Immunohistochemical detection of activin A, follistatin, and activin receptors during fracture healing in the rat

Journal of Orthopaedic Research

Volumn 16, Issue 3, 1998, Pages 314-321

  Nagamine, T ^a   Imamura, T ^a   Ishidou, Y ^a   Kato, M ^a   Murata, F ^a   Ten Dijke, P ^a   Sakou, T ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; ANTIGEN-ANTIBODY REACTIONS; BINDING ENERGY; BIOMECHANICS; BONE; CELLS; FRACTURE FIXATION; GROWTH KINETICS; PROTEINS;

ACTIVIN A; ACTIVIN RECEPTORS; ENDOCHONDRAL OSSIFICATION; FOLLISTATIN; FRACTURE HEALING; IMMUNOHISTOCHEMICAL DETECTION;

IMMUNOLOGY;

ACTIVIN A; ACTIVIN RECEPTOR; FOLLISTATIN; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; ENCHONDRAL OSSIFICATION; FRACTURE HEALING; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 0032078468     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.1100160307     Document Type: Article

References (65)

1. 1 Attisano L, Wrana JL, Cheifetz S, Massagué J: Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68: 97–108, 1992
2. 2 Attisano L, Cárcamo J, Ventura F, Weis FMB, Massagué J, Wrana JL: Identification of human activin and TGF‐β type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75: 671–680, 1993
3. 3 Bolander ME: Regulation of fracture repair by growth factors. Proc Soc Exp Biol Med 200: 165–170, 1992
4. 4 Bonnarens F, Einhorn TA: Production of a standard closed fracture in laboratory animal bone. J Orthop Res 2: 97–101, 1984
5. 5 Burstone MS: Histochemical demonstration of acid phosphatase activity in osteoclasts. J Histochem Cytochem 7: 39–41, 1959
6. 6 Cácamo J, Weis FMB, Ventura F, Wieser R, Wrana JL, Attisano L, Massagué J: Type I receptors specify growth‐inhibitory and transcriptional responses to transforming growth factor β and activin. Mol Cell Biol 14: 3810–3821, 1994
7. 7 Centrella M, McCarthy TL, Canalis E: Activin‐A binding and biochemical effects in osteoblast‐enriched cultures from fetalrat parietal bone. Mol Cell Biol 11: 250–258, 1991
8. 8 Chen P, Yu YM, Reddi AH: Chondrogenesis in chick limb bud mesodermal cells: reciprocal modulation by activin and inhibin. Exp Cell Res 206: 119–127, 1993
9. 9 Erlebacher A, Filvaroff EH, Gitelman SE, Derynck R: Toward a molecular understanding of skeletal development. Cell 80: 371–378, 1995
10. 10 Eto Y, Tsuji T, Takezawa M, Takano S, Yokogawa Y, Shibai H: Purification and characterization of erythroid differentiation factor (EDF) isolated from human leukemia cell line THP‐1. Biochem Biophys Res Commun 142: 1095–1103, 1987
11. 11 Fang J, Yin W, Smiley E, Wang SQ, Bonadio J: Molecular cloning of the mouse activin βE subunit gene. Biochem Biophys Res Commun 228: 669–674, 1996
12. 12 Feijen A, Goumans MJ, van den Eijnden‐van Raaij AJ: Expression of activin subunits, activin receptors and follistatin in post‐implantation mouse embryos suggests specific developmental functions for different activins. Development 120: 3621–3637, 1994
13. 13 Funaba M, Ogawa K, Murata T, Fujimura H, Murata E, Abe M, Takahashi M, Torii K: Follistatin and activin in bone: expression and localization during endochondral bone development. Endocrinology 137: 4250–4259, 1996
14. 14 Hashimoto M, Shoda A, Inoue S, Yamada R, Kondo T, Sakurai T, Ueno N, Muramatsu M: Functional regulation of osteoblastic cells by the interaction of activin‐A with follistatin. J Biol Chem 267: 4999–5004, 1992
15. 15 Hayashi K, Ishidou Y, Yonemori K, Nagamine T, Origuchi N, Maeda S, Imamura T, Kato M, Yoshida H, Sampath TK, ten Dijke P, Sakou T: Expression and localization of bone morphogenetic proteins (BMPs) and BMP receptors in ossification of the ligamentum flavum. Bone 21: 23–30, 1997
16. 16 Hoodless PA, Haerry T, Ahdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL: MADRl, a MAD‐related protein that functions in BMP2 signaling pathways. Cell 85: 489–500, 1996
17. 17 Hosoi T, Inoue S, Hoshino S, Ouchi Y, Orimo H: Immunohis‐tochemical detection of activin A in osteoclasts. Gerontology 42 (Suppl 1): 20–24. 1996
18. 18 Hötten G, Neidhardt H, Schneider C, Pohl J: Cloning of a new member of the TGF‐β family: a putative new activin βC chain. Biochen Biophys Res Commun 206: 608–613. 1995
19. 19 Hsu SM, Raine L, Fanger H: Use of avidin‐biotin‐peruxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. dures J Histochem Cytochem 29: 577–580, 1981
20. 20 Ichijo H, Yamashita H, ten Dijke P, Eto Y, Heldin C‐H, Miyazono K: Characterization of in vivo phosphorylation of activin type II receptor. Biochem Biophys Res Commun 194: 1508–1514, 1993
21. 21 Inoue S, Nomura S, Hosoi T, Ouchi Y, Orimo H, Muramatsu M: Localization of follistatin, an activin‐binding prolein, in bone tissues. Calcif Tissue Int 55: 395–397, 1994
22. 22 Ishidou Y, Kitajima I, Obama H, Maruyama I, Murata F, Imamura T, Yamada N, ten Dijke P, Miyazono K, Sakou T: Enhanced expression of type I receptors for bone morphogenetic proteins during bone formation. J Bone Miner Res 10: 1651–1659, 1995
23. 23 Jemmerson R, Morrow PR, Klinman NR, Paterson Y: Analysis of an evolutionarily conserved antigenic site on mammalian cytochrome c using synthetic peptides. Proc Natl Acad Sci US A 82: 1508–1512, 1985
24. 24 Jiang T‐X, Yi J‐R, Ying S‐Y, Chuong C‐M: Activin enhances chondrogenesis of limb bud cells: stimulation of precartilaginous mesenchymal condensations and expression of NCAM. Dev Biol 155: 545–557, 1993
25. 25 Jingushi S, Heydemann A, Kana SK, Macey LR, Bolander ME: Acidic fibroblast growth factor (aFGF) injection stimulates cartilage enlargement and inhibits cartilage gene expression in rat fracture healing. J Orthop Res 8: 364–371, 1990
26. 26 Joyce ME, Jingushi S, Bolander ME: Transforming growth factor‐β in the regulation of fracture repair. Onhop Clin North Am 21: 199–209, 1990
27. 27 Luyten FP, Chen P, Paralkar V, Reddi AH: Recombinant bone morphogenetic protein‐4, transforming growth factor‐β1, and activin A enhance the cartilage phenotype of articular chondrocytes in vitro. Exp Cell Res 210: 224–229, 1994
28. 28 Massagué J, Attisano L, Wrana JL: The TGF‐β family and its composite receptors. Trends Cell Biol 4: 172–178, 1994
29. 29 Mathews LS, Vale WW: Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65: 973–982, 1991
30. 30 Mathews LS, Vale WW, Kintner CR: Cloning of a second type of activin receptor and functional characterization in Xenopus embryos. Science 255: 1702–1705, 1992
31. 31 Mathews LS: Activin receptors and cellular signaling by the receptor serine kinase family. Endocr Rev 15: 310–325, 1994
32. 32 Matzuk MM, Kumar TR, Bradley A: Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374: 356–360, 1995
33. 33 Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A: Functional analysis of activins during mammalian development. Nature 374: 354–356, 1995
34. 34 Nakamura T, Takio K, Eto Y, Shibai H, Titani K, Sugino H: Activin‐binding protein from rat ovary is follistatin. Science 247: 836–838, 1990
35. 35 Nakamura T, Sugino K, Titani K, Sugino H: Follistatin, an activin‐binding protein, associates with heparan sulfate chains of proteoglycans on follicular granulosa cells. J Biol Chem 266: 19432–19437, 1991
36. 36 Nash TJ, Howlett CR, Martin C, Steele J, Johnson KA, Hicklin DJ: Effect of platelet‐derived growth factor on tibial osteotomies in rabbits. Bone 15: 203–208, 1994
37. 37 Oda S, Nishimatsu S, Murakami K, Ueno N: Molecular cloning and functional analysis of a new activin β subunit: a dorsal mesoderm‐inducing activity in Xenopus. Biochem Biophys Res Commun 210: 581–588, 1995
38. 38 Ogawa Y, Schmidt DK, Nathan RM, Armstrong RM, Miller KL, Sawamura SJ, Ziman JM, Erickson KL, de Leon ER, Rosen DM, Seyedin SM, Glaser CB, Chang RJ, Corrigan AZ, Vale W: Bovine bone activin enhances bone morphogenetic protein‐induced ectopic bone formation. J Biol Chem 267: 14233–14237, 1992
39. 39 Onishi T, Ishidou Y, Nagamine T, Yone K, Imamura T, Kato M, Sampath TK, ten Dijke P, Sakou T: Distinct and overlapping patterns of localization of bone morphogenetic protein (BMP) family members and a BMP type II receptor during fracture healing in rats. Unpublished data
40. 40 Oue Y, Kanatani H, Kiyoki M, Eto Y, Ogata E, Matsumoto T: Effect of local injection of activin A on bone formation in newborn rats. Bone 15: 361–366, 1994
41. 41 Reddi AH: Bone morphogenetic proteins: an unconventional approach to isolation of first mammalian morphogens. Cytokine Growth Factor Rev 8: 11–20, 1997
42. 42 Robertson DM, Klein R, de Vos FL, McLachlan RI, Wettenhall REH, Hearn MTW, Burger HG, de Kretser DM: The isolation of polypeptides with FSH suppressing activity from bovine follicular fluid which are structurally different to inhibin. Biochem Biophys Res Commun 149: 744–749, 1987
43. 43 Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten DijKe P, Heldin C‐H, Miyazono K: Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci U S A 92: 7632–7636, 1995
44. 44 Saito S, Sugino K, Yamanouchi K, Kogawa K, Titani K, Shiota K, Takahashi M, Sugino H: Characterization of antisera directed against follistatin/activin‐binding protein peptides. Endocrinol Jpn 38: 377–382, 1991
45. 45 Sakai R, Eto Y, Ohtsuka M, Hirafuji M, Shinoda H: Activin enhances osteoclast‐like cell formation in vitro. Biochem Biophys Res Commun 195: 39–46, 1993
46. 46 Schubert D, Kimura H, LaCorbiere M, Vaughan J, Karr D, Fischer WH: Activin is a nerve cell survival molecule. Nature 344: 868–870, 1990
47. 47 Shiozaki M, Sakai R, Tabuchi M, Nakamura T, Sugino K, Sugino H, Eto Y: Evidence for the participation of endogeneous activin A/erythroid differentiation factor in the regulation of erythropoiesis. Proc Natl Acad Sci U S A 89: 1553–1556, 1992
48. 48 ShutoT, Sarkar G, Bronk JT, Matsui N, Bolander ME: Osteoblasts express types I and II activin receptors during early intramembranous and endochondral bone formation. J Bone Miner Res 12: 403–411, 1997
49. 49 Smith JC, Price BMJ, Van Nimmen K, Huylebroeck D: Identification of a potent Xenopus mesoderm‐inducing factor as a homologue of activin A. Nature 345: 729–731, 1990
50. 50 ten Dijke P, Franzen P, Yamashita H, Ichijo H, Heldin C‐H, Miyazono K: Serine/threonine kinase receptors. Prog Growth Factor Res 5: 55–72, 1994
51. 51 ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Helden C‐H, Miyazono K: Identification of type I receptors for osteogenic protein‐1 and bone morphogenetic protein‐4. J Biol Chem 269: 16985–16988, 1994
52. 52 ten Dijke P, Yamashita H, Ichijo H, Franzen P, Laiho M, Miyazono K, Heldin C‐H: Characterization of type I receptore for transforming growth factor‐β and activin. Science 264: 101–104, 1994
53. 53 Thaller SR, Hoyt J, Tesluk H, Holmes R: Effect of insulin‐like growth factor‐1 on zygomatic arch bone regeneration: a preliminary histological and histometric study. Ann Plast Surg 31: 421–428, 1993
54. 54 Thomsen G, Woolf T, Whitman M, Sokol S, Vaughan J, Vale W, Melton DA: Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63: 485–493, 1990
55. 55 Tsuchida K, Mathews LS, Vale WW: Cloning and characterization of a transmembrane serine kinase that acts as an activin type I receptor. Proc Natl Acad Sci U S A 90: 11242–11246, 1993
56. 56 Tsuchiya T, Matsumoto Y, Kurihara S: The fluorescent simultaneous azo dye technique for demonstration of tartrateresistant acid phosphatase (TRAP) activity in osteoclast‐like multinucleate cells. J Bone Miner Metab 13: 71–76, 1995
57. 57 Tuuri T, Erämaa M, Hildén K, Ritvos O: The tissue distribution of activin β A ‐and β B subunit and follistatin messenger ribonucleic acids suggests multiple sites of action for the activin‐follistatin system during human development. J Clin Endocrinol Metab 78: 1521–1524, 1994
58. 58 Ueno N, Ling N, Ying S‐Y, Esch F, Shimasaki S, Guillemin R: Isolation and partial characterization of follistatin: a singlechain Mr 35,000 monomeric protein that inhibits the release of follicle‐stimulating hormone. Proc Natl Acad Sci U S A 84: 8282–8286, 1987
59. 59 Vale W, Hsueh A, Rivier C, Yu J: The inhibin/activin family of hormones and growth factors. In: Peptide Growth Factors and Their Receptors: Handbook of Experimental Pharmacology, pp 211–248. Ed by MB Sporn and AB Roberts, Berlin, Springer‐Verlag, 1990
60. 60 van de Wijngaert FP, Burger EH: Demonstration of tartrate‐resistant acid phosphatase in un‐decalcified. glycolmethacrylate‐embedded mouse bone: a possible marker for (pre)osteoclast identification. J Histochem Cytochem 34: 1317–1323, 1986
61. 61 Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick R M, Wang EA: Novel regulators of bone formation: molecular cloning and activities. Science 242: 1528–1534, 1988
62. 62 Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang X‐F, Massagué J: TGFβ signals through a heteromeric protein kinase receptor complex. Cell 71: 1003–1014, 1992
63. 63 Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC, Heldin C‐H, Miyazono K: Osteogenic protein‐1 binds to activin type II receptors and induces certain activin‐like effects. J Cell Biol 130: 217–226, 1995
64. 64 Yamashita H, ten Dijke P, Heldin C‐H, Miyazono K: Bone morphogenetic protein receptors. Bone 19: 569–574, 1996
65. 65 Yonemori K, Imamura T, Ishidou Y, Okano T, Matsunaga S, Yoshida H, Kato M, Sampath TK, Miyazono K, ten Dijke P, Sakou T: Bone morphogenetic protein receptors and activin receptors are highly expressed in ossified ligament tissues of patients with ossification of the posterior longitudinal ligament. Am J Pathol 150: 1335–1347, 1997