Home LiteratureArticle Details
PMID: 19050310 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Dysfunctional homologous recombination mediates genomic instability and progression in myeloma.

Blood ·Vol. 113 ·No. 10 ·2009-03-05 ·Pages 2290-7

Shammas MA, Shmookler Reis RJ, Koley H, Batchu RB, Li C, Munshi NC

Abstract

A prominent feature of most if not all cancers is a striking genetic instability, leading to ongoing accrual of mutational changes, some of which underlie tumor progression, including acquisition of invasiveness, drug resistance, and metastasis. Thus, the molecular basis for the generation of this genetic diversity in cancer cells has important implications in understanding cancer progression. Here we report that homologous recombination (HR) activity is elevated in multiple myeloma (MM) cells and leads to an increased rate of mutation and progressive accumulation of genetic variation over time. We demonstrate that the inhibition of HR activity in MM cells by small inhibitory RNA (siRNAs) targeting recombinase leads to significant reduction in the acquisition of new genetic changes in the genome and, conversely, the induction of HR activity leads to significant elevation in the number of new mutations over time and development of drug resistance in MM cells. These data identify dysregulated HR activity as a key mediator of DNA instability and progression of MM, with potential as a therapeutic target.

MeSH Terms
DNA-Binding Proteins/genetics,metabolism Disease Progression Gene Expression Profiling Genomic Instability Humans Immunohistochemistry Loss of Heterozygosity Multiple Myeloma/genetics Mutation Polymerase Chain Reaction Promoter Regions, Genetic RNA, Small Interfering Rad51 Recombinase/genetics,metabolism Recombination, Genetic Transfection
Chemicals
DNA-Binding Proteins RNA, Small Interfering X-ray repair cross complementing protein 3 XRCC2 protein, human RAD51 protein, human Rad51 Recombinase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Shammas Masood A
Department of Medicine, VA Health Care System and Harvard Medical School Boston, MA, USA.
Shmookler Reis Robert J
Koley Hemanta
Batchu Ramesh B
Li Cheng
Munshi Nikhil C
References (52)
52 references, click to expand
  1. Expression of SV40 large T antigen stimulates reversion of a chromosomal gene duplication in human cells.
    Exp Cell Res. 1997 Aug 1;234(2):300-12 PMID: 9260898
  2. Rapid assay for extrachromosomal homologous recombination in monkey cells.
    Mol Cell Biol. 1985 Mar;5(3):529-37 PMID: 2985956
  3. Chromosomal rearrangement and carcinogenesis.
    Mutat Res. 1982 May;98(3):249-64 PMID: 7050694
  4. Carcinogens stimulate intrachromosomal homologous recombination at an endogenous locus in human diploid fibroblasts.
    Mutat Res. 1997 Dec;385(3):173-93 PMID: 9506887
  5. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection.
    Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):31-6 PMID: 11134512
  6. DNA repair rate and etoposide (VP16) resistance of tumor cell subpopulations derived from a single human small cell lung cancer.
    Lung Cancer. 2003 May;40(2):157-64 PMID: 12711116
  7. Growth arrest, apoptosis, and telomere shortening of Barrett's-associated adenocarcinoma cells by a telomerase inhibitor.
    Gastroenterology. 2004 May;126(5):1337-46 PMID: 15131795
  8. Telomerase inhibition by siRNA causes senescence and apoptosis in Barrett's adenocarcinoma cells: mechanism and therapeutic potential.
    Mol Cancer. 2005 Jul 15;4:24 PMID: 16022731
  9. Multiple genes at 17q23 undergo amplification and overexpression in breast cancer.
    Cancer Res. 2000 Oct 1;60(19):5340-4 PMID: 11034067
  10. Illegitimate recombination leading to allelic loss and unbalanced translocation in p53-mutated human lymphoblastoid cells.
    Mol Cell Biol. 1997 Aug;17(8):4774-81 PMID: 9234733
  11. Translocations among antibody genes in human cancer.
    Science. 1983 Nov 18;222(4625):765-71 PMID: 6356357
  12. Evidence for simultaneous protein interactions between human Rad51 paralogs.
    J Biol Chem. 2000 Jun 2;275(22):16443-9 PMID: 10749867
  13. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro.
    Cell. 1996 Nov 15;87(4):757-66 PMID: 8929543
  14. Telomere maintenance by recombination in human cells.
    Nat Genet. 2000 Dec;26(4):447-50 PMID: 11101843
  15. High frequencies of chromosomal aberrations in multiple myeloma and monoclonal gammopathy of undetermined significance in direct chromosome preparation.
    Br J Haematol. 2004 Aug;126(4):487-94 PMID: 15287940
  16. Promiscuous translocations into immunoglobulin heavy chain switch regions in multiple myeloma.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13931-6 PMID: 8943038
  17. Insights into the multistep transformation of MGUS to myeloma using microarray expression analysis.
    Blood. 2003 Dec 15;102(13):4504-11 PMID: 12947006
  18. The genetic control of meiosis.
    Annu Rev Genet. 1976;10:53-134 PMID: 797314
  19. Loss of reiterated DNA sequences during serial passage of human diploid fibroblasts.
    Cell. 1980 Oct;21(3):739-49 PMID: 6254666
  20. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  21. The role of mitotic recombination in carcinogenesis.
    Crit Rev Toxicol. 1994;24(4):323-53 PMID: 7857521
  22. BRCA1 regulates RAD51 function in response to DNA damage and suppresses spontaneous sister chromatid replication slippage: implications for sister chromatid cohesion, genome stability, and carcinogenesis.
    Cancer Res. 2005 Dec 15;65(24):11384-91 PMID: 16357146
  23. p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction.
    EMBO J. 1996 Apr 15;15(8):1992-2002 PMID: 8617246
  24. DNA repair and recombination factor Rad51 is over-expressed in human pancreatic adenocarcinoma.
    Oncogene. 2000 May 25;19(23):2791-5 PMID: 10851081
  25. A central role for chromosome breakage in gene amplification, deletion formation, and amplicon integration.
    Genes Dev. 1991 Feb;5(2):160-74 PMID: 1995414
  26. Identification of genes modulated in multiple myeloma using genetically identical twin samples.
    Blood. 2004 Mar 1;103(5):1799-806 PMID: 12969976
  27. High-level expression of Rad51 is an independent prognostic marker of survival in non-small-cell lung cancer patients.
    Br J Cancer. 2005 Jul 11;93(1):137-43 PMID: 15956972
  28. Cytogenetic findings in 200 patients with multiple myeloma.
    Cancer Genet Cytogenet. 1995 Jul 1;82(1):41-9 PMID: 7627933
  29. DNA repair in lymphoblastoid cell lines from patients with head and neck cancer.
    Arch Otolaryngol Head Neck Surg. 1999 Feb;125(2):185-90 PMID: 10037285
  30. Chromosome aberrations and cancer.
    Science. 1991 Nov 22;254(5035):1153-60 PMID: 1957167
  31. Induction of duplication reversion in human fibroblasts, by wild-type and mutated SV40 T antigen, covaries with the ability to induce host DNA synthesis.
    Genetics. 1997 Aug;146(4):1417-28 PMID: 9258684
  32. Cluster-Rasch models for microarray gene expression data.
    Genome Biol. 2001;2(8):RESEARCH0031 PMID: 11532215
  33. High incidence of chromosome 13 deletion in multiple myeloma detected by multiprobe interphase FISH.
    Blood. 2000 Aug 15;96(4):1505-11 PMID: 10942398
  34. Specific killing of multiple myeloma cells by (-)-epigallocatechin-3-gallate extracted from green tea: biologic activity and therapeutic implications.
    Blood. 2006 Oct 15;108(8):2804-10 PMID: 16809610
  35. Telomerase inhibition and cell growth arrest by G-quadruplex interactive agent in multiple myeloma.
    Mol Cancer Ther. 2003 Sep;2(9):825-33 PMID: 14555701
  36. Characterization of homologous DNA recombination activity in normal and immortal mammalian cells.
    Nucleic Acids Res. 1996 Oct 15;24(20):4084-91 PMID: 8918816
  37. Normal diploid human and rodent cells lack a detectable frequency of gene amplification.
    Proc Natl Acad Sci U S A. 1990 Apr;87(8):3132-6 PMID: 2326271
  38. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application.
    Genome Biol. 2001;2(8):RESEARCH0032 PMID: 11532216
  39. Identification of essential genes in cultured mammalian cells using small interfering RNAs.
    J Cell Sci. 2001 Dec;114(Pt 24):4557-65 PMID: 11792820
  40. Genetic instabilities in human cancers.
    Nature. 1998 Dec 17;396(6712):643-9 PMID: 9872311
  41. Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase.
    Mol Cell Biol. 1997 Dec;17(12):7151-8 PMID: 9372947
  42. Targeting the single-strand G-rich overhang of telomeres with PNA inhibits cell growth and induces apoptosis of human immortal cells.
    Exp Cell Res. 2004 Apr 15;295(1):204-14 PMID: 15051503
  43. RecA protein: structure, function, and role in recombinational DNA repair.
    Prog Nucleic Acid Res Mol Biol. 1997;56:129-223 PMID: 9187054
  44. c-Ha-ras-1 proto-oncogene amplification and overexpression during the limited replicative life span of normal human fibroblasts.
    J Biol Chem. 1985 May 25;260(10):6404-9 PMID: 3997829
  45. Telomerase inhibition by peptide nucleic acids reverses 'immortality' of transformed human cells.
    Oncogene. 1999 Nov 4;18(46):6191-200 PMID: 10597217
  46. Multiple pathways leading to genomic instability and tumorigenesis.
    Ann N Y Acad Sci. 1994 Jul 29;726:165-77 PMID: 8092674
  47. Genome-wide detection of LOH in prostate cancer using human SNP microarray technology.
    Genomics. 2003 Mar;81(3):260-9 PMID: 12659810
  48. Lack of DNA homology in a pair of divergent chromosomes greatly sensitizes them to loss by DNA damage.
    Proc Natl Acad Sci U S A. 1989 Apr;86(7):2276-80 PMID: 2928332
  49. Radiation-induced recombination in Saccharomyces: the genetic control of recombination in mitosis and meiosis.
    Radiat Res. 1972 Jan;49(1):148-54 PMID: 4550515
  50. The molecular genetics of cancer.
    Science. 1987 Jan 16;235(4786):305-11 PMID: 3541204
  51. Homologous plasmid recombination is elevated in immortally transformed cells.
    Mol Cell Biol. 1989 Sep;9(9):4009-17 PMID: 2550810
  52. On the mechanism of UV and gamma-ray-induced intrachromosomal recombination in yeast cells synchronized in different stages of the cell cycle.
    Mol Gen Genet. 1995 Aug 21;248(3):301-10 PMID: 7565592
Article Info
Journal
Blood
Abbr.
Blood
ISSN
1528-0020
Published
2009-03-05
Epub
2008-00-02
Pages
2290-7
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC2652372
Subset
IM
Grants
NCI NIH HHS · R01 CA125711 · United States
PHS HHS · R01-124929 · United States
NCI NIH HHS · 1R01CA125711-01A2 · United States
NCI NIH HHS · R01 CA124929 · United States
PHS HHS · P01-78 378 · United States
PHS HHS · P50-100007 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]