Monocrotaline pyrrole-induced endothelial cell megalocytosis involves a Golgi blockade mechanism

American Journal of Physiology - Cell Physiology

Volumn 288, Issue 4 57-4, 2005, Pages

  Shah, Mehul ^a   Patel, Kirit ^a   Sehgal, Pravin B ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Caveolin 1; Pulmonary hypertension; Pyrrolizidine alkaloids

Indexed keywords

2 METHOXYESTRADIOL; CAVEOLIN 1; CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCROTALINE PYRROLE; NOCODAZOLE; PHOSPHOTRANSFERASE; PROTEIN GM130; SERINE; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DENSITY; ENDOTHELIUM CELL; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMAGING; IMMUNOFLUORESCENCE; LIVER CELL; LUNG ALVEOLUS EPITHELIUM; MEGALOCYTOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; AUTOANTIGENS; BLOTTING, WESTERN; CAVEOLIN 1; CAVEOLINS; CELL SIZE; CELLS, CULTURED; DNA-BINDING PROTEINS; ENDOTHELIUM, VASCULAR; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLUORESCENT ANTIBODY TECHNIQUE; GOLGI APPARATUS; HEPATOCYTES; HUMANS; MEMBRANE PROTEINS; MITOSIS; MONOCROTALINE; MUSCLE, SMOOTH, VASCULAR; PULMONARY ALVEOLI; PULMONARY ARTERY; STAT3 TRANSCRIPTION FACTOR; SWINE; TRANS-ACTIVATORS;

EID: 15444365139     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00327.2004     Document Type: Article

References (70)

1. Afzelius BA and Schoental R. The ultrastructure of the enlarged hepatocytes induced in rats with a single oral dose of retrorsine, a pyrrolizidine (Senecio) alkaloid. J Ultrastruct Res 20: 328-345, 1967.
2. Allen JR, Carstens LA, Norback DH, and Loh PM. Ultrastructural and biochemical changes associated with pyrrolizidine-induced hepatic megalocytosis. Cancer Res 30: 1857-1866, 1970.
3. Armstrong SJ and Zuckerman AJ. The effects of lasiocarpine, retrorsine and retronecine pyrrole on human embryo lung and liver cells in culture. Br J Exp Pathol 53: 138-144, 1972.
4. Attalla H, Mäkelä TP, Adlercreutz H, and Andersson LC. 2-Methoxyestradiol arrests cells in mitosis without depolymerizing tubulin. Biochem Biophys Res Commun 228: 467-473, 1996.
5. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, and Darnell JE Jr. Stat3 as an oncogene. Cell 98: 295-303, 1999.
6. Buettner R, Kortylewski M, Pardoll D, Yu H, and Jove R. STAT proteins as molecular targets for cancer therapy. In: Signal Transducers and Activators of Transcription (STATs): Activation and Biology, edited by Sehgal PB, Levy DE, and Hirano T. Boston, MA: Kluwer Academic, 2003, p. 645-661.
7. Bull LB. The histological evidence of liver damage from pyrrolizidine alkaloids: megalocytosis of the liver cells and inclusion globules. Aust Vet J 31: 33-40, 1955.
8. Carcedo CH, Bonazzi M, Spanò S, Turacchio G, Colanzi A, Luini A, and Corda D. Mitotic Golgi partitioning is driven by the membrane-fissioning protein CtBP3/BARS. Science 305: 93-96, 2004.
9. Charron AJ, Bacallao RL, and Wandinger-Ness A. ADPKD: a human disease altering Golgi function and basolateral exocytosis in renal epithelia. Traffic 1: 675-686, 2000.
10. Conrad PA, Smart EJ, Ying YS, Anderson RG, and Bloom GS. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J Cell Biol 131: 1421-1433, 1995.
11. Davidson J. The action of retrorsine on rat's liver. J Pathol Bacteriol 40: 285-295, 1935.
12. Diao A and Lowe M. The Golgi goes fission. Science 305: 48-49, 2004.
13. Harris PN, Anderson RC, and Chen KK. The action of monocrotaline and retronecine. J Pharmacol Exp Ther 75: 78-82, 1942.
14. Harris PN, Anderson RC, and Chen KK. The action of senecionine, integerrine, jocobine, longilobine and spartiodine, especially on the liver. J Pharmacol Exp Ther 75: 69-77, 1942.
15. Hayashi -Y and Lalich JJ. Renal and pulmonary alterations induced in rats by a single injection of monocrotaline. Proc Soc Exp Biol Med 124: 392-396, 1967.
16. Hirchinson V and Hill KR. The effects of a Senecio alkaloid (monocrotaline) on human embryo liver in tissue culture. Br J Cancer 14: 637-646, 1960.
17. Hsu IC, Chesney CF, and Allen JR. Chronic effects of monocrotaline pyrrole on hepatic mitosis and DNA synthesis. PTOC Soc Exp Biol Med 142: 1133-1136, 1973.
18. Jasmin JF, Mercier I, Hnasko R, Cheung MWC, Tanowitz HB, Dupuis J, and Lisanti MP. Lung remodeling and pulmonary hypertension after myocardial infarction: pathogenic role of reduced caveolin expression. Cardiovasc Res 63: 747-755, 2004.
19. Lafont F and Simons K. Raft-partitioning of the ubiquitin ligases Cbl and Nedd4 upon IgE-triggered cell signaling. Proc Natl Acad Sci USA 98: 3180-3184, 2001.
20. Lalich JJ and Merkow L. Pulmonary arteritis produced in rat by feeding Crotalaria spectabilis. Lab Invest 10: 744-750, 1961.
21. Lamé MW, Jones AD, Wilson DW, Dunston SK, and Segall HJ. Protein targets of monocrotaline pyrrole in pulmonary artery endothelial cells. J Biol Chem 275: 29091-29099, 2000.
22. Lappin PB, Ross KL, King LE, Fraker PJ, and Roth RA. The response of pulmonary vascular endothelial cells to monocrotaline pyrrole: cell proliferation and DNA synthesis in vitro and in vivo. Toxicol Appl Pharmacol 150: 37-48, 1998.
23. Lappin PB and Roth RA. Hypertrophy and prolonged DNA synthesis in smooth muscle cells characterize pulmonary arterial wall thickening after monocrotaline pyrrole administration to rats. Toxicol Pathol 25: 372-380, 1997.
24. Lee H, Park DS, Razani B, Russell RG, Pestell RG, and Lisant! MP. Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am J Pathol 161: 1357-1369, 2002.
25. Liu J, Razani B, Tang S, Terman BI, Ware JA, and Lisanti MP. Angiogenesis activators and inhibitors differentially regulate caveolin-1 expression and caveolae formation in vascular endothelial cells: angiogenesis inhibitors block vascular endothelial growth factor-induced down-regulation of caveolin-I. J Biol Chem 274: 15781-15785, 1999.
26. Lowe M, Gonatas NK, and Warren G. The mitotic phosphorylation cycle of the cis-Golgi matrix protein GM130. J Cell Biol 149: 341-356, 2000.
27. Lowe M, Rabouille C, Nakamura N, Watson R, Jackman M, Jamsa E, Rahman D, Pappin DJ, and Warren G. Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis. Cell 94: 783-793, 1998.
28. Mathew R, Huang J, Shah M, Patel K, Gewitz M, and Sehgal PB. Disruption of endothelial-cell caveolin-1α/raft scaffolding during development of monocrotaline-induced pulmonary hypertension. Circulation 110: 1499-1506, 2004.
29. Mathew R, Yuan N, Rosenfeld L, Gewitz MH, and Kumar A. Effects of monocrotaline on endothelial nitric oxide synthase expression and sulfhydryl levels in rat lungs. Heart Dis 4: 152-158, 2002.
30. Mattocks AR and Jukes R. Trapping and measurement of short-lived alkylating agents in a recirculating flow system. Chem Biol Interact 76: 19-30, 1990.
31. Mattocks AR, Jukes R, and Brown J. Simple procedures for preparing putative toxic metabolites of pyrrolizidine alkaloids. Toxicon 27: 561-567, 1989.
32. Mattocks AR and Legg RF. Antimitotic activity of dehydroretronecine, a pyrrolizidine alkaloid metabolite, and some analogous compounds, in a rat liver parenchymal cell line. Chem Biol Interact 30: 325-336, 1980.
33. Merkow L and Kleinerman J. An electron microscopic study of pulmonary vasculitis induced by monocrotaline. Lab Invest 15: 547-564, 1966.
34. 3H-thymidine by the cells of the pulmonary circulation and alveolar walls. Am J Pathol 106: 84-94, 1982.
35. Murata T, Sato K, Hori M, Ozaki H, and Karaki H. Decreased endothelial nitric-oxide synthase (eNOS) activity resulting from abnormal interaction between eNOS and its regulatory proteins in hypoxia-induced pulmonary hypertension. J Biol Chem 277: 44085-44092, 2002.
36. Nadasdy T, Laszik Z, Lajoie G, Blick KE, Wheeler DE, and Silva FG. Proliferative activity of cyst epithelium in human renal cystic diseases. J Am Soc Nephrol 5: 1462-1468, 1995.
37. Nakayasu H and Berezney R. Mapping replicational sites in the eucaryotic cell nucleus. J Cell Biol 108: 1-11, 1989.
38. Ndubuisi MI, Guo GG, Fried VA, Etlinger JD, and Sehgal PB. Cellular physiology of STAT3: where's the cytoplasmic monomer? J Biol Chem 274: 25499-25509, 1999.
39. Novotny-Diermayr V, Zhang T, Gu L, and Cao X. Protein kinase Cδ associates with the interleukin-6 receptor subunit glycoprotein (gp) 130 via Stat3 and enhances Stat3-gp130 interaction. J Biol Chem 277: 49134-49142, 2002.
40. Peterson JE. Effects of the pyrrolizidine alkaloid, lasiocarpine N-oxide, on nuclear and cell division in the liver rats. J Pathol Bacterial 89: 153-171, 1965.
41. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, and Parton RG. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 152: 1057-1070, 2001.
42. Pol A, Martin S, Fernandez MA, Ferguson C, Carozzi A, Luetterforst R, Enrich C, and Parton RG. Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol Biol Cell 15: 99-110, 2004.
43. Rabinovitch M. The mouse through the looking glass: a new door into the pathophysiology of pulmonary hypertension. Circ Res 94: 1001-1004, 2004.
44. Ramasubbu K, Gretz N, and Bachmann S. Increased epithelial cell proliferation and abnormal extracellular matrix in rat polycystic kidney disease. J Am Soc Nephrol 9: 937-945, 1998.
45. 135-containing human hepatoma Hep3B cell lines. J Immunol 161: 325-334, 1998.
46. Reindel JF and Roth RA. The effects of monocrotaline pyrrole on cultured bovine pulmonary artery endothelial and smooth muscle cells. Am J Pathol 138: 707-719, 1991.
47. Reiser F, Way D, Bernas M, Witte M, and Witte C. Inhibition of normal and experimental angiotumor endothelial cell proliferation and cell cycle progression by 2-methoxyestradiol. Proc Soc Exp Biol Med 219: 211-216, 1998.
48. Rose CL, Fink RD, Harris PN, and Chen KK. Effect of hepatotoxic alkaloids on prothrombin time of rats. J Pharmacol Exp Ther 83: 265-269, 1945.
49. Rosenberg HC and Rabinovitch M. Endothelial injury and vascular reactivity in monocrotaline pulmonary hypertension. Am J Physiol Heart Circ Physiol 255: H1484-H1491, 1988.
50. Schoental R. Hepatotoxic action of pyrrolizidine (Senecio) alkaloids in relation to their structure. Nature 179: 361-363, 1957.
51. Schick N, Oakeley EJ, Hynes NE, and Badache A. TEL/ETV6 is a signal transducer and activator of transcription 3 (Stat3)-induced represser of Stat3 activity. J Biol Chem 279: 38787-38796, 2004.
52. Schultze AE, Gunaga KP, Wagner JG, Hoorn CM, Moorehead WR, and Roth RA. Lactate dehydrogenase activity and isozyme patterns in tissues and bronchoalveolar lavage fluid from rats treated with monocrotaline pyrrole. Toxicol Appl Pharmacol 126: 301-310, 1994.
53. Seegers JC, Aveling ML, van Aswegen CH, Cross M, Koch F, and Joubert WS. The cytotoxic effects of estradiol-17β, catecholestradiols and methoxyestradiols on dividing MCF-7 and HeLa cells. J Steroid Biochem 32: 797-809, 1989.
54. Seemann J, Jokitalo E, Pypaert M, and Warren G. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407: 1022-1026, 2000.
55. Sehgal PB, Guo GG, Shah M, Kumar V, and Patel K. Cytokine signaling: STATS in plasma membrane rafts. J Biol Chem 277: 12067-12074, 2002.
56. Shah M, Patel K, Fried VA, and Sehgal PB. Interactions of STAT3 with caveolin-1 and heat shock protein 90 in plasma membrane raft and cytosolic complexes: preservation of cytokine signaling during fever. J Biol Chem 277: 45662-45669, 2002.
57. Sotgia F, Razani B, Bonuccelli G, Schubert W, Battista M, Lee H, Capozza F, Schubert AL, Minetti C, Buckley JT, and Lisanti MP. Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol Cell Biol 22: 3905-3926, 2002.
58. Sullman SF and Zuckerman AJ. The effect of heliotrine, a pyrrolizidine alkaloid, on human liver cells in culture. Br J Exp Pathol 50: 361-370, 1969.
59. Sütterlin C, Hsu P, Mallabiabarrena A, and Malhotra V. Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell 109: 359-369, 2002.
60. Svoboda D and Soga J. Early effects of pyrrolizidine alkaloids on the fine structure of rat liver cells. Am J Pathol 48: 347-373, 1966.
61. Taylor DW, Lamé MW, Nakayama LS, Segall HJ, and Wilson DW. Effects of monocrotaline pyrrole and thrombin on pulmonary endothelial cell junction and matrix adhesion proteins. Toxicology 184: 227-240, 2003.
62. Thomas HC, Lamé MW, Wilson DW, and Segall HJ. Cell cycle alterations associated with covalent binding of monocrotaline pyrrole to pulmonary artery endothelial cell DNA. Toxicol Appl Pharmacol 141: 319-329, 1996.
63. Todorovich-Hunter L, Johnson DJ, Ranger P, Keeley FW, and Rabinovitch M. Altered elastin and collagen synthesis associated with progressive pulmonary hypertension induced by monocrotaline: a biochemical and ultrastructural study. Lab Invest 58: 184-195, 1988.
64. Tropea JE, Molyneux RJ, Kaushal GP, Pan YT, Mitchell M, and Elbein AD. Australine, a pyrrolizidine alkaloid that inhibits amyloglucosidase and glycoprotein processing. Biochemistry 28: 2027-2034, 1989.
65. Tulsiani DR, Harris TM, and Touster O. Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of Golgi mannosidase II. J Biol Chem 257: 7936-7939, 1982.
66. Valdivia E, Sonnad J, Hayashi Y, and Lallich JJ. Experimental interstitial pulmonary edema. Angiology 18: 378-383, 1967.
67. Wilson DW, Lamé MW, Dunston SK, and Segall HJ. DNA damage cell checkpoint activities are altered in monocrotaline pyrrole-induced cell cycle arrest in human pulmonary artery endothelial cells. Toxicol Appl Pharmacol 166: 69-80, 2000.
68. Wilson DW, Lamé MW, Dunston SK, Taylor DW, and Segall HJ. Monocrotaline pyrrole interacts with actin and increases thrombin-mediated permeability in pulmonary artery endothelial cells. Toxicol Appl Pharmacol 152: 138-144, 1998.
69. Wilson DW and Segall HJ. Changes in type II cell populations in monocrotaline pneumotoxicity. Am J Pathol 136: 1293-1299, 1990.
70. Zhao YD, Campbell AI, Robb M, Ng D, and Stewart DJ. Protective role of angiopoietin-1 in experimental pulmonary hypertension. Circ Res 92: 984-991, 2003.