Mcl-1 functions as major epidermal survival protein required for proper keratinocyte differentiation

Journal of Investigative Dermatology

Volumn 129, Issue 6, 2009, Pages 1351-1360

  Sitailo, Leonid A ^a,b   Jerome Morais, Anita ^a,b   Denning, Mitchell F ^a,b  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b LOYOLA UNIVERSITY HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA ACTIN; BIOLOGICAL MARKER; CASPASE 14; CASPASE 3; FILAGGRIN; LORICRIN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN K1; PROTEIN K10; PROTEIN MCL 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EPIDERMIS; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN FAMILY; RNA INTERFERENCE; ULTRAVIOLET IRRADIATION;

APOPTOSIS; CASPASE 3; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME INHIBITORS; EPIDERMIS; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; SKIN;

EID: 67349117381     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2008.363     Document Type: Article

References (57)

1. Aragane Y, Kulms D, Metze D, Wilkes G, Poppelmann B, Luger TA et al. (1998) Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J Cell Biol 140:171-82
2. Calautti E, Li J, Saoncella S, Brissette JL, Goetinck PF (2005) Phosphoinositide 3-kinase signaling to AKT promotes keratinocyte differentiation versus death. J Biol Chem 280:32856-65
3. Candi E, Schmidt R, Melino G (2005) The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol 6:328-40
4. Chaturvedi V, Qin JZ, Denning MF, Choubey D, Diaz MO, Nickoloff BJ (1999) Apoptosis in proliferating, senescent, and immortalized keratinocytes. J Biol Chem 274:23358-67
5. Chaturvedi V, Sitailo LA, Bodner B, Denning MF, Nickoloff BJ (2006) Defining the caspase-containing apoptotic machinery contributing to cornification in human epidermal equivalents. Exp Dermatol 15:14-22
6. Chaturvedi V, Sitailo LA, Qin JZ, Bodner B, Denning MF, Curry J et al. (2005) Knockdown of p53 levels in human keratinocytes accelerates Mcl-1 and Bcl-xL reduction thereby enhancing UV-light induced apoptosis. Oncogene 24:5299-312
7. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG et al. (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17:393-403
8. Chien AJ, Presland RB, Kuechle MK (2002) Processing of native caspase-14 occurs at an atypical cleavage site in normal epidermal differentiation. Biochem Biophys Res Commun 296:911-7
9. Cho SH, Delehedde M, Rodriguez-Villanueva J, Brisbay S, McDonnell TJ (2001) Bax gene disruption alters the epidermal response to ultraviolet irradiation and in vivo induced skin carcinogenesis. Int J Mol Med 7:235-41
10. Clohessy JG, Zhuang J, de Boer J, Gil-Gomez G, Brady HJ (2006) Mcl-1 interacts with truncated Bid and inhibits its induction of cytochrome c release and its role in receptor-mediated apoptosis. J Biol Chem 281:5750-9
11. Denecker G, Hoste E, Gilbert B, Hochepied T, Ovaere P, Lippens S et al. (2007) Caspase-14 protects against epidermal UVB photodamage and water loss. Nat Cell Biol 9:666-74
12. Denning MF, Wang Y, Nickoloff BJ, Wrone-Smith T (1998) Protein kinase Cd is activated by caspase-dependent proteolysis during ultraviolet radiation-induced apoptosis of human keratinocytes. J Biol Chem 273:29995-30002
13. Eckhart L, Declercq W, Ban J, Rendl M, Lengauer B, Mayer C et al. (2000) Terminal differentiation of human keratinocytes and stratum corneum formation is associated with caspase-14 activation. J Invest Dermatol 115:1148-51
14. Fujise K, Zhang D, Liu J, Yeh ET (2000) Regulation of apoptosis and cell cycle progression by MCL1. Differential role of proliferating cell nuclear antigen. J Biol Chem 275:39458-65
15. Gandarillas A, Goldsmith LA, Gschmeissner S, Leigh IM, Watt FM (1999) Evidence that apoptosis and terminal differentiation of epidermal keratinocytes are distinct processes. Exp Dermatol 8:71-9
16. l and Bcl-2 on mitochondria in human B cells. Eur J Immunol 35:971-6
17. Graidist P, Yazawa M, Tonganunt M, Nakatomi A, Lin CC, Chang JY et al. (2007) Fortilin binds Ca2+ and blocks Ca2+-dependent apoptosis in vivo. Biochem J 408:181-91
18. Haghighat NG, Ruben L (1992) Purification of novel calcium binding proteins from Trypanosoma brucei: properties of 22-, 24- and 38-kilodalton proteins. Mol Biochem Parasitol 51:99-110
19. Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa SH (1980) Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19:245-54
20. Hough-Monroe L, Milstone LM (1991) Quantitation of cross-linked protein: an alternative to counting cornified envelopes as an index of keratinocyte differentiation. Anal Biochem 199:25-8
21. Hu S, Snipas SJ, Vincenz C, Salvesen G, Dixit VM (1998) Caspase-14 is a novel developmentally regulated protease. J Biol Chem 273:29648-53
22. Iglesias-Serret D, Pique M, Gil J, Pons G, Lopez JM (2003) Transcriptional and translational control of Mcl-1 during apoptosis. Arch Biochem Biophys 417:141-52
23. Jamil S, Sobouti R, Hojabrpour P, Raj M, Kast J, Duronio V (2005) A proteolytic fragment of Mcl-1 exhibits nuclear localization and regulates cell growth by interaction with Cdk1. Biochem J 387:659-67
24. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW (1993) MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 90:3516-20
25. Krajewski S, Bodrug S, Krajewska M, Shabaik A, Gascoyne R, Berean K et al. (1995) Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am J Pathol 146:1309-19
26. Kuechle MK, Predd HM, Fleckman P, Dale BA, Presland RB (2001) Caspase-14, a keratinocyte specific caspase: mRNA splice variants and expression pattern in embryonic and adult mouse. Cell Death Differ 8:868-70
27. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR et al. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17:525-35
28. 2+ inhibits murine keratinocyte differentiation in vitro. J Cell Physiol 163:105-14
29. Lippens S, Denecker G, Ovaere P, Vandenabeele P, Declercq W (2005) Death penalty for keratinocytes: apoptosis versus cornification. Cell Death Differ 12(Suppl 2):1497-508
30. Lippens S, Kockx M, Knaapen M, Mortier L, Polakowska R, Verheyen A et al. (2000) Epidermal differentiation does not involve the pro-apoptotic executioner caspases, but is associated with caspase-14 induction and processing. Cell Death Differ 7:1218-24
31. Meyers C, Frattini MG, Laiminis LA (1994) Tissue culture techniques for the study of human papillomaviruses in stratified epithelia. In: Cell Biology: A Laboratory Handbook. Celis JE (Ed) Academic Press Inc., San Diego, CA, 491-9
32. Michels J, Johnson PW, Packham G (2005) Mcl-1. Int J Biochem Cell Biol 37:267-71
33. Mitra RS, Wrone-Smith T, Simonian P, Foreman KE, Nunez G, Nickoloff BJ (1997) Apoptosis in keratinocytes is not dependent on induction of differentiation. Lab Invest 76:99-107
34. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K et al. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-10
35. Nickoloff BJ, Qin JZ, Chaturvedi V, Bacon P, Panella J, Denning MF (2002) Life and death signaling pathways contributing to skin cancer. J Investig Dermatol Symp Proc 7:27-35
36. Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F et al. (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 17:1475-86
37. Nischt R, Roop DR, Mehrel T, Yuspa SH, Rentrop M, Winter H et al. (1988) Aberrant expression during two-stage mouse skin carcinogenesis of a type I 47-kDa keratin, K13, normally associated with terminal differentiation of internal stratified epithelia. Mol Carcinog 1:96-108
38. Park K, Kuechle MK, Choe Y, Craik CS, Lawrence OT, Presland RB (2006) Expression and characterization of constitutively active human caspase-14. Biochem Biophys Res Commun 347:941-8
39. L transgene promotes malignant conversion of chemically initiated skin papillomas. Cancer Res 58:2111-6
40. Polakowska RR, Piacentini M, Bartlett R, Goldsmith LA, Haake AR (1994) Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev Dyn 199:176-88
41. Qin JZ, Xin H, Sitailo LA, Denning MF, Nickoloff BJ (2006) Enhanced killing of melanoma cells by simultaneously targeting Mcl-1 and NOXA. Cancer Res 66:9636-45
42. Raj D, Brash DE, Grossman D (2006) Keratinocyte apoptosis in epidermal development and disease. J Invest Dermatol 126:243-57
43. Raymond AA, Mechin MC, Nachat R, Toulza E, Tazi-Ahnini R, Serre G et al. (2007) Nine procaspases are expressed in normal human epidermis, but only caspase-14 is fully processed. Br J Dermatol 156:420-7
44. Rehemtulla A, Hamilton CA, Chinnaiyan AM, Dixit VM (1997) Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/ APO-1). J Biol Chem 272:25783-6
45. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ (2000) Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev 14:23-7
46. Schwarz A, Bhardwaj R, Aragane Y, Mahnke K, Riemann H, Metze D et al. (1995) Ultraviolet-B-induced apoptosis of keratinocytes: evidence for partial involvement of tumor necrosis factor-alpha in the formation of sunburn cells. J Invest Dermatol 104:922-7
47. Sheikh MS, Antinore MJ, Huang Y, Fornace AJ Jr (1998) Ultravioletirradiation-induced apoptosis is mediated via ligand independent activation of tumor necrosis factor receptor 1. Oncogene 17:2555-63
48. Sitailo LA, Tibudan SS, Denning MF (2002) Activation of caspase-9 is required for UV-induced apoptosis of human keratinocytes. J Biol Chem 277:19346-52
49. Sitailo LA, Tibudan SS, Denning MF (2006) The protein kinase Cδ catalytic fragment targets Mcl-1 for degradation to trigger apoptosis. J Biol Chem 281:29703-10
50. Thomkova H, Fujimoto W, Arata J (1999) Expression of the bcl-2 family of genes in the course of keratinocyte differentiation. Eur J Dermatol 9:191-6
51. Tibudan SS, Wang Y, Denning MF (2002) Activation of protein kinase C triggers irreversible cell cycle withdrawal in human keratinocytes. J Invest Dermatol 119:1282-9
52. Umeda J, Sano S, Kogawa K, Motoyama N, Yoshikawa K, Itami S et al. (2003) In vivo cooperation between Bcl-xL and the phosphoinositide 3-kinase-Akt signaling pathway for the protection of epidermal keratinocytes from apoptosis. FASEB J 17:610-20
53. Weil M, Raff MC, Braga VM (1999) Caspase activation in the terminal differentiation of human epidermal keratinocytes. Curr Biol 9:361-4
54. L, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19:1294-305
55. Zhang D, Li F, Weidner D, Mnjoyan ZH, Fujise K (2002) Physical and functional interaction between myeloid cell leukemia 1 protein (MCL1) and fortilin. The potential role of MCL1 as a fortilin chaperone. J Biol Chem 277:37430-8
56. Zhou P, Qian L, Kozopas KM, Craig RW (1997) Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 89:630-43
57. Ziegler A, Jonason AS, Leffell DJ, Simon JA, Sharma HW, Kimmelman J et al. (1994) Sunburn and p53 in the onset of skin cancer. Nature 372:773-6