Notch activation of Ca2+ signaling in the development of hypoxic pulmonary vasoconstriction and pulmonary hypertension

American Journal of Respiratory Cell and Molecular Biology

Volumn 53, Issue 3, 2015, Pages 355-367

  Smith, Kimberly A ^a   Voiriot, Guillaume ^a   Tang, Haiyang ^a,b   Fraidenburg, Dustin R ^a   Song, Shanshan ^a,b   Yamamura, Hisao ^a,c   Yamamura, Aya ^a,d   Guo, Qiang ^a,e   Wan, Jun ^a   Pohl, Nicole M ^a   Tauseef, Mohammad ^a   Bodmer, Rolf ^f   Ocorr, Karen ^f   Thistlethwaite, Patricia A ^g   Haddad, Gabriel G ^h   Powell, Frank L ⁱ   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)

^c NAGOYA CITY UNIVERSITY   (Japan)

^d KINJO GAKUIN UNIVERSITY   (Japan)

^e SOOCHOW UNIVERSITY   (China)

^f BURNHAM INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

ⁱ UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Hypoxia; Notch; Pulmonary artery; Store operated Ca2+ entry; TRPC6

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL; GAMMA SECRETASE INHIBITOR; JAGGED1; NOTCH RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; CALCIUM BINDING PROTEIN; MEMBRANE PROTEIN; NOTCH1 PROTEIN, MOUSE; NOTCH1 RECEPTOR; SERRATE PROTEINS; SIGNAL PEPTIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTICLE; CALCIUM SIGNALING; CELL PROLIFERATION; CYTOSOL; HUMAN; HUMAN CELL; HYPOXIC LUNG VASOCONSTRICTION; LUNG ARTERY PRESSURE; LUNG VENTILATION PERFUSION RATIO; MALE; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN TARGETING; PULMONARY ARTERY SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; RECEPTOR UPREGULATION; SYSTOLIC BLOOD PRESSURE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CELL HYPOXIA; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PULMONARY ARTERY; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELL HYPOXIA; CELLS, CULTURED; HUMANS; HYPERTENSION, PULMONARY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; RECEPTOR, NOTCH1; TRPC CATION CHANNELS; VASOCONSTRICTION;

EID: 84941559026     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0235OC     Document Type: Article

References (54)

1. Moudgil R, Michelakis ED, Archer SL. Hypoxic pulmonary vasoconstriction. J Appl Physiol 2005;98:390-403.
2. Sylvester JT, Shimoda LA, Aaronson PI, Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 2012;92:367-520.
3. Castaldi PJ, Hersh CP, Reilly JJ, Silverman EK. Genetic associations with hypoxemia and pulmonary arterial pressure in COPD. Chest 2009;135:737-744.
4. Voelkel NF, Cool CD. Pulmonary vascular involvement in chronic obstructive pulmonary disease. Eur Respir J Suppl 2003;46:28s-32s.
5. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 2009;54:S20-S31.
6. Stenmark KR, Davie N, Frid M, Gerasimovskaya E, Das M. Role of the adventitia in pulmonary vascular remodeling. Physiology (Bethesda) 2006;21:134-145.
7. Durmowicz AG, Parks WC, Hyde DM, Mecham RP, Stenmark KR. Persistence, re-expression, and induction of pulmonary arterial fibronectin, tropoelastin, and type I procollagen mRNA expression in neonatal hypoxic pulmonary hypertension. Am J Pathol 1994;145:1411-1420.
8. Platoshyn O, Yu Y, Golovina VA, McDaniel SS, Krick S, Li L, Wang JY, Rubin LJ, Yuan JX. Chronic hypoxia decreases KV channel expression and function in pulmonary artery myocytes. Am J Physiol Lung Cell Mol Physiol 2001;280:L801-L812.
9. Reeve HL, Michelakis E, Nelson DP, Weir EK, Archer SL. Alterations in a redox oxygen sensing mechanism in chronic hypoxia. J Appl Physiol 2001;90:2249-2256.
10. + current in rat pulmonary artery muscle cells. Am J Physiol 1994;266:H365-H370.
11. + channel alpha subunits in pulmonary artery smooth muscle cells. J Clin Invest 1997;100:2347-2353.
12. Hardingham GE, Chawla S, Johnson CM, Bading H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 1997;385:260-265.
13. 2+ pool content is linked to control of cell growth. Proc Natl Acad Sci USA 1993;90:4986-4990.
14. Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 2008;454:538-542.
15. 2+ channel function. J Cell Biol 2005;169:435-445.
16. 2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 2004;95:496-505.
17. 2+ in pulmonary arterial smooth muscle cells. Circ Res 2006;98:1528-1537.
18. 2+ responses to acute hypoxia in pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 2009;297:L17-L25.
19. 2+ entry in human pulmonary artery myocytes during proliferation. Am J Physiol Heart Circ Physiol 2001;280:H746-H755.
20. 2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Pulm Circ 2011;1:84-94.
21. Yu Y, Keller SH, Remillard CV, Safrina O, Nicholson A, Zhang SL, Jiang W, Vangala N, Landsberg JW, Wang J-Y, et al. A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation 2009;119:2313-2322.
22. Chigurupati S, Venkataraman R, Barrera D, Naganathan A, Madan M, Paul L, Pattisapu JV, Kyriazis GA, Sugaya K, Bushnev S, et al. Receptor channel TRPC6 is a key mediator of Notch-driven glioblastoma growth and invasiveness. Cancer Res 2010;70:418-427.
23. Kyriazis GA, Belal C, Madan M, Taylor DG, Wang J, Wei Z, Pattisapu JV, Chan SL. Stress-induced switch in Numb isoforms enhances Notch-dependent expression of subtype-specific transient receptor potential channel. J Biol Chem 2010;285:6811-6825.
24. Gridley T. Notch signaling in the vasculature. Curr Top Dev Biol 2010;92:277-309.
25. Li X, Zhang X, Leathers R, Makino A, Huang C, Parsa P, Macias J, Yuan JX, Jamieson SW, Thistlethwaite PA. Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat Med 2009;15:1289-1297.
26. 2+ entry in human pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 2014;306:C871-C878.
27. 2+ channel activity in pulmonary artery by upregulating Cav1.2 and Cav3.2. Am J Physiol Lung Cell Mol Physiol 2013;305:L154-L164.
28. Marshall C, Mamary AJ, Verhoeven AJ, Marshall BE. Pulmonary artery NADPH-oxidase is activated in hypoxic pulmonary vasoconstriction. Am J Respir Cell Mol Biol 1996;15:633-644.
29. 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 2013;3:396-405.
30. Koutelou E, Sato S, Tomomori-Sato C, Florens L, Swanson SK, Washburn MP, Kokkinaki M, Conaway RC, Conaway JW, Moschonas NK. Neuralized-like 1 (Neurl1) targeted to the plasma membrane by N-myristoylation regulates the Notch ligand Jagged1. J Biol Chem 2008;283:3846-3853.
31. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999;284:770-776.
32. Miele L, Osborne B. Arbiter of differentiation and death: Notch signaling meets apoptosis. J Cell Physiol 1999;181:393-409.
33. Campos AH, Wang W, Pollman MJ, Gibbons GH. Determinants of Notch-3 receptor expression and signaling in vascular smooth muscle cells: implications in cell-cycle regulation. Circ Res 2002;91:999-1006.
34. Morrow D, Sweeney C, Birney YA, Cummins PM, Walls D, Redmond EM, Cahill PA. Cyclic strain inhibits Notch receptor signaling in vascular smooth muscle cells in vitro. Circ Res 2005;96:567-575.
35. Sakata Y, Xiang F, Chen Z, Kiriyama Y, Kamei CN, Simon DI, Chin MT. Transcription factor CHF1/Hey2 regulates neointimal formation in vivo and vascular smooth muscle proliferation and migration in vitro. Arterioscler Thromb Vasc Biol 2004;24:2069-2074.
36. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, Klonjkowski B, Berrou E, Mericskay M, Li Z, et al. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 2004;18:2730-2735.
37. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 2001;128:3675-3683.
38. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 2008;105:6392-6397.
39. Zheng X, Linke S, Dias JM, Zheng X, Gradin K, Wallis TP, Hamilton BR, Gustafsson M, Ruas JL, Wilkins S, et al. Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc Natl Acad Sci USA 2008;105:3368-3373.
40. Mukherjee T, Kim WS, Mandal L, Banerjee U. Interaction between Notch and Hif-alpha in development and survival of Drosophila blood cells. Science 2011;332:1210-1213.
41. Coant N, Ben Mkaddem S, Pedruzzi E, Guichard C, Treton X, Ducroc R, Freund JN, Cazals-Hatem D, Bouhnik Y, Woerther PL, et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol Cell Biol 2010;30:2636-2650.
42. Hamanaka RB, Glasauer A, Hoover P, Yang S, Blatt H, Mullen AR, Getsios S, Gottardi CJ, DeBerardinis RJ, Lavker RM, et al. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci Signal 2013;6:ra8.
43. Zhu JH, Chen CL, Flavahan S, Harr J, Su B, Flavahan NA. Cyclic stretch stimulates vascular smooth muscle cell alignment by redox-dependent activation of Notch3. Am J Physiol Heart Circ Physiol 2011;300:H1770-H1780.
44. Guzy RD, Schumacker PT. Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 2006;91:807-819.
45. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M. Hypoxia requires Notch signaling to maintain the undifferentiated cell state. Dev Cell 2005;9:617-628.
46. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res 1997;81:940-952.
47. Wohrley JD, Frid MG, Moiseeva EP, Orton EC, Belknap JK, Stenmark KR. Hypoxia selectively induces proliferation in a specific subpopulation of smooth muscle cells in the bovine neonatal pulmonary arterial media. J Clin Invest 1995;96:273-281.
48. Morrow D, Scheller A, Birney YA, Sweeney C, Guha S, Cummins PM, Murphy R, Walls D, Redmond EM, Cahill PA. Notch-mediated CBF-1/RBP-J{kappa}-dependent regulation of human vascular smooth muscle cell phenotype in vitro. Am J Physiol Cell Physiol 2005;289:C1188-C1196.
49. Owens GK. Molecular control of vascular smooth muscle cell differentiation. Acta Physiol Scand 1998;164:623-635.
50. Proweller A, Pear WS, Parmacek MS. Notch signaling represses myocardin-induced smooth muscle cell differentiation. J Biol Chem 2005;280:8994-9004.
51. Tang Y, Urs S, Liaw L. Hairy-related transcription factors inhibit Notch-induced smooth muscle alpha-actin expression by interfering with Notch intracellular domain/CBF-1 complex interaction with the CBF-1-binding site. Circ Res 2008;102:661-668.
52. Shawber C, Nofziger D, Hsieh JJ, Lindsell C, Bogler O, Hayward D, Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 1996;122:3765-3773.
53. Kwon C, Cheng P, King IN, Andersen P, Shenje L, Nigam V, Srivastava D. Notch post-translationally regulates beta-catenin protein in stem and progenitor cells. Nat Cell Biol 2011;13:1244-1251.
54. Perumalsamy LR, Nagala M, Banerjee P, Sarin A. A hierarchical cascade activated by non-canonical Notch signaling and the mTOR-Rictor complex regulates neglect-induced death in mammalian cells. Cell Death Differ 2009;16:879-889.