Cell invasion of highly metastatic MTLn3 cancer cells is dependent on phospholipase D2 (PLD2) and janus kinase 3 (JAK3)

Journal of Molecular Biology

Volumn 408, Issue 5, 2011, Pages 850-862

  Henkels, Karen M ^a   Farkaly, Terry ^a   Mahankali, Madhu ^a   Segall, Jeffrey E ^b   Gomez Cambronero, Julian ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

DMEM; Dulbecco's modified Eagle's medium; EGF; epidermal growth factor; FBS; fetal bovine serum; FITC; fluorescein isothiocyanate; JAK3; Janus kinase 3; PA; phosphatidic acid; phospholipase D; PLD; SEM; SLB; special lysis buffer; standard error of the mean

Indexed keywords

EPIDERMAL GROWTH FACTOR; JANUS KINASE 3; MATRIGEL; PHOSPHOLIPASE D1; PHOSPHOLIPASE D2; STAT PROTEIN; TRIACYLGLYCEROL LIPASE;

ARTICLE; BREAST ADENOCARCINOMA; CANCER CELL; CANCER INVASION; CELL INVASION; CELL STRAIN MCF 7; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN;

BOVINAE;

EID: 79955480000     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.017     Document Type: Article

References (44)

1. Friedl P., and Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms Nat. Rev. Cancer 3 2003 362 374 (Pubitemid 37328856)
2. Sahai E. Mechanisms of cancer cell invasion Curr. Opin. Genet. Dev. 15 2005 87 96 (Pubitemid 40127636)
3. Powner D.J., Pettitt T.R., Anderson R., Nash G.B., and Wakelam M.J. Stable adhesion and migration of human neutrophils requires phospholipase D-mediated activation of the integrin CD11b/CD18 Mol. Immunol. 44 2007 3211 3221 (Pubitemid 46610503)
4. Wang W., Goswami S., Lapidus K., Wells A.L., Wyckoff J.B., and Sahai E. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors Cancer Res. 64 2004 8585 8594 (Pubitemid 39552071)
5. Lehman N., Di Fulvio M., McCray N., Campos I., Tabatabaian F., and Gomez-Cambronero J. Phagocyte cell migration is mediated by phospholipases PLD1 and PLD2 Blood 108 2006 3564 3572
6. Henkels K.M., Short S., Peng H.J., Di Fulvio M., and Gomez-Cambronero J. PLD2 has both enzymatic and cell proliferation-inducing capabilities, that are differentially regulated by phosphorylation and dephosphorylation Biochem. Biophys. Res. Commun. 389 2009 224 228
7. Agullo G., Gamet-Payrastre L., Manenti S., Viala C., Remesy C., Chap H., and Payrastre B. Relationship between flavonoid structure and inhibition of phosphatidylinositol 3-kinase: a comparison with tyrosine kinase and protein kinase C inhibition Biochem. Pharmacol. 53 1997 1649 1657 (Pubitemid 27356094)
8. Lee S.F., and Lin J.K. Inhibitory effects of phytopolyphenols on TPA-induced transformation, PKC activation, and c-jun expression in mouse fibroblast cells Nutr. Cancer 28 1997 177 183 (Pubitemid 27396207)
9. Fitzpatrick S.L., Brightwell J., Wittliff J.L., Barrows G.H., and Schultz G.S. Epidermal growth factor binding by breast tumor biopsies and relationship to estrogen receptor and progestin receptor levels Cancer Res. 44 1984 3448 3453 (Pubitemid 14098597)
10. Lichtner R.B., Kaufmann A.M., Kittmann A., Rohde-Schulz B., Walter J., and Williams L. Ligand mediated activation of ectopic EGF receptor promotes matrix protein adhesion and lung colonization of rat mammary adenocarcinoma cells Oncogene 10 1995 1823 1832
11. Imai Y., Leung C.K., Friesen H.G., and Shiu R.P. Epidermal growth factor receptors and effect of epidermal growth factor on growth of human breast cancer cells in long-term tissue culture Cancer Res. 42 1982 4394 4398 (Pubitemid 13205930)
12. Salomon D.S., Zwiebel J.A., Bano M., Losonczy I., Fehnel P., and Kidwell W.R. Presence of transforming growth factors in human breast cancer cells Cancer Res. 44 1984 4069 4077 (Pubitemid 14041638)
13. Exton J.H. Regulation of phospholipase D FEBS Lett. 531 2002 58 61 (Pubitemid 35232785)
14. Jenkins G.M., and Frohman M.A. Phospholipase D: a lipid centric review Cell. Mol. Life. Sci. 62 2005 2305 2316 (Pubitemid 41500546)
15. Frondorf K., Henkels K.M., Frohman M.A., and Gomez-Cambronero J. Phosphatidic acid (PA) is a leukocyte chemoattractant that acts through S6 kinase signaling J. Biol. Chem. 285 2010 15837 15847
16. Foster D.A., and Xu L. Phospholipase D in cell proliferation and cancer Mol. Cancer Res. 1 2003 789 800 (Pubitemid 37174450)
17. Noh D.Y., Ahn S.J., Lee R.A., Park I.A., Kim J.H., and Suh P.G. Overexpression of phospholipase D1 in human breast cancer tissues Cancer Lett. 161 2000 207 214
18. Su W., Chen Q., and Frohman M.A. Targeting phospholipase D with small-molecule inhibitors as a potential therapeutic approach for cancer metastasis Future Oncol. 5 2009 1477 1486
19. Park S.H., Chun Y.H., Ryu S.H., Suh P.G., and Kim H. Assignment of human PLD1 to human chromosome band 3q26 by fluorescence in situ hybridization Cytogenet. Cell Genet. 82 1998 224 (Pubitemid 29002469)
20. Kuukasjarvi T., Tanner M., Pennanen S., Karhu R., Visakorpi T., and Isola J. Optimizing DOP-PCR for universal amplification of small DNA samples in comparative genomic hybridization Genes. Chromosomes Cancer 18 1997 94 101 (Pubitemid 27068907)
21. Knuutila S., Bjorkqvist A.M., Autio K., Tarkkanen M., Wolf M., and Monni O. DNA copy number amplifications in human neoplasms: review of comparative genomic hybridization studies Am. J. Pathol. 152 1998 1107 1123 (Pubitemid 28221862)
22. Kallioniemi A., Kallioniemi O.P., Sudar D., Rutovitz D., Gray J.W., Waldman F., and Pinkel D. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors Science 258 1992 818 821
23. Courjal F., and Theillet C. Comparative genomic hybridization analysis of breast tumors with predetermined profiles of DNA amplification Cancer Res. 57 1997 4368 4377 (Pubitemid 27413448)
24. Kuukasjarvi T., Karhu R., Tanner M., Kahkonen M., Schaffer A., and Nupponen N. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer Cancer Res. 57 1997 1597 1604 (Pubitemid 27175581)
25. Park S.H., Ryu S.H., Suh P.G., and Kim H. Assignment of human PLD2 to chromosome band 17p13.1 by fluorescence in situ hybridization Cytogenet. Cell Genet. 82 1998 225 (Pubitemid 29002470)
26. Schiff M., Delahaye A., Andrieux J., Sanlaville D., Vincent-Delorme C., and Aboura A. Further delineation of the 17p13.3 microdeletion involving YWHAE but distal to PAFAH1B1: four additional patients Eur. J. Med. Genet. 53 2010 303 308
27. Thompson A.M., Anderson T.J., Condie A., Prosser J., Chetty U., and Carter D.C. p53 allele losses, mutations and expression in breast cancer and their relationship to clinico-pathological parameters Int. J. Cancer 50 1992 528 532
28. Takita K., Sato T., Miyagi M., Watatani M., Akiyama F., and Sakamoto G. Correlation of loss of alleles on the short arms of chromosomes 11 and 17 with metastasis of primary breast cancer to lymph nodes Cancer Res. 52 1992 3914 3917
29. Henkels K.M., Peng H.J., Frondorf K., and Gomez-Cambronero J. A comprehensive model that explains the regulation of phospholipase D2 activity by phosphorylation-dephosphorylation Mol. Cell. Biol. 30 2010 2251 2263
30. Henkels, K. M., Frondorf, K., Gonzalez-Mejia, M. E., Doseff, A. L. & Cambronero, J. G. IL-8-induced neutrophil chemotaxis is mediated by Janus kinase 3 (JAK3). FEBS Lett. 585, 159-166.
31. Li J., Nara H., Rahman M., Juliana F.M., Araki A., and Asao H. Impaired IL-7 signaling may explain a case of atypical JAK3-SCID Cytokine 49 2010 221 228
32. Zheng Y., Rodrik V., Toschi A., Shi M., Hui L., Shen Y., and Foster D.A. Phospholipase D couples survival and migration signals in stress response of human cancer cells J. Biol. Chem. 281 2006 15862 15868 (Pubitemid 43848477)
33. Price J.T., Tiganis T., Agarwal A., Djakiew D., and Thompson E.W. Epidermal growth factor promotes MDA-MB-231 breast cancer cell migration through a phosphatidylinositol 3′-kinase and phospholipase C-dependent mechanism Cancer Res. 59 1999 5475 5478 (Pubitemid 29526460)
34. Diamond M.E., Sun L., Ottaviano A.J., Joseph M.J., and Munshi H.G. Differential growth factor regulation of N-cadherin expression and motility in normal and malignant oral epithelium J. Cell Sci. 121 2008 2197 2207
35. Slack J.K., Catling A.D., Eblen S.T., Weber M.J., and Parsons J.T. c-Raf-mediated inhibition of epidermal growth factor-stimulated cell migration J. Biol. Chem. 274 1999 27177 27184
36. Xue C., Wyckoff J., Liang F., Sidani M., Violini S., and Tsai K.L. Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis Cancer Res. 66 2006 192 197 (Pubitemid 43166025)
37. Gibson S.B. Epidermal growth factor and trail interactions in epithelial-derived cells Vitam. Horm. 67 2004 207 227 (Pubitemid 39753665)
38. Yeo E.J., and Exton J.H. Stimulation of phospholipase D by epidermal growth factor requires protein kinase C activation in Swiss 3T3 cells J. Biol. Chem. 270 1995 3980 3988
39. Hayes T.S., Billington C.J., Robinson K.A., Sampt E.R., Fernandez G.A., and Gomez-Cambronero J. Binding of GM-CSF to adherent neutrophils activates phospholipase D Cell. Signalling 11 1999 195 204 (Pubitemid 29185138)
40. Mazie A.R., Spix J.K., Block E.R., Achebe H.B., and Klarlund J.K. Epithelial cell motility is triggered by activation of the EGF receptor through phosphatidic acid signaling J. Cell Sci. 119 2006 1645 1654 (Pubitemid 43732990)
41. Bourgoin S., Plante E., Gaudry M., Naccache P.H., Borgeat P., and Poubelle P.E. Involvement of a phospholipase D in the mechanism of action of granulocyte-macrophage colony-stimulating factor (GM-CSF): priming of human neutrophils in vitro with GM-CSF is associated with accumulation of phosphatidic acid and diradylglycerol J. Exp. Med. 172 1990 767 777 (Pubitemid 20301223)
42. Kim J.Y., Kwon E.Y., Lee Y.S., Kim W.B., and Ro J.Y. Eupatilin blocks mediator release via tyrosine kinase inhibition in activated guinea pig lung mast cells J. Toxicol. Environ. Health Part A 68 2005 2063 2080
43. Knoepp S.M., Chahal M.S., Xie Y., Zhang Z., Brauner D.J., and Hallman M.A. Effects of active and inactive phospholipase D2 on signal transduction, adhesion, migration, invasion, and metastasis in EL4 lymphoma cells Mol. Pharmacol. 74 2008 574 584
44. Soldevila G., Licona I., Salgado A., Ramirez M., Chavez R., and Garcia-Zepeda E. Impaired chemokine-induced migration during T-cell development in the absence of JAK3 Immunology 112 2004 191 200 (Pubitemid 38703565)