Support of concept that migrating progenitor cells from stem cell niches contribute to normal regeneration of the adult mammal intervertebral disc: A descriptive study in the New Zealand white rabbit

Spine

Volumn 37, Issue 9, 2012, Pages 722-732

  Henriksson, Helena Barreto ^a   Svala, Emilia ^b   Skioldebrand, Eva ^b   Lindahl, Anders ^a   Brisby, Helena ^a  

^a SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

BrdU; cell migration; Disc regeneration; GDF5; in vivo labeling; intervertebral disc; stem cell niches

Indexed keywords

BETA1 INTEGRIN; BROXURIDINE; GROWTH DIFFERENTIATION FACTOR 5; PROTEIN SNAI 1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIVISION; CELL MIGRATION; CONTROLLED STUDY; DESCRIPTIVE RESEARCH; EPIPHYSIS PLATE; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTERVERTEBRAL DISK; MITOSIS; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; STEM CELL NICHE;

AGE FACTORS; AGING; ANIMALS; ANTIGENS, CD29; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CHONDROGENESIS; DNA REPLICATION; FEMALE; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 5; IMMUNOHISTOCHEMISTRY; INTERVERTEBRAL DISC; RABBITS; REGENERATION; SOX9 TRANSCRIPTION FACTOR; STEM CELL NICHE; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84860326883     PISSN: 03622436     EISSN: 15281159     Source Type: Journal    
DOI: 10.1097/BRS.0b013e318231c2f7     Document Type: Article

References (52)

1. Maetzel A, Li L. The economic burden of low back pain: a review of studies published between 1996 and 2001. Best Pract Res Clin Rheumatol 2002;16:23-30.
2. Namba RS, Meuli M, Sullivan KM, et al. Spontaneous repair of superfi cial defects in articular cartilage in a fetal lamb model. J Bone Joint Surg Am 1998;80:4-10. (Pubitemid 28087294)
3. Vasara AI, Hyttinen MM, Pulliainen O, et al. Immature porcine knee cartilage lesions show good healing with or without autol-ogous chondrocyte transplantation. Osteoarthritis Cartilage 2006;14:1066-74. (Pubitemid 44309418)
4. Hollander AP, Dickinson SC, Kafienah W. Stem cells and car-tilage development: complexities of a simple tissue. Stem Cells 2010;28:1992-6.
5. Humzah MD, Soames RW. Human intervertebral disc: structure and function. Anat Rec 1988;220:337-56.
6. Melrose J, Smith SM, Fuller ES, et al. Biglycan and fi bromodulin fragmentation correlates with temporal and spatial annular remod-elling in experimentally injured ovine intervertebral discs. Eur Spine J 2007;16:2193-205. (Pubitemid 350276093)
7. Smith JW, Walmsley R. Experimental incision of the intervertebral disc. J Bone Joint Surg Br 1951;33-B:612-25.
8. Korecki CL, Costi JJ, Iatridis JC. Needle puncture injury affects intervertebral disc mechanics and biology in an organ culture model. Spine (Phila Pa 1976) 2008;33:235-41. (Pubitemid 351322927)
9. Risbud MV, Guttapalli A, Tsai TT, et al. Evidence for skeletal pro-genitor cells in the degenerate human intervertebral disc. Spine (Phila Pa 1976) 2007;32:2537-44. (Pubitemid 350059479)
10. Henriksson HB, Thornemo M, Karlsson C, et al. Identifi cation of cell proliferation zones, progenitor cells and a potential stem cell niche in the intervertebral disc region: a study in four species. Spine (Phila Pa 1976) 2009;34:2278-87.
11. Dowthwaite GP, Bishop JC, Redman SN, et al. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 2004;117 (pt 6): 889-97. (Pubitemid 38386946)
12. Karlsson C, Thornemo M, Henriksson HB, et al. Identification of a stem cell niche in the zone of Ranvier within the knee joint. J Anat 2009;215:355-63.
13. Crochiere ML, Kubilus JK, Linsenmayer TF. Identifi cation and characterization of a previously undetected region between the peri-chondrium and periosteum of the developing avian limb. Dev Biol 2006;299:505-16. (Pubitemid 44637275)
14. Fenichel I, Evron Z, Nevo Z. The perichondrial ring as a reservoir for precartilaginous cells. In vivo model in young chicks' epiphysis. Int Orthop 2006;30:353-6.
15. Hunziker EB, Kapfinger E, Geiss J. The structural architecture of adult mammalian articular cartilage evolves by a synchronized pro-cess of tissue resorption and neoformation during postnatal devel-opment. Osteoarthritis Cartilage 2007;15:403-13. (Pubitemid 46381564)
16. Allen JW, Shuler CF, Latt SA. Bromodeoxyuridine tablet method-ology for in vivo studies of DNA synthesis. Somatic Cell Genet 1978;4:393-405. (Pubitemid 8397102)
17. Voog J, Jones DL. Stem cells and the niche: a dynamic duo. Cell Stem Cell 2010;6:103-15.
18. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002;115 (pt 11): 2381-8. (Pubitemid 34752981)
19. Eriksson PS, Perfilieva E, Bjork-Eriksson T, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998;4:1313-7. (Pubitemid 28512114)
20. Horsley V, O'Carroll D, Tooze R, et al. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 2006;126:597-609. (Pubitemid 44163616)
21. Baur ST, Mai JJ, Dymecki SM. Combinatorial signaling through BMP receptor IB and GDF5: shaping of the distal mouse limb and the genetics of distal limb diversity. Development 2000;127:605-19. (Pubitemid 30093408)
22. Storm EE, Kingsley DM. GDF5 coordinates bone and joint forma-tion during digit development. Dev Biol 1999;209:11-27. (Pubitemid 29194309)
23. Pacifici M, Koyama E, Shibukawa Y, et al. Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Ann N Y Acad Sci 2006; 1068: 74-86. (Pubitemid 43824138)
24. Rountree RB, Schoor M, Chen H, et al. BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol 2004; 2:1545-785.
25. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins. Growth Factors 2004;22:233-41. (Pubitemid 40136452)
26. Seemann P, Schwappacher R, Kjaer KW, et al. Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J Clin Invest 2005; 115:2373-81. (Pubitemid 41266199)
27. Chimal-Monroy J, Rodriguez-Leon J, Montero JA, et al. Analysis of the molecular cascade responsible for mesodermal limb chondro-genesis: Sox genes and BMP signaling. Dev Biol 2003;257:292-301. (Pubitemid 36506845)
28. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003;15:740-6. (Pubitemid 37487967)
29. Doherty GJ, McMahon HT. Mediation, modulation, and conse-quences of membrane-cytoskeleton interactions. Annu Rev Biophys 2008;37:65-95.
30. Laird DJ, von Andrian UH, Wagers AJ. Stem cell trafficking in tis-sue development, growth, and disease. Cell 2008;132:612-30. (Pubitemid 351253693)
31. Hattori N, Mochizuki S, Kishi K, et al. MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am J Pathol 2009;175:533-46.
32. Brabletz T, Hlubek F, Spaderna S, et al. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchy-mal-epithelial transition, stem cells and beta-catenin. Cells Tissues Organs 2005;179:56-65. (Pubitemid 40976289)
33. Hotz B, Visekruna A, Buhr HJ, et al. Beyond epithelial to mes-enchymal transition: a novel role for the transcription factor snail in inflammation and wound healing. J Gastrointest Surg 2009;14:388-97.
34. Barrallo-Gimeno A, Nieto MA. Evolutionary history of the Snail/Scratch superfamily. Trends Genet 2009;25:248-52.
35. Nieto MA. The snail superfamily of zinc-finger transcription fac-tors. Nat Rev Mol Cell Biol 2002;3:155-66.
36. Gottschling S, Saffrich R, Seckinger A, et al. Human mesenchymal stromal cells regulate initial self-renewing divisions of hematopoi-etic progenitor cells by a beta1-integrin-dependent mechanism. Stem Cells 2007;25:798-806. (Pubitemid 46354240)
37. Quintarelli G, Scott JE, Dellovo MC. The chemical and histochemi-cal properties of Alcian Blue. II. Dye binding of tissue polyanions. Histochemie 1964;4:86-98.
38. Barkho BZ, Munoz AE, Li X, et al. Endogenous matrix metallo-proteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemo-kines. Stem Cells 2008;26:3139-49.
39. Sablowski R. Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol 2004;14:605-11. (Pubitemid 39440609)
40. Ohlstein B, Kai T, Decotto E, et al. The stem cell niche: theme and variations. Curr Opin Cell Biol 2004;16:693-9. (Pubitemid 39463122)
41. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-7. (Pubitemid 350014593)
42. Mitsiadis TA, Barrandon O, Rochat A, et al. Stem cell niches in mammals. Exp Cell Res 2007;313:3377-85. (Pubitemid 47404556)
43. Fathke C, Wilson L, Shah K, et al. Wnt signaling induces epithelial differentiation during cutaneous wound healing. BMC Cell Biol 2006; 7:1471-2121
44. Leong KG, Niessen K, Kulic I, et al. Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J Exp Med 2007;204:2935-48. (Pubitemid 350179562)
45. Koelling S, Kruegel J, Irmer M, et al. Migratory chondrogenic pro-genitor cells from repair tissue during the later stages of human osteoarthritis. Cell Stem Cell 2009;4:324-35.
46. Kim KW, Ha KY, Park JB, et al. Expressions of membrane-type I matrix metalloproteinase, Ki-67 protein, and type II collagen by chondrocytes migrating from cartilage endplate into nucleus pulpo-sus in rat intervertebral discs: a cartilage endplate-fracture model using an intervertebral disc organ culture. Spine (Phila Pa 1976) 2005;30:1373-8.
47. Le Maitre CL, Freemont AJ, Hoyland JA. Expression of cartilage-derived morphogenetic protein in human intervertebral discs and its effect on matrix synthesis in degenerate human nucleus pulposus cells. Arthritis Res Ther 2009;11:R137.
48. Gruber HE, Norton HJ, Ingram JA, et al. The SOX9 transcription factor in the human disc: decreased immunolocalization with age and disc degeneration. Spine (Phila Pa 1976) 2005;30:625-30. (Pubitemid 40388644)
49. Wei A, Williams LA, Bhargav D, et al. BMP13 prevents the effects of annular injury in an ovine model. Int J Biol Sci 2009;5:388-96.
50. Chujo T, An HS, Akeda K, et al. Effects of growth differentiation factor-5 on the intervertebral disc-in vitro bovine study and in vivo rabbit disc degeneration model study. Spine (Phila Pa 1976) 2006;31:2909-17. (Pubitemid 44885707)
51. Walsh AJ, Bradford DS, Lotz JC. In vivo growth factor treat-ment of degenerated intervertebral discs. Spine (Phila pa 1976) 2004;29:156-63. (Pubitemid 38112496)
52. Daans M, Lories RJ, Luyten FP. Dynamic activation of bone mor-phogenetic protein signaling in collagen-induced arthritis supports their role in joint homeostasis and disease. Arthritis Res Ther 2008;10:R115.