Frontiers of Medicine

, Volume 5, Issue 1, pp 33–39 | Cite as

Regulatory factors of mesenchymal stem cell migration into injured tissues and their signal transduction mechanisms

Review

Abstract

Adult stem cells hold great promise for wound healing and tissue regeneration. Mesenchymal stem cells (MSCs), for example, have been shown to play a role in tissue repair. Research has shown that endogenous bone marrow MSCs or exogenously delivered MSCs migrate to the sites of injury and participate in the repair process. The precise mechanisms underlying migration of MSCs into the injured tissue are still not fully understood, although multiple signaling pathways and molecules were reported, including both chemoattractive factors and endogenous electric fields at wounds. This review will briefly summarize the regulatory facors and signaling transduction pathways involved in migration of MSCs. A better understanding of the molecular mechanisms involved in the migration of MSCs will help us to develop new stem cell-based therapeutic strategies in regenerative medicine.

Keywords

mesenchymal stem cells migration molecular mechanisms signaling pathway 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Friedenstein A J, Chailakhyan R K, Latsinik N V, Panasyuk A F, Keiliss-Borok I V. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation, 1974, 17(4): 331–340PubMedCrossRefGoogle Scholar
  2. 2.
    Ortiz L A, Dutreil M, Fattman C, Pandey A C, Torres G, Go K, Phinney D G. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA, 2007, 104(26): 11002–11007PubMedCrossRefGoogle Scholar
  3. 3.
    Ohnishi S, Yanagawa B, Tanaka K, Miyahara Y, Obata H, Kataoka M, Kodama M, Ishibashi-Ueda H, Kangawa K, Kitamura S, Nagaya N. Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Mol Cell Cardiol, 2007, 42(1): 88–97PubMedCrossRefGoogle Scholar
  4. 4.
    Shake J G, Gruber P J, Baumgartner WA, Senechal G, Meyers J, Redmond J M, Pittenger M F, Martin B J. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg. 2002; 73(6): 1919–1926PubMedCrossRefGoogle Scholar
  5. 5.
    Zohlnhöfer D, Dibra A, Koppara T, deWaha A, Ripa R S, Kastrup J, Valgimigli M, Schömig A, Kastrati A. Stem cell mobilization by granulocyte colony-stimulating factor for myocardial recovery after acute myocardial infarction: a meta-analysis. J Am Coll Cardiol, 2008, 51(15): 1429–1437PubMedCrossRefGoogle Scholar
  6. 6.
    Patschan D, Plotkin M, Goligorsky M S. Therapeutic use of stem and endothelial progenitor cells in acute renal injury: ça ira. Curr Opin Pharmacol, 2006, 6(2): 176–183PubMedCrossRefGoogle Scholar
  7. 7.
    Liang L, Ma T, Chen W, Hu J, Bai X, Li J, Liang T. Therapeutic potential and related signal pathway of adipose-derived stem cell transplantation for rat liver injury. Hepatol Res, 2009, 39(8): 822–832PubMedCrossRefGoogle Scholar
  8. 8.
    Németh K, Leelahavanichkul A, Yuen P S, Mayer B, Parmelee A, Doi K, Robey P G, Leelahavanichkul K, Koller B H, Brown JM, Hu X, Jelinek I, Star R A, Mezey E. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med, 2009, 15(1): 42–49PubMedCrossRefGoogle Scholar
  9. 9.
    Chapel A, Bertho J M, Bensidhoum M, Fouillard L, Young R G, Frick J, Demarquay C, Cuvelier F, Mathieu E, Trompier F, Dudoignon N, Germain C, Mazurier C, Aigueperse J, Borneman J, Gorin N C, Gourmelon P, Thierry D. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med, 2003, 5(12): 1028–1038PubMedCrossRefGoogle Scholar
  10. 10.
    Ortiz L A, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney D G. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA, 2003, 100(14): 8407–8411PubMedCrossRefGoogle Scholar
  11. 11.
    Moser B, Willimann K. Chemokines: role in inflammation and immune surveillance. Ann Rheum Dis, 2004, 63(Suppl 2): ii84–ii89PubMedCrossRefGoogle Scholar
  12. 12.
    Li Y, Yu X, Lin S, Li X, Zhang S, Song Y H. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun, 2007, 356(3): 780–784PubMedCrossRefGoogle Scholar
  13. 13.
    Ji J F, He B P, Dheen S T, Tay S S. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells, 2004, 22(3): 415–427PubMedCrossRefGoogle Scholar
  14. 14.
    Ryu C H, Park S A, Kim S M, Lim J Y, Jeong C H, Jun J A, Oh J H, Park S H, Oh W I, Jeun S S. Migration of human umbilical cord blood mesenchymal stem cells mediated by stromal cell-derived factor-1/CXCR4 axis via Akt, ERK, and p38 signal transduction pathways. Biochem Biophys Res Commun, 2010, 398(1): 105–110PubMedCrossRefGoogle Scholar
  15. 15.
    Wynn R F, Hart C A, Corradi-Perini C, O’Neill L, Evans C A, Wraith J E, Fairbairn L J, 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): 2643–2645PubMedCrossRefGoogle Scholar
  16. 16.
    Son B R, Marquez-Curtis L A, Kucia M, Wysoczynski M, Turner A R, Ratajczak J, Ratajczak M Z, Janowska-Wieczorek A. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells, 2006, 24(5): 1254–1264PubMedCrossRefGoogle Scholar
  17. 17.
    Tsai L K, Leng Y, Wang Z, Leeds P, Chuang D M. The mood stabilizers valproic acid and lithium enhance mesenchymal stem cell migration via distinct mechanisms. Neuropsychopharmacology, 2010, 35(11): 2225–2237PubMedCrossRefGoogle Scholar
  18. 18.
    Ip J E, Wu Y, Huang J, Zhang L, Pratt R E, Dzau V J. Mesenchymal stem cells use integrin beta1 not CXC chemokine receptor 4 for myocardial migration and engraftment. Mol Biol Cell, 2007, 18(8): 2873–2882PubMedCrossRefGoogle Scholar
  19. 19.
    Sordi V, Malosio M L, Marchesi F, Mercalli A, Melzi R, Giordano T, Belmonte N, Ferrari G, Leone B E, 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): 419–427PubMedCrossRefGoogle Scholar
  20. 20.
    Phinney D G, Prockop D J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views. Stem Cells, 2007, 25(11): 2896–2902PubMedCrossRefGoogle Scholar
  21. 21.
    Rüster B, Göttig S, Ludwig R J, Bistrian R, Müller S, Seifried E, Gille J, Henschler R. Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood, 2006, 108(12): 3938–3944PubMedCrossRefGoogle Scholar
  22. 22.
    Sackstein R, Merzaban J S, Cain DW, Dagia NM, Spencer J A, Lin C P, Wohlgemuth R. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med, 2008, 14(2): 181–187PubMedCrossRefGoogle Scholar
  23. 23.
    Jeon E S, Song H Y, Kim MR, Moon H J, Bae Y C, Jung J S, Kim J H. Sphingosylphosphorylcholine induces proliferation of human adipose tissue-derived mesenchymal stem cells via activation of JNK. J Lipid Res, 2006, 47(3): 653–664PubMedCrossRefGoogle Scholar
  24. 24.
    Song H Y, Lee MJ, Kim MY, Kim K H, Lee I H, Shin S H, Lee J S, Kim J H. Lysophosphatidic acid mediates migration of human mesenchymal stem cells stimulated by synovial fluid of patients with rheumatoid arthritis. Biochim Biophys Acta, 2010, 1801(1): 23–30PubMedGoogle Scholar
  25. 25.
    Song H Y, Lee MJ, Kim MY, Kim K H, Lee I H, Shin S H, Lee J S, Kim J H. Lysophosphatidic acid mediates migration of human mesenchymal stem cells stimulated by synovial fluid of patients with rheumatoid arthritis. Biochim Biophys Acta, 2010, 1801(1): 23–30PubMedGoogle Scholar
  26. 26.
    Jaganathan B G, Ruester B, Dressel L, Stein S, Grez M, Seifried E, Henschler R. Rho inhibition induces migration of mesenchymal stromal cells. Stem Cells, 2007, 25(8): 1966–1974PubMedCrossRefGoogle Scholar
  27. 27.
    Fu X, Han B, Cai S, Lei Y, Sun T, Sheng Z. Migration of bone marrow-derived mesenchymal stem cells induced by tumor necrosis factor-alpha and its possible role in wound healing. Wound Repair Regen, 2009, 17(2): 185–191PubMedCrossRefGoogle Scholar
  28. 28.
    Hemeda H, Jakob M, Ludwig A K, Giebel B, Lang S, Brandau S. Interferon-gamma and tumor necrosis factor-alpha differentially affect cytokine expression and migration properties of mesenchymal stem cells. Stem Cells Dev, 2010, 19(5): 693–706PubMedCrossRefGoogle Scholar
  29. 29.
    Zhang A, Wang Y, Ye Z, Xie H, Zhou L, Zheng S. Mechanism of TNF-α-induced migration and hepatocyte growth factor production in human mesenchymal stem cells. J Cell Biochem, 2010, 111(2): 469–475PubMedCrossRefGoogle Scholar
  30. 30.
    Fischer-Valuck B W, Barrilleaux B L, Phinney D G, Russell K C, Prockop D J, O’Connor K C. Migratory response of mesenchymal stem cells to macrophage migration inhibitory factor and its antagonist as a function of colony-forming efficiency. Biotechnol Lett, 2010, 32(1): 19–27PubMedCrossRefGoogle Scholar
  31. 31.
    Meng E, Guo Z, Wang H, Jin J, Wang J, Wang H, Wu C, Wang L. High mobility group box 1 protein inhibits the proliferation of human mesenchymal stem cells and promotes their migration and differentiation along osteoblastic pathway. Stem Cells Dev, 2008, 17(4): 805–813PubMedCrossRefGoogle Scholar
  32. 32.
    Wang L, Li Y, Chen X, Chen J, Gautam S C, Xu Y, Chopp M. MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology, 2002, 7(2): 113–117PubMedCrossRefGoogle Scholar
  33. 33.
    Wang L, Li Y, Chen J, Gautam S C, Zhang Z, Lu M, Chopp M. Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Exp Hematol, 2002, 30(7): 831–836PubMedCrossRefGoogle Scholar
  34. 34.
    Dwyer R M, Potter-Beirne S M, Harrington K A, Lowery A J, Hennessy E, Murphy J M, Barry F P, O’Brien T, Kerin M J. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res, 2007, 13(17): 5020–5027PubMedCrossRefGoogle Scholar
  35. 35.
    Xu F, Shi J, Yu B, Ni W, Wu X, Gu Z. Chemokines mediate mesenchymal stem cell migration toward gliomas in vitro. Oncol Rep, 2010, 23(6): 1561–1567PubMedGoogle Scholar
  36. 36.
    Picinich S C, Glod J W, Banerjee D. Protein kinase C zeta regulates interleukin-8-mediated stromal-derived factor-1 expression and migration of human mesenchymal stromal cells. Exp Cell Res, 2010, 316(4): 593–602PubMedCrossRefGoogle Scholar
  37. 37.
    Ponte A L, Marais E, Gallay N, Langonné A, Delorme B, Hérault O, Charbord P, Domenech J. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells, 2007, 25(7): 1737–1745PubMedCrossRefGoogle Scholar
  38. 38.
    Forte G, Minieri M, Cossa P, Antenucci D, Sala M, Gnocchi V, Fiaccavento R, Carotenuto F, De Vito P, Baldini P M, Prat M, Di Nardo P. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells, 2006, 24(1): 23–33PubMedCrossRefGoogle Scholar
  39. 39.
    Fiedler J, Röderer G, Günther K P, Brenner R E. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J Cell Biochem, 2002, 87(3): 305–312PubMedCrossRefGoogle Scholar
  40. 40.
    Fiedler J, Brill C, Blum W F, Brenner R E. IGF-I and IGF-II stimulate directed cell migration of bone-marrow-derived human mesenchymal progenitor cells. Biochem Biophys Res Commun, 2006, 345(3): 1177–1183PubMedCrossRefGoogle Scholar
  41. 41.
    Tamama K, Fan V H, Griffith L G, Blair H C, Wells A. Epidermal growth factor as a candidate for ex vivo expansion of bone marrowderived mesenchymal stem cells. Stem Cells, 2006, 24(3): 686–695PubMedCrossRefGoogle Scholar
  42. 42.
    Kollet O, Shivtiel S, Chen Y Q, Suriawinata J, Thung S N, Dabeva M D, Kahn J, Spiegel A, Dar A, Samira S, Goichberg P, Kalinkovich A, Arenzana-Seisdedos F, Nagler A, Hardan I, Revel M, Shafritz D A, Lapidot T. HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34 + stem cell recruitment to the liver. J Clin Invest, 2003, 112(2): 160–169PubMedGoogle Scholar
  43. 43.
    Jankowski K, Kucia M, Wysoczynski M, Reca R, Zhao D, Trzyna E, Trent J, Peiper S, Zembala M, Ratajczak J, Houghton P, Janowska-Wieczorek A, Ratajczak M Z. 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, 2003, 63(22): 7926–7935PubMedGoogle Scholar
  44. 44.
    Demetri G D, Griffin J D. Granulocyte colony-stimulating factor and its receptor. Blood, 1991, 78(11): 2791–2808PubMedGoogle Scholar
  45. 45.
    Yanqing Z, Yu-Min L, Jian Q, Bao-Guo X, Chuan-Zhen L. Fibronectin and neuroprotective effect of granulocyte colonystimulating factor in focal cerebral ischemia. Brain Res, 2006, 1098(1): 161–169PubMedCrossRefGoogle Scholar
  46. 46.
    Shyu W C, Lin S Z, Yang H I, Tzeng Y S, Pang C Y, Yen P S, Li H. Functional recovery of stroke rats induced by granulocyte colonystimulating factor-stimulated stem cells. Circulation, 2004, 110(13): 1847–1854PubMedCrossRefGoogle Scholar
  47. 47.
    Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine D M, Leri A, Anversa P. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci USA, 2001, 98(18): 10344–10349PubMedCrossRefGoogle Scholar
  48. 48.
    Watari K, Asano S, Shirafuji N, Kodo H, Ozawa K, Takaku F, Kamachi S. Serum granulocyte colony-stimulating factor levels in healthy volunteers and patients with various disorders as estimated by enzyme immunoassay. Blood, 1989, 73(1): 117–122PubMedGoogle Scholar
  49. 49.
    Zhao M, Song B, Pu J, Wada T, Reid B, Tai G, Wang F, Guo A, Walczysko P, Gu Y, Sasaki T, Suzuki A, Forrester J V, Bourne H R, Devreotes P N, McCaig C D, Penninger J M. Electrical signals control wound healing through phosphatidylinositol-3-OH kinasegamma and PTEN. Nature, 2006, 442(7101): 457–460PubMedCrossRefGoogle Scholar
  50. 50.
    Zhao M. Electrical fields in wound healing-An overriding signal that directs cell migration. Semin Cell Dev Biol, 2009, 20(6): 674–682PubMedCrossRefGoogle Scholar
  51. 51.
    Nuccitelli R. A role for endogenous electric fields in wound healing. Curr Top Dev Biol, 2003, 58: 1–26PubMedCrossRefGoogle Scholar
  52. 52.
    Reid B, Song B, McCaig C D, Zhao M. Wound healing in rat cornea: the role of electric currents. FASEB J, 2005, 19(3): 379–386PubMedCrossRefGoogle Scholar
  53. 53.
    Song B, Zhao M, Forrester J V, McCaig C D. Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proc Natl Acad Sci USA, 2002, 99(21): 13577–13582PubMedCrossRefGoogle Scholar
  54. 54.
    Hammerick K E, Longaker M T, Prinz F B. In vitro effects of direct current electric fields on adipose-derived stromal cells. Biochem Biophys Res Commun, 2010, 397(1): 12–17PubMedCrossRefGoogle Scholar
  55. 55.
    Sun S, Titushkin I, Cho M. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry, 2006, 69(2): 133–141PubMedCrossRefGoogle Scholar
  56. 56.
    Tandon N, Goh B, Marsano A, Chao PH, Montouri-Sorrentino C, Gimble J, Vunjak-Novakovic G. Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation. Conf Proc IEEE Eng Med Biol Soc. 2009; 2009: 6517–6521.PubMedGoogle Scholar
  57. 57.
    Zhao M. Electrical fields in wound healing-An overriding signal that directs cell migration. Semin Cell Dev Biol, 2009, 20(6): 674–682PubMedCrossRefGoogle Scholar
  58. 58.
    Zha Y H, He J F, Mei Y W, Yin T, Mao L. Zinc-finger transcription factor snail accelerates survival, migration and expression of matrix metalloproteinase-2 in human bone mesenchymal stem cells. Cell Biol Int, 2007, 31(10): 1089–1096PubMedCrossRefGoogle Scholar
  59. 59.
    Schmidt A, Ladage D, Schinköthe T, Klausmann U, Ulrichs C, Klinz F J, Brixius K, Arnhold S, Desai B, Mehlhorn U, Schwinger R H, Staib P, Addicks K, Bloch W. Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells, 2006, 24(7): 1750–1758PubMedCrossRefGoogle Scholar
  60. 60.
    Zhao M, Agius-Fernandez A, Forrester J V, McCaig C D. Directed migration of corneal epithelial sheets in physiological electric fields. Invest Ophthalmol Vis Sci, 1996, 37(13): 2548–2558PubMedGoogle Scholar
  61. 61.
    Farboud B, Nuccitelli R, Schwab I R, Isseroff R R. DC electric fields induce rapid directional migration in cultured human corneal epithelial cells. Exp Eye Res, 2000, 70(5): 667–673PubMedCrossRefGoogle Scholar
  62. 62.
    Wang E, Zhao M, Forrester J V, MCCaig C D. Re-orientation and faster, directed migration of lens epithelial cells in a physiological electric field. Exp Eye Res, 2000, 71(1): 91–98PubMedCrossRefGoogle Scholar
  63. 63.
    Pu J, McCaig C D, Cao L, Zhao Z, Segall J E, Zhao M. EGF receptor signalling is essential for electric-field-directed migration of breast cancer cells. J Cell Sci, 2007, 120(Pt 19): 3395–3403PubMedCrossRefGoogle Scholar
  64. 64.
    Yun D H, Song H Y, Lee M J, Kim M R, Kim M Y, Lee J S, Kim J H. Thromboxane A(2) modulates migration, proliferation, and differentiation of adipose tissue-derived mesenchymal stem cells. Exp Mol Med, 2009, 41(1): 17–24PubMedCrossRefGoogle Scholar
  65. 65.
    Li S, Deng Y, Feng J, Ye W. Oxidative preconditioning promotes bone marrow mesenchymal stem cells migration and prevents apoptosis. Cell Biol Int, 2009, 33(3): 411–418PubMedCrossRefGoogle Scholar
  66. 66.
    Kang Y J, Jeon E S, Song H Y, Woo J S, Jung J S, Kim Y K, Kim J H. Role of c-Jun N-terminal kinase in the PDGF-induced proliferation and migration of human adipose tissue-derived mesenchymal stem cells. J Cell Biochem, 2005, 95(6): 1135–1145PubMedCrossRefGoogle Scholar
  67. 67.
    Gu Y, Filippi M D, Cancelas J A, Siefring J E, Williams E P, Jasti A C, Harris C E, Lee AW, Prabhakar R, Atkinson S J, Kwiatkowski D J, Williams D A. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science, 2003, 302(5644): 445–449PubMedCrossRefGoogle Scholar
  68. 68.
    Lee M J, Jeon E S, Lee J S, Cho M, Suh D S, Chang C L, Kim J H. Lysophosphatidic acid in malignant ascites stimulates migration of human mesenchymal stem cells. J Cell Biochem, 2008, 104(2): 499–510PubMedCrossRefGoogle Scholar
  69. 69.
    Pinto D, Clevers H. Wnt, stem cells and cancer in the intestine. Biol Cell, 2005, 97(3): 185–196PubMedCrossRefGoogle Scholar
  70. 70.
    Qiang Y W, Walsh K, Yao L, Kedei N, Blumberg P M, Rubin J S, Shaughnessy J Jr, Rudikoff S. Wnts induce migration and invasion of myeloma plasma cells. Blood, 2005, 106(5): 1786–1793PubMedCrossRefGoogle Scholar
  71. 71.
    Shang Y C, Wang S H, Xiong F, Zhao C P, Peng F N, Feng S W, Li M S, Li Y, Zhang C. Wnt3a signaling promotes proliferation, myogenic differentiation, and migration of rat bone marrow mesenchymal stem cells. Acta Pharmacol Sin, 2007, 28(11): 1761–1774PubMedCrossRefGoogle Scholar
  72. 72.
    Karp J M, Leng Teo G S. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell, 2009, 4(3): 206–216PubMedCrossRefGoogle Scholar
  73. 73.
    Barrilleaux B L, Fischer-Valuck B W, Gilliam J K, Phinney D G, O’Connor K C. Activation of CD74 inhibits migration of human mesenchymal stem cells. In Vitro Cell Dev Biol Anim, 2010, 46(6): 566–572PubMedCrossRefGoogle Scholar
  74. 74.
    De Becker A, Van Hummelen P, Bakkus M, Vande Broek I, De Wever J, De Waele M, Van Riet I. Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica, 2007, 92(4): 440–449PubMedCrossRefGoogle Scholar
  75. 75.
    Rombouts WJ, Ploemacher R E. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia, 2003, 17(1): 160–170PubMedCrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.State Key Laboratory of Trauma, Burns and Combined Injury, Institute of Surgery Research, Daping HospitalThird Military Medical UniversityChongqingChina

Personalised recommendations