α II Spectrin Interacts with Specific Proteins in the Nucleus: Relevance to Fanconi Anemia.

Blood ◽  
2005 ◽  
Vol 106 (11) ◽  
pp. 184-184
Author(s):  
Muriel W. Lambert ◽  
Laura W. McMahon ◽  
Deepa M. Sridharan

Abstract Fanconi anemia (FA) is a genetic disorder characterized by bone marrow failure, a predisposition to cancer, congenital abnormalities and a cellular hypersensitivity to DNA interstrand cross-linking agents. We have previously shown that in FA cells there is a deficiency in the structural protein nonerythroid spectrin (α SpII∑*) and that this deficiency correlates with a defect in ability to repair DNA interstrand cross-links. In order to get a better understanding of the exact role that α IISp∑* plays in the repair of cross-links and the repair defect in FA, whether it may have additional and potentially critical functions in the nucleus, and the processes that might be most severely affected by a defect in this protein, studies were undertaken to determine precisely what other proteins α IISp∑* interacts with in the nucleus. Co-immunoprecipitation experiments were carried out in which chromatin-associated proteins from normal human lymphoblastoid cells that co-immunoprecipitated (Co-IP) with α II spectrin were examined and identified. These proteins could be grouped into five categories: structural proteins, proteins involved in DNA repair, chromatin remodeling proteins, FA proteins, and transcription and RNA processing proteins. The structural proteins that Co-IP with α II spectrin were: lamin A, actin, protein 4.1B, β IV spectrin, and emerin. This indicates that α II spectrin interacts with proteins in the nucleus that play a role in nuclear cytoskeleton stability, chromatin organization and transcription. A number of proteins that Co-IP with α II spectrin were involved in DNA repair: DNA interstrand cross-link repair (XPF), homologous recombinational repair (HRR) and non-homologous end joining (NHEJ) (MRE11, RAD 50, RAD 51, XRCC2, Ku 70, Ku 80), and nucleotide excision repair (NER) (hHR23B, XPA, RPA, XPB, XPG, XPF, ERCC1). Since both NER and HRR are thought to be involved in repair of DNA interstrand cross-links, association of α II spectrin with XPF and HRR proteins supports our hypothesis that α II spectrin acts as a scaffold for recruitment and alignment of repair proteins at sites of DNA damage. It may act as a scaffolding for proteins involved in more than one repair pathway. α II spectrin also associated with chromatin remodeling proteins: BRG1, hBRM and CSB. This indicates that, like actin, it not only plays a role in nuclear cytoskeletal structure but also in chromatin remodeling as well. In agreement with our previous findings, α II spectrin Co-IP with FANCA and FANCC. The present study showed that it also Co-IP with FANCD2, FANCG and FANCF. There was also a significantly greater association of several FANC proteins, such as FANCA, to α II spectrin after cross-link damage to the cells than in undamaged cells. This further indicates that there is an important interaction between these FANC proteins and α II spectrin during the repair process. Several proteins involved in transcription and RNA processing (p40 and hnRNP A2/B1) also Co-IP with aII spectrin. Again, like actin, aII spectrin in the nucleus may also be involved in these processes. These results indicate that aII spectrin may have multiple roles in the nucleus and, in addition to DNA repair, may be involved in processes such as nuclear cytoskeleton stability, chromatin remodeling, transcription and RNA processing. A deficiency in aII spectrin in FA cells could thus affect multiple pathways where interaction of aII spectrin with functionally important proteins is critical; loss of this interaction in FA cells may explain some of the diverse clinical characteristics of this disorder.

Cancers ◽  
2020 ◽  
Vol 12 (9) ◽  
pp. 2684 ◽  
Author(s):  
Giacomo Milletti ◽  
Luisa Strocchio ◽  
Daria Pagliara ◽  
Katia Girardi ◽  
Roberto Carta ◽  
...  

Fanconi anemia (FA) is a clinically and genetically heterogeneous disorder characterized by the variable presence of congenital somatic abnormalities, bone marrow failure (BMF), and a predisposition to develop cancer. Monoallelic germline mutations in at least five genes involved in the FA pathway are associated with the development of sporadic hematological and solid malignancies. The key function of the FA pathway is to orchestrate proteins involved in the repair of interstrand cross-links (ICLs), to prevent genomic instability and replication stress. Recently, many studies have highlighted the importance of FA genes in noncanonical pathways, such as mitochondria homeostasis, inflammation, and virophagy, which act, in some cases, independently of DNA repair processes. Thus, primary defects in DNA repair mechanisms of FA patients are typically exacerbated by an impairment of other cytoprotective pathways that contribute to the multifaceted clinical phenotype of this disease. In this review, we summarize recent advances in the understanding of the pathogenesis of FA, with a focus on the cytosolic noncanonical roles of FA genes, discussing how they may contribute to cancer development, thus suggesting opportunities to envisage novel therapeutic approaches.


Blood ◽  
2007 ◽  
Vol 110 (11) ◽  
pp. 838-838
Author(s):  
Deepa M. Sridharan ◽  
Laura W. McMahon ◽  
Muriel W. Lambert

Abstract Fanconi anemia (FA) is a genetic disorder characterized by bone marrow failure, a predisposition to cancer, congenital abnormalities and a cellular hypersensitivity to DNA interstrand cross-linking agents, which correlates with a defect in ability to repair interstrand cross-links. We have previously shown that in FA cells there is a deficiency in the structural protein nonerythroid a spectrin (aSpII), which is involved in repair of DNA interstrand cross-links and binds to cross-linked DNA. aSpII co-localizes in damage-induced nuclear foci with FANCA and the cross-link repair protein, XPF, after normal human cells are damaged with a DNA interstrand cross-linking agent. The present study was undertaken in order to get a better understanding of the relationship between aSpII and the FA proteins and the functional importance of this relationship in the repair of DNA interstrand cross-links and the repair defect in FA cells. Immunofluorescence microscopy was carried out to determine whether, after damage, additional FA proteins co-localize with aSpII in nuclear foci and whether the interaction between these proteins is enhanced after cross-link damage. The results show that in normal human cells another FA core complex protein, FANCF, co-localizes with aSpII in nuclear foci after cells are damaged with a DNA interstrand cross-linking agent, 8-methylpsoralen plus UVA light (8-MOP). Time course measurements show that these FANCF/aSpII foci are first visible between 6–8 hours after damage and the number of these foci peaks at 16 hours. By 24 hours after exposure, foci are no longer observed. This is the same time frame previously observed for formation and co-localization of FANCA and XPF foci with aSpII. In contrast, in FA-A cells, which are not deficient in FANCF, very few damage induced FANCF or aSpII foci are observed. In corrected FA-A cells, expressing the FANCA cDNA, FANCF and aSpII again co-localize in discrete foci in the nucleus after damage. Co-localization of FANCF in damage-induced foci with aSpII correlates with enhanced binding of FANCF to aSpII after damage. Co-immunoprecipitation studies show that after normal cells are damaged with 8-MOP there is enhanced binding of FANCF, as well as FANCA, to aSpII in the damaged cells compared to this binding in undamaged cells. This further indicates that there is an important interaction between FANCF, FANCA and aSpII during the repair process. These results support our model that aSpII plays a pivotal role in the recruitment of FA and DNA repair proteins to sites of damage where it acts as a scaffold aiding in their interactions with each other or with damaged DNA, thus enhancing the DNA repair process. In FA cells, where there is a deficiency in aSpII, this recruitment is defective as are the interactions of proteins at these sites. This correlates with the reduced repair of interstrand cross-links in FA cells. Thus a deficiency in the interaction of these FA proteins with aSpII may be an important factor in the defective DNA repair pathway in FA cells.


2019 ◽  
Vol 116 (7) ◽  
pp. 2561-2570 ◽  
Author(s):  
Samuel B. Sondalle ◽  
Simonne Longerich ◽  
Lisa M. Ogawa ◽  
Patrick Sung ◽  
Susan J. Baserga

Fanconi anemia (FA) is a disease of DNA repair characterized by bone marrow failure and a reduced ability to remove DNA interstrand cross-links. Here, we provide evidence that the FA protein FANCI also functions in ribosome biogenesis, the process of making ribosomes that initiates in the nucleolus. We show that FANCI localizes to the nucleolus and is functionally and physically tied to the transcription of pre-ribosomal RNA (pre-rRNA) and to large ribosomal subunit (LSU) pre-rRNA processing independent of FANCD2. While FANCI is known to be monoubiquitinated when activated for DNA repair, we find that it is predominantly in the deubiquitinated state in the nucleolus, requiring the nucleoplasmic deubiquitinase (DUB) USP1 and the nucleolar DUB USP36. Our model suggests a possible dual pathophysiology for FA that includes defects in DNA repair and in ribosome biogenesis.


2019 ◽  
Vol 39 (15) ◽  
Author(s):  
Karissa L. Paquin ◽  
Nicholas E. Mamrak ◽  
Jada L. Garzon ◽  
Juan A. Cantres-Velez ◽  
Paul A. Azzinaro ◽  
...  

ABSTRACT Fanconi anemia (FA) is an inherited disease characterized by bone marrow failure and increased cancer risk. FA is caused by mutation of any 1 of 22 genes, and the FA proteins function cooperatively to repair DNA interstrand cross-links (ICLs). A central step in the activation of the FA pathway is the monoubiquitination of the FANCD2 and FANCI proteins, which occurs within chromatin. How FANCD2 and FANCI are anchored to chromatin remains unknown. In this study, we identify and characterize a FANCD2 histone-binding domain (HBD) and embedded methyl-lysine-binding domain (MBD) and demonstrate binding specificity for H4K20me2. Disruption of the HBD/MBD compromises FANCD2 chromatin binding and nuclear focus formation and its ability to promote error-free DNA interstrand cross-link repair, leading to increased error-prone repair and genome instability. Our study functionally describes the first FA protein chromatin reader domain and establishes an important link between this human genetic disease and chromatin plasticity.


1997 ◽  
Vol 17 (12) ◽  
pp. 6822-6830 ◽  
Author(s):  
T Bessho ◽  
D Mu ◽  
A Sancar

Most DNA repair mechanisms rely on the redundant information inherent to the duplex to remove damaged nucleotides and replace them with normal ones, using the complementary strand as a template. Interstrand cross-links pose a unique challenge to the DNA repair machinery because both strands are damaged. To study the repair of interstrand cross-links by mammalian cells, we tested the activities of cell extracts of wild-type or excision repair-defective rodent cell lines and of purified human excision nuclease on a duplex with a site-specific cross-link. We found that in contrast to monoadducts, which are removed by dual incisions bracketing the lesion, the cross-link causes dual incisions, both 5' to the cross-link in one of the two strands. The net result is the generation of a 22- to 28-nucleotide-long gap immediately 5' to the cross-link. This gap may act as a recombinogenic signal to initiate cross-link removal.


2020 ◽  
Vol 64 (5) ◽  
pp. 807-817 ◽  
Author(s):  
Landing Li ◽  
Winnie Tan ◽  
Andrew J. Deans

Abstract The Fanconi anemia (FA) pathway coordinates a faithful repair mechanism for DNA damage that blocks DNA replication, such as interstrand cross-links. A key step in the FA pathway is the conjugation of ubiquitin on to FANCD2 and FANCI, which is facilitated by a large E3 ubiquitin ligase complex called the FA core complex. Mutations in FANCD2, FANCI or FA core complex components cause the FA bone marrow failure syndrome. Despite the importance of these proteins to DNA repair and human disease, our molecular understanding of the FA pathway has been limited due to a deficit in structural studies. With the recent development in cryo-electron microscopy (EM), significant advances have been made in structural characterization of these proteins in the last 6 months. These structures, combined with new biochemical studies, now provide a more detailed understanding of how FANCD2 and FANCI are monoubiquitinated and how DNA repair may occur. In this review, we summarize these recent advances in the structural and molecular understanding of these key components in the FA pathway, compare the activation steps of FANCD2 and FANCI monoubiquitination and suggest molecular steps that are likely to be involved in regulating its activity.


Science ◽  
2014 ◽  
Vol 346 (6213) ◽  
pp. 1127-1130 ◽  
Author(s):  
Renjing Wang ◽  
Nicole S. Persky ◽  
Barney Yoo ◽  
Ouathek Ouerfelli ◽  
Agata Smogorzewska ◽  
...  

DNA interstrand cross-links (ICLs) are highly toxic lesions associated with cancer and degenerative diseases. ICLs can be repaired by the Fanconi anemia (FA) pathway and through FA-independent processes involving the FAN1 nuclease. In this work, FAN1-DNA crystal structures and biochemical data reveal that human FAN1 cleaves DNA successively at every third nucleotide. In vitro, this exonuclease mechanism allows FAN1 to excise an ICL from one strand through flanking incisions. DNA access requires a 5′-terminal phosphate anchor at a nick or a 1- or 2-nucleotide flap and is augmented by a 3′ flap, suggesting that FAN1 action is coupled to DNA synthesis or recombination. FAN1’s mechanism of ICL excision is well suited for processing other localized DNA adducts as well.


Blood ◽  
2011 ◽  
Vol 117 (19) ◽  
pp. 5078-5087 ◽  
Author(s):  
Stacy A. Williams ◽  
Simonne Longerich ◽  
Patrick Sung ◽  
Cyrus Vaziri ◽  
Gary M. Kupfer

Abstract Fanconi anemia (FA) is a rare genetic disorder characterized by bone marrow failure, congenital abnormalities, and an increased risk for cancer and leukemia. Components of the FA-BRCA pathway are thought to function in the repair of DNA interstrand cross-links. Central to this pathway is the monoubiquitylation and chromatin localization of 2 FA proteins, FA complementation group D2 (FANCD2) and FANCI. In the present study, we show that RAD18 binds FANCD2 and is required for efficient monoubiquitylation and chromatin localization of both FANCD2 and FANCI. Human RAD18-knockout cells display increased sensitivity to mitomycin C and a delay in FANCD2 foci formation compared with their wild-type counterparts. In addition, RAD18-knockout cells display a unique lack of FANCD2 and FANCI localization to chromatin in exponentially growing cells. FANCD2 ubiquitylation is normal in cells containing a ubiquitylation-resistant form of proliferating cell nuclear antigen, and chromatin loading of FA core complex proteins appears normal in RAD18-knockout cells. Mutation of the RING domain of RAD18 ablates the interaction with and chromatin loading of FANCD2. These data suggest a key role for the E3 ligase activity of RAD18 in the recruitment of FANCD2 and FANCI to chromatin and the events leading to their ubiquitylation during S phase.


Blood ◽  
2008 ◽  
Vol 112 (11) ◽  
pp. 1041-1041
Author(s):  
Joel A Lefferts ◽  
Chuan Wang ◽  
Melissa Baralt ◽  
Muriel W Lambert

Abstract Fanconi anemia (FA) is a genetic disorder characterized by bone marrow failure, a predisposition to cancer, congenital abnormalities and a cellular hypersensitivity to DNA interstrand cross-linking agents. This hypersensitivity in FA cells correlates with a defect in ability to repair interstrand cross-links. We have shown that the structural protein, nonerythroid a spectrin (aIISp), plays an important role in the repair of DNA interstrand cross-links and that there is a deficiency in aIISp in FA cells. The reduced levels of aIISp in FA cells are due to reduced stability of this protein. We propose that the stability of aIISp is dependent upon one or more of the FA proteins. The present study was undertaken in order to get a clearer understanding of the proposed role of FA proteins in maintaining the stability of aIISp in the cell and the functional importance of this relationship in the repair of DNA interstrand cross-links and the repair defect in FA cells. For these studies, FA proteins were examined for their ability to directly interact with aIISp and, if so, to map the sites of interaction. Four overlapping regions of aIISp were constructed and binding of FA proteins to each of these regions was examined using yeast two-hybrid analysis. Of the proteins examined, FANCG was found to interact with one of these regions of aIISp and specifically with the SH3 domain within this region. The site of interaction in FANCG was mapped to a SH3 domain binding motif, which contains a consensus sequence with preference for the SH3 domain of aIISp. The sites of interaction in both FANCG and aIISp were confirmed using site-directed mutagenesis. Two FA proteins that did not contain any SH3 binding motifs, FANCC and FANCF, did not interact with the SH3 domain of aIISp or any of the other regions of aIISp. These results thus demonstrate that one of the FA proteins, FANCG, contains a class of motifs that has specificity for binding to SH3 domains and binds to the SH3 domain of aIISp via this motif. This binding is important in the DNA repair process and in the FA repair defect, as is shown by our in vivo studies in which FA-G cells, transformed with the FANCG cDNA and stably expressing FANCG, showed normal levels of aIISp and a correction of the defect in ability to repair DNA interstrand cross-links. We therefore propose that the binding of FANCG to aIISp is not only important for the stability of aIISp in cells but also for the role aIISp plays in the DNA repair process. Thus a deficiency in FANCG, such as occurs in FA-G cells, could lead to reduced stability of aIISp which in turn could be an important factor in the defective DNA repair pathway in FA cells.


2007 ◽  
Vol 85 (4) ◽  
pp. 249-256 ◽  
Author(s):  
Christopher James Wilds ◽  
Ernest Palus ◽  
Anne Marietta Noronha

DNA duplexes containing an interstrand cross-link have been synthesized utilizing a bis-3′-O-phosphoramidite deoxythymidine dimer where the N3 atoms are bridged by a butyl linker. With this approach sufficient quantities of high purity cross-linked duplexes are obtained that will enable various biochemical and structural studies to aid in research directed towards understanding the mechanism of interstrand cross-linked DNA repair. This methodology has advantages over a previously reported method to synthesize cross-linked DNA duplexes involving a monophosphoramidite of the same cross-linked thymidine dimer including circumventing the use of costly 5′-O-deoxyphosphoramidites in the assembly of the cross-linked duplex by solid-phase synthesis. This strategy can be employed to produce cross-linked duplexes in which the lesions are engineered to have a directly opposed (1–1) or staggered (1–2 or 2–1) orientations. Biophysical studies of duplexes containing this N3T-butyl-N3T cross-link in staggered 1–2 and 2–1 orientations reveal that both duplexes have a higher Tm than a non-cross-linked duplex suggesting that these linkages do not result in the destabilization of duplex DNA. Circular dichroism spectra of the 1–2 and 2–1 cross-linked duplexes exhibit minor differences from B-form structure, which correlates with molecular modeling studies.Key words: chemically modified oligonucleotides, interstrand cross-link, DNA adduct, DNA repair.


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