Painful, degenerating intervertebral discs up-regulate neurite sprouting and CGRP through nociceptive factors

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 6, 2014, Pages 1213-1225

  Krock, Emerson ^a   Rosenzweig, Derek H ^a   Chabot Doré, Anne Julie ^a,b   Jarzem, Peter ^a   Weber, Michael H ^a   Ouellet, Jean A ^a,b   Stone, Laura S ^a,b,c   Haglund, Lisbet ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

CGRP; Discogenic pain; Human; Inflammatory cytokines; Intervertebral disc degeneration; Nerve growth factor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE RELATED PEPTIDE; CULTURE MEDIUM; INTERLEUKIN 1BETA; MESSENGER RNA; NERVE GROWTH FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL; APOPTOSIS; CASE CONTROL STUDY; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; COMPLICATION; CULTURE MEDIUM; FEMALE; GENETICS; HUMAN; INTERVERTEBRAL DISK DEGENERATION; LOW BACK PAIN; MALE; METABOLISM; MIDDLE AGED; MOUSE; NERVE CELL; NEURITE; NOCICEPTION; PATHOLOGY; PATHOPHYSIOLOGY; PC12 CELL LINE; PHARMACOLOGY; PHYSIOLOGY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; YOUNG ADULT;

ADULT; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE-RELATED PEPTIDE; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; FEMALE; HUMANS; INTERLEUKIN-1BETA; INTERVERTEBRAL DISC DEGENERATION; LOW BACK PAIN; MALE; MICE; MIDDLE AGED; NERVE GROWTH FACTORS; NEURITES; NEURONS; NOCICEPTION; PC12 CELLS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84904725931     PISSN: 15821838     EISSN: 15824934     Source Type: Journal    
DOI: 10.1111/jcmm.12268     Document Type: Article

References (57)

1. Manchikanti L, Singh V, Datta S, et al. Comprehensive review of epidemiology, scope, and impact of spinal pain. Pain Physician. 2009; 12: E35-170.
2. Roughley PJ. Biology of intervertebral disc aging and degeneration - Involvement of the extracellular matrix. Spine. 2004; 29: 2691-9.
3. Freemont A, Peacock T, Goupille P, et al. Nerve ingrowth into diseased intervertebral disc in chronic back pain. Lancet. 1997; 350: 178-81.
4. Johnson WE, Caterson B, Eisenstein SM, et al. Human intervertebral disc aggrecan inhibits nerve growth in vitro. Arthritis Rheum. 2002; 46: 2658-64.
5. Aoki Y, Ohtori S, Takahashi K, et al. Innervation of the lumbar intervertebral disc by nerve growth factor-dependent neurons related to inflammatory pain. Spine. 2004; 29: 1077-81.
6. Miyagi M, Ishikawa T, Orita S, et al. Disk injury in rats produces persistent increases in pain-related neuropeptides in dorsal root ganglia and spinal cord glia but only transient increases in inflammatory mediators: pathomechanism of chronic diskogenic low back pain. Spine. 2011; 36: 2260-6.
7. Miyagi M, Ishikawa T, Kamoda H, et al. ISSLS prize winner: disc dynamic compression in rats produces long-lasting increases in inflammatory mediators in discs and induces long-lasting nerve injury and regeneration of the afferent fibers innervating discs: a pathomechanism for chronic discogenic low back pain. Spine. 2012; 37: 1810-8.
8. Freemont AJ, Watkins A, Le Maitre C, et al. Nerve growth factor expression and innervation of the painful intervertebral disc. J Pathol. 2002; 197: 286-92.
9. Ozawa T, Ohtori S, Inoue G, et al. The degenerated lumbar intervertebral disc is innervated primarily by peptide-containing sensory nerve fibers in humans. Spine. 2006; 31: 2418-22.
10. Pezet S, McMahon SB. NEUROTROPHINS: mediators and modulators of pain. Annu Rev Neurosci. 2006; 29: 507-38.
11. White FA, Bhangoo SK, Miller RJ. Chemokines: integrators of pain and inflammation. Nat Rev Drug Discovery. 2005; 4: 834-44.
12. Wuertz K, Haglund L. Inflammatory mediators in intervertebral disk degeneration and discogenic pain. Global Spine J. 2013; 3: 1-10.
13. Freemont TJ, LeMaitre C, Watkins A, et al. Degeneration of intervertebral discs: current understanding of cellular and molecular events, and implications for novel therapies. Expert Rev Mol Med. 2001; 3: 1-10.
14. Purmessur D, Freemont AJ, Hoyland JA. Expression and regulation of neurotrophins in the nondegenerate and degenerate human intervertebral disc. Arthritis Res Ther. 2008; 10: R99.
15. Le Maitre CL, Freemont AJ, Hoyland JA. The role of interleukin-1 in the pathogenesis of human intervertebral disc degeneration. Arthritis Res Ther. 2005; 7: R732-45.
16. Richardson SM, Purmessur D, Baird P, et al. Degenerate human nucleus pulposus cells promote neurite outgrowth in neural cells. PLoS ONE. 2012; 7: e47735.
17. Gawri R, Mwale F, Ouellet J, et al. Development of an organ culture system for long-term survival of the intact human intervertebral disc. Spine. 2011; 36: 1835-42.
18. Jim B, Steffen T, Moir J, et al. Development of an intact intervertebral disc organ culture system in which degeneration can be induced as a prelude to studying repair potential. Eur Spine J. 2011; 20: 1244-54.
19. Malin S, Davis B, Molliver D. Production of dissociated sensory neuron cultures and considerations for their use in studying neuronal function and plasticity. Nat Protoc. 2007; 2: 152-60.
20. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA. 1976; 73: 2424-8.
21. Vaudry D, Chen YUN, Hsu C-M, et al. PC12 cells as a model to study the neurotrophic activities of PACAP. Ann NY Acad Sci. 2002; 971: 491-6.
22. Westerink RHS, Ewing AG. The PC12 cell as model for neurosecretion. Acta Physiol. 2008; 192: 273-85.
23. Calabrese EJ. Enhancing and regulating neurite outgrowth. Crit Rev Toxicol. 2008; 38: 391-418.
24. Rosenzweig DH, Ou SJ, Quinn TM. P38 mitogen-activated protein kinase promotes dedifferentiation of primary articular chondrocytes in monolayer culture. J Cell Mol Med. 2013; 17: 508-17.
25. Chung J, Kubota H, Ozaki Y-I, et al. Timing-dependent actions of NGF required for cell differentiation. PLoS ONE. 2010; 5: e9011.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25: 402-8.
27. Yamauchi K, Inoue G, Koshi T, et al. Nerve growth factor of cultured medium extracted from human degenerative nucleus pulposus promotes sensory nerve growth and induces substance P in vitro. Spine. 2009; 34: 2263-9.
28. Moon HJ, Kim JH, Lee HS, et al. Annulus fibrosus cells interact with neuron-like cells to modulate production of growth factors and cytokines in symptomatic disc degeneration. Spine. 2012; 37: 2-9.
29. Navone SE, Marfia G, Canzi L, et al. Expression of neural and neurotrophic markers in nucleus pulposus cells isolated from degenerated intervertebral disc. J Orthop Res. 2012; 30: 1470-7.
30. Qin X, Wan Y, Wang X. CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J Neurosci Res. 2005; 82: 51-62.
31. Wang J-G, Strong J, Xie W, et al. The chemokine CXCL1/growth related oncogene increases sodium currents and neuronal excitability in small diameter sensory neurons. Mol Pain. 2008; 4: 38.
32. Yang R-H, Strong J, Zhang J-M. NF-kappaB mediated enhancement of potassium currents by the chemokine CXCL1/growth related oncogene in small diameter rat sensory neurons. Mol Pain. 2009; 5: 26.
33. Robertson B, Xu X-J, Hao J-X, et al. Interferon receptors in nociceptive pathways: role in neuropathic pain-related behaviour. NeuroReport. 1997; 8: 1311-6.
34. Vikman KS, Hill RH, Backström E, et al. Interferon-γ induces characteristics of central sensitization in spinal dorsal horn neurons in vitro. Pain. 2003; 106: 241-51.
35. Orita S, Ishikawa T, Miyagi M, et al. Pain-related sensory innervation in monoiodoacetate-induced osteoarthritis in rat knees that gradually develops neuronal injury in addition to inflammatory pain. BMC Musculoskelet Disord. 2011; 12: 134.
36. Vazquez E, Kahlenbach J, Segond von Banchet G, et al. Spinal interleukin-6 is an amplifier of arthritic pain in the rat. Arthritis Rheum. 2012; 64: 2233-42.
37. Jung H, Toth PT, White FA, et al. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem. 2008; 104: 254-63.
38. Gruber HE, Hoelscher GL, Bethea S, et al. Interleukin 1-beta upregulates brain-derived neurotrophic factor, neurotrophin 3 and neuropilin 2 gene expression and NGF production in annulus cells. Biotech Histochem. 2012; 87: 506-11.
39. Abe Y, Akeda K, An HS, et al. Proinflammatory cytokines stimulate the expression of nerve growth factor by human intervertebral disc cells. Spine. 2007; 32: 635-42.
40. Hayashi S, Taira A, Inoue G, et al. TNF-alpha in nucleus pulposus induces sensory nerve growth - A study of the mechanism of discogenic low back pain using TNF-alpha-deficient mice. Spine. 2008; 33: 1542-6.
41. Benarroch EE. CGRP: sensory neuropeptide with multiple neurologic implications. Neurology. 2011; 77: 281-7.
42. Aoki Y, Ohtori S, Ino H, et al. Disc inflammation potentially promotes axonal regeneration of dorsal root ganglion neurons innervating lumbar intervertebral disc in rats. Spine. 2004; 29: 2621-6.
43. Orita S, Ohtori S, Nagata M, et al. Inhibiting nerve growth factor or its receptors downregulates calcitonin gene-related peptide expression in rat lumbar dorsal root ganglia innervating injured intervertebral discs. J Orthop Res. 2010; 28: 1614-20.
44. Obreja O, Schmelz M, Poole S, et al. Interleukin-6 in combination with its soluble IL-6 receptor sensitises rat skin nociceptors to heat, in vivo. Pain. 2002; 96: 57-62.
45. Cata JP, Weng HR, Dougherty PM. Spinal injection of IL-2 or IL-15 alters mechanical and thermal withdrawal thresholds in rats. Neurosci Lett. 2008; 437: 45-9.
46. Imai S, Ikegami D, Yamashita A, et al. Epigenetic transcriptional activation of monocyte chemotactic protein 3 contributes to long-lasting neuropathic pain. Brain. 2013; 136: 828-43.
47. Endo H, Akahoshi T, Nishimura A, et al. Experimental arthritis induced by continuous infusion of IL-8 into rabbit knee joints. Clin Exp Immunol. 1994; 96: 31-5.
48. Liou J-T, Liu F-C, Mao C-C, et al. Inflammation confers dual effects on nociceptive processing in chronic neuropathic pain model. Anesthesiology. 2011; 114: 660-72.
49. Zhu Y, Colak T, Shenoy M, et al. Transforming growth factor beta induces sensory neuronal hyperexcitability, and contributes to pancreatic pain and hyperalgesia in rats with chronic pancreatitis. Mol Pain. 2012; 8: 65.
50. Bali KK, Venkataramani V, Satagopam VP, et al. Transcriptional mechanisms underlying sensitization of peripheral sensory neurons by Granulocyte-/Granulocyte-macrophage colony stimulating factors. Mol Pain. 2013; 9: 48.
51. Holm S, Mackiewicz Z, Holm AK, et al. Pro-inflammatory, pleiotropic, and anti-inflammatory TNF-alpha, IL-6, and IL-10 in experimental porcine intervertebral disk degeneration. Vet Pathol. 2009; 46: 1292-300.
52. Gruber HE, Hoelscher GL, Hanley EN. Annulus cells from more degenerated human discs show modified gene expression in 3D culture compared with expression in cells from healthier discs. Spine J. 2010; 10: 721-7.
53. Kepler C, Markova D, Dibra F, et al. The expression and relationship of pro-inflammatory chemokine RANTES/CCL5 and cytokine IL-1β in painful human intervertebral discs. Spine. 2013; 38: 873-80.
54. Kawaguchi S, Yamashita T, Katahira G-I, et al. Chemokine profile of herniated intervertebral discs infiltrated with monocytes and macrophages. Spine. 2002; 27: 1511-6.
55. Kivitz AJ, Gimbel JS, Bramson C, et al. Efficacy and safety of tanezumab versus naproxen in the treatment of chronic low back pain. Pain. 2013; 154: 1009-21.
56. Seidel MF, Wise BL, Lane NE. Nerve growth factor: an update on the science and therapy. Osteoarthritis Cartilage. 2013; 21: 1223-8.
57. Seidel M, Lane N. Control of arthritis pain with anti-nerve-growth factor: risk and benefit. Curr Rheumatol Rep. 2012; 14: 583-8.