Does complement play a role in bone development and regeneration?

Immunobiology

Volumn 218, Issue 1, 2013, Pages 1-9

  Schoengraf, Philipp ^a   Lambris, John D ^b   Recknagel, Stefan ^a   Kreja, Ludwika ^a   Liedert, Astrid ^a   Brenner, Rolf E ^a   Huber Lang, Markus ^a   Ignatius, Anita ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bone; Complement; Inflammation; Mesenchymal stem cells; Osteoblasts; Osteoclasts

Indexed keywords

COMPLEMENT COMPONENT C1Q;

BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; CALCIUM METABOLISM; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; FRACTURE HEALING; HOMEOSTASIS; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INNATE IMMUNITY; MOLECULAR INTERACTION; NONHUMAN; OSTEOARTHRITIS; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; PERIODONTITIS; PRIORITY JOURNAL; PROSTHESIS LOOSENING; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; BONE DEVELOPMENT; BONE REGENERATION; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; CYTOKINES; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; MUSCULOSKELETAL SYSTEM; OSTEOBLASTS; OSTEOCLASTS;

EID: 84870291715     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.01.020     Document Type: Review

References (98)

1. Aksamit R.R., Falk W., Leonard E.J. Chemotaxis by mouse macrophage cell lines. J. Immunol. 1981, 126:2194-2199.
2. Amara U., Flierl M.A., Rittirsch D., Klos A., Chen H., Acker B., Bruckner U.B., Nilsson B., Gebhard F., Lambris J.D., Huber-Lang M. Molecular intercommunication between the complement and coagulation systems. J. Immunol. 2010, 185:5628-5636.
3. Andersson J., Bexborn F., Klinth J., Nilsson B., Ekdahl K.N. Surface-attached PEO in the form of activated pluronic with immobilized factor H reduces both coagulation and complement activation in a whole-blood model. J. Biomed. Mater. Res. A 2006, 76:25-34.
4. Andersson J., Ekdahl K.N., Larsson R., Nilsson U.R., Nilsson B. C3 adsorbed to a polymer surface can form an initiating alternative pathway convertase. J. Immunol. 2002, 168:5786-5791.
5. Andrades J.A., Nimni M.E., Becerra J., Eisenstein R., Davis M., Sorgente N. Complement proteins are present in developing endochondral bone and may mediate cartilage cell death and vascularization. Exp. Cell Res. 1996, 227:208-213.
6. Asagiri M., Takayanagi H. The molecular understanding of osteoclast differentiation. Bone 2007, 40:251-264.
7. Bamberg C.E., Mackay C.R., Lee H., Zahra D., Jackson J., Lim Y.S., Whitfeld P.L., Craig S., Corsini E., Lu B., Gerard C., Gerard N.P. The C5a receptor (C5aR) C5L2 is a modulator of C5aR-mediated signal transduction. J. Biol. Chem. 2010, 285:7633-7644.
8. Banfi A., Bianchi G., Notaro R., Luzzatto L., Cancedda R., Quarto R. Replicative aging and gene expression in long-term cultures of human bone marrow stromal cells. Tissue Eng. 2002, 8:901-910.
9. Bock D., Martin U., Gartner S., Rheinheimer C., Raffetseder U., Arseniev L., Barker M.D., Monk P.N., Bautsch W., Kohl J., Klos A. The C terminus of the human C5a receptor (CD88) is required for normal ligand-dependent receptor internalization. Eur. J. Immunol. 1997, 27:1522-1529.
10. Bokisch V.A., Muller-Eberhard H.J. Anaphylatoxin inactivator of human plasma: its isolation and characterization as a carboxypeptidase. J. Clin. Invest. 1970, 49:2427-2436.
11. Bonewald L.F. The amazing osteocyte. J. Bone Miner. Res. 2010, 26:229-238.
12. Boyce B.F., Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch. Biochem. Biophys. 2008, 473:139-146.
13. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
14. Cain S.A., Monk P.N. The orphan receptor C5L2 has high affinity binding sites for complement fragments C5a and C5a des-Arg(74). J. Biol. Chem. 2002, 277:7165-7169.
15. Chakravarti A., Raquil M.A., Tessier P., Poubelle P.E. Surface RANKL of toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 2009, 114:1633-1644.
16. Chenoweth D.E. Complement activation in extracorporeal circuits. Ann. N. Y. Acad. Sci. 1987, 516:306-313.
17. Christmas S.E., de la Mata Espinosa C.T., Halliday D., Buxton C.A., Cummerson J.A., Johnson P.M. Levels of expression of complement regulatory proteins CD46, CD55 and CD59 on resting and activated human peripheral blood leucocytes. Immunology 2006, 119:522-528.
18. Cui W., Lapointe M., Gauvreau D., Kalant D., Cianflone K. Recombinant C3adesArg/acylation stimulating protein (ASP) is highly bioactive: a critical evaluation of C5L2 binding and 3T3-L1 adipocyte activation. Mol. Immunol. 2009, 46:3207-3217.
19. Djaafar S., Pierroz D.D., Chicheportiche R., Zheng X.X., Ferrari S.L., Ferrari-Lacraz S. Inhibition of T cell-dependent and RANKL-dependent osteoclastogenic processes associated with high levels of bone mass in interleukin-15 receptor-deficient mice. Arthritis Rheum. 2010, 62:3300-3310.
20. Ehrengruber M.U., Geiser T., Deranleau D.A. Activation of human neutrophils by C3a and C5a. Comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Lett. 1994, 346:181-184.
21. Ehrnthaller C., Ignatius A., Gebhard F., Huber-Lang M. New insights of an old defense system: structure, function, and clinical relevance of the complement system. Mol. Med. 2011, 17:317-329.
22. El-Lati S.G., Dahinden C.A., Church M.K. Complement peptides C3a- and C5a-induced mediator release from dissociated human skin mast cells. J. Invest. Dermatol. 1994, 102:803-806.
23. Elsner J., Oppermann M., Czech W., Kapp A. C3a activates the respiratory burst in human polymorphonuclear neutrophilic leukocytes via pertussis toxin-sensitive G-proteins. Blood 1994, 83:3324-3331.
24. Flannery S., Bowie A.G. The interleukin-1 receptor-associated kinases: critical regulators of innate immune signalling. Biochem. Pharmacol. 2010, 80:1981-1991.
25. Flierl M.A., Perl M., Rittirsch D., Bartl C., Schreiber H., Fleig V., Schlaf G., Liener U., Brueckner U.B., Gebhard F., Huber-Lang M.S. The role of C5a in the innate immune response after experimental blunt chest trauma. Shock 2008, 29:25-31.
26. Gao H., Neff T.A., Guo R.F., Speyer C.L., Sarma J.V., Tomlins S., Man Y., Riedemann N.C., Hoesel L.M., Younkin E., Zetoune F.S., Ward P.A. Evidence for a functional role of the second C5a receptor C5L2. FASEB J. 2005, 19:1003-1005.
27. Gerard N.P., Lu B., Liu P., Craig S., Fujiwara Y., Okinaga S., Gerard C. An anti-inflammatory function for the complement anaphylatoxin C5a-binding protein, C5L2. J. Biol. Chem. 2005, 280:39677-39680.
28. Gobeil F., Fortier A., Zhu T., Bossolasco M., Leduc M., Grandbois M., Heveker N., Bkaily G., Chemtob S., Barbaz D. G-protein-coupled receptors signalling at the cell nucleus: an emerging paradigm. Can. J. Physiol. Pharmacol. 2006, 84:287-297.
29. Goetzl E.J. Diverse pathways for nuclear signaling by G protein-coupled receptors and their ligands. FASEB J. 2007, 21:638-642.
30. Gough A.K., Lilley J., Eyre S., Holder R.L., Emery P. Generalised bone loss in patients with early rheumatoid arthritis. Lancet 1994, 344:23-27.
31. Hajishengallis G., Lambris J.D. Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol. 2010, 31:154-163.
32. Hajishengallis G., Liang S., Payne M.A., Hashim A., Jotwani R., Eskan M.A., McIntosh M.L., Alsam A., Kirkwood K.L., Lambris J.D., Darveau R.P., Curtis M.A. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011, 10:497-506.
33. Harboe M., Mollnes T.E. The alternative complement pathway revisited. J. Cell. Mol. Med. 2008, 12:1074-1084.
34. Hartmann K., Henz B.M., Kruger-Krasagakes S., Kohl J., Burger R., Guhl S., Haase I., Lippert U., Zuberbier T. C3a and C5a stimulate chemotaxis of human mast cells. Blood 1997, 89:2863-2870.
35. Hed J., Johansson M., Lindroth M. Complement activation according to the alternate pathway by glass and plastic surfaces and its role in neutrophil adhesion. Immunol. Lett. 1984, 8:295-299.
36. Heng B.C., Cao T., Stanton L.W., Robson P., Olsen B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J. Bone Miner. Res. 2004, 19:1379-1394.
37. Hong M.H., Jin C.H., Sato T., Ishimi Y., Abe E., Suda T. Transcriptional regulation of the production of the third component of complement (C3) by 1 alpha, 25-dihydroxyvitamin D3 in mouse marrow-derived stromal cells (ST2) and primary osteoblastic cells. Endocrinology 1991, 129:2774-2779.
38. Horton J.E., Raisz L.G., Simmons H.A., Oppenheim J.J., Mergenhagen S.E. Bone resorbing activity in supernatant fluid from cultured human peripheral blood leukocytes. Science 1972, 177:793-795.
39. Huber-Lang M., Sarma J.V., Zetoune F.S., Rittirsch D., Neff T.A., McGuire S.R., Lambris J.D., Warner R.L., Flierl M.A., Hoesel L.M., Gebhard F., Younger J.G., Drouin S.M., Wetsel R.A., Ward P.A. Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 2006, 12:682-687.
40. Huber-Lang M., Younkin E.M., Sarma J.V., Riedemann N., McGuire S.R., Lu K.T., Kunkel R., Younger J.G., Zetoune F.S., Ward P.A. Generation of C5a by phagocytic cells. Am. J. Pathol. 2002, 161:1849-1859.
41. Huch K., Kleffner S., Stove J., Puhl W., Gunther K.P., Brenner R.E. PTHrP, PTHr, and FGFR3 are involved in the process of endochondral ossification in human osteophytes. Histochem. Cell Biol. 2003, 119:281-287.
42. Ignatius A., Ehrnthaller C., Brenner R.E., Kreja L., Schoengraf P., Lisson P., Blakytny R., Recknagel S., Claes L., Gebhard F., Lambris J.D., Huber-Lang M. The anaphylatoxin receptor C5aR is present during fracture healing in rats and mediates osteoblast migration in vitro. J. Trauma 2011, 71:952-960.
43. Ignatius A., Schoengraf P., Kreja L., Liedert A., Recknagel S., Kandert S., Brenner R.E., Schneider M., Lambris J.D., Huber-Lang M. Complement C3a and C5a modulate osteoclast formation and inflammatory response of osteoblasts in synergism with IL-1beta. J. Cell. Biochem. 2011, 112:2594-2609.
44. Jin C.H., Shinki T., Hong M.H., Sato T., Yamaguchi A., Ikeda T., Yoshiki S., Abe E., Suda T. 1 alpha, 25-dihydroxyvitamin D3 regulates in vivo production of the third component of complement (C3) in bone. Endocrinology 1992, 131:2468-2475.
45. Kassem M., Abdallah B.M., Saeed H. Osteoblastic cells: differentiation and trans-differentiation. Arch. Biochem. Biophys. 2008, 473:183-187.
46. Kim D.D., Song W.C. Membrane complement regulatory proteins. Clin. Immunol. 2006, 118:127-136.
47. Konttinen Y.T., Ceponis A., Meri S., Vuorikoski A., Kortekangas P., Sorsa T., Sukura A., Santavirta S. Complement in acute and chronic arthritides: assessment of C3c, C9, and protectin (CD59) in synovial membrane. Ann. Rheum. Dis. 1996, 55:888-894.
48. Kreja L., Brenner R.E., Tautzenberger A., Liedert A., Friemert B., Ehrnthaller C., Huber-Lang M., Ignatius A. Non-resorbing osteoclasts induce migration and osteogenic differentiation of mesenchymal stem cells. J. Cell. Biochem. 2010, 109:347-355.
49. Kretzschmar T., Jeromin A., Gietz C., Bautsch W., Klos A., Kohl J., Rechkemmer G., Bitter-Suermann D. Chronic myelogenous leukemia-derived basophilic granulocytes express a functional active receptor for the anaphylatoxin C3a. Eur. J. Immunol. 1993, 23:558-561.
50. Li K., Anderson K.J., Peng Q., Noble A., Lu B., Kelly A.P., Wang N., Sacks S.H., Zhou W. Cyclic AMP plays a critical role in C3a-receptor-mediated regulation of dendritic cells in antigen uptake and T-cell stimulation. Blood 2008, 112:5084-5094.
51. Li K., Fazekasova H., Wang N., Peng Q., Sacks S.H., Lombardi G., Zhou W. Functional modulation of human monocytes derived DCs by anaphylatoxins C3a and C5a. Immunobiology 2011, 217:66-73.
52. Liang S., Krauss J.L., Domon H., McIntosh M.L., Hosur K.B., Qu H., Li F., Tzekou A., Lambris J.D., Hajishengallis G. The C5a receptor impairs IL-12-dependent clearance of Porphyromonas gingivalis and is required for induction of periodontal bone loss. J. Immunol. 2010, 186:869-877.
53. Lories R.J., Luyten F.P. The bone-cartilage unit in osteoarthritis. Nat. Rev. Rheumatol. 2011, 7:43-49.
54. Lu D., Yang H., Shaw G., Raizada M.K. Angiotensin II-induced nuclear targeting of the angiotensin type 1 (AT1) receptor in brain neurons. Endocrinology 1998, 139:365-375.
55. Mack C., Jungermann K., Gotze O., Schieferdecker H.L. Anaphylatoxin C5a actions in rat liver: synergistic enhancement by C5a of lipopolysaccharide-dependent alpha(2)-macroglobulin gene expression in hepatocytes via IL-6 release from Kupffer cells. J. Immunol. 2001, 167:3972-3979.
56. Maruotti N., Grano M., Colucci S., d'Onofrio F., Cantatore F.P. Osteoclastogenesis and arthritis. Clin. Exp. Med. 2010, 11:137-145.
57. Matsuo K., Irie N. Osteoclast-osteoblast communication. Arch. Biochem. Biophys. 2008, 473:201-209.
58. Meuer S., Hugli T.E., Andreatta R.H., Hadding U., Bitter-Suermann D. Comparative study on biological activities of various anaphylatoxins (C4a, C3a, C5a). Investigations on their ability to induce platelet secretion. Inflammation 1981, 5:263-273.
59. Murakami Y., Imamichi T., Nagasawa S. Characterization of C3a anaphylatoxin receptor on guinea-pig macrophages. Immunology 1993, 79:633-638.
60. Naik N., Giannini E., Brouchon L., Boulay F. Internalization and recycling of the C5a anaphylatoxin receptor: evidence that the agonist-mediated internalization is modulated by phosphorylation of the C-terminal domain. J. Cell Sci. 1997, 110(Pt 19):2381-2390.
61. Nakagawa K., Sakiyama H., Fukazawa T., Matsumoto M., Takigawa M., Toyoguchi T., Moriya H. Coordinated change between complement C1s production and chondrocyte differentiation in vitro. Cell Tissue Res. 1997, 289:299-305.
62. Nataf S., Davoust N., Ames R.S., Barnum S.R. Human T cells express the C5a receptor and are chemoattracted to C5a. J. Immunol. 1999, 162:4018-4023.
63. Neff J.A., Tresco P.A., Caldwell K.D. Surface modification for controlled studies of cell-ligand interactions. Biomaterials 1999, 20:2377-2393.
64. Nilsson B., Ekdahl K.N., Mollnes T.E., Lambris J.D. The role of complement in biomaterial-induced inflammation. Mol. Immunol. 2007, 44:82-94.
65. Nilsson B., Korsgren O., Lambris J.D., Ekdahl K.N. Can cells and biomaterials in therapeutic medicine be shielded from innate immune recognition?. Trends Immunol. 2010, 31:32-38.
66. O' Gradaigh D., Ireland D., Bord S., Compston J.E. Joint erosion in rheumatoid arthritis: interactions between tumour necrosis factor alpha, interleukin 1, and receptor activator of nuclear factor kappaB ligand (RANKL) regulate osteoclasts. Ann. Rheum. Dis. 2004, 63:354-359.
67. Okinaga S., Slattery D., Humbles A., Zsengeller Z., Morteau O., Kinrade M.B., Brodbeck R.M., Krause J.E., Choe H.R., Gerard N.P., Gerard C. C5L2, a nonsignaling C5A binding protein. Biochemistry 2003, 42:9406-9415.
68. Okusawa S., Dinarello C.A., Yancey K.B., Endres S., Lawley T.J., Frank M.M., Burke J.F., Gelfand J.A. C5a induction of human interleukin 1. Synergistic effect with endotoxin or interferon-gamma. J. Immunol. 1987, 139:2635-2640.
69. Ottonello L., Corcione A., Tortolina G., Airoldi I., Albesiano E., Favre A., D'Agostino R., Malavasi F., Pistoia V., Dallegri F. rC5a directs the in vitro migration of human memory and naive tonsillar B lymphocytes: implications for B cell trafficking in secondary lymphoid tissues. J. Immunol. 1999, 162:6510-6517.
70. Page G., Miossec P. RANK and RANKL expression as markers of dendritic cell-T cell interactions in paired samples of rheumatoid synovium and lymph nodes. Arthritis Rheum. 2005, 52:2307-2312.
71. Pobanz J.M., Reinhardt R.A., Koka S., Sanderson S.D. C5a modulation of interleukin-1 beta-induced interleukin-6 production by human osteoblast-like cells. J. Periodontal Res. 2000, 35:137-145.
72. Recknagel S., Bindl R., Kurz J., Wehner T., Ehrnthaller C., Knöferl M.W., Gebhard F., Huber-Lang M., Claes L., Ignatius A. Experimental blunt chest trauma impairs fracture healing in rats. J. Orthop. Res. 2012, 29:734-739.
73. Recknagel S., Bindl R., Kurz J., Wehner T., Schoengraf P., Ehrnthaller C., Qu H., Gebhard F., Huber-Lang M., Lambris J.D., Claes L., Ignatius A. C5aR-antagonist significantly reduces the deleterious effect of a blunt chest trauma on fracture healing. J. Orthop. Res. 2012, 30:581-586.
74. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010, 11:785-797.
75. Rousseau S., Dolado I., Beardmore V., Shpiro N., Marquez R., Nebreda A.R., Arthur J.S., Case L.M., Tessier-Lavigne M., Gaestel M., Cuenda A., Cohen P. CXCL12 and C5a trigger cell migration via a PAK1/2-p38alpha MAPK-MAPKAP-K2-HSP27 pathway. Cell. Signal. 2006, 18:1897-1905.
76. Rutkowski M.J., Sughrue M.E., Kane A.J., Ahn B.J., Fang S., Parsa A.T. The complement cascade as a mediator of tissue growth and regeneration. Inflamm. Res. 2010, 59:897-905.
77. Sakiyama H., Inaba N., Toyoguchi T., Okada Y., Matsumoto M., Moriya H., Ohtsu H. Immunolocalization of complement C1s and matrix metalloproteinase 9 (92kDa gelatinase/type IV collagenase) in the primary ossification center of the human femur. Cell Tissue Res. 1994, 277:239-245.
78. Sakiyama H., Nakagawa K., Kuriiwa K., Imai K., Okada Y., Tsuchida T., Moriya H., Imajoh-Ohmi S. Complement Cls, a classical enzyme with novel functions at the endochondral ossification center: immunohistochemical staining of activated Cls with a neoantigen-specific antibody. Cell Tissue Res. 1997, 288:557-565.
79. Sato T., Abe E., Jin C.H., Hong M.H., Katagiri T., Kinoshita T., Amizuka N., Ozawa H., Suda T. The biological roles of the third component of complement in osteoclast formation. Endocrinology 1993, 133:397-404.
80. Sato T., Hong M.H., Jin C.H., Ishimi Y., Udagawa N., Shinki T., Abe E., Suda T. The specific production of the third component of complement by osteoblastic cells treated with 1 alpha, 25-dihydroxyvitamin D3. FEBS Lett. 1991, 285:21-24.
81. Sayah S., Jauneau A.C., Patte C., Tonon M.C., Vaudry H., Fontaine M. Two different transduction pathways are activated by C3a and C5a anaphylatoxins on astrocytes. Brain Res. Mol. Brain Res. 2003, 112:53-60.
82. Schiano de Colella J.M., Barbarat B., Sweet R., Gastaut J.A., Olive D., Costello R.T. Rank ligand stimulation induces a partial but functional maturation of human monocyte-derived dendritic cells. Eur. Cytokine Netw. 2008, 19:81-88.
83. Schmal H., Niemeyer P., Roesslein M., Hartl D., Loop T., Sudkamp N.P., Stark G.B., Mehlhorn A.T. Comparison of cellular functionality of human mesenchymal stromal cells and PBMC. Cytotherapy 2007, 9:69-79.
84. Schraufstatter I.U., Discipio R.G., Zhao M., Khaldoyanidi S.K. C3a and C5a are chemotactic factors for human mesenchymal stem cells, which cause prolonged ERK1/2 phosphorylation. J. Immunol. 2009, 182:3827-3836.
85. Segal L.G., Lane N.E. Osteoporosis and systemic lupus erythematosus: etiology and treatment strategies. Ann. Med. Interne (Paris) 1996, 147:281-289.
86. Settmacher B., Bock D., Saad H., Gartner S., Rheinheimer C., Kohl J., Bautsch W., Klos A. Modulation of C3a activity: internalization of the human C3a receptor and its inhibition by C5a. J. Immunol. 1999, 162:7409-7416.
87. Sontheimer R.D., Racila E., Racila D.M. C1q: its functions within the innate and adaptive immune responses and its role in lupus autoimmunity. J. Invest. Dermatol. 2005, 125:14-23.
88. Takabayashi T., Shimizu S., Clark B.D., Beinborn M., Burke J.F., Gelfand J.A. Interleukin-1 upregulates anaphylatoxin receptors on mononuclear cells. Surgery 2004, 135:544-554.
89. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol. 2007, 7:292-304.
90. Toyoguchi T., Yamaguchi K., Nakagawa K., Fukusawa T., Moriya H., Sakiyama H. Change of complement C1s synthesis during development of hamster cartilage. Cell Tissue Res. 1996, 285:199-204.
91. Tu Z., Bu H., Dennis J.E., Lin F. Efficient osteoclast differentiation requires local complement activation. Blood 2010, 116:4456-4463.
92. Van Epps D.E., Simpson S., Bender J.G., Chenoweth D.E. Regulation of C5a and formyl peptide receptor expression on human polymorphonuclear leukocytes. J. Immunol. 1990, 144:1062-1068.
93. Wang Q., Rozelle A.L., Lepus C.M., Scanzello C.R., Song J.J., Larsen D.M., Crish J.F., Bebek G., Ritter S.Y., Lindstrom T.M., Hwang I., Wong H.H., Punzi L., Encarnacion A., Shamloo M., Goodman S.B., Wyss-Coray T., Goldring S.R., Banda N.K., Thurman J.M., Gobezie R., Crow M.K., Holers V.M., Lee D.M., Robinson W.H. Identification of a central role for complement in osteoarthritis. Nat. Med. 2011, 17:1674-1679.
94. Wuelling M., Vortkamp A. Transcriptional networks controlling chondrocyte proliferation and differentiation during endochondral ossification. Pediatr. Nephrol. 2010, 25:625-631.
95. Yamaguchi K., Sakiyama H., Matsumoto M., Moriya H., Sakiyama S. Degradation of type I and II collagen by human activated C1-s. FEBS Lett. 1990, 268:206-208.
96. Zhao C., Irie N., Takada Y., Shimoda K., Miyamoto T., Nishiwaki T., Suda T., Matsuo K. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab. 2006, 4:111-121.
97. Zhao M., Mueller B.M., DiScipio R.G., Schraufstatter I.U. Akt plays an important role in breast cancer cell chemotaxis to CXCL12. Breast Cancer Res. Treat. 2008, 110:211-222.
98. Zhou W. The new face of anaphylatoxins in immune regulation. Immunobiology 2011, 217:225-234.