Lysophosphatidic acid prevents apoptosis of Caco-2 colon cancer cells via activation of mitogen-activated protein kinase and phosphorylation of Bad

Biochimica et Biophysica Acta - General Subjects

Volumn 1770, Issue 8, 2007, Pages 1194-1203

  Rusovici, Raluca ^a   Ghaleb, Amr ^a   Shim, Hyunsuk ^a   Yang, Vincent W ^a   Yun, C Chris ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Lysophosphatidic acids; MAPK; Receptor

Indexed keywords

ANTIINFECTIVE AGENT; CASPASE; ETOPOSIDE; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BCL 2; SCAFFOLD PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL PROTECTION; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ANNEXIN A5; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; CACO-2 CELLS; CASPASE 3; CASPASE 7; COLONIC NEOPLASMS; ENZYME ACTIVATION; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOPHOSPHOLIPIDS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION;

EID: 34347240776     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2007.04.008     Document Type: Article

References (69)

1. Bronner M.P., Culin C., Reed J.C., and Furth E.E. The bcl-2 proto-oncogene and the gastrointestinal epithelial tumor progression model. Am. J. Pathol. 146 (1995) 20-26
2. Trisciuoglio D., Desideri M., Ciuffreda L., Mottolese M., Ribatti D., Vacca A., Del Rosso M., Marcocci L., Zupi G., and Del Bufalo D. Bcl-2 overexpression in melanoma cells increases tumor progression-associated properties and in vivo tumor growth. J. Cell. Physiol. 205 (2005) 414-421
3. Yamada T., Sato K., Komachi M., Malchinkhuu E., Tobo M., Kimura T., Kuwabara A., Yanagita Y., Ikeya T., Tanahashi Y., Ogawa T., Ohwada S., Morishita Y., Ohta H., Im D.-S., Tamoto K., Tomura H., and Okajima F. Lysophosphatidic acid (LPA) in malignant ascites stimulates motility of human pancreatic cancer cells through LPA1. J. Biol. Chem. 279 (2004) 6595-6605
4. Sano T., Baker D., Virag T., Wada A., Yatomi Y., Kobayashi T., Igarashi Y., and Tigyi G. Multiple mechanisms linked to platelet activation result in lysophosphatidic acid and sphingosine 1-phosphate generation in blood. J. Biol. Chem. 277 (2002) 21197-21206
5. Mills G.B., May C., Hill M., Campbell S., Shaw P., and Marks A. Ascitic fluid from human ovarian cancer patients contains growth factors necessary for intraperitoneal growth of human ovarian adenocarcinoma cells. J. Clin. Invest. 86 (1990) 851-855
6. Tigyi G., and Parrill A.L. Molecular mechanisms of lysophosphatidic acid action. Prog. Lipid Res. 42 (2003) 498-526
7. Ye X., Ishii I., Kingsbury M.A., and Chun J. Lysophosphatidic acid as a novel cell survival/apoptotic factor. Biochim. Biophys. Acta 1585 (2002) 108-113
8. Goetzl E.J., and An S. Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 12 (1998) 1589-1598
9. An S., Dickens M.A., Bleu T., Hallmark O.G., and Goetzl E.J. Molecular cloning of the human Edg2 protein and its identification as a functional cellular receptor for lysophosphatidic acid. Biochem. Biophys. Res. Commun. 231 (1997) 619-622
10. An S., Bleu T., Hallmark O.G., and Goetzl E.J. Characterization of a novel subtype of human G protein-coupled receptor for lysophosphatidic acid. J. Biol. Chem. 273 (1998) 7906-7910
11. Aoki J., Bandoh K., and Inoue K. A novel human G-protein-coupled receptor, EDG7, for lysophosphatidic acid with unsaturated fatty-acid moiety. Ann. N. Y. Acad. Sci. 905 (2000) 263-266
12. Noguchi K., Ishii S., and Shimizu T. Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J. Biol. Chem. 278 (2003) 25600-25606
13. Fang X., Yu S., LaPushin R., Lu Y., Furui T., Penn L.Z., Stokoe D., Erickson J.R., Bast Jr. R.C., and Mills G.B. Lysophosphatidic acid prevents apoptosis in fibroblasts via G(i)-protein-mediated activation of mitogen-activated protein kinase. Biochem. J. 352 (2000) 135-143
14. Hu X., Haney N., Kropp D., Kabore A.F., Johnston J.B., and Gibson S.B. Lysophosphatidic acid (LPA) protects primary chronic lymphocytic leukemia cells from apoptosis through LPA receptor activation of the anti-apoptotic protein AKT/PKB. J. Biol. Chem. 280 (2005) 9498-9508
15. Furui T., LaPushin R., Mao M., Khan H., Watt S.R., Watt M.A., Lu Y., Fang X., Tsutsui S., Siddik Z.H., Bast R.C., and Mills G.B. Overexpression of edg-2/vzg-1 induces apoptosis and anoikis in ovarian cancer cells in a lysophosphatidic acid-independent manner. Clin. Cancer Res. 5 (1999) 4308-4318
16. Deng W., Balazs L., Wang D.A., Van Middlesworth L., Tigyi G., and Johnson L.R. Lysophosphatidic acid protects and rescues intestinal epithelial cells from radiation- and chemotherapy-induced apoptosis. Gastroenterology 123 (2002) 206-216
17. Xu Y., Shen Z., Wiper D.W., Wu M., Morton R.E., Elson P., Kennedy A.W., Belinson J., Markman M., and Casey G. Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. JAMA 280 (1998) 719-723
18. Fang X., Schummer M., Mao M., Yu S., Tabassam F.H., Swaby R., Hasegawa Y., Tanyi J.L., LaPushin R., Eder A., Jaffe R., Erickson J., and Mills G.B. Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim. Biophys. Acta 1582 (2002) 257-264
19. Schulte K.M., Beyer A., Kohrer K., Oberhauser S., and Roher H.D. Lysophosphatidic acid, a novel lipid growth factor for human thyroid cells: over-expression of the high-affinity receptor edg4 in differentiated thyroid cancer. Int. J. Cancer 92 (2001) 249-256
20. Shida D., Watanabe T., Aoki J., Hama K., Kitayama J., Sonoda H., Kishi Y., Yamaguchi H., Sasaki S., Sako A., Konishi T., Arai H., and Nagawa H. Aberrant expression of lysophosphatidic acid (LPA) receptors in human colorectal cancer. Lab. Invest. 84 (2004) 1352-1362
21. Yun C.C., Sun H., Wang D., Rusovici R., Castleberry A., Hall R.A., and Shim H. LPA2 receptor mediates mitogenic signals in human colon cancer cells. Am. J. Physiol., Cell Physiol. 289 (2005) C2-C11
22. Xu J., Lai Y.-J., Lin W.-C., and Lin F.-T. TRIP6 enhances lysophosphatidic acid-induced cell migration by interacting with the lysophosphatidic acid 2 receptor. J. Biol. Chem. 279 (2004) 10459-10468
23. Oh Y.S., Jo N.W., Choi J.W., Kim H.S., Seo S.W., Kang K.O., Hwang J.I., Heo K., Kim S.H., Kim Y.H., Kim I.H., Kim J.H., Banno Y., Ryu S.H., and Suh P.G. NHERF2 specifically interacts with LPA2 receptor and defines the specificity and efficiency of receptor-mediated phospholipase C-β3 activation. Mol. Cell. Biol. 24 (2004) 5069-5079
24. Yamada T., Ohoka Y., Kogo M., and Inagaki S. Physical and functional interactions of the lysophosphatidic acid receptors with PDZ domain-containing rho guanine nucleotide exchange factors (RhoGEFs). J. Biol. Chem. 280 (2005) 19358-19363
25. Wang Q., Liu M., Kozasa T., Rothstein J.D., Sternweis P.C., and Neubig R.R. Thrombin and lysophosphatidic acid receptors utilize distinct rhoGEFs in prostate cancer cells. J. Biol. Chem. 279 (2004) 28831-28834
26. Hande K.R. Clinical applications of anticancer drugs targeted to topoisomerase II. Biochim. Biophys. Acta 1400 (1998) 173-184
27. Dufour G., Demers M.-J., Gagne D., Dydensborg A.B., Teller I.C., Bouchard V., Degongre I., Beaulieu J.-F., Cheng J.Q., Fujita N., Tsuruo T., Vallee K., and Vachon P.H. Human intestinal epithelial cell survival and anoikis. J. Biol. Chem. 279 (2004) 44113-44122
28. Gauthier R., Harnois C., Drolet J.-F., Reed J.C., Vezina A., and Vachon P.H. Human intestinal epithelial cell survival: differentiation state-specific control mechanisms. Am. J. Physiol., Cell Physiol. 280 (2001) C1540-C1554
29. Yun C.C., Oh S., Zizak M., Steplock D., Tsao S., Tse C.M., Weinman E.J., and Donowitz M. cAMP-mediated inhibition of the epithelial brush border Na/H exchanger, NHE3, requires an associated regulatory protein. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 3010-3015
30. Lee-Kwon W., Kim J.H., Choi J.W., Kawano K., Cha B., Dartt D.A., Zoukhri D., and Donowitz M. Ca2+-dependent inhibition of NHE3 requires PKC alpha which binds to E3KARP to decrease surface NHE3 containing plasma membrane complexes. Am. J. Physiol., Cell Physiol. 285 (2003) C1527-C1536
31. Fam S.R., Paquet M., Castleberry A.M., Oller H., Lee C.J., Traynelis S.F., Smith Y., Yun C.C., and Hall R.A. P2Y1 receptor signaling is controlled by interaction with the PDZ scaffold NHERF-2. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8042-8047
32. Hirose Y., Berger M.S., and Pieper R.O. p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res. 61 (2001) 1957-1963
33. Strasser A., O'Connor L., and Dixit V.M. Apoptotic signaling. Ann. Rev. Biochem. 69 (2000) 217-245
34. Villa P., Kaufmann S.H., and Earnshaw W.C. Caspases and caspase inhibitors. Trends Biochem. Sci. 22 (1997) 388-393
35. Cory S., Huang D.C., and Adams J.M. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22 (2003) 8590-8607
36. Yang E., Zha J., Jockel J., Boise L.H., Thompson C.B., and Korsmeyer S.J. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80 (1995) 285-291
37. Zha J., Harada H., Yang E., Jockel J., and Korsmeyer S.J. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87 (1996) 619-628
38. del Peso L., Gonzalez-Garcia M., Page C., Herrera R., and Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278 (1997) 687-689
39. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
40. Downward J. How BAD phosphorylation is good for survival. Nat. Cell Biol. 1 (1999) E33-E35
41. Valks D.M., Cook S.A., Pham F.H., Morrison P.R., Clerk A., and Sugden P.H. Phenylephrine promotes phosphorylation of bad in cardiac myocytes through the extracellular signal-regulated kinases 1/2 and protein kinase A. J. Mol. Cell. Cardiol. 34 (2002) 749-763
42. Kaufmann S.H., and Hengartner M.O. Programmed cell death: alive and well in the new millennium. Trends Cell Biol. 11 (2001) 526-534
43. Xu Y., Fang X.J., Casey G., and Mills G.B. Lysophospholipids activate ovarian and breast cancer cells. Biochem. J. 309 (1995) 933-940
44. Ding Q., Wang Q., and Evers B.M. Alterations of MAPK activities associated with intestinal cell differentiation. Biochem. Biophys. Res. Commun. 284 (2001) 282-288
45. Cross T.G., Scheel-Toellner D., Henriquez N.V., Deacon E., Salmon M., and Lord J.M. Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256 (2000) 34-41
46. Xia Z., Dickens M., Raingeaud J., Davis R.J., and Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270 (1995) 1326-1331
47. Ishikawa Y., Kusaka E., Enokido Y., Ikeuchi T., and Hatanaka H. Regulation of Bax translocation through phosphorylation at Ser-70 of Bcl-2 by MAP kinase in NO-induced neuronal apoptosis. Mol. Cell. Neurosci. 24 (2003) 451-459
48. Luschen S., Falk M., Scherer G., Ussat S., Paulsen M., and Adam-Klages S. The Fas-associated death domain protein/caspase-8/c-FLIP signaling pathway is involved in TNF-induced activation of ERK. Exp. Cell Res. 310 (2005) 33-42
49. Chen J.-R., Plotkin L.I., Aguirre J.I., Han L., Jilka R.L., Kousteni S., Bellido T., and Manolagas S.C. Transient versus sustained phosphorylation and nuclear accumulation of ERKs underlie anti-versus pro-apoptotic effects of estrogens. J. Biol. Chem. 280 (2005) 4632-4638
50. He Y.-Y., Huang J.-L., and Chignell C.F. Delayed and sustained activation of extracellular signal-regulated kinase in human keratinocytes by UVA: implications in carcinogenesis. J. Biol. Chem. 279 (2004) 53867-53874
51. Lee E.-R., Kang Y.-J., Kim J.-H., Lee H.T., and Cho S.-G. Modulation of apoptosis in HaCaT keratinocytes via differential regulation of ERK signaling pathway by flavonoids. J. Biol. Chem. 280 (2005) 31498-31507
52. Stefanelli C., Tantini B., Fattori M., Stanic, Rsquo, Ivana, Pignatti C., Clo C., Guarnieri C., Caldarera C.M., Mackintosh C.A., Pegg A.E., and Flamigni F. Caspase activation in etoposide-treated fibroblasts is correlated to ERK phosphorylation and both events are blocked by polyamine depletion. FEBS Lett. 527 (2002) 223-228
53. Sautin Y.Y., Crawford J.M., and Svetlov S.I. Enhancement of survival by LPA via Erk1/Erk2 and PI 3-kinase/Akt pathways in a murine hepatocyte cell line. Am. J. Physiol., Cell Physiol. 281 (2001) C2010-C2019
54. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev., Mol. Cell Biol. 6 (2005) 827-837
55. Deng W., Wang D.A., Gosmanova E., Johnson L.R., and Tigyi G. LPA protects intestinal epithelial cells from apoptosis by inhibiting the mitochondrial pathway. Am. J. Physiol.: Gasterointest. Liver Physiol. 284 (2003) G821-G829
56. Harnois C., Demers M., Bouchard V., Vallée K., Gagné D., Fujita N., Tsuruo T., Vézina A., Beaulieu J., Côté A., and Vachon P.H. Human intestinal epithelial crypt cell survival and death: complex modulations of Bcl-2 homologs by Fak, PI3-K/Akt-1, MEK/Erk, and p38 signaling pathways. J. Cell. Physiol. 198 (2004) 209-222
57. Goetzl E.J., Kong Y., and Mei B. Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of Bax. J. Immunol. 162 (1999) 2049-2056
58. Fernando R.I., and Wimalasena J. Estradiol abrogates apoptosis in breast cancer cells through inactivation of BAD: Ras-dependent nongenomic pathways requiring signaling through ERK and Akt. Mol. Biol. Cell 15 (2004) 3266-3284
59. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., and Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286 (1999) 1358-1362
60. Frodin M., and Gammeltoft S. Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol. 151 (1999) 65-77
61. Kang Y.C., Kim K.M., Lee K.S., Namkoong S., Lee S.J., Han J.A., Jeoung D., Ha K.S., Kwon Y.G., and Kim Y.M. Serum bioactive lysophospholipids prevent TRAIL-induced apoptosis via PI3K/Akt-dependent cFLIP expression and Bad phosphorylation. Cell Death Differ. 11 (2004) 1287-1298
62. Lizcano J.M., Morrice N., and Cohen P. Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem. J. 349 (2000) 547-557
63. Ishii I., Contos J.J., Fukushima N., and Chun J. Functional comparisons of the lysophosphatidic acid receptors, LP(A1)/VZG-1/EDG-2, LP(A2)/EDG-4, and LP(A3)/EDG-7 in neuronal cell lines using a retrovirus expression system. Mol. Pharmacol. 58 (2000) 895-902
64. Baudhuin L.M., Cristina K.L., Lu J., and Xu Y. Akt activation induced by lysophosphatidic acid and sphingosine-1-phosphate requires both mitogen-activated protein kinase kinase and p38 mitogen-activated protein kinase and is cell-line specific. Mol. Pharmacol. 62 (2002) 660-671
65. Miller R.R., Leanza C.M., Phillips E.E., and Blacquire K.D. Homocysteine-induced changes in brain membrane composition correlate with increased brain caspase-3 activities and reduced chick embryo viability. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 136 (2003) 521-532
66. Skurk C., Maatz H., Kim H.S., Yang J., Abid M.R., Aird W.C., and Walsh K. The Akt-regulated forkhead transcription factor FOXO3a controls endothelial cell viability through modulation of the caspase-8 inhibitor FLIP. J. Biol. Chem. 279 (2004) 1513-1525
67. Zhang Y., Hong Y., Bounhar Y., Blacker M., Roucou X., Tounekti O., Vereker E., Bowers W.J., Federoff H.J., Goodyer C.G., and LeBlanc A. p75 Neurotrophin receptor protects primary cultures of human neurons against extracellular amyloid β peptide cytotoxicity. J. Neurosci. 23 (2003) 7385-7394
68. Aoyama T., Matsui T., Novikov M., Park J., Hemmings B., and Rosenzweig A. Serum and glucocorticoid-responsive kinase-1 regulates cardiomyocyte survival and hypertrophic response. Circulation 111 (2005) 1652-1659
69. Leong M.L., Maiyar A.C., Kim B., O'Keeffe B.A., and Firestone G.L. Expression of the serum- and glucocorticoid-inducible protein kinase, Sgk, is a cell survival response to multiple types of environmental stress stimuli in mammary epithelial cells. J. Biol. Chem. 278 (2003) 5871-5882