Secretome protein signature of human pancreatic cancer stem-like cells

Journal of Proteomics

Volumn 136, Issue , 2016, Pages 1-12

  Brandi, Jessica ^a   Pozza, Elisa Dalla ^a   Dando, Ilaria ^a   Biondani, Giulia ^a   Robotti, Elisa ^b   Jenkins, Rosalind ^c   Elliott, Victoria ^d   Park, Kevin ^c   Marengo, Emilio ^b   Costello, Eithne ^d   Scarpa, Aldo ^e   Palmieri, Marta ^a   Cecconi, Daniela ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d Liverpool NIHR Pancreas Biomedical Research Unit   (United Kingdom)

^e UNIVERSITY AND HOSPITAL TRUST OF VERONA   (Italy)

Author keywords

ITRAQ based proteomic; Pancreatic cancer; Secretome

Indexed keywords

ALPHA 2 MACROGLOBULIN; ALPHA ACTININ 4; CA 19-9 ANTIGEN; CERULOPLASMIN; COFILIN 1; COPPER ZINC SUPEROXIDE DISMUTASE; DJ 1 PROTEIN; DYSTROGLYCAN; ELONGATION FACTOR 1BETA; FETUIN A; GALECTIN 3; GELATINASE A; GLUTATHIONE TRANSFERASE P1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; LACTADHERIN; LACTATE DEHYDROGENASE; LACTOYLGLUTATHIONE LYASE; MARCKS PROTEIN; PENTOSE PHOSPHATE; PEROXIREDOXIN 1; PHOSPHOGLUCOMUTASE; PHOSPHOGLYCERATE MUTASE; PROTEIN 14 3 3; SERUM ALBUMIN; TRANSALDOLASE; TRIOSEPHOSPHATE ISOMERASE; TUMOR PROTEIN; UROKINASE; VINCULIN; PROTEOME;

ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER PATIENT; CANCER RESEARCH; CANCER STEM CELL; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCONEOGENESIS; GLYCOLYSIS; HUMAN; HUMAN CELL; METASTASIS; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEOMICS; STEM CELL CULTURE; TUMOR DIFFERENTIATION; TUMOR INVASION; UPREGULATION; CELL LINE; CYTOLOGY; PANCREAS; SECRETION (PROCESS); STEM CELL;

CELL LINE; HUMANS; PANCREAS; PROTEOME; PROTEOMICS; STEM CELLS;

EID: 84957808379     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2016.01.017     Document Type: Article

References (65)

1. Saif M.W. Pancreatic neoplasm in 2011: an update. JOP 2011, 12:316-321.
2. Rhim A.D., Mirek E.T., Aiello N.M., Maitra A., Bailey J.M., McAllister F., et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012, 148:349-361.
3. Lee C.J., Dosch J., Simeone D.M. Pancreatic cancer stem cells. J. Clin. Oncol. 2008, 26:2806-2812.
4. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007, 67:1030-1037.
5. Kondo T. Stem cell-like cancer cells in cancer cell lines. Cancer Biomark. 2007, 3:245-250.
6. Dalla Pozza E., Dando I., Biondani G., Brandi J., Costanzo C., Zoratti E., et al. Pancreatic ductal adenocarcinoma cell lines display a plastic ability to bidirectionally convert into cancer stem cells. Int. J. Oncol. 2015, 46:1099-1108.
7. Dai L., Li C., Shedden K.A., Lee C.J., Quoc H., Simeone D.M., et al. Quantitative proteomic profiling studies of pancreatic cancer stem cells. J. Proteome Res. 2010, 9:3394-3402.
8. Zhu J., Nie S., Wu J., Lubman D.M. Target proteomic profiling of frozen pancreatic CD24+ adenocarcinoma tissues by immuno-laser capture microdissection and nano-LC-MS/MS. J. Proteome Res. 2013, 12:2791-2804.
9. Zhu J., He J., Liu Y., Simeone D.M., Lubman D.M. Identification of glycoprotein markers for pancreatic cancer CD24+CD44+ stem-like cells using nano-LC-MS/MS and tissue microarray. J. Proteome Res. 2012, 11:2272-2281.
10. Emmink B.L., Verheem A., Van Houdt W.J., Steller E.J., Govaert K.M., Pham T.V., et al. The secretome of colon cancer stem cells contains drug-metabolizing enzymes. J. Proteome 2013, 91:84-96.
11. Mateo F., Meca-Cortes O., Celia-Terrassa T., Fernandez Y., Abasolo I., Sanchez-Cid L., et al. SPARC mediates metastatic cooperation between CSC and non-CSC prostate cancer cell subpopulations. Mol. Cancer 2014, 13:237.
12. Loei H., Tan H.T., Lim T.K., Lim K.H., So J.B., Yeoh K.G., et al. Mining the gastric cancer secretome: identification of GRN as a potential diagnostic marker for early gastric cancer. J. Proteome Res. 2012, 11:1759-1772.
13. Shilov I.V., Seymour S.L., Patel A.A., Loboda A., Tang W.H., Keating S.P., et al. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell. Proteomics 2007, 6:1638-1655.
14. Tang W.H., Shilov I.V., Seymour S.L. Nonlinear fitting method for determining local false discovery rates from decoy database searches. J. Proteome Res. 2008, 7:3661-3667.
15. Bendtsen J.D., Jensen L.J., Blom N., Von Heijne G., Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 2004, 17:349-356.
16. Simpson R.J., Kalra H., Mathivanan S. ExoCarta as a resource for exosomal research. J. Extracellular Vesicles 2012, 1.
17. Kalra H., Simpson R.J., Ji H., Aikawa E., Altevogt P., Askenase P., et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012, 10:e1001450.
18. Karagiannis G.S., Pavlou M.P., Saraon P., Musrap N., Xie A., Batruch I., et al. In-depth proteomic delineation of the colorectal cancer exoproteome: mechanistic insight and identification of potential biomarkers. J. Proteome 2014, 103:121-136.
19. Jenkinson C., Elliott V., Menon U., Apostolidou S., Fourkala O.E., Gentry-Maharaj A., et al. Evaluation in pre-diagnosis samples discounts ICAM-and TIMP-as biomarkers for earlier diagnosis of pancreatic cancer. J. Proteome 2015, 113:400-402.
20. Makridakis M., Roubelakis M.G., Vlahou A. Stem cells: insights into the secretome. Biochim. Biophys. Acta 2013, 1834:2380-2384.
21. Abel E.V., Simeone D.M. Biology and clinical applications of pancreatic cancer stem cells. Gastroenterology 2013, 144:1241-1248.
22. Quan M., Wang P., Cui J., Gao Y., Xie K. The roles of FOXM1 in pancreatic stem cells and carcinogenesis. Mol. Cancer 2013, 12:159.
23. Guillaumond F., Iovanna J.L., Vasseur S. Pancreatic tumor cell metabolism: focus on glycolysis and its connected metabolic pathways. Arch. Biochem. Biophys. 2014, 545:69-73.
24. Capello M., Ferri-Borgogno S., Cappello P., Novelli F. alpha-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J. 2011, 278:1064-1074.
25. Perales-Clemente E., Folmes C.D., Terzic A. Metabolic regulation of redox status in stem cells. Antioxid. Redox Signal. 2014, 21:1648-1659.
26. Gonzalez-Rodriguez I., Sanchez B., Ruiz L., Turroni F., Ventura M., Ruas-Madiedo P., et al. Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl. Environ. Microbiol. 2012, 78:3992-3998.
27. Kaur S., Kumar S., Momi N., Sasson A.R., Batra S.K. Mucins in pancreatic cancer and its microenvironment. Nat. Rev. Gastroenterol. Hepatol. 2013, 10:607-620.
28. Binker M.G., Binker-Cosen A.A., Richards D., Gaisano H.Y., de Cosen R.H., Cosen-Binker L.I. Hypoxia-reoxygenation increase invasiveness of PANC-cells through Rac1/MMP-2. Biochem. Biophys. Res. Commun. 2010, 393:371-376.
29. Morifuji Y., Onishi H., Iwasaki H., Imaizumi A., Nakano K., Tanaka M., et al. Reoxygenation from chronic hypoxia promotes metastatic processes in pancreatic cancer through the Hedgehog signaling. Cancer Sci. 2014, 105:324-333.
30. Liu J., Ben Q.W., Yao W.Y., Zhang J.J., Chen D.F., He X.Y., et al. BMP2 induces PANC-cell invasion by MMP-overexpression through ROS and ERK. Front. Biosci. (Landmark Ed.) 2012, 17:2541-2549.
31. Sharma K.L., Misra S., Kumar A., Mittal B. Higher risk of matrix metalloproteinase (MMP-2, 7, 9) and tissue inhibitor of metalloproteinase (TIMP-2) genetic variants to gallbladder cancer. Liver Int. 2012, 32:1278-1286.
32. Bera A., Zhao S., Cao L., Chiao P.J., Freeman J.W. Oncogenic K-Ras and loss of Smad4 mediate invasion by activating an EGFR/NF-kappaB Axis that induces expression of MMP9 and uPA in human pancreas progenitor cells. PLoS One 2013, 8:e82282.
33. Dovrat S., Caspi M., Zilberberg A., Lahav L., Firsow A., Gur H., et al. 14-3-and beta-catenin are secreted on extracellular vesicles to activate the oncogenic Wnt pathway. Mol. Oncol. 2014, 8:894-911.
34. Chen C.H., Chuang S.M., Yang M.F., Liao J.W., Yu S.L., Chen J.J. A novel function of YWHAZ/beta-catenin axis in promoting epithelial-mesenchymal transition and lung cancer metastasis. Mol. Cancer Res. 2012, 10:1319-1331.
35. Lu J., Guo H., Treekitkarnmongkol W., Li P., Zhang J., Shi B., et al. 14-3-3zeta Cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 2009, 16:195-207.
36. Liu T.A., Jan Y.J., Ko B.S., Liang S.M., Chen S.C., Wang J., et al. 14-3-3epsilon overexpression contributes to epithelial-mesenchymal transition of hepatocellular carcinoma. PLoS One 2013, 8:e57968.
37. Ohmori T., Kashiwakura Y., Ishiwata A., Madoiwa S., Mimuro J., Furukawa Y., et al. Vinculin is indispensable for repopulation by hematopoietic stem cells, independent of integrin function. J. Biol. Chem. 2010, 285:31763-31773.
38. Yamashita H., Ichikawa T., Matsuyama D., Kimura Y., Ueda K., Craig S.W., et al. The role of the interaction of the vinculin proline-rich linker region with vinexin alpha in sensing the stiffness of the extracellular matrix. J. Cell Sci. 2014, 127:1875-1886.
39. Welsch T., Keleg S., Bergmann F., Bauer S., Hinz U., Schmidt J. Actinin-expression in primary and metastasized pancreatic ductal adenocarcinoma. Pancreas 2009, 38:968-976.
40. Hayashida Y., Honda K., Idogawa M., Ino Y., Ono M., Tsuchida A., et al. E-cadherin regulates the association between beta-catenin and actinin-4. Cancer Res. 2005, 65:8836-8845.
41. Koschinsky M.L., Funk W.D., van Oost B.A., MacGillivray R.T. Complete cDNA sequence of human preceruloplasmin. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:5086-5090.
42. Healy J., Tipton K. Ceruloplasmin and what it might do. J. Neural Transm. 2007, 114:777-781.
43. Hanas J.S., Hocker J.R., Cheung J.Y., Larabee J.L., Lerner M.R., Lightfoot S.A., et al. Biomarker identification in human pancreatic cancer sera. Pancreas 2008, 36:61-69.
44. Tye S.L., Gilg A.G., Tolliver L.B., Wheeler W.G., Toole B.P., Maria B.L. Hyaluronan regulates ceruloplasmin production by gliomas and their treatment-resistant multipotent progenitors. J. Child Neurol. 2008, 23:1221-1230.
45. Zhang K.H., Tian H.Y., Gao X., Lei W.W., Hu Y., Wang D.M., et al. Ferritin heavy chain-mediated iron homeostasis and subsequent increased reactive oxygen species production are essential for epithelial-mesenchymal transition. Cancer Res. 2009, 69:5340-5348.
46. Huang H., Li Y., Liu J., Zheng M., Feng Y., Hu K., et al. Screening and identification of biomarkers in ascites related to intrinsic chemoresistance of serous epithelial ovarian cancers. PLoS One 2012, 7:e51256.
47. Fortuna-Costa A., Gomes A.M., Kozlowski E.O., Stelling M.P., Pavao M.S. Extracellular galectin-in tumor progression and metastasis. Front. Oncol. 2014, 4:138.
48. Zhang D., Chen Z.G., Liu S.H., Dong Z.Q., Dalin M., Bao S.S., et al. Galectin-gene silencing inhibits migration and invasion of human tongue cancer cells in vitro via downregulating beta-catenin. Acta Pharmacol. Sin. 2013, 34:176-184.
49. Yamamoto-Sugitani M., Kuroda J., Ashihara E., Nagoshi H., Kobayashi T., Matsumoto Y., et al. Galectin-(Gal-3) induced by leukemia microenvironment promotes drug resistance and bone marrow lodgment in chronic myelogenous leukemia. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17468-17473.
50. Mehul B., Hughes R.C. Plasma membrane targetting, vesicular budding and release of galectin 3 from the cytoplasm of mammalian cells during secretion. J. Cell Sci. 1997, 110(Pt 10):1169-1178.
51. Sioud M., Mobergslien A., Boudabous A., Floisand Y. Evidence for the involvement of galectin-in mesenchymal stem cell suppression of allogeneic T-cell proliferation. Scand. J. Immunol. 2010, 71:267-274.
52. Jiang K., Lawson D., Cohen C., Siddiqui M.T. Galectin-and PTEN expression in pancreatic ductal adenocarcinoma, pancreatic neuroendocrine neoplasms and gastrointestinal tumors on fine-needle aspiration cytology. Acta Cytol. 2014, 58:281-287.
53. Song S., Ji B., Ramachandran V., Wang H., Hafley M., Logsdon C., et al. Overexpressed galectin-in pancreatic cancer induces cell proliferation and invasion by binding Ras and activating Ras signaling. PLoS One 2012, 7:e42699.
54. Kobayashi T., Shimura T., Yajima T., Kubo N., Araki K., Tsutsumi S., et al. Transient gene silencing of galectin-suppresses pancreatic cancer cell migration and invasion through degradation of beta-catenin. Int. J. Cancer 2011, 129:2775-2786.
55. Xie L., Ni W.K., Chen X.D., Xiao M.B., Chen B.Y., He S., et al. The expressions and clinical significances of tissue and serum galectin-in pancreatic carcinoma. J. Cancer Res. Clin. Oncol. 2012, 138:1035-1043.
56. Gaida M.M., Bach S.T., Gunther F., Baseras B., Tschaharganeh D.F., Welsch T., et al. Expression of galectin-in pancreatic ductal adenocarcinoma. Pathol. Oncol. Res. 2012, 18:299-307.
57. Barderas R., Mendes M., Torres S., Bartolome R.A., Lopez-Lucendo M., Villar-Vazquez R., et al. In-depth characterization of the secretome of colorectal cancer metastatic cells identifies key proteins in cell adhesion, migration, and invasion. Mol. Cell. Proteomics 2013, 12:1602-1620.
58. Miller J.D., Lankford S.M., Adler K.B., Brody A.R. Mesenchymal stem cells require MARCKS protein for directed chemotaxis in vitro. Am. J. Respir. Cell Mol. Biol. 2010, 43:253-258.
59. Chen C.H., Thai P., Yoneda K., Adler K.B., Yang P.C., Wu R. A peptide that inhibits function of Myristoylated Alanine-Rich C Kinase Substrate (MARCKS) reduces lung cancer metastasis. Oncogene 2014, 33:3696-3706.
60. Chen X., Rotenberg S.A. PhosphoMARCKS drives motility of mouse melanoma cells. Cell. Signal. 2010, 22:1097-1103.
61. Micallef J., Taccone M., Mukherjee J., Croul S., Busby J., Moran M.F., et al. Epidermal growth factor receptor variant III-induced glioma invasion is mediated through myristoylated alanine-rich protein kinase C substrate overexpression. Cancer Res. 2009, 69:7548-7556.
62. Jarboe J.S., Anderson J.C., Duarte C.W., Mehta T., Nowsheen S., Hicks P.H., et al. MARCKS regulates growth and radiation sensitivity and is a novel prognostic factor for glioma. Clin. Cancer Res. 2012, 18:3030-3041.
63. Brooks G., Brooks S.F., Goss M.W. MARCKS functions as a novel growth suppressor in cells of melanocyte origin. Carcinogenesis 1996, 17:683-689.
64. Gardner-Thorpe J., Ito H., Ashley S.W., Whang E.E. Differential display of expressed genes in pancreatic cancer cells. Biochem. Biophys. Res. Commun. 2002, 293:391-395.
65. Wojtaszek P.A., Stumpo D.J., Blackshear P.J., Macara I.G. Severely decreased MARCKS expression correlates with ras reversion but not with mitogenic responsiveness. Oncogene 1993, 8:755-760.