LPA protects intestinal epithelial cells from apoptosis by inhibiting the mitochondrial pathway

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 284, Issue 5 47-5, 2003, Pages

  Deng, Wenlin ^a   Wang, De An ^a   Gosmanova, Elvira ^a   Johnson, Leonard R ^a   Tigyi, Gabor ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Bcl 2 protein; Camptothecin; Caspase 3 cpp32; Caspase 9; Cytochrome c; Lysophosphatidic acid

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; CAMPTOTHECIN; CASPASE 3; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; DNA FRAGMENT; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; PERTUSSIS TOXIN; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME INHIBITION; GENE TRANSLOCATION; INTESTINE EPITHELIUM CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; UPREGULATION;

EID: 0037403718     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00406.2002     Document Type: Article

References (71)

1. Antonsson B, Montessuit S, Lauper S, Eskes R, and Martinou JC. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345: 271-278, 2000.
2. Baker DL, Desiderio DM, Miller DD, Tolley B, and Tigyi GJ. Direct quantitative analysis of lysophosphatidic acid molecular species by stable isotope dilution electrospray ionization liquid chromatography-mass spectrometry. Anal Biochem 292: 287-295, 2001.
3. Bedner E, Li X, Kunicki J, and Darzynkiewicz Z. Translocation of Bax to mitochondria during apoptosis measured by laser scanning cytometry. Cytometry 41: 83-88, 2000.
4. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, and Thompson CB. Bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597-608, 1993.
5. Budihardjo I, Oliver H, Lutter M, Luo X, and Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15: 269-290, 1999.
6. Cain K, Bratton SB, Langlais C, Walker G, Brown DG, Sun XM, and Cohen GM. Apaf-1 oligomerizes into biologically active approximately 700-kDa and inactive approximately 1.4-MDa apoptosome complexes. J Biol Chem 275: 6067-6070, 2000.
7. Chittenden T, Harrington EA, O'Connor R, Flemington C, Lutz RJ, Evan GI, and Guild BC. Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374: 733-736, 1995.
8. Contos JJ, Ishii I, and Chun J. Lysophosphatidic acid receptors. Mol Pharmacol 58: 1188-1196, 2000.
9. Cunningham D. Setting a new standard-irinotecan (Campto) in the second-line therapy of colorectal cancer: final results of two phase III studies and implications for clinical practice. Semin Oncol 26, Suppl 5: 1-5, 1999.
10. Cunningham D and Glimelius B. A phase III study of irinotecan (CPT-11) versus best supportive care in patients with metastatic colorectal cancer who have failed 5-fluorouracil therapy. V301 Study Group. Semin Oncol 26, Suppl 5: 6-12, 1999.
11. Deng W, Balazs L, Wang DA, Van Middlesworth L, and Tigyi G, Johnson LR. Lysophosphatidic acid protects and rescues intestinal epithelial cells from radiation- and chemotherapy-induced apoptosis. Gastroenterology 123: 206-216, 2002.
12. i-protein-mediated activation of mitogen-activated protein kinase. Biochem J 352: 135-143, 2000.
13. Fernandes-Alnemri T, Takahashi A, Armstrong R, Krebs J, Fritz L, Tomaselli KJ, Wang L, Yu Z, Croce CM, Salveson G, Earnshaw WC, Litwack G, and Alnemri ES. Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res 55: 6045-6052, 1995.
14. Fukushima N and Chun J. The LPA receptors. Prostaglandins Other Lipid Mediat 64: 21-32, 2001.
15. Godlewski MM, Motyl MA, Gajkowska B, Wareski P, Koronkiewicz M, and Motyl T. Subcellular redistribution of BAX during apoptosis induced by anticancer drugs. Anticancer Drugs 12: 607-617, 2001.
16. Goetzl EJ, 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 162:2049-2056, 1999.
17. Goetzl EJ, Lee H, Dolezalova H, Kalli KR, Conover CA, Hu YL, Azuma T, Stossel TP, Karliner JS, and Jaffe RB. Mechanisms of lysolipid phosphate effects on cellular survival and proliferation. Ann NY Acad Sci 905: 177-187, 2000.
18. Guy-Grand D, DiSanto JP, Henchoz P, Malassis-Seris M, and Vassalli P. Small bowel enteropathy: role of intraepithelial lymphocytes and of cytokines (IL-12, IFN-gamma, TNF) in the induction of epithelial cell death and renewal. Eur J Immunol 28:730-744, 1998.
19. Hall PA, Coates PJ, Ansari B, and Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 107: 3569-3577, 1994.
20. Heid CA, Stevens J, Livak KJ, and Williams PM. Real time quantitative PCR. Genome Res 6: 986-994, 1996.
21. 2-terminal BH4 domain of Bcl-2 is functional for heterodimerization with Bax and inhibition of apoptosis. J Biol Chem 274: 20415-20420, 1999.
22. Hofmann K, Bucher P, and Tschopp J. The CARD domain: a new apoptotic signalling motif. Trends Biochem Sci 22: 155-156, 1997.
23. Horwitz SB and Horwitz MS. Effects of camptothecin on the breakage and repair of DNA during the cell cycle. Cancer Res 33: 2834-2836, 1973.
24. Hsu YT and Youle RJ. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 273: 10777-10783, 1998.
25. Ijiri K and Potten CS. Response of intestinal cells of differing topographical and hierarchical status to ten cytotoxic drugs and five sources of radiation. Br J Cancer 47: 175-185, 1983.
26. Jalink K, Hordijk PL, and Moolenaar WH. Growth factor-like effects of lysophosphatidic acid, a novel lipid mediator. Biochim Biophys Acta 1198: 185 -196, 1994.
27. Kaufmann SH. Cell death induced by topoisomerase-targeted drugs: more questions than answers. Biochim Biophys Acta 1400: 195-211, 1998.
28. Keefe DM, Brealey J, Goland GJ, and Cummins AG. Chemotherapy for cancer causes apoptosis that precedes hypoplasia in crypts of the small intestine in humans. Gut 47: 632-637, 2000.
29. Kelekar A and Thompson CB. Bcl-2-family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol 8: 324-330, 1998.
30. Kim CN, Wang X, Huang Y, Ibrado AM, Liu L, Fang G, and Bhalla K. Overexpression of Bcl-X(L) inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res 57: 3115-3120, 1997.
31. Kluck RM, Bossy-Wetzel E, Green DR, and Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
32. Knudson CM and Korsmeyer SJ. Bcl-2 and Bax function independently to regulate cell death. Nat Genet 16: 358-363, 1997.
33. Kroemer G, Dallaporta B, and Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60: 619-642, 1998.
34. Kroemer G, Zamzami N, and Susin SA. Mitochondrial control of apoptosis. Immunol Today 18: 44-51, 1997.
35. Lansiaux A, Facompre M, Wattez N, Hildebrand MP, Bal C, Demarquay D, Lavergne O, Bigg DC, and Bailly C. Apoptosis induced by the homocamptothecin anticancer drug BN80915 in HL-60 cells. Mol Pharmacol 60: 450-461, 2001.
36. Lassus P, Opitz-Araya X, and Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297: 1352-1354, 2002.
37. Levine JS, Koh JS, Triaca V, and Lieberthal W. Lysophosphatidic acid: a novel growth and survival factor for renal proximal tubular cells. Am J Physiol Renal Physiol 273: F575-F585, 1997.
38. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, and Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
39. Liu X, Li P, Widlak P, Zou H, Luo X, Garrard WT, and Wang X. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci USA 95: 8461-8466, 1998.
40. Liu X, Zou H, Slaughter C, and Wang X. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175-184, 1997.
41. Mahajan NP, Linder K, Berry G, Gordon GW, Heim R, and Herman B. Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat Biotechnol 16: 547-552, 1998.
42. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, and Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031, 1998.
43. Mesner PW Jr, Budihardjo II, and Kaufmann SH. Chemotherapy-induced apoptosis. Adv Pharmacol 41: 461-499, 1997.
44. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H, and Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 95: 14681-14686, 1998.
45. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T, Yu VL, and Miller DK. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43, 1995.
46. Nunez G, Benedict MA, Hu Y, and Inohara N. Caspases: the proteases of the apoptotic pathway, Oncogene 17: 3237-3245, 1998.
47. Pritchard DM and Watson AJ. Apoptosis and gastrointestinal pharmacology. Pharmacol Ther 72: 149-169, 1996.
48. Potten CS, Merritt A, Hickman J, Hall P, and Faranda A. Characterization of radiation-induced apoptosis in the small intestine and its biological implications. Int J Radiat Biol 65: 71-78, 1994.
49. Quaroni A, Wands J, Trelstad RL, and Isselbacher KJ. Epithelioid cell cultures from rat small intestine. characterization by morphologic and immunologic criteria. J Cell Biol 80: 248-265, 1979.
50. Reed JC. Mechanisms of apoptosis avoidance in cancer. Curr Opin Oncol 11: 68-75, 1999.
51. Salvesen GS and Dixit VM. Caspases: intracellular signaling by proteolysis. Cell 91: 443-446, 1997.
52. Sane AT and Bertrand R. Caspase inhibition in camptothecintreated U-937 cells is coupled with a shift from apoptosis to transient G1 arrest followed by necrotic cell death. Cancer Res 59: 3565-3569, 1999.
53. 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: 21197-22106, 2002.
54. Sautin YY, Crawford JM, and Svetlov SI. Enhancement of survival by LPA via Erkl/Erk2 and PI 3-kinase/Akt pathways in a murine hepatocyte cell line. Am J Physiol Cell Physiol 281: C2010-C2019, 2001.
55. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB, and Korsmeyer SJ. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 92: 7834-7838, 1995.
56. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Litwack G, and Alnemri ES. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc Natl Acad Sci USA 93: 14486-14491, 1996.
57. Svejstrup JQ, Christiansen K, Gromova II, Andersen AH, and Westergaard O. New technique for uncoupling the cleavage and religation reactions of eukaryotic topoisomerase I. The mode of action of camptothecin at a specific recognition site. J Mol Biol 222: 669-678, 1991.
58. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, and Dixit VM. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801-809, 1995.
59. Thornberry NA and Lazebnik Y. Caspases: enemies within. Science 281: 1312-1316, 1998.
60. Tigyi G. Physiological responses to lysophosphatidic acid and related glycero-phospholipids. Prostaglandins Other Lipid Metiat 64: 47-62, 2001.
61. Tigyi G, Fischer DJ, Baker D, Wang DA, Yue J, Nusser N, Virag T, Zsiros V, Liliom K, Miller D, and Parrill A. Pharmacological characterization of phospholipid growth-factor receptors. Ann NY Acad Sci 905: 34-53, 2000.
62. Tigyi G, Liliom K, Fischer DJ, and Guo Z. Phospholipid growth factors: identification and mechanism of action. In: Lipid Second Messengers, edited by Laychock SG and Rubin RP. Boca Raton, FL: CRC, 1999: p. 51-81.
63. Tokumura A, Harada K, Fukuzawa K, and Tsukatani H. Involvement of lysophospholipase D in the production of lysophosphatidic acid in rat plasma. Biochim Biophys Acta 875: 31-38, 1986.
64. Umansky SR, Cuenco GM, Khutzian SS, Barr PJ, and Tomei LD. Post-ischemic apoptotic death of rat neonatal cardiomocytes. Cell Death Differ 2: 235-241, 1995.
65. Vaux DL and Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA 93: 2239-2244, 1996.
66. Weiner JA and Chun J. Schwann cell survival mediated by the signaling phospholipid lysophosphatidic acid. Proc Natl Acad Sci USA 96: 5233-5238, 1999.
67. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, and Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132, 1997.
68. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, and Korsmeyer SJ. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80: 285-291, 1995.
69. Yin XM, Oltvai ZN, and Korsmeyer SJ. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369: 321-23, 1994.
70. Yuan Q, Ray RM, and Johnson LR. Polyamine depletion prevents camptothecin -induced apoptosis by inhibiting the release of cytochrome c. Am J Physiol Cell Physiol 282: C1290-C1297, 2002.
71. Zou H, Henzel WJ, Liu X, Lutschg A, and Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413, 1997.