SHP-1 as a critical regulator of Mycoplasma pneumoniae-induced inflammation in human asthmatic airway epithelial cells

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3371-3381

  Wang, Ying ^a   Zhu, Zhou ^b   Church, Tony D ^a   Lugogo, Njira L ^a   Que, Loretta G ^a   Francisco, Dave ^a   Ingram, Jennifer L ^a   Huggins, Molly ^a   Beaver, Denise M ^a   Wright, Jo Rae ^a   Kraft, Monica ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; SALBUTAMOL;

ADULT; ARTICLE; ASTHMA; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MYCOPLASMA PNEUMONIA; MYCOPLASMA PNEUMONIAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM;

ADULT; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CELL NUCLEUS; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-8; MALE; MYCOPLASMA PNEUMONIAE; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; YOUNG ADULT;

EID: 84859398835     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100573     Document Type: Article

References (60)

1. Djukanović, R., J. W. Wilson, K. M. Britten, S. J. Wilson, A. F. Walls, W. R. Roche, P. H. Howarth, and S. T. Holgate. 1992. Effect of an inhaled corticosteroid on airway inflammation and symptoms in asthma. Am. Rev. Respir. Dis. 145: 669-674.
2. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261. (Pubitemid 29004074)
3. Allegra, L., F. Blasi, S. Centanni, R. Cosentini, F. Denti, R. Raccanelli, P. Tarsia, and V. Valenti. 1994. Acute exacerbations of asthma in adults: role of Chlamydia pneumoniae infection. Eur. Respir. J. 7: 2165-2168.
4. Berkovich, S., S. J. Millian, and R. D. Snyder. 1970. The association of viral and mycoplasma infections with recurrence of wheezing in the asthmatic child. Ann. Allergy 28: 43-49.
5. Hahn, D. L., R. W. Dodge, and R. Golubjatnikov. 1991. Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA 266: 225-230.
6. Huhti, E., T. Mokka, J. Nikoskelainen, and P. Halonen. 1974. Association of viral andmycoplasma infectionswith exacerbations of asthma. Ann. Allergy 33: 145-149.
7. Pelaia, G., A. Vatrella, L. Gallelli, T. Renda, M. Cazzola, R. Maselli, and S. A. Marsico. 2006. Respiratory infections and asthma. Respir. Med. 100: 775-784.
8. Biscardi, S., M. Lorrot, E. Marc, F. Moulin, B. Boutonnat-Faucher, C. Heilbronner, J. L. Iniguez, M. Chaussain, E. Nicand, J. Raymond, and D. Gendrel. 2004. Mycoplasma pneumoniae and asthma in children. Clin. Infect. Dis. 38: 1341-1346. (Pubitemid 38668576)
9. Schleimer, R. P., A. Kato, R. Kern, D. Kuperman, and P. C. Avila. 2007. Epithelium: at the interface of innate and adaptive immune responses. J. Allergy Clin. Immunol. 120: 1279-1284. (Pubitemid 350216601)
10. Wark, P. A., S. L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, S. T. Holgate, and D. E. Davies. 2005. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201: 937-947. (Pubitemid 40524463)
11. Kraft, M., K. B. Adler, J. L. Ingram, A. L. Crews, T. P. Atkinson, C. B. Cairns, D. C. Krause, and H. W. Chu. 2008. Mycoplasma pneumoniae induces airway epithelial cell expression of MUC5AC in asthma. Eur. Respir. J. 31: 43-46.
12. Takeuchi, O., A. Kaufmann, K. Grote, T. Kawai, K. Hoshino, M. Morr, P. F. Mühlradt, and S. Akira. 2000. Cutting edge: preferentially the Rstereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164: 554-557. (Pubitemid 30043671)
13. Chu, H. W., S. Jeyaseelan, J. G. Rino, D. R. Voelker, R. B. Wexler, K. Campbell, R. J. Harbeck, and R. J. Martin. 2005. TLR2 signaling is critical for Mycoplasma pneumoniae-induced airway mucin expression. J. Immunol. 174: 5713-5719. (Pubitemid 40593214)
14. Chambers, M. A., A. O. Whelan, R. Spallek, M. Singh, B. Coddeville, Y. Guerardel, and E. Elass. 2010. Non-acylated Mycobacterium bovis glycoprotein MPB83 binds to TLR1/2 and stimulates production of matrix metalloproteinase 9. Biochem. Biophys. Res. Commun. 400: 403-408.
15. Kurokawa, K., H. Lee, K. B. Roh, M. Asanuma, Y. S. Kim, H. Nakayama, A. Shiratsuchi, Y. Choi, O. Takeuchi, H. J. Kang, et al. 2009. The Triacylated ATP Binding Cluster Transporter Substrate-binding Lipoprotein of Staphylococcus aureus Functions as a Native Ligand for the Toll-like Receptor 2. J. Biol. Chem. 284: 8406-8411.
16. Nishiguchi, M., M. Matsumoto, T. Takao, M. Hoshino, Y. Shimonishi, S. Tsuji, N. A. Begum, O. Takeuchi, S. Akira, K. Toyoshima, and T. Seya. 2001. Mycoplasma fermentans lipoprotein M161Ag-induced cell activation is mediated by Toll-like receptor 2: role of N-terminal hydrophobic portion in its multiple functions. J. Immunol. 166: 2610-2616. (Pubitemid 32173499)
17. Seya, T., and M. Matsumoto. 2002. A lipoprotein family from Mycoplasma fermentans confers host immune activation through Toll-like receptor 2. Int. J. Biochem. Cell Biol. 34: 901-906. (Pubitemid 34499586)
18. Shimizu, T., Y. Kida, and K. Kuwano. 2007. Triacylated lipoproteins derived from Mycoplasma pneumoniae activate nuclear factor-kappaB through toll-like receptors 1 and 2. Immunology 121: 473-483. (Pubitemid 47030085)
19. Chmura, K., X. Bai, M. Nakamura, P. Kandasamy, M. McGibney, K. Kuronuma, H. Mitsuzawa, D. R. Voelker, and E. D. Chan. 2008. Induction of IL-8 by Mycoplasma pneumoniae membrane in BEAS-2B cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 295: L220-L230.
20. Shen, S. H., L. Bastien, B. I. Posner, and P. Chrétien. 1991. A protein-tyrosine phosphatase with sequence similarity to the SH2 domain of the protein-tyrosine kinases. Nature 352: 736-739. (Pubitemid 21912421)
21. Matthews, R. J., D. B. Bowne, E. Flores, and M. L. Thomas. 1992. Characterization of hematopoietic intracellular protein tyrosine phosphatases: description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences. Mol. Cell. Biol. 12: 2396-2405.
22. Freeman, R. M., Jr., J. Plutzky, and B. G. Neel. 1992. Identification of a human src homology 2-containing protein-tyrosine-phosphatase: a putative homolog of Drosophila corkscrew. Proc. Natl. Acad. Sci. USA. 89: 11239-11243.
23. Yi, T. L., J. L. Cleveland, and J. N. Ihle. 1992. Protein tyrosine phosphatase containing SH2 domains: characterization, preferential expression in hematopoietic cells, and localization to human chromosome 12p12-p13. Mol. Cell. Biol. 12: 836-846.
24. Kashiwada, M., C. C. Giallourakis, P. Y. Pan, and P. B. Rothman. 2001. Immunoreceptor tyrosine-based inhibitory motif of the IL-4 receptor associates with SH2-containing phosphatases and regulates IL-4-induced proliferation. J. Immunol. 167: 6382-6387. (Pubitemid 33081570)
25. Hanson, E. M., H. Dickensheets, C. K. Qu, R. P. Donnelly, and A. D. Keegan. 2003. Regulation of the dephosphorylation of Stat6. Participation of Tyr-713 in the interleukin-4 receptor alpha, the tyrosine phosphatase SHP-1, and the proteasome. J. Biol. Chem. 278: 3903-3911. (Pubitemid 36801121)
26. Cyster, J. G., and C. C. Goodnow. 1995. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 2: 13-24.
27. Lorenz, U., K. S. Ravichandran, S. J. Burakoff, and B. G. Neel. 1996. Lack of SHPTP1 results in src-family kinase hyperactivation and thymocyte hyperresponsiveness. Proc. Natl. Acad. Sci. USA 93: 9624-9629. (Pubitemid 26296658)
28. Zhang, J., A. K. Somani, D. Yuen, Y. Yang, P. E. Love, and K. A. Siminovitch. 1999. Involvement of the SHP-1 tyrosine phosphatase in regulation of T cell selection. J. Immunol. 163: 3012-3021. (Pubitemid 29431796)
29. Haque, S. J., P. Harbor, M. Tabrizi, T. Yi, and B. R. Williams. 1998. Protein-tyrosine phosphatase Shp-1 is a negative regulator of IL-4- and IL-13-dependent signal transduction. J. Biol. Chem. 273: 33893-33896. (Pubitemid 29008849)
30. Zhang, Q., P. N. Raghunath, E. Vonderheid, N. Odum, and M. A. Wasik. 2000. Lack of phosphotyrosine phosphatase SHP-1 expression in malignant T-cell lymphoma cells results from methylation of the SHP-1 promoter. Am. J. Pathol. 157: 1137-1146.
31. Khoury, J. D., G. Z. Rassidakis, L. J. Medeiros, H. M. Amin, and R. Lai. 2004. Methylation of SHP1 gene and loss of SHP1 protein expression are frequent in systemic anaplastic large cell lymphoma. Blood 104: 1580-1581. (Pubitemid 39166542)
32. Zhang, Q., H. Y. Wang, M. Marzec, P. N. Raghunath, T. Nagasawa, and M. A. Wasik. 2005. STAT3- and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc. Natl. Acad. Sci. USA 102: 6948-6953. (Pubitemid 40675422)
33. Christophi, G. P., C. A. Hudson, R. C. Gruber, C. P. Christophi, C. Mihai, L. J. Mejico, B. Jubelt, and P. T. Massa. 2008. SHP-1 deficiency and increased inflammatory gene expression in PBMCs of multiple sclerosis patients. Lab. Invest. 88: 243-255. (Pubitemid 351311285)
34. Christophi, G. P., C. A. Hudson, M. Panos, R. C. Gruber, and P. T. Massa. 2009. Modulation of macrophage infiltration and inflammatory activity by the phosphatase SHP-1 in virus-induced demyelinating disease. J. Virol. 83: 522-539.
35. Kamata, T., M. Yamashita, M. Kimura, K. Murata, M. Inami, C. Shimizu, K. Sugaya, C. R. Wang, M. Taniguchi, and T. Nakayama. 2003. src homology 2 domain-containing tyrosine phosphatase SHP-1 controls the development of allergic airway inflammation. J. Clin. Invest. 111: 109-119. (Pubitemid 36134854)
36. Oh, S. Y., T. Zheng, Y. K. Kim, L. Cohn, R. J. Homer, A. N. McKenzie, and Z. Zhu. 2009. A critical role of SHP-1 in regulation of type 2 inflammation in the lung. Am. J. Respir. Cell Mol. Biol. 40: 568-574.
37. Cho, Y. S., S. Y. Oh, and Z. Zhu. 2008. Tyrosine phosphatase SHP-1 in oxidative stress and development of allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 39: 412-419.
38. National Asthma Education and Prevention Program. 2007. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. [Published erratum appears in 2008 J. Allergy Clin. Immunol. 121: 1330.] J. Allergy Clin. Immunol. 120(5, Suppl.)S94-S138.
39. Wang, Y., L. Xu, H. Duan, D. A. Pasek, J. P. Eu, and G. Meissner. 2006. Knocking down type 2 but not type 1 calsequestrin reduces calcium sequestration and release in C2C12 skeletal muscle myotubes. J. Biol. Chem. 281: 15572-15581. (Pubitemid 43855150)
40. Li, J., R. J. Samulski, and X. Xiao. 1997. Role for highly regulated rep gene expression in adeno-associated virus vector production. J. Virol. 71: 5236-5243. (Pubitemid 27258196)
41. Xiao, X., J. Li, and R. J. Samulski. 1998. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72: 2224-2232. (Pubitemid 28100780)
42. Renard, P., I. Ernest, A. Houbion, M. Art, H. Le Calvez, M. Raes, and J. Remacle. 2001. Development of a sensitive multi-well colorimetric assay for active NFkappaB. Nucleic Acids Res. 29: E21.
43. Massa, P. T., and C. Wu. 1998. Increased inducible activation of NF-kappaB and responsive genes in astrocytes deficient in the protein tyrosine phosphatase SHP-1. J. Interferon Cytokine Res. 18: 499-507. (Pubitemid 28363577)
44. Plutzky, J., B. G. Neel, and R. D. Rosenberg. 1992. Isolation of a src homology 2-containing tyrosine phosphatase. Proc. Natl. Acad. Sci. USA 89: 1123-1127.
45. Craggs, G., and S. Kellie. 2001. A functional nuclear localization sequence in the C-terminal domain of SHP-1. J. Biol. Chem. 276: 23719-23725.
46. Slevogt, H., S. Zabel, B. Opitz, A. Hocke, J. Eitel, P. D. N'guessan, L. Lucka, K. Riesbeck, W. Zimmermann, J. Zweigner, et al. 2008. CEACAM1 inhibits Toll-like receptor 2-triggered antibacterial responses of human pulmonary epithelial cells. Nat. Immunol. 9: 1270-1278.
47. Cuevas, B., Y. Lu, S. Watt, R. Kumar, J. Zhang, K. A. Siminovitch, and G. B. Mills. 1999. SHP-1 regulates Lck-induced phosphatidylinositol 3-kinase phosphorylation and activity. J. Biol. Chem. 274: 27583-27589.
48. Kane, L. P., M. N. Mollenauer, Z. Xu, C. W. Turck, and A. Weiss. 2002. Akt-dependent phosphorylation specifically regulates Cot induction of NF-kappa Bdependent transcription. Mol. Cell. Biol. 22: 5962-5974. (Pubitemid 34815843)
49. Romashkova, J. A., and S. S. Makarov. 1999. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401: 86-90.
50. Ozes, O. N., L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner. 1999. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
51. Khaled, A. R., E. J. Butfiloski, E. S. Sobel, and J. Schiffenbauer. 1998. Functional consequences of the SHP-1 defect in motheaten viable mice: role of NFkappa B. Cell. Immunol. 185: 49-58. (Pubitemid 28272674)
52. Zhang, Z., E. Jimi, and A. L. Bothwell. 2003. Receptor activator of NF-kappa B ligand stimulates recruitment of SHP-1 to the complex containing TNFR-associated factor 6 that regulates osteoclastogenesis. J. Immunol. 171: 3620- 3626.
53. Zhao, J., D. M. Brooks, and D. I. Lurie. 2006. Lipopolysaccharide- activated SHP-1-deficient motheaten microglia release increased nitric oxide, TNF-alpha, and IL-1beta. Glia 53: 304-312. (Pubitemid 43221351)
54. Wang, Y., D. R. Voelker, N. L. Lugogo, G. Wang, J. Floros, J. L. Ingram, H.W. Chu, T. D. Church, P. Kandasamy, D. Fertel, et al. 2011. Surfactant protein A is defective in abrogating inflammation in asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 301: L598-L606.
55. Liu, J., Y. Yoshida, and U. Yamashita. 2008. DNA-binding activity of NFkappaB and phosphorylation of p65 are induced by N-acetylcysteine through phosphatidylinositol (PI) 3-kinase. Mol. Immunol. 45: 3984-3989.
56. Sizemore, N., S. Leung, and G. R. Stark. 1999. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol. Cell. Biol. 19: 4798-4805. (Pubitemid 29289518)
57. Nandan, D., R. Lo, and N. E. Reiner. 1999. Activation of phosphotyrosine phosphatase activity attenuates mitogen-activated protein kinase signaling and inhibits c-FOS and nitric oxide synthase expression in macrophages infected with Leishmania donovani. Infect. Immun. 67: 4055-4063. (Pubitemid 29357028)
58. Miyake, A., Y. Murata, H. Okazawa, H. Ikeda, Y. Niwayama, H. Ohnishi, Y. Hirata, and T. Matozaki. 2008. Negative regulation by SHPS-1 of Toll-like receptor-dependent proinflammatory cytokine production in macrophages. Genes Cells 13: 209-219. (Pubitemid 351192668)
59. An, H., J. Hou, J. Zhou, W. Zhao, H. Xu, Y. Zheng, Y. Yu, S. Liu, and X. Cao. 2008. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat. Immunol. 9: 542-550. (Pubitemid 351560523)
60. Jackson, D. J., and S. L. Johnston. 2010. The role of viruses in acute exacerbations of asthma. J. Allergy Clin. Immunol. 125: 1178-1187, quiz 1188-1189.