Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1021-335X Online ISSN: 1791-2431
Journal Cover
October-2019 Volume 42 Issue 4

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
October-2019 Volume 42 Issue 4

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article

Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells

  • Authors:
    • Sahib Zada
    • Jin Seok Hwang
    • Mahmoud Ahmed
    • Trang Huyen Lai
    • Trang Minh Pham
    • Dong‑Hee Kim
    • Deok Ryong Kim
  • View Affiliations / Copyright

    Affiliations: Department of Biochemistry and Convergence Medical Sciences, Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, South Gyeongsang 527‑27, Republic of Korea, Orthopaedic Surgery, Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, South Gyeongsang 527‑27, Republic of Korea
  • Pages: 1621-1630
    |
    Published online on: July 19, 2019
       https://doi.org/10.3892/or.2019.7243
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

One million females are diagnosed worldwide every year with breast cancer, and the mortality rate of these patients remains high. Several treatments, including surgery, are available for breast cancer. β‑Lapachone (β‑Lap), a natural quinone compound, has been developed for cancer treatment due to its strong cytotoxic effect through its action on NAD(P)H:quinone oxidoreductase 1 (NQO1)‑dependent activity. However, the mechanism in regards to how β‑Lap induces cytotoxicity in breast cancer cells is still elusive. In the present study, we showed that β‑Lap induced apoptotic cell death via activation of protein kinase A (PKA) in NQO1‑overexpressing MDA‑MB‑231 human breast cancer cells. This PKA‑dependent cell death was observed solely in NQO1‑overexpressing 231 cells via the high production of reactive oxygen species (ROS). Cell survival of antioxidant [N‑acetylcysteine (NAC)]‑treated NQO1‑overexpressing 231 cells was significantly recovered, and NQO1‑negative 231 cells did not respond to β‑Lap. Antiapoptotic proteins such as Bcl2 and Bcl‑xL were decreased, while proapoptotic proteins, including cytochrome c, activation of caspase‑3, and cleavage of PARP were increased after β‑Lap treatment of NQO1‑overexpressing 231 cells. Furthermore, PKA activators, forskolin or dibutyryl‑cAMP, an analog of cAMP, aggravated the β‑Lap‑induced apoptotic cell death by decreasing antiapoptotic proteins and further activating proapoptotic proteins in NQO1‑positive 231 cells. Treatment with a PKA inhibiter, H89, significantly increased cell viability even in NQO1‑overexpressing cells treated with β‑Lap. These data showed that β‑Lap activated PKA via ROS accumulation, subsequently leading to apoptotic cell death in NQO1‑positive breast cancer cells.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

View References

1 

Semenza GL: Molecular mechanisms mediating metastasis of hypoxic breast cancer cells. Trends Mol Med. 18:534–543. 2012. View Article : Google Scholar : PubMed/NCBI

2 

Valastyan S and Weinberg RA: Tumor metastasis: Molecular insights and evolving paradigms. Cell. 147:275–292. 2011. View Article : Google Scholar : PubMed/NCBI

3 

Lambert AW, Pattabiraman DR and Weinberg RA: Emerging biological principles of metastasis. Cell. 168:670–691. 2017. View Article : Google Scholar : PubMed/NCBI

4 

Lerebours F and Lidereau R: Molecular alterations in sporadic breast cancer. Crit Rev Oncol Hematol. 44:121–141. 2002. View Article : Google Scholar : PubMed/NCBI

5 

Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Li CI, Beaber EF, Tang MC, Porter PL, Daling JR and Malone KE: Reproductive factors and risk of estrogen receptor positive, triple-negative, and HER2-neu overexpressing breast cancer among women 20–44 years of age. Breast Cancer Res Treat. 137:579–587. 2013. View Article : Google Scholar : PubMed/NCBI

7 

Coughlin SS and Ekwueme DU: Breast cancer as a global health concern. Cancer Epidemiol. 33:315–318. 2009. View Article : Google Scholar : PubMed/NCBI

8 

Tangjitgamol S, Anderson BO, See HT, Lertbutsayanukul C, Sirisabya N, Manchana T, Ilancheran A, Lee KM, Lim SE, Chia YN, et al: Management of endometrial cancer in Asia: Consensus statement from the Asian Oncology Summit 2009. Lancet Oncol. 10:1119–1127. 2009. View Article : Google Scholar : PubMed/NCBI

9 

Mark HF, Aswad B, Bassily N, Taylor W, Brown S, Sun CL, Samy M, Zolnierz K, Wong E, Bland KI and Hsu PH: HER-2/neu gene amplification in stages I–IV breast cancer detected by fluorescent in situ hybridization. Genet Med. 1:98–103. 1999. View Article : Google Scholar : PubMed/NCBI

10 

Thompson CB: Apoptosis in the pathogenesis and treatment of disease. Science. 267:1456–1462. 1995. View Article : Google Scholar : PubMed/NCBI

11 

Fulda S: Apoptosis pathways and their therapeutic exploitation in pancreatic cancer. J Cell Mol Med. 13:1221–1227. 2009. View Article : Google Scholar : PubMed/NCBI

12 

Varfolomeev E and Vucic D: Inhibitor of apoptosis proteins: Fascinating biology leads to attractive tumor therapeutic targets. Future Oncol. 7:633–648. 2011. View Article : Google Scholar : PubMed/NCBI

13 

Taskén K and Aandahl EM: Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev. 84:137–167. 2004. View Article : Google Scholar : PubMed/NCBI

14 

Fimia GM and Sassone-Corsi P: Cyclic AMP signalling. J Cell Sci. 114:1971–1972. 2001.PubMed/NCBI

15 

Cross TG, Scheel-Toellner D, Henriquez NV, Deacon E, Salmon M and Lord JM: Serine/threonine protein kinases and apoptosis. Exp Cell Res. 256:34–41. 2000. View Article : Google Scholar : PubMed/NCBI

16 

Lerner A, Kim DH and Lee R: The cAMP signaling pathway as a therapeutic target in lymphoid malignancies. Leuk Lymphoma. 37:39–51. 2000. View Article : Google Scholar : PubMed/NCBI

17 

Insel PA, Bourne HR, Coffino P and Tomkins GM: Cyclic AMP-dependent protein kinase: Pivotal role in regulation of enzyme induction and growth. Science. 190:896–898. 1975. View Article : Google Scholar : PubMed/NCBI

18 

Hedrick ED, Agarwal E, Leiphrakpam PD, Haferbier KL, Brattain MG and Chowdhury S: Differential PKA activation and AKAP association determines cell fate in cancer cells. J Mol Signal. 8:102013. View Article : Google Scholar : PubMed/NCBI

19 

Almeida MQ and Stratakis CA: How does cAMP/protein kinase A signaling lead to tumors in the adrenal cortex and other tissues? Mol Cell Endocrinol. 336:162–168. 2011. View Article : Google Scholar : PubMed/NCBI

20 

Chowdhury S, Howell GM, Rajput A, Teggart CA, Brattain LE, Weber HR, Chowdhury A and Brattain MG: Identification of a novel TGFβ/PKA signaling transduceome in mediating control of cell survival and metastasis in colon cancer. PLoS One. 6:e193352011. View Article : Google Scholar : PubMed/NCBI

21 

Zambon AC, Zhang L, Minovitsky S, Kanter JR, Prabhakar S, Salomonis N, Vranizan K, Dubchak I, Conklin BR and Insel PA: Gene expression patterns define key transcriptional events in cell-cycle regulation by cAMP and protein kinase A. Proc Natl Acad Sci USA. 102:8561–8566. 2005. View Article : Google Scholar : PubMed/NCBI

22 

Zhang L, Zambon AC, Vranizan K, Pothula K, Conklin BR and Insel PA: Gene expression signatures of cAMP/Protein Kinase A (PKA)-promoted, Mitochondrial-dependent Apoptosis: Comparative analysis of wild-type and camp-deathless s49 lymphoma cells. J Biol Chem. 283:4304–4313. 2008. View Article : Google Scholar : PubMed/NCBI

23 

Coffino P, Bourne HR and Tomkins GM: Mechanism of lymphoma cell death induced by cyclic AMP. Am J Pathol. 81:199–204. 1975.PubMed/NCBI

24 

Yan L, Herrmann V, Hofer JK and Insel PA: beta-Adrenergic receptor/cAMP-mediated signaling and apoptosis of S49 lymphoma cells. Am J Physiol Cell Physio. 279:C1665–C1674. 2000. View Article : Google Scholar

25 

Zhang L and Insel PA: The pro-apoptotic protein Bim is a convergence point for cAMP/protein kinase A-and glucocorticoid-promoted apoptosis of lymphoid cells. J Biol Chem. 279:20858–20865. 2004. View Article : Google Scholar : PubMed/NCBI

26 

Naviglio S, Di Gesto D, Romano M, Sorrentino A, Illiano F, Sorvillo L, Abbruzzese A, Marra M, Caraglia M, Chiosi E, et al: Leptin enhances growth inhibition by cAMP elevating agents through apoptosis of MDA-MB-231 breast cancer cells. Cancer Biol Ther. 8:1183–1190. 2009. View Article : Google Scholar : PubMed/NCBI

27 

Ugland H, Boquest AC, Naderi S, Collas P and Blomhoff HK: cAMP-mediated induction of cyclin E sensitizes growth-arrested adipose stem cells to DNA damage-induced apoptosis. Mol Biol Cell. 19:5082–5092. 2008. View Article : Google Scholar : PubMed/NCBI

28 

Blanco E, Bey EA, Khemtong C, Yang SG, Setti-Guthi J, Chen H, Kessinger CW, Carnevale KA, Bornmann WG, Boothman DA and Gao J: Beta-lapachone micellar nanotherapeutics for non-small cell lung cancer therapy. Cancer Res. 70:3896–3904. 2010. View Article : Google Scholar : PubMed/NCBI

29 

Li CJ, Li YZ, Pinto AV and Pardee AB: Potent inhibition of tumor survival in vivo by beta-lapachone plus taxol: Combining drugs imposes different artificial checkpoints. Proc Natl Acad Sci USA. 96:13369–13374. 1999. View Article : Google Scholar : PubMed/NCBI

30 

Dong Y, Chin SF, Blanco E, Bey EA, Kabbani W, Xie XJ, Bornmann WG, Boothman DA and Gao J: Intratumoral delivery of beta-lapachone via polymer implants for prostate cancer therapy. Clin cancer Res. 15:131–139. 2009. View Article : Google Scholar : PubMed/NCBI

31 

Pardee AB, Li YZ and Li CJ: Cancer therapy with beta-lapachone. Curr Cancer Drug Targets. 2:2002.227–242. View Article : Google Scholar : PubMed/NCBI

32 

Reinicke KE, Bey EA, Bentle MS, Pink JJ, Ingalls ST, Hoppel CL, Misico RI, Arzac GM, Burton G, Bornmann WG, et al: Development of beta-lapachone prodrugs for therapy against human cancer cells with elevated NAD(P)H:Quinone oxidoreductase 1 levels. Clin Cancer Res. 11:3055–3064. 2005. View Article : Google Scholar : PubMed/NCBI

33 

Trachootham D, Alexandre J and Huang P: Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat Rev Drug Discov. 8:579–591. 2009. View Article : Google Scholar : PubMed/NCBI

34 

Pink JJ, Planchon SM, Tagliarino C, Varnes ME, Siegel D and Boothman DA: NAD(P)H:Quinone oxidoreductase activity is the principal determinant of beta-lapachone cytotoxicity. J Biol Chem. 275:5416–5424. 2000. View Article : Google Scholar : PubMed/NCBI

35 

Siegel D, Yan C and Ross D: NAD(P)H:Quinone oxidoreductase 1 (NQO1) in the sensitivity and resistance to antitumor quinones. Biochem Pharmacol. 83:1033–1040. 2012. View Article : Google Scholar : PubMed/NCBI

36 

Park EJ, Choi KS and Kwon TK: β-Lapachone-induced reactive oxygen species (ROS) generation mediates autophagic cell death in glioma U87 MG cells. Chem Biol Interact. 189:37–44. 2011. View Article : Google Scholar : PubMed/NCBI

37 

Choi EK, Terai K, Ji IM, Kook YH, Park KH, Oh ET, Griffin RJ, Lim BU, Kim JS, Lee DS, et al: Upregulation of NAD(P)H:Quinone oxidoreductase by radiation potentiates the effect of bioreductive beta-lapachone on cancer cells. Neoplasia. 9:634–642. 2007. View Article : Google Scholar : PubMed/NCBI

38 

Garate M, Wani AA and Li G: The NAD(P)H:Quinone oxidoreductase 1 induces cell cycle progression and proliferation of melanoma cells. Free Radic Biol Med. 48:1601–1609. 2010. View Article : Google Scholar : PubMed/NCBI

39 

Yang Y, Zhang Y, Wu Q, Cui X, Lin Z, Liu S and Chen L: Clinical implications of high NQO1 expression in breast cancers. J Exp Clin Cancer Res. 33:142014. View Article : Google Scholar : PubMed/NCBI

40 

Lewis AM, Ough M, Hinkhouse MM, Tsao MS, Oberley LW and Cullen JJ: Targeting NAD(P)H:quinone oxidoreductase (NQO1) in pancreatic cancer. Mol Carcinog. 43:215–224. 2005. View Article : Google Scholar : PubMed/NCBI

41 

Lyn-Cook BD, Yan-Sanders Y, Moore S, Taylor S, Word B and Hammons GJ: Increased levels of NAD(P)H:Quinone oxidoreductase 1 (NQO1) in pancreatic tissues from smokers and pancreatic adenocarcinomas: A potential biomarker of early damage in the pancreas. Cell Biol Toxicol. 22:73–80. 2006. View Article : Google Scholar : PubMed/NCBI

42 

Li JZ, Ke Y, Misra HP, Trush MA, Li YR, Zhu H and Jia Z: Mechanistic studies of cancer cell mitochondria- and NQO1-mediated redox activation of beta-lapachone, a potentially novel anticancer agent. Toxicol Appl Pharmacol. 281:285–293. 2014. View Article : Google Scholar : PubMed/NCBI

43 

Cao L, Li LS, Spruell C, Xiao L, Chakraberti G, Bey EA, Reinicke KE, Srougi MC, Moore Z, Dong Y, et al: Tumor-selective, futile redox cycle-induced bystander effects elicited by NQO1 bioactivatable radiosensitizing drugs in triple-negative breast cancers. Antioxid Redox Signal. 21:237–250. 2014. View Article : Google Scholar : PubMed/NCBI

44 

Liu Y, Yang F, Li S, Dai J and Deng H: Glutaredoxin deletion shortens chronological life span in saccharomyces cerevisiae via ROS-Mediated Ras/PKA activation. J Proteome Res. 17:2318–2327. 2018. View Article : Google Scholar : PubMed/NCBI

45 

Li Z, Ji G and Neugebauer V: Mitochondrial reactive oxygen species are activated by mGluR5 through IP3 and activate ERK and PKA to increase excitability of amygdala neurons and pain behavior. J Neurosci. 31:1114–1127. 2011. View Article : Google Scholar : PubMed/NCBI

46 

Bovo E, Lipsius SL and Zima AV: Reactive oxygen species contribute to the development of arrhythmogenic Ca2+ waves during β-adrenergic receptor stimulation in rabbit cardiomyocytes. J Physiol. 590:3291–3304. 2012. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Zada S, Hwang JS, Ahmed M, Lai TH, Pham TM, Kim DH and Kim DR: Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells. Oncol Rep 42: 1621-1630, 2019.
APA
Zada, S., Hwang, J.S., Ahmed, M., Lai, T.H., Pham, T.M., Kim, D., & Kim, D.R. (2019). Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells. Oncology Reports, 42, 1621-1630. https://doi.org/10.3892/or.2019.7243
MLA
Zada, S., Hwang, J. S., Ahmed, M., Lai, T. H., Pham, T. M., Kim, D., Kim, D. R."Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells". Oncology Reports 42.4 (2019): 1621-1630.
Chicago
Zada, S., Hwang, J. S., Ahmed, M., Lai, T. H., Pham, T. M., Kim, D., Kim, D. R."Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells". Oncology Reports 42, no. 4 (2019): 1621-1630. https://doi.org/10.3892/or.2019.7243
Copy and paste a formatted citation
x
Spandidos Publications style
Zada S, Hwang JS, Ahmed M, Lai TH, Pham TM, Kim DH and Kim DR: Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells. Oncol Rep 42: 1621-1630, 2019.
APA
Zada, S., Hwang, J.S., Ahmed, M., Lai, T.H., Pham, T.M., Kim, D., & Kim, D.R. (2019). Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells. Oncology Reports, 42, 1621-1630. https://doi.org/10.3892/or.2019.7243
MLA
Zada, S., Hwang, J. S., Ahmed, M., Lai, T. H., Pham, T. M., Kim, D., Kim, D. R."Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells". Oncology Reports 42.4 (2019): 1621-1630.
Chicago
Zada, S., Hwang, J. S., Ahmed, M., Lai, T. H., Pham, T. M., Kim, D., Kim, D. R."Protein kinase A activation by β‑Lapachone is associated with apoptotic cell death in NQO1‑overexpressing breast cancer cells". Oncology Reports 42, no. 4 (2019): 1621-1630. https://doi.org/10.3892/or.2019.7243
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team