Association of the α 2δ 1 subunit with Ca v3.2 enhances membrane expression and regulates mechanically induced ATP release in MLO-Y4 osteocytes

Journal of Bone and Mineral Research

Volumn 26, Issue 9, 2011, Pages 2125-2139

  Thompson, William R ^a   Majid, Amber S ^a   Czymmek, Kirk J ^a   Ruff, Albert L ^b   García, Jesús ^c   Duncan, Randall L ^a   Farach Carson, Mary C ^a,d  

^a UNIVERSITY OF DELAWARE   (United States)

^b US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d RICE UNIVERSITY   (United States)

Author keywords

ATP RELEASE; EXTRACELLULAR MATRIX; MECHANOSENSING; OSTEOCYTE; VOLTAGE SENSITIVE CALCIUM CHANNEL

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN SUBUNIT; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL 1.2 ALPHA1C; VOLTAGE GATED CALCIUM CHANNEL 3.2 ALPHA1H; VOLTAGE GATED CALCIUM CHANNEL 3.2 ALPHA2DELTA1; VOLTAGE GATED CALCIUM CHANNEL 3.2 BETA1; VOLTAGE GATED CALCIUM CHANNEL 3.2 BETA2; VOLTAGE GATED CALCIUM CHANNEL 3.2 GAMMA7;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCYTE; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM CHANNELS; CALCIUM CHANNELS, T-TYPE; CELL LINE; CELL MEMBRANE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MICE; MICE, INBRED C57BL; OSTEOCYTES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; RNA, MESSENGER;

EID: 80052006781     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.437     Document Type: Article

References (54)

1. Duncan RL, Turner CH,. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int. 1995; 57: 344-358.
2. Parfitt AM,. The cellular basis of bone turnover and bone loss: a rebuttal of the osteocytic resorption-bone flow theory. Clin Orthop Relat Res. 1977; 127: 236-247. (Pubitemid 8192287)
3. Tatsumi S, Ishii K, Amizuka N, et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 2007; 5: 464-475. (Pubitemid 46825494)
4. Piekarski K, Munro M,. Transport mechanism operating between blood supply and osteocytes in long bones. Nature. 1977; 269: 80-82. (Pubitemid 8160686)
5. Price C, Zhou X, Li W, Wang L,. Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J Bone Miner Res. 2011; 26: 277-285.
6. Miyauchi A, Notoya K, Mikuni-Takagaki Y, et al. Parathyroid hormone-activated volume-sensitive calcium influx pathways in mechanically loaded osteocytes. J Biol Chem. 2000; 275: 3335-3342. (Pubitemid 30083036)
7. Miyauchi A, Gotoh M, Kamioka H, et al. AlphaVbeta3 integrin ligands enhance volume-sensitive calcium influx in mechanically stretched osteocytes. J Bone Miner Metab. 2006; 24: 498-504. (Pubitemid 44663423)
8. Hung CT, Pollack SR, Reilly TM, Brighton CT,. Real-time calcium response of cultured bone cells to fluid flow. Clin Orthop Relat Res. 1995; 313: 256-269.
9. Duncan RL, Kizer N, Barry EL, Friedman PA, Hruska KA,. Antisense oligodeoxynucleotide inhibition of a swelling-activated cation channel in osteoblast-like osteosarcoma cells. Proc Natl Acad Sci U S A. 1996; 93: 1864-1869. (Pubitemid 26079845)
10. Kizer N, Harter L, Hruska K, Alvarez U, Duncan R,. Volume regulatory decrease in UMR-106.01cells is mediated by specific alpha1 subunits of L-type calcium channels. Cell Biochem Biophys. 1999; 31: 65-79. (Pubitemid 129555676)
11. Vadiakas GP, Banes AJ,. Verapamil decreases cyclic load-induced calcium incorporation in ROS 17/2.8 osteosarcoma cell cultures. Matrix. 1992; 12: 439-447. (Pubitemid 23024779)
12. Ryder KD, Duncan RL,. Parathyroid hormone enhances fluid shear-induced [Ca2+]i signaling in osteoblastic cells through activation of mechanosensitive and voltage-sensitive Ca2+ channels. J Bone Miner Res. 2001; 16: 240-248. (Pubitemid 32105405)
13. Genetos DC, Geist DJ, Liu D, Donahue HJ, Duncan RL,. Fluid shear-induced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J Bone Miner Res. 2005; 20: 41-49. (Pubitemid 41716217)
14. Rawlinson SC, Pitsillides AA, Lanyon LE,. Involvement of different ion channels in osteoblasts' and osteocytes' early responses to mechanical strain. Bone. 1996; 19: 609-614. (Pubitemid 27035840)
15. Liu D, Genetos DC, Shao Y, et al. Activation of extracellular-signal regulated kinase (ERK1/2) by fluid shear is Ca(2+)- and ATP-dependent in MC3T3-E1 osteoblasts. Bone. 2008; 42: 644-652.
16. Li J, Duncan RL, Burr DB, Turner CH,. L-type calcium channels mediate mechanically induced bone formation in vivo. J Bone Miner Res. 2002; 17: 1795-1800.
17. Li J, Duncan RL, Burr DB, Gattone VH, Turner CH,. Parathyroid hormone enhances mechanically induced bone formation, possibly involving L-type voltage-sensitive calcium channels. Endocrinology. 2003; 144: 1226-1233. (Pubitemid 36428463)
18. Meszaros JG, Karin NJ, Farach-Carson MC,. Voltage-sensitive calcium channels in osteoblasts: mediators of plasma membrane signalling events. Connect Tissue Res. 1996; 35: 107-111. (Pubitemid 27118842)
19. Liu R, Li W, Karin NJ, Bergh JJ, Adler-Storthz K, Farach-Carson MC,. Ribozyme ablation demonstrates that the cardiac subtype of the voltage-sensitive calcium channel is the molecular transducer of 1, 25-dihydroxyvitamin D(3)-stimulated calcium influx in osteoblastic cells. J Biol Chem. 2000; 275: 8711-8718. (Pubitemid 30180223)
20. Bergh JJ, Shao Y, Akanbi K, Farach-Carson MC,. Rodent osteoblastic cells express voltage-sensitive calcium channels lacking a gamma subunit. Calcif Tissue Int. 2003; 73: 502-510. (Pubitemid 37474158)
21. Shao Y, Alicknavitch M, Farach-Carson MC,. Expression of voltage sensitive calcium channel (VSCC) L-type Cav1.2 (alpha1C) and T-type Cav3.2 (alpha1H) subunits during mouse bone development. Dev Dyn. 2005; 234: 54-62. (Pubitemid 41192750)
22. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J,. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev. 2005; 57: 411-425. (Pubitemid 43036432)
23. Pragnell M, De Waard M, Mori Y, Tanabe T, Snutch TP, Campbell KP,. Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit. Nature. 1994; 368: 67-70.
24. De Waard M, Pragnell M, Campbell KP,. Ca2+ channel regulation by a conserved beta subunit domain. Neuron. 1994; 13: 495-503.
25. Bichet D, Cornet V, Geib S, et al. The I-II loop of the Ca2+ channel alpha1 subunit contains an endoplasmic reticulum retention signal antagonized by the beta subunit. Neuron. 2000; 25: 177-190. (Pubitemid 30316520)
26. Shao Y, Czymmek KJ, Jones PA, et al. Dynamic interactions between L-type voltage-sensitive calcium channel Cav1.2 subunits and ahnak in osteoblastic cells. Am J Physiol Cell Physiol. 2009; 296: C1067-1078.
27. Perez-Reyes E, Lory P,. Molecular biology of T-type calcium channels. CNS Neurol Disord Drug Targets. 2006; 5: 605-609. (Pubitemid 44890572)
28. Dolphin AC, Wyatt CN, Richards J, et al. The effect of alpha2-delta and other accessory subunits on expression and properties of the calcium channel alpha1G. J Physiol. 1999; 519 (Pt 1): 35-45. (Pubitemid 29417801)
29. Jay SD, Sharp AH, Kahl SD, Vedvick TS, Harpold MM, Campbell KP,. Structural characterization of the dihydropyridine-sensitive calcium channel alpha 2-subunit and the associated delta peptides. J Biol Chem. 1991; 266: 3287-3293. (Pubitemid 21909206)
30. De Jongh KS, Warner C, Catterall WA,. Subunits of purified calcium channels. Alpha 2 and delta are encoded by the same gene. J Biol Chem. 1990; 265: 14738-14741.
31. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF,. Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res. 1997; 12: 2014-2023. (Pubitemid 27524478)
32. You LD, Weinbaum S, Cowin SC, Schaffler MB,. Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A Discov Mol Cell Evol Biol. 2004; 278: 505-513. (Pubitemid 38724147)
33. Garcia K, Nabhani T, Garcia J,. The calcium channel alpha2/delta1 subunit is involved in extracellular signalling. J Physiol. 2008; 586: 727-738. (Pubitemid 351194113)
34. Liu H, De Waard M, Scott VE, Gurnett CA, Lennon VA, Campbell KP,. Identification of three subunits of the high affinity omega-conotoxin MVIIC-sensitive Ca2+ channel. J Biol Chem. 1996; 271: 13804-13810.
35. Thompson WR, Modla S, Grindel BJ, et al. Perlecan/Hspg2 deficiency alters the pericellular space of the lacuno-canalicular system surrounding osteocytic processes in cortical bone. J Bone Miner Res.
36. Avila T, Andrade A, Felix R,. Transforming growth factor-beta1 and bone morphogenetic protein-2 downregulate CaV3.1 channel expression in mouse C2C12 myoblasts. J Cell Physiol. 2006; 209: 448-456. (Pubitemid 44484636)
37. Berthier C, Monteil A, Lory P, Strube C,. Alpha(1H) mRNA in single skeletal muscle fibres accounts for T-type calcium current transient expression during fetal development in mice. J Physiol. 2002; 539 (Pt 3): 681-691. (Pubitemid 35175420)
38. Biswas P, Zanello LP,. 1alpha,25(OH)(2) vitamin D(3) induction of ATP secretion in osteoblasts. J Bone Miner Res. 2009; 24: 1450-1460.
39. Gu Y, Preston MR, Magnay J, El Haj AJ, Publicover SJ,. Hormonally-regulated expression of voltage-operated Ca(2+) channels in osteocytic (MLO-Y4) cells. Biochem Biophys Res Commun. 2001; 282: 536-542. (Pubitemid 32917904)
40. Barclay J, Balaguero N, Mione M, et al. Ducky mouse phenotype of epilepsy and ataxia is associated with mutations in the Cacna2d2 gene and decreased calcium channel current in cerebellar Purkinje cells. J Neurosci. 2001; 21: 6095-6104. (Pubitemid 32737743)
41. Anderson EJ, Kaliyamoorthy S, Iwan J, Alexander D, Knothe Tate ML,. Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body and processes. Ann Biomed Eng. 2005; 33: 52-62. (Pubitemid 40509494)
42. Curtis BM, Catterall WA,. Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry. 1984; 23: 2113-2118. (Pubitemid 14110715)
43. Hosey MM, Barhanin J, Schmid A, et al. Photoaffinity labelling and phosphorylation of a 165 kilodalton peptide associated with dihydropyridine and phenylalkylamine-sensitive calcium channels. Biochem Biophys Res Commun. 1987; 147: 1137-1145.
44. Martin-Moutot N, Charvin N, Leveque C, et al. Interaction of SNARE complexes with P/Q-type calcium channels in rat cerebellar synaptosomes. J Biol Chem. 1996; 271: 6567-6570. (Pubitemid 26104078)
45. Sharp AH, Black JL 3rd, Dubel SJ, et al. Biochemical and anatomical evidence for specialized voltage-dependent calcium channel gamma isoform expression in the epileptic and ataxic mouse, stargazer. Neuroscience. 2001; 105: 599-617. (Pubitemid 32769826)
46. Kang MG, Chen CC, Felix R, et al. Biochemical and biophysical evidence for gamma 2 subunit association with neuronal voltage-activated Ca2+ channels. J Biol Chem. 2001; 276: 32917-32924.
47. Wyatt CN, Page KM, Berrow NS, Brice NL, Dolphin AC,. The effect of overexpression of auxiliary Ca2+ channel subunits on native Ca2+ channel currents in undifferentiated mammalian NG108-15cells. J Physiol. 1998; 510 (Pt 2): 347-360. (Pubitemid 28370451)
48. Canti C, Nieto-Rostro M, Foucault I, et al. The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of alpha2delta subunits is key to trafficking voltage-gated Ca2+ channels. Proc Natl Acad Sci U S A. 2005; 102: 11230-11235. (Pubitemid 41153803)
49. Whittaker CA, Hynes RO,. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell. 2002; 13: 3369-3387. (Pubitemid 35191361)
50. Humphries MJ,. Integrin structure. Biochem Soc Trans. 2000; 28: 311-339.
51. Freise D, Held B, Wissenbach U, et al. Absence of the gamma subunit of the skeletal muscle dihydropyridine receptor increases L-type Ca2+ currents and alters channel inactivation properties. J Biol Chem. 2000; 275: 14476-14481. (Pubitemid 30339734)
52. Moss FJ, Viard P, Davies A, et al. The novel product of a five-exon stargazin-related gene abolishes Ca(V)2.2 calcium channel expression. EMBO J. 2002; 21: 1514-1523. (Pubitemid 34614608)
53. Tomita S, Chen L, Kawasaki Y, et al. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol. 2003; 161: 805-816. (Pubitemid 36648763)
54. Ferron L, Davies A, Page KM, et al. The stargazin-related protein gamma 7 interacts with the mRNA-binding protein heterogeneous nuclear ribonucleoprotein A2 and regulates the stability of specific mRNAs, including CaV2.2. J Neurosci. 2008; 28: 10604-10617.