Increased presence of capillaries next to remodeling sites in adult human cancellous bone

Journal of Bone and Mineral Research

Volumn 28, Issue 3, 2013, Pages 574-585

  Kristensen, Helene Bjoerg ^a   Andersen, Thomas Levin ^a   Marcussen, Niels ^b   Rolighed, Lars ^c   Delaisse, Jean Marie ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

BONE REMODELING COMPARTMENT CANOPY; HUMAN CANCELLOUS BONE REMODELING; OSTEOBLAST PROGENITOR; VASCULATURE

Indexed keywords

CD34 ANTIGEN; SMOOTH MUSCLE ACTIN;

ADULT; AGED; ARTICLE; BONE MARROW; BONE REMODELING; CAPILLARY; CELL PROLIFERATION; ELECTRON MICROSCOPY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MICROSCOPY; MORPHOMETRICS; OSTEOBLAST; PERICYTE; PROTEIN EXPRESSION; TRABECULAR BONE; VASCULARIZATION;

ADULT; BONE AND BONES; CAPILLARIES; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON;

EID: 84873967833     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1760     Document Type: Article

References (54)

1. Martin T, Sims N, Ng K., Regulatory pathways revealing new approaches to the development of anabolic drugs for osteoporosis. Osteoporos Int. 2008 Aug 1; 19 (8): 1125-38.
2. Colnot C, Lu C, Hu D, Helms JA., Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Dev Biol. 2004 May 1; 269 (1): 55-69.
3. Schipani E, Maes C, Carmeliet G, Semenza GL., Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF. J Bone Miner Res. 2009 Aug; 24 (8): 1347-53.
4. Zelzer E, Olsen BR., Multiple roles of vascular endothelial growth factor (VEGF) in skeletal development, growth, and repair. Curr Top Dev Biol. 2005; 65: 169-87.
5. Glowacki J., Angiogenesis in fracture repair. Clin Orthop Relat Res. 1998 Oct; (355 Suppl); S82-9.
6. Pacicca DM, Patel N, Lee C, Salisbury K, Lehmann W, Carvalho R, Gerstenfeld LC, Einhorn TA., Expression of angiogenic factors during distraction osteogenesis. Bone. 2003 Dec; 33 (6): 889-98.
7. Towler DA., The osteogenic-angiogenic interface: novel insights into the biology of bone formation and fracture repair. Curr Osteoporos Rep. 2008 Jun; 6 (2): 67-71.
8. Baltadjiev G., Ultrastructural features in the structure of blood capillaries of the Haversian canal. Folia Med (Plovdiv). 1994; 36 (2): 47-53.
9. Marotti G, Zambonin Zallone A., Changes in the vascular network during the formation of Haversian systems. Cells Tissues Organs. 1980; 106 (1): 84-100.
10. Parfitt AM., Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J Cell Biochem. 1994 Jul; 55 (3): 273-86.
11. Brånemark PI., Bone marrow microvascular structure and function. Adv Microcirc. 1968; 1: 1-65.
12. Inoue S, Osmond DG., Basement membrane of mouse bone marrow sinusoids shows distinctive structure and proteoglycan composition: a high resolution ultrastructural study. Anat Rec. 2001; 264 (3): 294-304.
13. Laroche M., Intraosseous circulation from physiology to disease. Joint Bone Spine. 2002 May; 69 (3): 262-9.
14. Burkhardt R, Kettner G, Bohm W, Schmidmeier M, Schlag R, Frisch B, Mallmann B, Eisenmenger W, Gilg T., Changes in trabecular bone, hematopoiesis and bone marrow vessels in aplastic anemia, primary osteoporosis, and old age: a comparative histomorphometric study. Bone. 1987; 8 (3): 157-64.
15. Griffith JF, Yeung DK, Tsang PH, Choi KC, Kwok TC, Ahuja AT, Leung KS, Leung PC., Compromised bone marrow perfusion in osteoporosis. J Bone Miner Res. 2008 Jul; 23 (7): 1068-75.
16. Reeve J, Arlot M, Wootton R, Edouard C, Tellez M, Hesp R, Green JR, Meunier PJ., Skeletal blood flow, iliac histomorphometry, and strontium kinetics in osteoporosis: a relationship between blood flow and corrected apposition rate. J Clin Endocrinol Metab. 1988 Jun; 66 (6): 1124-31.
17. Prisby R, Guignandon A, Vanden-Bossche A, Mac-Way F, Linossier M-T, Thomas M, Laroche N, Malaval L, Langer M, Peter ZA, et al. Intermittent PTH(1-84) is osteoanabolic but not osteoangiogenic and relocates bone marrow blood vessels closer to bone-forming sites. J Bone Miner Res. 2011; 26 (11): 2583-96.
18. Parfitt AM., The mechanism of coupling: a role for the vasculature. Bone. 2000 Apr; 26 (4): 319-23.
19. Hauge EM, Qvesel D, Eriksen EF, Mosekilde L, Melsen F., Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J Bone Miner Res. 2001 Sep; 16 (9): 1575-82.
20. Andersen TL, Sondergaard TE, Skorzynska KE, Dagnaes-Hansen F, Plesner TL, Hauge EM, Plesner T, Delaisse JM., A physical mechanism for coupling bone resorption and formation in adult human bone. Am J Pathol. 2009 Jan; 174 (1): 239-47.
21. Eghbali-Fatourechi GZ, Mödder UIL, Charatcharoenwitthaya N, Sanyal A, Undale AH, Clowes JA, Tarara JE, Khosla S., Characterization of circulating osteoblast lineage cells in humans. Bone. 2007 May; 40 (5): 1370-7.
22. Parfitt AM., The bone remodeling compartment: a circulatory function for bone lining cells. J Bone Miner Res. 2001; 16 (9): 1583-5.
23. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schuger R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B., A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008 Sep 11; 3 (3): 301-13.
24. Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE., Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res. 1998 May; 13 (5): 828-38.
25. Kalajzic Z, Li H, Wang LP, Jiang X, Lamothe K, Adams DJ, Aguila HL, Rowe DW, Kalajzic I., Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population. Bone. 2008 Sep; 43 (3): 501-10.
26. Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, Mackem S, Carmeliet G, Kronenberg HM., Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell. 2010 Aug 17; 19 (2): 329-44.
27. Arnett TR., Acidosis, hypoxia and bone. Arch Biochem Biophys. 2010 Nov 1; 503 (1): 103-9.
28. Eliasson P, Jönsson JI., The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol. 2010; 222 (1): 17-22.
29. Manolagas SC, Almeida M., Gone with the Wnts: B-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol. 2007 Nov 1; 21 (11): 2605-14.
30. Bianco P., Bone and the hematopoietic niche: a tale of two stem cells. Blood. 2011 May 19; 117 (20): 5281-8.
31. Jensen PR, Andersen TL, Søe K, Hauge EM, Bollerslev J, Amling M, Barvencik F, Delaissé J-M., Premature loss of bone remodeling compartment canopies is associated with deficient bone formation: a study of healthy individuals and patients with Cushing's syndrome. J Bone Miner Res. 2012; 27 (4): 770-80.
32. Kinner B, Spector M., Expression of smooth muscle actin in osteoblasts in human bone. J Orthop Res. 2002 May; 20 (3): 622-32.
33. Sillaber C, Walchshofer S, Mosberger I, Gaiger A, Simonitsch I, Chott A, Lechner K, Valent P., Immunophenotypic characterization of human bone marrow endosteal cells. Tissue Antigens. 1999 Jun; 53 (6): 559-68.
34. Scholzen T, Gerdes J., The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000; 182 (3): 311-22.
35. Barou O, Mekraldi S, Vico L, Boivin G, Alexandre C, Lafage-Proust M-H., Relationships between trabecular bone remodeling and bone vascularization: a quantitative study. Bone. 2002 Apr; 30 (4): 604-12.
36. Roche B, David V, Vanden-Bossche A, Peyrin F, Malaval L, Vico L, Lafage-Proust M-H., Structure and quantification of microvascularisation within mouse long bones: What and how should we measure?. Bone. 2012 Jan; 50 (1): 390-9.
37. Rasmussen HB, Bordier PHJ., Bone cells-morphology and physiology. In:, Rasmussen HB, Bordier PHJ, The physiological and cellular basis of metabolic bone disease. Baltimore, MD: Williams and Wilkins; p. 8-70. 1974.
38. Bourke VA, Watchman CJ, Reith JD, Jorgensen ML, Dieudonné A, Bolch WE., Spatial gradients of blood vessels and hematopoietic stem and progenitor cells within the marrow cavities of the human skeleton. Blood. 2009 Nov 5; 114 (19): 4077-80.
39. Watchman CJ, Bourke VA, Lyon JR, Knowlton AE, Butler SL, Grier DD, Wingard JR, Braylan RC, Bolch WE., Spatial distribution of blood vessels and CD34+ hematopoietic stem and progenitor cells within the marrow cavities of human cancellous bone. J Nucl Med. 2007 Apr; 48 (4): 645-54.
40. Fina L, Molgaard HV, Robertson D, Bradley NJ, Monaghan P, Delia D, Sutherland DR, Baker MA, Greaves MF., Expression of the CD34 gene in vascular endothelial cells. Blood. 1990 Jun 15; 75 (12): 2417-26.
41. Krause DS, Fackler MJ, Civin CI, May WS., CD34: structure, biology, and clinical utility [see comments]. Blood. 1996 Jan 1; 87 (1): 1-13.
42. Brandi ML, Collin-Osdoby P., Vascular biology and the skeleton. J Bone Miner Res. 2006 Feb; 21 (2): 183-92.
43. Nilsson SK, Johnston HM, Coverdale JA., Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood. 2001 Apr 15; 97 (8): 2293-9.
44. Adams GB, Scadden DT., The hematopoietic stem cell in its place. Nat Immunol. 2006 Apr; 7 (4): 333-7.
45. Lo CC, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, Cote D, Rowe DW, Lin CP, Scadden DT., Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature. 2009 Jan 1; 457 (7225): 92-6.
46. Brighton CT, Lorich DG, Kupcha R, Reilly TM, Jones AR, Woodbury RA., The pericyte as a possible osteoblast progenitor cell. Clin Orthop Relat Res. 1992 Feb; (275); 287-99.
47. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L., Jr. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol. 2009 Jul; 24 (7): 909-69.
48. Bianco P, Riminucci M, Gronthos S, Robey PG., Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 2001; 19 (3): 180-92.
49. Lee YS, Chuong CM., Adhesion molecules in skeletogenesis: I. Transient expression of neural cell adhesion molecules (NCAM) in osteoblasts during endochondral and intramembranous ossification. J Bone Miner Res. 1992 Dec; 7 (12): 1435-46.
50. Anagnostis P, Karagiannis A, Kakafika A, Tziomalos K, Athyros V, Mikhailidis D., Atherosclerosis and osteoporosis: age-dependent degenerative processes or related entities?. Osteoporos Int. 2009; Feb 1; 20 (2): 197-207.
51. Pettit AR, Chang MK, Hume DA, Raggatt LJ., Osteal macrophages: a new twist on coupling during bone dynamics. Bone. 2008 Dec; 43 (6): 976-82.
52. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T., Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006 Jun; 12 (6): 657-64.
53. Kato J, Hisha H, Wang Xl, Mizokami T, Okazaki S, Li Q, Song Cy, Maki M, Hosaka N, Adachi Y, Inba M, Ikehara S., Contribution of neural cell adhesion molecule (NCAM) to hemopoietic system in monkeys. Ann Hematol. 2008 Oct 1; 87 (10): 797-807.
54. Bi LX, Mainous EG, Yngve DA, Buford WL., Cellular isolation, culture and characterization of the marrow sac cells in human tubular bone. J Musculoskelet Neuronal Interact. 2008 Jan; 8 (1): 43-9.