Micropatterning of living cells by laser-guided direct
writing: application to fabrication of hepatic–
endothelial sinusoid-like structures
Yaakov Nahmias
1
& David J Odde
2
1
Center for Engineering in Medicine, Massachusetts General Hospital, Harvard Medical School, 51 Blossom Street, Boston, Massachusetts 02114, USA.
2
Department of
Biomedical Engineering, University of Minnesota, 7-132 Nils Hasselmo Hall, 312 Church Street SE, Minneapolis, Minnesota 55455, USA. Correspondence should be
addressed to D.J.O. (oddex002@umn.edu).
Published online 21 December 2006; doi:10.1038/nprot.2006.386
Here, we describe a simple protocol for the design and construction of a laser-guided direct writing (LGDW) system able to
micropattern the self-assembly of liver sinusoid-like structures with micrometer resolution in vitro. To the best of our knowledge,
LGDW is the only technique able to pattern cells ‘‘on the fly’’ with micrometer precision on arbitrary matrices, including soft gels such
as Matrigel. By micropatterning endothelial cells on Matrigel, one can control the self-assembly of vascular structures and associated
liver tissue. LGDW is therefore uniquely suited for studying the role of tissue architecture and mechanical properties at the single-cell
resolution, and for studying the effects of heterotypic cell–cell interactions underlying processes such as liver morphogenesis,
differentiation and angiogenesis. The total time required to carry out this protocol is typically 7 h.
INTRODUCTION
The liver is one of the largest internal organs in the body,
accounting for 2% of the weight of an adult
1,2
. It has been ascribed
over 500 functions including albumin secretion, urea production,
bile clearance and glycogen storage. The liver also serves as a hub for
carbohydrate, lipid and amino-acid metabolism
3
. In addition to its
metabolic activity, the liver is one of the body’s first lines of defense,
inactivating toxins and xenobiotics, clearing foreign particles and
producing acute-phase proteins in response to injury or infection
4–10
.
Finally, the liver has the unique capacity to regenerate from massive
injuries, restoring to its original mass even if less than 20% of the
organ is undamaged
3,11,12
.
Loss of liver function causes 25,000 deaths per year in the United
States alone, and is one of the most frequent causes of death
worldwide
13
. The only known treatment for liver failure is ortho-
topic liver transplantation, but unfortunately only a fraction of the
organs needed are available (less than 7,000 organs per year in the
United States). This organ shortage has spurred research in the field
of hepatic tissue engineering aiming to create functional liver tissue
to support or even cure patients awaiting transplantation
14,15
.
Similar liver tissue engineering technology is also used in the
pharmaceutical industry, screening potential new drugs before
in vivo animal and human studies
6,7
, and for basic science including
the study of liver development
16
, regeneration
12
, ischemia/reperfu-
sion injury
17
, fibrosis
18
, viral infection
19
and inflammation
20
.
One of the principal limitations to hepatic tissue engineering is
oxygen and nutrient transport. Primary hepatocytes are highly
metabolic cells, consuming oxygen at rates as high as 0.9 nmol per
second per 10
6
cells
21,22
. This requirement has limited the size of
engineered liver tissue to the oxygen diffusion limit, B200 mm (see
ref. 23). One possible solution to this problem is to directly write
microscale endothelial vascular structures within the tissue engi-
neered liver, reconstructing the tissue cell-by-cell according to its
native architecture
24
. This technique has the advantage of recaptur-
ing the heterotypic cell–cell interactions found in the adult liver and
is shown to be important in maintaining liver function
25
and
differentiated phenotype
26,27
and in mediating its response to
infection and toxic challenge
28,29
.
LGDW
LGDW is a unique cellular patterning technique able to deposit cells
with micrometer accuracy on arbitrary matrices, including soft gels
such as collagen or Matrigel
30–33
. The unique ability of LGDW to
micropattern cells on the basement membrane Matrigel allows us
to use the intrinsic ability of endothelial cells to self-assemble into
vascular structures
34,35
for the assembly of the liver tissue.
At its core, LGDW is a variation of the commonly used optical
trap (laser tweezers, optical tweezers)
30,36
. Like an optical trap, the
system is composed of a single-mode (TEM
00
) laser, which is
focused by a lens onto a target area. Cells in the laser beam path
experience radiation forces owing to the scattering of photons by
the cell–media interface
36
. As cells have a higher refractive index
than that of their surrounding media, most of the photons will be
scattered away from the axis of the laser beam, causing an opposite
and equal force trapping the cells in the beam axis
36
. In contrast to
an optical trap, in LGDW, the laser beam is weakly focused to a spot
about 5 mm in radius, allowing cells to be pushed along the beam
axis until they are deposited on the surface
30
. By translating the
surface relative to the beam, one can write arbitrary patterns using
living cells
31
. In this case, LGDW resolution is only limited by the
size of the cells (B10 mm in diameter) and the magnitude of the
opposing thermal forces. As an added advantage, weakly focused
beams have a long working distance, several centimeters on average,
allowing the remote patterning of cells, under sterile conditions, in
standard tissue culture wells and dishes.
To avoid optical damage to cells, LGDW uses the near-infrared
part of the electromagnetic spectrum (700–1,000 nm), which is past
the absorption spectra of most proteins and before the infrared
absorption of water. Photons in this range of the spectrum lack the
energy to create free radicals (as in the ultraviolet) and are not
absorbed by DNA, suggesting that the laser has little chance of
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