Epithelial anion transporter pendrin contributes to inflammatory lung pathology in mouse models of Bordetella pertussis infection

Infection and Immunity

Volumn 82, Issue 10, 2014, Pages 4212-4221

  Scanlon, Karen M ^a   Gau, Yael ^a   Zhu, Jingsong ^a   Skerry, Ciaran ^a   Wall, Susan M ^b   Soleimani, Manoocher ^c   Carbonetti, Nicholas H ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAZOLAMIDE; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; PENDRIN; PERTUSSIS TOXIN; RANTES; STAT6 PROTEIN; ANION TRANSPORT PROTEIN; SLC26A4 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERIAL STRAIN; CONTROLLED STUDY; GENETIC DIFFERENCE; MOUSE; NONHUMAN; PATHOLOGY; PERTUSSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; BACTERIAL PNEUMONIA; BAGG ALBINO MOUSE; BORDETELLA PERTUSSIS; C57BL MOUSE; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; INFANT; KNOCKOUT MOUSE; LUNG; METABOLISM; MICROBIOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANION TRANSPORT PROTEINS; BACTERIAL LOAD; BORDETELLA PERTUSSIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; INFANT; INTERLEUKIN-17; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PERTUSSIS TOXIN; PNEUMONIA, BACTERIAL; WHOOPING COUGH;

EID: 84907100425     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02222-14     Document Type: Article

References (60)

1. Berger JT, Carcillo JA, Shanley TP, Wessel DL, Clark A, Holubkov R, Meert KL, Newth CJ, Berg RA, Heidemann S, Harrison R, Pollack M, Dalton H, Harvill E, Karanikas A, Liu T, Burr JS, Doctor A, Dean JM, Jenkins TL, Nicholson CE, Eunice Kennedy Shriver National Institute of Child Health and Human Development Collaborative Pediatric Critical Care Research Network. 2013. Critical pertussis illness in children: a multicenter prospective cohort study. Pediatr. Crit. Care Med. 14:356-365. http://dx.doi.org/10.1097/PCC.0b013e31828a70fe.
2. Mooi FR, Van Der Maas NA, De Melker HE. 2014. Pertussis resurgence: waning immunity and pathogen adaptation-two sides of the same coin. Epidemiol. Infect. 142:685-694. http://dx.doi.org/10.1017/S0950268813 000071.
3. Ausiello CM, Urbani F, la Sala A, Lande R, Cassone A. 1997. Vaccineand antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole-cell or acellular pertussis vaccines. Infect. Immun. 65:2168-2174.
4. Klein NP, Bartlett J, Rowhani-Rahbar A, Fireman B, Baxter R. 2012. Waning protection after fifth dose of acellular pertussis vaccine in children. N. Engl. J. Med. 367:1012-1019. http://dx.doi.org/10.1056/NEJMoa1200850.
5. Ross PJ, Sutton CE, Higgins S, Allen AC, Walsh K, Misiak A, Lavelle EC, McLoughlin RM, Mills KH. 2013. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog. 9:e1003264. http://dx.doi.org/10.1371/journal.ppat.1003264.
6. Smits K, Pottier G, Smet J, Dirix V, Vermeulen F, De Schutter I, Carollo M, Locht C, Ausiello CM, Mascart F. 2013. Different T cell memory in preadolescents after whole-cell or acellular pertussis vaccination. Vaccine 32: 111-118. http://dx.doi.org/10.1016/j.vaccine.2013.10.056.
7. Warfel JM, Zimmerman LI, Merkel TJ. 2014. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc. Natl. Acad. Sci. U. S. A. 111:787-792. http://dx.doi.org/10.1073/pnas.1314688110.
8. Cherry JD. 2012. Epidemic pertussis in 2012-the resurgence of a vaccine-preventable disease. N. Engl. J. Med. 367:785-787. http://dx.doi.org /10.1056/NEJMp1209051.
9. Paddock CD, Sanden GN, Cherry JD, Gal AA, Langston C, Tatti KM, Wu KH, Goldsmith CS, Greer PW, Montague JL, Eliason MT, Holman RC, Guarner J, Shieh WJ, Zaki SR. 2008. Pathology and pathogenesis of fatal Bordetella pertussis infection in infants. Clin. Infect. Dis. 47:328- 338. http://dx.doi.org/10.1086/589753.
10. Carbonetti NH. 2010. Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol. 5:455-469. http://dx.doi.org/10.2217/fmb.09.133.
11. Witvliet MH, Burns DL, Brennan MJ, Poolman JT, Manclark CR. 1989. Binding of pertussis toxin to eucaryotic cells and glycoproteins. Infect. Immun. 57:3324-3330.
12. Wong WS, Rosoff PM. 1996. Pharmacology of pertussis toxin B-oligomer. Can. J. Physiol. Pharmacol. 74:559-564. http://dx.doi.org/10.1139/y96-045.
13. Hazes B, Read RJ. 1997. Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36:11051-11054. http: //dx.doi.org/10.1021/bi971383p.
14. Plaut RD, Carbonetti NH. 2008. Retrograde transport of pertussis toxin in the mammalian cell. Cell. Microbiol. 10:1130-1139. http://dx.doi.org /10.1111/j.1462-5822.2007.01115.x.
15. Worthington ZE, Carbonetti NH. 2007. Evading the proteasome: absence of lysine residues contributes to pertussis toxin activity by evasion of proteasome degradation. Infect. Immun. 75:2946-2953. http://dx.doi.org /10.1128/IAI.02011-06.
16. Burns DL. 1988. Subunit structure and enzymic activity of pertussis toxin. Microbiol. Sci. 5:285-287.
17. Katada T, Ui M. 1982. ADP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J. Biol. Chem. 257:7210-7216.
18. Carbonetti NH, Artamonova GV, Mays RM, Worthington ZE. 2003. Pertussis toxin plays an early role in respiratory tract colonization by Bordetella pertussis. Infect. Immun. 71:6358-6366. http://dx.doi.org/10.1128/IAI.71.11.6358-6366.2003.
19. Carbonetti NH, Artamonova GV, Van Rooijen N, Ayala VI. 2007. Pertussis toxin targets airway macrophages to promote Bordetella pertussis infection of the respiratory tract. Infect. Immun. 75:1713-1720. http: //dx.doi.org/10.1128/IAI.01578-06.
20. Andreasen C, Carbonetti NH. 2008. Pertussis toxin inhibits early chemokine production to delay neutrophil recruitment in response to Bordetella pertussis respiratory tract infection in mice. Infect. Immun. 76:5139- 5148. http://dx.doi.org/10.1128/IAI.00895-08.
21. Kirimanjeswara GS, Agosto LM, Kennett MJ, Bjornstad ON, Harvill ET. 2005. Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis. J. Clin. Invest. 115: 3594-3601. http://dx.doi.org/10.1172/JCI24609.
22. Andreasen C, Powell DA, Carbonetti NH. 2009. Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice. PLoS One 4:e7079. http://dx.doi.org/10.1371/journal.pone.0007079.
23. Carbonetti NH, Artamonova GV, Andreasen C, Dudley E, Mays RM, Worthington ZE. 2004. Suppression of serum antibody responses by pertussis toxin after respiratory tract colonization by Bordetella pertussis and identification of an immunodominant lipoprotein. Infect. Immun. 72: 3350-3358. http://dx.doi.org/10.1128/IAI.72.6.3350-3358.2004.
24. Wolfe DN, Mann PB, Buboltz AM, Harvill ET. 2007. Delayed role of tumor necrosis factor-alpha in overcoming the effects of pertussis toxin. J. Infect. Dis. 196:1228-1236. http://dx.doi.org/10.1086/521303.
25. Zhang X, Hester SE, Kennett MJ, Karanikas AT, Bendor L, Place DE, Harvill ET. 2011. Interleukin-1 receptor signaling is required to overcome the effects of pertussis toxin and for efficient infection- or vaccinationinduced immunity against Bordetella pertussis. Infect. Immun. 79:527- 541. http://dx.doi.org/10.1128/IAI.00590-10.
26. Weiss AA, Goodwin MS. 1989. Lethal infection by Bordetella pertussis mutants in the infant mouse model. Infect. Immun. 57:3757-3764.
27. Connelly CE, Sun Y, Carbonetti NH. 2012. Pertussis toxin exacerbates and prolongs airway inflammatory responses during Bordetella pertussis infection. Infect. Immun. 80:4317-4332. http://dx.doi.org/10.1128/IAI.00808-12.
28. Royaux IE, Suzuki K, Mori A, Katoh R, Everett LA, Kohn LD, Green ED. 2000. Pendrin, the protein encoded by the Pendred syndrome gene (PDS), is an apical porter of iodide in the thyroid and is regulated by thyroglobulin in FRTL-5 cells. Endocrinology 141:839-845. http://dx.doi.org/10.1210/endo.141.2.7303.
29. Royaux IE, Wall SM, Karniski LP, Everett LA, Suzuki K, Knepper MA, Green ED. 2001. Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc. Natl. Acad. Sci. U. S. A. 98:4221-4226. http://dx.doi.org/10.1073/pnas.071516798.
30. Scott DA, Wang R, Kreman TM, Sheffield VC, Karniski LP. 1999. The Pendred syndrome gene encodes a chloride-iodide transport protein. Nat. Genet. 21:440-443. http://dx.doi.org/10.1038/7783.
31. Alesutan I, Daryadel A, Mohebbi N, Pelzl L, Leibrock C, Voelkl J, Bourgeois S, Dossena S, Nofziger C, Paulmichl M, Wagner CA, Lang F. 2011. Impact of bicarbonate, ammonium chloride, and acetazolamide on hepatic and renal SLC26A4 expression. Cell. Physiol. Biochem. 28:553- 558. http://dx.doi.org/10.1159/000335114.
32. Kuperman DA, Lewis CC, Woodruff PG, Rodriguez MW, Yang YH, Dolganov GM, Fahy JV, Erle DJ. 2005. Dissecting asthma using focused transgenic modeling and functional genomics. J. Allergy Clin. Immunol. 116:305-311. http://dx.doi.org/10.1016/j.jaci.2005.03.024.
33. Nakao I, Kanaji S, Ohta S, Matsushita H, Arima K, Yuyama N, Yamaya M, Nakayama K, Kubo H, Watanabe M, Sagara H, Sugiyama K, Tanaka H, Toda S, Hayashi H, Inoue H, Hoshino T, Shiraki A, Inoue M, Suzuki K, Aizawa H, Okinami S, Nagai H, Hasegawa M, Fukuda T, Green ED, Izuhara K. 2008. Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. J. Immunol. 180:6262-6269. http://dx.doi.org/10.4049/jimmunol.180.9.6262.
34. Nofziger C, Vezzoli V, Dossena S, Schonherr T, Studnicka J, Nofziger J, Vanoni S, Stephan S, Silva ME, Meyer G, Paulmichl M. 2011. STAT6 links IL-4/IL-13 stimulation with pendrin expression in asthma and chronic obstructive pulmonary disease. Clin. Pharmacol. Ther. 90:399- 405. http://dx.doi.org/10.1038/clpt.2011.128.
35. Yick CY, Zwinderman AH, Kunst PW, Grunberg K, Mauad T, Dijkhuis A, Bel EH, Baas F, Lutter R, Sterk PJ. 2013. Transcriptome sequencing (RNASeq) ofhumanendobronchial biopsies: asthma versus controls. Eur. Respir. J. 42:662-670. http://dx.doi.org/10.1183/09031936.00115412.
36. Ishida A, Ohta N, Suzuki Y, Kakehata S, Okubo K, Ikeda H, Shiraishi H, Izuhara K. 2012. Expression of pendrin and periostin in allergic rhinitis and chronic rhinosinusitis. Allergol. Int. 61:589-595. http://dx.doi.org/10.2332/allergolint.11-OA-0370.
37. Garnett JP, Hickman E, Burrows R, Hegyi P, Tiszlavicz L, Cuthbert AW, Fong P, Gray MA. 2011. Novel role for pendrin in orchestrating bicarbonate secretion in cystic fibrosis transmembrane conductance regulator (CFTR)-expressing airway serous cells. J. Biol. Chem. 286:41069- 41082. http://dx.doi.org/10.1074/jbc.M111.266734.
38. Pedemonte N, Caci E, Sondo E, Caputo A, Rhoden K, Pfeffer U, Di Candia M, Bandettini R, Ravazzolo R, Zegarra-Moran O, Galietta LJ. 2007. Thiocyanate transport in resting and IL-4-stimulated human bronchial epithelial cells: role of pendrin and anion channels. J. Immunol. 178:5144-5153. http://dx.doi.org/10.4049/jimmunol.178.8.5144.
39. Ratner AJ, Prince A. 2000. Lactoperoxidase. New recognition of an "old" enzyme in airway defenses. Am. J. Respir. Cell Mol. Biol. 22:642-644. http://dx.doi.org/10.1165/ajrcmb.22.6.f186.
40. Nakagami Y, Favoreto Jr. S, ., Zhen G, Park SW, Nguyenvu LT, Kuperman DA, Dolganov GM, Huang X, Boushey HA, Avila PC, Erle DJ. 2008. The epithelial anion transporter pendrin is induced by allergy and rhinovirus infection, regulates airway surface liquid, and increases airway reactivity and inflammation in an asthma model. J. Immunol. 181:2203- 2210. http://dx.doi.org/10.4049/jimmunol.181.3.2203.
41. Bart MJ, van Gent M, van der Heide HG, Boekhorst J, Hermans P, Parkhill J, Mooi FR. 2010. Comparative genomics of prevaccination and modern Bordetella pertussis strains.BMCGenomics 11:627. http://dx.doi.org/10.1186/1471-2164-11-627.
42. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4:313-319. http://dx.doi.org/10.1016/S1074-7613(00)80439-2.
43. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, Sekikawa K, Asano M, Iwakura Y. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375-387. http://dx.doi.org /10.1016/S1074-7613(02)00391-6.
44. Amlal H, Petrovic S, Xu J, Wang Z, Sun X, Barone S, Soleimani M. 2010. Deletion of the anion exchanger Slc26a4 (pendrin) decreases apical Cl(-)/HCO3(-) exchanger activity and impairs bicarbonate secretion in kidney collecting duct. Am. J. Physiol. Cell Physiol. 299:C33-C41. http: //dx.doi.org/10.1152/ajpcell.00033.2010.
45. Knauf F, Yang CL, Thomson RB, Mentone SA, Giebisch G, Aronson PS. 2001. Identification of a chloride-formate exchanger expressed on the brush border membrane of renal proximal tubule cells. Proc. Natl. Acad. Sci. U. S. A. 98:9425-9430. http://dx.doi.org/10.1073/pnas.141241098.
46. Kasuga T, Nakase Y, Ukishima K, Takatsu K. 1954. Studies on Haemophilus pertussis. V. Relation between the phase of bacilli and the progress of the whooping-cough. Kitasato Arch. Exp. Med. 27:57-62.
47. Kreindler JL, Bertrand CA, Lee RJ, Karasic T, Aujla S, Pilewski JM, Frizzell RA, Kolls JK. 2009. Interleukin-17A induces bicarbonate secretion in normal human bronchial epithelial cells. Am. J. Physiol. 296:L257- L266. http://dx.doi.org/10.1152/ajplung.00344.2007.
48. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH. 2006. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177:7980-7989. http://dx.doi.org /10.4049/jimmunol.177.11.7980.
49. Khelef N, Bachelet CM, Vargaftig BB, Guiso N. 1994. Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect. Immun. 62: 2893-2900.
50. Milton AE, Weiner ID. 1998. Regulation of B-type intercalated cell apical anion exchange activity by CO2/HCO3. Am. J. Physiol. 274:F1086-F1094.
51. Pech V, Pham TD, Hong S, Weinstein AM, Spencer KB, Duke BJ, Walp E, Kim YH, Sutliff RL, Bao HF, Eaton DC, Wall SM. 2010. Pendrin modulates ENaC function by changing luminal HCO3. J. Am. Soc. Nephrol. 21:1928-1941. http://dx.doi.org/10.1681/ASN.2009121257.
52. Zahedi K, Barone S, Xu J, Soleimani M. 2013. Potentiation of the effect of thiazide derivatives by carbonic anhydrase inhibitors: molecular mechanisms and potential clinical implications. PLoS One 8:e79327. http://dx.doi.org/10.1371/journal.pone.0079327.
53. Banus S, Pennings J, Vandebriel R, Wester P, Breit T, Mooi F, Hoebee B, Kimman T. 2007. Lung response to Bordetella pertussis infection in mice identified by gene-expression profiling. Immunogenetics 59:555- 564. http://dx.doi.org/10.1007/s00251-007-0227-5.
54. Hogmalm A, Bry M, Strandvik B, Bry K. 2014. IL-1beta expression in the distal lung epithelium disrupts lung morphogenesis and epithelial cell differentiation in fetal mice. Am. J. Physiol. 306:L23-L34. http://dx.doi.org/10.1152/ajplung.00154.2013.
55. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Banfi B, Horswill AR, Stoltz DA, McCray Jr. PB, Welsh MJ, Zabner J. 2012. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487:109-113. http://dx.doi.org/10.1038/nature11130.
56. Dairaghi DJ, Oldham ER, Bacon KB, Schall TJ. 1997. Chemokine receptor CCR3 function is highly dependent on local pH and ionic strength. J. Biol. Chem. 272:28206-28209. http://dx.doi.org/10.1074/jbc.272.45.28206.
57. Ko SB, Zeng W, Dorwart MR, Luo X, Kim KH, Millen L, Goto H, Naruse S, Soyombo A, Thomas PJ, Muallem S. 2004. Gating of CFTR by the STAS domain of SLC26 transporters. Nat. Cell Biol. 6:343-350. http: //dx.doi.org/10.1038/ncb1115.
58. Garnett JP, Hickman E, Tunkamnerdthai O, Cuthbert AW, Gray MA. 2013. Protein phosphatase 1 coordinates CFTR-dependent airway epithelial HCO3-secretion by reciprocal regulation of apical and basolateral membrane Cl(-)-HCO3-exchangers. Br. J. Pharmacol. 168:1946-1960. http://dx.doi.org/10.1111/bph.12085.
59. Heming N, Urien S, Faisy C. 2012. Acetazolamide: a second wind for a respiratory stimulant in the intensive care unit? Crit. Care 16:318. http: //dx.doi.org/10.1186/cc11323.
60. Sawal M, Cohen M, Irazuzta JE, Kumar R, Kirton C, Brundler MA, Evans CA, Wilson JA, Raffeeq P, Azaz A, Rotta AT, Vora A, Vohra A, Abboud P, Mirkin LD, Cooper M, Dishop MK, Graf JM, Petros A, Klonin H. 2009. Fulminant pertussis: a multi-center study with new insights into the clinico-pathological mechanisms. Pediatr. Pulmonol. 44: 970-980. http://dx.doi.org/10.1002/ppul.21082.