Inflammation and pancreatic cancer: Molecular and functional interactions between S100A8, S100A9, NT-S100A8 and TGFβ1

Cell Communication and Signaling

Volumn 12, Issue 1, 2014, Pages 12-20

  Basso, Daniela ^a   Bozzato, Dania ^b   Padoan, Andrea ^b   Moz, Stefania ^b   Zambon, Carlo Federico ^b   Fogar, Paola ^a   Greco, Eliana ^b   Scorzeto, Michele ^b   Simonato, Francesca ^b   Navaglia, Filippo ^a   Fassan, Matteo ^b   Pelloso, Michela ^b   Dupont, Sirio ^b   Pedrazzoli, Sergio ^c   Fassina, Ambrogio ^b   Plebani, Mario ^a,b  

^a UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c Associazione Wirsung onlus   (Italy)

Author keywords

Akt; Calcium; Calcium binding proteins; Epithelial to mesenchymal transition; Mass spectrometry (MS); Matrix metalloproteinase (MMP); mTOR; Pancreatic cancer; SMAD transcription factor

Indexed keywords

CALGRANULIN A; CALGRANULIN B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEPTIDE FRAGMENT; PROTEIN KINASE B; SMAD4 PROTEIN; SMAD4 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CALCIUM SIGNALING; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; HUMAN; INFLAMMATION; METABOLISM; PANCREAS TUMOR; PROTEIN BINDING; PROTEIN DEGRADATION; TUMOR CELL LINE;

CALCIUM SIGNALING; CALGRANULIN A; CALGRANULIN B; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INFLAMMATION; NF-KAPPA B; PANCREATIC NEOPLASMS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84898884031     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-12-20     Document Type: Article

References (61)

1. European cancer mortality predictions for the year 2011. Malvezzi M, Arfé A, Bertuccio P, Levi F, La Vecchia C, Negri E, Ann Oncol 2011 22 947 956 10.1093/annonc/mdq774 21303801
2. Cancer statistics, 2012. Siegel R, Naishadham D, Jemal A, CA Cancer J Clin 2012 62 10 29 10.3322/caac.20138 22237781
3. Pancreatic cancer. Hidalgo M, N Engl J Med 2010 362 1605 1617 10.1056/NEJMra0901557 20427809
4. Pancreatic cancer biology and genetics. Bardeesy N, DePinho RA, Nat Rev Cancer 2002 2 897 909 10.1038/nrc949 12459728 (Pubitemid 37328891)
5. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Aguirre AJ, Bardeesy N, Sinha M, Lopez L, Tuveson DA, Horner J, Redston MS, DePinho RA, Genes Dev 2003 17 3112 3126 10.1101/gad.1158703 14681207 (Pubitemid 38040774)
6. Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Bardeesy N, Aguirre AJ, Chu GC, Cheng KH, Lopez LV, Hezel AF, Feng B, Brennan C, Weissleder R, Mahmood U, Hanahan D, Redston MS, Chin L, DePinho RA, Proc Natl Acad Sci USA 2006 103 5947 5952 10.1073/pnas.0601273103 16585505
7. PTEN is a major tumor suppressor in pancreatic ductal adenocarcinoma and regulates an NF-κB-cytokine network. Ying H, Elpek KG, Vinjamoori A, Zimmerman SM, Chu GC, Yan H, Fletcher-Sananikone E, Zhang H, Liu Y, Wang W, Ren X, Zheng H, Kimmelman AC, Paik JH, Lim C, Perry SR, Jiang S, Malinn B, Protopopov A, Colla S, Xiao Y, Hezel AF, Bardeesy N, Turley SJ, Wang YA, Chin L, Thayer SP, DePinho RA, Cancer Discov 2011 1 158 169 10.1158/2159-8290.CD-11- 0031 21984975
8. Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Bardeesy N, Cheng KH, Berger JH, Chu GC, Pahler J, Olson P, Hezel AF, Horner J, Lauwers GY, Hanahan D, DePinho RA, Genes Dev 2006 20 3130 3146 10.1101/gad.1478706 17114584 (Pubitemid 44790628)
9. The pathology and genetics of metastatic pancreatic cancer. Yachida S, Iacobuzio-Donahue CA, Arch Pathol Lab Med 2009 133 413 422 19260747
10. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, Henderson CM, Vilardell F, Wang Z, Keller JW, Banerjee P, Herman JM, Cameron JL, Yeo CJ, Halushka MK, Eshleman JR, Raben M, Klein AP, Hruban RH, Hidalgo M, Laheru D, J Clin Oncol 2009 27 1806 1813 10.1200/JCO.2008.17.7188 19273710
11. SMAD4 gene mutations are associated with poor prognosis in pancreatic cancer. Blackford A, Serrano OK, Wolfgang CL, Parmigiani G, Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Eshleman JR, Goggins M, Jaffee EM, Iacobuzio-Donahue CA, Maitra A, Cameron JL, Olino K, Schulick R, Winter J, Herman JM, Laheru D, Klein AP, Vogelstein B, Kinzler KW, Velculescu VE, Hruban RH, Clin Cancer Res 2009 15 4674 4679 10.1158/1078-0432.CCR-09-0227 19584151
12. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Bierie B, Moses HL, Nat Rev Cancer 2006 6 506 520 10.1038/nrc1926 16794634 (Pubitemid 43980540)
13. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, Calhoun ES, Kamiyama M, Walter K, Nikolskaya T, Nikolsky Y, Hartigan J, Smith DR, Hidalgo M, Leach SD, Klein AP, Jaffee EM, Goggins M, Maitra A, Iacobuzio-Donahue C, Eshleman JR, Kern SE, Hruban RH, et al. Science 2008 321 1801 1806 10.1126/science.1164368 18772397
14. A delicate balance: TGF-beta and the tumor microenvironment. Stover DG, Bierie B, Moses HL, J Cell Biochem 2007 101 851 861 10.1002/jcb.21149 17486574 (Pubitemid 47040867)
15. TGF-β and NF-κB signal pathway cross-talk is mediated through TAK1 and SMAD7 in a subset of head and neck cancers. Freudlsperger C, Bian Y, Contag Wise S, Burnett J, Coupar J, Yang X, Chen Z, Van Waes C, Oncogene 2013 32 1549 1559 10.1038/onc.2012.171 22641218
16. Transforming growth factor-β in the gastrointestinal and hepatic tumor microenvironment. Achyut BR, Yang L, Gastroenterology 2011 141 1167 1178 10.1053/j.gastro.2011.07.048 21839702
17. Transcriptional crosstalk between TGF-β and stem cell pathways in tumor cell invasion: role of EMT promoting Smad complexes. Fuxe J, Vincent T, Garcia de Herreros A, Cell Cycle 2010 9 2363 2374 10.4161/cc.9.12.12050 20519943
18. Transforming growth factor-β induces epithelial to mesenchymal transition and suppresses the proliferation and transdifferentiation of cultured human pancreatic duct cells. Shin JA, Hong OK, Lee HJ, Jeon SY, Kim JW, Lee SH, Cho JH, Lee JM, Choi YH, Chang SA, Son HY, Kim JH, Yoon KH, J Cell Biochem 2011 112 179 188 10.1002/jcb.22929 21069735
19. Response gene to complement-32 enhances metastatic phenotype by mediating transforming growth factor beta-induced epithelial-mesenchymal transition in human pancreatic cancer cell line BxPC-3. Zhu L, Qin H, Li PY, Xu SN, Pang HF, Zhao HZ, Li DM, Zhao Q, J Exp Clin Cancer Res 2012 31 29 10.1186/1756-9966-31-29 22458379
20. Pancreatic cancer. Maitra A, Hruban RH, Annu Rev Pathol 2008 3 157 188 10.1146/annurev.pathmechdis.3.121806.154305 18039136 (Pubitemid 351488279)
21. Inhibiting Cxcr2 disrupts tumor-stromal interactions and improves survival in a mouse model of pancreatic ductal adenocarcinoma. Ijichi H, Chytil A, Gorska AE, Aakre ME, Bierie B, Tada M, Mohri D, Miyabayashi K, Asaoka Y, Maeda S, Ikenoue T, Tateishi K, Wright V, Koike K, Omata M, Moses HL, J Clin Invest 2011 121 4106 4117 10.1172/JCI42754 21926469
22. Biochemical role of the collagen-rich tumour microenvironment in pancreatic cancer progression. Shields MA, Dangi-Garimella S, Redig AJ, Munshi HG, Biochem J 2012 441 541 552 10.1042/BJ20111240 22187935
23. Overexpression of TGF-beta by infiltrated granulocytes correlates with the expression of collagen mRNA in pancreatic cancer. Aoyagi Y, Oda T, Kinoshita T, Nakahashi C, Hasebe T, Ohkohchi N, Ochiai A, Br J Cancer 2004 91 1316 1326 10.1038/sj.bjc.6602141 15365564 (Pubitemid 39424793)
24. Inflammation-associated S100 proteins: new mechanisms that regulate function. Goyette J, Geczy CL, Amino Acids 2011 41 821 842 10.1007/s00726-010- 0528-0 20213444
25. Six S100 genes are clustered on human chromosome 1q21: identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E. Engelkamp D, Schafer BW, Mattei MG, Erne P, Heizmann CW, Proc Natl Acad Sci USA 1995 90 6547 6551 (Pubitemid 23207250)
26. Comparison of DNA gains and losses in primary renal clear cell carcinomas and metastatic sites: importance of 1q and 3p copy number changes in metastatic events. Gronwald J, Storkel S, Holtgreve-Grez H, Hadaczek P, Brinkschmidt C, Jauch A, Lubinski J, Cremer T, Cancer Res 1997 57 481 487 9012478 (Pubitemid 27081668)
27. Positional cloning identifies a novel cyclophilin as a candidate amplified oncogene in 1q21. Meza-Zepeda LA, Forus A, Lygren B, Dahlberg AB, Godager LH, South AP, Marenholz I, Lioumi M, Flørenes VA, Maelandsmo GM, Serra M, Mischke D, Nizetic D, Ragoussis J, Tarkkanen M, Nesland JM, Knuutila S, Myklebost O, Oncogene 2002 21 2261 2269 10.1038/sj.onc.1205339 11948409 (Pubitemid 34311380)
28. S100A8/A9: a Janus-faced molecule in cancer therapy and tumorgenesis. Ghavami S, Chitayat S, Hashemi M, Eshraghi M, Chazin WJ, Halayko AJ, Kerkhoff C, Eur J Pharmacol 2009 625 73 83 10.1016/j.ejphar.2009.08.044 19835859
29. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. Ehrchen JM, Sunderkötter C, Foell D, Vogl T, Roth J, J Leukoc Biol 2009 86 557 566 10.1189/jlb.1008647 19451397
30. RAGE signalling sustains inflammation and promotes tumor development. Gebhardt C, Riehl A, Durchdewald M, Németh J, Fürstenberger G, Müller-Decker K, Enk A, Arnold B, Bierhaus A, Nawroth PP, Hess J, Angel P, J Exp Med 2008 205 275 285 10.1084/jem.20070679 18208974 (Pubitemid 351281593)
31. The expression of S100A8 in pancreatic cancer-associated monocytes is associated with the Smad4 status of pancreatic cancer cells. Sheikh AA, Vimalachandran D, Thompson CC, Jenkins RE, Nedjadi T, Shekouh A, Campbell F, Dodson A, Prime W, Crnogorac-Jurcevic T, Lemoine NR, Costello E, Proteomics 2007 7 1929 1940 10.1002/pmic.200700072 17469085 (Pubitemid 46911010)
32. Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by two-dimensional gel electrophoresis and mass spectrometry. Shen J, Person MD, Zhu J, Abbruzzese JL, Li D, Cancer Res 2004 64 9018 9026 10.1158/0008-5472.CAN- 04-3262 15604267 (Pubitemid 39665512)
33. Smad4 loss is associated with fewer S100A8-positive monocytes in colorectal tumors and attenuated response to S100A8 in colorectal and pancreatic cancer cells. Ang CW, Nedjadi T, Sheikh AA, Tweedle EM, Tonack S, Honap S, Jenkins RE, Park BK, Schwarte-Waldhoff I, Khattak I, Azadeh B, Dodson A, Kalirai H, Neoptolemos JP, Rooney PS, Costello E, Carcinogenesis 2010 31 1541 1551 10.1093/carcin/bgq137 20622003
34. Altered intracellular calcium fluxes in pancreatic cancer induced diabetes mellitus: relevance of the S100A8 N-terminal peptide (NT-S100A8). Basso D, Greco E, Padoan A, Fogar P, Scorzeto M, Fadi E, Bozzato D, Moz S, Navaglia F, Zambon CF, Seraglia R, De Carlo E, Valerio A, Reggiani C, Pedrazzoli S, Plebani M, J Cell Physiol 2011 226 456 468 10.1002/jcp.22355 20717964
35. Extracellular calcium sensing receptor stimulation in human colonic epithelial cells induces intracellular calcium oscillations and proliferation inhibition. Rey O, Young SH, Jacamo R, Moyer MP, Rozengurt E, J Cell Physiol 2010 225 73 83 10.1002/jcp.22198 20648625
36. The Ca-calmodulin-dependent protein kinase cascade. Soderling TR, Trends Biochem Sci 1999 24 232 236 10.1016/S0968-0004(99)01383-3 10366852 (Pubitemid 29317289)
37. Positive regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by mammalian target of rapamycin (mTOR) in RINm5F cells. Frégeau MO, Régimbald-Dumas Y, Guillemette G, J Cell Biochem 2011 112 723 733 10.1002/jcb.23006 21268094
38. Mammalian target of rapamycin (mTOR) phosphorylates inositol 1,4,5-trisphosphate receptor type 2 and increases its Ca(2+) release activity. Régimbald-Dumas Y, Frégeau MO, Guillemette G, Cell Signal 2011 23 71 79 10.1016/j.cellsig.2010.08.005 20727967
39. Thapsigargin-induced Ca2+ increase inhibits TGFβ1-mediated Smad2 transcriptional responses via Ca2+/calmodulin-dependent protein kinase II. Ming M, Manzini I, Le W, Krieglstein K, Spittau B, J Cell Biochem 2010 111 1222 1230 10.1002/jcb.22843 20717921
40. Inactivation of smad-transforming growth factor beta signaling by Ca(2+)-calmodulin-dependent protein kinase II. Wicks SJ, Lui S, Abdel-Wahab N, Mason RM, Chantry A, Mol Cell Biol 2000 20 8103 8111 10.1128/MCB.20.21.8103- 8111.2000 11027280
41. Ukrain affects pancreas cancer cell phenotype in vitro by targeting MMP-9 and intra-/extracellular SPARC expression. Funel N, Costa F, Pettinari L, Taddeo A, Sala A, Chiriva-Internati M, Cobos E, Colombo G, Milzani A, Campani D, Dalle-Donne I, Gagliano N, Pancreatology 2010 10 545 552 10.1159/000266127 20975318
42. A comprehensive characterization of pancreatic ductal carcinoma cell lines: towards the establishment of an in vitro research platform. Sipos B, Möser S, Kalthoff H, Török V, Löhr M, Klöppel G, Virchows Arch 2003 442 444 452 12692724 (Pubitemid 36718311)
43. AKT/PKB signaling: navigating downstream. Manning BD, Cantley LC, Cell 2007 129 1261 1274 10.1016/j.cell.2007.06.009 17604717 (Pubitemid 46962095)
44. Primary tumours modulate innate immune signalling to create pre-metastatic vascular hyperpermeability foci. Hiratsuka S, Ishibashi S, Tomita T, Watanabe A, Akashi-Takamura S, Murakami M, Kijima H, Miyake K, Aburatani H, Maru Y, Nat Commun 1853 2013 4
45. The receptor RAGE: bridging inflammation and cancer. Riehl A, Németh J, Angel P, Hess J, Cell Commun Signal 2009 7 12 10.1186/1478-811X-7-12 19426472
46. Genetic profile of 22 pancreatic carcinoma cell lines. Analysis of K-ras, p53, p16 and DPC4/Smad4. Moore PS, Sipos B, Orlandini S, Sorio C, Real FX, Lemoine NR, Gress T, Bassi C, Klöppel G, Kalthoff H, Ungefroren H, Löhr M, Scarpa A, Virchows Arch 2001 439 798 802 11787853 (Pubitemid 33141325)
47. Identification of a key molecular regulator of liver metastasis in human pancreatic carcinoma using a novel quantitative model of metastasis in NOD/SCID/gammacnull (NOG) mice. Suemizu H, Monnai M, Ohnishi Y, Ito M, Tamaoki N, Nakamura M, Int J Oncol 2007 31 741 751 17786304
48. TLR4 mediates MAPK-STAT3 axis activation in bladder epithelial cells. Ying H, Da L, Yu-xiu S, Yu X, Li-xia L, Li-mei X, Wei-dong R, Inflammation 2013 36 1064 1074 10.1007/s10753-013-9638-7 23612802
49. Molecular pathogenesis of pancreatic cancer and clinical perspectives. Matthaios D, Zarogoulidis P, Balgouranidou I, Chatzaki E, Kakolyris S, Oncology 2011 81 259 272 10.1159/000334449 22116519
50. A unique substrate recognition profile for matrix metalloproteinase-2. Chen EI, Kridel SJ, Howard EW, Li W, Godzik A, Smith JW, J Biol Chem 2002 277 4485 4491 10.1074/jbc.M109469200 11694539 (Pubitemid 34968716)
51. Uncapping NF-κB activity in pancreatic cancer. Gurumurthy S, Bardeesy N, EMBO J 2011 30 1 2 10.1038/emboj.2010.324 21206509
52. Synergistic action of Smad4 and Pten in suppressing pancreatic ductal adenocarcinoma formation in mice. Xu X, Ehdaie B, Ohara N, Yoshino T, Deng CX, Oncogene 2010 29 674 686 10.1038/onc.2009.375 19901970
53. mTOR: from growth signal integration to cancer, diabetes and ageing. Zoncu R, Efeyan A, Sabatini DM, Nat Rev Mol Cell Biol 2011 12 21 35 10.1038/nrm3025 21157483
54. Suppression of AKT phosphorylation restores rapamycin-based synthetic lethality in SMAD4-defective pancreatic cancer cells. Le Gendre O, Sookdeo A, Duliepre SA, Utter M, Frias M, Foster DA, Mol Cancer Res 2013 11 474 481 10.1158/1541-7786.MCR-12-0679 23443316
55. Calcium-dependent and -independent interactions of the S100 protein family. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS, Biochem J 2006 396 201 214 10.1042/BJ20060195 16683912 (Pubitemid 43837235)
56. Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms. Qin Q, Xu Y, He T, Qin C, Xu J, Cell Res 2012 22 90 106 10.1038/cr.2011.144 21876555
57. Blocking of p53-Snail binding, promoted by oncogenic K-Ras, recovers p53 expression and function. Lee SH, Lee SJ, Jung YS, Xu Y, Kang HS, Ha NC, Park BJ, Neoplasia 2009 11 22 31 19107228
58. Epidermal growth factor receptor ligands as new extracellular targets for the metastasis-promoting S100A4 protein. Klingelhöfer J, Møller HD, Sumer EU, Berg CH, Poulsen M, Kiryushko D, Soroka V, Ambartsumian N, Grigorian M, Lukanidin EM, FEBS J 2009 276 5936 5948 10.1111/j.1742-4658.2009.07274.x 19740107
59. Structural insights into the interaction of human S100B and basic fibroblast growth factor (FGF2): effects on FGFR1 receptor signaling. Gupta AA, Chou RH, Li H, Yang LW, Yu C, Biochim Biophys Acta 1834 2013 2606 2619
60. S100B protein regulates myoblast proliferation and differentiation by activating FGFR1 in a bFGF-dependent manner. Riuzzi F, Sorci G, Donato R, J Cell Sci 2011 124 2389 2400 10.1242/jcs.084491 21693575
61. FAM/USP9x, a deubiquitinating enzyme essential for TGFbetasignaling, controls Smad4 monoubiquitination. Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, Inui M, Moro S, Modena N, Argenton F, Newfeld SJ, Piccolo S, Cell 2009 136 123 135 10.1016/j.cell.2008.10.051 19135894