Skip to main content
Log in

Enhanced expression of transforming growth factor-β1 in inflammatory cells and secretory granules in Paneth cells in the small intestine of mice infected with Toxocara canis

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The small intestine is the initial organ which Toxocara canis larvae invade. Information on intestinal pathological changes associated with transforming growth factor-β1 (TGF-β1) and secretory granules (SG) in Paneth cells (PCs) caused by T. canis is unclear. Mice orally inoculated with 250 T. canis infective eggs were evaluated by pathological and immunohistochemical assessments with a 294-day investigation. Pathologically, the inflammatory reactions with or without trapped larvae in the submucosa were observed only within the first 28 days post-infection (DPI), with inflammatory injury ranging from severe during 2 DPI to mild between 7 and 28 DPI. The crypts of Leiberkuhn were major larval penetration sites. Enhanced expression of SG in PCs appeared earlier than those of TGF-β1 in infiltrating cells. The significance of both effectors might be related to the host’s defense against larval invasion in the intestinal phase of toxocaral infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–D
Fig. 2A–D
Fig. 3A–D

Similar content being viewed by others

References

  • Abo-Shehada MN, Herbert IV (1984) The migration of larval Toxocara canis in mice. I. Migration through the intestine in primary infections. Vet Parasitol 17:65–73

    Article  CAS  PubMed  Google Scholar 

  • Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ (2000) Secretion of microbial α-defesins by intestinal Paneth cells in response to bacteria. Nat Immunol 1:113–118

    Article  CAS  PubMed  Google Scholar 

  • Bevins CL, Martin-Porter E, Ganz T (1999) Defensins and innate host defense of the gastrointestinal tract. Gut 45:911–915

    CAS  PubMed  Google Scholar 

  • Blobe GC, Schiemann WP, Lodish HF (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342:1350–1358

    Article  CAS  PubMed  Google Scholar 

  • Bowman DD, Mika-Grieve M, Grieve RB (1987) Circulating excretory-secretory antigen levels and specific antibody responses in mice infected with Toxocara canis. Am J Trop Med Hyg 36:75–82

    CAS  PubMed  Google Scholar 

  • Cuellar C, Fenoy S, del-Aguila C, Guillen L (2001) Isotype-specific immune responses in murine experimental toxocariasis. Mem Inst Oswaldo Cruz 96:549–553

    CAS  PubMed  Google Scholar 

  • Epe C, Stabel T, Schnieder T, Stoye M (1994) The behavior and pathogenicity of Toxocara canis larvae in mice of different strains. Parasitol Res 80:691–695

    CAS  PubMed  Google Scholar 

  • Fan CK, Su KE, Chung WC, Tsai YJ, Chang MH, Lu JL, Chao PH (1998) A parasitological survey among stray dogs in Taipei City with hematological findings (in Chinese, with English abstract). J Chin Soc Vet Sci 24:288–294

    Google Scholar 

  • Fan CK, Lin YH, Du WY, Su KE (2003) Infectivity and pathogenicity of 14-month-cultured embryonated eggs of Toxocara canis in mice. Vet Parasitol 113:145–155

    Article  PubMed  Google Scholar 

  • Gomez-Escobar N, Lewis E, Maizels RM (1998) A novel member of the transforming growth factor-beta (TGF-beta) superfamily from the filarial nematodes Brugia malayi and B. pahangi. Exp Parasitol 88:200–209

    Article  CAS  PubMed  Google Scholar 

  • Kamal M, Wakelin D, Ouellette AJ, Smith A, Podolsky DK, Mahida YR (2001) Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clin Exp Immunol 126:117–125

    Article  CAS  PubMed  Google Scholar 

  • Kerr-Muir MG (1994) Toxocara canis and human health. Br Med J 309:5-6

    CAS  Google Scholar 

  • Lawrance IC, Maxwell L, Doe W (2001) Inflammation location, but not type, determines the increase in TGF-beta1 and IGF-1 expression and collagen deposition in IBD intestine. Inflamm Bowel Dis 7:16–26

    CAS  PubMed  Google Scholar 

  • Lewin K (1969) Histochemical observations on Paneth cells. J Anat 105:171–176

    CAS  PubMed  Google Scholar 

  • O’Lorcain P (1995) The effects of freezing on the viability of Toxocara canis and T. cati embryonated eggs. J Helminthol 69:169–171

    PubMed  Google Scholar 

  • Porter EM, Bevins CL, Ghosh D, Ganz T (2002) The multifaceted Paneth cell. Cell Mol Life Sci 59:156–170

    Article  CAS  PubMed  Google Scholar 

  • Quellette AJ, Satchell DP, Hsieh MM, Hagen SJ, Selsted ME (2000) Characterization of luminal Paneth cell α-defesins in mouse small intestine. attenuated antimicrobial activities of peptides with truncated amino termini. J Biol Chem 275:33969-33973

    Article  PubMed  Google Scholar 

  • Seno H, Sawada M, Fukuzawa H, Morita Y, Takaishi S, Hiai H, Chiba T (2001) Enhanced expression of transforming growth factor (TGF)-alpha precursor and TGF-beta1 during Paneth cell regeneration. Dig Dis Sci 6:1004–1010

    Article  Google Scholar 

  • Shull MM, Ormsby I, Kier AB, et al (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359:693–699

    Article  CAS  PubMed  Google Scholar 

  • Smith HV (1991) Immune evasion and immunopathology in Toxocara canis infection. In: Kennedy MW (ed) Parasitic nematodes: antigens, membranes and genes. CRC Press, London, pp 116–139

  • Wahl SM, McCartney-Francis N, Mergenhagen SE (1989) Inflammatory and immunomodulatory roles of TGF-beta. Immunol Today 10:258–261

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Taipei Medical University for its support of this research (grants TMU-88-Y05-A106 and TMU-90-Y05-A142). We thank Mr. D.J. Kao and Mr. C.W. Liao for expert technical assistance; the Taipei Municipal Institute for Animal Health is acknowledged for providing experimental stray dogs from which adult Toxocara canis worms were collected. Also, Mr. D. Chamberlin is acknowledged for his critical revision of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chia-Kwung Fan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fan, CK., Hung, CC., Lin, YH. et al. Enhanced expression of transforming growth factor-β1 in inflammatory cells and secretory granules in Paneth cells in the small intestine of mice infected with Toxocara canis. Parasitol Res 94, 397–404 (2004). https://doi.org/10.1007/s00436-004-1233-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1233-2

Keywords

Navigation