Isolation and characterization of human anterior cruciate ligament-derived vascular stem cells

Stem Cells and Development

Volumn 21, Issue 6, 2012, Pages 859-872

  Matsumoto, Tomoyuki ^a,b,c   Ingham, Sheila M ^a,b   Mifune, Yutaka ^a,b,c   Osawa, Aki ^a,b   Logar, Alison ^a   Usas, Arvydas ^a   Kuroda, Ryosuke ^c   Kurosaka, Masahiro ^c   Fu, Freddie H ^b   Huard, Johnny ^a,b,d  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD146 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN;

ADIPOGENESIS; ADULT; ANGIOGENESIS; ANTERIOR CRUCIATE LIGAMENT; ANTERIOR CRUCIATE LIGAMENT RUPTURE; ARTICLE; BLOOD VESSEL; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; FETUS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; OSTEOBLAST; PRIORITY JOURNAL; STEM CELL; VASCULAR STEM CELL;

ANTERIOR CRUCIATE LIGAMENT; ANTIGENS, CD146; ANTIGENS, CD34; BLOOD VESSELS; CELL DIFFERENTIATION; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; STEM CELLS; WOUND HEALING;

EID: 84859405907     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2010.0528     Document Type: Article

References (60)

1. Agung M, M Ochi, S Yanada, N Adachi, Y Izuta, T Yamasaki and K Toda. (2006). Mobilization of bone marrow-derived mesenchymal stem cells into the injured tissues afterintraarticular injection and their contribution to tissue regeneration. Knee Surg Sports Traumatol Arthrosc 14:1307-1314.
2. Griffin LY, J Agel, MJ Albohm, EA Arendt, RW Dick, WE Garrett, JG Garrick, TE Hewett, L Huston, et al. (2000). Noncontact anterior cruciate ligament injuries: risk factors and prevention strategies. J Am Acad Orthop Surg 8:141-150.
3. Girgis FG, JL Marshall and A Monajem. (1975). The cruciate ligaments of the knee joint. Anatomical, functional and experimental analysis. Clin Orthop Relat Res (106):216-231.
4. Harner CD, GH Baek, TM Vogrin, GJ Carlin, S Kashiwaguchi and SL Woo. (1999). Quantitative analysis of human cruciate ligament insertions. Arthroscopy 15:741-749.
5. Kurosawa H, K Yamakoshi, K Yasuda and T Sasaki. (1991). Simultaneous measurement of changes in length of the cruciate ligaments during knee motion. Clin Orthop Relat Res (265):233-240.
6. Dienst M, RT Burks and PE Greis. (2002). Anatomy and biomechanics of the anterior cruciate ligament. Orthop Clin North Am 33:605-620, v.
7. Duthon VB, C Barea, S Abrassart, JH Fasel, D Fritschy and J Menetrey. (2006). Anatomy of the anterior cruciate ligament. Knee Surg Sports Traumatol Arthrosc 14:204-213.
8. Ferretti M, EA Levicoff, TA Macpherson, MS Moreland, M Cohen and FH Fu. (2007). The fetal anterior cruciate ligament: an anatomic and histologic study. Arthroscopy 23:278-283.
9. Ballock RT, SL Woo, RM Lyon, JM Hollis and WH Akeson. (1989). Use of patellar tendon autograft for anterior cruciate ligament reconstruction in the rabbit: a long-term histologic and biomechanical study. J Orthop Res 7:474-485.
10. Grana WA, DM Egle, R Mahnken and CW Goodhart. (1994). An analysis of autograft fixation after anterior cruciate ligament reconstruction in a rabbit model. Am J Sports Med 22:344-351.
11. Woo SL, M Inoue, E McGurk-Burleson and MA Gomez. (1987). Treatment of the medial collateral ligament injury. II: Structure and function of canine knees in response to differing treatment regimens. Am J Sports Med 15:22-29.
12. Weiss JA, SL Woo, KJ Ohland, S Horibe and PO Newton. (1991). Evaluation of a new injury model to study medial collateral ligament healing: primary repair versus nonoperative treatment. J Orthop Res 9:516-528.
13. Petrigliano FA, DR McAllister and BM Wu. (2006). Tissue engineering for anterior cruciate ligament reconstruction: a review of current strategies. Arthroscopy 22:441-451.
14. Frank CB and DW Jackson. (1997). The science of reconstruction of the anterior cruciate ligament. J Bone Joint Surg Am 79:1556-1576.
15. Murray MM, SD Martin, TL Martin and M Spector. (2000). Histological changes in the human anterior cruciate ligament after rupture. J Bone Joint Surg Am 82-A:1387-1397.
16. Sandberg R, B Balkfors, B Nilsson and N Westlin. (1987). Operative versus non-operative treatment of recent injuries to the ligaments of the knee. A prospective randomized study. J Bone Joint Surg Am 69:1120-1126.
17. Kurosaka M, S Yoshiya, T Mizuno and K Mizuno. (1998). Spontaneous healing of a tear of the anterior cruciate ligament. A report of two cases. J Bone Joint Surg Am 80:1200-1203.
18. Fujimoto E, Y Sumen, M Ochi and Y Ikuta. (2002). Spontaneous healing of acute anterior cruciate ligament (ACL) injuries-conservative treatment using an extension block soft brace without anterior stabilization. Arch Orthop Trauma Surg 122:212-216.
19. Marshall JL, RF Warren, TL Wickiewicz and B Reider. (1979). The anterior cruciate ligament: a technique of repair and reconstruction. Clin Orthop Relat Res (143):97-106.
20. Marshall JL, RF Warren and TL Wickiewicz. (1982). Primary surgical treatment of anterior cruciate ligament lesions. Am J Sports Med 10:103-107.
21. Strand T, A Molster, M Hordvik and Y Krukhaug. (2005). Long-term follow-up after primary repair of the anterior cruciate ligament: clinical and radiological evaluation 15-23 years postoperatively. Arch Orthop Trauma Surg 125:217-221.
22. Drogset JO, T Grontvedt, OR Robak, A Molster, AT Viset and L Engebretsen. (2006). A sixteen-year follow-up of three operative techniques for the treatment of acute ruptures of the anterior cruciate ligament. J Bone Joint Surg Am 88: 944-952.
23. Lee IC, JH Wang, YT Lee and TH Young. (2007). Development of a useful technique to discriminate anterior cruciate ligament cells and mesenchymal stem cells-the application of cell electrophoresis. J Biomed Mater Res A 82:230-237.
24. Lee SY, M Miwa, Y Sakai, R Kuroda, T Matsumoto, T Iwakura, H Fujioka, M Doita and M Kurosaka. (2007). In vitro multipotentiality and characterization of human unfractured traumatic hemarthrosis-derived progenitor cells: a potential cell source for tissue repair. J Cell Physiol 210:561-566.
25. Tavian M, B Zheng, E Oberlin, M Crisan, B Sun, J Huard and B Peault. (2005). The vascular wall as a source of stem cells. Ann N Y Acad Sci 1044:41-50.
26. Howson KM, AC Aplin, M Gelati, G Alessandri, EA Parati and RF Nicosia. (2005). The postnatal rat aorta contains pericyte progenitor cells that form spheroidal colonies in suspension culture. Am J Physiol Cell Physiol 289:C1396-C1407.
27. Zengin E, F Chalajour, UM Gehling, WD Ito, H Treede, H Lauke, J Weil, H Reichenspurner, N Kilic and S Ergun. (2006). Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development 133:1543-1551.
28. Crisan M, S Yap, L Casteilla, CW Chen, M Corselli, TS Park, G Andriolo, B Sun, B Zheng, et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301-313.
29. Zheng B, B Cao, M Crisan, B Sun, G Li, A Logar, S Yap, JB Pollett, L Drowley, et al. (2007). Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25:1025-1034.
30. Crisan M, B Deasy, M Gavina, B Zheng, J Huard, L Lazzari and B Peault. (2008). Purification and long-term culture of multipotent progenitor cells affiliated with the walls of human blood vessels: myoendothelial cells and pericytes. Methods Cell Biol 86:295-309.
31. Zheng B, B Cao, G Li and J Huard. (2006). Mouse adiposederived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng 12:1891-1901.
32. Zuk PA, M Zhu, H Mizuno, J Huang, JW Futrell, AJ Katz, P Benhaim, HP Lorenz and MH Hedrick. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228.
33. Barry F, RE Boynton, B Liu and JM Murphy. (2001). Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components. Exp Cell Res 268:189-200.
34. Johnstone B, TM Hering, AI Caplan, VM Goldberg and JU Yoo. (1998). In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265-272.
35. Mackay AM, SC Beck, JM Murphy, FP Barry, CO Chichester and MF Pittenger. (1998). Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4:415-428.
36. Asahara T, T Murohara, A Sullivan, M Silver, R van der Zee, T Li, B Witzenbichler, G Schatteman and JM Isner. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967.
37. Bahlmann FH, K De Groot, JM Spandau, AL Landry, B Hertel, T Duckert, SM Boehm, J Menne, H Haller and D Fliser (2004). Erythropoietin regulates endothelial progenitor cells. Blood 103:921-926.
38. Ma FX, LY Liu and XM Xiong. (2003). Protective effects of lovastatin on vascular endothelium injured by low density lipoprotein. Acta Pharmacol Sin 24:1027-1032.
39. Soeda S, T Kozako, K Iwata and H Shimeno. (2000). Oversulfated fucoidan inhibits the basic fibroblast growth factor-induced tube formation by human umbilical vein endothelial cells: its possible mechanism of action. Biochim Biophys Acta 1497:127-134.
40. Merida-Velasco JA, I Sanchez-Montesinos, J Espin-Ferra, JR Merida-Velasco, JF Rodriguez-Vazquez and J Jimenez- Collado. (1997). Development of the human knee joint ligaments. Anat Rec 248:259-268.
41. Gardner E and R O'Rahilly. (1968). The early development of the knee joint in staged human embryos. J Anat 102:289-299.
42. Scapinelli R. (1997). Vascular anatomy of the human cruciate ligaments and surrounding structures. Clin Anat 10:151-162.
43. Covas DT, RA Panepucci, AM Fontes, WA Silva, Jr., MD Orellana, MC Freitas, L Neder, AR Santos, LC Peres, MC Jamur and MA Zago. (2008). Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146 + perivascular cells and fibroblasts. Exp Hematol 36:642-654.
44. Yeh ET, S Zhang, HD Wu, M Korbling, JT Willerson and Z Estrov. (2003). Transdifferentiation of human peripheral blood CD34 + -enriched cell population into cardiomyocytes, endothelial cells, and smooth muscle cells in vivo. Circulation 108:2070-2073.
45. Iwasaki H, A Kawamoto, M Ishikawa, A Oyamada, S Nakamori, H Nishimura, K Sadamoto, M Horii, T Matsumoto, et al. (2006). Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 113:1311-1325.
46. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
47. Crain EH, DC Fithian, EW Paxton and WF Luetzow. (2005). Variation in anterior cruciate ligament scar pattern: does the scar pattern affect anterior laxity in anterior cruciate ligament-deficient knees? Arthroscopy 21:19-24.
48. Murray MM, KP Spindler, C Devin, BS Snyder, J Muller, M Takahashi, P Ballard, LB Nanney and D Zurakowski. (2006). Use of a collagen-platelet rich plasma scaffold to stimulate healing of a central defect in the canine ACL. J Orthop Res 24:820-830.
49. Murray MM, KP Spindler, P Ballard, TPWelch, D Zurakowski and LB Nanney. (2007). Enhanced histologic repair in a central wound in the anterior cruciate ligament with a collagenplatelet- rich plasma scaffold. J Orthop Res 25:1007-1017.
50. Lim JK, J Hui, L Li, A Thambyah, J Goh and EH Lee. (2004). Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 20:899-910.
51. Soon MY, A Hassan, JH Hui, JC Goh and EH Lee. (2007). An analysis of soft tissue allograft anterior cruciate ligament reconstruction in a rabbit model: a short-term study of the use of mesenchymal stem cells to enhance tendon osteointegration. Am J Sports Med 35:962-971.
52. Kanaya A, M Deie, N Adachi, M Nishimori, S Yanada and M Ochi. (2007). Intra-articular injection of mesenchymal stromal cells in partially torn anterior cruciate ligaments in a rat model. Arthroscopy 23:610-617.
53. Yoshikawa T, H Tohyama, T Katsura, E Kondo, Y Kotani, H Matsumoto, Y Toyama and K Yasuda. (2006). Effects of local administration of vascular endothelial growth factor on mechanical characteristics of the semitendinosus tendon graft after anterior cruciate ligament reconstruction in sheep. Am J Sports Med 34:1918-1925.
54. Yasuda K, F Tomita, S Yamazaki, A Minami and H Tohyama. (2004). The effect of growth factors on biomechanical properties of the bone-patellar tendon-bone graft after anterior cruciate ligament reconstruction: a canine model study. Am J Sports Med 32:870-880.
55. Sasaki K, R Kuroda, K Ishida, S Kubo, T Matsumoto, Y Mifune, K Kinoshita, K Tei, T Akisue, Y Tabata and M Kurosaka. (2008). Enhancement of tendon-bone osteointegration of anterior cruciate ligament graft using granulocyte colony-stimulating factor. Am J Sports Med 36:1519-1527.
56. Martinek V, C Latterman, A Usas, S Abramowitch, SL Woo, FH Fu and J Huard. (2002). Enhancement of tendon-bone integration of anterior cruciate ligament grafts with bone morphogenetic protein-2 gene transfer: a histological and biomechanical study. J Bone Joint Surg Am 84-A:1123-1131.
57. Mihelic R, M Pecina, M Jelic, S Zoricic, V Kusec, P Simic, D Bobinac, B Lah, D Legovic and S Vukicevic. (2004). Bone morphogenetic protein-7 (osteogenic protein-1) promotes tendon graft integration in anterior cruciate ligament reconstruction in sheep. Am J Sports Med 32:1619-1625.
58. Tei K, T Matsumoto, Y Mifune, K Ishida, K Sasaki, T Shoji, S Kubo, A Kawamoto, T Asahara, M Kurosaka and R Kuroda. (2008). Administrations of peripheral blood CD34-positive cells contribute to medial collateral ligament healing via vasculogenesis. Stem Cells 26:819-830.
59. Matsumoto T, A Kawamoto, R Kuroda, M Ishikawa, Y Mifune, H Iwasaki, M Miwa, M Horii, S Hayashi, et al. (2006). Therapeutic potential of vasculogenesis and osteogenesis promoted by peripheral blood CD34-positive cells for functional bone healing. Am J Pathol 169:1440-1457.
60. Mifune Y, T Matsumoto, A Kawamoto, R Kuroda, T Shoji, H Iwasaki, SM Kwon, M Miwa, M Kurosaka and T Asahara. (2008). Local delivery of granulocyte colony stimulating factor-mobilized CD34-positive progenitor cells using bioscaffold for modality of unhealing bone fracture. Stem Cells 26:1395-1405.