Differences in the Relative Abundance of ProBDNF and Mature BDNF in A549 and H1299 Human Lung Cancer Cell Media
Abstract
:1. Introduction
2. Results
2.1. Higher Levels of ProBDNF Are Detected in the Media of A549 Cells than in H1299 Cell Media
2.2. Treatment of A549 and H1299 Cells with the MMP2/9 Inhibitor Resulted in Increased ProBDNF Levels and Corresponded with Decreased Levels of mBDNF in the Media, While the Opposite Effect Was Observed upon Treatment with the p53 Inhibitor, Pifithrin-α, in A549 Cell Media
2.3. Treatment with the p53 Inhibitor, Pifithrin-α, Resulted in Higher Levels of MMP2 and MMP9 in the Conditioned Media of A549 Cells but Not in H1299 Cell Media
2.4. Treatment of A549 Cells with the p53 Inhibitor, Pifithrin-α, Resulted in Upregulation of PI3K and AKT Activities and the Phospho/Total NFκB Ratio
2.5. MMP9-siRNA Transfections Resulted in Decreased Levels of mBDNF and a Corresponding Increase in ProBDNF in the Media of A549 and H1299 Cells, while the Converse Was Observed upon Transfection of A549 Cells with p53 siRNA
2.6. Incubation with Exogenously Added MMP9, but Not MMP2, Resulted in Higher Levels of mBDNF and a Concomitant Decrease in the Levels of ProBDNF in the Media of A549 Cells, Effects That Were Relatively Minimal in H1299 Cell Media
2.7. MMP9 siRNA Treatment of Either A549 or H1299 Cells Decreased Cell Viability and Increased Apoptosis, an Effect Diminished upon the Same Treatment with ProBDNF Immunodepleted Media
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Cell Culture
4.3. MMP2/9 Level Measurement
4.4. PI3K Assay
4.5. AKT Assay
4.6. NFκB Assay
4.7. MTT Assay
4.8. Apoptosis Assay
4.9. Quantitation of proBDNF and mBDNF
4.10. Immunodepletion
4.11. Western Blotting
4.12. siRNA Transfection
4.13. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Xi, L.; Coello, M.C.; Litle, V.R.; Raja, S.; Gooding, W.E.; Yousem, S.A.; El-Hefnawy, T.; Landreneau, R.J.; Luketich, J.D.; Godfrey, T.E. A Combination of Molecular Markers Accurately Detects Lymph Node Metastasis in Non–Small Cell Lung Cancer Patients. Clin. Cancer Res. 2006, 12, 2484–2491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dasgupta, P.; Rizwani, W.; Pillai, S.; Kinkade, R.; Kovacs, M.; Rastogi, S.; Banerjee, S.; Carless, M.; Kim, E.; Coppola, D.; et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 2009, 124, 36–45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kowiański, P.; Lietzau, G.; Czuba, E.; Waśkow, M.; Steliga, A.; Moryś, J. BDNF: A Key Factor with Multipotent Impact on Brain Signaling and Synaptic Plasticity. Cell. Mol. Neurobiol. 2018, 38, 579–593. [Google Scholar] [CrossRef]
- Frisch, S.M.; Schaller, M.; Cieply, B. Mechanisms that link the oncogenic epithelial–mesenchymal transition to suppression of anoikis. J. Cell Sci. 2013, 126, 21–29. [Google Scholar] [CrossRef] [Green Version]
- De la Cruz-Morcillo, M.A.; Berger, J.; Sánchez-Prieto, R.; Saada, S.; Naves, T.; Guillaudeau, A.; Perraud, A.; Sindou, P.; Lacroix, A.; Descazeaud, A.; et al. p75 neurotrophin receptor and pro-BDNF promote cell survival and migration in clear cell renal cell carcinoma. Oncotarget 2016, 7, 34480–34497. [Google Scholar] [CrossRef] [PubMed]
- Radin, D.P.; Patel, P. BDNF: An Oncogene or Tumor Suppressor? Anticancer Res. 2017, 37, 3983–3990. [Google Scholar]
- Zhang, S.-Y.; Hui, L.-P.; Li, C.-Y.; Gao, J.; Cui, Z.-S.; Qiu, X.-S. More expression of BDNF associates with lung squamous cell carcinoma and is critical to the proliferation and invasion of lung cancer cells. BMC Cancer 2016, 16, 171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meng, L.; Liu, B.; Ji, R.; Jiang, X.; Yan, X.; Xin, Y. Targeting the BDNF/TrkB pathway for the treatment of tumors. Oncol. Lett. 2018, 17, 2031–2039. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blondy, S.; Christou, N.; David, V.; Verdier, M.; Jauberteau, M.-O.; Mathonnet, M.; Perraud, A. Neurotrophins and their involvement in digestive cancers. Cell Death Dis. 2019, 10, 1–12. [Google Scholar] [CrossRef]
- Pradhan, J.; Noakes, P.G.; Bellingham, M.C. The Role of Altered BDNF/TrkB Signaling in Amyo-trophic Lateral Sclerosis. Front. Cell Neurosci. 2019, 13, 368. [Google Scholar] [CrossRef] [PubMed]
- Xiong, J.; Zhou, L.; Yang, M.; Lim, Y.; Zhu, Y.; Fu, D.; Li, Z.; Zhong, J.; Xiao, Z.; Zhou, X.-F. ProB-DNF and its receptors are upregulated in glioma and inhibit the growth of glioma cells in vitro. Neuro-Oncology 2013, 15, 990–1007. [Google Scholar] [CrossRef] [Green Version]
- Sarris, E.G.; Saif, M.W.; Syrigos, K.N. The Biological Role of PI3K Pathway in Lung Cancer. Pharmaceuticals 2012, 5, 1236–1264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Das, K.; Lerner, N.; Sathe, S.; Cicek, M.; Casey, G.; Sizemore, N. The AKT/I kappa B kinase pathway promotes angiogenic/metastatic gene expression in colorectal cancer by activating nuclear factor-kappa B and beta-catenin. Oncogene 2005, 24, 1021–1031. [Google Scholar] [CrossRef] [Green Version]
- Wang, R.; Zhang, Q.; Peng, X.; Zhou, C.; Zhong, Y.; Chen, X.; Qiu, Y.; Jin, M.; Gong, M.; Kong, D. Stellettin B Induces G1 Arrest, Apoptosis and Autophagy in Human Non-small Cell Lung Cancer A549 Cells via Blocking PI3K/Akt/mTOR Pathway. Sci. Rep. 2016, 6, 27071. [Google Scholar] [CrossRef] [Green Version]
- Levine, A.J.; Oren, M. The first 30 years of p53: Growing ever more complex. Nat. Rev. Cancer 2009, 9, 749–758. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hafner, A.; Bulyk, M.L.; Jambhekar, A.; Lahav, G. The multiple mechanisms that regulate p53 activity and cell fate. Nat. Rev. Mol. Cell Biol. 2019, 20, 199–210. [Google Scholar] [CrossRef] [PubMed]
- Gottlieb, T.M.; Leal, J.F.M.; Seger, R.; Taya, Y.; Oren, M. Cross-talk between Akt, p53 and Mdm2: Possible implications for the regulation of apoptosis. Oncogene 2002, 21, 1299–1303. [Google Scholar] [CrossRef] [PubMed]
- Webster, G.A.; Perkins, N.D. Transcriptional Cross Talk between NF-κB and p53. Mol. Cell Biol. 1999, 19, 3485–3495. [Google Scholar] [CrossRef] [Green Version]
- Ozes, O.N.; Mayo, L.D.; Gustin, J.A.; Pfeffer, S.R.; Pfeffer, L.M.; Donner, D.B. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999, 401, 82–85. [Google Scholar] [CrossRef] [PubMed]
- Bai, D.; Ueno, L.; Vogt, P.K. Akt-mediated regulation of NFκB and the essentialness of NFκB for the oncogenicity of PI3K and Akt. Int. J. Cancer 2009, 125, 2863–2870. [Google Scholar] [CrossRef] [Green Version]
- Mancini, A.; Di Battista, J.A. Transcriptional regulation of matrix metalloprotease gene expression in health and disease. Front. Biosci. 2006, 11, 423–446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Senbanjo, L.T.; Chellaiah, M.A. CD44: A Multifunctional Cell Surface Adhesion Receptor Is a Regulator of Progression and Metastasis of Cancer Cells. Front. Cell Dev. Biol. 2017, 5, 18. [Google Scholar] [CrossRef] [Green Version]
- Saido, T.; Leissring, M.A. Proteolytic degradation of amyloid β-protein. Cold Spring Harb. Perspect. Med. 2012, 2, a006379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merchant, N.; Nagaraju, G.P.; Rajitha, B.; Lammata, S.; Jella, K.K.; Buchwald, Z.S.; Lakka, S.S.; Ali, A.N. Matrix metalloproteinases: Their functional role in lung cancer. Carcinogenesis 2017, 38, 766–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- A Diverse Role of MMP-2 and MMP-9 in the Onset of Alzheimer Disease and Cancer. Available online: https://austinpublishinggroup.com/neurology-neurosciences/fulltext/ann-v1-id1013.php (accessed on 20 June 2020).
- Zheng, S.; Chang, Y.; Hodges, K.B.; Sun, Y.; Ma, X.; Xue, Y.; Williamson, S.R.; Lopez-Beltran, A.; Montironi, R.; Cheng, L. Expression of KISS1 and MMP-9 in non-small cell lung cancer and their relations to metastasis and survival. Anticancer Res. 2010, 30, 713–718. [Google Scholar]
- Cai, X.; Zhu, H.; Li, Y. PKCζ, MMP-2 and MMP-9 expression in lung adenocarcinoma and association with a metastatic phenotype. Mol. Med. Rep. 2017, 16, 8301–8306. [Google Scholar] [CrossRef] [Green Version]
- González-Arriaga, P.; Pascual, T.; García-Alvarez, A.; Fernández-Somoano, A.; López-Cima, M.F.; Tardon, A. Genetic polymorphisms in MMP 2, 9 and 3genes modify lung cancer risk and survival. BMC Cancer 2012, 12, 121. [Google Scholar] [CrossRef] [Green Version]
- Han, L.; Sheng, B.; Zeng, Q.; Yao, W.; Jiang, Q. Correlation between MMP2 expression in lung cancer tissues and clinical parameters: A retrospective clinical analysis. BMC Pulm. Med. 2020, 20, 1–9. [Google Scholar] [CrossRef]
- Bian, J.; Sun, Y. Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter. Mol. Cell. Biol. 1997, 17, 6330–6338. [Google Scholar] [CrossRef] [Green Version]
- Chen, H.; Yuan, Y.; Zhang, C.; Luo, A.; Ding, F.; Ma, J.; Yang, S.; Tian, Y.; Tong, T.; Zhan, Q.; et al. Involvement of S100A14 Protein in Cell Invasion by Affecting Expression and Function of Matrix Metalloproteinase (MMP)-2 via p53-dependent Transcriptional Regulation. J. Biol. Chem. 2012, 287, 17109–17119. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Zhan, M.; Hannay, J.A.F.; Das, P.; Bolshakov, S.V.; Kotilingam, D.; Yu, D.; Lazar, A.F.; Pollock, R.E.; Lev, D. Wild-type p53 inhibits nuclear factor-kappaB-induced matrix metalloproteinase-9 promoter activation: Implications for soft tissue sarcoma growth and metastasis. Mol. Cancer Res. 2006, 4, 803–810. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.-Y.; Moon, H.; Chun, K.-H.; Chang, Y.-S.; Hassan, K.; Ji, L.; Lotan, R.; Khuri, F.R.; Hong, W.K. Effects of Insulin-like Growth Factor Binding Protein-3 and Farnesyltransferase Inhibitor SCH66336 on Akt Expression and Apoptosis in Non–Small-Cell Lung Cancer Cells. J. Natl. Cancer Inst. 2004, 96, 1536–1548. [Google Scholar] [CrossRef] [Green Version]
- Leroy, B.; Girard, L.; Hollestelle, A.; Minna, J.D.; Gazdar, A.F.; Soussi, T. Analysis of TP53 Mutation Status in Human Cancer Cell Lines: A Reassessment. Hum. Mutat. 2014, 35, 756–765. [Google Scholar] [CrossRef] [PubMed]
- Chen, B.; Liang, Y.; He, Z.; An, Y.; Zhao, W.; Wu, J. Autocrine activity of BDNF induced by the STAT3 signaling pathway causes prolonged TrkB activation and promotes human non-small-cell lung cancer proliferation. Sci. Rep. 2016, 6, 30404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akhtar, M.H.; Hussain, K.K.; Gurudatt, N.G.; Chandra, P.; Shim, Y.-B. Ultrasensitive dual probe immunosensor for the monitoring of nicotine induced-brain derived neurotrophic factor released from cancer cells. Biosens. Bioelectron. 2018, 116, 108–115. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Guo, D.; Luo, W.; Zhang, Q.; Zhang, Y.; Li, C.; Lu, Y.; Cui, Z.; Qiu, X. TrkB is highly expressed in NSCLC and mediates BDNF-induced the activation of Pyk2 signaling and the invasion of A549 cells. BMC Cancer 2010, 10, 43. [Google Scholar] [CrossRef] [Green Version]
- Okamura, K.; Harada, T.; Wang, S.; Ijichi, K.; Furuyama, K.; Koga, T.; Okamoto, T.; Takayama, K.; Yano, T.; Nakanishi, Y. Expression of TrkB and BDNF is associated with poor prognosis in non-small cell lung cancer. Lung Cancer 2012, 78, 100–106. [Google Scholar] [CrossRef]
- Tian, Q.; Cui, H.; Li, Y.; Lu, H. LY294002 induces differentiation and inhibits invasion of glioblastoma cells by targeting GSK-3beta and MMP. EXCLI J. 2012, 11, 68–77. [Google Scholar]
- Ding, L.; Getz, G.; Wheeler, D.A.; Mardis, E.R.; McLellan, M.D.; Cibulskis, K.; Sougnez, C.; Greulich, H.; Muzny, D.M.; Morgan, M.B.; et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008, 455, 1069–1075. [Google Scholar] [CrossRef]
- Zhang, Y.; Han, C.Y.; Duan, F.G.; Fan, X.-X.; Yao, X.-J.; Parks, R.J.; Tang, Y.-J.; Wang, M.-F.; Liu, L.; Tsang, B.K.; et al. p53 sensitizes chemoresistant non-small cell lung cancer via elevation of reactive oxygen species and suppression of EGFR/PI3K/AKT signaling. Cancer Cell Int. 2019, 19, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aubrey, B.J.; Kelly, G.L.; Janic, A.; Herold, M.J.; Strasser, A. How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death Differ. 2018, 25, 104–113. [Google Scholar] [CrossRef] [Green Version]
- Singh, B.; Reddy, P.G.; Goberdhan, A.; Walsh, C.; Dao, S.; Ngai, I.; Chou, T.C.; O-Charoenrat, P.; Levine, A.J.; Rao, P.H.; et al. p53 regulates cell survival by inhibiting PIK3CA in squamous cell carcinomas. Genes Dev. 2002, 16, 984–993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dorandish, S.; Williams, A.; Atali, S.; Sendo, S.; Price, D.; Thompson, C.; Guthrie, J.; Heyl, D.; Evans, H.G. Regulation of amyloid-β levels by matrix metalloproteinase-2/9 (MMP2/9) in the media of lung cancer cells. Sci. Rep. 2021, 11, 9708. [Google Scholar] [CrossRef]
- Pavlakis, E.; Stiewe, T. p53′s Extended Reach: The Mutant p53 Secretome. Biomolecules 2020, 10, 307. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Toschi, E.; Rota, R.; Antonini, A.; Melillo, G.; Capogrossi, M.C. Wild-type p53 gene transfer inhibits invasion and reduces matrix metalloproteinase-2 levels in p53-mutated human melanoma cells. J. Investig. Dermatol. 2000, 114, 1188–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, C.-J.; Chen, Y.-L.; Hsieh, C.-H.; Liu, Y.-J.; Yu, S.-L.; Chen, J.J.W.; Wang, C.-C. HOXA5 and p53 cooperate to suppress lung cancer cell invasion and serve as good prognostic factors in non-small cell lung cancer. J. Cancer 2017, 8, 1071–1081. [Google Scholar] [CrossRef] [Green Version]
- Abraham, A.G.; O’Neill, E. PI3K/Akt-mediated regulation of p53 in cancer. Biochem. Soc. Trans. 2014, 42, 798–803. [Google Scholar] [CrossRef]
- Xia, L.; Tan, S.; Zhou, Y.; Lin, J.; Wang, H.; Oyang, L.; Tian, Y.; Liu, L.; Su, M.; Wang, H.; et al. Role of the NFκB-signaling pathway in cancer. Onco Targets Ther. 2018, 11, 2063–2073. [Google Scholar] [CrossRef] [Green Version]
- Xia, Y.; Shen, S.; Verma, I.M. NF-κB, an Active Player in Human Cancers. Cancer Immunol. Res. 2014, 2, 823–830. [Google Scholar] [CrossRef] [Green Version]
- Je, H.S.; Yang, F.; Ji, Y.; Nagappan, G.; Hempstead, B.L.; Lu, B. Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses. Proc. Natl. Acad. Sci. USA 2012, 109, 15924–15929. [Google Scholar] [CrossRef] [Green Version]
- Niculescu, D.; Michaelsen-Preusse, K.; Güner, Ü.; van Dorland, R.; Wierenga, C.J.; Lohmann, C. A BDNF-Mediated Push-Pull Plasticity Mechanism for Synaptic Clustering. Cell Rep. 2018, 24, 2063–2074. [Google Scholar] [CrossRef] [Green Version]
- Majd, S.; Power, J.; Majd, Z. Alzheimer’s Disease and Cancer: When Two Monsters Cannot Be Together. Front. Neurosci. 2019, 13, 155. [Google Scholar] [CrossRef] [Green Version]
- Ganguli, M. Cancer and Dementia: It’s Complicated. Alzheimer Dis. Assoc. Disord. 2015, 29, 177–182. [Google Scholar] [CrossRef] [PubMed]
- Okereke, O.I.; Meadows, M.-E. More Evidence of an Inverse Association between Cancer and Alzheimer Disease. JAMA Netw. Open 2019, 2, e196167. [Google Scholar] [CrossRef] [PubMed]
- Price, D.; Dorandish, S.; Williams, A.; Iwaniec, B.; Stephens, A.; Marshall, K.; Guthrie, J.; Heyl, D.; Evans, H.G. Humanin Blocks the Aggregation of Amyloid-β Induced by Acetylcholinesterase, an Effect Abolished in the Presence of IGFBP-3. Biochemistry 2020, 59, 1981–2002. [Google Scholar] [CrossRef] [PubMed]
- Atali, S.; Dorandish, S.; Devos, J.; Williams, A.; Price, D.; Taylor, J.; Guthrie, J.; Heyl, D.; Evans, H.G. Interaction of amyloid beta with humanin and acetylcholinesterase is modulated by ATP. FEBS Open Bio 2020, 10, 2805–2823. [Google Scholar] [CrossRef] [PubMed]
- Zuccato, C.; Cattaneo, E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 2009, 5, 311–322. [Google Scholar] [CrossRef]
- Meylan, E.; Dooley, A.L.; Feldser, D.M.; Shen, L.; Turk, E.; Ouyang, C.; Jacks, T. Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma. Nature 2009, 462, 104–107. [Google Scholar] [CrossRef] [PubMed]
- Kyriakopoulos, G.; Katopodi, V.; Skeparnias, I.; Kaliatsi, E.G.; Grafanaki, K.; Stathopoulos, C. KRASG12C Can either Promote or Impair Cap-Dependent Translation in Two Different Lung Adenocarcinoma Cell Lines. Int. J. Mol. Sci. 2021, 22, 2222. [Google Scholar] [CrossRef] [PubMed]
- Yoon, Y.-K.; Kim, H.-P.; Han, S.-W.; Oh, D.Y.; Im, S.-A.; Bang, Y.-J.; Kim, T.-Y. KRAS mutant lung cancer cells are differentially responsive to MEK inhibitor due to AKT or STAT3 activation: Implication for combinatorial approach. Mol. Carcinog. 2010, 49, 353–362. [Google Scholar] [CrossRef]
- Xu, G.; Yu, H.; Shi, X.; Sun, L.; Zhou, Q.; Zheng, D.; Shi, H.; Li, N.; Zhang, X.; Shao, G. Cisplatin sensitivity is enhanced in non-small cell lung cancer cells by regulating epithelial-mesenchymal transition through inhibition of eukaryotic translation initiation factor 5A2. BMC Pulm. Med. 2014, 14, 174. [Google Scholar] [CrossRef] [Green Version]
- Prior, I.A.; Lewis, P.D.; Mattos, C. A Comprehensive Survey of Ras Mutations in Cancer. Cancer Res. 2012, 72, 2457–2467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leung, E.L.H.; Luo, L.X.; Liu, Z.Q.; Wong, V.K.W.; Lu, L.; Xie, Y.; Zhang, N.; Qu, Y.; Fan, X.X.; Li, Y.; et al. Inhibition of KRAS-dependent lung cancer cell growth by deltarasin: Blockage of autophagy increases its cytotoxicity. Cell Death Dis. 2018, 9, 216. [Google Scholar] [CrossRef] [PubMed]
- Gao, Q.; Ouyang, W.; Kang, B.; Han, X.; Xiong, Y.; Ding, R.; Li, Y.; Wang, F.; Huang, L.; Chen, L.; et al. Selective targeting of the oncogenic KRAS G12S mutant allele by CRISPR/Cas9 induces efficient tumor regression. Theranostics 2020, 10, 5137–5153. [Google Scholar] [CrossRef] [PubMed]
- Vreka, M.; Lilis, I.; Papageorgopoulou, M.; Giotopoulou, G.A.; Lianou, M.; Giopanou, I.; Kanellakis, N.I.; Spella, M.; Agalioti, T.; Armenis, V.; et al. IκB Kinase α Is Required for Development and Progression of KRAS-Mutant Lung Adenocarcinoma. Cancer Res. 2018, 78, 2939–2951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muterspaugh, R.; Price, D.; Esckilsen, D.; McEachern, S.; Guthrie, J.; Heyl, D.L.; Evans, H.G. Interaction of Insulin-Like Growth Factor-Binding Protein 3 With Hyaluronan and Its Regulation by Humanin and CD44. Biochemistry 2018, 57, 5726–5737. [Google Scholar] [CrossRef]
- Dorandish, S.; Devos, J.; Clegg, B.; Price, D.; Muterspaugh, R.; Guthrie, J.; Heyl, D.L.; Evans, H.G. Biochemical determinants of the IGFBP-3-hyaluronan interaction. FEBS Open Bio 2020, 10, 1668–1684. [Google Scholar] [CrossRef]
- Price, D.; Muterspaugh, R.; Clegg, B.; Williams, A.; Stephens, A.; Guthrie, J.; Heyl, D.; Evans, H.G. IGFBP-3 Blocks Hyaluronan-CD44 Signaling, Leading to Increased Acetylcholinesterase Levels in A549 Cell Media and Apoptosis in a p53-Dependent Manner. Sci. Rep. 2020, 10, 5083–5099. [Google Scholar] [CrossRef] [Green Version]
- Evans, H.G.; Guthrie, J.W.; Jujjavarapu, M.; Hendrickson, N.; Eitel, A.; Park, Y.; Garvey, J.; Newman, R.; Esckilsen, D.; Heyl, D.L. D-Amino Acid Analogues of the Antimicrobial Peptide CDT Exhibit Anti- Cancer Properties in A549, a Human Lung Adenocarcinoma Cell Line. Protein Pept. Lett. 2017, 24, 590–598. [Google Scholar] [CrossRef]
- Njomen, E.; Evans, H.G.; Gedara, S.H.; Heyl, D.L. Humanin Peptide Binds to Insulin-Like Growth Factor-Binding Protein 3 (IGFBP3) and Regulates Its Interaction with Importin-β. Protein Pept. Lett. 2015, 22, 869–876. [Google Scholar] [CrossRef] [PubMed]
- Patel, B.B.; Barrero, C.A.; Braverman, A.; Kim, P.D.; Jones, K.A.; Chen, D.E.; Bowler, R.P.; Merali, S.; Kelsen, S.G.; Yeung, A.T. Assessment of Two Immunodepletion Methods: Off-Target Effects and Variations in Immunodepletion Efficiency May Confound Plasma Proteomics. J. Proteome Res. 2012, 11, 5947–5958. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, X.; Zhang, C.; Chen, Y.; Zhou, T. Upregulation of Acetylcholinesterase Mediated by p53 Contributes to Cisplatin-Induced Apoptosis in Human Breast Cancer Cell. J. Cancer 2015, 6, 48–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Dorandish, S.; Atali, S.; Ray, R.; Al Khashali, H.; Coleman, K.-L.; Guthrie, J.; Heyl, D.; Evans, H.G. Differences in the Relative Abundance of ProBDNF and Mature BDNF in A549 and H1299 Human Lung Cancer Cell Media. Int. J. Mol. Sci. 2021, 22, 7059. https://doi.org/10.3390/ijms22137059
Dorandish S, Atali S, Ray R, Al Khashali H, Coleman K-L, Guthrie J, Heyl D, Evans HG. Differences in the Relative Abundance of ProBDNF and Mature BDNF in A549 and H1299 Human Lung Cancer Cell Media. International Journal of Molecular Sciences. 2021; 22(13):7059. https://doi.org/10.3390/ijms22137059
Chicago/Turabian StyleDorandish, Sadaf, Sarah Atali, Ravel Ray, Hind Al Khashali, Kai-Ling Coleman, Jeffrey Guthrie, Deborah Heyl, and Hedeel Guy Evans. 2021. "Differences in the Relative Abundance of ProBDNF and Mature BDNF in A549 and H1299 Human Lung Cancer Cell Media" International Journal of Molecular Sciences 22, no. 13: 7059. https://doi.org/10.3390/ijms22137059