Aligned collagen is a prognostic signature for survival in human breast carcinoma

American Journal of Pathology

Volumn 178, Issue 3, 2011, Pages 1221-1232

  Conklin, Matthew W ^a   Eickhoff, Jens C ^b   Riching, Kristin M ^a   Pehlke, Carolyn A ^a   Eliceiri, Kevin W ^a   Provenzano, Paolo P ^a,d   Friedl, Andreas ^b,c   Keely, Patricia J ^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   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; PROTEIN TACS 3; SYNDECAN 1; UNCLASSIFIED DRUG;

ARTICLE; BREAST CARCINOMA; CANCER SURVIVAL; DISEASE FREE SURVIVAL; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DETERMINATION; SURVIVAL RATE; TUMOR VOLUME;

EID: 79952747743     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.076     Document Type: Article

References (75)

1. Provenzano PP, Eliceiri KW, Keely PJ: Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment. Clin Exp Metastasis 2009, 26: 357-370
2. Yan L, Rueden CT, White JG, Eliceiri KW: Applications of combined spectral lifetime microscopy for biology. Biotechniques 2006, 41: 249-251
3. Skala MC, Squirrell JM, Vrotsos KM, Eickhoff JC, Gendron-Fitzpatrick A, Eliceiri KW, Ramanujam N: Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues. Cancer Res 2005, 65:1180-1186 (Pubitemid 40270142)
4. Conklin MW, Provenzano PP, Eliceiri KW, Sullivan R, Keely PJ: Fluorescence lifetime imaging of endogenous fluorophores in histopathology sections reveals differences between normal and tumor epithelium in carcinoma in situ of the breast. Cell Biochem Biophys 2009, 53:145-157
5. Boyd NF, Dite GS, Stone J, Gunasekara A, English DR, McCredie MR, Giles GG, Tritchler D, Chiarelli A, Yaffe MJ, Hopper JL: Heritability of mammographic density, a risk factor for breast cancer. N Engl J Med 2002, 347:886-894
6. Alowami S, Troup S, Al-Haddad S, Kirkpatrick I, Watson PH: Mammographic density is related to stroma and stromal proteoglycan expression. Breast Cancer Res 2003, 5:R129-R135
7. Arendt LM, Rudnick JA, Keller PJ, Kuperwasser C: Stroma in breast development and disease. Semin Cell Dev Biol 2010, 21:11-18
8. Tamimi SO, Ahmed A: Stromal changes in invasive breast carcinoma: an ultrastructural study. J Pathol 1987, 153:163-170 (Pubitemid 17153990)
9. Sahai E, Wyckoff J, Philippar U, Segall J, Gertler F, Condeelis J: Simultaneous imaging of GFP. CFP and collagen in tumors in vivo using multiphoton microscopy. BMC Biotech 2005, 5:14
10. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ, Stanley ER, Segall JE, Condeelis JS: Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/ epidermal growth factor paracrine loop. Cancer Res 2005, 65:5278-5283 (Pubitemid 40827339)
11. Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker E-B, Friedl P: Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 2003, 160:267-277 (Pubitemid 36254960)
12. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ: Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 2006, 4:38
13. Friedl P, Wolf K: Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003, 3:362-374 (Pubitemid 37328856)
14. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J, Condeelis J: A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 2004, 64:7022-7029 (Pubitemid 39331012)
15. Condeelis J, Pollard JW: Macrophages: obligate partners for tumor cell migration. Invasion and metastasis. Cell 2006, 124:263-266 (Pubitemid 43121975)
16. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG, Keely PJ: Collagen density promotes mammary tumor initiation and progression. BMC Med 2008, 6:11
17. Maglione JE, Moghanaki D, Young LJ, Manner CK, Ellies LG, Joseph SO, Nicholson B, Cardiff RD, MacLeod CL: Transgenic polyoma middle-T mice model premalignant mammary disease. Cancer Res 2001, 61:8298-8305 (Pubitemid 33091625)
18. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW: Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003, 163:2113-2126 (Pubitemid 37310040)
19. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG, Keely PJ: Collagen density promotes mammary tumor initiation and progression. BMC Med 2008, 6:11
20. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, Segall JE, Pollard JW, Condeelis J: Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 2007, 67: 2649-2656 (Pubitemid 46548952)
21. Wang W, Wyckoff JB, Frohlich VC, Oleynikov Y, Huttelmaier S, Zavadil J, Cermak L, Bottinger EP, Singer RH, White JG, Segall JE, Condeelis JS: Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 2002, 62:6278-6288 (Pubitemid 35244482)
22. Provenzano PP, Inman DR, Eliceiri KW, Trier SM, Keely PJ: Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 2008, 95: 5374-5384
23. Campagnola PJ, Loew LM: Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nature Biotechnol 2003, 21:1356-1360 (Pubitemid 37356622)
24. Raub CB, Unruh J, Suresh V, Krasieva T, Lindmo T, Gratton E, Tromberg BJ, George SC: Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties. Biophys J 2008, 94:2361-2373
25. Reiser KM, Bratton C, Yankelevich DR, Knoesen A, Rocha-Mendoza I, Lotz J: Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis. J Biomed Opt 2007, 12:064019
26. Erikson A, Ortegren J, Hompland T, de Lange Davies C, Lindgren M: Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope. J Biomed Opt 2007, 12:044002
27. Kirkpatrick ND, Brewer MA, Utzinger U: Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy. Cancer Epidemiol Biomarkers Prev 2007, 16:2048-2057 (Pubitemid 47621179)
28. Schenke-Layland K, Stock UA, Nsair R, Xie J, Angelis E, Fonseca CG, Larbig CG, Mahajan A, Shivkumar K, Fishbein MC, Maclellan WR: Cardiomyopathy is associated with structural remodelling of heart valve extracellular matrix. Eur Heart J 2009, 30:2254-2265
29. Lacomb R, Nadiarnykh O, Campagnola PJ: Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation. Biophys J 2008, 94:4504-4514
30. Hompland T, Erikson A, Lindgren M, Lindmo T, de Lange Davies C: Second-harmonic generation in collagen as a potential cancer diagnostic parameter. J Biomed Opt 2008, 13:054050
31. Wolberg WH, Street WN: Computer-generated nuclear features compared with axillary lymph node status and tumor size as indicators of breast cancer survival. Hum Pathol 2002, 33:1086-1091 (Pubitemid 35416705)
32. Dalton LW, Pinder SE, Elston CE, Ellis IO, Page DL, Dupont WD, Blamey RW: Histologic grading of breast cancer: linkage of patient outcome with level of pathologist agreement. Mod Pathol 2000, 13: 730-735 (Pubitemid 30470161)
33. Baba F, Swartz K, van Buren R, Eickhoff J, Zhang Y, Wolberg W, Friedl A: Syndecan-1 and syndecan-4 are overexpressed in an estrogen receptor-negative, highly proliferative breast carcinoma subtype. Breast Cancer Res Treat 2006, 98:91-98 (Pubitemid 44050783)
34. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A: Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008, 108:389-397 (Pubitemid 351431077)
35. Bird DK, Eliceiri KW, Fan CH, White JG: Simultaneous two-photon spectral and lifetime fluorescence microscopy. Appl Opt 2004, 43: 5173-5182
36. Breiman L, Friedman J, Stone CJ, Olshen RA: Classification and Regression Trees. Belmont, Wadsworth International Group, 1984, pp 358
37. Gordon L, Olshen RA: Tree-structured survival analysis. Cancer Treat Rep 1985, 69:1065-1069
38. Hothorn T, Buhlmann P, Dudoit S, Molinaro A, van der Laan MJ: Survival ensembles. Biostatistics 2006, 7:355-373 (Pubitemid 43955046)
39. Brown E, McKee T, diTomaso E, Pluen A, Seed B, Boucher Y, Jain RK: Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 2003, 9:796-800 (Pubitemid 36749232)
40. Williams RM, Zipfel WR, Webb WW: Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 2005, 88:1377-1386 (Pubitemid 40975965)
41. Stoller P, Reiser KM, Celliers PM, Rubenchik AM: Polarization-modulated second harmonic generation in collagen. Biophys J 2002, 82: 3330-3342 (Pubitemid 34547675)
42. Stoller P, Celliers PM, Reiser KM, Rubenchik AM: Quantitative second- harmonic generation microscopy in collagen. Appl Opt 2003, 42:5209-5219
43. Conklin MW, Provenzano PP, Eliceiri KW, Sullivan R, Keely PJ: Fluorescence lifetime imaging of endogenous fluorophores in histopathology sections reveals differences between normal and tumor epithelium in carcinoma in situ of the breast. Cell Biochem Biophys 2009, 53:145-157
44. Provenzano PP, Eliceiri KW, Keely PJ: Shining new light on 3D cell motility and the metastatic process. Trends Cell Biol 2009, 19:638-648
45. Zipfel WR, Williams RM, Christie R, Nikitin AY, Hyman BT, Webb WW: Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci USA: 2003, 100:7075-7080 (Pubitemid 36706395)
46. Skala MC, Riching KM, Gendron-Fitzpatrick A, Eickhoff J, Eliceiri KW, White JG, Ramanujam N: In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc Natl Acad Sci U S A: 2007, 104:19494-19499
47. Nadiarnykh O, LaComb RB, Brewer MA, Campagnola PJ: Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy. BMC Cancer 2010, 10:94
48. McCormack VA, dos Santos Silva I: Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2006, 15:1159-1169
49. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK: Pathology: cancer cells compress intratumour vessels. Nature 2004, 427:695 (Pubitemid 38294577)
50. Park CC, Rembert J, Chew K, Moore D, Kerlikowske K: High mammographic breast density is independent predictor of local but not distant recurrence after lumpectomy and radiotherapy for invasive breast cancer. Int J Radiat Oncol Biol Phys 2009, 73:75-79
51. Provenzano PP, Inman DR, Eliceiri KW, Trier SM, Keely PJ: Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 2008, 95:5374-5384
52. Wang W, Wyckoff JB, Goswami S, Wang Y, Sidani M, Segall JE, Condeelis JS: Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. Cancer Res 2007, 67:3505-3511 (Pubitemid 46762128)
53. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ: ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 2003, 163:583-595 (Pubitemid 37429871)
54. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM: Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254 (Pubitemid 41317594)
55. Boyd NF, Lockwood GA, Byng JW, Tritchler DL, Yaffe MJ: Mammographic densities and breast cancer risk. Cancer Epidemiol Biomarkers Prev 1998, 7:1133-1144 (Pubitemid 29001671)
56. Leek RD, Harris AL: Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia 2002, 7:177-189 (Pubitemid 38420774)
57. Ingman WV, Wyckoff J, Gouon-Evans V, Condeelis J, Pollard JW: Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev Dyn 2006, 235:3222-3229 (Pubitemid 44888188)
58. Walker R: The complexities of breast cancer desmoplasia. Breast Cancer Res 2001, 3:143-145
59. Maeda T, Desouky J, Friedl A: Syndecan-1 expression by stromal fibroblasts promotes breast carcinoma growth in vivo and stimulates tumor angiogenesis. Oncogene 2006, 25:1408-1412 (Pubitemid 43336469)
60. Shao ZM, Nguyen M, Barsky SH: Human breast carcinoma desmoplasia is PDGF initiated. Oncogene 2000, 19:4337-4345
61. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H: Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 1998, 141:1277-1286 (Pubitemid 28265620)
62. 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)
63. Wiseman BS, Werb Z: Stromal effects on mammary gland development and breast cancer. Science 2002, 296:1046-1049 (Pubitemid 34517108)
64. McDermott SP, Ranheim EA, Leatherberry VS, Khwaja SS, Klos KS, Alexander CM: Juvenile syndecan-1 null mice are protected from carcinogen- induced tumor development. Oncogene 2007, 26:1407-1416 (Pubitemid 46340817)
65. Slavik MA, Allen-Hoffmann BL, Liu BY, Alexander CM: Wnt signaling induces differentiation of progenitor cells in organotypic keratinocyte cultures. BMC Dev Biol 2007, 7:9
66. Yang N, Mosher R, Seo S, Beebe D, Friedl A: Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. Am J Pathol 2011, 178:325-335
67. Pollard JW: Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol 2008, 84:623-630
68. Bingle L, Brown NJ, Lewis CE: The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002, 196:254-265 (Pubitemid 34189413)
69. Sabeh F, Shimizu-Hirota R, Weiss SJ: Protease-dependent versus independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 2009, 185:11-19
70. McDaniel SM, Rumer KK, Biroc SL, Metz RP, Singh M, Porter W, Schedin P: Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathol 2006, 168:608-620 (Pubitemid 43271158)
71. Ginsburg OM, Martin LJ, Boyd NF: Mammographic density, lobular involution, and risk of breast cancer. Br J Cancer 2008, 99:1369-1374
72. Martin LJ, Boyd NF: Mammographic density. Potential mechanisms of breast cancer risk associated with mammographic density: hypotheses based on epidemiological evidence. Breast Cancer Res 2008, 10:201
73. Schedin P: Pregnancy-associated breast cancer and metastasis. Nat Rev Cancer 2006, 6:281-291
74. O'Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, Man YG, Borges V, Schedin P: Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol 2010, 176:1241-1255
75. O'Brien J, Schedin P: Macrophages in breast cancer: do involution macrophages account for the poor prognosis of pregnancy-associated breast cancer? J Mammary Gland Biol Neoplasia 2009, 14:145-157