The long pentraxin PTX3 as a correlate of cancer-related inflammation and prognosis of malignancy in gliomas

Journal of Neuroimmunology

Volumn 260, Issue 1-2, 2013, Pages 99-106

  Locatelli, Marco ^a   Ferrero, Stefano ^b   Martinelli Boneschi, Filippo ^c   Boiocchi, Leonardo ^b   Zavanone, Mario ^a,b   Maria Gaini, Sergio ^a,b   Bello, Lorenzo ^b,d   Valentino, Sonia ^d   Barbati, Elisa ^d   Nebuloni, Manuela ^e   Mantovani, Alberto ^b,d   Garlanda, Cecilia ^d  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

Cancer associated inflammation; Glioma; Immunohistochemistry; Macrophage; PTX3

Indexed keywords

CD68 ANTIGEN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PENTRAXIN 3;

ADULT; ARTICLE; ASTROCYTOMA; CANCER GRADING; CANCER PROGNOSIS; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME DELETION; CHROMOSOME DELETION 19Q; CHROMOSOME DELETION 1P; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GLIOBLASTOMA; GLIOMA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; OLIGODENDROGLIOMA; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT;

ADULT; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BRAIN NEOPLASMS; C-REACTIVE PROTEIN; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; ENCEPHALITIS; FEMALE; GLIOBLASTOMA; HUMANS; LOGISTIC MODELS; MACROPHAGES; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM GRADING; OLIGODENDROGLIOMA; PREDICTIVE VALUE OF TESTS; PROGNOSIS; SERUM AMYLOID P-COMPONENT; SEVERITY OF ILLNESS INDEX; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS;

EID: 84878658286     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2013.04.009     Document Type: Article

References (61)

1. Agrawal A. CRP after 2004. Mol. Immunol. 2005, 42:927-930.
2. Atkinson G.P., Nozell S.E., Harrison D.K., Stonecypher M.S., Chen D., Benveniste E.N. The prolyl isomerase Pin1 regulates the NF-kappaB signaling pathway and interleukin-8 expression in glioblastoma. Oncogene 2009, 28:3735-3745.
3. Balkwill F., Charles K.A., Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005, 7:211-217.
4. Barbashina V., Salazar P., Holland E.C., Rosenblum M.K., Ladanyi M. Allelic losses at 1p36 and 19q13 in gliomas: correlation with histologic classification, definition of a 150-kb minimal deleted region on 1p36, and evaluation of CAMTA1 as a candidate tumor suppressor gene. Clin. Cancer Res. 2005, 11:1119-1128.
5. Bellail A.C., Hunter S.B., Brat D.J., Tan C., Van Meir E.G. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int. J. Biochem. Cell Biol. 2004, 36:1046-1069.
6. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
7. Bottazzi B., Doni A., Garlanda C., Mantovani A. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu. Rev. Immunol. 2010, 28:157-183.
8. Bourne T.D., Schiff D. Update on molecular findings, management and outcome in low-grade gliomas. Nat. Rev. Neurol. 2010, 6:695-701.
9. Brat D.J., Bellail A.C., Van Meir E.G. The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro Oncol. 2005, 7:122-133.
10. Bryan L., Paugh B.S., Kapitonov D., Wilczynska K.M., Alvarez S.M., Singh S.K., Milstien S., Spiegel S., Kordula T. 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.
11. Colotta F., Allavena P., Sica A., Garlanda C., Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009, 30:1073-1081.
12. Deban L., Russo R.C., Sironi M., Moalli F., Scanziani M., Zambelli V., Cuccovillo I., Bastone A., Gobbi M., Valentino S., Doni A., Garlanda C., Danese S., Salvatori G., Sassano M., Evangelista V., Rossi B., Zenaro E., Constantin G., Laudanna C., Bottazzi B., Mantovani A. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat. Immunol. 2010, 11:328-334.
13. Desbaillets I., Diserens A.C., Tribolet N., Hamou M.F., Van Meir E.G. Upregulation of interleukin 8 by oxygen-deprived cells in glioblastoma suggests a role in leukocyte activation, chemotaxis, and angiogenesis. J. Exp. Med. 1997, 186:1201-1212.
14. Diamandis E.P., Goodglick L., Planque C., Thornquist M.D. Pentraxin-3 is a novel biomarker of lung carcinoma. Clin. Cancer Res. 2011, 17:2395-2399.
15. Doni A., Peri G., Chieppa M., Allavena P., Pasqualini F., Vago L., Romani L., Garlanda C., Mantovani A. Production of the soluble pattern recognition receptor PTX3 by myeloid, but not plasmacytoid, dendritic cells. Eur. J. Immunol. 2003, 33:2886-2893.
16. Doni A., Garlanda C., Bottazzi B., Meri S., Garred P., Mantovani A. Interactions of the humoral pattern recognition molecule PTX3 with the complement system. Immunobiology 2012, 217:1122-1128.
17. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
18. Engelhorn T., Savaskan N.E., Schwarz M.A., Kreutzer J., Meyer E.P., Hahnen E., Ganslandt O., Dorfler A., Nimsky C., Buchfelder M., Eyupoglu I.Y. Cellular characterization of the peritumoral edema zone in malignant brain tumors. Cancer Sci. 2009, 100:1856-1862.
19. Erreni M., Solinas G., Brescia P., Osti D., Zunino F., Colombo P., Destro A., Roncalli M., Mantovani A., Draghi R., Levi D., Rodriguez Y.B.R., Gaetani P., Pelicci G., Allavena P. Human glioblastoma tumours and neural cancer stem cells express the chemokine CX3CL1 and its receptor CX3CR1. Eur. J. Cancer 2010, 46:3383-3392.
20. Ferrer-Luna R., Mata M., Nunez L., Calvar J., Dasi F., Arias E., Piquer J., Cerda-Nicolas M., Taratuto A.L., Sevlever G., Celda B., Martinetto H. Loss of heterozygosity at 1p-19q induces a global change in oligodendroglial tumor gene expression. J. Neurooncol. 2009, 95:343-354.
21. Ferrer-Luna R., Nunez L., Piquer J., Arias E., Dasi F., Cervio A., Arakaki N., Sevlever G., Celda B., Martinetto H. Whole-genomic survey of oligodendroglial tumors: correlation between allelic imbalances and gene expression profiles. J. Neurooncol. 2011, 103:71-85.
22. Garlanda C., Bottazzi B., Bastone A., Mantovani A. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 2005, 23:337-366.
23. Germano G., Frapolli R., Simone M., Tavecchio M., Erba E., Pesce S., Pasqualini F., Grosso F., Sanfilippo R., Casali P.G., Gronchi A., Virdis E., Tarantino E., Pilotti S., Greco A., Nebuloni M., Galmarini C.M., Tercero J.C., Mantovani A., D'Incalci M., Allavena P. Antitumor and anti-inflammatory effects of trabectedin on human myxoid liposarcoma cells. Cancer Res. 2010, 70:2235-2244.
24. Hegi M.E., Diserens A.C., Gorlia T., Hamou M.F., de Tribolet N., Weller M., Kros J.M., Hainfellner J.A., Mason W., Mariani L., Bromberg J.E., Hau P., Mirimanoff R.O., Cairncross J.G., Janzer R.C., Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 2005, 352:997-1003.
25. Idbaih A., Omuro A., Ducray F., Hoang-Xuan K. Molecular genetic markers as predictors of response to chemotherapy in gliomas. Curr. Opin. Oncol. 2007, 19:606-611.
26. Inforzato A., Jaillon S., Moalli F., Barbati E., Bonavita E., Bottazzi B., Mantovani A., Garlanda C. The long pentraxin PTX3 at the crossroads between innate immunity and tissue remodelling. Tissue Antigens 2011, 77:271-282.
27. Jaillon S., Peri G., Delneste Y., Fremaux I., Doni A., Moalli F., Garlanda C., Romani L., Gascan H., Bellocchio S., Bozza S., Cassatella M.A., Jeannin P., Mantovani A. The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J. Exp. Med. 2007, 204:793-804.
28. Jeon H., Lee S., Lee W.H., Suk K. Analysis of glial secretome: the long pentraxin PTX3 modulates phagocytic activity of microglia. J. Neuroimmunol. 2010, 229:63-72.
29. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006, 441:431-436.
30. Kuppner M.C., Hamou M.F., de Tribolet N. Immunohistological and functional analyses of lymphoid infiltrates in human glioblastomas. Cancer Res. 1988, 48:6926-6932.
31. Locatelli M., Boiocchi L., Ferrero S., Martinelli Boneschi F., Zavanone M., Pesce S., Allavena P., Maria Gaini S., Bello L., Mantovani A. Human glioma tumors express high levels of the chemokine receptor CX3CR1. Eur. Cytokine Netw. 2010, 21:27-33.
32. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
33. 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.
34. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
35. Marchesi F., Piemonti L., Fedele G., Destro A., Roncalli M., Albarello L., Doglioni C., Anselmo A., Doni A., Bianchi P., Laghi L., Malesci A., Cervo L., Malosio M., Reni M., Zerbi A., Di Carlo V., Mantovani A., Allavena P. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res. 2008, 68:9060-9069.
36. Muller B., Peri G., Doni A., Torri V., Landmann R., Bottazzi B., Mantovani A. Circulating levels of the long pentraxin PTX3 correlate with severity of infection in critically ill patients. Crit. Care Med. 2001, 29:1404-1407.
37. Murat A., Migliavacca E., Hussain S.F., Heimberger A.B., Desbaillets I., Hamou M.F., Ruegg C., Stupp R., Delorenzi M., Hegi M.E. Modulation of angiogenic and inflammatory response in glioblastoma by hypoxia. PLoS One 2009, 4:e5947.
38. Norata G.D., Garlanda C., Catapano A.L. The long pentraxin PTX3: a modulator of the immunoinflammatory response in atherosclerosis and cardiovascular diseases. Trends Cardiovasc. Med. 2010, 20:35-40.
39. Palmisano W.A., Divine K.K., Saccomanno G., Gilliland F.D., Baylin S.B., Herman J.G., Belinsky S.A. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res. 2000, 60:5954-5958.
40. Paugh B.S., Bryan L., Paugh S.W., Wilczynska K.M., Alvarez S.M., Singh S.K., Kapitonov D., Rokita H., Wright S., Griswold-Prenner I., Milstien S., Spiegel S., Kordula T. Interleukin-1 regulates the expression of sphingosine kinase 1 in glioblastoma cells. J. Biol. Chem. 2009, 284:3408-3417.
41. Perdiki M., Korkolopoulou P., Thymara I., Agrogiannis G., Piperi C., Boviatsis E., Kotsiakis X., Angelidakis D., Diamantopoulou K., Thomas-Tsagli E., Patsouris E. Cyclooxygenase-2 expression in astrocytomas. Relationship with microvascular parameters, angiogenic factors expression and survival. Mol. Cell. Biochem. 2007, 295:75-83.
42. Phillips H.S., Kharbanda S., Chen R., Forrest W.F., Soriano R.H., Wu T.D., Misra A., Nigro J.M., Colman H., Soroceanu L., Williams P.M., Modrusan Z., Feuerstein B.G., Aldape K. 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.
43. Planque C., Kulasingam V., Smith C.R., Reckamp K., Goodglick L., Diamandis E.P. Identification of five candidate lung cancer biomarkers by proteomics analysis of conditioned media of four lung cancer cell lines. Mol. Cell. Proteomics 2009, 8:2746-2758.
44. Presta M., Camozzi M., Salvatori G., Rusnati M. Role of the soluble pattern recognition receptor PTX3 in vascular biology. J. Cell. Mol. Med. 2007, 11:723-738.
45. Ravenna L., Sale P., Di Vito M., Russo A., Salvatori L., Tafani M., Mari E., Sentinelli S., Petrangeli E., Gallucci M., Di Silverio F., Russo M.A. Up-regulation of the inflammatory-reparative phenotype in human prostate carcinoma. Prostate 2009, 69:1245-1255.
46. Raychaudhuri B., Han Y., Lu T., Vogelbaum M.A. Aberrant constitutive activation of nuclear factor kappaB in glioblastoma multiforme drives invasive phenotype. J. Neurooncol. 2007, 85:39-47.
47. Rius J., Guma M., Schachtrup C., Akassoglou K., Zinkernagel A.S., Nizet V., Johnson R.S., Haddad G.G., Karin M. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 2008, 453:807-811.
48. Salio M., Chimenti S., De Angelis N., Molla F., Maina V., Nebuloni M., Pasqualini F., Latini R., Garlanda C., Mantovani A. Cardioprotective function of the long pentraxin PTX3 in acute myocardial infarction. Circulation 2008, 117:1055-1064.
49. Samaras V., Piperi C., Levidou G., Zisakis A., Kavantzas N., Themistocleous M.S., Boviatsis E.I., Barbatis C., Lea R.W., Kalofoutis A., Korkolopoulou P. Analysis of interleukin (IL)-8 expression in human astrocytomas: associations with IL-6, cyclooxygenase-2, vascular endothelial growth factor, and microvessel morphometry. Hum. Immunol. 2009, 70:391-397.
50. Sarkar S., Yong V.W. Inflammatory cytokine modulation of matrix metalloproteinase expression and invasiveness of glioma cells in a 3-dimensional collagen matrix. J. Neurooncol. 2009, 91:157-164.
51. Schomas D.A., Laack N.N., Rao R.D., Meyer F.B., Shaw E.G., O'Neill B.P., Giannini C., Brown P.D. Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro Oncol. 2009, 11:437-445.
52. Sen E. Targeting inflammation-induced transcription factor activation: an open frontier for glioma therapy. Drug Discov. Today 2011, 16:1044-1051.
53. Smith J.S., Perry A., Borell T.J., Lee H.K., O'Fallon J., Hosek S.M., Kimmel D., Yates A., Burger P.C., Scheithauer B.W., Jenkins R.B. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J. Clin. Oncol. 2000, 18:636-645.
54. Sun L., Hui A.M., Su Q., Vortmeyer A., Kotliarov Y., Pastorino S., Passaniti A., Menon J., Walling J., Bailey R., Rosenblum M., Mikkelsen T., Fine H.A. Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 2006, 9:287-300.
55. Tafani M., Russo A., Di Vito M., Sale P., Pellegrini L., Schito L., Gentileschi S., Bracaglia R., Marandino F., Garaci E., Russo M.A. Up-regulation of pro-inflammatory genes as adaptation to hypoxia in MCF-7 cells and in human mammary invasive carcinoma microenvironment. Cancer Sci. 2010, 101:1014-1023.
56. Tafani M., Di Vito M., Frati A., Pellegrini L., De Santis E., Sette G., Eramo A., Sale P., Mari E., Santoro A., Raco A., Salvati M., De Maria R., Russo M.A. Pro-inflammatory gene expression in solid glioblastoma microenvironment and in hypoxic stem cells from human glioblastoma. J. Neuroinflammation 2011, 8:32.
57. Tothill R.W., Tinker A.V., George J., Brown R., Fox S.B., Lade S., Johnson D.S., Trivett M.K., Etemadmoghadam D., Locandro B., Traficante N., Fereday S., Hung J.A., Chiew Y.E., Haviv I., Gertig D., DeFazio A., Bowtell D.D. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res. 2008, 14:5198-5208.
58. van Rossum A.P., Pas H.H., Fazzini F., Huitema M.G., Limburg P.C., Jonkman M.F., Kallenberg C.G. Abundance of the long pentraxin PTX3 at sites of leukocytoclastic lesions in patients with small-vessel vasculitis. Arthritis Rheum. 2006, 54:986-991.
59. Wen P.Y., Kesari S. Malignant gliomas in adults. N. Engl. J. Med. 2008, 359:492-507.
60. Willeke F., Assad A., Findeisen P., Schromm E., Grobholz R., von Gerstenbergk B., Mantovani A., Peri S., Friess H.H., Post S., von Knebel Doeberitz M., Schwarzbach M.H. Overexpression of a member of the pentraxin family (PTX3) in human soft tissue liposarcoma. Eur. J. Cancer 2006, 42:2639-2646.
61. Yeung Y.T., Bryce N.S., Adams S., Braidy N., Konayagi M., McDonald K.L., Teo C., Guillemin G.J., Grewal T., Munoz L. p38 MAPK inhibitors attenuate pro-inflammatory cytokine production and the invasiveness of human U251 glioblastoma cells. J. Neurooncol. 2012, 109:35-44.