Deletion of Panx3 Prevents the Development of Surgically Induced Osteoarthritis

Journal of Molecular Medicine

Volumn 93, Issue 8, 2015, Pages 845-856

  Moon, Paxton M ^a   Penuela, Silvia ^a   Barr, Kevin ^a   Khan, Sami ^a   Pin, Christopher L ^a,b   Welch, Ian ^c   Attur, Mukundan ^d   Abramson, Steven B ^d   Laird, Dale W ^a   Beier, Frank ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d NYU HOSPITAL FOR JOINT DISEASES   (United States)

Author keywords

Cartilage; DMM; Mice; Osteoarthritis; Pannexin 3

Indexed keywords

PANNEXIN 3; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; COLLAGEN TYPE 2; COLLAGENASE 3; GAP JUNCTION PROTEIN; PANNEXIN 3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE; CONTROLLED STUDY; GENE DELETION; KNEE MENISCUS; KNOCKOUT MOUSE; MOUSE; NONHUMAN; OSTEOARTHRITIS; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; CELL LINE; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY;

ANIMALS; CARTILAGE, ARTICULAR; CELL LINE; COLLAGEN TYPE II; CONNEXINS; FEMALE; GENE DELETION; HUMANS; MALE; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; OSTEOARTHRITIS;

EID: 84937975694     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-015-1311-1     Document Type: Article

References (48)

1. Hunter DJ, Schofield D, Callander E (2014) The individual and socioeconomic impact of osteoarthritis. Nat Rev Rheumatol 10(7):437–441
2. Helmick CG, Felson DT, Lawrence RC, Gabriel S, Hirsch R, Kwoh CK, Liang MH, Kremers HM, Mayes MD, Merkel PA et al (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Arthritis Rheum 58(1):15–25
3. Nuesch E, Dieppe P, Reichenbach S, Williams S, Iff S, Juni P (2011) All cause and disease specific mortality in patients with knee or hip osteoarthritis: population based cohort study. BMJ 342:d1165
4. Lawrence RC, Felson DT, Helmick CG, Arnold LM, Choi H, Deyo RA, Gabriel S, Hirsch R, Hochberg MC, Hunder GG et al (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II Arthritis Rheum 58(1):26–35
5. Hochberg MC, Altman RD, April KT, Benkhalti M, Guyatt G, McGowan J, Towheed T, Welch V, Wells G, Tugwell P et al (2012) American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee. Arthritis Care Res 64(4):465–474
6. Weinstein AM, Rome BN, Reichmann WM, Collins JE, Burbine SA, Thornhill TS, Wright J, Katz JN, Losina E (2013) Estimating the burden of total knee replacement in the United States. J Bone Joint Surg Am 95(5):385–392
7. Loeser RF, Goldring SR, Scanzello CR, Goldring MB (2012) Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 64(6):1697–1707
8. Roach HI, Aigner T, Soder S, Haag J, Welkerling H (2007) Pathobiology of osteoarthritis: pathomechanisms and potential therapeutic targets. Curr Drug Targets 8(2):271–282
9. Aigner T, Sachse A, Gebhard PM, Roach HI (2006) Osteoarthritis: pathobiology-targets and ways for therapeutic intervention. Adv Drug Deliv Rev 58(2):128–149
10. Appleton CT, Pitelka V, Henry J, Beier F (2007) Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum 56(6):1854–1868
11. James CG, Stanton LA, Agoston H, Ulici V, Underhill TM, Beier F (2010) Genome-wide analyses of gene expression during mouse endochondral ossification. PLoS One 5(1), e8693. doi:10.1371/journal.pone.0008693
12. Penuela S, Gehi R, Laird DW (2013) The biochemistry and function of pannexin channels. Biochim Biophys Acta 1828(1):15–22
13. Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S (2000) A ubiquitous family of putative gap junction molecules. Curr Biol 10(13):R473–474
14. Bennett MV, Garre JM, Orellana JA, Bukauskas FF, Nedergaard M, Saez JC (2012) Connexin and pannexin hemichannels in inflammatory responses of glia and neurons. Brain Res 1487:3–15
15. Penuela S, Harland L, Simek J, Laird DW (2014) Pannexin channels and their links to human disease. Biochem J 461(3):371–381
16. Dahl G, Keane RW (2012) Pannexin: from discovery to bedside in 11+/−4 years? Brain Res 1487:150–159
17. Iwamoto T, Nakamura T, Doyle A, Ishikawa M, de Vega S, Fukumoto S, Yamada Y (2010) Pannexin 3 regulates intracellular ATP/cAMP levels and promotes chondrocyte differentiation. J Biol Chem 285(24):18948–18958
18. van der Kraan PM, van den Berg WB (2012) Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration? Osteoarthritis and cartilage / OARS. Osteoarthr Res Soc 20(3):223–232
19. Pitsillides AA, Beier F (2011) Cartilage biology in osteoarthritis–lessons from developmental biology. Nat Rev Rheumatol 7(11):654–663
20. D’Angelo M, Yan Z, Nooreyazdan M, Pacifici M, Sarment DS, Billings PC, Leboy PS (2000) MMP-13 is induced during chondrocyte hypertrophy. J Cell Biochem 77(4):678–693
21. Bond SR, Lau A, Penuela S, Sampaio AV, Underhill TM, Laird DW, Naus CC (2011) Pannexin 3 is a novel target for Runx2, expressed by osteoblasts and mature growth plate chondrocytes. J Bone Miner Resh Off J Am Soc Bone Miner Res 26(12):2911–2922
22. Wang G, Woods A, Agoston H, Ulici V, Glogauer M, Beier F (2007) Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 306(2):612–623
23. Solomon LA, Li JR, Berube NG, Beier F (2009) Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS One 4(9), e7106. doi:10.1371/journal.pone.0007106
24. Gillespie JR, Ulici V, Dupuis H, Higgs A, Dimattia A, Patel S, Woodgett JR, Beier F (2011) Deletion of glycogen synthase kinase-3beta in cartilage results in up-regulation of glycogen synthase kinase-3alpha protein expression. Endocrinology 152(5):1755–1766
25. Pest MA, Russell BA, Zhang YW, Jeong JW, Beier F (2014) Disturbed cartilage and joint homeostasis resulting from a loss of mitogen-inducible gene 6 in a mouse model of joint dysfunction. Arthritis Rheumatol 66(10):2816–2827
26. Penuela S, Bhalla R, Nag K, Laird DW (2009) Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 20(20):4313–4323
27. Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW (2007) Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 120(Pt 21):3772–3783
28. Glasson SS, Blanchet TJ, Morris EA (2007) The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthr Cartil / OARS Osteoarthr Res Soc 15(9):1061–1069
29. Welch ID, Cowan MF, Beier F, Underhill TM (2009) The retinoic acid binding protein CRABP2 is increased in murine models of degenerative joint disease. Arthritis Res Ther 11(1):R14
30. Ratneswaran A, LeBlanc EA, Walser E, Welch I, Mort JS, Borradaile N, Beier F (2015) Peroxisome proliferator-activated receptor delta promotes the progression of posttraumatic osteoarthritis in a mouse model. Arthritis Rheum 67(2):454–464
31. Usmani SE, Pest MA, Kim G, Ohora SN, Qin L, Beier F (2012) Transforming growth factor alpha controls the transition from hypertrophic cartilage to bone during endochondral bone growth. Bone 51(1):131–141
32. Glasson SS, Chambers MG, Van Den Berg WB, Little CB (2010) The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the mouse. Osteoarthr Cartil / OARS Osteoarthr Res Soc 18(Suppl 3):S17–23
33. Schwenk F, Baron U, Rajewsky K (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23(24):5080–5081
34. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS et al (2010) Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467(7317):863–867
35. Billaud M, Sandilos JK, Isakson BE (2012) Pannexin 1 in the regulation of vascular tone. Trends Cardiovasc Med 22(3):68–72
36. Poon IK, Chiu YH, Armstrong AJ, Kinchen JM, Juncadella IJ, Bayliss DA, Ravichandran KS (2014) Unexpected link between an antibiotic, pannexin channels and apoptosis. Nature 507(7492):329–334
37. Le Vasseur M, Lelowski J, Bechberger JF, Sin WC, Naus CC (2014) Pannexin 2 protein expression is not restricted to the CNS. Front Cell Neurosci 8:392
38. van der Kraan PM, van den Berg WB (2007) Osteophytes: relevance and biology. Osteoarthr Cartil 15(3):237–244
39. Garcia M, Knight MM (2010) Cyclic loading opens hemichannels to release ATP as part of a chondrocyte mechanotransduction pathway. J Orthop Res Off Pub Orthop Res Soc 28(4):510–515
40. Graff RD, Lazarowski ER, Banes AJ, Lee GM (2000) ATP release by mechanically loaded porcine chondrons in pellet culture. Arthritis Rheum 43(7):1571–1579
41. Ishikawa M, Iwamoto T, Nakamura T, Doyle A, Fukumoto S, Yamada Y (2011) Pannexin 3 functions as an ER Ca(2+) channel, hemichannel, and gap junction to promote osteoblast differentiation. J Cell Biol 193(7):1257–1274
42. Ogawa H, Kozhemyakina E, Hung HH, Grodzinsky AJ, Lassar AB (2014) Mechanical motion promotes expression of Prg4 in articular cartilage via multiple CREB-dependent, fluid flow shear stress-induced signaling pathways. Genes Dev 28(2):127–139
43. Waldman SD, Usprech J, Flynn LE, Khan AA (2010) Harnessing the purinergic receptor pathway to develop functional engineered cartilage constructs. Osteoarthr Cartil / OARS Osteoarthr Res Soc 18(6):864–872
44. Leong WS, Russell RG, Caswell AM (1994) Stimulation of cartilage resorption by extracellular ATP acting at P2-purinoceptors. Biochim Biophys Acta 1201(2):298–304
45. Papachristou DJ, Pirttiniemi P, Kantomaa T, Papavassiliou AG, Basdra EK (2005) JNK/ERK-AP-1/Runx2 induction “paves the way” to cartilage load-ignited chondroblastic differentiation. Histochem Cell Biol 124(3–4):215–223
46. Costessi A, Pines A, D’Andrea P, Romanello M, Damante G, Cesaratto L, Quadrifoglio F, Moro L, Tell G (2005) Extracellular nucleotides activate Runx2 in the osteoblast-like HOBIT cell line: a possible molecular link between mechanical stress and osteoblasts’ response. Bone 36(3):418–432
47. Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, Mitchell P, Hambor J, Diekmann O, Tschesche H et al (1997) Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 99(7):1534–1545
48. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G (1996) Biochemical characterization of human collagenase-3. J Biol Chem 271(3):1544–1550