Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage

Emma Bolderson, Joshua T. Burgess, Jun Li, Neha S. Gandhi, Didier Boucher, Laura V. Croft, Samuel Beard, Jennifer J. Plowman, Amila Suraweera, Mark N. Adams, Ali Naqi, Shu Dong Zhang, David A. Sinclair, Kenneth J. O’Byrne, Derek J. Richard

    Research output: Contribution to journalArticle

    Abstract

    The DNA repair capacity of human cells declines with age, in a process that is not clearly understood. Mutation of the nuclear envelope protein barrier-to-autointegration factor 1 (Banf1) has previously been shown to cause a human progeroid disorder, Néstor–Guillermo progeria syndrome (NGPS). The underlying links between Banf1, DNA repair and the ageing process are unknown. Here, we report that Banf1 controls the DNA damage response to oxidative stress via regulation of poly [ADP-ribose] polymerase 1 (PARP1). Specifically, oxidative lesions promote direct binding of Banf1 to PARP1, a critical NAD+-dependent DNA repair protein, leading to inhibition of PARP1 auto-ADP-ribosylation and defective repair of oxidative lesions, in cells with increased Banf1. Consistent with this, cells from patients with NGPS have defective PARP1 activity and impaired repair of oxidative lesions. These data support a model whereby Banf1 is crucial to reset oxidative-stress-induced PARP1 activity. Together, these data offer insight into Banf1-regulated, PARP1-directed repair of oxidative lesions.

    LanguageEnglish
    Article number5501
    JournalNature Communications
    Volume10
    Issue number1
    DOIs
    Publication statusPublished - 3 Dec 2019

    Fingerprint

    ribose
    adenosine diphosphate
    Poly(ADP-ribose) Polymerases
    DNA Damage
    Repair
    deoxyribonucleic acid
    damage
    DNA
    lesions
    Progeria
    DNA Repair
    Oxidative stress
    Oxidative Stress
    proteins
    Nuclear Envelope
    Nuclear Proteins
    NAD
    Adenosine Diphosphate
    mutations
    Poly (ADP-Ribose) Polymerase-1

    Cite this

    Bolderson, Emma ; Burgess, Joshua T. ; Li, Jun ; Gandhi, Neha S. ; Boucher, Didier ; Croft, Laura V. ; Beard, Samuel ; Plowman, Jennifer J. ; Suraweera, Amila ; Adams, Mark N. ; Naqi, Ali ; Zhang, Shu Dong ; Sinclair, David A. ; O’Byrne, Kenneth J. ; Richard, Derek J. / Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage. In: Nature Communications. 2019 ; Vol. 10, No. 1.
    @article{b60ec6c276dc404dad9cf858ded6b010,
    title = "Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage",
    abstract = "The DNA repair capacity of human cells declines with age, in a process that is not clearly understood. Mutation of the nuclear envelope protein barrier-to-autointegration factor 1 (Banf1) has previously been shown to cause a human progeroid disorder, N{\'e}stor–Guillermo progeria syndrome (NGPS). The underlying links between Banf1, DNA repair and the ageing process are unknown. Here, we report that Banf1 controls the DNA damage response to oxidative stress via regulation of poly [ADP-ribose] polymerase 1 (PARP1). Specifically, oxidative lesions promote direct binding of Banf1 to PARP1, a critical NAD+-dependent DNA repair protein, leading to inhibition of PARP1 auto-ADP-ribosylation and defective repair of oxidative lesions, in cells with increased Banf1. Consistent with this, cells from patients with NGPS have defective PARP1 activity and impaired repair of oxidative lesions. These data support a model whereby Banf1 is crucial to reset oxidative-stress-induced PARP1 activity. Together, these data offer insight into Banf1-regulated, PARP1-directed repair of oxidative lesions.",
    author = "Emma Bolderson and Burgess, {Joshua T.} and Jun Li and Gandhi, {Neha S.} and Didier Boucher and Croft, {Laura V.} and Samuel Beard and Plowman, {Jennifer J.} and Amila Suraweera and Adams, {Mark N.} and Ali Naqi and Zhang, {Shu Dong} and Sinclair, {David A.} and O’Byrne, {Kenneth J.} and Richard, {Derek J.}",
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    Bolderson, E, Burgess, JT, Li, J, Gandhi, NS, Boucher, D, Croft, LV, Beard, S, Plowman, JJ, Suraweera, A, Adams, MN, Naqi, A, Zhang, SD, Sinclair, DA, O’Byrne, KJ & Richard, DJ 2019, 'Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage', Nature Communications, vol. 10, no. 1, 5501. https://doi.org/10.1038/s41467-019-13167-5

    Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage. / Bolderson, Emma; Burgess, Joshua T.; Li, Jun; Gandhi, Neha S.; Boucher, Didier; Croft, Laura V.; Beard, Samuel; Plowman, Jennifer J.; Suraweera, Amila; Adams, Mark N.; Naqi, Ali; Zhang, Shu Dong; Sinclair, David A.; O’Byrne, Kenneth J.; Richard, Derek J.

    In: Nature Communications, Vol. 10, No. 1, 5501, 03.12.2019.

    Research output: Contribution to journalArticle

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    T1 - Barrier-to-autointegration factor 1 (Banf1) regulates poly [ADP-ribose] polymerase 1 (PARP1) activity following oxidative DNA damage

    AU - Bolderson, Emma

    AU - Burgess, Joshua T.

    AU - Li, Jun

    AU - Gandhi, Neha S.

    AU - Boucher, Didier

    AU - Croft, Laura V.

    AU - Beard, Samuel

    AU - Plowman, Jennifer J.

    AU - Suraweera, Amila

    AU - Adams, Mark N.

    AU - Naqi, Ali

    AU - Zhang, Shu Dong

    AU - Sinclair, David A.

    AU - O’Byrne, Kenneth J.

    AU - Richard, Derek J.

    PY - 2019/12/3

    Y1 - 2019/12/3

    N2 - The DNA repair capacity of human cells declines with age, in a process that is not clearly understood. Mutation of the nuclear envelope protein barrier-to-autointegration factor 1 (Banf1) has previously been shown to cause a human progeroid disorder, Néstor–Guillermo progeria syndrome (NGPS). The underlying links between Banf1, DNA repair and the ageing process are unknown. Here, we report that Banf1 controls the DNA damage response to oxidative stress via regulation of poly [ADP-ribose] polymerase 1 (PARP1). Specifically, oxidative lesions promote direct binding of Banf1 to PARP1, a critical NAD+-dependent DNA repair protein, leading to inhibition of PARP1 auto-ADP-ribosylation and defective repair of oxidative lesions, in cells with increased Banf1. Consistent with this, cells from patients with NGPS have defective PARP1 activity and impaired repair of oxidative lesions. These data support a model whereby Banf1 is crucial to reset oxidative-stress-induced PARP1 activity. Together, these data offer insight into Banf1-regulated, PARP1-directed repair of oxidative lesions.

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