Differential proteomic analysis of a human breast tumor and its matched bone metastasis identifies cell membrane and extracellular proteins associated with bone metastasis
Differential proteomic analysis of a human breast tumor and its matched bone metastasis identifies cell membrane and extracellular proteins associated with bone metastasis.pdf
bone metastasis; breast cancer; proteomics; matched; primary tumor
Abstract :
[en] The classical fate of metastasizing breast cancer cells is to seed and form secondary colonies in bones. The molecules closely associated with these processes are predominantly present at the cell surface and in the extracellular space, establishing the first contacts with the target tissue. In this study, we had the rare opportunity to analyze a bone metastatic lesion and its corresponding breast primary tumor obtained simultaneously from the same patient. Using mass spectrometry, we undertook a proteomic study on cell surface and extracellular protein-enriched material. We provide a repertoire of significantly modulated proteins, some with yet unknown roles in the bone metastatic process as well as proteins notably involved in cancer cell invasiveness and in bone metabolism. The comparison of these clinical data with those previously obtained using a human osteotropic breast cancer cell line highlighted an overlapping group of proteins. Certain differentially expressed proteins are validated in the present study using immunohistochemistry on a retrospective collection of breast tumors and matched bone metastases. Our exclusive set of selected proteins supports the set-up of further investigations on both clinical samples and experimental bone metastasis models that will help to reveal the finely coordinated expression of proteins that favor the development of metastases in the bone microenvironment.
Dumont, Bruno ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Labo de recherche sur les métastases
Castronovo, Vincenzo ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie générale et cellulaire
Peulen, Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
BLETARD, Noëlla ; Centre Hospitalier Universitaire de Liège - CHU > Anatomie pathologique
Clézardin, Philippe
Delvenne, Philippe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Turtoi, Andrei ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Labo de recherche sur les métastases
Bellahcene, Akeila ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Labo de recherche sur les métastases
Language :
English
Title :
Differential proteomic analysis of a human breast tumor and its matched bone metastasis identifies cell membrane and extracellular proteins associated with bone metastasis
Publication date :
February 2012
Journal title :
Journal of Proteome Research
ISSN :
1535-3893
eISSN :
1535-3907
Publisher :
American Chemical Society, Washington, United States - District of Columbia
Greenlee, R. T.; Hill-Harmon, M. B.; Murray, T.; Thun, M. Cancer statistics, 2001 CA Cancer J. Clin. 2001, 51 (1) 15-36
Fournier, P. G.; Stresing, V.; Ebetino, F. H.; Clezardin, P. How do bisphosphonates inhibit bone metastasis in vivo? Neoplasia 2010, 12 (7) 571-8
Chambers, A. F.; Groom, A. C.; MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites Nat. Rev. Cancer 2002, 2 (8) 563-72
Coleman, R. E.; Guise, T. A.; Lipton, A.; Roodman, G. D.; Berenson, J. R.; Body, J. J.; Boyce, B. F.; Calvi, L. M.; Hadji, P.; McCloskey, E. V.; Saad, F.; Smith, M. R.; Suva, L. J.; Taichman, R. S.; Vessella, R. L.; Weilbaecher, K. N. Advancing treatment for metastatic bone cancer: consensus recommendations from the Second Cambridge Conference Clin. Cancer Res. 2008, 14 (20) 6387-95
Bhattacharyya, S.; Byrum, S.; Siegel, E. R.; Suva, L. J. Proteomic analysis of bone cancer: a review of current and future developments Expert Rev. Proteomics 2007, 4 (3) 371-8
Kang, Y.; Siegel, P. M.; Shu, W.; Drobnjak, M.; Kakonen, S. M.; Cordon-Cardo, C.; Guise, T. A.; Massague, J. A multigenic program mediating breast cancer metastasis to bone Cancer Cell 2003, 3 (6) 537-49
Suzuki, M.; Tarin, D. Gene expression profiling of human lymph node metastases and matched primary breast carcinomas: clinical implications Mol. Oncol. 2007, 1 (2) 172-80
Aguirre-Ghiso, J. A. Models, mechanisms and clinical evidence for cancer dormancy Nat. Rev. Cancer 2007, 7 (11) 834-46
Li, J.; Gromov, P.; Gromova, I.; Moreira, J. M.; Timmermans-Wielenga, V.; Rank, F.; Wang, K.; Li, S.; Li, H.; Wiuf, C.; Yang, H.; Zhang, X.; Bolund, L.; Celis, J. E. Omics-based profiling of carcinoma of the breast and matched regional lymph node metastasis Proteomics 2008, 8 (23-24) 5038-52
Thongwatchara, P.; Promwikorn, W.; Srisomsap, C.; Chokchaichamnankit, D.; Boonyaphiphat, P.; Thongsuksai, P. Differential protein expression in primary breast cancer and matched axillary node metastasis Oncol. Rep. 2011, 26 (1) 185-91
Ho, J.; Kong, J. W.; Choong, L. Y.; Loh, M. C.; Toy, W.; Chong, P. K.; Wong, C. H.; Wong, C. Y.; Shah, N.; Lim, Y. P. Novel breast cancer metastasis-associated proteins J. Proteome Res. 2009, 8 (2) 583-94
Chen, H.; Pimienta, G.; Gu, Y.; Sun, X.; Hu, J.; Kim, M. S.; Chaerkady, R.; Gucek, M.; Cole, R. N.; Sukumar, S.; Pandey, A. Proteomic characterization of Her2/neu-overexpressing breast cancer cells Proteomics 2010, 10 (21) 3800-10
Bellahcene, A.; Bachelier, R.; Detry, C.; Lidereau, R.; Clezardin, P.; Castronovo, V. Transcriptome analysis reveals an osteoblast-like phenotype for human osteotropic breast cancer cells Breast Cancer Res. Treat. 2007, 101 (2) 135-48
Kischel, P.; Guillonneau, F.; Dumont, B.; Bellahcene, A.; Stresing, V.; Clezardin, P.; De Pauw, E. A.; Castronovo, V. Cell membrane proteomic analysis identifies proteins differentially expressed in osteotropic human breast cancer cells Neoplasia 2008, 10 (9) 1014-20
Turtoi, A.; Dumont, B.; Greffe, Y.; Blomme, A.; Mazzucchelli, G.; Delvenne, P.; Mutijima, E. N.; Lifrange, E.; De Pauw, E.; Castronovo, V. Novel Comprehensive Approach for Accessible Biomarker Identification and Absolute Quantification from Precious Human Tissues J. Proteome Res. 2011, 10 (7) 3160-3182
Segal, E.; Friedman, N.; Koller, D.; Regev, A. A module map showing conditional activity of expression modules in cancer Nat. Genet. 2004, 36 (10) 1090-8
Koeneman, K. S.; Yeung, F.; Chung, L. W. Osteomimetic properties of prostate cancer cells: a hypothesis supporting the predilection of prostate cancer metastasis and growth in the bone environment Prostate 1999, 39 (4) 246-61
Castronovo, V.; Kischel, P.; Guillonneau, F.; de Leval, L.; Defechereux, T.; De Pauw, E.; Neri, D.; Waltregny, D. Identification of specific reachable molecular targets in human breast cancer using a versatile ex vivo proteomic method Proteomics 2007, 7 (8) 1188-96
Scheurer, S. B.; Roesli, C.; Neri, D.; Elia, G. A comparison of different biotinylation reagents, tryptic digestion procedures, and mass spectrometric techniques for 2-D peptide mapping of membrane proteins Proteomics 2005, 5 (12) 3035-9
Nesvizhskii, A. I.; Aebersold, R. Interpretation of shotgun proteomic data: the protein inference problem Mol. Cell. Proteomics 2005, 4 (10) 1419-40
Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20 (18) 3551-67
Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein Mol. Cell. Proteomics 2005, 4 (9) 1265-72
Peyruchaud, O.; Winding, B.; Pecheur, I.; Serre, C. M.; Delmas, P.; Clezardin, P. Early detection of bone metastases in a murine model using fluorescent human breast cancer cells: application to the use of the bisphosphonate zoledronic acid in the treatment of osteolytic lesions J. Bone Miner. Res. 2001, 16 (11) 2027-34
Weigelt, B.; Glas, A. M.; Wessels, L. F.; Witteveen, A. T.; Peterse, J. L.; vant Veer, L. J. Gene expression profiles of primary breast tumors maintained in distant metastases Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (26) 15901-5
Ramaswamy, S.; Ross, K. N.; Lander, E. S.; Golub, T. R. A molecular signature of metastasis in primary solid tumors Nature genetics 2003, 33 (1) 49-54
van de Vijver, M. J.; He, Y. D.; vant Veer, L. J.; Dai, H.; Hart, A. A.; Voskuil, D. W.; Schreiber, G. J.; Peterse, J. L.; Roberts, C.; Marton, M. J.; Parrish, M.; Atsma, D.; Witteveen, A.; Glas, A.; Delahaye, L.; van der Velde, T.; Bartelink, H.; Rodenhuis, S.; Rutgers, E. T.; Friend, S. H.; Bernards, R. A gene-expression signature as a predictor of survival in breast cancer N. Engl. J. Med. 2002, 347 (25) 1999-2009
Klein, A.; Olendrowitz, C.; Schmutzler, R.; Hampl, J.; Schlag, P. M.; Maass, N.; Arnold, N.; Wessel, R.; Ramser, J.; Meindl, A.; Scherneck, S.; Seitz, S. Identification of brain- and bone-specific breast cancer metastasis genes Cancer Lett. 2009, 276 (2) 212-20
Brack, S. S.; Silacci, M.; Birchler, M.; Neri, D. Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C Clin. Cancer Res. 2006, 12 (10) 3200-8
Sauer, S.; Erba, P. A.; Petrini, M.; Menrad, A.; Giovannoni, L.; Grana, C.; Hirsch, B.; Zardi, L.; Paganelli, G.; Mariani, G.; Neri, D.; Durkop, H.; Menssen, H. D. Expression of the oncofetal ED-B-containing fibronectin isoform in hematologic tumors enables ED-B-targeted 131I-L19SIP radioimmunotherapy in Hodgkin lymphoma patients Blood 2009, 113 (10) 2265-74
Passlick, B.; Pantel, K.; Kubuschok, B.; Angstwurm, M.; Neher, A.; Thetter, O.; Schweiberer, L.; Izbicki, J. R. Expression of MHC molecules and ICAM-1 on non-small cell lung carcinomas: association with early lymphatic spread of tumour cells Eur. J. Cancer 1996, 32A (1) 141-5
Ramirez, N. E.; Zhang, Z.; Madamanchi, A.; Boyd, K. L.; ORear, L. D.; Nashabi, A.; Li, Z.; Dupont, W. D.; Zijlstra, A.; Zutter, M. M. The alphabeta integrin is a metastasis suppressor in mouse models and human cancer J. Clin. Invest. 2011, 121 (1) 226-37
Zutter, M. M.; Santoro, S. A.; Staatz, W. D.; Tsung, Y. L. Re-expression of the alpha 2 beta 1 integrin abrogates the malignant phenotype of breast carcinoma cells Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (16) 7411-5
Madjd, Z.; Pinder, S. E.; Paish, C.; Ellis, I. O.; Carmichael, J.; Durrant, L. G. Loss of CD59 expression in breast tumours correlates with poor survival J. Pathol. 2003, 200 (5) 633-9
Yi, C. H.; Smith, D. J.; West, W. W.; Hollingsworth, M. A. Loss of fibulin-2 expression is associated with breast cancer progression Am. J. Pathol. 2007, 170 (5) 1535-45
Mullany, S. A.; Moslemi-Kebria, M.; Rattan, R.; Khurana, A.; Clayton, A.; Ota, T.; Mariani, A.; Podratz, K. C.; Chien, J.; Shridhar, V. Expression and functional significance of HtrA1 loss in endometrial cancer Clin. Cancer Res. 2011, 17 (3) 427-36
Hayashido, Y.; Lucas, A.; Rougeot, C.; Godyna, S.; Argraves, W. S.; Rochefort, H. Estradiol and fibulin-1 inhibit motility of human ovarian- and breast-cancer cells induced by fibronectin Int. J. Cancer 1998, 75 (4) 654-8
Sugahara, T.; Yamashita, Y.; Shinomi, M.; Yamanoha, B.; Iseki, H.; Takeda, A.; Okazaki, Y.; Hayashizaki, Y.; Kawai, K.; Suemizu, H.; Andoh, T. Isolation of a novel mouse gene, mSVS-1/SUSD2, reversing tumorigenic phenotypes of cancer cells in vitro Cancer Sci. 2007, 98 (6) 900-8
Wiiger, M. T.; Gehrken, H. B.; Fodstad, O.; Maelandsmo, G. M.; Andersson, Y. A novel human recombinant single-chain antibody targeting CD166/ALCAM inhibits cancer cell invasion in vitro and in vivo tumour growth Cancer Immunol. Immunother. 2010, 59 (11) 1665-74
Davies, S. R.; Dent, C.; Watkins, G.; King, J. A.; Mokbel, K.; Jiang, W. G. Expression of the cell to cell adhesion molecule, ALCAM, in breast cancer patients and the potential link with skeletal metastasis Oncol. Rep. 2008, 19 (2) 555-61
King, J. A.; Ofori-Acquah, S. F.; Stevens, T.; Al-Mehdi, A. B.; Fodstad, O.; Jiang, W. G. Activated leukocyte cell adhesion molecule in breast cancer: prognostic indicator Breast Cancer Res. 2004, 6 (5) R478-87
Ihnen, M.; Kilic, E.; Kohler, N.; Loning, T.; Witzel, I.; Hagel, C.; Holler, S.; Kersten, J. F.; Muller, V.; Janicke, F.; Milde-Langosch, K. Protein expression analysis of ALCAM and CEACAM6 in breast cancer metastases reveals significantly increased ALCAM expression in metastases of the skin J. Clin. Pathol. 2011, 64 (2) 146-52
Putzke, A. P.; Ventura, A. P.; Bailey, A. M.; Akture, C.; Opoku-Ansah, J.; Celiktas, M.; Hwang, M. S.; Darling, D. S.; Coleman, I. M.; Nelson, P. S.; Nguyen, H. M.; Corey, E.; Tewari, M.; Morrissey, C.; Vessella, R. L.; Knudsen, B. S. Metastatic progression of prostate cancer and e-cadherin regulation by zeb1 and SRC family kinases Am. J. Pathol. 2011, 179 (1) 400-10
Jiang, W. G. E-cadherin and its associated protein catenins, cancer invasion and metastasis Br. J. Surg. 1996, 83 (4) 437-46
Castro-Sanchez, L.; Soto-Guzman, A.; Navarro-Tito, N.; Martinez-Orozco, R.; Salazar, E. P. Native type IV collagen induces cell migration through a CD9 and DDR1-dependent pathway in MDA-MB-231 breast cancer cells Eur. J. Cell Biol. 2010, 89 (11) 843-52
Saitoh, O.; Wang, W. C.; Lotan, R.; Fukuda, M. Differential glycosylation and cell surface expression of lysosomal membrane glycoproteins in sublines of a human colon cancer exhibiting distinct metastatic potentials J. Biol. Chem. 1992, 267 (8) 5700-11
Clezardin, P.; Teti, A. Bone metastasis: pathogenesis and therapeutic implications Clin. Exp. Metastasis 2007, 24 (8) 599-608
Roodman, G. D. Mechanisms of bone metastasis N. Engl. J. Med. 2004, 350 (16) 1655-64
Keller, C. L. The Biology of Skeletal Metastases; Kluwer Academic Publishers: Boston, 2004; Vol. 118.
OKeefe, R. J.; Guise, T. A. Molecular mechanisms of bone metastasis and therapeutic implications Clin. Orthop. Relat. Res. 2003, 415 Suppl) S100-4
Hirasawa, H.; Tanaka, S.; Sakai, A.; Tsutsui, M.; Shimokawa, H.; Miyata, H.; Moriwaki, S.; Niida, S.; Ito, M.; Nakamura, T. ApoE gene deficiency enhances the reduction of bone formation induced by a high-fat diet through the stimulation of p53-mediated apoptosis in osteoblastic cells J. Bone Miner. Res. 2007, 22 (7) 1020-30
Alford, A. I.; Terkhorn, S. P.; Reddy, A. B.; Hankenson, K. D. Thrombospondin-2 regulates matrix mineralization in MC3T3-E1 pre-osteoblasts Bone 2010, 46 (2) 464-71
Tucker, R. P.; Adams, J. C.; Lawler, J. Thrombospondin-4 is expressed by early osteogenic tissues in the chick embryo Dev. Dyn. 1995, 203 (4) 477-90
Wilson, T. J.; Nannuru, K. C.; Futakuchi, M.; Sadanandam, A.; Singh, R. K. Cathepsin G enhances mammary tumor-induced osteolysis by generating soluble receptor activator of nuclear factor-kappaB ligand Cancer Res. 2008, 68 (14) 5803-11
Thommesen, L.; Stunes, A. K.; Monjo, M.; Grosvik, K.; Tamburstuen, M. V.; Kjobli, E.; Lyngstadaas, S. P.; Reseland, J. E.; Syversen, U. Expression and regulation of resistin in osteoblasts and osteoclasts indicate a role in bone metabolism J. Cell Biochem. 2006, 99 (3) 824-34
Karlstrom, E.; Norgard, M.; Hultenby, K.; Somogyi-Ganss, E.; Sugars, R.; Andersson, G.; Wendel, M. Localization and expression of prothrombin in rodent osteoclasts and long bones Calcif. Tissue Int. 2011, 88 (3) 179-88
Schaefer, L.; Iozzo, R. V. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction J. Biol. Chem. 2008, 283 (31) 21305-9
Waddington, R. J.; Roberts, H. C.; Sugars, R. V.; Schonherr, E. Differential roles for small leucine-rich proteoglycans in bone formation Eur. Cell Mater. 2003, 6, 12-21; discussion 21
Kalamajski, S.; Aspberg, A.; Lindblom, K.; Heinegard, D.; Oldberg, A. Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization Biochem. J. 2009, 423 (1) 53-9
Raouf, A.; Ganss, B.; McMahon, C.; Vary, C.; Roughley, P. J.; Seth, A. Lumican is a major proteoglycan component of the bone matrix Matrix Biol. 2002, 21 (4) 361-7
Hamajima, S.; Hiratsuka, K.; Kiyama-Kishikawa, M.; Tagawa, T.; Kawahara, M.; Ohta, M.; Sasahara, H.; Abiko, Y. Effect of low-level laser irradiation on osteoglycin gene expression in osteoblasts Lasers Med. Sci. 2003, 18 (2) 78-82
Wang, X.; Harimoto, K.; Xie, S.; Cheng, H.; Liu, J.; Wang, Z. Matrix protein biglycan induces osteoblast differentiation through extracellular signal-regulated kinase and Smad pathways Biol. Pharm. Bull. 2010, 33 (11) 1891-7
Rucci, N.; Rufo, A.; Alamanou, M.; Capulli, M.; Del Fattore, A.; Ahrman, E.; Capece, D.; Iansante, V.; Zazzeroni, F.; Alesse, E.; Heinegard, D.; Teti, A. The glycosaminoglycan-binding domain of PRELP acts as a cell type-specific NF-kappaB inhibitor that impairs osteoclastogenesis J. Cell Biol. 2009, 187 (5) 669-83
Leygue, E.; Snell, L.; Dotzlaw, H.; Hole, K.; Hiller-Hitchcock, T.; Roughley, P. J.; Watson, P. H.; Murphy, L. C. Expression of lumican in human breast carcinoma Cancer Res. 1998, 58 (7) 1348-52
Naito, Z. Role of the small leucine-rich proteoglycan (SLRP) family in pathological lesions and cancer cell growth J. Nippon Med. Sch. 2005, 72 (3) 137-45
Seya, T.; Tanaka, N.; Shinji, S.; Yokoi, K.; Koizumi, M.; Teranishi, N.; Yamashita, K.; Tajiri, T.; Ishiwata, T.; Naito, Z. Lumican expression in advanced colorectal cancer with nodal metastasis correlates with poor prognosis Oncol. Rep. 2006, 16 (6) 1225-30
Zeltz, C.; Brezillon, S.; Kapyla, J.; Eble, J. A.; Bobichon, H.; Terryn, C.; Perreau, C.; Franz, C. M.; Heino, J.; Maquart, F. X.; Wegrowski, Y. Lumican inhibits cell migration through alpha2beta1 integrin Exp. Cell Res. 2010, 316 (17) 2922-31
Brezillon, S.; Radwanska, A.; Zeltz, C.; Malkowski, A.; Ploton, D.; Bobichon, H.; Perreau, C.; Malicka-Blaszkiewicz, M.; Maquart, F. X.; Wegrowski, Y. Lumican core protein inhibits melanoma cell migration via alterations of focal adhesion complexes Cancer Lett. 2009, 283 (1) 92-100
Iozzo, R. V.; Schaefer, L. Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans FEBS J. 2010, 277 (19) 3864-75
Araki, K.; Wakabayashi, H.; Shintani, K.; Morikawa, J.; Matsumine, A.; Kusuzaki, K.; Sudo, A.; Uchida, A. Decorin suppresses bone metastasis in a breast cancer cell line Oncology 2009, 77 (2) 92-9
Yamada, S.; Tomoeda, M.; Ozawa, Y.; Yoneda, S.; Terashima, Y.; Ikezawa, K.; Ikegawa, S.; Saito, M.; Toyosawa, S.; Murakami, S. PLAP-1/asporin, a novel negative regulator of periodontal ligament mineralization J. Biol. Chem. 2007, 282 (32) 23070-80
Ikegawa, S. Expression, regulation and function of asporin, a susceptibility gene in common bone and joint diseases Curr. Med. Chem. 2008, 15 (7) 724-8
Nakajima, M.; Kizawa, H.; Saitoh, M.; Kou, I.; Miyazono, K.; Ikegawa, S. Mechanisms for asporin function and regulation in articular cartilage J. Biol. Chem. 2007, 282 (44) 32185-92
Turashvili, G.; Bouchal, J.; Baumforth, K.; Wei, W.; Dziechciarkova, M.; Ehrmann, J.; Klein, J.; Fridman, E.; Skarda, J.; Srovnal, J.; Hajduch, M.; Murray, P.; Kolar, Z. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis BMC Cancer 2007, 7, 55
Peyruchaud, O.; Winding, B.; Pecheur, I.; Serre, C. M.; Delmas, P.; Clezardin, P. Early detection of bone metastases in a murine model using fluorescent human breast cancer cells: application to the use of the bisphosphonate zoledronic acid in the treatment of osteolytic lesions J. Bone Miner. Res. 2001, 16 (11) 2027-34
Pecheur, I.; Peyruchaud, O.; Serre, C. M.; Guglielmi, J.; Voland, C.; Bourre, F.; Margue, C.; Cohen-Solal, M.; Buffet, A.; Kieffer, N.; Clezardin, P. Integrin alpha(v)beta3 expression confers on tumor cells a greater propensity to metastasize to bone FASEB J. 2002, 16 (10) 1266-8
Le Gall, C.; Bellahcene, A.; Bonnelye, E.; Gasser, J. A.; Castronovo, V.; Green, J.; Zimmermann, J.; Clezardin, P. A cathepsin K inhibitor reduces breast cancer induced osteolysis and skeletal tumor burden Cancer Res. 2007, 67 (20) 9894-902
Futterer, A.; Kruppa, G.; Kramer, B.; Lemke, H.; Kronke, M. Molecular cloning and characterization of human kinectin Mol. Biol. Cell 1995, 6 (2) 161-70
Sjoblom, T.; Jones, S.; Wood, L. D.; Parsons, D. W.; Lin, J.; Barber, T. D.; Mandelker, D.; Leary, R. J.; Ptak, J.; Silliman, N.; Szabo, S.; Buckhaults, P.; Farrell, C.; Meeh, P.; Markowitz, S. D.; Willis, J.; Dawson, D.; Willson, J. K.; Gazdar, A. F.; Hartigan, J.; Wu, L.; Liu, C.; Parmigiani, G.; Park, B. H.; Bachman, K. E.; Papadopoulos, N.; Vogelstein, B.; Kinzler, K. W.; Velculescu, V. E. The consensus coding sequences of human breast and colorectal cancers Science 2006, 314 (5797) 268-74
Wang, H. C.; Su, Y. R.; Han, K. J.; Pang, X. W.; Peng, J. R.; Liang, B.; Wang, S.; Chen, W. F. Multiple variants and a differential splicing pattern of kinectin in human hepatocellular carcinoma Biochem. Cell. Biol. 2004, 82 (2) 321-7
Babeto, E.; Conceicao, A. L.; Valsechi, M. C.; Peitl Junior, P.; de Campos Zuccari, D. A.; de Lima, L. G.; Bonilha, J. L.; de Freitas Calmon, M.; Cordeiro, J. A.; Rahal, P. Differentially expressed genes in giant cell tumor of bone Virchows Arch. 2011, 458 (4) 467-76
Sutton, C. W.; Rustogi, N.; Gurkan, C.; Scally, A.; Loizidou, M. A.; Hadjisavvas, A.; Kyriacou, K. Quantitative proteomic profiling of matched normal and tumor breast tissues J. Proteome Res. 2010, 9 (8) 3891-902
Hergeth, S. P.; Aicher, W. K.; Essl, M.; Schreiber, T. D.; Sasaki, T.; Klein, G. Characterization and functional analysis of osteoblast-derived fibulins in the human hematopoietic stem cell niche Exp. Hematol. 2008, 36 (8) 1022-34
Akiyama, T.; Dass, C. R.; Shinoda, Y.; Kawano, H.; Tanaka, S.; Choong, P. F. PEDF regulates osteoclasts via osteoprotegerin and RANKL Biochem. Biophys. Res. Commun. 2010, 391 (1) 789-94
Litvin, J.; Selim, A. H.; Montgomery, M. O.; Lehmann, K.; Rico, M. C.; Devlin, H.; Bednarik, D. P.; Safadi, F. F. Expression and function of periostin-isoforms in bone J. Cell Biochem. 2004, 92 (5) 1044-61
Iba, K.; Chiba, H.; Yamashita, T.; Ishii, S.; Sawada, N. Phase-independent inhibition by retinoic acid of mineralization correlated with loss of tetranectin expression in a human osteoblastic cell line Cell Struct. Funct. 2001, 26 (4) 227-33
Kanakis, I.; Nikolaou, M.; Pectasides, D.; Kiamouris, C.; Karamanos, N. K. Determination and biological relevance of serum cross-linked type I collagen N-telopeptide and bone-specific alkaline phosphatase in breast metastatic cancer J. Pharm. Biomed. Anal. 2004, 34 (4) 827-32