Internalization and trafficking of nontypeable Haemophilus influenzae in human respiratory epithelial cells and roles of IgA1 proteases for optimal invasion and persistence

Infection and Immunity

Volumn 82, Issue 1, 2014, Pages 433-444

  Clementi, Cara F ^a,b   Håkansson, Anders P ^a,b   Murphy, Timothy F ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; IMMUNOGLOBULIN A1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROTEINASE; RNA;

ACIDIFICATION; ARTICLE; BACTERIAL GENE; BACTERIUM ADHERENCE; BRONCHUS MUCOSA; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CHILDHOOD DISEASE; CONFOCAL MICROSCOPY; ENDOSOME; ENZYME INHIBITION; EPITHELIUM CELL; HAEMOPHILUS INFLUENZAE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IGAB GENE; INTERNALIZATION; LYSOSOME; MEMBRANE VESICLE; NONHUMAN; OPPORTUNISTIC INFECTION; PH; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84890843616     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00864-13     Document Type: Article

References (54)

1. Murphy TF. 2003. Respiratory infections caused by non-typeable Haemophilus influenzae. Curr. Opin. Infect. Dis. 16:129-134. http://dx.doi.org/10.1097/00001432-200304000-00009.
2. Sethi S, Murphy TF. 2008. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N. Engl. J. Med. 359:2355-2365. http://dx.doi.org/10.1056/NEJMra0800353.
3. Clementi CF, Murphy TF. 2011. Non-typeable Haemophilus influenzae invasion and persistence in the human respiratory tract. Front. Cell. Infect. Microbiol. 1:1. http://dx.doi.org/10.3389/fcimb.2011.00001.
4. Carruthers MD, Tracy EN, Dickson AC, Ganser KB, Munson RS, Jr, Bakaletz LO. 2012. Biological roles of nontypeable Haemophilus influenzae type IV pilus proteins encoded by the pil and com operons. J. Bacteriol. 194:1927-1933. http://dx.doi.org/10.1128/JB.06540-11.
5. Hong W, Mason K, Jurcisek J, Novotny L, Bakaletz LO, Swords WE. 2007. Phosphorylcholine decreases early inflammation and promotes the establishment of stable biofilm communities of nontypeable Haemophilus influenzae strain 86-028NP in a chinchilla model of otitis media. Infect. Immun. 75:958-965. http://dx.doi.org/10.1128/IAI.01691-06.
6. Hong W, Juneau RA, Pang B, Swords WE. 2009. Survival of bacterial biofilms within neutrophil extracellular traps promotes nontypeable Haemophilus influenzae persistence in the chinchilla model for otitis media. J. Innate Immun. 1:215-224. http://dx.doi.org/10.1159/000205937.
7. Pang B, Winn D, Johnson R, Hong W, West-Barnette S, Kock N, Swords WE. 2008. Lipooligosaccharides containing phosphorylcholine delay pulmonary clearance of nontypeable Haemophilus influenzae. Infect. Immun. 76:2037-2043. http://dx.doi.org/10.1128/IAI.01716-07.
8. Sharpe SW, Kuehn MJ, Mason KM. 2011. Elicitation of epithelial cellderived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect. Immun. 79:4361-4369. http://dx.doi.org/10.1128/IAI.05332-11.
9. Shelton CL, Raffel FK, Beatty WL, Johnson SM, Mason KM. 2011. Sap transporter mediated import and subsequent degradation of antimicro-bial peptides in Haemophilus. PLoS Pathog. 7:e1002360. http://dx.doi.org/10.1371/journal.ppat.1002360.
10. Swords WE. 2012. Nontypeable Haemophilus influenzae biofilms: role in chronic airway infections. Front. Cell. Infect. Microbiol. 2:97. http://dx.doi.org/10.3389/fcimb.2012.00097.
11. Swords WE. 2012. Quorum signaling and sensing by nontypeable Haemophilus influenzae. Front. Cell. Infect. Microbiol. 2:100. http://dx.doi.org/10.3389/fcimb.2012.00100.
12. Juneau RA, Pang B, Weimer KED, Armbruster CE, Swords WE. 2011. Nontypeable Haemophilus influenzae initiates formation of neutrophil extracellular traps. Infect. Immun. 79:431-438. http://dx.doi.org/10.1128/IAI.00660-10.
13. Ahren IL, Williams DL, Rice PJ, Forsgren A, Riesbeck K. 2001. The importance of a beta-glucan receptor in the nonopsonic entry of nontypeable Haemophilus influenzae into human monocytic and epithelial cells. J. Infect. Dis. 184:150-158. http://dx.doi.org/10.1086/322016.
14. Bandi V, Apicella MA, Mason E, Murphy TF, Siddiqi A, Atmar RL, Greenberg SB. 2001. Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am. J. Respir. Crit. Care Med. 164:2114-2119. http://dx.doi.org/10.1164/ajrccm.164.11.2104093.
15. Forsgren J, Samuelson A, Ahlin A, Jonasson J, Rynnel-Dagoo B, Lindberg A. 1994. Haemophilus influenzae resides and multiplies intracellularly in human adenoid tissue as demonstrated by in situ hybridization and bacterial viability assay. Infect. Immun. 62:673-679.
16. Forsgren J, Samuelson A, Borrelli S, Christensson B, Jonasson J, Lindberg AA. 1996. Persistence of nontypeable Haemophilus influenzae in adenoid macrophages: a putative colonization mechanism. Acta Otolaryngol. 116:766-773. http://dx.doi.org/10.3109/00016489609137922.
17. Hers JF, Mulder J. 1953. The mucosal epithelium of the respiratory tract in muco-purulent bronchitis caused by Haemophilus influenzae. J. Pathol. Bacteriol. 66:103-108. http://dx.doi.org/10.1002/path.1700660114.
18. Hotomi M, Arai J, Billal DS, Takei S, Ikeda Y, Ogami M, Kono M, Beder LB, Toya K, Kimura M, Yamanaka N. 2010. Nontypeable Haemophilus influenzae isolated from intractable acute otitis media internalized into cultured human epithelial cells. Auris Nasus Larynx 37:137-144. http://dx.doi.org/10.1016/j.anl.2009.03.012.
19. Ketterer MR, Shao JQ, Hornick DB, Buscher B, Bandi VK, Apicella MA. 1999. Infection of primary human bronchial epithelial cells by Haemophilus influenzae: macropinocytosis as a mechanism of airway epithelial cell entry. Infect. Immun. 67:4161-4170.
20. Marti-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, Sauleda J, Agusti AGN, Bengoechea JA, Garmendia J. 2009. Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect. Immun. 77:4232-4242. http://dx.doi.org/10.1128/IAI.00305-09.
21. Moller LV, Timens W, van der Bij W, Kooi K, de Wever B, Dankert J, van Alphen L. 1998. Haemophilus influenzae in lung explants of patients with end-stage pulmonary disease. Am. J. Respir. Crit. Care Med. 157: 950-956. http://dx.doi.org/10.1164/ajrccm.157.3.9707010.
22. Morey P, Cano V, Marti-Lliteras P, Lopez-Gomez A, Regueiro V, Saus C, Bengoechea JA, Garmendia J. 2011. Evidence for a non-replicative intracellular stage of nontypable Haemophilus influenzae in epithelial cells. Microbiology 157:234-250. http://dx.doi.org/10.1099/mic.0.040451-0.
23. St. Geme JW, III, Falkow S. 1990. Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect. Immun. 58:4036-4044.
24. Swords WE, Buscher BA, Ver Steeg Ii K, Preston A, Nichols WA, Weiser JN, Gibson BW, Apicella MA. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:13-27. http://dx.doi.org/10.1046/j.1365-2958.2000.01952.x.
25. Swords WE, Ketterer MR, Shao J, Campbell CA, Weiser JN, Apicella MA. 2001. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell. Microbiol. 3:525-536. http://dx.doi.org/10.1046/j.1462-5822.2001.00132.x.
26. van Schilfgaarde M, Eijk P, Regelink A, van Ulsen P, Everts V, Dankert J, van Alphen L. 1999. Haemophilus influenzae localized in epithelial cell layers is shielded from antibiotics and antibody-mediated bactericidal activity. Microb. Pathog. 26:249-262. http://dx.doi.org/10.1006/mpat.1998.0269.
27. van Schilfgaarde M, van Alphen L, Eijk P, Everts V, Dankert J. 1995. Paracytosis of Haemophilus influenzae through cell layers of NCI-H292 lung epithelial cells. Infect. Immun. 63:4729-4737.
28. Casey JR, Pichichero ME. 2004. Changes in frequency and pathogens causing acute otitis media in 1995-2003. Pediatr. Infect. Dis. J. 23:824-828. http://dx.doi.org/10.1097/01.inf.0000136871.51792.19.
29. Groeneveld K, van Alphen L, Eijk PP, Visschers G, Jansen HM, Zanen HC. 1990. Endogenous and exogenous reinfections by Haemophilus influenzae in patients with chronic obstructive pulmonary disease: the effect of antibiotic treatment on persistence. J. Infect. Dis. 161:512-517. http://dx.doi.org/10.1093/infdis/161.3.512.
30. Moller LV, Regelink AG, Grasselier H, Dankert-Roelse JE, Dankert J, van Alphen L. 1995. Multiple Haemophilus influenzae strains and strain variants coexist in the respiratory tract of patients with cystic fibrosis. J. Infect. Dis. 172:1388-1392. http://dx.doi.org/10.1093/infdis/172.5.1388.
31. Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. 2004. Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 170:266-272. http://dx.doi.org/10.1164/rccm.200403-354OC.
32. Holmes KA, Bakaletz LO. 1997. Adherence of non-typeable Haemophilus influenzae promotes reorganization of the actin cytoskeleton in human or chinchilla epithelial cells in vitro. Microb. Pathog. 23:157-166. http://dx.doi.org/10.1006/mpat.1997.0145.
33. Lopez-Gomez A, Cano V, Moranta D, Morey P, Garcia del Portillo F, Bengoechea JA, Garmendia J. 2012. Host cell kinases, alpha5 and beta1 integrins, and Rac1 signalling on the microtubule cytoskeleton are important for non-typable Haemophilus influenzae invasion of respiratory epithelial cells. Microbiology 158:2384-2398. http://dx.doi.org/10.1099/mic.0.059972-0.
34. Forbes SJ, Martinelli D, Hsieh C, Ault JG, Marko M, Mannella CA, Mantis NJ. 2012. Association of a protective monoclonal IgA with the O antigen of Salmonella enterica serovar Typhimurium impacts type 3 secretion and outer membrane integrity. Infect. Immun. 80:2454-2463. http://dx.doi.org/10.1128/IAI.00018-12.
35. Hooper LV. 2009. Do symbiotic bacteria subvert host immunity? Nat. Rev. Microbiol. 7:367-374. http://dx.doi.org/10.1038/nrmicro2114.
36. Fernaays MM, Lesse AJ, Sethi S, Cai X, Murphy TF. 2006. Differential genome contents of nontypeable Haemophilus influenzae strains from adults with chronic obstructive pulmonary disease. Infect. Immun. 74:3366-3374. http://dx.doi.org/10.1128/IAI.01904-05.
37. Fernaays MM, Lesse AJ, Cai X, Murphy TF. 2006. Characterization of igaB, a second immunoglobulin A1 protease gene in nontypeable Haemophilus influenzae. Infect. Immun. 74:5860-5870. http://dx.doi.org/10.1128/IAI.00796-06.
38. Poulsen K, Hjorth JP, Kilian M. 1988. Limited diversity of the immunoglobulin A1 protease gene (iga) among Haemophilus influenzae serotype b strains. Infect. Immun. 56:987-992.
39. Senior BW, Ip CL. 1999. An investigation into the influences of species and biotype on the type of IgA1 protease produced by isolates of Haemophilus. J. Med. Microbiol. 48:389-394. http://dx.doi.org/10.1099/00222615-48-4-389.
40. Vitovski S, Dunkin KT, Howard AJ, Sayers JR. 2002. Nontypeable Haemophilus influenzae in carriage and disease: a difference in IgA1 protease activity levels. JAMA 287:1699-1705. http://dx.doi.org/10.1001/jama.287.13.1699.
41. Murphy TF, Lesse AJ, Kirkham C, Zhong HC, Sethi S, Munson RS. 2011. A clonal group of nontypeable Haemophilus influenzae with two iga proteases is adapted to infection in chronic obstructive pulmonary disease. PLoS One 6:e25923. http://dx.doi.org/10.1371/journal.pone.0025923.
42. Binker MG, Cosen-Binker LI, Terebiznik MR, Mallo GV, McCaw SE, Eskelinen E-L, Willenborg M, Brumell JH, Saftig P, Grinstein S, Gray-Owen SD. 2007. Arrested maturation of Neisseria-containing phagosomes in the absence of the lysosome-associated membrane proteins, LAMP-1 and LAMP-2. Cell. Microbiol. 9:2153-2166. http://dx.doi.org/10.1111/j.1462-5822.2007.00946.x.
43. Lin L, Ayala P, Larson J, Mulks M, Fukuda M, Carlsson SR, Enns C, So M. 1997. The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Mol. Microbiol. 24:1083-1094. http://dx.doi.org/10.1046/j.1365-2958.1997.4191776.x.
44. Eskelinen EL, Tanaka Y, Saftig P. 2003. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13:137-145. http://dx.doi.org/10.1016/S0962-8924(03)00005-9.
45. Saftig P, Schroder B, Blanz J. 2010. Lysosomal membrane proteins: life between acid and neutral conditions. Biochem. Soc. Trans. 38:1420-1423. http://dx.doi.org/10.1042/BST0381420.
46. Van Leeuwen MR, Golovina EA, Dijksterhuis J. 2009. The polyene antimycotics nystatin and filipin disrupt the plasma membrane, whereas natamycin inhibits endocytosis in germinating conidia of Penicillium discolor. J. Appl. Microbiol. 106:1908-1918. http://dx.doi.org/10.1111/j.1365-2672.2009.04165.x.
47. Hopper S, Vasquez B, Merz A, Clary S, Wilbur JS, So M. 2000. Effects of the immunoglobulin A1 protease on Neisseria gonorrhoeae trafficking across polarized T84 epithelial monolayers. Infect. Immun. 68:906-911. http://dx.doi.org/10.1128/IAI.68.2.906-911.2000.
48. Weiser JN, Bae D, Fasching C, Scamurra RW, Ratner AJ, Janoff EN. 2003. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc. Natl. Acad. Sci. U.S.A. 100:4215-4220. http://dx.doi.org/10.1073/pnas.0637469100.
49. Serruto D, Spadafina T, Scarselli M, Bambini S, Comanducci M, Hohle S, Kilian M, Veiga E, Cossart P, Oggioni MR, Savino S, Ferlenghi I, Taddei AR, Rappuoli R, Pizza M, Masignani V, Arico B. 2009. HadA is an atypical new multifunctional trimeric coiled-coil adhesin of Haemophilus influenzae biogroup aegyptius, which promotes entry into host cells. Cell. Microbiol. 11:1044-1063. http://dx.doi.org/10.1111/j.1462-5822.2009.01306.x.
50. Ayala BP, Vasquez B, Clary S, Tainer JA, Rodland K, So M. 2001. The pilus-induced Ca2+ flux triggers lysosome exocytosis and increases the amount of Lamp1 accessible to Neisseria IgA1 protease. Cell. Microbiol. 3:265-275. http://dx.doi.org/10.1046/j.1462-5822.2001.00112.x.
51. Ayala P, Lin L, Hopper S, Fukuda M, So M. 1998. Infection of epithelial cells by pathogenic neisseriae reduces the levels of multiple lysosomal constituents. Infect. Immun. 66:5001-5007.
52. Ayala P, Vasquez B, Wetzler L, So M. 2002. Neisseria gonorrhoeae porin P1.B induces endosome exocytosis and a redistribution of Lamp1 to the plasma membrane. Infect. Immun. 70:5965-5971. http://dx.doi.org/10.1128/IAI.70.11.5965-5971.2002.
53. Kilian M, Russell MW. 2005. Microbial evasion of IgA functions, p 291-303. In Mestecky J,LammME, Strober W, Bienenstock J, McGhee JR, Mayer L (ed), Mucosal immunology, 3rd ed. Elsevier-Academic Press, Burlington, MA.
54. Poole J, Foster E, Chaloner K, Hunt J, Jennings MP, Bair T, Knudtson K, Christensen E, Munson RS, Jr, Winokur PL, Apicella MA. 2013. Analysis of nontypeable Haemophilus influenzae phase variable genes during experimental human nasopharyngeal colonization. J. Infect. Dis. 208:720-727. http://dx.doi.org/10.1093/infdis/jit240.