Upregulated expression of STIM2, TRPC6, and orai2 contributes to the transition of pulmonary arterial smooth muscle cells from a contractile to proliferative phenotype

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 8, 2015, Pages C581-C593

  Fernandez, Ruby A ^a,b   Wan, Jun ^a   Song, Shanshan ^a,b   Smith, Kimberly A ^a   Gu, Yali ^b   Tauseef, Mohammad ^a   Tang, Haiyang ^b   Makino, Ayako ^a,b   Mehta, Dolly ^a   Yuan, Jason X J ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Pasmc; Phenotype; Pulmonary artery; Store operated calcium channel

Indexed keywords

CALCIUM ION; HEPARIN; PROTEIN; PROTEIN ORAI2; SMALL INTERFERING RNA; STROMAL INTERACTION MOLECULE 2; TRANSFORMING GROWTH FACTOR BETA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; MEMBRANE PROTEIN; NIFEDIPINE; ORAI2 PROTEIN, MOUSE; STIM2 PROTEIN, MOUSE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LUNG ARTERY PRESSURE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; RAT; STORE OPERATED CALCIUM ENTRY; UPREGULATION; VOLTAGE DEPENDENT CALCIUM ENTRY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CALCIUM SIGNALING; CELL CULTURE; CYTOLOGY; GENETICS; MALE; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; PULMONARY ARTERY; RNA INTERFERENCE; SMOOTH MUSCLE FIBER; SPRAGUE DAWLEY RAT; VASCULAR REMODELING; VASCULAR RESISTANCE; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALIA;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELL DEDIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; HYPERTENSION, PULMONARY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NIFEDIPINE; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFORMING GROWTH FACTOR BETA; TRPC CATION CHANNELS; VASCULAR REMODELING; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 84928042453     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00202.2014     Document Type: Article

References (48)

1. Aubart FC, Sassi Y, Coulombe A, Mougenot N, Vrignaud C, Leprince P, Lechat P, Lompre AM, Hulot JS. RNA interference targeting STIM1 suppresses vascular smooth muscle cell proliferation and neointima formation in the rat. Mol Ther 17: 455–462, 2009.
2. Barst RJ, Agnoletti G, Fraisse A, Baldassarre J, Wessel DL. Vasodilator testing with nitric oxide and/or oxygen in pediatric pulmonary hypertension. Pediatr Cardiol 31: 598–606, 2010.
3. Berna-Erro A, Galan C, Dionisio N, Gomez LJ, Salido GM, Rosado JA. Capacitative and non-capacitative signaling complexes in human platelets. Biochim Biophys Acta 1823: 1242–1251, 2012.
4. Bravo R, Macdonald-Bravo H. Existence of two populations of cyclin/ proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J Cell Biol 105: 1549–1554, 1987.
5. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol 34: 1345–1356, 2002.
6. Davis-Dusenbery BN, Wu C, Hata A. Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler Thromb Vasc Biol 31: 2370–2377, 2011.
7. Duband JL, Gimona M, Scatena M, Sartore S, Small JV. Calponin and SM 22 as differentiation markers of smooth muscle: spatiotemporal distribution during avian embryonic development. Differentiation 55: 1–11, 1993.
8. Fantozzi I, Zhang S, Platoshyn O, Remillard CV, Cowling RT, Yuan JX. Hypoxia increases AP-1 binding activity by enhancing capacitative Ca2+ entry in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 285: L1233–L1245, 2003.
9. Fatigati V, Murphy RA. Actin and tropomyosin variants in smooth muscles. Dependence on tissue type. J Biol Chem 259: 14383–14388, 1984.
10. Frid MG, Shekhonin BV, Koteliansky VE, Glukhova MA. Phenotypic changes of human smooth muscle cells during development: late expression of heavy caldesmon and calponin. Dev Biol 153: 185–193, 1992.
11. Galie N, Corris PA, Frost A, Girgis RE, Granton J, Jing ZC, Klepetko W, McGoon MD, McLaughlin VV, Preston IR, Rubin LJ, Sandoval J, Seeger W, Keogh A. Updated treatment algorithm of pulmonary arterial hypertension. J Am Coll Cardiol 62: D60–D72, 2013.
12. Galie N, Simonneau G. The Fifth World Symposium on Pulmonary Hypertension. J Am Coll Cardiol 62: D1–D3, 2013.
13. Garg HG, Thompson BT, Hales CA. Structural determinants of antiproliferative activity of heparin on pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 279: L779–L789, 2000.
14. Garg HG, Yu L, Hales CA, Toida T, Islam T, Linhardt RJ. Sulfation patterns in heparin and heparan sulfate: effects on the proliferation of bovine pulmonary artery smooth muscle cells. Biochim Biophys Acta 1639: 225–231, 2003.
15. Goumans MJ, Mummery C. Functional analysis of the TGFβ receptor/ Smad pathway through gene ablation in mice. Int J Dev Biol 44: 253–265, 2000.
16. Guo RW, Wang H, Gao P, Li MQ, Zeng CY, Yu Y, Chen JF, Song MB, Shi YK, Huang L. An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc Res 81: 660–668, 2009.
17. Hautmann MB, Madsen CS, Owens GK. A transforming growth factor β (TGF β) control element drives TGFβ-induced stimulation of smooth muscle alpha-actin gene expression in concert with two CArG elements. J Biol Chem 272: 10948–10956, 1997.
18. Kim S, Ip HS, Lu MM, Clendenin C, Parmacek MS. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol Cell Biol 17: 2266–2278, 1997.
19. Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L. Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 105: 2895–2900, 2008.
20. Manabe I, Owens GK. CArG elements control smooth muscle subtypespecific expression of smooth muscle myosin in vivo. J Clin Invest 107: 823–834, 2001.
21. Mandegar M, Remillard CV, Yuan JX. Ion channels in pulmonary arterial hypertension. Prog Cardiovasc Dis 45: 81–114, 2002.
22. Marchand A, Abi-Gerges A, Saliba Y, Merlet E, Lompre AM. Calcium signaling in vascular smooth muscle cells: from physiology to pathology. Adv Exp Med Biol 740: 795–810, 2012.
23. Montani D, Savale L, Natali D, Jais X, Herve P, Garcia G, Humbert M, Simonneau G, Sitbon O. Long-term response to calcium-channel blockers in non-idiopathic pulmonary arterial hypertension. Eur Heart J 31: 1898–1907, 2010.
24. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 54: S20–S31, 2009.
25. Mrabat H, Garg HG, Hales CA. Growth inhibition of bovine pulmonary artery smooth muscle cells following long-term heparin treatment. J Cell Physiol 221: 603–608, 2009.
26. Ogawa A, Firth AL, Smith KA, Maliakal MV, Yuan JX. PDGF enhances store-operated Ca2+ entry by upregulating STIM1/Orai1 via activation of Akt/mTOR in human pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 302: C405–C411, 2012.
27. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487–517, 1995.
28. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767–801, 2004.
29. Reid L. Vascular remodeling. In: The Pulmonary Circulation: Normal and Abnormal: Mechanisms, Management, and the National Registry, edited by Fishman A. Philadelphia, PA: Univ. of Pennsylvania Press, 1990, p. 264.
30. Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J 15: 100–108, 2007.
31. Rich S, Kaufmann E, Levy PS. The effect of high doses of calciumchannel blockers on survival in primary pulmonary hypertension. N Engl J Med 327: 76–81, 1992.
32. Roe MW, Lemasters JJ, Herman B. Assessment of Fura-2 for measurements of cytosolic free calcium. Cell Calcium 11: 63–73, 1990.
33. Sitbon O, Humbert M, Jais X, Ioos V, Hamid AM, Provencher S, Garcia G, Parent F, Herve P, Simonneau G. Long-term response to calcium channel blockers in idiopathic pulmonary arterial hypertension. Circulation 111: 3105–3111, 2005.
34. Solik P, Lesny P, Luknar M, Varga I, Goncalvesova E. The long-term response to treatment with calcium channel blockers in a patient with idiopathic pulmonary arterial hypertension. Bratisl Lek Listy 114: 283– 286, 2013.
35. Song MY, Makino A, Yuan JX. STIM2 contributes to enhanced storeoperated Ca2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Pulm Circ 1: 84–94, 2011.
36. Takahashi Y, Watanabe H, Murakami M, Ono K, Munehisa Y, Koyama T, Nobori K, Iijima T, Ito H. Functional role of stromal interaction molecule 1 (STIM1) in vascular smooth muscle cells. Biochem Biophys Res Commun 361: 934–940, 2007.
37. Tang H, Chen J, Fraidenburg DR, Song S, Sysol JR, Drennan AR, Offermanns S, Ye RD, Bonini MG, Minshall RD, Garcia JG, Machado RF, Makino A, Yuan JX. Deficiency of Akt1, but not Akt2, attenuates the development of pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 308: L208–L220, 2015.
38. ten Dijke P, Arthur HM. Extracellular control of TGFβ signalling in vascular development and disease. Nat Rev Mol Cell Biol 8: 857–869, 2007.
39. Thorneloe KS, Nelson MT. Ion channels in smooth muscle: regulators of intracellular calcium and contractility. Can J Physiol Pharmacol 83: 215–242, 2005.
40. Tuder RM, Archer SL, Dorfmuller P, Erzurum SC, Guignabert C, Michelakis E, Rabinovitch M, Schermuly R, Stenmark KR, Morrell NW. Relevant issues in the pathology and pathobiology of pulmonary hypertension. J Am Coll Cardiol 62: D4–D12, 2013.
41. Wan J, Yamamura A, Zimnicka AM, Voiriot G, Smith KA, Tang H, Ayon RJ, Choudhury MS, Ko EA, Wang J, Wang C, Makino A, Yuan JX. Chronic hypoxia selectively enhances L- and T-type voltage-dependent Ca2+ channel activity in pulmonary artery by upregulating CaV1.2 and CaV3.2. Am J Physiol Lung Cell Mol Physiol 305: L154–L164, 2013.
42. Wang J, Weigand L, Lu W, Sylvester JT, Semenza GL, Shimoda LA. Hypoxia inducible factor 1 mediates hypoxia-induced TRPC expression and elevated intracellular Ca2+ in pulmonary arterial smooth muscle cells. Circ Res 98: 1528–1537, 2006.
43. Xu M, Platoshyn O, Makino A, Dillmann WH, Akassoglou K, Remillard CV, Yuan JX. Characterization of agonist-induced vasoconstriction in mouse pulmonary artery. Am J Physiol Heart Circ Physiol 294: H220–H228, 2008.
44. Yoo HY, Zeifman A, Ko EA, Smith KA, Chen J, Machado RF, Zhao YY, Minshall RD, Yuan JX. Optimization of isolated perfused/ventilated mouse lung to study hypoxic pulmonary vasoconstriction. Pulm Circ 3: 396–405, 2013.
45. Yu Y, Fantozzi I, Remillard CV, Landsberg JW, Kunichika N, Platoshyn O, Tigno DD, Thistlethwaite PA, Rubin LJ, Yuan JX. Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc Natl Acad Sci USA 101: 13861– 13866, 2004.
46. Yu Y, Keller SH, Remillard CV, Safrina O, Nicholson A, Zhang SL, Jiang W, Vangala N, Landsberg JW, Wang JY, Thistlethwaite PA, Channick RN, Robbins IM, Loyd JE, Ghofrani HA, Grimminger F, Schermuly RT, Cahalan MD, Rubin LJ, Yuan JX. A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation 119: 2313– 2322, 2009.
47. Yu Y, Sweeney M, Zhang S, Platoshyn O, Landsberg J, Rothman A, Yuan JX. PDGF stimulates pulmonary vascular smooth muscle cell proliferation by upregulating TRPC6 expression. Am J Physiol Cell Physiol 284: C316–C330, 2003.
48. Zhang S, Dong H, Rubin LJ, Yuan JX. Upregulation of Na+/Ca2+ exchanger contributes to the enhanced Ca2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Am J Physiol Cell Physiol 292: C2297–C2305, 2007.