KI, Collins SM. Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infect Immun 2001; 69: 838-844. https://doi.org/10.1128/IAI.69.2.838-844.2001
  38. Anthony RM, Rutitzky LI, Urban Jr JF, Stadecker M.J., Gause WC. Protective immune mechanisms in helminth infection. Nature Rev Med 2007; 7: 975-987.
  39. Trelis M, Sotillo J, Monteagudo C, Fried B, Marcilla A, Estaban JG, Toledo R. Echinostoma caproni (Trematoda): differential in vivo cytokine responses in high and low compatible hosts. Exp Parasitol 2011; 127: 387-397. https://doi.org/10.1016/j.exppara.2010.09.004

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