Intracellular trafficking and endocytosis of CXCR4 in fetal mesenchymal stem/stromal cells

BMC Cell Biology

Volumn 15, Issue 1, 2014, Pages

  Pelekanos, Rebecca A ^a   Ting, Michael J ^a   Sardesai, Varda S ^a   Ryan, Jennifer M ^a   Lim, Yaw Chyn ^b   Chan, Jerry K Y ^a,b,c   Fisk, Nicholas M ^a,b,d  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^d ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Bone marrow; Chemokine receptor; CXCR4; Endocytosis; Fetal mesenchymal stromal cells; Migration; MSC; Small molecule

Indexed keywords

BLEBBISTATIN; CHEMOKINE RECEPTOR CXCR4; STROMAL CELL DERIVED FACTOR 1;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; ENDOCYTOSIS; FETUS; FETUS CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; MESENCHYMAL STROMA CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TRANSCELLULAR CELL MIGRATION; BONE MARROW CELL; CELL CULTURE; CELL MOTION; CELL NUCLEUS; CYTOLOGY; ENDOSOME; FEMALE; LYSOSOME; METABOLISM;

BONE MARROW CELLS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL NUCLEUS; CELLS, CULTURED; ENDOCYTOSIS; ENDOSOMES; FEMALE; FETUS; HUMANS; LYSOSOMES; MESENCHYMAL STROMAL CELLS; PROTEIN TRANSPORT; RECEPTORS, CXCR4;

EID: 84903401891     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-15-15     Document Type: Article

References (65)

1. Guillot PV, Gotherstrom C, Chan J, Kurata H, Fisk NM. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007, 25(3):646-654.
2. World's first cell race no small affair Updated [http://blogs.nature.com/news/2011/12/worlds_first_cell_race_no_smal.html].
3. Ramirez M, Lucia A, Gomez-Gallego F, Esteve-Lanao J, Perez-Martinez A, Foster C, Andreu AL, Martin MA, Madero L, Arenas J, García-Castro J. Mobilisation of mesenchymal cells into blood in response to skeletal muscle injury. Br J Sports Med 2006, 40(8):719-722. 10.1136/bjsm.2006.028639, 2579469, 16807304.
4. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat. J Neurosci Res 2006, 84(7):1495-1504. 10.1002/jnr.21056, 2605367, 16998918.
5. Hauger O, Frost EE, van Heeswijk R, Deminiere C, Xue R, Delmas Y, Combe C, Moonen CT, Grenier N, Bulte JW. MR evaluation of the glomerular homing of magnetically labeled mesenchymal stem cells in a rat model of nephropathy. Radiology 2006, 238(1):200-210. 10.1148/radiol.2381041668, 16373768.
6. Guillot PV, Abass O, Bassett JH, Shefelbine SJ, Bou-Gharios G, Chan J, Kurata H, Williams GR, Polak J, Fisk NM. Intrauterine transplantation of human fetal mesenchymal stem cells from first-trimester blood repairs bone and reduces fractures in osteogenesis imperfecta mice. Blood 2008, 111(3):1717-1725.
7. Guillot PV, Cook HT, Pusey CD, Fisk NM, Harten S, Moss J, Shore I, Bou-Gharios G. Transplantation of human fetal mesenchymal stem cells improves glomerulopathy in a collagen type I alpha 2-deficient mouse. J Pathol 2008, 214(5):627-636. 10.1002/path.2325, 18266309.
8. O'Donoghue K, Sultan HA, Al-Allaf FA, Anderson JR, Wyatt-Ashmead J, Fisk NM. Microchimeric fetal cells cluster at sites of tissue injury in lung decades after pregnancy. Reprod Biomed Online 2008, 16(3):382-390. 10.1016/S1472-6483(10)60600-1, 18339261.
9. Marquez-Curtis LA, Gul-Uludag H, Xu P, Chen J, Janowska-Wieczorek A. CXCR4 transfection of cord blood mesenchymal stromal cells with the use of cationic liposome enhances their migration toward stromal cell-derived factor-1. Cytotherapy 2013, 15(7):840-849. 10.1016/j.jcyt.2013.02.009, 23623275.
10. Fernandis AZ, Cherla RP, Ganju RK. Differential regulation of CXCR4-mediated T-cell chemotaxis and mitogen-activated protein kinase activation by the membrane tyrosine phosphatase, CD45. J Biol Chem 2003, 278(11):9536-9543. 10.1074/jbc.M211803200, 12519755.
11. Ehlin-Henriksson B, Liang W, Cagigi A, Mowafi F, Klein G, Nilsson A. Changes in chemokines and chemokine receptor expression on tonsillar B cells upon Epstein-Barr virus infection. Immunology 2009, 127(4):549-557. 10.1111/j.1365-2567.2008.03029.x, 2729532, 19604305.
12. O'Hayre M, Salanga CL, Kipps TJ, Messmer D, Dorrestein PC, Handel TM. Elucidating the CXCL12/CXCR4 signaling network in chronic lymphocytic leukemia through phosphoproteomics analysis. PLoS One 2010, 5(7):e11716. 10.1371/journal.pone.0011716, 2908618, 20661426.
13. Saur D, Seidler B, Schneider G, Algul H, Beck R, Senekowitsch-Schmidtke R, Schwaiger M, Schmid RM. CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer. Gastroenterology 2005, 129(4):1237-1250. 10.1053/j.gastro.2005.06.056, 16230077.
14. Wynn RF, Hart CA, Corradi-Perini C, O'Neill L, Evans CA, Wraith JE, Fairbairn LJ, Bellantuono I. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 2004, 104(9):2643-2645. 10.1182/blood-2004-02-0526, 15251986.
15. Zhang D, Fan GC, Zhou X, Zhao T, Pasha Z, Xu M, Zhu Y, Ashraf M, Wang Y. Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J Mol Cell Cardiol 2008, 44(2):281-292. 10.1016/j.yjmcc.2007.11.010, 2601571, 18201717.
16. Schioppa T, Uranchimeg B, Saccani A, Biswas S, 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(9):1391-1402. 10.1084/jem.20030267, 2194248, 14597738.
17. Shi M, Li J, Liao L, Chen B, Li B, Chen L, Jia H, Zhao RC. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica 2007, 92(7):897-904. 10.3324/haematol.10669, 17606439.
18. Jones GN, Moschidou D, Lay K, Abdulrazzak H, Vanleene M, Shefelbine SJ, Polak J, de Coppi P, Fisk NM, Guillot PV. Upregulating CXCR4 in human fetal mesenchymal stem cells enhances engraftment and bone mechanics in a mouse model of osteogenesis imperfecta. Stem Cells Transl Med 2012, 1(1):70-78. 10.5966/sctm.2011-0007, 3727689, 23197643.
19. Rose JJ, Foley JF, Murphy PM, Venkatesan S. On the mechanism and significance of ligand-induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2. J Biol Chem 2004, 279(23):24372-24386. 10.1074/jbc.M401364200, 15028716.
20. Su Y, Raghuwanshi SK, Yu Y, Nanney LB, Richardson RM, Richmond A. Altered CXCR2 signaling in beta-arrestin-2-deficient mouse models. J Immunol 2005, 175(8):5396-5402. 10.4049/jimmunol.175.8.5396, 2668249, 16210646.
21. Zhang Y, Foudi A, Geay J, Berthebaud M, Buet D, Jarrier P, Jalil A, Vainchenker W, Louachea F. Intracellular Localization and Constitutive Endocytosis of CXCR4 in Human CD34+ Hematopoietic Progenitor Cells. Stem Cells 2004, 22:1015-1029. 10.1634/stemcells.22-6-1015, 15536192.
22. Kollet O, Petit I, Kahn J, Samira S, Dar A, Peled A, Deutsch V, Gunetti M, Piacibello W, Nagler A, Lapidot T. Human CD34 (+) CXCR4 (-) sorted cells harbor intracellular CXCR4, which can be functionally expressed and provide NOD/SCID repopulation. Blood 2002, 100(8):2778-2786. 10.1182/blood-2002-02-0564, 12351385.
23. Kim SW, Kim HY, Song IC, Jin SA, Lee HJ, Yun HJ, Kim S, Jo DY. Cytoplasmic trapping of CXCR4 in hepatocellular carcinoma cell lines. Cancer Res Treat 2008, 40(2):53-61. 10.4143/crt.2008.40.2.53, 2697487, 19688049.
24. Ding Z, Issekutz TB, Downey GP, Waddell TK. L-selectin stimulation enhances functional expression of surface CXCR4 in lymphocytes: implications for cellular activation during adhesion and migration. Blood 2003, 101(11):4245-4252. 10.1182/blood-2002-06-1782, 12609846.
25. Goichberg P, Kalinkovich A, Borodovsky N, Tesio M, Petit I, Nagler A, Hardan I, Lapidot T. cAMP-induced PKCzeta activation increases functional CXCR4 expression on human CD34+ hematopoietic progenitors. Blood 2006, 107(3):870-879.
26. Barlow S, Brooke G, Chatterjee K, Price G, Pelekanos R, Rossetti T, Doody M, Venter D, Pain S, Gilshenan K, Atkinson K. Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev 2008, 17(6):1095-1107. 10.1089/scd.2007.0154, 19006451.
27. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001, 98(8):2396-2402. 10.1182/blood.V98.8.2396, 11588036.
28. Chen Y-S, Pelekanos RA, Ellis RL, Horne R, Wolvetang EJ, Fisk NM. Small molecule mesengenic nduction of human induced pluripotent stem cells to generate mesenchymal stem/stromal cells. Stem Cells Transl Med 2012, 1(2):83-95. 10.5966/sctm.2011-0022, 3659681, 23197756.
29. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells: the International Society for Cellular Therapy position statement. Cytotherapy 2006, 8(4):315-317. 10.1080/14653240600855905, 16923606.
30. Brooke G, Tong H, Levesque JP, Atkinson K. Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev 2008, 17(5):929-940. 10.1089/scd.2007.0156, 18564033.
31. Gupta SK, Pillarisetti K, Lysko PG. Modulation of CXCR4 expression and SDF-1alpha functional activity during differentiation of human monocytes and macrophages. J Leukoc Biol 1999, 66(1):135-143.
32. Sloane AJ, Raso V, Dimitrov DS, Xiao X, Deo S, Muljadi N, Restuccia D, Turville S, Kearney C, Broder CC, Zoellner H, Cunningham AL, Bendall L, Lynch GW. Marked structural and functional heterogeneity in CXCR4: separation of HIV-1 and SDF-1alpha responses. Immunol Cell Biol 2005, 83(2):129-143. 10.1111/j.1440-1711.2004.01304.x, 15748209.
33. Van Overstraeten-Schlögel NBY, Gothot A. Role of stromal-derived factor-1 in the hematopoietic-supporting activity of human mesenchymal stem cells. Eur J Haematol 2006, 76(6):488-493. 10.1111/j.1600-0609.2006.00633.x, 16494621.
34. Wang HH, Tanaka H, Qin X, Zhao T, Ye LH, Okagaki T, Katayama T, Nakamura A, Ishikawa R, Thatcher SE, Wright GL, Kohama K. Blebbistatin inhibits the chemotaxis of vascular smooth muscle cells by disrupting the myosin II-actin interaction. Am J Physiol Heart Circ Physiol 2008, 294(5):H2060-H2068. 10.1152/ajpheart.00970.2007, 18296570.
35. Liu Z, van Grunsven LA, Van Rossen E, Schroyen B, Timmermans JP, Geerts A, Reynaert H. Blebbistatin inhibits contraction and accelerates migration in mouse hepatic stellate cells. Br J Pharmacol 2010, 159(2):304-315. 10.1111/j.1476-5381.2009.00477.x, 2825352, 20039876.
36. Niggli V, Schmid M, Nievergelt A. Differential roles of Rho-kinase and myosin light chain kinase in regulating shape, adhesion, and migration of HT1080 fibrosarcoma cells. Biochem Biophys Res Commun 2006, 343(2):602-608. 10.1016/j.bbrc.2006.03.022, 16554034.
37. Munevar S, Wang YL, Dembo M. Distinct roles of frontal and rear cell-substrate adhesions in fibroblast migration. Mol Biol Cell 2001, 12(12):3947-3954. 10.1091/mbc.12.12.3947, 60767, 11739792.
38. Zhu B, Xu D, Deng X, Chen Q, Huang Y, Peng H, Li Y, Jia B, Thoreson WB, Ding W, Ding J, Zhao L, Wang Y, Wavrin KL, Duan S, Zheng J. CXCL12 enhances human neural progenitor cell survival through a CXCR7- and CXCR4-mediated endocytotic signaling pathway. Stem Cells 2012, 30(11):2571-2583. 10.1002/stem.1239, 3969741, 22987307.
39. Cheng Z, Ou L, Zhou X, Li F, Jia X, Zhang Y, Liu X, Li Y, Ward CA, Melo LG, Kong D. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol Ther 2008, 16(3):571-579. 10.1038/sj.mt.6300374, 18253156.
40. Zhang M, Rao PV. Blebbistatin, a novel inhibitor of myosin II ATPase activity, increases aqueous humor outflow facility in perfused enucleated porcine eyes. Invest Ophthalmol Vis Sci 2005, 46(11):4130-4138. 10.1167/iovs.05-0164, 16249490.
41. Li Y, Yu X, Lin S, Li X, Zhang S, Song YH. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun 2007, 356(3):780-784. 10.1016/j.bbrc.2007.03.049, 17382293.
42. Hung SC, Pochampally RR, Hsu SC, Sanchez C, Chen SC, Spees J, Prockop DJ. Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One 2007, 2(5):e416. 10.1371/journal.pone.0000416, 1855077, 17476338.
43. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T, Belmonte N, Ferrari G, Leone BE, Bertuzzi F, Zerbini G, Allavena P, Bonifacio E, Piemonti L. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005, 106(2):419-427. 10.1182/blood-2004-09-3507, 15784733.
44. Ryan JM, Pettit AR, Guillot PV, Chan JK, Fisk NM. Unravelling the Pluripotency Paradox in fetal and placental mesenchymal stem cells: Oct-4 expression and the case of the Emperor's new clothes. Stem Cell Rev 2013, 9(4):408-421. 10.1007/s12015-011-9336-5, 22161644.
45. Wang LH, Liu Q, Xu B, Chen W, Yang Q, Wang ZX, Sun YH. Identification of nuclear localization sequence of CXCR4 in renal cell carcinoma by constructing expression plasmids of different deletants. Plasmid 2010, 63(1):68-72. 10.1016/j.plasmid.2009.09.004, 19796655.
46. Speetjens FM, Liefers GJ, Korbee CJ, Mesker WE, van de Velde CJ, van Vlierberghe RL, Morreau H, Tollenaar RA, Kuppen PJ. Nuclear localization of CXCR4 determines prognosis for colorectal cancer patients. Cancer Microenviron 2009, 2(1):1-7. 10.1007/s12307-008-0016-1, 2787924,2787924, 19308676.
47. Wang SC, Lin JK, Wang HS, Yang SH, Li AF, Chang SC. Nuclear expression of CXCR4 is associated with advanced colorectal cancer. Int J Colorectal Dis 2010, 25(10):1185-1191. 10.1007/s00384-010-0999-1, 20607251.
48. Wang L, Wang Z, Yang B, Yang Q, Sun Y. CXCR4 nuclear localization follows binding of its ligand SDF-1 and occurs in metastatic but not primary renal cell carcinoma. Oncol Rep 2009, 22(6):1333-1339.
49. Oda Y, Ohishi Y, Basaki Y, Kobayashi H, Hirakawa T, Wake N, Ono M, Nishio K, Kuwano M, Tsuneyoshi M. Prognostic implications of the nuclear localization of Y-box-binding protein-1 and CXCR4 expression in ovarian cancer: their correlation with activated Akt, LRP/MVP and P-glycoprotein expression. Cancer Sci 2007, 98(7):1020-1026. 10.1111/j.1349-7006.2007.00492.x, 17459055.
50. Fischer T, Nagel F, Jacobs S, Stumm R, Schulz S. Reassessment of CXCR4 chemokine receptor expression in human normal and neoplastic tissues using the novel rabbit monoclonal antibody UMB-2. PLoS One 2008, 3(12):e4069. 10.1371/journal.pone.0004069, 2605258, 19116653.
51. Wegner SA, Ehrenberg PK, Chang G, Dayhoff DE, Sleeker AL, Michael NL. Genomic organization and functional characterization of the chemokine receptor CXCR4, a major entry co-receptor for human immunodeficiency virus type 1. J Biol Chem 1998, 273(8):4754-4760. 10.1074/jbc.273.8.4754, 9468539.
52. Gupta SK, Pillarisetti K. Cutting edge: CXCR4-Lo: molecular cloning and functional expression of a novel human CXCR4 splice variant. J Immunol 1999, 163(5):2368-2372.
53. Carlisle AJ, Lyttle CA, Carlisle RY, Maris JM. CXCR4 expression heterogeneity in neuroblastoma cells due to ligand-independent regulation. Mol Cancer 2009, 8:126. 10.1186/1476-4598-8-126, 2807429, 20028517.
54. Lisignoli G, Cristino S, Piacentini A, Cavallo C, Caplan AI, Facchini A. Hyaluronan-based polymer scaffold modulates the expression of inflammatory and degradative factors in mesenchymal stem cells: Involvement of Cd44 and Cd54. J Cell Physiol 2006, 207(2):364-373. 10.1002/jcp.20572, 16331675.
55. Wu Y, Zhao RC. The role of chemokines in mesenchymal stem cell homing to myocardium. Stem Cell Rev 2012, 8(1):243-250. 10.1007/s12015-011-9293-z, 21706142.
56. Kollar K, Cook MM, Atkinson K, Brooke G. Molecular mechanisms involved in mesenchymal stem cell migration to the site of acute myocardial infarction. Int J Cell Biol 2009, 2009:904682. 2809335, 20130773.
57. Ziarek JJ, Veldkamp CT, Zhang F, Murray NJ, Kartz GA, Liang X, Su J, Baker JE, Linhardt RJ, Volkman BF. Heparin oligosaccharides inhibit chemokine (C-X-C motif) ligand 12 (CXCL12) cardioprotection by binding orthogonal to the dimerization interface, promoting oligomerization, and competing with the chemokine (C-X-C motif) receptor 4 (CXCR4) N terminus. J Biol Chem 2013, 288(1):737-746. 10.1074/jbc.M112.394064, 3537072, 23148226.
58. Munoz LM, Holgado BL, Martinez AC, Rodriguez-Frade JM, Mellado M. Chemokine receptor oligomerization: a further step toward chemokine function. Immunol Lett 2012, 145(1-2):23-29.
59. Munoz LM, Lucas P, Holgado BL, Barroso R, Vega B, Rodriguez-Frade JM, Mellado M. Receptor oligomerization: a pivotal mechanism for regulating chemokine function. Pharmacol Ther 2011, 131(3):351-358. 10.1016/j.pharmthera.2011.05.002, 21600920.
60. Kramp BK, Sarabi A, Koenen RR, Weber C. Heterophilic chemokine receptor interactions in chemokine signaling and biology. Exp Cell Res 2011, 317(5):655-663. 10.1016/j.yexcr.2010.11.014, 21146524.
61. Wang J, Norcross M. Dimerization of chemokine receptors in living cells: key to receptor function and novel targets for therapy. Drug Discov Today 2008, 13(13-14):625-632.
62. Pello OM, Moreno-Ortiz Mdel C, Rodriguez-Frade JM, Martinez-Munoz L, Lucas D, Gomez L, Lucas P, Samper E, Aracil M, Martinez C, Bernad A, Mellado M. SOCS up-regulation mobilizes autologous stem cells through CXCR4 blockade. Blood 2006, 108(12):3928-3937. 10.1182/blood-2006-02-006353, 16912231.
63. Schwartz V, Kruttgen A, Weis J, Weber C, Ostendorf T, Lue H, Bernhagen J. Role for CD74 and CXCR4 in clathrin-dependent endocytosis of the cytokine MIF. Eur J Cell Biol 2012, 91(6-7):435-449.
64. Pelekanos RA, Li J, Gongora M, Chandrakanthan V, Scown J, Suhaimi N, Brooke G, Christensen ME, Doan T, Rice AM, Osborne GW, Grimmond SM, Harvey RP, Atkinson K, Little MH. Comprehensive transcriptome and immunophenotype analysis of renal and cardiac MSC-like populations supports strong congruence with bone marrow MSC despite maintenance of distinct identities. Stem Cell Res 2012, 8(1):58-73. 10.1016/j.scr.2011.08.003, 22099021.
65. Park SA, Ryu CH, Kim SM, Lim JY, Park SI, Jeong CH, Jun JA, Oh JH, Park SH, Oh W, Jeun SS. CXCR4-transfected human umbilical cord blood-derived mesenchymal stem cells exhibit enhanced migratory capacity toward gliomas. Int J Oncol 2011, 38(1):97-103.