Indian hedgehog gene transfer is a chondrogenic inducer of human mesenchymal stem cells

Arthritis Research and Therapy

Volumn 14, Issue 4, 2012, Pages

  Steinert, Andre F ^a   Weissenberger, Manuel ^a   Kunz, Manuela ^a   Gilbert, Fabian ^a   Ghivizzani, Steven C ^b   Göbel, Sascha ^a   Jakob, Franz ^a   Nöth, Ulrich ^a   Rudert, Maximilian ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COMPLEMENTARY DNA; GAG PROTEIN; GLYCOSAMINOGLYCAN; LIPOCORTIN 5; MESSENGER RNA; PROTEOGLYCAN; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; IHH PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CARBOHYDRATE SYNTHESIS; CELL AGGREGATION; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE TARGETING; GENE TRANSFER; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; FEMALE; GENETICS; MALE; MESENCHYMAL STROMA CELL; MIDDLE AGED; PHYSIOLOGY;

CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROGENESIS; FEMALE; GENE TRANSFER TECHNIQUES; HEDGEHOG PROTEINS; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED;

EID: 84866182766     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3921     Document Type: Article

References (47)

1. Steinert AF, Ghivizzani SC, Rethwilm A, Tuan RS, Evans CH, Noth U. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res Ther 2007, 9:213. 10.1186/ar2195, 2206353, 17561986.
2. Wakitani S, Mitsuoka T, Nakamura N, Toritsuka Y, Nakamura Y, Horibe S. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports. Cell Transplant 2004, 13:595-600. 10.3727/000000004783983747, 15565871.
3. Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007, 15:226-231. 10.1016/j.joca.2006.08.008, 17002893.
4. Noth U, Steinert AF, Tuan RS. Technology insight: adult mesenchymal stem cells for osteoarthritis therapy. Nat Clin Pract Rheumatol 2008, 4:371-380.
5. Fortier LA, Barker JU, Strauss EJ, McCarrel TM, Cole BJ. The role of growth factors in cartilage repair. Clin Orthop Relat Res 2011, 469:2706-2715. 10.1007/s11999-011-1857-3, 21403984.
6. Nesic D, Whiteside R, Brittberg M, Wendt D, Martin I, Mainil-Varlet P. Cartilage tissue engineering for degenerative joint disease. Adv Drug Deliv Rev 2006, 58:300-322. 10.1016/j.addr.2006.01.012, 16574268.
7. Evans CH, Robbins PD, Ghivizzani SC, Wasko MC, Tomaino MM, Kang R, Muzzonigro TA, Vogt M, Elder EM, Whiteside TL, Watkins SC, Herndon JH. Gene transfer to human joints: progress toward a gene therapy of arthritis. Proc Natl Acad Sci USA 2005, 102:8698-8703. 10.1073/pnas.0502854102, 1150836, 15939878.
8. Steinert AF, Noth U, Tuan RS. Concepts in gene therapy for cartilage repair. Injury 2008, 39:S97-S113.
9. Cucchiarini M, Madry H. Gene therapy for cartilage defects. J Gene Med 2005, 7:1495-1509. 10.1002/jgm.824, 16142829.
10. Gelse K, Schneider H. Ex vivo gene therapy approaches to cartilage repair. Adv Drug Deliv Rev 2006, 58:259-284. 10.1016/j.addr.2006.01.019, 16574266.
11. Steinert AF, Proffen B, Kunz M, Hendrich C, Ghivizzani SC, Noth U, Rethwilm A, Eulert J, Evans CH. Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther 2009, 11:R148. 10.1186/ar2822, 2787261, 19799789.
12. Pelttari K, Winter A, Steck E, Goetzke K, Hennig T, Ochs BG, Aigner T, Richter W. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 2006, 54:3254-3266. 10.1002/art.22136, 17009260.
13. Gelse K, von der Mark K, Aigner T, Park J, Schneider H. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum 2003, 48:430-441. 10.1002/art.10759, 12571853.
14. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622. 10.1126/science.273.5275.613, 8662546.
15. Palmer GD, Steinert A, Pascher A, Gouze E, Gouze JN, Betz O, Johnstone B, Evans CH, Ghivizzani SC. Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro. Mol Ther 2005, 12:219-228. 10.1016/j.ymthe.2005.03.024, 16043093.
16. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML. Construction of adenovirus vectors through Cre-lox recombination. J Virol 1997, 71:1842-1849. 191254, 9032314.
17. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual 2001, 1. New York: CSHL Press, 3.
18. Palmer G, Gouze E, Gouze JN, Betz O, Evans CH, Ghivizzani SC. Gene transfer to articular chondrocytes with recombinant adenovirus. Methods Mol Biol 2003, 215:235-246.
19. Noth U, Tuli R, Osyczka AM, Danielson KG, Tuan RS. In vitro engineered cartilage constructs produced by press-coating biodegradable polymer with human mesenchymal stem cells. Tissue Eng 2002, 8:131-144. 10.1089/107632702753503126, 11886661.
20. Steinert AF, Kunz M, Prager P, Barthel T, Jakob F, Noth U, Murray MM, Evans CH, Porter RM. Mesenchymal stem cell characteristics of human anterior cruciate ligament outgrowth cells. Tissue Eng Part A 2011, 17:1375-1388. 10.1089/ten.tea.2010.0413, 3079172, 21247268.
21. McMahon LA, Prendergast PJ, Campbell VA. A comparison of the involvement of p38, ERK1/2 and PI3K in growth factor-induced chondrogenic differentiation of mesenchymal stem cells. Biochem Biophys Res Commun 2008, 368:990-995. 10.1016/j.bbrc.2008.01.160, 18267113.
22. Rockel JS, Alman BA. Don't hedge your bets: hedgehog signaling as a central mediator of endochondral bone development and cartilage diseases. J Orthop Res 2011, 29:810-815. 10.1002/jor.21372, 21308758.
23. Steinert AF, Palmer GD, Pilapil C, Noth U, Evans CH, Ghivizzani SC. Enhanced in vitro chondrogenesis of primary mesenchymal stem cells by combined gene transfer. Tissue Eng Part A 2009, 15:1127-1139. 10.1089/ten.tea.2007.0252, 2810414, 18826340.
24. Kellner K, Lang K, Papadimitriou A, Leser U, Milz S, Schulz MB, Blunk T, Gopferich A. Effects of hedgehog proteins on tissue engineering of cartilage in vitro. Tissue Eng 2002, 8:561-572. 10.1089/107632702760240481, 12201996.
25. Enomoto-Iwamoto M, Nakamura T, Aikawa T, Higuchi Y, Yuasa T, Yamaguchi A, Nohno T, Noji S, Matsuya T, Kurisu K, Koyama E, Pacifici M, Iwamoto M. Hedgehog proteins stimulate chondrogenic cell differentiation and cartilage formation. J Bone Miner Res 2000, 15:1659-1668. 10.1359/jbmr.2000.15.9.1659, 10976986.
26. Park J, Zhang JJ, Moro A, Kushida M, Wegner M, Kim PC. Regulation of Sox9 by Sonic Hedgehog (Shh) is essential for patterning and formation of tracheal cartilage. Dev Dyn 2010, 239:514-526. 10.1002/dvdy.22192, 20034104.
27. Akiyama H, Shigeno C, Iyama K, Ito H, Hiraki Y, Konishi J, Nakamura T. Indian hedgehog in the late-phase differentiation in mouse chondrogenic EC cells, ATDC5: upregulation of type X collagen and osteoprotegerin ligand mRNAs. Biochem Biophys Res Commun 1999, 257:814-820. 10.1006/bbrc.1999.0494, 10208865.
28. Grande DA, Mason J, Light E, Dines D. Stem cells as platforms for delivery of genes to enhance cartilage repair. J Bone Joint Surg Am 2003, 85-A:111-116.
29. Vortkamp A. Interaction of growth factors regulating chondrocyte differentiation in the developing embryo. Osteoarthritis Cartilage 2001, 9:S109-S117.
30. Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LH, Ho C, Mulligan RC, Abou-Samra AB, Jüppner H, Segre GV, Kronenberg HM. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 1996, 273:663-666. 10.1126/science.273.5275.663, 8662561.
31. Kronenberg HM. PTHrP and skeletal development. Ann N Y Acad Sci 2006, 1068:1-13. 10.1196/annals.1346.002, 16831900.
32. Kronenberg HM. Developmental regulation of the growth plate. Nature 2003, 423:332-336. 10.1038/nature01657, 12748651.
33. Wang W, Lian N, Ma Y, Li L, Gallant RC, Elefteriou F, Yang X. Chondrocytic Atf4 regulates osteoblast differentiation and function via Ihh. Development 2012, 139:601-611. 10.1242/dev.069575, 22190639.
34. Chau M, Forcinito P, Andrade AC, Hegde A, Ahn S, Lui JC, Baron J, Nilsson O. Organization of the Indian hedgehog - parathyroid hormone-related protein system in the postnatal growth plate. J Mol Endocrinol 2011, 47:99-107. 10.1530/JME-10-0177, 21642420.
35. Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, McMahon AP, Vortkamp A. BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 2001, 128:4523-4534.
36. Mueller MB, Tuan RS. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 2008, 58:1377-1388. 10.1002/art.23370, 18438858.
37. Steinert A, Weber M, Dimmler A, Julius C, Schutze N, Noth U, Cramer H, Eulert J, Zimmermann U, Hendrich C. Chondrogenic differentiation of mesenchymal progenitor cells encapsulated in ultrahigh-viscosity alginate. J Orthop Res 2003, 21:1090-1097. 10.1016/S0736-0266(03)00100-1, 14554223.
38. Poole AR, Matsui Y, Hinek A, Lee ER. Cartilage macromolecules and the calcification of cartilage matrix. Anat Rec 1989, 224:167-179. 10.1002/ar.1092240207, 2672883.
39. Cheung JO, Hillarby MC, Ayad S, Hoyland JA, Jones CJ, Denton J, Thomas JT, Wallis GA, Grant ME. A novel cell culture model of chondrocyte differentiation during mammalian endochondral ossification. J Bone Miner Res 2001, 16:309-318. 10.1359/jbmr.2001.16.2.309, 11204431.
40. Bahrami S, Plate U, Dreier R, DuChesne A, Willital GH, Bruckner P. Endochondral ossification of costal cartilage is arrested after chondrocytes have reached hypertrophic stage of late differentiation. Matrix Biol 2001, 19:707-715. 10.1016/S0945-053X(00)00125-6, 11223330.
41. Mwale F, Yao G, Ouellet JA, Petit A, Antoniou J. Effect of parathyroid hormone on type X and type II collagen expression in mesenchymal stem cells from osteoarthritic patients. Tissue Eng Part A 2010, 16:3449-3455. 10.1089/ten.tea.2010.0091, 20569194.
42. Weiss S, Hennig T, Bock R, Steck E, Richter W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J Cell Physiol 2010, 223:84-93.
43. Fischer J, Dickhut A, Rickert M, Richter W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 2010, 62:2696-2706. 10.1002/art.27565, 20496422.
44. Gelse K, Muhle C, Knaup K, Swoboda B, Wiesener M, Hennig F, Olk A, Schneider H. Chondrogenic differentiation of growth factor-stimulated precursor cells in cartilage repair tissue is associated with increased HIF-1α activity. Osteoarthritis Cartilage 2008, 16:1457-1465. 10.1016/j.joca.2008.04.006, 18524637.
45. Keller B, Yang T, Chen Y, Munivez E, Bertin T, Zabel B, Lee B. Interaction of TGFβ and BMP signaling pathways during chondrogenesis. PLoS One 2011, 6:e16421. 10.1371/journal.pone.0016421, 3030581, 21297990.
46. Klotz B, Mentrup B, Regensburger M, Zeck S, Schneidereit J, Schupp N, Linden C, Merz C, Ebert R, Jakob F. 1,25-dihydroxyvitamin D3 treatment delays cellular aging in human mesenchymal stem cells while maintaining their multipotent capacity. PLoS One 2012, 7:e29959. 10.1371/journal.pone.0029959, 3252365, 22242193.
47. Dreier R, Gunther BK, Mainz T, Nemere I, Bruckner P. Terminal differentiation of chick embryo chondrocytes requires shedding of a cell surface protein that binds 1,25-dihydroxyvitamin D3. J Biol Chem 2008, 283:1104-1112. 10.1074/jbc.M703336200, 17984094.