A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion

Molecular and Biochemical Parasitology

Volumn 96, Issue 1-2, 1998, Pages 93-110

  Barnes, Debra A ^a,e   Bonnin, Alain ^b   Huang, Jin Xing ^a   Gousset, Laurent ^a   Wu, Jie ^a   Gut, Jiri ^a   Doyle, Patricia ^a,f   Dubremetz, Jean Francois ^c   Ward, Honorine ^d   Petersen, Carolyn ^a  

^a SAN FRANCISCO GENERAL HOSPITAL   (United States)

^b HÔPITAL DU BOCAGE   (France)

^c INSERM   (France)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BAYER AG   (Germany)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cryptosporidium; GP900; Invasion; Merozoite; Sporozoite; Surface antigen

Indexed keywords

GLYCOPROTEIN; MEMBRANE ANTIGEN;

ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CRYPTOSPORIDIUM PARVUM; GENE STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SPOROZOITE;

CRYPTOSPORIDIUM PARVUM;

EID: 0032582846     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(98)00119-4     Document Type: Article

References (63)

1. [1] Petersen C. Cryptosporidiosis in patients infected with the human immunodeficiency virus. Clin Infect Dis 1992;15:903-9.
2. [2] Colford JM, Tager IB, Hirozawa AM, Lemp G, Aragon T, Petersen C. Cryptosporidiosis among patients infected with human immunodeficiency virus Factors related to symptomatic infection and survival. Am J Epi 1996;144:807-16.
3. [3] Millard PS, Gensheimer KF, Addiss DG, et al. An outbreak of Cryptosporidiosis from fresh-pressed apple cider. J Am Med Assoc 1994;272:1592-6.
4. [4] MacKenzie WR, Hoxie NJ, Proctor ME, et al. A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N Engl J Med 1994;331:161-7.
5. [5] Fayer R. Cryptosporidium and Cryptosporidiosis. Boca Raton: CRC, 1997.
6. [6] DuPont HL, Chappell CL, Sterling C, Okhuysen PC, Rose JB, Jakubowski W. The infectivity of Cryptosporidium parvum in healthy volunteers. N Eng J Med 1995;332:855-9.
7. [7] Perkins M. Rhoptry organelles of Apicomplexan parasites. Parasitol Today 1992;8:28-32.
8. [8] Potocnjak PN, Yoshida N, Nussenzweig RS, Nussenzweig V. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (PB44) protect mice against malarial infection. J Exp Med 1980;151:1504-13.
9. [9] Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells: an in vitro assay of protective antibodies. J Immunol 1984;1332:909-13.
10. [10] Schofield L, Bushell GR, Cooper JA, Saul AJ, Upcroft J, Kidson C. A rhoptry antigen of Plasmodium falciparum contains conserved and variable epitopes recognized by inhibitory monoclonal antibodies. Mol Biochem Parasitol 1986;18:183-95.
11. [11] Schwartzman JD. Inhibition of penetration-enhancing factor of Toxoplasma gondii by monoclonal antibodies specific for rhoptries. Infect Immunol 1986;55:760-4.
12. [12] Whitmire WM, Kyle JE, Speer CA, Burgess DE. Inhibition of penetration of cultured cells by Eimeria bovis sporozoites by monoclonal immunoglobulin G antibodies against the parasite surface protein P20. Infect Immunol 1988;56:2538-43.
13. [13] Holder AA. Proteins on the surface of the malaria parasite and cell invasion. Parasitology 1994; 108 (Suppl.):S5-S18.
14. [14] Zu SX, Fang GD, Fayer R, Guerrant RL. Cryptosporidiosis: pathogenesis and immunology. Parasitol Today 1992;8:24-8.
15. [15] Arrowood MJ, Mead JR, Mahrt JL, Sterling CR. Effects of immune colostrum and orally administered antisporozoite monoclonal antibodies on the outcome of Cryptosporidium parvum infections in neonatal mice. Infect Immun 1989;57:2283-8.
16. [16] Fayer R, Andrews C, Ungar BL, Blagburn B. Efficacy of hyperimmune bovine colostrum for prophylaxis of cryptosporidiosis in neonatal calves. J Parasitol 1989;75:393-7.
17. [17] Fayer R, Ferryman LE, Riggs MW. Hyperimmune bovine colostrum neutralizes Cryptosporidium sporozoites and protects mice against oocyst challenge. J Parasitol 1989;75:151-3.
18. [18] Riggs MW, McGuire TC, Mason PH, Perryman LE. Neutralization-sensitive epitopes are exposed on the surface of infectious Cryptosporidium parvum sporozoites. J Immunol 1989;143:1340-5.
19. [19] Fayer R, Guidry A, Blagburn BL. Immunotherapeutic efficacy of bovine colostral immunoglobulins from a hyperimmunized cow against cryptosporidiosis in neonatal mice. Infect Immun 1990;58:2962-5.
20. [20] Bjorneby JM, Hunsaker BD, Riggs MW, Perryman LE. Monoclonal antibody immunotherapy in nude mice persistently infected with Cryptosporidium parvum. Infect Immun 1991;59:1172-6.
21. [21] Doyle PS, Crabb J, Petersen C. Anti-Cryptosporidium parvum antibodies inhibit infectivity in vitro and in vivo. Infect Immunol 1993;61:4079-84.
22. [22] Tzipori S, Roberten D, Chapman C. Remission of diarrhoea due to cryptosporidiosis in an immunodeficient child treated with hyperimmune bovine colostrum. Br Med J 1986;293:1276-7.
23. [23] Ungar BL, Ward DJ, Fayer R, Quinn CA. Cessation of Cryptosporidium-associated diarrhea in an acquired immunodeficiency syndrome patient after treatment with hyperimmune bovine colostrum. Gastroenterol 1990;98:486-9.
24. [24] Nord J, Ma P, DiJohn D, Tzipori S, Tacket CO. Treatment with bovine hyperimmune colostrum of cryptosporidial diarrhea in AIDS patients. AIDS 1990;4:581-4.
25. [25] Petersen C, Gut J, Doyle PS, Crabb JH, Nelson RG, Leech JH. Characterization of a > 900000-Mr Cryptosporidium parvum sporozoite glycoprotein recognized by protective hyperimmune bovine colostral immunoglobulin. Infect Immunol 1992;60:5132-8.
26. [26] Rehg JE, Hancock ML, Woodmansee DB. Characterization of cyclophosphamide-rat model of cryptosporidiosis. Infect Immunol 1987;55:2669-74.
27. [27] Petersen C, Nelson R, Magowan C, Wollish W, Jensen J, Leech J. The mature erythrocyte surface antigen of Plasmodium falciparum is not required for knobs or cytoadherence. Mol Biochem Parasitol 1989;36:61-6.
28. [28] Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning A Laboratory Manual, 2nd ed. New York: Cold Spring Harbor Laboratory Press, 1989:942-60.
29. [29] Petersen C, Gut J, Leech JH, Nelson RG. Identification and initial characterization of five Cryptosporidium parvum sporozoite antigen genes. Infect Immunol 1992;60:2343-8.
30. [30] Kim K, Gooze L, Petersen C, Gut J, Nelson RG. Isolation, sequence and molecular karyotype analysis of the actin gene of Cryptosporidium parvum. Mol Biochem Parasitol 1992;50:105-13.
31. [31] Gut J, Petersen C, Nelson R, Leech J. Cryptosporidium parvum: in vitro cultivation in Madin-Darby canine kidney cells. J Protozool 1991;38:72S-73.
32. [32] Gut J, Nelson RG. Cryptosporidium parvum sporozoites deposit trails of 11A5 antigen during gliding locomotion and shed 11A5 antigen during invasion of MDCK cells in vitro. J Eukaryot Microbiol 1994;41:42S-43.
33. [33] Adams JH, Hudson DE, Torii M, et al. The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 1990;63:141-53.
34. [34] Bonnin A, Dubremetz JF, Camerlynck P. Characterization of microneme antigens of Cryptosporidium parvum (Protozoa, Apicomplexa). Infect Immunol 1991;59:1703-8.
35. [35] Akiyama SK, Olden K, Yamada KM. Fibronectin and integrins in invasion and metastasis. Cancer Metastasis Rev 1995;14:173-89.
36. [36] Dominguez-Jimenez C, Sanchez-Aparicio P, Albar JP, Garcia-Pardo A. The α-4, β-1 fibronectinligands Cs-1, Hep II, and RGD induce different cellular events in B lymphoid cells. Comparison with the effects of the endothelial ligand VCAM-1. Cell Adhesion Comm 1996;4:251-67.
37. [37] Petersen C, Barnes DA, Gousset L. Cryptosporidium parvum GP900, a unique invasion protein. J Eukaryotic Microbiol 1997; Nov-Dec:S89-S90.
38. [38] Cerami C, Frevert U, Sinnis P, et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 1992;70:1021-33.
39. [39] Kim K, Bulow R, Kampmeier J, Boothroyd JC. Conformationally appropriate expression of the Toxoplasma antigen SAGl (p30) in CHO cells. Infect Immunol 1994;62:203-9.
40. [40] Su X-Z, Heatwole SK, Wertheimer SK, et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium-infected erythrocytes. Cell 1995;82:89-100.
41. [41] Baruch DI, Pasloske BL, Singh HB, et al. Cloning the P. falciparum gene encoding PfEMP1, the malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 1995;82:77-87.
42. [42] Carraway M, Tzipori S, Widmer G. A new restriction fragment length polymorphism from Cryptosporidium parvum identifies genetically different parasite populations and genotypic changes following transmission from bovine to human hosts. Infect Immunol 1997;65:3958-60.
43. [43] Steinmetz M, Frelinger JG, Fisher D, et al. Three cDNA clones encoding mouse transplantation antigens: homology to immunoglobulin genes. Cell 1981;24:125-34.
44. [44] Voorhees P, Deignan E, van Donselaar E, et al. An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J 1995;14:4961-75.
45. [45] Bernfield M, Kokenyesi R, Kato M, et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Ann Rev Cell Biol 1992;8:367-93.
46. [46] Petry F, Shirley M, Miles M McDonald V. Characterization of a Cryptosporidium parvum-specific cDNA clone encoding an oocyst protein with an repetitive octapeptide sequence motif (Unpublished, sequence in EMBL data bank).
47. [47] Nussenzweig R, Nussenzweig V. Circumsporozoite proteins of malaria parasites. Cell 1985;42:401.
48. [48] Riggs MW, Stone AL, Yount PA, Langer RC, Arrowood MJ, Bentley DL. Protective monoclonal antibody defines a circumsporozoite-like exoantigen of Cryptosporidium parvum sporozoites and merozoites. J Immunol 1997;158:1787-95.
49. [49] Van Klinken J-W, Dekker J, Buller HA, Einerhand AWC. Mucin gene structure and expression: protection vs. adhesion. Am J Physiol 1995;269:G614-27.
50. [50] Harding SE. The macrostructure of mucus glycoproteins in solution. Adv Carb Biochem 1989;47:345-81.
51. [51] Butenhof KJ, Gerken TA. Structure and dynamics of mucin-like glycopeptides. Examination of peptide chain expansion and peptide-carbohydrate interactions by stochastic dynamics simulations. Biochemistry 1993;32:2650-63.
52. [52] Gum JR, Hicks JW, Toribara NW, Siddiki B, Kim YS. Molecular cloning of human intestinal mucin (MUC2) cDNA Identification of the amino terminus and overall sequence similarity to prepro-Willebrand factor. J Biol Chem 1994;269:2440-6.
53. [53] Guyonnet-Duperat M, Audie J-P, Debailleul V, et al. Characterization of the human mucin gene MUC5AC: a consensus cysteine-rich domain for 11p15 mucin genes? Biochem J 1995;305:211-9.
54. [54] Hauser F, Hoffmann W. P-domains as shuffled cysteine rich modules in integumentary mucin C.l (FIM-C.l) from Xenopus laevis. J Biol Chem 1992;267:24620-4.
55. [55] Altschul SF, Madden TL, Schaffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nuc Acids Res 1997;25:3389-402.
56. [56] Brown JC, Golbik R, Mann K, Timpl R. Structure and stability of the triple-helical domains of human collagen XIV. Matrix Biol 1994;14:287-95.
57. [57] Jentoft N. Why are proteins O-glycosylated? Trends Biochem Sci 1990;15:291-4.
58. [58] Joe A, Hamer DH, Kelley MA, et al. Role of a Gal/Gal-NAc-specific sporozoite surface lectin in Cryptosporidium parvum-host cell interaction. J Eukaryot Microbiol 1994;41:44S.
59. [59] Lasky LA, Singer MS, Dowbenko D, et al. An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell 1992;69:927-38.
60. [60] Coulson BS, Londrigan SL, Lee DJ. Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc Nat Acad Sci USA 1997;94:5389-94.
61. [61] Dowbenko D, Watson SR, Lasky LA. Cloning of the rat homologue of mouse glyCAM 1 reveals conservation of structural domains. J Biol Chem 1993;268:14399-403.
62. [62] Ruiz RC, Rigoni VL, Gonzalez J, Yoshida N. The 30/50 kDa surface antigen of Trypanosoma cruzi metacyclic trypomastigotes, an adhesion molecule involved in host cell invasion. Parasite Immunol 1993;15:121-5.
63. [63] Ward H, Cevallos AM. Cryptosporidiium: molecular basis of host-parasite interaction. Adv Parasitol 1998;40: 157-85.