Trafficking of murine hematopoietic stem and progenitor cells in health and vascular disease

Microcirculation

Volumn 16, Issue 6, 2009, Pages 497-507

  Schulz, Christian ^a   Von Andrian, Ulrich ^a   Massberg, Steffen ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Mouse model; Progenitor cells; Stem cells; Trafficking; Vascular disease

Indexed keywords

CHEMOKINE; INTEGRIN; PARATHYROID HORMONE; PHOSPHOLIPID; PROTEINASE; SELECTIN; SPHINGOSINE 1 PHOSPHATE;

ATHEROSCLEROSIS; BONE MARROW; CELL DIFFERENTIATION; CELL FUNCTION; CELL HOMING; CELL LINEAGE; CELL MIGRATION; CELL RENEWAL; DISEASE MODEL; EXPERIMENTAL MOUSE; HEMATOPOIETIC STEM CELL; IMMUNE RESPONSE; IMMUNOMODULATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; STEADY STATE; STEM CELL MOBILIZATION; TARGET CELL; VASCULAR DISEASE; VASCULAR TISSUE;

ANIMALS; BONE MARROW CELLS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; HEMATOPOIETIC STEM CELLS; LYSOPHOSPHOLIPIDS; MICE; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; SPHINGOSINE; VASCULAR DISEASES;

MURINAE; MUS;

EID: 68549122804     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680902948351     Document Type: Review

References (92)

1. Adams GB, Chabner KT, Alley IR, Olson DP, Szczepiorkowski ZM, Poznansky MC, Kos CH, Pollak MR, Brown EM, Scadden DT. (2006). Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 439:599-603.
2. Adams GB, Martin RP, Alley IR, Chabner KT, Cohen KS, Calvi LM, Kronenberg HM, Scadden DT. (2007). Therapeutic targeting of a stem cell niche. Nat Biotechnol 25:238-243.
3. Adams GB, Scadden DT. (2008). A niche opportunity for stem cell therapeutics. Gene Ther 15:96-99.
4. Aranguren XL, McCue JD, Hendrickx B, Zhu XH, Du F, Chen E, Pelacho B, Penuelas I, Abizanda G, Uriz M, Frommer SA, Ross JJ, Schroeder BA, Seaborn MS, Adney JR, Hagenbrock J, Harris NH, Zhang Y, Zhang X, Nelson-Holte MH, Jiang Y, Billiau AD, Chen W, Prosper F, Verfaillie CM, Luttun A. (2008). Multipotent adult progenitor cells sustain function of ischemic limbs in mice. J Clin Invest 118:505-514.
5. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967.
6. Berrios VM, Dooner GJ, Nowakowski G, Frimberger A, Valinski H, Quesenberry PJ, Becker PS. (2001). The molecular basis for the cytokine-induced defect in homing and engraftment of hematopoietic stem cells. Exp Hematol 29:1326-1335.
7. Bittner RE, Schofer C, Weipoltshammer K, Ivanova S, Streubel B, Hauser E, Freilinger M, Hoger H, Elbe-Burger A, Wachtler F. (1999). Recruitment of bone marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl) 199:391-396.
8. Bonig H, Priestley GV, Oehler V, Papayannopoulou T. (2007). Hematopoietic progenitor cells (HPC) from mobilized peripheral blood display enhanced migration and marrow homing compared to steadystate bone marrow HPC. Exp Hematol 35:326-334.
9. Bonig H, Priestley GV, Papayannopoulou T. (2006). Hierarchy of molecular-pathway usage in bone marrow homing and its shift by cytokines. Blood 107:79-86.
10. Bowie MB, McKnight KD, Kent DG, McCaffrey L, Hoodless PA, Eaves CJ. (2006). Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J Clin Invest 116:2808-2816.
11. Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF. (2005). Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201:1307-1318.
12. Brunner S, Zaruba MM, Huber B, David R, Vallaster M, Assmann G, Mueller-Hoecker J, Franz WM. (2008). Parathyroid hormone effectively induces mobilization of progenitor cells without depletion of bone marrow. Exp Hematol 36:1157-1166.
13. Cancelas JA, Lee AW, Prabhakar R, Stringer KF, Zheng Y, Williams DA. (2005). Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. Nat Med 11:886-891.
14. Chan JY, Watt SM. (2001). Adhesion receptors on haematopoietic progenitor cells. Br J Haematol 112:541-557.
15. Chavakis E, Aicher A, Heeschen C, Sasaki K, Kaiser R, El Makhfi N, Urbich C, Peters T, Scharffetter- Kochanek K, Zeiher AM, Chavakis T, Dimmeler S. (2005). Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med 201:63-72.
16. Christopherson KW, 2nd, Cooper S, Broxmeyer HE. (2003). Cell-surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood 101:4680-4686.
17. Christopherson KW, 2nd, Hangoc G, Mantel CR, Broxmeyer HE. (2004). Modulation of hematopoietic stem cell homing and engraftment by CD26. Science. 305:1000-1003.
18. Denhardt DT, Noda M, O'Regan AW, Pavlin D, Berman JS. (2001). Osteopontin as a means to cope with environmental insults: Regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 107:1055-1061.
19. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. (2001). CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 153:1277-1286.
20. Eto T, Winkler I, Purton LE, Levesque JP. (2005). Contrasting effects of P-selectin and E-selectin on the differentiation of murine hematopoietic progenitor cells. Exp Hematol 33:232-242.
21. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528-1530.
22. Fortunel NO, Hatzfeld JA, Monier MN, Hatzfeld A. (2003). Control of hematopoietic stem/progenitor cell fate by transforming growth factor-beta. Oncol Res 13(6-10):445-453.
23. Foteinos G, Hu Y, Xiao Q, Metzler B, Xu Q. (2008). Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apolipoprotein E-deficient mice. Circulation 117:1856-1863.
24. Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD. (1998). Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci U S A 95:14423-14428.
25. Fukuda S, Bian H, King AG, Pelus LM. (2007). The chemokine GRObeta mobilizes early hematopoietic stem cells characterized by enhanced homing and engraftment. Blood 110:860-869.
26. Galkina E, Ley K. (2007). Leukocyte influx in atherosclerosis. Curr Drug Targ 8:1239-1248.
27. George J. (2008). Mechanisms of disease: The evolving role of regulatory T cells in atherosclerosis. Nat Clin Pract Cardiovasc Med 5:531-540.
28. Gnecchi M, Zhang Z, Ni A, Dzau VJ. (2008). Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 103:1204-1219.
29. Gu Y, Filippi MD, Cancelas JA, Siefring JE, Williams EP, Jasti AC, Harris CE, Lee AW, Prabhakar R, Atkinson SJ, Kwiatkowski DJ, Williams DA. (2003). Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302:445-449.
30. Guo Y, Hangoc G, Bian H, Pelus LM, Broxmeyer HE. (2005). SDF-1/CXCL12 enhances survival and chemotaxis of murine embryonic stem cells and production of primitive and definitive hematopoietic progenitor cells. Stem Cells 23:1324-1332.
31. Guthrie SM, Curtis LM, Mames RN, Simon GG, Grant MB, Scott EW. (2005). The nitric oxide pathway modulates hemangioblast activity of adult hematopoietic stem cells. Blood 105:1916-1922.
32. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S. (2002). Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625-637.
33. Hla T, Venkataraman K, Michaud J. (2008). The vascular S1P gradient-cellular sources and biological significance. Biochim Biophys Acta 1781:477-482.
34. Jin F, Zhai Q, Qiu L, Meng H, Zou D, Wang Y, Li Q, Yu Z, Han J, Zhou B. (2008). Degradation of BM SDF-1 by MMP-9: The role in G-CSF-induced hematopoietic stem/progenitor cell mobilization. Bone Marrow Transpl 42:581-588.
35. Karra R, Vemullapalli S, Dong C, Herderick EE, Song X, Slosek K, Nevins JR, West M, Goldschmidt- Clermont PJ, Seo D. (2005). Molecular evidence for arterial repair in atherosclerosis. Proc Natl Acad Sci U S A 102:16789-16794.
36. Katayama Y, Hidalgo A, Furie BC, Vestweber D, Furie B, Frenette PS. (2003). PSGL-1 participates in E-selectin-mediated progenitor homing to bone marrow: Evidence for cooperation between E-selectin ligands and alpha4 integrin. Blood 102:2060-2067.
37. Kiel MJ, Morrison SJ. (2008). Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8:290-301.
38. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109-1121.
39. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T. (2006). Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12:657-664.
40. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229-1234.
41. Laird DJ, von Andrian UH, Wagers AJ. (2008). Stem cell trafficking in tissue development, growth, and disease. Cell 132:612-630.
42. Lapidot T, Dar A, Kollet O. (2005). How do stem cells find their way home? Blood 106:1901-1910.
43. Lapidot T, Kollet O. (2002). The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immune-deficient NOD/SCID and NOD/SCID/B2m(null) mice. Leukemia 16:1992-2003.
44. Lee BC, Cheng T, Adams GB, Attar EC, Miura N, Lee SB, Saito Y, Olszak I, Dombkowski D, Olson DP, Hancock J, Choi PS, Haber DA, Luster AD, Scadden DT. (2003). P2Y-like receptor, GPR105 (P2Y14), identifies and mediates chemotaxis of bone-marrow hematopoietic stem cells. Genes Dev 17:1592-1604.
45. Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. (2003). Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111:187-196.
46. Levesque JP, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C, Link DC. (2004). Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 104:65-72.
47. Lucas D, Battista M, Shi PA, Isola L, Frenette PS. (2008). Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 3:364-366.
48. Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, Hirschi KK. (2003). Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111:71-79.
49. Massberg S, Gawaz M, Gruner S, Schulte V, Konrad I, Zohlnhofer D, Heinzmann U, Nieswandt B. (2003). A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 197:41-49.
50. Massberg S, Konrad I, Schurzinger K, Lorenz M, Schneider S, Zohlnhoefer D, Hoppe K, Schiemann M, Kennerknecht E, Sauer S, Schulz C, Kerstan S, Rudelius M, Seidl S, Sorge F, Langer H, Peluso M, Goyal P, Vestweber D, Emambokus NR, Busch DH, Frampton J, Gawaz M. (2006). Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med 203:1221-1233.
51. Massberg S, Schaerli P, Knezevic-Maramica I, Kollnberger M, Tubo N, Moseman EA, Huff IV, Junt T, Wagers AJ, Mazo IB, von Andrian UH. (2007). Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994-1008.
52. Massberg S, von Andrian UH. (2006). Fingolimod and sphingosine-1-phosphate--modifiers of lymphocyte migration. N Engl J Med 355:1088-1091.
53. Mayack SR, Wagers AJ. (2008). Osteolineage niche cells initiate hematopoietic stem cell mobilization. Blood 112:519-531.
54. Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH. (1998). Hematopoietic progenitor cell rolling in bone marrow microvessels: Parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 188:465-474.
55. Mazo IB, von Andrian UH. (1999). Adhesion and homing of blood-borne cells in bone marrow microvessels. J Leukoc Biol 66:25-32.
56. Mendez-Ferrer S, Lucas D, Battista M, Frenette PS. (2008). Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452:442-447.
57. Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, Takatsu K, Kincade PW. (2006). Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24:801-812.
58. Nie Y, Han YC, Zou YR. (2008). CXCR4 is required for the quiescence of primitive hematopoietic cells. J Exp Med 205:777-783.
59. Orkin SH, Zon LI. (2008). Hematopoiesis: An evolving paradigm for stem cell biology. Cell 132: 631-644.
60. Papayannopoulou T. (2003). Bone marrow homing: The players, the playfield, and their evolving roles. Curr Opin Hematol 10:214-219.
61. Papayannopoulou T, Craddock C, Nakamoto B, Priestley GV, Wolf NS. (1995). The VLA4/VCAM-1 adhesion pathway defines contrasting mechanisms of lodgement of transplanted murine hemopoietic progenitors between bone marrow and spleen. Proc Natl Acad Sci U S A 92:9647-9651.
62. Papayannopoulou T, Priestley GV, Nakamoto B, Zafiropoulos V, Scott LM. (2001). Molecular pathways in bone marrow homing: Dominant role of alpha(4)beta(1) over beta(2)-integrins and selectins. Blood 98:2403-2411.
63. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y, Camerer E, Zheng YW, Huang Y, Cyster JG, Coughlin SR. (2007). Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316:295-298.
64. Pelus LM, Bian H, Fukuda S, Wong D, Merzouk A, Salari H. (2005). The CXCR4 agonist peptide, CTCE-0021, rapidly mobilizes polymorphonuclear neutrophils and hematopoietic progenitor cells into peripheral blood and synergizes with granulocyte colony-stimulating factor. Exp Hematol 33: 295-307.
65. Pelus LM, Fukuda S. (2006). Peripheral blood stem cell mobilization: The CXCR2 ligand GRObeta rapidly mobilizes hematopoietic stem cells with enhanced engraftment properties. Exp Hematol 34:1010-1020.
66. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. (1999). Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170.
67. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T. (2002). G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and upregulating CXCR4. Nat Immunol 3:687-694.
68. Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, Arenzana-Seisdedos F, Magerus A, Caruz A, Fujii N, Nagler A, Lahav M, Szyper-Kravitz M, Zipori D, Lapidot T. (2000). Induction of the chemokine stromal-derived factor- 1 following DNA damage improves human stem cell function. J Clin Invest 106:1331-1339.
69. Potocnik AJ, Brakebusch C, Fassler R. (2000). Fetal and adult hematopoietic stem cells require beta1 integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity 12:653-663.
70. Rafii DC, Psaila B, Butler J, Jin DK, Lyden D. (2008). Regulation of vasculogenesis by platelet-mediated recruitment of bone marrow-derived cells. Arterioscler Thromb Vasc Biol 28:217-222.
71. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C, Taylor DA. (2003). Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 108:457-463.
72. Reid S, Ritchie A, Boring L, Gosling J, Cooper S, Hangoc G, Charo IF, Broxmeyer HE. (1999). Enhanced myeloid progenitor cell cycling and apoptosis in mice lacking the chemokine receptor, CCR2. Blood 93:1524-1533.
73. Rosen H, Goetzl EJ. (2005). Sphingosine 1- phosphate and its receptors: an autocrine and paracrine network. Nat Rev Immunol 5:560-570.
74. Rosen H, Gonzalez-Cabrera P, Marsolais D, Cahalan S, Don AS, Sanna MG. (2008). Modulating tone: The overture of S1P receptor immunotherapeutics. Immunol Rev 223:221-235.
75. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA. (2000). Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106:571-578.
76. Schatteman GC, Ma N. (2006). Old bone marrow cells inhibit skin wound vascularization. Stem Cells 24:717-721.
77. Schulz C, Penz S, Hoffmann C, Langer H, Gillitzer A, Schneider S, Brandl R, Seidl S, Massberg S, Pichler B, Kremmer E, Stellos K, Schonberger T, Siess W, Gawaz M. (2008). Platelet GPVI binds to collagenous structures in the core region of human atheromatous plaque and is critical for atheroprogression in vivo. Basic Res Cardiol 103:356-367.
78. Schulz C, Schafer A, Stolla M, Kerstan S, Lorenz M, von Bruhl ML, Schiemann M, Bauersachs J, Gloe T, Busch DH, Gawaz M, Massberg S. (2007). Chemokine fractalkine mediates leukocyte recruitment to inflammatory endothelial cells in flowing whole blood: A critical role for P-selectin expressed on activated platelets. Circulation 116:764-773.
79. Schwab SR, Pereira JP, Matloubian M, Xu Y, Huang Y, Cyster JG. (2005). Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309:1735-1739.
80. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. (1998). Evidence for circulating bone marrow-derived endothelial cells. Blood 92:362-367.
81. Springer TA. (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76:301-314.
82. Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grunewald E, Cheng T, Dombkowski D, Calvi LM, Rittling SR, Scadden DT. (2005). Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 201:1781-1791.
83. Sugiyama T, Kohara H, Noda M, Nagasawa T. (2006). Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25: 977-988.
84. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. (1999). Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434-438.
85. Tanaka K, Sata M, Hirata Y, Nagai R. (2003). Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res 93:783-790.
86. Valenzuela-Fernandez A, Planchenault T, Baleux F, Staropoli I, Le-Barillec K, Leduc D, Delaunay T, Lazarini F, Virelizier JL, Chignard M, Pidard D, Arenzana-Seisdedos F. (2002). Leukocyte elastase negatively regulates stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by aminoterminal processing of SDF-1 and CXCR4. J Biol Chem 277:15677-15689.
87. Vermeulen M, Le Pesteur F, Gagnerault MC, Mary JY, Sainteny F, Lepault F. (1998). Role of adhesion molecules in the homing and mobilization of murine hematopoietic stem and progenitor cells. Blood 92:894-900.
88. Wagers AJ, Weissman IL. (2004). Plasticity of adult stem cells. Cell 116:639-648.
89. Welner RS, Kincade PW. (2007). Stem cells on patrol. Cell 131:842-844.
90. Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL. (2001). Physiological migration of hematopoietic stem and progenitor cells. Science 294:1933-1936.
91. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R, Asazuma N, Satoh K, Ozaki Y, Kume S. (1997). Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem 121: 969-973.
92. Zohlnhofer D, Dibra A, Koppara T, de Waha A, Ripa RS, Kastrup J, Valgimigli M, Schomig A, Kastrati A. (2008). Stem cell mobilization by granulocyte colony-stimulating factor for myocardial recovery after acute myocardial infarction: A meta-analysis. J Am Coll Cardiol 51:1429-1437.