Infectious diarrhea: Cellular and molecular mechanisms

Gut Microbes

Volumn 1, Issue 1, 2010, Pages 4-21

  Hodges, Kim ^a   Gill, Ravinder ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Enteric pathogens; EPEC; Infectious diarrhea; Ion absorption; Mechanisms of diarrhea

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL VACCINE; PROSTAGLANDIN E2; SEROTONIN;

ASTROVIRUS; CLOSTRIDIUM DIFFICILE; ENTAMOEBA HISTOLYTICA; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GASTROENTERITIS; GIARDIA LAMBLIA; HUMAN; IMMUNE RESPONSE; INFECTION PREVENTION; INFECTIOUS DIARRHEA; ION TRANSPORT; NONHUMAN; NOROVIRUS; ORAL REHYDRATION THERAPY; PATHOPHYSIOLOGY; RADIATION ABSORPTION; REVIEW; ROTAVIRUS; VIBRIO CHOLERAE;

ASTROVIRIDAE; BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; ENTAMOEBA HISTOLYTICA; ESCHERICHIA COLI; GIARDIA INTESTINALIS; NOROVIRUS; ROTAVIRUS; SHIGELLA; VIBRIO CHOLERAE;

EID: 77954821992     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.1.1.11036     Document Type: Review

References (151)

1. Slutsker L, Ries AA, Greene KD, Wells JG, Hutwagner L, Griffin PM. Escherichia coli O157:H7 diarrhea in the United States: clinical and epidemiologic features. Ann Intern Med 1997; 126:505-13.
2. Kyne L, Hamel MB, Polavaram R, Kelly CP. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 2002; 34:346-53.
3. Zhang RG, Scott DL, Westbrook ML, Nance S, Spangler BD, Shipley GG, Westbrook EM. The three-dimensional crystal structure of cholera toxin. J Mol Biol 1995; 251:563-73.
4. Cassell JT. Neil A. Dayton 1893-1977. A personal tribute. Am J Ment Defic 1977; 82:227-8.
5. Cheng SH, Rich DP, Marshall J, Gregory RJ, Welsh MJ, Smith AE. Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 1991; 66:1027-36.
6. Lencer WI, Constable C, Moe S, Jobling MG, Webb HM, Ruston S, et al. Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J Cell Biol 1995; 131:951-62.
7. Lord JM, Roberts LM, Lencer WI. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr Top Microbiol Immunol 2005; 300:149-68.
8. Subramanya SB, Rajendran VM, Srinivasan P, Nanda Kumar NS, Ramakrishna BS, Binder HJ. Differential regulation of cholera toxin-inhibited Na-H exchange isoforms by butyrate in rat ileum. Am J Physiol Gastrointest Liver Physiol 2007; 293:857-63.
9. Trucksis M, Conn TL, Wasserman SS, Sears CL. Vibrio cholerae ACE stimulates Ca(2+)-dependent Cl(-)/HCO(3)(-) secretion in T84 cells in vitro. Am J Physiol Cell Physiol 2000; 279:567-77.
10. Krasilnikov OV, Muratkhodjaev JN, Zitzer AO. The mode of action of Vibrio cholerae cytolysin. The influences on both erythrocytes and planar lipid bilayers. Biochim Biophys Acta 1992; 1111:7-16.
11. Visweswariah SS, Shanthi G, Balganesh TS. Interaction of heat-stable enterotoxins with human colonic (T84) cells: modulation of the activation of guanylyl cyclase. Microb Pathog 1992; 12:209-18.
12. Gutierrez MG, Saka HA, Chinen I, Zoppino FC, Yoshimori T, Bocco JL, Colombo MI. Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae. Proc Natl Acad Sci USA 2007; 104:1829-34.
13. Wu Z, Nybom P, Magnusson KE. Distinct effects of Vibrio cholerae haemagglutinin/protease on the structure and localization of the tight junction-associated proteins occludin and ZO-1. Cell Microbiol 2000; 2:11-7.
14. Fullner KJ, Lencer WI, Mekalanos JJ. Vibrio cholerae-induced cellular responses of polarized T84 intestinal epithelial cells are dependent on production of cholera toxin and the RTX toxin. Infect Immun 2001; 69:6310-7.
15. Kudryashov DS, Cordero CL, Reisler E, Satchell KJ. Characterization of the enzymatic activity of the actin cross-linking domain from the Vibrio cholerae MARTX Vc toxin. J Biol Chem 2008; 283:445-52.
16. Uzzau S, Cappuccinelli P, Fasano A. Expression of Vibrio cholerae zonula occludens toxin and analysis of its subcellular localization. Microb Pathog 1999; 27:377-85.
17. Davis BM, Waldor MK. Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol 2003; 6:35-42.
18. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996; 272:1910-4.
19. Wang W, Uzzau S, Goldblum SE, Fasano A. Human zonulin, a potential modulator of intestinal tight junctions. J Cell Sci 2000; 113:4435-40.
20. Gopalakrishnan S, Pandey N, Tamiz AP, Vere J, Carrasco R, Somerville R, et al. Mechanism of action of ZOT-derived peptide AT-1002, a tight junction regulator and absorption enhancer. Int J Pharm 2009; 365:121-30.
21. Bartlett JG, Gorbach SL. Pseudomembranous enterocolitis (antibiotic-related colitis). Adv Intern Med 1977; 22:455-76.
22. Deneve C, Janoir C, Poilane I, Fantinato C, Collignon A. New trends in Clostridium difficile virulence and pathogenesis. Int J Antimicrob Agents 2009; 33:24-8.
23. Perelle S, Gibert M, Bourlioux P, Corthier G, Popoff MR. Production of a complete binary toxin (actin-specific ADP-ribosyltransferase) by Clostridium difficile CD196. Infect Immun 1997; 65:1402-7.
24. Na X, Kim H, Moyer MP, Pothoulakis C, LaMont JT. gp96 is a human colonocyte plasma membrane binding protein for Clostridium difficile toxin A. Infect Immun 2008; 76:2862-71.
25. Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 2009; 7:526-36.
26. Thelestam M, Chaves-Olarte E. Cytotoxic effects of the Clostridium difficile toxins. Curr Top Microbiol Immunol 2000; 250:85-96.
27. Thelestam M. Bacterial protein toxins-general conclusions. Int J Med Microbiol 2000; 290:503-6.
28. Barbut F, Decre D, Lalande V, Burghoffer B, Noussair L, Gigandon A, et al. Clinical features of Clostridium difficile-associated diarrhoea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J Med Microbiol 2005; 54:181-5.
29. Lyras D, O'Connor JR, Howarth PM, Sambol SP, Carter GP, Phumoonna T, et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009; 458:1176-9.
30. Lima AA, Lyerly DM, Wilkins TD, Innes DJ, Guerrant RL. Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect Immun 1988; 56:582-8.
31. Moore R, Pothoulakis C, LaMont JT, Carlson S, Madara JL. C. difficile toxin A increases intestinal permeability and induces Clsecretion. Am J Physiol 1990; 259:165-72.
32. Hecht G, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J Clin Invest 1988; 82:1516-24.
33. Pothoulakis C, Lamont JT. Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol 2001; 280:178-83.
34. Flegel WA, Muller F, Daubener W, Fischer HG, Hadding U, Northoff H. Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun 1991; 59:3659-66.
35. Kelly CP, Becker S, Linevsky JK, Joshi MA, O'Keane JC, Dickey BF, et al. Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 1994; 93:1257-65.
36. Keates AC, Castagliuolo I, Qiu B, Nikulasson S, Sengupta A, Pothoulakis C. CGRP upregulation in dorsal root ganglia and ileal mucosa during Clostridium difficile toxin A-induced enteritis. Am J Physiol 1998; 274:196-202.
37. Pothoulakis C, Castagliuolo I, Leeman SE, Wang CC, Li H, Hoffman BJ, Mezey E. Substance P receptor expression in intestinal epithelium in Clostridium difficile toxin A enteritis in rats. Am J Physiol 1998; 275:68-75.
38. Castagliuolo I, Wang CC, Valenick L, Pasha A, Nikulasson S, Carraway RE, Pothoulakis C. Neurotensin is a proinflammatory neuropeptide in colonic inflammation. J Clin Invest 1999; 103:843-9.
39. Castagliuolo I, Riegler M, Pasha A, Nikulasson S, Lu B, Gerard C, et al. Neurokinin-1 (NK-1) receptor is required in Clostridium difficile-induced enteritis. J Clin Invest 1998; 101:1547-50.
40. Centers for Disease Control and Prevention, www. cdc.gov.
41. Wassef JS, Keren DF, Mailloux JL. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 1989; 57:858-63.
42. Prevost MC, Lesourd M, Arpin M, Vernel F, Mounier J, Hellio R, Sansonetti PJ. Unipolar reorganization of F-actin layer at bacterial division and bundling of actin filaments by plastin correlate with movement of Shigella flexneri within HeLa cells. Infect Immun 1992; 60:4088-99.
43. Schroeder GN, Hilbi H. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion and death by type III secretion. Clin Microbiol Rev 2008; 21:134-56.
44. Yee RB, Buffenmyer CL. Infection of Cultured Mouse Macrophages with Shigella flexneri. Infect Immun 1970; 1:459-63.
45. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Banerjee S, Akira S, et al. Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 2000; 12:581-90.
46. Rallabhandi P, Awomoyi A, Thomas KE, Phalipon A, Fujimoto Y, Fukase K, et al. Differential activation of human TLR4 by Escherichia coli and Shigella flexneri 2a lipopolysaccharide: combined effects of lipid A acylation state and TLR4 polymorphisms on signaling. J Immunol 2008; 180:1139-47.
47. Aliprantis AO, Weiss DS, Radolf JD, Zychlinsky A. Release of Toll-like receptor-2-activating bacterial lipoproteins in Shigella flexneri culture supernatants. Infect Immun 2001; 69:6248-55.
48. Nigro G, Fazio LL, Martino MC, Rossi G, Tattoli I, Liparoti V, et al. Muramylpeptide shedding modulates cell sensing of Shigella flexneri. Cell Microbiol 2008; 10:682-95.
49. Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, et al. The phosphothreonine lyase activity of a bacterial type III effector family. Science 2007; 315:1000-3.
50. Rohde JR, Breitkreutz A, Chenal A, Sansonetti PJ, Parsot C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 2007; 1:77-83.
51. Kim DW, Lenzen G, Page AL, Legrain P, Sansonetti PJ, Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 2005; 102:14046-51.
52. Sansonetti PJ, Arondel J, Huerre M, Harada A, Matsushima K. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect Immun 1999; 67:1471-80.
53. Kim M, Ogawa M, Fujita Y, Yoshikawa Y, Nagai T, Koyama T, et al. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 2009; 459:578-82.
54. Sakaguchi T, Kohler H, Gu X, McCormick BA, Reinecker HC. Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells. Cell Microbiol 2002; 4:367-81.
55. Al-Hasani K, Henderson IR, Sakellaris H, Rajakumar K, Grant T, Nataro JP, et al. The sigA gene which is borne on the she pathogenicity island of Shigella flexneri 2a encodes an exported cytopathic protease involved in intestinal fluid accumulation. Infect Immun 2000; 68:2457-63.
56. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2:123-40.
57. Golin-Bisello F, Bradbury N, Ameen N. STa and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G. Am J Physiol Cell Physiol 2005; 289:708-16.
58. Vaandrager AB. Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. Mol Cell Biochem 2002; 230:73-83.
59. Lucas ML. Enterocyte chloride and water secretion into the small intestine after enterotoxin challenge: unifying hypothesis or intellectual dead end? J Physiol Biochem 2008; 64:69-88.
60. Sellers ZM, Mann E, Smith A, Ko KH, Giannella R, Cohen MB, et al. Heat-stable enterotoxin of Escherichia coli (STa) can stimulate duodenal HCO3(-) secretion via a novel GC-C and CFTR-independent pathway. Faseb J 2008; 22:1306-16.
61. Pratha VS, Hogan DL, Martensson BA, Bernard J, Zhou R, Isenberg JI. Identification of transport abnormalities in duodenal mucosa and duodenal enterocytes from patients with cystic fibrosis. Gastroenterology 2000; 118:1051-60.
62. Sellers ZM, Childs D, Chow JY, Smith AJ, Hogan DL, Isenberg JI, et al. Heat-stable enterotoxin of Escherichia coli stimulates a non-CFTR-mediated duodenal bicarbonate secretory pathway. Am J Physiol Gastrointest Liver Physiol 2005; 288:654-63.
63. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998; 11:142-201.
64. +/peptide cotransporter in the human intestinal cell line Caco-2 by cyclic AMP. Biochem Biophys Res Commun 1996; 218:461-5.
65. Kenny B, Abe A, Stein M, Finlay BB. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect Immun 1997; 65:2606-12.
66. Hecht G. Microbes and microbial toxins: paradigms for microbial-mucosal interactions VII. Enteropathogenic Escherichia coli: physiological alterations from an extracellular position. Am J Physiol Gastrointest Liver Physiol 2001; 281:1-7.
67. Donnenberg MS, Tacket CO, James SP, Losonsky G, Nataro JP, Wasserman SS, et al. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 1993; 92:1412-7.
68. Gill RK, Borthakur A, Hodges K, Turner JR, Clayburgh DR, Saksena S, et al. Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli. J Clin Invest 2007; 117:428-37.
69. + exchange isoform activities by enteropathogenic E. coli in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2004; 287:370-8.
70. Hecht G, Koutsouris A. Enteropathogenic E. coli attenuates secretagogue-induced net intestinal ion transport but not Cl secretion. Am J Physiol 1999; 276:781-8.
71. Collington GK, Booth IW, Knutton S. Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection. Gut 1998; 42:200-7.
72. + exchanger. Nat Genet 1998; 19:282-5.
73. + exchanger isoform 2 gene causes reduced viability of gastric parietal cells and loss of net acid secretion. J Clin Invest 1998; 101:1243-53.
74. Ledoussal C, Woo AL, Miller ML, Shull GE. Loss of the NHE2 Na(+)/H(+) exchanger has no apparent effect on diarrheal state of NHE3-deficient mice. Am J Physiol Gastrointest Liver Physiol 2001; 281:1385-96.
75. Hodges K, Alto NM, Ramaswamy K, Dudeja PK, Hecht G. The enteropathogenic Escherichia coli effector protein EspF decreases sodium hydrogen exchanger 3 activity. Cell Microbiol 2008; 10:1735-45.
76. + exchanger regulatory factor (NHERF) proteins. Clin Exp Pharmacol Physiol 2008; 35:863-71.
77. Dean P, Maresca M, Schuller S, Phillips AD, Kenny B. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 2006; 103:1876-81.
78. Tomson FL, Viswanathan VK, Kanack KJ, Kanteti RP, Straub KV, Menet M, et al. Enteropathogenic Escherichia coli EspG disrupts microtubules and in conjunction with Orf3 enhances perturbation of the tight junction barrier. Mol Microbiol 2005; 56:447-64.
79. Makela S, Kere J, Holmberg C, Hoglund P. SLC26A3 mutations in congenital chloride diarrhea. Hum Mutat 2002; 20:425-38.
80. Schweinfest CW, Spyropoulos DD, Henderson KW, Kim JH, Chapman JM, Barone S, et al. slc26a3 (dra)-deficient mice display chloride-losing diarrhea, enhanced colonic proliferation, and distinct upregulation of ion transporters in the colon. J Biol Chem 2006; 281:37962-71.
81. Seidler U, Rottinghaus I, Hillesheim J, Chen M, Riederer B, Krabbenhoft A, et al. Sodium and chloride absorptive defects in the small intestine in Slc26a6 null mice. Pflugers Arch 2008; 455:757-66.
82. Borenshtein D, Schlieper KA, Rickman BH, Chapman JM, Schweinfest CW, Fox JG, Schauer DB. Decreased expression of colonic Slc26a3 and carbonic anhydrase iv as a cause of fatal infectious diarrhea in mice. Infect Immun 2009; 77:3639-50.
83. Borenshtein D, Fry RC, Groff EB, Nambiar PR, Carey VJ, Fox JG, Schauer DB. Diarrhea as a cause of mortality in a mouse model of infectious colitis. Genome Biol 2008; 9:122.
84. Guttman JA, Samji FN, Li Y, Deng W, Lin A, Finlay BB. Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol 2007; 9:131-41.
85. + exchange activity via 5-HT4 receptors and activation of PKC alpha in human intestinal epithelial cells. Gastroenterology 2005; 128:962-74.
86. Eklund S, Brunsson I, Jodal M, Lundgren O. Changes in cyclic 3'5'-adenosine monophosphate tissue concentration and net fluid transport in the cat's small intestine elicited by cholera toxin, arachidonic acid, vasoactive intestinal polypeptide and 5-hydroxytryptamine. Acta Physiol Scand 1987; 129:115-25.
87. Esmaili A, Nazir SF, Borthakur A, Yu D, Turner JR, Saksena S, et al. Enteropathogenic E. coli Infection Inhibits Intestinal Serotonin Transporter (SERT) Function and Expression. Gastroenterology 2009.
88. Borthakur A, Gill RK, Hodges K, Ramaswamy K, Hecht G, Dudeja PK. Enteropathogenic Escherichia coli inhibits butyrate uptake in Caco-2 cells by altering the apical membrane MCT1 level. Am J Physiol Gastrointest Liver Physiol 2006; 290:30-5.
89. Manjarrez-Hernandez HA, Baldwin TJ, Williams PH, Haigh R, Knutton S, Aitken A. Phosphorylation of myosin light chain at distinct sites and its association with the cytoskeleton during enteropathogenic Escherichia coli infection. Infect Immun 1996; 64:2368-70.
90. Thanabalasuriar A, Koutsouris A, Weflen A, Mimee M, Hecht G, Gruenheid S. The bacterial virulence factor NleA is required for the disruption of intestinal tight junctions by enteropathogenic Escherichia coli. Cell Microbiol 2009.
91. Shifflett DE, Clayburgh DR, Koutsouris A, Turner JR, Hecht GA. Enteropathogenic E. coli disrupts tight junction barrier function and structure in vivo. Lab Invest 2005; 85:1308-24.
92. Savkovic SD, Koutsouris A, Hecht G. PKCzeta participates in activation of inflammatory response induced by enteropathogenic E. coli. Am J Physiol Cell Physiol 2003; 285:512-21.
93. Sharma R, Tesfay S, Tomson FL, Kanteti RP, Viswanathan VK, Hecht G. Balance of bacterial pro and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2006; 290:685-94.
94. Obrig TG, Moran TP, Brown JE. The mode of action of Shiga toxin on peptide elongation of eukaryotic protein synthesis. Biochem J 1987; 244:287-94.
95. Cohen A, Hannigan GE, Williams BR, Lingwood CA. Roles of globotriosyland galabiosylceramide in verotoxin binding and high affinity interferon receptor. J Biol Chem 1987; 262:17088-91.
96. Hauf N, Chakraborty T. Suppression of NFkappaB activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J Immunol 2003; 170:2074-82.
97. Schuller S, Heuschkel R, Torrente F, Kaper JB, Phillips AD. Shiga toxin binding in normal and inflamed human intestinal mucosa. Microbes Infect 2007; 9:35-9.
98. Creydt VP, Miyakawa MF, Martin F, Zotta E, Silberstein C, Ibarra C. The Shiga toxin 2 B subunit inhibits net fluid absorption in human colon and elicits fluid accumulation in rat colon loops. Braz J Med Biol Res 2004; 37:799-808.
99. Ferreira AJ, Elias WP Jr, Pelayo JS, Giraldi R, Pedroso MZ, Scaletsky IC. Culture supernatant of Shiga toxin-producing Escherichia coli strains provoke fluid accumulation in rabbit ileal loops. FEMS Immunol Med Microbiol 1997; 19:285-8.
100. Laiko M, Murtazina R, Malyukova I, Zhu C, Boedeker EC, Gutsal O, et al. Shiga toxin 1 interaction with enterocytes causes apical protein mistargeting through the depletion of intracellular galectin-3. Exp Cell Res 2009.
101. Muller S, Schaffer T, Flogerzi B, Fleetwood A, Weimann R, Schoepfer AM, Seibold F. Galectin-3 modulates T cell activity and is reduced in the inflamed intestinal epithelium in IBD. Inflamm Bowel Dis 2006; 12:588-97.
102. Musher DM, Musher BL. Contagious acute gastrointestinal infections. N Engl J Med 2004; 351:2417-27.
103. Ciarlet M, Estes MK. Rotavirus and calicivirus infections of the gastrointestinal tract. Curr Opin Gastroenterol 2001; 17:10-6.
104. Rodriguez WJ, Kim HW, Brandt CD, Schwartz RH, Gardner MK, Jeffries B, et al. Longitudinal study of rotavirus infection and gastroenteritis in families served by a pediatric medical practice: clinical and epidemiologic observations. Pediatr Infect Dis J 1987; 6:170-6.
105. Greenberg HB, Estes MK. Rotaviruses: from pathogenesis to vaccination. Gastroenterology 2009; 136:1939-51.
106. Pesavento JB, Crawford SE, Estes MK, Prasad BV. Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 2006; 309:189-219.
107. Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 1996; 272:101-4.
108. Boshuizen JA, Rossen JW, Sitaram CK, Kimenai FF, Simons-Oosterhuis Y, Laffeber C, et al. Rotavirus enterotoxin NSP4 binds to the extracellular matrix proteins laminin-beta3 and fibronectin. J Virol 2004; 78:10045-53.
109. Jourdan N, Brunet JP, Sapin C, Blais A, Cotte-Laffitte J, Forestier F, et al. Rotavirus infection reduces sucrase-isomaltase expression in human intestinal epithelial cells by perturbing protein targeting and organization of microvillar cytoskeleton. J Virol 1998; 72:7228-36.
110. Halaihel N, Lievin V, Alvarado F, Vasseur M. Rotavirus infection impairs intestinal brush-border membrane Na(+)-solute cotransport activities in young rabbits. Am J Physiol Gastrointest Liver Physiol 2000; 279:587-96.
111. Collins J, Candy DC, Starkey WG, Spencer AJ, Osborne MP, Stephen J. Disaccharidase activities in small intestine of rotavirus-infected suckling mice: a histochemical study. J Pediatr Gastroenterol Nutr 1990; 11:395-403.
112. Dickman KG, Hempson SJ, Anderson J, Lippe S, Zhao L, Burakoff R, Shaw RD. Rotavirus alters paracellular permeability and energy metabolism in Caco-2 cells. Am J Physiol Gastrointest Liver Physiol 2000; 279:757-66.
113. Lorrot M, Vasseur M. Physiopathology of Rotavirus diarrhea. Arch Pediatr 2007; 14:145-51.
114. Morris AP, Estes MK. Microbes and microbial toxins: paradigms for microbial-mucosal interactions VIII. Pathological consequences of rotavirus infection and its enterotoxin. Am J Physiol Gastrointest Liver Physiol 2001; 281:303-10.
115. Salazar-Lindo E, Santisteban-Ponce J, Chea-Woo E, Gutierrez M. Racecadotril in the treatment of acute watery diarrhea in children. N Engl J Med 2000; 343:463-7.
116. Berkova Z, Morris AP, Estes MK. Cytoplasmic calcium measurement in rotavirus enterotoxin-enhanced green fluorescent protein (NSP4-EGFP) expressing cells loaded with Fura-2. Cell Calcium 2003; 34:55-68.
117. Berkova Z, Crawford SE, Blutt SE, Morris AP, Estes MK. Expression of rotavirus NSP4 alters the actin network organization through the actin remodeling protein cofilin. J Virol 2007; 81:3545-53.
118. DesMarais V, Macaluso F, Condeelis J, Bailly M. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 2004; 117:3499-510.
119. Lorrot M, Vasseur M. How do the rotavirus NSP4 and bacterial enterotoxins lead differently to diarrhea? Virol J 2007; 4:31.
120. Morris AP, Scott JK, Ball JM, Zeng CQ, O'Neal WK, Estes MK. NSP4 elicits age-dependent diarrhea and Ca(2+)mediated I(-) influx into intestinal crypts of CF mice. Am J Physiol 1999; 277:431-44.
121. Kuyumcu-Martinez M, Belliot G, Sosnovtsev SV, Chang KO, Green KY, Lloyd RE. Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein. J Virol 2004; 78:8172-82.
122. Ettayebi K, Hardy ME. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J Virol 2003; 77:11790-7.
123. Troeger H, Loddenkemper C, Schneider T, Schreier E, Epple HJ, Zeitz M, et al. Structural and functional changes of the duodenum in human norovirus infection. Gut 2009; 58:1070-7.
124. Sebire NJ, Malone M, Shah N, Anderson G, Gaspar HB, Cubitt WD. Pathology of astrovirus associated diarrhoea in a paediatric bone marrow transplant recipient. J Clin Pathol 2004; 57:1001-3.
125. Koci MD, Moser LA, Kelley LA, Larsen D, Brown CC, Schultz-Cherry S. Astrovirus induces diarrhea in the absence of inflammation and cell death. J Virol 2003; 77:11798-808.
126. Moser LA, Schultz-Cherry S. Suppression of astrovirus replication by an ERK1/2 inhibitor. J Virol 2008; 82:7475-82.
127. Bonaparte RS, Hair PS, Banthia D, Marshall DM, Cunnion KM, Krishna NK. Human astrovirus coat protein inhibits serum complement activation via C1, the first component of the classical pathway. J Virol 2008; 82:817-27.
128. Moser LA, Carter M, Schultz-Cherry S. Astrovirus increases epithelial barrier permeability independently of viral replication. J Virol 2007; 81:11937-45.
129. Mendez E, Salas-Ocampo E, Arias CF. Caspases mediate processing of the capsid precursor and cell release of human astroviruses. J Virol 2004; 78:8601-8.
130. Muller N, von Allmen N. Recent insights into the mucosal reactions associated with Giardia lamblia infections. Int J Parasitol 2005; 35:1339-47.
131. D'Anchino M, Orlando D, De Feudis L. Giardia lamblia infections become clinically evident by eliciting symptoms of irritable bowel syndrome. J Infect 2002; 45:169-72.
132. Hanevik K, Dizdar V, Langeland N, Hausken T. Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol 2009; 9:27.
133. Buret AG. Mechanisms of epithelial dysfunction in giardiasis. Gut 2007; 56:316-7.
134. Chin AC, Teoh DA, Scott KG, Meddings JB, Macnaughton WK, Buret AG. Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect Immun 2002; 70:3673-80.
135. Buret A, Hardin JA, Olson ME, Gall DG. Pathophysiology of small intestinal malabsorption in gerbils infected with Giardia lamblia. Gastroenterology 1992; 103:506-13.
136. Cevallos A, Carnaby S, James M, Farthing JG. Small intestinal injury in a neonatal rat model of giardiasis is strain dependent. Gastroenterology 1995; 109:766-73.
137. Gorowara S, Ganguly NK, Mahajan RC, Walia BN. Study on the mechanism of Giardia lamblia induced diarrhoea in mice. Biochim Biophys Acta 1992; 1138:122-6.
138. Troeger H, Epple HJ, Schneider T, Wahnschaffe U, Ullrich R, Burchard GD, et al. Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 2007; 56:328-35.
139. Bracha R, Nuchamowitz Y, Mirelman D. Transcriptional silencing of an amoebapore gene in Entamoeba histolytica: molecular analysis and effect on pathogenicity. Eukaryot Cell 2003; 2:295-305.
140. Que X, Reed SL. Cysteine proteinases and the pathogenesis of amebiasis. Clin Microbiol Rev 2000; 13:196-206.
141. Braga LL, Ninomiya H, McCoy JJ, Eacker S, Wiedmer T, Pham C, et al. Inhibition of the complement membrane attack complex by the galactose-specific adhesion of Entamoeba histolytica. J Clin Invest 1992; 90:1131-7.
142. Takeuchi A, Phillips BP. Electron microscope studies of experimental Entamoeba histolytica infection in the guinea pig II. Early cellular and vascular changes accompanying invasion of the lamina propria. Virchows Arch B Cell Pathol 1976; 20:1-13.
143. Riahi Y, Siman-Tov R, Ankri S. Molecular cloning, expression and characterization of a serine proteinase inhibitor gene from Entamoeba histolytica. Mol Biochem Parasitol 2004; 133:153-62.
144. Maldonado-Bernal C, Kirschning CJ, Rosenstein Y, Rocha LM, Rios-Sarabia N, Espinosa-Cantellano M, et al. The innate immune response to Entamoeba histolytica lipopeptidophosphoglycan is mediated by toll-like receptors 2 and 4. Parasite Immunol 2005; 27:127-37.
145. Ivory CP, Prystajecky M, Jobin C, Chadee K. Toll-like receptor 9-dependent macrophage activation by Entamoeba histolytica DNA. Infect Immun 2008; 76:289-97.
146. Leroy A, Lauwaet T, De Bruyne G, Cornelissen M, Mareel M. Entamoeba histolytica disturbs the tight junction complex in human enteric T84 cell layers. FASEB J 2000; 14:1139-46.
147. Lauwaet T, Oliveira MJ, Callewaert B, De Bruyne G, Mareel M, Leroy A. Proteinase inhibitors TPCK and TLCK prevent Entamoeba histolytica induced disturbance of tight junctions and microvilli in enteric cell layers in vitro. Int J Parasitol 2004; 34:785-94.
148. McGowan K, Kane A, Asarkof N, Wicks J, Guerina V, Kellum J, et al. Entamoeba histolytica causes intestinal secretion: role of serotonin. Science 1983; 221:762-4.
149. Dey I, Keller K, Belley A, Chadee K. Identification and characterization of a cyclooxygenase-like enzyme from Entamoeba histolytica. Proc Natl Acad Sci USA 2003; 100:13561-6.
150. Stenson WF, Zhang Z, Riehl T, Stanley SL Jr. Amebic infection in the human colon induces cyclooxygenase-2. Infect Immun 2001; 69:3382-8.
151. McGowan K, Piver G, Stoff JS, Donowitz M. Role of prostaglandins and calcium in the effects of Entamoeba histolytica on colonic electrolyte transport. Gastroenterology 1990; 98:873-80.