From DNA repair to proteome protection: New molecular insights for preventing non-melanoma skin cancers and skin aging

Journal of Drugs in Dermatology

Volumn 13, Issue 3, 2014, Pages 274-281

  Emanuele, Enzo ^a   Spencer, James M ^b   Braun, Martin ^c  

^a Living Research sas   (Italy)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BIOLOGICAL MARKER; NUCLEOTIDE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN P53; PROTEOME; PYRIMIDINE DIMER; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CANCER MORTALITY; CANCER PREVENTION; CUTANEOUS MELANOMA; CUTANEOUS PARAMETERS; CYCLOADDITION; DISULFIDE BOND; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENVIRONMENTAL STRESS; EXCISION REPAIR; GENOMIC INSTABILITY; HUMAN; MORBIDITY; NON MELANOMA SKIN CANCER; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN CARBONYLATION; RADIATION EXPOSURE; RADIATION PROTECTION; RADIOSENSITIVITY; SKIN CARCINOGENESIS; SURVIVAL TIME; TELOMERE SHORTENING; ULTRAVIOLET B RADIATION; METABOLISM; SKIN NEOPLASMS; ULTRAVIOLET RADIATION;

DNA DAMAGE; DNA REPAIR; HUMANS; OXIDATIVE STRESS; PROTEOME; REACTIVE OXYGEN SPECIES; SKIN AGING; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 84896336815     PISSN: 15459616     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (103)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009; 59:225-249.
2. Chen AC, Halliday GM, Damian DL. Non-melanoma skin cancer: carcinogenesis and chemoprevention. Pathology. 2013; 45:331-341.
3. Guy GP, Ekwueme DU. Years of potential life lost and indirect costs of melanoma and non-melanoma skin cancer: a systematic review of the literature. Pharmacoeconomics. 2011;29: 863-874.
4. Marghoob AA. Skin cancers and their etiologies. Semin Cutan Med Surg.2011; 30(4 Suppl):S1-5.
5. Saladi RN, Persaud AN. The causes of skin cancer: a comprehensive review.Drugs Today (Barc). 2005; 41:37-53. (Pubitemid 40393035)
6. Rigel DS. Cutaneous ultraviolet exposure and its relationship to the development of skin cancer. J Am Acad Dermatol. 2008; 58(5 Suppl 2):S129-132. (Pubitemid 351506511)
7. Narayanan DL, Saladi RN, Fox JL. Ultraviolet radiation and skin cancer. Int J Dermatol. 2010; 49:978-986.
8. D'Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. UV Radiation and the skin. Int J Mol Sci. 2013; 14:12222-12248.
9. Yanofsky VR, Mercer SE, Phelps RG. Histopathological variants of cutaneous squamous cell carcinoma: a review. J Skin Cancer. 2011;2011:210813.
10. Patel RV, Frankel A, Goldenberg G. An update on nonmelanoma skin cancer. J Clin Aesthet Dermatol. 2011; 4:20-7.
11. de Gruijl FR, van Kranen HJ, Mullenders LH. UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J Photochem Photobiol B. 2001; 63:19-27. (Pubitemid 33040719)
12. Cleaver JE, Crowley E. UV damage, DNA repair and skin carcinogenesis. Front Biosci. 2002; 7:d1024-1043.
13. Mabruk MJ, Toh LK, Murphy M, Leader M, Kay E, Murphy GM. Investigation of the effect of UV irradiation on DNA damage: comparison between skin cancer patients and normal volunteers. J Cutan Pathol.2009; 36:760-765.
14. Sinha RP, Häder DP. UV-induced DNA damage and repair: a review. Photochem Photobiol Sci. 2002; 1:225-236. (Pubitemid 37069733)
15. Rastogi RP, Richa, Kumar A, Tyagi MB, Sinha RP. Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids. 2010; 2010:592980.
16. Rass K, Reichrath J. UV damage and DNA repair in malignant melanoma and nonmelanoma skin cancer. Adv Exp Med Biol. 2008; 624:162-178.
17. Tsaalbi-Shtylik A, Verspuy JW, Jansen JG, Rebel H, Carlée LM, van der Valk MA, Jonkers J, de Gruijl FR, de Wind N. Error-prone translesion replication of damaged DNA suppresses skin carcinogenesis by controlling inflammatory hyperplasia. Proc Natl Acad Sci. 2009; 106:21836-21841.
18. Cadet J, Sage E, Douki T. Ultraviolet radiation-mediated damage to cellular DNA. Mutat Res. 2005; 571:3-17. (Pubitemid 40313428)
19. Pattison DI, Davies MJ. Actions of ultraviolet light on cellular structures. EXS.2006; 96:131-157.
20. Scharffetter-Kochanek K, Wlaschek M, Brenneisen P, Schauen M, Blaudschun R, Wenk J. UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biol Chem. 1997; 378:1247-1257. (Pubitemid 27507540)
21. Hanson KM, Clegg RM. Observation and quantification of ultraviolet-induced reactive oxygen species in ex vivo human skin. Photochem Photobiol. 2002; 76:57-63.
22. Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, Tsuru K, Horikawa T. UV-induced skin damage. Toxicology. 2003; 189:21-39. (Pubitemid 36725021)
23. Svobodova A, Walterova D, Vostalova J. Ultraviolet light induced alteration to the skin. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub.2006; 150:25-38.
24. Hattori Y, Nishigori C, Tanaka T, Uchida K, Nikaido O, Osawa T, Hiai H, Imamura S, Toyokuni S. 8-hydroxy-2′-deoxyguanosine is increased in epidermal cells of hairless mice after chronic ultraviolet B exposure. J Invest Dermatol.1996; 107:733-737. (Pubitemid 26371090)
25. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol. 2010; 38:96-109.
26. Kumar A, Pant MC, Singh HS, Khandelwal S. Assessment of the redox profile and oxidative DNA damage (8-OHdG) in squamous cell carcinoma of head and neck. J Cancer Res Ther. 2012; 8:254-259.
27. Daly MJ. Death by protein damage in irradiated cells. DNA Repair (Amst).2012; 11:12-21.
28. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature. 2001; 411:366-374. (Pubitemid 32467046)
29. Moraes MC, Neto JB, Menck CF. DNA repair mechanisms protect our genome from carcinogenesis. Front Biosci (Landmark Ed). 2012; 17:1362-1388.
30. Kuper J, Kisker C. Damage recognition in nucleotide excision DNA repair. Curr Opin Struct Biol. 2012; 22:88-93.
31. Slade D, Radman M. Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev. 2011; 75:133-91.
32. Krisko A, Radman M. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol. 2013; 5(7).
33. Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL. Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One. 2010; 5:e12570.
34. Krisko A, Radman M. Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci U S A. 2010; 107:14373-14377.
35. Suzuki YJ, Carini M, Butterfield DA. Protein carbonylation. Antioxid Redox Signal.2010; 12:323-325.
36. Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med. 2006; 10:389-406. (Pubitemid 44870187)
37. Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases. Trends Mol Med. 2003; 9:169-176. (Pubitemid 36626706)
38. Webb KM, DiRuggiero J. Role of Mn2+ and compatible solutes in the radiation resistance of thermophilic bacteria and archaea. Archaea. 2012; 2012:845756.
39. Vink AA, Roza L. Biological consequences of cyclobutane pyrimidine dimers. J Photochem Photobiol B. 2001; 65:101-104. (Pubitemid 34110723)
40. Matsumura Y, Ananthaswamy HN. Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol. 2004; 195:298-308. (Pubitemid 38338650)
41. Yamamoto J, Nishiguchi K, Manabe K, Masutani C, Hanaoka F, Iwai S. Photosensitized [2 + 2] cycloaddition of N-acetylated cytosine affords stereoselective formation of cyclobutane pyrimidine dimer. Nucleic Acids Res. 2011; 39:1165-1175.
42. You YH, Szabó PE, Pfeifer GP. Cyclobutane pyrimidine dimers form preferentially at the major p53 mutational hotspot in UVB-induced mouse skin tumors. Carcinogenesis. 2000; 21:2113-7.
43. You YH, Lee DH, Yoon JH, Nakajima S, Yasui A, Pfeifer GP. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J Biol Chem. 2001; 276:44688-44694.
44. Rünger TM, Farahvash B, Hatvani Z, Rees A. Comparison of DNA damage responses following equimutagenic doses of UVA and UVB: a less effective cell cycle arrest with UVA may render UVA-induced pyrimidine dimers more mutagenic than UVB-induced ones. Photochem Photobiol Sci. 2012; 11:207-215.
45. Cortat B, Garcia CC, Quinet A, Schuch AP, de Lima-Bessa KM, Menck CF. The relative roles of DNA damage induced by UVA irradiation in human cells. Photochem Photobiol Sci. 2013; 12:1483-1495.
46. Mouret S, Baudouin C, Charveron M, Favier A, Cadet J, Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc Natl Acad Sci. 2006; 103:13765-13770. (Pubitemid 44413982)
47. Segerbäck D, Strozyk M, Snellman E, Hemminki K. Repair of UV dimers in skin DNA of patients with basal cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2008; 17:2388-2392.
48. Rochette PJ, Brash DE. Human telomeres are hypersensitive to UV-induced DNA Damage and refractory to repair. PLoS Genet. 2010; 6:e1000926.
49. Buckingham EM, Klingelhutz AJ. The role of telomeres in the ageing of human skin. Exp Dermatol. 2011; 20:297-302.
50. Yarosh DB. DNA repair, immunosuppression, and skin cancer. Cutis. 2004; 74(5 Suppl):10-13. (Pubitemid 39612327)
51. Gerlini G, Romagnoli P, Pimpinelli N. Skin cancer and immunosuppression. Crit Rev Oncol Hematol. 2005; 56:127-136. (Pubitemid 41278651)
52. Herman S, Rogers HD, Ratner D. Immunosuppression and squamous cell carcinoma: a focus on solid organ transplant recipients. Skinmed. 2007; 6:234-238.
53. Kobayashi N, Katsumi S, Imoto K, Nakagawa A, Miyagawa S, Furumura M, Mori T. Quantitation and visualization of ultraviolet-induced DNA damage using specific antibodies: application to pigment cell biology. Pigment Cell Res.2001; 14:94-102. (Pubitemid 32258346)
54. Berardesca E, Bertona M, Altabas K, Altabas V, Emanuele E. Reduced ultraviolet-induced DNA damage and apoptosis in human skin with topical application of a photolyase-containing DNA repair enzyme cream: clues to skin cancer prevention. Mol Med Rep. 2012; 5:570-574.
55. DeBoyes T, Kouba D, Ozog D, Fincher E, Moy L, Iwata K, Moy R. Reduced number of actinic keratoses with topical application of DNA repair enzyme creams. J Drugs Dermatol. 2010; 9:1519-1521.
56. Yokoo S, Furumoto K, Hiyama E, Miwa N. Slow-down of age-dependent telomere shortening is executed in human skin keratinocytes by hormesis-like-effects of trace hydrogen peroxide or by antioxidative effects of pro-vitamin C in common concurrently with reduction of intracellular oxidative stress. J Cell Biochem. 2004; 93:588-597. (Pubitemid 44264193)
57. Indo HP, Davidson M, Yen HC, Suenaga S, Tomita K, Nishii T, Higuchi M, Koga Y, Ozawa T, Majima HJ. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion. 2007; 7:106-118. (Pubitemid 46351959)
58. Cadet J, Wagner JR. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol. 2013; 5(2).
59. Cadet J, Douki T, Gasparutto D, Ravanat JL. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat Res. 2003; 531:5-23. (Pubitemid 37456721)
60. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-2′- deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2009; 27:120-139.
61. Kasai H, Crain PF, Kuchino Y, Nishimura S, Ootsuyama A, Tanooka H. Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis. 1986; 7:1849-1851.
62. Sunaga N, Kohno T, Shinmura K, Saitoh T, Matsuda T, Saito R, Yokota J. OGG1 protein suppresses G:C>T:A mutation in a shuttle vector containing 8-hydroxyguanine in human cells. Carcinogenesis. 2001; 22:1355-1362. (Pubitemid 32898690)
63. Kato M, Iida M, Goto Y, Kondo T, Yajima I. Sunlight exposure-mediated DNA damage in young adults. Cancer Epidemiol Biomarkers Prev. 2011; 20:1622-1628.
64. Kvam E, Tyrrell RM. Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis. 1997; 18:2379-2384. (Pubitemid 28134653)
65. Liardet S, Scaletta C, Panizzon R, Hohlfeld P, Laurent-Applegate L. Protection against pyrimidine dimers, p53, and 8-hydroxy-2′-deoxyguanosine expression in ultraviolet-irradiated human skin by sunscreens: difference between UVB + UVA and UVB alone sunscreens. J Invest Dermatol. 2001; 117:1437-1441. (Pubitemid 34032770)
66. Nishigori C, Arima Y, Matsumura Y, Matsui M, Miyachi Y. Impaired removal of 8-hydroxydeoxyguanosine induced by UVB radiation in naevoid basal cell carcinoma syndrome cells. Br J Dermatol. 2005; 153 Suppl 2:52-56.
67. Orimo H, Tokura Y, Hino R, Kasai H. Formation of 8-hydroxy-2′- deoxyguanosine in the DNA of cultured human keratinocytes by clinically used doses of narrowband and broadband ultraviolet B and psoralen plus ultraviolet A. Cancer Sci. 2006; 97:99-105. (Pubitemid 43379476)
68. Murtas D, Piras F, Minerba L, Ugalde J, Floris C, Maxia C, Demurtas P, Perra MT, Sirigu P. Nuclear 8-hydroxy-2′-deoxyguanosine as survival biomarker in patients with cutaneous melanoma. Oncol Rep. 2010; 23:329-335.
69. Kim YJ, Wilson DM 3rd. Overview of base excision repair biochemistry. Curr Mol Pharmacol. 2012; 5:3-13.
70. Kozmin SG, Jinks-Robertson S. The mechanism of nucleotide excision repair-mediated UV-induced mutagenesis in nonproliferating cells. Genetics. 2013; 193:803-817.
71. Moriwaki S. Hereditary disorders with defective repair of UV-induced DNA damage. Jpn Clin Med. 2013; 4:29-35.
72. Lehmann AR, McGibbon D, Stefanini M. Xeroderma pigmentosum. Orphanet J Rare Dis. 2011; 6:70.
73. Fassihi H. Spotlight on 'xeroderma pigmentosum'. Photochem Photobiol Sci.2013; 12:78-84.
74. Yarosh DB, Kibitel JT, Green LA, Spinowitz A. Enhanced unscheduled DNA synthesis in UV-irradiated human skin explants treated with T4N5 liposomes. J Invest Dermatol. 1991; 97:147-150.
75. Yarosh D, Klein J, Kibitel J, Alas L, O'Connor A, Cummings B, Grob D, Gerstein D, Gilchrest BA, Ichihashi M, Ogoshi M, Ueda M, Fernandez V, Chadwick C, Potten CS, Proby CM, Young AR, Hawk JL. Enzyme therapy of xeroderma pigmentosum: safety and efficacy testing of T4N5 liposome lotion containing a prokaryotic DNA repair enzyme. Photodermatol Photoimmunol Photomed. 1996; 12:122-130. (Pubitemid 26385214)
76. Yarosh D, Klein J, O'Connor A, Hawk J, Rafal E, Wolf P. Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: a randomised study. Xeroderma Pigmentosum Study Group. Lancet.2001; 357:926-929. (Pubitemid 32247282)
77. Yarosh DB, O'Connor A, Alas L, Potten C, Wolf P. Photoprotection by topical DNA repair enzymes: molecular correlates of clinical studies. Photochem Photobiol. 1999; 69:136-140. (Pubitemid 129606897)
78. Yarosh DB. Enhanced DNA repair of cyclobutane pyrimidine dimers changes the biological response to UV-B radiation. Mutat Res. 2002; 509:221-226. (Pubitemid 35341463)
79. Kraemer KH, DiGiovanna JJ. Topical enzyme therapy for skin diseases? J Am Acad Dermatol. 2002; 46:463-466. (Pubitemid 34225420)
80. Thiagarajan V, Villette S, Espagne A, Eker AP, Brettel K, Byrdin M. DNA repair by photolyase: a novel substrate with low background absorption around 265 nm for transient absorption studies in the UV. Biochemistry. 2010; 49:297-303.
81. Aubert C, Mathis P, Eker AP, Brettel K. Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans. Proc Natl Acad Sci. 1999; 96:5423-5427. (Pubitemid 29234633)
82. Piersen CE, Prince MA, Augustine ML, Dodson ML, Lloyd RS. Purification and cloning of Micrococcus luteus ultraviolet endonuclease, an N-glycosylase/abasic lyase that proceeds via an imino enzyme-DNA intermediate. J Biol Chem. 1995; 270:23475-23484.
83. Shiota S, Nakayama H. UV endonuclease of Micrococcus luteus, a cyclobutane pyrimidine dimer-DNA glycosylase/abasic lyase: cloning and characterization of the gene. Proc Natl Acad Sci. 1997; 94:593-598.
84. Mees A, Klar T, Gnau P, Hennecke U, Eker AP, Carell T, Essen LO. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science. 2004; 306:1789-1793. (Pubitemid 39601399)
85. Su YH, Lee YL, Chen SF, Lee YP, Hsieh YH, Tsai JH, Hsu JL, Tian WT, Huang W. Essential role of β-human 8-oxoguanine DNA glycosylase 1 in mitochondrial oxidative DNA repair. Environ Mol Mutagen. 2013; 54:54-64.
86. Javeri A, Huang XX, Bernerd F, Mason RS, Halliday GM. Human 8-oxoguanine-DNA glycosylase 1 protein and gene are expressed more abundantly in the superficial than basal layer of human epidermis. DNA Repair (Amst).2008; 7:1542-1550.
87. Stege H, Roza L, Vink AA, Grewe M, Ruzicka T, Grether-Beck S, Krutmann J. Enzyme plus light therapy to repair DNA damage in ultraviolet-B-irradiated human skin. Proc Natl Acad Sci. 2000; 97:1790-1795. (Pubitemid 30118521)
88. Decome L, De Méo M, Geffard A, Doucet O, Duménil G, Botta A. Evaluation of photolyase (Photosome) repair activity in human keratinocytes after a single dose of ultraviolet B irradiation using the comet assay. J Photochem Photobiol B. 2005; 79:101-108. (Pubitemid 40614102)
89. Emanuele E, Altabas V, Altabas K, Berardesca E. Topical application of preparations containing DNA repair enzymes prevents ultraviolet-induced telomere shortening and c-FOS proto-oncogene hyperexpression in human skin: an experimental pilot study. J Drugs Dermatol. 2013; 12:1017-1021.
90. Wulff BC, Schick JS, Thomas-Ahner JM, Kusewitt DF, Yarosh DB, Oberyszyn TM. Topical treatment with OGG1 enzyme affects UVB-induced skin carcinogenesis. Photochem Photobiol. 2008; 84:317-321. (Pubitemid 351421383)
91. Hu ML, Tappel AL. Potentiation of oxidative damage to proteins by ultraviolet-A and protection by antioxidants. Photochem Photobiol. 1992; 56:357-363.
92. Schweikert K, Gafner F, Dell'Acqua G. A bioactive complex to protect proteins from UV-induced oxidation in human epidermis. Int J Cosmet Sci. 2010; 32:29-34.
93. Stadtman ER. Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci. 2001; 928:22-38. (Pubitemid 32386064)
94. Minton KW. DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol Microbiol. 1994; 13:9-15.
95. Varghese AJ, Day RS 3rd. Excision of cytosine-thymine adduct from the DNA of ultraviolet-irradiated Micrococcus radiodurans. Photochem Photobiol. 1970; 11:511-517.
96. Kaushik JK, Bhat R. Why is trehalose an exceptional protein stabilizer? An analysis of the thermal stability of proteins in the presence of the compatible osmolyte trehalose. J Biol Chem. 2003; 278:26458-26465. (Pubitemid 36876786)
97. Lins RD, Pereira CS, Hünenberger PH. Trehalose-protein interaction in aqueous solution. Proteins. 2004; 55:177-186. (Pubitemid 38292845)
98. Jain NK, Roy I. Effect of trehalose on protein structure. Protein Sci. 2009; 18:24-36.
99. Jain NK, Roy I. Trehalose and protein stability. Curr Protoc Protein Sci. 2010; Chapter 4:Unit 4.9.
100. Muller HK, Woods GM. Ultraviolet radiation effects on the proteome of skin cells. Adv Exp Med Biol. 2013; 990:111-119.
101. Perluigi M, Di Domenico F, Blarzino C, Foppoli C, Cini C, Giorgi A, Grillo C, De Marco F, Butterfield DA, Schininà ME, Coccia R. Effects of UVB-induced oxidative stress on protein expression and specific protein oxidation in normal human epithelial keratinocytes: a proteomic approach. Proteome Sci. 2010; 8:13.
102. Bulteau AL, Moreau M, Nizard C, Friguet B. Proteasome and photoaging: the effects of UV irradiation. Ann N Y Acad Sci. 2007; 1100:280-290. (Pubitemid 47092663)
103. Almond JB, Cohen GM. The proteasome: a novel target for cancer chemotherapy. Leukemia. 2002; 16:433-43. (Pubitemid 34449723)