Giardia duodenalis induces paracellular bacterial translocation and causes postinfectious visceral hypersensitivity

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 310, Issue 8, 2016, Pages G574-G585

  Halliez, Marie C M ^a,b   Motta, Jean Paul ^b   Feener, Troy D ^b   Guérin, Gaetan ^a   Legoff, Laetitia ^a   François, Arnaud ^a   Colasse, Elodie ^a   Favennec, Loic ^a   Gargala, Gilles ^a   Lapointe, Tamia K ^b   Altier, Christophe ^b   Buret, André G ^b  

^a ROUEN UNIVERSITY HOSPITAL   (France)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bacterial translocation; Irritable bowel syndrome; Tight junctions; Visceral hypersensitivity

Indexed keywords

CLAUDIN 4; OCCLUDIN; PROTEIN C FOS; TIGHT JUNCTION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CACO 2 CELL LINE; CELL PROLIFERATION; COMMENSAL; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; GIARDIA INTESTINALIS; GIARDIASIS; HISTOLOGY; HUMAN; HUMAN CELL; HYPERPLASIA; HYPERSENSITIVITY; IMMUNOCOMPETENCE; IN VITRO STUDY; IN VIVO STUDY; INFECTION COMPLICATION; INTERNALIZATION; INTESTINE CRYPT; INTESTINE DISTENSION; INTESTINE FLORA; INTESTINE MUCOSA; INTESTINE VILLUS ATROPHY; IRRITABLE COLON; JEJUNUM; LYMPHOCYTE; MAST CELL; MONOLAYER CULTURE; NEWBORN; NOCICEPTION; NONHUMAN; PARASITE CLEARANCE; PERMEABILITY BARRIER; POSTINFECTIOUS VISCERAL HYPERSENSITIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECTUM; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; TROPHOZOITE; ANIMAL; CACO-2 CELL LINE; COMPLICATION; IRRITABLE BOWEL SYNDROME; MALE; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSCELLULAR CELL MIGRATION;

ANIMALS; CACO-2 CELLS; ESCHERICHIA COLI; FEMALE; GASTROINTESTINAL MICROBIOME; GIARDIASIS; HUMANS; INTESTINAL MUCOSA; IRRITABLE BOWEL SYNDROME; MALE; NOCICEPTION; RATS; RATS, SPRAGUE-DAWLEY; TIGHT JUNCTION PROTEINS; TRANSCELLULAR CELL MIGRATION;

EID: 84983802563     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00144.2015     Document Type: Article

References (82)

1. Arebi N, Gurmany S, Bullas D, Hobson A, Stagg A, Kamm M. The psychoneuroimmunology of irritable bowel syndrome—an exploration of interactions between psychological, neurological and immunological observations. Aliment Pharmacol Ther 28: 830-840, 2008.
2. Arévalo F, Aragon V, Montes P, Guzmán E, Monge E. [Increase of intraepithelial lymphocytes in patients with irritable bowel syndrome]. Rev Gastroenterol Perú 31: 315-318, 2011.
3. Azpiroz F, Bouin M, Camilleri M, Mayer EA, Poitras P, Serra J, Spiller RC. Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 19: 62-88, 2007.
4. Balestra B, Vicini R, Cremon C, Zecchi L, Dothel G, Vasina V, De Giorgio R, Paccapelo A, Pastoris O, Stanghellini V, Corinaldesi R, De Ponti F, Tonini M, Barbara G. Colonic mucosal mediators from patients with irritable bowel syndrome excite enteric cholinergic motor neurons. Neurogastroenterol Motil 24: 1118-e570, 2012.
5. Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126: 693-702, 2004.
6. Beatty JK, Akierman S, Rioux K, Beck P, McKnight W, Feener T, Wallace J, Buret A. Gut microbiota biofilm disruptions by Giardia: pathology in human enterocytes and germ-free mice (Abstract). FASEB J 27: 131.1, 2013.
7. Beatty JK, Bhargava A, Buret AG. Post-infectious irritable bowel syndrome: mechanistic insights into chronic disturbances following enteric infection. World J Gastroenterol 20: 3976-3985, 2014.
8. Bénéré E, Van Assche T, Van Ginneken C, Peulen O, Cos P, Maes L. Intestinal growth and pathology of Giardia duodenalis assemblage subtype AI, AII, B and E in the gerbil model. Parasitology 139: 424-433, 2012.
9. Bercík P, Wang L, Verdú EF, Mao YK, Blennerhassett P, Khan WI, Kean I, Tougas G, Collins SM. Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 127: 179-187, 2004.
10. Bertiaux-Vandaële N, Youmba SB, Belmonte L, Lecleire S, Antonietti M, Gourcerol G, Leroi AM, Déchelotte P, Ménard JF, Ducrotté P, Coëffier M. The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 106: 2165-2173, 2011.
11. Buret A, denHollander N, Wallis PM, Befus D, Olson ME. Zoonotic potential of giardiasis in domestic ruminants. J Infect Dis 162: 231-237, 1990.
12. Buret A, Gall DG, Olson ME. Effects of murine giardiasis on growth, intestinal morphology, and disaccharidase activity. J Parasitol 76: 403-409, 1990.
13. Buret A, Gall DG, Olson ME. Growth, activities of enzymes in the small intestine, and ultrastructure of microvillous border in gerbils infected with Giardia duodenalis. Parasitol Res 77: 109-114, 1991.
14. Buret A, Hardin JA, Olson ME, Gall DG. Pathophysiology of small intestinal malabsorption in gerbils infected with Giardia lamblia. Gastroenterology 103: 506-513, 1992.
15. Camilleri M, Lasch K, Zhou W. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. The confluence of increased permeability, inflammation, and pain in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 303: G775-G785, 2012.
16. Cenac N, Andrews CN, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, Steinhoff M, Barbara G, Beck P, Bunnett NW, Sharkey KA, Ferraz JG, Shaffer E, Vergnolle N. Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 117: 636-647, 2007.
17. Cevallos A, Carnaby S, James M, Farthing JG. Small intestinal injury in a neonatal rat model of giardiasis is strain dependent. Gastroenterology 109: 766-773, 1995.
18. Chen TL, Chen S, Wu HW, Lee TC, Lu YZ, Wu LL, Ni YH, Sun CH, Yu WH, Buret AG, Yu LC. Persistent gut barrier damage and commensal bacterial influx following eradication of Giardia infection in mice. Gut Pathog 5: 26, 2013.
19. Clarke G, Quigley EM, Cryan JF, Dinan TG. Irritable bowel syndrome: towards biomarker identification. Trends Mol Med 15: 478-489, 2009.
20. Coelho AM, Fioramonti J, Buéno L. Systemic lipopolysaccharide influences rectal sensitivity in rats: role of mast cells, cytokines, and vagus nerve. Am J Physiol Gastrointest Liver Physiol 279: G781-G790, 2000.
21. Collins SM. A role for the gut microbiota in IBS. Nat Rev Gastroenterol 11: 497-505, 2014.
22. Costantini M, Sturniolo GC, Zaninotto G, D’Incà R, Polo R, Naccarato R, Ancona E. Altered esophageal pain threshold in irritable bowel syndrome. Dig Dis Sci 38: 206-212, 1993.
23. Cotton JA, Beatty JK, Buret AG. Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol 41: 925-933, 2011.
24. Diamond LS, Harlow DR, Cunnick CC. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg 72: 431-432, 1978.
25. Evans PR, Bennett EJ, Bak YT, Tennant CC, Kellow JE. Jejunal sensorimotor dysfunction in irritable bowel syndrome: clinical and psychosocial features. Gastroenterology 110: 393-404, 1996.
26. Evans PR, Piesse C, Bak YT, Kellow JE. Fructose-sorbitol malabsorption and symptom provocation in irritable bowel syndrome: relationship to enteric hypersensitivity and dysmotility. Scand J Gastroenterol 33: 1158-1163, 1998.
27. Fent J, Balázs L, Buzás G, Erasmus LP, Hölzl R, Kovács A, Weisz J, Adám G. Colonic sensitivity in irritable bowel syndrome and normal subjects according to their hemispheric preference and cognitive style. Integr Physiol Behav Sci 34: 54-62, 1999.
28. Gaykema RP, Goehler LE, Tilders FJ, Bol JG, McGorry M, Fleshner M, Maier SF, Watkins LR. Bacterial endotoxin induces fos immunoreactivity in primary afferent neurons of the vagus nerve. Neuroimmunomodulation 5: 234-240, 1998.
29. Geurden T, Geldhof P, Levecke B, Martens C, Berkvens D, Casaert S, Vercruysse J, Claerebout E. Mixed Giardia duodenalis assemblage A and E infections in calves. Int J Parasitol 38: 259-264, 2008.
30. Gibney SM, Gosselin RD, Dinan TG, Cryan JF. Colorectal distensioninduced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience 165: 675-683, 2010.
31. Gillon J, Al Thamery D, Ferguson A. Features of small intestinal pathology (epithelial cell kinetics, intraepithelial lymphocytes, disaccharidases) in a primary Giardia muris infection. Gut 23: 498-506, 1982.
32. Goldstein R, Braverman D, Stankiewicz H. Carbohydrate malabsorption and the effect of dietary restriction on symptoms of irritable bowel syndrome and functional bowel complaints. Isr Med Assoc J 2: 583-587, 2000.
33. Halliez MC, Buret AG. Extra-intestinal and long term consequences of Giardia duodenalis infections. World J Gastroenterol 19: 8974-8985, 2013.
34. Halvorson HA, Schlett CD, Riddle MS. Postinfectious irritable bowel syndrome—a meta-analysis. Am J Gastroenterol 101: 1894-1899; quiz 1942, 2006.
35. Hanevik K, Dizdar V, Langeland N, Hausken T. Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol 9: 27, 2009.
36. Hanevik K, Wensaas KA, Rortveit G, Eide GE, Mørch K, Langeland N. Irritable bowel syndrome and chronic fatigue 6 years after Giardia infection: a controlled prospective cohort study. Clin Infect Dis 59: 1394-1400, 2014.
37. Hardin JA, Buret AG, Olson ME, Kimm MH, Gall DG. Mast cell hyperplasia and increased macromolecular uptake in an animal model of giardiasis. J Parasitol 83: 908-912, 1997.
38. Ibeakanma C, Ochoa-Cortes F, Miranda-Morales M, McDonald T, Spreadbury I, Cenac N, Cattaruzza F, Hurlbut D, Vanner S, Bunnett N, Vergnolle N, Vanner S. Brain-gut interactions increase peripheral nociceptive signaling in mice with postinfectious irritable bowel syndrome. Gastroenterology 141: 2098-2108, 2011.
39. Jacobson K, McHugh K, Collins S. The mechanism of altered neural function in a rat model of acute colitis. Gastroenterology 112: 156-162, 1997.
40. Jawed H, Jamall S, Shah SU, Perveen K, Hanif F, Simjee SU. N-(2-hydroxy phenyl) acetamide produces profound inhibition of c-Fos protein and mRNA expression in the brain of adjuvant-induced arthritic rats. Mol Cell Biochem 387: 81-90, 2014.
41. Jones R, Lydeard S. Irritable bowel syndrome in the general population. BMJ 304: 87-90, 1992.
42. Kalischuk LD, Inglis GD, Buret AG. Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts. Gut Pathog 1: 2, 2009.
43. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, Malinen E, Apajalahti J, Palva A. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133: 24-33, 2007.
44. Keister DB. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77: 487-488, 1983.
45. Kellow JE, Phillips SF, Miller LJ, Zinsmeister AR. Dysmotility of the small intestine in irritable bowel syndrome. Gut 29: 1236-1243, 1988.
46. Khaldi S, Gargala G, Le Goff L, Parey S, Francois A, Fioramonti J, Ballet JJ, Dupont JP, Ducrotté P, Favennec L. Cryptosporidium parvum isolate-dependent postinfectious jejunal hypersensitivity and mast cell accumulation in an immunocompetent rat model. Infect Immun 77: 5163-5169, 2009.
47. Levecke B, Geldhof P, Claerebout E, Dorny P, Vercammen F, Cacciò SM, Vercruysse J, Geurden T. Molecular characterisation of Giardia duodenalis in captive non-human primates reveals mixed assemblage A and B infections and novel polymorphisms. Int J Parasitol 39: 1595-1601, 2009.
48. Levy D, Kainz V, Burstein R, Strassman AM. Mast cell degranulation distinctly activates trigemino-cervical and lumbosacral pain pathways and elicits widespread tactile pain hypersensitivity. Brain Behav Immun 26: 311-317, 2012.
49. Li E, Zhao A, Shea-Donohue T, Singer SM. Mast cell-mediated changes in smooth muscle contractility during mouse giardiasis. Infect Immun 75: 4514-4518, 2007.
50. Li WM, Suzuki A, Cui KM. Responses of blood pressure and renal sympathetic nerve activity to colorectal distension in anesthetized rats. J Physiol Sci 56: 153-156, 2006.
51. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol 10: 712-721, 2012.
52. Maia-Brigagão C, Morgado-Díaz JA, De Souza W. Giardia disrupts the arrangement of tight, adherens and desmosomal junction proteins of intestinal cells. Parasitol Int 61: 280-287, 2012.
53. Marshall JK, Thabane M, Borgaonkar MR, James C. Postinfectious irritable bowel syndrome after a food-borne outbreak of acute gastroenteritis attributed to a viral pathogen. Clin Gastroenterol Hepatol 5: 457-460, 2007.
54. Marshall JK, Thabane M, Garg AX, Clark WF, Moayyedi P, Collins SM, Walkerton Health Study Investigators. Eight year prognosis of postinfectious irritable bowel syndrome following waterborne bacterial dysentery. Gut 59: 605-611, 2010.
55. Marshall JK, Thabane M, Garg AX, Clark WF, Salvadori M, Collins SM, Walkerton Health Study Investigators. Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology 131: 445-450, 2006.
56. Martínez C, Vicario M, Ramos L, Lobo B, Mosquera JL, Alonso C, Sánchez A, Guilarte M, Antolín M, de Torres I, González-Castro AM, Pigrau M, Saperas E, Azpiroz F, Santos J. The jejunum of diarrheapredominant irritable bowel syndrome shows molecular alterations in the tight junction signaling pathway that are associated with mucosal pathobiology and clinical manifestations. Am J Gastroenterol 107: 736-746, 2012.
57. McLean PG, Picard C, Garcia-Villar R, Moré J, Fioramonti J, Buéno L. Effects of nematode infection on sensitivity to intestinal distension: role of tachykinin NK2 receptors. Eur J Pharmacol 337: 279-282, 1997.
58. Mearin F, Pérez-Oliveras M, Perelló A, Vinyet J, Ibañez A, Coderch J, Perona M. Dyspepsia and irritable bowel syndrome after a Salmonella gastroenteritis outbreak: one-year follow-up cohort study. Gastroenterology 129: 98-104, 2005.
59. Meleine M, Matricon J. Gender-related differences in irritable bowel syndrome: potential mechanisms of sex hormones. World J Gastroenterol 20: 6725-6743, 2014.
60. Mertz H, Naliboff B, Munakata J, Niazi N, Mayer EA. Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109: 40-52, 1995.
61. Morgan JI, Curran T. Inducible proto-oncogenes of the nervous system: their contribution to transcription factors and neuroplasticity. Prog Brain Res 86: 287-294, 1990.
62. O’Leary C, Quigley EM. Small bowel bacterial overgrowth, celiac disease, and IBS: what are the real associations? Am J Gastroenterol 98: 720-722, 2003.
63. Piche T, Barbara G, Aubert P, Bruley des Varannes S, Dainese R, Nano JL, Cremon C, Stanghellini V, De Giorgio R, Galmiche JP, Neunlist M. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 58: 196-201, 2009.
64. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105: 2420-2428, 2010.
65. Posserud I, Stotzer PO, Björnsson ES, Abrahamsson H, Simrén M. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Gut 56: 802-808, 2007.
66. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14: 125-132, 1973.
67. Romero-Calvo I, Ocón B, Martínez-Moya P, Suárez MD, Zarzuelo A, Martínez-Augustin O, de Medina FS. Reversible Ponceau staining as a loading control alternative to actin in Western blots. Anal Biochem 401: 318-320, 2010.
68. Roxström-Lindquist K, Palm D, Reiner D, Ringqvist E, Svärd SG. Giardia immunity—an update. Trends Parasitol 22: 26-31, 2006.
69. Saleh TM, Connell BJ, Allen GV. Visceral afferent activation-induced changes in sympathetic nerve activity and baroreflex sensitivity. Am J Physiol Regul Integr Comp Physiol 276: R1780-R1791, 1999.
70. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108, 2008.
71. Scott KG, Meddings JB, Kirk DR, Lees-Miller SP, Buret AG. Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 123: 1179-1190, 2002.
72. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev 90: 859-904, 2010.
73. Sohn W, Lee OY, Lee SP, Lee KN, Jun DW, Lee HL, Yoon BC, Choi HS, Sim J, Jang KS. Mast cell number, substance P and vasoactive intestinal peptide in irritable bowel syndrome with diarrhea. Scand J Gastroenterol 49: 43-51, 2014.
74. Sundin J, Rangel I, Kumawat AK, Hultgren-Hörnquist E, Brummer RJ. Aberrant mucosal lymphocyte number and subsets in the colon of post-infectious irritable bowel syndrome patients. Scand J Gastroenterol 49: 1068-1075, 2014.
75. Teoh DA, Kamieniecki D, Pang G, Buret AG. Giardia lamblia rearranges F-actin and α-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistance. J Parasitol 86: 800-806, 2000.
76. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther 26: 535-544, 2007.
77. Thabane M, Simunovic M, Akhtar-Danesh N, Garg AX, Clark WF, Collins SM, Salvadori M, Marshall JK. An outbreak of acute bacterial gastroenteritis is associated with an increased incidence of irritable bowel syndrome in children. Am J Gastroenterol 105: 933-939, 2010.
78. Walker MM, Talley NJ, Prabhakar M, Pennaneac’h CJ, Aro P, Ronkainen J, Storskrubb T, Harmsen WS, Zinsmeister AR, Agreus L. Duodenal mastocytosis, eosinophilia and intraepithelial lymphocytosis as possible disease markers in the irritable bowel syndrome and functional dyspepsia. Aliment Pharmacol Ther 29: 765-773, 2009.
79. Wang B, Glatzle J, Mueller MH, Kreis M, Enck P, Grundy D. Lipopolysaccharide-induced changes in mesenteric afferent sensitivity of rat jejunum in vitro: role of prostaglandins. Am J Physiol Gastrointest Liver Physiol 289: G254-G260, 2005.
80. Willot S, Gauthier C, Patey N, Faure C. Nerve growth factor content is increased in the rectal mucosa of children with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 24: 734-739, e347, 2012.
81. World Health Organization. Guidelines for Drinking-Water Quality — Volume 1: Recommendations (3rd ed., incorporating first and second addenda). Geneva: World Health Organization, 2008. http://www.who.int/water_sanitation_health/dwq/gdwq3/en/.
82. Zhang R, Zou N, Li J, Lv H, Wei J, Fang XC, Qian JM. Elevated expression of c-fos in central nervous system correlates with visceral hypersensitivity in irritable bowel syndrome (IBS): a new target for IBS treatment. Int J Colorectal Dis 26: 1035-1044, 2011.