Cyclosporine A enhances apoptosis in gingival keratinocytes of rats and in OECM1 cells via the mitochondrial pathway

Journal of Periodontal Research

Volumn 44, Issue 6, 2009, Pages 767-775

  Tu, H P ^a,b   Chen, Y T ^a   Chiu, H C ^a   Chin, Y T ^a   Huang, S M ^a   Cheng, L C ^c   Fu, E ^a   Chiang, C Y ^a  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Cyclosporine A; Gingiva; Keratinocyte

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; APOPTOSIS INDUCING FACTOR; BAX PROTEIN, HUMAN; BAX PROTEIN, RAT; CASP3 PROTEIN, RAT; CASP8 PROTEIN, HUMAN; CASP9 PROTEIN, RAT; CASPASE 3; CASPASE 8; CASPASE 9; CYCLOSPORIN; DIAGNOSTIC AGENT; FAS ANTIGEN; FAS PROTEIN, HUMAN; FLUORESCENT DYE; IMMUNOSUPPRESSIVE AGENT; INDOLE DERIVATIVE; PROTEIN BAX; PROTEIN BCL 2; TNFRSF6 PROTEIN, RAT;

ANIMAL; APOPTOSIS; ARTICLE; COMPARATIVE STUDY; CYTOLOGY; DNA FRAGMENTATION; DNA MICROARRAY; DRUG EFFECT; FLOW CYTOMETRY; GINGIVA; HUMAN; KERATINOCYTE; MALE; MITOCHONDRION; PATHOLOGY; RANDOMIZATION; RAT; SPRAGUE DAWLEY RAT; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; CARCINOMA, SQUAMOUS CELL; CASPASE 3; CASPASE 8; CASPASE 9; CELL LINE, TUMOR; CYCLOSPORINE; DNA FRAGMENTATION; FLOW CYTOMETRY; FLUORESCENT DYES; GINGIVA; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INDOLES; KERATINOCYTES; MALE; MITOCHONDRIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 70350520356     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2008.01189.x     Document Type: Article

References (47)

1. Afonso M, Bello Vde O, Shibli JA, Sposto MR. Cyclosporin A-induced gingival overgrowth in renal transplant patients. J Periodontol 2003 74 : 51 56.
2. Tuter G, Serdar MA, Yalim M, Gurhan IS, Balos K. Evaluation of matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 levels in gingival fibroblasts of cyclosporin A-treated patients. J Periodontol 2002 73 : 1273 1278. (Pubitemid 35469674)
3. Nurmenniemi PK, Pernu HE, Knuuttila ML. Mitotic activity of keratinocytes in nifedipine- and immunosuppressive medication-induced gingival overgrowth. J Periodontol 2001 72 : 167 173.
4. Fu E, Hsieh YD, Shen EC, Nieh S, Mao TK, Chiang CY. Cyclosporin-induced gingival overgrowth at the newly formed edentulous ridge in rats: a morphological and histometric evaluation. J Periodontol 2001 72 : 889 894.
5. Das SJ, Parkar MH, Olsen I. Upregulation of keratinocyte growth factor in cyclosporin A-induced gingival overgrowth. J Periodontol 2001 72 : 745 752.
6. Chin YT, Chen YT, Tu HP et al. Upregulation of the expression of epidermal growth factor and its receptor in gingiva upon cyclosporin a treatment. J Periodontol 2006 77 : 647 656.
7. Tu HP, Fu E, Chen YT, Wu MH, Cheng LC, Yang SF. Expression of p21 and p53 in rat gingival and human oral epithelial cells after cyclosporine A treatment. J Periodont Res 2008 43 : 32 39.
8. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. p21 is a universal inhibitor of cyclin kinases. Nature 1993 366 : 701 704.
9. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1-WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995 82 : 675 684.
10. Niculescu AB III., Chen X, Smeets M, Hengst L, Prives C, Reed SI. Effects of p21(Cip1-Waf1) at both the G1-S and the G2-M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 1998 18 : 629 643.
11. Ogryzko VV, Wong P, Howard BH. WAF1 retards S-phase progression primarily by inhibition of cyclin-dependent kinases. Mol Cell Biol 1997 17 : 4877 4882.
12. Weinberg WC, Denning MF. P21Waf1 control of epithelial cell cycle and cell fate. Crit Rev Oral Biol Med 2002 13 : 453 464.
13. Maruoka Y, Harada H, Mitsuyasu T et al. Keratinocytes become terminally differentiated in a process involving programmed cell death. Biochem Biophys Res Commun 1997 238 : 886 890.
14. Ortiz A, Lorz C, Egido J. New kids in the block: the role of FasL and Fas in kidney damage. J Nephrol 1999 12 : 150 158.
15. Healy E, Dempsey M, Lally C, Ryan MP. Apoptosis and necrosis: mechanisms of cell death induced by cyclosporine A in a renal proximal tubular cell line. Kidney Int 1998 54 : 1955 1966.
16. Yang CW, Faulkner GR, Wahba IM et al. Expression of apoptosis-related genes in chronic cyclosporine nephrotoxicity in mice. Am J Transplant 2002 2 : 391 399.
17. Muller M, Strand S, Hug H et al. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1-Fas) receptor-ligand system and involves activation of wild-type p53. J Clin Invest 1997 99 : 403 413.
18. Faubion WA, Guicciardi ME, Miyoshi H et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999 103 : 137 145.
19. Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002 192 : 131 137.
20. Oyadomari S, Takeda K, Takiguchi M et al. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 2001 98 : 10845 10850.
21. Reynolds NJ, Al-Daraji WI. Calcineurin inhibitors and sirolimus: mechanisms of action and applications in dermatology. Clin Exp Dermatol 2002 27 : 555 561.
22. Takahashi T, Kamimura A. Cyclosporin a promotes hair epithelial cell proliferation and modulates protein kinase C expression and translocation in hair epithelial cells. J Invest Dermatol 2001 117 : 605 611.
23. Esposito C, Fornoni A, Cornacchia F et al. Cyclosporine induces different responses in human epithelial, endothelial and fibroblast cell cultures. Kidney Int 2000 58 : 123 130.
24. Justo P, Lorz C, Sanz A, Egido J, Ortiz A. Intracellular mechanisms of cyclosporin A-induced tubular cell apoptosis. J Am Soc Nephrol 2003 14 : 3072 3080.
25. Bulut S, Ozdemir BH. Apoptosis and expression of caspase-3 in cyclosporin-induced gingival overgrowth. J Periodontol 2007 78 : 2364 2368.
26. Bulut S, Ozdemir BH, Alaaddinoglu EE, Oduncuoglu FB, Bulut OE, Demirhan B. Effect of cyclosporin A on apoptosis and expression of p53 and bcl-2 proteins in the gingiva of renal transplant patients. J Periodontol 2005 76 : 691 695.
27. Alaaddinoglu EE, Karabay G, Bulut S et al. Apoptosis in cyclosporin A-induced gingival overgrowth: a histological study. J Periodontol 2005 76 : 166 170.
28. Birraux J, Kirby JA, Thomason JM, Taylor JJ. The effect of cyclosporin on cell division and apoptosis in human oral keratinocytes. J Periodont Res 2006 41 : 297 302.
29. Liu CY, Takemasa A, Liles WC et al. Broad-spectrum caspase inhibition paradoxically augments cell death in TNF-alpha-stimulated neutrophils. Blood 2003 101 : 295 304.
30. Walker PR, Kwast-Welfeld J, Gourdeau H, Leblanc J, Neugebauer W, Sikorska M. Relationship between apoptosis and the cell cycle in lymphocytes: roles of protein kinase C, tyrosine phosphorylation, and AP1. Exp Cell Res 1993 207 : 142 151.
31. Takaoka A, Hayakawa S, Yanai H et al. Integration of interferon-alpha- beta signalling to p53 responses in tumour suppression and antiviral defence. Nature 2003 424 : 516 523.
32. Johnson M, Dimitrov D, Vojta PJ et al. Evidence for a p53-independent pathway for upregulation of SDI1-CIP1-WAF1-p21 RNA in human cells. Mol Carcinog 1994 11 : 59 64.
33. Chen YT, Tu HP, Chin YT et al. Upregulation of transforming growth factor-beta1 and vascular endothelial growth factor gene and protein expression in cyclosporin-induced overgrown edentulous gingiva in rats. J Periodontol 2005 76 : 2267 2275.
34. Wright HJ, Chapple IL, Matthews JB. TGF-beta isoforms and TGF-beta receptors in drug-induced and hereditary gingival overgrowth. J Oral Pathol Med 2001 30 : 281 289.
35. Cotrim P, Martelli-Junior H, Graner E, Sauk JJ, Coletta RD. Cyclosporin A induces proliferation in human gingival fibroblasts via induction of transforming growth factor-beta1. J Periodontol 2003 74 : 1625 1633.
36. Tipton DA, Dabbous MK. Autocrine transforming growth factor beta stimulation of extracellular matrix production by fibroblasts from fibrotic human gingiva. J Periodontol 1998 69 : 609 619.
37. Cotrim P, de Andrade CR, Martelli-Junior H, Graner E, Sauk JJ, Coletta RD. Expression of matrix metalloproteinases in cyclosporin-treated gingival fibroblasts is regulated by transforming growth factor (TGF)-beta1 autocrine stimulation. J Periodontol 2002 73 : 1313 1322.
38. Khanna AK, Hosenpud JD. Cyclosporine induces the expression of the cyclin inhibitor p21. Transplantation 1999 67 : 1262 1268.
39. Taketani Y, Oka T. Epidermal growth factor stimulates cell proliferation and inhibits functional differentiation of mouse mammary epithelial cells in culture. Endocrinology 1983 113 : 871 877.
40. Cao L, Yao Y, Lee V et al. Epidermal growth factor induces cell cycle arrest and apoptosis of squamous carcinoma cells through reduction of cell adhesion. J Cell Biochem 2000 77 : 569 583.
41. Fan Z, Lu Y, Wu X, DeBlasio A, Koff A, Mendelsohn J. Prolonged induction of p21Cip1-WAF1-CDK2-PCNA complex by epidermal growth factor receptor activation mediates ligand-induced A431 cell growth inhibition. J Cell Biol 1995 131 : 235 242.
42. Brozovic S, Sahoo R, Barve S et al. Porphyromonas gingivalis enhances FasL expression via up-regulation of NFkappaB-mediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 2006 152 : 797 806.
43. Kato S, Nakashima K, Inoue M et al. Human epithelial cell death caused by Actinobacillus actinomycetemcomitans infection. J Med Microbiol 2000 49 : 739 745.
44. Mao S, Park Y, Hasegawa Y et al. Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol 2007 9 : 1997 2007.
45. Hasebe A, Yoshimura A, Into T et al. Biological activities of Bacteroides forsythus lipoproteins and their possible pathological roles in periodontal disease. Infect Immun 2004 72 : 1318 1325.
46. Leung WK, Wu Q, Hannam PM, McBride BC, Uitto VJ. Treponema denticola may stimulate both epithelial proliferation and apoptosis through MAP kinase signal pathways. J Periodont Res 2002 37 : 445 455.
47. Tu HP, Chen YT, Shieh YS et al. Cyclosporin-induced downregulation of the expression of E-cadherin during proliferation of edentulous gingival epithelium in rats. J Periodontol 2006 77 : 832 839.