Dopamine regulates mobilization of mesenchymal stem cells during wound angiogenesis

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Shome, Saurav ^a   Dasgupta, Partha Sarathi ^a   Basu, Sujit ^b,c,d  

^a CHITTARANJAN NATIONAL CANCER INSTITUTE   (India)

^b OHIO STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; PROTEIN KINASE B; SMALL INTERFERING RNA; VASCULOTROPIN RECEPTOR 2;

ACTIN POLYMERIZATION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DOPAMINE RELEASE; MESENCHYMAL STEM CELL; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PROTEIN PHOSPHORYLATION; SKIN INJURY; STEM CELL MOBILIZATION; SYMPATHETIC NERVE; WOUND HEALING; ADIPOGENESIS; ANIMAL; BONE DEVELOPMENT; BONE MARROW; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DERMIS; DRUG ANTAGONISM; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; INJURY; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ACTINS; ADIPOGENESIS; ANIMALS; BONE MARROW; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; DERMIS; DOPAMINE; DOPAMINE AGENTS; DOPAMINE ANTAGONISTS; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOGENESIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, DOPAMINE D2; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; WOUND HEALING; WOUNDS AND INJURIES;

EID: 84857097116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031682     Document Type: Article

References (60)

1. Tonnesen MG, Feng X, Clark RA, (2000) Angiogenesis in wound healing. J Investig Dermatol Symp Proc 5: 40-46.
2. Eming SA, Brachvogel B, Odorisio T, Koch M, (2007) Regulation of angiogenesis: wound healing as a model. Prog Histochem Cytochem 42: 115-170.
3. Rehman J, Li J, Orschell CM, March KL, (2003) Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107: 1164-1169.
4. Edelberg JM, Tang L, Hattori K, Lyden D, Rafii S, (2002) Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res 90: E89-93.
5. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, et al. (2002) Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106: 2781-2786.
6. Wu Y, Chen L, Scott PG, Tredget EE, (2007) Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 25: 2648-2659.
7. Javazon EH, Keswani SG, Badillo AT, Crombleholme TM, Zoltick PW, et al. (2007) Enhanced epithelial gap closure and increased angiogenesis in wounds of diabetic mice treated with adult murine bone marrow stromal progenitor cells. Wound Repair Regen 15: 350-359.
8. Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D, et al. (2008) Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol 180: 2581-2587.
9. Kasper G, Dankert N, Tuischer J, Hoeft M, Gaber T, (2007) Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells 25: 903-910.
10. Rustad KC, Wong VW, Sorkin M, Glotzbach JP, Major MR, et al. (2012) Enhancement of mesenchymal stem cell angiogenic capacity and stemness by a biomimetic hydrogel scaffold. Biomaterials 33: 80-90.
11. Ding DC, Shyu WC, Lin SZ, (2011) Mesenchymal stem cells. Cell Transplant 20: 5-14.
12. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
13. Hocking AM, Gibran NS, (2010) Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp Cell Res 316: 2213-2219.
14. Karp JM, Leng Teo GS, (2009) Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4: 206-216.
15. Wang CH, Cherng WJ, Yang NI, Kuo LT, Hsu CM, et al. (2008) Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler Thromb Vasc Biol 28: 54-60.
16. He Q, Wan C, Li G, (2007) Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells 25: 69-77.
17. Wu Y, Zhao RC, Tredget EE, (2010) Bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells 28: 905-915.
18. Lau K, Paus R, Tiede S, Day P, Bayat A, (2009) Exploring the role of stem cells in cutaneous wound healing. Exp Dermatol 18: 921-933.
19. Sorrell JM, Caplan AI, (2010) Topical delivery of mesenchymal stem cells and their function in wounds. Stem Cell Res Ther 1: 30.
20. Kaigler D, Krebsbach PH, Polverini PJ, Mooney DJ, (2003) Role of vascular endothelial growth factor in bone marrow stromal cell modulation of endothelial cells. Tissue Eng 9: 95-103.
21. Basu S, Nagy JA, Pal S, Vasile E, Eckelhoefer IA, et al. (2001) The neurotransmitter dopamine inhibits angiogenesis induced by vascular permeability factor/vascular endothelial growth factor. Nat Med 7: 569-574.
22. Sarkar C, Chakroborty D, Mitra RB, Banerjee S, Dasgupta PS, et al. (2004) Dopamine in vivo inhibits VEGF-induced phosphorylation of VEGFR-2, MAPK, and focal adhesion kinase in endothelial cells. Am J Physiol Heart Circ Physiol 287: H1554-H1560.
23. Basu S, Sarkar C, Chakroborty D, Nagy J, Mitra RB, et al. (2004) Ablation of peripheral dopaminergic nerves stimulates malignant tumor growth by inducing vascular permeability factor/vascular endothelial growth factor-mediated angiogenesis. Cancer Res 64: 5551-5555.
24. Chakroborty D, Chowdhury UR, Sarkar C, Baral R, Dasgupta PS, et al. (2008) Dopamine regulates endothelial progenitor cell mobilization from mouse bone marrow in tumor vascularization. J Clin Invest 118: 1380-1389.
25. Shome S, Rana T, Ganguly S, Basu B, Chaki Choudhury S, et al. (2011) Dopamine regulates angiogenesis in normal dermal wound tissues. PLoS ONE 6: e25215.
26. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
27. Forte G, Minieri M, Cossa P, Antenucci D, Sala M, et al. (2006) Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 24: 23-33.
28. Gang EJ, Bosnakovski D, Figueiredo CA, Visser JW, Perlingeiro RC, (2007) SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109: 1743-1751.
29. Shiota M, Heike T, Haruyama M, Baba S, Tsuchiya A, et al. (2007) Isolation and characterization of bone marrow-derived mesenchymal progenitor cells with myogenic and neuronal properties. Exp Cell Res 313: 1008-1023.
30. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
31. Galiano RD, Tepper OM, Pelo CR, Bhatt KA, Callaghan M, et al. (2004) Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 164: 1935-1947.
32. Weis SM, Cheresh DA, (2005) Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437: 497-504.
33. Nissen NN, Polverini PJ, Koch AE, Volin MV, Gamelli RL, et al. (1998) Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 152: 1445-1452.
34. Lee SH, Lee YJ, Song CH, Ahn YK, Han HJ, (2010) Role of FAK phosphorylation in hypoxia-induced hMSCS migration: involvement of VEGF as well as MAPKS and eNOS pathways. Am J Physiol Cell Physiol 298: C847-C856.
35. Liu L, Yu Q, Lin J, Lai X, Cao W, et al. (2011) Hypoxia-inducible factor-1α is essential for hypoxia-induced mesenchymal stem cell mobilization into the peripheral blood. Stem Cells Dev 20: 1961-1971.
36. Fiedler J, Leucht F, Waltenberger J, Dehio C, Brenner RE, (2005) VEGF-A and PlGF-1 stimulate chemotactic migration of human mesenchymal progenitor cells. Biochem Biophys Res Commun 334: 561-568.
37. Busletta C, Novo E, Valfrè Di Bonzo L, Povero D, Paternostro C, et al. (2011) Dissection of the biphasic nature of hypoxia-induced motogenic action in bone marrow-derived human mesenchymal stem cells. Stem Cells 29: 952-963.
38. Seiffert K, (2008) Regualtion of cutaneous immunity by catecholamines. In: Granstein RD, Luger TA, editors. Neuroimmunology of the Skin: Basic Science to Clinical Practice Berlin Springer pp. 65-74.
39. Rubí B, Maechler P, (2010) Minireview: new roles for peripheral dopamine on metabolic control and tumor growth: let's seek the balance. Endocrinology 151: 5570-5581.
40. Ewing AG, Bigelow JC, Wightman RM, (1983) Direct in vivo monitoring of dopamine released from two striatal compartments in the rat. Science 221: 169-171.
41. Li L, Xia Y, Wang Z, Cao X, Da Z, et al. (2011) Suppression of the PI3K-Akt pathway is involved in the decreased adhesion and migration of bone marrow-derived mesenchymal stem cells from non-obese diabetic mice. Cell Biol Int 35: 961-966.
42. Liu H, Xue W, Ge G, Luo X, Li Y, et al. (2010) Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1α in MSCs. Biochem Biophys Res Commun 401: 509-515.
43. Ryu CH, Park SA, Kim SM, Lim JY, Jeong CH, et al. (2010) 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 398: 105-110.
44. Schmidt A, Ladage D, Schinköthe T, Klausmann U, Ulrichs C, et al. (2006) Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells 24: 1750-1758.
45. Ma J, Shi M, Li J, Chen B, Wang H, et al. (2007) Senescence-unrelated impediment of osteogenesis from Flk1+ bone marrow mesenchymal stem cells induced by total body irradiation and its contribution to long-term bone and hematopoietic injury. Haematologica 92: 889-896.
46. Ritter E, Perry A, Yu J, Wang T, Tang L, et al. (2008) Breast cancer cell-derived fibroblast growth factor 2 and vascular endothelial growth factor are chemoattractants for bone marrow stromal stem cells. Ann Surg 247: 310-314.
47. Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, et al. (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22: 377-384.
48. Al-Khaldi A, Eliopoulos N, Martineau D, Lejeune L, Lachapelle K, et al. (2003) Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther 10: 621-629.
49. Gruber R, Kandler B, Holzmann P, Vögele-Kadletz M, Losert U, et al. (2005) Bone marrow stromal cells can provide a local environment that favors migration and formation of tubular structures of endothelial cells. Tissue Eng 11: 896-903.
50. Bartness TJ, Song CK, (2007) Thematic review series: adipocyte biology. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res 48: 1655-1672.
51. Romijn JA, Fliers E, (2005) Sympathetic and parasympathetic innervation of adipose tissue: metabolic implications. Curr Opin Clin Nutr Metab Care 8: 440-444.
52. Berthoud HR, Fox EA, Neuhuber WL, (2006) Vagaries of adipose tissue innervation. Am J Physiol Regul Integr Comp Physiol 291: R1240-R1242.
53. Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, et al. (2002) Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 113: 155-166.
54. Vargovic P, Ukropec J, Laukova M, Cleary S, Manz B, et al. (2011) Adipocytes as a new source of catecholamine production. FEBS Lett 585: 2279-2284.
55. Shi E, Kazui T, Jiang X, Washiyama N, Yamashita K, et al. (2007) Therapeutic benefit of intrathecal injection of marrow stromal cells on ischemia-injured spinal cord. Ann Thorac Surg 83: 1484-1490.
56. Ferrari A, Hannouche D, Oudina K, Bourguignon M, Meunier A, et al. (2001) In vivo tracking of bone marrow fibroblasts with fluorescent carbocyanine dye. J Biomed Mater Res 56: 361-367.
57. Bartunek J, Croissant JD, Wijns W, Gofflot S, de Lavareille A, et al. (2007) Pretreatment of adult bone marrow mesenchymal stem cells with cardiomyogenic growth factors and repair of the chronically infarcted myocardium. Am J Physiol Heart Circ Physiol 292: H1095-H1104.
58. Ponte AL, Marais E, Gallay N, Langonné A, Delorme B, et al. (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25: 1737-1745.
59. Ganguly S, Basu B, Shome S, Jadhav T, Roy S, et al. (2010) Dopamine, by acting through its D2 receptor, inhibits insulin-like growth factor-I (IGF-I)-induced gastric cancer cell proliferation via up-regulation of Krüppel-like factor 4 through down-regulation of IGF-IR and AKT phosphorylation. Am J Pathol 177: 2701-2707.
60. Chiou WF, Don MJ, (2007) Cryptotanshinone inhibits macrophage migration by impeding F-actin polymerization and filopodia extension. Life Sci 81: 109-114.