Dysfunctions at human intestinal barrier by water-borne protozoan parasites: Lessons from cultured human fully differentiated colon cancer cell lines

Cellular Microbiology

Volumn 15, Issue 6, 2013, Pages 860-869

  Liévin Le Moal, Vanessa ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 27; INTERLEUKIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1;

BRUSH BORDER; CANCER CELL CULTURE; CELL CLONE; CELL SUBPOPULATION; COLON CANCER; CRYPTOSPORIDIUM PARVUM; ENTAMOEBA DISPAR; ENTAMOEBA HISTOLYTICA; GIARDIA LAMBLIA; HUMAN; HUMAN CELL CULTURE; INTESTINE EPITHELIUM; INTESTINE FLORA; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTOZOON; REVIEW;

CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; COLON; COLONIC NEOPLASMS; CRYPTOSPORIDIUM; ENTAMOEBA; GIARDIA; HOST-PARASITE INTERACTIONS; HUMANS; INTESTINAL MUCOSA; MICROVILLI;

CRYPTOSPORIDIUM; ENTAMOEBA; GIARDIA; PROTOZOA;

EID: 84877834425     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12126     Document Type: Review

References (92)

1. Adams, R.B., Guerrant, R.L., Zu, S., Fang, G., and Roche, J.K. (1994) Cryptosporidium parvum infection of intestinal epithelium: morphologic and functional studies in an in vitro model. J Infect Dis 169: 170-177.
2. Aji, T., Flanigan, T., Marshall, R., Kaetzel, C., and Aikawa, M. (1991) Ultrastructural study of asexual development of Cryptosporidium parvum in a human intestinal cell line. J Protozool 38: 82S-84S.
3. Alcantara Warren, C., Destura, R.V., Sevilleja, J.E., Barroso, L.F., Carvalho, H., Barrett, L.J., etal. (2008) Detection of epithelial-cell injury, and quantification of infection, in the HCT-8 organoid model of cryptosporidiosis. J Infect Dis 198: 143-149.
4. Ankarklev, J., Jerlstrom-Hultqvist, J., Ringqvist, E., Troell, K., and Svard, S.G. (2010) Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 8: 413-422.
5. Araujo, N.S., Mundim, M.J., Gomes, M.A., Amorim, R.M., Viana, J.C., Queiroz, R.P., etal. (2008) Giardia duodenalis: pathological alterations in gerbils, Meriones unguiculatus, infected with different dosages of trophozoites. Exp Parasitol 118: 449-457.
6. Augeron, C., and Laboisse, C.L. (1984) Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res 44: 3961-3969.
7. Bansal, D., Ave, P., Kerneis, S., Frileux, P., Boche, O., Baglin, A.C., etal. (2009) An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Negl Trop Dis 3: e551.
8. Barakat, F.M., McDonald, V., Foster, G.R., Tovey, M.G., and Korbel, D.S. (2009) Cryptosporidium parvum infection rapidly induces a protective innate immune response involving type I interferon. J Infect Dis 200: 1548-1555.
9. Bhat, N., Joe, A., PereiraPerrin, M., and Ward, H.D. (2007) Cryptosporidium p30, a galactose/N-acetylgalactosamine-specific lectin, mediates infection in vitro. J Biol Chem 282: 34877-34887.
10. Borowski, H., Thompson, R.C., Armstrong, T., and Clode, P.L. (2010) Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology 137: 13-26.
11. Buret, A.G., Chin, A.C., and Scott, K.G. (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.
12. Carvalho, H.M., Teel, L.D., Goping, G., and O'Brien, A.D. (2005) A three-dimensional tissue culture model for the study of attach and efface lesion formation by enteropathogenic and enterohaemorrhagic Escherichia coli. Cell Microbiol 7: 1771-1781.
13. Castro-Hermida, J.A., Gonzalez-Losada, Y.A., and Ares-Mazas, E. (2002) Prevalence of and risk factors involved in the spread of neonatal bovine cryptosporidiosis in Galicia (NW Spain). Vet Parasitol 106: 1-10.
14. Chantret, I., Rodolosse, A., Barbat, A., Dussaulx, E., Brot-Laroche, E., Zweibaum, A., and Rousset, M. (1994) Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci 107: 213-225.
15. Choudhry, N., Bajaj-Elliott, M., and McDonald, V. (2008) The terminal sialic acid of glycoconjugates on the surface of intestinal epithelial cells activates excystation of Cryptosporidium parvum. Infect Immun 76: 3735-3741.
16. Choudhry, N., Korbel, D.S., Edwards, L.A., Bajaj-Elliott, M., and McDonald, V. (2009) Dysregulation of interferon-gamma-mediated signalling pathway in intestinal epithelial cells by Cryptosporidium parvum infection. Cell Microbiol 11: 1354-1364.
17. Costa de Beauregard, M.A., Pringault, E., Robine, S., and Louvard, D. (1995) Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J 14: 409-421.
18. Coudrier, E., Amblard, F., Zimmer, C., Roux, P., Olivo-Marin, J.C., Rigothier, M.C., and Guillen, N. (2005) Myosin II and the Gal-GalNAc lectin play a crucial role in tissue invasion by Entamoeba histolytica. Cell Microbiol 7: 19-27.
19. Dann, S.M., Wang, H.C., Gambarin, K.J., Actor, J.K., Robinson, P., Lewis, D.E., etal. (2005) Interleukin-15 activates human natural killer cells to clear the intestinal protozoan Cryptosporidium. J Infect Dis 192: 1294-1302.
20. Dawson, S.C. (2010) An insider's guide to the microtubule cytoskeleton of Giardia. Cell Microbiol 12: 588-598.
21. Del Coco, V.F., Cordoba, M.A., and Basualdo, J.A. (2008) Cryptosporidium infection in calves from a rural area of Buenos Aires, Argentina. Vet Parasitol 158: 31-35.
22. Devine, P.L., Layton, G.T., Clark, B.A., Birrell, G.W., Ward, B.G., Xing, P.X., and McKenzie, I.F. (1991) Production of MUC1 and MUC2 mucins by human tumor cell lines. Biochem Biophys Res Commun 178: 593-599.
23. Dey, I., and Chadee, K. (2008) Prostaglandin E2 produced by Entamoeba histolytica binds to EP4 receptors and stimulates interleukin-8 production in human colonic cells. Infect Immun 76: 5158-5163.
24. Dharmsathaphorn, K., McRoberts, J.A., Mandel, K.G., Tisdale, L.D., and Masui, H. (1984) A human colonic tumor cell line that maintains vectorial electrolyte transport. Am J Physiol 246: G204-G208.
25. Fantini, J., Abadie, B., Tirard, A., Remy, L., Ripert, J.P., el Battari, A., and Marvaldi, J. (1986) Spontaneous and induced dome formation by two clonal cell populations derived from a human adenocarcinoma cell line, HT29. J Cell Sci 83: 235-249.
26. Favennec, L., Egraz-Bernard, M., Comby, E., Lemeteil, D., Ballet, J.J., and Brasseur, P. (1994) Immunofluorescence detection of Cryptosporidium parvum in Caco-2 cells: a new screening method for anticryptosporidial agents. J Eukaryot Microbiol 41: 39S.
27. Fogh, J., and Trempe, G. (1975) New human tumor cell lines. In Human Tumor Cells in Vitro. Fogh, J. (ed.). New York: Plenum Publishing Corp., pp. 115-141.
28. Fogh, J., Fogh, J.M., and Orfeo, T. (1977) One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst 59: 221-226.
29. Goldston, A.M., Powell, R.R., and Temesvari, L.A. (2012) Sink or swim: lipid rafts in parasite pathogenesis. Trends Parasitol 28: 417-426.
30. Guo, A., Yin, J.G., Xiang, M., Liu, X.Y., Zhang, Y., and Chen, Q.J. (2009) Screening for relevant proteins involved in adhesion of Cryptosporidium parvum sporozoites to host cells. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27: 87-88.
31. Hansen, W.R., and Fletcher, D.A. (2008) Tonic shock induces detachment of Giardia lamblia. PLoS Negl Trop Dis 2: e169.
32. Hashim, A., Mulcahy, G., Bourke, B., and Clyne, M. (2006) Interaction of Cryptosporidium hominis and Cryptosporidium parvum with primary human and bovine intestinal cells. Infect Immun 74: 99-107.
33. He, C., Nora, G.P., Schneider, E.L., Kerr, I.D., Hansell, E., Hirata, K., etal. (2010) A novel Entamoeba histolytica cysteine proteinase, EhCP4, is key for invasive amebiasis and a therapeutic target. J Biol Chem 285: 18516-18527.
34. Horie, K., Tang, F., and Borchardt, R.T. (2003) Isolation and characterization of Caco-2 subclones expressing high levels of multidrug resistance protein efflux transporter. Pharm Res 20: 161-168.
35. Hou, Y., Mortimer, L., and Chadee, K. (2010) Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses. J Biol Chem 285: 35497-35504.
36. Huet, C., Sahuquillo-Merino, C., Coudrier, E., and Louvard, D. (1987) Absorptive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol 105: 345-357.
37. Humen, M.A., Perez, P.F., and Lievin-Le Moal, V. (2011) Lipid raft-dependent adhesion of Giardia intestinalis trophozoites to a cultured human enterocyte-like Caco-2/TC7 cell monolayer leads to cytoskeleton-dependent functional injuries. Cell Microbiol 13: 1683-1702.
38. Jakobi, V., and Petry, F. (2006) Differential expression of Cryptosporidium parvum genes encoding sporozoite surface antigens in infected HCT-8 host cells. Microbes Infect 8: 2186-2194.
39. Jarry, A., Bossard, C., Bou-Hanna, C., Masson, D., Espaze, E., Denis, M.G., and Laboisse, C.L. (2008) Mucosal IL-10 and TGF-beta play crucial roles in preventing LPS-driven, IFN-gamma-mediated epithelial damage in human colon explants. J Clin Invest 118: 1132-1142.
40. Kammanadiminti, S.J., and Chadee, K. (2006) Suppression of NF-kappaB activation by Entamoeba histolytica in intestinal epithelial cells is mediated by heat shock protein 27. J Biol Chem 281: 26112-26120.
41. Kammanadiminti, S.J., Dey, I., and Chadee, K. (2007) Induction of monocyte chemotactic protein 1 in colonic epithelial cells by Entamoeba histolytica is mediated via the phosphatidylinositol 3-kinase/p65 pathway. Infect Immun 75: 1765-1770.
42. Langer, R.C., Schaefer, D.A., and Riggs, M.W. (2001) Characterization of an intestinal epithelial cell receptor recognized by the Cryptosporidium parvum sporozoite ligand CSL. Infect Immun 69: 1661-1670.
43. Lauwaet, T., Oliveira, M.J., Callewaert, B., De Bruyne, G., Saelens, X., Ankri, S., etal. (2003) Proteolysis of enteric cell villin by Entamoeba histolytica cysteine proteinases. J Biol Chem 278: 22650-22656.
44. Leitch, G.J., and He, Q. (2012) Cryptosporidiosis - an overview. J Biomed Res 25: 1-16.
45. Lejeune, M., Moreau, F., and Chadee, K. (2011) Prostaglandin E2 produced by Entamoeba histolytica signals via EP4 receptor and alters claudin-4 to increase ion permeability of tight junctions. Am J Pathol 179: 807-818.
46. Lelievre, V., Caigneaux, E., Muller, J.M., and Falcon, J. (2000) Extracellular adenosine deprivation induces epithelial differentiation of HT29 cells: evidence for a concomitant adenosine A(1)/A(2) receptor balance regulation. Eur J Pharmacol 391: 21-29.
47. Lesuffleur, T., Kornowski, A., Augeron, C., Dussaulx, E., Barbat, A., Laboisse, C., and Zweibaum, A. (1991a) Increased growth adaptability to 5-fluorouracil and methotrexate of HT-29 sub-populations selected for their commitment to differentiation. Int J Cancer 49: 731-737.
48. Lesuffleur, T., Kornowski, A., Luccioni, C., Muleris, M., Barbat, A., Beaumatin, J., etal. (1991b) Adaptation to 5-fluorouracil of the heterogeneous human colon tumor cell line HT-29 results in the selection of cells committed to differentiation. Int J Cancer 49: 721-730.
49. Lievin-Le Moal, V., and Servin, A.L. (2006) The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin Microbiol Rev 19: 315-337.
50. Louvard, D., Kedinger, M., and Hauri, H.P. (1992) The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol 8: 157-195.
51. Magne, D., Favennec, L., Chochillon, C., Gorenflot, A., Meillet, D., Kapel, N., etal. (1991) Role of cytoskeleton and surface lectins in Giardia duodenalis attachment to Caco-2 cells. Parasitol Res 77: 659-662.
52. Maia-Brigagao, C., Morgado-Diaz, J.A., and De Souza, W. (2012) Giardia disrupts the arrangement of tight, adherens and desmosomal junction proteins of intestinal cells. Parasitol Int 61: 280-287.
53. Millership, J.J., Cai, X., and Zhu, G. (2004) Functional characterization of replication protein A2 (RPA2) from Cryptosporidium parvum. Microbiology 150: 1197-1205.
54. Mirza, H., Wu, Z., Kidwai, F., and Tan, K.S. (2011) A metronidazole-resistant isolate of Blastocystis spp. is susceptible to nitric oxide and downregulates intestinal epithelial inducible nitric oxide synthase by a novel parasite survival mechanism. Infect Immun 79: 5019-5026.
55. Mirza, H., Wu, Z., Teo, J.D., and Tan, K.S. (2012) Statin pleiotropy prevents rho kinase-mediated intestinal epithelial barrier compromise induced by Blastocystis cysteine proteases. Cell Microbiol 14: 1474-1484.
56. Mokrzycka, M., Kolasa, A., Kosierkiewicz, A., and Wiszniewska, B. (2010) Inducible nitric oxide synthase in duodenum of children with Giardia lamblia infection. Folia Histochem Cytobiol 48: 191-196.
57. Mounier, J., Prevost, M., Coudrier, E., and Guillen, N. (2000) Cytoskeleton activities during the interaction of Entamoeba histolytica with epithelial cells. Arch Med Res 31: S134-S136.
58. O'Connor, R.M., Thorpe, C.M., Cevallos, A.M., and Ward, H.D. (2002) Expression of the highly polymorphic Cryptosporidium parvum Cpgp40/15 gene in genotype I and II isolates. Mol Biochem Parasitol 119: 203-215.
59. O'Connor, R.M., Burns, P.B., Ha-Ngoc, T., Scarpato, K., Khan, W., Kang, G., and Ward, H. (2009) Polymorphic mucin antigens CpMuc4 and CpMuc5 are integral to Cryptosporidium parvum infection in vitro. Eukaryot Cell 8: 461-469.
60. O'Hara, S.P., and Lin, J.J. (2006) Accumulation of tropomyosin isoform 5 at the infection sites of host cells during Cryptosporidium invasion. Parasitol Res 99: 45-54.
61. O'Hara, S.P., Yu, J.R., and Lin, J.J. (2004) A novel Cryptosporidium parvum antigen, CP2, preferentially associates with membranous structures. Parasitol Res 92: 317-327.
62. Panaro, M.A., Cianciulli, A., Mitolo, V., Mitolo, C.I., Acquafredda, A., Brandonisio, O., and Cavallo, P. (2007) Caspase-dependent apoptosis of the HCT-8 epithelial cell line induced by the parasite Giardia intestinalis. FEMS Immunol Med Microbiol 51: 302-309.
63. Peterson, M.D., and Mooseker, M.S. (1992) Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J Cell Sci 102: 581-600.
64. Phillips, T.E., Huet, C., Bilbo, P.R., Podolsky, D.K., Louvard, D., and Neutra, M.R. (1988) Human intestinal goblet cells in monolayer culture: characterization of a mucus-secreting subclone derived from the HT29 colon adenocarcinoma cell line. Gastroenterology 94: 1390-1403.
65. Pinto, M., Appay, S., Simon-Assmann, P., Chevalier, G., Dracopoli, N., Fogh, J., and Zweibaum, A. (1982) Enterocytic differenciation of cultured human colon cancer cells by replacements of glucose by galactose in the medium. Biol Cell 44: 193-196.
66. Pinto, M., Robine-Leon, S., Appay, M.D., Kedinger, M., Triadou, N., Dussaulx, E., etal. (1983) Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 47: 323-330.
67. Pollok, R.C., Farthing, M.J., Bajaj-Elliott, M., Sanderson, I.R., and McDonald, V. (2001) Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 120: 99-107.
68. Pollok, R.C., McDonald, V., Kelly, P., and Farthing, M.J. (2003) The role of Cryptosporidium parvum-derived phospholipase in intestinal epithelial cell invasion. Parasitol Res 90: 181-186.
69. Ponce-Macotela, M., Gonzalez-Maciel, A., Reynoso-Robles, R., and Martinez-Gordillo, M.N. (2008) Goblet cells: are they an unspecific barrier against Giardia intestinalis or a gate? Parasitol Res 102: 509-513.
70. Ralston, K.S., and Petri, W.A., Jr. (2011) Tissue destruction and invasion by Entamoeba histolytica. Trends Parasitol 27: 254-263.
71. Rao, C.K., Kaetzel, C.S., and Lamm, M.E. (1987) Induction of secretory component synthesis in colonic epithelial cells. Adv Exp Med Biol 216B: 1071-1077.
72. Rigothier, M.C., Coconnier, M.H., Servin, A.L., and Gayral, P. (1991) A new in vitro model of Entamoeba histolytica adhesion, using the human colon carcinoma cell line Caco-2: scanning electron microscopic study. Infect Immun 59: 4142-4146.
73. Ringqvist, E., Palm, J.E., Skarin, H., Hehl, A.B., Weiland, M., Davids, B.J., etal. (2008) Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells. Mol Biochem Parasitol 159: 85-91.
74. Ringqvist, E., Avesson, L., Soderbom, F., and Svard, S.G. (2011) Transcriptional changes in Giardia during host-parasite interactions. Int J Parasitol 41: 277-285.
75. Rosales, M.J., Cordon, G.P., Moreno, M.S., and Sanchez, C.M. (2005) Extracellular like-gregarine stages of Cryptosporidium parvum. Acta Trop 95: 74-78.
76. Roxstrom-Lindquist, K., Ringqvist, E., Palm, D., and Svard, S. (2005) Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect Immun 73: 8204-8208.
77. Seigneur, M., Mounier, J., Prevost, M.C., and Guillen, N. (2005) A lysine- and glutamic acid-rich protein, KERP1, from Entamoeba histolytica binds to human enterocytes. Cell Microbiol 7: 569-579.
78. Stadelmann, B., Merino, M.C., Persson, L., and Svard, S.G. (2012) Arginine consumption by the intestinal parasite Giardia intestinalis reduces proliferation of intestinal epithelial cells. PLoS ONE 7: e45325.
79. Stein, B., Stover, L., Gillem, A., Winters, K., Leet, J.H., and Chauret, C. (2006) The effect of lectins on Cryptosporidium parvum oocyst in vitro attachment to host cells. J Parasitol 92: 1-9.
80. Thompson, R.C., and Monis, P. (2012) Giardia - from genome to proteome. Adv Parasitol 78: 57-95.
81. Tian, J.Q., and Quaroni, A. (1999) Dissociation between growth arrest and differentiation in Caco-2 subclone expressing high levels of sucrase. Am J Physiol 276: G1094-G1104.
82. Tompkins, W.A., Watrach, A.M., Schmale, J.D., Schultz, R.M., and Harris, J.A. (1974) Cultural and antigenic properties of newly established cell strains derived from adenocarcinomas of the human colon and rectum. J Natl Cancer Inst 52: 1101-1110.
83. Tzipori, S., and Griffiths, J.K. (1998) Natural history and biology of Cryptosporidium parvum. Adv Parasitol 40: 5-36.
84. Upton, S.J., Tilley, M., and Brillhart, D.B. (1994) Comparative development of Cryptosporidium parvum (Apicomplexa) in 11 continuous host cell lines. FEMS Microbiol Lett 118: 233-236.
85. Wanyiri, J.W., O'Connor, R., Allison, G., Kim, K., Kane, A., Qiu, J., etal. (2007) Proteolytic processing of the Cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infect Immun 75: 184-192.
86. Wanyiri, J.W., Techasintana, P., O'Connor, R.M., Blackman, M.J., Kim, K., and Ward, H.D. (2009) Role of CpSUB1, a subtilisin-like protease, in Cryptosporidium parvum infection in vitro. Eukaryot Cell 8: 470-477.
87. Widmer, G., Lee, Y., Hunt, P., Martinelli, A., Tolkoff, M., and Bodi, K. (2012) Comparative genome analysis of two Cryptosporidium parvum isolates with different host range. Infect Genet Evol 12: 1213-1221.
88. Wilson, I.W., Weedall, G.D., and Hall, N. (2012) Host-Parasite interactions in Entamoeba histolytica and Entamoeba dispar: what have we learned from their genomes? Parasite Immunol 34: 90-99.
89. Woodcook, S., Williamson, I., Hassan, I., and Mackay, M. (1991) Isolation and characterisation of clones from the Caco-2 cell line displaying increased taurocholic acid transport. J Cell Sci 98: 323-332.
90. Yu, L.C., Huang, C.Y., Kuo, W.T., Sayer, H., Turner, J.R., and Buret, A.G. (2008) SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis. Int J Parasitol 38: 923-934.
91. Zweibaum, A., Pinto, M., Chevalier, G., Dussaulx, E., Triadou, N., Lacroix, B., etal. (1985) Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J Cell Physiol 122: 21-29.
92. Zweibaum, A., Laburthe, M., Grasset, E., and Louvard, D. (1991) Use of cultured cell lines in studies of intestinal cell differentiation and function. In Handbook of Physiology, the Gastrointestinal System, Intestinal Absorption and Secretion. Schultz, S.J., Field, M., and Frizell, R.A. (eds). Bethesda: American Physiological Society, pp. 223-255.