Identification of hypoxia-regulated proteins using MALDI-mass spectrometry imaging combined with quantitative proteomics

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2297-2313

  Djidja, Marie Claude ^a,e   Chang, Joan ^a,d   Hadjiprocopis, Andreas ^a   Schmich, Fabian ^a,f   Sinclair, John ^b   Mršnik, Martina ^a,g   Schoof, Erwin M ^c   Barker, Holly E ^a   Linding, Rune ^c   Jørgensen, Claus ^b   Erler, Janine T ^a,d  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e NOVARTIS PHARMA AG   (Switzerland)

^f ETH ZURICH   (Switzerland)

^g EORTC DATA CENTER   (Belgium)

Author keywords

hypoxia; mass spectrometry imaging; proteomics

Indexed keywords

6 PHOSPHOFRUCTOKINASE ISOENZYME L; ACETYL COENZYME A CARBOXYLASE; ALPHA ENOLASE; ALPHA TROPOMYOSIN; FRUCTOSE BISPHOSPHATE ALDOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE A; GALECTIN 1; GALECTIN 3; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE H2B; KERATIN TYPE I; KERATIN TYPE II; LACTATE DEHYDROGENASE; LIPOCORTIN 2; LIPOCORTIN 4; NEDD8 PROTEIN; PEROXIREDOXIN 1; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE KINASE 1; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 1; PROHIBITIN; PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; STABLE ISOTOPE; SUMO PROTEIN; TRIOSEPHOSPHATE ISOMERASE; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; UNINDEXED DRUG; AMINO ACID; PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CELL ADHESION; CELL COMMUNICATION; CELL MOTION; CONTROLLED STUDY; FEMALE; HYPOXIA; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION MASS SPECTROMETRY IMAGING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UPREGULATION; ANIMAL; ANOXIA; BAGG ALBINO MOUSE; CELL HYPOXIA; EXPERIMENTAL MAMMARY NEOPLASM; IMMUNOHISTOCHEMISTRY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; NUDE MOUSE; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

AMINO ACIDS; ANIMALS; ANOXIA; CELL HYPOXIA; CELL LINE, TUMOR; FEMALE; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE, INBRED BALB C; MICE, NUDE; PEPTIDES; PROTEINS; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84899858253     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401056c     Document Type: Article

References (48)

1. Carroll, V. A.; Ashcroft, M. Targeting the molecular basis for tumour hypoxia Expert Rev. Mol. Med. 2005, 7 (6) 1-16
2. Vaupel, P.; Mayer, A. Hypoxia in cancer: significance and impact on clinical outcome Cancer Metastasis Rev. 2007, 26 (2) 225-239
3. Harris, A. L. Hypoxia - a key regulatory factor in tumour growth Nat. Rev. Cancer 2002, 2 (1) 38-47
4. Vaupel, P.; Hockel, M. Hypoxia in cervical cancer: pathogenesis, characterization, and biological/clinical consequences Zentralbl. Gynakol. 2001, 123 (4) 192-197
5. Vaupel, P.; Kelleher, D. K.; Hockel, M. Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy Semin. Oncol. 2001, 28 (2 Suppl 8) 29-35
6. Chaudary, N.; Hill, R. P. Hypoxia and metastasis Clin. Cancer Res. 2007, 13 (7) 1947-1949
7. Erler, J. T.; Weaver, V. M. Three-dimensional context regulation of metastasis Clin. Exp. Metastasis 2009, 26 (1) 35-49
8. Finger, E. C.; Giaccia, A. J. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease Cancer Metastasis Rev. 2010, 29 (2) 285-293
9. Overgaard, J.; Horsman, M. R. Modification of Hypoxia-Induced Radioresistance in Tumors by the Use of Oxygen and Sensitizers Semin. Radiat. Oncol. 1996, 6 (1) 10-21
10. Erler, J. T.; Giaccia, A. J. Lysyl oxidase mediates hypoxic control of metastasis Cancer Res. 2006, 66 (21) 10238-10241
11. Caprioli, R. M.; Farmer, T. B.; Gile, J. Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS Anal. Chem. 1997, 69 (23) 4751-4760
12. Trim, P. J.; Francese, S.; Clench, M. R. Imaging mass spectrometry for the assessment of drugs and metabolites in tissue Bioanalysis 2009, 1 (2) 309-319
13. Chaurand, P.; Stoeckli, M.; Caprioli, R. M. Direct profiling of proteins in biological tissue sections by MALDI mass spectrometry Anal. Chem. 1999, 71 (23) 5263-5270
14. Heeren, R. M.; Smith, D. F.; Stauber, J.; Kukrer-Kaletas, B.; MacAleese, L. Imaging mass spectrometry: hype or hope? J. Am. Soc. Mass Spectrom. 2009, 20 (6) 1006-14
15. Stoeckli, M.; Staab, D.; Schweitzer, A.; Gardiner, J.; Seebach, D. Imaging of a beta-peptide distribution in whole-body mice sections by MALDI mass spectrometry J. Am. Soc. Mass Spectrom. 2007, 18 (11) 1921-1924
16. Rauser, S.; Deininger, S. O.; Suckau, D.; Hofler, H.; Walch, A. Approaching MALDI molecular imaging for clinical proteomic research: current state and fields of application Expert Rev. Proteomics 2010, 7 (6) 927-941
17. Rauser, S.; Marquardt, C.; Balluff, B.; Deininger, S. O.; Albers, C.; Belau, E.; Hartmer, R.; Suckau, D.; Specht, K.; Ebert, M. P.; Schmitt, M.; Aubele, M.; Hofler, H.; Walch, A. Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry J. Proteome Res. 2010, 9 (4) 1854-1863
18. Wisztorski, M.; Lemaire, R.; Stauber, J.; Menguelet, S. A.; Croix, D.; Mathe, O. J.; Day, R.; Salzet, M.; Fournier, I. New developments in MALDI imaging for pathology proteomic studies Curr. Pharm. Des. 2007, 13 (32) 3317-3324
19. Djidja, M. C.; Claude, E.; Snel, M. F.; Francese, S.; Scriven, P.; Carolan, V.; Clench, M. R. Novel molecular tumour classification using MALDI-mass spectrometry imaging of tissue micro-array Anal. Bioanal. Chem. 2010, 397 (2) 587-601
20. Groseclose, M. R.; Massion, P. P.; Chaurand, P.; Caprioli, R. M. High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry Proteomics 2008, 8 (18) 3715-3724
21. Lemaire, R.; Desmons, A.; Tabet, J. C.; Day, R.; Salzet, M.; Fournier, I. Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections J. Proteome Res. 2007, 6 (4) 1295-1305
22. Aslakson, C. J.; Miller, F. R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor Cancer Res. 1992, 52 (6) 1399-1405
23. Jorgensen, C.; Sherman, A.; Chen, G. I.; Pasculescu, A.; Poliakov, A.; Hsiung, M.; Larsen, B.; Wilkinson, D. G.; Linding, R.; Pawson, T. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells Science 2009, 326 (5959) 1502-1509
24. United Kingdom Co-ordinating Committee on Cancer Research (UKCCCR) Guidelines for the Welfare of Animals in Experimental Neoplasia (2nd Edition). Br. J. Cancer 1998, 77 (1), 1-10.
25. Djidja, M. C.; Claude, E.; Snel, M. F.; Scriven, P.; Francese, S.; Carolan, V.; Clench, M. R. MALDI-ion mobility separation-mass spectrometry imaging of glucose-regulated protein 78 kDa (Grp78) in human formalin-fixed, paraffin-embedded pancreatic adenocarcinoma tissue sections J. Proteome Res. 2009, 8 (10) 4876-4884
26. Lemaire, R.; Tabet, J. C.; Ducoroy, P.; Hendra, J. B.; Salzet, M.; Fournier, I. Solid ionic matrixes for direct tissue analysis and MALDI imaging Anal. Chem. 2006, 78 (3) 809-819
27. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P.; Jensen, L. J.; von Mering, C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 2011, 39 (Database issue) D561-D568
28. Smoot, M. E.; Ono, K.; Ruscheinski, J.; Wang, P. L.; Ideker, T. Cytoscape 2.8: new features for data integration and network visualization Bioinformatics 2011, 27 (3) 431-432
29. Bos, R.; Zhong, H.; Hanrahan, C. F.; Mommers, E. C.; Semenza, G. L.; Pinedo, H. M.; Abeloff, M. D.; Simons, J. W.; van Diest, P. J.; van der Wall, E. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis J. Natl. Cancer Inst. 2001, 93 (4) 309-314
30. Erler, J. T.; Bennewith, K. L.; Cox, T. R.; Lang, G.; Bird, D.; Koong, A.; Le, Q. T.; Giaccia, A. J. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche Cancer Cell 2009, 15 (1) 35-44
31. Raleigh, J. A.; Miller, G. G.; Franko, A. J.; Koch, C. J.; Fuciarelli, A. F.; Kelly, D. A. Fluorescence immunohistochemical detection of hypoxic cells in spheroids and tumours Br. J. Cancer 1987, 56 (4) 395-400
32. Chaurand, P.; Fouchecourt, S.; DaGue, B. B.; Xu, B. J.; Reyzer, M. L.; Orgebin-Crist, M. C.; Caprioli, R. M. Profiling and imaging proteins in the mouse epididymis by imaging mass spectrometry Proteomics 2003, 3 (11) 2221-2239
33. Coyle, J. H.; Bor, Y. C.; Rekosh, D.; Hammarskjold, M. L. The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway RNA 2011, 17 (7) 1344-1356
34. Robin, E. D.; Murphy, B. J.; Theodore, J. Coordinate regulation of glycolysis by hypoxia in mammalian cells J. Cell. Physiol. 1984, 118 (3) 287-290
35. Bernad, R.; van der Velde, H.; Fornerod, M.; Pickersgill, H. Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export Mol. Cell. Biol. 2004, 24 (6) 2373-2384
36. Bell, A. W.; Deutsch, E. W.; Au, C. E.; Kearney, R. E.; Beavis, R.; Sechi, S.; Nilsson, T.; Bergeron, J. J. A HUPO Test Sample Study Reveals Common Problems in Mass Spectrometry-Based Proteomics Nat. Methods 2009, 6 (6) 423-430
37. Le, Q. T.; Shi, G.; Cao, H.; Nelson, D. W.; Wang, Y.; Chen, E. Y.; Zhao, S.; Kong, C.; Richardson, D.; O'Byrne, K. J.; Giaccia, A. J.; Koong, A. C. Galectin-1: a Link between Tumor Hypoxia and Tumor Immune Privilege J. Clin. Oncol. 2005, 23 (35) 8932-8941
38. Semenza, G. L.; Jiang, B. H.; Leung, S. W.; Passantino, R.; Concordet, J. P.; Maire, P.; Giallongo, A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1 J. Biol. Chem. 1996, 271 (51) 32529-32537
39. Koong, A. C.; Auger, E. A.; Chen, E. Y.; Giaccia, A. J. The regulation of GRP78 and messenger RNA levels by hypoxia is modulated by protein kinase C activators and inhibitors Radiat. Res. 1994, 138 (1 Suppl) S60-S63
40. Song, M. S.; Park, Y. K.; Lee, J. H.; Park, K. Induction of glucose-regulated protein 78 by chronic hypoxia in human gastric tumor cells through a protein kinase C-epsilon/ERK/AP-1 signaling cascade Cancer Res. 2001, 61 (22) 8322-8330
41. Graven, K. K.; McDonald, R. J.; Farber, H. W. Hypoxic regulation of endothelial glyceraldehyde-3-phosphate dehydrogenase Am. J. Physiol. 1998, 274 (2 Pt 1) C347-C355
42. Graven, K. K.; Troxler, R. F.; Kornfeld, H.; Panchenko, M. V.; Farber, H. W. Regulation of endothelial cell glyceraldehyde-3-phosphate dehydrogenase expression by hypoxia J. Biol. Chem. 1994, 269 (39) 24446-24453
43. Li, H.; Ko, H. P.; Whitlock, J. P. Induction of phosphoglycerate kinase 1 gene expression by hypoxia. Roles of Arnt and HIF1alpha J. Biol. Chem. 1996, 271 (35) 21262-21267
44. Yamaji, R.; Fujita, K.; Takahashi, S.; Yoneda, H.; Nagao, K.; Masuda, W.; Naito, M.; Tsuruo, T.; Miyatake, K.; Inui, H.; Nakano, Y. Hypoxia up-regulates glyceraldehyde-3-phosphate dehydrogenase in mouse brain capillary endothelial cells: involvement of Na+/Ca2+ exchanger Biochim. Biophys. Acta 2003, 1593 (2-3) 269-276
45. Marotta, D.; Karar, J.; Jenkins, W. T.; Kumanova, M.; Jenkins, K. W.; Tobias, J. W.; Baldwin, D.; Hatzigeorgiou, A.; Alexiou, P.; Evans, S. M.; Alarcon, R.; Maity, A.; Koch, C.; Koumenis, C. In vivo profiling of hypoxic gene expression in gliomas using the hypoxia marker EF5 and laser-capture microdissection Cancer Res. 2011, 71 (3) 779-789
46. Li, D. Q.; Wang, L.; Fei, F.; Hou, Y. F.; Luo, J. M.; Zeng, R.; Wu, J.; Lu, J. S.; Di, G. H.; Ou, Z. L.; Xia, Q. C.; Shen, Z. Z.; Shao, Z. M. Identification of breast cancer metastasis-associated proteins in an isogenic tumor metastasis model using two-dimensional gel electrophoresis and liquid chromatography-ion trap-mass spectrometry Proteomics 2006, 6 (11) 3352-3368
47. Semenza, G. L. Targeting HIF-1 for cancer therapy Nat. Rev. Cancer 2003, 3 (10) 721-732
48. Wong, C. C.; Zhang, H.; Gilkes, D. M.; Chen, J.; Wei, H.; Chaturvedi, P.; Hubbi, M. E.; Semenza, G. L. Inhibitors of hypoxia-inducible factor 1 block breast cancer metastatic niche formation and lung metastasis J. Mol. Med. 2012, 90 (7) 803-815