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Cryptosporidium parvum and mucosal immunity in neonatal cattle

Published online by Cambridge University Press:  28 February 2007

Carol R. Wyatt*
Affiliation:
Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA, USA
*
P.O. Box 647040, Washington State University, Pullman, WA 99164–7040, USA

Abstract

Cryptosporidium parvum is an important zoonotic protozoan pathogen that causes acute infection and self-limiting gastrointestinal disease in neonatal calves. There are currently no consistently effective antimicrobials available to control cryptosporidiosis. Therefore, immunotherapeutic and vaccination protocols offer the greatest potential for long-term control of the disease. In order to devise effective control measures, it is important to better define mucosal immunity to C. parvum in young calves. This review summarizes the information that has accumulated over the last decade which helps to define the intestinal mucosal immune system in neonatal calves, and the events that occur in the intestinal mucosa after infection by C. parvum.

Type
Research Article
Copyright
Copyright © CAB International 2000

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References

Abrahamsen, MS, Lancto, CA, Walcheck, B, Layton, W and Jutila, MA (1997). Localization of α/β and γ/δ T lymphocytes in Cryptosporidium parvum-infected tissues in naïve and immune calves. Infection and Immunity 65: 24282433.CrossRefGoogle ScholarPubMed
Adjei, AA, Jones, JT, Riggs, MW and Enriquez, FJ (1999). Evidence of thymus-independent local and systemic antibody responses to Cryptosporidium parvum infection in nude mice. Infection and Immunity 67: 39473951.CrossRefGoogle ScholarPubMed
Aguirre, SA, Mason, PH and Perryman, LE (1994). Susceptibility of major histocompatibility complex (MHC) class I-and MHC class-II deficient mice to Cryptosporidium parvum infection. Infection and Immunity 62: 697699.CrossRefGoogle ScholarPubMed
Anusz, KZ, Mason, PH, Riggs, MW and Perryman, LE (1990). Detection of Cryptosporidium parvum oocysts in bovine feces by monoclonal antibody capture enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 28: 27702774.CrossRefGoogle ScholarPubMed
Atwill, ER, Johnson, E, Klingborg, DJ, Veserat, GM, Markegard, G, Jensen, WA, Pratt, DW, Delmas, RE, George, HA, Forero, LC, Philips, RL, Barry, SJ, McDougald, NK, Gildersleeve, RR and Frost, WE (1999). Age, geographic, and temporal distribution of fecal shedding of Cryptosporidium parvum oocysts in cow–calf herds. American Journal of Veterinary Research 60: 420425.CrossRefGoogle ScholarPubMed
Barnes, DA, Bonnin, A, Huang, JX, Gousset, L, Wu, J, Gut, J, Doyle, P, Dubremetz, JF, Ward, H and Petersen, C (1998). A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion. Molecular and Biochemical Parasitology 96: 93110.CrossRefGoogle ScholarPubMed
Besser, TE (1993). Concentrations of passively acquired IgG1 antibodies in the intestinal lumen of the neonatal calf. Veterinary Immunology and Immunopathology 38: 103112.CrossRefGoogle ScholarPubMed
Besser, TE and Gay, CC (1994). The importance of colostrum to the health of the neonatal calf. Veterinary Clinics of North America: Food Animal Practice 10: 107117.Google Scholar
Bjorneby, JM, Riggs, MW and Perryman, LE (1990). Cryptosporidium parvum merozoites share neutralization-sensitive epitopes with sporozoites. Journal of Immunology 145: 298304.CrossRefGoogle ScholarPubMed
Bjorneby, JM, Hunsaker, BD, Riggs, MW and Perryman, LE (1991). Monoclonal antibody immunotherapy in nude mice persistently infected with Cryptosporidium parvum. Infection and Immunity 59: 11721176.CrossRefGoogle ScholarPubMed
Bonnin, A, Dubremetz, JF and Camerlynck, P (1991). Characterization of microneme antigens of Cryptosporidium parvum (Protozoa, Apicomplexa). Infection and Immunity 59: 17031708.CrossRefGoogle ScholarPubMed
Bonnin, A, Gut, J, Dubremetz, JF, Nelson, RG and Camerlynck, P (1995). Monoclonal antibodies identify a subset of dense granules in Cryptosporidium parvum zoites and gamonts. Journal of Eukaryotic Microbiology 42: 395401.CrossRefGoogle ScholarPubMed
Canals, A, Pasquali, P, Zarlenga, DS, Fayer, R, Almeria, S and Gasbarre, LC (1998). Local ileal cytokine responses in cattle during a primary infection with Cryptosporidium parvum. Journal of Parasitology 84: 125130.CrossRefGoogle ScholarPubMed
Chen, W, Harp, JA and Harmsen, AG (1993 a). Requirements for CD4+ cells and gamma interferon in resolution of established Cryptosporidium parvum infection in mice. Infection and Immunity 61: 39283932.CrossRefGoogle ScholarPubMed
Chen, W, Harp, JA, Harmsen, AG and Havell, EA (1993 b). Gamma interferon functions in resistance to Cryptosporidium parvum infection in severe combined immunodeficient mice. Infection and Immunity 61: 35483551.CrossRefGoogle ScholarPubMed
De Graaf, DC and Peeters, JE (1997). Specific interferon-gamma, IgA and IgM responses after experimental infection of neonatal calves with Cryptosporidium parvum. International Journal for Parasitology 27: 131134.CrossRefGoogle ScholarPubMed
De Graaf, DC, Walravens, K, Godfroid, J and Peeters, JE (1998). A Cryptosporidium parvum oocyst low molecular mass fraction evokes a CD4+ T-cell-dependent IFN-gamma response in bovine peripheral blood mononuclear cell cultures. International Journal for Parasitology 28: 18751880.CrossRefGoogle ScholarPubMed
Doyle, PS, Crabb, J and Petersen, C (1993). Anti-Cryptosporidium parvum antibodies inhibit infectivity in vitro and in vivo. Infection and Immunity 61: 40794084.CrossRefGoogle ScholarPubMed
Enriquez, FJ and Riggs, MW (1998). Role of immunoglobulin A monoclonal antibodies against P23 in controlling murine Cryptosporidium parvum infection. Infection and Immunity 66: 44694473.CrossRefGoogle ScholarPubMed
Estes, DM (1996). Differentiation of B cells in the bovine. Role of cytokines in immunoglobulin isotype expression. Veterinary Immunology and Immunopathology 54: 6167.CrossRefGoogle ScholarPubMed
Estes, DM, Closser, NM and Allen, GK (1994). IFN-γ stimulates IgG2 production from bovine B cells costimulated with anti-μ and mitogen. Cellular Immunology 154: 287295.CrossRefGoogle ScholarPubMed
Estes, DM, Hirano, A, Heussler, VT, Dobbelaere, DAE and Brown, WC (1995). Expression and biological activities of bovine interleukin 4: effects of recombinant bovine interleukin 4 on T cell proliferation and B cell differentiation and proliferation in vitro. Cellular Immunology 163: 268279.CrossRefGoogle Scholar
Fayer, R, Andrews, C, Ungar, BL and Blagburn, B (1989 a). Efficacy of hyperimmune bovine colostrum for prophylaxis of cryptosporidiosis in neonatal calves. Journal of Parasitology 75: 393397.CrossRefGoogle ScholarPubMed
Fayer, R, Perryman, LE and Riggs, MW (1989 b). Hyperimmune colostrum neutralizes Cryptosporidium sporozoites and protects mice against oocyst challenge. Journal of Parasitology 75: 151153.CrossRefGoogle ScholarPubMed
Fayer, R, Gasbarre, L, Pasquali, P, Canals, A, Almeria, S and Zarlenga, D (1998). Cryptosporidium parvum infection in bovine neonates: dynamic clinical, parasitic and immunologic patterns. International Journal for Parasitology 28: 4956.CrossRefGoogle ScholarPubMed
Harp, JA and Goff,, JP (1995). Protection of calves with a vaccine against Cryptosporidium parvum. Journal of Parasitology 81: 5457.CrossRefGoogle ScholarPubMed
Harp, JA and Goff, JP (1998). Strategies for the control of Cryptosporidium parvum infection in calves. Journal of Dairy Science 81: 289294.CrossRefGoogle ScholarPubMed
Harp, JA, Woodmansee, DB and Moon, HW (1990). Resistance of calves to Cryptosporidium parvum: effects of age and previous exposure. Infection and Immunity 58: 22372240.CrossRefGoogle ScholarPubMed
Harp, JA, Franklin, ST, Goff, JP and Nonnecke, BJ (1995). Effects of Cryptosporidium parvum infection on lymphocyte phenotype and reactivity in calves. Veterinary Immunology and Immunopathology 44: 197207.CrossRefGoogle ScholarPubMed
Harp, JA, Jardon, P, Atwill, ER, Zylstra, M, Checel, S, Goff, JP and De Simone, C (1996). Field testing of prophylactic measures against Cryptosporidium parvum infection in calves in a California dairy herd. American Journal of Veterinary Research 57: 15861588.CrossRefGoogle Scholar
Huang, DS, Lopez, MC, Wang, JY, Martinez, F and Watson, RR (1996). Alterations of the mucosal immune system due to Cryptosporidium parvum infection in normal mice. Cellular Immunology 173: 176182.CrossRefGoogle ScholarPubMed
Jenkins, MC, Fayer, R, Tilley, M and Upton, SJ (1993). Cloning and expression of a cDNA encoding epitopes shared by 15-and 60-kilodalton proteins of Cryptosporidium parvum sporozoites. Infection and Immunity 61: 23772382.CrossRefGoogle Scholar
Jenkins, MC, O'Brien, C, Trout, J, Guidry, A and Fayer, R (1999). Hyperimmune bovine colostrum specific for recombinant Cryptosporidium parvum antigen confers partial protection against cryptosporidiosis in immunosuppressed adult mice. Vaccine 17: 24532460.CrossRefGoogle ScholarPubMed
Khramtsov, NV, Tilley, M, Blunt, DS, Montelone, BA and Upton, SJ (1995). Cloning and analysis of a Cryptosporidium parvum gene encoding a protein with homology to cytoplasmic form Hsp70. Journal of Eukaryotic Microbiology 42: 416422.CrossRefGoogle ScholarPubMed
Kraehenbuhl, J-P and Neutra, MR (1992). Molecular and cellular basis of immune protection of mucosal surfaces. Physiological Reviews 72: 853879.CrossRefGoogle ScholarPubMed
Langer, RC and Riggs, MW (1996). Neutralizing monoclonal antibody protects against Cryptosporidium parvum infection by inhibiting sporozoite attachment and invasion. Journal of Eukaryotic Microbiology 43: 76S-77S.CrossRefGoogle ScholarPubMed
Langer, RC and Riggs, MW (1999). Cryptosporidium parvum apical complex glycoprotein CSL contains a sporozoite ligand for intestinal epithelial cells. Infection and Immunity 67: 52825291.CrossRefGoogle ScholarPubMed
Leitch, GJ and He, Q (1994). Arginine-derived nitric oxide reduces fecal oocyst shedding in nude mice infected with Cryptosporidium parvum. Infection and Immunity 62: 51735176.CrossRefGoogle ScholarPubMed
McDonald, V and Bancroft, GJ (1994). Mechanisms of innate and acquired resistance to Cryptosporidium parvum infection in SCID mice. Parasite Immunology 16: 315320.CrossRefGoogle ScholarPubMed
McIntyre, TM and Strober, W (1999). Gut-associated lymphoid tissue: regulation of IgA B-cell development. In: Ogra, PL, Mestecky, J, Lamm, ME, Strober, W, Bienenstock, J and McGhee, JR (eds), Mucosal immunity. 2nd ed. San Diego: Academic Press. pp. 319356.Google Scholar
Mead, JR, Humphreys, RC, Sammons, DW and Sterling, CR (1990). Identification of isolate-specific sporozoite proteins of Cryptosporidium parvum by two-dimensional gel electrophoresis. Infection and Immunity 58: 20712075.CrossRefGoogle ScholarPubMed
Mosier, DA, Kuhls, TL, Simons, KR and Oberst, RD (1992). Bovine humoral immune response to Cryptosporidium parvum. Journal of Clinical Microbiology 30: 32773279.CrossRefGoogle ScholarPubMed
Pasquali, P, Fayer, R, Almeria, S, Trout, J, Polidori, GA and Gasbarre, LC (1997). Lymphocyte dynamic patterns in cattle during a primary infection with Cryptosporidium parvum. Journal of Parasitology 83: 247250.CrossRefGoogle ScholarPubMed
Peeters, JE, Villacorta, I, Vanopdenbosch, E, Vandergheynst, D, Naciri, M, Ares-Mazas, E and Yvore, P (1992). Cryptosporidium parvum in calves: kinetics and immunoblot analysis of specific serum and local antibody responses (immunoglobulin A [IgA], IgG, and IgM). after natural and experimental infections. Infection and Immunity 60: 23092316.CrossRefGoogle ScholarPubMed
Peng, MM, Xiao, L, Freeman, AR, Arrowood, MJ, Escalante, AA, Weltman, AC, Ong, CSL, MacKenzie, WR, Lal, AA and Beard, CB (1997). Genetic polymorphism among Cryptosporidium parvum isolates: evidence for two distinct human transmission cycles. Emerging Infectious Diseases 3: 567573.CrossRefGoogle ScholarPubMed
Perryman, LE and Bjorneby, JM (1991). Immunotherapy of cryptosporidiosis in immunodeficient animal models. Journal of Protozoology 38: 98S100S.Google ScholarPubMed
Perryman, LE, Riggs, MW, Mason, PH and Fayer, R (1990). Kinetics of Cryptosporidium parvum sporozoite neutralization by monoclonal antibodies, immune bovine serum, and immune bovine colostrum. Infection and Immunity 58: 257259.CrossRefGoogle ScholarPubMed
Perryman, LE, Mason, PH and Chrisp, CE (1994). Effect of spleen cell populations in resolution of Cryptosporidium parvum infection in SCID mice. Infection and Immunity 62: 14741477.CrossRefGoogle ScholarPubMed
Perryman, LE, Jasmer, DP, Riggs, MW, Bohnet, SG, McGuire, TC and Arrowood, MJ (1996). A cloned gene of Cryptosporidium parvum encodes neutralization-sensitive epitopes. Molecular and Biochemical Parasitology 80: 137147.CrossRefGoogle ScholarPubMed
Perryman, LE, Kapil, SJ, Jones, ML and Hunt, EL (1999). Protection of calves against cryptosporidiosis with immune bovine colostrum induced by a Cryptosporidium parvum recombinant protein. Vaccine 17: 21422149.CrossRefGoogle ScholarPubMed
Petersen, C, Gut, J, Doyle, PS, Crabb, JH, Nelson, RG and Leech, JH (1992 a). Characterization of a >900, 000-MrCryptosporidium parvum sporozoite glycoprotein recognized by protective hyperimmune bovine colostral immunoglobulin. Infection and Immunity 60: 51325138.CrossRefGoogle ScholarPubMed
Petersen, C, Gut, J, Leech, JH and Nelson, RG (1992 b). Identification and initial characterization of five Cryptosporidium parvum sporozoite antigen genes. Infection and Immunity 60: 23432348.CrossRefGoogle ScholarPubMed
Riggs, MW, McGuire, TC, Mason, PH and Perryman, LE (1989). Neutralization-sensitive epitopes are exposed on the surface of infectious Cryptosporidium parvum sporozoites. Journal of Immunology 143: 13401345.CrossRefGoogle ScholarPubMed
Riggs, MW, Cama, VA, Leary, HL Jr and Sterling, CR (1994). Bovine antibody against Cryptosporidium parvum elicits a circumsporozoite precipitate-like reaction and has immunotherapeutic effect against persistent cryptosporidiosis in SCID mice. Infection and Immunity 62: 19271939.CrossRefGoogle ScholarPubMed
Riggs, MW, Stone, AL, Yount, PA, Langer, RC, Arrowood, MJ and Bentley, DL (1997). Protective monoclonal antibody defines a circumsporozoite-like glycoprotein exoantigen of Cryptosporidium parvum sporozoites and merozoites. Journal of Immunology 158: 17871795.CrossRefGoogle ScholarPubMed
Riggs, MW, McNeil, MR, Perryman, LE, Stone, AL, Scherman, MS and O'Connor, RM (1999). Cryptosporidium parvum sporozoite pellicle antigen recognized by a neutralizing monoclonal antibody is a β-mannosylated glycolipid. Infection and Immunity 67: 13171322.CrossRefGoogle ScholarPubMed
Spano, F, Putignani, L, Naitza, S, Puri, C, Wright, S and Crisanti, A (1998). Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. Molecular and Biochemical Parasitology 92: 147162.CrossRefGoogle ScholarPubMed
Taghi-Kilani, R, Sekla, L and Hayglass, KT (1990). The role of humoral immunity in Cryptosporidium spp. infection: studies with B cell-depleted mice. Journal of Immunology 145: 15711576.CrossRefGoogle ScholarPubMed
Tarazona, R, Lally, NC, Dominguez-Carmona, M and Blewett, DA (1997). Characterization of secretory IgA responses in mice infected with Cryptosporidium parvum. International Journal for Parasitology 27: 417423.CrossRefGoogle ScholarPubMed
Theodos, CM, Sullivan, KL, Griffiths, JK and Tzipori, S (1997). Profiles of healing and nonhealing Cryptosporidium parvum infection in C57BL/6 mice with functional B and T lymphocytes: the extent of gamma interferon modulation determines the outcome of infection. Infection and Immunity 65: 47614769.CrossRefGoogle Scholar
Tilley, M Jr, Fayer, R, Guidry, A, Upton, SJ and Blagburn, BL (1990). Cryptosporidium parvum (Apicomplexa: Cryptosporidiidae) oocyst and sporozoite antigens recognized by bovine colostral antibodies. Infection and Immunity 58: 29662971.CrossRefGoogle ScholarPubMed
Uhl, EW, O'Connor, RM, Perryman, LE and Riggs, MW (1992). Neutralization-sensitive epitopes are conserved among geographically diverse isolates of Cryptosporidium parvum. Infection and Immunity 60: 17031706.CrossRefGoogle ScholarPubMed
Ungar, BLP, Kao, T-C, Burris, JA and Finkelman, FD (1991). Cryptosporidium infection in an adult mouse model: independent roles for IFN-γ and CD4+ T lymphocytes in protective immunity. Journal of Immunology 147: 10141022.CrossRefGoogle Scholar
Urban, JF, Fayer, R, Chen, S-J, Gause, WC, Gately, MK and Finkelman, FD (1996). IL-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. Journal of Immunology 156: 263268.CrossRefGoogle ScholarPubMed
Waters, WR, Harp, JA and Nonnecke, BJ (1996). In vitro blastogenic responses and inferferon-γ production by intestinal intraepithelial lymphocytes of calves. Research in Veterinary Science 61: 4548.CrossRefGoogle Scholar
Whitmire, WM and Harp, JA (1991). Characterization of bovine cellular and serum antibody responses during infection by Cryptosporidium parvum. Infection and Immunity 59: 990995.CrossRefGoogle ScholarPubMed
Wyatt, CR and Perryman, LE (2000). Detection of mucosally delivered antibody to Cryptosporidium parvum p23 in infected calves. Annals of the New York Academy of Sciences. In press.CrossRefGoogle ScholarPubMed
Wyatt, CR, Brackett, EJ, Perryman, LE and Davis, WC (1996). Identification of γδ?T lymphocyte subsets that populate calf ileal mucosa after birth. Veterinary Immunology and Immunopathology 52: 91103.CrossRefGoogle Scholar
Wyatt, CR, Brackett, EJ, Perryman, LE, Rice-Ficht, AC, Brown, WC and O'Rourke, KI (1997). Activation of intestinal intra-epithelial T lymphocytes in calves infected with Cryptosporidium parvum. Infection and Immunity 65: 185190.CrossRefGoogle Scholar
Wyatt, CR, Barrett, WJ, Brackett, EJ, Davis, WC and Besser, TE (1999 a). Phenotypic comparison of ileal intraepithelial lymphocyte populations of suckling and weaned calves. Veterinary Immunology and Immunopathology 67: 213222.CrossRefGoogle ScholarPubMed
Wyatt, CR, Brackett, EJ and Barrett, WJ (1999 b). Accumulation of mucosal T lymphocytes around epithelial cells after in vitro infection with Cryptosporidium parvum. Journal of Parasitology 85: 765768.CrossRefGoogle ScholarPubMed