In our laboratory we study the mechanical properties of cells and the mechanochemistry of cell adhesion. We are particularly interested in learning about the molecular mechanisms underlying the control of cell deformability and cell adhesion, and the role that mechanical forces and membrane stability play in both the formation and separation of adhesive contacts. Our fundamental approach is to perform mechanical measurements on individual cells or cell pairs to measure response of cells to applied forces or the probability of cell adhesion under controlled conditions. Our main focus is the study of cells in the peripheral vasculature. The deformability of circulating cells and adhesive interactions between cells in the vasculature has relevance to diverse aspects of human physiology ranging from oxygen delivery and hemolytic anemia, to atherosclerosis or immune response and inflammation. Historically, our lab has been one of the leading facilities for investigating red blood cell mechanical properties and the stability of biological membranes. More recently we have begun to examine the physical mechanisms underlying neutrophil adhesion to endothelium, a key event in the body's response to infection or injury. Another area of interest is in the late stage maturation of red blood cells. We have observed changes in the mechanical properties that occur as red cells develop and mature. We are working on developing methods to observe the maturation of red cells in culture so that we can follow the maturation process in the laboratory. By correlating changes in mechanical stability with the appearance and assembly of cytoskeletal proteins we can deduce which molecules and what interactions are important for developing proper mechanical function. Maintaining mechanical stability appears to be critical for the successful completion of red blood cell maturation, as it appears that instabilities in the cell surface lead to loss of cell membrane and cell death if the membranes are not properly supported mechanically as they mature.

• Hyun YM, Sumagin R, Sarangi PP, Lomakina E, Overstreet MG, Baker CM, Fowell DJ, Waugh RE, Sarelius IH, Kim M. Uropod elongation is a common final step in leukocyte extravasation through inflamed vessels. J Exp Med. 2012 Jul 2; 209(7):1349-62.
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• Baker CM, Comrie WA, Hyun YM, Chung HL, Fedorchuk CA, Lim K, Brakebusch C, McGrath JL, Waugh RE, Meier-Schellersheim M, Kim M. Opposing roles for RhoH GTPase during T-cell migration and activation. Proc Natl Acad Sci U S A. 2012 Jun 26; 109(26):10474-9.
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• Gregoire S, Xiao J, Silva BB, Gonzalez I, Agidi PS, Klein MI, Ambatipudi KS, Rosalen PL, Bauserman R, Waugh RE, Koo H. Role of glucosyltransferase B in interactions of Candida albicans with Streptococcus mutans and with an experimental pellicle on hydroxyapatite surfaces. Appl Environ Microbiol. 2011 Sep; 77(18):6357-67.
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• Sumagin R, Prizant H, Lomakina E, Waugh RE, Sarelius IH. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J Immunol. 2010 Dec 1; 185(11):7057-66.
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• Gaborski TR, Sealander MN, Ehrenberg M, Waugh RE, McGrath JL. Image correlation microscopy for uniform illumination. J Microsc. 2010 Jan; 237(1):39-50.
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• Lefort CT, Hyun YM, Schultz JB, Law FY, Waugh RE, Knauf PA, Kim M. Outside-in signal transmission by conformational changes in integrin Mac-1. J Immunol. 2009 Nov 15; 183(10):6460-8.
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• Hocdé SA, Hyrien O, Waugh RE. Molecular accessibility in relation to cell surface topography and compression against a flat substrate. Biophys J. 2009 Jul 8; 97(1):369-78.
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• Hocdé SA, Hyrien O, Waugh RE. Cell adhesion molecule distribution relative to neutrophil surface topography assessed by TIRFM. Biophys J. 2009 Jul 8; 97(1):379-87.
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• Hyun YM, Chung HL, McGrath JL, Waugh RE, Kim M. Activated integrin VLA-4 localizes to the lamellipodia and mediates T cell migration on VCAM-1. J Immunol. 2009 Jul 1; 183(1):359-69.
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• Lomakina E, Knauf PA, Schultz JB, Law FY, McGraw MD, Waugh RE. Activation of human neutrophil Mac-1 by anion substitution. Blood Cells Mol Dis. 2009 May-Jun; 42(3):177-84.
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• Lomakina EB, Waugh RE. Adhesion between human neutrophils and immobilized endothelial ligand vascular cell adhesion molecule 1: divalent ion effects. Biophys J. 2009 Jan; 96(1):276-84.
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• Waugh RE, Lomakina EB. Active site formation, not bond kinetics, limits adhesion rate between human neutrophils and immobilized vascular cell adhesion molecule 1. Biophys J. 2009 Jan; 96(1):268-75.
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• Kaba NK, Schultz J, Law FY, Lefort CT, Martel-Gallegos G, Kim M, Waugh RE, Arreola J, Knauf PA. Inhibition of Na+/H+ exchanger enhances low pH-induced L-selectin shedding and beta2-integrin surface expression in human neutrophils. Am J Physiol Cell Physiol. 2008 Nov; 295(5):C1454-63.
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• Gaborski TR, Clark A, Waugh RE, McGrath JL. Membrane mobility of beta2 integrins and rolling associated adhesion molecules in resting neutrophils. Biophys J. 2008 Nov 15; 95(10):4934-47.
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• Butler J, Mohandas N, Waugh RE. Integral protein linkage and the bilayer-skeletal separation energy in red blood cells. Biophys J. 2008 Aug; 95(4):1826-36.
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• Tober J, Koniski A, McGrath KE, Vemishetti R, Emerson R, de Mesy-Bentley KK, Waugh R, Palis J. The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood. 2007 Feb 15; 109(4):1433-41.
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• Lomakina EB, Waugh RE. Dynamics of increased neutrophil adhesion to ICAM-1 after contacting immobilized IL-8. Ann Biomed Eng. 2006 Oct; 34(10):1553-63.
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• Hammer DA, Waugh RE. Teaching cellular engineering. Ann Biomed Eng. 2006 Feb; 34(2):253-6.
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• Lomakina EB, Spillmann CM, King MR, Waugh RE. Rheological analysis and measurement of neutrophil indentation. Biophys J. 2004 Dec; 87(6):4246-58.
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• Spillmann CM, Lomakina E, Waugh RE. Neutrophil adhesive contact dependence on impingement force. Biophys J. 2004 Dec; 87(6):4237-45.
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• Svetina S, Kuzman D, Waugh RE, Ziherl P, Zeks B. The cooperative role of membrane skeleton and bilayer in the mechanical behaviour of red blood cells. Bioelectrochemistry. 2004 May; 62(2):107-13.
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• Lomakina EB, Waugh RE. Micromechanical tests of adhesion dynamics between neutrophils and immobilized ICAM-1. Biophys J. 2004 Feb; 86(2):1223-33.
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• Kuzman D, Svetina S, Waugh RE, Zeks B. Elastic properties of the red blood cell membrane that determine echinocyte deformability. Eur Biophys J. 2004 Feb; 33(1):1-15.
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• He X, Liu Y, Sharma V, Dirksen RT, Waugh R, Sheu SS, Min W. ASK1 associates with troponin T and induces troponin T phosphorylation and contractile dysfunction in cardiomyocytes. Am J Pathol. 2003 Jul; 163(1):243-51.
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• Spillmann C, Osorio D, Waugh R. Integrin activation by divalent ions affects neutrophil homotypic adhesion. Ann Biomed Eng. 2002 Sep; 30(8):1002-11.
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• Raphael RM, Waugh RE, Svetina S, Zeks B. Fractional occurrence of defects in membranes and mechanically driven interleaflet phospholipid transport. Phys Rev E Stat Nonlin Soft Matter Phys. 2001 Nov; 64(5 Pt 1):051913.
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• Waugh RE, Mantalaris A, Bauserman RG, Hwang WC, Wu JH. Membrane instability in late-stage erythropoiesis. Blood. 2001 Mar 15; 97(6):1869-75.
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• Tees DF, Waugh RE, Hammer DA. A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys J. 2001 Feb; 80(2):668-82.
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• Murdock RC, Reynolds C, Sarelius IH, Waugh RE. Adaptation and survival of surface-deprived red blood cells in mice. Am J Physiol Cell Physiol. 2000 Oct; 279(4):C970-80.
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• Tsai MA, Waugh RE, Keng PC. Passive mechanical behavior of human neutrophils: effects of colchicine and paclitaxel. Biophys J. 1998 Jun; 74(6):3282-91.
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• Svetina S, Zeks B, Waugh RE, Raphael RM. Theoretical analysis of the effect of the transbilayer movement of phospholipid molecules on the dynamic behavior of a microtube pulled out of an aspirated vesicle. Eur Biophys J. 1998; 27(3):197-209.
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• Hwang WC, Waugh RE. Energy of dissociation of lipid bilayer from the membrane skeleton of red blood cells. Biophys J. 1997 Jun; 72(6):2669-78.
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• Waugh RE, McKenney JB, Bauserman RG, Brooks DM, Valeri CR, Snyder LM. Surface area and volume changes during maturation of reticulocytes in the circulation of the baboon. J Lab Clin Med. 1997 May; 129(5):527-35.
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• Waugh RE, Sarelius IH. Effects of lost surface area on red blood cells and red blood cell survival in mice. Am J Physiol. 1996 Dec; 271(6 Pt 1):C1847-52.
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• Raphael RM, Waugh RE. Accelerated interleaflet transport of phosphatidylcholine molecules in membranes under deformation. Biophys J. 1996 Sep; 71(3):1374-88.
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• Heinrich V, Waugh RE. A piconewton force transducer and its application to measurement of the bending stiffness of phospholipid membranes. Ann Biomed Eng. 1996 Sep-Oct; 24(5):595-605.
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• Tsai MA, Waugh RE, Keng PC. Cell cycle-dependence of HL-60 cell deformability. Biophys J. 1996 Apr; 70(4):2023-9.
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• Waugh RE. Elastic energy of curvature-driven bump formation on red blood cell membrane. Biophys J. 1996 Feb; 70(2):1027-35.
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• Khodadad JK, Waugh RE, Podolski JL, Josephs R, Steck TL. Remodeling the shape of the skeleton in the intact red cell. Biophys J. 1996 Feb; 70(2):1036-44.
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• Tsai MA, Waugh RE, Keng PC. Changes in HL-60 cell deformability during differentiation induced by DMSO. Biorheology. 1996 Jan-Feb; 33(1):1-15.
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• Waugh RE, Hwang WC, Sarelius IH. Combined use of fluorescence microscopy and micromechanical measurement to assess cell and membrane properties. Pflugers Arch. 1996; 431(6 Suppl 2):R271-2.
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• Waugh RE, Bauserman RG. Physical measurements of bilayer-skeletal separation forces. Ann Biomed Eng. 1995 May-Jun; 23(3):308-21.
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• Tsai MA, Frank RS, Waugh RE. Passive mechanical behavior of human neutrophils: effect of cytochalasin B. Biophys J. 1994 Jun; 66(6):2166-72.
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• Tsai MA, Frank RS, Waugh RE. Passive mechanical behavior of human neutrophils: power-law fluid. Biophys J. 1993 Nov; 65(5):2078-88.
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• Song J, Waugh RE. Bending rigidity of SOPC membranes containing cholesterol. Biophys J. 1993 Jun; 64(6):1967-70.
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• Bozic B, Svetina S, Zeks B, Waugh RE. Role of lamellar membrane structure in tether formation from bilayer vesicles. Biophys J. 1992 Apr; 61(4):963-73.
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• Waugh RE, Song J, Svetina S, Zeks B. Local and nonlocal curvature elasticity in bilayer membranes by tether formation from lecithin vesicles. Biophys J. 1992 Apr; 61(4):974-82.
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• Waugh RE, Narla M, Jackson CW, Mueller TJ, Suzuki T, Dale GL. Rheologic properties of senescent erythrocytes: loss of surface area and volume with red blood cell age. Blood. 1992 Mar 1; 79(5):1351-8.
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• Waugh RE. Reticulocyte rigidity and passage through endothelial-like pores. Blood. 1991 Dec 1; 78(11):3037-42.
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• Song J, Waugh RE. Bilayer membrane bending stiffness by tether formation from mixed PC-PS lipid vesicles. J Biomech Eng. 1990 Aug; 112(3):235-40.
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• Katnik C, Waugh R. Electric fields induce reversible changes in the surface to volume ratio of micropipette-aspirated erythrocytes. Biophys J. 1990 Apr; 57(4):865-75.
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• Katnik C, Waugh R. Alterations of the apparent area expansivity modulus of red blood cell membrane by electric fields. Biophys J. 1990 Apr; 57(4):877-82.
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• Waugh RE, Erwin G. Flexural rigidity of marginal bands isolated from erythrocytes of the newt. J Cell Biol. 1989 May; 108(5):1711-6.
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• Bo L, Waugh RE. Determination of bilayer membrane bending stiffness by tether formation from giant, thin-walled vesicles. Biophys J. 1989 Mar; 55(3):509-17.
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• Waugh RE, Agre P. Reductions of erythrocyte membrane viscoelastic coefficients reflect spectrin deficiencies in hereditary spherocytosis. J Clin Invest. 1988 Jan; 81(1):133-41.
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• Shields M, La Celle P, Waugh RE, Scholz M, Peters R, Passow H. Effects of intracellular Ca2+ and proteolytic digestion of the membrane skeleton on the mechanical properties of the red blood cell membrane. Biochim Biophys Acta. 1987 Nov 27; 905(1):181-94.
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• Waugh RE, Hochmuth RM. Mechanical equilibrium of thick, hollow, liquid membrane cylinders. Biophys J. 1987 Sep; 52(3):391-400.
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• Waugh RE. Effects of inherited membrane abnormalities on the viscoelastic properties of erythrocyte membrane. Biophys J. 1987 Mar; 51(3):363-9.
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• Hochmuth RM, Waugh RE. Erythrocyte membrane elasticity and viscosity. Annu Rev Physiol. 1987; 49:209-19.
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• Waugh RE, Erwin G, Bouzid A. Measurement of the extensional and flexural rigidities of a subcellular structure: marginal bands isolated from erythrocytes of the newt. J Biomech Eng. 1986 Aug; 108(3):201-7.
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• Waugh RE. Effects of 2,3-diphosphoglycerate on the mechanical properties of erythrocyte membrane. Blood. 1986 Jul; 68(1):231-8.
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• Waugh RE, Sassi M. An in vitro model of erythroid egress in bone marrow. Blood. 1986 Jul; 68(1):250-7.
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• Waugh RE, Hsu LL, Clark P, Clark A. Analysis of cell egress in bone marrow. Kroc Found Ser. 1984; 16:221-36.
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• Waugh RE. Effects of abnormal cytoskeletal structure on erythrocyte membrane mechanical properties. Cell Motil. 1983; 3(5-6):609-22.
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• Waugh RE. Temperature dependence of the yield shear resultant and the plastic viscosity coefficient of erythrocyte membrane. Implications about molecular events during membrane failure. Biophys J. 1982 Sep; 39(3):273-8.
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• Waugh RE. Surface viscosity measurements from large bilayer vesicle tether formation. II. Experiments. Biophys J. 1982 Apr; 38(1):29-37.
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• Waugh RE. Surface viscosity measurements from large bilayer vesicle tether formation. I. Analysis. Biophys J. 1982 Apr; 38(1):19-27.
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• Waugh RE, La Celle PL. Abnormalities in the membrane material properties of hereditary spherocytes. J Biomech Eng. 1980 Aug; 102(3):240.
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• Waugh R, Evans EA. Thermoelasticity of red blood cell membrane. Biophys J. 1979 Apr; 26(1):115-31.
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• Evans EA, Waugh R. Osmotic correction to elastic area compressibility measurements on red cell membrane. Biophys J. 1977 Dec; 20(3):307-13.
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• Waugh R, Evans EA. Viscoelastic properties of erythrocyte membranes of different vertebrate animals. Microvasc Res. 1976 Nov; 12(3):291-304.
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• Evans EA, Waugh R, Melnik L. Elastic area compressibility modulus of red cell membrane. Biophys J. 1976 Jun; 16(6):585-95.
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