Paneth cell ablation in the presence of Klebsiella pneumoniae induces necrotizing enterocolitis (NEC)-like injury in the small intestine of immature mice

DMM Disease Models and Mechanisms

Volumn 5, Issue 4, 2012, Pages 522-532

  Zhang, Chunxian ^a   Sherman, Michael P ^b   Prince, Lawrence S ^a   Bader, David ^a   Weitkamp, Jörn Hendrik ^a   Slaughter, James C ^a   McElroy, Steven J ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DITHIZONE;

ARTICLE; CELL DISRUPTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMATURITY; INFANT; INNATE IMMUNITY; INTESTINE INJURY; KLEBSIELLA PNEUMONIAE; MOUSE; NECROTIZING ENTEROCOLITIS; NONHUMAN; PANETH CELL; PATHOGENESIS; PERINATAL PERIOD; PRIORITY JOURNAL;

AGING; ANIMALS; CELL DIFFERENTIATION; CYTOPLASMIC GRANULES; DISEASE MODELS, ANIMAL; DITHIZONE; ENTERAL NUTRITION; ENTEROCOLITIS, NECROTIZING; HUMANS; INFANT, NEWBORN; INFLAMMATION; INTESTINE, SMALL; KLEBSIELLA PNEUMONIAE; MICE; PANETH CELLS; ZINC;

ANIMALIA; KLEBSIELLA PNEUMONIAE; MUS;

EID: 84863470791     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.009001     Document Type: Article

References (57)

1. Bajwa, N. M., Berner, M., Worley, S. and Pfister, R. E. (2011). Population based age stratified morbidities of premature infants in Switzerland. Swiss Med. Wkly 141, w13212.
2. Baker, S. J. and Reddy, E. P. (1998). Modulation of life and death by the TNF receptor superfamily. Oncogene 17, 3261-3270. (Pubitemid 29043978)
3. Barlow, B., Santulli, T. V., Heird, W. C., Pitt, J., Blanc, W. A. and Schullinger, J. N. (1974). An experimental study of acute neonatal enterocolitis-the importance of breast milk. J. Pediatr. Surg. 9, 587-595.
4. Beierle, E. A., Chen, M. K., Hartwich, J. E., Iyengar, M., Dai, W., Li, N., Demarco, V. and Neu, J. (2004). Artificial rearing of mouse pups: development of a mouse pup in a cup model. Pediatr. Res. 56, 250-255. (Pubitemid 38971820)
5. Bevins, C. L. and Salzman, N. H. (2011). Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat. Rev. Microbiol. 9, 356-368.
6. Bry, L., Falk, P., Huttner, K., Ouellette, A., Midtvedt, T. and Gordon, J. I. (1994). Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc. Natl. Acad. Sci. USA 91, 10335-10339. (Pubitemid 24328991)
7. Caplan, M. S. and Hsueh, W. (1990). Necrotizing enterocolitis: role of platelet activating factor, endotoxin, and tumor necrosis factor. J. Pediatr. 117, S47-S51. (Pubitemid 20219510)
8. Caplan, M. S. and MacKendrick, W. (1994). Inflammatory mediators and intestinal injury. Clin. Perinatol. 21, 235-246. (Pubitemid 24184711)
9. Coutinho, H. B., da Mota, H. C., Coutinho, V. B., Robalinho, T. I., Furtado, A. F., Walker, E., King, G., Mahida, Y. R., Sewell, H. F. and Wakelin, D. (1998). Absence of lysozyme (muramidase) in the intestinal Paneth cells of newborn infants with necrotising enterocolitis. J. Clin. Pathol. 51, 512-514. (Pubitemid 28375030)
10. Drobac, E., Durand, E., Laudenbach, V., Mantz, J. and Gallego, J. (2004). A simple method for short-term controlled anesthesia in newborn mice. Physiol. Behav. 82, 279-283. (Pubitemid 38981613)
11. Dvorak, B., McWilliam, D. L., Williams, C. S., Dominguez, J. A., Machen, N. W., McCuskey, R. S. and Philipps, A. F. (2000). Artificial formula induces precocious maturation of the small intestine of artificially reared suckling rats. J. Pediatr. Gastroenterol. Nutr. 31, 162-169. (Pubitemid 30618306)
12. Dvorak, B., Halpern, M. D., Holubec, H., Williams, C. S., McWilliam, D. L., Dominguez, J. A., Stepankova, R., Payne, C. M. and McCuskey, R. S. (2002). Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G156-G164. (Pubitemid 34650110)
13. Edde, L., Hipolito, R. B., Hwang, F. F., Headon, D. R., Shalwitz, R. A. and Sherman, M. P. (2001). Lactoferrin protects neonatal rats from gut-related systemic infection. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G1140-G1150.
14. Fitzgibbons, S. C., Ching, Y., Yu, D., Carpenter, J., Kenny, M., Weldon, C., Lillehei, C., Valim, C., Horbar, J. D. and Jaksic, T. (2009). Mortality of necrotizing enterocolitis expressed by birth weight categories. J. Pediatr. Surg. 44, 1072-1075; discussion 1075-1076.
15. Ford, H., Watkins, S., Reblock, K. and Rowe, M. (1997). The role of inflammatory cytokines and nitric oxide in the pathogenesis of necrotizing enterocolitis. J. Pediatr. Surg. 32, 275-282. (Pubitemid 27082170)
16. Frost, B. L., Jilling, T. and Caplan, M. S. (2008). The importance of pro-inflammatory signaling in neonatal necrotizing enterocolitis. Semin. Perinatol. 32, 100-106. (Pubitemid 351381163)
17. Ganz, T. (2000). Paneth cells-guardians of the gut cell hatchery. Nat. Immun. 1, 99-100.
18. Garabedian, E. M., Roberts, L. J., McNevin, M. S. and Gordon, J. I. (1997). Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J. Biol. Chem. 272, 23729-23740. (Pubitemid 27410949)
19. Grootjans, J., Hodin, C. M., de Haan, J. J., Derikx, J. P., Rouschop, K. M., Verheyen, F. K., van Dam, R. M., Dejong, C. H., Buurman, W. A. and Lenaerts, K. (2011). Level of activation of the unfolded protein response correlates with Paneth cell apoptosis in human small intestine exposed to ischemia/reperfusion. Gastroenterology 140, 529-539.
20. Halpern, M. D., Holubec, H., Dominguez, J. A., Williams, C. S., Meza, Y. G., McWilliam, D. L., Payne, C. M., McCuskey, R. S., Besselsen, D. G. and Dvorak, B. (2002). Up-regulation of IL-18 and IL-12 in the ileum of neonatal rats with necrotizing enterocolitis. Pediatr. Res. 51, 733-739. (Pubitemid 34547337)
21. Hambidge, K. M. and Krebs, N. F. (2007). Zinc deficiency: a special challenge. J. Nutr. 137, 1101-1105. (Pubitemid 46596920)
22. Hennig, B., Wang, Y., Ramasamy, S. and McClain, C. J. (1993). Zinc protects against tumor necrosis factor-induced disruption of porcine endothelial cell monolayer integrity. J. Nutr. 123, 1003-1009. (Pubitemid 23175935)
23. Henning, S. J. (1985). Ontogeny of enzymes in the small intestine. Annu. Rev. Physiol. 47, 231-245.
24. Hill, H. R., Hunt, C. E. and Matsen, J. M. (1974). Nosocomial colonization with Klebsiella, type 26, in a neonatal intensive-care unit associated with an outbreak of sepsis, meningitis, and necrotizing enterocolitis. J. Pediatr. 85, 415-419.
25. Hintz, S. R., Kendrick, D. E., Stoll, B. J., Vohr, B. R., Fanaroff, A. A., Donovan, E. F., Poole, W. K., Blakely, M. L., Wright, L. and Higgins, R. (2005). Neurodevelopmental and growth outcomes of extremely low birth weight infants after necrotizing enterocolitis. Pediatrics 115, 696-703. (Pubitemid 43373031)
26. Hirayama, K., Miyaji, K., Kawamura, S., Itoh, K., Takahashi, E. and Mitsuoka, T. (1995). Development of intestinal flora of human-flora-associated (HFA) mice in the intestine of their offspring. Exp. Anim. 44, 219-222.
27. Jilling, T., Simon, D., Lu, J., Meng, F. J., Li, D., Schy, R., Thomson, R. B., Soliman, A., Arditi, M. and Caplan, M. S. (2006). The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J. Immunol. 177, 3273-3282. (Pubitemid 44277847)
28. Kliegman, R. M. and Fanaroff, A. A. (1984). Necrotizing enterocolitis. N. Engl. J. Med. 310, 1093-1103. (Pubitemid 14131503)
29. Leaphart, C. L., Cavallo, J., Gribar, S. C., Cetin, S., Li, J., Branca, M. F., Dubowski, T. D., Sodhi, C. P. and Hackam, D. J. (2007). A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J. Immunol. 179, 4808-4820.
30. Lee, A. and Gemmell, E. (1972). Changes in the mouse intestinal microflora during weaning: role of volatile fatty acids. Infect. Immun. 5, 1-7.
31. Lee, A., Gordon, J., Lee, C. J. and Dubos, R. (1971). The mouse intestinal microflora with emphasis on the strict anaerobes. J. Exp. Med. 133, 339-352.
32. Lin, P. W., Nasr, T. R. and Stoll, B. J. (2008). Necrotizing enterocolitis: recent scientific advances in pathophysiology and prevention. Semin. Perinatol. 32, 70-82. (Pubitemid 351381166)
33. Lucas, A. and Cole, T. J. (1990). Breast milk and neonatal necrotising enterocolitis. Lancet 336, 1519-1523.
34. Maheshwari, A., Kelly, D. R., Nicola, T., Ambalavanan, N., Jain, S. K., Murphy-Ullrich, J., Athar, M., Shimamura, M., Bhandari, V., Aprahamian, C. et al. (2011). TGF-beta2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 140, 242-253.
35. Mallow, E. B., Harris, A., Salzman, N., Russell, J. P., DeBerardinis, R. J., Ruchelli, E. and Bevins, C. L. (1996). Human enteric defensins. Gene structure and developmental expression. J. Biol. Chem. 271, 4038-4045.
36. McElroy, S. J. and Weitkamp, J. H. (2011). Innate immunity in the small intestine of the preterm infant. NeoReviews 12, 517-526.
37. McElroy, S. J., Frey, M. R., Yan, F., Edelblum, K. L., Goettel, J. A., John, S. and Polk, D. B. (2008). Tumor necrosis factor inhibits ligand-stimulated EGF receptor activation through a TNF receptor 1-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 2, G285-G293.
38. McElroy, S. J., Prince, L. S., Weitkamp, J. H., Reese, J., Slaughter, J. C. and Polk, D. B. (2011). Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: a potential role in neonatal necrotizing enterocolitis. Am J. Physiol. Gastrointest. Liver Physiol. 4, G656-G666.
39. Mizrahi, A., Barlow, O., Berdon, W., Blanc, W. A. and Silverman, W. A. (1965). Necrotizing enterocolitis in premature infants. J. Pediatr. 66, 697-705.
40. Montgomery, R. K., Mulberg, A. E. and Grand, R. J. (1999). Development of the human gastrointestinal tract: twenty years of progress. Gastroenterology 116, 702-731. (Pubitemid 29106779)
41. Moxey, P. C. (1978). Is the human colon an endocrine organ? Gastroenterology 75, 147-149.
42. Moxey, P. C. and Trier, J. S. (1978). Specialized cell types in the human fetal small intestine. Anat. Rec. 191, 269-285. (Pubitemid 8362054)
43. Musemeche, C., Caplan, M., Hsueh, W., Sun, X. and Kelly, A. (1991). Experimental necrotizing enterocolitis: the role of polymorphonuclear neutrophils. J. Pediatr. Surg. 26, 1047-1049; discussion 1049-1050.
44. Nadler, E. P., Stanford, A., Zhang, X. R., Schall, L. C., Alber, S. M., Watkins, S. C. and Ford, H. R. (2001). Intestinal cytokine gene expression in infants with acute necrotizing enterocolitis: interleukin-11 mRNA expression inversely correlates with extent of disease. J. Pediatr. Surg. 36, 1122-1129. (Pubitemid 32705688)
45. Nanthakumar, N. N., Fusunyan, R. D., Sanderson, I. and Walker, W. A. (2000). Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis. Proc. Natl. Acad. Sci. USA 97, 6043-6048. (Pubitemid 30367520)
46. Ouellette, A. J. (2010). Paneth cells and innate mucosal immunity. Curr. Opin. Gastroenterol. 26, 547-553.
47. Petty, J. K. and Ziegler, M. M. (2005). Operative strategies for necrotizing enterocolitis: the prevention and treatment of short-bowel syndrome. Semin. Pediatr. Surg. 14, 191-198. (Pubitemid 41111606)
48. Puiman, P. J., Burger-Van Paassen, N., Schaart, M. W., De Bruijn, A. C., De Krijger, R. R., Tibboel, D., Van Goudoever, J. B. and Renes, I. B. (2011). Paneth cell hyperplasia and metaplasia in necrotizing enterocolitis. Pediatr. Res. 69, 217-223.
49. Salzman, N. H., Underwood, M. A. and Bevins, C. L. (2007). Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin. Immunol. 19, 70-83. (Pubitemid 46824070)
50. Sanderson, I. R. and Walker, A. (1999). Development of the Gastrointestinal Tract, pp. 1- 10, 147-159. Hamilton, ON: B C Decker.
51. Sato, T., van, Es, J. H., Snippert, H. J., Stange, D. E., Vries, R. G., van den Born, M., Barker, N., Shroyer, N. F., van de Wetering, M. and Clevers, H. (2011). Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418.
52. Sawada, M., Takahashi, K., Sawada, S. and Midorikawa, O. (1991). Selective killing of Paneth cells by intravenous administration of dithizone in rats. Int. J. Exp. Pathol. 72, 407-421.
53. Seno, H., Sawada, M., Fukuzawa, H., Morita, Y., Takaishi, S., Hiai, H. and Chiba, T. (2001). Enhanced expression of transforming growth factor (TGF) -alpha precursor and TGF-beta1 during Paneth cell regeneration. Dig. Dis. Sci. 46, 1004-1010. (Pubitemid 32375028)
54. Sherman, M. P., Bennett, S. H., Hwang, F. F., Sherman, J. and Bevins, C. L. (2005). Paneth cells and antibacterial host defense in neonatal small intestine. Infect. Immun. 73, 6143-6146. (Pubitemid 41193054)
55. Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D. et al. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144.
56. Waage, A., Brandtzaeg, P., Halstensen, A., Kierulf, P. and Espevik, T. (1989). The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J. Exp. Med. 169, 333-338. (Pubitemid 19035565)
57. Yan, F., Cao, H., Cover, T. L., Whitehead, R., Washington, M. K. and Polk, D. B. (2007). Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132, 562-575. (Pubitemid 46274659)