Stem cells in degenerative orthopaedic pathologies: effects of aging on therapeutic potential

Knee Surgery, Sports Traumatology, Arthroscopy

Volumn 25, Issue 2, 2017, Pages 626-636

  Atesok, Kivanc ^a   Fu, Freddie H ^a   Sekiya, Ichiro ^b   Stolzing, Alexandra ^c,d   Ochi, Mitsuo ^e   Rodeo, Scott A ^f  

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

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c LOUGHBOROUGH UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF LEIPZIG   (Germany)

^e HIROSHIMA UNIVERSITY   (Japan)

^f HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

Aging; Degenerative orthopaedic pathologies; Osteoarthritis; Stem cells; Tissue regeneration

Indexed keywords

AGED; AGING; HUMAN; INTERVERTEBRAL DISC DEGENERATION; OSTEOARTHRITIS; PATHOPHYSIOLOGY; PHYSIOLOGY; STEM CELL TRANSPLANTATION; TENDINOPATHY; TISSUE REGENERATION;

AGED; AGING; GUIDED TISSUE REGENERATION; HUMANS; INTERVERTEBRAL DISC DEGENERATION; OSTEOARTHRITIS; STEM CELL TRANSPLANTATION; TENDINOPATHY;

EID: 84939817320     PISSN: 09422056     EISSN: 14337347     Source Type: Journal    
DOI: 10.1007/s00167-015-3763-9     Document Type: Review

References (71)

1. Al Faqeh H, Nor Hamdan BM, Chen HC, Aminuddin BS, Ruszymah BH (2012) The potential of intra-articular injection of chondrogenic-induced bone marrow stem cells to retard the progression of osteoarthritis in a sheep model. Exp Gerontol 47:458–464
2. Ando W, Heard BJ, Chung M, Nakamura N, Frank CB, Hart DA (2012) Ovine synovial membrane-derived mesenchymal progenitor cells retain the phenotype of the original tissue that was exposed to in vivo inflammation: evidence for a suppressed chondrogenic differentiation potential of the cells. Inflamm Res 61:599–608
3. Avery NC, Bailey AJ (2005) Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports 15:231–240
4. Badowski M, Muise A, Harris DT (2014) Mixed effects of long-term frozen storage on cord tissue stem cells. Cytotherapy 16:1313–1321
5. Beane OS, Fonseca VC, Cooper LL, Koren G, Darling EM (2014) Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS ONE 9:e115963
6. Bogdanova A, Berzins U, Nikulshin S, Skrastina D, Ezerta A, Legzdina D, Kozlovska T (2014) Characterization of human adipose-derived stem cells cultured in autologous serum after subsequent passaging and long term cryopreservation. J Stem Cells. 9:135–148
7. Centeno CJ, Schultz JR, Cheever M, Freeman M, Faulkner S, Robinson B, Hanson R (2011) Safety and complications reporting update on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate technique. Curr Stem Cell Res Ther 6:368–378
8. Chatterjea A, LaPointe VL, Alblas J, Chatterjea S, van Blitterswijk CA, de Boer J (2014) Suppression of the immune system as a critical step for bone formation from allogeneic osteoprogenitors implanted in rats. J Cell Mol Med 18:134–142
9. Chen B, Deng Y, Tan Y, Qin J, Chen LB (2014) Association between severity of knee osteoarthritis and serum and synovial fluid interleukin 17 concentrations. J Int Med Res 42:138–144
10. Clayton RA, Court-Brown CM (2008) The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury 39:1338–1344
11. De Miguel MP, Fuentes-Julián S, Blázquez-Martínez A, Pascual CY, Aller MA, Arias J, Arnalich-Montiel F (2012) Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr Mol Med 12:574–591
12. Diekman BO, Guilak F (2013) Stem cell-based therapies for osteoarthritis: challenges and opportunities. Curr Opin Rheumatol 25:119–126
13. Emadedin M, Aghdami N, Taghiyar L, Fazeli R, Moghadasali R, Jahangir S, Farjad R, Baghaban Eslaminejad M (2012) Intra-articular injection of autologous mesenchymal stem cells in six patients with knee osteoarthritis. Arch Iran Med 15:422–428
14. Fernyhough LJ, Buchan VA, McArthur LT, Hock BD (2013) Relative recovery of haematopoietic stem cell products after cryogenic storage of up to 19 years. Bone Marrow Transpl 48:32–35
15. Goldring MB, Otero M (2011) Inflammation in osteoarthritis. Curr Opin Rheumatol 23:471–478
16. Gupta PK, Das AK, Chullikana A, Majumdar AS (2012) Mesenchymal stem cells for cartilage repair in osteoarthritis. Stem Cell Res Ther 3:25
17. Hauser RA, Orlofsky A (2013) Regenerative injection therapy with whole bone marrow aspirate for degenerative joint disease: a case series. Clin Med Insights Arthritis Musculoskelet Disord 6:65–72
18. Heldens GT, Blaney Davidson EN, Vitters EL, Schreurs BW, Piek E, van den Berg WB, van der Kraan PM (2012) Catabolic factors and osteoarthritis-conditioned medium inhibit chondrogenesis of human mesenchymal stem cells. Tissue Eng Part A 18(1–2):45–54
19. Ippolito E, Natali PG, Postacchini F, Accinni L, De Martino C (1980) Morphological, immunochemical, and biochemical study of rabbit achilles tendon at various ages. J Bone Joint Surg Am 62:583–598
20. Jenkins EC, Ye L, Gu H, Ni SA, Velinov M, Pang D, Krinsky-McHale SJ, Zigman WB, Schupf N, Silverman WP (2010) Shorter telomeres may indicate dementia status in older individuals with Down syndrome. Neurobiol Aging 31:765–771
21. Jiang Y, Mishima H, Sakai S, Liu YK, Ohyabu Y, Uemura T (2008) Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders. J Orthop Res 26:910–917
22. Jo CH, Lee YG, Shin WH, Kim H, Chai JW, Jeong EC, Kim JE, Shim H, Shin JS, Shin IS, Ra JC, Oh S, Yoon KS (2014) Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: a proof-of-concept clinical trial. Stem Cells 32:1254–1266
23. Kelsey JL, Hochberg MC (1988) Epidemiology of chronic musculoskeletal disorders. Ann Rev Public Health 9:379–401
24. Koh YG, Choi YJ (2012) Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee 19:902–907
25. Kondo M, Yamaoka K, Sonomoto K, Fukuyo S, Oshita K, Okada Y, Tanaka Y (2013) IL-17 inhibits chondrogenic differentiation of human mesenchymal stem cells. PLoS ONE 8:e79463
26. Koshy PJ, Henderson N, Logan C, Life PF, Cawston TE, Rowan AD (2002) Interleukin 17 induces cartilage collagen breakdown: novel synergistic effects in combination with proinflammatory cytokines. Ann Rheum Dis 61:704–713
27. Kristjánsson B, Honsawek S (2014) Current perspectives in mesenchymal stem cell therapies for osteoarthritis. Stem Cells Int 2014:194318
28. Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K (2008) Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. Haematologica 93:1457–1465
29. Li J, Pei M (2012) Cell senescence: a challenge in cartilage engineering and regeneration. Tissue Eng Part B Rev 18:270–287
30. Loeser RF (2011) Aging and osteoarthritis. Curr Opin Rheumatol 23:492–496
31. Loeser RF (2012) The effects of aging on the development of osteoarthritis. HSS J. 8:18–19
32. Maerz T, Herkowitz H, Baker K (2013) Molecular and genetic advances in the regeneration of the intervertebral disc. Surg Neurol Int 4:S94–S105
33. Marks PH, Donaldson ML (2005) Inflammatory cytokine profiles associated with chondral damage in the anterior cruciate ligament-deficient knee. Arthroscopy 21:1342–1347
34. Matsukura Y, Muneta T, Tsuji K, Miyatake K, Yamada J, Abula K, Koga H, Tomita M, Sekiya I (2015) Mouse synovial mesenchymal stem cells increase in yield with knee inflammation. J Orthop Res 33:246–253
35. Mochizuki T, Muneta T, Sakaguchi Y, Nimura A, Yokoyama A, Koga H, Sekiya I (2006) Higher chondrogenic potential of fibrous synovium- and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum 54:843–853
36. Muschler GF, Nitto H, Boehm CA, Easley KA (2001) Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 19:117–125
37. Nishimori M, Deie M, Kanaya A, Exham H, Adachi N, Ochi M (2006) Repair of chronic osteochondral defects in the rat. A bone marrow-stimulating procedure enhanced by cultured allogenic bone marrow mesenchymal stromal cells. J Bone Joint Surg Br 88:1236–1244
38. Nöth U, Steinert AF, Tuan RS (2008) Technology insight: adult mesenchymal stem cells for osteoarthritis therapy. Nat Clin Pract Rheumatol 4:371–380
39. Orozco L, Munar A, Soler R, Alberca M, Soler F, Huguet M, Sentís J, Sánchez A, García- Sancho J (2013) Treatment of knee osteoarthritis with autologous mesenchymal stem cells: a pilot study. Transplantation 95:1535–1541
40. Pan J, Wang B, Li W, Zhou X, Scherr T, Yang Y, Price C, Wang L (2012) Elevated cross-talk between subchondral bone and cartilage in osteoarthritic joints. Bone 51:212–217
41. Peffers MJ, Thorpe CT, Collins JA, Eong R, Wei TK, Screen HR, Clegg PD (2014) Proteomic analysis reveals age-related changes in tendon matrix composition, with age- and injury-specific matrix fragmentation. J Biol Chem 289:25867–25878
42. Pintan GF, de Oliveira AS, Jr LenzaM, Antonioli E, Ferretti M (2014) Update on biological therapies for knee injuries: osteoarthritis. Curr Rev Musculoskelet Med. 7:263–269
43. Rohani L, Johnson AA, Arnold A, Stolzing A (2014) The aging signature: a hallmark of induced pluripotent stem cells? Aging Cell 13(1):2–7
44. Saeed H, Iqtedar M (2013) Stem cell function and maintenance—ends that matter: role of telomeres and telomerase. J Biosci 38:641–649
45. Saw KY, Anz A, Siew-Yoke Jee C, Merican S, Ching-Soong Ng R, Roohi SA, Ragavanaidu K (2013) Articular cartilage regeneration with autologous peripheral blood stem cells versus hyaluronic acid: a randomized controlled trial. Arthroscopy 29:684–694
46. Scanzello CR, Umoh E, Pessler F, Diaz-Torne C, Miles T, Dicarlo E, Potter HG, Mandl L, Marx R, Rodeo S, Goldring SR, Crow MK (2009) Local cytokine profiles in knee osteoarthritis: elevated synovial fluid interleukin-15 differentiates early from end-stage disease. Osteoarthr Cartil 17:1040–1048
47. Schu S, Nosov M, O’Flynn L, Shaw G, Treacy O, Barry F, Murphy M, O’Brien T, Ritter T (2012) Immunogenicity of allogeneic mesenchymal stem cells. J Cell Mol Med 16:2094–2103
48. Sekiya I, Ojima M, Suzuki S, Yamaga M, Horie M, Koga H, Tsuji K, Miyaguchi K, Ogishima S, Tanaka H, Muneta T (2012) Human mesenchymal stem cells in synovial fluid increase in the knee with degenerated cartilage and osteoarthritis. J Orthop Res 30:943–949
49. Shane Anderson A, Loeser RF (2010) Why is osteoarthritis an age-related disease? Best Pract Res Clin Rheumatol 24:15–26
50. Smith RK, Werling NJ, Dakin SG, Alam R, Goodship AE, Dudhia J (2013) Beneficial effects of autologous bone marrow-derived mesenchymal stem cells in naturally occurring tendinopathy. PLoS ONE 8:e75697
51. Stenderup K, Justesen J, Clausen C, Kassem M (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919–926
52. Stolzing A, Colley H, Scutt A (2011) Effect of age and diabetes on the response of mesenchymal progenitor cells to fibrin matrices. Int J Biomater. 2011:378034
53. Stolzing A, Jones E, McGonagle D, Scutt A (2008) Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129:163–173
54. Stolzing A, Scutt A (2006) Age-related impairment of mesenchymal progenitor cell function. Aging Cell 5:213–224
55. Suram A, Herbig U (2014) The replicometer is broken: telomeres activate cellular senescence in response to genotoxic stresses. Aging Cell 13:780–786
56. Takano T, Li YJ, Kukita A, Yamaza T, Ayukawa Y, Moriyama K, Uehara N, Nomiyama H, Koyano K, Kukita T (2014) Mesenchymal stem cells markedly suppress inflammatory bone destruction in rats with adjuvant-induced arthritis. Lab Invest 94:286–296
57. Teraguchi M, Yoshimura N, Hashizume H, Muraki S, Yamada H, Minamide A, Oka H, Ishimoto Y, Nagata K, Kagotani R, Takiguchi N, Akune T, Kawaguchi H, Nakamura K, Yoshida M (2014) Prevalence and distribution of intervertebral disc degeneration over the entire spine in a population-based cohort: the Wakayama Spine Study. Osteoarthr Cartil 22:104–110
58. Thorpe CT, Streeter I, Pinchbeck GL, Goodship AE, Clegg PD, Birch HL (2010) Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging. J Biol Chem 285:15674–15681
59. van Buul GM, Siebelt M, Leijs MJ, Bos PK, Waarsing JH, Kops N, Weinans H, Verhaar JA, Bernsen MR, van Osch GJ (2014) Mesenchymal stem cells reduce pain but not degenerative changes in a mono-iodoacetate rat model of osteoarthritis. J Orthop Res 32:1167–1174
60. Vangsness CT Jr, Farr J 2nd, Boyd J, Dellaero DT, Mills CR, LeRoux-Williams M (2014) Adult human mesenchymal stem cells delivered via intra-articular injection to the knee following partial medial meniscectomy: a randomized, double-blind, controlled study. J Bone Joint Surg Am 96:90–98
61. Vega A, Martín-Ferrero MA, Del Canto F, Alberca M, García V, Munar A, Orozco L, Soler R, Fuertes JJ, Huguet M, Sánchez A, García-Sancho J (2015) Treatment of knee osteoarthritis with allogeneic bone marrow mesenchymal stem cells: a randomized controlled trial. Transplantation. doi:10.1097/TP.0000000000000678
62. Wang Z, Perez-Terzic CM, Smith J, Mauck WD, Shelerud RA, Maus TP, Yang TH, Murad MH, Gou S, Terry MJ, Dauffenbach JP, Pingree MJ, Eldrige JS, Mohammed K, Benkhadra K, van Wijnen AJ, Qu W (2015) Efficacy of intervertebral disc regeneration with stem cells—a systematic review and meta-analysis of animal controlled trials. Gene 564:1–8
63. Wehling N, Palmer GD, Pilapil C, Liu F, Wells JW, Müller PE, Evans CH, Porter RM (2009) Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum 60:801–812
64. Wojdasiewicz P, Poniatowski ŁA, Szukiewicz D (2014) The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediat Inflamm. doi:10.1155/2014/561459
65. Wong KL, Lee KB, Tai BC, Law P, Lee EH, Hui JH (2013) Injectable cultured bone marrow-derived mesenchymal stem cells in varus knees with cartilage defects undergoing high tibial osteotomy: a prospective, randomized controlled clinical trial with 2 years’ follow-up. Arthroscopy 29:2020–2028
66. Yang YM, Li P, Cui DC, Dang RJ, Zhang L, Wen N, Jiang XX (2015) Effect of aged bone marrow microenvironment on mesenchymal stem cell migration. Age (Dordr) 37:16
67. Yelin EH, Trupin LS, Sebesta DS (1999) Transitions in employment, morbidity, and disability among persons ages 51–61 with musculoskeletal and non-musculoskeletal conditions in the US, 1992–94. Arthritis Rheumatol 42:769–779
68. Zhang J, Wang JH (2014) PRP treatment effects on degenerative tendinopathy—an in vitro model study. Muscles Ligaments Tendons J 4:10–17
69. Zhou Z, Akinbiyi T, Xu L, Ramcharan M, Leong DJ, Ros SJ, Colvin AC, Schaffler MB, Majeska RJ, Flatow EL, Sun HB (2010) Tendon-derived stem/progenitor cell aging: defective self-renewal and altered fate. Aging Cell 9:911–915
70. Zhu X, Yuan F, Li H, Zheng Y, Xiao Y, Yan F (2013) Evaluation of canine bone marrow-derived mesenchymal stem cells after long-term cryopreservation. Zool Sci 30:1032–1037
71. Zimmermann S, Voss M, Kaiser S, Kapp U, Waller CF, Martens UM (2003) Lack of telomerase activity in human mesenchymal stem cells. Leukemia 17:1146–1149