Wnt1 expression induces short-range and long-range cell recruitments that modify mammary tumor development and are not induced by a cell-autonomous β-catenin effector

Cancer Research

Volumn 68, Issue 24, 2008, Pages 10145-10153

  Young, Chul Kim ^a   Clark, Rod J ^a   Ranheim, Erik A ^b   Alexander, Caroline M ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DELTA N BETA CATENIN; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ADENOCARCINOMA; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST TUMOR; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; EFFECTOR CELL; ENDOTHELIUM CELL; EPITHELIUM CELL; GENE EXPRESSION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; STROMA; STROMA CELL; TRANSGENIC MOUSE; TUMOR GROWTH;

ANIMALS; BETA CATENIN; DISEASE PROGRESSION; FEMALE; MACROPHAGES; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; STROMAL CELLS; WNT1 PROTEIN;

EID: 57749105327     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2992     Document Type: Article

References (50)

1. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001;1:46-54.
2. Barcellos-Hoff MH, Ravani SA. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res 2000;60:1254-60.
3. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 1999;59:5002-11.
4. Skobe M, Fusenig NE. Tumorigenic conversion of immortal human keratinocytes through stromal cell activation. Proc Natl Acad Sci U S A 1998;95:1050-5.
5. Kurose K, Gilley K, Matsumoto S, Watson PH, Zhou XP, Eng C. Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet 2002;32:355-7.
6. Hill R, Song Y, Cardiff RD, Van Dyke T. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell 2005;123:1001-11.
7. Hu M, Yao J, Cai L, et al. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 2005;37:899-905.
8. Bhowmick NA, Chytil A, Plieth D, et al. TGF-β signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004;303:848-51.
9. Ronnov-Jessen L, Petersen OW, Bissell MJ. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev 1996;76:69-125.
10. Allinen M, Beroukhim R, Cai L, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004;6:17-32.
11. Finak G, Bertos N, Pepin F, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008;14:518-27.
12. Finak G, Sadekova S, Pepin F, et al. Gene expression signatures of morphologically normal breast tissue identify basal-like tumors. Breast Cancer Res 2006;8:R58.
13. Vainio S, Muller U. Inductive tissue interactions, cell signaling, and the control of kidney organogenesis. Cell 1997;90:975-8.
14. Kratochwil K, Galceran J, Tontsch S, Roth W, Grosschedl R. FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev 2002;16:3173-85.
15. Boras-Granic K, Chang H, Grosschedl R, Hamel PA. Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland. Dev Biol 2006;295:219-31.
16. Polakis P. Wnt signaling and cancer. Genes Dev 2000;14:1837-51.
17. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004;20:781-810.
18. Clevers H. Wnt/β-catenin signaling in development and disease. Cell 2006;127:469-80.
19. Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 1988;55:619-25.
20. Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. Δ N89 β-Catenin induces precocious development, differentiation, and neoplasia in mammary gland. J Cell Biol 2001;153:555-68.
21. Li Y, Welm B, Podsypanina K, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci U S A 2003;100:15853-8.
22. Liu BY, McDermott SP, Khwaja SS, Alexander CM. The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc Natl Acad Sci U S A 2004;101:4158-63.
23. Sternlicht MD, Lochter A, Sympson CJ, et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999;98:137-46.
24. Wiseman BS, Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002;296:1046-9.
25. Orimo A, Gupta PB, Sgroi DC, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005;121:335-48.
26. Weber-Hall SJ, Phippard DJ, Niemeyer CC, Dale TC. Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 1994;57:205-14.
27. Sugimoto H, Mundel TM, Kieran MW, Kalluri R. Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 2006;5:1640-6.
28. Michaelson JS, Leder P. β-catenin is a downstream effector of Wnt-mediated tumorigenesis in the mammary gland. Oncogene 2001;20:5093-9.
29. Gunther EJ, Moody SE, Belka GK, et al. Impact of p53 loss on reversal and recurrence of conditional Wnt-induced tumorigenesis. Genes Dev 2003;17:488-501.
30. Lane TF, Leder P. Wnt-10b directs hypermorphic development and transformation in mammary glands of male and female mice. Oncogene 1997;15:2133-44.
31. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 2001;10:545-53.
32. Bradley RS, Brown AM. The proto-oncogene int-1 encodes a secreted protein associated with the extracellular matrix. EMBO J 1990;9:1569-75.
33. Coudreuse D, Korswagen HC. The making of Wnt: new insights into Wnt maturation, sorting and secretion. Development 2007;134:3-12.
34. Pennica D, Swanson TA, Welsh JW, et al. WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci U S A 1998;95:14717-22.
35. Xu L, Corcoran RB, Welsh JW, Pennica D, Levine AJ. WISP-1 is a Wnt-1- and β-catenin-responsive oncogene. Genes Dev 2000;14:585-95.
36. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002;22:1172-83.
37. Huang S, Li Y, Chen Y, et al. Changes in gene expression during the development of mammary tumors in MMTV-Wnt-1 transgenic mice. Genome Biol 2005;6:R84.
38. Brack AS, Conboy MJ, Roy S, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007;317:807-10.
39. Tuxhorn JA, Ayala GE, Rowley DR. Reactive stroma in prostate cancer progression. J Urol 2001;166:2472-83.
40. Rafii S, Lyden D, Benezra R, Hattori K, Heissig B. Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2002;2:826-35.
41. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer towards marker and target identification. Nat Rev Cancer 2006;6:835-45.
42. Direkze NC, Hodivala-Dilke K, Jeffery R, et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004;64:8492-5.
43. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006;66:605-12.
44. Lindvall C, Evans NC, Zylstra CR, Li Y, Alexander CM, Williams BO. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J Biol Chem 2006;281:35081-7.
45. Zhou W, Lin L, Majumdar A, et al. Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFβ2. Nat Genet 2007;39:1225-34.
46. Panakova D, Sprong H, Marois E, Thiele C, Eaton S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 2005;435:58-65.
47. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 1999;18:3964-72.
48. Grunewald M, Avraham I, Dor Y, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006;124:175-89.
49. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004;10:858-64.
50. Ugolini F, Charafe-Jauffret E, Bardou VJ, et al. WNT pathway and mammary carcinogenesis: loss of expression of candidate tumor suppressor gene SFRP1 in most invasive carcinomas except of the medullary type. Oncogene 2001;20:5810-7.