Role for circulating osteogenic precursor cells in aortic valvular disease

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 12, 2011, Pages 2965-2971

  Egan, Kevin P ^a   Kim, Jung Hoon ^a   Mohler, Emile R ^a   Pignolo, Robert J ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

aging; blood cells; collagen; heart valves; pathology

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CD45 ANTIGEN; COLLAGEN TYPE 1; OSTEOCALCIN;

AORTA VALVE DISEASE; ARTICLE; FLOW CYTOMETRY; HEART VALVE; HEART VALVE STENOSIS; HETEROTOPIC OSSIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; OSTEOBLAST; OSTEOGENIC PRECURSOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

AGED; AGED, 80 AND OVER; ANTIGENS, CD45; AORTIC VALVE STENOSIS; CASE-CONTROL STUDIES; COLLAGEN TYPE I; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MESENCHYMAL STEM CELLS; OSSIFICATION, HETEROTOPIC; OSTEOCALCIN; OSTEOGENESIS; RETROSPECTIVE STUDIES;

EID: 81755173571     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.234724     Document Type: Article

References (54)

1. Mohler ER III. Mechanisms of aortic valve calcification. Am J Cardiol. 2004;94:1396-1402.
2. Mohler ER III, Gannon F, Reynolds C, Zimmerman R, Keane MG, Kaplan FS. Bone formation and inflammation in cardiac valves. Circulation. 2001;103:1522-1528. (Pubitemid 32226259)
3. Rajamannan NM, Subramaniam M, Rickard D, Stock SR, Donovan J, Springett M, Orszulak T, Fullerton DA, Tajik AJ, Bonow RO, Spelsberg T. Human aortic valve calcification is associated with an osteoblast phenotype. Circulation. 2003;107:2181-2184. (Pubitemid 36547209)
4. Suda RK, Billings PC, Egan KP, Kim JH, McCarrick-Walmsley R, Glaser DL, Porter DL, Shore EM, Pignolo RJ. Circulating osteogenic precursor cells in heterotopic bone formation. Stem Cells. 2009;27:2209-2219.
5. Pignolo RJ, Kassem M. Circulating osteogenic cells: implications for injury, repair, and regeneration. J Bone Miner Res. 2011;26:1-9.
6. Kiernan JA. Histological and Histochemical methods. 4th ed. Oxford, UK: Scion Publishing; 2008.
7. Cherian S, Moore J, Bantly A, Vergilio JA, Klein P, Luger S, Bagg A. Peripheral blood MDS score: a new flow cytometric tool for the diagnosis of myelodysplastic syndromes. Cytometry B Clin Cytom. 2005;64:9-17. (Pubitemid 40960407)
8. Roederer M. Spectral compensation for flow cytometry: visualization artifacts, limitations, and caveats. Cytometry. 2001;45:194-205. (Pubitemid 33064141)
9. Hunt JL, Fairman R, Mitchell ME, Carpenter JP, Golden M, Khalapyan T, Wolfe M, Neschis D, Milner R, Scoll B, Cusack A, Mohler ER III. Bone formation in carotid plaques: a clinicopathological study. Stroke. 2002;33:1214-1219. (Pubitemid 34517038)
10. Qiao JH, Mertens RB, Fishbein MC, Geller SA. Cartilaginous metaplasia in calcified diabetic peripheral vascular disease: morphologic evidence of enchondral ossification. Hum Pathol. 2003;34:402-407. (Pubitemid 36535026)
11. Dhore CR, Cleutjens JP, Lutgens E, Cleutjens KB, Geusens PP, Kitslaar PJ, Tordoir JH, Spronk HM, Vermeer C, Daemen MJ. Differential expression of bone matrix regulatory proteins in human atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2001;21:1998-2003. (Pubitemid 34219753)
12. Fitzpatrick LA, Turner RT, Ritman ER. Endochondral bone formation in the heart: a possible mechanism of coronary calcification. Endocrinology. 2003;144:2214-2219. (Pubitemid 36629869)
13. Mohler ER III, Adam LP, McClelland P, Graham L, Hathaway DR. Detection of osteopontin in calcified human aortic valves. Arterioscler Thromb Vasc Biol. 1997;17:547-552. (Pubitemid 27133146)
14. O'Brien KD, Kuusisto J, Reichenbach DD, Ferguson M, Giachelli C, Alpers CE, Otto CM. Osteopontin is expressed in human aortic valvular lesions. Circulation. 1995;92:2163-2168.
15. Srivatsa SS, Harrity PJ, Maercklein PB, Kleppe L, Veinot J, Edwards WD, Johnson CM, Fitzpatrick LA. Increased cellular expression of matrix proteins that regulate mineralization is associated with calcification of native human and porcine xenograft bioprosthetic heart valves. J Clin Invest. 1997;99:996-1009. (Pubitemid 27123637)
16. Rubin MR, Manavalan JS, Dempster DW, Shah J, Cremers S, Kousteni S, Zhou H, McMahon DJ, Kode A, Sliney J, Shane E, Silverberg SJ, Bilezikian JP. Parathyroid hormone stimulates circulating osteogenic cells in hypoparathyroidism. J Clin Endocrinol Metab. 2011;96:176-186.
17. Mohler ER III, Chawla MK, Chang AW, Vyavahare N, Levy RJ, Graham L, Gannon FH. Identification and characterization of calcifying valve cells from human and canine aortic valves. J Heart Valve Dis. 1999;8: 254-260. (Pubitemid 29274326)
18. Rajamannan NM, Subramaniam M, Springett M, Sebo TC, Niekrasz M, McConnell JP, Singh RJ, Stone NJ, Bonow RO, Spelsberg TC. Atorvastatin inhibits hypercholesterolemia-induced cellular proliferation and bone matrix production in the rabbit aortic valve. Circulation. 2002;105: 2660-2665. (Pubitemid 34596044)
19. Rajamannan NM. Calcific aortic stenosis: lessons learned from experimental and clinical studies. Arterioscler Thromb Vasc Biol. 2009;29: 162-168.
20. Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S. Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J Immunol. 2003;171:380-389. (Pubitemid 36745311)
21. Mirzaie M, Meyer T, Schwarz P, Lotfi S, Rastan A, Schondube F. Ultrastructural alterations in acquired aortic and mitral valve disease as revealed by scanning and transmission electron microscopical investigations. Ann Thorac Cardiovasc Surg. 2002;8:24-30.
22. Hishikawa K, Nakaki T, Fujii T. Transforming growth factor-2(1) induces apoptosis via connective tissue growth factor in human aortic smooth muscle cells. Eur J Pharmacol. 1999;385:287-290.
23. Jian B, Narula N, Li QY, Mohler ER III, Levy RJ. Progression of aortic valve stenosis: TGF-21 is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification via apoptosis. Ann Thorac Surg. 2003;75:457-465. (Pubitemid 36184488)
24. Tedgui A, Mallat Z. Anti-inflammatory mechanisms in the vascular wall. Circ Res. 2001;88:877-887. (Pubitemid 32441465)
25. Wallby L, Janerot-Sjoberg B, Steffensen T, Broqvist M. T lymphocyte infiltration in non-rheumatic aortic stenosis: a comparative descriptive study between tricuspid and bicuspid aortic valves. Heart. 2002;88: 348-351.
26. Olsson M, Dalsgaard CJ, Haegerstrand A, Rosenqvist M, Ryden L, Nilsson J. Accumulation of T lymphocytes and expression of interleukin-2 receptors in nonrheumatic stenotic aortic valves. J Am Coll Cardiol. 1994;23:1162-1170. (Pubitemid 24117151)
27. Otto CM, Kuusisto J, Reichenbach DD, Gown AM, O'Brien KD. Characterization of the early lesion of 'degenerative' valvular aortic stenosis: histological and immunohistochemical studies. Circulation. 1994;90: 844-853. (Pubitemid 24242754)
28. Shahi CN, Ghaisas NK, Goggins M, Foley B, Crean P, Kelleher D, Walsh M. Elevated levels of circulating soluble adhesion molecules in patients with nonrheumatic aortic stenosis. Am J Cardiol. 1997;79:980-982. (Pubitemid 27197939)
29. Ghaisas NK, Foley JB, O'Briain DS, Crean P, Kelleher D, Walsh M. Adhesion molecules in nonrheumatic aortic valve disease: endothelial expression, serum levels and effects of valve replacement. J Am Coll Cardiol. 2000;36:2257-2262.
30. Muller AM, Cronen C, Kupferwasser LI, Oelert H, Muller KM, Kirkpatrick CJ. Expression of endothelial cell adhesion molecules on heart valves: up-regulation in degeneration as well as acute endocarditis. J Pathol. 2000;191:54-60. (Pubitemid 30235649)
31. Cunningham NS, Paralkar V, Reddi AH. Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor 21 mRNA expression. Proc Natl Acad Sci USA. 1992;89:11740-11744. (Pubitemid 23004719)
32. Aikawa E, Nahrendorf M, Figueiredo JL, Swirski FK, Shtatland T, Kohler RH, Jaffer FA, Aikawa M, Weissleder R. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation. 2007;116:2841-2850. (Pubitemid 350301146)
33. New SE, Aikawa E. Molecular imaging insights into early inflammatory stages of arterial and aortic valve calcification. Circ Res. 2011;108: 1381-1391.
34. Fadini GP, Albiero M, Menegazzo L, Boscaro E, Vigili de Kreutzenberg S, Agostini C, Cabrelle A, Binotto G, Rattazzi M, Bertacco E, Bertorelle R, Biasini L, Mion M, Plebani M, Ceolotto G, Angelini A, Castellani C, Menegolo M, Grego F, Dimmeler S, Seeger F, Zeiher A, Tiengo A, Avogaro A. Widespread increase in myeloid calcifying cells contributes to ectopic vascular calcification in type 2 diabetes. Circ Res. 2011;108: 1112-1121.
35. Kan L, Liu Y, McGuire TL, Palila Berger DM, Awatramani RB, Dymecki SM, Kessler JA. Dysregulation of local stem/progenitor cells as a common cellular mechanism for heterotopic ossification. Stem Cells. 2009;27:150-156.
36. Yu PB, Deng DY, Lai CS, Hong CC, Cuny GD, Bouxsein ML, Hong DW, McManus PM, Katagiri T, Sachidanandan C, Kamiya N, Fukuda T, Mishina Y, Peterson RT, Bloch KD. BMP type I receptor inhibition reduces heterotopic ossification. Nat Med. 2008;14:1363-1369.
37. Lounev VY, Ramachandran R, Wosczyna MN, Yamamoto M, Maidment AD, Shore EM, Glaser DL, Goldhamer DJ, Kaplan FS. Identification of progenitor cells that contribute to heterotopic skeletogenesis. J Bone Joint Surg Am. 2009;91:652-663.
38. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol. 2001;166:7556-7562. (Pubitemid 32525636)
39. Kuwana M, Okazaki Y, Kodama H, Izumi K, Yasuoka H, Ogawa Y, Kawakami Y, Ikeda Y. Human circulating CD14f monocytes as a source of progenitors that exhibit mesenchymal cell differentiation. J Leukoc Biol. 2003;74:833-845. (Pubitemid 38040360)
40. Medbury HJ, Tarran SL, Guiffre AK, Williams MM, Lam TH, Vicaretti M, Fletcher JP. Monocytes contribute to the atherosclerotic cap by transformation into fibrocytes. Int Angiol. 2008;27:114-123. (Pubitemid 351796013)
41. Tanaka K, Sata M, Fukuda D, Suematsu Y, Motomura N, Takamoto S, Hirata Y, Nagai R. Age-associated aortic stenosis in apolipoprotein E-deficient mice. J Am Coll Cardiol. 2005;46:134-141. (Pubitemid 40905141)
42. Park HC, Yasuda K, Ratliff B, Stoessel A, Sharkovska Y, Yamamoto I, Jasmin JF, Bachmann S, Lisanti MP, Chander P, Goligorsky MS. Postobstructive regeneration of kidney is derailed when surge in renal stem cells during course of unilateral ureteral obstruction is halted. Am J Physiol Renal Physiol. 2010;298:F357-F364.
43. Jie KE, Zaikova MA, Bergevoet MW, Westerweel PE, Rastmanesh M, Blankestijn PJ, Boer WH, Braam B, Verhaar MC. Progenitor cells and vascular function are impaired in patients with chronic kidney disease. Nephrol Dial Transplant. 2010;25:1875-1882.
44. Bostrom KI, Jumabay M, Matveyenko A, Nicholas SB, Yao Y. Activation of vascular bone morphogenetic protein signaling in diabetes mellitus. Circ Res. 2011;108:446-457.
45. Wong WT, Tian XY, Chen Y, Leung FP, Liu L, Lee HK, Ng CF, Xu A, Yao X, Vanhoutte PM, Tipoe GL, Huang Y. Bone morphogenic protein-4 impairs endothelial function through oxidative stress-dependent cyclooxygenase-2 upregulation: implications on hypertension. Circ Res. 2010; 107:984-991.
46. Miriyala S, Gongora Nieto MC, Mingone C, Smith D, Dikalov S, Harrison DG, Jo H. Bone morphogenic protein-4 induces hypertension in mice: role of noggin, vascular NADPH oxidases, and impaired vasorelaxation. Circulation. 2006;113:2818-2825. (Pubitemid 44305294)
47. Csiszar A, Ahmad M, Smith KE, Labinskyy N, Gao Q, Kaley G, Edwards JG, Wolin MS, Ungvari Z. Bone morphogenetic protein-2 induces proinflammatory endothelial phenotype. Am J Pathol. 2006;168:629-638. (Pubitemid 43271160)
48. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864. (Pubitemid 39070860)
49. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY, Belperio JA, Keane MP, Strieter RM. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest. 2004; 114:438-446. (Pubitemid 39071616)
50. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G. HIF1f induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13:206-220. (Pubitemid 351318372)
51. Otsuru S, Tamai K, Yamazaki T, Yoshikawa H, Kaneda Y. Bone marrowderived osteoblast progenitor cells in circulating blood contribute to ectopic bone formation in mice. Biochem Biophys Res Commun. 2007; 354:453-458. (Pubitemid 46161345)
52. Otsuru S, Tamai K, Yamazaki T, Yoshikawa H, Kaneda Y. Circulating bone marrow-derived osteoblast progenitor cells are recruited to the bone-forming site by CXCR4/SDF-1 pathway. Stem Cells. 2008;26: 223-234.
53. Zhang M, Yan Y, Lim YB, Tang D, Xie R, Chen A, Tai P, Harris SE, Xing L, Qin YX, Chen D. BMP-2 modulateś-catenin signaling through stimulation of Lrp5 expression and inhibition oF2-TrCP expression in osteoblasts. J Cell Biochem. 2009;108:896-905.
54. Caira FC, Stock SR, Gleason TG, McGee EC, Huang J, Bonow RO, Spelsberg TC, McCarthy PM, Rahimtoola SH, Rajamannan NM. Human degenerative valve disease is associated with up-regulation of low-density lipoprotein receptor-related protein 5 receptor-mediated bone formation. J Am Coll Cardiol. 2006;47:1707-1712.