家蚕核酸切除修复相关基因的克隆与功能分析
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摘要
DNA是生物体内携带遗传信息的重要物质,由于自身结构的特殊性和外界环境的影响,DNA在复制过程中必然会受到各种损伤从而需要细胞进行修复。研究DNA损伤修复机制,可以使人们更准确地理解生物稳定其遗传信息的机理,更深入地了解基因突变与进化的分子过程。核酸切除修复(NER)途径是生物体内DNA损伤的主要修复方式,Rad23基因、Rad4基因等是该NER途径中具有重要功能的修复因子。已有的研究发现Rad23基因在单细胞的低等生物(酵母)和高等哺乳生物细胞(人类)中对造成DNA损伤的紫外射线等外界因素的响应机制存在差异,家蚕在进化关系上是属于酵母和人类之间的高等生物,并且是鳞翅目的模式昆虫。家蚕遗传性状的长期研究积累和功能基因组学的研究结果为全面、准确的了解家蚕生物性状分子调控机制提供了基础。因此,研究家蚕BmRad23基因和BmRad4基因的结构与功能,探讨家蚕修复DNA损伤机理,对于阐明生物细胞NER等DNA损伤修复机理具有重要意义,对于辐射肓种、提高肿瘤放疗效果等也具有重要参考价值。
本论文在分析大量家蚕组织EST数据、基因组数据等的基础上,利用RT-PCR和RACE技术克隆了家蚕BmRad23基因和BmRad4基因,并对BmRad23基因的功能做了研究,具体研究结果如下：
(1)利用电子与实验克隆相结合的方法,成功克隆了家蚕BmRad23基因,BmRad23 cDNA全长序列由1304 bp碱基组成,5’UTR和3’UTR分别为165bp、164bp, ORF长975bp,编码324个氨基酸。利用生物信息学的方法解析氨基酸序列的结构与功能域信息,BmRad23氨基酸序列分别包含有UbL(1-74位氨基酸)、两个UBA(135-172、282-319位氨基酸)功能域以及一个XPC结合位点。
(2)构建了pET28a/BmRad23表达载体,在大肠杆菌中成功表达了BmRad23蛋白,纯化后的BmRad23蛋白作为抗原免疫新西兰兔,得到了特异性良好的多克隆抗体。
(3)通过Northern blot、Western blot技术对BmRad23基因组织表达特异性和时期表达特异性进行了分析,发现BmRad23基因在家蚕精、卵巢中表达量明显偏高,推测BmRad23在5龄后期幼虫精巢、卵巢中表达量的增加是由于生殖细胞减数分裂的原因造成的。此结果表明：BmRad23具有与其它物种Rad23在细胞减数分裂中发挥重要功能相似特性,在细胞减数分裂等组织细胞重要发肓时期发挥关键作用。此外,BmRad23在家蚕变态时期(预蛹期与蛹期)的丝腺中表达量增高,因BmRad23具有UBL/UBA功能域,在变态期组织蛋白质的降解过程中具有起到运送目的蛋白和控制蛋白降解过程的作用。因此BmRad23在家蚕变态期的组织细胞凋亡、蛋白质降解过程中也具有重要功能,是调节和控制蛋白降解的一个关键因素。
BmRad23在家蚕细胞受到具有遗传毒性的因素(如紫外辐射、NA-AAF)伤害时表达量会增高,而没有遗传毒性的热激反应并不会对BmRad23的表达量产生影响。此结果显示家蚕细胞也具有修复DNA损伤机制的NER途径,并且BmRad23基因功能具有一定的专一性。家蚕虽然是多细胞的高等生物,但其细胞在紫外线照射下BmRad23基因的应答反应是与单细胞的酵母相似,而与高等哺乳生物的人类细胞对紫外线照射下Rad23基因的应答反应有差异,推测家蚕细胞对于修复DNA损伤的机制更接近于单细胞的酵母。
(5)利用电子克隆和RACE方法首次克隆了家蚕Rad4基因,cDNA全长为3397bp,命名为BmRad4。BmRad4cDNA的5'UTR为52bp,3'UTR为459bp,ORF长2886bp,编码961个氨基酸,分子量为110kDa,等电点为9.03。生物信息学分析表明BmRad4氨基酸序列中含有典型的Rad4功能结构域和Rad4β发卡结构。
DNA is the important material which carrys the genetic information. Because of the harmful environmental element and its own special structure, DNA is often damaged during the duplicate pathway. Studing on DNA repair pathway can provide the detail knowledge about the mechanism of sustaining the genetic information in cells, as well as understand the molecular process of gene mutation and evolution. Nucleotide excision repair (NER) is the principal pathway of DNA repair and Rad23 and Rad4 gene are important factors in the NER pathway. However, the responsed mechanism of Rad23 gene to UV irradiation is different between yeast and human cells. Silkworm, Bombyx mori, is the model insect of Lepidoptera and its evolutional relationship is located between yeast and human. In addtition, the accumulation of the researched work in the filed of functional gene and genomics of silkworm can provide the foundation for basic biological study. Therefore, studing the structure and functions of BmRad23 and BmRad4, investigating the mechanism the DNA repair pathway in silkworm have the significance to interpret the detail mechanism of NER, as well as radiation breeding and other medical treatment.
In this article, we cloned Rad23 and Rad4 gene of B. mori successfully base on the information of genome database and other relevant database. What's more, we studied the detail function of BmRad23 gene. The research process and the main conclusions are present as follows:
1. The homologous gene of Rad23 was cloned from B. mori and designated as BmRad23. The full-length BmRad23 cDNA contained a 165-bp 5'-UTR (5'-untranslated region), a 3'-UTR of 164 bp. The open reading frame (ORF) of the BmRad23 cDNA is 975bp, encoding a deduced 324 amino acids with a calculated molecular weight of 36.13 kDa and an estimated pI of 4.50. The deduced amino acid sequence of the BmRad23 cDNA revealed several indispensable domains for the function of Rad23 protein family, such as one ubiquitin-like region (UbL) domain (residues 1-74), two ubiquitin associated (UBA) domains (residues 135-172 and residues 282-319), as well as a XPC-binding domain.
2. The BmRad23 protein was expressed in E.coil using pET28a vector. The Polyclonal antibody of BmRad23 was collected from blood of New Zealand rabbits which was treated with purified BmRad23 protein.
3. The northern blot and immunoblot analysis showed the BmRad23 gene was expressed in all examined organs, and elevated expression was observed in testis and ovary. The result suggesting that the BmRad23 functions in the mitosis like its homologous gene in other species. In addition, the enhanced expression of BmRad23 after day 3 of the wandering stage in the silk gland. From the present results it is suggested that BmRad23 functions in UPP during the silkworm metamorphosis and it is a key element in tar geting and carrying the substrates to proteasomes and controlling the protein degradation.
4. UV irradiation and treatment with chemical DNA damaging reagent increased the expression of BmRad23 but heat shock failed to induced the expression change of BmRad23 gene. The results suggesting that BmRad23 gene specially participate in the NER when the genetic material is damaged. Although silkworm is the high species, but the mechanism of BmRad23 is similar to its homologous gene in yeast but not in human. Those results may not only suggest that the silkworm has the NER pathway, but also BmRad23 gene has the special and vital function in this pathway.
5. The homologous gene of Rad4 was cloned from B. mori and designated as BmRad4. The full-length BmRad23 cDNA contained a 52 bp 5'-UTR (5'-untranslated region), a 3'-UTR of 459 bp. The ORF of BmRad4 is 2886bp and encoded a deduced 961 amino acids with a calculated molecular weight of 110kDa and an estimated pI of 9.30. The deduced amino acid sequence of the BmRad4 cDNA revealed a Rad4 domain which is indispensable domains for the function of Rad4 protein family.
本论文在分析大量家蚕组织EST数据、基因组数据等的基础上,利用RT-PCR和RACE技术克隆了家蚕BmRad23基因和BmRad4基因,并对BmRad23基因的功能做了研究,具体研究结果如下：
(1)利用电子与实验克隆相结合的方法,成功克隆了家蚕BmRad23基因,BmRad23 cDNA全长序列由1304 bp碱基组成,5’UTR和3’UTR分别为165bp、164bp, ORF长975bp,编码324个氨基酸。利用生物信息学的方法解析氨基酸序列的结构与功能域信息,BmRad23氨基酸序列分别包含有UbL(1-74位氨基酸)、两个UBA(135-172、282-319位氨基酸)功能域以及一个XPC结合位点。
(2)构建了pET28a/BmRad23表达载体,在大肠杆菌中成功表达了BmRad23蛋白,纯化后的BmRad23蛋白作为抗原免疫新西兰兔,得到了特异性良好的多克隆抗体。
(3)通过Northern blot、Western blot技术对BmRad23基因组织表达特异性和时期表达特异性进行了分析,发现BmRad23基因在家蚕精、卵巢中表达量明显偏高,推测BmRad23在5龄后期幼虫精巢、卵巢中表达量的增加是由于生殖细胞减数分裂的原因造成的。此结果表明：BmRad23具有与其它物种Rad23在细胞减数分裂中发挥重要功能相似特性,在细胞减数分裂等组织细胞重要发肓时期发挥关键作用。此外,BmRad23在家蚕变态时期(预蛹期与蛹期)的丝腺中表达量增高,因BmRad23具有UBL/UBA功能域,在变态期组织蛋白质的降解过程中具有起到运送目的蛋白和控制蛋白降解过程的作用。因此BmRad23在家蚕变态期的组织细胞凋亡、蛋白质降解过程中也具有重要功能,是调节和控制蛋白降解的一个关键因素。
BmRad23在家蚕细胞受到具有遗传毒性的因素(如紫外辐射、NA-AAF)伤害时表达量会增高,而没有遗传毒性的热激反应并不会对BmRad23的表达量产生影响。此结果显示家蚕细胞也具有修复DNA损伤机制的NER途径,并且BmRad23基因功能具有一定的专一性。家蚕虽然是多细胞的高等生物,但其细胞在紫外线照射下BmRad23基因的应答反应是与单细胞的酵母相似,而与高等哺乳生物的人类细胞对紫外线照射下Rad23基因的应答反应有差异,推测家蚕细胞对于修复DNA损伤的机制更接近于单细胞的酵母。
(5)利用电子克隆和RACE方法首次克隆了家蚕Rad4基因,cDNA全长为3397bp,命名为BmRad4。BmRad4cDNA的5'UTR为52bp,3'UTR为459bp,ORF长2886bp,编码961个氨基酸,分子量为110kDa,等电点为9.03。生物信息学分析表明BmRad4氨基酸序列中含有典型的Rad4功能结构域和Rad4β发卡结构。
DNA is the important material which carrys the genetic information. Because of the harmful environmental element and its own special structure, DNA is often damaged during the duplicate pathway. Studing on DNA repair pathway can provide the detail knowledge about the mechanism of sustaining the genetic information in cells, as well as understand the molecular process of gene mutation and evolution. Nucleotide excision repair (NER) is the principal pathway of DNA repair and Rad23 and Rad4 gene are important factors in the NER pathway. However, the responsed mechanism of Rad23 gene to UV irradiation is different between yeast and human cells. Silkworm, Bombyx mori, is the model insect of Lepidoptera and its evolutional relationship is located between yeast and human. In addtition, the accumulation of the researched work in the filed of functional gene and genomics of silkworm can provide the foundation for basic biological study. Therefore, studing the structure and functions of BmRad23 and BmRad4, investigating the mechanism the DNA repair pathway in silkworm have the significance to interpret the detail mechanism of NER, as well as radiation breeding and other medical treatment.
In this article, we cloned Rad23 and Rad4 gene of B. mori successfully base on the information of genome database and other relevant database. What's more, we studied the detail function of BmRad23 gene. The research process and the main conclusions are present as follows:
1. The homologous gene of Rad23 was cloned from B. mori and designated as BmRad23. The full-length BmRad23 cDNA contained a 165-bp 5'-UTR (5'-untranslated region), a 3'-UTR of 164 bp. The open reading frame (ORF) of the BmRad23 cDNA is 975bp, encoding a deduced 324 amino acids with a calculated molecular weight of 36.13 kDa and an estimated pI of 4.50. The deduced amino acid sequence of the BmRad23 cDNA revealed several indispensable domains for the function of Rad23 protein family, such as one ubiquitin-like region (UbL) domain (residues 1-74), two ubiquitin associated (UBA) domains (residues 135-172 and residues 282-319), as well as a XPC-binding domain.
2. The BmRad23 protein was expressed in E.coil using pET28a vector. The Polyclonal antibody of BmRad23 was collected from blood of New Zealand rabbits which was treated with purified BmRad23 protein.
3. The northern blot and immunoblot analysis showed the BmRad23 gene was expressed in all examined organs, and elevated expression was observed in testis and ovary. The result suggesting that the BmRad23 functions in the mitosis like its homologous gene in other species. In addition, the enhanced expression of BmRad23 after day 3 of the wandering stage in the silk gland. From the present results it is suggested that BmRad23 functions in UPP during the silkworm metamorphosis and it is a key element in tar geting and carrying the substrates to proteasomes and controlling the protein degradation.
4. UV irradiation and treatment with chemical DNA damaging reagent increased the expression of BmRad23 but heat shock failed to induced the expression change of BmRad23 gene. The results suggesting that BmRad23 gene specially participate in the NER when the genetic material is damaged. Although silkworm is the high species, but the mechanism of BmRad23 is similar to its homologous gene in yeast but not in human. Those results may not only suggest that the silkworm has the NER pathway, but also BmRad23 gene has the special and vital function in this pathway.
5. The homologous gene of Rad4 was cloned from B. mori and designated as BmRad4. The full-length BmRad23 cDNA contained a 52 bp 5'-UTR (5'-untranslated region), a 3'-UTR of 459 bp. The ORF of BmRad4 is 2886bp and encoded a deduced 961 amino acids with a calculated molecular weight of 110kDa and an estimated pI of 9.30. The deduced amino acid sequence of the BmRad4 cDNA revealed a Rad4 domain which is indispensable domains for the function of Rad4 protein family.
引文
1. Friedberg, E.C., Walker, G.C., and Siede, W., DNA repair and mutagenesis.1995, Washington DC:ASM Press.
2. Sancar, A., Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev,2003.103(6):2203-37.
3. Crowley, D.J., I. Boubriak, B.R. Berquist, et al., The uvrA, uvrB and uvrC genes are required for repair of ultraviolet light induced DNA photoproducts in Halobacterium sp. NRC-1. Saline Systems,2006.2:11.
4. Wood, R.D., DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie,1999.81(1-2):39-44.
5. Sancar, A., L.A. Lindsey-Boltz, K. Unsal-Kacmaz, et al., Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem,2004. 73:39-85.
6. Lehmann, A.R., DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie,2003.85(11):1101-11.
7. Mitchell, J.R., J.H. Hoeijmakers, and L.J. Niedernhofer, Divide and conquer:nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol,2003.15(2):232-40.
8. Hader, D.P. and R.P. Sinha, Solar ultraviolet radiation-induced DNA damage in aquatic organisms:potential environmental impact Mutat Res,2005.571(1-2):221-33.
9. Kotova, N., K. Hemminki, and D. Segerback, Urinary thymidine dimer as a marker of total body burden of UV-inflicted DNA damage in humans. Cancer Epidemiol Biomarkers Prev,2005.14(12):2868-72.
10. van Hoffen, A., A.S. Balajee, A.A. van Zeeland, et al., Nucleotide excision repair and its interplay with transcription. Toxicology,2003.193(1-2):79-90.
11. Gillet, L.C. and O.D. Scharer, Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev,2006.106(2):253-76.
12. Houtgraaf, J.H., J. Versmissen, and W.J. van der Giessen, A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med,2006.7(3): 165-72.
13. Prakash, S. and L. Prakash, Nucleotide excision repair in yeast Mutat Res,2000. 451(1-2):13-24.
14. Min, J.H. and N.P. Pavletich, Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature,2007.449(7162):570-5.
15. Guzder, S.N., P. Sung, L. Prakash, et al., Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. J Biol Chem,1998.273(47):31541-6.
16. Gillette, T.G., S. Yu, Z. Zhou, et al., Distinct functions of the ubiquitin-proteasome
pathway influence nucleotide excision repair. EMBO J,2006.25(11):2529-38.
17. van der Spek, P.J., C.E. Visser, F. Hanaoka, et al., Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23. Genomics,1996.31(1):20-7.
18. Hershko, A. and A. Ciechanover, The ubiquitin system. Annu Rev Biochem,1998.67: 425-79.
19. Sherman, M.Y. and A.L. Goldberg, Cellular defenses against unfolded proteins:a cell biologist thinks about neurodegenerative diseases. Neuron,2001.29(1):15-32.
20. Pickart, C.M., Mechanisms underlying ubiquitination. Annu Rev Biochem,2001.70: 503-33.
21. Ravid, T. and M. Hochstrasser, Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol,2008.9(9):679-90.
22. Pickart, C.M., Ubiquitin in chains. Trends Biochem Sci,2000.25(11):544-8.
23. Koegl, M., T. Hoppe, S. Schlenker, et al., A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell,1999.96(5):635-44.
24. Thrower, J.S., L. Hoffman, M. Rechsteiner, et al., Recognition of the polyubiquitin proteolytic signal. EMBO J,2000.19(1):94-102.
25. Stelter, P. and H.D. Ulrich, Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation Nature,2003.425(6954):188-91.
26. Hoege, C., B. Pfander, G.L. Moldovan, et al., RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature,2002.419(6903):135-41.
27. Nijman, S.M., M.P. Luna-Vargas, A. Velds, et al., A genomic and functional inventory of deubiquitinating enzymes. Cell,2005.123(5):773-86.
28. Glickman, M.H., D.M. Rubin, O. Coux, et al., A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell,1998.94(5):615-23.
29. Voges, D., P. Zwickl, and W. Baumeister, The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem,1999.68:1015-68.
30. Yao, T. and R.E. Cohen, A cryptic protease couples deubiquitination and degradation by the proteasome. Nature,2002.419(6905):403-7.
31. Verma, R., L. Aravind, R. Oania, et al., Role of Rpnll metalloprotease in deubiquitination and degradation by the 26S proteasome. Science,2002.298(5593): 611-5.
32. Schreiner, P., X. Chen, K. Husnjak, et al., Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interactioa Nature,2008.453(7194):548-52.
33. Husnjak, K., S. Elsasser, N. Zhang, et al., Proteasome subunit Rpnl3 is a novel ubiquitin receptor. Nature,2008.453(7194):481-8.
34. Verma, R., R. Oania, J. Graumann, et al., Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell,2004.118(1):99-110.
35. Clarke, D.J., G. Mondesert, M. Segal, et al., Dosage suppressors of pdsl implicate ubiquitin-associated domains in checkpoint control. Mol Cell Biol,2001.21(6): 1997-2007.
36. Biggins, S., I. Ivanovska, and M.D. Rose, Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. J Cell Biol,1996.133(6):1331-46.
37. Buchberger, A., From UBA to UBX:new words in the ubiquitin vocabulary. Trends Cell Biol,2002.12(5):216-21.
38. Watkins, J.F., P. Sung, L. Prakash, et al., The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol Cell Biol,1993.13(12):7757-65.
39. Lambertson, D., L. Chen, and K. Madura, Investigating the importance of proteasome-interaction for Rad23 function. Curr Genet,2003.42(4):199-208.
40. Elsasser, S., R.R. Gali, M. Schwickart, et al., Proteasome subunit Rpnl binds ubiquitin-like protein domains. Nat Cell Biol,2002.4(9):725-30.
41. Saeki, Y, T. Sone, A. Toh-e, et al., Identification of ubiquitin-like protein-binding subunits of the 26S proteasome. Biochem Biophys Res Commun,2002.296(4):813-9.
42. Rosenzweig, R., P.A. Osmulski, M. Gaczynska, et al., The central unit within the 19S regulatory particle of the proteasome. Nat Struct Mol Biol,2008.15(6):573-80.
43. Ishii, T., M. Funakoshi, and H. Kobayashi, Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway. EMBO J,2006.25(23): 5492-503.
44. Kim, I., K. Mi, and H. Rao, Multiple interactions of rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis. Mol Biol Cell,2004.15(7): 3357-65.
45. Goh, A.M., K.J. Walters, S. Elsasser, et al., Components of the ubiquitin-proteasome pathway compete for surfaces on Rad23 family proteins. BMC Biochem,2008.9:4.
46. Hofmann, K. and P. Bucher, The UBA domain:a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci,1996.21(5):172-3.
47. Wilkinson, C.R., M. Seeger, R. Hartmann-Petersen, et al., Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat Cell Biol,2001.3(10):939-43.
48. Mueller, T.D. and J. Feigon, Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J Mol Biol,2002.319(5):1243-55.
49. Dieckmann, T., E.S. Withers-Ward, M.A. Jarosinski, et al., Structure of a human DNA repair protein UBA domain that interacts with HIV-1 Vpr. Nat Struct Biol,1998.5(12): 1042-7.
50. Mueller, T.D., M. Kamionka, and J. Feigon, Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J Biol Chem,2004.279(12):11926-36.
51. Rao, H. and A. Sastry, Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J Biol Chem,2002.277(14):11691-5.
52. Chen, L., U. Shinde, T.G. Ortolan, et al., Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep, 2001.2(10):933-8.
53. Raasi, S., R. Varadan, D. Fushman, et al., Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol,2005.12(8):708-14.
54. Wang, Q., A.M. Goh, P.M. Howley, et al., Ubiquitin recognition by the DNA repair protein hHR23a Biochemistry,2003.42(46):13529-35.
55. Kang, Y., N. Zhang, D.M. Koepp, et al., Ubiquitin receptor proteins hHR23a and hPLIC2 interact J Mol Biol,2007.365(4):1093-101.
56. Walters, K.J., P.J. Lech, A.M. Goh, et al., DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a Proc Natl Acad Sci U S A,2003. 100(22):12694-9.
57. Miao, F., M. Bouziane, R. Dammann, et al.,3-Methyladenine-DNA glycosylase (MPG protein) interacts with human RAD23 proteins. J Biol Chem,2000.275(37):28433-8.
58. Withers-Ward, E.S., T.D. Mueller, I.S. Chen, et al., Biochemical and structural analysis of the interaction between the UBA(2) domain of the DNA repair protein HHR23A and HIV-1 Vpr. Biochemistry,2000.39(46):14103-12.
59. Jansen, L.E., R.A. Verhage, and J. Brouwer, Preferential binding of yeast Rad4. Rad23 complex to damaged DNA. J Biol Chem,1998.273(50):33111-4.
60. Ng, J.M., W. Vermeulen, GT. van der Horst, et al., A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev,2003.17(13):1630-45.
61. Kamionka, M. and J. Feigon, Structure of the XPC binding domain of hHR23A reveals hydrophobic patches for protein interaction. Protein Sci,2004.13(9):2370-7.
62. Lee, J.H., J.M. Choi, C. Lee, et al., Structure of a peptide:N-glycanase-Rad23 complex: insight into the deglycosylation for denatured glycoproteins. Proc Natl Acad Sci U S A, 2005.102(26):9144-9.
63. Ciechanover, A., H. Heller, S. Elias, et al., ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation. Proc Natl Acad Sci U S A, 1980.77(3):1365-8.
64. Matthews, W., J. Driscoll, K. Tanaka, et al., Involvement of the proteasome in various degradative processes in mammalian cells. Proc Natl Acad Sci U S A,1989.86(8): 2597-601.
65. Wilkinson, C.R., K. Ferrell, M. Penney, et al., Analysis of a gene encoding Rpn10 of the fission yeast proteasome reveals that the polyubiquitin-binding site of this subunit is essential when Rpnl2/Mts3 activity is compromised. J Biol Chem,2000.275(20): 15182-92.
66. Jelinsky, S.A., P. Estep, GM. Church, et al., Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells:Rpn4 links base excision repair with proteasomes. Mol Cell Biol,2000.20(21):8157-67.
67. Liu, Y., H. Dai, and W. Xiao, UAS(MAG1), a yeast cis-acting element that regulates the expression of MAGI, is located within the protein coding region of DDI1. Mol Gen Genet,1997.255(5):533-42.
68. Chen, L. and K. Madura, Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol,2002.22(13):4902-13.
69. Ortolan, T.G, P. Tongaonkar, D. Lambertson,-et al., The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat Cell Biol,2000.2(9):601-8.
70. Ortolan, T.G, L. Chen, P. Tongaonkar, et al., Rad23 stabilizes Rad4 from degradation by the Ub/proteasome pathway. Nucleic Acids Res,2004.32(22):6490-500.
71. Elsasser, S., D. Chandler-Militello, B. Muller, et al., Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J Biol Chem,2004.279(26): 26817-22.
72. Raasi, S. and C.M. Pickart, Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem,2003.278(11):8951-9.
73. Richly, H., M. Rape, S. Braun, et al., A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell,2005. 120(1):73-84.
74. Janse, D.M., B. Crosas, D. Finley, et al., Localization to the proteasome is sufficient for degradation. J Biol Chem,2004.279(20):21415-20.
75. Heessen, S., M.G. Masucci, and N.P. Dantuma, The UBA2 domain functions as an intrinsic stabilization signal that protects Rad23 from proteasomal degradation. Mol Cell, 2005.18(2):225-35.
76. Rothstein, R.J. and F. Sherman, Genes affecting the expression of cytochrome c in yeast: genetic mapping and genetic interactions. Genetics,1980.94(4):871-89.
77. Hoogstraten, D., S. Bergink, J.M. Ng, et al., Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J Cell Sci,2008.121(Pt 17): 2850-9.
78. Gong, F., D. Fahy, and M.J. Smerdon, Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol,2006.13(10):902-7.
79. McKnight, GL., T.S. Cardillo, and F. Sherman, An extensive deletion causing overproduction of yeast iso-2-cytochrome c. Cell,1981.25(2):409-19.
80. den Dulk, B., S.M. Sun, M. de Ruijter, et al., Rad33, a new factor involved in nucleotide excision repair in Saccharomyces cerevisiae. DNA Repair (Amst),2006.5(6):683-92.
81. Schauber, C., L. Chen, P. Tongaonkar, et al., Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature,1998.391(6668):715-8.
82. Russell, S.J., S.H. Reed, W. Huang, et al., The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell,1999.3(6):687-95.
83. Gillette, T.G, W. Huang, SX Russell, et al., The 19S complex of the proteasome regulates nucleotide excision repair in yeast Genes Dev,2001.15(12):1528-39.
84. Wang, Q.E., M.A. Wani, J. Chen, et al., Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol Carcinog, 2005.42(1):53-64.
85. Krogan, N.J., M.H. Lam, J. Fillingham, et al., Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell,2004.16(6):1027-34.
86. Masutani, C, K. Sugasawa, J. Yanagisawa, et al., Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J,1994.13(8):1831-43.
87. Goncu, E. and O. Parlak, Some autophagic and apoptotic features of programmed cell death in the anterior silk glands of the silkworm, Bombyx mori. Autophagy,2008.4(8): 1069-72.
88. Madura, K. and S. Prakash, Transcript levels of the Saccharomyes cerevisiae DNA repair gene RAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle. Nucleic Acids Res,1990.18(16):4737-42.
89. Shiba, H., D. Uchida, H. Kobayashi, et al., Involvement of cathepsin B-and L-like proteinases in silk gland histolysis during metamorphosis of Bombyx mori. Arch Biochem Biophys,2001.390(1):28-34.
90. Yang, X.J., Multisite protein modification and intramolecular signaling. Oncogene,2005. 24(10):1653-62.
91. Zakeri, Z.F., D. Quaglino, T. Latham, et al., Delayed internucleosomal DNA fragmentation in programmed cell death. FASEB J,1993.7(5):470-8.
92. Jones, H.E. and I.D. Bowen, Acid phosphatase activity in the larval salivary glands of developing Drosophila melanogaster. Cell Biol Int,1993.17(3):305-15.
93. Fuchs, R.P., J.F. Lefevre, J. Pouyet, et al., Comparative orientation of the fluorene residue in native DNA modified by N-acetoxy-N-2-acetylaminofluorene and two 7-halogeno derivatives. Biochemistry,1976.15(15):3347-51.
94. Evans, F.E., D.W. Miller, and F.A. Beland, Sensitivity of the conformation of deoxyguanosine to binding at the C-8 position by N-acetylated and unacetylated 2-aminofluorene. Carcinogenesis,1980.1(11):955-9.
2. Sancar, A., Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev,2003.103(6):2203-37.
3. Crowley, D.J., I. Boubriak, B.R. Berquist, et al., The uvrA, uvrB and uvrC genes are required for repair of ultraviolet light induced DNA photoproducts in Halobacterium sp. NRC-1. Saline Systems,2006.2:11.
4. Wood, R.D., DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie,1999.81(1-2):39-44.
5. Sancar, A., L.A. Lindsey-Boltz, K. Unsal-Kacmaz, et al., Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem,2004. 73:39-85.
6. Lehmann, A.R., DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie,2003.85(11):1101-11.
7. Mitchell, J.R., J.H. Hoeijmakers, and L.J. Niedernhofer, Divide and conquer:nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol,2003.15(2):232-40.
8. Hader, D.P. and R.P. Sinha, Solar ultraviolet radiation-induced DNA damage in aquatic organisms:potential environmental impact Mutat Res,2005.571(1-2):221-33.
9. Kotova, N., K. Hemminki, and D. Segerback, Urinary thymidine dimer as a marker of total body burden of UV-inflicted DNA damage in humans. Cancer Epidemiol Biomarkers Prev,2005.14(12):2868-72.
10. van Hoffen, A., A.S. Balajee, A.A. van Zeeland, et al., Nucleotide excision repair and its interplay with transcription. Toxicology,2003.193(1-2):79-90.
11. Gillet, L.C. and O.D. Scharer, Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev,2006.106(2):253-76.
12. Houtgraaf, J.H., J. Versmissen, and W.J. van der Giessen, A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med,2006.7(3): 165-72.
13. Prakash, S. and L. Prakash, Nucleotide excision repair in yeast Mutat Res,2000. 451(1-2):13-24.
14. Min, J.H. and N.P. Pavletich, Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature,2007.449(7162):570-5.
15. Guzder, S.N., P. Sung, L. Prakash, et al., Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. J Biol Chem,1998.273(47):31541-6.
16. Gillette, T.G., S. Yu, Z. Zhou, et al., Distinct functions of the ubiquitin-proteasome
pathway influence nucleotide excision repair. EMBO J,2006.25(11):2529-38.
17. van der Spek, P.J., C.E. Visser, F. Hanaoka, et al., Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23. Genomics,1996.31(1):20-7.
18. Hershko, A. and A. Ciechanover, The ubiquitin system. Annu Rev Biochem,1998.67: 425-79.
19. Sherman, M.Y. and A.L. Goldberg, Cellular defenses against unfolded proteins:a cell biologist thinks about neurodegenerative diseases. Neuron,2001.29(1):15-32.
20. Pickart, C.M., Mechanisms underlying ubiquitination. Annu Rev Biochem,2001.70: 503-33.
21. Ravid, T. and M. Hochstrasser, Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol,2008.9(9):679-90.
22. Pickart, C.M., Ubiquitin in chains. Trends Biochem Sci,2000.25(11):544-8.
23. Koegl, M., T. Hoppe, S. Schlenker, et al., A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell,1999.96(5):635-44.
24. Thrower, J.S., L. Hoffman, M. Rechsteiner, et al., Recognition of the polyubiquitin proteolytic signal. EMBO J,2000.19(1):94-102.
25. Stelter, P. and H.D. Ulrich, Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation Nature,2003.425(6954):188-91.
26. Hoege, C., B. Pfander, G.L. Moldovan, et al., RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature,2002.419(6903):135-41.
27. Nijman, S.M., M.P. Luna-Vargas, A. Velds, et al., A genomic and functional inventory of deubiquitinating enzymes. Cell,2005.123(5):773-86.
28. Glickman, M.H., D.M. Rubin, O. Coux, et al., A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell,1998.94(5):615-23.
29. Voges, D., P. Zwickl, and W. Baumeister, The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem,1999.68:1015-68.
30. Yao, T. and R.E. Cohen, A cryptic protease couples deubiquitination and degradation by the proteasome. Nature,2002.419(6905):403-7.
31. Verma, R., L. Aravind, R. Oania, et al., Role of Rpnll metalloprotease in deubiquitination and degradation by the 26S proteasome. Science,2002.298(5593): 611-5.
32. Schreiner, P., X. Chen, K. Husnjak, et al., Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interactioa Nature,2008.453(7194):548-52.
33. Husnjak, K., S. Elsasser, N. Zhang, et al., Proteasome subunit Rpnl3 is a novel ubiquitin receptor. Nature,2008.453(7194):481-8.
34. Verma, R., R. Oania, J. Graumann, et al., Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell,2004.118(1):99-110.
35. Clarke, D.J., G. Mondesert, M. Segal, et al., Dosage suppressors of pdsl implicate ubiquitin-associated domains in checkpoint control. Mol Cell Biol,2001.21(6): 1997-2007.
36. Biggins, S., I. Ivanovska, and M.D. Rose, Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. J Cell Biol,1996.133(6):1331-46.
37. Buchberger, A., From UBA to UBX:new words in the ubiquitin vocabulary. Trends Cell Biol,2002.12(5):216-21.
38. Watkins, J.F., P. Sung, L. Prakash, et al., The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol Cell Biol,1993.13(12):7757-65.
39. Lambertson, D., L. Chen, and K. Madura, Investigating the importance of proteasome-interaction for Rad23 function. Curr Genet,2003.42(4):199-208.
40. Elsasser, S., R.R. Gali, M. Schwickart, et al., Proteasome subunit Rpnl binds ubiquitin-like protein domains. Nat Cell Biol,2002.4(9):725-30.
41. Saeki, Y, T. Sone, A. Toh-e, et al., Identification of ubiquitin-like protein-binding subunits of the 26S proteasome. Biochem Biophys Res Commun,2002.296(4):813-9.
42. Rosenzweig, R., P.A. Osmulski, M. Gaczynska, et al., The central unit within the 19S regulatory particle of the proteasome. Nat Struct Mol Biol,2008.15(6):573-80.
43. Ishii, T., M. Funakoshi, and H. Kobayashi, Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway. EMBO J,2006.25(23): 5492-503.
44. Kim, I., K. Mi, and H. Rao, Multiple interactions of rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis. Mol Biol Cell,2004.15(7): 3357-65.
45. Goh, A.M., K.J. Walters, S. Elsasser, et al., Components of the ubiquitin-proteasome pathway compete for surfaces on Rad23 family proteins. BMC Biochem,2008.9:4.
46. Hofmann, K. and P. Bucher, The UBA domain:a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci,1996.21(5):172-3.
47. Wilkinson, C.R., M. Seeger, R. Hartmann-Petersen, et al., Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat Cell Biol,2001.3(10):939-43.
48. Mueller, T.D. and J. Feigon, Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J Mol Biol,2002.319(5):1243-55.
49. Dieckmann, T., E.S. Withers-Ward, M.A. Jarosinski, et al., Structure of a human DNA repair protein UBA domain that interacts with HIV-1 Vpr. Nat Struct Biol,1998.5(12): 1042-7.
50. Mueller, T.D., M. Kamionka, and J. Feigon, Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J Biol Chem,2004.279(12):11926-36.
51. Rao, H. and A. Sastry, Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J Biol Chem,2002.277(14):11691-5.
52. Chen, L., U. Shinde, T.G. Ortolan, et al., Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep, 2001.2(10):933-8.
53. Raasi, S., R. Varadan, D. Fushman, et al., Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol,2005.12(8):708-14.
54. Wang, Q., A.M. Goh, P.M. Howley, et al., Ubiquitin recognition by the DNA repair protein hHR23a Biochemistry,2003.42(46):13529-35.
55. Kang, Y., N. Zhang, D.M. Koepp, et al., Ubiquitin receptor proteins hHR23a and hPLIC2 interact J Mol Biol,2007.365(4):1093-101.
56. Walters, K.J., P.J. Lech, A.M. Goh, et al., DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a Proc Natl Acad Sci U S A,2003. 100(22):12694-9.
57. Miao, F., M. Bouziane, R. Dammann, et al.,3-Methyladenine-DNA glycosylase (MPG protein) interacts with human RAD23 proteins. J Biol Chem,2000.275(37):28433-8.
58. Withers-Ward, E.S., T.D. Mueller, I.S. Chen, et al., Biochemical and structural analysis of the interaction between the UBA(2) domain of the DNA repair protein HHR23A and HIV-1 Vpr. Biochemistry,2000.39(46):14103-12.
59. Jansen, L.E., R.A. Verhage, and J. Brouwer, Preferential binding of yeast Rad4. Rad23 complex to damaged DNA. J Biol Chem,1998.273(50):33111-4.
60. Ng, J.M., W. Vermeulen, GT. van der Horst, et al., A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev,2003.17(13):1630-45.
61. Kamionka, M. and J. Feigon, Structure of the XPC binding domain of hHR23A reveals hydrophobic patches for protein interaction. Protein Sci,2004.13(9):2370-7.
62. Lee, J.H., J.M. Choi, C. Lee, et al., Structure of a peptide:N-glycanase-Rad23 complex: insight into the deglycosylation for denatured glycoproteins. Proc Natl Acad Sci U S A, 2005.102(26):9144-9.
63. Ciechanover, A., H. Heller, S. Elias, et al., ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation. Proc Natl Acad Sci U S A, 1980.77(3):1365-8.
64. Matthews, W., J. Driscoll, K. Tanaka, et al., Involvement of the proteasome in various degradative processes in mammalian cells. Proc Natl Acad Sci U S A,1989.86(8): 2597-601.
65. Wilkinson, C.R., K. Ferrell, M. Penney, et al., Analysis of a gene encoding Rpn10 of the fission yeast proteasome reveals that the polyubiquitin-binding site of this subunit is essential when Rpnl2/Mts3 activity is compromised. J Biol Chem,2000.275(20): 15182-92.
66. Jelinsky, S.A., P. Estep, GM. Church, et al., Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells:Rpn4 links base excision repair with proteasomes. Mol Cell Biol,2000.20(21):8157-67.
67. Liu, Y., H. Dai, and W. Xiao, UAS(MAG1), a yeast cis-acting element that regulates the expression of MAGI, is located within the protein coding region of DDI1. Mol Gen Genet,1997.255(5):533-42.
68. Chen, L. and K. Madura, Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol,2002.22(13):4902-13.
69. Ortolan, T.G, P. Tongaonkar, D. Lambertson,-et al., The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat Cell Biol,2000.2(9):601-8.
70. Ortolan, T.G, L. Chen, P. Tongaonkar, et al., Rad23 stabilizes Rad4 from degradation by the Ub/proteasome pathway. Nucleic Acids Res,2004.32(22):6490-500.
71. Elsasser, S., D. Chandler-Militello, B. Muller, et al., Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J Biol Chem,2004.279(26): 26817-22.
72. Raasi, S. and C.M. Pickart, Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem,2003.278(11):8951-9.
73. Richly, H., M. Rape, S. Braun, et al., A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell,2005. 120(1):73-84.
74. Janse, D.M., B. Crosas, D. Finley, et al., Localization to the proteasome is sufficient for degradation. J Biol Chem,2004.279(20):21415-20.
75. Heessen, S., M.G. Masucci, and N.P. Dantuma, The UBA2 domain functions as an intrinsic stabilization signal that protects Rad23 from proteasomal degradation. Mol Cell, 2005.18(2):225-35.
76. Rothstein, R.J. and F. Sherman, Genes affecting the expression of cytochrome c in yeast: genetic mapping and genetic interactions. Genetics,1980.94(4):871-89.
77. Hoogstraten, D., S. Bergink, J.M. Ng, et al., Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J Cell Sci,2008.121(Pt 17): 2850-9.
78. Gong, F., D. Fahy, and M.J. Smerdon, Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol,2006.13(10):902-7.
79. McKnight, GL., T.S. Cardillo, and F. Sherman, An extensive deletion causing overproduction of yeast iso-2-cytochrome c. Cell,1981.25(2):409-19.
80. den Dulk, B., S.M. Sun, M. de Ruijter, et al., Rad33, a new factor involved in nucleotide excision repair in Saccharomyces cerevisiae. DNA Repair (Amst),2006.5(6):683-92.
81. Schauber, C., L. Chen, P. Tongaonkar, et al., Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature,1998.391(6668):715-8.
82. Russell, S.J., S.H. Reed, W. Huang, et al., The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell,1999.3(6):687-95.
83. Gillette, T.G, W. Huang, SX Russell, et al., The 19S complex of the proteasome regulates nucleotide excision repair in yeast Genes Dev,2001.15(12):1528-39.
84. Wang, Q.E., M.A. Wani, J. Chen, et al., Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol Carcinog, 2005.42(1):53-64.
85. Krogan, N.J., M.H. Lam, J. Fillingham, et al., Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell,2004.16(6):1027-34.
86. Masutani, C, K. Sugasawa, J. Yanagisawa, et al., Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J,1994.13(8):1831-43.
87. Goncu, E. and O. Parlak, Some autophagic and apoptotic features of programmed cell death in the anterior silk glands of the silkworm, Bombyx mori. Autophagy,2008.4(8): 1069-72.
88. Madura, K. and S. Prakash, Transcript levels of the Saccharomyes cerevisiae DNA repair gene RAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle. Nucleic Acids Res,1990.18(16):4737-42.
89. Shiba, H., D. Uchida, H. Kobayashi, et al., Involvement of cathepsin B-and L-like proteinases in silk gland histolysis during metamorphosis of Bombyx mori. Arch Biochem Biophys,2001.390(1):28-34.
90. Yang, X.J., Multisite protein modification and intramolecular signaling. Oncogene,2005. 24(10):1653-62.
91. Zakeri, Z.F., D. Quaglino, T. Latham, et al., Delayed internucleosomal DNA fragmentation in programmed cell death. FASEB J,1993.7(5):470-8.
92. Jones, H.E. and I.D. Bowen, Acid phosphatase activity in the larval salivary glands of developing Drosophila melanogaster. Cell Biol Int,1993.17(3):305-15.
93. Fuchs, R.P., J.F. Lefevre, J. Pouyet, et al., Comparative orientation of the fluorene residue in native DNA modified by N-acetoxy-N-2-acetylaminofluorene and two 7-halogeno derivatives. Biochemistry,1976.15(15):3347-51.
94. Evans, F.E., D.W. Miller, and F.A. Beland, Sensitivity of the conformation of deoxyguanosine to binding at the C-8 position by N-acetylated and unacetylated 2-aminofluorene. Carcinogenesis,1980.1(11):955-9.