Interleukin 32 (IL-32) contains a typical α-helix bundle structure that resembles focal adhesion targeting region of focal adhesion kinase-1

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5733-5743

  Heinhuis, Bas ^a   Koenders, Marije I ^a   Van Den Berg, Wim B ^a   Netea, Mihai G ^a   Dinarello, Charles A ^a,b   Joosten, Leo A B ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; CASPASE-3; DUAL ROLE; EXTRACELLULAR; EXTRACELLULAR DOMAINS; FOCAL ADHESION KINASE; FOCAL ADHESIONS; HELIX BUNDLE; INTEGRINS; INTRACELLULAR PROTEINS; ISOFORMS; PAXILLIN; PROTEIN STRUCTURES; RGD MOTIF; RGD PEPTIDE; SECONDARY PROTEIN STRUCTURE;

AMINO ACIDS; ENZYME ACTIVITY; FOCUSING; GLYCOPROTEINS; PEPTIDES;

ADHESION;

ALPHAVBETA6 INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; CASPASE 3; CYTOKINE; FOCAL ADHESION KINASE 1; INTERLEUKIN 32; INTERLEUKIN 32 ALPHA; INTERLEUKIN 32 BETA; INTERLEUKIN 32 GAMMA; PAXILLIN; PROCASPASE 3; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CELL DEATH; COMPUTER MODEL; COMPUTER PROGRAM; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; FOCAL ADHESION; GENE MUTATION; HUMAN; HUMAN CELL; PREDICTION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CASPASE 3; CELL DEATH; COMPUTATIONAL BIOLOGY; ENZYME ACTIVATION; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; HEK293 CELLS; HUMANS; INTEGRIN ALPHAVBETA3; INTEGRINS; INTERLEUKINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOPEPTIDES; PAXILLIN; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SOFTWARE;

EID: 84857267860     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.288290     Document Type: Article

References (74)

1. Calabrese, F., Baraldo, S., Bazzan, E., Lunardi, F., Rea, F., Maestrelli, P., Turato, G., Lokar-Oliani, K., Papi, A., Zuin, R., Sfriso, P., Balestro, E., Dinarello, C. A., and Saetta, M. (2008) IL-32, a novel proinflammatory cytokine in chronic obstructive pulmonary disease. Am. J. Respir. Crit Care Med. 178, 894-901
2. Dinarello, C. A., and Kim, S. H. (2006) IL-32, a novel cytokine with a possible role in disease. Ann. Rheum. Dis. 65, iii61-iii64 (Pubitemid 44629106)
3. Heinhuis, B., Koenders, M. I., van de Loo, F. A., van Lent, P. L., Kim, S. H., Dinarello, C. A., Joosten, L. A., and van den Berg, W. B. (2010) IL-32γ and Streptococcus pyogenes cell wall fragments synergise for IL-1-dependent destructive arthritis via upregulation of TLR-2 and NOD2. Ann. Rheum. Dis. 69, 1866-1872
4. Heinhuis, B., Koenders, M. I., van Riel, P. L., van de Loo, F. A., Dinarello, C. A., Netea, M. G., van den Berg, W. B., and Joosten, L. A. (2011) Tumour necrosis factor α-driven IL-32 expression in rheumatoid arthritis synovial tissue amplifies an inflammatory cascade. Ann. Rheum. Dis. 70, 660-667
5. Heinhuis, B., Koenders, M. I., van de Loo, F. A., Netea, M. G., van den Berg, W. B., and Joosten, L. A. (2011) Inflammation-dependent secretion and splicing of IL-32γ in rheumatoid arthritis. Proc. Natl. Acad. Sci. U.S.A. 108, 4962-4967
6. Joosten, L. A., Netea, M. G., Kim, S. H., Yoon, D. Y., Oppers-Walgreen, B., Radstake, T. R., Barrera, P., van de Loo, F. A., Dinarello, C. A., and van den Berg, W. B. (2006) IL-32, a proinflammatory cytokine in rheumatoid arthritis. Proc. Natl. Acad. Sci. U.S.A. 103, 3298-3303 (Pubitemid 43346464)
7. Kim, S. H., Han, S. Y., Azam, T., Yoon, D. Y., and Dinarello, C. A. (2005) Interleukin-32. A cytokine and inducer of TNFα. Immunity. 22, 131-142
8. Li, W., Liu, Y., Mukhtar, M. M., Gong, R., Pan, Y., Rasool, S. T., Gao, Y., Kang, L., Hao, Q., Peng, G., Chen, Y., Chen, X., Wu, J., and Zhu, Y. (2008) Activation of interleukin-32 pro-inflammatory pathway in response to influenza A virus infection. PLoS ONE 3, e1985
9. Li, W., Yang, F., Liu, Y., Gong, R., Liu, L., Feng, Y., Hu, P., Sun, W., Hao, Q., Kang, L., Wu, J., and Zhu, Y. (2009) Negative feedback regulation of IL-32 production by iNOS activation in response to dsRNA or influenza virus infection. Eur. J. Immunol. 39, 1019-1024
10. Li, W., Sun, W., Liu, L., Yang, F., Li, Y., Chen, Y., Fang, J., Zhang, W., Wu, J., and Zhu, Y. (2010) IL-32. A host proinflammatory factor against influenza viral replication is upregulated by aberrant epigenetic modifications during influenza A virus infection. J. Immunol. 185, 5056-5065
11. Nold, M. F., Nold-Petry, C. A., Pott, G. B., Zepp, J. A., Saavedra, M. T., Kim, S. H., and Dinarello, C. A. (2008) Endogenous IL-32 controls cytokine and HIV-1 production. J. Immunol. 181, 557-565
12. Rasool, S. T., Tang, H., Wu, J., Li, W., Mukhtar, M. M., Zhang, J., Mu, Y., Xing, H. X., Wu, J., and Zhu, Y. (2008) Increased level of IL-32 during human immunodeficiency virus infection suppresses HIV replication. Immunol. Lett. 117, 161-167
13. Zepp, J. A., Nold-Petry, C. A., Dinarello, C. A., and Nold, M. F. (2011) Protection from RNA and DNA viruses by IL-32. J. Immunol. 186, 4110-4118
14. Bai, X., Kim, S. H., Azam, T., McGibney, M. T., Huang, H., Dinarello, C. A., and Chan, E. D. (2010) IL-32 is a host protective cytokine against Mycobacterium tuberculosis in differentiated THP-1 human macrophages. J. Immunol. 184, 3830-3840
15. Netea, M. G., Azam, T., Ferwerda, G., Girardin, S. E., Walsh, M., Park, J. S., Abraham, E., Kim, J. M., Yoon, D. Y., Dinarello, C. A., and Kim, S. H. (2005) IL-32 synergizes with nucleotide oligomerization domain (NOD) 1 and NOD2 ligands for IL-1β and IL-6 production through a caspase 1-dependent mechanism. Proc. Natl. Acad. Sci. U.S.A. 102, 16309-16314 (Pubitemid 41688910)
16. Netea, M. G., Azam, T., Lewis, E. C., Joosten, L. A., Wang, M., Langenberg, D., Meng, X., Chan, E. D., Yoon, D. Y., Ottenhoff, T., Kim, S. H., and Dinarello, C. A. (2006) Mycobacterium tuberculosis induces interleukin- 32 production through a caspase-1/IL-18/interferon-γ-dependent mechanism. PLoS Med. 3, e277
17. Majid, S., Dar, A. A., Saini, S., Yamamura, S., Hirata, H., Tanaka, Y., Deng, G., and Dahiya, R. (2010) MicroRNA-205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 116, 5637-5649
18. Marcondes, A. M., Mhyre, A. J., Stirewalt, D. L., Kim, S. H., Dinarello, C. A., and Deeg, H. J. (2008) Dysregulation of IL-32 in myelodysplastic syndrome and chronic myelomonocytic leukemia modulates apoptosis and impairs NK function. Proc. Natl. Acad. Sci. U.S.A. 105, 2865-2870 (Pubitemid 351723635)
19. Nishida, A., Andoh, A., Inatomi, O., and Fujiyama, Y. (2009) Interleukin- 32 expression in the pancreas. J. Biol. Chem. 284, 17868-17876
20. Seo, E. H., Kang, J., Kim, K. H., Cho, M. C., Lee, S., Kim, H. J., Kim, J. H., Kim, E. J., Park, D. K., Kim, S. H., Choi, Y. K., Kim, J. M., Hong, J. T., and Yoon, D. Y. (2008) Detection of expressed IL-32 in human stomach cancer using ELISA and immunostaining. J. Microbiol. Biotechnol. 18, 1606-1612
21. Sorrentino, C., and Di Carlo, E. (2009) Expression of IL-32 in human lung cancer is related to the histotype and metastatic phenotype. Am. J. Respir. Crit Care Med. 180, 769-779
22. Cagnard, N., Letourneur, F., Essabbani, A., Devauchelle, V., Mistou, S., Rapinat, A., Decraene, C., Fournier, C., and Chiocchia, G. (2005) Interleukin- 32, CCL2, PF4F1, and GFD10 are the only cytokine/chemokine genes differentially expressed by in vitro cultured rheumatoid and osteoarthritis fibroblast-like synoviocytes. Eur. Cytokine Netw. 16, 289-292 (Pubitemid 350056544)
23. Shoda, H., Fujio, K., Yamaguchi, Y., Okamoto, A., Sawada, T., Kochi, Y., and Yamamoto, K. (2006) Interactions between IL-32 and tumor necrosis factor alpha; contribute to the exacerbation of immune-inflammatory diseases. Arthritis Res. Ther. 8, R166
24. Shioya, M., Nishida, A., Yagi, Y., Ogawa, A., Tsujikawa, T., Kim-Mitsuyama, S., Takayanagi, A., Shimizu, N., Fujiyama, Y., and Andoh, A. (2007) Epithelial overexpression of interleukin-32α in inflammatory bowel disease. Clin. Exp. Immunol. 149, 480-486 (Pubitemid 47256156)
25. Goda, C., Kanaji, T., Kanaji, S., Tanaka, G., Arima, K., Ohno, S., and Izuhara, K. (2006) Involvement of IL-32 in activation-induced cell death in T cells. Int. Immunol. 18, 233-240 (Pubitemid 43160136)
26. Kim, Y. G., Lee, C. K., Oh, J. S., Kim, S. H., Kim, K. A., and Yoo, B. (2010) Effect of interleukin-32γ on differentiation of osteoclasts from CD14+ monocytes. Arthritis Rheum. 62, 515-523
27. Mabilleau, G., and Sabokbar, A. (2009) Interleukin-32 promotes osteoclast differentiation but not osteoclast activation. PLoS ONE. 4, e4173
28. Netea, M. G., Lewis, E. C., Azam, T., Joosten, L. A., Jaekal, J., Bae, S. Y., Dinarello, C. A., and Kim, S. H. (2008) Interleukin-32 induces the differentiation of monocytes into macrophage-like cells. Proc. Natl. Acad. Sci. U.S.A. 105, 3515-3520 (Pubitemid 351723584)
29. Hasegawa, H., Thomas, H. J., Schooley, K., and Born, T. L. (2011) Native IL-32 is released from intestinal epithelial cells via a non-classical secretory pathway as a membrane-associated protein. Cytokine 53, 74-83
30. Nold-Petry, C. A., Nold, M. F., Zepp, J. A., Kim, S. H., Voelkel, N. F., and Dinarello, C. A. (2009) IL-32-dependent effects of IL-1β on endothelial cell functions. Proc. Natl. Acad. Sci. U.S.A. 106, 3883-3888
31. Mun, S. H., Kim, J. W., Nah, S. S., Ko, N. Y., Lee, J. H., Kim, J. D., Kim, D. K., Kim, H. S., Choi, J. D., Kim, S. H., Lee, C. K., Park, S. H., Kim, B. K., Kim, H. S., Kim, Y. M., and Choi, W. S. (2009) Tumor necrosis factor α-induced interleukin-32 is positively regulated via the Syk/protein kinase Cδ/JNK pathway in rheumatoid synovial fibroblasts. Arthritis Rheum. 60, 678-685
32. Kim, S., Lee, S., Her, E., Bae, S., Choi, J., Hong, J., Jaekal, J., Yoon, D., Azam, T., Dinarello, C. A., and Kim, S. (2008) Proteinase 3-processed form of the recombinant IL-32 separate domain. BMB Rep. 41, 814-819
33. Novick, D., Rubinstein, M., Azam, T., Rabinkov, A., Dinarello, C. A., and Kim, S. H. (2006) Proteinase 3 is an IL-32 binding protein. Proc. Natl. Acad. Sci. U.S.A. 103, 3316-3321 (Pubitemid 43346467)
34. Dahl, C. A., Schall, R. P., He, H. L., and Cairns, J. S. (1992) Identification of a novel gene expressed in activated natural killer cells and T cells. J. Immunol. 148, 597-603
35. Abram, C. L., and Lowell, C. A. (2009) The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 27, 339-362
36. D'Souza, S. E., Ginsberg, M. H., and Plow, E. F. (1991) Arginyl-glycylaspartic acid (RGD). A cell adhesion motif. Trends Biochem. Sci. 16, 246-250 (Pubitemid 121004445)
37. Giancotti, F. G., and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032
38. Broxterman, H. J., and Hoekman, K. (1999) Direct activation of caspases by RGD-peptides may increase drug sensitivity of tumour cells. Drug Resist. Updat. 2, 139-141
39. Wilder, R. L. (2002) Integrin alpha V beta 3 as a target for treatment of rheumatoid arthritis and related rheumatic diseases. Ann. Rheum. Dis. 61, (Suppl. 2) ii96-ii99
40. Stupp, R., and Ruegg, C. (2007) Integrin inhibitors reaching the clinic. J. Clin. Oncol. 25, 1637-1638 (Pubitemid 46797938)
41. Beierle, E. A., Ma, X., Stewart, J., Nyberg, C., Trujillo, A., Cance, W. G., and Golubovskaya, V. M. (2010) Inhibition of focal adhesion kinase decreases tumor growth in human neuroblastoma. Cell Cycle 9, 1005-1015
42. Hochwald, S. N., Nyberg, C., Zheng, M., Zheng, D., Wood, C., Massoll, N. A., Magis, A., Ostrov, D., Cance, W. G., and Golubovskaya, V. M. (2009) A novel small molecule inhibitor of FAK decreases growth of human pancreatic cancer. Cell Cycle 8, 2435-2443
43. Slack-Davis, J. K., Martin, K. H., Tilghman, R. W., Iwanicki, M., Ung, E. J., Autry, C., Luzzio, M. J., Cooper, B., Kath, J. C., Roberts, W. G., and Parsons, J. T. (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 282, 14845-14852 (Pubitemid 47093369)
44. Millard, M., Odde, S., and Neamati, N. (2011) Integrin targeted therapeutics. Theranostics. 1, 154-188
45. Aguzzi, M. S., Fortugno, P., Giampietri, C., Ragone, G., Capogrossi, M. C., and Facchiano, A. (2010) Intracellular targets of RGDS peptide in melanoma cells. Mol. Cancer 9, 84
46. Buckley, C. D., Pilling, D., Henriquez, N. V., Parsonage, G., Threlfall, K., Scheel-Toellner, D., Simmons, D. L., Akbar, A. N., Lord, J. M., and Salmon, M. (1999) RGD peptides induce apoptosis by direct caspase-3 activation. Nature 397, 534-539
47. Matsuki, K., Sasho, T., Nakagawa, K., Tahara, M., Sugioka, K., Ochiai, N., Ogino, S., Wada, Y., and Moriya, H. (2008) RGD peptide-induced cell death of chondrocytes and synovial cells. J. Orthop. Sci. 13, 524-532
48. Porter, A. G. (2006) Flipping the safety catch of procaspase-3. Nat. Chem. Biol. 2, 509-510
49. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER. A unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
50. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
51. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb- Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
52. Tusnády, G. E., and Simon, I. (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics. 17, 849-850 (Pubitemid 32970487)
53. Parsons, J. T., Martin, K. H., Slack, J. K., Taylor, J. M., and Weed, S. A. (2000) Focal adhesion kinase. A regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606-5613
54. Hayashi, I., Vuori, K., and Liddington, R. C. (2002) The focal adhesion targeting (FAT) region of focal adhesion kinase is a four-helix bundle that binds paxillin. Nat. Struct. Biol. 9, 101-106 (Pubitemid 34132410)
55. Witko-Sarsat, V., Lesavre, P., Lopez, S., Bessou, G., Hieblot, C., Prum, B., Noë H., Guillevin, L., Ravaud, P., Sermet-Gaudelus, I., Timsit, J., Grü, J. P., and Halbwachs-Mecarelli, L. (1999)Alarge subset of neutrophils expressing membrane proteinase 3 is a risk factor for vasculitis and rheumatoid arthritis. J. Am. Soc. Nephrol. 10, 1224-1233 (Pubitemid 29246987)
56. Du, X. P., Plow, E. F., Frelinger, A. L., 3rd, O'Toole, T. E., Loftus, J. C., and Ginsberg, M. H. (1991) Ligands "activate" integrin αIIb β3 (platelet GPIIb- IIIa). Cell 65, 409-416 (Pubitemid 121002050)
57. Pierschbacher, M. D., and Ruoslahti, E. (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30-33 (Pubitemid 14134132)
58. Pytela, R., Pierschbacher, M. D., and Ruoslahti, E. (1985) A 125/115-kDa cell surface receptor specific for vitronectin interacts with the arginineglycine- aspartic acid adhesion sequence derived from fibronectin. Proc. Natl. Acad. Sci. U.S.A. 82, 5766-5770 (Pubitemid 16218844)
59. Pytela, R., Pierschbacher, M. D., and Ruoslahti, E. (1985) Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell 40, 191-198 (Pubitemid 15169319)
60. Ruoslahti, E. (1996) RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715
61. Luo, B. H., Carman, C. V., and Springer, T. A. (2007) Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647 (Pubitemid 46697919)
62. Shimaoka, M., and Springer, T. A. (2003) Therapeutic antagonists and conformational regulation of integrin function. Nat. Rev. Drug Discov. 2, 703-716 (Pubitemid 37361786)
63. Xiong, J. P., Stehle, T., Zhang, R., Joachimiak, A., Frech, M., Goodman, S. L., and Arnaout, M. A. (2002) Crystal structure of the extracellular segment of integrin αVβ3 in complex with an Arg-Gly-Asp ligand. Science 296, 151-155 (Pubitemid 34280076)
64. Hayman, E. G., Pierschbacher, M. D., Suzuki, S., and Ruoslahti, E. (1985) Vitronectin. A major cell attachment-promoting protein in fetal bovine serum. Exp. Cell Res. 160, 245-258 (Pubitemid 16251280)
65. Richards, S., Leavesley, D., Topping, G., and Upton, Z. (2008) Development of defined media for the serum-free expansion of primary keratinocytes and human embryonic stem cells. Tissue Eng. Part C Methods 14, 221-232
66. Lietha, D., Cai, X., Ceccarelli, D. F., Li, Y., Schaller, M. D., and Eck, M. J. (2007) Structural basis for the autoinhibition of focal adhesion kinase. Cell 129, 1177-1187 (Pubitemid 46891044)
67. Neff, L., Zeisel, M., Druet, V., Takeda, K., Klein, J. P., Sibilia, J., and Wachsmann, D. (2003) ERK 1/2- and JNKs-dependent synthesis of interleukins 6 and 8 by fibroblast-like synoviocytes stimulated with protein I/II, a modulin from oral streptococci, requires focal adhesion kinase. J. Biol. Chem. 278, 27721-27728 (Pubitemid 36899961)
68. Mould, A. P., Symonds, E. J., Buckley, P. A., Grossmann, J. G., McEwan, P. A., Barton, S. J., Askari, J. A., Craig, S. E., Bella, J., and Humphries, M. J. (2003) Structure of an integrin-ligand complex deduced from solution x-ray scattering and site-directed mutagenesis. J. Biol. Chem. 278, 39993-39999 (Pubitemid 37248564)
69. Semaan, N., Alsaleh, G., Gottenberg, J. E., Wachsmann, D., and Sibilia, J. (2008) Etk/BMX, a Btk family tyrosine kinase, and Mal contribute to the cross-talk between MyD88 and FAK pathways. J. Immunol. 180, 3485-3491
70. Zeisel, M. B., Druet, V. A., Sibilia, J., Klein, J. P., Quesniaux, V., and Wachsmann, D. (2005) Cross-talk between MyD88 and focal adhesion kinase pathways. J. Immunol. 174, 7393-7397 (Pubitemid 40705710)
71. Nolan, K., Lacoste, J., and Parsons, J. T. (1999) Regulated expression of focal adhesion kinase-related nonkinase, the autonomously expressed Cterminal domain of focal adhesion kinase. Mol. Cell Biol. 19, 6120-6129 (Pubitemid 29399317)
72. Richardson, A., and Parsons, T. (1996) A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 380, 538-540
73. Gilmore, A. P., and Romer, L. H. (1996) Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell 7, 1209-1224 (Pubitemid 26260738)
74. Xu, L. H., Yang, X., Bradham, C. A., Brenner, D. A., Baldwin, A. S., Jr., Craven, R. J., and Cance, W. G. (2000) The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. Involvement of death receptor-related signaling pathways. J. Biol. Chem. 275, 30597-30604