Heparanase regulates retention and proliferation of primitive Sca-l +/c-Kit+/Lin-cells via modulation of the bone marrow microenvironment

Blood

Volumn 111, Issue 10, 2008, Pages 4934-4943

  Spiegel, Asaf ^a   Zcharia, Eyal ^b   Vagima, Yaron ^a   Itkin, Tomer ^a   Kalinkovich, Alexander ^a   Dar, Ayelet ^a   Kollet, Orit ^a   Netzer, Neta ^a   Golan, Karin ^a   Shafat, Itay ^c   Nan, Neta ^c   Nagler, Arnon ^d   Vlodavsky, Israel ^c   Lapidot, Tsvee ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d SHEBA MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; CATHEPSIN K; ELASTASE; GELATINASE B; HEPARANASE; MYC PROTEIN; PROTEINASE; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; STROMAL CELL DERIVED FACTOR 1; BETA GLUCURONIDASE; CXCL12 PROTEIN, MOUSE; PEPTIDE HYDROLASE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL ADHESION; CELL COUNT; CELL MATURATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME REGULATION; HEMATOPOIETIC STEM CELL; LEUKOCYTE; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; UPREGULATION; WILD TYPE; ANIMAL; BONE MARROW CELL; CELL MOTION; CYTOLOGY; IMMUNOPHENOTYPING; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BONE MARROW; BONE MARROW CELLS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; GLUCURONIDASE; HEMATOPOIETIC STEM CELLS; IMMUNOPHENOTYPING; MICE; MICE, TRANSGENIC; NEOPLASM PROTEINS; PEPTIDE HYDROLASES;

EID: 46749131949     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-10-116145     Document Type: Article

References (53)

1. Papayannopoulou T. Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood. 2004;103:1580-1585.
2. Suda T, Arai F. Hirao A. Hematopoietic stem cells and their niche. Trends Immunol. 2005;26:426- 433.
3. Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood. 2005;105:2631- 2639.
4. Weissman IL. Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science. 2000;287:1442-1446.
5. Adams GB, Scadden DT. The hematopoietic stem cell in its place. Nat Immunol. 2006:7:333- 337.
6. Yin T. Li L. The stem cell niches in bone. J Clin Invest. 2006;116:1195-1201.
7. Calvi LM, Adams GB; Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841-846.
8. Zhang J; Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836-841.
9. Arai F. Hirao A. Ohmura M. et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004: 118:149-161.
10. Kiel MJ, Yilmaz OH, Iwashita T. Yilmaz OH. Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121:1109-1121.
11. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25: 977-988.
12. Visnjic D. Kalajzic Z, Rowe DW. Katavic V, Lorenzo J, Aguila HL. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood. 2004;103:3258-3264.
13. Kollet O, Dar A, Shivtiel S, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006;12:657-664.
14. Toksoz D, Zsebo KM, Smith KA, et al. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci USA. 1992;89:7350-7354.
15. Nagasawa T Hirota S, Tachibana K, et al. Defects of B-cell lymphopoiesis and bone-marrow myelo- poiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 1996;382:635-638.
16. Ponomaryov T, Peled A, Petit I, et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest. 2000;106:1331-1339.
17. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci USA. 1992;89:1502-1506.
18. Williams DA, Majumdar MK Analysis of steel factor (stem cell factor) isoforms in the hematopoietic microenvironment. Stem Cells. 1994; 12(Suppl 1):67-74; discussion 75-77.
19. Huang EJ, Nocka KR Buck J, Besmer P. Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol Biol Cell. 1992;3:349-362.
20. Papayannopoulou T, Priestley GV, Nakamoto B. Anti-VLA4A/CAM-1-induced mobilization requires cooperative signaling through the kit/mkit ligand pathway. Blood. 1998;91:2231-2239.
21. Driessen RL, Johnston HM, Nilsson SK. Membrane-bound stem cell factor is a key regulator in the initial lodgment of stem cells within the endosteal marrow region. Exp Hematol. 2003;31: 1284-1291.
22. Heissig B, Hattori K, Dias S, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires mmp-9 mediated release of kit- ligand. Cell. 2002;109:625-637.
23. Peled A, Petit I, Kollet O, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science. 1999;283: 845-848.
24. Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med. 2002;195:1145-1154.
25. Imai K, Kobayashi M, Wang J, et al. Selective secretion of chemoattractants for haemopoietic progenitor cells by bone marrow endothelial cells: a possible role in homing of haemopoietic progenitor cells to bone marrow. Br J Haematol. 1999; 106:905-911.
26. Kollet O, Spiegel A, Peled A, et al. Rapid and efficient homing of human CD34(+)CD38- (-/low)GXCR4(+) stem and progenitor cells to the bone marrow and spleen of NOD/SCID and NOD/ SCID/B2m(null) mice. Blood. 2001 ;97:3283- 3291.
27. Nan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol. 2006;38:2018-2039.
28. lozzo RV, San Antonio JD. Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J Clin Invest. 2001:108:349-355.
29. Kjellen L, Lindahl U. Proteoglycans: structures and interactions. Annu Rev Biochem. 1991 ;60: 443-475.
30. Bernfield M, Gotte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999;68:729-777.
31. Hulett MD, Freeman C, Hamdorf BJ, Baker RT, Harris MJ, Parish CR. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat Med. 1999;5:803-809.
32. Vlodavsky I, Friedmann Y, Elkin M, et al. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat Med. 1999;5:793-802.
33. McKenzie EA. Heparanase: a target for drug discovery in cancer and inflammation. Br J Pharmacol. 2007;151:1-14.
34. Parish CR, Freeman C, Hulett MD. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta. 2001 ;1471 :M99-M108.
35. Vreys V, David G. Mammalian heparanase: what is the message? J Cell Mol Med. 2007;11:427- 452.
36. Elkin M, Man N, Ishai-Michaeli R, et al. Heparanase as mediator of angiogenesis: mode of action. FASEB J. 2001 ;15:1661 -1663.
37. Vlodavsky I, Goldshmidt O, Zcharia E, et al. Mammalian heparanase: involvement in cancer metastasis, angiogenesis and normal development. Semin Cancer Biol. 2002;12:121-129.
38. Zcharia E, Metzger S, Chajek-Shaul T, et al. Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J. 2004;18:252- 263.
39. Spiegel A, Kollet O, Peled A, et al. Unique SDF-1- induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood. 2004;103:2900-2907.
40. Petit I, Szyper-Kravitz M. Nagler A, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002;3:687-694.
41. Nardella C, Lahm A, Pallaoro M, Brunetti M, Vannini A, Steinkuhler C. Mechanism of activation of human heparanase investigated by protein engineering. Biochemistry. 2004;43:1862-1873.
42. Shafat I, Zcharia E, Nisman B, et al. An ELISA method for the detection and quantification of human heparanase. Biochem Biophys Res Commun. 2006;341:958-963.
43. Levy-Adam F, Miao HQ, Heinrikson RL, Vlodavsky I, Nan N. Heterodimerformation is essential for heparanase enzymatic activity. Biochem Biophys Res Commun. 2003;308:885-891.
44. Janowska-Wieczorek A, Matsuzaki A, Marquez LA. The hematopoietic microenvironment: matrix metalloproteinases in the hematopoietic microenvironment. Hematology. 2000;4:515-527.
45. Janowska-Wieczorek A, Marquez LA, Nabholtz JM; et al. Growth factors and cytokines upregu- late gelatinase expression in bone marrow CD34(+) cells and their transmigration through reconstituted basement membrane. Blood. 1999; 93:3379-3390.
46. Lambert E, Dasse E, Haye B, Petitfrere E. TIMPs as multifacial proteins. Crit Rev Oncol Hematol. 2004;49:187-198.
47. Adams GB. Chabner KT. Alley IR, et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature. 2006;439: 599-603.
48. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9:702-712.
49. Wilson A, Murphy MJ, Oskarsson T, et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004;18:2747-2763.
50. Kram V, Zcharia E, Yacoby-Zeevi O, et al. Heparanase is expressed in osteoblastic cells and stimulates bone formation and bone mass. J Cell Physiol. 2006;207:784-792.
51. Wright DE, Wagers AJ, Gulati AR Johnson FL Weissman IL. Physiological migration of hematopoietic stem and progenitor cells. Science. 2001; 294:1933-1936.
52. Lapidot T, Petit I. Current understanding of stem cell mobilization: the roles of chemokines. proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp Hematol. 2002;30:973- 981.
53. Levesque JP. Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest. 2003;111:187-196.