Interleukin-1-induced changes in the glioblastoma secretome suggest its role in tumor progression

Journal of Proteomics

Volumn 99, Issue , 2014, Pages 152-168

  Tarassishin, Leonid ^a   Lim, Jihyeon ^a   Weatherly, D Brent ^b   Angeletti, Ruth H ^a   Lee, Sunhee C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Extracellular matrix; Innate immunity; Interleukin 1; Label free quantitation; Secretome; TGF

Indexed keywords

EXTRACELLULAR MATRIX; INNATE IMMUNITY; INTERLEUKIN-1; LABEL FREE QUANTITATION; SECRETOME; TGFΒ;

CELL LINE, TUMOR; CELL MOVEMENT; GLIOBLASTOMA; HUMANS; INTERLEUKIN-1; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PROTEOME; TUMOR MICROENVIRONMENT;

EID: 84894288399     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.01.024     Document Type: Article

References (100)

1. Sul J., Fine H.A. Malignant gliomas: new translational therapies Mt Sinai. J Med 2010, 77:655-666.
2. Henriksson R., Asklund T., Poulsen H.S. Impact of therapy on quality of life, neurocognitive function and their correlates in glioblastoma multiforme: a review. J Neurooncol 2011, 104:639-646.
3. Charles N.A., Holland E.C., Gilbertson R., Glass R., Kettenmann H. The brain tumor microenvironment. Glia 2011, 59:1169-1180.
4. Kleihues P., Soylemezoglu F., Schauble B., Scheithauer B.W., Burger P.C. Histopathology, classification, and grading of gliomas. Glia 1995, 15:211-221.
5. Heimberger A.B., Sampson J.H. Immunotherapy coming of age: what will it take to make it standard of care for glioblastoma?. Neuro Oncol 2011, 13:3-13.
6. Basu A., Krady J.K., Levison S.W. Interleukin-1: a master regulator of neuroinflammation. J Neurosci Res 2004, 78:151-156.
7. Mrak R.E., Griffin W.S. Interleukin-1, neuroinflammation, and Alzheimer's disease. Neurobiol Aging 2001, 22:903-908.
8. Simi A., Tsakiri N., Wang P., Rothwell N.J. Interleukin-1 and inflammatory neurodegeneration. Biochem Soc Trans 2007, 35:1122-1126.
9. John G.R., Lee S.C., Song X., Rivieccio M., Brosnan C.F. IL-1-regulated responses in astrocytes: relevance to injury and recovery. Glia 2005, 49:161-176.
10. Tarassishin L., Lee S.C. Interferon regulatory factor 3 alters glioma inflammatory and invasive properties. J Neurooncol 2013, 113:185-194.
11. Lu T., Tian L., Han Y., Vogelbaum M., Stark G.R. Dose-dependent cross-talk between the transforming growth factor-beta and interleukin-1 signaling pathways. Proc Natl Acad Sci U S A 2007, 104:4365-4370.
12. Sasaki A., Tamura M., Hasegawa M., Ishiuchi S., Hirato J., Nakazato Y. Expression of interleukin-1beta mRNA and protein in human gliomas assessed by RT-PCR and immunohistochemistry. J Neuropathol Exp Neurol 1998, 57:653-663.
13. Lee S.C., Liu W., Dickson D.W., Brosnan C.F., Berman J.W. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J Immunol 1993, 150:2659-2667.
14. John G.R., Lee S.C., Brosnan C.F. Cytokines: powerful regulators of glial cell activation. Neuroscientist 2003, 9:10-22.
15. Basu A., Krady J.K., O'Malley M., Styren S.D., DeKosky S.T., Levison S.W. The type 1 interleukin-1 receptor is essential for the efficient activation of microglia and the induction of multiple proinflammatory mediators in response to brain injury. J Neurosci 2002, 22:6071-6082.
16. Downen M., Amaral T.D., Hua L.L., Zhao M.L., Lee S.C. Neuronal death in cytokine-activated primary human brain cell culture: role of tumor necrosis factor-alpha. Glia 1999, 28:114-127.
17. Rothwell N. Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. Brain Behav Immun 2003, 17:152-157.
18. Zitvogel L., Kepp O., Galluzzi L., Kroemer G. Inflammasomes in carcinogenesis and anticancer immune responses. Nat Immunol 2012, 13:343-351.
19. Sen E. Targeting inflammation-induced transcription factor activation: an open frontier for glioma therapy. Drug Discov Today 2011, 16:1044-1051.
20. Morgan A.C., Chang H.Y., Liu J.S., Hua L.L., Lee S.C. High extracellular potassium modulates nitric oxide synthase expression in human astrocytes. J Neurochem 2000, 74:1903-1912.
21. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1:2856-2860.
22. Deutsch E.W., Mendoza L., Shteynberg D., Farrah T., Lam H., Tasman N., et al. A guided tour of the trans-proteomic pipeline. Proteomics 2010, 10:1150-1159.
23. Mi H., Dong Q., Muruganujan A., Gaudet P., Lewis S., Thomas P.D. PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 2010, 38:D204-D210.
24. Bendtsen J.D., Jensen L.J., Blom N., von H.G., Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004, 17:349-356.
25. Thomas P.D., Kejariwal A., Campbell M.J., Mi H., Diemer K., Guo N., et al. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res 2003, 31:334-341.
26. Nickel W. Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 2005, 6:607-614.
27. Kucharzewska P., Christianson H.C., Welch J.E., Svensson K.J., Fredlund E., Ringner M., et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A 2013, 110:7312-7317.
28. Lopez L.C., Youakim A., Evans S.C., Shur B.D. Evidence for a molecular distinction between Golgi and cell surface forms of beta 1,4-galactosyltransferase. J Biol Chem 1991, 266:15984-15991.
29. Formolo C.A., Williams R., Gordish-Dressman H., MacDonald T.J., Lee N.H., Hathout Y. Secretome signature of invasive glioblastoma multiforme. J Proteome Res 2011, 10:3149-3159.
30. Polisetty R.V., Gupta M.K., Nair S.C., Ramamoorthy K., Tiwary S., Shiras A., et al. Glioblastoma cell secretome: analysis of three glioblastoma cell lines reveal 148 non-redundant proteins. J Proteomics 2011, 74:1918-1925.
31. Khwaja F.W., Svoboda P., Reed M., Pohl J., Pyrzynska B., Van Meir E.G. Proteomic identification of the wt-p53-regulated tumor cell secretome. Oncogene 2006, 25:7650-7661.
32. Dwyer J., Hebda J.K., Le G.A., Galan-Moya E.M., Smith S.S., Azzi S., et al. Glioblastoma cell-secreted interleukin-8 induces brain endothelial cell permeability via CXCR2. PLoS One 2012, 7:e45562.
33. Zhang J., Sarkar S., Cua R., Zhou Y., Hader W., Yong V.W. A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinogenesis 2012, 33:312-319.
34. Zhu X., Fujita M., Snyder L.A., Okada H. Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J Neurooncol 2011, 104:83-92.
35. Cieslik P., Hrycek A. Long pentraxin 3 (PTX3) in the light of its structure, mechanism of action and clinical implications. Autoimmunity 2012, 45:119-128.
36. Deban L., Jaillon S., Garlanda C., Bottazzi B., Mantovani A. Pentraxins in innate immunity: lessons from PTX3. Cell Tissue Res 2011, 343:237-249.
37. Ravizza T., Moneta D., Bottazzi B., Peri G., Garlanda C., Hirsch E., et al. Dynamic induction of the long pentraxin PTX3 in the CNS after limbic seizures: evidence for a protective role in seizure-induced neurodegeneration. Neuroscience 2001, 105(1):43-53.
38. Polentarutti N., Bottazzi B., Di S.E., Blasi E., Agnello D., Ghezzi P., et al. Inducible expression of the long pentraxin PTX3 in the central nervous system. J Neuroimmunol 2000, 106(3):87-94.
39. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
40. Penuelas S., Anido J., Prieto-Sanchez R.M., Folch G., Barba I., Cuartas I., et al. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009, 15:315-327.
41. Dieterich L.C., Mellberg S., Langenkamp E., Zhang L., Zieba A., Salomaki H., et al. Transcriptional profiling of human glioblastoma vessels indicates a key role of VEGF-A and TGFbeta2 in vascular abnormalization. J Pathol 2012, 228:378-390.
42. Carro M.S., Lim W.K., Alvarez M.J., Bollo R.J., Zhao X., Snyder E.Y., et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010, 463:318-325.
43. Brantley E.C., Benveniste E.N. Signal transducer and activator of transcription-3: a molecular hub for signaling pathways in gliomas. Mol Cancer Res 2008, 6:675-684.
44. Pen A., Moreno M.J., Durocher Y., Deb-Rinker P., Stanimirovic D.B. Glioblastoma-secreted factors induce IGFBP7 and angiogenesis by modulating Smad-2-dependent TGF-beta signaling. Oncogene 2008, 27:6834-6844.
45. Munger J.S., Sheppard D. Cross talk among TGF-beta signaling pathways, integrins, and the extracellular matrix. Cold Spring Harb Perspect Biol 2011, 3:a005017.
46. Neptune E.R., Frischmeyer P.A., Arking D.E., Myers L., Bunton T.E., Gayraud B., et al. Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet 2003, 33:407-411.
47. Doyle J.J., Gerber E.E., Dietz H.C. Matrix-dependent perturbation of TGFbeta signaling and disease. FEBS Lett 2012, 586:2003-2015.
48. Hu Y., Pioli P.D., Siegel E., Zhang Q., Nelson J., Chaturbedi A., et al. EFEMP1 suppresses malignant glioma growth and exerts its action within the tumor extracellular compartment. Mol Cancer 2011, 10:123.
49. Kim Y.H., Kwon H.J., Kim D.S. Matrix metalloproteinase 9 (MMP-9)-dependent processing of betaig-h3 protein regulates cell migration, invasion, and adhesion. J Biol Chem 2012, 287:38957-38969.
50. Nam J.O., Son H.N., Jun E., Cha K., Lee B.H., Park R.W., et al. FAS1 domain protein inhibits VEGF165-induced angiogenesis by targeting the interaction between VEGFR-2 and alphavbeta3 integrin. Mol Cancer Res 2012, 10:1010-1020.
51. Gritsenko P.G., Ilina O., Friedl P. Interstitial guidance of cancer invasion. J Pathol 2012, 226:185-199.
52. Rettig W.J., Erickson H.P., Albino A.P., Garin-Chesa P. Induction of human tenascin (neuronectin) by growth factors and cytokines: cell type-specific signals and signalling pathways. J Cell Sci 1994, 107(Pt 2):487-497.
53. Midwood K.S., Hussenet T., Langlois B., Orend G. Advances in tenascin-C biology. Cell Mol Life Sci 2011, 68:3175-3199.
54. Sarkar S., Nuttall R.K., Liu S., Edwards D.R., Yong V.W. Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-1215. Cancer Res 2006, 66:11771-11780.
55. Herold-Mende C., Mueller M.M., Bonsanto M.M., Schmitt H.P., Kunze S., Steiner H.H. Clinical impact and functional aspects of tenascin-C expression during glioma progression. Int J Cancer 2002, 98:362-369.
56. Huang J.Y., Cheng Y.J., Lin Y.P., Lin H.C., Su C.C., Juliano R., et al. Extracellular matrix of glioblastoma inhibits polarization and transmigration of T cells: the role of tenascin-C in immune suppression. J Immunol 2010, 185:1450-1459.
57. Wuchty S., Arjona D., Li A., Kotliarov Y., Walling J., Ahn S., et al. Prediction of associations between microRNAs and gene expression in glioma biology. PLoS One 2011, 6:e14681.
58. Nowinski D., Koskela A., Kiwanuka E., Bostrom M., Gerdin B., Ivarsson M. Inhibition of connective tissue growth factor/CCN2 expression in human dermal fibroblasts by interleukin-1alpha and beta. J Cell Biochem 2010, 110:1226-1233.
59. Chong H.C., Tan C.K., Huang R.L., Tan N.S. Matricellular proteins: a sticky affair with cancers. J Oncol 2012, 2012:351089.
60. Lopez-Dee Z., Pidcock K., Gutierrez L.S. Thrombospondin-1: multiple paths to inflammation. Mediators Inflamm 2011, 2011:296069.
61. Nakada M., Miyamori H., Yamashita J., Sato H. Testican 2 abrogates inhibition of membrane-type matrix metalloproteinases by other testican family proteins. Cancer Res 2003, 63:3364-3369.
62. Paulus W., Baur I., Dours-Zimmermann M.T., Zimmermann D.R. Differential expression of versican isoforms in brain tumors. J Neuropathol Exp Neurol 1996, 55:528-533.
63. Arslan F., Bosserhoff A.K., Nickl-Jockschat T., Doerfelt A., Bogdahn U., Hau P. The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-beta2. Br J Cancer 2007, 96:1560-1568.
64. Kaminska B., Kocyk M., Kijewska M. TGF beta signaling and its role in glioma pathogenesis. Adv Exp Med Biol 2013, 986:171-187.
65. Yong V.W., Power C., Forsyth P., Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001, 2:502-511.
66. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 2005, 6:931-944.
67. Bryan L., Paugh B.S., Kapitonov D., Wilczynska K.M., Alvarez S.M., Singh S.K., et al. Sphingosine-1-phosphate and interleukin-1 independently regulate plasminogen activator inhibitor-1 and urokinase-type plasminogen activator receptor expression in glioblastoma cells: implications for invasiveness. Mol Cancer Res 2008, 6:1469-1477.
68. Colin C., Voutsinos-Porche B., Nanni I., Fina F., Metellus P., Intagliata D., et al. High expression of cathepsin B and plasminogen activator inhibitor type-1 are strong predictors of survival in glioblastomas. Acta Neuropathol 2009, 118:745-754.
69. Yamaguchi Y., Shao Z., Sharif S., Du X.Y., Myles T., Merchant M., et al. Thrombin-cleaved fragments of osteopontin are overexpressed in malignant glial tumors and provide a molecular niche with survival advantage. J Biol Chem 2013, 288:3097-3111.
70. Yamahata H., Takeshima H., Kuratsu J., Sarker K.P., Tanioka K., Wakimaru N., et al. The role of thrombin in the neo-vascularization of malignant gliomas: an intrinsic modulator for the up-regulation of vascular endothelial growth factor. Int J Oncol 2002, 20:921-928.
71. Isaka T., Yoshimine T., Maruno M., Kuroda R., Ishii H., Hayakawa T. Altered expression of antithrombotic molecules in human glioma vessels. Acta Neuropathol 1994, 87:81-85.
72. Le M.M., Fortin S., Mathieu V., Kiss R., Lefranc F. Galectins and gliomas. Brain Pathol 2010, 20:17-27.
73. Starossom S.C., Mascanfroni I.D., Imitola J., Cao L., Raddassi K., Hernandez S.F., et al. Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 2012, 37:249-263.
74. Jiang J., Westberg J.A., Andersson L.C. Stanniocalcin 2, forms a complex with heme oxygenase 1, binds hemin and is a heat shock protein. Biochem Biophys Res Commun 2012, 421:274-279.
75. Westberg J.A., Serlachius M., Lankila P., Penkowa M., Hidalgo J., Andersson L.C. Hypoxic preconditioning induces neuroprotective stanniocalcin-1 in brain via IL-6 signaling. Stroke 2007, 38:1025-1030.
76. Hill J.J., Moreno M.J., Lam J.C., Haqqani A.S., Kelly J.F. Identification of secreted proteins regulated by cAMP in glioblastoma cells using glycopeptide capture and label-free quantification. Proteomics 2009, 9:535-549.
77. Sepporta M.V., Tumminello F.M., Flandina C., Crescimanno M., Giammanco M., La G.M., et al. Follistatin as potential therapeutic target in prostate cancer. Target Oncol 2013, 8:215-223.
78. Reddy S.P., Britto R., Vinnakota K., Aparna H., Sreepathi H.K., Thota B., et al. Novel glioblastoma markers with diagnostic and prognostic value identified through transcriptome analysis. Clin Cancer Res 2008, 14:2978-2987.
79. Vadasz Z., Toubi E. Semaphorins: their dual role in regulating immune-mediated diseases. Clin Rev Allergy Immunol 2013, [Electronic publication ahead of print].
80. Tamagnone L. Emerging role of semaphorins as major regulatory signals and potential therapeutic targets in cancer. Cancer Cell 2012, 22:145-152.
81. Bagci T., Wu J.K., Pfannl R., Ilag L.L., Jay D.G. Autocrine semaphorin 3A signaling promotes glioblastoma dispersal. Oncogene 2009, 28:3537-3550.
82. Tanco S., Zhang X., Morano C., Aviles F.X., Lorenzo J., Fricker L.D. Characterization of the substrate specificity of human carboxypeptidase A4 and implications for a role in extracellular peptide processing. J Biol Chem 2010, 285:18385-18396.
83. Ross P.L., Cheng I., Liu X., Cicek M.S., Carroll P.R., Casey G., et al. Carboxypeptidase 4 gene variants and early-onset intermediate-to-high risk prostate cancer. BMC Cancer 2009, 9:69.
84. Shannan B., Seifert M., Leskov K., Willis J., Boothman D., Tilgen W., et al. Challenge and promise: roles for clusterin in pathogenesis, progression and therapy of cancer. Cell Death Differ 2006, 13:12-19.
85. Bello L., Lucini V., Carrabba G., Giussani C., Machluf M., Pluderi M., et al. Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2. Cancer Res 2001, 61:8730-8736.
86. Gnad F., Gunawardena J., Mann M. PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res 2011, 39:D253-D260.
87. Jellinek D.A., Chang A.C., Larsen M.R., Wang X., Robinson P.J., Reddel R.R. Stanniocalcin 1 and 2 are secreted as phosphoproteins from human fibrosarcoma cells. Biochem J 2000, 350(Pt 2):453-461.
88. Neilson K.A., Ali N.A., Muralidharan S., Mirzaei M., Mariani M., Assadourian G., et al. Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011, 11:535-553.
89. Venugopal C., Wang X.S., Manoranjan B., McFarlane N., Nolte S., Li M., et al. GBM secretome induces transient transformation of human neural precursor cells. J Neurooncol 2012, 109:457-466.
90. Phillips H.S., Kharbanda S., Chen R., Forrest W.F., Soriano R.H., Wu T.D., et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006, 9:157-173.
91. Huse J.T., Phillips H.S., Brennan C.W. Molecular subclassification of diffuse gliomas: seeing order in the chaos. Glia 2011, 59:1190-1199.
92. Feinstein D.L., Heneka M.T., Gavrilyuk V., Dello R.C., Weinberg G., Galea E. Noradrenergic regulation of inflammatory gene expression in brain. Neurochem Int 2002, 41:357-365.
93. Dinarello C.A. Why not treat human cancer with interleukin-1 blockade?. Cancer Metastasis Rev 2010, 29:317-329.
94. Baltimore D., Boldin M.P., O'Connell R.M., Rao D.S., Taganov K.D. MicroRNAs: new regulators of immune cell development and function. Nat Immunol 2008, 9:839-845.
95. O'Connell R.M., Taganov K.D., Boldin M.P., Cheng G., Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 2007, 104:1604-1609.
96. O'Connell R.M., Rao D.S., Chaudhuri A.A., Boldin M.P., Taganov K.D., Nicoll J., et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 2008, 205:585-594.
97. O'Connell R.M., Kahn D., Gibson W.S., Round J.L., Scholz R.L., Chaudhuri A.A., et al. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 2010, 33:607-619.
98. Tili E., Croce C.M., Michaille J.J. miR-155: on the crosstalk between inflammation and cancer. Int Rev Immunol 2009, 28:264-284.
99. Tili E., Michaille J.J., Wernicke D., Alder H., Costinean S., Volinia S., et al. Mutator activity induced by microRNA-155 (miR-155) links inflammation and cancer. Proc Natl Acad Sci U S A 2011, 108:4908-4913.
100. Okamoto M., Liu W., Luo Y., Tanaka A., Cai X., Norris D.A., et al. Constitutively active inflammasome in human melanoma cells mediating autoinflammation via caspase-1 processing and secretion of interleukin-1beta. J Biol Chem 2010, 285:6477-6488.