Donor-matched comparison of chondrogenic progenitors resident in human infrapatellar fat pad, synovium, and periosteum - implications for cartilage repair

References

• Chu CR, Rodeo S, Bhutani N, Goodrich LR, Huard J, Irrgang J, LaPrade RF, Lattermann C, Lu Y, Mandelbaum B, Mao J, McIntyre L, Mishra A, Muschler GF, Piuzzi NS, Potter H, Spindler K, Tokish JM, Tuan R, Zaslav K, Maloney W. Optimizing clinical use of biologics in orthopaedic surgery: consensus recommendations from the 2018 AAOS/NIH U-13 conference. J Am Acad Orthop Surg. 2019; 27(2):e50–e63. doi:10.5435/JAAOS-D-18-00305.
   PubMed Web of Science ®Google Scholar
• Mantripragada VP, Bova WA, Boehm C, Piuzzi NS, Obuchowski NA, Midura RJ, Muschler GF. Progenitor cells from different zones of human cartilage and their correlation with histopathological osteoarthritis progression. J Orthop Res. 2018; 36(3):1728–1738. doi:10.1002/jor.23829.
   PubMedGoogle Scholar
• Piuzzi NS, Dominici M, Long M, Pascual-Garrido C, Rodeo S, Huard J, Guicheux J, McFarland R, Goodrich LR, Maddens S, Robey PG, Bauer TW, Barrett J, Barry F, Karli D, Chu CR, Weiss DJ, Martin I, Jorgensen C, Muschler GF Proceedings of the signature series symposium “Cellular therapies for orthopaedics and musculoskeletal disease proven and unproven therapies-promise, facts and fantasy,” international society for cellular therapy, Montreal, Canada, May 2, 2018. Cytotherapy. 2018; 20(11):1381–1400. doi:10.1016/j.jcyt.2018.09.001.
   PubMed Web of Science ®Google Scholar
• Mantripragada VP, Bova WA, Boehm C, Piuzzi NS, Obuchowski NA, Midura RJ, Muschler GF. Primary cells isolated from human knee cartilage reveal decreased prevalence of progenitor cells but comparable biological potential during osteoarthritic disease progression. J Bone Jt Surg. 2018;(100):1771–1780. doi:10.2106/JBJS.18.00005.
   PubMedGoogle Scholar
• Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A; International Society for Cellular Therapy. Clarification of the nomenclature for MSC: the international society for cellular therapy position statement. Cytotherapy. 2005;7(5):393–395. doi:10.1080/14653240500319234.
   PubMed Web of Science ®Google Scholar
• Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell. 2012; 10(6):709–716. doi:10.1016/j.stem.2012.05.015.
   PubMed Web of Science ®Google Scholar
• D’souza N, Rossignoli F, Golinelli G, Grisendi G, Spano C, Candini O, Osturu S, Catani F, Paolucci P, Horwitz EM, Dominici M. Mesenchymal stem/stromal cells as a delivery platform in cell and gene therapies. BMC Med. 2015; 13(1):186. doi:10.1186/s12916-015-0426-0.
   PubMedGoogle Scholar
• Phinney DG. Biochemical heterogeneity of mesenchymal stem cell populations: clues to their therapeutic efficacy. Cell Cycle. 2007; 6(23):2884–2889. doi:10.4161/cc.6.23.5095.
   PubMed Web of Science ®Google Scholar
• Bianco P, Robey PG. Skeletal stem cells. Development. 2015; 142(6):1023–1027. doi:10.1242/dev.102210.
   PubMed Web of Science ®Google Scholar
• Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell. 2011; 9(1):11–15. doi:10.1016/j.stem.2011.06.008.
   PubMed Web of Science ®Google Scholar
• Lodi D, Iannitti T, Palmieri B. Stem cells in clinical practice: applications and warnings. J Exp Clin Cancer Res. 2011; 30(1):1–20. doi:10.1186/1756-9966-30-9.
   PubMedGoogle Scholar
• Muschler GF, Nakamoto C, Griffith LG. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am. 2004 [accessed 2017 March 29];86-A(7):1541–1558. http://www.ncbi.nlm.nih.gov/pubmed/15252108.
   PubMedGoogle Scholar
• Muschler GF, Midura RJ, Nakamoto C. Practical modeling concepts for connective tissue stem cell and progenitor compartment kinetics. J Biomed Biotechnol. 2003;2003(3):170–193. doi:10.1155/S1110724303209165.
   PubMedGoogle Scholar
• Muschler GF, Midura RJ. Connective tissue progenitors: practical concepts for clinical applications. Clin Orthop Relat Res. 2002 [accessed 2017 Mar 29];395:66–80. http://www.ncbi.nlm.nih.gov/pubmed/11937867
   PubMed Web of Science ®Google Scholar
• ASTM F2944-12 standard test method for automated colony forming unit (CFU) assays—image acquisition and analysis method for enumerating and characterizing cells and colonies in culture. West Conshohocken (PA): ASTM International. 2012. doi:10.1520/F2944.
   Google Scholar
• Muschler GF, Midura RJ, Nakamoto C. Practical modeling concepts for connective tissue stem cell and progenitor compartment kinetics. J Biomed Biotechnol. 2003; 2003(3):170–193. doi:10.1155/S1110724303209165.
   PubMedGoogle Scholar
• Koh YG, Jo SB, Kwon OR, Suh DS, Lee SW, Park SH, Choi YJ. Mesenchymal stem cell injections improve symptoms of knee osteoarthritis. Arthrosc - J Arthrosc Relat Surg. 2013; 29(4):748–755. doi:10.1016/j.arthro.2012.11.017.
   PubMed Web of Science ®Google Scholar
• Koh YG, Choi YJ. Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee. 2012; 19(6):902–907. doi:10.1016/j.knee.2012.04.001.
   PubMed Web of Science ®Google Scholar
• Akgun I, Unlu MC, Erdal OA, Ogut T, Erturk M, Ovali E, Kantarci F, Caliskan G, Akgun Y. Matrix-induced autologous mesenchymal stem cell implantation versus matrix-induced autologous chondrocyte implantation in the treatment of chondral defects of the knee: a 2-year randomized study. Arch Orthop Trauma Surg. 2015; 135(2):251–263. doi:10.1007/s00402-014-2136-z.
   PubMed Web of Science ®Google Scholar
• Sekiya I, Muneta T, Horie M, Koga H. Arthroscopic transplantation of synovial stem cells improves clinical outcomes in knees with cartilage defects. Clin Orthop Relat Res. 2015; 473(7):2316–2326. doi:10.1007/s11999-015-4324-8.
   PubMed Web of Science ®Google Scholar
• Lee WY, Wang B. Cartilage repair by mesenchymal stem cells: clinical trial update and perspectives. J Orthop Transl. 2017;9:76–88. doi:10.1016/j.jot.2017.03.005.
   PubMed Web of Science ®Google Scholar
• Ball MD, Bonzani IC, Bovis MJ, Williams A, Stevens MM. Human periosteum is a source of cells for orthopaedic tissue engineering: A pilot study. Clin Orthop Relat Res. 2011; 469(11):3085–3093. doi:10.1007/s11999-011-1895-x.
   PubMed Web of Science ®Google Scholar
• Vozzi G, Lucarini G, Dicarlo M, Andreoni C, Salvolini E, Ferretti C, Mattioli-Belmonte M. In vitro lifespan and senescent behaviour of human periosteal derived stem cells. Bone. 2016;88:1–12. doi:10.1016/j.bone.2016.04.013.
   PubMed Web of Science ®Google Scholar
• Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum. 2005; 52(8):2521–2529. doi:10.1002/art.21212.
   PubMedGoogle Scholar
• Ogata Y, Mabuchi Y, Yoshida M, Suto EG, Suzuki N, Muneta T, Sekiya I, Akazawa C. Purified human synovium mesenchymal stem cells as a good resource for cartilage regeneration. PLoS One. 2015; 10(6):5–9. doi:10.1371/journal.pone.0129096.
   Web of Science ®Google Scholar
• Kubosch EJ, Heidt E, Niemeyer P, Bernstein A, Südkamp NP, Schmal H. In-vitro chondrogenic potential of synovial stem cells and chondrocytes allocated for autologous chondrocyte implantation — a comparison. Int Orthop. 2017; 41(5):991–998. doi:10.1007/s00264-017-3400-y.
   PubMed Web of Science ®Google Scholar
• English A, Jones EA, Corscadden D, Henshaw K, Chapman T, Emery P, McGonagle D. A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis. Rheumatology. 2007; 46(11):1676–1683. doi:10.1093/rheumatology/kem217.
   PubMed Web of Science ®Google Scholar
• Shirasawa S, Sekiya I, Sakaguchi Y, Yagishita K, Ichinose S, Muneta T. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem. 2006; 97(1):84–97. doi:10.1002/jcb.20546.
   PubMed Web of Science ®Google Scholar
• Ichinose S, Muneta T, Koga H, Segawa Y, Tagami M, Tsuji K, Sekiya I. Morphological differences during in vitro chondrogenesis of bone marrow-, synovium-MSCs, and chondrocytes. Lab Investig. 2010; 90(2):210–221. doi:10.1038/labinvest.2009.125.
   PubMed Web of Science ®Google Scholar
• Lopa S, Colombini A, Stanco D, de Girolamo L, Sansone V, Moretti M. Donor-matched mesenchymal stem cells from knee infrapatellar and subcutaneous adipose tissue of osteoarthritic donors display differential chondrogenic and osteogenic commitment. Eur Cells Mater. 2014;27:298–311. doi:10.22203/eCM.v027a21.
   PubMed Web of Science ®Google Scholar
• Ioan-Facsinay A, Kloppenburg M. An emerging player in knee osteoarthritis: the infrapatellar fat pad. Arthritis Res Ther. 2013; 15(6):225–234. doi:10.1186/ar4422.
   PubMed Web of Science ®Google Scholar
• Do Amaral RJFC, Almeida HV, Kelly DJ, O’Brien FJ, Kearney CJ. Infrapatellar fat pad stem cells: from developmental biology to cell therapy. Stem Cells Int. 2017;2017:6843727. doi:10.1155/2017/6843727.
   PubMedGoogle Scholar
• De Bari C, Dell ’Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001; 44(8):1928–1942. doi:10.1002/1529-0131(200108)44:8<1928::AID-ART331>3.0.CO;2-P.
   PubMed Web of Science ®Google Scholar
• Chang H, Knothe Tate ML. Concise review: the periosteum: tapping into a reservoir of clinically useful progenitor cells. Stem Cells Transl Med. 2012; 1(6):480–491. doi:10.5966/sctm.2011-0056.
   PubMed Web of Science ®Google Scholar
• Enochson L, Brittberg M, Lindahl A. Optimization of a chondrogenic medium through the use of factorial design of experiments. Biores Open Access. 2012; 1(6):306–313. doi:10.1089/biores.2012.0277.
   PubMedGoogle Scholar
• Dragoo JL, Samimi B, Zhu M, Hame SL, Thomas BJ, Lieberman JR, Hedrick MH, Benhaim P. Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. J Bone Joint Surg Br. 2003; 85(5):740–747. doi:10.1302/0301-620X.85B5.13587.
   PubMedGoogle Scholar
• Neri S, Guidotti S, Lilli NL, Cattini L, Mariani E. Infrapatellar fat pad-derived mesenchymal stromal cells from osteoarthritis patients: in vitro genetic stability and replicative senescence. J Orthop Res. 2017; 35(5):1029–1037. doi:10.1002/jor.23349.
   PubMed Web of Science ®Google Scholar
• Fossett E, Khan WS, Longo UG, Smitham PJ. Effect of age and gender on cell proliferation and cell surface characterization of synovial fat pad derived mesenchymal stem cells. J Orthop Res. 2012; 30(7):1013–1018. doi:10.1002/jor.22057.
   PubMed Web of Science ®Google Scholar
• Gigante A, Andreoni C, Salvolini E, Ferretti C, Bianchi N, Mattioli-Belmonte M, Lucarini G, Vozzi G. Human periosteal derived stem cell potential: the impact of age. Stem Cell Rev Reports. 2014; 11(3):487–500. doi:10.1007/s12015-014-9559-3.
   Web of Science ®Google Scholar
• Katagiri K, Matsukura Y, Muneta T, Ozeki N, Mizuno M, Katano H, Sekiya I. Fibrous synovium releases higher numbers of mesenchymal stem cells than adipose synovium in a suspended synovium culture model. Arthrosc - J Arthrosc Relat Surg. 2017; 33(4):800–810. doi:10.1016/j.arthro.2016.09.033.
   PubMed Web of Science ®Google Scholar
• Tangchitphisut P, Srikaew N, Numhom S, Tangprasittipap A, Woratanarat P, Wongsak S, Kijkunasathian C, Hongeng S, Murray IR, Tawonsawatruk T. Infrapatellar fat pad: an alternative source of adipose-derived mesenchymal stem cells. Arthritis. 2016;2016:1–10. doi:10.1155/2016/4019873.
   Google Scholar
• Jones E. Synovial mesenchymal stem cells in vivo: potential key players for joint regeneration. World J Rheumatol. 2011; 1(1):4. doi:10.5499/wjr.v1.i1.4.
   Google Scholar
• De Bari C, Dell’Accio F, Vanlauwe J, Eyckmans J, Khan IM, Archer CW, Jones EA, McGonagle D, Mitsiadis TA, Pitzalis C, Luyten FP. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum. 2006; 54(4):1209–1221. doi:10.1002/art.21753.
   PubMed Web of Science ®Google Scholar
• De Bari C, Dell’Accio F, Luyten FP. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum. 2001; 44(1):85–95. doi:10.1002/1529-0131(200101)44:1<85::AID-ANR12>3.0.CO;2-6.
   PubMed Web of Science ®Google Scholar
• Stich S, Loch A, Park S, Ha T, Ringe J, Sittinger M. Characterization of single cell derived cultures of periosteal progenitor cells to ensure the cell quality for clinical application. PLoS One. 2017;12:e0178560.
   PubMed Web of Science ®Google Scholar
• Karystinou A, Dell’Accio F, Kurth TBA, Wackerhage H, Khan IM, Archer CW, Jones EA, Mitsiadis TA, de Bari C. Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology. 2009; 48(9):1057–1064. doi:10.1093/rheumatology/kep192.
   PubMed Web of Science ®Google Scholar
• Lee D-H, Joo S-D, Han S-B, Im J, Lee S-H, Sonn CH, Lee K-M. Isolation and expansion of synovial CD34 − CD44 + CD90 + mesenchymal stem cells: comparison of an enzymatic method and a direct explant technique. Connect Tissue Res. 2011; 52(3):226–234. doi:10.3109/03008207.2010.516850.
   PubMed Web of Science ®Google Scholar
• Qadan MA, Piuzzi NS, Boehm C, Bova W, Moos M, Midura RJ, Hascall VC, Malcuit C, Muschler GF. Variation in primary and culture-expanded cells derived from connective tissue progenitors in human bone marrow space, bone trabecular surface and adipose tissue. Cytotherapy. 2018; 20(3):343–360. doi:10.1016/j.jcyt.2017.11.013.
   PubMed Web of Science ®Google Scholar
• Mendicino M, Bailey AM, Wonnacott K, Puri RK, Bauer SR. MSC-based product characterization for clinical trials: an FDA perspective. Cell Stem Cell. 2014; 14(2):141–145. doi:10.1016/j.stem.2014.01.013.
   PubMed Web of Science ®Google Scholar
• McLeod CM, Mauck RL. On the origin and impact of mesenchymal stem cell heterogeneity: new insights and emerging tools for single cell analysis. Eur Cells Mater. 2017;34:217–231. doi:10.22203/eCM.v034a14.
   PubMed Web of Science ®Google Scholar
• Matsuoka F, Takeuchi I, Agata H, Kagami H, Shiono H, Kiyota Y, Honda H, Kato R. Morphology-based prediction of osteogenic differentiation potential of human mesenchymal stem cells. PLoS One. 2013;8:2. doi:10.1371/journal.pone.0055082.
   Web of Science ®Google Scholar
• Kwee E, Saidel G, Powell K, Heylman C, Boehm C, Muschler G. Quantifying Proliferative and Surface Marker Heterogeneity in Colony Founding Connective Tissue Progenitors and Their Progeny Using Time-Lapse Microscopy. Tissue Eng Regen Med. 2018. In Press. doi:10.1002/term.2782
   Web of Science ®Google Scholar
• Chan CKF, Gulati GS, Sinha R, Tompkins JV, Lopez M, Carter AC, Ransom RC, Reinisch A, Wearda T, Murphy M, Brewer RE, Koepke LS, Marecic O, Manjunath A, Seo EY, Leavitt T, Lu W-J, Nguyen A, Conley SD, Salhotra A, Ambrosi TH, Borrelli MR, Siebel T, Chan K, Schallmoser K, Seita J, Sahoo D, Goodnough H, Bishop J, Gardner M, Majeti R, Wan DC, Goodman S, Weissman IL, Chang HY, Longaker MT. Identification of the human skeletal stem cell. Cell. 2018; 175(1):43–56.e21. doi:10.1016/j.cell.2018.07.029.
   PubMed Web of Science ®Google Scholar
• Fickert S, Fiedler J, Brenner RE. Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res Ther. 2004; 6(5):R422–R432. doi:10.1186/ar1210.
   PubMed Web of Science ®Google Scholar
• Campbell D, Pei M. Surface markers for chondrogenic determination: a highlight of synovium-derived stem cells. Cells. 2012; 1(4):1107–1120. doi:10.3390/cells1041107.
   PubMedGoogle Scholar
• McCarthy HE, Bara JJ, Brakspear K, Singhrao SK, Archer CW. The comparison of equine articular cartilage progenitor cells and bone marrow-derived stromal cells as potential cell sources for cartilage repair in the horse. Vet J. 2012; 192(3):345–351. doi:10.1016/j.tvjl.2011.08.036.
   PubMed Web of Science ®Google Scholar
• Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJPF, van Milligen FJ. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy. 2006; 8(2):166–177. doi:10.1080/14653240600621125.
   PubMed Web of Science ®Google Scholar
• Jayasuriya CT, Chen Q. Potential benefits and limitations of utilizing chondroprogenitors in cell-based cartilage therapy. Connect Tissue Res. 2015; 56(4):265–271. doi:10.3109/03008207.2015.1040547.
   PubMed Web of Science ®Google Scholar
• Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev. 2008; 129(3):163–173. doi:10.1016/j.mad.2007.12.002.
   PubMed Web of Science ®Google Scholar
• Choi Y-S, Noh S-E, Lim S-M, Lee C-W, Kim C-S, Im M-W, Lee M-H, Kim D-I. Multipotency and growth characteristic of periosteum-derived progenitor cells for chondrogenic, osteogenic, and adipogenic differentiation. Biotechnol Lett. 2008; 30(4):593–601. doi:10.1007/s10529-007-9584-2.
   PubMed Web of Science ®Google Scholar
• Ding D-C, Wu K-C, Chou H-L, Hung W-T, Liu H-W, Chu T-Y. Human infrapatellar fat pad-derived stromal cells have more potent differentiation capacity than other mesenchymal cells and can be enhanced by hyaluronan. Cell Transplant. 2015; 24(7):1221–1232. doi:10.3727/096368914X681937.
   PubMed Web of Science ®Google Scholar
• Alegre-Aguaron E, Desportes P, Garcia-Alvarez F, Castiella T, Larrad L, Martinez-Lorenzo MJ. Differences in surface marker expression and chondrogenic potential among various tissue-derived mesenchymal cells from elderly patients with osteoarthritis. Cells Tissues Organs. 2012; 196(3):231–240. doi:10.1159/000334400.
   PubMed Web of Science ®Google Scholar
• Garcia J, Mennan C, McCarthy HS, Roberts S, Richardson JB, Wright KT. Chondrogenic potency analyses of donor-matched chondrocytes and mesenchymal stem cells derived from bone marrow, infrapatellar fat pad, and subcutaneous fat. Stem Cells Int. 2016;2016. doi:10.1155/2016/6969726.
   Web of Science ®Google Scholar
• Pires de Carvalho P, Hamel KM, Duarte R, King AGS, Haque M, Dietrich MA, Wu X, Shah F, Burk D, Reis RL, Rood J, Zhang P, Lopez M, Gimble JM, Dasa V. Comparison of infrapatellar and subcutaneous adipose tissue stromal vascular fraction and stromal/stem cells in osteoarthritic subjects. J Tissue Eng Regen Med. 2014; 8(10):757–762. doi:10.1002/term.1565.
   PubMed Web of Science ®Google Scholar
• Mantripragada VP, Piuzzi NS, Zachos T, Obuchowski NA, Muschler GF, Midura RJ. Histopathological assessment of primary osteoarthritic knees in large patient cohort reveal the possibility of several potential patterns of osteoarthritis initiation. Curr Res Transl Med. 2017; 65(4):133–139. doi:10.1016/j.retram.2017.09.002.
   PubMed Web of Science ®Google Scholar
• Mantripragada VP, Piuzzi NS, Zachos T, Obuchowski NA, Muschler GF, Midura RJ. High occurrence of osteoarthritic histopathological features unaccounted for by traditional scoring systems in lateral femoral condyles from total knee arthroplasty patients with varus alignment. Acta Orthop. 2018; 89(2):197–203. doi:10.1080/17453674.2017.1398559.
   PubMed Web of Science ®Google Scholar
• Van Landuyt KB, Jones EA, McGonagle D, Luyten FP, Lories RJ. Flow cytometric characterization of freshly isolated and culture expanded human synovial cell populations in patients with chronic arthritis. Arthritis Res Ther. 2010; 12(1):1–14. doi:10.1186/ar2916.
   Web of Science ®Google Scholar