PCNA ubiquitination-independent activation of polymerase η during somatic hypermutation and DNA damage tolerance

► Polη can be activated dependent and independent of PCNA-Ub during both SHM and DDT. ► PCNA-Ub and Polη are necessary, but not essential, for efficient DDT of UV-lesions. ► PCNA-Ub/ Polh independent DDT of UV-lesions involves Rev1 and Rev3. The generation of high affinity antibodies in B cells crit...

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Vydané v:	DNA repair Ročník 10; číslo 10; s. 1051 - 1059
Hlavní autori:	Krijger, Peter H.L., van den Berk, Paul C.M., Wit, Niek, Langerak, Petra, Jansen, Jacob G., Reynaud, Claude-Agnès, de Wind, Niels, Jacobs, Heinz
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	Amsterdam Elsevier B.V 10.10.2011 Elsevier
Predmet:	Animals B-Lymphocytes - cytology B-Lymphocytes - metabolism Bacteriology Biological and medical sciences DNA Damage - genetics DNA damage tolerance DNA Repair - genetics DNA-Directed DNA Polymerase - metabolism Enzyme Activation Fundamental and applied biological sciences. Psychology Growth, nutrition, cell differenciation Lysine - genetics Mice Mice, Inbred C57BL Microbiology Molecular and cellular biology Molecular genetics Mutagenesis Mutagenesis. Repair Mutation PCNA Polη Proliferating Cell Nuclear Antigen - genetics Proliferating Cell Nuclear Antigen - metabolism Somatic hypermutation Somatic Hypermutation, Immunoglobulin - genetics Translesion synthesis Ubiquitination Ultraviolet Rays DNA damage tolerance Somatic hypermutation Ubiquitination PCNA Polη Translesion synthesis Immunoglobulins DNA Activation Lesion Repair
ISSN:	1568-7864, 1568-7856, 1568-7856
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Abstract	► Polη can be activated dependent and independent of PCNA-Ub during both SHM and DDT. ► PCNA-Ub and Polη are necessary, but not essential, for efficient DDT of UV-lesions. ► PCNA-Ub/ Polh independent DDT of UV-lesions involves Rev1 and Rev3. The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase η (Polη)-deficient, PCNA K164R-mutant, and PCNA K164R;Polη double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Polη. In addition, upon exposure to various DNA damaging agents, PCNA K164R mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNA K164R;Polη double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Polη during SHM and DNA damage tolerance.
AbstractList	The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase η (Polη)-deficient, PCNA(K164R)-mutant, and PCNA(K164R);Polη double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Polη. In addition, upon exposure to various DNA damaging agents, PCNA(K164R) mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNA(K164R);Polη double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Polη during SHM and DNA damage tolerance.The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase η (Polη)-deficient, PCNA(K164R)-mutant, and PCNA(K164R);Polη double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Polη. In addition, upon exposure to various DNA damaging agents, PCNA(K164R) mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNA(K164R);Polη double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Polη during SHM and DNA damage tolerance. The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase eta (Pol eta )-deficient, PCNAK164R-mutant, and PCNAK164R; Pol eta double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Pol eta . In addition, upon exposure to various DNA damaging agents, PCNAK164R mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNAK164R; Pol eta double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Pol eta during SHM and DNA damage tolerance. ► Polη can be activated dependent and independent of PCNA-Ub during both SHM and DDT. ► PCNA-Ub and Polη are necessary, but not essential, for efficient DDT of UV-lesions. ► PCNA-Ub/ Polh independent DDT of UV-lesions involves Rev1 and Rev3. The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase η (Polη)-deficient, PCNA K164R-mutant, and PCNA K164R;Polη double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Polη. In addition, upon exposure to various DNA damaging agents, PCNA K164R mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNA K164R;Polη double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Polη during SHM and DNA damage tolerance. The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into immunoglobulin genes during somatic hypermutation (SHM). The majority of mutations at A/T base pairs during SHM require ubiquitination of PCNA at lysine 164 (PCNA-Ub), which activates TLS polymerases. By comparing the mutation spectra in B cells of WT, TLS polymerase η (Polη)-deficient, PCNA(K164R)-mutant, and PCNA(K164R);Polη double-mutant mice, we now find that most PCNA-Ub-independent A/T mutagenesis during SHM is mediated by Polη. In addition, upon exposure to various DNA damaging agents, PCNA(K164R) mutant cells display strongly impaired recruitment of TLS polymerases, reduced daughter strand maturation and hypersensitivity. Interestingly, compared to the single mutants, PCNA(K164R);Polη double-mutant cells are dramatically delayed in S phase progression and far more prone to cell death following UV exposure. Taken together, these data support the existence of PCNA ubiquitination-dependent and -independent activation pathways of Polη during SHM and DNA damage tolerance.
Author	van den Berk, Paul C.M. Jacobs, Heinz Langerak, Petra Reynaud, Claude-Agnès Wit, Niek Jansen, Jacob G. Krijger, Peter H.L. de Wind, Niels
Author_xml	– sequence: 1 givenname: Peter H.L. surname: Krijger fullname: Krijger, Peter H.L. organization: Division of Immunology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Netherlands – sequence: 2 givenname: Paul C.M. surname: van den Berk fullname: van den Berk, Paul C.M. organization: Division of Immunology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Netherlands – sequence: 3 givenname: Niek surname: Wit fullname: Wit, Niek organization: Division of Immunology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Netherlands – sequence: 4 givenname: Petra surname: Langerak fullname: Langerak, Petra organization: Division of Immunology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Netherlands – sequence: 5 givenname: Jacob G. surname: Jansen fullname: Jansen, Jacob G. organization: Department of Toxicogenetics, Leiden University Medical Center, 2300 RC Leiden, The Netherlands – sequence: 6 givenname: Claude-Agnès surname: Reynaud fullname: Reynaud, Claude-Agnès organization: Institut National de la Santé et de la Recherche Médicale U783 ‘Développement du système immunitaire’, Université Paris Descartes, Faculté de Médecine, Site Necker-Enfants Malades, Paris, France – sequence: 7 givenname: Niels surname: de Wind fullname: de Wind, Niels organization: Department of Toxicogenetics, Leiden University Medical Center, 2300 RC Leiden, The Netherlands – sequence: 8 givenname: Heinz surname: Jacobs fullname: Jacobs, Heinz email: h.jacobs@nki.nl organization: Division of Immunology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Netherlands
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Keywords	DNA damage tolerance Somatic hypermutation Ubiquitination PCNA Polη Translesion synthesis Immunoglobulins DNA Activation Lesion Repair
Language	English
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Snippet	► Polη can be activated dependent and independent of PCNA-Ub during both SHM and DDT. ► PCNA-Ub and Polη are necessary, but not essential, for efficient DDT of... The generation of high affinity antibodies in B cells critically depends on translesion synthesis (TLS) polymerases that introduce mutations into...
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SubjectTerms	Animals B-Lymphocytes - cytology B-Lymphocytes - metabolism Bacteriology Biological and medical sciences DNA Damage - genetics DNA damage tolerance DNA Repair - genetics DNA-Directed DNA Polymerase - metabolism Enzyme Activation Fundamental and applied biological sciences. Psychology Growth, nutrition, cell differenciation Lysine - genetics Mice Mice, Inbred C57BL Microbiology Molecular and cellular biology Molecular genetics Mutagenesis Mutagenesis. Repair Mutation PCNA Polη Proliferating Cell Nuclear Antigen - genetics Proliferating Cell Nuclear Antigen - metabolism Somatic hypermutation Somatic Hypermutation, Immunoglobulin - genetics Translesion synthesis Ubiquitination Ultraviolet Rays
Title	PCNA ubiquitination-independent activation of polymerase η during somatic hypermutation and DNA damage tolerance
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