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On the recovery of adhesiveness by trypsin-dissociated cells

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Summary

A sensitive method for assaying aggregation of dissociated cells has been developed which allows the determination of the mean number of cells per aggregate of a cell population. We have demonstrated that exposure of dissociated 6- or 7-day chick embryo neural retinal cells to trypsin in calcium-free solution renders them unable to aggregate for a half hour in stirred cell suspensions. Aggregation was noticeable first at 30 to 40 minutes and, progressed to the formation of massive compact aggregates. Because the half-hour aggregation lag occurred both in the absence of serum and in medium reclaimed from aggregated preparations, the possibilities were excluded that it was due either to an inhibitor of aggregation in the serum, or was the time required for release into the medium of soluble aggregation-promoting materials emanating from the cells themselves. Cells dissociated by divalent cation withdrawal (Ca++, Mg++-free saline with EDTA) aggregated without a lag. The trypsin-induced lag does not appear to be the result of trypsin adsorbed to the, surfaces of dissociated cells, as the lag is not abolished by addition of trypsin inhibitors to the aggregation medium. Microelectrophoresis of dissociated cells did not reveal changes in surface charge density during recovery from trypsinization. A variety of proteins and calcium ion, if present during trypsinization, protect the cells against the trypsin-induced aggregation lag. If the temperature was reduced from 37 to 6°C, aggregation of fully adhesive cell populations came to a complete halt within 2 to 3 minutes. Aggregation resumed with a 5 to 10 minute delay when the temperature was returned to 37°C. The rapidity of onset and reversal of inhibition of aggregation by low temperature treatment militates against the hypothesis that the low-temperature inhibition of aggregation acts by suppressing the synthesis of cell surface components necessary for adhesion. The abolition of the aggregation lag in trypsinized cells was also shown to be temperature-dependent; a 20-minute cold, pulse administered in the middle of the lag period extended the length of the lag by exactly 20 minutes.

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References

  • Abramson, H. A., Moyer, L. S., Gorin, M. H. 1942. Electrophoresis of Proteins, pp. 13–37. Reinhold, New York

    Google Scholar 

  • Aketa, K., Onitake, K., Tsuzuki, H. 1972. Tryptic disruption, of sperm-binding site of sea urchin egg surface.Exp. Cell Res. 71:27

    PubMed  Google Scholar 

  • Allen, A., Snow, C. 1970. The effect of trypsin and ethylendiamene-tetraacetate on the surface of cells in tissue culture.Biochem. J. 117:32P

    Google Scholar 

  • Armstrong, P. B. 1966. On the role of metal cations in cellular adhesion: Effect on cell surface charge.J. Exp. Zool. 163:99

    PubMed  Google Scholar 

  • Armstrong, P. B. 1970. A fine structural study of adhesive cell junctions in heterotypic cell aggregates.J. Cell Biol. 47:197

    PubMed  Google Scholar 

  • Armstrong, P. B. 1971. Light and electron microscope studies of cell sorting in combinations of chick embryo neural retina and retinal pigment epithelium.Wilhelm Roux' Archiv 168:125

    Google Scholar 

  • Bangham, A. D., Flemans, R., Heard, D. H., Seaman, G. V. F. 1958. An apparatus for microelectrophoresis of small particles.Nature 182:642

    PubMed  Google Scholar 

  • Barnard, P. J., Weiss, L., Ratcliff, T. 1969. Changes in the surface properties of embryonic chick neural retinal cells after dissociation.Exp. Cell Res. 54:293

    PubMed  Google Scholar 

  • Boeryd, B., Lundin, P. M., Norrby, K., Schelin, U. 1967. Ultrastructure of a mouse sarcoma in its solid, enzymatically dissociated, and ascitic forms.Acta Path. Microbiol. Scand., suppl.187:7

    Google Scholar 

  • Branton, D., Deamer, D. W. 1972. Membrane structure.Protoplasmatologia II. E.1:1

    Google Scholar 

  • Brent, T. P., Forrester, J. A. 1967. Changes in surface charge of HeLa cells during the cell cycle.Nature 215:92

    PubMed  Google Scholar 

  • Burger, M. M. 1969. A difference in the architecture of the surface membrane of normal and virally transformed cells.Proc. Nat. Acad. Sci. 62:994

    PubMed  Google Scholar 

  • Burger, M. M. 1970. Proteolytic enzymes initiating cell division and escape from contact inhibition of growth.Nature 227:170

    PubMed  Google Scholar 

  • Codington, J. F., Sanford, B. H., Jeanlog, R. W. 1970. Glycoprotein coat of the TA3 cell. I. Removal of carbohydrate and protein material from viable cells.J. Nat. Cancer Inst. 45:637

    PubMed  Google Scholar 

  • Collins, M. F. 1966. Electrokinetic properties of dissociated chick embryo cells. I. pH-surface charge relationships and the effect of calcium ions.J. Exp. Zool. 163:23

    PubMed  Google Scholar 

  • Cook, G. M. W., Heard, D. H., Seaman, G. V. F. 1960. A sialomucopeptide liberated by trypsin from the human erythrocyte.Nature 188:1011

    PubMed  Google Scholar 

  • Coon, H. G. 1966. Clonal stability and phenotypic expression of chick cartilage cells in vitro.Proc. Nat. Acad. Sci. 55:66

    PubMed  Google Scholar 

  • Curtis, A. S. G. 1962. Cell contact and adhesion.Biol. Rev. 37:82

    PubMed  Google Scholar 

  • Curtis, A. S. G. 1969. The measurement of cell adhesiveness by an absolute method.J. Embryol. 22:305

    Google Scholar 

  • Curtis, A. S. G. 1970. On the occurrence of specific adhesion between cells.J. Embryol. 23:253

    Google Scholar 

  • Curtis, A. S. G., Greaves, M. F. 1965. The inhibition of cell aggregation by a pure serum protein.J. Embryol. 13:309

    Google Scholar 

  • Dalen, H., Todd, P. W. 1971. Surface morphology of trypsinized human cellsin vitro.Exp. Cell Res. 66:353

    PubMed  Google Scholar 

  • Dunn, M. J., Owen, E., Kemp, R. B. 1970. Studies on the mechanism underlying the inhibiton by puromycin of cell aggregationin vitro.J. Cell Sci. 7:557

    PubMed  Google Scholar 

  • Eagle, H. 1959. Amino acid metabolism in mammalian cell cultures.Science 130:432

    PubMed  Google Scholar 

  • Easty, G. C., Easty, D. M., Ambrose, E. J. 1960. Studies of cellular adhesiveness.Exp. Cell Res. 19:539

    PubMed  Google Scholar 

  • Easty, G. C., Mutolo, V. 1960. The nature of the intercellular material of adult mammalian tissues.Exp. Cell Res. 21:371

    Google Scholar 

  • Ede, D. A., Agerbak, G. S. 1968. Cell adhesion and movement in relation to the developing limb pattern in normal andtalpid 3 mutant chick embryo.J. Embryol. 20:81

    Google Scholar 

  • Edidin, M. 1966. The release of soluble H-2 alloantigens during disaggregation of mouse embryo tissue by a chelating agent.J. Embryol. 16:519

    Google Scholar 

  • Edwards, G. A., Fogh, J. 1959. Micromorphologic changes in human amnion cells during trypsinization.Cancer Res. 19:608

    PubMed  Google Scholar 

  • Engel, M. B., Pumper, R. W., Joseph, N. R. 1968. Electrometric determination of surface charge of cultured mammalian cells.Proc. Soc. Exp. Biol., N. Y. 128:990

    Google Scholar 

  • Feldman, M. 1955. Dissociation and reaggregation of embryonic cells ofTriturus alpestris.J. Embryol. 3:251

    Google Scholar 

  • Fischer, H. W., Puck, T. T., Sato, G. 1958. Molecular growth requirements of single mammalian cells: The action of fetuin in promoting cell attachment to glass.Proc. Nat. Acad. Sci. 44:4

    Google Scholar 

  • Forstner, G. G. 1971. Release of intestinal surface-membrane glycoproteins associated with enzyme activity by brief digestion with papain.Biochem. J. 121:781

    PubMed  Google Scholar 

  • Frye, L. D., Edidin, M. 1970. The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons.J. Cell Sci. 7:319

    PubMed  Google Scholar 

  • Gershman, H. 1970. On the measurement of cell adhesiveness.J. Exp. Zool. 174:391

    PubMed  Google Scholar 

  • Giudice, G. 1965. The mechanism of aggregation of embryonic sea urchin cells; a biochemical approach.Devel. Biol. 12:233

    Google Scholar 

  • Glaeser, R. M. 1963. The Electrical Charge and Surface Properties of Intact Cells. Ph. D. Thesis. University of California.Also: Office of Technical Services, U. S. Dept. Commerce, Washington

  • Glaeser, R. M., Richmond, J. E., Todd, P. W. 1968. Histotypic self-organization by trypsin-dissociated and EDTA-dissociated chick embryo cells.Exp. Cell Res. 52:71

    PubMed  Google Scholar 

  • Hakomori, S., Teather, C., Andrews, H. 1968. Organizational differences of cell surface “hematoside” in normal and virally transformed cells.Biochem. Biophys. Res. Commun. 33:563

    PubMed  Google Scholar 

  • Haydon, D. A. 1961. The surface charge of cells and some other small particles as indicated by electrophoresis. I. The zeta potential-surface charge relationships.Biochim. Biophys. Acta 50:450

    Google Scholar 

  • Häyry, P., Penttinen, K., Saxén, L. 1965. The different effects of some methods of disaggregation on the electrophoretic mobility of the HeLa-cell.Ann. Med. Exp. Fenn. 43:91

    PubMed  Google Scholar 

  • Hebb, C. R., Chu, M. Y. W. 1960. Reversible injury of L-strain mouse cells by trypsin.Exp. Cell Res. 20:453

    PubMed  Google Scholar 

  • Holtfreter, J. 1943. A study of the mechanics of gastrulation. Part I.J. Exp. Zool. 94:261

    Google Scholar 

  • Humphreys, T. 1963. Chemical dissolution andin vitro reconstruction of sponge cell adhesions: Isolation and function l demonstration of the components involved.Devel. Biol. 8:27

    Google Scholar 

  • Inbar, M., Sachs, L. 1969. Interaction of the carbohydrate-binding protein concanavalin A with normal and transformed cells.Proc. Nat. Acad. Sci. 63:1418

    PubMed  Google Scholar 

  • Jensen, A. B. 1948. Activation of unfertilized sea urchin eggs by trypsin.Nature 162:931

    Google Scholar 

  • Johnson, C. F. 1966. Disaccharidase: Localization in hamster intestine brush borders.Science 155:1670

    Google Scholar 

  • Jones, B. M. 1965. Inhibitory effect ofp-benzoquinone on the aggregation behavior of embryo-chick fibroblast cells.Nature 206:1280

    Google Scholar 

  • Jones, B. M., Kemp, R. B. 1970. Aggregation and electrophoretic mobility studies on dissociated cells (2). The effects of ATP and ADP.Exp. Cell Res. 63:301

    PubMed  Google Scholar 

  • Jones, B. M., Kemp, R. B., Groschel-Stewart, U. 1970. Inhibition of cell aggregation by antibodies directed against actomyosin.Nature 226:261

    PubMed  Google Scholar 

  • Jones, B. M., Morrison, G. A. 1969. A molecular basis for indiscriminate and selective cell adhesion.J. Cell Sci. 4:799

    PubMed  Google Scholar 

  • Jones, P. C. T. 1966. A contractile protein model for cell adhesion.Nature 211:365

    Google Scholar 

  • Kemp, R. B. 1969. Studies on the effect of dissociating agents on the electrophoretic mobility and aggregative competence of embryonic chick muscle cells.Cytobios 1:187

    Google Scholar 

  • Kemp, R. B. 1970. The effect of neuraminidase (3∶2∶1∶19) on the aggregation of cells dissociated from embryonic chick muscle tissue.J. Cell Sci. 6:751

    PubMed  Google Scholar 

  • Kemp, R. B., Jones, B. M. 1970. Aggregation and electrophoretic mobility studies of cells. I. The effects ofp-benzoquinone and tannic acid.Exp. Cell Res. 63:293

    PubMed  Google Scholar 

  • Kemp, R. B., Jones, B. M., Cunningham, I., James, M. C. M. 1967. Quantitative investigation on the effect of puromycin on the aggregation of trypsin- and versene-dissociated chick fibroblast cells.J. Cell Sci. 2:323

    PubMed  Google Scholar 

  • Kiremidjian, L., Kopac, M. J. 1972. Changes in cell adhesiveness associated with the development ofRana pipiens pronephros.Devel. Biol. 27:116

    Google Scholar 

  • Kleinschuster, S. J., Moscona, A. A. 1972. Interactions of embryonic and fetal neural retinal cells with carbohydrate-binding photohemagglutinins: Cell surface changes with differentiation.Exp. Cell Res. 70:397

    PubMed  Google Scholar 

  • Knight, V. A., Jones, B. M., Jones, P. C. T. 1966. Inhibition of the aggregation of dissociated embryo-chick fibroblast cells by adenosine triphosphate.Nature 210:1008

    PubMed  Google Scholar 

  • Kobamoto, N., Löfroth, G., Camp, P., Van Amburg, G., Augenstein, L. 1966. Specificity of trypsin adsorption onto cellulose, glass, and quartz.Biochem. Biophys. Res. Commun. 24:622

    Google Scholar 

  • Kolodny, G. M. 1972. Effect of various inhibitors on readhesion of trypsinized cells in culture.Exp. Cell Res. 70:196

    PubMed  Google Scholar 

  • Kossard, S., Nelson, D. S. 1968. Studies on cytophilic antibodies. IV. The effects of proteolytic enzymes (trypsin and papain) on the attachment to macrophages of cytophilic antibodies.Aust. J. Exp. Biol. Sci. 46:63

    Google Scholar 

  • Kuo, J. F., Holmlund, C. E., Dill, I. K. 1966. The effect of proteolytic enzymes in isolated adipose cells.Life Sci. 5:2257

    PubMed  Google Scholar 

  • Kuroda, Y. 1963. Changes in aggregation and differentiation of cartilage cells grown in monolayer cultures.Exp. Cell Res. 30:446

    PubMed  Google Scholar 

  • Langley, O. K., Ambrose, E. J. 1964. Isolation of a mucopeptide from the surface of Ehrlich ascites tumor cells.Nature 204:53

    PubMed  Google Scholar 

  • Lefford, F. 1965. Pretreatment with enzymes on explant outgrowthin vitro.Exp. Cell Res. 38:285

    PubMed  Google Scholar 

  • Lesseps, R. J. 1963. Cell surface projections: Their role in the aggregation of embryonic chick cells as revealed by electron microscopy.J. Exp. Zool. 153:171

    PubMed  Google Scholar 

  • Lilien, J. E. 1968. Specific enhancement of cell aggregationin vitro.Devel. Biol. 17:657

    Google Scholar 

  • Mäkelä, O., Miettinen, T., Pesola, R. 1960. Release of sialic acid and carbohydrates from human red cells by trypsin treatment.Vox Sang. 5:492

    PubMed  Google Scholar 

  • Martz, E., Steinberg, M. S. 1972. The role of cell-cell contact in “contact” inhibition of cell division: A review and new evidence.J. Cell Physiol. 79:189

    PubMed  Google Scholar 

  • Millipore Filter Corp. 1964. Techniques for Exfoliative Cytology. Application Data Manual −50

  • Moore, A. R. 1952. An animalizing effect of trypsin and its inhibition by lithium in the developing eggs ofStronglocentrotus droebachiensis.J. Exp. Zool. 121:99

    Google Scholar 

  • Moscona, A. 1952. Cell suspensions from organ rudiments of chick embryos.Exp. Cell Res. 3:535

    Google Scholar 

  • Moscona, A. 1961a. Rotation-mediated histogenic aggregation of dissociated cells. A quantifiable approach to cell interactionin vitro.Exp. Cell Res. 22:455

    PubMed  Google Scholar 

  • Moscona, A. 1961b. Effect of temperature on adhesion to glass and histogenic cohesion of dissociated cells.Nature 190:408

    PubMed  Google Scholar 

  • Moscona, A. A. 1963. Inhibition by trypsin inhibitors of dissociation of embryonic tissue by trypsin.Nature 199:379

    PubMed  Google Scholar 

  • Moscona, A. A. 1971. Embryonic and neoplastic cell surfaces: Availability of receptors for concanavalin A and wheat germ agglutinin.Science 171:905

    PubMed  Google Scholar 

  • Moscona, A., Moscona, H. 1952. The dissociation and aggregation of cells from organ rudiments of the early chick embryo.J. Anat. 86:287

    PubMed  Google Scholar 

  • Moscona, A., Moscona, H. 1966. Aggregation of embryonic cells in a serum-free medium and its inhibition at suboptimal temperatures.Exp. Cell Res. 41:697

    PubMed  Google Scholar 

  • Moscona, A., Trowell, O. A., Willmer, E. N. 1965. Methods.In: Cells and Tissues in Culture. E. N. Willmer. editor. Vol. I. p. 19. Academic Press Inc., New York

    Google Scholar 

  • Neville, D. M. 1968. Isolation of an organ specific protein antigen from cell-surface membrane of rat liver.Biochim. Biophys. Acta 154:540

    PubMed  Google Scholar 

  • Nicolson, G. L. 1972. Topography of membrane concanavalin A sites modified by proteolysis.Nature, New Biol. 239:193

    Google Scholar 

  • Nicolson, G. L., Blaustein, J. 1972. The interaction ofRicinus communis agglutinin with normal and tumor cell surfaces.Biochim. Biophys. Acta 226:543

    Google Scholar 

  • Nicolson, G. L., Hyman, R., Singer, S. J. 1971. The two dimensional topographic distribution of H-2 histocompatibility alloantigens on mouse red blood cell membranes.J. Cell Biol. 50:905

    PubMed  Google Scholar 

  • Nicolson, G. L., Singer, S. J. 1971. Ferritin-conjugated plant agglutinis as specific saccharide stains for electron microscopy. Application to saccharides bound to cell membranes.Proc. Nat. Acad. Sci. 68:942

    PubMed  Google Scholar 

  • Northrop, J. H. 1926. The resistance of living organisms to digestion by pepsin or trypsin.J. Gen. Physiol. 9:497

    Google Scholar 

  • Ohkuma, S., Ikemoto, S. 1965. Release of a sialomucopeptide from human red cells and destruction of the I blood group receptor of their cells by crystalline trypsin treatment.Proc. Japan Acad. 41:482

    Google Scholar 

  • Orr, C. W., Roseman, S. 1969. Intercellular adhesion. I. A quantitative assay for measuring the rate of adhesion.J. Membrane Biol. 1:109

    Google Scholar 

  • Pethica, B. A. 1961. The physical chemistry of cell adhesion.Exp. Cell Res., suppl.8:123

    PubMed  Google Scholar 

  • Phillips, H. J. 1967. Some metabolic changes resulting from treating kidney tissue with trypsin.Canad. J. Biochem. 45:1495

    Google Scholar 

  • Pinto da Silva, P. 1972. Translational mobility of the membrane intercalated particles of human erythrocyte ghosts: pH-dependent, reversible aggregation.J. Cell Biol. 53:777

    PubMed  Google Scholar 

  • Pinto da Silva, P., Douglas, S. D., Branton, D. 1971a. Localization of A antigen sites on human erythrocyte ghosts.Nature 232:194

    PubMed  Google Scholar 

  • Pinto da Silva, P., Douglas, S. D., Branton, D. 1971b. Location of A1 antigens on the human erythrocyte membrane.J. Cell Biol. 47:159 a.

    Google Scholar 

  • Ponder, E. 1951. Effects produced by trypsin on certain properties of the human red cell.Blood 6:350

    PubMed  Google Scholar 

  • Poste, G. 1971. Tissue dissociation with proteolytic enzymes. Adsorption and activity of enzymes at the cell surface.Exp. Cell Res. 65:359

    PubMed  Google Scholar 

  • Price, P. G. 1970. Electron microscopic observations of the surface of L-cells in culture.J. Membrane Biol. 2:300

    Google Scholar 

  • Rosenberg, M. D. 1960. Microexudates from cells grown in tissue culture.Biophys. J. 1:137

    PubMed  Google Scholar 

  • Roth, S. A. 1968. Studies on intercellular adhesive selectivity.Devel. Biol. 18:602

    Google Scholar 

  • Roth, S. A., Weston, J. A. 1967. The measurement of intercellular adhesion.Proc. Nat. Acad. Sci. 58:974

    Google Scholar 

  • Seaman, G. V. F., Heard, D. H. 1960. The surface of the washed human erythrocyte as a polyanion.J. Gen. Physiol. 44 (1):251

    PubMed  Google Scholar 

  • Sefton, B. M., Rubin, H. 1970. Release from density dependent growth inhibition by proteolytic enzymes.Nature 227:843

    PubMed  Google Scholar 

  • Sela, B.-A., Lis, H., Sharon, N., Sachs, L. 1970. Different locations of carbohydrate-containing sites in the surface membrane of normal and transformed mammalian cells.J. Membrane Biol. 3:267

    Google Scholar 

  • Shea, L., Ginsburg, V. 1968. Release of sugars from HeLa cells by trypsin.In: Biological Properties of the Mammalian Surface Membrane. A. Manson, editor. p. 67. Wistar Inst. Symp. #8, Wistar Institute Press, Philadelphia, Pa.

    Google Scholar 

  • Simms, H. S., Stillman, N. P. 1937. Substances affecting adult tissuein vitro. I. The stimulating action of trypsin on fresh adult tissue.J. Gen Physiol. 20:603

    Google Scholar 

  • Singer, S. J., Nicolson, G. L. 1972. The fluid mosaic model of the structure of cell membranes.Science 175:720

    PubMed  Google Scholar 

  • Smith, S. B., Revel, J.-P. 1972. Mapping of concanavalin A binding sites on the surface of several cell types.Devel. Biol. 27:434

    Google Scholar 

  • Steinberg, M. S. 1958. On the chemical bonds between animal cells. A mechanism for type-specific association.Amer. Naturalist 92:65

    Google Scholar 

  • Steinberg, M. S. 1962. Role of temperature in the control of aggregation of dissociated embryonic cells.Exp. Cell Res. 28:1

    PubMed  Google Scholar 

  • Steinberg, M. S. 1963. ECM: Its nature, origin, and function in cell aggregation.Exp. Cell Res. 30:257

    PubMed  Google Scholar 

  • Steinberg, M. S. 1967. Avian and mammalian cell dissociation.In: Methods in Developmental Biology. F. Wilt and N. K. Wessells, editors. p. 565. T. Y. Crowell Co., New York

    Google Scholar 

  • Steinberg, M. S., Granger, R. E. 1966. The re-acquisition of adhesiveness of trypsinized chick embryonic cellsin vitro.Amer. Zool. 6:579 (abstr).

    Google Scholar 

  • Steinberg, M. S., Roth, S. A. 1964. Phases in cell aggregation and tissue reconstruction. An approach to the kinetics of cell aggregation.J. Exp. Zool. 157:327

    PubMed  Google Scholar 

  • Tillack, T. W., Scott, R. E., Marchesi, V. T. 1971. Further studies on the association between glycoprotein receptors and the intramembranous particles of the red cell membrane.Abstr. 11 th Ann. Mtg. Amer. Soc. Cell Biology, New Orleans, p. 305

  • Townes, P. L. 1953. Effects of proteolytic enzymes on the fertilization membrane and jelly layers of the amphibian embryo.Exp. Cell Res. 4:96

    Google Scholar 

  • Townes, P. L., Holtfreter, J. 1955. Directed movements and selective adhesion of embryonic amphibian cells.J. Exp. Zool. 128:53

    Google Scholar 

  • Weiss, L. 1960. Studies on cellular adhesion in tissue culture. III. Some effects of calcium.Exp. Cell Res. 21:71

    PubMed  Google Scholar 

  • Weiss, L. 1963. The pH value at the surface ofBacillus subtilis.J. Gen. Microbiol. 32:331

    PubMed  Google Scholar 

  • Weiss, L. 1966. Studies on cell deformability. II. Effects of some proteolytic enzymes.J. Cell Biol. 30:39

    PubMed  Google Scholar 

  • Weiss, L., Kapes, D. L. 1966. Observations on cell adhesion and separation following enzyme treatment.Exp. Cell Res. 41:601

    PubMed  Google Scholar 

  • Wiseman, L. L., Steinberg, M. S., Phillips, H. M. 1972. Experimental modulation of intercellular cohesiveness: Reversal of tissue assembly patterns.Devel. Biol. 28:498

    Google Scholar 

  • Zajac, I., Crowell, R. J. 1965. Location and regeneration of enterovirus receptors of HeLa cells.J. Bacteriol. 89:1097

    PubMed  Google Scholar 

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Steinberg, M.S., Armstrong, P.B. & Granger, R.E. On the recovery of adhesiveness by trypsin-dissociated cells. J. Membrain Biol. 13, 97–128 (1973). https://doi.org/10.1007/BF01868223

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