Hypoxic regulation of mesenchymal stem cell migration: The role of RhoA and HIF-1α

Cell Biology International

Volumn 35, Issue 10, 2011, Pages 981-989

  Raheja, Leah F ^a   Genetos, Damian C ^a   Wong, Alice ^a   Yellowley, Clare E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

GTPase; Hypoxia; Hypoxia inducible factor 1 (HIF 1 ); Mesenchymal stem cell (MSC); Oxygen; RhoA

Indexed keywords

GUANOSINE TRIPHOSPHATE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ADULT; ARTICLE; CELL HYPOXIA; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MALE; MESENCHYMAL STEM CELL; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM;

ACTIN CYTOSKELETON; ADOLESCENT; BONE MARROW CELLS; CELL HYPOXIA; CELL MOVEMENT; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MESENCHYMAL STEM CELLS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 80053577540     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1042/CBI20100733     Document Type: Article

References (44)

1. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-22.
2. Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, Champagne M et al. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells 2003;21:337-47.
3. Ardyanto TD, Osaki M, Nagahama Y, Yamaga K, Maeta N, Tamura T et al. Down-regulation of cobalt-induced HIF-1alpha expression correlates with cell proliferation and apoptosis in human gastric carcinoma cells. Oncol Rep 2008;19:339-43.
4. Awad HA, Butler DL, Boivin GP, Smith FN, Malaviya P, Huibregtse B et al. Autologous mesenchymal stem cell-mediated repair of tendon. Tissue Eng 1999;5:267-77.
5. Awad HA, Butler DL, Harris MT, Ibrahim RE, Wu Y, Young RG et al. In vitro characterization of mesenchymal stem cell-seeded collagen scaffolds for tendon repair: effects of initial seeding density on contraction kinetics. J Biomed Mater Res 2000;51:233-40.
6. Bennett MH, Stanford R, Turner R. Hyperbaric oxygen therapy for promoting fracture healing and treating fracture non-union. Cochrane Database Syst Rev 2005;1:CD004712.
7. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 1998;80:985-96.
8. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991;9:641-50.
9. Ellenbroek SI, Collard JG. Rho GTPases: functions and association with cancer. Clin Exp Metastasis 2007;24:657-72.
10. Fukata M, Nakagawa M, Kaibuchi K. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 2003;15:590-7.
11. Grande DA, Southerland SS, Manji R, Pate DW, Schwartz RE, Lucas PA. Repair of articular cartilage defects using mesenchymal stem cells. Tissue Eng 1995;1:345-53.
12. Grimshaw MJ, Balkwill FR. Inhibition of monocyte and macrophage chemotaxis by hypoxia and inflammation - a potential mechanism. Eur J Immunol 2001;31:480-9.
13. Hayashi M, Sakata M, Takeda T, Tahara M, Yamamoto T, Minekawa R et al. Hypoxia up-regulates hypoxia-inducible factor-1alpha expression through RhoA activation in trophoblast cells. J Clin Endocrinol Metab 2005;90:1712-9.
14. Heppenstall RB, Grislis G, Hunt TK. Tissue gas tensions and oxygen consumption in healing bone defects. Clin Orthop Relat Res 1975;106:357-65.
15. Jaganathan BG, Ruester B, Dressel L, Stein S, Grez M, Seifried E et al. Rho inhibition induces migration of mesenchymal stromal cells. Stem Cells 2007;25:1966-74.
16. Jin HG, Yamashita H, Nagano Y, Fukuba H, Hiji M, Ohtsuki T et al. Hypoxia-induced upregulation of endothelial small G protein RhoA and Rho-kinase/ROCK2 inhibits eNOS expression. Neurosci Lett 2006;408:62-7.
17. Lash GE, Hornbuckle J, Brunt A, Kirkley M, Searle RF, Robson SC et al. Effect of low oxygen concentrations on trophoblast-like cell line invasion. Placenta 2007;28:390-8.
18. Le Blanc K. Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy 2003;5:485-9.
19. Lee MJ, Jeon ES, Lee JS, Cho M, Suh DS, Chang CL et al. Lysophosphatidic acid in malignant ascites stimulates migration of human mesenchymal stem cells. J Cell Biochem 2008;104:499-510.
20. Mizutani T, Kawabata K, Koyama Y, Takahashi M, Haga H. Regulation of cellular contractile force in response to mechanical stretch by diphosphorylation of myosin regulatory light chain via RhoA signaling cascade. Cell Motil Cytoskeleton 2009;66:389-97.
21. Narumiya S, Tanji M, Ishizaki T. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 2009;28:65-76.
22. Negash S, Narasimhan SR, Zhou W, Liu J, Wei FL, Tian J et al. Role of cGMP-dependent protein kinase in regulation of pulmonary vascular smooth muscle cell adhesion and migration:effect of hypoxia. Am J Physiol Heart Circ Physiol 2009;297:H304-12.
23. Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995;81:53-62.
24. O9Toole EA, Marinkovich MP, Peavey CL, Amieva MR, Furthmayr H, Mustoe TA et al. Hypoxia increases human keratinocyte motility on connective tissue. J Clin Invest 1997;100:2881-91.
25. Pacary E, Tixier E, Coulet F, Roussel S, Petit E, Bernaudin M. Crosstalk between HIF-1 and ROCK pathways in neuronal differentiation of mesenchymal stem cells, neurospheres and in PC12 neurite outgrowth. Mol Cell Neurosci 2007;35:409-23.
26. Pennathur-Das R, Levitt L. Augmentation of in vitro human marrow erythropoiesis under physiological oxygen tensions is mediated by monocytes and T lymphocytes. Blood 1987;69:899-907.
27. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
28. Qu ZH, Zhang XL, Tang TT, Dai KR. Promotion of osteogenesis through beta-catenin signaling by desferrioxamine. Biochem Biophys Res Commun 2008;370:332-7.
29. Quevedo HC, Hatzistergos KE, Oskouei BN, Feigenbaum GS, Rodriguez JE, Valdes D et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009;106:14022-7.
30. Raheja LF, Genetos DC, Yellowley CE. Hypoxic osteocytes recruit human MSCs through an OPN/CD44-mediated pathway. Biochem Biophys Res Commun 2008;366:1061-6.
31. Raheja LF, Genetos DC, Yellowley CE. The effect of oxygen tension on the long-term osteogenic differentiation and MMP/TIMP expression of human mesenchymal stem cells. Cells Tissues Organs 2010;191:175-84.
32. Rodriguez PG, Felix FN, Woodley DT, Shim EK. The role of oxygen in wound healing: a review of the literature. Dermatol Surg 2008;34:1159-69.
33. Rosova I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008;26:2173-82.
34. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 2008;105:6392-7.
35. Semenza GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007;2007:cm8.
36. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992;12:5447-54.
37. Steinbrech DS, Mehrara BJ, Saadeh PB, Greenwald JA, Spector JA, Gittes GK et al. VEGF expression in an osteoblast-like cell line is regulated by a hypoxia response mechanism. Am J Physiol Cell Physiol 2000;278:C853-60.
38. Turcotte S, Desrosiers RR, Beliveau R. HIF-1alpha mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J Cell Sci 2003;116:2247-60.
39. Turner L, Scotton C, Negus R, Balkwill F. Hypoxia inhibits macrophage migration. Eur J Immunol 1999;29:2280-7.
40. van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ. Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration. Brain Behav Immun 2010;24:387-93.
41. Vega FM, Ridley AJ. Rho GTPases in cancer cell biology. FEBS Lett 2008;582:2093-101.
42. Viault F. Sur l'augmentation considerable du nombres des globules rouge dans le sange chez Les inhabitants des hauts plateux de l9Amerique due Sud. C.R. Acad Sci Paris 1890;111:917-8.
43. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994;76:579-92.
44. Wixler V, Hirner S, Muller JM, Gullotti L, Will C, Kirfel J et al. Deficiency in the LIM-only protein Fhl2 impairs skin wound healing. J Cell Biol 2007;177:163-72.