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Mini-Reviews in Medicinal Chemistry, 2014, 14, 805-811 805
The Development of Ataxia Telangiectasia Mutated Kinase Inhibitors
Martin Andrs
1,2
, Jan Korabecny
1,2
, Eugenie Nepovimova
1,2
, Daniel Jun
1,2
, Zdenek Hodny
3
,
Simona Moravcova
3
, Hana Hanzlikova
3
and Kamil Kuca
1,2,*
1
Department of Toxicology, Department of Public Health, Centre for Advanced Studies, Faculty of Military Health
Sciences, University of Defence, Trebesska 1575, 500 01 Hradec Kralove, Czech Republic;
2
Biomedical Research
Centre, University Hospital Hradec Kralove, Sokolska 581, 500 05 Hradec Kralove, Czech Republic;
3
Department of
Genome Integrity, Institute of Molecular Genetics of the ASCR, v.v.i., Videnska 1083, 142 20 Prague, Czech Republic
Abstract: Radiation and genotoxic drugs are two of the cornerstones of current cancer treatment strategy. However, this
type of therapy often suffers from radio- or chemo-resistance caused by DNA repair mechanisms. With the aim of
increasing the efficacy of these treatments, there has been great interest in studying DNA damage responses (DDR).
Among the plethora of signal and effector proteins involved in DDR, three related kinases ATM (ataxia telangiectasia
mutated), ATR (ATM and Rad3-related) and DNA-PK (DNA-dependent protein kinase) play the main roles in initiation
and regulation of signaling pathways in response to DNA double and single strand breaks (DSB and SSB). ATM
inhibitors, as well as those of ATR and DNA-PK, provide an opportunity to sensitize cancer cells to therapy. Moreover,
they can lead to selective killing of cancer cells, exploiting a concept known as synthetic lethality. However, only a very
few selective inhibitors have been identified to this date. This mini-review is focused both on the development of selective
inhibitors of ATM and other inhibitors which have ATM as one of their targets.
Keywords: Ataxia telangiectasia mutated, cancer, chemosensitization, DNA damage response, phosphatidylinositol 3-kinase-
related protein kinases, radiosensitization.
INTRODUCTION
The ataxia telangiectasia mutated (ATM) kinase is named
from the rare multisystem disorder ataxia telangiectasia (A-T),
which is caused by mutation in the ATM gene. This
autosomal recessive disorder is characterized by various
symptoms such as progressive cerebellar ataxia, telangiectasias,
immunodeficiency, cancer predisposition and extreme
radiation sensitivity. Cells with mutation in the ATM gene
exhibit genomic instability, defective DNA damage-induced
signaling pathways and cell cycle anomalies [1-4].
ATM is an atypical serine/threonine protein kinase and
belongs to the phosphatidylinositol 3-kinase (PI3K)-related
protein kinase (PIKK) family. Besides ATM, this family
contains five other members: ataxia telangiectasia and Rad3-
related (ATR), DNA-dependent protein kinase (DNA-PK),
and human suppressor of morphogenesis in genitalia-1
(hSMG-1), which are all involved in DNA damage response
(DDR); and mammalian target of rapamycin (mTOR), which
plays a crucial role in regulation of cell proliferation and
metabolism [5], and transformation/transcription associated
protein (TRRAP), which is the only member devoid of
kinase activity. All these proteins are large (ATM is 350 kDa
protein with 3056 residues) and bear a kinase domain very
similar to that of the PI3K family members [6, 7].
*Address correspondence to this author at the University Hospital Hradec
Kralove, Sokolska 581, 500 05 Hradec Kralove, Czech Republic;
Tel: 00 420 495 832 923; E-mail: kamil.kuca@fnhk.cz
ATM together with DNA-PK is a primary activator of the
responses to double strand breaks (DSB), whereas ATR is
activated by replication protein A (RPA)-coated single
strand DNA [8]. The DSBs are probably the most lethal
DNA lesions, and are caused by ionizing radiation (IR),
certain chemotherapeutic drugs (e.g. topoisomerase inhibitors),
reactive oxygen species (ROS), and by mechanical stress on
the chromosomes [7, 9]. In non-irradiated cells, ATM kinase
is held inactive as a dimer. The DSBs initiate rapid ATM
autophosphorylation on Ser1981 and dimer dissociation, in
cooperation with the MRE11-Rad50-NBS1 (MRN) complex,
which acts as the main DSB sensor [1, 10, 11]. Dissociated
and activated ATM passes the signal by phosphorylation of a
broad range of downstream proteins triggering the complex
and highly-branched signaling network (Fig. 1) [6, 12-14].
This network, in turn, activates both cell survival and cell
death pathways, and the final outcome depends on a delicate
balance between these opposing processes. Proper DNA
repair is essential for maintaining genome stability and, in
the case of DSBs, it occurs primarily by two distinct
mechanisms: nonhomologous end-joining (NHEJ) and
homologous recombination (HR) [15, 16].
ATM is an apical kinase, which is activated by various
stimuli, including DSBs (the MRE-Rad50-NBS1 complex
acts as a sensor), insulin, replication stress, chromatin
modifications, hypoxia, hyperthermia and reactive oxygen
species (ROS). In response to DSBs, ATM phosphorylates
hundreds of proteins, represented in figure by p53, checkpoint
kinase 2 (CHK2), breast and ovarian cancer-specific tumor
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