Stromal-derived factor-1α/CXCL12-CXCR4 chemotactic pathway promotes perineural invasion in pancreatic cancer

Oncotarget

Volumn 6, Issue 7, 2015, Pages 4717-4732

  Xu, Qinhong ^a   Wang, Zheng ^a   Chen, Xin ^a   Duan, Wanxing ^a   Lei, Jianjun ^a   Zong, Liang ^a   Li, Xuqi ^a   Sheng, Liang ^a   Ma, Jiguang ^a   Han, Liang ^a   Li, Wei ^a   Zhang, Lun ^a   Guo, Kun ^a   Ma, Zhenhua ^a   Wu, Zheng ^a   Wu, Erxi ^b   Ma, Qingyong ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

CXCL12 CXCR4 axis; Pancreatic cancer; Perineural invasion; Tumor microenvironment

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; STROMAL CELL DERIVED FACTOR 1ALPHA; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; MESSENGER RNA; SMALL INTERFERING RNA; STROMAL CELL DERIVED FACTOR 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; METASTASIS; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PARACRINE SIGNALING; PATHOGENESIS; PERINEURAL INVASION; PERIPHERAL NERVE; RAT; SCIATIC NERVE; SIGNAL TRANSDUCTION; SPINAL GANGLION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CANCER GRADING; CANCER STAGING; CASE CONTROL STUDY; CELL MOTION; CELL PROLIFERATION; COMPARATIVE STUDY; DRUG SCREENING; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; FOLLOW UP; GENETICS; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; MOUSE; PANCREAS; PANCREAS TUMOR; PATHOLOGY; PERIPHERAL NERVE TUMOR; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY; TUMOR CELL CULTURE; TUMOR INVASION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; FOLLOW-UP STUDIES; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHATIC METASTASIS; MALE; MICE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PANCREAS; PANCREATIC NEOPLASMS; PERIPHERAL NERVOUS SYSTEM NEOPLASMS; PROGNOSIS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924943497     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3069     Document Type: Article

References (54)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9-29.
2. Cartwright T, Richards DA, Boehm KA. Cancer of the pancreas: are we making progress? A review of studies in the US Oncology Research Network. Cancer Control. 2008;15:308-13.
3. Marchesi F, Piemonti L, Mantovani A, Allavena P. Molecular mechanisms of perineural invasion, a forgotten pathway of dissemination and metastasis. Cytokine Growth Factor Rev. 2010;21:77-82.
4. Bapat AA, Hostetter G, Von Hoff DD, Han H. Perineural invasion and associated pain in pancreatic cancer. Nat Rev Cancer. 2011;11:695-707.
5. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet. 2011.
6. Nakao A, Harada A, Nonami T, Kaneko T, Takagi H. Clinical significance of carcinoma invasion of the extrapancreatic nerve plexus in pancreatic cancer. Pancreas. 1996;12:357-61.
7. Li J, Ma Q, Liu H, Guo K, Li F, Li W, Han L, Wang F, Wu E. Relationship between Neural Alteration and Perineural Invasion in Pancreatic Cancer Patients with Hyperglycemia. PLoS One. 2011;6:e17385.
8. Pour PM, Bell RH, Batra SK. Neural invasion in the staging of pancreatic cancer. Pancreas. 2003;26:322-5.
9. Liebig C, Ayala G, Wilks JA, Berger DH, Albo D. Perineural invasion in cancer: a review of the literature. Cancer. 2009;115:3379-91.
10. Bockman DE, Buchler M, Beger HG. Interaction of pancreatic ductal carcinoma with nerves leads to nerve damage. Gastroenterology. 1994;107:219-30.
11. Liu H, Li X, Xu Q, Lv S, Li J, Ma Q. Role of glial cell line-derived neurotrophic factor in perineural invasion of pancreatic cancer. Biochim Biophys Acta. 2012;1826:112-20.
12. Marchesi F, Piemonti L, Fedele G, Destro A, Roncalli M, Albarello L, Doglioni C, Anselmo A, Doni A, Bianchi P, Laghi L, Malesci A, Cervo L, et al. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res. 2008;68:9060-9.
13. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001;410:50-6.
14. Helbig G, Christopherson KW 2nd, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, Broxmeyer HE, Nakshatri H. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem. 2003;278:21631-8.
15. Hart CA, Brown M, Bagley S, Sharrard M, Clarke NW. Invasive characteristics of human prostatic epithelial cells: understanding the metastatic process. Br J Cancer. 2005;92:503-12.
16. Jiang YP, Wu XH, Shi B, Wu WX, Yin GR. Expression of chemokine CXCL12 and its receptor CXCR4 in human epithelial ovarian cancer: an independent prognostic factor for tumor progression. Gynecol Oncol. 2006;103:226-33.
17. Schimanski CC, Bahre R, Gockel I, Muller A, Frerichs K, Horner V, Teufel A, Simiantonaki N, Biesterfeld S, Wehler T, Schuler M, Achenbach T, Junginger T, et al. Dissemination of hepatocellular carcinoma is mediated via chemokine receptor CXCR4. Br J Cancer. 2006;95:210-7.
18. Kollmar O, Rupertus K, Scheuer C, Junker B, Tilton B, Schilling MK, Menger MD. Stromal cell-derived factor-1 promotes cell migration and tumor growth of colorectal metastasis. Neoplasia. 2007;9:862-70.
19. Wang Z, Ma Q, Liu Q, Yu H, Zhao L, Shen S, Yao J. Blockade of SDF-1/CXCR4 signalling inhibits pancreatic cancer progression in vitro via inactivation of canonical Wnt pathway. Br J Cancer. 2008;99:1695-703.
20. Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, Bhat K, Wang F, Wu E, Wang Z. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of Hedgehog pathway. Cancer Lett. 2012;322:169-76.
21. Gleichmann M, Gillen C, Czardybon M, Bosse F, Greiner-Petter R, Auer J, Muller HW. Cloning and characterization of SDF-1gamma, a novel SDF-1 chemokine transcript with developmentally regulated expression in the nervous system. Eur J Neurosci. 2000;12:1857-66.
22. Dubovy P, Klusakova I, Svizenska I, Brazda V. Spatio-temporal changes of SDF1 and its CXCR4 receptor in the dorsal root ganglia following unilateral sciatic nerve injury as a model of neuropathic pain. Histochem Cell Biol. 2010;133:323-37.
23. Odemis V, Moepps B, Gierschik P, Engele J. Interleukin-6 and cAMP induce stromal cell-derived factor-1 chemotaxis in astroglia by up-regulating CXCR4 cell surface expression. Implications for brain inflammation. J Biol Chem. 2002;277:39801-8.
24. Ceyhan GOD, I. E. Altintas BR, U. Thiel GM, M. W. Giese NAF, H. Schafer KH. Neural invasion in pancreatic cancer: a mutual tropism between neurons and cancer cells. Biochemical and Biophysical Research Communications. 2008;374:442-7.
25. Li X, Ma Q, Xu Q, Duan W, Lei J, Wu E. Targeting the cancer-stroma interaction: a potential approach for pancreatic cancer treatment. Curr Pharm Des. 2012;18:2404-15.
26. Liu H, Ma Q, Xu Q, Lei J, Li X, Wang Z, Wu E. Therapeutic potential of perineural invasion, hypoxia and desmoplasia in pancreatic cancer. Curr Pharm Des. 2012;18:2395-403.
27. Sarvaiya PJ, Guo D, Ulasov I, Gabikian P, Lesniak MS. Chemokines in tumor progression and metastasis. Oncotarget. 2013;4:2171-85.
28. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-64.
29. Zagzag D, Lukyanov Y, Lan L, Ali MA, Esencay M, Mendez O, Yee H, Voura EB, Newcomb EW. Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab Invest. 2006;86:1221-32.
30. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol. 2004;14:171-9.
31. Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci. 2005;25:3995-4003.
32. Odemis V, Lamp E, Pezeshki G, Moepps B, Schilling K, Gierschik P, Littman DR, Engele J. Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci. 2005;30:494-505.
33. Cui K, Zhao W, Wang C, Wang A, Zhang B, Zhou W, Yu J, Sun Z, Li S. The CXCR4-CXCL12 Pathway Facilitates the Progression of Pancreatic Cancer Via Induction of Angiogenesis and Lymphangiogenesis. J Surg Res. 2010.
34. Bachelder RE, Wendt MA, Mercurio AM. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res. 2002;62:7203-6.
35. Staller P, Sulitkova J, Lisztwan J, Moch H, Oakeley EJ, Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature. 2003;425:307-11.
36. Matteucci E, Locati M, Desiderio MA. Hepatocyte growth factor enhances CXCR4 expression favoring breast cancer cell invasiveness. Exp Cell Res. 2005;310:176-85.
37. Mahadevan D, Von Hoff DD. Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol Cancer Ther. 2007;6:1186-97.
38. Zhu Z, Friess H, diMola FF, Zimmermann A, Graber HU, Korc M, Buchler MW. Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer. J Clin Oncol. 1999;17:2419-28.
39. Ben QW, Wang JC, Liu J, Zhu Y, Yuan F, Yao WY, Yuan YZ. Positive expression of L1-CAM is associated with perineural invasion and poor outcome in pancreatic ductal adenocarcinoma. Ann Surg Oncol. 2010;17:2213-21.
40. Sroka IC, Anderson TA, McDaniel KM, Nagle RB, Gretzer MB, Cress AE. The laminin binding integrin alpha6beta1 in prostate cancer perineural invasion. J Cell Physiol. 2010;224:283-8.
41. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, Arenzana-Seisdedos F, Thelen M, Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem. 2005;280:35760-6.
42. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E. Control of chemokine-guided cell migration by ligand sequestration. Cell. 2008;132:463-73.
43. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, Gerard C, Lefkowitz RJ. Beta-arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc Natl Acad Sci U S A. 2010;107:628-32.
44. Xiao K, Sun J, Kim J, Rajagopal S, Zhai B, Villen J, Haas W, Kovacs JJ, Shukla AK, Hara MR, Hernandez M, Lachmann A, Zhao S, et al. Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc Natl Acad Sci U S A. 2010;107:15299-304.
45. Dona E, Barry JD, Valentin G, Quirin C, Khmelinskii A, Kunze A, Durdu S, Newton LR, Fernandez-Minan A, Huber W, Knop M, Gilmour D. Directional tissue migration through a self-generated chemokine gradient. Nature. 2013;503:285-9.
46. Domanska UM, Kruizinga RC, Nagengast WB, Timmer-Bosscha H, Huls G, de Vries EG, Walenkamp AM. A review on CXCR4/CXCL12 axis in oncology: no place to hide. Eur J Cancer. 2013;49:219-30.
47. Zaitseva L, Murray MY, Shafat MS, Lawes MJ, MacEwan DJ, Bowles KM, Rushworth SA. Ibrutinib inhibits SDF1/CXCR4 mediated migration in AML. Oncotarget. 2014;5:9930-8.
48. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, editors. AJCC cancer staging manual (7th ed). 2010;New York, NY: Springer.
49. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-8.
50. Ayala GE, Wheeler TM, Shine HD, Schmelz M, Frolov A, Chakraborty S, Rowley D. In vitro dorsal root ganglia and human prostate cell line interaction: redefining perineural invasion in prostate cancer. Prostate. 2001;49:213-23.
51. Gil Z, Cavel O, Kelly K, Brader P, Rein A, Gao SP, Carlson DL, Shah JP, Fong Y, Wong RJ. Paracrine regulation of pancreatic cancer cell invasion by peripheral nerves. J Natl Cancer Inst. 2010;102:107-18.
52. Li X, Wang Z, Ma Q, Xu Q, Liu H, Duan W, Lei J, Ma J, Wang X, Lv S, Han L, Li W, Guo J, et al. Sonic hedgehog paracrine signaling activates stromal cells to promote perineural invasion in pancreatic cancer. Clin Cancer Res. 2014;20:4326-38.
53. Koide N, Yamada T, Shibata R, Mori T, Fukuma M, Yamazaki K, Aiura K, Shimazu M, Hirohashi S, Nimura Y, Sakamoto M. Establishment of perineural invasion models and analysis of gene expression revealed an invariant chain (CD74) as a possible molecule involved in perineural invasion in pancreatic cancer. Clin Cancer Res. 2006;12:2419-26.
54. Gil Z, Rein A, Brader P, Li S, Shah JP, Fong Y, Wong RJ. Nerve-sparing therapy with oncolytic herpes virus for cancers with neural invasion. Clinical cancer research: an official journal of the American Association for Cancer Research. 2007;13:6479-85.