Kinetics of spleen and Peyer's patch lymphocyte populations during gut parasite clearing in Cryptosporidium parvum infected suckling mice
Corresponding Author
D. Mariotte
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Delphine Mariotte, Laboratoire d’Immunologie et Immunopathologie, UPRES-EA 2128, CHU – Clemenceau, 14033 Caen Cedex, France (e-mail: [email protected]).Search for more papers by this authorE. Comby
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Search for more papers by this authorP. Brasseur
Laboratoire de Parasitologie, Faculté de Médecine et Pharmacie, Rouen, France
Search for more papers by this authorJ. J. Ballet
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Search for more papers by this authorCorresponding Author
D. Mariotte
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Delphine Mariotte, Laboratoire d’Immunologie et Immunopathologie, UPRES-EA 2128, CHU – Clemenceau, 14033 Caen Cedex, France (e-mail: [email protected]).Search for more papers by this authorE. Comby
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Search for more papers by this authorP. Brasseur
Laboratoire de Parasitologie, Faculté de Médecine et Pharmacie, Rouen, France
Search for more papers by this authorJ. J. Ballet
Laboratoire d’Immunologie et Immunopathologie, CHU-Clemenceau, Caen, France
Search for more papers by this authorSUMMARY
Data from experimental and human cryptosporidiosis have established a major role of specific immunity in the control of Cryptosporidium parvum infection. In this work, alterations in spleen and Peyer's patch (Pp) lymphocytes were investigated in the course of a spontaneously resolutive gut cryptosporidiosis in four-day-old suckling NMRI mice infected with either 4 × 105 or 30 viable oocysts. Oocysts from entire small intestines, and spleen and Pp lymphocytes were examined using flow cytometry from day 7 to day 27 post-infection. Compared to uninfected animals, a 3–5 fold increase in the numbers of spleen TCR αβ+, CD4+, CD8+, TCR γδ+ and CD45R/B220+ lymphocytes was observed on day 17 post-infection in heavily infected animals. In Pp, more than ten-fold increases were observed, except for TCR γδ+ lymphocytes. At termination of infection, i.e. on days 21–23 after ingestion of 4 × 105 oocysts, T and B lymphocytes decreased rapidly in both organs, and remained lower than in uninfected animals on days 19–23 post-infection. In mice infected with 30 oocysts, similar alterations were observed in Pp, but not in spleen. Data suggest that in normally developing mice, clearance of gut C. parvum infection is associated with an initial increase in systemic and local lymphocyte numbers, followed by their decrease to below control levels during the recovery phase.
REFERENCES
- 1 Fayer R, Morgan U & Upton SJ. Epidemiology of Cryptosporidium: transmission, detection and identification. Int J Parasitol 2000; 30: 1305–1322.
- 2 Lemoing V, Bissuel F, Costagliola D, et al. Decreased prevalence of intestinal cryptosporidiosis in HIV-infected patients concomitant to the widespread use of protease inhibitors. AIDS 1998; 12: 1395–1397.
- 3
Theodos CM.
Innate and cell-mediated immune responses to Cryptosporidium parvum.
Adv Parasitol
1998; 40: 88–119.
10.1016/S0065-308X(08)60118-9 Google Scholar
- 4 McDonald V & Bancroft GJ. Immunological control of Cryptosporidium infection. Chem Immunol 1998; 70: 103–123.
- 5 McDonald V. Host cell-mediated responses to infection with Cryptosporidium. Parasite Immunol 2000; 22: 597–604.
- 6 O'Donoghue PJ. Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 1995; 25: 139–195.
- 7 Boher Y, Perez-Schael I, Caceres-Dittmar G, et al. Enumeration of selected leukocytes in the small intestine of BALB/c mice infected with Cryptosporidium parvum. Am J Trop Med Hyg 1994; 50: 145–151.
- 8 Upton SJ & Gillock HH. Infection dynamics of Cryptosporidium parvum in ICR outbred suckling mice. Folia Parasit 1996; 43: 101–106.
- 9 Blagburn BL, Drain KL, Land TM, et al. Comparative efficacy evaluation of dicationic carbazole compounds, nitazoxanide and paromomycin against Cryptosporidium parvum infections in a neonatal mouse model. Antimicrob Agents Chemother 1998; 42: 2877–2882.
- 10 Harp JA, Akili D & Pesch BA. Changes in murine intestinal epithelium following Cryptosporidium parvum infection. J Eukaryot Microbiol 1999; 46: 64S–65S.
- 11 Lindsay DS, Woods KM, Upton SJ & Blagburn BL. Activity of decoquinate against Cryptosporidium parvum in cell cultures and neonatal mice. Vet Parasitol 2000; 89: 307–311.
- 12 Neumann NF, Gyurek LL, Gammie L, Finch GR & Belosevic M. Comparison of animal infectivity and nucleic acid staining for assessment of Cryptosporidium parvum viability in water. Appl Environ Microbiol 2000; 66: 406–412.
- 13 Korich DG, Marshall MM, Smith HV, et al. Inter-laboratory comparison of the CD-1 neonatal mouse logistic dose–response model for Cryptosporidium parvum oocysts. J Eukaryot Microbiol 2000; 47: 294–298.
- 14 Vergara-Castiblanco CA, Freire-Santos F, Oteiza-Lopez AM & Ares-Mazas ME. Viability and infectivity of two Cryptosporidium parvum bovine isolates from different geographical location. Vet Parasitol 2000; 89: 261–267.
- 15 Lacroix S, Mancassola R, Naciri M & Laurent F. Cryptosporidium parvum-specific mucosal immune response in C57BL/6 neonatal and gamma interferon-deficient mice: role of tumor necrosis factor alpha in protection. Infect Immun 2001; 69: 1635–1642.
- 16 Castro Hermida JA, Ares-Mazas ME, Nieto Reyes L, Otero Espinar F & Blanco Mendez J. Inhibition of Cryptosporidium infection in mice treated with a cyclodextrin inclusion complex with diloxanide furoate. Parasitol Res 2001; 87: 449–452.
- 17 Freire-Santos F, Gomez-Couso H, Ortega-Inarrea MR, et al. Survival of Cryptosporidium parvum oocysts recovered from experimentally contaminated oysters (Ostrea edulis) and clams (Tapes decussatus). Parasitol Res 2002; 88: 130–133.
- 18 Buraud M, Kapel N, Benhamou Y, Savel J & Gobert JG. A high-yield outbred suckling mouse model of cryptosporidiosis. Parasite 1995; 2: 81–84.
- 19 Delaunay A, Gargala G, Xunde L, Favennec L & Ballet JJ. Quantitative flow cytometric evaluation of maximal Cryptosporidium parvum oocyst infectivity in a neonate mouse model. Appl Environ Microbiol 2000; 66: 4315–4317.
- 20 Kapel N, Benhamou Y, Buraud M, Magne O, Opolon P & Gobert JG. Kinetics of mucosal ileal gamma-interferon response during cryptosporidiosis in immunocompetent neonatal mice. Parasitol Res 1996; 82: 664–667.
- 21 Yang S, Du Benson SKC & Healey MC. Infection of immunosuppressed C57BL/6N adult mice with a single oocyst of Cryptosporidium parvum. J Parasitol 2000; 86: 884–887.
- 22 Okhuysen PC, Rich SM, Chappell CL, et al. Infectivity of a Cryptosporidium parvum isolate of cervine origin for healthy adults and interferon-γ knockout mice. J Infect Dis 2002; 185: 1320–1325.
- 23 Arrowood MJ, Hurd MR & Mead JR. A new method for evaluating experimental cryptosporidial parasite loads using immunofluorecent flow cytometry. J Parasitol 1995; 81: 404–409.
- 24 Bennett JW, Gauci MR, Le Moenic S, Schaefer FW & Lindquist HDA. A comparison of enumeration techniques for Cryptosporidium parvum oocysts. J Parasitol 1999; 85: 1165–1168.
- 25 Harp JA & Sacco RE. Development of cellular immune functions in neonatal to weanling mice: relationship to Cryptosporidium parvum infection. J Parasitol 1996; 82: 245–249.
- 26 Waters WR & Harp JA. Cryptosporidium parvum infection in T-cell receptor (TCR)-α- and TCR-δ-deficient mice. Infect Immun 1996; 64: 1854–1857.
- 27 Eichelberger MC, Suresh P & Rehg JE. Protection from Cryptosporidium parvum infection by γδ T cells in mice that lack αβ T cells. Comp Med 2000; 50: 270–276.
- 28 Aguirre SA, Mason PH & Perryman LE. Susceptibility of major histocompatibility complex (MHC) class I- and MHC class II-deficient mice to Cryptosporidium parvum infection. Infect Immunity 1994; 62: 697–699.
- 29 Cosyns M, Tsirkin S, Jones M, Flavell R, Kikutani H & Hayward AR. Requirement of CD40–CD40 ligand interaction for elimination of Cryptosporidium parvum from mice. Infect Immun 1998; 66: 603–607.
- 30 You X & Mead JR. Characterization of experimental Cryptosporidium parvum infection in IFN-γ knockout mice. Parasitol 1998; 117: 525–531.
- 31 Abrahamsen MS, Lancto CA, Walcheck B, Layton W & Jutila MA. Localization of alpha/beta and gamma/delta T lymphocytes in Cryptosporidium parvum-infected tissues in naive and immune calves. Infect Immun 1997; 65: 2428–2433.
- 32 Riggs MW. Recent advances in cryptosporidiosis: the immune response. Microbes Infect 2002; 4: 1067–1080.
- 33 Topouchian A, Kapel N, Huneau JF, et al. Impairment of amino-acid absorption in suckling rats infected with Cryptosporidium parvum. Parasitol Res 2001; 87: 891–896.
- 34 Adjei AA, Jones JT, Enriquez FJ & Yamamoto S. Dietary nucleosides and nucleotides reduce Cryptosporidium parvum infection in dexamethasone immunosuppressed adult mice. Exp Parasitol 1999; 92: 199–208.
- 35 Barbot L, Topouchian A, Capet C, et al. Recherches actuelles sur les Apicomplexa Cryptosporidium parvum: étude fonctionnelle du syndrome de malabsorption intestinale. Ann Pharm Fr 2001; 59: 305–311.
- 36 Harp JA. Oral dosing of neonatal mice with sucrose reduces infection with Cryptosporidium parvum. J Parasitol 1999; 85: 952–955.
- 37 Motta I, Gissot M, Kanellopoulos JM & Ojcius DM. Absence of weight loss during Cryptosporidium infection in susceptible mice deficient in Fas-mediated apoptosis. Microbes Infect 2002; 4: 821–827.
- 38 Chen W, Chadwick V, Tie A & Harp J. Cryptosporidium parvum in intestinal mucosal biopsies from patients with inflammatory bowel disease. Am J Gastroenterol 2001; 96: 3463–3464.
- 39 Manthey MW, Ross AB & Soergel KH. Cryptosporidiosis and inflammatory bowel disease. Digest Dis Sci 1997; 42: 1580–1586.