Abstract

We have used optical tweezers to trap normal and Plasmodium-infected red blood cells (iRBCs). Two different facets of the behavior of RBCs in infrared light fields emerge from our experiments. Firstly, while the optical field modifies both types of RBCs in the same fashion, by folding the original biconcave disk into a rod-like shape, iRBCs rotate with linearly polarized light whereas normal RBCs do not. Secondly, and in the context of known molecular motors, our measurements indicate that the torque of rotating iRBCs is up to three orders of magnitude larger.

© 2004 Optical Society of America

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    [CrossRef] [PubMed]

Adv. Parasitol. (1)

B.M. Cooke, N. Mohandas, and R.L. Coppel, �??The malaria-infected red blood cell: structural and functional changes,�?? Adv. Parasitol. 50, 1-86 (2001).
[CrossRef]

Am. J. Physiol. Cell Physiol. (1)

H.M. Staines, J.C. Ellory, and K. Kirk, �??Perturbation of the pump-leak balance of Na+ and K+ in malariainfected erythrocytes,�?? Am. J. Physiol. Cell Physiol. 380, C1575-C1587 (2001).

Biophys. J. (2)

A.J. Hunt, F. Gittes, and J. Howard, �??The force exerted by a single kinesin molecule against a viscous load,�?? Biophys. J. 67, 766-781 (1994).
[CrossRef] [PubMed]

S. Henon, G. Lenormand, A. Richert, and F. Gallet, �??A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers,�?? Biophys. J. 76, 1145-1151 (1999).
[CrossRef] [PubMed]

Biorheology Suppl. (1)

H.G. Roggenkamp, F. Jung, R. Schneider, and H. Kiesewetter, �??A new device for the routine measurement of erythrocyte deformability,�?? Biorheology Suppl. 1, 241-243 (1984).
[PubMed]

Blood Cells, Molecules and Diseases (1)

A. Krantz, �??Red-cell mediated therapy: opportunities and challenges,�?? Blood Cells, Molecules and Diseases 23, 58-68 (1997).
[CrossRef]

Cell Phys. Biochem. (1)

C. Duranton, S.M. Huber, V. Tanneur, K.S. Lang, B.B. Brand, C.D. Sandu, and F. Lang, �??Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes,�?? Cell Phys. Biochem. 13, 189-198 (2003).
[CrossRef]

Cell. Mol. Biol. (2)

K. Schutze, G. Posl, and G. Lahr, �??Laser micromanipulation systems as universal tools in cellular and molecular biology and in medicine,�?? Cell. Mol. Biol. 44, 735-746 (1998).
[PubMed]

M. Zahn, and S. Seeger, �??Optical tweezers in pharmacology,�?? Cell. Mol. Biol. 44, 747-761 (1998).
[PubMed]

FEBS Lett. (1)

M. Zahn, J. Renken, and S. Seeger, �??Fluorimetric multiparameter cell assay at the single cell level fabricated by optical tweezers,�?? FEBS Lett. 443, 337-340 (1999).
[CrossRef] [PubMed]

Immunol. Rev. (1)

K. Ley, �??Integration of inflammatory signals by rolling neutrophils,�?? Immunol. Rev. 186, 8-18 (2002).
[CrossRef] [PubMed]

J. Assisted Reproduction Genetics (1)

A. Clement-Sengewald, K. Schutze, A. Ashkin, G.A. Palma, G. Kerlen, and G. Brem, �??Fertilization of bovine oocytesinduced solely with combined laser microbeam and optical tweezers,�?? J. Assisted Reproduction Genetics 13, 259-265 (1996).
[CrossRef]

J. Biol. Chem. (1)

A. Goswami, S. Singh, V.D. Redkar, and S. Sharma, �??Characterization of P0, a ribosomal phosphoprotein of Plasmodium falciparum,�?? J. Biol. Chem. 272, 12138-12143 (1997).
[CrossRef] [PubMed]

J. Parasitol. (1)

C. Lambros, and J.P. Vanderberg, �??Synchronization of Plasmodium falciparum erythrocytic stages in culture,�?? J. Parasitol. 65, 418-420 (1979).
[CrossRef] [PubMed]

Membr. Biochem. (1)

F.F. Vargas, M.H. Osorio, U.S. Ryan, and M. De Jesus, �??Surface charge of endothelial cells estimated from electrophoretic mobility,�?? Membr. Biochem. 8, 221-227 (1989).
[CrossRef] [PubMed]

Nature (5)

B.T. Marshall, M. Long, J.W. Piper, T. Yago, R.P. McEver, and C. Zhu, �??Direct observation of catch bonds involving cell-adhesion molecules,�?? Nature 423, 190-193 (2003).
[CrossRef] [PubMed]

M.E.J. Friese, T.A. Nieminen, R.N. Heckenberg, and H. Rubinsztein-Dunlop, �??Optical alignment and spinning of laser-trapped microscopic particles,�?? Nature 394, 348-350 (1998).
[CrossRef]

H. Noji., R. Yasuda., M. Yoshida, and K. Kinosita, �??Direct observation of the rotation of F1-ATPase,�?? Nature 386, 299-302 (1997).
[CrossRef] [PubMed]

W.S. Ryu, R.M. Berry, and H.C. Berg, �??Torque generating units of the flagellar motor of Escherichia coli have a high duty ratio,�?? Nature 403, 444-447 (2000).
[CrossRef] [PubMed]

C. Bustamante, Z. Bryant, and S.B. Smith, �??Ten years of tension: single-molecule DNA mechanics,�?? Nature 421, 423-427 (2003).
[CrossRef] [PubMed]

Opt. Lett. (2)

Phil. Trans. Roy. Soc. London B (1)

K. Kinosita Jr., R.Yasuda, H. Noji, and K. Adachi, �??A rotary molecular motor that can work at near 100% efficiency,�?? Phil. Trans. Roy. Soc. London B 355, 473-489 (2000).
[CrossRef] [PubMed]

Phys. Rev. (1)

R.A. Beth, �??Mechanical detection and measurement of the angular momentum of light,�?? Phys. Rev. 50, 115-125 (1936).
[CrossRef]

Phys. Rev. A (1)

M.E.J. Friese, J. Enger, H. Rubinsztein-Dunlop, and R.N. Heckenberg, �??Optical angular-momentum transfer to trapped absorbing particles,�?? Phys. Rev. A 54, 1593-1596 (1996).
[CrossRef] [PubMed]

PNAS (1)

J.P. Shelby, J. White, K. Ganeshan, P.K. Rathod, and D.T. Chiu, �??A microfluidic model for single-cell capillary obstruction by Plasmodium falcipuram-infected erythrocytes,�?? PNAS 100, 14618-14622 (2003).
[CrossRef] [PubMed]

Science (2)

H.A. Cranston, C.W. Boylan, G.L. Carroll, S.P. Sutera, J.R. Williamson, I.Y. Gluzman, and D.J. Krogstad, �??Plasmodium falcipuram maturation abolishes Physiologic Red cell deformability,�?? Science 223, 400-403 (1984).
[CrossRef] [PubMed]

L. Paterson, M.P. MacDonald, J. Arlt, W. Sibbett, P.E. Bryant, and K. Dholakia, �??Controlled rotation of optically-trapped microscopic particles,�?? Science 292, 912-914 (2001)
[CrossRef] [PubMed]

Other (1)

L.D. Landau, and E.M. Lifshitz, Theory of elasticity, (Pergamon Press, New York, 1959) p. 56.

Supplementary Material (4)

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Figures (3)

Fig. 1.
Fig. 1.

Time evolution of folding (334 KB) and unfolding (1.04 MB) of red blood cells (RBCs) infected with Plasmodium falciparum [29] in an optical trap using a linearly polarized infrared laser. Panel a shows the initial state where an infected RBC approaches the laser focus (ca. 1 µm diameter). Panels b and c show the trapped RBC undergoing folding and twisting due to polarization-induced optical forces such that a rod-like shape is achieved within ~2 s. On removal of the laser beam, unfolding to the original shape occurs (panels d-f) on a longer time scale.

Fig. 2.
Fig. 2.

Discrete frames from a movie (1.29 MB) depicting rotation of an infected RBC in the optical trap. The arrow helps identify the direction of rotation. Times associated with each frame are indicated; the speed of rotation was 120 revolutions per minute (rpm). The rotational speeds achieved in these experiments covered the range 19–300 rpm. The untrapped cells visible in the frames were outside the laser focus and underwent Brownian motion.

Fig. 3.
Fig. 3.

Controlling the sense of rotation by altering the position of the infected RBC with respect to the focal plane of laser beam. If the cell is at position a), anti-clockwise rotation is observed (1.29 MB). The cell at position b) rotates in clockwise direction (1.20 MB). The rotational speeds remain the same as long as laser power does not change. The k-vector (see text) is along the laser propagation direction while the E-vector lies perpendicular to it but in the same plane.

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