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[Cancer Research 62, 1832-1837, March 15, 2002]
© 2002 American Association for Cancer Research

Tumor Biology

Use of the Stromal Cell-derived Factor-1/CXCR4 Pathway in Prostate Cancer Metastasis to Bone1

Russell S. Taichman2, Carlton Cooper, Evan T. Keller, Kenneth J. Pienta, Norton S. Taichman and Laurie K. McCauley

Departments of Periodontics, Prevention, and Geriatrics, and the Center for Biorestoration of Oral Health, School of Dentistry, University of Michigan, Ann Arbor, Michigan 48109-1078 [R. S. T., L. K. M.]; Division of Hematology and Medical Oncology, Department of Internal Medicine, University of Michigan School of Medicine, Ann Arbor, Michigan 48109 [C. C., K. J. P.]; Department of Pathology and Unit for Laboratory Animal Medicine, School of Medicine, University of Michigan, Ann Arbor, Michigan [E. T. K.]; and Department of Pathology, University of Pennsylvania Dental School, Philadelphia, Pennsylvania 19104 [N. S. T.]

Neoplasms have a striking tendency to metastasize or "home" to bone. Hematopoietic cells also home to bone during embryonic development, where evidence points to the chemokine stromal cell-derived factor-1 (SDF-1 or CXCL12; expressed by osteoblasts and endothelial cells) and its receptor (CXCR4) as key elements in these processes. We hypothesized that metastatic prostate carcinomas also use the SDF-1/CXCR4 pathway to localize to the bone. To test this, levels of CXCR4 expression were determined for several human prostate cancer cell lines by reverse transcription-PCR and Western blotting. Positive results were obtained for cell lines derived from malignancies that had spread to bone and marrow. Prostate cancer cells were also observed migrating across bone marrow endothelial cell monolayers in response to SDF-1. In in vitro adhesion assays, pretreatment of the prostate cancer cells with SDF-1 significantly increased their adhesion to osteosarcomas and endothelial cell lines in a dose-dependent manner. Invasion of the cancer cell lines through basement membranes was also supported by SDF-1 and inhibited by antibody to CXCR4. Collectively, these results suggest that prostate cancers and perhaps other neoplasms may use the SDF-1/CXCR4 pathway to spread to bone.




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S. Miwa, A. Mizokami, E. T. Keller, R. Taichman, J. Zhang, and M. Namiki
The Bisphosphonate YM529 Inhibits Osteolytic and Osteoblastic Changes and CXCR-4-Induced Invasion in Prostate Cancer
Cancer Res., October 1, 2005; 65(19): 8818 - 8825.
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 Endocr Relat CancerHome page
G A Clines and T A Guise
Hypercalcaemia of malignancy and basic research on mechanisms responsible for osteolytic and osteoblastic metastasis to bone
Endocr. Relat. Cancer, September 1, 2005; 12(3): 549 - 583.
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C. Christensen, N. Ambartsumian, G. Gilestro, B. Thomsen, P. Comoglio, L. Tamagnone, P. Guldberg, and E. Lukanidin
Proteolytic Processing Converts the Repelling Signal Sema3E into an Inducer of Invasive Growth and Lung Metastasis
Cancer Res., July 15, 2005; 65(14): 6167 - 6177.
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C. J. Dimitroff, L. Descheny, N. Trujillo, R. Kim, V. Nguyen, W. Huang, K. J. Pienta, J. L. Kutok, and M. A. Rubin
Identification of Leukocyte E-Selectin Ligands, P-Selectin Glycoprotein Ligand-1 and E-Selectin Ligand-1, on Human Metastatic Prostate Tumor Cells
Cancer Res., July 1, 2005; 65(13): 5750 - 5760.
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J. Hu, X. Deng, X. Bian, G. Li, Y. Tong, Y. Li, Q. Wang, R. Xin, X. He, G. Zhou, et al.
The Expression of Functional Chemokine Receptor CXCR4 Is Associated with the Metastatic Potential of Human Nasopharyngeal Carcinoma
Clin. Cancer Res., July 1, 2005; 11(13): 4658 - 4665.
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R. J. Phillips, J. Mestas, M. Gharaee-Kermani, M. D. Burdick, A. Sica, J. A. Belperio, M. P. Keane, and R. M. Strieter
Epidermal Growth Factor and Hypoxia-induced Expression of CXC Chemokine Receptor 4 on Non-small Cell Lung Cancer Cells Is Regulated by the Phosphatidylinositol 3-Kinase/PTEN/AKT/Mammalian Target of Rapamycin Signaling Pathway and Activation of Hypoxia Inducible Factor-1{alpha}
J. Biol. Chem., June 10, 2005; 280(23): 22473 - 22481.
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 BloodHome page
A. Kortesidis, A. Zannettino, S. Isenmann, S. Shi, T. Lapidot, and S. Gronthos
Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells
Blood, May 15, 2005; 105(10): 3793 - 3801.
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J. Kim, H. Takeuchi, S. T. Lam, R. R. Turner, H.-J. Wang, C. Kuo, L. Foshag, A. J. Bilchik, and D. S.B. Hoon
Chemokine Receptor CXCR4 Expression in Colorectal Cancer Patients Increases the Risk for Recurrence and for Poor Survival
J. Clin. Oncol., April 20, 2005; 23(12): 2744 - 2753.
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A. Katayama, T. Ogino, N. Bandoh, S. Nonaka, and Y. Harabuchi
Expression of CXCR4 and Its Down-Regulation by IFN-{gamma} in Head and Neck Squamous Cell Carcinoma
Clin. Cancer Res., April 15, 2005; 11(8): 2937 - 2946.
[Abstract] [Full Text] [PDF]

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 BloodHome page
S. Fukuda, H. E. Broxmeyer, and L. M. Pelus
Flt3 ligand and the Flt3 receptor regulate hematopoietic cell migration by modulating the SDF-1{alpha}(CXCL12)/CXCR4 axis
Blood, April 15, 2005; 105(8): 3117 - 3126.
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 Mol Cancer ResHome page
S.-B. Peng, V. Peek, Y. Zhai, D. C. Paul, Q. Lou, X. Xia, T. Eessalu, W. Kohn, and S. Tang
Akt Activation, but not Extracellular Signal-Regulated Kinase Activation, Is Required for SDF-1{alpha}/CXCR4-Mediated Migration of Epitheloid Carcinoma Cells
Mol. Cancer Res., April 1, 2005; 3(4): 227 - 236.
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 EndocrinologyHome page
A. Schneider, L. M. Kalikin, A. C. Mattos, E. T. Keller, M. J. Allen, K. J. Pienta, and L. K. McCauley
Bone Turnover Mediates Preferential Localization of Prostate Cancer in the Skeleton
Endocrinology, April 1, 2005; 146(4): 1727 - 1736.
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C. Laverdiere, B. H. Hoang, R. Yang, R. Sowers, J. Qin, P. A. Meyers, A. G. Huvos, J. H. Healey, and R. Gorlick
Messenger RNA Expression Levels of CXCR4 Correlate with Metastatic Behavior and Outcome in Patients with Osteosarcoma
Clin. Cancer Res., April 1, 2005; 11(7): 2561 - 2567.
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A. C.W. Zannettino, A. N. Farrugia, A. Kortesidis, J. Manavis, L. B. To, S. K. Martin, P. Diamond, H. Tamamura, T. Lapidot, N. Fujii, et al.
Elevated Serum Levels of Stromal-Derived Factor-1{alpha} Are Associated with Increased Osteoclast Activity and Osteolytic Bone Disease in Multiple Myeloma Patients
Cancer Res., March 1, 2005; 65(5): 1700 - 1709.
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S. Scala, A. Ottaiano, P. A. Ascierto, M. Cavalli, E. Simeone, P. Giuliano, M. Napolitano, R. Franco, G. Botti, and G. Castello
Expression of CXCR4 Predicts Poor Prognosis in Patients with Malignant Melanoma
Clin. Cancer Res., March 1, 2005; 11(5): 1835 - 1841.
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E. Perissinotto, G. Cavalloni, F. Leone, V. Fonsato, S. Mitola, G. Grignani, N. Surrenti, D. Sangiolo, F. Bussolino, W. Piacibello, et al.
Involvement of Chemokine Receptor 4/Stromal Cell-Derived Factor 1 System during Osteosarcoma Tumor Progression
Clin. Cancer Res., January 15, 2005; 11(2): 490 - 497.
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S. Singh, U. P. Singh, J. K. Stiles, W. E. Grizzle, and J. W. Lillard Jr.
Expression and Functional Role of CCR9 in Prostate Cancer Cell Migration and Invasion
Clin. Cancer Res., December 15, 2004; 10(24): 8743 - 8750.
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F. Marchesi, P. Monti, B. E. Leone, A. Zerbi, A. Vecchi, L. Piemonti, A. Mantovani, and P. Allavena
Increased Survival, Proliferation, and Migration in Metastatic Human Pancreatic Tumor Cells Expressing Functional CXCR4
Cancer Res., November 15, 2004; 64(22): 8420 - 8427.
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 Clin. Cancer Res.Home page
G. G. Vaday, S.-B. Hua, D. M. Peehl, M. H. Pauling, Y.-H. Lin, L. Zhu, D. M. Lawrence, H. D. Foda, and S. Zucker
CXCR4 and CXCL12 (SDF-1) in Prostate Cancer: Inhibitory Effects of Human Single Chain Fv Antibodies
Clin. Cancer Res., August 15, 2004; 10(16): 5630 - 5639.
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C. J. Dimitroff, M. Lechpammer, D. Long-Woodward, and J. L. Kutok
Rolling of Human Bone-Metastatic Prostate Tumor Cells on Human Bone Marrow Endothelium under Shear Flow Is Mediated by E-Selectin
Cancer Res., August 1, 2004; 64(15): 5261 - 5269.
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S. A. Shulby, N. G. Dolloff, M. E. Stearns, O. Meucci, and A. Fatatis
CX3CR1-Fractalkine Expression Regulates Cellular Mechanisms Involved in Adhesion, Migration, and Survival of Human Prostate Cancer Cells
Cancer Res., July 15, 2004; 64(14): 4693 - 4698.
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Z. Liang, T. Wu, H. Lou, X. Yu, R. S. Taichman, S. K. Lau, S. Nie, J. Umbreit, and H. Shim
Inhibition of Breast Cancer Metastasis by Selective Synthetic Polypeptide against CXCR4
Cancer Res., June 15, 2004; 64(12): 4302 - 4308.
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 Molecular Cancer TherapeuticsHome page
Y. S. Haviv, W. J. van Houdt, B. Lu, D. T. Curiel, and Z. B. Zhu
Transcriptional targeting in renal cancer cell lines via the human CXCR4 promoter
Mol. Cancer Ther., June 1, 2004; 3(6): 687 - 691.
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K.-i. Oonakahara, W. Matsuyama, I. Higashimoto, M. Kawabata, K. Arimura, and M. Osame
Stromal-Derived Factor-1{alpha}/CXCL12-CXCR 4 Axis Is Involved in the Dissemination of NSCLC Cells into Pleural Space
Am. J. Respir. Cell Mol. Biol., May 1, 2004; 30(5): 671 - 677.
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S. Tavor, I. Petit, S. Porozov, A. Avigdor, A. Dar, L. Leider-Trejo, N. Shemtov, V. Deutsch, E. Naparstek, A. Nagler, et al.
CXCR4 Regulates Migration and Development of Human Acute Myelogenous Leukemia Stem Cells in Transplanted NOD/SCID Mice
Cancer Res., April 15, 2004; 64(8): 2817 - 2824.
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V. I. Romanov, T. Whyard, H. L. Adler, W. C. Waltzer, and S. Zucker
Prostate Cancer Cell Adhesion to Bone Marrow Endothelium: The Role of Prostate-Specific Antigen
Cancer Res., March 15, 2004; 64(6): 2083 - 2089.
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A. Prasad, A. Z. Fernandis, Y. Rao, and R. K. Ganju
Slit Protein-mediated Inhibition of CXCR4-induced Chemotactic and Chemoinvasive Signaling Pathways in Breast Cancer Cells
J. Biol. Chem., March 5, 2004; 279(10): 9115 - 9124.
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R. Wang, J. Xu, O. Saramaki, T. Visakorpi, W. M. Sutherland, J. Zhou, B. Sen, S. D. Lim, N. Mabjeesh, M. Amin, et al.
PrLZ, a Novel Prostate-Specific and Androgen-Responsive Gene of the TPD52 Family, Amplified in Chromosome 8q21.1 and Overexpressed in Human Prostate Cancer
Cancer Res., March 1, 2004; 64(5): 1589 - 1594.
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N. Sato, N. Fukushima, A. Maitra, C. A. Iacobuzio-Donahue, N. T. van Heek, J. L. Cameron, C. J. Yeo, R. H. Hruban, and M. Goggins
Gene Expression Profiling Identifies Genes Associated with Invasive Intraductal Papillary Mucinous Neoplasms of the Pancreas
Am. J. Pathol., March 1, 2004; 164(3): 903 - 914.
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K. Jankowski, M. Kucia, M. Wysoczynski, R. Reca, D. Zhao, E. Trzyna, J. Trent, S. Peiper, M. Zembala, J. Ratajczak, et al.
Both Hepatocyte Growth Factor (HGF) and Stromal-Derived Factor-1 Regulate the Metastatic Behavior of Human Rhabdomyosarcoma Cells, But Only HGF Enhances Their Resistance to Radiochemotherapy
Cancer Res., November 15, 2003; 63(22): 7926 - 7935.
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S. Manes, E. Mira, R. Colomer, S. Montero, L. M. Real, C. Gomez-Mouton, S. Jimenez-Baranda, A. Garzon, R. A. Lacalle, K. Harshman, et al.
CCR5 Expression Influences the Progression of Human Breast Cancer in a p53-dependent Manner
J. Exp. Med., November 3, 2003; 198(9): 1381 - 1389.
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X. Chen, J. A. Beutler, T. G. McCloud, A. Loehfelm, L. Yang, H.-F. Dong, O. Y. Chertov, R. Salcedo, J. J. Oppenheim, and O. M. Z. Howard
Tannic Acid Is an Inhibitor of CXCL12 (SDF-1{alpha})/CXCR4 with Antiangiogenic Activity
Clin. Cancer Res., August 1, 2003; 9(8): 3115 - 3123.
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Y. Ding, Y. Shimada, M. Maeda, A. Kawabe, J. Kaganoi, I. Komoto, Y. Hashimoto, M. Miyake, H. Hashida, and M. Imamura
Association of CC Chemokine Receptor 7 with Lymph Node Metastasis of Esophageal Squamous Cell Carcinoma
Clin. Cancer Res., August 1, 2003; 9(9): 3406 - 3412.
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C. R. Cogle, S. M. Guthrie, R. C. Sanders, W. L. Allen, E. W. Scott, and B. E. Petersen
An Overview of Stem Cell Research and Regulatory Issues
Mayo Clin. Proc., August 1, 2003; 78(8): 993 - 1003.
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I. S. Zeelenberg, L. Ruuls-Van Stalle, and E. Roos
The Chemokine Receptor CXCR4 Is Required for Outgrowth of Colon Carcinoma Micrometastases
Cancer Res., July 1, 2003; 63(13): 3833 - 3839.
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Y. Zhou, P. H. Larsen, C. Hao, and V. W. Yong
CXCR4 Is a Major Chemokine Receptor on Glioma Cells and Mediates Their Survival
J. Biol. Chem., December 13, 2002; 277(51): 49481 - 49487.
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