Mechanical loading of the intervertebral disc: From the macroscopic to the cellular level

European Spine Journal

Volumn 23, Issue SUPPL. 3, 2014, Pages

  Neidlinger Wilke, Cornelia ^a   Galbusera, Fabio ^a,b   Pratsinis, Harris ^c   Mavrogonatou, Eleni ^c   Mietsch, Antje ^a   Kletsas, Dimitris ^c   Wilke, Hans Joachim ^a  

^a UNIVERSITY OF ULM   (Germany)

^b IRCCS ISTITUTO ORTOPEDICO GALEAZZI   (Italy)

^c INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

Degenerative environment; Intervertebral disc mechanobiology; Intradiscal pressure; Mechanotransduction; Spinal loads

Indexed keywords

AGING; BIOCHEMICAL COMPOSITION; BONE METABOLISM; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; DEGENERATION; DEGRADATION KINETICS; ENVIRONMENT; HUMAN; INTERVERTEBRAL DISK; INTRACELLULAR SIGNALING; MECHANICAL LOADING; MECHANOTRANSDUCTION; MEDICAL LITERATURE; MEDICAL PARAMETERS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS; TURNOVER TIME;

AGING; ANIMALS; CELL CULTURE TECHNIQUES; HUMANS; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; MECHANOTRANSDUCTION, CELLULAR; MODELS, ANIMAL;

EID: 84905400560     PISSN: 09406719     EISSN: 14320932     Source Type: Journal    
DOI: 10.1007/s00586-013-2855-9     Document Type: Review

References (108)

1. Abouhossein A, Weisse B, Ferguson SJ (2011) A multibody modelling approach to determine load sharing between passive elements of the lumbar spine. Comput Methods Biomech Biomed Engin 14(6):527-537
2. Adams MA, Dolan P, McNally DS (2009) The internal mechanical functioning of intervertebral discs and articular cartilage, and its relevance to matrix biology. Matrix Biol 28(7):384-389
3. Adams MA, McNally DS, Dolan P (1996) 'Stress' distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br 78(6):965-972 (Pubitemid 26392131)
4. Arjmand N, Gagnon D, Plamondon A, Shirazi-Adl A, Lariviere C (2010) A comparative study of two trunk biomechanical models under symmetric and asymmetric loadings. J Biomech 43(3):485-491
5. Barbir A, Godburn KE, Michalek AJ, Lai A, Monsey RD, Iatridis JC (2011) Effects of torsion on intervertebral disc gene expression and biomechanics, using a rat tail model. Spine 36(8):607-614
6. Barrey C, Roussouly P, Perrin G, Le Huec JC (2011) Sagittal balance disorders in severe degenerative spine. Can we identify the compensatory mechanisms? Eur Spine J 20(Suppl 5):626-633
7. Boos N, Weissbach S, Rohrbach H, Weiler C, Spratt KF, Nerlich AG (2002) Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine 27(23):2631-2644 (Pubitemid 35425317)
8. Boubriak OA, Watson N, Sivan SS, Stubbens N, Urban JP (2013) Factors regulating viable cell density in the intervertebral disc: blood supply in relation to disc height. J Anat 222(3):341-348
9. Carragee EJ, Don AS, Hurwitz EL, Cuellar JM, Carrino J, Herzog R (2009) 2009 ISSLS Prize Winner: does discography cause accelerated progression of degeneration changes in the lumbar disc: a ten-year matched cohort study. Spine (Phila Pa 1976) 34(21):2338-2345
10. Cho H, Seth A, Warmbold J, Robertson JT, Hasty KA (2011) Aging affects response to cyclic tensile stretch: paradigm for intervertebral disc degeneration. Eur Cell Mater 22:137-145 (discussion 145-6)
11. Christophy M, Faruk Senan NA, Lotz JC, O'Reilly OM (2012) A musculoskeletal model for the lumbar spine. Biomech Model Mechanobiol 11(1-2):19-34
12. Court C, Chin JR, Liebenberg E, Colliou OK, Lotz JC (2007) Biological and mechanical consequences of transient intervertebral disc bending. Eur Spine J 16(11):1899-1906 (Pubitemid 350105333)
13. Dolan P, Adams MA (2001) Recent advances in lumbar spinal mechanics and their significance for modelling. Clin Biomech (Bristol, Avon) 16(Suppl 1):S8-S16 (Pubitemid 33732988)
14. Ferguson SJ, Steffen T (2003) Biomechanics of the aging spine. Eur Spine J 12(Suppl 2):S97-S103 (Pubitemid 37409927)
15. Fernando HN, Czamanski J, Yuan TY, Gu W, Salahadin A, Huang CY (2011) Mechanical loading affects the energy metabolism of intervertebral disc cells. J Orthop Res: Off Pub Orthop Res Soc 29(11):1634-1641
16. Frost HM (2003) Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275(2):1081-1101
17. Gagnon D, Arjmand N, Plamondon A, Shirazi-Adl A, Lariviere C (2011) An improved multi-joint EMG-assisted optimization approach to estimate joint and muscle forces in a musculoskeletal model of the lumbar spine. J Biomech 44(8):1521-1529
18. Gantenbein B, Grunhagen T, Lee CR, van Donkelaar CC, Alini M, Ito K (2006) An in vitro organ culturing system for intervertebral disc explants with vertebral endplates: a feasibility study with ovine caudal discs. Spine 31(23):2665-2673 (Pubitemid 44673377)
19. Gilbert HT, Hoyland JA, Freemont AJ, Millward-Sadler SJ (2011) The involvement of interleukin-1 and interleukin-4 in the response of human annulus fibrosus cells to cyclic tensile strain: an altered mechanotransduction pathway with degeneration. Arthr Res Ther 13(1):R8
20. Gordeladze JO, Djouad F, Brondello JM, Noel D, Duroux-Richard I, Apparailly F, Jorgensen C (2009) Concerted stimuli regulating osteo-chondral differentiation from stem cells: phenotype acquisition regulated by microRNAs. Acta Pharmacol Sin 30(10):1369-1384
21. Grivas TB, Vasiliadis ES, Kaspiris A, Khaldi L, Kletsas D (2011) Expression of matrix metalloproteinase-1 (MMP-1) in Wistar rat's intervertebral disc after experimentally induced scoliotic deformity. Scoliosis 6(1):9
22. Guehring T, Unglaub F, Lorenz H, Omlor G, Wilke HJ, Kroeber MW (2006) Intradiscal pressure measurements in normal discs, compressed discs and compressed discs treated with axial posterior disc distraction: an experimental study on the rabbit lumbar spine model. Eur Spine J 15(5):597-604
23. Haglund L, Moir J, Beckman L, Mulligan KR, Jim B, Ouellet JA, Roughley P, Steffen T (2011) Development of a bioreactor for axially loaded intervertebral disc organ culture. Tissue Eng Part C Methods 17(10):1011-1019
24. Han KS, Rohlmann A, Yang SJ, Kim BS, Lim TH (2011) Spinal muscles can create compressive follower loads in the lumbar spine in a neutral standing posture. Med Eng Phys 33(4):472-478
25. Han KS, Zander T, Taylor WR, Rohlmann A (2012) An enhanced and validated generic thoraco-lumbar spine model for prediction of muscle forces. Med Eng Phys 34(6):709-716
26. Handa T, Ishihara H, Ohshima H, Osada R, Tsuji H, Obata K (1997) Effects of hydrostatic pressure on matrix synthesis and matrix metalloproteinase production in the human lumbar intervertebral disc. Spine 22(10):1085-1091 (Pubitemid 27209349)
27. Haschtmann D, Stoyanov JV, Ferguson SJ (2006) Influence of diurnal hyperosmotic loading on the metabolism and matrix gene expression of a whole-organ intervertebral disc model. J Orthop Res 24(10):1957-1966 (Pubitemid 44559956)
28. Hsieh AH, Twomey JD (2010) Cellular mechanobiology of the intervertebral disc: new directions and approaches. J Biomech 43(1):137-145
29. Iatridis JC, MacLean JJ, Roughley PJ, Alini M (2006) Effects of mechanical loading on intervertebral disc metabolism in vivo. J Bone Joint Surg Am 88(Suppl 2):41-46
30. Iatridis JC, Mente PL, Stokes IA, Aronsson DD, Alini M (1999) Compression-induced changes in intervertebral disc properties in a rat tail model. Spine 24(10):996-1002 (Pubitemid 29222621)
31. Illien-Junger S, Gantenbein-Ritter B, Grad S, Lezuo P, Ferguson SJ, Alini M, Ito K (2010) The combined effects of limited nutrition and high-frequency loading on intervertebral discs with endplates. Spine 35(19):1744-1752
32. Illien-Junger S, Pattappa G, Peroglio M, Benneker LM, Stoddart MJ, Sakai D, Mochida J, Grad S, Alini M (2012) Homing of mesenchymal stem cells in induced degenerative intervertebral discs in a whole organ culture system. Spine 37(22):1865-1873
33. Johnson WE, Patterson AM, Eisenstein SM, Roberts S (2007) The presence of pleiotrophin in the human intervertebral disc is associated with increased vascularization: an immunohistologic study. Spine 32(12):1295-1302 (Pubitemid 46791447)
34. Kasra M, Goel V, Martin J, Wang ST, Choi W, Buckwalter J (2003) Effect of dynamic hydrostatic pressure on rabbit intervertebral disc cells. J Orthop Res 21(4):597-603 (Pubitemid 36758202)
35. Kasra M, Merryman WD, Loveless KN, Goel VK, Martin JD, Buckwalter JA (2006) Frequency response of pig intervertebral disc cells subjected to dynamic hydrostatic pressure. J Orthop Res 24(10):1967-1973 (Pubitemid 44559957)
36. Kletsas D, Basdra EK, Papavassiliou AG (2002) Effect of protein kinase inhibitors on the stretch-elicited c-Fos and c-Jun upregulation in human PDL osteoblast-like cells. J Cell Physiol 190(3):313-321 (Pubitemid 34111972)
37. Korecki CL, Kuo CK, Tuan RS, Iatridis JC (2009) Intervertebral disc cell response to dynamic compression is age and frequency dependent. J Orthop Res 27(6):800-806
38. Korecki CL, MacLean JJ, Iatridis JC (2008) Dynamic compression effects on intervertebral disc mechanics and biology. Spine 33(13):1403-1409
39. Le Huec JC, Saddiki R, Franke J, Rigal J, Aunoble S (2011) Equilibrium of the human body and the gravity line: the basics. Eur Spine J 20(Suppl 5):558-563
40. Le Maitre CL, Frain J, Fotheringham AP, Freemont AJ, Hoyland JA (2008) Human cells derived from degenerate intervertebral discs respond differently to those derived from non-degenerate intervertebral discs following application of dynamic hydrostatic pressure. Biorheology 45(5):563-575
41. Le Maitre CL, Frain J, Millward-Sadler J, Fotheringham AP, Freemont AJ, Hoyland JA (2009) Altered integrin mechanotransduction in human nucleus pulposus cells derived from degenerated discs. Arthr Rheum 60(2):460-469
42. Le Maitre CL, Freemont AJ, Hoyland JA (2004) Localization of degradative enzymes and their inhibitors in the degenerate human intervertebral disc. J Pathol 204(1):47-54 (Pubitemid 39214481)
43. Lee CR, Iatridis JC, Poveda L, Alini M (2006) In vitro organ culture of the bovine intervertebral disc: effects of vertebral endplate and potential for mechanobiology studies. Spine (Phila Pa 1976) 31(5):515-522
44. Li S, Jia X, Duance VC, Blain EJ (2011) The effects of cyclic tensile strain on the organisation and expression of cytoskeletal elements in bovine intervertebral disc cells: an in vitro study. Eur Cell Mater 21:508-522
45. Liu GZ, Ishihara H, Osada R, Kimura T, Tsuji H (2001) Nitric oxide mediates the change of proteoglycan synthesis in the human lumbar intervertebral disc in response to hydrostatic pressure. Spine 26(2):134-141 (Pubitemid 32115602)
46. Lotz JC, Hsieh AH, Walsh AL, Palmer EI, Chin JR (2002) Mechanobiology of the intervertebral disc. Biochem Soc Trans 30(Pt 6):853-858 (Pubitemid 36002366)
47. Maclean JJ, Lee CR, Alini M, Iatridis JC (2005) The effects of short-term load duration on anabolic and catabolic gene expression in the rat tail intervertebral disc. J Orthop Res 23(5):1120-1127 (Pubitemid 41245437)
48. MacLean JJ, Lee CR, Grad S, Ito K, Alini M, Iatridis JC (2003) Effects of immobilization and dynamic compression on intervertebral disc cell gene expression in vivo. Spine 28(10):973-981 (Pubitemid 36583325)
49. Marie PJ (2008) Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys 473(2):98-105
50. Matsumoto T, Kawakami M, Kuribayashi K, Takenaka T, Tamaki T (1999) Cyclic mechanical stretch stress increases the growth rate and collagen synthesis of nucleus pulposus cells in vitro. Spine 24(4):315-319 (Pubitemid 29101939)
51. Mavrogonatou E, Kletsas D (2009) High osmolality activates the G1 and G2 cell cycle checkpoints and affects the DNA integrity of nucleus pulposus intervertebral disc cells triggering an enhanced DNA repair response. DNA Repair (Amst) 8(8):930-943
52. Mavrogonatou E, Kletsas D (2010) Effect of varying osmotic conditions on the response of bovine nucleus pulposus cells to growth factors and the activation of the ERK and Akt pathways. J Orthop Res 28(10):1276-1282
53. Mavrogonatou E, Kletsas D (2012) Differential response of nucleus pulposus intervertebral disc cells to high salt, sorbitol, and urea. J Cell Physiol 227(3):1179-1187
54. McMillan DW, McNally DS, Garbutt G, Adams MA (1996) Stress distributions inside intervertebral discs: the validity of experimental "stress profilometry'. Proc Inst Mech Eng H 210(2):81-87 (Pubitemid 126814183)
55. McNally DS, Adams MA (1992) Internal intervertebral disc mechanics as revealed by stress profilometry. Spine (Phila Pa 1976) 17(1):66-73
56. Mietsch A, Neidlinger-Wilke C, Schrezenmeier H, Mauer UM, Friemert B, Wilke HJ, Ignatius A (2011) Evaluation of platelet-rich plasma and hydrostatic pressure regarding cell differentiation in nucleus pulposus tissue engineering. J Tissue Eng Regen Med 7(3):244-252
57. Miyamoto K, Masuda K, Kim JG, Inoue N, Akeda K, Andersson GB, An HS (2006) Intradiscal injections of osteogenic protein-1 restore the viscoelastic properties of degenerated intervertebral discs. Spine J: Off J N Am Spine Soc 6(6):692-703 (Pubitemid 44660878)
58. Nachemson A, Morris J (1963) Lumbar discometry. Lumbar intradiscal pressure measurements in vivo. Lancet 1(7291):1140-1142
59. Nakamura T, Iribe T, Asou Y, Miyairi H, Ikegami K, Takakuda K (2009) Effects of compressive loading on biomechanical properties of disc and peripheral tissue in a rat tail model. Eur Spine J 18(11):1595-1603
60. Neidlinger-Wilke C, Liedert A, Wuertz K, Buser Z, Rinkler C, Kafer W, Ignatius A, Claes L, Roberts S, Johnson WE (2009) Mechanical stimulation alters pleiotrophin and aggrecan expression by human intervertebral disc cells and influences their capacity to stimulate endothelial migration. Spine 34(7):663-669
61. Neidlinger-Wilke C, Mietsch A, Rinkler C, Wilke HJ, Ignatius A, Urban J (2012) Interactions of environmental conditions and mechanical loads have influence on matrix turnover by nucleus pulposus cells. J Orthop Res: Off Pub Orthop Res Soc 30(1):112-121
62. Neidlinger-Wilke C, Wurtz K, Liedert A, Schmidt C, Borm W, Ignatius A, Wilke HJ, Claes L (2005) A three-dimensional collagen matrix as a suitable culture system for the comparison of cyclic strain and hydrostatic pressure effects on intervertebral disc cells. J Neurosurg Spine 2(4):457-465
63. Neidlinger-Wilke C, Wurtz K, Urban JP, Borm W, Arand M, Ignatius A, Wilke HJ, Claes LE (2006) Regulation of gene expression in intervertebral disc cells by low and high hydrostatic pressure. Eur Spine J 15(Suppl 3):S372-S378 (Pubitemid 44371016)
64. Nerurkar NL, Elliott DM, Mauck RL (2010) Mechanical design criteria for intervertebral disc tissue engineering. J Biomech 43(6):1017-1030
65. O'Connell GD, Johannessen W, Vresilovic EJ, Elliott DM (2007) Human internal disc strains in axial compression measured noninvasively using magnetic resonance imaging. Spine (Phila Pa 1976) 32(25):2860-2868
66. O'Connell GD, Vresilovic EJ, Elliott DM (2011) Human intervertebral disc internal strain in compression: the effect of disc region, loading position, and degeneration. J Orthop Res 29(4):547-555
67. Omlor GW, Lorenz H, Engelleiter K, Richter W, Carstens C, Kroeber MW, Guehring T (2006) Changes in gene expression and protein distribution at different stages of mechanically induced disc degeneration - an in vivo study on the New Zealand white rabbit. J Orthop Res 24(3):385-392 (Pubitemid 43772999)
68. Oshima H, Ishihara H, Urban JP, Tsuji H (1993) The use of coccygeal discs to study intervertebral disc metabolism. J Orthop Res 11(3):332-338 (Pubitemid 23182769)
69. Papachristou DJ, Papachroni KK, Basdra EK, Papavassiliou AG (2009) Signaling networks and transcription factors regulating mechanotransduction in bone. Bioessays 31(7):794-804
70. Papachroni KK, Karatzas DN, Papavassiliou KA, Basdra EK, Papavassiliou AG (2009) Mechanotransduction in osteoblast regulation and bone disease. Trends Mol Med 15(5):208-216
71. Pratap J, Galindo M, Zaidi SK, Vradii D, Bhat BM, Robinson JA, Choi JY, Komori T, Stein JL, Lian JB, Stein GS, van Wijnen AJ (2003) Cell growth regulatory role of Runx2 during proliferative expansion of preosteoblasts. Cancer Res 63(17):5357-5362 (Pubitemid 37139851)
72. Pratsinis H, Constantinou V, Pavlakis K, Sapkas G, Kletsas D (2012) Exogenous and autocrine growth factors stimulate human intervertebral disc cell proliferation via the ERK and Akt pathways. J Orthop Res 30(6):958-964
73. Pratsinis H, Kletsas D (2007) PDGF, bFGF and IGF-I stimulate the proliferation of intervertebral disc cells in vitro via the activation of the ERK and Akt signaling pathways. Eur Spine J 16(11):1858-1866 (Pubitemid 350105321)
74. Pratsinis H, Kletsas D (2008) Growth factors in intervertebral disc homeostasis. Connect Tissue Res 49(3):273-276
75. Rajpurohit R, Risbud MV, Ducheyne P, Vresilovic EJ, Shapiro IM (2002) Phenotypic characteristics of the nucleus pulposus: expression of hypoxia inducing factor-1, glucose transporter-1 and MMP-2. Cell Tissue Res 308(3):401-407 (Pubitemid 34666966)
76. Ramage L, Nuki G, Salter DM (2009) Signalling cascades in mechanotransduction: cell-matrix interactions and mechanical loading. Scand J Med Sci Sports 19(4):457-469
77. Rannou F, Lee TS, Zhou RH, Chin J, Lotz JC, Mayoux-Benhamou MA, Barbet JP, Chevrot A, Shyy JY (2004) Intervertebral disc degeneration: the role of the mitochondrial pathway in annulus fibrosus cell apoptosis induced by overload. Am J Pathol 164(3):915-924 (Pubitemid 38235473)
78. Rannou F, Poiraudeau S, Foltz V, Boiteux M, Corvol M, Revel M (2000) Monolayer anulus fibrosus cell cultures in a mechanically active environment: local culture condition adaptations and cell phenotype study. J Lab Clin Med 136(5):412-421
79. Rannou F, Richette P, Benallaoua M, Francois M, Genries V, Korwin-Zmijowska C, Revel M, Corvol M, Poiraudeau S (2003) Cyclic tensile stretch modulates proteoglycan production by intervertebral disc annulus fibrosus cells through production of nitrite oxide. J Cell Biochem 90(1):148-157 (Pubitemid 37052317)
80. Reza AT, Nicoll SB (2008) Hydrostatic pressure differentially regulates outer and inner annulus fibrosus cell matrix production in 3D scaffolds. Ann Biomed Eng 36(2):204-213
81. Rinkler C, Heuer F, Pedro MT, Mauer UM, Ignatius A, Neidlinger-Wilke C (2010) Influence of low glucose supply on the regulation of gene expression by nucleus pulposus cells and their responsiveness to mechanical loading. J Neurosurg Spine 13(4):535-542
82. Risbud MV, Guttapalli A, Stokes DG, Hawkins D, Danielson KG, Schaer TP, Albert TJ, Shapiro IM (2006) Nucleus pulposus cells express HIF-1 alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment. J Cell Biochem 98(1):152-159
83. Rohlmann A, Arntz U, Graichen F, Bergmann G (2001) Loads on an internal spinal fixation device during sitting. J Biomech 34(8):989-993 (Pubitemid 32633770)
84. Rohlmann A, Gabel U, Graichen F, Bender A, Bergmann G (2007) An instrumented implant for vertebral body replacement that measures loads in the anterior spinal column. Med Eng Phys 29(5):580-585 (Pubitemid 46330872)
85. Rohlmann A, Graichen F, Bender A, Kayser R, Bergmann G (2008) Loads on a telemeterized vertebral body replacement measured in three patients within the first postoperative month. Clin Biomech (Bristol, Avon) 23(2):147-158 (Pubitemid 351172534)
86. Rohlmann A, Graichen F, Weber U, Bergmann G (2000) 2000 Volvo Award winner in biomechanical studies: monitoring in vivo implant loads with a telemeterized internal spinal fixation device. Spine (Phila Pa 1976) 25(23):2981-2986
87. Rohlmann A, Petersen R, Schwachmeyer V, Graichen F, Bergmann G (2012) Spinal loads during position changes. Clin Biomech (Bristol, Avon) 27(8):754-758
88. Rohlmann A, Zander T, Graichen F, Dreischarf M, Bergmann G (2011) Measured loads on a vertebral body replacement during sitting. Spine J 11(9):870-875
89. Salvatierra JC, Yuan TY, Fernando H, Castillo A, Gu WY, Cheung HS, Huant CY (2011) Difference in energy metabolism of annulus fibrosus and nucleus pulposus cells of the intervertebral disc. Cell Mol Bioeng 4(2):302-310
90. Sato K, Kikuchi S, Yonezawa T (1999) In vivo intradiscal pressure measurement in healthy individuals and in patients with ongoing back problems. Spine (Phila Pa 1976) 24(23):2468-2474
91. Setton LA, Chen J (2004) Cell mechanics and mechanobiology in the intervertebral disc. Spine 29(23):2710-2723 (Pubitemid 40353257)
92. Setton LA, Chen J (2006) Mechanobiology of the intervertebral disc and relevance to disc degeneration. J Bone Joint Surg Am 88(Suppl 2):52-57
93. Sowa G, Vadala G, Studer R, Kompel J, Iucu C, Georgescu H, Gilbertson L, Kang J (2008) Characterization of intervertebral disc aging: longitudinal analysis of a rabbit model by magnetic resonance imaging, histology, and gene expression. Spine 33(17):1821-1828
94. Sowa G, Westrick E, Pacek C, Coelho P, Patel D, Vadala G, Georgescu H, Vo N, Studer R, Kang J (2011) In vitro and in vivo testing of a novel regulatory system for gene therapy for intervertebral disc degeneration. Spine 36(10):E623-E628
95. Stokes IA, Aronsson DD, Spence H, Iatridis JC (1998) Mechanical modulation of intervertebral disc thickness in growing rat tails. J Spinal Disord 11(3):261-265 (Pubitemid 28278175)
96. Stokes IA, Iatridis JC (2004) Mechanical conditions that accelerate intervertebral disc degeneration: overload versus immobilization. Spine 29(23):2724-2732 (Pubitemid 40353258)
97. Urban JP (2002) The role of the physicochemical environment in determining disc cell behaviour. Biochem Soc Trans 30(Pt 6):858-864
98. Urban JP, Roberts S (2003) Degeneration of the intervertebral disc. Arthr Res Ther 5(3):120-130 (Pubitemid 36849758)
99. Walter BA, Korecki CL, Purmessur D, Roughley PJ, Michalek AJ, Iatridis JC (2011) Complex loading affects intervertebral disc mechanics and biology. Osteoarthr Cartilage (Osteoarthr Res Soc) 19(8):1011-1018
100. Wenger KH, Woods JA, Holecek A, Eckstein EC, Robertson JT, Hasty KA (2005) Matrix remodeling expression in anulus cells subjected to increased compressive load. Spine (Phila Pa 1976) 30(10):1122-1126
101. Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE (1999) New in vivo measurements of pressures in the intervertebral disc in daily life. Spine 24(8):755-762 (Pubitemid 29181527)
102. Wilke HJ, Rohlmann A, Neller S, Graichen F, Claes L, Bergmann G (2003) ISSLS prize winner: a novel approach to determine trunk muscle forces during flexion and extension: a comparison of data from an in vitro experiment and in vivo measurements. Spine (Phila Pa 1976) 28(23):2585-2593
103. Wuertz K, Godburn K, MacLean JJ, Barbir A, Donnelly JS, Roughley PJ, Alini M, Iatridis JC (2009) In vivo remodeling of intervertebral discs in response to short- and long-term dynamic compression. J Orthop Res 27(9):1235-1242
104. Wuertz K, Urban JP, Klasen J, Ignatius A, Wilke HJ, Claes L, Neidlinger-Wilke C (2007) Influence of extracellular osmolarity and mechanical stimulation on gene expression of intervertebral disc cells. J Orthop Res 25(11):1513-1522 (Pubitemid 350205600)
105. Wuertz K, Vo N, Kletsas D, Boos N (2012) Inflammatory and catabolic signalling in intervertebral discs: the roles of NF-kappaB and MAP kinases. Eur CellMater 23:103-119 (discussion 119-20)
106. Yurube T, Nishida K, Suzuki T, Kaneyama S, Zhang Z, Kakutani K, Maeno K, Takada T, Fujii M, Kurosaka M, Doita M (2010) Matrix metalloproteinase (MMP)-3 gene up-regulation in a rat tail compression loading-induced disc degeneration model. J Orthop Res: Off Pub Orthop Res Soc 28(8):1026-1032
107. Zhang YH, Zhao CQ, Jiang LS, Dai LY (2011) Cyclic stretchinduced apoptosis in rat annulus fibrosus cells is mediated in part by endoplasmic reticulum stress through nitric oxide production. Eur Spine J 20(8):1233-1243
108. Ziros PG, Gil AP, Georgakopoulos T, Habeos I, Kletsas D, Basdra EK, Papavassiliou AG (2002) The bone-specific transcriptional regulator Cbfa1 is a target of mechanical signals in osteoblastic cells. J Biol Chem 277(26):23934-23941 (Pubitemid 34952238)