Hypoxia differentially regulated CXCR4 and CXCR7 signaling in colon cancer

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Romain, Benoît ^a,b   Hachet Haas, Muriel ^c   Rohr, Serge ^a   Brigand, Cécile ^a   Galzi, Jean Luc ^c   Gaub, Marie Pierre ^a,b   Pencreach, Erwan ^a,b,d   Guenot, Dominique ^b  

^a HÔPITAL DE HAUTEPIERRE   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Institut de Recherche de l'Ecole de Biotechnologie de Strasbourg   (France)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

Chemokines; Colon; Hypoxia; Metastasis; Migration

Indexed keywords

CHALCONE 4; CHALCONE DERIVATIVE; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IRINOTECAN; MESSENGER RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR CXCR; CXCR4 PROTEIN, HUMAN; CXCR7 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; PROTEIN KINASE B;

ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CELL MEMBRANE; CELL MIGRATION; CLINICAL ARTICLE; COLON CANCER; COLON MUCOSA; COLON POLYP; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MALE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; CELL MOTION; COLON TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CXCR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84897479412     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-58     Document Type: Article

References (42)

1. Vaupel P, Kelleher DK, Höckel M. Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 2001, 28:29-35.
2. Semenza GL. Life with oxygen. Science 2007, 318:62-64. 10.1126/science.1147949, 17916722.
3. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Rer 1999, 59:5830-5835.
4. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2:38-47. 10.1038/nrc704, 11902584.
5. Wels J, Kaplan RN, Rafii S, Lyden D. Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 2008, 22:559-574. 10.1101/gad.1636908, 2731657, 18316475.
6. Ottaiano A, Franco R, Aiello Talamanca A, Liguori G, Tatangelo F, Delrio P, Nasti G, Barletta E, Facchini G, Daniele B, Di Blasi A, Napolitano M, Ieranò C, Calemma R, Leonardi E, Albino V, De Angelis V, Falanga M, Boccia V, Capuozzo M, Parisi V, Botti G, Castello G, Vincenzo Iaffaioli R, Scala S. Overexpression of both CXC chemokine receptor 4 and vascular endothelial growth factor proteins predicts early distant relapse in stage II-III colorectal cancer patients. Clin Cancer Res 2006, 12:2795-2803. 10.1158/1078-0432.CCR-05-2142, 16675573.
7. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol 2004, 14:171-179. 10.1016/j.semcancer.2003.10.003, 15246052.
8. Luker KE, Luker DG. Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett 2006, 238:30-41. 10.1016/j.canlet.2005.06.021, 16046252.
9. Raman D, Baugher PJ, Thu YM, Richmond A. Role of chemokines in tumor growth. Cancer Lett 2007, 256:137-165. 10.1016/j.canlet.2007.05.013, 2065851, 17629396.
10. Balabanian K, Lagane B, Pablos JL, Laurent L, Planchenault T, Verola O, Lebbe C, Kerob D, Dupuy A, Hermine O, Nicolas JF, Latger-Cannard V, Bensoussan D, Bordigoni P, Baleux F, Le Deist F, Virelizier JL, Arenzana-Seisdedos F, Bachelerie F. WHIM syndromes with different genetic anomalies are accounted for by impaired CXCR4 desensitization to CXCL12. Blood 2005, 105:2449-2457. 10.1182/blood-2004-06-2289, 15536153.
11. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z, Penfold MET, Sunshine MJ, Littman DR, Kuo CJ, Wei K, McMaster BE, Wright K, Howard MC, Schall TJ. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 2006, 203:2201-2213. 10.1084/jem.20052144, 2118398, 16940167.
12. Mazzinghi B, Ronconi E, Lazzeri E, Sagrinati C, Ballerini L, Angelotti ML, Parente E, Mancina R, Netti GS, Becherucci F, Gacci M, Carini M, Gesualdo L, Rotondi M, Maggi E, Lasagni L, Serio M, Romagnani S, Romagnani P. Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J Exp Med 2008, 205:479-490. 10.1084/jem.20071903, 2271008, 18268039.
13. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojani MS, Rehemtulla A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC, Schall TJ. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc Natl Acad Sci U S A 2007, 104:15735-15740. 10.1073/pnas.0610444104, 1994579, 17898181.
14. Salmaggi A, Maderna E, Calatozzolo C, Gaviani P, Canazza A, Milanesi I, Silvani A, DiMeco F, Carbone A, Pollo B. CXCL12, CXCR4 and CXCR7 expression in brain metastases. Cancer Biol Ther 2009, 8:1608-1614. 10.4161/cbt.8.17.9202, 19625779.
15. Rapisarda A, Mellilo G. Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia. Nat Rev Clin Oncol 2012, 9:378-390. 10.1038/nrclinonc.2012.64, 22525710.
16. Guérin E, Raffelsberger W, Pencreach E, Maier A, Neuville A, Schneider A, Bachellier P, Rohr S, Petitprez A, Poch O, Moras D, Oudet P, Larsen AK, Gaub MP, Guenot D. In vivo topoisomerase I inhibition attenuates the expression of hypoxia-inducible factor 1α target genes and decreases tumor angiogenesis. Mol Med 2012, 18:83-94. 10.1007/s00894-011-1029-0, 3269639, 22033674.
17. Hachet-Haas M, Balabanian K, Rohmer F, Pons F, Franchet C, Lecat S, Chow KYC, Dagher R, Gizzi P, Didier B, Lagane B, Kellenberger E, Bonnet D, Baleux F, Haiech J, Parmentier M, Frossard N, Arenzana-Seisdedos F, Hibert M, Galzi JL. Small neutralizing molecules to inhibit actions of the chemokine CXCL12. J Biol Chem 2008, 283:23189-23199. 10.1074/jbc.M803947200, 18556651.
18. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56. 10.1038/35065016, 11242036.
19. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003, 3:401-410. 10.1038/nrc1093, 12778130.
20. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86:353-364. 10.1016/S0092-8674(00)80108-7, 8756718.
21. Bikfalvi A, Moenner M, Javerzat S, North S, Hagedorn M. Inhibition of angiogenesis and the angiogenesis/invasion shift. Biochem Soc Trans 2011, 39:1560-1564. 10.1042/BST20110710, 22103487.
22. Kim J, Mori T, Chen SL, Amersi FF, Martinez SR, Kuo C, Turner RR, Ye X, Bilchik AJ, Morton DL, Hoon DS. Chemokine receptor CXCR4 expression in patients with melanoma and colorectal cancer liver metastases and the association with disease outcome. Ann Surg 2006, 244:113-120. 10.1097/01.sla.0000217690.65909.9c, 1570598, 16794396.
23. Dwinell MB, Eckmann L, Leopard JD, Varki NM, Kagnoff M. Chemokine receptor expression by human intestinal epithelial cells. Gastroenterology 1999, 117:359-367. 10.1053/gast.1999.0029900359, 10419917.
24. Wendt MK, Johanesen PA, Kang-Decker N, Binion DG, Shah V, Dwinell MB. Silencing of epithelial CXCL12 expression by DNA hypermethylation promotes colonic carcinoma metastasis. Oncogene 2006, 25:4986-4997. 10.1038/sj.onc.1209505, 16568088.
25. Wendt MK, Cooper AN, Dwinell MB. Epigenetic silencing of CXCL12 increases the metastatic potential of mammary carcinoma cells. Oncogene 2008, 27:1461-1471. 10.1038/sj.onc.1210751, 17724466.
26. 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 Investig 2006, 86:1221-1232. 10.1038/labinvest.3700482, 17075581.
27. Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, Bernasconi S, Saccani S, Nebuloni M, Vago L, Mantovani A, Melillo G, Sica A. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 2003, 198:1391-1402. 10.1084/jem.20030267, 2194248, 14597738.
28. 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, 425:307-311. 10.1038/nature01874, 13679920.
29. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat Rev Cancer 2004, 4:448-456. 10.1038/nrc1370, 15170447.
30. Gassmann P, Haier J, Schlüter K, Domikowsky B, Wendel C, Wiesner U, Kubitza R, Engers R, Schneider SW, Homey B, Müller A. CXCR4 regulates the early extravasation of metastatic tumor cells in vivo. Neoplasia 2009, 11:651-661. 2697351, 19568410.
31. Guillemot E, Karimdjee-Soilihi B, Pradelli E, Benchetrit M, Goguet-Surmenian E, Millet MA, Larbret F, Michiels JF, Birnbaum D, Alemanno P, Schmid-Antomarchi H, Schmid-Alliana A. CXCR7 receptors facilitate the progression of colon carcinoma within lung not within liver. Br J Cancer 2012, 107:1944-1949. 10.1038/bjc.2012.503, 3516689, 23169289.
32. Dambly-Chaudière C, Cubedo N, Ghysen A. Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1. BMC Dev Biol 2007, 7:23. 10.1186/1471-213X-7-23, 1847803, 17394634.
33. Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, Newman W, Groopman JE. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem 1998, 273:23169-23175. 10.1074/jbc.273.36.23169, 9722546.
34. Zhang XF, Wang JF, Matczak E, Proper JA, Groopman JE. Janus kinase 2 is involved in stromal cell-derived factor-1alpha-induced tyrosine phosphorylation of focal adhesion proteins and migration of hematopoietic progenitor cells. Blood 2001, 97:3342-3348. 10.1182/blood.V97.11.3342, 11369622.
35. Parsons DW, Wang TL, Samuels Y, Bardelli A, Cummins JM, DeLong L, Silliman N, Ptak J, Szabo S, Willson JK, Markowitz S, Kinzler KW, Vogelstein B, Lengauer C, Velculescu VE. Colorectal cancer: mutations in a signalling pathway. Nature 2005, 436:792. 10.1038/436792a, 16094359.
36. Hwang MK, Song NR, Kang NJ, Lee KW, Lee HJ. Activation of phosphatidylinositol 3-kinase is required for tumor necrosis factor-alpha-induced upregulation of matrix metalloproteinase-9: its direct inhibition by quercetin. Int J Biochem 2009, 41:1592-1600.
37. Shukla S, Maclennan GT, Hartman DJ, Fu P, Resnick MI, Gupta S. Activation of PI3K-Akt signaling pathway promotes prostate cancer cell invasion. Int J Cancer 2007, 121:1424-1432. 10.1002/ijc.22862, 17551921.
38. Zabel BA, Wang Y, Lewén S, Berahovich RD, Penfold ME, Zhang P, Powers J, Summers BC, Miao Z, Zhao B, Jalili A, Janowska-Wieczorek A, Jaen JC, Schall TJ. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 2009, 183:3204-3211. 10.4049/jimmunol.0900269, 19641136.
39. Kucia M, Jankowski K, Reca R, Wysoczynski M, Bandura L, Allendorf DJ, Zhang J, Ratajczak J, Ratajczak MZ. CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. J Mol Histol 2004, 35:233-245.
40. Miyoshi K, Wakioka T, Nishinakamura H, Kamio M, Yang L, Inoue M, Hasegawa M, Yonemitsu Y, Komiya S, Yoshimura A. The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 2004, 23:5567-5576. 10.1038/sj.onc.1207759, 15184877.
41. Sahai E, Marshall CJ. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 2003, 5:711-719. 10.1038/ncb1019, 12844144.
42. Pencreach E, Guérin E, Nicolet C, Lelong-Rebel I, Voegeli AC, Oudet P, Larsen AK, Gaub MP, Guenot D. Marked activity of irinotecan and rapamycin combination toward colon cancer cells in vivo and in vitro is mediated through cooperative modulation of the mammalian target of rapamycin/hypoxia-inducible factor-1alpha axis. Clin Cancer Res 2009, 15:1297-1307. 10.1158/1078-0432.CCR-08-0889, 19190131.