RAD51

Last updated
RAD51
1SZP.jpg
Available structures
PDB Ortholog search: PDBe RCSB
Identifiers
Aliases RAD51 , BRCC5, FANCR, HHsRad51, HsT16930, MRMV2, RAD51A, RECA, RAD51 recombinase
External IDs OMIM: 179617; MGI: 97890; HomoloGene: 2155; GeneCards: RAD51; OMA:RAD51 - orthologs
Orthologs
SpeciesHumanMouse
Entrez

5888

19361

Ensembl

ENSG00000051180

n/a

UniProt

Q06609

Q08297

RefSeq (mRNA)

NM_001164269
NM_001164270
NM_002875
NM_133487

NM_011234

RefSeq (protein)

NP_001157741
NP_001157742
NP_002866
NP_597994

NP_035364

Location (UCSC) Chr 15: 40.69 – 40.73 Mb n/a
PubMed search [2] [3]
Wikidata
View/Edit Human View/Edit Mouse

DNA repair protein RAD51 homolog 1 is a protein encoded by the gene RAD51. The enzyme encoded by this gene is a member of the RAD51 protein family which assists in repair of DNA double strand breaks. RAD51 family members are homologous to the bacterial RecA, Archaeal RadA, and yeast Rad51. [4] [5] The protein is highly conserved in most eukaryotes, from yeast to humans. [6]

Contents

The name RAD51 derives from RADiation sensitive protein 51. [7]

Variants

Two alternatively spliced transcript variants of this gene have been reported, which encode distinct proteins. Transcript variants utilizing alternative polyA signals also exist.

Family

In mammals, seven recA-like genes have been identified: Rad51, Rad51L1/B, Rad51L2/C, Rad51L3/D, XRCC2, XRCC3, and DMC1/Lim15. [8] All of these proteins, with the exception of meiosis-specific DMC1, are essential for development in mammals. Rad51 is a member of the RecA-like NTPases.

Function

In humans, RAD51 is a 339-amino acid protein that plays a major role in homologous recombination of DNA during double strand break repair. In this repair process, an ATP-dependent DNA strand exchange takes place in which a template strand invades base-paired strands of homologous DNA molecules. RAD51 is involved in the search for homology and strand pairing stages of the process.

Unlike other proteins involved in DNA metabolism, the RecA/Rad51 family forms a helical nucleoprotein filament on DNA. [9]

This protein can interact with the ssDNA-binding protein RPA, BRCA2, PALB2 [10] and RAD52.

The structural basis for Rad51 filament formation and its functional mechanism still remain poorly understood. However, recent studies using fluorescent labeled Rad51 [11] have indicated that Rad51 fragments elongate via multiple nucleation events followed by growth, with the total fragment terminating when it reaches about 2 μm in length. However, disassociation of Rad51 from dsDNA is slow and incomplete, suggesting that there is a separate mechanism that accomplishes this.

RAD51 expression in cancer

In eukaryotes, the RAD51 protein has a central role in homologous recombinational repair, where it catalyses strand transfer between a broken sequence and its undamaged homologue, enabling re-synthesis of the damaged region (see homologous recombination models).

Numerous studies report that RAD51 is over-expressed in different cancers (see Table 1). In many of these studies, elevated expression of RAD51 is correlated with decreased patient survival. However, there are also some reports of under-expression of RAD51 in cancers (see Table 1).

Where RAD51 expression was quantified in conjunction with BRCA1 expression, an inverse correlation was found. [12] [13] This has been interpreted as selection, given that increased RAD51 expression and thus increased homologous recombinational repair (HRR) (by the HRR RAD52-RAD51 back-up pathway [14] ) may compensate for the accumulation of DNA damage arising from deficient BRCA1. [12] [13] [15]

Furthermore, many cancers have epigenetic deficiencies in various DNA repair genes (see Frequencies of epimutations in DNA repair genes in cancers) that can suppress their expression, likely leading to increases in unrepaired DNA damage. RAD51 overexpression seen in many cancers may therefore be compensatory (as seen in BRCA1 deficiency), resulting in increased HRR that may enable cancer cell survival by partially ameliorating the excess of DNA damage.

Under-expression of RAD51 would lead to increases in unrepaired DNA damage. When these DNA lesions are unrepaired, replication errors can occur near to the damaged sites (see translesion synthesis), leading to increased mutations and cancer.

Table 1. RAD51 expression reported in sporadic cancers
Cancer typeChange in expression observedFrequency of altered expression observed in cancer samples studiedEvaluation method usedRef.
Breast (invasive ductal)Over-expression-Immunohistochemistry [12]
Breast (BRCA1-deficient)Over-expression-Messenger RNA (mRNA) [13]
Breast (progesterone receptor negative)Over-expression-Messenger RNA (mRNA) [16]
Breast (overall)Under-expression30%Immunohistochemistry [17]
PancreaticOver-expression74%Immunohistochemistry [18]
PancreaticOver-expression66%Immunohistochemistry [19]
Head and neck (squamous)Over-expression75%Immunohistochemistry [20]
ProstateOver-expression33%Immunohistochemistry [21]
Non-small-cell lung cancerOver-expression29%Immunohistochemistry [22]
Soft tissue sarcomaOver-expression95%Immunohistochemistry [23]
Esophageal squamous cell cancerOver-expression47%Immunohistochemistry [24]
Renal cell carcinomaUnder-expression100%Western (protein) blotting and mRNA [25]

Role in double-strand break repair

Double-strand break (DSB) repair by homologous recombination is initiated by 5' to 3' strand resection (DSB resection). In humans, DNA2 nuclease resects the 5'-to-3' strand at the DSB to generate a 3' single-strand DNA (ssDNA) overhang. [26] [27]

In vertebrates, a number of RAD51 paralogs (see Figure) are essential for RAD51 protein recruitment or stabilization at sites of DNA damage.

Protein domains in homologous recombination-related proteins are conserved across the three main groups of life: archaea, bacteria and eukaryotes. HR proteins conserved domains.svg
Protein domains in homologous recombination-related proteins are conserved across the three main groups of life: archaea, bacteria and eukaryotes.

In vertebrates and plants, five paralogs of RAD51 are expressed in somatic cells, including RAD51B (RAD51L1), RAD51C (RAD51L2), RAD51D (RAD51L3), XRCC2 and XRCC3. They each share about 25% amino acid sequence identity with RAD51 and with each other. [28]

Outside of plants and vertebrates, a much broader diversity of Rad51 recombinase paralog proteins exist. In budding yeast (Saccharomyces cerevisiae), the paralogs Rad55 and Rad57 form a complex that associates with Rad51 at ssDNA. The recombinase paralog rfs-1 is found in the round worm Caenorhabditis elegans, however it is not essential for homologous recombination. Among archaea, RadB and RadC recombinase paralogs are found in many organisms belonging to Euryarchaeota, while a broader diversity of related recombinase paralogs are found in Crenarchaea, including Ral1, Ral2, Ral3, RadC, RadC1, and RadC2.

The RAD51 paralogs contribute to efficient DNA double-strand break repair by homologous recombination. Consequently, experimental depletion of these paralogs often result in significantly reduced homologous recombination. [29]

The paralogs form two identified complexes: BCDX2 (RAD51B-RAD51C-RAD51D-XRCC2) and CX3 (RAD51C-XRCC3). These two complexes act at two different stages of homologous recombinational DNA repair. The BCDX2 complex is responsible for RAD51 recruitment or stabilization at damage sites. [29] The BCDX2 complex appears to act by facilitating the assembly or stability of the RAD51 nucleoprotein filament. The CX3 complex acts downstream of RAD51 recruitment to damage sites. [29]

Another complex, the BRCA1-PALB2-BRCA2 complex, cooperates with the RAD51 paralogs to load RAD51 onto ssDNA coated with RPA to form the essential recombination intermediate, the RAD51-ssDNA filament. [30]

In mice and humans, the BRCA2 complex primarily mediates orderly assembly of RAD51 on ssDNA, which is an active substrate in homologous pairing and strand invasion. [31] BRCA2 also redirects RAD51 from dsDNA and prevents its dissociation from ssDNA. [31] However, in the presence of a BRCA2 mutation, human RAD52 can mediate RAD51 assembly on ssDNA and substitute for BRCA2 in homologous recombinational DNA repair, [32] though with lower efficiency than BRCA2.

Further steps are detailed in the article Homologous recombination.

Meiosis

Rad51 has a crucial function in meiotic prophase in mice, with Rad51 knockout leading to a depletion of late prophase I spermatocytes. [33]

During meiosis, the two recombinases, Rad51 and Dmc1, interact with single-stranded DNA to form specialized filaments that are adapted for facilitating recombination between homologous chromosomes. Both Rad51 and Dmc1 have an intrinsic ability to self-aggregate. [34] The presence of Dmc1 stabilizes the adjacent Rad51 filaments suggesting that cross-talk between these two recombinases may affect their biochemical properties.

Chemotherapy and aging

In aged and chemotherapy treated females, oocytes and follicles are depleted by apoptosis (programmed cell death) leading to ovarian failure. DNA damage-induced oocyte apoptosis depends on the efficiency of the DNA repair machinery that in turn declines with age. Survival of oocytes following chemotherapy or aging can be enhanced by increased expression of Rad51. [35] The Rad51-induced oocyte resistance to apoptosis is likely due to Rad51’s central role in homologous recombinational repair of DNA damage.

MicroRNA control of RAD51 expression

In mammals, microRNAs (miRNAs) regulate about 60% of the transcriptional activity of protein-encoding genes. [36] Some miRNAs also undergo methylation-associated silencing in cancer cells. [37] [38] If a repressive miRNA is silenced by hypermethylation or deletion, then the gene it typically targets becomes over-expressed.

At least eight miRNAs repressing RAD51 expression have been identified, with five of these appearing significant in cancer. For instance, in triple-negative breast cancers (TNBC), over-expression of miR-155 was reported to coincide with RAD51 repression. [39] Further study demonstrated that transfecting breast cancer cells with a vector over-expressing miR-155 represses RAD51 expression, resulting in decreased homologous recombination and increased sensitivity to ionizing radiation. [39]

Four further miRNAs that repress RAD51 (miR-148b* and miR-193b*, [40] miR-506, [41] and miR-34a [42] ) are under-expressed in cancers, presumably leading to induction of RAD51 expression, with under-expression of miR-148b and miR-193b causing an observed induction of RAD51 expression. [40] Furthermore, deletions of miR-148b* and miR-193b* in serous ovarian tumors correlates with increased losses of heterozygosity (LOH), which may be carcinogenic. This is thought to arise from increased RAD51 expression that can drive excess recombination. [40]

Under-expression of miR-506 is associated with both faster cancer recurrence and reduced survival in epithelial ovarian cancer patients. [43]

Methylation of the promoter of miR-34a, which leads to miR-34a under-expression, is observed in 79% of prostate cancers and 63% of primary melanomas. [44] Reduced miR-34a expression has also been observed in 63% of non-small cell lung cancers, [45] and 36% of colon cancers, [46] and is generally also under-expressed in primary neuroblastomas. [47]

Table 2 summarizes these five microRNAs and the nature of their altered expression in cancers were it has been observed.

Table 2. Altered expression of microRNAs that affect RAD51 expression in sporadic cancers
MicroRNAChange in miRNA expressionCancerRef.
miR-155Over-expressionTriple-negative breast cancer [39]
miR-148b*Under-expressionOvarian cancer [40]
miR-193b*Under-expressionOvarian cancer [40]
miR-506Under-expressionOvarian cancer [43]
miR-34aUnder-expressionProstate cancer and melanoma [44]
Non-small cell lung cancer [45]
Colon cancer [46]
Neuroblastoma [47]

Three other microRNAs have been identified, by various criteria, as likely to repress RAD51 (miR-96, [48] miR-203, [49] and miR-103/107 [50] ). These microRNAs were then tested by over-expressing them in cells in vitro, and they were found to indeed repress RAD51. This repression was generally associated with decreased HR and increased sensitivity of the cells to DNA damaging agents.

Pathology

This protein is also found to interact with PALB2 [10] and BRCA2, which may be important for the cellular response to DNA damage. BRCA2 is shown to regulate both the intracellular localization and DNA-binding ability of this protein. Loss of these controls following BRCA2 inactivation may be a key event leading to genomic instability and tumorigenesis. [51]

Several alterations of the Rad51 gene have been associated with an increased risk of developing breast cancer. The breast cancer susceptibility protein BRCA2 and PALB2 controls the function of Rad51 in the pathway for DNA repair by homologous recombination. [10] [52] In addition to the data listed in Table 1, increased RAD51 expression levels have been identified in metastatic canine mammary carcinoma, indicating that genomic instability plays an important role in the carcinogenesis of this tumor type. [53] [54] [55] [56]

Fanconi anemia

Fanconi anemia (FA) is a hereditary condition characterized by cellular hypersensitivity to DNA cross-linking agents. A dominant negative mutation in the Rad51 gene has been reported to give rise to an FA-like phenotype with features of mental retardation. [57] [58] This report included evidence that Rad51-mediated homologous recombinational repair likely has an important role in neurodevelopment.

Interactions

RAD51 has been shown to interact with:

Related Research Articles

<span class="mw-page-title-main">Chromosomal crossover</span> Cellular process

Chromosomal crossover, or crossing over, is the exchange of genetic material during sexual reproduction between two homologous chromosomes' non-sister chromatids that results in recombinant chromosomes. It is one of the final phases of genetic recombination, which occurs in the pachytene stage of prophase I of meiosis during a process called synapsis. Synapsis begins before the synaptonemal complex develops and is not completed until near the end of prophase I. Crossover usually occurs when matching regions on matching chromosomes break and then reconnect to the other chromosome.

<span class="mw-page-title-main">BRCA1</span> Gene known for its role in breast cancer

Breast cancer type 1 susceptibility protein is a protein that in humans is encoded by the BRCA1 gene. Orthologs are common in other vertebrate species, whereas invertebrate genomes may encode a more distantly related gene. BRCA1 is a human tumor suppressor gene and is responsible for repairing DNA.

<span class="mw-page-title-main">BRCA2</span> Gene known for its role in breast cancer

BRCA2 and BRCA2 are human genes and their protein products, respectively. The official symbol and the official name are maintained by the HUGO Gene Nomenclature Committee. One alternative symbol, FANCD1, recognizes its association with the FANC protein complex. Orthologs, styled Brca2 and Brca2, are common in other vertebrate species. BRCA2 is a human tumor suppressor gene, found in all humans; its protein, also called by the synonym breast cancer type 2 susceptibility protein, is responsible for repairing DNA.

<span class="mw-page-title-main">Homologous recombination</span> Genetic recombination between identical or highly similar strands of genetic material

Homologous recombination is a type of genetic recombination in which genetic information is exchanged between two similar or identical molecules of double-stranded or single-stranded nucleic acids.

Recombinases are genetic recombination enzymes.

<span class="mw-page-title-main">XRCC3</span> Protein-coding gene in the species Homo sapiens

DNA repair protein XRCC3 is a protein that in humans is encoded by the XRCC3 gene.

<span class="mw-page-title-main">RAD52</span> Protein-coding gene in the species Homo sapiens

RAD52 homolog , also known as RAD52, is a protein which in humans is encoded by the RAD52 gene.

<span class="mw-page-title-main">RAD51L1</span> Protein-coding gene in the species Homo sapiens

DNA repair protein RAD51 homolog 2 is a protein that in humans is encoded by the RAD51L1 gene.

<span class="mw-page-title-main">RAD51C</span> Protein-coding gene in the species Homo sapiens

RAD51 homolog C , also known as RAD51C, is a protein which in humans is encoded by the RAD51C gene.

<span class="mw-page-title-main">RAD51L3</span> Protein-coding gene in the species Homo sapiens

DNA repair protein RAD51 homolog 4 is a protein that in humans is encoded by the RAD51L3 gene.

<span class="mw-page-title-main">XRCC2</span> Protein-coding gene in the species Homo sapiens

DNA repair protein XRCC2 is a protein that in humans is encoded by the XRCC2 gene.

<span class="mw-page-title-main">RAD54L</span> Protein-coding gene in the species Homo sapiens

DNA repair and recombination protein RAD54-like is a protein that in humans is encoded by the RAD54L gene.

In molecular biology, a displacement loop or D-loop is a DNA structure where the two strands of a double-stranded DNA molecule are separated for a stretch and held apart by a third strand of DNA. An R-loop is similar to a D-loop, but in that case the third strand is RNA rather than DNA. The third strand has a base sequence which is complementary to one of the main strands and pairs with it, thus displacing the other complementary main strand in the region. Within that region the structure is thus a form of triple-stranded DNA. A diagram in the paper introducing the term illustrated the D-loop with a shape resembling a capital "D", where the displaced strand formed the loop of the "D".

<span class="mw-page-title-main">DMC1 (gene)</span> Protein-coding gene in the species Homo sapiens

Meiotic recombination protein DMC1/LIM15 homolog is a protein that in humans is encoded by the DMC1 gene.

<span class="mw-page-title-main">RAD54B</span> Protein-coding gene in the species Homo sapiens

DNA repair and recombination protein RAD54B is a protein that in humans is encoded by the RAD54B gene.

<span class="mw-page-title-main">BRCC3</span> Protein-coding gene in humans

Lys-63-specific deubiquitinase BRCC36 is an enzyme that in humans is encoded by the BRCC3 gene.

<span class="mw-page-title-main">PALB2</span> Protein-coding gene in the species Homo sapiens

Partner and localizer of BRCA2, also known as PALB2 or FANCN, is a protein which in humans is encoded by the PALB2 gene.

<span class="mw-page-title-main">Protein ZGRF1</span> Protein-coding gene in the species Homo sapiens

Protein ZGRF1 is a protein encoded in the human by the ZGRF1 gene also known as C4orf21, that has a weight of 236.6 kDa. The ZGRF1 gene product localizes to the cell nucleus and promotes DNA repair by stimulating homologous recombination. This gene shows relatively low expression in most human tissues, with increased expression in situations of chemical dependence. ZGRF1 is orthologous to nearly all eukaryotes. Functional domains of this protein link it to a series of helicases, most notably the AAA_12 and AAA_11 domains.

GT198 is a human oncogene located within the BRCA1 locus at chromosome 17q21. It encodes protein product named GT198, Hop2 or TBPIP. The GT198 gene is found to be mutated with its protein overexpressed in human cancers including breast and ovarian cancers.

<span class="mw-page-title-main">Double-strand break repair model</span>

A double-strand break repair model refers to the various models of pathways that cells undertake to repair double strand-breaks (DSB). DSB repair is an important cellular process, as the accumulation of unrepaired DSB could lead to chromosomal rearrangements, tumorigenesis or even cell death. In human cells, there are two main DSB repair mechanisms: Homologous recombination (HR) and non-homologous end joining (NHEJ). HR relies on undamaged template DNA as reference to repair the DSB, resulting in the restoration of the original sequence. NHEJ modifies and ligates the damaged ends regardless of homology. In terms of DSB repair pathway choice, most mammalian cells appear to favor NHEJ rather than HR. This is because the employment of HR may lead to gene deletion or amplification in cells which contains repetitive sequences. In terms of repair models in the cell cycle, HR is only possible during the S and G2 phases, while NHEJ can occur throughout whole process. These repair pathways are all regulated by the overarching DNA damage response mechanism. Besides HR and NHEJ, there are also other repair models which exists in cells. Some are categorized under HR, such as synthesis-dependent strain annealing, break-induced replication, and single-strand annealing; while others are an entirely alternate repair model, namely, the pathway microhomology-mediated end joining (MMEJ).

References

  1. 1 2 3 GRCh38: Ensembl release 89: ENSG00000051180 – Ensembl, May 2017
  2. ↑ "Human PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  3. ↑ "Mouse PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  4. ↑ Shinohara A, Ogawa H, Ogawa T (May 1992). "Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein". Cell. 69 (3): 457–70. doi:10.1016/0092-8674(92)90447-K. PMID   1581961. S2CID   35937283.
  5. ↑ Seitz EM, Brockman JP, Sandler SJ, Clark AJ, Kowalczykowski SC (May 1998). "RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange". Genes & Development. 12 (9): 1248–53. doi:10.1101/gad.12.9.1248. PMC   316774 . PMID   9573041.
  6. ↑ Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (July 1993). "Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA". Nature Genetics. 4 (3): 239–43. doi:10.1038/ng0793-239. PMID   8358431. S2CID   28220010.
  7. ↑ Khoo, Kelvin H. P.; Jolly, Hayley R.; Able, Jason A. (2008). "The RAD51 gene family in bread wheat is highly conserved across eukaryotes, with RAD51A upregulated during early meiosis". Functional Plant Biology. 35 (12): 1267–1277. doi:10.1071/fp08203. ISSN   1445-4408. PMID   32688873.
  8. ↑ Kawabata M, Kawabata T, Nishibori M (February 2005). "Role of recA/RAD51 family proteins in mammals". Acta Medica Okayama. 59 (1): 1–9. doi:10.18926/AMO/31987. PMID   15902993.
  9. ↑ Galkin VE, Wu Y, Zhang XP, Qian X, He Y, Yu X, Heyer WD, Luo Y, Egelman EH (June 2006). "The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity". Structure. 14 (6): 983–92. doi: 10.1016/j.str.2006.04.001 . PMID   16765891.
  10. 1 2 3 Buisson R, Dion-Côté AM, Coulombe Y, Launay H, Cai H, Stasiak AZ, Stasiak A, Xia B, Masson JY (October 2010). "Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination". Nature Structural & Molecular Biology. 17 (10): 1247–54. doi:10.1038/nsmb.1915. PMC   4094107 . PMID   20871615.
  11. ↑ Hilario J, Amitani I, Baskin RJ, Kowalczykowski SC (January 2009). "Direct imaging of human Rad51 nucleoprotein dynamics on individual DNA molecules". Proceedings of the National Academy of Sciences of the United States of America. 106 (2): 361–8. doi: 10.1073/pnas.0811965106 . PMC   2613362 . PMID   19122145.
  12. 1 2 3 Maacke H, Opitz S, Jost K, Hamdorf W, Henning W, Krüger S, Feller AC, Lopens A, Diedrich K, Schwinger E, Stürzbecher HW (December 2000). "Over-expression of wild-type Rad51 correlates with histological grading of invasive ductal breast cancer". International Journal of Cancer. 88 (6): 907–13. doi:10.1002/1097-0215(20001215)88:6<907::aid-ijc11>3.0.co;2-4. PMID   11093813. S2CID   33032737.
  13. 1 2 3 Martin RW, Orelli BJ, Yamazoe M, Minn AJ, Takeda S, Bishop DK (October 2007). "RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1-deficient breast tumors". Cancer Research. 67 (20): 9658–65. doi: 10.1158/0008-5472.CAN-07-0290 . PMID   17942895.
  14. ↑ Lok BH, Carley AC, Tchang B, Powell SN (July 2013). "RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination". Oncogene. 32 (30): 3552–8. doi:10.1038/onc.2012.391. PMC   5730454 . PMID   22964643.
  15. ↑ Klein HL (May 2008). "The consequences of Rad51 overexpression for normal and tumor cells". DNA Repair. 7 (5): 686–93. doi:10.1016/j.dnarep.2007.12.008. PMC   2430071 . PMID   18243065.
  16. ↑ Barbano R, Copetti M, Perrone G, Pazienza V, Muscarella LA, Balsamo T, Storlazzi CT, Ripoli M, Rinaldi M, Valori VM, Latiano TP, Maiello E, Stanziale P, Carella M, Mangia A, Pellegrini F, Bisceglia M, Muda AO, Altomare V, Murgo R, Fazio VM, Parrella P (August 2011). "High RAD51 mRNA expression characterize estrogen receptor-positive/progesteron receptor-negative breast cancer and is associated with patient's outcome". International Journal of Cancer. 129 (3): 536–45. doi: 10.1002/ijc.25736 . PMID   21064098.
  17. ↑ Yoshikawa K, Ogawa T, Baer R, Hemmi H, Honda K, Yamauchi A, Inamoto T, Ko K, Yazumi S, Motoda H, Kodama H, Noguchi S, Gazdar AF, Yamaoka Y, Takahashi R (October 2000). "Abnormal expression of BRCA1 and BRCA1-interactive DNA-repair proteins in breast carcinomas". International Journal of Cancer. 88 (1): 28–36. doi: 10.1002/1097-0215(20001001)88:1<28::aid-ijc5>3.0.co;2-4 . PMID   10962436. S2CID   24405295.
  18. ↑ Han H, Bearss DJ, Browne LW, Calaluce R, Nagle RB, Von Hoff DD (May 2002). "Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray". Cancer Research. 62 (10): 2890–6. PMID   12019169.
  19. ↑ Maacke H, Jost K, Opitz S, Miska S, Yuan Y, Hasselbach L, Lüttges J, Kalthoff H, Stürzbecher HW (May 2000). "DNA repair and recombination factor Rad51 is over-expressed in human pancreatic adenocarcinoma". Oncogene. 19 (23): 2791–5. doi:10.1038/sj.onc.1203578. PMID   10851081. S2CID   38416402.
  20. ↑ Connell PP, Jayathilaka K, Haraf DJ, Weichselbaum RR, Vokes EE, Lingen MW (May 2006). "Pilot study examining tumor expression of RAD51 and clinical outcomes in human head cancers". International Journal of Oncology. 28 (5): 1113–9. doi: 10.3892/ijo.28.5.1113 . PMID   16596227.
  21. ↑ Mitra A, Jameson C, Barbachano Y, Sanchez L, Kote-Jarai Z, Peock S, Sodha N, Bancroft E, Fletcher A, Cooper C, Easton D, Eeles R, Foster CS (December 2009). "Overexpression of RAD51 occurs in aggressive prostatic cancer". Histopathology. 55 (6): 696–704. doi:10.1111/j.1365-2559.2009.03448.x. PMC   2856636 . PMID   20002770.
  22. ↑ Qiao GB, Wu YL, Yang XN, Zhong WZ, Xie D, Guan XY, Fischer D, Kolberg HC, Kruger S, Stuerzbecher HW (July 2005). "High-level expression of Rad51 is an independent prognostic marker of survival in non-small-cell lung cancer patients". British Journal of Cancer. 93 (1): 137–43. doi:10.1038/sj.bjc.6602665. PMC   2361489 . PMID   15956972.
  23. ↑ Hannay JA, Liu J, Zhu QS, Bolshakov SV, Li L, Pisters PW, Lazar AJ, Yu D, Pollock RE, Lev D (May 2007). "Rad51 overexpression contributes to chemoresistance in human soft tissue sarcoma cells: a role for p53/activator protein 2 transcriptional regulation". Molecular Cancer Therapeutics. 6 (5): 1650–60. doi: 10.1158/1535-7163.MCT-06-0636 . PMID   17513613.
  24. ↑ Li Y, Yu H, Luo RZ, Zhang Y, Zhang MF, Wang X, Jia WH (November 2011). "Elevated expression of Rad51 is correlated with decreased survival in resectable esophageal squamous cell carcinoma". Journal of Surgical Oncology. 104 (6): 617–22. doi:10.1002/jso.22018. PMID   21744352. S2CID   21940444.
  25. ↑ Liu S, Li Y, Xu H, Wang K, Li N, Li J, Sun T, Xu Y (July 2016). "Increased expression of SET domain-containing proteins and decreased expression of Rad51 in different classes of renal cell carcinoma". Bioscience Reports. 36 (3): e00349. doi:10.1042/BSR20160122. PMC   5293581 . PMID   27170370.
  26. ↑ Hoa NN, Akagawa R, Yamasaki T, Hirota K, Sasa K, Natsume T, Kobayashi J, Sakuma T, Yamamoto T, Komatsu K, Kanemaki MT, Pommier Y, Takeda S, Sasanuma H (December 2015). "Relative contribution of four nucleases, CtIP, Dna2, Exo1 and Mre11, to the initial step of DNA double-strand break repair by homologous recombination in both the chicken DT40 and human TK6 cell lines". Genes to Cells. 20 (12): 1059–76. doi: 10.1111/gtc.12310 . PMC   7747012 . PMID   26525166.
  27. ↑ Hoa NN, Kobayashi J, Omura M, Hirakawa M, Yang SH, Komatsu K, Paull TT, Takeda S, Sasanuma H (2015). "BRCA1 and CtIP Are Both Required to Recruit Dna2 at Double-Strand Breaks in Homologous Recombination". PLOS ONE. 10 (4): e0124495. Bibcode:2015PLoSO..1024495H. doi: 10.1371/journal.pone.0124495 . PMC   4409214 . PMID   25909997.
  28. ↑ Miller KA, Sawicka D, Barsky D, Albala JS (2004). "Domain mapping of the Rad51 paralog protein complexes". Nucleic Acids Research. 32 (1): 169–78. doi:10.1093/nar/gkg925. PMC   373258 . PMID   14704354.
  29. 1 2 3 Chun J, Buechelmaier ES, Powell SN (January 2013). "Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway". Molecular and Cellular Biology. 33 (2): 387–95. doi:10.1128/MCB.00465-12. PMC   3554112 . PMID   23149936.
  30. ↑ Prakash R, Zhang Y, Feng W, Jasin M (April 2015). "Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins". Cold Spring Harbor Perspectives in Biology. 7 (4): a016600. doi:10.1101/cshperspect.a016600. PMC   4382744 . PMID   25833843.
  31. 1 2 Holloman WK (July 2011). "Unraveling the mechanism of BRCA2 in homologous recombination". Nature Structural & Molecular Biology. 18 (7): 748–54. doi:10.1038/nsmb.2096. PMC   3647347 . PMID   21731065.
  32. ↑ Feng Z, Scott SP, Bussen W, Sharma GG, Guo G, Pandita TK, Powell SN (January 2011). "Rad52 inactivation is synthetically lethal with BRCA2 deficiency". Proceedings of the National Academy of Sciences of the United States of America. 108 (2): 686–91. doi: 10.1073/pnas.1010959107 . PMC   3021033 . PMID   21148102.
  33. ↑ Dai J, Voloshin O, Potapova S, Camerini-Otero RD (February 2017). "Meiotic Knockdown and Complementation Reveals Essential Role of RAD51 in Mouse Spermatogenesis". Cell Reports. 18 (6): 1383–1394. doi:10.1016/j.celrep.2017.01.024. PMC   5358547 . PMID   28178517.
  34. ↑ Crickard JB, Kaniecki K, Kwon Y, Sung P, Greene EC (March 2018). "Spontaneous self-segregation of Rad51 and Dmc1 DNA recombinases within mixed recombinase filaments". The Journal of Biological Chemistry. 293 (11): 4191–4200. doi: 10.1074/jbc.RA117.001143 . PMC   5858004 . PMID   29382724.
  35. ↑ Kujjo LL, Laine T, Pereira RJ, Kagawa W, Kurumizaka H, Yokoyama S, Perez GI (February 2010). "Enhancing survival of mouse oocytes following chemotherapy or aging by targeting Bax and Rad51". PLOS ONE. 5 (2): e9204. Bibcode:2010PLoSO...5.9204K. doi: 10.1371/journal.pone.0009204 . PMC   2820548 . PMID   20169201.
  36. ↑ Friedman RC, Farh KK, Burge CB, Bartel DP (January 2009). "Most mammalian mRNAs are conserved targets of microRNAs". Genome Research. 19 (1): 92–105. doi:10.1101/gr.082701.108. PMC   2612969 . PMID   18955434.
  37. ↑ Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA (June 2006). "Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells". Cancer Cell. 9 (6): 435–43. doi: 10.1016/j.ccr.2006.04.020 . PMID   16766263.
  38. ↑ Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setién F, Casado S, Suarez-Gauthier A, Sanchez-Cespedes M, Git A, Gitt A, Spiteri I, Das PP, Caldas C, Miska E, Esteller M (February 2007). "Genetic unmasking of an epigenetically silenced microRNA in human cancer cells". Cancer Research. 67 (4): 1424–9. doi: 10.1158/0008-5472.CAN-06-4218 . PMID   17308079.
  39. 1 2 3 Gasparini P, Lovat F, Fassan M, Casadei L, Cascione L, Jacob NK, Carasi S, Palmieri D, Costinean S, Shapiro CL, Huebner K, Croce CM (March 2014). "Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation". Proceedings of the National Academy of Sciences of the United States of America. 111 (12): 4536–41. Bibcode:2014PNAS..111.4536G. doi: 10.1073/pnas.1402604111 . PMC   3970505 . PMID   24616504. (Erratum:  doi:10.1073/pnas.1700727114, PMID   28242688,  Retraction Watch)
  40. 1 2 3 4 5 Choi YE, Pan Y, Park E, Konstantinopoulos P, De S, D'Andrea A, Chowdhury D (April 2014). "MicroRNAs down-regulate homologous recombination in the G1 phase of cycling cells to maintain genomic stability". eLife. 3: e02445. doi: 10.7554/eLife.02445 . PMC   4031983 . PMID   24843000.
  41. ↑ Liu G, Xue F, Zhang W (September 2015). "miR-506: a regulator of chemo-sensitivity through suppression of the RAD51-homologous recombination axis". Chinese Journal of Cancer. 34 (11): 485–7. doi: 10.1186/s40880-015-0049-z . PMC   4593343 . PMID   26369335.
  42. ↑ Cortez MA, Valdecanas D, Niknam S, Peltier HJ, Diao L, Giri U, Komaki R, Calin GA, Gomez DR, Chang JY, Heymach JV, Bader AG, Welsh JW (December 2015). "In Vivo Delivery of miR-34a Sensitizes Lung Tumors to Radiation Through RAD51 Regulation". Molecular Therapy: Nucleic Acids. 4 (12): e270. doi:10.1038/mtna.2015.47. PMC   5014539 . PMID   26670277.
  43. 1 2 Liu G, Yang D, Rupaimoole R, Pecot CV, Sun Y, Mangala LS, Li X, Ji P, Cogdell D, Hu L, Wang Y, Rodriguez-Aguayo C, Lopez-Berestein G, Shmulevich I, De Cecco L, Chen K, Mezzanzanica D, Xue F, Sood AK, Zhang W (July 2015). "Augmentation of response to chemotherapy by microRNA-506 through regulation of RAD51 in serous ovarian cancers". Journal of the National Cancer Institute. 107 (7): djv108. doi:10.1093/jnci/djv108. PMC   4554255 . PMID   25995442.
  44. 1 2 Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H, Knyazev P, Diebold J, Hermeking H (August 2008). "Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer". Cell Cycle. 7 (16): 2591–600. doi: 10.4161/cc.7.16.6533 . PMID   18719384.
  45. 1 2 Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, Bader AG (July 2010). "Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34". Cancer Research. 70 (14): 5923–30. doi:10.1158/0008-5472.CAN-10-0655. PMC   2913706 . PMID   20570894.
  46. 1 2 Tazawa H, Tsuchiya N, Izumiya M, Nakagama H (September 2007). "Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells". Proceedings of the National Academy of Sciences of the United States of America. 104 (39): 15472–7. Bibcode:2007PNAS..10415472T. doi: 10.1073/pnas.0707351104 . PMC   2000550 . PMID   17875987.
  47. 1 2 Welch C, Chen Y, Stallings RL (July 2007). "MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells". Oncogene. 26 (34): 5017–22. doi: 10.1038/sj.onc.1210293 . PMID   17297439.
  48. ↑ Wang Y, Huang JW, Calses P, Kemp CJ, Taniguchi T (August 2012). "MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition". Cancer Research. 72 (16): 4037–46. doi:10.1158/0008-5472.CAN-12-0103. PMC   3421071 . PMID   22761336.
  49. ↑ Chang JH, Hwang YH, Lee DJ, Kim DH, Park JM, Wu HG, Kim IA (February 2016). "MicroRNA-203 Modulates the Radiation Sensitivity of Human Malignant Glioma Cells". International Journal of Radiation Oncology, Biology, Physics. 94 (2): 412–20. doi:10.1016/j.ijrobp.2015.10.001. PMID   26678661.
  50. ↑ Huang JW, Wang Y, Dhillon KK, Calses P, Villegas E, Mitchell PS, Tewari M, Kemp CJ, Taniguchi T (December 2013). "Systematic screen identifies miRNAs that target RAD51 and RAD51D to enhance chemosensitivity". Molecular Cancer Research. 11 (12): 1564–73. doi:10.1158/1541-7786.MCR-13-0292. PMC   3869885 . PMID   24088786.
  51. ↑ Daniel DC (October 2002). "Highlight: BRCA1 and BRCA2 proteins in breast cancer". Microscopy Research and Technique. 59 (1): 68–83. doi: 10.1002/jemt.10178 . PMID   12242698. S2CID   30091586.
  52. 1 2 Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL, Venkitaraman AR (November 2002). "Insights into DNA recombination from the structure of a RAD51-BRCA2 complex". Nature. 420 (6913): 287–93. Bibcode:2002Natur.420..287P. doi:10.1038/nature01230. PMID   12442171. S2CID   4359383.
  53. ↑ Klopfleisch R, von Euler H, Sarli G, Pinho SS, Gärtner F, Gruber AD (January 2011). "Molecular carcinogenesis of canine mammary tumors: news from an old disease". Veterinary Pathology. 48 (1): 98–116. doi:10.1177/0300985810390826. PMID   21149845. S2CID   206509356.
  54. ↑ Klopfleisch R, Gruber AD (May 2009). "Increased expression of BRCA2 and RAD51 in lymph node metastases of canine mammary adenocarcinomas". Veterinary Pathology. 46 (3): 416–22. doi: 10.1354/vp.08-VP-0212-K-FL . PMID   19176491. S2CID   11583190.
  55. ↑ Klopfleisch R, Schütze M, Gruber AD (January 2010). "RAD51 protein expression is increased in canine mammary carcinomas". Veterinary Pathology. 47 (1): 98–101. doi:10.1177/0300985809353310. PMID   20080488. S2CID   37774507.
  56. ↑ Klopfleisch R, Klose P, Gruber AD (May 2010). "The combined expression pattern of BMP2, LTBP4, and DERL1 discriminates malignant from benign canine mammary tumors". Veterinary Pathology. 47 (3): 446–54. doi:10.1177/0300985810363904. PMID   20375427. S2CID   24379106.
  57. ↑ Wang AT, Kim T, Wagner JE, Conti BA, Lach FP, Huang AL, et al. (August 2015). "A Dominant Mutation in Human RAD51 Reveals Its Function in DNA Interstrand Crosslink Repair Independent of Homologous Recombination". Molecular Cell. 59 (3): 478–90. doi:10.1016/j.molcel.2015.07.009. PMC   4529964 . PMID   26253028.
  58. ↑ Ameziane N, May P, Haitjema A, van de Vrugt HJ, van Rossum-Fikkert SE, Ristic D, Williams GJ, Balk J, Rockx D, Li H, Rooimans MA, Oostra AB, Velleuer E, Dietrich R, Bleijerveld OB, Maarten Altelaar AF, Meijers-Heijboer H, Joenje H, Glusman G, Roach J, Hood L, Galas D, Wyman C, Balling R, den Dunnen J, de Winter JP, Kanaar R, Gelinas R, Dorsman JC (December 2015). "A novel Fanconi anaemia subtype associated with a dominant-negative mutation in RAD51". Nature Communications. 6: 8829. Bibcode:2015NatCo...6.8829A. doi:10.1038/ncomms9829. PMC   4703882 . PMID   26681308.
  59. 1 2 3 Chen G, Yuan SS, Liu W, Xu Y, Trujillo K, Song B, Cong F, Goff SP, Wu Y, Arlinghaus R, Baltimore D, Gasser PJ, Park MS, Sung P, Lee EY (April 1999). "Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl". The Journal of Biological Chemistry. 274 (18): 12748–52. doi: 10.1074/jbc.274.18.12748 . PMID   10212258.
  60. 1 2 3 4 5 6 Dong Y, Hakimi MA, Chen X, Kumaraswamy E, Cooch NS, Godwin AK, Shiekhattar R (November 2003). "Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair". Molecular Cell. 12 (5): 1087–99. doi: 10.1016/s1097-2765(03)00424-6 . PMID   14636569.
  61. 1 2 Chen J, Silver DP, Walpita D, Cantor SB, Gazdar AF, Tomlinson G, Couch FJ, Weber BL, Ashley T, Livingston DM, Scully R (September 1998). "Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells". Molecular Cell. 2 (3): 317–28. doi:10.1016/s1097-2765(00)80276-2. PMID   9774970.
  62. ↑ Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, Ashley T, Livingston DM (January 1997). "Association of BRCA1 with Rad51 in mitotic and meiotic cells". Cell. 88 (2): 265–75. doi: 10.1016/s0092-8674(00)81847-4 . PMID   9008167. S2CID   8044855.
  63. ↑ Wang Q, Zhang H, Guerrette S, Chen J, Mazurek A, Wilson T, Slupianek A, Skorski T, Fishel R, Greene MI (August 2001). "Adenosine nucleotide modulates the physical interaction between hMSH2 and BRCA1". Oncogene. 20 (34): 4640–9. doi: 10.1038/sj.onc.1204625 . PMID   11498787.
  64. ↑ Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A (April 1997). "Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2". Nature. 386 (6627): 804–10. Bibcode:1997Natur.386..804S. doi:10.1038/386804a0. hdl: 11858/00-001M-0000-0010-5059-F . PMID   9126738. S2CID   4238943.
  65. ↑ Lin HR, Ting NS, Qin J, Lee WH (September 2003). "M phase-specific phosphorylation of BRCA2 by Polo-like kinase 1 correlates with the dissociation of the BRCA2-P/CAF complex". The Journal of Biological Chemistry. 278 (38): 35979–87. doi: 10.1074/jbc.M210659200 . PMID   12815053.
  66. ↑ Yu DS, Sonoda E, Takeda S, Huang CL, Pellegrini L, Blundell TL, Venkitaraman AR (October 2003). "Dynamic control of Rad51 recombinase by self-association and interaction with BRCA2". Molecular Cell. 12 (4): 1029–41. doi:10.1016/s1097-2765(03)00394-0. PMID   14580352.
  67. ↑ Chen PL, Chen CF, Chen Y, Xiao J, Sharp ZD, Lee WH (April 1998). "The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment". Proceedings of the National Academy of Sciences of the United States of America. 95 (9): 5287–92. Bibcode:1998PNAS...95.5287C. doi: 10.1073/pnas.95.9.5287 . PMC   20253 . PMID   9560268.
  68. ↑ Sarkisian CJ, Master SR, Huber LJ, Ha SI, Chodosh LA (October 2001). "Analysis of murine Brca2 reveals conservation of protein-protein interactions but differences in nuclear localization signals". The Journal of Biological Chemistry. 276 (40): 37640–8. doi: 10.1074/jbc.M106281200 . PMID   11477095.
  69. ↑ Wong AK, Pero R, Ormonde PA, Tavtigian SV, Bartel PL (December 1997). "RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2". The Journal of Biological Chemistry. 272 (51): 31941–4. doi: 10.1074/jbc.272.51.31941 . PMID   9405383.
  70. ↑ Katagiri T, Saito H, Shinohara A, Ogawa H, Kamada N, Nakamura Y, Miki Y (March 1998). "Multiple possible sites of BRCA2 interacting with DNA repair protein RAD51". Genes, Chromosomes & Cancer. 21 (3): 217–22. doi:10.1002/(SICI)1098-2264(199803)21:3<217::AID-GCC5>3.0.CO;2-2. PMID   9523196. S2CID   45954246.
  71. ↑ Tarsounas M, Davies AA, West SC (January 2004). "RAD51 localization and activation following DNA damage". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 359 (1441): 87–93. doi:10.1098/rstb.2003.1368. PMC   1693300 . PMID   15065660.
  72. ↑ Liu J, Yuan Y, Huan J, Shen Z (January 2001). "Inhibition of breast and brain cancer cell growth by BCCIPalpha, an evolutionarily conserved nuclear protein that interacts with BRCA2". Oncogene. 20 (3): 336–45. doi: 10.1038/sj.onc.1204098 . PMID   11313963.
  73. ↑ Marmorstein LY, Ouchi T, Aaronson SA (November 1998). "The BRCA2 gene product functionally interacts with p53 and RAD51". Proceedings of the National Academy of Sciences of the United States of America. 95 (23): 13869–74. Bibcode:1998PNAS...9513869M. doi: 10.1073/pnas.95.23.13869 . PMC   24938 . PMID   9811893.
  74. ↑ Wu L, Davies SL, Levitt NC, Hickson ID (June 2001). "Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51". The Journal of Biological Chemistry. 276 (22): 19375–81. doi: 10.1074/jbc.M009471200 . PMID   11278509.
  75. ↑ Masson JY, Davies AA, Hajibagheri N, Van Dyck E, Benson FE, Stasiak AZ, Stasiak A, West SC (November 1999). "The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51". The EMBO Journal. 18 (22): 6552–60. doi:10.1093/emboj/18.22.6552. PMC   1171718 . PMID   10562567.
  76. ↑ Sigurdsson S, Van Komen S, Petukhova G, Sung P (November 2002). "Homologous DNA pairing by human recombination factors Rad51 and Rad54". The Journal of Biological Chemistry. 277 (45): 42790–4. doi: 10.1074/jbc.M208004200 . PMID   12205100.
  77. ↑ Stürzbecher HW, Donzelmann B, Henning W, Knippschild U, Buchhop S (April 1996). "p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction". The EMBO Journal. 15 (8): 1992–2002. doi:10.1002/j.1460-2075.1996.tb00550.x. PMC   450118 . PMID   8617246.
  78. ↑ Buchhop S, Gibson MK, Wang XW, Wagner P, Stürzbecher HW, Harris CC (October 1997). "Interaction of p53 with the human Rad51 protein". Nucleic Acids Research. 25 (19): 3868–74. doi:10.1093/nar/25.19.3868. PMC   146972 . PMID   9380510.
  79. ↑ Tanaka K, Hiramoto T, Fukuda T, Miyagawa K (August 2000). "A novel human rad54 homologue, Rad54B, associates with Rad51". The Journal of Biological Chemistry. 275 (34): 26316–21. doi: 10.1074/jbc.M910306199 . PMID   10851248.
  80. ↑ Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI (April 1996). "Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes". Proceedings of the National Academy of Sciences of the United States of America. 93 (7): 2958–63. Bibcode:1996PNAS...93.2958K. doi: 10.1073/pnas.93.7.2958 . PMC   39742 . PMID   8610150.
  81. ↑ Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ (October 1996). "Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system". Genomics. 37 (2): 183–6. doi:10.1006/geno.1996.0540. PMID   8921390.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.