Sains Malaysiana 53(8)(2024): 1749-1765
http://doi.org/10.17576/jsm-2024-5308-03
Proteomic Profiling of Serum of Women with BI-RADS 1
to 5: Identification of Potential Complementary Biomarkers for Early Detection
of Breast Cancer
(Pemprofilan Proteomik Serum Wanita dengan BI-RADS
1 hingga 5: Pengenalpastian Penanda Bio Pelengkap Berpotensi untuk Pengesanan Awal Kanser Payudara)
JAIME JACQUELINE JAYAPALAN1,2,*,
CHRISTINA JANE VELLAN1, TANIA ISLAM3, NUR AISHAH MOHD
TAIB3 & KARUTHAN CHINNA4
1Department of Molecular Medicine, Faculty of Medicine, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
2Universiti Malaya Centre for Proteomics Research (UMCPR), Universiti Malaya, 50603 Kuala Lumpur, Malaysia
3Department of Surgery, Faculty of Medicine, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
4Faculty of Business and Management, UCSI University, Cheras,
56100 Kuala Lumpur, Malaysia
Diserahkan: 20 Februari 2024/Diterima: 26 Jun 2024
Abstract
Mammography remains the gold standard for the screening of breast cancer
(BrCa) despite its shortcomings. Cancer antigen 15-3,
an FDA-approved biomarker, is most useful as a treatment response and
recurrence monitoring tool rather than for early detection of BrCa. Given this, we aimed to screen for potential
complementary diagnostic protein biomarkers in the serum of women with BI-RADS
1 to 5. Individual neat sera of women with BI-RADS 1 to 5 (N = 33) were
subjected to two-dimensional electrophoresis (2-DE) for the separation of
proteins. Comparative analysis of the 2-DE silver-stained gel images was
performed using Progenesis SameSpots software. The identification of protein spots of interest was determined
following tandem MS/MS analysis and database search using either MASCOT or X! Tandem Vengeance search engines. Data are
available via ProteomeXchange with the
identifier PXD040427. The Bioinformatics tools of The Database for Annotation,
Visualization, and Integrated Discovery were used for the functional
annotation of the proteins of
altered abundance. A total of 8 non-redundant proteins including albumin, apolipoprotein A-I, apolipoprotein A-II, clusterin, complement C3, immunoglobulin kappa
constant, kininogen-1, and leucine-rich alpha-2 glycoprotein were found
significantly overexpressed in the sera of women with BI-RADS 4 and/or 5 (p < 0.01, FC ≥ 2). Functional annotation of the significantly
differentially expressed proteins showed their possible roles in the
development of BrCa. The identified protein
signatures are potential biomarkers for use in complement with mammography for
improved detection of BrCa at an early stage.
Keywords: BI-RADS; biomaker; breast cancer; early detection;
mass spectrometry;
two-dimensional electrophoresis
Abstrak
Mamografi tetap dianggap sebagai piawaian emas dalam saringan kanser payudara (BrCa) walaupun terdapat beberapa kelemahan. Antigen kanser 15-3
yang diluluskan oleh FDA lebih berguna sebagai alat pemantauan tindak balas rawatan dan pengesan kanser berulang daripada untuk pengesanan awal BrCa. Oleh itu, kajian ini bertujuan untuk menyaring dan mengenal pasti penanda protein diagnostik yang mungkin menjadi pelengkap dalam serum wanita yang tergolong dalam kategori BI-RADS 1 hingga 5.
Serum individu wanita tersebut telah diuji menggunakan teknik elektroforesis dua dimensi (2-DE) untuk memisahkan protein (N = 33). Analisis imej gel 2-DE dilakukan dengan menggunakan perisian Progenesis SameSpots. Pengenalpastian tompok protein yang berkaitan dilakukan melalui analisis spektrometri jisim berganda dan pencarian dalam pangkalan data menggunakan enjin carian MASCOT atau X! Tandem Vengeance. Maklumat mengenai data kajian boleh didapati melalui repositori ProteomeXchange dengan kod pengenalan PXD040427. Alat Bioinformatik Pangkalan Data untuk Anotasi, Visualisasi dan Penemuan Bersepadu (DAVID) telah digunakan untuk anotasi fungsi protein yang mempunyai kelimpahan yang berbeza. Sejumlah 8
protein termasuk albumin, apolipoprotein A-I, apolipoprotein A-II, clusterin, complement C3, immunoglobulin
kappa constant, kininogen-1 dan leucine-rich
alpha-2 glycoprotein didapati meningkat secara signifikan dalam serum wanita yang tergolong dalam kategori BI-RADS 4 dan/atau 5 (p < 0.01, FC ≥ 2). Anotasi fungsi protein ini menunjukkan keterlibatan potensi mereka dalam proses perkembangan BrCa. Penemuan protein ini menonjolkan potensi sebagai penanda bio tambahan untuk digunakan bersama mammografi bagi meningkatkan keupayaan pengesanan BrCa pada peringkat awal.
Kata kunci: BI-RADS; elektroforesis dua dimensi; kanser payudara; penanda bio; pengesanan awal; spektrometri jisim
RUJUKAN
Abdul-Rahman, P.S.,
Lim, B.K. & Hashim, O.H. 2007. Expression of high-abundance proteins in
sera of patients with endometrial and cervical cancers: Analysis using 2-DE
with silver staining and lectin detection methods. Electrophoresis 28(12):
1989-1996. https://doi.org/10.1002/elps.200600629
Barsnes, H. & Vaudel, M. 2018. SearchGUI: A highly adaptable common
interface for proteomics search and de novo engines. Journal of Proteome
Research 17(7): 2552-2555. https://doi.org/10.1021/acs.jproteome.8b00175
Ben Hassen, C., Gutierrez-Pajares, J.L., Guimaraes, C., Guibon, R.,
Pinault, M., Fromont, G., & Frank, P.G. 2020. Apolipoprotein-mediated
regulation of lipid metabolism induces distinctive effects in different types
of breast cancer cells. Breast Cancer Research 22(1): 38. https://doi.org/10.1186/s13058-020-01276-9
Benjamini, Y. & Hochberg, Y. 1995. Controlling the false discovery
rate: A practical and powerful approach to multiple testing. Journal of the
Royal Statistical Society: Series B (Methodological) 57(1): 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bevers, T.B., Helvie, M., Bonaccio, E., Calhoun, K.E., Daly, M.B.,
Farrar, W.B., Garber, J.E., Gray, R., Greenberg, C.C., Greenup, R., Hansen,
N.M., Harris, R.E., Heerdt, A.S., Helsten, T., Hodgkiss, L., Hoyt, T.L., Huff,
J.G., Jacobs, L., Lehman, C.D., Monsees, B., Niell, B.L., Parker, C.C.,
Pearlman, M., Philpotts, L., Shepardson, L.B., Smith, M.L., Stein, M., Tumyan,
L., Williams, C., Bergman, M.A. & Kumar, R. 2018. Breast cancer screening
and diagnosis, version 3.2018, NCCN clinical practice guidelines in oncology. Journal
of National Comprehensive Cancer Network 16(11): 1362-1389. https://doi.org/10.6004/jnccn.2018.0083
Boire, A., Zou, Y., Shieh, J., Macalinao, D.G., Pentsova, E. &
Massagué, J. 2017. Complement component 3 adapts the cerebrospinal fluid for
leptomeningeal metastasis. Cell 168(6): 1101-1113.e13. https://doi.org/10.1016/j.cell.2017.02.025
Borgquist, S., Hall, P., Lipkus, I. & Garber, J.E. 2018. Towards
prevention of breast cancer: What are the clinical challenges? Cancer
Prevention Research 11(5): 255-264. https://doi.org/10.1158/1940-6207.capr-16-0254
Borrebaeck, C.A.K. 2017. Precision diagnostics: Moving towards protein
biomarker signatures of clinical utility in cancer. Nature Reviews Cancer 17(3):
199-204. https://doi.org/10.1038/nrc.2016.153
Cedó, L., Reddy, S.T., Mato, E., Blanco-Vaca, F. & Escolà-Gil, J.C.
2019. HDL and LDL: Potential new players in breast cancer development. Journal
of Clinical Medicine 8(6): 853. https://doi.org/10.3390/jcm8060853
Chen, Q.F., Chang, L., Su, Q., Zhao, Y. & Kong, B. 2021. Clinical
importance of serum secreted clusterin in predicting invasive breast cancer and
treatment responses. Bioengineered 12(1): 278-285. https://doi.org/10.1080/21655979.2020.1868732
Choi, J.W., Moon, B.I., Lee, J.W., Kim, H.J., Jin, Y. & Kim, H.J.
2018. Use of CA15‑3 for screening breast cancer: An antibody‑lectin
sandwich assay for detecting glycosylation of CA15‑3 in sera. Oncology
Reports 40(1): 145-154. https://doi.org/10.3892/or.2018.6433
Craig, R. & Beavis, R.C. 2004. TANDEM: Matching proteins with tandem
mass spectra. Bioinformatics 20(9): 1466-1467. https://doi.org/10.1093/bioinformatics/bth092
Duffy, M.J., McDermott, E.W. & Crown, J. 2018. Blood-based
biomarkers in breast cancer: From proteins to circulating tumor cells to circulating
tumor DNA. Tumour Biology 40(5): 1010428318776169. https://doi.org/10.1177/1010428318776169
Fouda, M.S., Aljarwani, R.M., Aboul-Enein, K. & Omran, M.M. 2021.
Diagnostic performances of leucine-rich α-2-glycoprotein 1 and stem cell
factor for diagnosis and follow-up of colorectal cancer. Journal of Genetic
Engineering and Biotechnology 19(1): 17. https://doi.org/10.1186/s43141-021-00116-3
Gajbhiye, A., Dabhi, R., Taunk, K., Vannuruswamy, G., RoyChoudhury, S.,
Adhav, R., Seal, S., Mane, A., Bayatigeri, S., Santra, M.K., Chaudhury, K.
& Rapole, S. 2016. Urinary proteome alterations in HER2 enriched breast
cancer revealed by multipronged quantitative proteomics. Proteomics 16(17):
2403-2418. https://doi.org/10.1002/pmic.201600015
George, A.L., Shaheed, S.U. & Sutton, C.W. 2021. High-throughput
proteomic profiling of nipple aspirate fluid from breast cancer patients
compared with non-cancer controls: A step closer to clinical feasibility. Journal
of Clinical Medicine 10(11): 2243. https://doi.org/10.3390/jcm10112243
Gupta, D. & Lis, C.G. 2010. Pretreatment serum albumin as a
predictor of cancer survival: A systematic review of the epidemiological
literature. Nutrition Journal 9: 69. https://doi.org/10.1186/1475-2891-9-69
Harkness, E.F., Astley, S.M. & Evans, D.G. 2020. Risk-based breast
cancer screening strategies in women. Best Practice & Research Clinical
Obstetrics & Gynaecology 65: 3-17. https://doi.org/10.1016/j.bpobgyn.2019.11.005
Honda, K., Katzke, V.A., Hüsing, A., Okaya, S., Shoji, H., Onidani, K.,
Olsen, A., Tjønneland, A., Overvad, K., Weiderpass, E., Vineis, P., Muller, D.,
Tsilidis, K., Palli, D., Pala, V., Tumino, R., Naccarati, A., Panico, S.,
Aleksandrova, K., Boeing, H., Bueno-de-Mesquita, H.B., Peeters, P.H.,
Trichopoulou, A., Lagiou, P., Khaw, K.T., Wareham, N., Travis, R.C., Merino,
S., Duell, E.J., Rodríguez-Barranco, M., Chirlaque, M.D., Barricarte, A.,
Rebours, V., Boutron-Ruault, M.C., Romana Mancini, F., Brennan, P., Scelo, G.,
Manjer, J., Sund, M., Öhlund, D., Canzian, F. & Kaaks, R. 2019. CA19-9 and
apolipoprotein-A2 isoforms as detection markers for pancreatic cancer: A
prospective evaluation. International Journal of Cancer 144(8):
1877-1887. https://doi.org/10.1002/ijc.31900
Huang, D.W., Sherman, B.T. & Lempicki, R.A. 2009. Systematic and
integrative analysis of large gene lists using DAVID bioinformatics resources. Nature
Protocols 4(1): 44-57. https://doi.org/10.1038/nprot.2008.211
Jackson, W.D., Gulino, A., Fossati-Jimack, L., Castro Seoane, R., Tian,
K., Best, K., Köhl, J., Belmonte, B., Strid, J. & Botto, M. 2021. C3 drives
inflammatory skin carcinogenesis independently of C5. The Journal of
Investigative Dermatology 141(2): 404-414.e406. https://doi.org/10.1016/j.jid.2020.06.025
Jayapalan, J.J., Ng, K.L., Razack, A.H. & Hashim, O.H. 2012.
Identification of potential complementary serum biomarkers to differentiate
prostate cancer from benign prostatic hyperplasia using gel- and lectin-based
proteomics analyses. Electrophoresis 33(12): 1855-1862. https://doi.org/10.1002/elps.201100608
Jin, J., Kim, J-M., Hur, Y-S., Cho, W.P., Lee, K-Y., Ahn, S-I., Hong,
K.C. & Park, I-S. 2012. Clinical significance of clusterin expression in
pancreatic adenocarcinoma. World Journal of Surgical Oncology 10(1):
146. https://doi.org/10.1186/1477-7819-10-146
Kosmas, C.E., Martinez, I., Sourlas, A., Bouza, K.V., Campos, F.N.,
Torres, V., Montan, P.D. & Guzman, E. 2018. High-density lipoprotein (HDL)
functionality and its relevance to atherosclerotic cardiovascular disease. Drugs
in Context 7: 212525. https://doi.org/10.7573/dic.212525
Kühn, T., Sookthai, D., Graf, M.E., Schübel, R., Freisling, H., Johnson,
T., Katzke, V. & Kaaks, R. 2017. Albumin, bilirubin, uric acid and cancer
risk: Results from a prospective population-based study. British Journal of
Cancer 117(10): 1572-1579. https://doi.org/10.1038/bjc.2017.313
Kwon, Y.W., Jo, H.S., Bae, S., Seo, Y., Song, P., Song, M. & Yoon,
J.H. 2021. Application of proteomics in cancer: Recent trends and approaches
for biomarkers discovery. Frontiers in Medicine 8: 747333. https://doi.org/10.3389/fmed.2021.747333
Lang, T.A. & Altman, D.G. 2015. Basic statistical reporting for
articles published in biomedical journals: The "Statistical analyses and
methods in the published literature" or the SAMPL guidelines. International
Journal of Nursing Studies 52(1): 5-9. https://doi.org/10.1016/j.ijnurstu.2014.09.006
Lee, K.A., Talati, N., Oudsema, R., Steinberger, S. & Margolies,
L.R. 2018. BI-RADS 3: Current and future use of probably benign. Current
Radiology Reports 6(2): 5. https://doi.org/10.1007/s40134-018-0266-8
Lee, P.Y., Saraygord-Afshari, N. & Low, T.Y. 2020. The evolution of
two-dimensional gel electrophoresis - from proteomics to emerging alternative
applications. Journal of Chromatography A 1615: 460763. https://doi.org/10.1016/j.chroma.2019.460763
Li, J., Guan, X., Fan, Z., Ching, L-M., Li, Y., Wang, X., Cao, W-M.
& Liu, D-X. 2020. Non-invasive biomarkers for early detection of breast
cancer. Cancers 12(10): 2767. https://doi.org/10.3390/cancers12102767
Lobo, M.D., Moreno, F.B., Souza, G.H., Verde, S.M., Moreira, R.A. &
Monteiro-Moreira, A.C. 2017. Label-free proteome analysis of plasma from
patients with breast cancer: Stage-specific protein expression. Frontiers in
Oncology 7: 14. https://doi.org/10.3389/fonc.2017.00014
Meleady, P. 2023. Two-dimensional gel electrophoresis and 2D-DIGE. Methods
in Molecular Biology 2596: 3-15. https://doi.org/10.1007/978-1-0716-2831-7_1
Monticciolo, D.L., Helvie, M.A. & Hendrick, R.E. 2018. Current
issues in the overdiagnosis and overtreatment of breast cancer. AJR American
Journal of Roentgenology 210(2): 285-291. https://doi.org/10.2214/ajr.17.18629
Moujaess, E., Fakhoury, M., Assi, T., Elias, H., El Karak, F., Ghosn, M.
& Kattan, J. 2017. The therapeutic use of human albumin in cancer patients'
management. Critical Reviews in Oncology/Hematology 120: 203-209. https://doi.org/10.1016/j.critrevonc.2017.11.008
Nunez, C. 2019. Blood-based protein biomarkers in breast cancer. Clinica
Chimica Acta 490: 113-127. https://doi.org/10.1016/j.cca.2018.12.028
Palacios-Acedo, A-L., Langiu, M., Crescence, L., Mège, D., Dubois, C.
& Panicot-Dubois, L. 2022. Platelet and cancer-cell interactions modulate
cancer-associated thrombosis risk in different cancer types. Cancers 14(3):
730. https://www.mdpi.com/2072-6694/14/3/730
Palacios-Acedo, A.L., Mège, D., Crescence, L., Dignat-George, F.,
Dubois, C. & Panicot-Dubois, L. 2019. Platelets, thrombo-inflammation, and
cancer: Collaborating with the enemy. Frontiers in Immunology 10: 1805. https://doi.org/10.3389/fimmu.2019.01805
Pang, W.W., Abdul-Rahman, P.S., Wan-Ibrahim, W.I. & Hashim, O.H.
2010. Can the acute-phase reactant proteins be used as cancer biomarkers? The
International Journal of Biological Markers 25(1): 1-11.
Peng, M., Deng, J., Zhou, S., Tao, T., Su, Q., Yang, X. & Yang, X.
2019. The role of clusterin in cancer metastasis. Cancer Management &
Research 11: 2405-2414. https://doi.org/10.2147/cmar.S196273
Perez-Riverol, Y., Bai, J., Bandla, C., García-Seisdedos, D.,
Hewapathirana, S., Kamatchinathan, S., Kundu, Deepti J., Prakash, A.,
Frericks-Zipper, A., Eisenacher, M., Walzer, M., Wang, S., Brazma, A. &
Vizcaíno, J.A. 2021. The PRIDE database resources in 2022: A hub for mass
spectrometry-based proteomics evidences. Nucleic Acids Research 50(D1):
D543-D552. https://doi.org/10.1093/nar/gkab1038
Perkins, D.N., Pappin, D.J., Creasy, D.M. & Cottrell, J.S. 1999.
Probability-based protein identification by searching sequence databases using
mass spectrometry data. Electrophoresis 20(18): 3551-3567. https://doi.org/10.1002/(sici)1522-2683(19991201)20:18<3551::aid-elps3551>3.0.co;2-2
Pio, R., Corrales, L. & Lambris, J.D. 2014. The role of complement
in tumor growth. Advances in Experimental Medicine and Biology 772:
229-262. https://doi.org/10.1007/978-1-4614-5915-6_11
Qiu, Y.,
Korteweg, C., Chen, Z., Li, J., Luo, J., Huang, G. & Gu, J. 2012. Immunoglobulin
G expression and its colocalization with complement proteins in papillary
thyroid cancer. Mod. Pathol. 25(1): 36-45.
doi:10.1038/modpathol.2011.139
Ren, L., Yi, J., Li, W., Zheng, X., Liu, J., Wang, J. & Du, G. 2019.
Apolipoproteins and cancer. Cancer Medicine 8(16): 7032-7043. https://doi.org/10.1002/cam4.2587
Revel, M., Daugan, M.V., Sautés-Fridman, C., Fridman, W.H. &
Roumenina, L.T. 2020. Complement system: Promoter or suppressor of cancer
progression? Antibodies (Basel) 9(4): 57. https://doi.org/10.3390/antib9040057
Roumenina, L.T., Daugan, M.V., Noé, R., Petitprez, F., Vano, Y.A.,
Sanchez-Salas, R., Becht, E., Meilleroux, J., Clec'h, B. L., Giraldo, N. A.,
Merle, N.S., Sun, C.M., Verkarre, V., Validire, P., Selves, J., Lacroix, L.,
Delfour, O., Vandenberghe, I., Thuilliez, C., Keddani, S., Sakhi, I.B., Barret,
E., Ferré, P., Corvaïa, N., Passioukov, A., Chetaille, E., Botto, M., de Reynies,
A., Oudard, S.M., Mejean, A., Cathelineau, X., Sautès-Fridman, C. &
Fridman, W.H. 2019. Tumor cells hijack macrophage-produced complement C1q to
promote tumor growth. Cancer Immunology Research 7(7): 1091-1105. https://doi.org/10.1158/2326-6066.cir-18-0891
Schrödl, W., Büchler, R., Wendler, S., Reinhold, P., Muckova, P.,
Reindl, J. & Rhode, H. 2016. Acute phase proteins as promising biomarkers:
Perspectives and limitations for human and veterinary medicine. Proteomics
Clinical Applications 10(11): 1077-1092. https://doi.org/10.1002/prca.201600028
Schwartz, G.G., Tretli, S., Vos, L. & Robsahm, T.E. 2017.
Prediagnostic serum calcium and albumin and ovarian cancer: A nested
case-control study in the Norwegian Janus serum bank cohort. Cancer
Epidemiology 49: 225-230. https://doi.org/10.1016/j.canep.2017.07.004
Seely, J.M. & Alhassan, T. 2018. Screening for breast cancer in 2018
- what should we be doing today? Current Oncology 25(Suppl 1):
S115-S124. https://doi.org/10.3747/co.25.3770
Senent, Y., Tavira, B., Pio, R. & Ajona, D. 2022. The complement
system as a regulator of tumor-promoting activities mediated by myeloid-derived
suppressor cells. Cancer Letters 549: 215900. https://doi.org/https://doi.org/10.1016/j.canlet.2022.215900
Shah, T.A. & Guraya, S.S. 2017. Breast cancer screening programs:
Review of merits, demerits, and recent recommendations practiced across the
world. Journal of Microscopy and Ultrastructure 5(2): 59-69. https://doi.org/10.1016/j.jmau.2016.10.002
Sharma, B. & Agnihotri, N. 2019. Role of cholesterol homeostasis and
its efflux pathways in cancer progression. The Journal of Steroid
Biochemistry and Molecular Biology 191: 105377. https://doi.org/10.1016/j.jsbmb.2019.105377
Sickles, E.A., D'Orsi, C.J. & Bassett, L.W. 2013. ACR BI-RADS®
mammography. In ACR BI-RADS® Atlas, Breast Imaging Reporting and Data System.
5th ed., edited by D'Orsi, C.J., Sickles, E.A., Mendelson, E.B. & Morris,
E.A. American College of Radiology. pp. 121-140.
Sun, X-B., Liu, W-W., Wang, B., Yang, Z-P., Tang, H-Z., Lu, S., Wang, Y-Y.,
Qu, J-X. & Rao, B-Q. 2023. Correlations between serum lipid and Ki‑67
levels in different breast cancer molecular subcategories. Oncology Letters 25(2):
53. https://doi.org/10.3892/ol.2022.13639
Sung, H., Ferlay, J., Siegel, R.L., Laversanne, M., Soerjomataram, I.,
Jemal, A. & Bray, F. 2021. Global cancer statistics 2020: GLOBOCAN
estimates of incidence and mortality worldwide for 36 cancers in 185 countries CA:
A Cancer Journal for Clinicians 71(3): 209-249. https://doi.org/https://doi.org/10.3322/caac.21660
Tellez, T., Garcia-Aranda, M. & Redondo, M. 2016. The role of
clusterin in carcinogenesis and its potential utility as therapeutic target. Current
Medicinal Chemistry 23(38): 4297-4308. https://doi.org/10.2174/0929867323666161024150540
Tomczak, M. & Tomczak, E. 2014. The need to report effect size
estimates revisited. An overview of some recommended measures of effect size. Trends
in Sport Sciences 1(21): 19-25.
van der Vorst, E.P.C. 2020. High-density lipoproteins and apolipoprotein
A-I. Subcell Biochem. 94: 399-420. https://doi.org/10.1007/978-3-030-41769-7_16
Vaudel, M., Burkhart, J.M., Zahedi, R.P., Oveland, E., Berven, F.S.,
Sickmann, A., Martens, L. & Barsnes, H. 2015. PeptideShaker enables
reanalysis of MS-derived proteomics data sets. Nature Biotechnology 33(1):
22-24. https://doi.org/10.1038/nbt.3109
Wang, W., Wang, S. & Zhang, M. 2020. Evaluation of kininogen 1,
osteopontin and alpha-1-antitrypsin in plasma, bronchoalveolar lavage fluid and
urine for lung squamous cell carcinoma diagnosis. Oncology Letters 19(4):
2785-2792. https://doi.org/10.3892/ol.2020.11376
Xie, Z-B., Zhang, Y-F., Jin, C., Mao, Y-S. & Fu, D-L. 2019. LRG-1
promotes pancreatic cancer growth and metastasis via modulation of the EGFR/p38
signaling. Journal of Experimental & Clinical Cancer Research 38(1):
75. https://doi.org/10.1186/s13046-019-1088-0
Yan, J.X., Wait, R., Berkelman, T., Harry, R.A., Westbrook, J.A.,
Wheeler, C.H. & Dunn, M.J. 2000. A modified silver staining protocol for
visualization of proteins compatible with matrix-assisted laser
desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21(17): 3666-3672. https://doi.org/10.1002/1522-2683(200011)21:17<3666::aid-elps3666>3.0.co;2-6
Yang, B., Ma, C., Chen, Z., Yi, W., McNutt, M.A., Wang, Y., Korteweg, C.
& Gu, J. 2013. Correlation of immunoglobulin G expression and histological
subtype and stage in breast cancer. PLoS ONE 8(3): e58706. https://doi.org/10.1371/journal.pone.0058706
Yang, Y., Zhang, H., Zhang, M., Meng, Q., Cai, L. & Zhang, Q. 2017.
Elevation of serum CEA and CA15-3 levels during antitumor therapy predicts poor
therapeutic response in advanced breast cancer patients. Oncology Letters 14(6):
7549-7556. https://doi.org/10.3892/ol.2017.7164
Yuan, B., Wu, C., Wang, X., Wang, D., Liu, H., Guo, L., Li, X.A., Han,
J. & Feng, H. 2016. High scavenger receptor class B type I expression is
related to tumor aggressiveness and poor prognosis in breast cancer. Tumour
Biology 37(3): 3581-3588. https://doi.org/10.1007/s13277-015-4141-4
Zhang, J., Zhu, L., Fang, J., Ge, Z. & Li, X. 2016. LRG1 modulates
epithelial-mesenchymal transition and angiogenesis in colorectal cancer via
HIF-1α activation. Journal of Experimental & Clinical Cancer
Research 35: 29. https://doi.org/10.1186/s13046-016-0306-2
Zhang, R., Liu, Q., Li, T., Liao, Q. & Zhao, Y. 2019. Role of the
complement system in the tumor microenvironment. Cancer Cell International 19:
300. https://doi.org/10.1186/s12935-019-1027-3
Zhang, Y.S., Han, L., Yang, C., Liu, Y.J. & Zhang, X.M. 2021.
Prognostic value of LRG1 in breast cancer: A retrospective study. Oncology
Research and Treatment 44(1-2): 36-42. https://doi.org/10.1159/000510945
Zhou, Y., Wang, W., Wei, R., Jiang, G., Li, F., Chen, X., Wang, X.,
Long, S., Ma, D. & Xi, L. 2019. Serum bradykinin levels as a diagnostic
marker in cervical cancer with a potential mechanism to promote VEGF expression
via BDKRB2. International Journal of Oncology 55(1): 131-141. https://doi.org/10.3892/ijo.2019.4792
Zografos, E., Anagnostopoulos, A.K., Papadopoulou, A., Legaki, E.,
Zagouri, F., Marinos, E., Tsangaris, G.T. & Gazouli, M. 2019. Serum proteomic
signatures of male breast cancer. Cancer Genomics & Proteomics 16(2):
129-137.
Zou, Y., Xu, Y., Chen, X., Wu, Y., Fu, L. & Lv, Y. 2022. Research
progress on leucine-rich alpha-2 glycoprotein 1: A review. Frontiers in
Pharmacology 12. https://doi.org/10.3389/fphar.2021.809225
*Pengarang untuk surat-menyurat; email: jaime_jacklyn@um.edu.my
|