Altered spinal MicroRNA-146a and the microRNA-183 cluster contribute to osteoarthritic pain in knee joints

Journal of Bone and Mineral Research

Volumn 28, Issue 12, 2013, Pages 2512-2522

  Li, Xin ^a   Kroin, Jeffrey S ^a   Kc, Ranjan ^a   Gibson, Gary ^b   Chen, Di ^a   Corbett, Grant T ^a   Pahan, Kalipada ^a   Fayyaz, Sana ^a   Kim, Jae Sung ^a   Van Wijnen, Andre J ^d   Suh, Joon ^a   Kim, Su Gwan ^c   Im, Hee Jeong ^a,e  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c Chosun University   (South Korea)

^d MAYO CLINIC   (United States)

^e University of Illinois at Chicago   (United States)

Author keywords

knee joint pain; microglial cells; micrornas; osteoarthritis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MICRORNA; MICRORNA 146A; MICRORNA 183; NERVE GROWTH FACTOR; NEUROPEPTIDE Y; SODIUM CHANNEL NAV1.3; SODIUM CHANNEL NAV1.7; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CENTRAL NERVOUS SYSTEM; CHRONIC PAIN; CONTROLLED STUDY; DOWN REGULATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GLIA CELL; HISTOLOGY; HYPERALGESIA; KNEE MENISCUS; KNEE OSTEOARTHRITIS; KNEE PAIN; LOSS OF FUNCTION MUTATION; MALE; NOCICEPTION; NONHUMAN; RAT; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL GANGLION; UPREGULATION;

KNEE JOINT PAIN; MICROGLIAL CELLS; MICRORNAS; OSTEOARTHRITIS;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HYPERALGESIA; INFLAMMATION; INFLAMMATION MEDIATORS; KNEE JOINT; MALE; MICE; MICRORNAS; OSTEOARTHRITIS; PAIN; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SPINAL CORD;

EID: 84888050795     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2002     Document Type: Article

References (50)

1. Sprangers MA, de Regt EB, Andries F, van Agt HM, Bijl RV, de Boer JB, Foets M, Hoeymans N, Jacobs AE, Kempen GI, Miedema HS, Tijhuis MA, de Haes HC., Which chronic conditions are associated with better or poorer quality of life?. J Clin Epidemiol. 2000; 53 (9): 895-907.
2. Ferreira-Gomes J, Adaes S, Castro-Lopes JM., Assessment of movement-evoked pain in osteoarthritis by the knee-bend and CatWalk tests: a clinically relevant study. J Pain. 2008; 9 (10): 945-54.
3. Busch M, Zernecke A., microRNAs in the regulation of dendritic cell functions in inflammation and atherosclerosis. J Mol Med (Berl). 2012; 90 (8): 877-85.
4. Bartel DP., MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136 (2): 215-33.
5. Taganov KD, Boldin MP, Chang KJ, Baltimore D., NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA. 2006; 103 (33): 12481-6.
6. Taganov KD, Boldin MP, Baltimore D., MicroRNAs and immunity: tiny players in a big field. Immunity. 2007; 26 (2): 133-7.
7. Tsai CY, Allie SR, Zhang W, Usherwood EJ., MicroRNA miR-155 affects antiviral effector and effector Memory CD8 T cell differentiation. J Virol. 2013; 87 (4): 2348-51.
8. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, Fabbri M, Alder H, Liu CG, Calin GA, Croce CM., Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol. 2007; 179 (8): 5082-9.
9. Murphy AJ, Guyre PM, Pioli PA., Estradiol suppresses NF-kappa B activation through coordinated regulation of let-7a and miR-125b in primary human macrophages. J Immunol. 184 (9): 5029-37.
10. Williams AE, Perry MM, Moschos SA, Larner-Svensson HM, Lindsay MA., Role of miRNA-146a in the regulation of the innate immune response and cancer. Biochem Soc Trans. 2008; 36 (Pt 6): 1211-5.
11. Chiyomaru T, Enokida H, Tatarano S, Kawahara K, Uchida Y, Nishiyama K, Fujimura L, Kikkawa N, Seki N, Nakagawa M., miR-145 and miR-133a function as tumour suppressors and directly regulate FSCN1 expression in bladder cancer. Br J Cancer. 2010; 102 (5): 883-91.
12. Li X, Gibson G, Kim JS, Kroin J, Xu S, van Wijnen AJ, Im HJ., MicroRNA-146a is linked to pain-related pathophysiology of osteoarthritis. Gene. 2011; 480 (1-2): 34-41.
13. Gwak YS, Hulsebosch CE., Remote astrocytic and microglial activation modulates neuronal hyperexcitability and below-level neuropathic pain after spinal injury in rat. Neuroscience. 2009; 161 (3): 895-03.
14. Griffin RS, Costigan M, Brenner GJ, Ma CH, Scholz J, Moss A, Allchorne AJ, Stahl GL, Woolf CJ., Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity. J Neurosci. 2007; 27 (32): 8699-708.
15. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, Przewlocki R, Przewlocka B., Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol. 2009; 623 (1-3): 65-72.
16. Ji RR, Suter MR., p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain. 2007; 3: 33.
17. Temburni MK, Jacob MH., New functions for glia in the brain. Proc Natl Acad Sci USA. 2001; 98 (7): 3631-32.
18. Constandil L, Hernandez A, Pelissier T, Arriagada O, Espinoza K, Burgos H, Laurido C., Effect of interleukin-1beta on spinal cord nociceptive transmission of normal and monoarthritic rats after disruption of glial function. Arthritis Res Ther. 2009; 11 (4): R105.
19. Aldrich BT, Frakes EP, Kasuya J, Hammond DL, Kitamoto T., Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience. 2009; 164 (2): 711-23.
20. Glasson SS, Blanchet TJ, Morris EA., The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage. 2007; 15 (9): 1061-9.
21. Im HJ, Kim JS, Li X, Kotwal N, Sumner DR, van Wijnen AJ, Davis FJ, Yan D, Levine B, Henry JL, Desevre J, Kroin JS., Alteration of sensory neurons and spinal response to an experimental osteoarthritis pain model. Arthritis Rheum. 2010; 62 (10): 2995-3005.
22. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL., Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994; 53 (1): 55-63.
23. van der Sluijs JA, Geesink RG, van der Linden AJ, Bulstra SK, Kuyer R, Drukker J., The reliability of the Mankin score for osteoarthritis. J Orthop Res. 1992; 10 (1): 58-61.
24. Livak KJ, Schmittgen TD., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25 (4): 402-8.
25. Im HJ, Muddasani P, Natarajan V, Schmid TM, Block JA, Davis F, van Wijnen AJ, Loeser RF., Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cdelta pathways in human adult articular chondrocytes. J Biol Chem. 2007; 282 (15): 11110-21.
26. Brahmachari S, Pahan K., Sodium benzoate, a food additive and a metabolite of cinnamon, modifies T cells at multiple steps and inhibits adoptive transfer of experimental allergic encephalomyelitis. J Immunol. 2007; 179 (1): 275-83.
27. Corbett GT, Roy A, Pahan K., Sodium phenylbutyrate enhances astrocytic neurotrophin synthesis via protein kinase C (PKC)-mediated activation of cAMP-response element-binding protein (CREB): implications for Alzheimer disease therapy. J Biol Chem. 2013; 288 (12): 8299-312.
28. Giulian D, Baker TJ., Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci. 1986; 6 (8): 2163-78.
29. Bai G, Ambalavanar R, Wei D, Dessem D., Downregulation of selective microRNAs in trigeminal ganglion neurons following inflammatory muscle pain. Mol Pain. 2007; 3: 15.
30. Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, Yasunaga Y, Asahara H, Ochi M., Expression of MicroRNA-146a in osteoarthritis cartilage. Arthritis Rheum. 2009; 60 (4): 1035-41.
31. Obata K, Noguchi K., BDNF in sensory neurons and chronic pain. Neurosci Res. 2006; 55 (1): 1-10.
32. Tucker K, Fadool DA., Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J Physiol. 2002; 542 (Pt 2): 413-29.
33. Chen Z, Jalabi W, Shpargel KB, Farabaugh KT, Dutta R, Yin X, Kidd GJ, Bergmann CC, Stohlman SA, Trapp BD., Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. J Neurosci. 2012; 32 (34): 11706-15.
34. Thulasingam S, Massilamany C, Gangaplara A, Dai H, Yarbaeva S, Subramaniam S, Riethoven JJ, Eudy J, Lou M, Reddy J., miR-27b*, an oxidative stress-responsive microRNA modulates nuclear factor-kB pathway in RAW 264.7 cells. Mol Cell Biochem. 2011; 352 (1-2): 181-8.
35. Miyaki S, Sato T, Inoue A, Otsuki S, Ito Y, Yokoyama S, Kato Y, Takemoto F, Nakasa T, Yamashita S, Takada S, Lotz MK, Ueno-Kudo H, Asahara H., MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev. 2012; 24 (11): 1173-85.
36. Bocchini V, Mazzolla R, Barluzzi R, Blasi E, Sick P, Kettenmann H., An immortalized cell line expresses properties of activated microglial cells. J Neurosci Res. 1992; 31 (4): 616-21.
37. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J, Benz CC., Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene. 2008; 27 (42): 5643-7.
38. Kappelmann M, Kuphal S, Meister G, Vardimon L, Bosserhoff AK., MicroRNA miR-125b controls melanoma progression by direct regulation of c-Jun protein expression. Oncogene. 2012 Jul 16 [Epub ahead of print].
39. Wang DJ, Legesse-Miller A, Johnson EL, Coller HA., Regulation of the let-7a-3 promoter by NF-kappaB. PLoS One. 2012; 7 (2): e31240.
40. Sheedy FJ, O'Neill LA., Adding fuel to fire: microRNAs as a new class of mediators of inflammation. Ann Rheum Dis. 2008; 67 (Suppl 3): iii50-5.
41. Jin ZB, Hirokawa G, Gui L, Takahashi R, Osakada F, Hiura Y, Takahashi M, Yasuhara O, Iwai N., Targeted deletion of miR-182, an abundant retinal microRNA. Mol Vis. 2009; 15: 523-33.
42. Chatzikyriakidou A, Voulgari PV, Georgiou I, Drosos AA., A polymorphism in the 3'-UTR of interleukin-1 receptor-associated kinase (IRAK1), a target gene of miR-146a, is associated with rheumatoid arthritis susceptibility. Joint Bone Spine. 2010; 77 (5): 411-3.
43. Chatzikyriakidou A, Voulgari PV, Georgiou I, Drosos AA., The role of microRNA-146a (miR-146a) and its target IL-1R-associated kinase (IRAK1) in psoriatic arthritis susceptibility. Scand J Immunol. 2010; 71 (5): 382-5.
44. Chen Y, Willcockson HH, Valtschanoff JG., Influence of the vanilloid receptor TRPV1 on the activation of spinal cord glia in mouse models of pain. Exp Neurol. 2009; 220 (2): 383-90.
45. Xu S, Witmer PD, Lumayag S, Kovacs B, Valle D., MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J Biol Chem. 2007; 282 (34): 25053-66.
46. Alloui A, Zimmermann K, Mamet J, Duprat F, Noel J, Chemin J, Guy N, Blondeau N, Voilley N, Rubat-Coudert C, Borsotto M, Romey G, Heurteaux C, Reeh P, Eschalier A, Lazdunski M., TREK-1, K+ channel involved in polymodal pain perception. EMBO.J. 2006; 25 (11): 2368-76.
47. Azevedo FA, Carvalho LR, Grinberg LT, Farfel JM, Ferretti RE, Leite RE, Jacob Filho W, Lent R, Herculano-Houzel S., Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol. 2009; 513 (5): 532-41.
48. Levin ME, Jin JG, Ji RR, Tong J, Pomonis JD, Lavery DJ, Miller SW, Chiang LW., Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain. Pain. 2008; 137 (1): 182-201.
49. McMahon SB, Malcangio M., Current challenges in glia-pain biology. Neuron. 2009; 64 (1): 46-54.
50. Gomez-Nicola D, Valle-Argos B, Suardiaz M, Taylor JS, Nieto-Sampedro M., Role of IL-15 in spinal cord and sciatic nerve after chronic constriction injury: regulation of macrophage and T-cell infiltration. J Neurochem. 2008; 107 (6): 1741-52.