Modeling long-term host cell-Giardia lamblia interactions in an in vitro co-culture system

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Fisher, Bridget S ^a   Estraño, Carlos E ^a   Cole, Judith A ^a  

^a University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FORMONONETIN; INTERLEUKIN 8; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL INTERACTION; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; GIARDIA LAMBLIA; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MACROPHAGE; MOUSE; NONHUMAN; PARASITE SURVIVAL; TROPHOZOITE;

ANIMALS; APOPTOSIS; CACO-2 CELLS; CASPASE 3; CHEMOKINE CXCL1; COCULTURE TECHNIQUES; EPITHELIAL CELLS; GIARDIA LAMBLIA; GIARDIASIS; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; MACROPHAGES, PERITONEAL; MICE; MODELS, BIOLOGICAL;

EID: 84891822253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081104     Document Type: Article

References (84)

1. Escobedo AA, Almirall P, Robertson LJ, Franco RMB, Havenik K, et al. (2010) Giardiasis: The ever-present threat of a neglected disease. Infectious Disorders - Drug Targets 10: 329-348.
2. Petri Jr WA (2003) Therapy of intestinal protozoa. Trends in Parasitology 19: 523-526. doi: 10.1016/j.pt.2003.09.003.
3. Ashbolt NJ (2004) Microbial contamination of drinking water and disease outcomes in developing regions. Toxicology 198: 229-238. doi: 10.1016/j.tox.2004.01.030.
4. Keystone JS, Krajden S, Warren M.R. (1978) Person-to-person transmission of Giardia lamblia in day-care nurseries. Can Med Assoc J 119: 241-242.
5. Stark D, Barratt JLN, van Hal S, Marriott D, Harkness J, et al. (2009) Clinical significance of enteric protozoa in the immunosuppressed human population. Clin Microbiol Rev 22: 634-650.
6. Savioli L, Smith H, Thompson A (2006) Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trends in Parasitology 22: 203-208. doi:10.1016/j.pt.2006.02.015.
7. Cotton JA, Beatty JK, Buret AG (2011) Host parasite interactions and pathophysiology in Giardia infections. International Journal for Parasitology 41: 925-933. doi: 10.1016/j.ijpara.2011.05.002.
8. Oberhuber G, Stolte M (1990) Giardiasis: analysis of histological changes in biopsy specimens of 80 patients. J Clin Pathol 43: 641-643.
9. Hanevik K, Hausken T, Morken MH, Strand EA, Mørch K, et al. (2007) Persisting symptoms and duodenal inflammation related to Giardia duodenalis infection. Journal of Infection 55: 524-530. doi: 10.1016/j.jinf.2007.09.004.
10. Petri WA, Haque R, Mondal D, Karim A, Molla IH, et al. (2009) Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clinical Infectious Diseases 48: 1191-1197.
11. Ward HD (2009) Intestinal protozoal parasites and diarrheal disease in Bangladesh. Clinical Infectious Diseases 48: 1198-1200.
12. Read C, Walters J, Robertson ID, Thompson RCA (2002) Correlation between genotype of Giardia duodenalis and diarrhoea. International Journal for Parasitology 32: 229-231. doi: 10.1016/S0020-7519(01)00340-X.
13. Gottstein B, Harriman GR, Conrad JT, Nash TE (1990) Antigenic variation in Giardia lamblia: cellular and humoral immune response in a mouse model. parasite Immunol 12: 659-673.
14. Rendtorff RC (1954) The experimental transmission of human intestinal protozoan parasites II. Giardia lamblia cysts given in capsules. American Journal of Epidemiology 59: 209-222.
15. Roxström-Lindquist K, Ringqvist E, Palm D, Svärd S (2005) Giardia lamblia-induced changes in gene expression in differentiated caco-2 human intestinal epithelial cells. Infect Immun 73: 8204-8208.
16. Teoh DA, Kamieniecki D, Pang G, Buret AG (2000) Giardia lamblia rearranges F-actin and a-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistanc. Journal of Parasitology 86: 800-806. doi:10.1645/0022-3395(2000)086[0800:GLRFAA]2.0.CO;2.
17. Troeger H, Epple HJ, Schneider T, Wahnschaffe U, Ullrich R, et al. (2007) Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 56: 328-335.
18. Panaro MA, Cianciulli A, Mitolo V, Mitolo CI, Acquafredda A, et al. (2007) Caspase-dependent apoptosis of the HCT-8 epithelial cell line induced by the parasite Giardia intestinalis. FEMS Immunology & Medical Microbiology 51: 302-309. 10.1111/j.1574-695X.2007.00304.x.
19. Chin AC, Teoh DA, Scott KGE, Meddings JB, Macnaughton WK, et al. (2002) Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect Immun 70: 3673-3680.
20. Belosevic M, Faubert GM (1986) Comparative studies of inflammatory responses in susceptible and resistant mice infected with Giardia muris. Clinical and experimental immunology 65: 622.
21. Owen RL, Allen CL, Stevens DP (1981) Phagocytosis of Giardia muris by macrophages in Peyer's patch epithelium in mice. Infect Immun 33: 591-601.
22. Hill DR, Pearson RD (1987) Ingestion of Giardia lamblia trophozoites by human mononuclear phagocytes. Infect Immun 55: 3155-3161.
23. Belosevic M, Daniels CW (1992) Phagocytosis of Giardia lamblia trophozoites by cytokine-activated macrophages. Clinical & Experimental Immunology 87: 304-309. 10.1111/j.1365-2249.1992.tb02992.x.
24. Mestas J, Hughes CCW (2004) Of mice and not men: differences between mouse and human immunology. The Journal of Immunology 172: 2731-2738.
25. Enkatesan P, Finch RG, Wakelin D (1997) A comparison of mucosal inflammatory responses to Giardia muris in resistant B10 and susceptible BALB/c mice. Parasite Immunology 19: 137-143.
26. Roberts-Thompson I, Mitchell GF (1978) Giardiasis in mice. I. Prolonged infections in certain mouse strains and hypothymic (nude) mice. Gastroenterol 75: 42-46.
27. Singer SM, Nash TE (2000) The role of normal flora in Giardia lamblia infections in mice. Journal of Infectious Diseases 181: 1510-1512.
28. Duell BL, Cripps AW, Schembri MA, Ulett GC (2011) Epithelial cell coculture models for studying infectious diseases: benefits and limitations. J Biomed Biotechnol 2011: Article ID 852419, 9 pages.
29. Pampaloni F, Reynaud EG, Stelzer EHK (2007) The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 8: 839-845. 10.1038/nrm2236.
30. Peterson MD, Mooseker MS (1992) Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. Journal of Cell Science 102: 581-600.
31. Mauel J, Defendi V (1971) Infection and transformation of mouse peritoneal macrophages by simian virus 40. J Exp Med 134: 335-350.
32. Davids B, Gillin F (2011) Methods for giardia culture, cryopreservation, encystation, and excystation in vitro. In: Luján H, Svärd S, editors. Giardia. Springer Vienna. pp. 381-394.
33. Lauwaet T, Andersen Y, Van de Ven L, Eckmann L, Gillin FD (2010) Rapid detachment of Giardia lamblia trophozoites as a mechanism of antimicrobial action of the isoflavone formononetin. Journal of Antimicrobial Chemotherapy 65: 531-534.
34. Versteeg HH, Nijhuis E, van den Brink GR, Evertzen M, Pynaert GN, et al. (2000) A new phosphospecific cell-based ELISA for p42/p44 mitogen-activated protein kinase (MAPK), p38 MAPK, protein kinase B and cAMP-response-element- binding protein. Biochem J 350: 717-722.
35. Felice DL, Sun J, Liu RH (2009) A modified methylene blue assay for accurate cell counting. Journal of Functional Foods 1: 109-118. doi: 10.1016/j.jff.2008.09.014.
36. Lichtenberger C, Zakeri S, Baier K, Willheim M, Holub M, et al. (1999) A novel high-purity isolation method for human peripheral blood neutrophils permitting polymerase chain reaction-based mRNA studies. Journal of Immunological Methods 227: 75-84.
37. Leonard F, Collnot EM, Lehr CM (2010) A three-dimensional coculture of enterocytes, monocytes and dendritic cells to model inflamed intestinal mucosa in vitro. Mol Pharmaceutics 7: 2103-2119. doi: 10.1021/mp1000795.
38. Kane AV, Ward HD, Keusch GT, Pereira ME (1991) In vitro encystation of Giardia lamblia: large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. J Parasitol 77: 974-981.
39. Luján HD, Mowatt MR, Byrd LG, Nash TE (1996) Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proceedings of the National Academy of Sciences 93: 7628-7633.
40. Hubert A, Cauliez B, Chedeville A, Husson A, Lavoinne A (2004) Osmotic stress, a proinflammatory signal in Caco-2 cells. Biochimie 86: 533-541.
41. Samak G, Suzuki T, Bhargava A, Rao RK (2010) c-Jun NH2-terminal kinase-2 mediates osmotic stress-induced tight junction disruption in the intestinal epithelium. American Journal of Physiology - Gastrointestinal and Liver Physiology 299: G572-G584.
42. Kayali AG, Austin DA, Webster NJ (2000) Stimulation of MAPK cascades by insulin and osmotic shock: lack of an involvement of p38 mitogen-activated protein kinase in glucose transport in 3T3-L1 adipocytes. Diabetes 49: 1783-1793.
43. Robinson MJ, Cobb MH (1997) Mitogen-activated protein kinase pathways. Current Opinion in Cell Biology 9: 180-186.
44. Müller N, von Allmen N (2005) Recent insights into the mucosal reactions associated with Giardia lamblia infections. International Journal for Parasitology 35: 1339-1347. doi: 10.1016/j.ijpara.2005.07.008.
45. Hansen WR, Fletcher DA (2008) Tonic shock induces detachment of Giardia lamblia. PLoS Negl Trop Dis 2: e169. doi:10.1371/journal.pntd.0000169.
46. Ringqvist E, Avesson L, Söderbom F, Svárd SG (2011) Transcriptional changes in Giardia during host-parasite interactions. International Journal for Parasitology 41: 277-285. doi: 10.1016/j.ijpara.2010. 09.011.
47. Ma'ayeh SY, Brook-Carter PT (2012) Representational difference analysis identifies specific genes in the interaction of Giardia duodenalis with the murine intestinal epithelial cell line, IEC-6. International Journal for Parasitology 42: 501-509.
48. Fujita J (1999) Cold shock response in mammalian cells. J Mol Microbiol Biotechnol 1: 243-255.
49. Wang Y, Zhu Y, Gao L, Yin H, Wang D, et al. (2012) Formononetin attenuates IL-1β induced apoptosis and NF-κB activation in INS-1 cells. Molecules 17: 10052-10064.
50. Auyeung KW, Ko JS (2010) Novel herbal flavonoids promote apoptosis but differentially induce cell cycle arrest in human colon cancer cell. Invest New Drugs 28: 1-13.
51. Lo YL, Wang W (2013) Formononetin potentiates epirubicin-induced apoptosis via ROS production in HeLa cells in vitro. Chemico-Biological Interactions 205: 188-197.
52. Bai F, Makino T, Kono K, Nagatsu A, Ono T, et al. (2013) Calycosin and formononetin from astragalus root enhance dimethylarginine dimethylaminohydrolase 2 and nitric oxide synthase expressions in Madin Darby Canine Kidney II cells. J Nat Med 1-8.
53. Chen J, Zeng J, Xin M, Huang W, Chen X (2011) Formononetin induces cell cycle arrest of human breast cancer cells via IGF1/PI3K/Akt pathways in vitro and in vivo. Horm Metab Res 43: 681-686.
54. Stadelmann B, Merino MC, Persson L, Svárd SG (2012) Arginine consumption by the intestinal parasite Giardia intestinalis reduces proliferation of intestinal epithelial cells. PLoS ONE 7: e45325. doi:10.1371/journal.pone.0045325.
55. Cakarova L, Marsh LM, Wilhelm J, Mayer K, Grimminger F, et al. (2009) Macrophage tumor necrosis factor-α induces epithelial expression of granulocyte-macrophage colony-stimulating factor: Impact on alveolar epithelial repair. American Journal of Respiratory and Critical Care Medicine 180: 521-532.
56. Elmore S (2007) Apoptosis: A review of programmed cell death. Toxicologic Pathology 35: 495-516.
57. Ulukan H, Muller MT, Swaan PW (2001) Downregulation of topoisomerase I in differentiating human intestinal epithelial cells. Int J Cancer 94: 200-207.
58. Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, et al. (2005) The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol 21: 1-26.
59. Basset C, Holton J, O'Mahony R, Roitt I (2003) Innate immunity and pathogen2 host interaction. Vaccine 21, Supplement 2: S12-S23. doi: 10.1016/S0264-410X(03)00195-6.
60. Bienz M, Dai WJ, Welle M, Gottstein B, Muller N (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.
61. Muñoz-Cruz S, Gómez-García A, Millán-Ibarra J, Giono-Cerezo S, Yépez-Mulia L (2010) Giardia lamblia: Interleukin 6 and tumor necrosis factor-alpha release from mast cells induced through an Ig-independent pathway. Experimental Parasitology 126: 298-303. doi: 10.1016/j.exppara.2010.06.013.
62. Bayraktar MR, Mehmet N, Durmaz R (2005) Serum cytokine changes in Turkish children infected with Giardia lamblia with and without allergy: Effect of metronidazole treatment. Acta Tropica 95: 116-122. doi: 10.1016/j.actatropica. 2005.05.006.
63. Kasper LH, Buzoni-Gatel D (2001) Ups and downs of mucosal cellular immunity against protozoan parasites. Infect Immun 69: 1-8.
64. Kanwar SS, Walia BNS, Ganguly NK, Mahajan RC (1987) The macrophages as an effector cell in Giardia lamblia infections. Med Microbiol Immunol 176: 83-88.
65. Nash TE, Herrington DA, Losonky GA, Levine MM (1987) Experimental human infections with Giardia lamblia. The Journal of Infectious Diseases 156: 974-984.
66. Kanzato H, Manabe M, Shimizu M (2001) An in vitro approach to the evaluation of the cross talk between intestinal epithelium and macrophages. Biosci Biotechnol Biochem 65: 449-451.
67. Buret AG, Mitchell K, Muench DG, Scott KG (2002) Giardia lamblia disrupts tight junctional ZO-1 and increases permeability in non-transformed human small intestinal epithelial monolayers: effects of epidermal growth factor. Parasitology 125: 11-19.
68. Walker WS (1976) Separate Fc-receptors for immunoglobulins IgG2a and IgG2b on an established cell line of mouse macrophages. The Journal of Immunology 116: 911-914.
69. Ferrec EL, Chesne C, Artusson P, Brayden D, Fabre G, et al. (2001) In vitro models of the intestinal barrier. The report and recommendations of ECVAM Workshop 46. European Centre for the Validation of Alternative methods. Altern Lab Anim 29: 649-668.
70. van der Flier LG, Clevers H (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260. doi: 10.1146/annurev.physiol.010908.163145.
71. Turner HL, Turner JR (2010) Good fences make good neighbors: Gastrointestinal mucosal structure. Gut Microbes 1: 22-29.
72. Fleet JC, Wang L, Vitek O, Craig BA, Edenberg HJ (2003) Gene expression profiling of Caco-2 BBe cells suggests a role for specific signaling pathways during intestinal differentiation. Physiological Genomics 13: 57-68.
73. Tremblay E, Auclair J, Delvin E, Levy E, Ménard D, et al. (2006) Gene expression profiles of normal proliferating and differentiating human intestinal epithelial cells: A comparison with the Caco-2 cell model. J Cell Biochem 99: 1175-1186.
74. Lenaerts K, Bouwman F, Lamers W, Renes J, Mariman E (2007) Comparative proteomic analysis of cell lines and scrapings of the human intestinal epithelium. BMC Genomics 8: 91. 10.1186/1471-2164-8-91.
75. Scott KG, Meddings JB, Kirk DR, Lees-Miller SP, Buret AG (2002) Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase2dependent fashion. Gastroenterology 123: 1179-1190.
76. Gillin FD, Diamond LS (1981) Entamoeba histolytica and Giardia lamblia: Effects of cysteine and oxygen tension on trophozoite attachment to glass and survival in culture media. Experimental Parasitology 52: 9-17.
77. Haller D, Bode C, Hammes WP, Pfeifer AMA, Schiffrin EJ, et al. (2000) Nonpathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 47: 79-87.
78. Kamda JD, Singer SM (2009) Phosphoinositide 3-kinase-dependent inhibition of dendritic cell interleukin-12 production by Giardia lamblia. Infect Immun 77: 685-693.
79. Sacks D, Sher A (2002) Evasion of innate immunity by parasitic protozoa. Nat Immunol 3: 1041-1047. 10.1038/ni1102-1041.
80. Lee HY, Hyung S, Lee NY, Yong TS, Han SH, et al. (2012) Excretory2 secretory products of Giardia lamblia induce interleukin-8 production in human colonic cells via activation of p38, ERK1/2, NF-kB and AP-1. Parasite Immunology 34: 183-198. 10.1111/j.1365-3024.2012.01354.x.
81. Heyworth MF, Owen RL, Jones AL (1985) Comparison of leukocytes obtained from the intestinal lumen of Giardia-infected immunocompetent mice and nude mice. Gastroenterol 89: 1360-1365.
82. Fritz J, Dwyer-Nield L, Malkinson A (2011) Stimulation of neoplastic mouse lung cell proliferation by alveolar macrophage-derived, insulin-like growth factor-1 can be blocked by inhibiting MEK and PI3K activation. Molecular Cancer 10: 76. 10.1186/1476-4598-10-76.
83. Smith PD, Smythies LE, Shen R, Greenwell-Wild T, Gliozzi M, et al. (2011) Intestinal macrophages and response to microbial encroachment. Mucosal Immunol 4: 31-42.
84. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, et al. (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115: 66-75.