Microbial exposure early in life regulates airway inflammation in mice after infection with Streptococcus pneumoniae with enhancement of local resistance

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 1, 2010, Pages

  Yasuda, Yasuki ^a   Matsumura, Yoko ^a   Kasahara, Kazuki ^a   Ouji, Noriko ^a   Sugiura, Shigeki ^a   Mikasa, Keiichi ^a   Kita, Eiji ^a  

^a NARA MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Airway innate resistance; Hygiene hypothesis; Pneumococcal pneumonia; Regulation of acute inflammation; TLR tolerance

Indexed keywords

GAMMA INTERFERON; GELATINASE B; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPOSURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; SURVIVAL TIME; TH1 CELL; UPREGULATION;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL MOVEMENT; CHEMOKINES; COLONY COUNT, MICROBIAL; ENZYME ACTIVATION; IMMUNITY, INNATE; IMMUNOGLOBULIN A; LUNG; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; NEUTROPHILS; PNEUMOCOCCAL INFECTIONS; PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TOLL-LIKE RECEPTORS;

EID: 73549107627     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00193.2009     Document Type: Article

References (64)

1. Abreu MT, Arnold ET, Thomas LS, Gonsky R, Zhou Y, Hu B, Arditi M.TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 277: 20431-20437, 2002.
2. Allen BL, Katz B, Hook M.Streptococcus anginosus adheres to vascular endothelium basement membrane and purified extracellular matrix proteins. Microb Pathog 32: 191-204, 2002.
3. Atkinson JJ, Senior RM.Matrix metalloproteinase-9 in lung remodeling. Am J Respir Cell Mol Biol 28: 12-24, 2003.
4. Auten RL, Whorton MH, Mason NS.Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol 26: 391-397, 2002.
5. Balckwill F, Mantovani A.Inflammation and cancer: back to Virchow? Lancet 357: 539-545, 2001.
6. Ball TM, Castro-Rodriguez JA, Griffith KA, Holberg CJ, Martinez FD, Wright AL.Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med 343: 538-543, 2000.
7. Bardin PG, Fraenkel DJ, Sanderson G, Lampe F, Holgate ST.Lower airways inflammatory response during rhinovirus colds. Int Arch Allergy Immunol 107: 127-129, 1995.
8. Braman SS.The global burden of asthma. Chest 130: 4S-12S, 2006.
9. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, Maisch S, Carr D, Gerlach F, Bufe A, Lauener RP, Schierl R, Renz H, Nowak D, von Mutius E; Allergy and Endotoxin Study Team.Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 347: 869-877, 2002.
10. Cebra JJ.Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69: 1046S-1051S, 1999.
11. Celedon JC, Wright RJ, Litonjua AA, Sredl D, Ryan L, Weiss ST, Gold DR.Day care attendance in early life, maternal history of asthma, and asthma at the age of 6 years. Am J Respir Crit Care Med 167: 1239-1243, 2003.
12. Cong Y, Weaver CT, Lazenby A, Elson CO.Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J Immunol 169: 6112-6119, 2002.
13. Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, Ren T, Cody MJ, Michalek SM, Rice NR, Vogel SN.Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-κB signaling pathway components. J Immunol 170: 508-519, 2003.
14. Dockrell DH, Marriott HM, Prince LR, Ridger VC, Ince PG, Hellewell PG, Whyte MK.Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J Immunol 171: 5380-5388, 2003.
15. Ferry G, Lonchampt M, Pennel L, de Nanteuil G, Canet E, Tucker GC.Activation of MMP-9 by neutrophil elastase in an in vivo model of acute lung injury. FEBS Lett 402: 111-115, 1997.
16. Gajewski TF, Fitch FW.Anti-proliferative effect of IFN-gamma in immune regulation. I: IFN-gamma inhibits the proliferation of Th2 but not Th1 murine helper T lymphocyte clones. J Immunol 140: 4245-4252, 1988.
17. Haro H, Crawford HC, Fingleton B, MacDougall JR, Shinomiya K, Spengler DM, Matrisian LM.Matrisian, matrix metalloproteinase-3-dependent generation of a macrophage chemoattractant in a model of herniated disc resorption. J Clin Invest 105: 133-141, 2000.
18. Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA.Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 121: 1005-1014, 1995.
19. Hayashi M, Schellenberg RR, Tsang S, Roberts CR.Matrix metalloproteinase-9 in myeloid cells: implications for allergic inflammation. Int Arch Allergy Immunol 118: 429-432, 1999.
20. Heflin AC, Brigham KL.Prevention by granulocyte depletion of increased vascular permeability of sheep lung following endotoxemia. J Clin Invest 68: 1253-1260, 1981.
21. Heritage PL, Underdown BJ, Arsenault AL, Snider DP, McDermott MR.Comparison of murine nasal-associated lymphoid tissue and Peyer's patches. Am J Respir Crit Care Med 156: 1256-1262, 1997.
22. Iwasaki A, Medzhitov R.Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995, 2004.
23. Jawad A, Hawkey PM, Heritage J, Snelling AM.Description of Leeds Acinetobacter Medium, a new selective and differential medium for isolation of clinically important Acinetobacter spp., and comparison with Herellea agar and Holton's agar. J Clin Microbiol 32: 2353-2358, 1994.
24. Johnston SL, Pattemore PK, Sanderson G, Campbell MJ, Josephs LK, Cunningham A, Robinson BS, Myint SH, Ward ME, Tyrrell DA, Holgate ST.The relationship between upper respiratory infections and hospital admissions for asthma: a time-trend analysis. Am J Respir Crit Care Med 154: 654-660, 1996.
25. Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, Andrew PW.Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 68: 492-501, 2000.
26. Kelly D, King T, Aminov R.Importance of microbial colonization of the gut in early life to the development of immunity. Mutat Res 622: 58-69, 2007.
27. Kline JN.Eat dirt: CpG DNA and immunomodulation of asthma. Proc Am Thorac Soc 4: 283-288, 2007.
28. Knapp S, Leemans JC, Florquin S, Branger J, Maris NA, Pater J, van Rooijen N, van der Poll T.Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am J Respir Crit Care Med 167: 171-179, 2003.
29. Lacroix-Lamandé S, Mancassola R, Naciri M, Laurent F.Role of gamma interferon in chemokine expression in the ileum of mice and in a murine intestinal epithelial cell line after Cryptosporidium parvum infection. Infect Immun 70: 2090-2099, 2002.
30. Leco KJ, Khokha R, Pavloff N, Hawkes SP, Edwards DR.Tissue inhibitor of metalloproteinases-3 (TIMP-3) is an extracellular matrix-associated protein with a distinctive pattern of expression in mouse cells and tissues. J Biol Chem 269: 9352-9360, 1994.
31. Lyons S, Wang L, Casanova JE, Sitaraman SV, Merlin D, Gewirtz AT.Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 117: 5771-5780, 2004.
32. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, Thompson CM, Kurt-Jones E, Paton JC, Wessels MR, Golenbock DT. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci USA 100: 1966-1971, 2003.
33. Marler L, Siders J, Wolters L, Pettigrew Y, Skitt B, Allen S.Comparison of five cultural procedures for isolation of Clostridium difficile from stools. J Clin Microbiol 30: 514-516, 1992.
34. Matricardi PM, Bonini S.High microbial turnover rate preventing atopy: a solution to inconsistencies impinging on the hygiene hypothesis? Clin Exp Allergy 30: 1506-1510, 2000.
35. Melmed G, Thomas LS, Lee N, Tesfay SY, Lukasek K, Michelsen KS, Zhou Y, Hu B, Arditi M, Abreu MT.Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J Immunol 170: 1406-1415, 2003.
36. Mulligan MS, Till GO, Smith CW, Anderson DC, Miyasaka M, Tamatani T, Todd RF, Issekutz TB, Ward PA.Role of leukocyte adhesion molecules in lung and dermal vascular injury after thermal trauma of skin. Am J Pathol 144: 1008-1015, 1994.
37. Murphy G, Docherty AJ.The matrix metalloproteinases and their inhibitors. Am J Respir Cell Mol Biol 7: 120-125, 1992.
38. von Mutius E, Martinez FD, Fritzsch C, Nicolai T, Reitmeir P, Thiemann HH.Skin test reactivity and number of siblings. BMJ 308: 692-695, 1994.
39. Naik S, Kelly EJ, Meijer L, Pettersson S, Sanderson IR.Absence of Toll-like receptor 4 explains endotoxin hyporesponsiveness in human intestinal epithelium. J Pediatr Gastroenterol Nutr 32: 449-453, 2001.
40. Newman SL, Tucci MA.Regulation of human monocyte/macrophage function by extracellular matrix. Adherence of monocytes to collagen matrices phagocytosis of opsonized bacteria. J Clin Invest 86: 703-714, 1990.
41. Nicholson KG, Kent J, Ireland DC.Respiratory viruses and exacerbations of asthma in adults. BMJ 307: 982-986, 1993.
42. Oliver GW, Leferson JD, Stetler-Stevenson WG, Kleiner DE.Quantitative reverse zymography: analysis of picogram amounts of metalloproteinase inhibitors using gelatinase A and B reverse zymograms. Anal Biochem 244: 161-166, 1997.
43. Parronchi P, De Carli M, Manetti R, Simonelli C, Sampognaro S, Piccinni MP, Macchia D, Maggi E, Del Prete G, Romagnani S.IL-4 and IFN (α and γ) exert opposite regulatory effects on the development of cytolytic potential by Th1 or Th2 human T cell clones. J Immunol 149: 2977-2983, 1992.
44. Patti JM, Allen BL, McGavin MJ, Höök M.MSCRAMM-mediated adherence of microorganisms to host tissues. Ann Rev Microbiol 48: 585-617, 1994.
45. Perry JA, Olver CS, Burnett RC, Avery AC.Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation. J Immunol 174: 5921-5925, 2005.
46. Renz H, Herzb U.The bidirectional capacity of bacterial antigens to modulate allergy and asthma. Eur Respir J 19: 158-171, 2002.
47. Riedler J, Braun-Fahrlander C, Eder W, Schreuer M, Waser M, Maisch S, Carr D, Schierl R, Nowak D, von Mutius E.Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 358: 1129-1133, 2001.
48. Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J Immunol 168: 1813-1822, 2002.
49. Sato S, Takeuchi O, Fujitav T, Tomizawa H, Takeda K, Akira S.A variety of microbial components induce tolerance to lipopolysaccharide by differentially affecting MyD88-dependent and -independent pathways. Int Immunol 14: 783-791, 2002.
50. Schroder NW, Morath S, Alexander C, Hamann L, Hartung T, Zahringer U, Gobel UB, Weber JR, Schumann RR.Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem l278: 15587-15594, 2003.
51. Shingu M, Nagai Y, Isayama T, Naono T, Nobunaga M, Nagai Y.The effects of cytokines on metalloproteinase inhibitors (TIMP) and collagenase production by human chondrocytes and TIMP production by synovial cells and endothelial cells. Clin Exp Immunol 94: 145-149, 1993.
52. Simpson JM, Martineau B, Jones WE, Ballam JM, Mackie RI. Characterization of fecal bacterial populations in canines: effects of age, breed and dietary fiber. Microb Ecol 44: 186-197, 2002.
53. Steege JC, Buurman WA, Forget PP.The neonatal development of intraepithelial and lamina propria lymphocytes in the murine small intestine. Dev Immunol 5: 121-128, 1997.
54. Strachan DP.Hay fever, hygiene, and household size. BMJ 299: 1259-1260, 1989.
55. Tang WW, Yi ES, Remick DG, Wittwer A, Yin S, Qi M, Ulich TR. Intratracheal injection of endotoxin and cytokines. IX: Contribution of CD11a/ICAM-1 to neutrophil emigration. Am J Physiol Lung Cell Mol Physiol 269: L653-L659, 1995.
56. Taylor JL, Hattle JM, Dreitz SA, Troudt JM, Izzo LS, Basaraba RJ, Orme IM, Matrisian LM, Izzo AA.Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 74: 6135-6144, 2006.
57. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP.Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 289: L322-L328, 2005.
58. Vollaard EJ, Clasener HA.Colonization resistance. Antimicrob Agents Chemother 38: 409-414, 1994.
59. van der Waai D, Berghuis JM, van der Wees JECL.Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg 69: 405-411, 1971.
60. Wang Z, Zheng T, Zhu Z, Homer RJ, Riese RJ, Chapman HA Jr, Shapiro SD, Elias JA.Interferon γ induction of pulmonary emphysema in the adult murine lung. J Exp Med 192: 1587-1600, 2000.
61. Wysocka M, Robertson S, Riemann H, Caamano J, Hunter CA, Mackiewicz A, Montaner LJ, Trinchieri G, Karp CL.IL-12 suppression during experimental endotoxin tolerance: dendritic cell loss and macrophage hyporesponsiveness. J Immunol 166: 7504-7513, 2001.
62. Yasuda Y, Kasahara K, Mizuno F, Nishi K, Mikasa K, Kita E. Roxithromycin favorably modifies the initial phase of resistance against infection with macrolide-resistant Streptococcus pneumoniae in a murine pneumonia model. Antimicrob Agents Chemother 51: 1741-1752, 2007.
63. Yazdanbakhsh M, Kremsner PG, van Ree R.Allergy, parasites, and the hygiene hypothesis. Science 296: 490-494, 2002.
64. Yeo SJ, Yoon GJ, Hong SC, Yi AK.CpG DNA induces self and cross-hyporesponsiveness of RAW264.7 cells in response to CpG DNA and lipopolysaccharide: alterations in IL-1 receptor-associated kinase expression. J Immunol 170: 1052-1061, 2003.