Tumor formation and malignant invasion: role of basal lamina

  • D. E. Ingber
  • J. D. Jamieson
Part of the Developments in Oncology book series (DION, volume 7)


Carcinoma is by far the most commonly occurring form of cancer and is a neoplasm of epithelial cell origin. In any neoplasm, local invasion and metastasis are the two most reliable criteria that designate the tumor as malignant. Direct invasion is the first and most crucial step in the malignant process and is defined in carcinomata by local disruption of basal lamina with tumor cell infiltration info the underlying connective tissue space (Figure 1).


Basal Lamina Connective Tissue Cell Type Versus Collagen Malignant Invasion Basement Membrane Collagen 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Banerjee SD, Cohn RH, Bernfield MR: Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol 73:445–463, 1977.PubMedCrossRefGoogle Scholar
  2. 2.
    Dodson JW, Hay ED: Secretion of collagenous stroma by isolated epithelium grown in vitro. Exp Cell Res 65:215–220, 1971.PubMedCrossRefGoogle Scholar
  3. 3.
    Emerman JT, Pitelka DR: Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro 13:316–328, 1977.PubMedCrossRefGoogle Scholar
  4. 4.
    Meier S, Hay E: Control of corneal differentiation by extracellular materials. Collagen as promoter and stabilizer of epithelial stroma production. Dev Biol 38:249–270, 1974.PubMedCrossRefGoogle Scholar
  5. 5.
    Timpl R, Martin GR, Bruckner P, Wick G, Wiedeman H: Nature of the collagenous protein in a tumor basement membrane. Eur J Biochem 84:43–52, 1978.PubMedCrossRefGoogle Scholar
  6. 6.
    Burgeson RE, El Adli FA, Kaitila II, Hollister DW: Fetal membrane collagens: identification of two new collagen alpha chains. Proc Natl Acad Sci USA 73:2579–2583, 1976.PubMedCrossRefGoogle Scholar
  7. 7.
    Timpl R, Rohde H, Robey PG, Rennard SI, Foidart J-M, Martin GR: Laminin — A glycoprotein from basement membrane. J Biol Chem 254:9933–9937, 1979.PubMedGoogle Scholar
  8. 8.
    Vaheri A, Ruoslahti E, Mosher DF (eds): Fibroblast surface protein. Ann NY Acad Sci 312:1–456, 1978.Google Scholar
  9. 9.
    Madri JA, Roll FJ, Furthmayr H, Foidart J-M: Ultrastructural localization of fibronectin and laminin in the basement membranes of the murine kidney. J Cell Biol 86:682–687, 1980.PubMedCrossRefGoogle Scholar
  10. 10.
    Kanwar YS, Farquhar MG: Presence of heparan sulfate in the glomerular basement membranes of the murine kidney. Proc Natl Acad Sci USA 76:1303–1307, 1979.PubMedCrossRefGoogle Scholar
  11. 11.
    Lemkin MC, Farquhar MG: Sulfated and nonsulfated glycosaminoglycans and glycopeptides are synthesized by kidney in vivo and incorporated into glomerular basement membranes. Proc Natl Acad Sci USA 78:1726–1730, 1981.PubMedCrossRefGoogle Scholar
  12. 12.
    Cohn RH, Banerjee SD, Bernfield MR: Basal lamina of embryonic salivary epithelia. Nature of glycosaminoglycan and organization of extracellular materials. J Cell Biol 73:464–478, 1977.PubMedCrossRefGoogle Scholar
  13. 13.
    Bernfield MR, Banerjee SD: The basal lamina in epithelial-mesenchymal interactions. In: Biology and chemistry of basement membranes, Kefalides N (ed). New York: Academic Press, 1978, pp 137–148.Google Scholar
  14. 14.
    Bernfield MR, Banerjee SD, Cohn RH: Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein proteoglycan at the epithelial surface. J Cell Biol 52:674–689, 1972.PubMedCrossRefGoogle Scholar
  15. 15.
    David G, Bernfield MR: Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: possible mechanism for basal lamina formation. Proc Natl Acad Sci USA 76:786–790, 1979.PubMedCrossRefGoogle Scholar
  16. 16.
    Dodson JW, Hay ED: Secretion of collagen by corneal epithelium. J Exp Zool 189:51–72, 1974.PubMedCrossRefGoogle Scholar
  17. 17.
    Abercrombie M: Contact inhibition: the phenomenon and its biological implications. Natl Cancer Inst Monogr 26:249–277, 1967.PubMedGoogle Scholar
  18. 18.
    Stoker MGP, Rubin H: Density dependent inhibition of cell growth in culture. Nature 215:171–172, 1967.PubMedCrossRefGoogle Scholar
  19. 19.
    Iwig M, Lasch J, Glaesser D: Growth regulation of lens epithelial cells. Chemically-modified sepharose as a suitable substratum for studying cell-substratum interactions. Cell Diff 9:1–12, 1980.CrossRefGoogle Scholar
  20. 20.
    Ben-Zeev A, Farmer SR, Penman S: Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchorage-dependent fibroblasts. Cell 21:365–372, 1980.CrossRefGoogle Scholar
  21. 21.
    Folkman J, Moscona A: Role of cell shape in growth control. Nature 273:345–349, 1978.PubMedCrossRefGoogle Scholar
  22. 22.
    Iwig M, Glaesser D, Bethge M: Cell shape-mediated growth control of lens epithelial cells grown in culture. Exp Cell Res 131:47–56, 1981.PubMedCrossRefGoogle Scholar
  23. 23.
    Folkman J, Greenspan HP: Influence of geometry on control of cell growth. Biochim Biophys Acta 417:211–236, 1975.PubMedGoogle Scholar
  24. 24.
    Holley RW: Control of growth of mammalian cells in cell culture. Nature 258:487–490, 1975.PubMedCrossRefGoogle Scholar
  25. 25.
    Kleinman HK, Klebe RJ, Martin GR: Role of collagenous matrices in the adhesion and growth of cells. J Cell Biol 88:473–485, 1981.PubMedCrossRefGoogle Scholar
  26. 26.
    Terranova VP, Rohrbach DH, Martin GR: Role of laminin in the attachment of PAM 212 epithelial cells to basement membrane collagen. Cell 22:719–726, 1980.PubMedCrossRefGoogle Scholar
  27. 27.
    Yamada KM, Yamada SS, Pastan I: Cell surface protein partially restores morphology, adhesiveness, and contact inhibition of movement to transformed fibroblasts. Proc Natl Acad Sci USA 73:1217–1221, 1976.PubMedCrossRefGoogle Scholar
  28. 28.
    Roblin R, Albert SO, Gelb NA, Black PH: Cell surface changes correlated with density-dependent growth inhibition. Glycosaminoglycan metabolism in 3T3, SV3T3, and Con A selected revertant cells. Biochemistry 14:347–357, 1975.PubMedCrossRefGoogle Scholar
  29. 29.
    Underhill CB, Keller JM: Density-dependent changes in the amount of sulfated glycosamino-glycans associated with mouse 3T3 cells. J Cell Physiol 89:53–64, 1976.PubMedCrossRefGoogle Scholar
  30. 30.
    Underhill CB, Keller JM: A transformation-dependent difference in the heparan sulfate associated with the cell surface. Biochem Biophys Res Comm 63:448–454, 1975.PubMedCrossRefGoogle Scholar
  31. 31.
    Hayman EG, Engvall E, Ruoslahti E: Concomitant loss of cell surface fibronectin and laminin from transformed rat kidney cells. J Cell Biol 88:352–357, 1981.PubMedCrossRefGoogle Scholar
  32. 32.
    Wessels NK: Substrate and nutrient effects upon epidermal basal cell orientation and proliferation. Proc Natl Acad Sci USA 52:252–259, 1964.CrossRefGoogle Scholar
  33. 33.
    Kallman F, Evans J, Wessells NK: Normal epidermal basal cell behavior in the absence of basement membrane. J Cell Biol 32:231–236, 1967.PubMedCrossRefGoogle Scholar
  34. 34.
    Jensen H, Mottet N: Ultrastructural changes in keratinizing epithelium following trypsinization, epidermal detachment and apposition to mesenchymes. J Cell Sci 6:511–535, 1970.PubMedGoogle Scholar
  35. 35.
    Carter WG, Rauvala H, Hakomori SI: Studies on cell adhesion on surfaces coated with carbohydrate-reactive proteins (glycosidases and lectins) and fibronectin. J Cell Biol 88:138–148, 1981.PubMedCrossRefGoogle Scholar
  36. 36.
    Elsdale T, Bard J: Collagen substrata for studies on cell behavior. J Cell Biol 54:626–637, 1972.PubMedCrossRefGoogle Scholar
  37. 37.
    Michalopoulos G, Pitot HC: Primary culture of parenchymal liver cells on collagen membranes. Exp Cell Res 94:70–78, 1975.PubMedCrossRefGoogle Scholar
  38. 38.
    Yang J, Guzman R, Richards J, Nandi S: Primary cultures of mouse mammary tumor epithelial cells embedded in collagen gels. In Vitro 16:502–506, 1980.PubMedCrossRefGoogle Scholar
  39. 39.
    Yang J, Richards J, Bowman P, Guzman R, Enami J, McCormick K, Hamamoto S, Pitelka D, Nandi S: Sustained growth and three-dimensional organization of primary mammary tumor epithelial cells embedded on collagen gels. Proc Natl Acad Sci USA 76:3401–3405, 1979.PubMedCrossRefGoogle Scholar
  40. 40.
    Wicha MS, Liotta LA, Vonderhaar BK, Kidwell WR: Effects of inhibition of basement membrane collagen deposition on rat mammary gland development. Dev Biol 80:253–266, 1980.PubMedCrossRefGoogle Scholar
  41. 41.
    Potten CS: The epidermal proliferative unit: the possible role of the central basal cell. Cell Tissue Kinet 7:77–88, 1974.PubMedGoogle Scholar
  42. 42.
    Walker F: Basement-membrane turnover in the rat. J Pathol 107:119–121, 1972.PubMedCrossRefGoogle Scholar
  43. 43.
    Vracko R: Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structures. Am J Pathol 77:314–346, 1974.PubMedGoogle Scholar
  44. 44.
    Wicha MS, Liotta LA, Garbisa G, Kidwell WR: Basement membrane collagen requirements for attachment and growth of mammary epithelium. Exp Cell Res 124:181–190, 1979.PubMedCrossRefGoogle Scholar
  45. 45.
    Stenn KS, Madri JA, Roll FJ: Migrating epidermis produces AB2 collagen and requires continual collagen synthesis for movement. Nature 277:229–232, 1979.PubMedCrossRefGoogle Scholar
  46. 46.
    Liotta LA, Vembu D, Kleinman HK, Martin GR, Boone C: Collagen required for proliferation of cultured connective tissue cells but not their transformed counterparts. Nature 272:622–624, 1978.PubMedCrossRefGoogle Scholar
  47. 47.
    Vembu D, Liotta LA, Paranjpe M, Boone CW: Correlation of tumorigenicity with resistance to growth inhibition by cishydroxyproline. Exp Cell Res 124:247–252, 1979.PubMedCrossRefGoogle Scholar
  48. 48.
    Pierce GB, Shikes R, Fink LM: Cancer: a problem of development biology. Englewood Cliffs, NJ: Prentice Hall, 1978.Google Scholar
  49. 49.
    Sakakura T, Sakagami Y, Nishizura Y: Persistence of responsiveness of adult mouse mammary gland to induction by embryonic mesenchyme. Dev Biol 72:201–210, 1979.PubMedCrossRefGoogle Scholar
  50. 50.
    Tarin D: Tissue interactions and the maintenance of histological structure in adults. In: Tissue interactions in carcinogenesis, Tarin D (ed). New York: Academic Press, 1972, pp 81–94.Google Scholar
  51. 51.
    Leighton J: Propagation of cancer: target for future chemotherapy. Cancer Res 29:2457–2465, 1969.PubMedGoogle Scholar
  52. 52.
    Gullino PM: The internal milieu of tumors. Prog Exp Tumor Res 8:1–25, 1966.PubMedGoogle Scholar
  53. 53.
    Foley JF, Aftonomos B-Th, Heidrick ML: Influence of fibroblast collagen and mucopolysaccharides on HeLa cell colonial morphology. Life Sci 7:1003–1008, 1968.PubMedCrossRefGoogle Scholar
  54. 54.
    Orr JW, Spencer AT: Transplantation studies on the mechanism of carcinogenesis. In: Tissue interactions in carcinogenesis, Tarin D (ed). New York: Academic Press, 1972, pp 291–304.Google Scholar
  55. 55.
    Folkman J: Tumor Angiogenesis. Adv Canc Res 19:331–358, 1974.CrossRefGoogle Scholar
  56. 56.
    Dawe CJ, Morgan WD, Slatick MS: Influence of epithelio-mesenchymal interactions on tumor induction by polyoma virus. Int J Cancer 1:419–450, 1966.PubMedCrossRefGoogle Scholar
  57. 57.
    Dawe CJ, Whang-Peng J, Morgan WD, Hearon EC, Knutsen T: Epithelial origin of polyoma salivary tumors in mice: evidence based on chromosome-marked cells. Science 171:394–397, 1971.PubMedCrossRefGoogle Scholar
  58. 58.
    Dawe CJ, Morgan WD, Slatick MS: Salivary gland neoplasms in the role of normal mesenchyme during salivary gland morphogenesis. In: Epithelial-mesenchymal interactions, Fleischmajer R, Billingham RE (eds). Baltimore: Williams & Wilkins, 1968, pp 293–312.Google Scholar
  59. 59.
    Argyris TS, Argyris BF: Differential response of skin epithelium to growth-promoting effects of subcutaneous transplanted tumor. Cancer Res 22:73–77, 1962.PubMedGoogle Scholar
  60. 60.
    Redler P, Lustig ES: Differences in the growth-promoting effect of normal and peritumoral dermis on epidermis in vitro. Dev Biol 17:679–691, 1968.PubMedCrossRefGoogle Scholar
  61. 61.
    Goldenberg DM, Pavia RA: Malignant potential of murine stroma cells after transplantation of human tumors into nude mice. Science 212:65–67, 1981.PubMedCrossRefGoogle Scholar
  62. 62.
    Lakshmi MS, Sherbet GV: Embryonic and tumour cell interactions. In: Neoplasia and cell differentiation, Sherbet GV (ed). New York: S. Karger, 1974, pp 380–396.Google Scholar
  63. 63.
    DeCosse JJ, Gossens CL, Kuzma JF: Breast cancer: induction of differentiation by embryonic tissue. Science 181:1057–1058, 1973.PubMedCrossRefGoogle Scholar
  64. 64.
    Ellison ML, Ambrose EJ, Easty GC: Differentiation in a transplantable rat tumour maintained in organ culture. Exp Cell Res 55:198–204, 1969.PubMedCrossRefGoogle Scholar
  65. 65.
    Vasiliev JVM: The role of connective tissue proliferation in invasive growth of normal and malignant tissues: a review. Br J Cancer 12:524–536, 1958.PubMedCrossRefGoogle Scholar
  66. 66.
    Tarin D: 1972 Morphological studies on the mechanism of carcinogenesis. In: Tissue interactions in carcinogenesis, Tarin D (ed). New York: Academic Press, 1972, pp 227–290.Google Scholar
  67. 67.
    Sugar J: Ultrastructural and histochemical changes during the development of cancer in various human organs. In: Tissue interactions in carcinogenesis Tarin D (ed). New York: Academic Press, 1972, pp 127–160.Google Scholar
  68. 68.
    Mainardi CL, Dixit SN, Kang AH: Degradation of type IV basement membrane collagen by a proteinase isolated from human polymorphonuclear leukocyte granules. J Biol Chem 255:5435–5441, 1980.PubMedGoogle Scholar
  69. 69.
    Leighton J, Kalla RL, Kline I, Belkin M: Pathogenesis of tumor invasion. I. Interactions between normal tissues and ‘transformed’ cells in tissue culture. Cancer Res 19:23–27, 1959.PubMedGoogle Scholar
  70. 70.
    Luibel FJ, Sanders E, Ashworth CT: An electron microscopic study of carcinoma in situ and invasive carcinoma of the cervix uteri. Cancer Res 20:357–361, 1960.PubMedGoogle Scholar
  71. 71.
    Ozzello L: The behavior of basement membranes in intraductal carcinoma of the breast. Am J Pathol 35:887–895, 1959.PubMedGoogle Scholar
  72. 72.
    Rubio CA, Biberfeld P: The basement membrane in experimental induced atypias and carcinoma of the uterine cervix in mice. Virchows Arch A Path Anat Histol 381:205–209, 1979.CrossRefGoogle Scholar
  73. 73.
    Pitelka DR, Hamamoto ST, Taggart BN: Basal lamina and tissue recognition in malignant mammary tumors. Cancer Res 40:1600–1611, 1980.PubMedGoogle Scholar
  74. 74.
    Fidler IJ: Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res 38:2651–2660, 1978.PubMedGoogle Scholar
  75. 75.
    Gould V, Battifora H: Origin and significance of the basal lamina and some interstitial fibrillar components in epithelial neoplasms. Pathol Ann 11:353–386, 1976.Google Scholar
  76. 76.
    Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S: Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67–68, 1980.PubMedCrossRefGoogle Scholar
  77. 77.
    Ingber DE, Madri JA, Jamieson JD: Role of basal lamina in neoplastic disorganization of tissue architecture. Proc Natl Acad Sci USA 78:3901–3905, 1981.PubMedCrossRefGoogle Scholar
  78. 78.
    Reddy JK, Rao MS: Transplantable pancreatic carcinoma of the rat. Science 198:78–80, 1977.PubMedCrossRefGoogle Scholar
  79. 79.
    Jamieson JD, Ingber DE, Muresan V, Sarras MP Jr, Maylie-Pfenninger M-F, Iwanij V: Cell surface properties of normal, differentiating, and neoplastic pancreatic acinar cells. Cancer 47:1516–1525, 1981.PubMedCrossRefGoogle Scholar
  80. 80.
    Liotta LA, Tryggvason K, Garbisa S, Robey PG, Abe SG: Partial purification and characterization of a neutral protease which cleaves type IV collagen. Biochemistry 20:100–104, 1981.PubMedCrossRefGoogle Scholar
  81. 81.
    Leivo I, Vaheri A, Timpl R, Wartiovaara J: Appearance and distribution of collagens and laminin in the early mouse embryo. Dev Biol 76:100–114, 1980.PubMedCrossRefGoogle Scholar
  82. 82.
    Ekblom P, Alitalo K, Vaheri A, Timpl R, Saxen L: Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci USA 77:485–489, 1980.PubMedCrossRefGoogle Scholar
  83. 83.
    Farquhar MG: Structure and function in glomerular capillaries: role of the basement membrane in glomerular filtration. In: Biology and chemistry of basement membranes, Kefalides NA (ed). New York: Academic Press, 1978, pp 43–80.Google Scholar
  84. 84.
    Grobstein C: Mechanisms of organogenetic tissue interaction. Natl Cancer Inst Monogr 26:279–299, 1967.PubMedGoogle Scholar
  85. 85.
    Koch JC: The laws of bone architecture. Am J Anat 21:177–298, 1917.CrossRefGoogle Scholar
  86. 86.
    Thompson DW: On growth and form, New York: Cambridge University Press, 1977.Google Scholar
  87. 87.
    Buckminster Fuller R: Synergetics, New York: Macmillan, 1975, p 372.Google Scholar
  88. 88.
    Otto F: Pneumatic structures. In: Tensile structures, Otto F (ed). Cambridge, Mass: M.I.T. Press, 1973, p 148.Google Scholar
  89. 89.
    Kenner H: Geodesic Math, Berkeley, Calif.: University of California Press, 1976, pp 3–7.Google Scholar

Copyright information

© Martinus Nijhoff Publishers, The Hague/Boston/London 1982

Authors and Affiliations

  • D. E. Ingber
  • J. D. Jamieson

There are no affiliations available

Personalised recommendations