Therapeutic potential of anterior cruciate ligament-derived stem cells for anterior cruciate ligament reconstruction

Cell Transplantation

Volumn 21, Issue 8, 2012, Pages 1651-1665

  Mifune, Yutaka ^a,b,c   Matsumoto, Tomoyuki ^a,b,c   Ota, Shusuke ^a,b   Nishimori, Makoto ^a,b   Usas, Arvydas ^a,b   Kopf, Sebastian ^a,b   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

Angiogenesis; Anterior cruciate ligament; Osteogenesis; Reconstruction; Stem cells; Tendon bone healing

Indexed keywords

CD34 ANTIGEN; COLLAGEN FIBER; COLLAGEN TYPE 2; ISOLECTIN B4; OSTEOCALCIN; PHOSPHATE BUFFERED SALINE; VASCULOTROPIN;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CRUCIATE LIGAMENT; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; ANTERIOR CRUCIATE LIGAMENT RUPTURE; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSPLANTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; FRACTURE HEALING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE DEFICIENCY; IMMUNOHISTOCHEMISTRY; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; RAT; STEM CELL;

ANIMALS; ANTERIOR CRUCIATE LIGAMENT; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; ANTIGENS, CD34; BONE AND BONES; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN TYPE II; ENDOTHELIAL CELLS; FEMALE; GLYCOPROTEINS; HUMANS; LECTINS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOBLASTS; OSTEOCALCIN; OSTEOGENESIS; RATS; RATS, NUDE; STEM CELL TRANSPLANTATION; STEM CELLS; TENSILE STRENGTH; TOMOGRAPHY, X-RAY COMPUTED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

RATTUS;

EID: 84868141331     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X647234     Document Type: Article

References (42)

1. Agung, M.; Ochi, M.; Yanada, S.; Adachi, N.; Izuta, Y.; Yamasaki, T.; Toda, K. Mobilization of bone marrowderived mesenchymal stem cells into the injured tissues after intraarticular injection and their contribution to tissue regeneration. Knee Surg. Sports Traumatol. Arthrosc. 14(12):1307-1314; 2006
2. Asahara, T.; Murohara, T.; Sullivan, A.; Silver, M.; van der Zee, R.; Li, T.; Witzenbichler, B.; Schatteman, G.; Isner, J. M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964-967; 1997
3. Ballock, R. T.; Woo, S. L.; Lyon, R. M.; Hollis, J. M.; Akeson, W. H. Use of patellar tendon autograft for anterior cruciate ligament reconstruction in the rabbit: A longterm histologic and biomechanical study. J. Orthop. Res. 7(4):474-485; 1989
4. Butler, D. L. Kappa Delta Award paper. Anterior cruciate ligament: Its normal response and replacement. J. Orthop. Res. 7(6):910-921; 1989
5. Clancy Jr., W. G.; Narechania, R. G.; Rosenberg, T. D.; Gmeiner, J. G.; Wisnefske, D. D.; Lange, T. A. Anterior and posterior cruciate ligament reconstruction in rhesus monkeys. J. Bone Joint Surg. 63(8):1270-1284; 1981
6. Cobellis, G.; Maione, C.; Botti, C.; Coppola, A.; Silvestroni, A.; Lillo, S.; Schiavone, V.; Molinari, A. M.; Sica, V. Beneficial effects of VEGF secreted from stromal cells in supporting endothelial cell functions: Therapeutic implications for critical limb ischemia. Cell Transplant. 19(11):1425-1437; 2010
7. Crisan, M.; Deasy, B.; Gavina, M.; Zheng, B.; Huard, J.; Lazzari, L.; Peault, B. 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; 2008
8. Crisan, M.; Yap, S.; Casteilla, L.; Chen, C. W.; Corselli, M.; Park, T. S.; Andriolo, G.; Sun, B.; Zheng, B.; Zhang, L.; Norotte, C.; Teng, P. N.; Traas, J.; Schugar, R.; Deasy, B. M.; Badylak, S.; Buhring, H. J.; Giacobino, J. P.; Lazzari, L.; Huard, J.; Peault, B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3):301-313; 2008
9. Delay, B. S.; McGrath, B. E.; Mindell, E. R. Observations on a retrieved patellar tendon autograft used to reconstruct the anterior cruciate ligament. A case report. J. Bone Joint Surg. 84-A(8):1433-1438; 2002
10. Grana, W. A.; Egle, D. M.; Mahnken, R.; Goodhart, C. W. An analysis of autograft fixation after anterior cruciate ligament reconstruction in a rabbit model. Am. J. Sports Med. 22(3):344-351; 1994
11. Grassman, S. R.; McDonald, D. B.; Thornton, G. M.; Shrive, N. G.; Frank, C. B. Early healing processes of free tendon grafts within bone tunnels is bone-specific: A morphological study in a rabbit model. Knee 9(1):21-26; 2002
12. Griffin, L. Y.; Agel, J.; Albohm, M. J.; Arendt, E. A.; Dick, R. W.; Garrett, W. E.; Garrick, J. G.; Hewett, T. E.; Huston, L.; Ireland, M. L.; Johnson, R. J.; Kibler, W. B.; Lephart, S.; Lewis, J. L.; Lindenfeld, T. N.; Mandelbaum, B. R.; Marchak, P.; Teitz, C. C.; Wojtys, E. M. Noncontact anterior cruciate ligament injuries: Risk factors and prevention strategies. J. Am. Acad. Orthop. Surg. 8(3):141-150; 2000
13. Horie, M.; Sekiya, I.; Muneta, T.; Ichinose, S.; Matsumoto, K.; Saito, H.; Murakami, T.; Kobayashi, E. Intra-articular Injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 27(4):878-887; 2009
14. Howson, K. M.; Aplin, A. C.; Gelati, M.; Alessandri, G.; Parati, E. A.; Nicosia, R. F. The postnatal rat aorta contains pericyte progenitor cells that form spheroidal colonies in suspension culture. Am. J. Physiol. Cell Physiol. 289(6):C1396-1407; 2005
15. Ju, Y. J.; Tohyama, H.; Kondo, E.; Yoshikawa, T.; Muneta, T.; Shinomiya, K.; Yasuda, K. Effects of local administration of vascular endothelial growth factor on properties of the in situ frozen-thawed anterior cruciate ligament in rabbits. Am. J. Sports Med. 34(1):84-91; 2006
16. Kalka, C.; Masuda, H.; Takahashi, T.; Kalka-Moll, W. M.; Silver, M.; Kearney, M.; Li, T.; Isner, J. M.; Asahara, T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA 97(7):3422-3427; 2000
17. Kanaya, A.; Deie, M.; Adachi, N.; Nishimori, M.; Yanada, S.; Ochi, M. Intra-articular injection of mesenchymal stromal cells in partially torn anterior cruciate ligaments in a rat model. Arthroscopy 23(6):610-617; 2007
18. Kawamoto, A.; Gwon, H. C.; Iwaguro, H.; Yamaguchi, J. I.; Uchida, S.; Masuda, H.; Silver, M.; Ma, H.; Kearney, M.; Isner, J. M.; Asahara, T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103(5):634-637; 2001
19. Kawamoto, A.; Tkebuchava, T.; Yamaguchi, J.; Nishimura, H.; Yoon, Y. S.; Milliken, C.; Uchida, S.; Masuo, O.; Iwaguro, H.; Ma, H.; Hanley, A.; Silver, M.; Kearney, M.; Losordo, D. W.; Isner, J. M.; Asahara, T. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107(3):461-468; 2003
20. Kawamura, S.; Ying, L.; Kim, H. J.; Dynybil, C.; Rodeo, S. A. Macrophages accumulate in the early phase of tendon- bone healing. J. Orthop. Res. 23(6):1425-1432; 2005
21. Kohno, T.; Ishibashi, Y.; Tsuda, E.; Kusumi, T.; Tanaka, M.; Toh, S. Immunohistochemical demonstration of growth factors at the tendon-bone interface in anterior cruciate ligament reconstruction using a rabbit model. J. Orthop. Sci. 12(1):67-73; 2007
22. Li, F.; Jia, H.; Yu, C. ACL reconstruction in a rabbit model using irradiated Achilles allograft seeded with mesenchymal stem cells or PDGF-B gene-transfected mesenchymal stem cells. Knee Surg. Sports Traumatol. Arthrosc. 15(10):1219-1227; 2007
23. Lim, J. K.; Hui, J.; Li, L.; Thambyah, A.; Goh, J.; Lee, E. H. Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 20(9):899-910; 2004
24. Majka, M.; Janowska-Wieczorek, A.; Ratajczak, J.; Ehrenman, K.; Pietrzkowski, Z.; Kowalska, M. A.; Gewirtz, A. M.; Emerson, S. G.; Ratajczak, M. Z. Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/ paracrine manner. Blood 97(10):3075-3085; 2001
25. Martinek, V.; Latterman, C.; Usas, A.; Abramowitch, S.; Woo, S. L.; Fu, F. H.; Huard, J. 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. 84-A(7):1123-1131; 2002
26. Matsumoto, T., Ingham, M.S., Mifune, Y., Osawa, A., Logar, A., Usas, A., Kuroda, R., Kurosaka, M., Fu, F. H., and Huard, J. Isolation and characterization of human anterior cruciate ligament-derived vascular stem cells. Stem Cells Dev. 21(6):859-872; 2012
27. Mihelic, R.; Pecina, M.; Jelic, M.; Zoricic, S.; Kusec, V.; Simic, P.; Bobinac, D.; Lah, B.; Legovic, D.; Vukicevic, S. Bone morphogenetic protein-7 (osteogenic protein-1) promotes tendon graft integration in anterior cruciate ligament reconstruction in sheep. Am. J. Sports Med. 32(7):1619-1625; 2004
28. Nakamura, T.; Tsutsumi, V.; Torimura, T.; Naitou, M.; Iwamoto, H.; Masuda, H.; Hashimoto, O.; Koga, H.; Abe, M.; Ii, M.; Kawamoto, A.; Asahara, T.; Ueno, T.; Sata, M. Human peripheral blood CD34-positive cells enhance therapeutic regeneration of chronically injured liver in nude rats. J. Cell. Physiol. 227(4):1538-1552; 2012
29. Ouyang, H. W.; Goh, J. C.; Lee, E. H. Use of bone marrow stromal cells for tendon graft-to-bone healing: Histological and immunohistochemical studies in a rabbit model. Am. J. Sports Med. 32(2):321-327; 2004
30. Payne, T. R.; Oshima, H.; Okada, M.; Momoi, N.; Tobita, K.; Keller, B. B.; Peng, H.; Huard, J. A relationship between vascular endothelial growth factor, angiogenesis, and cardiac repair after muscle stem cell transplantation into ischemic hearts. J. Am. Coll. Cardiol. 50(17):1677-1684; 2007
31. Petersen, W.; Petersen, F.; Tillmann, B. Structure and vascularization of the acetabular labrum with regard to the pathogenesis and healing of labral lesions. Arch. Orthop. Trauma Surg. 123(6):283-288; 2003
32. Rodeo, S. A.; Suzuki, K.; Deng, X. H.; Wozney, J.; Warren, R. F. Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am. J. Sports Med. 27(4):476-488; 1999
33. Sasaki, K.; Kuroda, R.; Ishida, K.; Kubo, S.; Matsumoto, T.; Mifune, Y.; Kinoshita, K.; Tei, K.; Akisue, T.; Tabata, Y.; Kurosaka, M. Enhancement of tendon-bone osteointegration of anterior cruciate ligament graft using granulocyte colony-stimulating factor. Am. J. Sports Med. 36(8):1519-1527; 2008
34. Soon, M. Y.; Hassan, A.; Hui, J. H.; Goh, J. C.; Lee, E. H. 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(6):962-971; 2007
35. Tavian, M.; Zheng, B.; Oberlin, E.; Crisan, M.; Sun, B.; Huard, J.; Peault, B. The vascular wall as a source of stem cells. Ann. N. Y. Acad. Sci. 1044:41-50; 2005
36. Tohyama, H.; Yoshikawa, T.; Ju, Y. J.; Yasuda, K. Revascularization in the tendon graft following anterior cruciate ligament reconstruction of the knee: Its mechanisms and regulation. Chang Gung Med. J. 32(2):133-139; 2009
37. Weiss, J. A.; Woo, S. L.; Ohland, K. J.; Horibe, S.; Newton, P. O. Evaluation of a new injury model to study medial collateral ligament healing: Primary repair versus nonoperative treatment. J. Orthop. Res. 9(4):516-528; 1991
38. Wen, C. Y.; Qin, L.; Lee, K. M.; Chan, K. M. Perigraft bone mass and connectivity as predictors for the strength of tendon-to-bone attachment after anterior cruciate ligament reconstruction. Bone 45(3):545-552; 2009
39. Woo, S. L.; Inoue, M.; McGurk-Burleson, E.; Gomez, M. A. 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(1):22-29; 1987
40. Yasuda, K.; Tomita, F.; Yamazaki, S.; Minami, A.; Tohyama, H. 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(4):870-880; 2004
41. Yoshikawa, T.; Tohyama, H.; Katsura, T.; Kondo, E.; Kotani, Y.; Matsumoto, H.; Toyama, Y.; Yasuda, K. 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(12):1918-1925; 2006
42. Zheng, B.; Cao, B.; Crisan, M.; Sun, B.; Li, G.; Logar, A.; Yap, S.; Pollett, J. B.; Drowley, L.; Cassino, T.; Gharaibeh, B.; Deasy, B. M.; Huard, J.; Péault, B. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat. Biotechnol. 25(9):1025-1034; 2007.