ARTICLES
Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, 75 Francis Street, Boston, Massachusetts, 02115 USA. Correspondence
should be addressed to V.J.D. (vdzau@partners.org).
Published online 10 August 2003; doi:10.1038/nm912
NATURE MEDICINE VOLUME 9 | NUMBER 9 | SEPTEMBER 2003 1195
Prolonged interruption of myocardial blood flow initiates events that
culminate in cardiac myocyte death
1
. Proposed endogenous reparative
mechanisms include cardiac myocyte hypertrophy
2
and hyperplasia
3
and the trafficking of bone marrow–derived stem cells (BMCs) to the
myocardium for repair and angiogenesis
4,5
. None of these proposed
mechanisms are adequate in restoring lost myocardium or sustaining
cardiac function. Harvesting BMCs followed by direct injection into
ischemic myocardium results in angiogenesis and myogenesis
6–8
, but
functional improvement is incomplete. It is unclear whether trans-
plantation of BMCs affects repair of the ischemic myocardium pri-
marily by angioblast-mediated vasculogenesis
9,10
, which prevents
apoptosis of native cardiac myocytes, or by direct regeneration of the
lost myocytes.
Mesenchymal stem cells (MSCs) are self-renewing, clonal pre-
cursors of non-hematopoietic tissues. They are expandable in culture
and multipotent, and can differentiate into osteoblasts
11
, chondro-
cytes
11
, astrocytes
12
, neurons
13
and skeletal muscle
14
. Several groups
have reported that putative MSCs derived from bone marrow can dif-
ferentiate into cardiac muscle in vitro
15
and in vivo
16,17
. However, it has
been observed that transplantation of as many as 6 × 10
7
of these puta-
tive MSCs into infarcted porcine hearts yielded only marginal
improvement in cardiac function
17
. This is explained at least in part by
poor viability of the transplanted cells. It has been estimated that
>99% of MSCs die 4 d after transplantation into uninjured nude-
mouse hearts
16
. Cell transplantation strategies to replace lost
myocardium are limited by the inability to deliver large numbers of
cells that resist peritransplantation graft cell death
17–20
.
Accordingly, we set out to isolate and expand a highly purified pop-
ulation of adult rat bone marrow–derived MSCs, and to engineer these
cells to overexpress Akt, a serine threonine kinase and powerful sur-
vival signal in many systems
21,22
, to test the hypothesis that Akt-
engineered MSCs are more resistant to apoptosis and can enhance
cardiac repair after transplantation into the ischemic rat heart. Our
results documented significant retention of Akt-MSCs in the ischemic
heart that was associated with inhibition of cardiac remodeling, a
greater volume of regenerated myocardium, and near-complete
normalization of systolic and diastolic cardiac function.
RESULTS
MSCs express markers distinct from hematopoietic stem cells
MSCs proliferated in mixed culture with hematopoietic cells, yielding
5 × 10
6
cells by day 15 of culture. We separated MSCs from hematopoi-
etic cells based on their preferential attachment to polystyrene sur-
faces
23
. By immunocytochemistry, over 99% of MSCs expressed CD29,
CD71, CD90, CD106 and CD117 (Fig. 1); 60% expressed Ki67 and 15%
expressed the transcription factors Nkx2.5 (Fig. 1) and Gata-4 (data
not shown). MSCs did not express the hematopoietic markers CD34
and CD45 (Fig. 1) or the cardiac-specific markers myosin heavy chain
(MHC), myosin light chain (MLC), cardiac troponin I (CTnI), α-sarc-
omeric-actin (αSA) or MEF-2 (data not shown). In addition, MSCs
also expressed the gap junction protein connexin-43 as verified by RT-
PCR (data not shown). We further purified MSCs using negative para-
magnetic bead sorting targeting CD34, resulting in a population that
was >99.9% pure.We were unable to induce these MSCs to differentiate
into megakaryocytes and erythroid cells using described methods
24
.
Increased Akt activity protects against MSC apoptosis
We used retroviruses to transduce MSCs with genes expressing green
Mesenchymal stem cells modified with Akt prevent
remodeling and restore performance of infarcted hearts
Abeel A Mangi, Nicolas Noiseux, Deling Kong, Huamei He, Mojgan Rezvani, Joanne S Ingwall & Victor J Dzau
Transplantation of adult bone marrow–derived mesenchymal stem cells has been proposed as a strategy for cardiac repair following
myocardial damage. However, poor cell viability associated with transplantation has limited the reparative capacity of these cells
in vivo. In this study, we genetically engineered rat mesenchymal stem cells using ex vivo retroviral transduction to overexpress
the prosurvival gene Akt1 (encoding the Akt protein). Transplantation of 5 × 10
6
cells overexpressing Akt into the ischemic rat
myocardium inhibited the process of cardiac remodeling by reducing intramyocardial inflammation, collagen deposition and
cardiac myocyte hypertrophy, regenerated 80–90% of lost myocardial volume, and completely normalized systolic and diastolic
cardiac function. These observed effects were dose (cell number) dependent. Mesenchymal stem cells transduced with Akt1
restored fourfold greater myocardial volume than equal numbers of cells transduced with the reporter gene lacZ. Thus,
mesenchymal stem cells genetically enhanced with Akt1 can repair infarcted myocardium, prevent remodeling and nearly
normalize cardiac performance.
© 2003 Nature Publishing Group http://www.nature.com/naturemedicine