A delicate balance: TGF-β and the tumor microenvironment

Journal of Cellular Biochemistry

Volumn 101, Issue 4, 2007, Pages 851-861

  Stover, Daniel G ^a   Bierie, Brian ^b   Moses, Harold L ^a,b,c,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d 691 Preston Research Building ^*  (United States)

Author keywords

Cancer; Carcinoma; Stromal epithelial interactions; TGF ; Transforming growth factor beta; Tumor microenvironment

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

CANCER IMMUNOLOGY; CARCINOGENESIS; EPITHELIUM CELL; FIBROBLAST; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR GROWTH;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; HUMANS; MESODERM; MODELS, BIOLOGICAL; NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 34447261691     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21149     Document Type: Review

References (49)

1. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K. 2004. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6:17-32.
2. Annes JP, Munger JS, Rifkin DB. 2003. Making sense of latent TGFbeta activation. J Cell Sci 116:217-224.
3. Barcellos-Hoff MH, Ravani SA. 2000. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res 60:1254-1260.
4. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, Washington MK, Neilson EG, Moses HL. 2004. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303:848-851.
5. Bierie B, Moses HL. 2006a. TGF-beta and cancer. Cytokine Growth Factor Rev 17:29-40.
6. Bierie B, Moses HL. 2006b. Tumour microenvironment: TGFbeta: The molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6:506-520.
7. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, Pietenpol JA, Moses HL. 2004. Induction by transforming growth factor-beta1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res 6:R215-R231.
8. Chen RH, Derynck R. 1994. Homomeric interactions between type II transforming growth factor-beta receptors. J Biol Chem 269:22868-22874.
9. Cheng N, Bhowmick NA, Chytil A, Gorksa AE, Brown KA, Muraoka R, Arteaga CL, Neilson EG, Hayward SW, Moses HL. 2005. Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene 24:5053-5068.
10. Coffey RJ, Jr., Goustin AS, Soderquist AM, Shipley GD, Wolfshohl J, Carpenter G, Moses HL. 1987. Transforming growth factor alpha and beta expression in human colon cancer lines: Implications for an autocrine model. Cancer Res 47:4590-4594.
11. Coussens LM, Werb Z. 2002. Inflammation and cancer. Nature 420:860-867.
12. Crawford SE, Stellmach V, Murphy-Ullrich JE, Ribeiro SM, Lawler J, Hynes RO, Boivin GP, Bouck N. 1998. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93:1159-1170.
13. Cui W, Fowlis DJ, Bryson S, Duffie E, Ireland H, Balmain A, Akhurst RJ. 1996. TGFbeta1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 86:531-542.
14. Dalai BI, Keown PA, Greenberg AH. 1993. Immunocytochemical localization of secreted transforming growth factor-beta 1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am J Pathol 143:381-389.
15. de Larco JE, Todaro GJ. 1978. Growth factors from murine sarcoma virus-transformed cells. Proc Natl Acad Sci USA 75:4001-4005.
16. Derynck R, Zhang YE. 2003. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425:577-584.
17. Derynck R, Jarrett JA, Chen EY, Eaton DH, Bell JR, Assoian RK, Roberts AB, Sporn MB, Goeddel DV. 1985. Human transforming growth factor-beta complementary DNA sequence and expression in normal and transformed cells. Nature 316:701-705.
18. Ewan KB, Shyamala G, Ravani SA, Tang Y, Akhurst R, Wakefield L, Barcellos-Hoff MH. 2002. Latent transforming growth factor-beta activation in mammary gland: Regulation by ovarian hormones affects ductal and alveolar proliferation. Am J Pathol 160:2081-2093.
19. Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61:759-767.
20. Feng XH, Derynck R. 1996. Ligand-independent activation of transforming growth factor (TGF) beta signaling pathways by heteromeric cytoplasmic domains of TGF-beta receptors. J Biol Chem 271:13123-13129.
21. Harpel JG, Schultz-Cherry S, Murphy-Ullrich JE, Rifkin DB. 2001. Tamoxifen and estrogen effects on TGF-beta formation: Role of thrombospondin-1, alphavbeta3, and integrin-associated protein. Biochem Biophys Res Commun 284:11-14.
22. Hayward SW, Wang Y, Cao M, Hom YK, Zhang B, Grossfeld GD, Sudilovsky D, Cunha GR. 2001. Malignant transformation in a nontumorigenic human prostatic epithelial cell line. Cancer Res 61:8135-8142.
23. Hu M, Yao J, Cai L, Bachman KE, van den Brule F, Velculescu V, Polyak K. 2005. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 37:899-905.
24. Hyytiainen M, Penttinen C, Keski-Oja J. 2004. Latent TGF-beta binding proteins: Extracellular matrix association and roles in TGF-beta activation. Crit Rev Clin Lab Sci 41:233-264.
25. Joesting MS, Perrin S, Elenbaas B, Fawell SE, Rubin JS, Franco OE, Hayward SW, Cunha GR, Marker PC. 2005. Identification of SFRP1 as a candidate mediator of stromal-to-epithelial signaling in prostate cancer. Cancer Res 65:10423-10430.
26. Joseph H, Gorska AE, Sohn P, Moses HL, Serra R. 1999. Overexpression of a kinase-deficient transforming growth factor-beta type II receptor in mouse mammary stroma results in increased epithelial branching. Mol Biol Cell 10:1221-1234.
27. Kim SJ, Im YH, Markowitz SD, Bang YJ. 2000. Molecular mechanisms of inactivation of TGF-beta receptors during carcinogenesis. Cytokine Growth Factor Rev 11:159-168.
28. Kim BG, Li C, Qiao W, Mamura M, Kasperczak B, Anver M, Wolfraim L, Hong S, Mushinski E, Potter M, Kim SJ, Fu XY, Deng C, Letterio JJ. 2006. Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 441:1015-1019.
29. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, Richardson A, Weinberg RA. 2004. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 101:4966-4971.
30. Kurose K, Hoshaw-Woodard S, Adeyinka A, Lemeshow S, Watson PH, Eng C. 2001. Genetic model of multi-step breast carcinogenesis involving the epithelium and stroma: Clues to tumour-microenvironment interactions. Hum Mol Genet 10:1907-1913.
31. Kurose K, Gilley K, Matsumoto S, Watson PH, Zhou XP, Eng C. 2002. Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet 32:355-357.
32. Lawler J, Detmar M. 2004. Tumor progression: The effects of thrombospondin-1 and -2. Int J Biochem Cell Biol 36:1038-1045.
33. Levy L, Hill CS. 2006. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 17:41-58.
34. Miettinen PJ, Ebner R, Lopez AR, Derynck R. 1994. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127:2021-2036.
35. Minn AJ, Kang Y, Serganova I, Gupta GP, Giri DD, Doubrovin M, Ponomarev V, Gerald WL, Blasberg R, Massague J. 2005. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest 115:44-55.
36. Moses HL, Branum EL, Proper JA, Robinson RA. 1981. Transforming growth factor production by chemically transformed cells. Cancer Res 41:2842-2848.
37. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. 1999. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59:5002-5011.
38. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. 2005. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121:335-348.
39. Rifkin DB. 2005. Latent transforming growth factor-beta (TGF-beta) binding proteins: Orchestrators of TGF-beta availability. J Biol Chem 280:7409-7412.
40. Roberts AB, Wakefield LM. 2003. The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci USA 100:8621-8623.
41. Roberts AB, Anzano MA, Lamb LC, Smith JM, Sporn MB. 1981. New class of transforming growth factors potentiated by epidermal growth factor: Isolation from non-neoplastic tissues. Proc Natl Acad Sci USA 78:5339-5343.
42. Roberts AB, Anzano MA, Wakefield LM, Roche NS, Stern DF, Sporn MB. 1985. Type beta transforming growth factor: A bifunctional regulator of cellular growth. Proc Natl Acad Sci USA 82:119-123.
43. Schultz-Cherry S, Chen H, Mosher DF, Misenheimer TM, Krutzsch HC, Roberts DD, Murphy-Ullrich JE. 1995. Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J Biol Chem 270:7304-7310.
44. Seemayer TA, Lagace R, Schurch W, Tremblay G. 1979. Myofibroblasts in the stroma of invasive and metastatic carcinoma: A possible host response to neoplasia. Am J Surg Pathol 3:525-533.
45. Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. 2001. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: Implications for tumor development and progression. Cancer Res 61:1320-1326.
46. Shipley GD, Pittelkow MR, Wille JJ, Jr., Scott RE, Moses HL. 1986. Reversible inhibition of normal human prokeratinocyte proliferation by type beta transforming growth factor-growth inhibitor in serum-free medium. Cancer Res 46:2068-2071.
47. Sterner-Kock A, Thorey IS, Koli K, Wempe F, Otte J, Bangsow T, Kuhlmeier K, Kirchner T, Jin S, Keski-Oja J, von Melchner H. 2002. Disruption of the gene encoding the latent transforming growth factor-beta binding protein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev 16:2264-2273.
48. Tucker RF, Shipley GD, Moses HL, Holley RW. 1984. Growth inhibitor from BSC-1 cells closely related to platelet type beta transforming growth factor. Science 226:705-707.
49. Yu Q, Stamenkovic I. 2000. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14:163-176.