Humoral response to therapeutic low-intensity pulsed ultrasound (LIPUS) treatment of rat maxillary socket after the removal of a molar tooth

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1 Humoral response to therapeutic low-intensity pulsed ultrasound (LIPUS) treatment of rat maxillary socket after the removal of a molar tooth Kouki Hidaka *1, Chihiro Miyamoto *2, Satoko Wada-Takahashi *3, Makiko Saita 4, Akira Kawata 5, Ryota Kawamata 6, Yojiro Maehata 2, Masato Minabe 1, Shun-suke Takahashi **3 and Yuko Mikuni-Takagaki 2 LIPUS treatment of the socket of removed first molar tooth from the upper jaws of retired breeder rats induced neovascularization at the wound site. In addition, LIPUS treatment transiently but significantly increased the blood flow rate at remote sites while transiently reducing the socket flow rate. In vivo preincubation with the EP4 receptor antagonist abrogated the LIPUS-induced reduction in socket flow rate, whereas the EP3 antagonist did not. Topical application of PGE2 to the socket also transiently reduced socket flow rate, whereas topical PGE2 to intact gingival epithelium did not. Moreover, increased CXCR4-positive tibia bone marrow cells without increased CXCL12 staining suggested the possibility that PGE2 released from the socket was responsible, at least in part, for the effects of LIPUS through the circulation directly affecting bone marrow cells. LIPUS exerts humoral effects on remote tissues through factor(s) released by mechanically stimulated cells in the healing oral tissues. LIPUS, Prostaglandin E2, Socket healing, CXCR4, Angiogenesis

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3 Int J Anal Bio-Sci Vol. 3, No 1 (2015) 5. Immunohistochemical analysis After LIPUS treatment for 2-weeks, isolated tissue pieces were trimmed and fixed with 4% PFA for two undecalcified sections were cut and placed on the films. The sections on the films were fixed and stored in 70% ethanol at -20. Except for VEGF staining, days, placed in 10% sucrose and 20% sucrose for more than 2 days each and into Super Cryo Embedding Medium (SCEM; Leica Microsystems Japan; Tokyo, Japan), and frozen at -103 in a UT2000F cooling unit (Tokyo Rikakikai, Co., Ltd; samples were decalcified with 10% formic acid for 10 min prior to immunostaining. The sections were washed three times with phosphate-buffered saline (PBS), treated with 0.1% Triton X-100/PBS for 10 min, washed another 3 times with PBS, and incubated Tokyo, Japan), which uses as coolant a solution of equal volumes of hexane and isopentane. In a cryomicrotome (CM3050S, Leica Microsystems GmbH, for 2 h at room temperature with primary antibodies against VEGF (1:50), CD34 (1:50), CXCL12 (1:100) and CXCR4 (1:1,000), all diluted in blocking PBS Wetzlar, Germany), the sample block surface was covered with an adhesive thin plastic CryofilmⅡ(9) solution containing 1.5% normal goat serum and 0.05% Triton X-100. The sections were washed with (Leica Microsystems) and serial 3-µm thick frozen PBS and subsequently incubated for 1 h with Fig. 2 Fig. 1 Histologic morphology of healing sockets with regenerated gingival epithelium after LIPUS treatment for 2 weeks. A: LIPUS treated rat socket at the original magnification of x4. B: LIPUS treated rat socket at the original magnification of x10. C: mock treated rat socket at the original magnification of x4. D: mock treated rat socket at the original magnification of x10. Hematoxylin and eosin staining was performed with 3- µm thick sections after decalcification with 10% formic acid. Squared areas in (A) and (C) were magnified in (B) and (D). Scale bars = 300 µm. 19 Profiles of CD34 and VEGF immunohistochemical staining of healing sockets after LIPUS treatment for two weeks. A: Socket tissue sections from a LIPUS-treated rat to detect endothelial cells, and B: from a mock-treated rat. C: Socket tissue sections from a LIPUS-treated rat to detect secreted VEGF, and D: from a mock-treated rat. Sections were decalcified and incubated with anti-cd34 primary antibody and Alexa 488 conjugated secondary antibody in (A) and (B) or anti-vegf primary antibody and Alexa 546 conjugated secondary antibody without decalcification in (C) and (D). Arrowheads indicate the areas of intense staining. Scale bars = 300 µm.

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6 International Journal of Analytical Bio-Science The blood flow rate in the tail, which is also remote from the wound/lipus exposure site, tended to be elevated and was significant on day 14. Injection of the marrow (B vs. C). No significant difference was seen EP4 receptor antagonist L-161,982 prior to LIPUS treatment completely abrogated the effects of LIPUS treatment, whereas the EP3 receptor antagonist L798,106 had no effect, suggesting that the effects of LIPUS are dependent on PGE2 (Fig. 4C). In contrast, topical application of PGE 2 to socket epithelium mimicked the effects of LIPUS by reducing the blood flow rate in the socket. 4. Discussion ization and increased the density and possibly the width of peripheral blood vessels in the wound site of sockets from which teeth had been removed. Immunohistochemical analysis showed increased CD34 and VEGF staining, indicating that LIPUS had 4. Effect of LIPUS on the CXCL12-CXCR4 axis of cell recruitment from tibial bone marrow Levels of CXCR4 and CXCL12 proteins were assessed immunochemically in bone marrow cells angiogenic effects in the socket. LIPUS exposure increased the baseline blood flow rate in the socket, suggesting that LIPUS increased the width of peripheral blood vessels in the socket. Elevated blood flow was not observed in the tail or the foot, indicating that (BMCs) of the sagittal sections of tibias derived from LIPUS-treated and control rats as in Fig. 5. In Fig. 5A, the equivalent area depicted in Fig. 5B, C, D and E the effects of socket LIPUS exposure did not alter the blood vessels at distant sites. LIPUS exposure also transiently reduced blood flow rate in the socket, was framed in a film section of proximal half of the whole tibia. With CXCR4 antibody, more intense beginning after 7 days of LIPUS exposure, accompanied by increased blood flow rates at remote sites staining was detected in LIPUS-treated rat bone such as the feet. Pretreatment with EP receptor antag- Fig. 5 with CXCL12 antibody (D vs. E). Results show that LIPUS induced neovascular- Profiles of CXCR4 immunohistochemical staining of tibial bone marrow after LIPUS treatment for two weeks. A: sagittal section of the proximal end of tibia prepared on a film as described in Materials and Methods. B: Equivalent area to that in the box in (A) was tested for BMC recruitment in the LIPUS-treated rat. C: Equivalent area to that in the box in (A) was tested for BMC recruitment in the control rat. Tissue sections were stained with anticxcr4 primary antibody and Alexa 546 conjugated secondary antibody after decalcification. Scale bar = 1 mm in (A) and 100 µm in (B) to (E). Note that more cells with intense staining were seen in (B) than in (C). On the other hand, sections stained with anti-cxcl12 primary antibody and Alexa 488 conjugated secondary antibody after decalcification in (D) and (E) did not give any significant difference. 22

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