Morphological and biological observations relating to the development and progression of breast cancer

  • Thomas J. Anderson
  • William R. Miller
Part of the Cancer Treatment and Research book series (CTAR, volume 71)


Mammary glands are basically modified sweat glands comprising a group of ducts descending from the skin in a radial system of dichotomously branching structures. The human female is unique in that the breast develops fully without the stimulus of copulation or pregnancy. Indeed, there are three overlapping phases of activity that can conveniently be termed structural, functional, and differentiated. The first is associated with puberty, the second with ovulatory menstrual cycles, and only the last with pregnancy and lactation. During the structural phase, the lengthening ducts descend into the fibrous disc below the nipple, extending within and along the contours of the fat spaces, giving rise to an inverted tree-like parenchymal structure. A crucial distinction of the human female from the other members of her species is the virginal development of terminal duct lobular units (TDLUs). These units are spherical or conical in shape due to the compact arrangement of multiple short branchings of the smaller blind-ended ductules, usually enclosed in a specialized stroma (figure 1). They form in groups and individually from the sides and ends of major, intermediate, and small ducts, measure well under 1 mm, and are situated most commonly in the outer third of the breast disc and axillary tail, often amounting to tens of thousands in number. The TDLUs consists of several cell types; the parenchymal branching component is composed of two principal cells, the luminal cuboidal or columnar epithelium and an outer layer of myo-epithelium, all enclosed by a basement membrane; on the opposite stromal side of the membrane lie fibroblasts and a loose textured collagen containing ground substance, traversed by small blood vessels and a variable component of lymphocytes, macrophages, and plasma cells. This intralobular stroma is usually distinguished microscopically from the denser collagen containing extralobular stroma, which is itself surrounded by fat cells. The adipose tissue composes the bulk of the breast, but it is the parenchymal and stromal components that constitute the responsive elements of the basic functioning unit that will become fully differentiated during pregnancy and lactation.


Breast Cancer Menstrual Cycle Normal Breast Breast Development Messenger System 
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.
    Russo J, Gusterson BA, Rogers AE, et al. 1990. Comparative studies of human and rat mammary tumorigenisis. Lab Invest 62: 244–277.PubMedGoogle Scholar
  2. 2.
    Rudland PS. 1991. Histochemical organisation and cellular composition of ductal buds in developing human breast: evidence of cytochemical intermediates between epithelial and myoepithelial cells. J Histochem Cytochem 39: 1471–1484.PubMedGoogle Scholar
  3. 3.
    McFarland J. 1922. Respiratory lactation assay in the female breast: Their relation to chronic cystic mastitis and malignant disease. Arch Surg 5: 1–64.Google Scholar
  4. 4.
    Going JJ, Anderson TJ, Battersby S, Maclntyre C. 1988. Proliferative and secretory activity in human breast during natural and artificial menstrual cycles. Am J Pathol 130: 193–204.PubMedGoogle Scholar
  5. 5.
    Anderson TJ, Battersby S, King RJB, et al. 1989. Oral contraceptive use influences resting breast proliferation. Hum Pathol 20: 1139–1144.PubMedGoogle Scholar
  6. 6.
    Williams G, Anderson E, Howell A, et al. 1991. Oral contraceptive (OCP) use increases proliferation and decreases oestrogen receptor content of epithelial cells in the normal human breast. Int J Cancer 48: 206–210.PubMedGoogle Scholar
  7. 7.
    Anderson TJ, Ferguson DJP, Raab GM. 1982. Cell turnover in the ‘resting’ human breast: Influence of parity, contraceptive pill, age and laterality. Br J Cancer 46: 376–382.PubMedGoogle Scholar
  8. 8.
    Potten CS, Watson RJ, Williams GT, et al. 1988. The effect of age and menstrual cycle upon proliferative activity of the normal breast. Br J Cancer 58: 163–170.PubMedGoogle Scholar
  9. 9.
    Russo J, Calef G, Roi L, Russo IH. 1987. Influence of age and gland topography on cell kinetics of normal human breast tissue. J Natl Cancer Inst 98: 413–418.Google Scholar
  10. 10.
    Muir R. 1941. The evolution of carcinoma of the mamma. J Pathol Bacteriol 52: 155–172.Google Scholar
  11. 11.
    Foote FW, Stewart FW. 1945. Comparitive studies of cancerous versus non-cancerous breasts. Ann Surg 121: 6–53, 197-222.PubMedGoogle Scholar
  12. 12.
    Battersby S, Anderson TJ. 1989. Histological changes in breast tissue that characterise recent pregnancy. Histopathology 15: 41–419.Google Scholar
  13. 13.
    McMahon B, Cole P, Linn TM, et al. 1970. Age at first birth and breast cancer risk. Bull WHO 43: 209–221.Google Scholar
  14. 14.
    Laron Z, Kanli R, Pertzelan A. 1988. Clinical evidence on the role of oestrogens in the development of the breasts. Proc R Soc Edin 95B: 13–22.Google Scholar
  15. 15.
    Howell A. 1988. Clinical evidence for the involvement of oestrogen in the development and progression of breast cancer. Proc R Soc Edin 95B: 49–57.Google Scholar
  16. 16.
    Husseby RA, Thomas LB. 1954. Histological and histochemical alterations in the normal breast tissues of patients with advanced breast cancer being treated with estrogenic hormones. Cancer 7: 54–62.Google Scholar
  17. 17.
    Stoll BA. 1992. Breast cancer risk in Japanese women with special reference to the growth hormone-insulin-like growth factor axis. Jpn J Clin Oncol 22: 1–5.PubMedGoogle Scholar
  18. 18.
    Bidlingmaier F, Knorr D. 1978. Oestrogens — Physiological and Clinical Aspects, Pediatric and Adolescent Endocrinology, vol. 4. Karger: Basle, pp 6–81.Google Scholar
  19. 19.
    Ferenczy A, Bertrand G, Gelfand MM. 1988. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol 133: 859–867.Google Scholar
  20. 20.
    Anderson TJ, Battersby S. 1988. The involvement of oestrogen in the development and function of the normal breast; histological evidence. Proc R Soc Edin 95B: 23–32.Google Scholar
  21. 21.
    King RJB. 1991. A discussion of the roles of oestrogen and progestin in human mammary carcinogenesis. J Steroid Biochem Molec Biol 39(5B): 811–818.PubMedGoogle Scholar
  22. 22.
    Chalbos D, Escot C, Joyeux C, Tissot-Carayon MJ, Pages A, Rochefort H. 1990. Expression of the progestin-induced fatty acid synthetase in benign mastopathies and breast cancer as measured by RNA in situ hybridization. J Natl Cancer Inst 82: 602–606.PubMedGoogle Scholar
  23. 23.
    McManus MJ, Welsch CW. 1984. The effect of estrogen, progesterone, thyroxine and human placental lactogen on DNA synthesis of human breast ductal epithelium maintained in athymic nude mice. Cancer 54: 1920–1927.PubMedGoogle Scholar
  24. 24.
    Laidlaw IJ, Clarke R, Anderson E, Howell A. 1990. Proliferation of normal human breast tissue in nude mice after ovarian hormone stimulation. Br J Surg 77: A1419.Google Scholar
  25. 25.
    Mauvais-Jarvis P, Kuttenn F, Gompel A. 1986. Antiestrogen action of progesterone in breast cancer. Breast Cancer Res Treat 8: 179–188.PubMedGoogle Scholar
  26. 26.
    Carpenter S, Georgiade G, McCarty KS Sr, McCarty KS Jr. 1988. Immunohistochemical expression of oestrogen receptor in normal breast tissue. Proc R Soc Edin 95B: 59–66.Google Scholar
  27. 27.
    Battersby S, Robertson BJ, Anderson TJ, King RJB, McPherson K. 1992. Influence of menstrual cycle, parity and oral contraceptive use on steroid hormone receptors in normal breast. Br J Cancer 65: 601–607.PubMedGoogle Scholar
  28. 28.
    Press MF, Greene GL. 1988. Localization of progesterone receptor with monoclonal antibodies to the human progestin receptor. Endocrinology 122: 1165–1175.PubMedGoogle Scholar
  29. 29.
    Lippman ME, Dickson RB. 1988. Growth control of normal and malignant breast epithelium. Proc R Soc Edin 95B: 89–106.Google Scholar
  30. 30.
    Dickson RB, Johnson MD, Bano M, Shi E, et al. 1992. Growth factors in breast cancer: mitogenesis to transformation. J Steroid Biochem Mol Biol 43(l–3): 69–78.PubMedGoogle Scholar
  31. 31.
    Bano M, Worland P, Kidwell WR, et al. 1991. Receptor-induced phosphorylation by mammary-derived growth factor 1 in mammary epithelial cell lines. J Biol Chem 267: 10389–10392.Google Scholar
  32. 32.
    Osbournc CK, Clemmons DR, Arteaga CL. 1990. Rcgulation of breast cancer growth by insulin-like growth factors. J Steroid Biochem Mol Biol 37(6): 805–810.Google Scholar
  33. 33.
    Rosenfield RJ, Furlanetto R, Bock D. 1983. Relationship of somatomedin C concentration to pubertal changes. Pediatrics 103: 723–728.Google Scholar
  34. 34.
    Damjanov I, Mildner B, Knowles BB. 1986. Immunohistochemical localisation of epidcrmal growth factor receptor in normal tissues. Lab Invest 55: 588–592.PubMedGoogle Scholar
  35. 35.
    Perusinghe NP, Monaghan P, O’Hare MJ, Ashley S, Gusterson BA. 1992. Effects of growth factors on proliferation of basal and luminal cells in human breast epithelial expiants in serum-free culture. In Vitro Cell Dev Biol 28A: 90–96.Google Scholar
  36. 36.
    Battersby S, Anderson TJ, Miller WR. 1994. Patterns of cyclic AMP binding proteins in normal breast. Breast Cancer Res Treat (in press).Google Scholar
  37. 37.
    Cho-Chung YS. 1990. Role of cyclic AMP receptor proteins in growth differentiation and suppression of malignancy: new approaches to therapy. Cancer Res 50(22): 7093–7100.PubMedGoogle Scholar
  38. 38.
    O’Brian CA, Vogel VG, Singletary SE, Ward NE. 1989. Elevated protein kinase C expression in human breast tumor biopsies relative to normal breast tissue. Cancer Res 49: 3215–3217.PubMedGoogle Scholar
  39. 39.
    Hennipman A, van Oirschot BA, Smith J, Rijksen G, Staal GEJ. 1989. Tyrosine kinase activity in breast cancer, benign breast disease and normal breast tissue. Cancer Res 49: 516–521.PubMedGoogle Scholar
  40. 40.
    Anderson TJ, Wyllie AH. 1989. Neoplasia. In Kyle J, Carey LC (eds), Scientific Foundations of Surgery, 4th ed. Heinemann: London, pp 547–557.Google Scholar
  41. 41.
    Gallager HS. 1980. The developmental pathology of breast cancer. Cancer 46: 905–907.PubMedGoogle Scholar
  42. 42.
    Wellings SR, Jensen HM, Marcum RG. 1975. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J Natl Cancer Inst 55: 231–273.PubMedGoogle Scholar
  43. 43.
    Page DL, Dupont WD, Rogers LW, Landenberger M. 1982. Intraductal carcinoma of the breast: Follow-up after treatment by biopsy only. Cancer 49: 751–758.PubMedGoogle Scholar
  44. 44.
    Betsill WL, Rosen PP, Lieberman PH, Robbins GF. 1978. Intra ductal carcinoma: Long-term follow-up after treatment by biopsy alone. JAMA 239: 1863–1867.PubMedGoogle Scholar
  45. 45.
    Haggensen CD, Lane N, Lattes R, Bodian C. 1978. Lobular neoplasia (so called lobular carcinoma in situ) of the breast. Cancer 42: 737–769.Google Scholar
  46. 46.
    Dupont WD, Page DL. 1985. Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 312: 146–151.PubMedGoogle Scholar
  47. 47.
    Rywlin AM. 1984. Perspectives in pathology: Terminology of premalignant lesions in light of the multistep theory of carcinogenesis. Hum Pathol 15: 806–807.PubMedGoogle Scholar
  48. 48.
    Page DL, Dupont WD. 1990. Anatomic markers of human premalignancy and risk of breast cancer. Cancer 66: 1326–1335.PubMedGoogle Scholar
  49. 49.
    Anderson TJ. 1991. Genesis and source of breast cancer. Br Med Bull 47: 305–318.PubMedGoogle Scholar
  50. 50.
    Hutter RVP, et al. 1986. Consensus meeting. Is ‘fibrocystic disease’ of the breast precancerous? Arch Pathol Lab Med 110: 171–173.Google Scholar
  51. 51.
    Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61: 759–767.PubMedGoogle Scholar
  52. 52.
    Arends MJ, Wyllie AH, Bird CC. 1990. Papillomaviruses and human cancer. Hum Pathol 21: 686–698.PubMedGoogle Scholar
  53. 53.
    Chamberlain J. 1982. Screening and natural history of breast cancer. In Baum M (ed), Clinics in Oncology: Breast Cancer, vol. 1(3). Saunders: Philadelphia, pp 679–701.Google Scholar
  54. 54.
    Anderson TJ. 1989. Breast cancer screening: Principles and practicalities for histopathologists. In Anthony P, MacSween RNM (eds), Recent Advances in Histopathology, vol. 14. Churchill Livingstone: Edinburgh, pp 43–61.Google Scholar
  55. 55.
    Miller AB. 1984. Biological aspects of natural history and its relevance to screening. In Prorock PC, Miller AB (eds), Screening for Cancer. UICC Technical Report Series 78: 44–54.Google Scholar
  56. 56.
    Forrest P. 1990. Breast cancer: the decision to screen. Nuffield Provisional Hospital Trust, London, pp 62–103.Google Scholar
  57. 57.
    Arnerlov C, Emdin SÖ, Lundgren B, et al. 1992. Breast carcinoma growth rate described by mammographic doubling time and s-phase fraction; Correlations to clinical and histopathologic factors in a screened population. Cancer 70: 1928–1934.PubMedGoogle Scholar
  58. 58.
    Tabar L, Fagerberg G, Day NE, et al. 1992. Breast cancer treatment and natural history; new insights from results of screening. Lancet 339: 412–414.PubMedGoogle Scholar
  59. 59.
    Hellman S, Harris JR. 1987. The appropriate breast cancer paradigm. Cancer Res 47: 339–342.PubMedGoogle Scholar
  60. 60.
    Tubiana M, Koscielny S. 1991. Natural history of human breast cancer: Recent data and clinical implications. Breast Cancer Res Treat 18.125–140.PubMedGoogle Scholar
  61. 61.
    Linell F, Rank F. 1989. Breast Cancer. Comments on Histologic Classifications with Reference to Histogenesis and Prognosis. Universitetsforlaget Dialogos: Lund, pp 18–68.Google Scholar
  62. 62.
    Anderson TJ, Battersby S. 1985. Radial scars of benign and malignant breasts: comparitive features and significance. J Pathol 147: 23–32.PubMedGoogle Scholar
  63. 63.
    Andersen JA, Gram JB. 1984. Radial scar in the female breast: a long term follow-up of 32 cases. Cancer 53: 2557–2560.PubMedGoogle Scholar
  64. 64.
    Andersen JA, Carter D, Linell F. 1986. A symposium on sclerosing duct lesions of the breast. Pathol Annu 21(2): 145–179.PubMedGoogle Scholar
  65. 65.
    Anderson TJ, Lamb J, Donnan P, et al. 1991. Comparative pathology of breast cancer in a randomised trial of screening. Br J Cancer 64: 108–113.PubMedGoogle Scholar
  66. 66.
    Hawkins RA, Miller WR. 1988. Endogenous sex hormones in cancer development. In Stoll BA (ed), Endocrine Management of Cancer: Biological Basis. Kargel Press: pp 45–60.Google Scholar
  67. 67.
    Preston-Martin S, Pike MC, Ross RK, Jones PA, Henderson BE. 1990. Increased cell division as a cause of human cancer. Cancer Res 50: 7415–7421.PubMedGoogle Scholar
  68. 68.
    World Health Organization/ International Agency for Research on Cancer Genetic and Related Effects. 1987. An Updating of Selected IARC Monographs from Vols. 1-42. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Supplement. pp 250–256, 293-295, 369-371, 426-433, 437-443.Google Scholar
  69. 69.
    Nenci I, Marchetti E, Querzoli P. 1988. Commentary on human mammary preneoplasia: the estrogen receptor promotion hypothesis. J Steroid Biochem 30: 105–106.PubMedGoogle Scholar
  70. 70.
    Hawkins RA, Tesdale AL, Ferguson WA, Going JJ. 1987. Oestrogen receptor activity in intraduct and invasive breast carcinomas. Breast Cancer Res Treat 9: 129–133.PubMedGoogle Scholar
  71. 71.
    Alpers CE, Wellings SR. 1985. The prevalence of carcinoma in-situ in normal and cancer-associated breasts. Hum Pathol 16: 796–807.PubMedGoogle Scholar
  72. 72.
    Dao TL, Sinha DK, Memota T, Patel J. 1982. Effects of estrogen and progesterone on cellular replication of human breast tumours. Cancer Res 42: 359–362.PubMedGoogle Scholar
  73. 73.
    Miller WR 1990. Endocrine treatment for breast cancers: biological rationale and current progress. J Steroid Biochem Mol Biol 37: 467–480.PubMedGoogle Scholar
  74. 74.
    Miller WR. 1991. Oestrogens and breast cancer: biological considerations. Br Med Bull 47: 470–483.PubMedGoogle Scholar
  75. 75.
    Hawkins RA, Roberts MM, Forrest APM. 1980. Oestrogen receptors in breast cancer: Current status. Br J Surg 67: 153–169.PubMedGoogle Scholar
  76. 76.
    Merkel DE, Osborne CK. 1988. Steroid receptors in relation to response. In Stoll BA (ed), Endocrine Management of Cancer: Biological Basis. Kargel Press: pp 84–89.Google Scholar
  77. 77.
    Weimer DA, Donegan WL. 1987. Changes in estrogen and progesterone receptor content of primary breast carcinoma during the menstrual cycle. Breast Cancer Res Treat 10: 273–278.PubMedGoogle Scholar
  78. 78.
    Press MF, Nousek-Goebi N, King WJ, Herbst AL, Greene GL. 1984. Immunohisto-chemical assessment of estrogen receptor distribution in the human endometrium throughout the menstrual cycle. Lab Invest 51: 495–503.PubMedGoogle Scholar
  79. 79.
    Santen RJ, Marini A, Harvey H, Richmond C. 1990. Endocrine treatment of breast cancer in women. Endocrine Rev 2: 221–265.Google Scholar
  80. 80.
    Horwitz KB, Freidenberg GR. 1985. Growth inhibition and increase of insulin receptors in antiestrogen-resistant T47DCO human brcast canccr cells by progcstins; implications for endocrine therapies. Cancer Res 45:167–173.PubMedGoogle Scholar
  81. 81.
    Clark JH, Peck EJ Jr. 1979. Female sex steroids. Receptors and Function. Springer: Berlin, pp 99–113.Google Scholar
  82. 82.
    King RJB. 1990. Role of oestrogen and progestin in human mammary carcinogenesis. In Goldhirsch A (ed), Endocrine Therapy of Breast Cancer IV. Springer-Verlag: Berlin, pp 3–8.Google Scholar
  83. 83.
    King RJB. 1992. Progression from steroid sensitive to insensitive state in breast tumours. Cancer Surv 14: 131–146.PubMedGoogle Scholar
  84. 84.
    Isaacs JT. 1988. Clinical heterogeneity in relation to response. In Stoll BA (ed), Endocrine Management of Cancer: Biological Basis. Pub Kargel Press: pp 125–145.Google Scholar
  85. 85.
    Hamon JT, Allegra JC. 1988. Loss of hormonal responsiveness in cancer. In Stoll BA (ed), Endocrine Management of Cancer: Biological Basis. Kargel Press: pp 61–71.Google Scholar
  86. 86.
    Allegra JC, Barlock A, Huff KK, Lippman ME. 1980. Changes in multiple or sequential estrogen receptors in breast cancer. Cancer 45: 792–794.PubMedGoogle Scholar
  87. 87.
    Hawkins RA, Tesdale A, Anderson L, et al. 1990. Does the oestrogen receptor concentration of a breast cancer change during system therapy. Br J Cancer 61: 877–880.PubMedGoogle Scholar
  88. 88.
    McGuire WL, Chamness GC, Fuqua SAW. 1992. Abnormal estrogen receptors in clinical breast cancer. J Steroid Biochem Mol Biol 43: 243–247.PubMedGoogle Scholar
  89. 89.
    Klijn JGM, Berns PMJJ, Bontenbal M, Alexieva-Figusch J, Foeckens JA. 1992. Clinical breast cancer, new developments in selection and endocrine treatment of patients. J Steroid Biochem Mol Biol 43: 211–221.PubMedGoogle Scholar
  90. 90.
    Allred DC, Clark GM, Molina R, Tandon AK, Schnitt SJ, Gilchrist KW, Osborne CK, Tormey DC, McGuire WL. 1992. Overexpression of HER-2/neu and its relationship with other prognostic factors change during the progression of in situ to invasive breast cancer. Hum Pathol 23: 974–979.PubMedGoogle Scholar
  91. 91.
    Bates SE, Davidson NE, Valverius EM, Dickson RB, Freter CE, Tarn JP, Kudlow JE, Lippman ME, Salomon DS. 1988. Expression of transforming growth factor alpha and mRNAin human breast cancer: Its regulation by oestrogen and its possible functional significance. Mol Endocrinol 2: 543–555PubMedGoogle Scholar
  92. 92.
    Travers MR, Barrett-Lee PJ, Berger U, Luqmani YA, Gazet J-C, Powles TJ, Coombes R. 1988. Growth factor expression in normal, benign and malignant breast tissue. Br Med J 296: 1621–1630.Google Scholar
  93. 93.
    Gregory H, Thomas CE, Willshire IR, Young JA, Anderson H, Baildan A, Howell A. 1989. Epidermal and transforming growth factor x in patients with breast tumours. Br J Cancer 59: 605–609.PubMedGoogle Scholar
  94. 94.
    Dickson RB, Lippman ME. 1986. Hormonal control of human breast cancer cell lines. Cancer Surv 5: 617–624.PubMedGoogle Scholar
  95. 95.
    King RJB, Wang DY, Daly RJ, Darbre PDJ. 1989. Approaches to studying the role of growth factors in the progression of breast tumours from the steroid sensitivity in insensitive state. J Steroid Biochem 34: 133–138.PubMedGoogle Scholar
  96. 96.
    Knabbe C, Lippman ME, Wakefield LM, Flanders K, Hanoi A, Derynck R, Dickson RB. 1987. Evidence that TGFβ is a hormonally regulated growth factor in human breast cancer. Cell 48: 417–428.PubMedGoogle Scholar
  97. 97.
    Coombes RC, Barrett-Lee P, Lugnani Y. 1990. Growth factor expression in breast tissue. J Steroid Biochem Mol Biol 37: 833–836.PubMedGoogle Scholar
  98. 98.
    Delvenne CG, Winkler-Gol RA, Piccard MJ, Hustin J, Michaux D, Leclercq G, Nogaret JM, Autier Ph. 1992. Expression of c-erbB2, TGF-ßl and pS2 genes in primary human breast cancers. Eur J Cancer 28: 700–705.PubMedGoogle Scholar
  99. 99.
    Butta A, macLennan K, Flanders KC, et al. 1992. Induction of transforming growth factor ßl in human breast cancer in vivo following tamoxifen treatment. Cancer Res 52: 4261–4264.PubMedGoogle Scholar
  100. 100.
    Pekonen F, Partanen S, Makinen T, Rutanen EM. 1988. Receptors for epidermal growth factor and insulin growth factor 1 and their relation to steroid receptors in human breast cancer. Cancer Res 1343–1347.Google Scholar
  101. 101.
    Jammes H, Peyrat JP, Ban E, Vilain MO, Haour F, Djiane J, Bonneterre J. 1992. Insulinlike growth factor — receptors in human breast tumor — localization and quantification by histo-autoradiographic analysis. Br J Cancer 66(N2): 248–253.PubMedGoogle Scholar
  102. 102.
    Cantley LC, Auger KR, Carpenter C, Duckworth B, Granziani A, Kapeller R, Soltoff. 1991. Oncogenes and signal transduction. Cell 64: 281–302.PubMedGoogle Scholar
  103. 103.
    Ullrich A, Schlessinger J. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212.PubMedGoogle Scholar
  104. 104.
    Waterfield MD. 1989. Growth factor receptors. Br Med Bull 45: 541–553.PubMedGoogle Scholar
  105. 105.
    Ottenhoff-Kaff, AE, Rijksen G, van Beurden EACM, Hennipman A, Michels AA, Staal GEJ. 1992. Characterization of protein tyrosine kinases from human breast cancer: Involvement of the c-src oncogene product. Cancer Res 52: 4773–4778.Google Scholar
  106. 106.
    O’Brian CA, Ward NE. 1989. Biology of the protein kinase C family. Cancer Metastasis Rev 8: 199–214.PubMedGoogle Scholar
  107. 107.
    Miller WR, Elton RA, Dixon JM, Chetty U, Watson DMA. 1990. Cyclic AMP binding proteins and prognosis in breast cancer. Br J Cancer 61: 263–266.PubMedGoogle Scholar
  108. 108.
    Miller WR, Hulme MJ, Cho-Chung Y-S, Elton RA. In press. Types of cyclic AMP binding proteins in human breast cancers. Eur J Cancer.Google Scholar
  109. 109.
    Cho-Chung YS, Clair T, Tortora G, et al. 1991. Role of site-selective cAMP analogs in the control and reversal of malignancy. Pharmacol Ther 50: 1–33.PubMedGoogle Scholar
  110. 110.
    Page DL, Dupont WD. 1992. Indicators of increased breast cancer risk in humans. J Cell Biochem Suppl 16G: 175–182.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • Thomas J. Anderson
  • William R. Miller

There are no affiliations available

Personalised recommendations