Leukocyte-platelet-rich plasma (L-PRP) induces an abnormal histophenotype in craniofacial bone repair associated with changes in the immunopositivity of the hematopoietic clusters of differentiation, osteoproteins, and TGF-β1

Clinical Implant Dentistry and Related Research

Volumn 16, Issue 2, 2014, Pages 259-272

  Giovanini, Allan Fernando ^a   Grossi, João Ricardo Almeida ^a   Gonzaga, Carla Castiglia ^a   Zielak, João Cesar ^a   Göhringer, Isabella ^a   Vieira, Juliana de Souza ^a   Kuczera, Juliane ^a   Filho, Marco Antonio de Oliveira ^b   Deliberador, Tatiana Miranda ^a  

^a POSITIVO UNIVERSITY   (Brazil)

^b University Evangelic Hospital   (Brazil)

Author keywords

BMP 2; Bone regeneration; CD34; CD45; Platelet rich plasma; Runx2

Indexed keywords

BONE MORPHOGENETIC PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; BONE DEVELOPMENT; CELL DIFFERENTIATION; FEMALE; LEUKOCYTE; PHYSIOLOGY; RABBIT; THROMBOCYTE RICH PLASMA;

ANIMALS; BONE DEVELOPMENT; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; FEMALE; LEUKOCYTES; PLATELET-RICH PLASMA; RABBITS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84899634794     PISSN: 15230899     EISSN: 17088208     Source Type: Journal    
DOI: 10.1111/j.1708-8208.2012.00478.x     Document Type: Article

References (73)

1. Aghaloo TL, Moy PK, Freymiller EG. Evaluation of platelet-rich plasma in combination with anorganic bovine bone in the rabbit cranium: a pilot study. Int J Oral Maxillofac Implants 2004; 19:59-65.
2. Freymiller EG, Aghaloo TL. Platelet-rich plasma: ready or not? J Oral Maxillofac Surg 2004; 62:484-488.
3. Marx RE. Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 2004; 62:489-496.
4. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood 2003; 102:449-461.
5. Roberts DE, McNicol A, Bose R. Mechanism of collagen activation in human platelets. J Biol Chem 2004; 279:19421-19430.
6. Eppley BL, Woodell JE, Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg 2004; 114:1502-1508.
7. Mooren RE, Hendriks EJ, van den Beucken JJ, etal. The effect of platelet-rich plasma in vitro on primary cells: rat osteoblast-like cells and human endothelial cells. Tissue Eng Part A 2010; 16:3159-3172.
8. Intini G. The use of platelet-rich plasma in bone reconstruction therapy. Biomaterials 2009; 30:4956-4966.
9. Nikolidakis D, Jansen JA. The biology of platelet-rich plasma and its application in oral surgery: literature review. Tissue Eng Part B Rev 2008; 14:249-258.
10. Balaguer T, Boukhechba F, Clave A, etal. Biphasic calcium phosphate microparticles for bone formation: benefits of combination with blood clot. Tissue Eng Part A 2010; 16:3495-3505.
11. Arnoczky SP, Delos D, Rodeo SA. What is platelet-rich plasma? Operative techniques in sports. Medicine 2011; 19:142-148.
12. Dohan Ehrenfest DM, Rasmusson L, Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol 2009; 27:158-167.
13. Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeff KR. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998; 85:638-646.
14. Giovanini AF, Deliberador TM, Gonzaga CC, etal. Platelet-rich plasma diminishes calvarial bone repair associated with alterations in collagen matrix composition and elevated CD34+ cell prevalence. Bone 2010; 46:1597-1603.
15. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem 2006; 98:251-266.
16. Kassem M, Abdallah BM, Saeed H. Osteoblastic cells: differentiation and trans-differentiation. Arch Biochem Biophys 2008; 473:183-187.
17. Schaffler A, Muller-Ladner U, Scholmerich J, Buchler C. Role of adipose tissue as an inflammatory organ in human diseases. Endocr Rev 2006; 27:449-467.
18. Zhou L, Nguyen AN, Sohal D, etal. Inhibition of the TGF-beta receptor I kinase promotes hematopoiesis in MDS. Blood 2008; 112:3434-3443.
19. Fortunel NO, Hatzfeld A, Hatzfeld JA. Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis. Blood 2000; 96:2022-2036.
20. Majeti R, Park CY, Weissman IL. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell 2007; 1:635-645.
21. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303:83-86.
22. Paquette R, Dorshkind K. Optimizing hematopoietic recovery following bone marrow transplantation. J Clin Invest 2002; 109:1527-1528.
23. Shivtiel S, Kollet O, Lapid K, etal. CD45 regulates retention, motility, and numbers of hematopoietic progenitors, and affects osteoclast remodeling of metaphyseal trabecules. J Exp Med 2008; 205:2381-2395.
24. Craig W, Poppema S, Little MT, Dragowska W, Lansdorp PM. CD45 isoform expression on human haemopoietic cells at different stages of development. Br J Haematol 1994; 88:24-30.
25. Penninger JM, Irie-Sasaki J, Sasaki T, Oliveira-dos-Santos AJ. CD45: new jobs for an old acquaintance. Nat Immunol 2001; 2:389-396.
26. Oki Y, Watanabe S, Endo T, Kano K. Mature adipocyte-derived dedifferentiated fat cells can trans-differentiate into osteoblasts in vitro and in vivo only by all-trans retinoic acid. Cell Struct Funct 2008; 33:211-222.
27. Rosen V. BMP2 signaling in bone development and repair. Cytokine Growth Factor Rev 2009; 20:475-480.
28. Wang Q, Huang C, Xue M, Zhang X. Expression of endogenous BMP-2 in periosteal progenitor cells is essential for bone healing. Bone 2011; 48:524-532.
29. Abzhanov A, Rodda SJ, McMahon AP, Tabin CJ. Regulation of skeletogenic differentiation in cranial dermal bone. Development 2007; 134:3133-3144.
30. Nie X, Luukko K, Kettunen P. BMP signalling in craniofacial development. Int J Dev Biol 2006; 50:511-521.
31. Wan DC, Shi YY, Nacamuli RP, Quarto N, Lyons KM, Longaker MT. Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling. Proc Natl Acad Sci U S A 2006; 103:12335-12340.
32. Sahni V, Mukhopadhyay A, Tysseling V, etal. BMPR1a and BMPR1b signaling exert opposing effects on gliosis after spinal cord injury. J Neurosci 2010; 30:1839-1855.
33. Ashique AM, Fu K, Richman JM. Signalling via type IA and type IB bone morphogenetic protein receptors (BMPR) regulates intramembranous bone formation, chondrogenesis and feather formation in the chicken embryo. Int J Dev Biol 2002; 46:243-253.
34. Chen D, Ji X, Harris MA, etal. Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J Cell Biol 1998; 142:295-305.
35. Di Cataldo S, Ficarra E, Acquaviva A, Macii E. Automated segmentation of tissue images for computerized IHC analysis. Comput Methods Programs Biomed 2010; 100:1-15.
36. Boilard E, Nigrovic PA, Larabee K, etal. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327:580-583.
37. Klongnoi B, Rupprecht S, Kessler P, Thorwarth M, Wiltfang J, Schlegel KA. Influence of platelet-rich plasma on a bioglass and autogenous bone in sinus augmentation. An explorative study. Clin Oral Implants Res 2006; 17:312-320.
38. Klongnoi B, Rupprecht S, Kessler P, etal. Lack of beneficial effects of platelet-rich plasma on sinus augmentation using a fluorohydroxyapatite or autogenous bone: an explorative study. J Clin Periodontol 2006; 33:500-509.
39. Fennis JP, Stoelinga PJ, Jansen JA. Mandibular reconstruction: a histological and histomorphometric study on the use of autogenous scaffolds, particulate cortico-cancellous bone grafts and platelet rich plasma in goats. Int J Oral Maxillofac Surg 2004; 33:48-55.
40. Aghaloo TL, Moy PK, Freymiller EG. Investigation of platelet-rich plasma in rabbit cranial defects: a pilot study. J Oral Maxillofac Surg 2002; 60:1176-1181.
41. Jakse N, Tangl S, Gilli R, etal. Influence of PRP on autogenous sinus grafts. An experimental study on sheep. Clin Oral Implants Res 2003; 14:578-583.
42. Pryor ME, Yang J, Polimeni G, etal. Analysis of rat calvaria defects implanted with a platelet-rich plasma preparation: radiographic observations. J Periodontol 2005; 76:1287-1292.
43. Chizzolini C, Brembilla NC, Montanari E, Truchetet ME. Fibrosis and immune dysregulation in systemic sclerosis. Autoimmun Rev 2011; 10:276-281.
44. Sangaletti S, Tripodo C, Cappetti B, etal. SPARC oppositely regulates inflammation and fibrosis in bleomycin-induced lung damage. Am J Pathol 2011; 179:3000-3010.
45. Tomasek JJ, McRae J, Owens GK, Haaksma CJ. Regulation of alpha-smooth muscle actin expression in granulation tissue myofibroblasts is dependent on the intronic CArG element and the transforming growth factor-beta1 control element. Am J Pathol 2005; 166:1343-1351.
46. Nagata MJ, Messora M, Pola N, etal. Influence of the ratio of particulate autogenous bone graft/platelet-rich plasma on bone healing in critical-size defects: a histologic and histometric study in rat calvaria. J Orthop Res 2010; 28:468-473.
47. Nagata M, Messora M, Okamoto R, etal. Influence of the proportion of particulate autogenous bone graft/platelet-rich plasma on bone healing in critical-size defects: an immunohistochemical analysis in rat calvaria. Bone 2009; 45:339-345.
48. Merrill AE, Eames BF, Weston SJ, Heath T, Schneider RA. Mesenchyme-dependent BMP signaling directs the timing of mandibular osteogenesis. Development 2008; 135:1223-1234.
49. Canalis E, Economides AN, Gazzerro E. Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 2003; 24:218-235.
50. Rawadi G, Vayssiere B, Dunn F, Baron R, Roman-Roman S. BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J Bone Miner Res 2003; 18:1842-1853.
51. Roman-Roman S, Garcia T, Jackson A, etal. Identification of genes regulated during osteoblastic differentiation by genome-wide expression analysis of mouse calvaria primary osteoblasts in vitro. Bone 2003; 32:474-482.
52. Fritsch G, Buchinger P, Printz D, etal. Rapid discrimination of early CD34+ myeloid progenitors using CD45-RA analysis. Blood 1993; 81:2301-2309.
53. Strobl H, Takimoto M, Majdic O, etal. Myeloperoxidase expression in CD34+ normal human hematopoietic cells. Blood 1993; 82:2069-2078.
54. Oliveira Filho MA, Nassif PA, Malafaia O, etal. Effects of a highly concentrated platelet-rich plasma on the bone repair using non-critical defects in the calvaria of rabbits. Acta Cir Bras 2010; 25:28-33.
55. Choi BH, Im CJ, Huh JY, Suh JJ, Lee SH. Effect of platelet-rich plasma on bone regeneration in autogenous bone graft. Int J Oral Maxillofac Surg 2004; 33:56-59.
56. Fauvel F, Legrand YJ. Inhibition of type III collagen induced platelet aggregation by active alpha 1 (III) CB4 peptide fragments. Thromb Res 1980; 17:285-287.
57. Chiang TM, Seyer JM, Kang AH. Collagen-platelet interaction: separate receptor sites for types I and III collagen. Thromb Res 1993; 71:443-456.
58. Chiang TM, Zhu J, Woo-Rasberry V. Peptides derived from platelet non-integrin collagen-receptors or types I and III collagen inhibit collagen-platelet interaction. Cardiovasc Hematol Disord Drug Targets 2007; 7:71-75.
59. Sakariassen KS, Joss R, Muggli R, etal. Collagen type III induced ex vivo thrombogenesis in humans. Role of platelets and leukocytes in deposition of fibrin. Arteriosclerosis 1990; 10:276-284.
60. Zhu J, Cole F, Woo-Rasberry V, Fang XR, Chiang TM. Type I and type III collagen-platelet interaction: inhibition by type specific receptor peptides. Thromb Res 2007; 119:111-119.
61. Gronthos S, Stewart K, Graves SE, Hay S, Simmons PJ. Integrin expression and function on human osteoblast-like cells. J Bone Miner Res 1997; 12:1189-1197.
62. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007; 117:524-529.
63. Wells RG. Fibrogenesis. V. TGF-beta signaling pathways. Am J Physiol Gastrointest Liver Physiol 2000; 279:G845-G850.
64. Pohlers D, Brenmoehl J, Loffler I, etal. TGF-beta and fibrosis in different organs - molecular pathway imprints. Biochim Biophys Acta 2009; 1792:746-756.
65. Giovanini AF, Gonzaga CC, Zielak JC, etal. Platelet-rich plasma (PRP) impairs the craniofacial bone repair associated with its elevated TGF-beta levels and modulates the co-expression between collagen III and alpha-smooth muscle actin. J Orthop Res 2011; 29:457-463.
66. Zhang J, Niu C, Ye L, etal. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425:836-841.
67. Spinella-Jaegle S, Roman-Roman S, Faucheu C, etal. Opposite effects of bone morphogenetic protein-2 and transforming growth factor-beta1 on osteoblast differentiation. Bone 2001; 29:323-330.
68. Kang JS, Alliston T, Delston R, Derynck R. Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3. EMBO J 2005; 24:2543-2555.
69. Gimble JM, Nuttall ME. Bone and fat: old questions, new insights. Endocrine 2004; 23:183-188.
70. Choy L, Derynck R. Transforming growth factor-beta inhibits adipocyte differentiation by Smad3 interacting with CCAAT/enhancer-binding protein (C/EBP) and repressing C/EBP transactivation function. J Biol Chem 2003; 278:9609-9619.
71. Thorwarth M, Wehrhan F, Schultze-Mosgau S, Wiltfang J, Schlegel KA. PRP modulates expression of bone matrix proteins in vivo without long-term effects on bone formation. Bone 2006; 38:30-40.
72. Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG. Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 2006; 38:758-768.
73. van den Bos T, Speijer D, Bank RA, Bromme D, Everts V. Differences in matrix composition between calvaria and long bone in mice suggest differences in biomechanical properties and resorption: special emphasis on collagen. Bone 2008; 43:459-468.