Interstitial guidance of cancer invasion

Journal of Pathology

Volumn 226, Issue 2, 2012, Pages 185-199

  Gritsenko, Pavlo G ^a   Ilina, Olga ^a   Friedl, Peter ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

3D histology; breast cancer; CD44; collagen; glioma; guidance; integrins; invasion; tumour cell; tumour microenvironment

Indexed keywords

ALPHA DYSTROGLYCAN; ALPHA6BETA4 INTEGRIN; ALPHAVBETA5 INTEGRIN; BETA DYSTROGLYCAN; CELL SURFACE RECEPTOR; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; HERMES ANTIGEN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; KALININ; LAMININ; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE L1; SYNDECAN 1; SYNDECAN 2; SYNDECAN 3; SYNDECAN 4; TENASCIN; TISSUE SCAFFOLD; UVOMORULIN; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 5; VERY LATE ACTIVATION ANTIGEN 6; VITRONECTIN; VITRONECTIN RECEPTOR;

ADIPOSE TISSUE; ARACHNOID; ASTROCYTE; BASEMENT MEMBRANE; BRAIN; BRAIN BLOOD VESSEL; BRAIN CELL; BRAIN CORTEX; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER INVASION; CARCINOMA CELL; CELL INTERACTION; CELL STRUCTURE; EXTRACELLULAR MATRIX; FIBROBLAST; GLIA; GLIOMA; GLIOMA CELL; HUMAN; LYMPH VESSEL; MAMMARY GLAND; METASTASIS; MYELINATED NERVE; NERVE CELL; NERVE TRACT; NONHUMAN; PIA MATER; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STROMA CELL; SUBARACHNOID SPACE;

ADIPOSE TISSUE; ANTIGENS, CD44; BLOOD VESSELS; BRAIN NEOPLASMS; BREAST NEOPLASMS; CADHERINS; CARCINOMA, DUCTAL, BREAST; CELL ADHESION MOLECULES; CELL MOVEMENT; COLLAGEN; DYSTROGLYCANS; EXTRACELLULAR MATRIX; FEMALE; GLIOMA; HUMANS; IMMUNOGLOBULIN G; INTEGRINS; MAMMARY GLANDS, HUMAN; NEOPLASM INVASIVENESS; NERVE FIBERS, MYELINATED; RECEPTORS, CELL SURFACE; SYNDECANS;

EID: 81855199496     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.3031     Document Type: Review

References (179)

1. Langley RR, Fidler IJ,. The seed and soil hypothesis revisited-the role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 2011; 128: 2527-2535.
2. Ilina O, Friedl P,. Mechanisms of collective cell migration at a glance. J Cell Sci 2009; 122: 3203-3208.
3. Coleman RE,. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 2006; 12: 6243s-6249s. (Pubitemid 44703797)
4. Humphries JD, Byron A, Humphries MJ,. Integrin ligands at a glance. J Cell Sci 2006; 119: 3901-3903. (Pubitemid 44650863)
5. Schmidt S, Friedl P,. Interstitial cell migration: integrin-dependent and alternative adhesion mechanisms. Cell Tissue Res 2010; 339: 83-92.
6. Anthis NJ, Campbell ID,. The tail of integrin activation. Trends Biochem Sci 2011; 36: 191-198.
7. Robinson EE, Zazzali KM, Corbett SA, et al., Alpha5beta1 integrin mediates strong tissue cohesion. J Cell Sci 2003; 116: 377-386. (Pubitemid 36163878)
8. Morgan MR, Humphries MJ, Bass MD,. Synergistic control of cell adhesion by integrins and syndecans. Nature Rev Mol Cell Biol 2007; 8: 957-969. (Pubitemid 350174639)
9. Xian X, Gopal S, Couchman JR,. Syndecans as receptors and organizers of the extracellular matrix. Cell Tissue Res 2010; 339: 31-46.
10. Bozzi M, Morlacchi S, Bigotti MG, et al., Functional diversity of dystroglycan. Matrix Biol 2009; 28: 179-187.
11. Rougon G, Hobert O,. New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 2003; 26: 207-238. (Pubitemid 37064933)
12. Shapiro L, Weis WI,. Structure and biochemistry of cadherins and catenins. Cold Spring Harbor Perspect Biol 2009; 1: a003053.
13. Shapiro L, Love J, Colman DR,. Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci 2007; 30: 451-474. (Pubitemid 47218764)
14. Nollet F, Kools P, van Roy F,. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 2000; 299: 551-572.
15. Ponta H, Sherman L, Herrlich PA,. CD44: from adhesion molecules to signalling regulators. Nature Rev Mol Cell Biol 2003; 4: 33-45. (Pubitemid 36077255)
16. Naor D, Wallach-Dayan SB, Zahalka MA, et al., Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Semin Cancer Biol 2008; 18: 260-267.
17. Friedl P, Wolf K,. Plasticity of cell migration: a multiscale tuning model. J Cell Biol 2010; 188: 11-19.
18. Zhang ET, Inman CB, Weller RO,. Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 1990; 170: 111-123. (Pubitemid 20209323)
19. Krueger M, Bechmann I,. CNS pericytes: concepts, misconceptions, and a way out. Glia 2010; 58: 1-10.
20. Owens T, Bechmann I, Engelhardt B,. Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 2008; 67: 1113-1121.
21. Sykova E, Nicholson C,. Diffusion in brain extracellular space. Physiol Rev 2008; 88: 1277-1340.
22. Zimmermann DR, Dours-Zimmermann MT,. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 2008; 130: 635-653.
23. Itano N,. Simple primary structure, complex turnover regulation and multiple roles of hyaluronan. J Biochem 2008; 144: 131-137.
24. Joester A, Faissner A,. The structure and function of tenascins in the nervous system. Matrix Biol 2001; 20: 13-22. (Pubitemid 32178103)
25. Viapiano MS, Matthews RT,. From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology. Trends Mol Med 2006; 12: 488-496. (Pubitemid 44441998)
26. Yamaguchi Y,. Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 2000; 57: 276-289. (Pubitemid 30311415)
27. Mohan H, Krumbholz M, Sharma R, et al., Extracellular matrix in multiple sclerosis lesions: fibrillar collagens, biglycan and decorin are upregulated and associated with infiltrating immune cells. Brain Pathol 2010; 20: 966-975.
28. Reina MA, De Leon Casasola Ode L, Villanueva MC, et al., Ultrastructural findings in human spinal pia mater in relation to subarachnoid anesthesia. Anesth Analg 2004; 98: 1479-1485, table of contents. (Pubitemid 38525613)
29. Kalluri R,. Basement membranes: structure, assembly and role in tumour angiogenesis. Nature Rev Cancer 2003; 3: 422-433. (Pubitemid 37328846)
30. Khoshnoodi J, Pedchenko V, Hudson BG,. Mammalian collagen IV. Microsc Res Tech 2008; 71: 357-370. (Pubitemid 351620858)
31. Durbeej M,. Laminins. Cell Tissue Res 2010; 339: 259-268.
32. Canoll P, Goldman JE,. The interface between glial progenitors and gliomas. Acta Neuropathol 2008; 116: 465-477.
33. Riemenschneider MJ, Jeuken JW, Wesseling P, et al., Molecular diagnostics of gliomas: state of the art. Acta Neuropathol 2010; 120: 567-584.
34. Claes A, Idema AJ, Wesseling P,. Diffuse glioma growth: a guerilla war. Acta Neuropathol 2007; 114: 443-458. (Pubitemid 47521501)
35. Taylor LP,. Diagnosis, treatment, and prognosis of glioma: five new things. Neurology 2010; 75: S28-S32.
36. Giese A, Bjerkvig R, Berens ME, et al., Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 2003; 21: 1624-1636. (Pubitemid 46594118)
37. Giese A, Westphal M,. Glioma invasion in the central nervous system. Neurosurgery 1996; 39: 235-250; discussion 250-232.
38. Arita N, Taneda M, Hayakawa T,. Leptomeningeal dissemination of malignant gliomas. Incidence, diagnosis and outcome. Acta Neurochir (Wien) 1994; 126: 84-92. (Pubitemid 24068174)
39. Schweitzer T, Vince GH, Herbold C, et al., Extraneural metastases of primary brain tumors. J Neurooncol 2001; 53: 107-114.
40. Paulus W, Roggendorf W, Schuppan D,. Immunohistochemical investigation of collagen subtypes in human glioblastomas. Virchows Arch A Pathol Anat Histopathol 1988; 413: 325-332.
41. Farin A, Suzuki SO, Weiker M, et al., Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 2006; 53: 799-808.
42. Gingras MC, Roussel E, Bruner JM, et al., Comparison of cell adhesion molecule expression between glioblastoma multiforme and autologous normal brain tissue. J Neuroimmunol 1995; 57: 143-153.
43. Paulus W, Baur I, Schuppan D, et al., Characterization of integrin receptors in normal and neoplastic human brain. Am J Pathol 1993; 143: 154-163. (Pubitemid 24058169)
44. Watanabe A, Mabuchi T, Satoh E, et al., Expression of syndecans, a heparan sulfate proteoglycan, in malignant gliomas: participation of nuclear factor-kappaB in upregulation of syndecan-1 expression. J Neurooncol 2006; 77: 25-32. (Pubitemid 43870558)
45. Calogero A, Pavoni E, Gramaglia T, et al., Altered expression of alpha-dystroglycan subunit in human gliomas. Cancer Biol Ther 2006; 5: 441-448.
46. Kawataki T, Yamane T, Naganuma H, et al., Laminin isoforms and their integrin receptors in glioma cell migration and invasiveness: evidence for a role of alpha5-laminin(s) and alpha3beta1 integrin. Exp Cell Res 2007; 313: 3819-3831. (Pubitemid 47566379)
47. Jahn O, Tenzer S, Werner HB,. Myelin proteomics: molecular anatomy of an insulating sheath. Mol Neurobiol 2009; 40: 55-72.
48. Giger RJ, Venkatesh K, Chivatakarn O, et al., Mechanisms of CNS myelin inhibition: evidence for distinct and neuronal cell type specific receptor systems. Restor Neurol Neurosci 2008; 26: 97-115.
49. Buss A, Sellhaus B, Wolmsley A, et al., Expression pattern of NOGO-A protein in the human nervous system. Acta Neuropathol 2005; 110: 113-119. (Pubitemid 41245199)
50. Nakada M, Kita D, Futami K, et al., Roles of membrane type 1 matrix metalloproteinase and tissue inhibitor of metalloproteinases 2 in invasion and dissemination of human malignant glioma. J Neurosurg 2001; 94: 464-473. (Pubitemid 32786027)
51. Belien AT, Paganetti PA, Schwab ME,. Membrane-type 1 matrix metalloprotease (MT1-MMP) enables invasive migration of glioma cells in central nervous system white matter. J Cell Biol 1999; 144: 373-384. (Pubitemid 29066039)
52. Kuppner MC, Van Meir E, Gauthier T, et al., Differential expression of the CD44 molecule in human brain tumours. Int J Cancer 1992; 50: 572-577.
53. Brown MC, Staniszewska I, Lazarovici P, et al., Regulatory effect of nerve growth factor in alpha9beta1 integrin-dependent progression of glioblastoma. Neuro Oncol 2008; 10: 968-980.
54. Nakada M, Miyamori H, Kita D, et al., Human glioblastomas overexpress ADAMTS-5 that degrades brevican. Acta Neuropathol 2005; 110: 239-246. (Pubitemid 41430652)
55. Matthews RT, Gary SC, Zerillo C, et al., Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem 2000; 275: 22695-22703. (Pubitemid 30648860)
56. Friedl P, Wolf K, Lammerding J,. Nuclear mechanics during cell migration. Curr Opin Cell Biol 2011; 23: 55-64.
57. Beadle C, Assanah MC, Monzo P, et al., The role of myosin II in glioma invasion of the brain. Mol Biol Cell 2008; 19: 3357-3368.
58. Tom VJ, Doller CM, Malouf AT, et al., Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J Neurosci 2004; 24: 9282-9290. (Pubitemid 39426165)
59. Hirsch S, Bahr M,. Immunocytochemical characterization of reactive optic nerve astrocytes and meningeal cells. Glia 1999; 26: 36-46. (Pubitemid 29103166)
60. Gladson CL, Cheresh DA,. Glioblastoma expression of vitronectin and the alpha v beta 3 integrin. Adhesion mechanism for transformed glial cells. J Clin Invest 1991; 88: 1924-1932.
61. Naganuma H, Satoh E, Asahara T, et al., Quantification of thrombospondin-1 secretion and expression of alphavbeta3 and alpha3beta1 integrins and syndecan-1 as cell-surface receptors for thrombospondin-1 in malignant glioma cells. J Neurooncol 2004; 70: 309-317. (Pubitemid 40057959)
62. Fidler IJ,. The role of the organ microenvironment in brain metastasis. Semin Cancer Biol 2011; 21: 107-112.
63. Leenders WP, Kusters B, Verrijp K, et al., Antiangiogenic therapy of cerebral melanoma metastases results in sustained tumor progression via vessel co-option. Clin Cancer Res 2004; 10: 6222-6230. (Pubitemid 39287530)
64. Carbonell WS, Ansorge O, Sibson N, et al., The vascular basement membrane as 'soil' in brain metastasis. PLoS One 2009; 4: e5857.
65. Kienast Y, von Baumgarten L, Fuhrmann M, et al., Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 2010; 16: 116-122.
66. Maller O, Martinson H, Schedin P,. Extracellular matrix composition reveals complex and dynamic stromal-epithelial interactions in the mammary gland. J Mammary Gland Biol Neoplasia 2010; 15: 301-318.
67. Fata JE, Werb Z, Bissell MJ,. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 2004; 6: 1-11. (Pubitemid 38195555)
68. Exposito JY, Valcourt U, Cluzel C, et al., The fibrillar collagen family. Int J Mol Sci 2010; 11: 407-426.
69. Colige A, Ruggiero F, Vandenberghe I, et al., Domains and maturation processes that regulate the activity of ADAMTS-2, a metalloproteinase cleaving the aminopropeptide of fibrillar procollagens types I-III and V. J Biol Chem 2005; 280: 34397-34408. (Pubitemid 41504567)
70. Colige A, Vandenberghe I, Thiry M, et al., Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem 2002; 277: 5756-5766. (Pubitemid 34968353)
71. Colige A, Nuytinck L, Hausser I, et al., Novel types of mutation responsible for the dermatosparactic type of Ehlers-Danlos syndrome (type VIIC) and common polymorphisms in the ADAMTS2 gene. J Invest Dermatol 2004; 123: 656-663. (Pubitemid 39281605)
72. Kessler E, Takahara K, Biniaminov L, et al., Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 1996; 271: 360-362.
73. Fernandez M, Keyrilainen J, Serimaa R, et al., Small-angle x-ray scattering studies of human breast tissue samples. Phys Med Biol 2002; 47: 577-592. (Pubitemid 34232654)
74. Wolf K, Alexander S, Schacht V, et al., Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 2009; 20: 931-941.
75. Siegel RC,. Biosynthesis of collagen crosslinks: increased activity of purified lysyl oxidase with reconstituted collagen fibrils. Proc Natl Acad Sci U S A 1974; 71: 4826-4830.
76. Robins SP,. Biochemistry and functional significance of collagen cross-linking. Biochem Soc Trans 2007; 35: 849-852. (Pubitemid 350206380)
77. Sweeney SM, Orgel JP, Fertala A, et al., Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J Biol Chem 2008; 283: 21187-21197.
78. Birk DE,. Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 2001; 32: 223-237.
79. Singh P, Carraher C, Schwarzbauer JE,. Assembly of fibronectin extracellular matrix. Annu Rev Cell Dev Biol 2010; 26: 397-419.
80. Scott JE,. Proteoglycan: collagen interactions in connective tissues. Ultrastructural, biochemical, functional and evolutionary aspects. Int J Biol Macromol 1991; 13: 157-161.
81. Schonherr E, Witsch-Prehm P, Harrach B, et al., Interaction of biglycan with type I collagen. J Biol Chem 1995; 270: 2776-2783.
82. Schwarzbauer JE, DeSimone DW,. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harbor Perspect Biol 2011; 3: a005041.
83. Sasisekharan R, Shriver Z, Venkataraman G, et al., Roles of heparan-sulphate glycosaminoglycans in cancer. Nature Rev Cancer 2002; 2: 521-528. (Pubitemid 37328933)
84. Toole BP,. Hyaluronan: from extracellular glue to pericellular cue. Nature Rev Cancer 2004; 4: 528-539. (Pubitemid 38868622)
85. Wu YJ, La Pierre DP, Wu J, et al., The interaction of versican with its binding partners. Cell Res 2005; 15: 483-494. (Pubitemid 41653919)
86. Pierleoni C, Verdenelli F, Castellucci M, et al., Fibronectins and basal lamina molecules expression in human subcutaneous white adipose tissue. Eur J Histochem 1998; 42: 183-188. (Pubitemid 28548246)
87. Sbarbati A, Accorsi D, Benati D, et al., Subcutaneous adipose tissue classification. Eur J Histochem 2010; 54: e48.
88. Mariman EC, Wang P,. Adipocyte extracellular matrix composition, dynamics and role in obesity. Cell Mol Life Sci 2010; 67: 1277-1292.
89. Julien P, Despres JP, Angel A,. Scanning electron microscopy of very small fat cells and mature fat cells in human obesity. J Lipid Res 1989; 30: 293-299. (Pubitemid 19067234)
90. Glukhova M, Koteliansky V, Sastre X, et al., Adhesion systems in normal breast and in invasive breast carcinoma. Am J Pathol 1995; 146: 706-716.
91. Cowin P, Rowlands TM, Hatsell SJ,. Cadherins and catenins in breast cancer. Curr Opin Cell Biol 2005; 17: 499-508. (Pubitemid 41267164)
92. Yoder BJ, Wilkinson EJ, Massoll NA,. Molecular and morphologic distinctions between infiltrating ductal and lobular carcinoma of the breast. Breast J 2007; 13: 172-179. (Pubitemid 46280603)
93. Ewald AJ, Brenot A, Duong M, et al., Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 2008; 14: 570-581. (Pubitemid 351479940)
94. Jeschke U, Mylonas I, Kuhn C, et al., Expression of E-cadherin in human ductal breast cancer carcinoma in situ, invasive carcinomas, their lymph node metastases, their distant metastases, carcinomas with recurrence and in recurrence. Anticancer Res 2007; 27: 1969-1974. (Pubitemid 46954710)
95. Friedl P, Gilmour D,. Collective cell migration in morphogenesis, regeneration and cancer. Nature Rev Mol Cell Biol 2009; 10: 445-457.
96. Brennan K, Offiah G, McSherry EA, et al., Tight junctions: a barrier to the initiation and progression of breast cancer? J Biomed Biotechnol 2010; 2010: 460607.
97. Kowalski PJ, Rubin MA, Kleer CG,. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res 2003; 5: R217-R222.
98. Guelstein VI, Tchypysheva TA, Ermilova VD, et al., Myoepithelial and basement membrane antigens in benign and malignant human breast tumors. Int J Cancer 1993; 53: 269-277. (Pubitemid 23042878)
99. Egeblad M, Nakasone ES, Werb Z,. Tumors as organs: complex tissues that interface with the entire organism. Dev Cell 2010; 18: 884-901.
100. Shumate SD, El-Shenawee M,. Computational model of ductal carcinoma in situ: the effects of contact inhibition on pattern formation. IEEE Trans Biomed Eng 2009; 56: 1341-1347.
101. Koukoulis GK, Howeedy AA, Korhonen M, et al., Distribution of tenascin, cellular fibronectins and integrins in the normal, hyperplastic and neoplastic breast. J Submicrosc Cytol Pathol 1993; 25: 285-295.
102. Kadar A, Tokes AM, Kulka J, et al., Extracellular matrix components in breast carcinomas. Semin Cancer Biol 2002; 12: 243-257. (Pubitemid 34833067)
103. Egeblad M, Rasch MG, Weaver VM,. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 2010; 22: 697-706.
104. Lotz T, Simpson PD, Stocker D, et al., In vitro evaluation of surface based non-invasive breast cancer screening with digital image based Elasto tomography (DIET). Conf Proc IEEE Eng Med Biol Soc 2010; 2010: 3077-3080.
105. Levental KR, Yu H, Kass L, et al., Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009; 139: 891-906.
106. Kim BG, An HJ, Kang S, et al., Laminin-332-rich tumor microenvironment for tumor invasion in the interface zone of breast cancer. Am J Pathol 2011; 178: 373-381.
107. Verhoeven D, Bourgeois N, Buyssens N, et al., Ultrastructural demonstration of type IV collagen deposits in periductal elastosis in breast cancer. Pathol Res Pract 1993; 189: 144-149. (Pubitemid 23123619)
108. Ioachim E, Charchanti A, Briasoulis E, et al., Immunohistochemical expression of extracellular matrix components tenascin, fibronectin, collagen type IV and laminin in breast cancer: their prognostic value and role in tumour invasion and progression. Eur J Cancer 2002; 38: 2362-2370. (Pubitemid 35387487)
109. Aznavoorian S, Stracke ML, Krutzsch H, et al., Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells. J Cell Biol 1990; 110: 1427-1438.
110. Kischel P, Waltregny D, Dumont B, et al., Versican overexpression in human breast cancer lesions: known and new isoforms for stromal tumor targeting. Int J Cancer 2010; 126: 640-650.
111. Potapenko IO, Haakensen VD, Luders T, et al., Glycan gene expression signatures in normal and malignant breast tissue; possible role in diagnosis and progression. Mol Oncol 2010; 4: 98-118.
112. Herrera-Gayol A, Jothy S,. Adhesion proteins in the biology of breast cancer: contribution of CD44. Exp Mol Pathol 1999; 66: 149-156. (Pubitemid 29347503)
113. Auvinen P, Tammi R, Parkkinen J, et al., Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol 2000; 156: 529-536. (Pubitemid 30643808)
114. Afify A, McNiel MA, Braggin J, et al., Expression of CD44s, CD44v6, and hyaluronan across the spectrum of normal-hyperplasia-carcinoma in breast. Appl Immunohistochem Mol Morphol 2008; 16: 121-127.
115. Clezardin P, Frappart L, Clerget M, et al., Expression of thrombospondin (TSP1) and its receptors (CD36 and CD51) in normal, hyperplastic, and neoplastic human breast. Cancer Res 1993; 53: 1421-1430. (Pubitemid 23097127)
116. Guttery DS, Shaw JA, Lloyd K, et al., Expression of tenascin-C and its isoforms in the breast. Cancer Metastasis Rev 2010; 29: 595-606.
117. Hsiao YH, Lien HC, Hwa HL, et al., SPARC (osteonectin) in breast tumors of different histologic types and its role in the outcome of invasive ductal carcinoma. Breast J 2010; 16: 305-308.
118. Allan AL, George R, Vantyghem SA, et al., Role of the integrin-binding protein osteopontin in lymphatic metastasis of breast cancer. Am J Pathol 2006; 169: 233-246.
119. Zhang Y, Zhang G, Li J, et al., The expression analysis of periostin in human breast cancer. J Surg Res 2010; 160: 102-106.
120. Tuck AB, Arsenault DM, O'Malley FP, et al., Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelial cells. Oncogene 1999; 18: 4237-4246. (Pubitemid 29377854)
121. Senger DR, Perruzzi CA,. Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin. Biochim Biophys Acta 1996; 1314: 13-24. (Pubitemid 26395494)
122. Wang TN, Qian X, Granick MS, et al., Thrombospondin-1 (TSP-1) promotes the invasive properties of human breast cancer. J Surg Res 1996; 63: 39-43. (Pubitemid 26197174)
123. Kyutoku M, Taniyama Y, Katsuragi N, et al., Role of periostin in cancer progression and metastasis: inhibition of breast cancer progression and metastasis by anti-periostin antibody in a murine model. Int J Mol Med 2011; 28: 181-186.
124. Tuck AB, Chambers AF, Allan AL,. Osteopontin overexpression in breast cancer: knowledge gained and possible implications for clinical management. J Cell Biochem 2007; 102: 859-868. (Pubitemid 350036926)
125. Kii I, Nishiyama T, Li M, et al., Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J Biol Chem 2010; 285: 2028-2039.
126. Bristow J, Carey W, Egging D, et al., Tenascin-X, collagen, elastin, and the Ehlers-Danlos syndrome. Am J Med Genet C Semin Med Genet 2005; 139C: 24-30. (Pubitemid 41739244)
127. Conklin MW, Eickhoff JC, Riching KM, et al., Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am J Pathol 2011; 178: 1221-1232.
128. Goetz JG, Minguet S, Navarro-Lerida I, et al., Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011; 146: 148-163.
129. Wolf K, Wu YI, Liu Y, et al., Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biol 2007; 9: 893-904. (Pubitemid 47190444)
130. Alexander S, Koehl GE, Hirschberg M, et al., Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem Cell Biol 2008; 130: 1147-1154.
131. Condeelis J, Segall JE,. Intravital imaging of cell movement in tumours. Nature Rev Cancer 2003; 3: 921-930. (Pubitemid 37500177)
132. Ilina O, Bakker GJ, Vasaturo A, et al., Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion. Phys Biol 2011; 8: 015010.
133. Yamaguchi J, Ohtani H, Nakamura K, et al., Prognostic impact of marginal adipose tissue invasion in ductal carcinoma of the breast. Am J Clin Pathol 2008; 130: 382-388.
134. Fiedler S, Bravin A, Keyrilainen J, et al., Imaging lobular breast carcinoma: comparison of synchrotron radiation DEI-CT technique with clinical CT, mammography and histology. Phys Med Biol 2004; 49: 175-188. (Pubitemid 38139425)
135. Bon G, Folgiero V, Di Carlo S, et al., Involvement of alpha6beta4 integrin in the mechanisms that regulate breast cancer progression. Breast Cancer Res 2007; 9: 203.
136. Morini M, Mottolese M, Ferrari N, et al., The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer 2000; 87: 336-342. (Pubitemid 30451643)
137. Park CC, Zhang H, Pallavicini M, et al., Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 2006; 66: 1526-1535. (Pubitemid 43259934)
138. Tuck AB, Elliott BE, Hota C, et al., Osteopontin-induced, integrin-dependent migration of human mammary epithelial cells involves activation of the hepatocyte growth factor receptor (Met). J Cell Biochem 2000; 78: 465-475. (Pubitemid 30491074)
139. Felding-Habermann B, O'Toole TE, Smith JW, et al., Integrin activation controls metastasis in human breast cancer. Proc Natl Acad Sci U S A 2001; 98: 1853-1858. (Pubitemid 32165587)
140. Murphy-Ullrich JE,. The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest 2001; 107: 785-790. (Pubitemid 32274027)
141. Sloan EK, Pouliot N, Stanley KL, et al., Tumor-specific expression of alphavbeta3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res 2006; 8: R20.
142. Subbaram S, Dipersio CM,. Integrin alpha3beta1 as a breast cancer target. Expert Opin Ther Targets 2011; 15: 1197-1210.
143. Klinowska TC, Alexander CM, Georges-Labouesse E, et al., Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 2001; 233: 449-467. (Pubitemid 32467688)
144. Chen J, Diacovo TG, Grenache DG, et al., The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol 2002; 161: 337-344. (Pubitemid 34760799)
145. Li N, Zhang Y, Naylor MJ, et al., Beta1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO J 2005; 24: 1942-1953. (Pubitemid 40896166)
146. Baluk P, Morikawa S, Haskell A, et al., Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol 2003; 163: 1801-1815. (Pubitemid 37310012)
147. Arnaout-Alkarain A, Kahn HJ, Narod SA, et al., Significance of lymph vessel invasion identified by the endothelial lymphatic marker D2-40 in node negative breast cancer. Mod Pathol 2007; 20: 183-191. (Pubitemid 46422172)
148. Van den Eynden GG, Van der Auwera I, Van Laere SJ, et al., Distinguishing blood and lymph vessel invasion in breast cancer: a prospective immunohistochemical study. Br J Cancer 2006; 94: 1643-1649. (Pubitemid 43924927)
149. Dai J, Li B, Shi J, et al., A humanized anti-osteopontin antibody inhibits breast cancer growth and metastasis in vivo. Cancer Immunol Immunother 2010; 59: 355-366.
150. McAllister SS, Gifford AM, Greiner AL, et al., Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008; 133: 994-1005. (Pubitemid 351787747)
151. Lammermann T, Bader BL, Monkley SJ, et al., Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008; 453: 51-55. (Pubitemid 351630331)
152. Mechtersheimer G, Munk M, Barth T, et al., Expression of beta 1 integrins in non-neoplastic mammary epithelium, fibroadenoma and carcinoma of the breast. Virchows Arch A Pathol Anat Histopathol 1993; 422: 203-210. (Pubitemid 23131501)
153. Zutter MM, Mazoujian G, Santoro SA,. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am J Pathol 1990; 137: 863-870. (Pubitemid 20337801)
154. Pignatelli M, Cardillo MR, Hanby A, et al., Integrins and their accessory adhesion molecules in mammary carcinomas: loss of polarization in poorly differentiated tumors. Hum Pathol 1992; 23: 1159-1166.
155. Jones JL, Critchley DR, Walker RA,. Alteration of stromal protein and integrin expression in breast-a marker of premalignant change? J Pathol 1992; 167: 399-406.
156. Gould VE, Koukoulis GK, Virtanen I,. Extracellular matrix proteins and their receptors in the normal, hyperplastic and neoplastic breast. Cell Differ Dev 1990; 32: 409-416.
157. D'Ardenne AJ, Richman PI, Horton MA, et al., Co-ordinate expression of the alpha-6 integrin laminin receptor sub-unit and laminin in breast cancer. J Pathol 1991; 165: 213-220.
158. Previtali S, Quattrini A, Nemni R, et al., Alpha6 beta4 and alpha6 beta1 integrins in astrocytomas and other CNS tumors. J Neuropathol Exp Neurol 1996; 55: 456-465. (Pubitemid 26112099)
159. Allen MD, Vaziri R, Green M, et al., Clinical and functional significance of alpha9beta1 integrin expression in breast cancer: a novel cell-surface marker of the basal phenotype that promotes tumour cell invasion. J Pathol 2011; 223: 646-658.
160. Zutter MM, Krigman HR, Santoro SA,. Altered integrin expression in adenocarcinoma of the breast. Analysis by in situ hybridization. Am J Pathol 1993; 142: 1439-1448. (Pubitemid 24058131)
161. Bello L, Francolini M, Marthyn P, et al., Alpha(v)beta3 and alpha(v)beta5 integrin expression in glioma periphery. Neurosurgery 2001; 49: 380-389; discussion 390.
162. Lendorf ME, Manon-Jensen T, Kronqvist P, et al., Syndecan-1 and syndecan-4 are independent indicators in breast carcinoma. J Histochem Cytochem 2011; 59: 615-629.
163. Henry MD, Cohen MB, Campbell KP,. Reduced expression of dystroglycan in breast and prostate cancer. Hum Pathol 2001; 32: 791-795. (Pubitemid 32803978)
164. Cross SS, Lippitt J, Mitchell A, et al., Expression of beta-dystroglycan is reduced or absent in many human carcinomas. Histopathology 2008; 53: 561-566.
165. Auvinen P, Tammi R, Tammi M, et al., Expression of CD 44 s, CD 44 v 3 and CD 44 v 6 in benign and malignant breast lesions: correlation and colocalization with hyaluronan. Histopathology 2005; 47: 420-428. (Pubitemid 41428491)
166. Gotte M, Yip GW,. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res 2006; 66: 10233-10237. (Pubitemid 44799736)
167. Burim RV, Teixeira SA, Colli BO, et al., ICAM-1 (Lys469Glu) and PECAM-1 (Leu125Val) polymorphisms in diffuse astrocytomas. Clin Exp Med 2009; 9: 157-163.
168. Schroder C, Witzel I, Muller V, et al., Prognostic value of intercellular adhesion molecule (ICAM)-1 expression in breast cancer. J Cancer Res Clin Oncol 2011; 137: 1193-1201.
169. Duenisch P, Reichart R, Mueller U, et al., Neural cell adhesion molecule isoform 140 declines with rise of WHO grade in human gliomas and serves as indicator for the invasion zone of multiform glioblastomas and brain metastases. J Cancer Res Clin Oncol 2011; 137: 399-414.
170. Todaro L, Christiansen S, Varela M, et al., Alteration of serum and tumoral neural cell adhesion molecule (NCAM) isoforms in patients with brain tumors. J Neurooncol 2007; 83: 135-144. (Pubitemid 46784986)
171. Yamamoto J, Ohshima K, Nabeshima K, et al., Comparative study of primary mammary small cell carcinoma, carcinoma with endocrine features and invasive ductal carcinoma. Oncol Rep 2004; 11: 825-831.
172. Tsuzuki T, Izumoto S, Ohnishi T, et al., Neural cell adhesion molecule L1 in gliomas: correlation with TGF-beta and p53. J Clin Pathol 1998; 51: 13-17. (Pubitemid 28122578)
173. Izumoto S, Ohnishi T, Arita N, et al., Gene expression of neural cell adhesion molecule L1 in malignant gliomas and biological significance of L1 in glioma invasion. Cancer Res 1996; 56: 1440-1444. (Pubitemid 26080991)
174. Yang M, Adla S, Temburni MK, et al., Stimulation of glioma cell motility by expression, proteolysis, and release of the L1 neural cell recognition molecule. Cancer Cell Int 2009; 9: 27.
175. Schroder C, Schumacher U, Fogel M, et al., Expression and prognostic value of L1-CAM in breast cancer. Oncol Rep 2009; 22: 1109-1117.
176. Asano K, Kubo O, Tajika Y, et al., Expression and role of cadherins in astrocytic tumors. Brain Tumor Pathol 1997; 14: 27-33.
177. Utsuki S, Sato Y, Oka H, et al., Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J Neurooncol 2002; 57: 187-192. (Pubitemid 34692627)
178. Bassarova AV, Torlakovic E, Sedloev T, et al., Simultaneous bilateral breast carcinoma: histopathological characteristics and CD44/catenin-cadherin profile. Histol Histopathol 2005; 20: 791-799. (Pubitemid 40932597)
179. Prasad CP, Rath G, Mathur S, et al., Expression analysis of E-cadherin, Slug and GSK3beta in invasive ductal carcinoma of breast. BMC Cancer 2009; 9: 325.