CXCL12-CXCR4 contributes to the implication of bone marrow in cancer metastasis

Future Oncology

Volumn 10, Issue 5, 2014, Pages 749-759

  Shi, Jingsheng ^a   Wei, Yibing ^a   Xia, Jun ^a   Wang, Siqun ^a   Wu, Jianguo ^a   Chen, Feiyan ^a   Huang, Gangyong ^a   Chen, Jie ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

bone marrow; CXCL12; CXCR4; hematopoietic stem cells; metastasis

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MIGRATION INHIBITION FACTOR; N [1,4,8,11 TETRAAZACYCLOTETRADECANYL 1,4 PHENYLENEBIS(METHYLENE)] 2 (AMINOMETHYL)PYRIDINE; PHOSPHATIDYLINOSITOL 3 KINASE; PLERIXAFOR; PROTEIN KINASE B; VASCULOTROPIN; VERY LATE ACTIVATION ANTIGEN 4; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

ANGIOGENESIS; BONE MARROW; BONE MARROW METASTASIS; BREAST CANCER; CANCER CELL; CANCER GROWTH; CIRCULATING TUMOR CELL; DISTANT METASTASIS; DNA DAMAGE; ENZYME PHOSPHORYLATION; GLIOBLASTOMA; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; METASTASIS; MULTIPLE MYELOMA; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; REVIEW; RNA INTERFERENCE; T LYMPHOCYTE ACTIVATION; THYROID CANCER; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; CANCER STEM CELL; GENETICS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

BONE MARROW; CHEMOKINE CXCL12; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CXCR4; TUMOR MICROENVIRONMENT;

EID: 84899878794     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.13.193     Document Type: Review

References (96)

1. Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G. Chemokines and their receptors in the central nervous system. Front. Neuroendocrinol. 22(3), 147-184 (2001).
2. Deutsch AJ, Steinbauer E, Hofmann NA et al. Chemokine receptors in gastric MALT lymphoma: loss of CXCR4 and upregulation of CXCR7 is associated with progression to diffuse large B-cell lymphoma. Mod. Pathol. 26(2), 182-194 (2013).
3. Sun X, Charbonneau C, Wei L, Yang W, Chen Q, Terek RM. CXCR4-targeted therapy inhibits VEGF expression and chondrosarcoma angiogenesis and metastasis. Mol. Cancer Ther. 12(7), 1163-11670 (2013).
4. Tanaka G, Nakase I, Fukuda Y et al. CXCR4 stimulates macropinocytosis: implications for cellular uptake of arginine-rich cell-penetrating peptides and HIV. Chem. Biol. 19(11), 1437-1446 (2012).
5. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin. Cancer Res. 16(11), 2927-2931 (2010).
6. Shahnazari M, Chu V, Wronski TJ, Nissenson RA, Halloran BP. CXCL12/CXCR4 signaling in the osteoblast regulates the mesenchymal stem cell and osteoclast lineage populations. FASEB J. 27(9), 3505-3513 (2013).
7. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 113(24), 6085-6093 (2009).
8. Domanska UM, Kruizinga RC, Nagengast WB et al. A review on CXCR4/CXCL12 axis in oncology: no place to hide. Eur. J. Cancer 49(1), 219-230 (2013).
9. Wang L, Chen W, Gao L et al. High expression of CXCR4, CXCR7 and SDF-1 predicts poor survival in renal cell carcinoma. World J. Surg. Oncol. 10, 212 (2012).
10. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107(5), 1761-1767 (2006).
11. Jin F, Brockmeier U, Otterbach F, Metzen E. New insight into the SDF-1/CXCR4 axis in a breast carcinoma model: hypoxia-induced endothelial SDF-1 and tumor cell CXCR4 are required for tumor cell intravasation. Mol. Cancer Res. 10(8), 1021-1031 (2012).
12. Xu Y, Xia X, Pan H. Active autophagy in the tumor microenvironment: a novel mechanism for cancer metastasis. Oncol. Lett. 5(2), 411-416 (2013).
13. Smith JN, Calvi LM. Concise review: current concepts in bone marrow microenvironmental regulation of hematopoietic stem and progenitor cells. Stem Cells 31(6), 1044-1050 (2013).
14. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382), 457-462 (2012).
15. Doan PL, Chute JP. The vascular niche: home for normal and malignant hematopoietic stem cells. Leukemia 26(1), 54-62 (2012).
16. Yin T, Li L. The stem cell niches in bone. J. Clin. Invest. 116(5), 1195-1201 (2006).
17. Pedersen EA, Shiozawa Y, Pienta KJ, Taichman RS. The prostate cancer bone marrow niche: more than just 'fertile soil'. Asian J. Androl. 14(3), 423-427 (2012).
18. Chantrain CF, Feron O, Marbaix E, Declerck YA. Bone marrow microenvironment and tumor progression. Cancer Microenviron. 1(1), 23-35 (2008).
19. Martinez-Agosto JA, Mikkola HK, Hartenstein V, Banerjee U. The hematopoietic stem cell and its niche: a comparative view. Genes Dev. 21(23), 3044-3060 (2007).
20. Jung Y, Song J, Shiozawa Y et al. Hematopoietic stem cells regulate mesenchymal stromal cell induction into osteoblasts thereby participating in the formation of the stem cell niche. Stem Cells 26(8), 2042-2051 (2008).
21. Arai F, Hirao A, Ohmura M et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118(2), 149-161 (2004).
22. Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105(7), 2631-2639 (2005).
23. Stier S, Ko Y, Forkert R et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J. Exp. Med. 201(11), 1781-1791 (2005).
24. Kaplan RN, Psaila B, Lyden D. Niche-to-niche migration of bone-marrow-derived cells. Trends Mol. Med. 13(2), 72-81 (2007).
25. Lawal RA, Calvi LM. The niche as a target for hematopoietic manipulation and regeneration. Tissue Eng. Part B Rev. 17(6), 415-422 (2011).
26. Dar A, Kollet O, Lapidot T. Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp. Hematol. 34(8), 967-975 (2006).
27. Liekens S, Schols D, Hatse S. CXCL12-CXCR4 axis in angiogenesis, metastasis and stem cell mobilization. Curr. Pharm. Des. 16(35), 3903-3920 (2010).
28. Chabannon C, Calmels B, Habibi S, Mohty M, Imbert AM. New molecular targets and new clinical practices for hematopoietic stem cell mobilization. Bull. Cancer 98(8), 951-961 (2011).
29. Mcquibban GA, Gong JH, Wong JP, Wallace JL, Clark-Lewis I, Overall CM. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100(4), 1160-1167 (2002).
30. Askari AT, Unzek S, Popovic ZB et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362(9385), 697-703 (2003).
31. Zhang D, Fan G-C, Zhou X et al. Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J. Mol. Cell Cardiol. 44(2), 281-292 (2008).
32. Nagasawa T, Hirota S, Tachibana K et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382(6592), 635-638 (1996).
33. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393(6685), 595-599 (1998).
34. Roodman GD. Mechanisms of bone metastasis. Discov. Med. 4(22), 144-148 (2004).
35. Kaplan RN, Psaila B, Lyden D. Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Cancer Metastasis Rev. 25(4), 521-529 (2006).
36. Guo YF, Wang XB, Tian XY et al. Tumor-derived hepatocyte growth factor is associated with poor prognosis of patients with glioma and influences the chemosensitivity of glioma cell line to cisplatin in vitro. World J. Surg. Oncol. 10, 128 (2012).
37. Chen P, Bonaldo P. Role of macrophage polarization in tumor angiogenesis and vessel normalization: implications for new anticancer therapies. Int. Rev. Cell Mol. Biol. 301, 1-35 (2013).
38. Savai R, Langheinrich AC, Schermuly RT et al. Evaluation of angiogenesis using micro-computed tomography in a xenograft mouse model of lung cancer. Neoplasia 11(1), 48-56 (2009).
39. Krock BL, Skuli N, Simon MC. Hypoxia-induced angiogenesis: good and evil. Genes Cancer 2(12), 1117-1133 (2011).
40. Allavena P, Sica A, Solinas G, Porta C, Mantovani A. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit. Rev. Oncol. Hematol. 66(1), 1-9 (2008).
41. Bergers G, Brekken R, Mcmahon G et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2(10), 737-744 (2000).
42. Eichmann A, Marcelle C, Breant C, Le Douarin NM. Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech. Dev. 42(1-2), 33-48 (1993).
43. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat. Rev. Cancer 6(11), 835-845 (2006).
44. Kopp HG, Ramos CA, Rafii S. Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr. Opin. Hematol. 13(3), 175-181 (2006).
45. Hillen F, Griffioen AW. Tumour vascularization: sprouting angiogenesis and beyond. Cancer Metastasis Rev. 26(3-4), 489-502 (2007).
46. Nakagawa H, Liyanarachchi S, Davuluri RV et al. Role of cancer-associated stromal fibroblasts in metastatic colon cancer to the liver and their expression profiles. Oncogene 23(44), 7366-7377 (2004).
47. Orimo A, Gupta PB, Sgroi DC et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121(3), 335-348 (2005).
48. Vaupel P. The role of hypoxia-induced factors in tumor progression. Oncologist 9(Suppl. 5), 10-17 (2004).
49. Hall JM, Korach KS. Stromal cell-derived factor 1, a novel target of estrogen receptor action, mediates the mitogenic effects of estradiol in ovarian and breast cancer cells. Mol. Endocrinol. 17(5), 792-803 (2003).
50. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, Mccauley LK. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res. 62(6), 1832-1837 (2002).
51. Kaifi JT, Yekebas EF, Schurr P et al. Tumor-cell homing to lymph nodes and bone marrow and CXCR4 expression in esophageal cancer. J. Natl Cancer Inst. 97(24), 1840-1847 (2005).
52. Kim SY, Lee CH, Midura BV et al. Inhibition of the CXCR4/CXCL12 chemokine pathway reduces the development of murine pulmonary metastases. Clin. Exp. Metastasis 25(3), 201-211 (2008).
53. Geminder H, Sagi-Assif O, Goldberg L et al. A possible role for CXCR4 and its ligand, the CXC chemokine stromal cell-derived factor-1, in the development of bone marrow metastases in neuroblastoma. J. Immunol. 167(8), 4747-4757 (2001).
54. Zagzag D, Krishnamachary B, Yee H et al. Stromal cell-derived factor-1alpha and CXCR4 expression in hemangioblastoma and clear cell-renal cell carcinoma: von Hippel-Lindau loss-of-function induces expression of a ligand and its receptor. Cancer Res. 65(14), 6178-6188 (2005).
55. De Nigris F, Schiano C, Infante T, Napoli C. CXCR4 inhibitors: tumor vasculature and therapeutic challenges. Recent Pat. Anticancer Drug Discov. 7(3), 251-264 (2012).
56. Smith MC, Luker KE, Garbow JR et al. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res. 64(23), 8604-8612 (2004).
57. Yano T, Liu Z, Donovan J, Thomas MK, Habener JF. Stromal cell derived factor-1 (SDF-1)/CXCL12 attenuates diabetes in mice and promotes pancreatic beta-cell survival by activation of the prosurvival kinase Akt. Diabetes 56(12), 2946-2957 (2007).
58. Yasumoto K, Koizumi K, Kawashima A et al. Role of the CXCL12/CXCR4 axis in peritoneal carcinomatosis of gastric cancer. Cancer Res. 66(4), 2181-2187 (2006).
59. Kijowski J, Baj-Krzyworzeka M, Majka M et al. The SDF-1-CXCR4 axis stimulates VEGF secretion and activates integrins but does not affect proliferation and survival in lymphohematopoietic cells. Stem Cells 19(5), 453-466 (2001).
60. Liang Z, Brooks J, Willard M et al. CXCR4/CXCL12 axis promotes VEGF-mediated tumor angiogenesis through Akt signaling pathway. Biochem. Biophys. Res. Commun. 359(3), 716-722 (2007).
61. Cabioglu N, Summy J, Miller C et al. CXCL-12/stromal cell-derived factor-1alpha transactivates HER2-neu in breast cancer cells by a novel pathway involving Src kinase activation. Cancer Res. 65(15), 6493-6497 (2005).
62. Barbero S, Bonavia R, Bajetto A et al. Stromal cell-derived factor 1alpha stimulates human glioblastoma cell growth through the activation of both extracellular signal-regulated kinases 1/2 and Akt. Cancer Res. 63(8), 1969-1974 (2003).
63. Huang M, Li Y, Zhang H, Nan F. Breast cancer stromal fibroblasts promote the generation of CD44+CD24- cells through SDF-1/CXCR4 interaction. J. Exp. Clin. Cancer Res. 29, 80 (2010).
64. Brand S, Dambacher J, Beigel F et al. CXCR4 and CXCL12 are inversely expressed in colorectal cancer cells and modulate cancer cell migration, invasion and MMP-9 activation. Exp. Cell Res. 310(1), 117-130 (2005).
65. Chinni SR, Sivalogan S, Dong Z et al. CXCL12/CXCR4 signaling activates Akt-1 and MMP-9 expression in prostate cancer cells: the role of bone microenvironment-associated CXCL12. Prostate 66(1), 32-48 (2006).
66. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 140(6), 883-899 (2010).
67. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med. 190(10), 1375-1382 (1999).
68. Coussens LM, Werb Z. Inflammation and cancer. Nature 420(6917), 860-867 (2002).
69. Robinson SC, Coussens LM. Soluble mediators of inflammation during tumor development. Adv. Cancer Res. 93, 159-187 (2005).
70. Szlosarek P, Charles KA, Balkwill FR. Tumour necrosis factor-alpha as a tumour promoter. Eur. J. Cancer 42(6), 745-750 (2006).
71. Liakou CI, Kamat A, Tang DN et al. CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc. Natl Acad. Sci. USA 105(39), 14987-14992 (2008).
72. Peled A, Kollet O, Ponomaryov T et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34+ cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 95(11), 3289-3296 (2000).
73. Wright N, Hidalgo A, Rodriguez-Frade JM et al. The chemokine stromal cell-derived factor-1 alpha modulates alpha 4 beta 7 integrin-mediated lymphocyte adhesion to mucosal addressin cell adhesion molecule-1 and fibronectin. J. Immunol. 168(10), 5268-5277 (2002).
74. Karin N. The multiple faces of CXCL12 (SDF-1alpha) in the regulation of immunity during health and disease. J. Leukoc. Biol. 88(3), 463-473 (2010).
75. Nanki T, Hayashida K, El-Gabalawy HS et al. Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J. Immunol. 165(11), 6590-6598 (2000).
76. Werner L, Guzner-Gur H, Dotan I. Involvement of CXCR4/CXCR7/CXCL12 Interactions in inflammatory bowel disease. Theranostics 3(1), 40-46 (2013).
77. Minamiya Y, Saito H, Takahashi N et al. Expression of the chemokine receptor CXCR4 correlates with a favorable prognosis in patients with adenocarcinoma of the lung. Lung Cancer 68(3), 466-471 (2010).
78. D'alterio C, Barbieri A, Portella L et al. Inhibition of stromal CXCR4 impairs development of lung metastases. Cancer Immunol. Immunother. 61(10), 1713-1720 (2012).
79. Debnath B, Xu S, Grande F, Garofalo A, Neamati N. Small molecule inhibitors of CXCR4. Theranostics 3(1), 47-75 (2013).
80. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9(4), 239-252 (2009).
81. Hermann PC, Huber SL, Herrler T et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 1(3), 313-323 (2007).
82. Zeelenberg IS, Ruuls-Van Stalle L, Roos E. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res. 63(13), 3833-3839 (2003).
83. Scotton CJ, Wilson JL, Scott K et al. Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res. 62(20), 5930-5938 (2002).
84. Kozlow W, Guise TA. Breast cancer metastasis to bone: mechanisms of osteolysis and implications for therapy. J. Mammary Gland Biol. Neoplasia 10(2), 169-180 (2005).
85. Psaila B, Kaplan RN, Port ER, Lyden D. Priming the 'soil' for breast cancer metastasis: the pre-metastatic niche. Breast Dis. 26, 65-74 (2006).
86. Peng SB, Peek V, Zhai Y et al. Akt activation, but not extracellular signal-regulated kinase activation, is required for SDF-1alpha/CXCR4-mediated migration of epitheloid carcinoma cells. Mol. Cancer Res. 3(4), 227-236 (2005).
87. Roy SK, Srivastava RK, Shankar S. Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J. Mol. Signal. 5, 10 (2010).
88. Hartmann TN, Burger JA, Glodek A, Fujii N, Burger M. CXCR4 chemokine receptor and integrin signaling co-operate in mediating adhesion and chemoresistance in small cell lung cancer (SCLC) cells. Oncogene 24(27), 4462-4471 (2005).
89. Chen Y, Jacamo R, Konopleva M, Garzon R, Croce C, Andreeff M. CXCR4 downregulation of let-7a drives chemoresistance in acute myeloid leukemia. J. Clin. Invest. 123(6), 2395-2407 (2013).
90. Zeng Z, Shi YX, Samudio IJ et al. Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood 113(24), 6215-6224 (2009).
91. Weekes CD, Song D, Arcaroli J et al. Stromal cell-derived factor 1alpha mediates resistance to mTOR-directed therapy in pancreatic cancer. Neoplasia 14(8), 690-701 (2012).
92. Jung MJ, Rho JK, Kim YM et al. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene 32(2), 209-221 (2013).
93. Fahham D, Weiss ID, Abraham M et al. In vitro and in vivo therapeutic efficacy of CXCR4 antagonist BKT140 against human non-small cell lung cancer. J. Thorac. Cardiovasc. Surg. 144(5), 1167-1175.e1 (2012).
94. Maftouh M, Avan A, Galvani E, Peters GJ, Giovannetti E. Molecular mechanisms underlying the role of microRNAs in resistance to epidermal growth factor receptor-targeted agents and novel therapeutic strategies for treatment of non-small-cell lung cancer. Crit. Rev. Oncog. 18(4), 317-326 (2013).
95. Papachristou DJ, Basdra EK, Papavassiliou AG. Bone metastases: molecular mechanisms and novel therapeutic interventions. Med. Res. Rev. 32(3), 611-636 (2012).
96. Furstenberger G, Von Moos R, Lucas R et al. Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy of primary breast cancer. Br. J. Cancer 94(4), 524-531 (2006).