Abstract
Cryptosporidium parvum is a protozoan parasite that causes intestinal malabsorptive syndrome and malnutrition. Considering the importance of di-tripeptide absorption for nutritional status, we previously investigated the regulation of PepT1 transporter in the suckling rat model of acute cryptosporidiosis and showed that PepT1 protein expression and activity were not modified in the parasitized intestine. Here we used confocal microscopy performed on intestinal villi to determine the subcellular localization of PepT1 together with f-actin and parasites. For this purpose, confocal microscopy using vibratome thick sections was developed on the distal small intestine, the preferential site of parasite implantation. Results showed major heterogeneity of apical PepT1 expression among enterocytes, which did not correlate with actin staining or parasite implantation. These results underscore the importance of considering the effect of C. parvum at the cellular scale and not only in the entire epithelium.
Similar content being viewed by others
References
Buret AG, Chin AC, Skott KG (2003) Infection of human and bovine epithelial cells with Cryptosporidium andersoni induces apoptosis and disrupts tight junctional ZO-1: effects of epidermal growth factor. Int J Parasitol 33:1363–1371
Buyse M, Charrier L, Sitaraman S, Gewirtz A, Merlin D (2003) Interferon gamma increases hPepT1-mediated uptake of di-tripeptides including the bacterial tripeptide fMLP in polarized intestinal epithelia. Am J Pathol 163:1969–1977
Capet C, Kapel N, Huneau JF, Magne D, Laikuen R, Tricottet V, Benhamou Y, Tome D, Gobert JG (1999) Cryptosporidium parvum infection in suckling rats: impairment of mucosal permeability and Na+-glucose cotransport. Exp Parasitol 91:119–125
Checkley W, Gilman RH, Epstein LD, Suarez M, Diaz JF, Cabrera L, Black RE, Sterling CR (1997) Asymptomatic and symptomatic cryptosporidiosis: their acute effect in weight gain in Peruvian children. Am J Epidemiol 145:156–163
Checkley W, Epstein LD, Gilman RH, Black RE, Cabrera L, Sterling CR (1998) Effects of Cryptosporidium parvum infection in Peruvian children: growth faltering and subsequent catch-up growth. Am J Epidemiol 148:497–506
Chen XM, LaRusso NF (2000) Mechanisms of attachment and internalization of Cryptosporidium parvum to biliary and intestinal epithelial cells. Gastroenterology 118:368–379
Chen XM, Levine SA, Splinter TL, Tietz PL, Ganong AL, Jobin C, Gores GJ, Paya CW, LaRusso NF (2001) Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 120:1774–1783
Colford JM Jr, Tager IB, Hirozawa AM, Lemp GF, Aragon T, Petersen C (1996) Cryptosporidiosis among patients infected with human immunodeficiency virus: factors related to symptomatic infection and survival. Am J Epidemiol 144:807–816
Current WL, Garcia LS (1991) Cryptosporidiosis. Clin Microbiol Rev 4:325–358
Elliott DA, Clark DP (2000) Cryptosporidium parvum induces host cell actin accumulation at the host–parasite interface. Infect Immun 68:2315–2322
Farthing MJ (2000) Clinical aspects of human cryptosporidiosis. Contrib Microbiol 6:50–74
Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL (1999) Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg 61:707–713
Hang CHH, Shi JX, Sun BW, Li JS (2007) Apoptosis and functional changes of dipeptide transporter (PepT1) in the rat small intestine after traumatic brain injury. J Surg Res 137:53–60
Huang BQ, Chen XM, LaRusso NF (2004) Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: a morphologic study. J Parasitol 90:212–221
Ihara T, Tsujikawa T, Fujiyama Y, Bamba T (2000) Regulation of PepT1 peptide transporter expression in the rat small intestine under malnourished conditions. Digestion 61:59–67
Marcial MA, Madara JL (1986) Cryptosporidium: cellular localization, structural analysis of absorptive cell-parasite membrane interaction in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology 90:583–594
Maresca M, Mahfoud R, Garmy N, Fantini J (2002) The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J Nutr 132:2723–2731
Marquet P, Barbot L, Planté A, Huneau JF, Gobert JG, Kapel N (2007) Cryptosporidiosis induces a transient upregulation of the oligopeptides transporter (PepT1) activity in neonatal rats. Exp Biol Med (Maywood) 232:454–460
McCole DF, Eckmann L, Laurent F, Kagnoff MF (2000) Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infect Immun 68:1710–1713
Mele R, Gomez Morales MA, Tosini F, Pozio E (2004) Cryptosporidium parvum at different developmental stages modulates host cell apoptosis in vitro. Infect Immun 72:6061–6067
Molbak K, Andersen M, Aaby P, Hojlyng N, Jakobsen M, Sodemann M, Da Silva AP (1997) Cryptosporidium infection in infancy as a cause of malnutrition: a community study from Guinea-Bissau, West Africa. Am J Clin Nutr 65:149–152
Ogihara H, Suzuki T, Nagamachi Y, Inui K, Takata K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochem J 31:169–174
Ojcius D, Perfettini JL, Bonnin A, Laurent F (1999) Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect 1:1163–1168
Rome S, Barbot L, Windsor E, Kapel N, Tricottet V, Huneau JF, Reynes M, Gobert JG, Tome D (2002) The regionalization of PepT1, NBAT and EAAC1 transporters in the small intestine of rats are unchanged from birth to adulthood. J Nutr 132:1009–1011
Suzuki T, Fujikura K, Takata K (1996) Na(+)-dependent glucose transporter SGLT1 is localized in the apical plasma membrane upon completion of tight junction formation in MDCK cells. Histochem Cell Biol 106:529–533
Topouchian A, Huneau JF, Barbot L, Rome S, Gobert JG, Tome D, Kapel N (2003) Evidence for the absence of an intestinal adaptive mechanism to compensate for C. parvum-induced amino acid malabsorption in suckling rats. Parasitol Res 91:197–203
Topouchian A, Kapel N, Larue-Achiagiotis C, Barbot L, Tome D, Gobert JG, Huneau JF (2005) Cryptosporidium infection impairs growth and muscular protein synthesis in suckling rats. Parasitol Res 96:326–330
Vavricka SR, Musch MW, Fujiya M, Kles K, Chang L, Eloranta JJ, Kullak-Ublick GA, Drabik K, Merlin D, Chang FB (2006) Tumor necrosis factor-alpha and interferon-gamma increase PepT1 expression and activity in the human colon carcinoma cell line Caco-2/bbe and in mouse intestine. Pfugers Arch Eur J Physiol 452:71–80
Acknowledgments
We thank René Laikuen for expert technical assistance for electron microscopy experiments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marquet, P., Saubaméa, B., Snouber-Choucha, L. et al. Evidence for intestinal heterogenic expression of di-tripeptides transporter PepT1 during experimental cryptosporidiosis in neonatal rats. Parasitol Res 104, 985–991 (2009). https://doi.org/10.1007/s00436-008-1278-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-008-1278-8