Mycoplasma pneumoniae CARDS toxin induces pulmonary eosinophilic and lymphocytic inflammation

American Journal of Respiratory Cell and Molecular Biology

Volumn 46, Issue 6, 2012, Pages 815-822

  Medina, Jorge L ^a   Coalson, Jacqueline J ^a   Brooks, Edward G ^b   Winter, Vicki T ^a   Chaparro, Adriana ^a   Principe, Molly F R ^b   Kannan, Thirumalai R ^a   Baseman, Joel B ^a   Dube, Peter H ^a  

^a University of Texas Health Science Center   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Asthma; Eosinophilia; Mycoplasma pneumoniae; rCARDS toxin; T cell

Indexed keywords

BACTERIAL TOXIN; CD4 ANTIGEN; INTERLEUKIN 13; INTERLEUKIN 4; MACROPHAGE DERIVED CHEMOKINE; MAJOR BASIC PROTEIN; MESSENGER RNA; MUCIN; MUCIN 5AC; RECOMBINANT COMMUNITY ACQUIRED RESPIRATORY DISTRESS SYNDROME TOXIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

ALLERGIC DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; B LYMPHOCYTE; BRONCHUS HYPERREACTIVITY; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE EXACERBATION; GENE EXPRESSION; HISTOPATHOLOGY; LUNG COMPLIANCE; LUNG FUNCTION; LUNG RESISTANCE; MORBIDITY; MOUSE; MYCOPLASMA PNEUMONIA; MYCOPLASMA PNEUMONIAE; NONHUMAN; PULMONARY EOSINOPHILIC AND LYMPHOCYTIC INFLAMMATION; RESPIRATORY TRACT INFLAMMATION; T LYMPHOCYTE; TH2 CELL; WHEEZING;

ANIMALS; BACTERIAL TOXINS; BRONCHOALVEOLAR LAVAGE FLUID; ENZYME-LINKED IMMUNOSORBENT ASSAY; EOSINOPHILS; FLOW CYTOMETRY; LUNG; LYMPHOCYTES; MICE; MYCOPLASMA PNEUMONIAE; REAL-TIME POLYMERASE CHAIN REACTION;

ANIMALIA; MUS; MYCOPLASMA PNEUMONIAE;

EID: 84861772496     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0135OC     Document Type: Article

References (45)

1. Waites KB, Talkington DF. Mycoplasma pneumoniae and its role as a human pathogen. Clin Microbiol Rev 2004;17:697-728. (Pubitemid 39372513)
2. Baseman JB, Tully JG. Mycoplasmas: Sophisticated, reemerging, and burdened by their notoriety. Emerg Infect Dis 1997;3:21-32. (Pubitemid 127433636)
3. Tryon VV, Baseman JB. Pathogenic determinants and mechanisms. In: Maniloff J, McElhaney RN, Finch LR, Baseman JB, editors. Mycoplasmas: molecular biology and pathogenesis.Washington, DC: American Society for Microbiology; 1992. pp. 457-471.
4. Krause DC. Mycoplasma pneumoniae cytadherence: unravelling the tie that binds. Mol Microbiol 1996;20:247-253. (Pubitemid 26141834)
5. Baseman JB, Reddy SP, Dallo SF. Interplay between mycoplasma surface proteins, airway cells, and the protean manifestations of mycoplasma-mediated human infections. Am J Respir Crit Care Med 1996;154:S137-S144. (Pubitemid 26346897)
6. Kannan TR, Baseman JB. Adp-ribosylating and vacuolating cytotoxin of Mycoplasma pneumoniae represents unique virulence determinant among bacterial pathogens. Proc Natl Acad Sci USA 2006;103: 6724-6729.
7. Kannan TR, Provenzano D, Wright JR, Baseman JB. Identification and characterization of human surfactant protein a binding protein of Mycoplasma pneumoniae. Infect Immun 2005;73:2828-2834. (Pubitemid 40570350)
8. Hardy RD, Coalson JJ, Peters J, Chaparro A, Techasaensiri C, Cantwell AM, Kannan TR, Baseman JB, Dube PH. Analysis of pulmonary inflammation and function in the mouse and baboon after exposure to Mycoplasma pneumoniae CARDS toxin. PLoS ONE 2009;4:e7562.
9. Johnson C, Kannan TR, Baseman JB. Cellular vacuoles induced by Mycoplasma pneumoniae CARDS toxin originate from rab9-associated compartments. PLoS ONE 2011;6:e22877.
10. Kannan TR, Musatovova O, Balasubramanian S, Cagle M, Jordan JL, Krunkosky TM, Davis A, Hardy RD, Baseman JB. Mycoplasma pneumoniae community acquired respiratory distress syndrome toxin expression reveals growth phase and infection-dependent regulation. Mol Microbiol 2010;76:1127-1141.
11. Techasaensiri C, Tagliabue C, CagleM, Iranpour P, Katz K, Kannan TR, Coalson JJ, Baseman JB, Hardy RD. Variation in colonization, adp-ribosylating and vacuolating cytotoxin, and pulmonary disease severity among Mycoplasma pneumoniae strains. Am J Respir Crit Care Med 2010;182:797-804.
12. Fonseca-Aten M, Rios AM, Mejias A, Chavez-Bueno S, Katz K, Gomez AM, McCracken GH Jr, Hardy RD. Mycoplasma pneumoniae induces host-dependent pulmonary inflammation and airway obstruction in mice. Am J Respir Cell Mol Biol 2005;32:201-210. (Pubitemid 40387646)
13. Hardy RD, Jafri HS, Olsen K, Hatfield J, Iglehart J, Rogers BB, Patel P, Cassell G, McCracken GH, Ramilo O. Mycoplasma pneumoniae induces chronic respiratory infection, airway hyperreactivity, and pulmonary inflammation: a murine model of infection-associated chronic reactive airway disease. Infect Immun 2002;70:649-654. (Pubitemid 34083823)
14. Hardy RD, Jafri HS, Olsen K, Wordemann M, Hatfield J, Rogers BB, Patel P, Duffy L, Cassell G, McCracken GH, et al. Elevated cytokine and chemokine levels and prolonged pulmonary airflow resistance in a murine Mycoplasma pneumoniae pneumonia model: a microbiologic, histologic, immunologic, and respiratory plethysmographic profile. Infect Immun 2001;69:3869-3876. (Pubitemid 32493307)
15. Chu HW, Honour JM, Rawlinson CA, Harbeck RJ, Martin RJ. Effects of respiratory Mycoplasma pneumoniae infection on allergen-induced bronchial hyperresponsiveness and lung inflammation in mice. Infect Immun 2003;71:1520-1526. (Pubitemid 36254340)
16. Chu HW, Rino JG, Wexler RB, Campbell K, Harbeck RJ, Martin RJ. Mycoplasma pneumoniae infection increases airway collagen deposition in a murine model of allergic airway inflammation. Am J Physiol Lung Cell Mol Physiol 2005;289:L125-L133. (Pubitemid 40863562)
17. Chu HW, Breed R, Rino JG, Harbeck RJ, Sills MR, Martin RJ. Repeated respiratory Mycoplasma pneumoniae infections in mice: effect of host genetic background. Microbes Infect 2006;8:1764-1772. (Pubitemid 44128878)
18. Martin RJ, Chu HW, Honour JM, Harbeck RJ. Airway inflammation and bronchial hyperresponsiveness after Mycoplasma pneumoniae infection in a murine model. Am J Respir Cell Mol Biol 2001;24: 577-582. (Pubitemid 32442765)
19. Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol 2001; 107:595-601. (Pubitemid 32397743)
20. Blasi F. Atypical pathogens and respiratory tract infections. Eur Respir J 2004;24:171-181. (Pubitemid 39029084)
21. Johnston SL, Martin RJ. Chlamydophila pneumoniae and Mycoplasma pneumoniae: a role in asthma pathogenesis? Am J Respir Crit Care Med 2005;172:1078-1089. (Pubitemid 43066642)
22. Kraft M, Cassell GH, Henson JE, Watson H, Williamson J, Marmion BP, Gaydos CA, Martin RJ. Detection of Mycoplasma pneumoniae in the airways of adults with chronic asthma. Am J Respir Crit Care Med 1998;158:998-1001. (Pubitemid 28449473)
23. Kraft M, Cassell GH, Pak J, Martin RJ. Mycoplasma pneumoniae and Chlamydia pneumoniae in asthma: effect of clarithromycin. Chest 2002;121:1782-1788. (Pubitemid 34634396)
24. Lieberman D, Printz S, Ben-Yaakov M, Lazarovich Z, Ohana B, Friedman MG, Dvoskin B, Leinonen M, Boldur I. Atypical pathogen infection in adults with acute exacerbation of bronchial asthma. Am J Respir Crit Care Med 2003;167:406-410. (Pubitemid 36216424)
25. Seggev JS, Lis I, Siman-Tov R, Gutman R, Abu-Samara H, Schey G, Naot Y. Mycoplasma pneumoniae is a frequent cause of exacerbation of bronchial asthma in adults. Ann Allergy 1986;57:263-265. (Pubitemid 16008807)
26. Bubeck SS, Cantwell AM, Dube PH. Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. Infect Immun 2007;75:697-705. (Pubitemid 46203431)
27. Handley SA, Dube PH, Miller VL. Histamine signaling through the H(2) receptor in the peyer's patch is important for controlling Yersinia enterocolitica infection. Proc Natl Acad Sci USA 2006;103:9268-9273. (Pubitemid 43902567)
28. Bell RE, Kuehl TJ, Coalson JJ, Ackerman NB Jr, Null DM Jr, Escobedo MB, Yoder BA, Cornish JD, Nalle L, Skarin RM, et al. High-frequency ventilation compared to conventional positive-pressure ventilation in the treatment of hyaline membrane disease in primates. Crit Care Med 1984;12:764-768. (Pubitemid 14041824)
29. Delemos RA, Coalson JJ, Gerstmann DR, Null DM Jr, Ackerman NB, Escobedo MB, Robotham JL, Kuehl TJ. Ventilatory management of infant baboons with hyaline membrane disease: the use of high frequency ventilation. Pediatr Res 1987;21:594-602. (Pubitemid 17076194)
30. Dube PH, Revell PA, Chaplin DD, Lorenz RG, Miller VL. A role for IL-1 alpha in inducing pathologic inflammation during bacterial infection. Proc Natl Acad Sci USA 2001;98:10880-10885. (Pubitemid 32878713)
31. Zhong Y, Cantwell A, Dube PH. Transforming growth factor {beta} and CD25 are important for controlling systemic dissemination following Yersinia enterocolitica infection of the gut. Infect Immun 2010; 78:3716-3725.
32. Chu HW, Jeyaseelan S, Rino JG, Voelker DR, Wexler RB, Campbell K, Harbeck RJ, Martin RJ. Tlr2 signaling is critical for Mycoplasma pneumoniae-induced airway mucin expression. J Immunol 2005;174: 5713-5719. (Pubitemid 40593214)
33. Hamid Q, Tulic M. Immunobiology of asthma. Annu Rev Physiol 2009; 71:489-507.
34. Shekels LL, Lyftogt C, Kieliszewski M, Filie JD, Kozak CA, Ho SB. Mouse gastric mucin: cloning and chromosomal localization. Biochem J 1995;311:775-785.
35. Holt PG, Strickland DH, Bosco A, Jahnsen FL. Pathogenic mechanisms of allergic inflammation: atopic asthma as a paradigm. Adv Immunol 2009;104:51-113.
36. Jacobsen EA, Ochkur SI, Lee NA, Lee JJ. Eosinophils and asthma. Curr Allergy Asthma Rep 2007;7:18-26. (Pubitemid 46655380)
37. Afshar R, Medoff BD, Luster AD. Allergic asthma: a tale of many t cells. Clin Exp Allergy 2008;38:1847-1857.
38. Sutherland ER, Martin RJ. Asthma and atypical bacterial infection. Chest 2007;132:1962-1966.
39. Tang LF, Shi YC, Xu YC, Wang CF, Yu ZS, Chen ZM. The change of asthma-associated immunological parameters in children with Mycoplasma pneumoniae infection. J Asthma 2009;46:265-269.
40. Panina-Bordignon P, Papi A, MarianiM, Di Lucia P, Casoni G, Bellettato C, Buonsanti C, Miotto D, Mapp C, Villa A, et al. The c-c chemokine receptors CCR4 and CCR8 identify airway T cells of allergen-challenged atopic asthmatics. J Clin Invest 2001;107:1357-1364. (Pubitemid 32522029)
41. Peters J, Singh H, Brooks EG, Diaz J, Kannan TR, Coalson JJ, Baseman JG, Cagle M, Baseman JB. Persistence of CARDS toxin-producing Mycoplasma pneumoniae in refractory asthma. Chest 2011;140:401-407.
42. Gil JC, Cedillo RL, Mayagoitia BG, Paz MD. Isolation of Mycoplasma pneumoniae from asthmatic patients. Ann Allergy 1993;70:23-25. (Pubitemid 23042030)
43. Hou AC, Lu Y, Sha L, Liu LG, Shen J, Xu Y. (T(h1) and T(h2) cells in children with Mycoplasma pneumonia). Zhonghua Er Ke Za Zhi 2003;41:652-656.
44. Michels NM, Chu HW, LaFasto SC, Case SR, Minor MN, Martin RJ. Mast cells protect against airway Mycoplasma pneumoniae under allergic conditions. Clin Exp Allergy 2010;40:1406-1413.
45. Muir MT, Cohn SM, Louden C, Kannan TR, Baseman JB. Novel toxin assays implicate Mycoplasma pneumoniae in prolonged ventilator course and hypoxemia. Chest 2011;139:305-310.