An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers

American Journal of Pathology

Volumn 174, Issue 6, 2009, Pages 2023-2034

  Witkiewicz, Agnieszka K ^a,b,c   Dasgupta, Abhijit ^c   Sotgia, Federica ^a,b   Mercier, Isabelle ^a,b   Pestell, Richard G ^a,b   Sabel, Michael ^d   Kleer, Celina G ^d   Brody, Jonathan R ^a   Lisanti, Michael P ^a,b,c  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; TAMOXIFEN;

ADULT; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STAGING; CANCER SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; PATIENT CODING; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TISSUE MICROARRAY;

EID: 66549114050     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080873     Document Type: Article

References (43)

1. Bhowmick NA, Neilson EG, Moses HL: Stromal fibroblasts in cancer initiation and progression. Nature 2004, 432:332-337 (Pubitemid 39551661)
2. Bissell MJ, Radisky D: Putting tumours in context. Nat Rev Cancer 2001, 1:46-54 (Pubitemid 33741880)
3. Mueller MM, Fusenig NE: Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 2004, 4:839-849 (Pubitemid 39472951)
4. Kim JB, Stein R, O'Hare MJ: Tumour-stromal interactions in breast cancer: the role of stroma in tumourigenesis. Tumour Biol 2005, 26:173-185 (Pubitemid 41379743)
5. 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, 59:5002-5011 (Pubitemid 29472907)
6. Kalluri R, Zeisberg M: Fibroblasts in cancer. Nat Rev Cancer 2006, 6:392-401
7. Serini G, Gabbiani G: Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 1999, 250:273-283 (Pubitemid 29367440)
8. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA: Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348 (Pubitemid 40692295)
9. Hnasko R, Lisanti MP: The biology of caveolae: lessons from caveolin knockout mice and implications for human disease. Mol Interv 2003, 3:445-464
10. Koleske AJ, Baltimore D, Lisanti MP: Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 1995, 92:1381-1385
11. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, Lisanti MP: Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 1997, 272:16374-16381 (Pubitemid 27276462)
12. Williams TM, Lisanti MP: Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 2005, 288:C494-C506 (Pubitemid 40229478)
13. Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, Lisanti MP: Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 1998, 17:6633-6648 (Pubitemid 28521797)
14. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H, Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP: Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001, 276:38121-38138 (Pubitemid 37384066)
15. Mercier I, Casimiro MC, Wang C, Rosenberg AL, Quong J, Minkeu A, Allen KG, Danilo C, Sotgia F, Bonuccelli G, Jasmin JF, Xu H, Bosco E, Aronow B, Witkiewicz A, Pestell RG, Knudsen ES, Lisanti MP: Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: implications for the response to hormonal therapy. Cancer Biol Ther 2008, 7:1212-1225
16. Williams TM, Sotgia F, Lee H, Hassan G, Di Vizio D, Bonuccelli G, Capozza F, Mercier I, Rui H, Pestell RG, Lisanti MP: Stromal and epithelial caveolin-1 both confer a protective effect against mammary hyperplasia and tumorigenesis: caveolin-1 antagonizes cyclin D1 function in mammary epithelial cells. Am J Pathol 2006, 169:1784-1801 (Pubitemid 351182008)
17. Elston CW, Ellis IO: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. C. W. Elston & I. O. Ellis. Histo- pathology 1991;19: 403-410,
18. Histopathology 2002, 41:151-152, discussion 152-153
19. Kaplan EL, Meier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958, 53:457-481
20. Cox DR: Regression models and life tables. J Royal Stat Soc 1972, 34:187-220
21. Breiman L, Friedman J, Stone CJ, Olshen RA: Classification and Regression Trees. Chapman and Hall, 1984, Belmont, CA, pp 216-264
22. LeBlanc M, Crowley J: Relative risk trees for censored survival data. Biometrics 1992, 48:411-425
23. R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing, 2008
24. Sotgia F, Del Galdo F, Casimiro MC, Bonuccelli G, Mercier I, Whitaker-Menezes D, Daumer KM, Zhou J, Wang C, Katiyar S, Xu H, Bosco E, Quong AA, Aronow B, Witkiewicz AK, Minetti C, Frank PG, Jimenez SA, Knudsen ES, Pestell RG, Lisanti MP: Caveolin-1 (-/-) null mammary stromal fibroblasts share characteristics with human breast cancer-associated fibroblasts, Am J Pathol 2008, 174:746-761
25. Elsheikh SE, Green AR, Rakha EA, Samaka RM, Ammar AA, Powe D, Reis-Filho JS, Ellis IO: Caveolin 1 and Caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br J Cancer 2008, 99:327-334
26. Li T, Sotgia F, Vuolo MA, Li M, Yang WC, Pestell RG, Sparano JA, Lisanti MP: Caveolin-1 mutations in human breast cancer: functional association with estrogen receptor alpha-positive status. Am J Pathol 2006, 168:1998-2013 (Pubitemid 43825319)
27. Sagara Y, Mimori K, Yoshinaga K, Tanaka F, Nishida K, Ohno S, Inoue H, Mori M: Clinical significance of Caveolin-1. Caveolin-2 and HER2/neu mRNA expression in human breast cancer. Br J Cancer 2004, 91:959-965 (Pubitemid 39273791)
28. Iwaya K, Ogawa H, Izumi M, Kuroda M, Mukai K: Stromal expression of CD10 in invasive breast carcinoma: a new predictor of clinical outcome. Virchows Arch 2002, 440:589-593 (Pubitemid 34809689)
29. Makretsov NA, Hayes M, Carter BA, Dabiri S, Gilks CB, Huntsman DG: Stromal CD10 expression in invasive breast carcinoma correlates with poor prognosis, estrogen receptor negativity, and high grade. Mod Pathol 2007, 20:84-89 (Pubitemid 44967953)
30. Mylona E, Nomikos A, Magkou C, Kamberou M, Papassideri I, Keramopoulos A, Nakopoulou L: The clinicopathological and prognostic significance of membrane type 1 matrix metalloproteinase (MT1-MMP) and MMP-9 according to their localization in invasive breast carcinoma. Histopathology 2007, 50:338-347 (Pubitemid 46169418)
31. West RB, Nuyten DS, Subramanian S, Nielsen TO, Corless CL, Rubin BP, Montgomery K, Zhu S, Patel R, Hernandez-Boussard T, Goldblum JR, Brown PO, van de Vijver M, van de Rijn M: Determination of stromal signatures in breast carcinoma. PLoS Biol 2005, 3:E187 (Pubitemid 41032219)
32. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, Brown PO: Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2004, 2:E7 (Pubitemid 39234559)
33. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M: Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008, 14:518-527 (Pubitemid 351655218)
34. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP: Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem 2001, 276:6727-6738 (Pubitemid 37373538)
35. Cat B, Stuhlmann D, Steinbrenner H, Alili L, Holtkotter O, Sies H, Brenneisen P: Enhancement of tumor invasion depends on transdifferentiation of skin fibroblasts mediated by reactive oxygen species. J Cell Sci 2006, 119:2727-2738 (Pubitemid 44184009)
36. Patocs A, Zhang L, Xu Y, Weber F, Caldes T, Mutter GL, Platzer P, Eng C: Breast-cancer stromal cells with TP53 mutations and nodal metastases. N Engl J Med 2007, 357:2543-2551 (Pubitemid 350294221)
37. Bist A, Fielding CJ, Fielding PE: p53 regulates caveolin gene transcription, cell cholesterol, and growth by a novel mechanism. Biochemistry 2000, 39:1966-1972 (Pubitemid 30124004)
38. Hasebe T, Tsuda H, Hirohashi S, Shimosato Y, Iwai M, Imoto S, Mukai K: Fibrotic focus in invasive ductal carcinoma: an indicator of high tumor aggressiveness. Jpn J Cancer Res 1996, 87:385-394 (Pubitemid 26000499)
39. Hasebe T, Tsuda H, Hirohashi S, Shimosato Y, Tsubono Y, Yamamoto H, Mukai K: Fibrotic focus in infiltrating ductal carcinoma of the breast: a significant histopathological prognostic parameter for predicting the long-term survival of the patients. Breast Cancer Res Treat 1998, 49:195-208 (Pubitemid 28416785)
40. Baak JP, Colpaert CG, van Diest PJ, Janssen E, van Diermen B, Albernaz E, Vermeulen PB, Van Marck EA: Multivariate prognostic evaluation of the mitotic activity index and fibrotic focus in node-negative invasive breast cancers. Eur J Cancer 2005, 41:2093-2101 (Pubitemid 41337951)
41. Colpaert C, Vermeulen P, Van Marck E, Dirix L: The presence of a fibrotic focus is an independent predictor of early metastasis in lymph node-negative breast cancer patients. Am J Surg Pathol 2001, 25:1557-1558 (Pubitemid 33096974)
42. Van den Eynden GG, Smid M, Van Laere SJ, Colpaert CG, Van der Auwera I, Bich TX, van Dam P, den Bakker MA, Dirix LY, Van Marck EA, Vermeulen PB, Foekens JA: Gene expression profiles associated with the presence of a fibrotic focus and the growth pattern in lymph node-negative breast cancer. Clin Cancer Res 2008, 14:2944-2952
43. Witkiewicz AK, Dasgupta A, Nguyen KH, Liu C, Kovatich AJ, Schwartz GF, Pestell RG, Sotgia F, Rui H, Lisanti MP: Stromal Caveolin-1 Levels Predict Early DCIS Progression to Invasive Breast Cancer, Cancer Biology & Therapy 2009, 8:65-73