Proteoglycan 4, a novel immunomodulatory factor, regulates parathyroid hormone actions on hematopoietic cells

American Journal of Pathology

Volumn 179, Issue 5, 2011, Pages 2431-2442

  Novince, Chad M ^a   Koh, Amy J ^a   Michalski, Megan N ^a   Marchesan, Julie T ^a   Wang, Jason ^a   Jung, Younghun ^a   Berry, Janice E ^a   Eber, Matthew R ^a   Rosol, Thomas J ^c   Taichman, Russell S ^a   McCauley, Laurie K ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MESSENGER RNA; OSTEOCALCIN; PARATHYROID HORMONE; PROTEOGLYCAN; PROTEOGLYCAN 4; STROMAL CELL DERIVED FACTOR 1; THROMBOPOIETIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BONE MARROW; CONTROLLED STUDY; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER; MEGAKARYOPOIESIS; MOUSE; NEUTROPHIL; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; UPREGULATION;

ANIMALS; BONE MARROW; CHEMOKINE CXCL12; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; INTERLEUKIN-6; LYMPHOCYTES; MEGAKARYOCYTE PROGENITOR CELLS; MICE; MICE, INBRED C57BL; PARATHYROID HORMONE; PROTEOGLYCANS; RNA, MESSENGER; THROMBOPOIETIN;

EID: 80055024618     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.07.032     Document Type: Article

References (65)

1. S. Kousteni, and J.P. Bilezikian Cellular actions of parathyroid hormone J.P. Bilezikian, L.G. Raisz, T.J. Martin, Principles of Bone Biology ed 3 2008 639 656
2. L.M. Calvi, G.B. Adams, K.W. Welbrecht, J.M. Weber, D.P. Olson, M.C. Knight, R.P. Martin, E. Schipani, P. Divieti, F.R. Bringhurst, L.A. Milner, H.M. Kronenberg, and D.T. Scadden Osteoblastic cells regulate the haematopoietic stem cell niche Nature 425 2003 841 846
3. S. Brunner, M. Zaruba, B. Huber, R. David, M. Vallaster, G. Assmann, J. Mueller-Hoecker, and W.M. Franz Parathyroid hormone effectively induces mobilization of progenitor cells without depletion of bone marrow Exp Hematol 36 2008 1157 1166
4. G.B. Adams, R.P. Martin, I.R. Alley, K.T. Chabner, K.S. Cohen, L.M. Calvi, H.M. Kronenberg, and D.T. Scadden Therapeutic targeting of a stem cell niche [Erratum appeared in Nat Biotechnol 2007, 25:944, and in Nat Biotechnol 2008, 26:241] Nat Biotechnol 25 2007 238 243
5. K.K. Ballen, E.J. Shpall, D. Avigan, B.Y. Yeap, D.C. Fisher, K. McDermott, B.R. Dey, E. Attar, S. McAfee, M. Konopleva, J.H. Antin, and T.R. Spitzer Phase I trial of parathyroid hormone to facilitate stem cell mobilization Biol Blood Marrow Transplant 13 2007 838 843
6. L.K. McCauley, T.J. Rosol, J.I. Merryman, and C.C. Capen Parathyroid hormone-related protein binding to human T-cell lymphotropic virus type-I-infected lymphocytes Endocrinology 130 1992 300 306
7. M. Terauchi, J.Y. Li, B. Bedi, K.H. Baek, H. Tawfeek, S. Galley, L. Gilbert, M.S. Nanes, M. Zayzafoon, R. Guldberg, D.L. Lamar, M.A. Singer, T.F. Lane, H.M. Kronenberg, and R. Pacifici T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling Cell Metab 10 2009 229 240
8. X. Li, H. Liu, L. Qin, J. Tamasi, M. Bergenstock, S. Shapses, J.H. Feyen, D.A. Notterman, and N.C. Partridge Determination of dual effects of parathyroid hormone on skeletal gene expression in vivo by microarray and network analysis J Biol Chem 282 2007 33086 33097
9. Y.L. Ma, R.L. Cain, D.L. Halladay, X. Yang, Q. Zeng, R.R. Miles, S. Chandrasekhar, T.J. Martin, and J.E. Onyia Catabolic effects of continuous human PTH (138) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation Endocrinology 142 2001 4047 4054
10. R.M. Locklin, S. Khosla, R.T. Turner, and B.L. Riggs Mediators of biphasic responses of bone to intermittent and continuously administered parathyroid hormone J Cell Biochem 89 2003 180 190
11. G. Silvestrini, P. Ballanti, M. Leopizzi, N. Gualtieri, D. Sardella, P. Monnazzi, S. Simeoni, M. Sebastiani, E. Bonucci, and F.R. Patacchioli Effects of the administration of corticosterone, parathyroid hormone, or both, and of their withdrawal, on rat bone and cartilage histomorphometric parameters, and on osteoprotegerin and RANKL mRNA expression and proteins J Mol Histol 38 2007 215 226
12. S.K. Lee, and J.A. Lorenzo Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation J Bone Miner Res 140 1999 3552 3561
13. F.Q. Pirih, M.N. Michalski, S.W. Cho, A.J. Koh, J.E. Berry, E. Ghaname, P. Kamarajan, E. Bonnelye, C.W. Ross, Y.L. Kapila, P. Jurdic, and L.K. McCauley Parathyroid hormone mediates hematopoietic cell expansion through interleukin-6 PLoS One 5 2010 e13657
14. Y.J. Liu, S.H. Lu, B. Xu, R.C. Yang, Q. Ren, B. Liu, B. Li, M. Lu, F.Y. Yan, Z.B. Han, and Z.C. Han Hemangiopoietin, a novel human growth factor for the primitive cells of both hematopoietic and endothelial cell lineages Blood 103 2004 4449 4456
15. Z.L. Xu, B. Zhou, X.L. Cong, Y.J. Liu, B. Xu, Y.H. Li, J. Gu, and Z.C. Han Hemangiopoietin supports animal survival and accelerates hematopoietic recovery of chemotherapy-suppressed mice Eur J Haematol 79 2007 477 485
16. Z.S. Xu, Y.J. Liu, L.L. Lv, Z.B. Han, R. He, S.H. Lu, T. Wang, B. Xu, Z.Z. Chen, and Z.C. Han Bone marrow stromal cells transduced with human hemangiopoietin gene support hematopoiesis in vitro Haematologica 90 2005 157 165
17. D.M. Merberg, L.J. Fitz, P. Temple, J. Giannotti, P. Murtha, M. Fitzgerald, H. Scaltreto, K. Kelleher, K. Preissner, R. Kriz, K. Jacobs, and K. Turner A comparison of vitronectin and megakaryocyte stimulating factor K.T. Preissner, S. Rosenblatt, C. Kost, J. Wegerhoff, D.F. Mosher, Biology of Vitronectins and Their Receptors: Proceedings of the First International Vitronectin Workshop, Rauischholzhausen Castle, Marburg, Germany, 2528 August, 1993 1992 Elsevier Philadelphia 45 53
18. S.M. Greenberg, D.J. Kuter, and R.D. Rosenberg In vitro stimulation of megakaryocyte maturation by megakaryocyte stimulatory factor J Biol Chem 262 1987 3269 3277
19. G. Tayrien, and R.D. Rosenberg Purification and properties of a megakaryocyte stimulatory factor present both in the serum-free conditioned medium of human embryonic kidney cells and in thrombocytopenic plasma J Biol Chem 262 1987 3262 3268
20. C.M. Novince, A.J. Koh, J.T. Marchesan, and L.K. McCauley Proteoglycan-4: a novel gene regulating parathyroid hormone actions in bone anabolism and hematopoiesis (abstract 1186) ASBMR 31st Annual Meeting 10011300 J Bone Miner Res 24 2009 S56 S57
21. C.M. Novince, M.N. Michalski, B.P. Sinder, P. Entezami, A.J. Koh, M.J. Eber, G.J. Pettway, T.J. Rosol, T.J. Wronski, K.M. Kozloff, and L.K. McCauley Proteoglycan 4: a dynamic regulator of skeletogenesis and PTH skeletal anabolism J Bone Miner Res 2011 10.1002/jbmr.508
22. S. Ikegawa, M. Sano, Y. Koshizuka, and Y. Nakamura Isolation, characterization and mapping of the mouse and human PRG4 (proteoglycan 4) genes Cytogenet Genome Res 90 2000 291 297
23. D.K. Rhee, J. Marcelino, M. Baker, Y. Gong, P. Smits, V. Lefebvre, G.D. Jay, M. Stewart, H. Wang, M.L. Warman, and J.D. Carpten The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth J Clin Invest 115 2005 622 631
24. B.L. Schumacher, J.A. Block, T.M. Schmid, M.B. Aydelotte, and K.E. Kuettner A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage Arch Biochem Biophys 311 1994 144 152
25. J. Marcelino, J.D. Carpten, W.M. Suwairi, O.M. Gutierrez, S. Schwartz, C. Robbins, R. Sood, I. Makalowska, A. Baxevanis, B. Johnstone, R.M. Laxer, L. Zemel, C.A. Kim, J.K. Herd, J. Ihle, C. Williams, M. Johnson, V. Raman, L.G. Alonso, D. Brunoni, A. Gerstein, N. Papadopoulos, S.A. Bahabri, J.M. Trent, and M.L. Warman CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome Nat Genet 23 1999 319 322
26. T.D. Schmittgen, and K.J. Livak Analyzing real-time PCR data by the comparative CT method Nat Protocols 3 2008 1101 1108
27. L.K. McCauley, A.J. Koh, C.A. Beecher, Y. Cui, J.D. Decker, and R.T. Francheschi Effects of differentiation and transforming growth factor beta on PTH/PTHrP receptor mRNA levels in MC3T3-E1 cells J Bone Miner Res 10 1995 1243 1255
28. M. Kopf, A. Ramsay, F. Brombacher, H. Baumann, G. Freer, C. Galanos, J.C. Gutierrez-Ramos, and G. Köhler Pleiotropic defects of IL-6-deficient mice including early hematopoiesis T and B cell function, and acute phase responses Ann N Y Acad Sci 21 1985 308 318
29. K. Ikebuchi, G.G. Wong, S.C. Clark, J.N. Ihle, Y. Hirai, and M. Ogawa Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemopoietic progenitors Proc Natl Acad Sci USA 84 1987 9035 9039
30. T. Imai, K. Koike, T. Kubo, T. Kikuchi, Y. Amano, M. Takagi, N. Okumura, and T. Nakahata Interleukin-6 supports human megakaryocytic proliferation and differentiation in vitro Blood 78 1991 1969 1974
31. R.J. Hill, M.K. Warren, P. Stenberg, J. Levin, L. Corash, R. Drummond, G. Baker, F. Levin, and Y. Mok Stimulation of megakaryocytopoiesis in mice by human recombinant interleukin-6 Blood 77 1991 42 48
32. E.M. Greenfield, S.A. Gornik, M.C. Horowitz, H.J. Donahue, and S.M. Shaw Regulation of cytokine expression in osteoblasts by parathyroid hormone: rapid stimulation of interleukin-6 and leukemia inhibitory factor mRNA J Bone Miner Res 8 1993 1163 1171
33. J.E. Onyia, J. Bidwell, J. Herring, J. Hulman, and J.M. Hock In vivo, human parathyroid hormone fragment (hPTH 1-34) transiently stimulates immediate early response gene expression, but not proliferation, in trabecular bone cells of young rats Bone 17 1995 479 484
34. J.H. Pollock, M.J. Blaha, S.A. Lavish, S. Stevenson, and E.M. Greenfield In vivo demonstration that parathyroid hormone and parathyroid hormone-related protein stimulate expression by osteoblasts of interleukin-6 and leukemia inhibitory factor J Bone Miner Res 11 1996 754 759
35. M. Murone, D.A. Carpenter, and F.J. de Sauvage Hematopoietic deficiencies in c-mpl and TPO knockout mice Stem Cells 16 1998 1 6
36. A. Peled, I. Petit, O. Kollet, M. Magid, T. Ponomaryov, T. Byk, A. Nagler, H. Ben-Hur, A. Many, L. Shultz, O. Lider, R. Alon, D. Zipori, and T. Lapidot Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4 Science 283 1999 845 848
37. D.Y. Jo, S. Rafii, T. Hamada, and M.A. Moore Chemotaxis of primitive hematopoietic cells in response to stromal cell-derived factor-1 J Clin Invest 105 2000 101 111
38. J.F. Wang, Z.Y. Liu, and J.E. Groopman The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion Blood 92 1998 756 764
39. B.T. Suratt, J.M. Petty, S.K. Young, K.C. Malcom, J.A. Lieber, J.A. Nick, J.A. Gonzalo, P.M. Henson, and G.S. Worthen Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis Blood 104 2004 565 571
40. Q. Ma, D. Jones, and T.A. Springer The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment Immunity 10 1999 463 471
41. Y. Jung, J. Wang, A. Schneider, Y.X. Sun, A.J. Koh-Paige, N.I. Osman, L.K. McCauley, and R.S. Taichman Regulation of SDF-1 (CXCL12) production by osteoblasts in the hematopoietic microenvironment and a possible mechanism for stem cell homing Bone 38 2006 497 508
42. C.E. Jacome-Galarza, S.K. Lee, J.A. Lorenzo, and H.L. Aguila Parathyroid hormone regulates the distribution and osteoclastogenic potential of hematopoietic progenitors in the bone marrow J Bone Miner Res 26 2011 1207 1216
43. Y.H. Cheng, B.R. Chitteti, D.A. Streicher, J.A. Morgan, S. Rodriguez-Rodriguez, N. Carlesso, E.F. Srour, and M.A. Kacena Impact of maturational status on the ability of osteoblasts to enhance the hematopoietic function of stem and progenitor cells J Bone Miner Res 26 2011 1111 1121
44. J.A. Gonzalo, C.M. Lloyd, A. Peled, T. Delaney, A.J. Coyle, and J.C. Gutierrez-Ramos Critical involvement of the chemotactic axis CXCR4/stromal cell-derived factor-1 alpha in the inflammatory component of allergic airway disease J Immunol 165 2000 499 508
45. S.K. Gupta, K. Pillarisetti, and N. Aiyar CXCR4 undergoes complex lineage and inducing agent-dependent dissociation of expression and functional responsiveness to SDF-1alpha during myeloid differentiation J Leukocyte Biol 70 2001 431 438
46. R. Förster, E. Kremmer, A. Schubel, D. Breitfeld, A. Kleinschmidt, C. Nerl, G. Bernhardt, and M. Lipp Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: rapid internalization and recycling upon activation J Immunology 160 1998 1522 1531
47. C.W. Hendrix, C. Flexner, R.T. MacFarland, C. Giandomenico, E.J. Fuchs, E. Redpath, G. Bridger, and G.W. Henson Pharmacokinetics and safety of AMD-3100, a novel antagonist of the CXCR-4 chemokine receptor, in human volunteers Antimicrob Agents Chemother 44 2000 1667 1673
48. M. D'Appuzzo, A. Rolink, M. Loetscher, J.A. Hoxie, I. Clark-Lewis, F. Melchers, M. Baggiolini, and M. Moser The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4 Eur J Immunol 27 1997 1788 1793
49. E.R. Fedyk, D.H. Ryyan, I. Ritterman, and T.A. Springer Maturation decreases responsiveness of human bone marrow B lineage cells to stromal-derived factor 1 (SDF-1) J Leukocyte Biol 66 1999 667 673
50. T. Nagasawa, S. Hirota, K. Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, and T. Kishimoto Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1 Nature 382 1996 635 638
51. Q. Ma, D. Jones, P.R. Borghesani, R.A. Segal, T. Nagasawa, T. Kishimoto, R.T. Bronson, and T.A. Springer Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice Proc Natl Acad Sci USA 95 1998 9448 9453
52. T. Nagasawa, H. Kikutani, and T. Kishimoto Molecular cloning and structure of a pre-B-cell growth-stimulating factor Proc Natl Acad Sci USA 91 1994 2305 2309
53. M. Kopf, H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler Impaired immune and acute-phase responses in interleukin-6-deficient mice Nature 368 1994 339 342
54. J. Zhu, R. Garrett, Y. Jung, Y. Zhang, N. Kim, J. Wang, G.J. Joe, E. Hexner, Y. Choi, R.S. Taichman, and S.G. Emerson Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells [Erratum appeared in Blood 2007 Jul 1;110(1):17] Blood 109 2007 3706 3712
55. J.Y. Wu, L.E. Purton, S.J. Rodda, M. Chen, L.S. Weinstein, A.P. McMahon, D.T. Scadden, and H.M. Kronenberg Osteoblastic regulation of B lymphopoiesis is mediated by Gs{alpha}-dependent signaling pathways Proc Natl Acad Sci USA 105 2008 16976 16981
56. A. Aiuti, I.J. Webb, C. Bleul, T. Springer, and J.C. Gutierrez-Ramos The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood J Exp Med 185 1997 111 120
57. R. Mohle, F. Bautz, S. Rafii, J. Moore, W. Brugger, and L. Kanz The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1 Blood 91 1998 4523 4530
58. M.C. Rodríguez, A. Bernad, and M. Aracil Interleukin-6 deficiency affects bone marrow stromal precursors, resulting in defective hematopoietic support Blood 103 2004 3349 3354
59. A. Bernad, M. Kopf, R. Kulbacki, N. Weich, G. Koehler, and J.C. Gutierrez-Ramos Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system Immunity 1 1994 725 731
60. A. Amara, O. Lorthioir, A. Valenzuela, A. Magerus, M. Thelen, M. Montes, J.L. Virelizier, M. Delepierre, F. Baleux, H. Lortat-Jacob, and F. Arenzana-Seisdedos Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine J Biol Chem 274 1999 23916 23925
61. E. Mbemba, J.C. Gluckman, and L. Gattegno Glycan and glycosaminoglycan binding properties of stromal cell-derived factor (SDF)-1alpha Glycobiology 10 2000 21 29
62. T. Netelenbos, S. Zuijderduin, J. Van Den Born, F.L. Kessler, S. Zweegman, P.C. Huijgens, and A.M. Drger Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells J Leukocyte Biol 72 2002 353 362
63. T. Netelenbos, J. van den Born, F.L. Kessler, S. Zweegman, P.A. Merle, J.W. van Oostveen, J.J. Zwaginga, P.C. Huijgens, and A.M. Drger Proteoglycans on bone marrow endothelial cells bind and present SDF-1 towards hematopoietic progenitor cells Leukemia 17 2003 175 184
64. B. Santiago, F. Baleux, P. Paleo, I. Gutiérrez-Caas, J.C. Ramírez, F. Arenzana-Seisdedos, and J.L. Pablos CXCL12 is displayed by rheumatoid endothelial cells through its basic amino-terminal motif on heparan sulfate proteoglycans Arthritis Res Ther 8 2006 R43
65. + stem cells into the ischaemic heart Cardiovasc Res 90 2011 529 537