Overexpression of secretory phospholipase A2-IIa supports cancer stem cell phenotype via HER/ERBB-elicited signaling in lung and prostate cancer cells
- Authors:
- Shan Lu
- Zhongyun Dong
-
Affiliations: Department of Medicine, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA - Published online on: April 19, 2017 https://doi.org/10.3892/ijo.2017.3964
- Pages: 2113-2122
This article is mentioned in:
Abstract
O'Flaherty JD, Barr M, Fennell D, Richard D, Reynolds J, O'Leary J and O'Byrne K: The cancer stem-cell hypothesis: Its emerging role in lung cancer biology and its relevance for future therapy. J Thorac Oncol. 7:1880–1890. 2012. View Article : Google Scholar : PubMed/NCBI | |
Leon G, MacDonagh L, Finn SP, Cuffe S and Barr MP: Cancer stem cells in drug resistant lung cancer: Targeting cell surface markers and signaling pathways. Pharmacol Ther. 158:71–90. 2016. View Article : Google Scholar | |
MacDonagh L, Gray SG, Breen E, Cuffe S, Finn SP, O'Byrne KJ and Barr MP: Lung cancer stem cells: The root of resistance. Cancer Lett. 372:147–156. 2016. View Article : Google Scholar : PubMed/NCBI | |
Liu T, Xu F, Du X, Lai D, Liu T, Zhao Y, Huang Q, Jiang L, Huang W, Cheng W, et al: Establishment and characterization of multidrug resistant, prostate carcinoma-initiating stem-like cells from human prostate cancer cell lines 22RV1. Mol Cell Biochem. 340:265–273. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fang DD, Cao J, Jani JP, Tsaparikos K, Blasina A, Kornmann J, Lira ME, Wang J, Jirout Z, Bingham J, et al: Combined gemcitabine and CHK1 inhibitor treatment induces apoptosis resistance in cancer stem cell-like cells enriched with tumor spheroids from a non-small cell lung cancer cell line. Front Med. 7:462–476. 2013. View Article : Google Scholar : PubMed/NCBI | |
Vlashi E and Pajonk F: The metabolic state of cancer stem cells - a valid target for cancer therapy? Free Radic Biol Med. 79:264–268. 2015. View Article : Google Scholar | |
Pfeiffer MJ and Schalken JA: Stem cell characteristics in prostate cancer cell lines. Eur Urol. 57:246–254. 2010. View Article : Google Scholar | |
Lagadec C, Vlashi E, Della Donna L, Dekmezian C and Pajonk F: Radiation-induced reprogramming of breast cancer cells. Stem Cells. 30:833–844. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ghisolfi L, Keates AC, Hu X, Lee DK and Li CJ: Ionizing radiation induces stemness in cancer cells. PLoS One. 7:e436282012. View Article : Google Scholar : PubMed/NCBI | |
Li P, Yang R and Gao WQ: Contributions of epithelial-mesen-chymal transition and cancer stem cells to the development of castration resistance of prostate cancer. Mol Cancer. 13:552014. View Article : Google Scholar | |
Brown MD, Gilmore PE, Hart CA, Samuel JD, Ramani VA, George NJ and Clarke NW: Characterization of benign and malignant prostate epithelial Hoechst 33342 side populations. Prostate. 67:1384–1396. 2007. View Article : Google Scholar : PubMed/NCBI | |
Antonio V, Brouillet A, Janvier B, Monne C, Bereziat G, Andreani M and Raymondjean M: Transcriptional regulation of the rat type IIA phospholipase A2 gene by cAMP and interleukin-1beta in vascular smooth muscle cells: Interplay of the CCAAT/enhancer binding protein (C/EBP), nuclear factor-kappaB and Ets transcription factors. Biochem J. 368:415–424. 2002. View Article : Google Scholar : PubMed/NCBI | |
Dong Z, Liu Y, Scott KF, Levin L, Gaitonde K, Bracken RB, Burke B, Zhai QJ, Wang J, Oleksowicz L, et al: Secretory phospholipase A2-IIa is involved in prostate cancer progression and may potentially serve as a biomarker for prostate cancer. Carcinogenesis. 31:1948–1955. 2010. View Article : Google Scholar : PubMed/NCBI | |
Cummings BS: Phospholipase A2 as targets for anti-cancer drugs. Biochem Pharmacol. 74:949–959. 2007. View Article : Google Scholar : PubMed/NCBI | |
Triggiani M, Granata F, Giannattasio G and Marone G: Secretory phospholipases A2 in inflammatory and allergic diseases: Not just enzymes. J Allergy Clin Immunol. 116:1000–1006. 2005. View Article : Google Scholar : PubMed/NCBI | |
Saegusa J, Akakura N, Wu CY, Hoogland C, Ma Z, Lam KS, Liu FT, Takada YK and Takada Y: Pro-inflammatory secretory phospholipase A2 type IIA binds to integrins alphavbeta3 and alpha4beta1 and induces proliferation of monocytic cells in an integrin-dependent manner. J Biol Chem. 283:26107–26115. 2008. View Article : Google Scholar : PubMed/NCBI | |
Triggiani M, Granata F, Balestrieri B, Petraroli A, Scalia G, Del Vecchio L and Marone G: Secretory phospholipases A2 activate selective functions in human eosinophils. J Immunol. 170:3279–3288. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tada K, Murakami M, Kambe T and Kudo I: Induction of cyclooxygenase-2 by secretory phospholipases A2 in nerve growth factor-stimulated rat serosal mast cells is facilitated by interaction with fibroblasts and mediated by a mechanism independent of their enzymatic functions. J Immunol. 161:5008–5015. 1998.PubMed/NCBI | |
Cupillard L, Mulherkar R, Gomez N, Kadam S, Valentin E, Lazdunski M and Lambeau G: Both group IB and group IIA secreted phospholipases A2 are natural ligands of the mouse 180-kDa M-type receptor. J Biol Chem. 274:7043–7051. 1999. View Article : Google Scholar : PubMed/NCBI | |
Nicolas JP, Lambeau G and Lazdunski M: Identification of the binding domain for secretory phospholipases A2 on their M-type 180-kDa membrane receptor. J Biol Chem. 270:28869–28873. 1995. View Article : Google Scholar : PubMed/NCBI | |
Scott KF, Sajinovic M, Hein J, Nixdorf S, Galettis P, Liauw W, de Souza P, Dong Q, Graham GG and Russell PJ: Emerging roles for phospholipase A2 enzymes in cancer. Biochimie. 92:601–610. 2010. View Article : Google Scholar : PubMed/NCBI | |
Meyer AM, Dwyer-Nield LD, Hurteau GJ, Keith RL, O'Leary E, You M, Bonventre JV, Nemenoff RA and Malkinson AM: Decreased lung tumorigenesis in mice genetically deficient in cytosolic phospholipase A2. Carcinogenesis. 25:1517–1524. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kallajoki M, Alanen KA, Nevalainen M and Nevalainen TJ: Group II phospholipase A2 in human male reproductive organs and genital tumors. Prostate. 35:263–272. 1998. View Article : Google Scholar : PubMed/NCBI | |
Jiang J, Neubauer BL, Graff JR, Chedid M, Thomas JE, Roehm NW, Zhang S, Eckert GJ, Koch MO, Eble JN, et al: Expression of group IIA secretory phospholipase A2 is elevated in prostatic intraepithelial neoplasia and adenocarcinoma. Am J Pathol. 160:667–671. 2002. View Article : Google Scholar : PubMed/NCBI | |
Graff JR, Konicek BW, Deddens JA, Chedid M, Hurst BM, Colligan B, Neubauer BL, Carter HW and Carter JH: Expression of group IIa secretory phospholipase A2 increases with prostate tumor grade. Clin Cancer Res. 7:3857–3861. 2001.PubMed/NCBI | |
Dong Z, Liu Y, Levin L, Oleksowicz L, Wang J and Lu S: Vav3 oncogene is involved in regulation of secretory phospholipase A2-IIa expression in prostate cancer. Oncol Rep. 25:1511–1516. 2011.PubMed/NCBI | |
Sved P, Scott KF, McLeod D, King NJ, Singh J, Tsatralis T, Nikolov B, Boulas J, Nallan L, Gelb MH, et al: Oncogenic action of secreted phospholipase A2 in prostate cancer. Cancer Res. 64:6934–6940. 2004. View Article : Google Scholar : PubMed/NCBI | |
Mirtti T, Laine VJ, Hiekkanen H, Hurme S, Rowe O, Nevalainen TJ, Kallajoki M and Alanen K: Group IIA phospholipase A as a prognostic marker in prostate cancer: Relevance to clinicopathological variables and disease-specific mortality. APMIS. 117:151–161. 2009. View Article : Google Scholar : PubMed/NCBI | |
Oleksowicz L, Liu Y, Bracken RB, Gaitonde K, Burke B, Succop P, Levin L, Dong Z and Lu S: Secretory phospholipase A2-IIa is a target gene of the HER/HER2-elicited pathway and a potential plasma biomarker for poor prognosis of prostate cancer. Prostate. 72:1140–1149. 2012. View Article : Google Scholar : | |
Kupert E, Anderson M, Liu Y, Succop P, Levin L, Wang J, Wikenheiser-brokamp K, Chen P, Pinney SM, Macdonald T, et al: Plasma secretory phospholipase A2-IIa as a potential biomarker for lung cancer in patients with solitary pulmonary nodules. BMC Cancer. 11:5132011. View Article : Google Scholar : PubMed/NCBI | |
Menschikowski M, Hagelgans A, Schuler U, Froeschke S, Rosner A and Siegert G: Plasma levels of phospholipase A2-IIA in patients with different types of malignancies: Prognosis and association with inflammatory and coagulation biomarkers. Pathol Oncol Res. 19:839–846. 2013. View Article : Google Scholar : PubMed/NCBI | |
Dong Z, Meller J, Succop P, Wang J, Wikenheiser-Brokamp K, Starnes S and Lu S: Secretory phospholipase A2-IIa upregulates HER/HER2-elicited signaling in lung cancer cells. Int J Oncol. 45:978–984. 2014.PubMed/NCBI | |
Mimeault M, Hauke R, Mehta PP and Batra SK: Recent advances in cancer stem/progenitor cell research: Therapeutic implications for overcoming resistance to the most aggressive cancers. J Cell Mol Med. 11:981–1011. 2007. View Article : Google Scholar : PubMed/NCBI | |
Schneider MR and Yarden Y: The EGFR-HER2 module: A stem cell approach to understanding a prime target and driver of solid tumors. Oncogene. 35:2949–2960. 2016. View Article : Google Scholar : | |
Singh S, Trevino J, Bora-Singhal N, Coppola D, Haura E, Altiok S and Chellappan SP: EGFR/Src/Akt signaling modulates Sox2 expression and self-renewal of stem-like side-population cells in non-small cell lung cancer. Mol Cancer. 11:732012. View Article : Google Scholar : PubMed/NCBI | |
Lu S, Tsai SY and Tsai MJ: Molecular mechanisms of androgen- independent growth of human prostate cancer LNCaP-AI cells. Endocrinology. 140:5054–5059. 1999. View Article : Google Scholar : PubMed/NCBI | |
Ho MM, Ng AV, Lam S and Hung JY: Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res. 67:4827–4833. 2007. View Article : Google Scholar : PubMed/NCBI | |
Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, Stass SA and Jiang F: ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest. 90:234–244. 2010. View Article : Google Scholar | |
Doherty RE, Haywood-Small SL, Sisley K and Cross NA: Aldehyde dehydrogenase activity selects for the holoclone phenotype in prostate cancer cells. Biochem Biophys Res Commun. 414:801–807. 2011. View Article : Google Scholar : PubMed/NCBI | |
Marcato P, Dean CA, Giacomantonio CA and Lee PW: Aldehyde dehydrogenase: Its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle. 10:1378–1384. 2011. View Article : Google Scholar : PubMed/NCBI | |
Januchowski R, Wojtowicz K and Zabel M: The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomed Pharmacother. 67:669–680. 2013. View Article : Google Scholar : PubMed/NCBI | |
Singh S, Brocker C, Koppaka V, Chen Y, Jackson BC, Matsumoto A, Thompson DC and Vasiliou V: Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radic Biol Med. 56:89–101. 2013. View Article : Google Scholar : | |
Wu A, Luo W, Zhang Q, Yang Z, Zhang G, Li S and Yao K: Aldehyde dehydrogenase 1, a functional marker for identifying cancer stem cells in human nasopharyngeal carcinoma. Cancer Lett. 330:181–189. 2013. View Article : Google Scholar | |
Nishida S, Hirohashi Y, Torigoe T, Kitamura H, Takahashi A, Masumori N, Tsukamoto T and Sato N: Gene expression profiles of prostate cancer stem cells isolated by aldehyde dehydrogenase activity assay. J Urol. 188:294–299. 2012. View Article : Google Scholar : PubMed/NCBI | |
Nishida S, Hirohashi Y, Torigoe T, Inoue R, Kitamura H, Tanaka T, Takahashi A, Asanuma H, Masumori N, Tsukamoto T, et al: Prostate cancer stem-like cells/cancer-initiating cells have an autocrine system of hepatocyte growth factor. Cancer Sci. 104:431–436. 2013. View Article : Google Scholar : PubMed/NCBI | |
Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, Wang H, Liu Z, Su Y, Stass SA, et al: Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res. 7:330–338. 2009. View Article : Google Scholar : PubMed/NCBI | |
Mimeault M and Batra SK: Recent progress on tissue-resident adult stem cell biology and their therapeutic implications. Stem Cell Rev. 4:27–49. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hu R, Dunn TA, Wei S, Isharwal S, Veltri RW, Humphreys E, Han M, Partin AW, Vessella RL, Isaacs WB, et al: Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormone-refractory prostate cancer. Cancer Res. 69:16–22. 2009. View Article : Google Scholar : PubMed/NCBI | |
Dehm SM, Schmidt LJ, Heemers HV, Vessella RL and Tindall DJ: Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res. 68:5469–5477. 2008. View Article : Google Scholar : PubMed/NCBI | |
Munoz M, Henderson M, Haber M and Norris M: Role of the MRP1/ABCC1 multidrug transporter protein in cancer. IUBMB Life. 59:752–757. 2007. View Article : Google Scholar : PubMed/NCBI | |
Modok S, Mellor HR and Callaghan R: Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer. Curr Opin Pharmacol. 6:350–354. 2006. View Article : Google Scholar : PubMed/NCBI | |
Signore M, Ricci-Vitiani L and De Maria R: Targeting apoptosis pathways in cancer stem cells. Cancer Lett. 332:374–382. 2013. View Article : Google Scholar | |
Bennett DT, Deng XS, Yu JA, Bell MT, Mauchley DC, Meng X, Reece TB, Fullerton DA and Weyant MJ: Cancer stem cell phenotype is supported by secretory phospholipase A2 in human lung cancer cells. Ann Thorac Surg. 98:439–445; discussion 445–436. 2014. View Article : Google Scholar : PubMed/NCBI | |
Di Lorenzo G, Tortora G, D'Armiento FP, De Rosa G, Staibano S, Autorino R, D'Armiento M, De Laurentiis M, De Placido S, Catalano G, et al: Expression of epidermal growth factor receptor correlates with disease relapse and progression to androgen-independence in human prostate cancer. Clin Cancer Res. 8:3438–3444. 2002.PubMed/NCBI | |
Shi Y, Brands FH, Chatterjee S, Feng AC, Groshen S, Schewe J, Lieskovsky G and Cote RJ: Her-2/neu expression in prostate cancer: High level of expression associated with exposure to hormone therapy and androgen independent disease. J Urol. 166:1514–1519. 2001. View Article : Google Scholar : PubMed/NCBI | |
Osman I, Scher HI, Drobnjak M, Verbel D, Morris M, Agus D, Ross JS and Cordon-Cardo C: HER-2/neu (p185neu) protein expression in the natural or treated history of prostate cancer. Clin Cancer Res. 7:2643–2647. 2001.PubMed/NCBI | |
Signoretti S, Montironi R, Manola J, Altimari A, Tam C, Bubley G, Balk S, Thomas G, Kaplan I, Hlatky L, et al: Her-2-neu expression and progression toward androgen independence in human prostate cancer. J Natl Cancer Inst. 92:1918–1925. 2000. View Article : Google Scholar : PubMed/NCBI | |
Yeh S, Lin HK, Kang HY, Thin TH, Lin MF and Chang C: From HER2/Neu signal cascade to androgen receptor and its coacti-vators: A novel pathway by induction of androgen target genes through MAP kinase in prostate cancer cells. Proc Natl Acad Sci USA. 96:5458–5463. 1999. View Article : Google Scholar | |
Craft N, Shostak Y, Carey M and Sawyers CL: A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat Med. 5:280–285. 1999. View Article : Google Scholar : PubMed/NCBI | |
Schulze WX, Deng L and Mann M: Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol Syst Biol. 1:2005 00082005. View Article : Google Scholar | |
Hsieh AC and Moasser MM: Targeting HER proteins in cancer therapy and the role of the non-target HER3. Br J Cancer. 97:453–457. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tsao MS, Sakurada A, Cutz JC, Zhu CQ, Kamel-Reid S, Squire J, Lorimer I, Zhang T, Liu N, Daneshmand M, et al: Erlotinib in lung cancer - molecular and clinical predictors of outcome. N Engl J Med. 353:133–144. 2005. View Article : Google Scholar : PubMed/NCBI | |
Patel MI, Singh J, Niknami M, Kurek C, Yao M, Lu S, Maclean F, King NJ, Gelb MH, Scott KF, et al: Cytosolic phospholipase A2-alpha: A potential therapeutic target for prostate cancer. Clin Cancer Res. 14:8070–8079. 2008. View Article : Google Scholar : PubMed/NCBI | |
Belinsky GS, Rajan TV, Saria EA, Giardina C and Rosenberg DW: Expression of secretory phospholipase A2 in colon tumor cells potentiates tumor growth. Mol Carcinog. 46:106–116. 2007. View Article : Google Scholar | |
Hernández M, Martín R, García-Cubillas MD, Maeso- Hernández P and Nieto ML: Secreted PLA2 induces proliferation in astrocytoma through the EGF receptor: Another inflammation-cancer link. Neuro-oncol. 12:1014–1023. 2010. View Article : Google Scholar : PubMed/NCBI | |
Martín R, Hernández M, Ibeas E, Fuentes L, Salicio V, Arnés M and Nieto ML: Secreted phospholipase A2-IIA modulates key regulators of proliferation on astrocytoma cells. J Neurochem. 111:988–999. 2009. View Article : Google Scholar : PubMed/NCBI | |
Valentin E and Lambeau G: Increasing molecular diversity of secreted phospholipases A(2) and their receptors and binding proteins. Biochim Biophys Acta. 1488:59–70. 2000. View Article : Google Scholar : PubMed/NCBI | |
Lambeau G and Lazdunski M: Receptors for a growing family of secreted phospholipases A2. Trends Pharmacol Sci. 20:162–170. 1999. View Article : Google Scholar : PubMed/NCBI | |
Hernández M, Burillo SL, Crespo MS and Nieto ML: Secretory phospholipase A2 activates the cascade of mitogen-activated protein kinases and cytosolic phospholipase A2 in the human astrocytoma cell line 1321N1. J Biol Chem. 273:606–612. 1998. View Article : Google Scholar : PubMed/NCBI | |
Park DW, Kim JR, Kim SY, Sonn JK, Bang OS, Kang SS, Kim JH and Baek SH: Akt as a mediator of secretory phospholipase A2 receptor-involved inducible nitric oxide synthase expression. J Immunol. 170:2093–2099. 2003. View Article : Google Scholar : PubMed/NCBI | |
Ibeas E, Fuentes L, Martín R, Hernández M and Nieto ML: Inflammatory protein sPLA(2)-IIA abrogates TNFalpha-induced apoptosis in human astroglioma cells: Crucial role of ERK. Biochim Biophys Acta. 1793:1837–1847. 2009. View Article : Google Scholar : PubMed/NCBI | |
Morgenbesser SD, McLaren RP, Richards B, Zhang M, Akmaev VR, Winter SF, Mineva ND, Kaplan-Lefko PJ, Foster BA, Cook BP, et al: Identification of genes potentially involved in the acquisition of androgen-independent and metastatic tumor growth in an autochthonous genetically engineered mouse prostate cancer model. Prostate. 67:83–106. 2007. View Article : Google Scholar | |
Yu JA, Mauchley D, Li H, Meng X, Nemenoff RA, Fullerton DA and Weyant MJ: Knockdown of secretory phospholipase A2 IIa reduces lung cancer growth in vitro and in vivo. J Thorac Cardiovasc Surg. 144:1185–1191. 2012. View Article : Google Scholar : PubMed/NCBI | |
Larzabal L, El-Nikhely N, Redrado M, Seeger W, Savai R and Calvo A: Differential effects of drugs targeting cancer stem cell (CSC) and non-CSC populations on lung primary tumors and metastasis. PLoS One. 8:e797982013. View Article : Google Scholar : PubMed/NCBI | |
Lopez-Ayllon BD, Moncho-Amor V, Abarrategi A, Ibañez de Cáceres I, Castro-Carpeño J, Belda-Iniesta C, Perona R and Sastre L: Cancer stem cells and cisplatin-resistant cells isolated from non-small-lung cancer cell lines constitute related cell populations. Cancer Med. 3:1099–1111. 2014. View Article : Google Scholar : PubMed/NCBI |