Skip to main content
Log in

Chemotaxis of metastatic tumor cells: Clues to mechanisms from the Dictyostelium paradigm

  • Overview
  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Summary

Amoeboid movement, and in some cases, amoeboid chemotaxis, is a key step in tumor metastasis. The high degree of conservation in signal transduction pathways and motile machinery in eukaryotic cells suggests that insights and molecular probes developed from the study of these processes in easily manipulated experimental model systems will be applicable directly to experimentally intractable tumor cells. One such model system, Dictyostelium discoideum, is discussed in terms of the molecular events involved in amoeboid chemotaxis. The application of insights and assays developed with Dictyostelium to early events in the chemotaxis of Lewis lung carcinoma cells is reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Virchow R: Uber bewegliche tierische zellen. Arch Path Anat Physiol 28: 237–240, 1863

    Google Scholar 

  2. Enterline HT, Coman DR: The amoeboid motility of human and animal neoplastic cells. Cancer 3: 1033–1038, 1950

    Google Scholar 

  3. Coman DR: Mechanisms responsible for the origin and distribution of blood-borne tumor metastases. A review. Cancer Res 13: 397–404, 1953

    Google Scholar 

  4. Wood S: Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. Arch Path 66: 550–568, 1958

    Google Scholar 

  5. Hosaka S, Suzuki M, Goto M, Sato H: Motility of rat ascites hepatoma cells, with reference to malignant characteristics in cancer metastasis. Gann 69: 273–276, 1978

    Google Scholar 

  6. Raz A, Ben-Ze'ev A: Cell-contact and-architecture of malignant cells and their relationship to metastasis. Cancer Metastasis Rev 6: 3–21, 1987

    Google Scholar 

  7. Hosaka S, Suzuki M, Sato H: Leucocyte-like motility of cancer cells, with reference to the mechanism of extravasation in metastasis. Gann 70: 559–561, 1979

    Google Scholar 

  8. Locker J, Goldblatt PJ, Leighton J: Ultrastructural features of invasion in chick embryo liver metastasis of Yoshida ascites hepatoma. Cancer Res 30: 1632–1644, 1970

    Google Scholar 

  9. Mohler JL, Partin AW, Isaacs WB, Coffey DS: Time lapse videomicroscopic identification of Dunning R-3327 adenocarcinoma and normal rate prostate cells. J Urol 137: 544–547, 1987

    Google Scholar 

  10. Mohler JL, Partin AW, Coffey DS: Prediction of metastatic potential by a new grading system of cell motility: validation in the Dunning R-3327 prostatic adenocarcinoma model. J Urol 138: 168–170, 1987

    Google Scholar 

  11. Liotta LA, Mandler R, Murano G, Katz DA, Gordon RK, Chiang PK, Schiffmann E: Tumor cell autocrine motility factor. Proc Natl Acad Sci USA 82: 3302–3306, 1986

    Google Scholar 

  12. Stracke ML, Engel JD, Wilson LW, Rechler MM, Liotta LA, Schiffman E: The type I IGF receptor is a motility receptor in human melanoma cells. J Biol Chem 264: 21544–21549, 1989

    Google Scholar 

  13. Aznavoorian SA, Stracke ML, Krutzsch H, Schiffman E, Liotta LA: Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells. J Cell Biol 110: 1427–1438, 1990

    Google Scholar 

  14. McCarthy JB, Hager SJ, Furcht LT: Human fibronectin contains distinct adhesion- and motility-promoting domains for metastatic melanoma cells. J Cell Biol 102: 179–188, 1986

    Google Scholar 

  15. Mensing H, Albini A, Krieg T, Pontz BF, Muller PK: Enhanced chemotaxis of tumor-derived and virus-transformed cells to fibronectin and fibroblast-conditioned medium. Int J Cancer 33: 43–48, 1985

    Google Scholar 

  16. McCarthy JB, Basara ML, Palm SL, Sas DF, Furcht LT: The role of cell adhesion proteins—laminin and if fibronectin — in the movement of malignant and metastatic cells. Cancer Metastasis Rev 4: 125–152, 1985

    Google Scholar 

  17. Yusa T, Blood CM, Zetter BR: Tumor cell interactions with elastin: implications for pulmonary metastasis. Am Rev Respir Dis 140: 1458–1462, 1989

    Google Scholar 

  18. Devreotes PN, Zigmond SH: Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu Rev Cell Biol 4: 649–686, 1988

    Google Scholar 

  19. Firtel RA, Van Haastert PJ, Kimmel AR, Devreotes PN: G protein linked signal transduction pathways in development: dictyostelium as an experimental system. Cell 58: 235–239, 1989

    Google Scholar 

  20. Devreotes P: Dictyostelium discoideum: a model system for cell-cell interactions in development. Science 245: 1054–1058, 1989

    Google Scholar 

  21. Segall JE: Mutational studies of amoeboid chemotaxis using Dictyostelium discoideum. In: Lackie JM, Armitage JP, (eds). Biology of the Chemotactic Response. p. 241–272, Cambridge University Press, Cambridge, 1990

    Google Scholar 

  22. Newell PC, Europe-Finner GN, Liu G, Gammon B, Wood CA: Chemotaxis of Dictyostelium: the signal transduction pathway to actin and myosin. In: Lackie JM, Armitage JP, (eds). Biology of the Chemotactic Response. p. 273–296, Cambridge University Press, Cambridge, 1990

    Google Scholar 

  23. Van Haastert PJ: Transmembrane signal transduction pathways in Dictyostelium. Adv Second Messenger Phosphoprotein Res 23: 185–226, 1991

    Google Scholar 

  24. Van Haastert PJ, De Wit RJ: Demonstration of receptor heterogeneity and affinity modulation by nonequilibrium binding experiments. The cell surface cAMP receptor of Dictyostelium discoideum. J Biol Chem 259: 13321–13328, 1984

    Google Scholar 

  25. Van Haastert PJ, De Wit RJ, Janssens PM, Kesbeke F, DeGoede J: G-protein-mediated interconversions of cell-surface cAMP receptors and their involvement in excitation and desensitization of guanylate cyclase in Dictyostelium discoideum. J Biol Chem 261: 6904–6911, 1986

    Google Scholar 

  26. Klein PS, Sun TJ, Saxe CL, Kimmel AR, Johnson RL, Devreotes PN: A chemoattractant receptor controls development in Dictyostelium discoideum. Science 241: 1467–1472, 1988

    Google Scholar 

  27. Sun TJ, Van Haastert PJ, Devreotes PN: Surface cAMP receptors mediate multiple responses during development in Dictyostelium: evidenced by antisense mutagenesis. J Cell Biol 110: 1549–1554, 1990

    Google Scholar 

  28. Sun TJ, Devreotes PN: Gene targeting of the aggregation stage cAMP receptor cAR1 in Dictyostelium. Genes Dev 5: 572–582, 1991

    Google Scholar 

  29. Saxe CL, Johnson RL, Devreotes PN, Kimmel AR: Expression of a cAMP receptor gene of Dictyostelium and evidence for a multigene family. Genes Dev 5: 1–8, 1991

    Google Scholar 

  30. Vaughan RA, Devreotes PN: Ligand-induced phosphorylation of the cAMP receptor from Dictyostelium discoideum. J Biol Chem 263: 14538–14543, 1988

    Google Scholar 

  31. Johnson RL, Vaughan RA, Caterina MJ, Van Haastert PJ, Devreotes PN: Overexpression of the cAMP receptor 1 in growing Dictyostelium cells. Biochemistry 30: 6982–6986, 1991

    Google Scholar 

  32. Kesbeke F, Snaar Jagalska BE, Van Haastert PJ: Signal transduction in Dictyostelium fgd A mutants with a defective interaction between surface cAMP receptors and a GTP-binding regulatory protein. J Cell Biol 107: 521–528, 1988

    Google Scholar 

  33. Coukell MB, Lappano S, Cameron AM: Isolation and Characterization of cAMP Unresponsive (Frigid) Aggregation-Deficient Mutants of Dictyostelium discoideum. Dev Genet 3: 283–297, 1983

    Google Scholar 

  34. Pupillo M, Kumagai A, Pitt GS, Firtel RA, Devreotes PN: Multiple alpha subunits of guanine nucleotide-binding proteins in Dictyostelium. Proc Natl Acad Sci USA 86: 4892–4896, 1989

    Google Scholar 

  35. Kumugai A, Pupillo M, Gundersen R, Miake Lye R, Devreotes PN, Firtel RA: Regulation and function of G alpha protein subunits in Dictyostelium. Cell 57: 265–275, 1989

    Google Scholar 

  36. Hall AL, Warren V, Condeelis J: Transduction of the chemotactic signal to the actin cytoskeleton of Dictyostelium discoideum. Dev Biol 136: 517–525, 1989

    Google Scholar 

  37. Kumagai A, Hadwiger JA, Pupillo M, Firtel RA: Molecular genetic analysis of two G alpha protein subunits in Dictyostelium. J Biol Chem 266: 1220–1228, 1991

    Google Scholar 

  38. Snaar Jagalska BE, Van Haastert PJ: Pertussis toxin inhibits cAMP-induced desensitization of adenylate cyclase in Dictyostelium discoideum. Mol Cell Biochem 92: 177–189, 1990

    Google Scholar 

  39. Hadwiger JA, Wilkie TM, Strathmann M, Firtel RA: Identification of Dictyostelium Galpha genes expressed during multicellular development. Proc Natl Acad Sci USA 88: 8213–8217, 1991

    Google Scholar 

  40. Kesbeke F, Van Haastert PJM, de Wit RJW, Snaar-Jagalska BE: Chemotaxis to cyclic cAMP and folic acid is mediated by different G proteins in Dictyostelium discoideum. J Cell Sci 96: 669–673, 1990

    Google Scholar 

  41. Gundersen RE, Devreotes PN: In vivo receptor-mediated phosphorylation of a G protein in Dictyostelium. Science 248: 591–593, 1990

    Google Scholar 

  42. Van Haastert PJ, De Vries MJ, Penning LC, Roovers E, Van der Kaay J, Erneux C, Van Lookeren Campagne MM: Chemoattractant and guanosine 5′-[gamma-thio]triphosphate induce the accumulation of inositol 1,4,5-trisphosphate in Dictyostelium cells that are labelled with [3H]inositol by electroporation. Biochem J 258: 577–586, 1989

    Google Scholar 

  43. Europe Finner GN, Gammon B, Wood CA, Newell PC: Inositol tris- and polyphosphate formation during chemotaxis of Dictyostelium. J Cell Sci 93: 585–592, 1989

    Google Scholar 

  44. Coukell MB, Cameron AM: Characterization of revertants of stmF mutants of Dictyostelium discoideum: evidence that stmF is the structural gene of the cGMP-specific phosphodiesterase. Dev Genet 6: 163–177, 1986

    Google Scholar 

  45. Van Haastert PJ, Van Lookeren Campagne MM, Ross FM: Altered cGMP-phosphodiesterase activity in chemotactic mutants of Dictyostelium discoideum. FEBS Lett 147: 149–152, 1982

    Google Scholar 

  46. Ross FM, Newell PC: Streamers: chemotactic mutants of Dictyostelium discoideum with altered cyclic GMP metabolism. J Gen Microbiol 127: 339–350, 1981

    Google Scholar 

  47. Liu G, Newell PC: Evidence that cyclic GMP regulates myosin interaction with the cytoskeleton during chemotaxis of Dictyostelium. J Cell Sci 90: 123–129, 1988

    Google Scholar 

  48. Abe T, Maeda Y, Iijima T: Transient increase of the intracellular Ca2+ concentration during chemotactic signal transduction in Dictyostelium discoideum cells. Differentiation 39: 90–96, 1988

    Google Scholar 

  49. Van Duijn B, Wang M: Chemoattractant-induced membrane hyperpolarization in Dictyostelium discoideum. A possible role for cyclic GMP. FEBS Lett 275: 201–204, 1990

    Google Scholar 

  50. Van Duijn B, Vogelzang SA, Ypey DL, Van der Molen LG, Van Haastert PJ: Normal chemotaxis in Dictyostelium discoideum cells with a depolarized plasma membrane potential. J Cell Sci 95: 177–183, 1990

    Google Scholar 

  51. Van Duijn B, Inouye K: Regulation of movement speed by intracellular pH during Dictyostelium discoideum chemotaxis. Proc Natl Acad Sci USA 88: 4951–4955, 1991

    Google Scholar 

  52. Snaar Jagalska BE, Van Haastert PJ: Dictyostelium discoideum mutant synag 7 with altered G-protein-adenylate cyclase interaction. J Cell Sci 91: 287–294, 1988

    Google Scholar 

  53. Darmon M, Barrand P, Brachet P, Klein C, Pereira Da Silva L: Phenotypic suppression of morphogenetic mutants of Dictyostelium discoideum. Dev Biol 58: 174–184, 1977

    Google Scholar 

  54. Mast S: Structure, movement, locomotion and stimulation in amoebae. J Morphol Physiol 41: 347–425, 1926

    Google Scholar 

  55. Rubino S, Fighetti M, Unger E, Cappuccinelli P: Location of actin, myosin and microtubular structures during directed locomotion of Dictyostelium amoebae. J Cell Biol 98: 282–390, 1984

    Google Scholar 

  56. Yumura S, Mori H, Fukui Y: Localization of actin and myosin for the study of amoeboid movement in Dictyostelium using improved immunofluorescence. J Cell Biol 99: 894–899, 1984

    Google Scholar 

  57. Berlot CH, Devreotes PN, Spudich JA: Role of myosin phosphorylation in Dictyostelium chemotaxis. In: Satir P, Condeelis JS, Lazarides E, (eds). Signal Transduction in Cytoplasmic Organization and Cell Motility, UCLA Symposia of Molecular and Cellular Biology, New Series, Volume 77. p. 287–292, Alan R. Liss, Inc., New York, 1988

    Google Scholar 

  58. DeLozanne A, Spudich J: Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236: 1086–1091, 1987

    Google Scholar 

  59. Knecht D, Loomis W: Antisense RNA inactivation of myosin heavy chain gene expressions in Dictyostelium discoideum. Science 236: 1081–1086, 1987

    Google Scholar 

  60. Wessels D, Soll D, Knecht D, Loomis W, Delozanne A, Spudich J: Cell motility and chemotaxis in Dictyostelium amoebae lacking myosin heavy chain. Dev Biol 128: 164–177, 1988

    Google Scholar 

  61. Allen R: A new theory of amoeboid movement and protoplasmic streaming. Exp Cell Res Supp 8: 17–31, 1961

    Google Scholar 

  62. Korn E, Hammer J: Myosin I. Current Opinion in Cell Biology 2: 57–61, 1990

    Google Scholar 

  63. Fukui Y, Lynch J, Brzeska H, Korn E: Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341: 328–331, 1989

    Google Scholar 

  64. Jung G, Hammer J: Generation and characterization of Dictyostelium cells deficient in a myosin I heavy chain isoform. J Cell Biol 110: 1955–1964, 1990

    Google Scholar 

  65. Wessels D, Murray J, Jung G, Hammer J, Soll D: Myosin IB null mutants of Dictyostelium exhibit abnormalities in motility. Cell Mot Cytoskel 20: 301–315.

  66. Tilney L, Inoue S: Acrosomal reaction of thyone sperm II. The kinetics and mechanism of acrosomal process elongation. J Cell Biol 93: 820–827, 1982

    Google Scholar 

  67. Detmers P, Goodenough U, Condeelis J: Elongation of the fertilization tubule of Chlamydomonas: New observations on the core microfilaments and the effect of transient intracellular signals on their structural integrity. J Cell Biol 97: 522–532, 1983

    Google Scholar 

  68. Fricke K, Wirthensohn K, Laxhuber R, Sackman E: Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness. Eur Biophys J 14: 67–81, 1986

    Google Scholar 

  69. Oster G, Perelson A, Tilney L: A mechanical model for elongation of the acrosomal process in Thyone sperm. J Math Biol 15: 259–265, 1982

    Google Scholar 

  70. Hill T, Kirschner M: Bioenergetics and kinetics of microtubule and actin filament assembly and disassembly. Int Rev Cytol 78: 1–125, 1982

    Google Scholar 

  71. Cooper J: The role of actin polymerization in cell motility. Annual Rev Physiol 53: 585–605, 1991

    Google Scholar 

  72. Hall A, Schlein A, Condeelis J: Relationship of pseudopod extension to chemotactic hormone induced actin polymerization in amoeboid cells. J Cell Biochem 37: 285–299, 1988

    Google Scholar 

  73. Carson M, Weber A, Zigmond S: An actin-nucleating activity in polymorphonuclear leukocytes is modulated by chemotactic peptides. J Cell Biol 103: 2707–2714, 1986

    Google Scholar 

  74. Hall A, Warren V, Dharmawardhane S, Condeelis J: Identification of actin nucleation activity and polymerization inhibitor in amoeboid cells: Their regulation by chemotactic stimulation. J Cell Biol 109: 2207–2213, 1989

    Google Scholar 

  75. Condeelis J, Bresnick A, Demma M, Dharmawardhane S, Eddy R, Hall A, Sauterer R, Warren V: Mechanisms of amoeboid chemotaxis: An evaluation of the cortical expansion model. Devlop Genetics 11: 333–340, 1990

    Google Scholar 

  76. Symons M, Mitchison T: Control of actin polymerization in live and permeabilized fibroblasts. J Cell Biol 114: 503–513, 1991

    Google Scholar 

  77. Theriot J, Mitchison T: Actin microfilament dynamics in locomoting cells. Nature 352: 126–131, 1991

    Google Scholar 

  78. Howard T, Chaponnier C, Yin H, Stossel T: Gelsolinactin interaction and actin polymerization in human neutrophils. J Cell Biol 10: 1983–1991, 1990

    Google Scholar 

  79. Sauterer R, Eddy R, Hall A, Condeelis J: Purification and characterization of aginactin, a newly identified agonistregulated actin capping protein from Dictyostelium amoebe. J Biol Chem 266: 24533–24539, 1991

    Google Scholar 

  80. Schwartz M, Luna E: How actin binds and assembles onto plasma membrane from Dictyostelium discoideum. J Cell Biol 107: 201–209, 1988

    Google Scholar 

  81. Goldman W, Isenberg G: Kinetic determination of talinactin binding. Biochem Biophys Res Com 178: 718–723, 1991

    Google Scholar 

  82. Oosawa F, Asakura S: Thermodynamics of the polymerization of protein. Academic Press, New York, 1975

    Google Scholar 

  83. Wolosewick J, Condeelis J: Fine structure of gels prepared from an actin binding protein and actin. J Cellular Biochem 30: 227–243, 1986

    Google Scholar 

  84. Ogihara S, Carboni J, Condeelis J: Electron microscopic localization of myosin II and ABP-120 in the cortical actin matrix of Dictyostelium amoebae using IgG-gold conjugates. Develop. Genetics 9: 505–520, 1988

    Google Scholar 

  85. Condeelis J, Hall A, Bresnick A, Warren V, Hock R, Bennett H, Ogihara S: Actin polymerization and pseudopod extension during amoeboid chemotaxis. Cell Mot Cytoskel 10: 77–90, 1988

    Google Scholar 

  86. Dharmawardhane S, Warren V, Hall A, Condeelis J: Changes in the association of actin binding proteins with the actin cytoskeleton during stimulation of Dictyostelium discoideum. Cell Motil. Cytoskel. 13: 57–63, 1989

    Google Scholar 

  87. Condeelis J, Vahey M, Carboni J, Demey J, Ogihara S: Properties of the 120,000 and 95,000 dalton actin binding proteins from Dictyostelium discoideum and their possible functions in assembling the cytoplasmic matrix. J Cell Biol 99: 119S-126S, 1984

    Google Scholar 

  88. Noegel A, Rapp S, Lottspeich F, Schleicher M, Stewart M: The Dictyostelium gelation factor shares a putative actin binding site with alpha actinins and dystrophin and also has a rod domain containing six 100 residue motifs that appear to have a cross-beta conformation. J Cell Biol 109: 607–618, 1989

    Google Scholar 

  89. Bresnick A, Warren V, Condeelis J: Identification of a short sequence essential for actin binding by Dictyostelium ABP-120. J Biol Chem 265: 9236–9240, 1990

    Google Scholar 

  90. Bresnick A, Janmey P, Condeelis J: Evidence that a 27-residue sequence is the actin binding site of ABP-120. J Biol Chem 266: 12989–12993, 1991

    Google Scholar 

  91. Gorlin J, Yamin R, Egan S, Stewart M, Stossel T, Kwiakowski D, Hartwig J: Human endothelial actin binding protein (ABP-280, non-muscle filamin): A molecular leaf spring. J Cell Biol 111: 1089–1105, 1990

    Google Scholar 

  92. Demma M, Warren V, Hock R, Dharmawardhane S, Condeelis J: Isolation of an abundant 50,000 dalton actin filament bundling protein from Dictyostelium amoebae. J Biol Chem 265: 2286–2291, 1990

    Google Scholar 

  93. Dharmawardhane S, Demma M, Yang F, Condeelis J: Compartmentalization and actin binding properties of ABP-50: The elongation factor-1 alpha of Dictyostelium. Cell Motility Cytoskel 20: 279–288, 1991

    Google Scholar 

  94. Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J: Identification of an actin binding protein from Dictyostelium as elongation factor 1 alpha. Nature 347: 494–496, 1990

    Google Scholar 

  95. Cervra M, Dreyfuss G, Penman S: Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected Hela cells. Cell 23: 113–120, 1981

    Google Scholar 

  96. Nielson, Goetz, Tracshel: The role of the cytoskeleton in eukaryotic protein synthesis. Cell Biol Int Rep 7: 245–254, 1983

    Google Scholar 

  97. Singer R, Langevin G, Lawrence J: Ultrastructural visualization of cytoskeletal mRNAs and their associated proteins using double-label in situ hybridization. J Cell Biol 108: 2343–2353, 1989

    Google Scholar 

  98. Oster G: On the crawling of cells. J Embryol Exp Morph 83 Supplement: 329–364, 1984

    Google Scholar 

  99. Liotta L, Stetler-Stevenson W: Metalloproteinases and malignant conversion: does correlation imply causality? J Natl Cancer Inst 81: 556–557, 1989

    Google Scholar 

  100. Blood C, Sasse J, Brodt P, Zetter B: Identification of a tumor cell receptor for VGVAPG, an elastin derived chemotactic peptide. J Cell Biol 107: 1987–1993, 1988

    Google Scholar 

  101. Magro C, Orr F, Manishern W, Sivamanthan K, Mokashi S: Adhesion, Chemotaxis and aggregation of Walker carcinosarcoma cells in response to products of resorbing bone. J Natl Cancer Int 74: 829–838, 1985

    Google Scholar 

  102. Brodt P: Characterization of two highly metastatic variants of Lewis lung carcinoma with different organ specificities. Cancer Res 46: 2442–2448, 1986

    Google Scholar 

  103. Senior R, Griffin G, Mecham R, Wrenn D, Prasdad K, Urry D: VGVAPG, a repeating peptide in elastin, is chemotactic for fibroblasts and monocytes. J Cell Biol 99: 870–874, 1984

    Google Scholar 

  104. Blood C, Zetter B: Membrane bound protein kinase C modulates receptor affinity and chemotactic responsiveness of Lewis lung carcinoma sublimes to an elastin derived peptide. J Biol Chem 264: 10614–10620, 1989

    Google Scholar 

  105. Jones J, Segall J, Condeelis J: Molecular analysis of amoeboid chemotaxis: Parallel observations in amoeboid phagocytes and metastatic tumor cells. In: Cell Motility Factors (I.D. Goldberg, ed.) Birkhauser Verlag, Basel, 1991

    Google Scholar 

  106. Segall J, Jones J, Condeelis J: Analysis of responses of metastatic M27 tumor cells to the chemotactic peptide VGVAPG. J Cell Biol (abstract) 115: 346a.

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Condeelis, J., Jones, J. & Segall, J.E. Chemotaxis of metastatic tumor cells: Clues to mechanisms from the Dictyostelium paradigm. Cancer Metast Rev 11, 55–68 (1992). https://doi.org/10.1007/BF00047603

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00047603

Key words

Navigation