Polymeric immunoglobulin receptor in intestinal immune defense against the lumen-dwelling protozoan parasite Giardia

Journal of Immunology

Volumn 177, Issue 9, 2006, Pages 6281-6290

  Davids, Barbara J ^a   Palm, J E Daniel ^b   Housley, Michael P ^c   Smith, Jennifer R ^c   Andersen, Yolanda S ^c   Martin, Martin G ^d   Hendrickson, Barbara A ^e   Johansen, Finn Eirik ^f   Svärd, Staffan G ^b   Gillin, Frances D ^a   Eckmann, Lars ^c,g  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF OSLO   (Norway)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ENOLASE; ALPHA GIARDIN; ARGININE DEIMINASE; BETA GIARDIN; CHOLERA TOXIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; IMMUNOGLOBULIN RECEPTOR; ORNITHINE CARBAMOYLTRANSFERASE; PARASITE ANTIGEN; SECRETORY COMPONENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; DIARRHEA; ERADICATION THERAPY; EVOLUTION; GASTROINTESTINAL INFECTION; GIARDIA; GIARDIA LAMBLIA; GIARDIA MURIS; GIARDIASIS; IMMUNITY; INTESTINE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 33750309518     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.9.6281     Document Type: Article

References (70)

1. Fagarasan, S., and T. Honjo. 2003. Intestinal IgA synthesis: regulation of frontline body defences. Nat. Rev. Immunol. 3: 63-72.
2. Johansen, F. E., and P. Brandtzaeg. 2004. Transcriptional regulation of the mucosal IgA system. Trends Immunol. 25: 150-157.
3. Hendrickson, B. A., D. A. Conner, D. J. Ladd, D. Kendall, J. E. Casanova, B. Corthesy, E. E. Max, M. R. Neutra, C. E. Seidman, and J. G. Seidman. 1995. Altered hepatic transport of immunoglobulin A in mice lacking the J chain. J. Exp. Med. 182: 1905-1911.
4. Kaetzel, C. S. 2005. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol. Rev. 206: 83-99.
5. Blanch, V. J., J. F. Piskurich, and C. S. Kaetzel. 1999. Cutting edge: coordinate regulation of IFN regulatory factor-1 and the polymeric Ig receptor by proinflammatory cytokines. J. Immunol. 162: 1232-1235.
6. Schjerven, H., T. N. Tran, P. Brandtzaeg, and F. E. Johansen. 2004. De novo synthesized RelB mediates TNF-induced up-regulation of the human polymeric Ig receptor. J. Immunol. 173: 1849-1857.
7. Pal, K., C. S. Kaetzel, K. Brundage, C. A. Cunningham, and C. F. Cuff. 2005. Regulation of polymeric immunoglobulin receptor expression by reovirus. J. Gen. Virol. 86: 2347-2357.
8. Tamer, C. M., M. E. Lamm, J. K. Robinson, J. F. Piskurich, and C. S. Kaetzel. 1995. Comparative studies of transcytosis and assembly of secretory IgA in Madin-Darby canine kidney cells expressing human polymeric Ig receptor. J. Immunol. 155: 707-714.
9. Johansen, F. E., M. Pekna, I. N. Norderhaug, B. Haneberg, M. A. Hietala, P. Krajci, C. Betsholtz, and P. Brandtzaeg. 1999. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice. J. Exp. Med. 190: 915-922.
10. Shimada, S., M. Kawaguchi-Miyashita, A. Kushiro, T. Sato, M. Nanno, T. Sako, Y. Matsuoka, K. Sudo, Y. Tagawa, Y. Iwakura, et al. 1999. Generation of polymeric immunoglobulin receptor-deficient mouse with marked reduction of secretory IgA. J. Immunol. 163: 5367-5373.
11. Uren, T. K., F. E. Johansen, O. L. Wijburg, F. Koentgen, P. Brandtzaeg, and R. A. Strugnell. 2003. Role of the polymeric Ig receptor in mucosal B cell homeostasis. J. Immunol. 170: 2531-2539.
12. Yamazaki, K., S. Shimada, N. Kato-Nagaoka, H. Soga, T. Itoh, and M. Nanno. 2005. Accumulation of intestinal intraepithelial lymphocytes in association with lack of polymeric immunoglobulin receptor. Eur. J. Immunol. 35: 1211-1219.
13. Sun, K., F. E. Johansen, L. Eckmann, and D. W. Metzger. 2004. An important role for polymeric Ig receptor-mediated transport of IgA in protection against Streptococcus pneumoniae nasopharyngeal carriage. J. Immunol. 173: 4576-4581.
14. Tjamlund, A., A. Rodriguez, P. J. Cardona, E. Guirado, J. Ivanyi, M. Singh, M. Troye-Blomberg, and C. Fernandez. 2006. Polymeric IgR knockout mice are more susceptible to mycobacterial infections in the respiratory tract than wild-type mice. Int. Immunol. 18: 807-816.
15. Asahi, Y., T. Yoshikawa, I. Watanabe, T. Iwasaki, H. Hasegawa, Y. Sato, S. Shimada, M. Nanno, Y. Matsuoka, M. Ohwaki, et al. 2002. Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines. J. Immunol. 168: 2930-2938.
16. Maaser, C., M. P. Housley, M. Iimura, J. R. Smith, B. A. Vallance, B. B. Finlay, J. R. Schreiber, N. M. Varki, M. F. Kagnoff, and L. Eckmann. 2004. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72: 3315-3324.
17. Uren, T. K., O. L. Wijburg, C. Simmons, F. E. Johansen, P. Brandtzaeg, and R. A. Strugnell. 2005. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur. J. Immunol. 35: 180-188.
18. Wijburg, O. L., T. K. Uren, K. Simpfendorfer, F. E. Johansen, P. Brandtzaeg, and R. A. Strugnell. 2006. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med. 203: 21-26.
19. Lane, S., and D. Lloyd. 2002. Current trends in research into the waterborne parasite Giardia. Crit. Rev. Microbiol. 28: 123-147.
20. Leclerc, H., L. Schwartzbrod, and E. Dei-Cas. 2002. Microbial agents associated with waterborne diseases. Crit. Rev. Microbiol. 28: 371-409.
21. Eckmann, L. 2003. Mucosal defences against Giardia. Parasite Immunol. 25: 259-254.
22. Langford, T. D., M. P. Housley, M. Boes, J. Chen, M. F. Kagnoff, F. D. Gillin, and L. Eckmann. 2002. Central importance of immunoglobulin A in host defense against Giardia spp. Infect. Immun. 70: 11-18.
23. Heyworth, M. F., J. R. Carlson, and T. H. Ermak. 1987. Clearance of Giardia muris infection requires helper/inducer T lymphocytes. J. Exp. Med. 165: 1743-1748.
24. Singer, S. M., and T. E. Nash. 2000. T-cell-dependent control of acute Giardia lamblia infections in mice. Infect. Immun. 68: 170-175.
25. Hardin, J. A., A. G. Buret, M. E. Olson, M. H. Kimm, and D. G. Gall. 1997. Mast cell hyperplasia and increased macromolecular uptake in an animal model of giardiasis. J. Parasitol. 83: 908-912.
26. Li, E., P. Zhou, Z. Petrin, and S. M. Singer. 2004. Mast cell-dependent control of Giardia lamblia infections in mice. Infect. Immun. 72: 6642-6649.
27. Bienz, M., W. J. Dai, M. Welle, B. Gottstein, and N. Muller. 2003. Interleukin-6-deficient mice are highly susceptible to Giardia lamblia infection but exhibit normal intestinal immunoglobulin A responses against the parasite. Infect. Immun. 71: 1569-1573.
28. Zhou, P., E. Li, N. Zhu, J. Robertson, T. Nash, and S. M. Singer. 2003. Role of interleukin-6 in the control of acute and chronic Giardia lamblia infections in mice. Infect. Immun. 71: 1566-1568.
29. Harriman, G. R., M. Bogue, P. Rogers, M. Finegold, S. Pacheco, A. Bradley, Y. Zhang, and I. N. Mbawuike. 1999. Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other Ig isotypes. J. Immunol. 162: 2521-2529.
30. Belosevic, M., G. M. Faubert, E. Skamene, and J. D. MacLean. 1984. Susceptibility and resistance of inbred mice to Giardia muris. Infect. Immun. 44: 282-286.
31. Nash, T. E., D. A. Herrington, G. A. Losonsky, and M. M. Levine. 1987. Experimental human infections with Giardia lamblia. J. Infect. Dis. 156: 974-984.
32. Smith, P. D., F. D. Gillin, W. M. Spira, and T. E. Nash. 1982. Chronic giardiasis: studies on drug sensitivity, toxin production, and host immune response. Gastroenterology 83: 797-803.
33. Boucher, S. E., and F. D. Gillin. 1990. Excystation of in vitro-derived Giardia lamblia cysts. Infect. Immun. 58: 3516-3522.
34. Jenkins, S. L., J. Wang, M. Vazir, J. Vela, O. Sahagun, P. Gabbay, L. Hoang, R. L. Diaz, R. Aranda, and M. G. Martin. 2003. Role of passive and adaptive immunity in influencing enterocyte-specific gene expression. Am. J. Physiol. 285: G714-G725.
35. Eckmann, L., G. T. Huang, J. R. Smith, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1994. Increased transcription and coordinate stabilization of mRNAs for secreted immunoglobulin a heavy chain and κ light chain following stimulation of immunoglobulin A expressing B cells. J. Biol. Chem. 269: 33102-33108.
36. Hetsko, M. L., J. M. McCaffery, S. G. Svard, T. C. Meng, X. Que, and F. D. Gillin. 1998. Cellular and transcriptional changes during excystation of Giardia lamblia in vitro. Exp. Parasitol. 88: 172-183.
37. Palm, J. E., M. E. Weiland, W. J. Griffiths, I. Ljungstrom, and S. G. Svard. 2003: Identification of immunoreactive proteins during acute human giardiasis. J. Infect. Dis. 187: 1849-1859.
38. Tellez, A., D. Palm, M. Weiland, J. Aleman, J. Winiecka-Krusnell, E. Linder, and S. Svard. 2005. Secretory antibodies against Giardia intestinalis in lactating Nicaraguan women. Parasite Immunol. 21: 163-169.
39. De Groot, N., P. Van Kuik-Romeijn, S. H. Lee, and H. A. De Boer. 2000. Increased immunoglobulin A levels in milk by over-expressing the murine polymeric immunoglobulin receptor gene in the mammary gland epithelial cells of transgenic mice. Immunology 101: 218-224.
40. Johansen, F. E., R. Braathen, and P. Brandtzaeg. 2001. The J chain is essential for polymeric Ig receptor-mediated epithelial transport of IgA. J. Immunol. 167: 5185-5192.
41. Byrd, L. G., J. T. Conrad, and T. E. Nash. 1994. Giardia lamblia infections in adult mice. Infect. Immun. 62: 3583-3585.
42. Adam, R. D. 2001. Biology of Giardia lamblia. Clin. Microbiol. Rev. 14: 447-475.
43. Wieland, W. H., D. Orzaez, A. Lammers, H. K. Parmentier, M. W. Verstegen, and A. Schots. 2004. A functional polymeric immunoglobulin receptor in chicken (Callus gallus) indicates ancient role of secretory IgA in mucosal immunity. Biochem. J. 380: 669-676.
44. Lycke, N., L. Erlandsson, L. Ekman, K. Schon, and T. Leanderson. 1999. Lack of J chain inhibits the transport of gut IgA and abrogates the development of intestinal antitoxic protection. J. Immunol. 163: 913-919.
45. Michetti, P., M. J. Mahan, J. M. Slauch, J. J. Mekalanos, and M. R. Neutra. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60: 1786-1792.
46. Belosevic, M., G. M. Faubert, and S. Dharampaul. 1994. Antimicrobial action of antibodies against Giardia muris trophozoites. Clin. Exp. Immunol. 95: 485-489.
47. Singer, S. M., and T. E. Nash. 2000. The role of normal flora in Giardia lamblia infections in mice. J. Infect. Dis. 181: 1510-1512.
48. Sait, L., M. Galic, R. A. Strugnell, and P. H. Janssen. 2003. Secretory antibodies do not affect the composition of the bacterial microbiota in the terminal ileum of 10-week-old mice. Appl. Environ. Microbiol. 69: 2100-2109.
49. Amin, N. 1979. Giardiasis: a common cause of diarrheal disease. Postgrad. Med. 66: 151-158.
50. Lai Ping So, A., and L. Mayer. 1997. Gastrointestinal manifestations of primary immunodeficiency disorders. Semin. Gastrointest. Dis. 8: 22-32.
51. Cunningham-Rundles, C. 2001. Physiology of IgA and IgA deficiency. J. Clin. Immunol. 21: 303-309.
52. Patiroglu, T., A. Kursad, S. Kurtoglu, and H. Poyrazoglu. 2002. Growth retardation in children with IgA deficiency. J. Pediatr. Endocrinol. Metab. 15: 1035-1038.
53. Hammarstrom, L., I. Vorechovsky, and D. Webster. 2000. Selective IgA deficiency (SIgAD) and common variable immunodeficiency (CVID). Clin. Exp. Immunol. 120: 225-231.
54. Prince, H. E., G. L. Norman, and W. L. Binder. 2000. Immunoglobulin A (IgA) deficiency and alternative celiac disease-associated antibodies in sera submitted to a reference laboratory for endomysial IgA testing. Clin. Diagn. Lab. Immunol. 7: 192-196.
55. Scott, K. G., J. B. Meddings, D. R. Kirk, S. P. Lees-Miller, and A. G. Buret. 2002. Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 123: 1179-1190.
56. Schiff, J. M., M. M. Fisher, and B. J. Underdown. 1984. Receptor-mediated biliary transport of immunoglobulin A and asialoglycoprotein: sorting and missorting of ligands revealed by two radiolabeling methods. J. Cell Biol. 98: 79-89.
57. Tomana, M., J. Zikan, R. Kulhavy, J. C. Bennett, and J. Mestecky. 1993. Interactions of galactosyltransferase with serum and secretory immunoglobulins and their component chains. Mol. Immunol. 30: 277-286.
58. Kitamura, T., R. P. Garofalo, A. Kamijo, D. K. Hammond, J. A. Oka, C. R. Caflisch, M. Shenoy, A. Casola, P. H. Weigel, and R. M. Goldblum. 2000. Human intestinal epithelial cells express a novel receptor for IgA. J. Immunol. 164: 5029-5034.
59. Gardner, M. L. 1988. Gastrointestinal absorption of intact proteins. Annu. Rev. Nutr. 8: 329-350.
60. Castell, J. V., G. Friedrich, C. S. Kuhn, and G. E. Poppe. 1997. Intestinal absorption of undegraded proteins in men: presence of bromelain in plasma after oral intake. Am. J. Physiol. 273: G139-G146.
61. Nishikawa, M., S. Hasegawa, F. Yamashita, Y. Takakura, and M. Hashida. 2002. Electrical charge on protein regulates its absorption from the rat small intestine. Am. J. Physiol. 282: G711-G719.
62. Martin, M. G., S. V. Wu, and J. H. Walsh. 1997. Ontogenetic development and distribution of antibody transport and Fc receptor mRNA expression in rat intestine. Dig. Dis. Sci. 42: 1062-1069.
63. Faubert, G. 2000. Immune response to Giardia duodenalis. Clin. Microbiol. Rev. 13: 35-54, table of contents.
64. Nash, T. E. 2002. Surface antigenic variation in Giardia lamblia. Mol. Microbiol. 45: 585-590.
65. Stager, S., B. Gottstein, H. Sager, T. W. Jungi, and N. Muller. 1998. Influence of antibodies in mother's milk on antigenic variation of Giardia lamblia in the murine mother-offspring model of infection. Infect. Immun. 66: 1287-1292.
66. Schofield, P. J., M. R. Edwards, J. Matthews, and J. R. Wilson. 1992. The pathway of arginine catabolism in Giardia intestinalis. Mol. Biochem. Parasitol. 51: 29-36.
67. Knodler, L. A., E. O. Sekyere, T. S. Stewart, P. J. Schofield, and M. R. Edwards. 1998. Cloning and expression of a prokaryotic enzyme, arginine deiminase, from a primitive eukaryote Giardia intestinalis. J. Biol. Chem. 273: 4470-4477.
68. Brown, D. M., J. A. Upcroft, M. R. Edwards, and P. Upcroft. 1998. Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int. J. Parasitol. 28: 149-164.
69. Weiland, M. E., A. G. McArthur, H. G. Morrison, M. L. Sogin, and S. G. Svard. 2005. Annexin-like α giardins: a new cytoskeletal gene family in Giardia lamblia. Int. J. Parasitol. 35: 617-626.
70. Weiland, M. E., J. E. Palm, W. J. Griffiths, J. M. McCaffery, and S. G. Svard. 2003. Characterisation of β-1 giardin: an immunodominant Giardia lamblia annexin with glycosaminoglycan-binding activity. Int. J. Parasitol. 33: 1341-1351.