Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T02:57:27.107Z Has data issue: false hasContentIssue false

Neuronal plasticity of the enteric nervous system is correlated with chagasic megacolon development

Published online by Cambridge University Press:  29 July 2008

A. B. M. da SILVEIRA*
Affiliation:
Research Center René Rachou, FIOCRUZ, Belo Horizonte, Minas Gerais, Brazil – CEP 30.190-002
M. A. R. FREITAS
Affiliation:
Department of Parasitology, ICB, Universidade Federal de Minas Gerais, Brazil – CEP 31.270-901
E. C. de OLIVEIRA
Affiliation:
Department of Surgery, Medical School, Universidade Federal de Goiás, Brazil – CEP 74.001-970
S. G. NETO
Affiliation:
Department of Surgery, Medical School, Universidade Federal de Goiás, Brazil – CEP 74.001-970
A. O. LUQUETTI
Affiliation:
Chagas' Disease Research Laboratory, IPTSP, Universidade Federal de Goiás, Brazil – CEP 74.001-970
J. B. FURNESS
Affiliation:
Department of Anatomy & Cell Biology, University of Melbourne, Victoria, Australia – Postal Code 3010
R. CORREA-OLIVEIRA
Affiliation:
Research Center René Rachou, FIOCRUZ, Belo Horizonte, Minas Gerais, Brazil – CEP 30.190-002
D. d'AVILA REIS
Affiliation:
Department of Morphology, ICB, Universidade Federal de Minas Gerais, Brazil – CEP 31.270-901
*
*Corresponding author: Research Center René Rachou, FIOCRUZ, Av. Augusto de Lima, 1715 Barro Preto, Belo Horizonte, Minas Gerais – Brasil. E-mail: alec@cpqrr.fiocruz.br

Summary

Chagas' disease is one of the few functional gastrointestinal disorders for which a causative agent has been identified. However, some pathological aspects of the chagasic megasyndromes are still incompletely understood. Chagasic megacolon is characterized by an inflammatory process, organ dilatation and neuronal reduction in both plexuses of the enteric nervous system (ENS). Although some studies on the ENS in Chagas' disease have been performed, the process of neuronal destruction and neuronal regeneration still remains unclear. Our hypothesis is that the regeneration process of the ENS may be involved with the mechanisms that prevent or retard organ dilatation and chagasic megacolon development. For that reason, we evaluated the neuronal regeneration with the marker GAP-43 in the colon's neuronal plexuses from chagasic patients with megacolon, and from non-infected individuals. Visual examination and quantitative analysis revealed an increased neuronal regeneration process in the dilated portion from chagasic patients when compared with the non-dilated portion and with non-infected individuals. We believe that this increased regeneration can be interpreted as an accentuated neuronal plasticity that may be a response of the ENS to avoid megacolon propagation to the entire organ and maintain the colon functional innervation.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adad, S. J., Andrade, D. C., Lopes, E. R. and Chapadeiro, E. (1991). Pathological anatomy of chagasic megaesophagus. Revista do Instituto de Medicina Tropical de São Paulo 33, 443450.CrossRefGoogle ScholarPubMed
Adad, S. J., Cancado, C. G., Etchebehere, R. M., Teixeira, V. P., Gomes, U. A., Chapadeiro, E. and Lopes, E. R. (2001). Neuron count reevaluation in the myenteric plexus of chagasic megacolon after morphometric neuron analysis. Virchows Arch 438, 254258.CrossRefGoogle ScholarPubMed
Anderson, K. D., Merhege, M. A., Morin, M., Bolognani, F. and Perrone-Bizzozero, N. I. (2003). Increased expression and localization of the RNA-binding protein HuD and GAP-43 mRNA to cytoplasmic granules in DRG neurons during nerve regeneration. Experimental Neurology 183, 100108.CrossRefGoogle ScholarPubMed
Anderson, K. D., Sengupta, J., Morin, M., Neve, R. L., Valenzuela, C. F. and Perrone-Bizzozero, N. I. (2001). Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Experimental Neurology 168, 250258.CrossRefGoogle ScholarPubMed
Basi, G. S., Jacobson, R. D., Virag, I., Schilling, J. and Skene, J. H. (1987). Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth. Cell 49, 785791.CrossRefGoogle ScholarPubMed
Corbett, C. E., Ribeiro, U. Jr., Prianti, M. G., Habr-Gama, A., Okumura, M. and Gama-Rodrigues, J. (2001). Cell-mediated immune response in megacolon from patients with chronic Chagas' disease. Diseases of the Colon and Rectum 44, 993998.CrossRefGoogle ScholarPubMed
Da Silveira, A. B., Arantes, R. M., Vago, A. R., Lemos, E. M., Adad, S. J., Correa-Oliveira, R. and D'avila Reis, D. (2005). Comparative study of the presence of Trypanosoma cruzi kDNA, inflammation and denervation in chagasic patients with and without megaesophagus. Parasitology 131, 627634.CrossRefGoogle ScholarPubMed
Da Silveira, A. B., D'avila Reis, D., De Oliveira, E. C., Neto, S. G., Luquetti, A. O., Poole, D., Correa-Oliveira, R. and Furness, J. B. (2007 a). Neurochemical coding of the enteric nervous system in chagasic patients with megacolon. Digestive Diseases and Sciences 52, 28772883.CrossRefGoogle ScholarPubMed
Da Silveira, A. B., Freitas, M. A. R., De Oliveira, E. C., Neto, S. G., Luquetti, A. O., Furness, J. B., Correa-Oliveira, R. and D'avila Reis, D. (2008). Substance P and NK1 receptor expression in the enteric nervous system is related to the development of chagasic megacolon. The Royal Society of Tropical Medicine and Hygiene. doi:10.1016/j.trstmh.2008.04.043CrossRefGoogle Scholar
Da Silveira, A. B., Lemos, E. M., Adad, S. J., Correa-Oliveira, R., Furness, J. B. and D'avila Reis, D. (2007 b). Megacolon in Chagas disease: a study of inflammatory cells, enteric nerves, and glial cells. Human Pathology 38, 12561264.CrossRefGoogle ScholarPubMed
Dias, J. C. (2007). Globalization, inequity and Chagas disease. Cadernos de Saide Pública 23 Suppl, S1322.CrossRefGoogle ScholarPubMed
Dias, J. C., Silveira, A. C. and Schofield, C. J. (2002). The impact of Chagas disease control in Latin America: a review. Memórias do Instituto Oswaldo Cruz 97, 603612.CrossRefGoogle ScholarPubMed
Furness, J. B. and Costa, M. (1980). Types of nerves in the enteric nervous system. Neuroscience 5, 120.CrossRefGoogle ScholarPubMed
Jones, E. M., Colley, D. G., Tostes, S., Lopes, E. R., Vnencak-Jones, C. L. and Mccurley, T. L. (1993). Amplification of a Trypanosoma cruzi DNA sequence from inflammatory lesions in human chagasic cardiomyopathy. American Journal of Tropical Medicine and Hygiene 48, 348357.CrossRefGoogle ScholarPubMed
Koberle, F. (1968). Chagas' disease and Chagas' syndromes: the pathology of American trypanosomiasis. Advances in Parasitology 6, 63116.CrossRefGoogle ScholarPubMed
McPhail, L. T., Fernandes, K. J., Chan, C. C., Vanderluit, J. L. and Tetzlaff, W. (2004). Axonal reinjury reveals the survival and re-expression of regeneration-associated genes in chronically axotomized adult mouse motoneurons. Experimental Neurology 188, 331340.CrossRefGoogle ScholarPubMed
Oliveira, E. C., Lette, M. S., Ostermayer, A. L., Almeida, A. C. and Moreira, H. (1997). Chagasic megacolon associated with colon cancer. American Journal of Tropical Medicine and Hygiene 56, 596598.CrossRefGoogle ScholarPubMed
Reinshagen, M., Von Boyen, G., Adler, G. and Steinkamp, M. (2002). Role of neurotrophins in inflammation of the gut. Current Opinion in Investigational Drugs 3, 565568.Google ScholarPubMed
Skene, J. H., Jacobson, R. D., Snipes, G. J., Mcguire, C. B., Norden, J. J. and Freeman, J. A. (1986). A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233, 783786.CrossRefGoogle Scholar
Tafuri, W. L. (1970). Pathogenesis of lesions of the autonomic nervous system of the mouse in experimental acute Chagas' disease. Light and electron microscope studies. American Journal of Tropical Medicine and Hygiene 19, 405417.CrossRefGoogle ScholarPubMed
Tafuri, W. L. (1971). Light and electron microscope studies of the autonomic nervous system in experimental and human American trypanosomiasis. Virchows Archiv 54, 136149.CrossRefGoogle Scholar
Theodorou, V., Fioramonti, J. and Bueno, L. (1996). Integrative neuroimmunology of the digestive tract. Veterinary Research 27, 427442.Google ScholarPubMed
Vago, A. R., Macedo, A. M., Adad, S. J., Reis, D. D. and Correa-Oliveira, R. (1996). PCR detection of Trypanosoma cruzi DNA in oesophageal tissues of patients with chronic digestive Chagas' disease. Lancet 348, 891892.CrossRefGoogle ScholarPubMed
Vento, P. and Soinila, S. (1999). Quantitative comparison of growth-associated protein GAP-43, neuron-specific enolase, and protein gene product 9.5 as neuronal markers in mature human intestine. The Journal of Histochemistry and Cytochemistry 47, 14051415.CrossRefGoogle ScholarPubMed
Von Boyen, G. B., Steinkamp, M., Reinshagen, M., Schafer, K. H., Adler, G. and Kirsch, J. (2006). Nerve growth factor secretion in cultured enteric glia cells is modulated by proinflammatory cytokines. Journal of Neuroendocrinology 18, 820825.CrossRefGoogle ScholarPubMed
Wakamatsu, Y. and Weston, J. A. (1997). Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124, 34493460.CrossRefGoogle ScholarPubMed
Yamada, M., Terayama, R., Bando, Y., Kasai, S. and Yoshida, S. (2006). Regeneration of the abdominal postganglionic sympathetic system. Neuroscience Research 54, 261268.CrossRefGoogle ScholarPubMed