Iranian
Biomedical Journal
Volume 28, Issue 1 (1-2024)
IBJ 2024, 28(1): 23-30 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Damavandi Z, Riahi P, Majidizadeh T, Houshmand M. Evaluation of t-DARPP Expression Alteration in Association with DDR1 Expression in Non-Small Cell Lung Cancer. IBJ 2024; 28 (1) :23-30
URL: http://ibj.pasteur.ac.ir/article-1-3878-en.html
URL: http://ibj.pasteur.ac.ir/article-1-3878-en.html
Abstract:
Background: Discoidin domain receptor 1 (DDR1) signaling plays a critical role in various cellular functions. Increased DDR1 expression has been shown in different human cancers. t-DARPP is a truncated isoform of DARPP-32, and its upregulation promotes cell survival and migration. Most lung cancer patients have non-small cell lung cancer (NSCLC), and their survival rate is low. Therefore, it is necessary to study new and effective targeted therapies. Increased t-DARPP expression in NSCLC patients is associated with patient survival and can act as a prognostic marker correlated with increasing stages of NSCLC. The current study aimed to evaluate alteration in DDR1 expression and its effects on t-DARPP expression in NSCLC.
Methods: Two human lung adenocarcinoma cell lines, A549 and Calu-3, were treated with collagen type I and transfected with DDR1 siRNA. The relative expression of DDR1 and t-DARPP was evaluated using qRT-PCR.
Results: The results indicated that collagen type I could stimulate DDR1 expression in NSCLC cells. Also, DDR1 upregulation resulted in a significant increase in t-DARPP expression. In contrast, suppression of DDR1 expression significantly decreased t-DARPP expression.
Conclusion: Our findings propose that modification in the expression of DDR1, caused by collagen type I and siRNA, might influence the expression of t-DARPP in NSCLC that is linked to NSCLC progression. Moreover, this alteration could potentially serve as an innovative target for therapeutic intervention.
Methods: Two human lung adenocarcinoma cell lines, A549 and Calu-3, were treated with collagen type I and transfected with DDR1 siRNA. The relative expression of DDR1 and t-DARPP was evaluated using qRT-PCR.
Results: The results indicated that collagen type I could stimulate DDR1 expression in NSCLC cells. Also, DDR1 upregulation resulted in a significant increase in t-DARPP expression. In contrast, suppression of DDR1 expression significantly decreased t-DARPP expression.
Conclusion: Our findings propose that modification in the expression of DDR1, caused by collagen type I and siRNA, might influence the expression of t-DARPP in NSCLC that is linked to NSCLC progression. Moreover, this alteration could potentially serve as an innovative target for therapeutic intervention.
Keywords: Collagen type I, Discoidin domain receptor 1, Non-small cell lung cancer, Phosphoprotein phosphatase-1 regulatory subunit 1B
Type of Study: Full Length/Original Article |
Subject:
Cancer Biology
References
1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021; 71(3):209-49. [DOI:10.3322/caac.21660]
2. Yang IA, Holloway JW, Fong KM. Genetic susceptibility to lung cancer and co-morbidities. J Thorac Dis. 2013; 5(Suppl 5):S454-62.
3. Jing H, Song J, Zheng J. Discoidin domain receptor 1: New star in cancer-targeted therapy and its complex role in breast carcinoma. Oncol Lett. 2018; 15(3):3403-8. [DOI:10.3892/ol.2018.7795]
4. Valiathan RR, Marco M, Leitinger B, Kleer CG, Fridman R. Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 2012; 31(1-2):295-321. [DOI:10.1007/s10555-012-9346-z]
5. Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell. 1997; 1(1):13-23. [DOI:10.1016/S1097-2765(00)80003-9]
6. Carafoli F, Hohenester E. Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim Biophys Acta. 2013; 1834(10):2187-94. [DOI:10.1016/j.bbapap.2012.10.014]
7. Borza CM, Pozzi A. Discoidin domain receptors in disease. Matrix Biol. 2014; 34:185-92. [DOI:10.1016/j.matbio.2013.12.002]
8. Leitinger B. Discoidin domain receptor functions in physiological and pathological conditions. Int Rev Cell Mol Biol. 2014; 310:39-87. [DOI:10.1016/B978-0-12-800180-6.00002-5]
9. Prakoura N, Chatziantoniou C. Periostin and discoidin dmain receptor 1: new biomarkers or targets for therapy of renal disease. Front Med. 2017; 4:52 [DOI:10.3389/fmed.2017.00052]
10. Rammal H, Saby C, Magnien K, Van Gulick L, Garnotel R, Buache E, et al. Discoidin domain receptors: potential actors and targets in cancer. Front Pharmacol. 2016; 7:55. [DOI:10.3389/fphar.2016.00055]
11. Shimada K, Nakamura M, Ishida E, Higuchi T, Yamamoto H, Tsujikawa K, et al. Prostate cancer antigen-1 contributes to cell survival and invasion though discoidin receptor 1 in human prostate cancer. Cancer Sci. 2008; 99(1):39-45. [DOI:10.1111/j.1349-7006.2007.00655.x]
12. Hansen C, Greengard P, Nairn AC, Andersson T, Vogel WF. Phosphorylation of DARPP-32 regulates breast cancer cell migration downstream of the receptor tyrosine kinase DDR1. Exp Cell Res. 2006; 312(20):4011-8. [DOI:10.1016/j.yexcr.2006.09.003]
13. Koo DHH, McFadden C, Huang Y, Abdulhussein R, Friese Hamim M, Vogel WF. Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 2006; 580(1):15-22. [DOI:10.1016/j.febslet.2005.11.035]
14. Svenningsson P, Nishi A, Fisone G, Girault JA, Nairn AC, Greengard P. DARPP-32: an integrator of neurotransmission. Annu Rev Pharmacol Toxicol. 2004; 44:269-96. [DOI:10.1146/annurev.pharmtox.44.101802.121415]
15. Ivar Walaas S, Aswad DW, Greengard P. A dopamine and cyclic AMP regulated phosphoprotein enriched in dopamine innervated brain regions. Nature. 1983; 301(5895):69-71. [DOI:10.1038/301069a0]
16. Kotecha S, Lebot MN, Sukkarn B, Ball G, Moseley PM, Chan SY, et al. Dopamine and cAMP-regulated phosphoprotein 32 kDa (DARPP-32) and survival in breast cancer: a retrospective analysis of protein and mRNA expression. Sci Rep. 2019; 9(1):16987. [DOI:10.1038/s41598-019-53529-z]
17. El-Rifai W, Smith MF, Jr., Li G, Beckler A, Carl VS, Montgomery E, et al. Gastric cancers overexpress DARPP-32 and a novel isoform, t-DARPP. Cancer Res. 2002; 62(14):4061-4.
18. Belkhiri A, Zaika A, Pidkovka N, Knuutila S, Moskaluk C, El-Rifai W. Darpp-32: a novel antiapoptotic gene in upper gastrointestinal carcinomas. Cancer Res. 2005; 65(15):6583-92. [DOI:10.1158/0008-5472.CAN-05-1433]
19. Belkhiri A, Zhu S, Chen Z, Soutto M, El-Rifai W. Resistance to TRAIL is mediated by DARPP-32 in gastric cancer. Clin Cancer Res. 2012; 18(14):3889-900. [DOI:10.1158/1078-0432.CCR-11-3182]
20. Chen Z, Zhu S, Hong J, Soutto M, Peng D, Belkhiri A, et al. Gastric tumour-derived ANGPT2 regulation by DARPP-32 promotes angiogenesis. Gut. 2016; 65(6):925-34. [DOI:10.1136/gutjnl-2014-308416]
21. Gu L, Waliany S, Kane SE. Darpp-32 and its truncated variant t-Darpp have antagonistic effects on breast cancer cell growth and herceptin resistance. Plos one. 2009; 4(7):e6220. [DOI:10.1371/journal.pone.0006220]
22. Vangamudi B, Peng DF, Cai Q, El-Rifai W, Zheng W, Belkhiri A. t-DARPP regulates phosphatidylinositol-3-kinase-dependent cell growth in breast cancer. Mol Cancer. 2010; 9:240. [DOI:10.1186/1476-4598-9-240]
23. Wang MS, Pan Y, Liu N, Guo C, Hong L, Fan D. Overexpression of DARPP-32 in colorectal adeno-carcinoma. Int J Clin Prac. 2005; 59(1):58-61. [DOI:10.1111/j.1742-1241.2004.00305.x]
24. Avanes A, Lenz G, Momand J. Darpp-32 and t-Darpp protein products of PPP1R1B: old dogs with new tricks. Biochem Pharmacol. 2019; 160:71-9. [DOI:10.1016/j.bcp.2018.12.008]
25. Christenson JL, Denny EC, Kane SE. t-Darpp overexpression in HER2-positive breast cancer confers a survival advantage in lapatinib. Oncotarget. 2015; 6(32):33134-45. [DOI:10.18632/oncotarget.5311]
26. Belkhiri A, Dar AA, Zaika A, Kelley M, El-Rifai W. t-Darpp promotes cancer cell survival by up-regulation of Bcl2 through Akt-dependent mechanism. Cancer Res. 2008; 68(2):395-403. [DOI:10.1158/0008-5472.CAN-07-1580]
27. Beckler A, Moskaluk CA, Zaika A, Hampton GM, Powell SM, Frierson Jr HF, et al. Overexpression of the 32-kilodalton dopamine and cyclic adenosine 3',5'-monophosphate-regulated phosphoprotein in common adenocarcinomas. Cancer. 2003; 98(7):1547-51. [DOI:10.1002/cncr.11654]
28. Mehta V, Chander H, Munshi A. Complex roles of discoidin domain receptor tyrosine kinases in cancer. Clin Transl Oncol. 2021; 23(8):1497-510. [DOI:10.1007/s12094-021-02552-6]
29. Alam SK, Astone M, Liu P, Hall SR, Coyle AM, Dankert EN, et al. DARPP-32 and t-DARPP promote non-small cell lung cancer growth through regulation of IKKα-dependent cell migration. Commun Biol. 2018; 1:43. [DOI:10.1038/s42003-018-0050-6]
30. Miao L, Zhu S, Wang Y, Li Y, Ding J, Dai J, et al. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung cancer and promotes cell invasion via epithelial-to-mesenchymal transition. Med Oncol. 2013; 30(3):626. [DOI:10.1007/s12032-013-0626-4]
31. Matada GSP, Das A, Dhiwar PS, Ghara A. DDR1 and DDR2: a review on signaling pathway and small molecule inhibitors as an anticancer agent. Med Chem Res. 2021; 30:535-51. [DOI:10.1007/s00044-020-02694-2]
32. Majo S, Auguste P. The yin and yang of discoidin domain receptors (DDRs): implications in tumor growth and metastasis development. Cancers. 2021; 13(7):1725. [DOI:10.3390/cancers13071725]
33. Ruiz PA, Jarai G. Collagen I induces discoidin domain receptor (DDR) 1 expression through DDR2 and a JAK2-ERK1/2-mediated mechanism in primary human lung fibroblasts. J Biol Chem. 2011; 286(15):12912-23. [DOI:10.1074/jbc.M110.143693]
34. Momand J, Magdziarz P, Feng Y, Jiang D, Parga E, Celis A, et al. t-Darpp is an elongated monomer that binds calcium and is phosphorylated by cyclin-dependent kinases 1 and 5. FEBS Open Bio. 2017; 7(9):1328-37. [DOI:10.1002/2211-5463.12269]
35. Alam SK, Wang L, Ren Y, Hernandez CE, Kosari F, Roden AC, et al. ASCL1-regulated DARPP-32 and t-DARPP stimulate small cell lung cancer growth and neuroendocrine tumour cell proliferation. Br J Cancer. 2020; 123(5):819-32. [DOI:10.1038/s41416-020-0923-6]
36. Belkhiri A, Dar AA, Peng DF, Razvi MH, Rinehart C, Arteaga CL, et al. Expression of t-DARPP mediates trastuzumab resistance in breast cancer cells. Clin Cancer Res. 2008; 14(14):4564-71. [DOI:10.1158/1078-0432.CCR-08-0121]
37. Theile D, Geng S, Denny EC, Momand J, Kane SE. t-Darpp stimulates protein kinase A activity by forming a complex with its RI regulatory subunit. Cell Signal. 2017; 40:53-61. [DOI:10.1016/j.cellsig.2017.08.012]
38. Hansen C, Howlin J, Tengholm A, Dyachok O, Vogel WF, Nairn AC, et al. Wnt-5a-induced phosphorylation of DARPP-32 inhibits breast cancer cell migration in a CREB-dependent manner. J Biol Chem. 2009; 284 (40):27533-43. [DOI:10.1074/jbc.M109.048884]
39. Zhu S, Soutto M, Chen Z, Peng D, Romero-Gallo J, Krishna US, et al. Helicobacter pylori-induced cell death is counteracted by NF-κB-mediated transcription of DARPP-32. Gut. 2017; 66(5):761-2. [DOI:10.1136/gutjnl-2016-312141]
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
IBJ is a member of Committee on Publication Ethics (COPE)
and follows its guidelines |
The articles of this journal are licensed under
a Creative Commons Attribution-NonDerivatives 4.0 International License. .png) |
 IBJ is owned and published by Pasteur Institute of Iran |