Helicobacter hepaticus increases intestinal injury in a rat model of necrotizing enterocolitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 305, Issue 8, 2013, Pages

  Dvorak, Katerina ^a   Coursodon Boyiddle, Christine F ^a   Snarrenberg, Chelsea L ^a   Kananurak, Anchasa ^b   Underwood, Mark A ^b   Dvorak, Bohuslav ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autophagy; Cytokines; Enteral bacteria; Mucosal inflammation

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPHYXIA; AUTOPHAGY; BACTERIAL COLONIZATION; COLD STRESS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HELICOBACTER HEPATICUS; HELICOBACTER HEPATICUS INFECTION; HELICOBACTER INFECTION; INCIDENCE; INTESTINE INJURY; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AUTOPHAGY; CYTOKINES; ENTERAL BACTERIA; MUCOSAL INFLAMMATION;

ANIMALS; AUTOPHAGY; CYTOKINES; ENTEROCOLITIS, NECROTIZING; FEMALE; GENE EXPRESSION REGULATION; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; ILEUM; INFLAMMATION; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA, BACTERIAL;

EID: 84885617693     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00483.2012     Document Type: Article

References (60)

1. Afrazi A, Sodhi CP, Richardson W, Neal M, Good M, Siggers R, Hackam DJ. New insights into the pathogenesis and treatment of necrotizing enterocolitis: Toll-like receptors and beyond. Pediatr Res 69: 183-188, 2011.
2. Battles JK, Williamson JC, Pike KM, Gorelick PL, Ward JM, Gonda MA. Diagnostic assay for Helicobacter hepaticus based on nucleotide sequence of its 16S rRNA gene. J Clin Microbiol 33: 1344-1347, 1995.
3. Caplan MS, Simon D, Jilling T. The role of PAF, TLR, and the inflammatory response in neonatal necrotizing enterocolitis. Semin Pediatr Surg 14: 145-151, 2005.
4. Chichlowski M, Hale LP. Effects of Helicobacter infection on research: the case for eradication of Helicobacter from rodent research colonies. Comp Med 59: 10-17, 2009.
5. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, Dvorak K, Boitano SA, Dvorak B. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol 291: G938-G949, 2006.
6. Claud EC, Walker WA. Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15: 1398-1403, 2001.
7. Coursodon-Boyiddle CF, Snarrenberg CL, Adkins-Rieck CK, Bassaganya- Riera J, Hontecillas R, Lawrence P, Brenna JT, Jouni ZE, Dvorak B. Pomegranate seed oil reduces intestinal damage in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 303: G744-G751, 2012.
8. De Plaen IG, Liu SX, Tian R, Neequaye I, May MJ, Han XB, Hsueh W, Jilling T, Lu J, Caplan MS. Inhibition of nuclear factor-kappaB ameliorates bowel injury and prolongs survival in a neonatal rat model of necrotizing enterocolitis. Pediatr Res 61: 716-721, 2007.
9. Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5: 527-549, 2009.
10. Drazenovich NL, Franklin CL, Livingston RS, Besselsen DG. Detection of rodent Helicobacter spp. by use of fluorogenic nuclease polymerase chain reaction assays. Comp Med 52: 347-353, 2002.
11. Dvorak B, Halpern MD, Holubec H, Dvorakova K, Dominguez JA, Williams CS, Meza YG, Kozakova H, McCuskey RS. Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res 53: 426-433, 2003.
12. Dvorak B, Halpern MD, Holubec H, Williams CS, McWilliam DL, Dominguez JA, Stepankova R, Payne CM, McCuskey RS. Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am J Physiol Gastrointest Liver Physiol 282: G156-G164, 2002.
13. Dvorak B, McWilliam DL, Williams CS, Dominguez JA, Machen NW, McCuskey RS, Philipps AF. Artificial formula induces precocious maturation of the small intestine of artificially reared suckling rats. J Pediatr Gastroenterol Nutr 31: 162-169, 2000.
14. Edelson MB, Bagwell CE, Rozycki HJ. Circulating pro- and counterinflammatory cytokine levels and severity in necrotizing enterocolitis. Pediatrics 103: 766-771, 1999.
15. Feng S, Ku K, Hodzic E, Lorenzana E, Freet K, Barthold SW. Differential detection of five mouse-infecting helicobacter species by multiplex PCR. Clin Diagn Lab Immunol 12: 531-536, 2005.
16. Fox JG, Ge Z, Whary MT, Erdman SE, Horwitz BH. Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol 4: 22-30, 2011.
17. Grave GD, Nelson SA, Walker WA, Moss RL, Dvorak B, Hamilton FA, Higgins R, Raju TN. New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr Res 62: 510-514, 2007.
18. Gribar SC, Anand RJ, Sodhi CP, Hackam DJ. The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J Leukoc Biol 83: 493-498, 2008.
19. 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 104: 1829-1834, 2007.
20. Halpern MD, Clark JA, Saunders TA, Doelle SM, Hosseini DM, Stagner AM, Dvorak B. Reduction of experimental necrotizing enterocolitis with anti-TNF-_. Am J Physiol Gastrointest Liver Physiol 290: G757-G764, 2006.
21. Halpern MD, Holubec H, Saunders TA, Dvorak K, Clark JA, Doelle SM, Ballatori N, Dvorak B. Bile acids induce ileal damage during experimental necrotizing enterocolitis. Gastroenterology 130: 359-372, 2006.
22. Hansen R, Thomson JM, Fox JG, El-Omar EM, Hold GL. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol Med Microbiol 61: 1-14, 2011.
23. Harris J. Autophagy and cytokines. Cytokine 56: 140-144, 2011.
24. Hoffman SM, Wang H, Pope MR, Fleming SD. Helicobacter infection alters MyD88 and Trif signalling in response to intestinal ischaemiareperfusion. Exp Physiol 96: 104-113, 2011.
25. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 177: 3273-3282, 2006.
26. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, Yajima M, Dvorak B. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G940-G949, 2009.
27. Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B. Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 299: G1118-G1127, 2010.
28. Kullberg MC, Jankovic D, Feng CG, Hue S, Gorelick PL, McKenzie BS, Cua DJ, Powrie F, Cheever AW, Maloy KJ, Sher A. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 203: 2485-2494, 2006.
29. Le Mandat Schultz A, Bonnard A, Barreau F, Aigrain Y, Pierre-Louis C, Berrebi D, Peuchmaur M. Expression of TLR-2, TLR-4, NOD2 and pNF-kappaB in a neonatal rat model of necrotizing enterocolitis. PLoS ONE 2: e1102, 2007.
30. Leaphart CL, Cavallo J, Gribar SC, Cetin S, Li J, Branca MF, Dubowski TD, Sodhi CP, Hackam DJ. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J Immunol 179: 4808-4820, 2007.
31. Liu Y, Zhu L, Fatheree NY, Liu X, Pacheco SE, Tatevian N, Rhoads JM. Changes in intestinal Toll-like receptors and cytokines precede histological injury in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G442-G450, 2009.
32. Maheshwari A, Kelly DR, Nicola T, Ambalavanan N, Jain SK, Murphy- Ullrich J, Athar M, Shimamura M, Bhandari V, Aprahamian C, Dimmitt RA, Serra R, Ohls RK. TGF-beta2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 140: 242-253, 2011.
33. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, Neu J. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 6: e20647, 2011.
34. Malaty HM. Epidemiology of Helicobacter pylori infection. Best Pract Res Clin Gastroenterol 21: 205-214, 2007.
35. Maloy KJ, Kullberg MC. IL-23 and Th17 cytokines in intestinal homeostasis. Mucosal Immunol 1: 339-349, 2008.
36. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474: 298-306, 2011.
37. Matharu KS, Mizoguchi E, Cotoner CA, Nguyen DD, Mingle B, Iweala OI, McBee ME, Stefka AT, Prioult G, Haigis KM, Bhan AK, Snapper SB, Murakami H, Schauer DB, Reinecker HC, Mizoguchi A, Nagler CR. Toll-like receptor 4-mediated regulation of spontaneous Helicobacter-dependent colitis in IL-10-deficient mice. Gastroenterology 137: 1380-1390, 2009.
38. Maynard AA, Dvorak K, Khailova L, Dobrenen H, Arganbright KM, Halpern MD, Kurundkar AR, Maheshwari A, Dvorak B. Epidermal growth factor reduces autophagy in intestinal epithelium and in the rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 299: G614-G622, 2010.
39. McElroy SJ, Weitkamp JH. Innate immunity in the small intestine of the preterm infant. Neoreviews 12: e517-e526, 2011.
40. Morecroft JA, Spitz L, Hamilton PA, Holmes SJ. Plasma cytokine levels in necrotizing enterocolitis. Acta Paediatr Suppl 396: 18-20, 1994.
41. Morrison PJ, Ballantyne SJ, Kullberg MC. Interleukin-23 and T helper 17-type responses in intestinal inflammation: from cytokines to T-cell plasticity. Immunology 133: 397-408, 2011.
42. Navabi N, Johansson ME, Raghavan S, Linden SK. Helicobacter pylori infection impairs the mucin production rate and turnover in the murine gastric mucosa. Infect Immun 81: 829-837, 2013.
43. Neal MD, Sodhi CP, Dyer M, Craig BT, Good M, Jia H, Yazji I, Afrazi A, Richardson WM, Beer-Stolz D, Ma C, Prindle T, Grant Z, Branca MF, Ozolek J, Hackam DJ. A critical role for TLR4 induction of autophagy in the regulation of enterocyte migration and the pathogenesis of necrotizing enterocolitis. J Immunol 190: 3541-3551, 2013.
44. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 364: 255-264, 2011.
45. Normann E, Fahlen A, Engstrand L, Lilja HE. Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis. Acta Paediatr 102: 129-136, 2013.
46. Ran-Ressler RR, Khailova L, Arganbright KM, Adkins-Rieck CK, Jouni ZE, Koren O, Ley RE, Brenna JT, Dvorak B. Branched chain Fatty acids reduce the incidence of necrotizing enterocolitis and alter gastrointestinal microbial ecology in a neonatal rat model. PLoS One 6: e29032, 2011.
47. Sakiyama T, Musch MW, Ropeleski MJ, Tsubouchi H, Chang EB. Glutamine increases autophagy under Basal and stressed conditions in intestinal epithelial cells. Gastroenterology 136: 924-932, 2009.
48. Scharl M, Rogler G. Inflammatory bowel disease: dysfunction of autophagy? Dig Dis 30, Suppl 3: 12-19, 2012.
49. Sodhi CP, Neal MD, Siggers R, Sho S, Ma C, Branca MF, Prindle T Jr, Russo AM, Afrazi A, Good M, Brower-Sinning R, Firek B, Morowitz MJ, Ozolek JA, Gittes GK, Billiar TR, Hackam DJ. Intestinal epithelial toll-like receptor 4 regulates goblet cell development and is required for necrotizing enterocolitis in mice. Gastroenterology 143: 708-718, 2012.
50. Solnick JV, Franceschi F, Roccarina D, Gasbarrini A. Extragastric manifestations of Helicobacter pylori infection-other Helicobacter species. Helicobacter 11, Suppl 1: 46-51, 2006.
51. Solnick JV, Schauer DB. Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin Microbiol Rev 14: 59-97, 2001.
52. Sterzenbach T, Lee SK, Brenneke B, von Goetz F, Schauer DB, Fox JG, Suerbaum S, Josenhans C. Inhibitory effect of enterohepatic Helicobacter hepaticus on innate immune responses of mouse intestinal epithelial cells. Infect Immun 75: 2717-2728, 2007.
53. Stewart CJ, Marrs EC, Magorrian S, Nelson A, Lanyon C, Perry JD, Embleton ND, Cummings SP, Berrington JE. The preterm gut microbiota: changes associated with necrotizing enterocolitis and infection. Acta Paediatr 101: 1121-1127, 2012.
54. Suemori S, Lynch-Devaney K, Podolsky DK. Identification and characterization of rat intestinal trefoil factor: tissue- and cell-specific member of the trefoil protein family. Proc Natl Acad Sci USA 88: 11017-11021, 1991.
55. Taylor NS, Xu S, Nambiar P, Dewhirst FE, Fox JG. Enterohepatic Helicobacter species are prevalent in mice from commercial and academic institutions in Asia, Europe, and North America. J Clin Microbiol 45: 2166-2172, 2007.
56. Turner S, Pryer KM, Miao VP, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46: 327-338, 1999.
57. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, Antonopoulos DA, Chang EB, Claud EC. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 3: 944-954, 2009.
58. Wu J, Dang Y, Su W, Liu C, Ma H, Shan Y, Pei Y, Wan B, Guo J, Yu L. Molecular cloning and characterization of rat LC3A and LC3B-two novel markers of autophagosome. Biochem Biophys Res Commun 339: 437-442, 2006.
59. Young VB, Knox KA, Schauer DB. Cytolethal distending toxin sequence and activity in the enterohepatic pathogen Helicobacter hepaticus. Infect Immun 68: 184-191, 2000.
60. Yu Y, Shiou SR, Guo Y, Lu L, Westerhoff M, Sun J, Petrof EO, Claud EC. Erythropoietin protects epithelial cells from excessive autophagy and apoptosis in experimental neonatal necrotizing enterocolitis. PLoS One 8: e69620, 2013.