Z Gerontol Geriat 2013 · 46:629–634
DOI 10.1007/s00391-013-0531-7
Received: 4 June 2013
Revised: 19 June 2013
Accepted: 23 June 2013
Published online: 14 October 2013
© Springer-Verlag Berlin Heidelberg 2013
M. Hodzic
1
· Y. Naaldijk
2, 3
· A. Stolzing
2, 3
1
University of Berlin
2
Fraunhofer Institute for Cell Therapy and Immunology, Leipzig
3
Translational Research Centre for Regenerative Medicine (TRM), University of Leipzig
Regulating aging in adult
stem cells with microRNA
Introduction
MicroRNA biosynthesis
MicroRNAs (miRNAs) originate from
noncoding regions of the genome and
from introns of coding regions [1]. MiR-
NAs are transcribed by the RNA polymer-
ases 2 and 3 [2]. Transcription of miRNA
from noncoding regions yields longer
primary transcripts called primary miR-
NA (pri-miRNA). Pri-miRNA is cleaved
in the nucleus by the Drosha/DGCR8
complex into a 70-nt long hairpin struc-
ture, the precursor miRNA (pre-miRNA)
(. Fig. 1). The pre-miRNA is exported
from nucleus by the Ran-GTP and ex-
portin 5 system through nuclear pores. In
the cytosol, a complex of the RNase3-Dic-
er and the transactivation response RNA-
binding protein cleaves the hairpin struc-
ture, resulting in a core RNA duplex of ap-
proximately 22 nt. Only one strand of this
duplex, the mature miRNA, is used fur-
ther for loading onto the silencing com-
plex consisting of Dicer/TRBP and the
Argonaute 2 protein. This RNA-induced
silencing complex (RISC) binds to mes-
senger RNA transcripts and regulates gene
expression by translational inhibition [3],
deadenylation [4] and degradation [5].
This review concentrates on the in-
volvement of miRNAs in the aging pro-
cess of adult stem cells. More detailed de-
scriptions of transcriptional regulation or
the RNAi machinery are not given here.
MSC aging and senescence
Mesenchymal stem cells (MSC) are adult,
multipotent stem cells, which can dif-
ferentiate to osteoblasts, chondrocytes
and adipocytes. Isolation of heterogen-
ic MSC populations has been performed
from various tissues such as bone marrow
(BM), adipose tissue, muscle and umbili-
cal cord blood (UCB), among others [6,
7]. The regenerative capacity of MSCs of-
fers huge potential to the field of regen-
erative medicine. New knowledge about
aging and senescence processes after pro-
longed cultivation will enable us to under-
stand problems behind in vitro expansion
of MSCs for clinical applications [8].
BM-MSC cultivation results in in-
creased miRNA (miR-371, miR-369-5p,
miR-29c, miR-499 and let-7f) due to pas-
sage effects and not due to senescence [9].
Expression of miR-369-5p, miR-371 and
miR-499 miRNAs reduces MSC prolifera-
tive potential. MiR-369-5p further impairs
adipogenic differentiation and down-reg-
ulates de novo DNA methyltransferase
DNMT3a, while miR-371 shows the op-
posite effects [10]. The role of miR-499 in
age-related up-regulation in MSCs is un-
known.
On the other hand, human UCB-
MSCs (hUCB-MSC) cultured to reach
replicative senescence showed a senes-
cence-dependent decrease in histone
deacetylases (HDACs), down-regulation
of high mobility group AT-hook 2 protein
(HMGA2), as well as increased expres-
sion of p16 (. Fig. 2), p21 and p27 [11].
HDACs are involved in the transcription-
al silencing of several miRNAs. Inhibition
of HDACs induces changes in chromatin
structure and increases the transcription
of pre-let-7a1, pre-let-7d, pre-let-7f1, pre-
miR-23a, pre-miR-26a and pre-miR-30a
in hUCB-MSCs [11]. Interestingly, oxida-
tive stress caused by H
2
O
2
induced senes-
cence and decreased HMGA2 level, but
lowered let-7a and miR-23a expression,
suggesting an additional mechanism be-
hind HMGA2 regulation. While p16 was
increased in senescence caused by pro-
longed passaging of hUCB-MSCs and
HDAC inhibition, there was no change
in p16 levels when cells were exposed to
H
2
0
2
. However, p21 expression was in-
duced by H
2
0
2
[11].
MiR-23a is involved in apoptosis and is
a negative regulator of PGC-1α [12]. The
peroxisome proliferator-activated recep-
tor (PPAR) gamma co-activator 1 (PGC-
1α) is involved in mitochondrial biogen-
esis and is induced by caloric restriction
in mice [13, 14, 15]. Increased miR-23a ex-
pression in senescent hUCB-MSCs could
indicate impairment of mitochondrial
biogenesis and function (. Fig. 2). A re-
cent study demonstrated that the mito-
chondrial deacetylase SIRT3 is a PGC-1α
downstream target. SIRT3 mediates ROS
protection and mitochondrial biogenesis
[16]. These results further illuminate the
positive association between SIRT3 pro-
tein and human longevity [17].
A publication by Hackl et al. high-
lights the importance of the involvement
of miRNA in aging and senescence. The
authors searched for differences and com-
monalities between replicative and organ-
ismal aging. In their model of MSC aging,
five miRNAs were down-regulated, four
of which belong to the polycistronic miR-
17~92 cluster that contains miR-19a, miR-
17, miR-19b, miR-20a [18, 19]. MiR-19 is
one of the most important members of
this cluster regarding oncogenic potential.
By inhibiting the expression of its target,
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