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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Quantifying Serum Derived Differential Expressed and Low Molecular Weight Protein in Breast Cancer Patients

Author(s): Ayesha Zafar, Maryum Jabbar, Yasmeen Manzoor, Huma Gulzar, Shahzad Gul Hassan, Muniba Anum Nazir, Ain-ul-Haq, Ghazala Mustafa, Romana Sahar, Aqeel Masood, Ahtesham Iqbal, Mulazim Hussain and Murtaza Hasan*

Volume 27, Issue 7, 2020

Page: [658 - 673] Pages: 16

DOI: 10.2174/0929866527666200110155609

Price: $65

Abstract

Background: Searching the biomarker from complex heterogeneous material for early detection of disease is a challenging task in the field of biomedical sciences.

Objective: The study has been arranged to explore the proteomics serum derived profiling of the differential expressed and low molecular weight protein in breast cancer patient.

Methods: Quantitative proteome was analyzed using the Nano LC/Mass and Bioinformatics tool.

Results: This quantification yields 239 total protein constituting 29% of differentially expressed protein, with 82% downregulated differential protein and 18% up-regulated differential protein. While 12% of total protein were found to be cancer inducing proteins. Gene Ontology (GO) described that the altered proteins with 0-60 kDa mass in nucleus, cytosol, ER, and mitochondria were abundant that chiefly controlled the RNA, DNA, ATP, Ca ion and receptor bindings.

Conclusion: The study demonstrate that the organelle specific, low molecular weighted proteins are significantly important biomarker. That act as strong agents in the prognosis and diagnosis of breast cancer at early stage.

Keywords: Breast cancer, proteomics, low weighted serum protein, Nano LC/Mass, bioinformatics, gene ontology.

Graphical Abstract

[1]
Donepudi, M.S.; Kondapalli, K.; Amos, S.J.; Venkanteshan, P. Breast cancer statistics and markers. J. Cancer Res. Ther., 2014, 10(3), 506-511.
[PMID: 25313729]
[2]
Khokher, S.; Qureshi, M.U.; Riaz, M.; Akhtar, N.; Saleem, A. Clinicopathologic profile of breast cancer patients in Pakistan: ten years data of a local cancer hospital. Asian Pac. J. Cancer Prev., 2012, 13(2), 693-698.
[http://dx.doi.org/10.7314/APJCP.2012.13.2.693] [PMID: 22524846]
[3]
Liede, A.; Malik, I.A.; Aziz, Z.; Rios Pd, Pde.L.; Kwan, E.; Narod, S.A. Contribution of BRCA1 and BRCA2 mutations to breast and ovarian cancer in Pakistan. Am. J. Hum. Genet., 2002, 71(3), 595-606.
[http://dx.doi.org/10.1086/342506] [PMID: 12181777]
[4]
Majeed, A.I. Awareness and screening of breast cancer among rural areas of Islamabad capital territory. Ann. Pak. Inst. Med. Sci, 2017, 2, 103-107.
[5]
Li, L.; Liu, C.C.; Chen, X.; Xu, S.; Hernandez Cortes-Manno, S.; Cheng, S.H. Mechanistic study of bakuchiol-induced anti-breast cancer stem cell and in vivo anti-metastasis effects. Front. Pharmacol., 2017, 8, 746.
[http://dx.doi.org/10.3389/fphar.2017.00746] [PMID: 29093680]
[6]
Hasan, M.; Mustafa, G.; Iqbal, J.; Ashfaq, M.; Mahmood, N. Quantitative proteomic analysis of HeLa cells in response to biocompatible Fe2C@C nanoparticles: 16O/18O-labelling & HPLC-ESI-orbit-trap profiling approach. Toxicol. Res. (Camb.), 2017, 7(1), 84-92.
[http://dx.doi.org/10.1039/C7TX00248C] [PMID: 30090565]
[7]
Iqbal, J.; Li, W.; Hasan, M.; Liu, K.; Awan, U.; Saeed, Y.; Zhang, Y.; Muhammad Khan, A.; Shah, A.; Qing, H.; Deng, Y. Differential expression of specific cellular defense proteins in rat hypothalamus under simulated microgravity induced conditions: comparative proteomics. Proteomics, 2014, 14(11), 1424-1433.
[http://dx.doi.org/10.1002/pmic.201400019] [PMID: 24648329]
[8]
Hasan, M. Biocompatibility of iron carbide and detection of metals ions signaling proteomic analysis via HPLC/ESI-Orbitrap. Nano Res., 2017, 10(6), 1912-1923.
[http://dx.doi.org/10.1007/s12274-016-1375-4]
[9]
Gu, W.Y.; Liu, M.X.; Sun, B.Q.; Guo, M.Q.; Wu, J.L.; Li, N. Profiling of polyunsaturated fatty acids in human serum using off-line and on-line solid phase extraction-nano-liquid chromatography-quadrupole-time-of-flight mass spectrometry. J. Chromatogr. A, 2018, 1537, 141-146.
[http://dx.doi.org/10.1016/j.chroma.2018.01.015] [PMID: 29373129]
[10]
Wang, H.; Shi, T.; Qian, W.J.; Liu, T.; Kagan, J.; Srivastava, S.; Smith, R.D.; Rodland, K.D.; Camp, D.G., II The clinical impact of recent advances in LC-MS for cancer biomarker discovery and verification. Expert Rev. Proteomics, 2016, 13(1), 99-114.
[http://dx.doi.org/10.1586/14789450.2016.1122529] [PMID: 26581546]
[11]
Iqbal, J.; Li, W.; Hasan, M.; Juan Li, Y.; Ullah, K.; Yun, W.; Awan, U.; Qing, H.; Deng, Y. Distortion of homeostatic signaling proteins by simulated microgravity in rat hypothalamus: A(16) O/(18) O-labeled comparative integrated proteomic approach. Proteomics, 2014, 14(2-3), 262-273.
[http://dx.doi.org/10.1002/pmic.201300337] [PMID: 24323493]
[12]
Zhang, Y.; Wang, H.; Lai, C.; Wang, L.; Deng, Y. Comparative proteomic analysis of human SH-SY5Y neuroblastoma cells under simulated microgravity. Astrobiology, 2013, 13(2), 143-150.
[http://dx.doi.org/10.1089/ast.2012.0822] [PMID: 23421552]
[13]
Castello, A.; Fischer, B.; Eichelbaum, K.; Horos, R.; Beckmann, B.M.; Strein, C.; Davey, N.E.; Humphreys, D.T.; Preiss, T.; Steinmetz, L.M.; Krijgsveld, J.; Hentze, M.W. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell, 2012, 149(6), 1393-1406.
[http://dx.doi.org/10.1016/j.cell.2012.04.031] [PMID: 22658674]
[14]
Gaudet, P.; Livstone, M.S.; Lewis, S.E.; Thomas, P.D. Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Brief. Bioinform., 2011, 12(5), 449-462.
[http://dx.doi.org/10.1093/bib/bbr042] [PMID: 21873635]
[15]
Jakobsson, M.E.; Moen, A.; Bousset, L.; Egge-Jacobsen, W.; Kernstock, S.; Melki, R.; Falnes, P.Ø. Identification and characterization of a novel human methyltransferase modulating Hsp70 protein function through lysine methylation. J. Biol. Chem., 2013, 288(39), 27752-27763.
[http://dx.doi.org/10.1074/jbc.M113.483248] [PMID: 23921388]
[16]
Sánchez-Font, M.F.; Sebastià, J.; Sanfeliu, C.; Cristòfol, R.; Marfany, G.; Gonzàlez-Duarte, R. Peroxiredoxin 2 (PRDX2), an antioxidant enzyme, is under-expressed in Down syndrome fetal brains. Cell. Mol. Life Sci., 2003, 60(7), 1513-1523.
[http://dx.doi.org/10.1007/s00018-003-3048-1] [PMID: 12943237]
[17]
Shalom-Barak, T.; Knaus, U.G. A p21-activated kinase-controlled metabolic switch up-regulates phagocyte NADPH oxidase. J. Biol. Chem., 2002, 277(43), 40659-40665.
[http://dx.doi.org/10.1074/jbc.M206650200] [PMID: 12189148]
[18]
Fujita, Y.; Okamoto, T.; Noshiro, M.; McKeehan, W.L.; Crabb, J.W.; Whitney, R.G.; Kato, Y.; Sato, J.D.; Takada, K. A novel heparin-binding protein, HBp15, is identified as mammalian ribosomal protein L22. Biochem. Biophys. Res. Commun., 1994, 199(2), 706-713.
[http://dx.doi.org/10.1006/bbrc.1994.1286] [PMID: 8135813]
[19]
Jaeken, J.; Detheux, M.; Van Maldergem, L.; Foulon, M.; Carchon, H.; Van Schaftingen, E. 3-Phosphoglycerate dehydrogenase deficiency: an inborn error of serine biosynthesis. Arch. Dis. Child., 1996, 74(6), 542-545.
[http://dx.doi.org/10.1136/adc.74.6.542] [PMID: 8758134]
[20]
Bian, Y.; Song, C.; Cheng, K.; Dong, M.; Wang, F.; Huang, J.; Sun, D.; Wang, L.; Ye, M.; Zou, H. An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J. Proteomics, 2014, 96, 253-262.
[http://dx.doi.org/10.1016/j.jprot.2013.11.014] [PMID: 24275569]
[21]
Zhou, H.; Di Palma, S.; Preisinger, C.; Peng, M.; Polat, A.N.; Heck, A.J.; Mohammed, S. Toward a comprehensive characterization of a human cancer cell phosphoproteome. J. Proteome Res., 2013, 12(1), 260-271.
[http://dx.doi.org/10.1021/pr300630k] [PMID: 23186163]
[22]
Li, Z.; Liu, J-Y.; Zhang, J-T. 14-3-3σ, the double-edged sword of human cancers. Am. J. Transl. Res., 2009, 1(4), 326-340.
[PMID: 19956445]
[23]
Ponzetti, M.; Capulli, M.; Angelucci, A.; Ventura, L.; Monache, S.D.; Mercurio, C.; Calgani, A.; Sanità, P.; Teti, A.; Rucci, N. Non-conventional role of haemoglobin beta in breast malignancy. Br. J. Cancer, 2017, 117(7), 994-1006.
[http://dx.doi.org/10.1038/bjc.2017.247] [PMID: 28772282]
[24]
Li, X.; Wu, Z.; Wang, Y.; Mei, Q.; Fu, X.; Han, W. Characterization of adult α- and β-globin elevated by hydrogen peroxide in cervical cancer cells that play a cytoprotective role against oxidative insults. PLoS One, 2013, 8(1) e54342
[http://dx.doi.org/10.1371/journal.pone.0054342] [PMID: 23349856]
[25]
Maman, S.; Sagi-Assif, O.; Yuan, W.; Ginat, R.; Meshel, T.; Zubrilov, I.; Keisari, Y.; Lu, W.; Lu, W.; Witz, I.P. The beta subunit of hemoglobin (HBB2/HBB) suppresses neuroblastoma growth and metastasis. Cancer Res., 2017, 77(1), 14-26.
[http://dx.doi.org/10.1158/0008-5472.CAN-15-2929] [PMID: 27793844]
[26]
Miao, P.; Sheng, S.; Sun, X.; Liu, J.; Huang, G. Lactate dehydrogenase A in cancer: A promising target for diagnosis and therapy. IUBMB Life, 2013, 65(11), 904-910.
[http://dx.doi.org/10.1002/iub.1216] [PMID: 24265197]
[27]
Shapiro, R.; Vallee, B.L. Human placental ribonuclease inhibitor abolishes both angiogenic and ribonucleolytic activities of angiogenin. Proc. Natl. Acad. Sci. USA, 1987, 84(8), 2238-2241.
[http://dx.doi.org/10.1073/pnas.84.8.2238] [PMID: 3470787]
[28]
Tang, Y.; Ren, F.; Cong, X.; Kong, Y.; Tian, Y.; Xu, Y.; Fan, J. Overexpression of ribonuclease inhibitor induces autophagy in human colorectal cancer cells via the Akt/mTOR/ULK1 pathway. Mol. Med. Rep., 2019, 19(5), 3519-3526.
[http://dx.doi.org/10.3892/mmr.2019.10030] [PMID: 30896869]
[29]
Zhuang, X.; Lv, M.; Zhong, Z.; Zhang, L.; Jiang, R.; Chen, J. Interplay between intergrin-linked kinase and ribonuclease inhibitor affects growth and metastasis of bladder cancer through signaling ILK pathways. J. Exp. Clin. Cancer Res., 2016, 35(1), 130.
[http://dx.doi.org/10.1186/s13046-016-0408-x] [PMID: 27576342]
[30]
Bhavsar, R.B.; Makley, L.N.; Tsonis, P.A. The other lives of ribosomal proteins. Hum. Genomics, 2010, 4(5), 327-344.
[http://dx.doi.org/10.1186/1479-7364-4-5-327] [PMID: 20650820]
[31]
Wang, W.; Nag, S.; Zhang, X.; Wang, M.H.; Wang, H.; Zhou, J.; Zhang, R. Ribosomal proteins and human diseases: pathogenesis, molecular mechanisms, and therapeutic implications. Med. Res. Rev., 2015, 35(2), 225-285.
[http://dx.doi.org/10.1002/med.21327] [PMID: 25164622]
[32]
Krishnan, R.; Boddapati, N.; Mahalingam, S. Interplay between human nucleolar GNL1 and RPS20 is critical to modulate cell proliferation. Sci. Rep., 2018, 8(1), 11421.
[http://dx.doi.org/10.1038/s41598-018-29802-y] [PMID: 30061673]
[33]
Schläfli, P.; Tröger, J.; Eckhardt, K.; Borter, E.; Spielmann, P.; Wenger, R.H. Substrate preference and phosphatidylinositol monophosphate inhibition of the catalytic domain of the Per-Arnt-Sim domain kinase PASKIN. FEBS J., 2011, 278(10), 1757-1768.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08100.x] [PMID: 21418524]
[34]
Chen, B.; Tan, Z.; Gao, J.; Wu, W.; Liu, L.; Jin, W.; Cao, Y.; Zhao, S.; Zhang, W.; Qiu, Z.; Liu, D.; Mo, X.; Li, W. Hyperphosphorylation of ribosomal protein S6 predicts unfavorable clinical survival in non-small cell lung cancer. J. Exp. Clin. Cancer Res., 2015, 34(1), 126.
[http://dx.doi.org/10.1186/s13046-015-0239-1] [PMID: 26490682]
[35]
Weedon-Fekjaer, M.S.; Dalen, K.T.; Solaas, K.; Staff, A.C.; Duttaroy, A.K.; Nebb, H.I. Activation of LXR increases acyl-CoA synthetase activity through direct regulation of ACSL3 in human placental trophoblast cells. J. Lipid Res., 2010, 51(7), 1886-1896.
[http://dx.doi.org/10.1194/jlr.M004978] [PMID: 20219900]
[36]
Hseu, M-J.; Yen, C-H.; Tzeng, M-C. Crocalbin: a new calcium-binding protein that is also a binding protein for crotoxin, a neurotoxic phospholipase A2. FEBS Lett., 1999, 445(2-3), 440-444.
[http://dx.doi.org/10.1016/S0014-5793(99)00177-5] [PMID: 10094503]
[37]
Kozlov, G.; Maattanen, P.; Schrag, J.D.; Pollock, S.; Cygler, M.; Nagar, B.; Thomas, D.Y.; Gehring, K. Crystal structure of the bb’ domains of the protein disulfide isomerase ERp57. Structure, 2006, 14(8), 1331-1339.
[http://dx.doi.org/10.1016/j.str.2006.06.019] [PMID: 16905107]
[38]
Arita, K.; Hashimoto, H.; Shimizu, T.; Nakashima, K.; Yamada, M.; Sato, M. Structural basis for Ca(2+)-induced activation of human PAD4. Nat. Struct. Mol. Biol., 2004, 11(8), 777-783.
[http://dx.doi.org/10.1038/nsmb799] [PMID: 15247907]
[39]
Hayano, T.; Kikuchi, M. Cloning and sequencing of the cDNA encoding human P5. Gene, 1995, 164(2), 377-378.
[http://dx.doi.org/10.1016/0378-1119(95)00474-K] [PMID: 7590364]
[40]
Yoshimura, S.; Gerondopoulos, A.; Linford, A.; Rigden, D.J.; Barr, F.A. Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors. J. Cell Biol., 2010, 191(2), 367-381.
[http://dx.doi.org/10.1083/jcb.201008051] [PMID: 20937701]
[41]
Bruneel, A.; Labas, V.; Mailloux, A.; Sharma, S.; Royer, N.; Vinh, J.; Pernet, P.; Vaubourdolle, M.; Baudin, B. Proteomics of human umbilical vein endothelial cells applied to etoposide-induced apoptosis. Proteomics, 2005, 5(15), 3876-3884.
[http://dx.doi.org/10.1002/pmic.200401239] [PMID: 16130169]
[42]
Mezquita, L.; Charrier, M.; Faivre, L.; Dupraz, L.; Lueza, B.; Remon, J.; Planchard, D.; Bluthgen, M.V.; Facchinetti, F.; Rahal, A.; Polo, V.; Gazzah, A.; Caramella, C.; Adam, J.; Pignon, J.P.; Soria, J.C.; Chaput, N.; Besse, B. Prognostic value of HLA-A2 status in advanced non-small cell lung cancer patients. Lung Cancer, 2017, 112, 10-15.
[http://dx.doi.org/10.1016/j.lungcan.2017.07.004] [PMID: 29191581]
[43]
Yang, X.Z.; Li, X.X.; Zhang, Y.J.; Rodriguez-Rodriguez, L.; Xiang, M.Q.; Wang, H.Y.; Zheng, X.F. Rab1 in cell signaling, cancer and other diseases. Oncogene, 2016, 35(44), 5699-5704.
[http://dx.doi.org/10.1038/onc.2016.81] [PMID: 27041585]
[44]
Nijholt, D.A.; Ijsselstijn, L.; van der Weiden, M.M.; Zheng, P.P.; Sillevis Smitt, P.A.; Koudstaal, P.J.; Luider, T.M.; Kros, J.M. Pregnancy zone protein is increased in the Alzheimer’s disease brain and associates with senile plaques. J. Alzheimers Dis., 2015, 46(1), 227-238.
[http://dx.doi.org/10.3233/JAD-131628] [PMID: 25737043]
[45]
Petersen, C.M.; Jensen, P.H.; Bukh, A.; Sunde, L.; Lamm, L.U.; Ingerslev, J. Pregnancy zone protein: a re-evaluation of serum levels in healthy women and in women suffering from breast cancer or trophoblastic disease. Scand. J. Clin. Lab. Invest., 1990, 50(5), 479-485.
[http://dx.doi.org/10.1080/00365519009089162] [PMID: 1700464]
[46]
Rodríguez-Almazán, C.; Arreola, R.; Rodríguez-Larrea, D.; Aguirre-López, B.; de Gómez-Puyou, M.T.; Pérez-Montfort, R.; Costas, M.; Gómez-Puyou, A.; Torres-Larios, A. Structural basis of human triosephosphate isomerase deficiency: mutation E104D is related to alterations of a conserved water network at the dimer interface. J. Biol. Chem., 2008, 283(34), 23254-23263.
[http://dx.doi.org/10.1074/jbc.M802145200] [PMID: 18562316]
[47]
Tamesa, M.S.; Kuramitsu, Y.; Fujimoto, M.; Maeda, N.; Nagashima, Y.; Tanaka, T.; Yamamoto, S.; Oka, M.; Nakamura, K. Detection of autoantibodies against cyclophilin A and triosephosphate isomerase in sera from breast cancer patients by proteomic analysis. Electrophoresis, 2009, 30(12), 2168-2181.
[http://dx.doi.org/10.1002/elps.200800675] [PMID: 19582718]
[48]
Singh, P.K.; Parsek, M.R.; Greenberg, E.P.; Welsh, M.J. A component of innate immunity prevents bacterial biofilm development. Nature, 2002, 417(6888), 552-555.
[http://dx.doi.org/10.1038/417552a] [PMID: 12037568]
[49]
Baldi, A. Tumor suppressors and cell-cycle proteins in lung cancer. Pathology research international, 2011, 2011
[http://dx.doi.org/10.4061/2011/605042]
[50]
Baltz, A.G.; Munschauer, M.; Schwanhäusser, B.; Vasile, A.; Murakawa, Y.; Schueler, M.; Youngs, N.; Penfold-Brown, D.; Drew, K.; Milek, M.; Wyler, E.; Bonneau, R.; Selbach, M.; Dieterich, C.; Landthaler, M. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell, 2012, 46(5), 674-690.
[http://dx.doi.org/10.1016/j.molcel.2012.05.021] [PMID: 22681889]
[51]
Zhao, Z.; Sagare, A.P.; Ma, Q.; Halliday, M.R.; Kong, P.; Kisler, K.; Winkler, E.A.; Ramanathan, A.; Kanekiyo, T.; Bu, G.; Owens, N.C.; Rege, S.V.; Si, G.; Ahuja, A.; Zhu, D.; Miller, C.A.; Schneider, J.A.; Maeda, M.; Maeda, T.; Sugawara, T.; Ichida, J.K.; Zlokovic, B.V. Central role for PICALM in amyloid-β blood-brain barrier transcytosis and clearance. Nat. Neurosci., 2015, 18(7), 978-987.
[http://dx.doi.org/10.1038/nn.4025] [PMID: 26005850]
[52]
Totta, P.; Pesiri, V.; Enari, M.; Marino, M.; Acconcia, F. Clathrin heavy chain interacts with estrogen receptor α and modulates 17β-estradiol signaling. Mol. Endocrinol., 2015, 29(5), 739-755.
[http://dx.doi.org/10.1210/me.2014-1385] [PMID: 25860340]
[53]
Kubota, H.; Hynes, G.; Willison, K. The eighth Cct gene, Cctq, encoding the theta subunit of the cytosolic chaperonin containing TCP-1. Gene, 1995, 154(2), 231-236.
[http://dx.doi.org/10.1016/0378-1119(94)00880-2] [PMID: 7890169]
[54]
Bassiouni, R.; Nemec, K.N.; Iketani, A.; Flores, O.; Showalter, A.; Khaled, A.S.; Vishnubhotla, P.; Sprung, R.W., Jr; Kaittanis, C.; Perez, J.M.; Khaled, A.R. Chaperonin containing TCP-1 protein level in breast cancer cells predicts therapeutic application of a cytotoxic peptide. Clin. Cancer Res., 2016, 22(17), 4366-4379.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2502] [PMID: 27012814]
[55]
Esposito, G.; Vitagliano, L.; Costanzo, P.; Borrelli, L.; Barone, R.; Pavone, L.; Izzo, P.; Zagari, A.; Salvatore, F. Human aldolase A natural mutants: relationship between flexibility of the C-terminal region and enzyme function. Biochem. J., 2004, 380(Pt 1), 51-56.
[http://dx.doi.org/10.1042/bj20031941] [PMID: 14766013]
[56]
Huang, Z.; Hua, Y.; Tian, Y.; Qin, C.; Qian, J.; Bao, M.; Liu, Y.; Wang, S.; Cao, Q.; Ju, X.; Wang, Z.; Gu, M. High expression of fructose-bisphosphate aldolase A induces progression of renal cell carcinoma. Oncol. Rep., 2018, 39(6), 2996-3006.
[PMID: 29693182]
[57]
Kamijo, T.; Aoyama, T.; Komiyama, A.; Hashimoto, T. Structural analysis of cDNAs for subunits of human mitochondrial fatty acid β-oxidation trifunctional protein. Biochem. Biophys. Res. Commun., 1994, 199(2), 818-825.
[http://dx.doi.org/10.1006/bbrc.1994.1302] [PMID: 8135828]
[58]
Ling, M.; Merante, F.; Chen, H.S.; Duff, C.; Duncan, A.M.; Robinson, B.H. The human mitochondrial elongation factor tu (EF-Tu) gene: cDNA sequence, genomic localization, genomic structure, and identification of a pseudogene. Gene, 1997, 197(1-2), 325-336.
[http://dx.doi.org/10.1016/S0378-1119(97)00279-5] [PMID: 9332382]
[59]
Luo, L.; Wang, Y.; Feng, Q.; Zhang, H.; Xue, B.; Shen, J.; Ye, Y.; Han, X.; Ma, H.; Xu, J.; Chen, D.; Yin, Z. Recombinant protein glutathione S-transferases P1 attenuates inflammation in mice. Mol. Immunol., 2009, 46(5), 848-857.
[http://dx.doi.org/10.1016/j.molimm.2008.09.010] [PMID: 18962899]
[60]
Vilardo, E.; Rossmanith, W. Molecular insights into HSD10 disease: impact of SDR5C1 mutations on the human mitochondrial RNase P complex. Nucleic Acids Res., 2015, 43(10), 5112-5119.
[http://dx.doi.org/10.1093/nar/gkv408] [PMID: 25925575]
[61]
Yasuda, T.; Kaji, Y.; Agatsuma, T.; Niki, T.; Arisawa, M.; Shuto, S.; Ariga, H.; Iguchi-Ariga, S.M. DJ-1 cooperates with PYCR1 in cell protection against oxidative stress. Biochem. Biophys. Res. Commun., 2013, 436(2), 289-294.
[http://dx.doi.org/10.1016/j.bbrc.2013.05.095] [PMID: 23743200]
[62]
Blachly-Dyson, E.; Zambronicz, E.B.; Yu, W.H.; Adams, V.; McCabe, E.R.; Adelman, J.; Colombini, M.; Forte, M. Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J. Biol. Chem., 1993, 268(3), 1835-1841.
[PMID: 8420959]
[63]
Yin, K. Positive correlation between expression level of mitochondrial serine hydroxymethyltransferase and breast cancer grade. OncoTargets Ther., 2015, 8, 1069-1074.
[http://dx.doi.org/10.2147/OTT.S82433] [PMID: 25999742]
[64]
Baumgartner, M.R.; Hu, C.A.; Almashanu, S.; Steel, G.; Obie, C.; Aral, B.; Rabier, D.; Kamoun, P.; Saudubray, J.M.; Valle, D. Hyperammonemia with reduced ornithine, citrulline, arginine and proline: a new inborn error caused by a mutation in the gene encoding delta(1)-pyrroline-5-carboxylate synthase. Hum. Mol. Genet., 2000, 9(19), 2853-2858.
[http://dx.doi.org/10.1093/hmg/9.19.2853] [PMID: 11092761]
[65]
Ye, Y.; Wu, Y.; Wang, J. Pyrroline-5-carboxylate reductase 1 promotes cell proliferation via inhibiting apoptosis in human malignant melanoma. Cancer Manag. Res., 2018, 10, 6399-6407.
[http://dx.doi.org/10.2147/CMAR.S166711] [PMID: 30568501]
[66]
Pridgeon, J.W.; Olzmann, J.A.; Chin, L.S.; Li, L. PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol., 2007, 5(7)e172
[http://dx.doi.org/10.1371/journal.pbio.0050172] [PMID: 17579517]
[67]
Song, H.Y.; Dunbar, J.D.; Zhang, Y.X.; Guo, D.; Donner, D.B. Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor. J. Biol. Chem., 1995, 270(8), 3574-3581.
[http://dx.doi.org/10.1074/jbc.270.8.3574] [PMID: 7876093]
[68]
Kirkin, V.; Lamark, T.; Sou, Y.S.; Bjørkøy, G.; Nunn, J.L.; Bruun, J.A.; Shvets, E.; McEwan, D.G.; Clausen, T.H.; Wild, P.; Bilusic, I.; Theurillat, J.P.; Øvervatn, A.; Ishii, T.; Elazar, Z.; Komatsu, M.; Dikic, I.; Johansen, T. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell, 2009, 33(4), 505-516.
[http://dx.doi.org/10.1016/j.molcel.2009.01.020] [PMID: 19250911]
[69]
Du, C.; Mark, D.; Wappenschmidt, B.; Böckmann, B.; Pabst, B.; Chan, S.; Cao, H.; Morlot, S.; Scholz, C.; Auber, B.; Rhiem, K.; Schmutzler, R.; Illig, T.; Schlegelberger, B.; Steinemann, D. A tandem duplication of BRCA1 exons 1-19 through DHX8 exon 2 in four families with hereditary breast and ovarian cancer syndrome. Breast Cancer Res. Treat., 2018, 172(3), 561-569.
[http://dx.doi.org/10.1007/s10549-018-4957-x] [PMID: 30191368]
[70]
Hoshide, R.; Matsuura, T.; Haraguchi, Y.; Endo, F.; Yoshinaga, M.; Matsuda, I. Carbamyl phosphate synthetase I deficiency. One base substitution in an exon of the CPS I gene causes a 9-basepair deletion due to aberrant splicing. J. Clin. Invest., 1993, 91(5), 1884-1887.
[http://dx.doi.org/10.1172/JCI116405] [PMID: 8486760]
[71]
Th’ng, J.P.; Sung, R.; Ye, M.; Hendzel, M.J. H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J. Biol. Chem., 2005, 280(30), 27809-27814.
[http://dx.doi.org/10.1074/jbc.M501627200] [PMID: 15911621]
[72]
Giessrigl, B.; Krieger, S.; Rosner, M.; Huttary, N.; Saiko, P.; Alami, M.; Messaoudi, S.; Peyrat, J.F.; Maciuk, A.; Gollinger, M.; Kopf, S.; Kazlauskas, E.; Mazal, P.; Szekeres, T.; Hengstschläger, M.; Matulis, D.; Jäger, W.; Krupitza, G. Hsp90 stabilizes Cdc25A and counteracts heat shock-mediated Cdc25A degradation and cell-cycle attenuation in pancreatic carcinoma cells. Hum. Mol. Genet., 2012, 21(21), 4615-4627.
[http://dx.doi.org/10.1093/hmg/dds303] [PMID: 22843495]
[73]
Buschow, S.I.; van Balkom, B.W.; Aalberts, M.; Heck, A.J.; Wauben, M.; Stoorvogel, W. MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol. Cell Biol., 2010, 88(8), 851-856.
[http://dx.doi.org/10.1038/icb.2010.64] [PMID: 20458337]
[74]
Sahni, N.; Yi, S.; Taipale, M.; Fuxman Bass, J.I.; Coulombe-Huntington, J.; Yang, F.; Peng, J.; Weile, J.; Karras, G.I.; Wang, Y.; Kovács, I.A.; Kamburov, A.; Krykbaeva, I.; Lam, M.H.; Tucker, G.; Khurana, V.; Sharma, A.; Liu, Y.Y.; Yachie, N.; Zhong, Q.; Shen, Y.; Palagi, A.; San-Miguel, A.; Fan, C.; Balcha, D.; Dricot, A.; Jordan, D.M.; Walsh, J.M.; Shah, A.A.; Yang, X.; Stoyanova, A.K.; Leighton, A.; Calderwood, M.A.; Jacob, Y.; Cusick, M.E.; Salehi-Ashtiani, K.; Whitesell, L.J.; Sunyaev, S.; Berger, B.; Barabási, A.L.; Charloteaux, B.; Hill, D.E.; Hao, T.; Roth, F.P.; Xia, Y.; Walhout, A.J.M.; Lindquist, S.; Vidal, M. Widespread macromolecular interaction perturbations in human genetic disorders. Cell, 2015, 161(3), 647-660.
[http://dx.doi.org/10.1016/j.cell.2015.04.013] [PMID: 25910212]
[75]
Grande-García, A.; Lallous, N.; Díaz-Tejada, C.; Ramón-Maiques, S. Structure, functional characterization, and evolution of the dihydroorotase domain of human CAD. Structure, 2014, 22(2), 185-198.
[http://dx.doi.org/10.1016/j.str.2013.10.016] [PMID: 24332717]
[76]
Deloulme, J.C.; Assard, N.; Mbele, G.O.; Mangin, C.; Kuwano, R.; Baudier, J. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J. Biol. Chem., 2000, 275(45), 35302-35310.
[http://dx.doi.org/10.1074/jbc.M003943200] [PMID: 10913138]
[77]
Li, F.; Bullough, K.Z.; Vashisht, A.A.; Wohlschlegel, J.A.; Philpott, C.C. Poly (rC)-binding Protein 2 regulates Hippo signaling to control growth in breast epithelial cells. Mol. Cell. Biol., 2016, 36(16), 2121-2131.
[http://dx.doi.org/10.1128/MCB.00104-16] [PMID: 27215387]
[78]
Gregório, A.C.; Lacerda, M.; Figueiredo, P.; Simões, S.; Dias, S.; Moreira, J.N. Meeting the needs of breast cancer: A nucleolin’s perspective. Crit. Rev. Oncol. Hematol., 2018, 125, 89-101.
[http://dx.doi.org/10.1016/j.critrevonc.2018.03.008] [PMID: 29650282]
[79]
Kininis, M.; Isaacs, G.D.; Core, L.J.; Hah, N.; Kraus, W.L. Postrecruitment regulation of RNA polymerase II directs rapid signaling responses at the promoters of estrogen target genes. Mol. Cell. Biol., 2009, 29(5), 1123-1133.
[http://dx.doi.org/10.1128/MCB.00841-08] [PMID: 19103744]
[80]
Zafrakas, M.; Losen, I.; Knüchel, R.; Dahl, E. Enhancer of the rudimentary gene homologue (ERH) expression pattern in sporadic human breast cancer and normal breast tissue. BMC Cancer, 2008, 8(1), 145.
[http://dx.doi.org/10.1186/1471-2407-8-145] [PMID: 18500978]
[81]
Carpenter, B.; Hill, K.J.; Charalambous, M.; Wagner, K.J.; Lahiri, D.; James, D.I.; Andersen, J.S.; Schumacher, V.; Royer-Pokora, B.; Mann, M.; Ward, A.; Roberts, S.G. BASP1 is a transcriptional cosuppressor for the Wilms’ tumor suppressor protein WT1. Mol. Cell. Biol., 2004, 24(2), 537-549.
[http://dx.doi.org/10.1128/MCB.24.2.537-549.2004] [PMID: 14701728]
[82]
Park, N.; Yoo, J.C.; Lee, Y.S.; Choi, H.Y.; Hong, S.G.; Hwang, E.M.; Park, J.Y. Copine1 C2 domains have a critical calcium-independent role in the neuronal differentiation of hippocampal progenitor HiB5 cells. Biochem. Biophys. Res. Commun., 2014, 454(1), 228-233.
[http://dx.doi.org/10.1016/j.bbrc.2014.10.075] [PMID: 25450385]
[83]
Harrison, J.K.; Jiang, Y.; Chen, S.; Xia, Y.; Maciejewski, D.; McNamara, R.K.; Streit, W.J.; Salafranca, M.N.; Adhikari, S.; Thompson, D.A.; Botti, P.; Bacon, K.B.; Feng, L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. USA, 1998, 95(18), 10896-10901.
[http://dx.doi.org/10.1073/pnas.95.18.10896] [PMID: 9724801]
[84]
Hirasaka, K.; Tokuoka, K.; Nakao, R.; Yamada, C.; Oarada, M.; Imagawa, T.; Ishidoh, K.; Okumura, Y.; Kishi, K.; Nikawa, T. Cathepsin C propeptide interacts with intestinal alkaline phosphatase and heat shock cognate protein 70 in human Caco-2 cells. J. Physiol. Sci., 2008, 58(2), 105-111.
[http://dx.doi.org/10.2170/physiolsci.RP013007] [PMID: 18307834]
[85]
Ciancaglini, P.; Yadav, M.C.; Simão, A.M.; Narisawa, S.; Pizauro, J.M.; Farquharson, C.; Hoylaerts, M.F.; Millán, J.L. Kinetic analysis of substrate utilization by native and TNAP-, NPP1-, or PHOSPHO1-deficient matrix vesicles. J. Bone Miner. Res., 2010, 25(4), 716-723.
[PMID: 19874193]
[86]
Weissbach, L.; Settleman, J.; Kalady, M.F.; Snijders, A.J.; Murthy, A.E.; Yan, Y.X.; Bernards, A. Identification of a human rasGAP-related protein containing calmodulin-binding motifs. J. Biol. Chem., 1994, 269(32), 20517-20521.
[PMID: 8051149]
[87]
Zeng, F.; Jiang, W.; Zhao, W.; Fan, Y.; Zhu, Y.; Zhang, H. Ras GTPase-Activating-Like Protein IQGAP1 (IQGAP1) promotes breast cancer proliferation and invasion and correlates with poor clinical outcomes. Med. Sci. Monit., 2018, 24, 3315-3323.
[http://dx.doi.org/10.12659/MSM.909916] [PMID: 29779034]
[88]
Xu, Y.; Rong, J.; Duan, S.; Chen, C.; Li, Y.; Peng, B.; Yi, B.; Zheng, Z.; Gao, Y.; Wang, K.; Yun, M.; Weng, H.; Zhang, J.; Ye, S. High expression of GNA13 is associated with poor prognosis in hepatocellular carcinoma. Sci. Rep., 2016, 6, 35948.
[http://dx.doi.org/10.1038/srep35948] [PMID: 27883022]
[89]
Scallon, B.J.; Fung, W.J.; Tsang, T.C.; Li, S.; Kado-Fong, H.; Huang, K.S.; Kochan, J.P. Primary structure and functional activity of a phosphatidylinositol-glycan-specific phospholipase D. Science, 1991, 252(5004), 446-448.
[http://dx.doi.org/10.1126/science.2017684] [PMID: 2017684]
[90]
Wick, M.R.; Swanson, P.E.; Manivel, J.C. Placental-like alkaline phosphatase reactivity in human tumors: An immunohistochemical study of 520 cases. Hum. Pathol., 1987, 18(9), 946-954.
[http://dx.doi.org/10.1016/S0046-8177(87)80274-5] [PMID: 3623553]

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