Comparative proteomic analysis of different stages of breast cancer tissues using ultra high performance liquid chromatography tandem mass spectrometer


Autoři: Abdullah Saleh Al-wajeeh aff001;  Salizawati Muhamad Salhimi aff003;  Majed Ahmed Al-Mansoub aff003;  Imran Abdul Khalid aff004;  Thomas Michael Harvey aff001;  Aishah Latiff aff001;  Mohd Nazri Ismail aff002
Působiště autorů: Anti-Doping Lab Qatar, Doha, Qatar aff001;  Analytical Biochemistry Research Centre (ABrC), Universiti Sains Malaysia, USM, Penang, Malaysia aff002;  School of Pharmaceutical Sciences, Universiti Sains Malaysia, USM, Penang, Malaysia aff003;  Seberang Jaya Hospital, Perai, Penang, Malaysia aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227404

Souhrn

Background

Breast cancer is the fifth most prevalent cause of death among women worldwide. It is also one of the most common types of cancer among Malaysian women. This study aimed to characterize and differentiate the proteomics profiles of different stages of breast cancer and its matched adjacent normal tissues in Malaysian breast cancer patients. Also, this study aimed to construct a pertinent protein pathway involved in each stage of cancer.

Methods

In total, 80 samples of tumor and matched adjacent normal tissues were collected from breast cancer patients at Seberang Jaya Hospital (SJH) and Kepala Batas Hospital (KBH), both in Penang, Malaysia. The protein expression profiles of breast cancer and normal tissues were mapped by sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE). The Gel-Eluted Liquid Fractionation Entrapment Electrophoresis (GELFREE) Technology System was used for the separation and fractionation of extracted proteins, which also were analyzed to maximize protein detection. The protein fractions were then analyzed by tandem mass spectrometry (LC-MS/MS) analysis using LC/MS LTQ-Orbitrap Fusion and Elite. This study identified the proteins contained within the tissue samples using de novo sequencing and database matching via PEAKS software. We performed two different pathway analyses, DAVID and STRING, in the sets of proteins from stage 2 and stage 3 breast cancer samples. The lists of molecules were generated by the REACTOME-FI plugin, part of the CYTOSCAPE tool, and linker nodes were added in order to generate a connected network. Then, pathway enrichment was obtained, and a graphical model was created to depict the participation of the input proteins as well as the linker nodes.

Results

This study identified 12 proteins that were detected in stage 2 tumor tissues, and 17 proteins that were detected in stage 3 tumor tissues, related to their normal counterparts. It also identified some proteins that were present in stage 2 but not stage 3 and vice versa. Based on these results, this study clarified unique proteins pathways involved in carcinogenesis within stage 2 and stage 3 breast cancers.

Conclusions

This study provided some useful insights about the proteins associated with breast cancer carcinogenesis and could establish an important foundation for future cancer-related discoveries using differential proteomics profiling. Beyond protein identification, this study considered the interaction, function, network, signaling pathway, and protein pathway involved in each profile. These results suggest that knowledge of protein expression, especially in stage 2 and stage 3 breast cancer, can provide important clues that may enable the discovery of novel biomarkers in carcinogenesis.

Klíčová slova:

Biomarkers – Breast cancer – Cancer detection and diagnosis – DNA-binding proteins – Nutrient and storage proteins – Protein domains – Protein interaction networks – Proteomics


Zdroje

1. Lee J, Oh M. Effects of interval between age at first pregnancy and age at diagnosis on breast cancer survival according to menopausal status: a register-based study in Korea. BMC womens health. 2014;14(1):113. doi: 10.1186/1472-6874-14-113 25231360.

2. Lee JS, Oh M, Ahn S, Bae J, Bae Y, Baek J, et al. Reproductive factors and subtypes of breast cancer defined by estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2: a register-based study from Korea. Clin Breast Cancer. 2014;14(6):426–34. doi: 10.1016/j.clbc.2014.05.003 25034438.

3. Molina-Montes E, Pérez-Nevot B, Pollán M, Sánchez-Cantalejo E, Espín J, Sánchez M-J. Cumulative risk of second primary contralateral breast cancer in BRCA1/BRCA2 mutation carriers with a first breast cancer: a systematic review and meta-analysis. The Breast. 2014;23(6):721–42. doi: 10.1016/j.breast.2014.10.005 25467311.

4. Dowling P, Palmerini V, Henry M, Meleady P, Lynch V, Ballot J, et al. Transferrin-bound proteins as potential biomarkers for advanced breast cancer patients. BBA Clin. 2014;2:24–30. doi: 10.1016/j.bbacli.2014.08.004 26673961.

5. Lam S, Jimenez C, Boven E. Breast cancer classification by proteomic technologies: current state of knowledge. Cancer Treat Rev. 2014;40(1):129–38. doi: 10.1016/j.ctrv.2013.06.006 23891266.

6. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P. Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol. 2007;18(3):581–92. doi: 10.1093/annonc/mdl498 17287242.

7. Ziegler YS, Moresco JJ, Tu PG, Yates JR III, Nardulli AM. Plasma membrane proteomics of human breast cancer cell lines identifies potential targets for breast cancer diagnosis and treatment. PloS one. 2014;9(7):e102341. doi: 10.1371/journal.pone.0102341 25029196.

8. Baig RM, Mahjabeen I, Sabir M, Masood N, Hafeez S, Malik FA, et al. Genetic changes in the PTEN gene and their association with breast cancer in Pakistan. Asian Pac J Cancer Prev. 2011;12(10):2773–8. 22320991.

9. Basnet P, Skalko-Basnet N. Curcumin: an anti-inflammatory molecule from a curry spice on the path to cancer treatment. Molecules. 2011;16(6):4567–98. doi: 10.3390/molecules16064567 21642934.

10. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74–108. doi: 10.3322/canjclin.55.2.74 15761078.

11. Marotta LL, Almendro V, Marusyk A, Shipitsin M, Schemme J, Walker SR, et al. The JAK2/STAT3 signaling pathway is required for growth of CD44+ CD24–stem cell–like breast cancer cells in human tumors. J Clin Invest. 2011;121(7):2723–35. doi: 10.1172/JCI44745 21633165.

12. Medina PP, Nolde M, Slack FJ. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature. 2010;467(7311):86. doi: 10.1038/nature09284 20693987.

13. Azeem E, Gillani SW, Siddiqui A, Shammary H, Poh V, Syed Sulaiman S. Knowledge, attitude and behavior of healthcare providers towards breast cancer in Malaysia: A systematic review. Asian Pac J Cancer Prev. 2015;16(13):5233–5. doi: 10.7314/apjcp.2015.16.13.5233 26225658.

14. Rufa’i AA, Muda WAMW, Yen SH, Shatar AKA, Murali BVK, Tan SW. Design of a randomised intervention study: the effect of dumbbell exercise therapy on physical activity and quality of life among breast cancer survivors in Malaysia. BMJ Glob Health. 2016;1(1):e000015. doi: 10.1136/bmjgh-2015-000015 28588911.

15. Yip CH, Bhoo PN, Teo S. A review of breast cancer research in Malaysia. Med J Malaysia. 2014;69(suppl A):8–22. doi: 10.23880/oajco-16000105 25417947.

16. Cadoo KA, McArdle O, O’Shea A-M, Power CP, Hennessy BT. Management of unusual histological types of breast cancer. Oncologist. 2012;17(9):1135–45. doi: 10.1634/theoncologist.2012-0134 22826373.

17. Akram M, Iqbal M, Daniyal M, Khan AU. Awareness and current knowledge of breast cancer. Biological research. 2017;50(1):33-. doi: 10.1186/s40659-017-0140-9 28969709.

18. Beretov J, Wasinger VC, Millar EKA, Schwartz P, Graham PH, Li Y. Proteomic analysis of urine to identify breast cancer biomarker candidates using a label-free LC-MS/MS approach. PLOS ONE. 2015;10(11):e0141876. doi: 10.1371/journal.pone.0141876 26544852.

19. Goto R, Nakamura Y, Takami T, Sanke T, Tozuka Z. Quantitative LC-MS/MS analysis of proteins involved in metastasis of breast cancer. PLOS ONE. 2015;10(7):e0130760. doi: 10.1371/journal.pone.0130760 26176947.

20. Ducret A, James I, Wilson S, Feilke M, Tebbe A, Dybowski N, et al. Translation and evaluation of a pre-clinical 5-protein response prediction signature in a breast cancer phase Ib clinical trial. PLOS ONE. 2019;14(3):e0213892. doi: 10.1371/journal.pone.0213892 30897176.

21. Devlin L, Perkins G, Bowen JR, Montagna C, Spiliotis ET. Proteomic profiling of the oncogenic septin 9 reveals isoform-specific interactions in breast cancer cells. bioRxiv. 2019:566513. doi: 10.1101/566513

22. Lakhani S, Ellis I, Schnitt S, Tan P, Van de Vijver M. WHO classification of tumours of the breast. 4th ed. Lyon: IARC. 2012:143–7.

23. Sinn HP, Kreipe H. A brief overview of the WHO classification of breast tumors, 4th edition, focusing on issues and updates from the 3rd edition. Breast care (Basel, Switzerland). 2013;8(2):149–54. Epub 2014/01/15. doi: 10.1159/000350774 24415964.

24. Akhtari-Zavare M, Mohd-Sidik S, Periasamy U, Rampal L, Fadhilah SI, Mahmud R. Determinants of quality of life among Malaysian cancer patients: a cross-sectional study. Health and Quality of Life Outcomes. 2018;16(1):163. doi: 10.1186/s12955-018-0989-5 30103759.

25. Dahlui M, Ramli S, Bulgiba AM. Breast cancer prevention and control programs in Malaysia. Asian Pacific Journal of Cancer Prevention. 2011;12(6):1631–4. 22126511.

26. Tan M-M, Ho W-K, Yoon S-Y, Mariapun S, Hasan SN, Lee DS-C, et al. A case-control study of breast cancer risk factors in 7,663 women in Malaysia. PloS one. 2018;13(9):e0203469. doi: 10.1371/journal.pone.0203469 30216346.

27. Jang‐Lee J, North SJ, Sutton‐Smith M, Goldberg D, Panico M, Morris H, et al. Glycomic profiling of cells and tissues by mass spectrometry: Fingerprinting and sequencing methodologies. Methods Enzymol. 415: Academic Press; 2006. p. 59–86. doi: 10.1016/S0076-6879(06)15005-3 17116468

28. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal biochem. 1976;72(1–2):248–54. doi: 10.1016/0003-2697(76)90527-3 942051.

29. Witkowski C, Harkins J. Using the GELFREE 8100 Fractionation System for molecular weight-based fractionation with liquid phase recovery. J Vis Exp. 2009;(34). doi: 10.3791/1842 19959987.

30. Ru QC, Zhu LA, Katenhusen RA, Silberman J, Brzeski H, Liebman M, et al. Exploring human plasma proteome strategies: high efficiency in-solution digestion protocol for multi-dimensional protein identification technology. J Chromatogr A. 2006;1111(2):175–91. doi: 10.1016/j.chroma.2005.06.080 16569577.

31. Saba J, Dutta S, Hemenway E, Viner R. Increasing the productivity of glycopeptides analysis by using higher-energy collision dissociation-accurate mass-product-dependent electron transfer dissociation. Int J Proteomics. 2012;2012. doi: 10.1155/2012/560391 22701174.

32. Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, McNeal J, et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 2012;13(1):R3. doi: 10.1186/gb-2012-13-1-r3 22280555.

33. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(D1):D447–D52. doi: 10.1093/nar/gku1003 25352553.

34. Yu T, Zhao Y, Hu Z, Li J, Chu D, Zhang J, et al. MetaLnc9 facilitates lung cancer metastasis via a PGK1-activated AKT/mTOR pathway. Cancer Res. 2017;77(21):5782–94. doi: 10.1158/0008-5472.CAN-17-0671 28923857.

35. Fabregat A, Jupe S, Matthews L, Sidiropoulos K, Gillespie M, Garapati P, et al. The Reactome pathway knowledgebase. Nucleic Acids Res. 2018;46(D1):D649–D55. doi: 10.1093/nar/gkx1132 29145629.

36. Li J, Abraham S, Cheng L, Witzmann FA, Koch M, Xie J, et al. Proteomic-based approach for biomarkers discovery in early detection of invasive urothelial carcinoma. PROTEOMICS–Clinical Applications. 2008;2(1):78–89. doi: 10.1002/prca.200780027 21136781.

37. Torres-Luquis O, Madden K, N’Dri NsM, Berg R, Olopade OF, Ngwa W, et al. LXR/RXR pathway signaling associated with triple-negative breast cancer in African American women. Breast cancer (Dove Medical Press). 2019;11:1–12. doi: 10.2147/BCTT.S185960 30588086.

38. Al-wajeeh AS, Alsayrafi M, Harvey T, Latiff A, Ismail S, Salhimi S, et al. Identification of glycobiomarker candidates for breast cancer using LTQ-orbitrap fusion technique. Int J Pharmacol. 2017;13(5):425–37. doi: 10.3923/ijp.2017.425.437

39. Cabral WA, Chang W, Barnes AM, Weis M, Scott MA, Leikin S, et al. Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nature Genet. 2007;39(3):359. doi: 10.1038/ng1968 17277775.

40. Velasco HM, Morales JL. Novel mutation of FKBp10 in a pediatric patient with osteogenesis imperfecta type XI identified by clinical exome sequencing. Appl Clin Genet. 2017;10:75. doi: 10.2147/TACG.S126277 29158687.

41. Arai S, Kita K, Tanimoto A, Takeuchi S, Fukuda K, Sato H, et al. In vitro and in vivo anti-tumor activity of alectinib in tumor cells with NCOA4-RET. Oncotarget. 2017;8(43):73766. doi: 10.18632/oncotarget.17900 29088743.

42. Pandey R, Bhattacharya A, Bhardwaj V, Jha V, Mandal AK, Mukerji M. Alu-miRNA interactions modulate transcript isoform diversity in stress response and reveal signatures of positive selection. Sci Rep. 2016;6:32348. doi: 10.1038/srep32348 27586304.

43. Gewurz BE, Towfic F, Mar JC, Shinners NP, Takasaki K, Zhao B, et al. Genome-wide siRNA screen for mediators of NF-κB activation. Proc Natl Acad Sci U S A. 2012;109(7):2467–72. doi: 10.1073/pnas.1120542109 22308454.

44. Maeda K, Enomoto A, Hara A, Asai N, Kobayashi T, Horinouchi A, et al. Identification of Meflin as a potential marker for mesenchymal stromal cells. Sci Rep. 2016;6:22288. doi: 10.1038/srep22288 26924503.

45. Otsubo K, Goto H, Nishio M, Kawamura K, Yanagi S, Nishie W, et al. MOB1-YAP1/TAZ-NKX2. 1 axis controls bronchioalveolar cell differentiation, adhesion and tumour formation. Oncogene. 2017;36(29):4201–11. doi: 10.1038/onc.2017.58 28346423.

46. Wang D, Shi W, Tang Y, Liu Y, He K, Hu Y, et al. Prefoldin 1 promotes EMT and lung cancer progression by suppressing cyclin A expression. Oncogene. 2017;36(7):885. doi: 10.1038/onc.2016.257 27694898.

47. Berchtold S, Grünwald B, Krüger A, Reithmeier A, Hähl T, Cheng T, et al. Collagen type V promotes the malignant phenotype of pancreatic ductal adenocarcinoma. Cancer Lett. 2015;356(2):721–32. doi: 10.1016/j.canlet.2014.10.020 25449434.

48. Satish L, Krill-Burger JM, Gallo PH, Des Etages S, Liu F, Philips BJ, et al. Expression analysis of human adipose-derived stem cells during in vitro differentiation to an adipocyte lineage. BMC Med Genomics. 2015;8(1):41. doi: 10.1186/s12920-015-0119-8 26205789.

49. Li Z, Lin S, Jiang T, Wang J, Lu H, Tang H, et al. Overexpression of eIF3e is correlated with colon tumor development and poor prognosis. Int J Clin Exp Pathol. 2014;7(10):6462–74. 25400724.

50. Oku M, Tanakura S, Uemura A, Sohda M, Misumi Y, Taniguchi M, et al. Novel cis-acting element GASE regulates transcriptional induction by the Golgi stress response. Cell Struct Funct. 2011;36(1):1–12. doi: 10.1247/csf.10014 21150128.

51. Stoddart A, Qian Z, Fernald AA, Bergerson RJ, Wang J, Karrison T, et al. Retroviral insertional mutagenesis identifies the del (5q) genes, CXXC5, TIFAB and ETF1, as well as the Wnt pathway, as potential targets in del (5q) myeloid neoplasms. Haematologica. 2016;101(6):e232–e6. doi: 10.3324/haematol.2015.139527 26944478.

52. Tsao N, Yang Y-C, Deng Y-J, Chang Z-F. The direct interaction of NME3 with Tip60 in DNA repair. Biochem J. 2016;473(9):1237–45. doi: 10.1042/BCJ20160122 26945015.

53. Herold N, Rudd SG, Sanjiv K, Kutzner J, Myrberg IH, Paulin CB, et al. With me or against me: Tumor suppressor and drug resistance activities of SAMHD1. Exp Hematol Oncol. 2017;52:32–9. doi: 10.1016/j.exphem.2017.05.001 28502830.

54. Moreira TG, Zhang L, Shaulov L, Harel A, Kuss SK, Williams J, et al. Sec13 regulates expression of specific immune factors involved in inflammation in vivo. Sci Rep. 2015;5:17655. doi: 10.1038/srep17655 26631972.

55. Wang L, Hirohashi Y, Ogawa T, Shen M, Takeda R, Murai A, et al. LY6/PLAUR domain containing 3 has a role in the maintenance of colorectal cancer stem-like cells. Biochem Biophys Res Commun. 2017;486(2):232–8. doi: 10.1016/j.bbrc.2017.02.112 28238780.

56. Li J-p, Liu Y, Yin Y-h. ARHGAP1 overexpression inhibits proliferation, migration and invasion of C-33A and SiHa cell lines. Onco Targets Ther. 2017;10:691. doi: 10.2147/OTT.S112223 28223826.

57. Tapia O, Fong LG, Huber MD, Young SG, Gerace L. Nuclear envelope protein Lem2 is required for mouse development and regulates MAP and AKT kinases. PloS one. 2015;10(3):e0116196. doi: 10.1371/journal.pone.0116196 25790465.

58. Park YY, Kim SB, Han HD, Sohn BH, Kim JH, Liang J, et al. Tat‐activating regulatory DNA‐binding protein regulates glycolysis in hepatocellular carcinoma by regulating the platelet isoform of phosphofructokinase through microRNA 520. Hepatology. 2013;58(1):182–91. doi: 10.1002/hep.26310 23389994.

59. Guo H, Chitiprolu M, Roncevic L, Javalet C, Hemming FJ, Trung MT, et al. Atg5 disassociates the V 1 V 0-ATPase to promote exosome production and tumor metastasis independent of canonical macroautophagy. Dev Cell. 2017;43(6):716–30. e7. doi: 10.1016/j.devcel.2017.11.018 29257951.

60. Von Ohlen T, Luce-Fedrow A, Ortega MT, Ganta RR, Chapes SK. Identification of critical host mitochondrion-associated genes during Ehrlichia chaffeensis infections. Infect Immun. 2012;80(10):3576–86. doi: 10.1128/IAI.00670-12 22851751.

61. Hofer-Warbinek R, Schmid J, Mayer H, Winsauer G, Orel L, Mueller B, et al. A highly conserved proapoptotic gene, IKIP, located next to the APAF1 gene locus, is regulated by p53. Cell Death Differ. 2004;11(12):1317–25. doi: 10.1038/sj.cdd.4401502 15389287.

62. Hu M, Du J, Cui L, Huang T, Guo X, Zhao Y, et al. IL-10 and PRKDC polymorphisms are associated with glioma patient survival. Oncotarget. 2016;7(49):80680–7. doi: 10.18632/oncotarget.13028 27811370.

63. Zhang Y-x, Qin C-p, Zhang X-q, Wang Q-r, Zhao C-b, Yuan Y-q, et al. Knocking down glycoprotein nonmetastatic melanoma protein B suppresses the proliferation, migration, and invasion in bladder cancer cells. Tumour Biol. 2017;39(4):1010428317699119. doi: 10.1177/1010428317699119 28443476.

64. Pokidysheva E, Boudko S, Vranka J, Zientek K, Maddox K, Moser M, et al. Biological role of prolyl 3-hydroxylation in type IV collagen. Proc Natl Acad Sci U S A. 2014;111(1):161–6. doi: 10.1073/pnas.1307597111 24368846.

65. Ge Y, Xu A, Zhang M, Xiong H, Fang L, Zhang X, et al. FK506 binding protein 10 is overexpressed and promotes renal cell carcinoma. Urol Int. 2017;98(2):169–76. doi: 10.1159/000448338 27602571.

66. Boudko SP, Ishikawa Y, Nix J, Chapman MS, Bächinger HP. Structure of human peptidyl‐prolyl cis–trans isomerase FKBP22 containing two EF‐hand motifs. Protein Sci. 2014;23(1):67–75. doi: 10.1002/pro.2391 24272907.

67. Liang J, Wang J, Azfer A, Song W, Tromp G, Kolattukudy PE, et al. A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem. 2008;283(10):6337–46. doi: 10.1074/jbc.M707861200 18178554.

68. Faraz M, Herdenberg C, Holmlund C, Henriksson R, Hedman H. A protein interaction network centered on leucine-rich repeats and immunoglobulin-like domains 1 (LRIG1) regulates growth factor receptors. J Biol Chem. 2018;293(9):3421–35. doi: 10.1074/jbc.M117.807487 29317492.

69. Shen J, Su J, Wu D, Zhang F, Fu H, Zhou H, et al. Growth inhibition accompanied by MOB1 upregulation in human acute lymphoid leukemia cells by 3-deazaneplanocin A. Biochem Genet. 2015;53(9–10):268–79. doi: 10.1007/s10528-015-9688-7 26298709.

70. Lignitto L, Arcella A, Sepe M, Rinaldi L, Delle Donne R, Gallo A, et al. Proteolysis of MOB1 by the ubiquitin ligase praja2 attenuates Hippo signalling and supports glioblastoma growth. Nat Commun. 2013;4:1822. doi: 10.1038/ncomms2791 23652010.

71. Nishio M, Hamada K, Kawahara K, Sasaki M, Noguchi F, Chiba S, et al. Cancer susceptibility and embryonic lethality in Mob1a/1b double-mutant mice. J Clin Invest. 2012;122(12):4505–18. doi: 10.1172/JCI63735 23143302.

72. Wang D-D, Jin Q, Wang L-L, Han S-F, Chen Y-B, Sun G-D, et al. The significance of ENAH in carcinogenesis and prognosis in gastric cancer. Oncotarget. 2017;8(42):72466. doi: 10.18632/oncotarget.19801 29069803.

73. Takahashi K, Suzuki K. WAVE2, N‐WASP, and mena facilitate cell invasion via phosphatidylinositol 3‐kinase‐dependent local accumulation of actin filaments. J Cell Biochem. 2011;112(11):3421–9. doi: 10.1002/jcb.23276 21769917.

74. Santiago-Medina M, Yang J. MENA promotes tumor-intrinsic metastasis through ECM remodeling and haptotaxis. Cancer Discov. 2016;6(5):474–6. doi: 10.1158/2159-8290.CD-16-0231 27138561.

75. Shintani Y, Fukumoto Y, Chaika N, Svoboda R, Wheelock MJ, Johnson KR. Collagen I–mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J Cell Biol. 2008;180(6):1277–89. doi: 10.1083/jcb.200708137 18362184.

76. Barsky SH, Rao CN, Grotendorst GR, Liotta LA. Increased content of Type V Collagen in desmoplasia of human breast carcinoma. Am J Pathol. 1982;108(3):276. 6287844.

77. Fischer H, Stenling R, Rubio C, Lindblom A. Differential expression of aquaporin 8 in human colonic epithelial cells and colorectal tumors. BMC Physiol. 2001;1(1):1. doi: 10.1186/1472-6793-1-1 11231887.

78. Bernardi P, Bonaldo P. Dysfunction of mitochondria and sarcoplasmic reticulum in the pathogenesis of collagen VI muscular dystrophies. Ann N Y Acad Sci 2008;1147(1):303–11. doi: 10.1196/annals.1427.009 19076452.

79. Karousou E, D’Angelo ML, Kouvidi K, Vigetti D, Viola M, Nikitovic D, et al. Collagen VI and hyaluronan: the common role in breast cancer. Biomed Res Int. 2014;2014. doi: 10.1155/2014/606458 25126569.

80. Dong Y, Zhao Q, Ma X, Ma G, Liu C, Chen Z, et al. Establishment of a new OSCC cell line derived from OLK and identification of malignant transformation-related proteins by differential proteomics approach. Sci Rep. 2015;5:12668. doi: 10.1038/srep12668 26234610.

81. Fan J, Liu J, Culty M, Papadopoulos V. Acyl-coenzyme A binding domain containing 3 (ACBD3; PAP7; GCP60): an emerging signaling molecule. Prog Lipid Res. 2010;49(3):218–34. doi: 10.1016/j.plipres.2009.12.003 20043945.

82. Yokdang N, Nordmeier S, Speirs K, Burkin HR, Buxton IL. Blockade of extracellular NM23 or its endothelial target slows breast cancer growth and metastasis. Integr Cancer Sci Ther. 2015;2(4):192–200. doi: 10.15761/icst.1000139 26413311.

83. Burbelo P, Wellstein A, Pestell RG. Altered Rho GTPase signaling pathways in breast cancer cells. Breast Cancer Res Treat. 2004;84(1):43–8. doi: 10.1023/B:BREA.0000018422.02237.f9 14999153.

84. Sasahira T, Nishiguchi Y, Kurihara-Shimomura M, Nakashima C, Kuniyasu H, Kirita T. NIPA-like domain containing 1 is a novel tumor-promoting factor in oral squamous cell carcinoma. J Cancer Res Clin Oncol. 2018;144(5):875–82. doi: 10.1007/s00432-018-2612-x 29464350.

85. Zeng Q, Cao K, Liu R, Huang J, Xia K, Tang J, et al. Identification of TDP-43 as an oncogene in melanoma and its function during melanoma pathogenesis. Cancer Biol Ther. 2017;18(1):8–15. doi: 10.1080/15384047.2016.1250984 27786596.

86. Kim PY, Tan O, Liu B, Trahair T, Liu T, Haber M, et al. High TDP43 expression is required for TRIM16-induced inhibition of cancer cell growth and correlated with good prognosis of neuroblastoma and breast cancer patients. Cancer lett. 2016;374(2):315–23. doi: 10.1016/j.canlet.2016.02.021 26902425.

87. Ke H, Zhao L, Zhang H, Feng X, Xu H, Hao J, et al. Loss of TDP43 inhibits progression of triple-negative breast cancer in coordination with SRSF3. Proc Natl Acad Sci U S A. 2018;115(15):E3426–E35. doi: 10.1073/pnas.1714573115 29581274.

88. Gong Y, Li X, Jin J, Zhou L, Guo Y. AB015. The expression and function of coiled-coil domain-containing protein 34 in human bladder carcinoma. Transl Androl Urol. 2016;5(Suppl 1). doi: 10.21037/tau.2016.s015

89. Liu J, Li J, Li P, Wang Y, Liang Z, Jiang Y, et al. Loss of DLG5 promotes breast cancer malignancy by inhibiting the Hippo signaling pathway. Sci Rep. 2017;7:42125. doi: 10.1038/srep42125 28169360.

90. Gu F, Ma Y, Zhang J, Qin F, Fu L. Function of Slit/Robo signaling in breast cancer. Front Med. 2015;9(4):431–6. doi: 10.1007/s11684-015-0416-9 26542734.

91. Kitching R, Li H, Wong MJ, Kanaganayakam S, Kahn H, Seth A. Characterization of a novel human breast cancer associated gene (BCA3) encoding an alternatively spliced proline-rich protein. Biochim Biophys Acta-Gene Struct Expression. 2003;1625(1):116–21. doi: 10.1016/S0167-4781(02)00562-6 12527432.

92. Gao N, Hibi Y, Cueno M, Asamitsu K, Okamoto T. A-kinase-interacting protein 1 (AKIP1) acts as a molecular determinant of PKA in NF-κB signaling. J Biol Chem. 2010;285(36):28097–104. doi: 10.1074/jbc.M110.116566 20562110.

93. Ito Y, Ito T, Karasawa S, Enomoto T, Nashimoto A, Hase Y, et al. Identification of DNA-dependent protein kinase catalytic subunit (DNA-PKcs) as a novel target of bisphenol A. PloS one. 2012;7(12):e50481. doi: 10.1371/journal.pone.0050481 23227178.

94. Lee HS, Yang H-K, Kim WH, Choe G. Loss of DNA-dependent protein kinase catalytic subunit (DNA-PKcs) expression in gastric cancers. Cancer Res Treat. 2005;37(2):98. doi: 10.4143/crt.2005.37.2.98 19956487.

95. Tajima JY, Futamura M, Gaowa S, Mori R, Tanahashi T, Tanaka Y, et al. Clinical significance of glycoprotein non-metastatic B and its association with EGFR/HER2 in gastrointestinal cancer. J Cancer. 2018;9(2):358–66. doi: 10.7150/jca.20266 29344282.

96. Maric G, Rose AA, Annis MG, Siegel PM. Glycoprotein non-metastatic b (GPNMB): A metastatic mediator and emerging therapeutic target in cancer. Onco Targets Ther. 2013;6:839–52. doi: 10.2147/OTT.S44906 23874106.

97. Rose AA, Pepin F, Russo C, Khalil JEA, Hallett M, Siegel PM. Osteoactivin promotes breast cancer metastasis to bone. Mol Cancer Res. 2007;5(10):1001–14. doi: 10.1158/1541-7786.MCR-07-0119 17951401.

98. Sannino S, Brodsky JL. Targeting protein quality control pathways in breast cancer. BMC Biol. 2017;15(1):109. doi: 10.1186/s12915-017-0449-4 29145850.

99. Garcia MR, Steinbauer B, Srivastava K, Singhal M, Mattijssen F, Maida A, et al. Acetyl-CoA carboxylase 1-dependent protein acetylation controls breast cancer metastasis and recurrence. Cell Metab. 2017;26(6):842–55.e5. doi: 10.1016/j.cmet.2017.09.018 29056512.

100. Takeuchi H, Abe M, Takumi Y, Hashimoto T, Kobayashi R, Osoegawa A, et al. The prognostic impact of the platelet distribution width-to-platelet count ratio in patients with breast cancer. PloS one. 2017;12(12):e0189166. doi: 10.1371/journal.pone.0189166 29216259.

101. Tang Y, Olufemi L, Wang M-T, Nie D. Role of Rho GTPases in breast cancer. Front Biosci. 2008;13:759–76. doi: 10.2741/2718 17981586.

102. Sigismund S, Avanzato D, Lanzetti L. Emerging functions of the EGFR in cancer. Molecular Oncology. 2018;12(1):3–20. doi: 10.1002/1878-0261.12155 29124875.

103. Henson E, Chen Y, Gibson S. EGFR family members’ regulation of autophagy is at a crossroads of cell survival and death in cancer. Cancers. 2017;9(4):27. doi: 10.3390/cancers9040027 28338617.

104. Pendharkar N, Dhali S, Abhang S. A novel strategy to investigate tissue-secreted tumor microenvironmental proteins in serum toward development of breast cancer early diagnosis biomarker signature. PROTEOMICS–Clinical Applications. 0(0):1700119. doi: 10.1002/prca.201700119 30281209.

105. Gomig THB, Cavalli IJ, Souza RLRd, Vieira E, Lucena ACR, Batista M, et al. Quantitative label-free mass spectrometry using contralateral and adjacent breast tissues reveal differentially expressed proteins and their predicted impacts on pathways and cellular functions in breast cancer. Journal of Proteomics. 2019;199:1–14. doi: 10.1016/j.jprot.2019.02.007 30772490.

106. Fang S, Tian H, Li X, Jin D, Li X, Kong J, et al. Clinical application of a microfluidic chip for immunocapture and quantification of circulating exosomes to assist breast cancer diagnosis and molecular classification. PLOS ONE. 2017;12(4):e0175050. doi: 10.1371/journal.pone.0175050 28369094.

107. Xie H, Tong G, Zhang Y, Liang S, Tang K, Yang Q. PGK1 drives hepatocellular carcinoma metastasis by enhancing metabolic process. Int J Mol Sci. 2017;18(8):E1630. doi: 10.3390/ijms18081630 28749413.

108. Zygulska A, Krzemieniecki K, Pierzchalski P. Hippo pathway-brief overview of its relevance in cancer. J Physiol Pharmacol. 2017;68(3):311–35. 28820389.


Článek vyšel v časopise

PLOS One


2020 Číslo 1