Connexin 43 hemichannel regulates H9c2 cell proliferation by modulating intracellular ATP and Ca2+

Acta Biochimica et Biophysica Sinica

Volumn 42, Issue 7, 2010, Pages 472-482

  Song, Dongli ^a   Liu, Xiaoyu ^a   Liu, Rujiao ^a   Yang, Ling ^a   Zuo, Ji ^a   Liu, Wen ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

connexin 43; H9c2 cell; hemichannel; proliferation; Wnt 3a

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; 18ALPHA-GLYCYRRHETINIC ACID; ADENOSINE TRIPHOSPHATE; CALCIUM; CONNEXIN 43; DRUG DERIVATIVE; GLYCYRRHETINIC ACID; WNT PROTEIN; WNT3 PROTEIN;

ANIMAL; ARTICLE; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETICS; HEART MUSCLE CELL; METABOLISM; PHYSIOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CALCIUM; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CONNEXIN 43; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLYCYRRHETINIC ACID; MYOCYTES, CARDIAC; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WNT PROTEINS;

MAMMALIA; RATTUS;

EID: 77954404657     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmq047     Document Type: Article

References (60)

1. Söhl G and Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 2003, 10: 173-180.
2. Essenfelder GM, Bruzzone R, Lamartine J, Charollais A, Blanchet-Bardon C, Barbe MT, Meda P and Waksman G. Connexin 30 mutations responsible for hidrotic ectodermal dysplasia cause abnormal hemichannel activity. Hum Mol Genet 2004, 13: 1703-1714.
3. George CH, Kendall JM and Evans WH. Intracellular trafficking pathways in the assembly of connexins into gap junctions. J Biol Chem 1999, 274: 8678-8685.
4. Sarma JD, Wang F and Koval M. Targeted gap junction protein constructs reveal connexin-specific differences in oligomerization. J Biol Chem 2002, 277: 20911-20918.
5. Ramachandran S, Xie LH, John SA, Subramaniam S and Lal R. A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury. PLoS One 2007, 2: e712.
6. Lauf U, Giepmans BN, Lopez P, Braconnot S, Chen SC and Falk MM. Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA 2002, 99: 10446-10451.
7. King TJ and Bertram JS. Connexins as targets for cancer chemoprevention and chemotherapy. Biochim Biophys Acta 2005, 1719: 146-160
8. Jiang JX and Gu S. Gap junction- and hemichannel-independent actions of connexins. Biochim Biophys Acta 2005, 1711: 208-214
9. Quist AP, Rhee SK, Lin H and Lal R. Physiological role of gap-junctional hemichannels: extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 2000, 148: 1063-1074.
10. Bruzzone S, Guida L, Zocchi E, Franco L and De Flora A. Connexin 43 hemi channels mediate Ca2+ regulated transmembrane NAD+ fluxes in intact cells. FASEB J 2001, 15: 10-12.
11. Franco L, Zocchi E, Usai C, Guida L, Bruzzone S, Costa A and De Flora A. Paracrine roles of NAD+ and cyclic ADP-ribose in increasing intracellular calcium and enhancing cell proliferation of 3T3 fibroblasts. J Biol Chem 2001, 276: 21642-21648.
12. Stout CE, Costantin JL, Naus CC and Charles AC. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 2002, 277: 10482-10488.
13. Davidson JS and Baumgarten IM. Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharmacol Exp Ther 1988, 246: 1104-1107.
14. Contreras JE, Sánchez HA, Eugenin EA, Speidel D, Theis M, Willecke K, Bukauskas FF and Bennett MV, et al. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci USA 2002, 99: 495-500.
15. Chung TH, Wang SM, Chang YC, Chen YL and Wu JC. 18betaglycyrrhetinic acid promotes Src interaction with Connexin 43 in rat cardiomyocytes. J Cell Biochem 2007, 100: 653-664.
16. Meyer RA, Cohen MF, Recalde S, Zakany J, Bell SM, Scott WJ, Jr and Lo CW. Developmental regulation and asymmetric expression of the gene encoding Cx43 gap junctions in the mouse limb bud. Dev Genet 1997, 21: 290-300.
17. Liu X, Liu W, Yang L, Xia B, Li J, Zuo J and Li X. Increased connexin expression improves the migratory and proliferative ability of H9c2 cells by Wnt-3a overexpression. Acta Biochim Biophys Sin 2007, 39: 391-398.
18. Kunapuli SP and Daniel JL. P2 receptor subtypes in the cardiovascular system. Biochem J 1998, 336: 513-523.
19. Sanches G, de Alencar LS and Ventura AL. ATP induces proliferation of retinal cells in culture via activation of PKC and extracellular signalregulated kinase cascade. Int J Dev Neurosci 2002, 20: 21-27.
20. Pearson RA, Dale N, Llaudet E and Mobbs P. ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 2005, 46: 731-744.
21. Koizumi S, Fujishita K and Inoue K. Regulation of cell-to-cell communication mediated by astrocytic ATP in the CNS. Purinergic Signal 2005, 1: 211-217.
22. Dong L, Liu X, Li H, Vertel BM and Ebihara L. Role of the N-terminus in permeability of chicken connexin45.6 gap junctional channels. J Physiol 2006, 576: 787-799.
23. Decrock E, De Vuyst E, Vinken M, Van Moorhem M, Vranckx K, Wang N and Van Laeken L, et al. Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ 2009, 16: 151-163.
24. Boengler K, Konietzka I, Buechert A, Heinen Y, Garcia-Dorado D, Heusch G and Schulz R. Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43. Am J Physiol Heart Circ Physiol 2007, 292: H1764-H1769.
25. Retamal MA, Froger N, Palacios-Prado N, Ezan P, Sáez PJ, Sáez JC and Giaume C. Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J Neurosci 2007, 27: 13781-13792.
26. Riddle RC, Taylor AF, Rogers JR and Donahue HJ. ATP release mediates fluid flow-induced proliferation of human bone marrow stromal cells. J Bone Miner Res 2007, 22: 589-600.
27. Giles WR and Smith GL. Evidence of intercellular coupling between co-cultured adult rabbit ventricular myocytes and myofibroblasts. J Physiol 2007, 583: 225-236.
28. Wang T, Zhang ZX, Xu YJ and Hu QH. 5-Hydroxydecanoate inhibits proliferation of hypoxic human pulmonary artery smooth muscle cells by blocking mitochondrial K (ATP) channels. Acta Pharmacol Sin 2007, 28: 1531-1540.
29. Liang JY, Wang SM, Chung TH, Yang SH and Wu JC. Effects of 18-glycyrrhetinic acid on serine 368 phosphorylation of Connexin 43 in rat neonatal cardiomyocytes. Cell Biol Int 2008, 32: 1371-1379.
30. Zhu CH, Lu FP, He YN, Han ZL and Du LX. Regulation of avilamycin biosynthesis in Streptomyces viridochromogenes: effects of glucose, ammonium ion, and inorganic phosphate. Appl Microbiol Biotechnol 2007, 73: 1031-1038.
31. Formigli L, Francini F, Tani A, Squecco R, Nosi D, Polidori L and Nistri S, et al. Morphofunctional integration between skeletal myoblasts and adult cardiomyocytes in coculture is favored by direct cell-cell contacts and relaxin treatment. Am J Physiol Cell Physiol 2005, 288: C795-804.
32. Kim SE and Choi KY. EGF receptor is involved in WNT3a-mediated proliferation and motility of NIH3T3 cells via ERK pathway activation. Cell Signal 2007, 19: 1554-1564
33. Kim SE, Lee WJ and Choi KY. The PI3 kinase-Akt pathway mediates Wnt3a-induced proliferation. Cell Signal 2007, 19: 511-518.
34. Jia L, Zhou J, Peng S, Li J, Cao Y and Duan E. Effects of Wnt3a on proliferation and differentiation of human epidermal stem cells. Biochem Biophys Res Commun 2008, 368: 483-488.
35. Loughrey CM, MacEachern KE, Cooper J and Smith GL. Measurement of the dissociation constant of Fluo-3 for Ca2+ in isolated rabbit cardiomyocytes using Ca2+ wave characteristics. Cell Calcium 2003, 34: 1-9.
36. Du WJ, Li JK, Wang QY, Hou JB and Yu B. Lithium chloride regulates Connexin 43 in skeletal myoblasts in vitro: possible involvement in Wnt/ beta-catenin signaling. Cell Commun Adhes 2008, 15: 261-271.
37. Zhai Y, Wu R, Schwartz DR, Darrah D, Reed H, Kolligs FT and Nieman MT, et al. Role of beta-catenin/T-cell factor-regulated genes in ovarian endometrioid adenocarcinomas. Am J Pathol 2002, 160: 1229-1238.
38. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, Cullen DM, Zhao W, Li C and Kharode Y, et al. Wnt/b-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem 2006, 281: 31720-31728.
39. Constantinou T, Baumann F, Lacher MD, Saurer S, Friis R and Dharmarajan A. SFRP-4 abrogates Wnt-3a-induced beta-catenin and Akt/ PKB signaling and reverses a Wnt-3a-imposed inhibition of in vitro mammary differentiation. J Mol Signal 2008, 3: 10.
40. Ai Z, Fischer A, Spray DC, Brown AM and Fishman GI. Wnt-1 regulation of Connexin 43 in cardiac myocytes. J Clin Invest 2000, 105: 161-171.
41. Almeida M, Han L, Bellido T, Manolagas SC and Kousteni S. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/ AKT. J Biol Chem 2005, 280: 41342-41351.
42. Pahujaa M, Anikin M and Goldberg GS. Phosphorylation of connexin43 induced by Src: regulation of gap junctional communication between transformed cells. Exp Cell Res 2007, 313: 4083-4090.
43. Tong D, Li TY, Naus KE, Bai D and Kidder GM. In vivo analysis of undocked connexin 43 gap junction hemichannels in ovarian granulosa cells. J Cell Sci 2007, 120: 4016-4024.
44. Gittens JE and Kidder GM. Differential contributions of connexin37 and Connexin 43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J Cell Sci 2005, 118: 5071-5078.
45. Li WE, Waldo K, Linask KL, Chen T, Wessels A, Parmacek MS, Kirby ML and Lo CW. An essential role for connexin 43 gap junctions in mouse coronary artery development. Development 2002, 129: 2031-2042
46. Moorby C and Patel M. Dual functions for connexins: Cx43 regulates growth independently of gap junction formation. Exp Cell Res 2001, 271: 238-248.
47. Dang XT, Doble BW and Kardami E. The carboxy-tail of connexin-43 localizes to the nucleus and inhibits cell growth. Mol Cell Biochem 2003, 242: 35-38.
48. Yamasaki H, Krutovskikh V, Mesnil M, Tanaka T, Zaidan-Dagli ML and Omori Y. Role of connexin (gap junction) genes in cell growth control and carcinogenesis. C R Acad Sci III 1999, 322: 151-159.
49. Mesnil M. Connexins and cancer. Biol Cell 2002, 94: 493-500.
50. Yamasaki H and Naus CCG. Role of connexin genes in growth control. Carcinogenesis 1996, 17: 1199-1213.
51. Dale N. Dynamic ATP signaling and neural development. J Physiol 2008, 586: 2429-2436.
52. Nunes PH, Calaza Kda C, Albuquerque LM, Fragel-Madeira L, Sholl-Franco A and Ventura AL. Signal transduction pathways associated with ATP-induced proliferation of cell progenitors in the intact embryonic retina. Int J Dev Neurosci 2007, 25: 499-508.
53. Pearson R, Catsicas M, Becker D and Mobbs P. Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci 2002, 22: 7569-7579.
54. Webb SE and Miller AL. Calcium signaling during embryonic development. Nat Rev Mol Cell Biol 2003, 4: 539-551.
55. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD and Kessaris N,, et al. . ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci USA 2008, 105: 18770-18775.
56. Bruzzone R and Dermietzel R. Structure and function of gap junctions in the developing brain. Cell Tissue Res 2006, 326: 239-248. (Pubitemid 44435805)
57. Arakawa E and Hasegawa K. Benidipine, a calcium channel blocker, regulates proliferation and phenotype of vascular smooth muscle cells. J Pharmacol Sci 2006, 100: 149-156.
58. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS and MacDougald OA. Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulin-like growth factors. J Biol Chem, 2002, 277: 38239-38244.
59. Khan MT, Wagner L, Yule DI, Bhanumathy C and Joseph SK. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J Biol Chem 2006, 281: 3731-3737.
60. Stamatakis M and Mantzaris NV. Modeling of ATP-mediated signal transduction and wave propagation in astrocytic cellular networks. J Theor Biol 2006, 241: 649-668.