Abstract
Cyclic AMP and Ca2+ are the first second or intracellular messengers identified, unveiling the cellular mechanisms activated by a plethora of extracellular signals, including hormones. Cyclic AMP generation is catalyzed by adenylyl cyclases (ACs), which convert ATP into cAMP and pyrophosphate. By the way, Ca2+, as energy, can neither be created nor be destroyed; Ca2+ can only be transported, from one compartment to another, or chelated by a variety of Ca2+-binding molecules. The fine regulation of cytosolic concentrations of cAMP and free Ca2+ is crucial in cell function and there is an intimate cross-talk between both messengers to fine-tune the cellular responses. Cancer is a multifactorial disease resulting from a combination of genetic and environmental factors. Frequent cases of cAMP and/or Ca2+ homeostasis remodeling have been described in cancer cells. In those tumoral cells, cAMP and Ca2+ signaling plays a crucial role in the development of hallmarks of cancer, including enhanced proliferation and migration, invasion, apoptosis resistance, or angiogenesis. This review summarizes the cross-talk between the ACs/cAMP and Ca2+ intracellular pathways with special attention to the functional and reciprocal regulation between Orai1 and AC8 in normal and cancer cells.
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Abbreviations
- [Ca2+]c :
-
Cytosolic Ca2+ concentration
- AC:
-
Adenylyl cyclase
- ACBD3:
-
Acyl CoA binding domain protein-3
- AKAP:
-
A-kinase anchoring protein
- ARC:
-
Arachidonic acid-regulated Ca2+
- CAD:
-
CRAC activation domain
- CaM:
-
Calmodulin
- CaMK:
-
Calmodulin-dependent kinase
- CaN:
-
Calcineurin
- CAP1:
-
Adenylyl cyclase-associated protein 1
- CC:
-
Coiled-coil domain
- CDI:
-
Ca2+-dependent inactivation
- CRAC:
-
Ca2+ release-activated Ca2+
- CTPD:
-
C-terminal polybasic domain
- DRG:
-
Dorsal root ganglion
- Epac:
-
Exchange factor directly activated by cAMP
- ER:
-
Endoplasmic reticulum
- FCDI:
-
Fast Ca2+-dependent inactivation
- FRET:
-
Förster resonance energy transfer
- GRK:
-
G-protein coupled receptor kinase
- I CRAC :
-
Ca2+ released-activated Ca2+ current
- IP3:
-
Inositol 1,4,5-trisphosphate
- I SOC :
-
Store-operated Ca2+ currents
- NCX:
-
Na+-Ca2+ exchanger
- NFAT:
-
Nuclear factor of activated T-cells
- OASF:
-
ORAI1-activating small fragment
- PIP2:
-
Phosphatidylinositol 4,5-bisphosphate
- PKA:
-
cAMP-dependent protein kinase
- PKC:
-
Protein kinase C
- PLC:
-
Phospholipase C
- PM:
-
Plasma membrane
- PMCA:
-
Plasma membrane Ca2+ ATPase
- PTH:
-
Parathyroid hormone
- RGS:
-
Regulator of G protein signaling
- SAM :
-
Sterile alpha motif
- SCDI:
-
Slow Ca2+-dependent inactivation
- SERCA:
-
Sarco/endoplasmic reticulum Ca2+ ATPase
- SOAR:
-
STIM1 Orai-activating region
- SOC:
-
Store-operated channels
- SOCE:
-
Store-operated Ca2+ entry
- STIM1:
-
Stromal interaction molecule 1
- TRP:
-
Transient receptor potential channels
- TRPC:
-
Transient receptor potential-canonical
References
Akin BL, Hurley TD, Chen Z, Jones LR (2013) The structural basis for phospholamban inhibition of the calcium pump in sarcoplasmic reticulum. J Biol Chem 288(42):30181–30191
Albarran L, Berna-Erro A, Dionisio N, Redondo PC, Lopez E, Lopez JJ, Salido GM, Brull Sabate JM, Rosado JA (2014) TRPC6 participates in the regulation of cytosolic basal calcium concentration in murine resting platelets. Biochim Biophys Acta 1843(4):789–796
Albarran L, Lopez JJ, Ben Amor N, Martín-Cano FE, Berna-Erro A, Smani T, Salido GM, Rosado JA (2016a) Dynamic interaction of SARAF with STIM1 and Orai1 to modulate store-operated calcium entry. Sci Rep 6:24452
Albarran L, Lopez JJ, Salido GM, Rosado JA (2016b) Historical overview of store-operated Ca(2+) entry. Adv Exp Med Biol 898:3–24
Ambudkar IS, de Souza LB, Ong HL (2017) TRPC1, Orai1, and STIM1 in SOCE: friends in tight spaces. Cell Calcium 63:33–39
Antoni FA, Palkovits M, Simpson J, Smith SM, Leitch AL, Rosie R, Fink G, Paterson JM (1998) Ca2+/calcineurin-inhibited adenylyl cyclase, highly abundant in forebrain regions, is important for learning and memory. J Neurosci 18(23):9650–9661
Averaimo S, Assali A, Ros O, Couvet S, Zagar Y, Genescu I, Rebsam A, Nicol X (2016) A plasma membrane microdomain compartmentalizes ephrin-generated cAMP signals to prune developing retinal axon arbors. Nat Commun 7:12896
Axelband F, Dias J, Miranda F, Ferrao FM, Reis RI, Costa-Neto CM, Lara LS, Vieyra A (2012) Angiotensin-(3-4) counteracts the angiotensin II inhibitory action on renal Ca2+-ATPase through a cAMP/PKA pathway. Regul Pept 177(1–3):27–34
Baggaley E, McLarnon S, Demeter I, Varga G, Bruce JI (2007) Differential regulation of the apical plasma membrane Ca(2+) -ATPase by protein kinase A in parotid acinar cells. J Biol Chem 282(52):37678–37693
Baldwin TA, Dessauer CW (2018) Function of adenylyl cyclase in heart: the AKAP connection. J Cardiovasc Dev Dis 5(1)
Baldwin TA, Li Y, Brand CS, Watts VJ, Dessauer CW (2019) Insights into the regulatory properties of human adenylyl cyclase type 9. Mol Pharmacol 95(4):349–360
Bassler J, Schultz JE, Lupas AN (2018) Adenylate cyclases: receivers, transducers, and generators of signals. Cell Signal 46:135–144
Bauman AL, Soughayer J, Nguyen BT, Willoughby D, Carnegie GK, Wong W, Hoshi N, Langeberg LK, Cooper DM, Dessauer CW, Scott JD (2006) Dynamic regulation of cAMP synthesis through anchored PKA-adenylyl cyclase V/VI complexes. Mol Cell 23(6):925–931
Bayewitch ML, Avidor-Reiss T, Levy R, Pfeuffer T, Nevo I, Simonds WF, Vogel Z (1998) Inhibition of adenylyl cyclase isoforms V and VI by various Gbetagamma subunits. FASEB J 12(11):1019–1025
Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11–21
Betzenhauser MJ, Yule DI (2010) Regulation of inositol 1,4,5-trisphosphate receptors by phosphorylation and adenine nucleotides. Curr Top Membr 66:273–298
Bhardwaj R, Augustynek BS, Ercan-Herbst E, Kandasamy P, Seedorf M, Peinelt C, Hediger MA (2020) Ca(2+)/Calmodulin binding to STIM1 hydrophobic residues facilitates slow Ca(2+)-dependent inactivation of the Orai1 channel. Cell Physiol Biochem 54(2):252–270
Bogard AS, Adris P, Ostrom RS (2012) Adenylyl cyclase 2 selectively couples to E prostanoid type 2 receptors, whereas adenylyl cyclase 3 is not receptor-regulated in airway smooth muscle. J Pharmacol Exp Ther 342(2):586–595
Bogard AS, Birg AV, Ostrom RS (2014) Non-raft adenylyl cyclase 2 defines a cAMP signaling compartment that selectively regulates IL-6 expression in airway smooth muscle cells: differential regulation of gene expression by AC isoforms. Naunyn Schmiedeberg’s Arch Pharmacol 387(4):329–339
Bol GF, Hulster A, Pfeuffer T (1997) Adenylyl cyclase type II is stimulated by PKC via C-terminal phosphorylation. Biochim Biophys Acta 1358(3):307–313
Bouron A, Chauvet S, Dryer S, Rosado JA (2016) Second messenger-operated calcium entry through TRPC6. Adv Exp Med Biol 898:201–249
Boutin B, Tajeddine N, Monaco G, Molgo J, Vertommen D, Rider M, Parys JB, Bultynck G, Gailly P (2015) Endoplasmic reticulum Ca(2+) content decrease by PKA-dependent hyperphosphorylation of type 1 IP3 receptor contributes to prostate cancer cell resistance to androgen deprivation. Cell Calcium 57(4):312–320
Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131(7):1327–1339
Broertjes J, Klarenbeek J, Habani Y, Langeslag M, Jalink K (2019) TRPM7 residue S1269 mediates cAMP dependence of Ca2+ influx. PLoS One 14(1):e0209563
Brown DA, Yule DI (2010) Protein kinase A regulation of P2X(4) receptors: requirement for a specific motif in the C-terminus. Biochim Biophys Acta 1803(2):275–287
Bruce JI, Yule DI, Shuttleworth TJ (2002) Ca2+-dependent protein kinase--a modulation of the plasma membrane Ca2+-ATPase in parotid acinar cells. J Biol Chem 277(50):48172–48181
Buck J, Sinclair ML, Schapal L, Cann MJ, Levin LR (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci U S A 96(1):79–84
Bunemann M, Gerhardstein BL, Gao T, Hosey MM (1999) Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the beta(2) subunit. J Biol Chem 274(48):33851–33854
Burgess GM, Bird GS, Obie JF, Putney JW Jr (1991) The mechanism for synergism between phospholipase C- and adenylylcyclase-linked hormones in liver. Cyclic AMP-dependent kinase augments inositol trisphosphate-mediated Ca2+ mobilization without increasing the cellular levels of inositol polyphosphates. J Biol Chem 266(8):4772–4781
Cali JJ, Zwaagstra JC, Mons N, Cooper DM, Krupinski J (1994) Type VIII adenylyl cyclase. A Ca2+/calmodulin-stimulated enzyme expressed in discrete regions of rat brain. J Biol Chem 269(16):12190–12195
Calloway N, Vig M, Kinet JP, Holowka D, Baird B (2009) Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions. Mol Biol Cell 20(1):389–399
Calloway N, Holowka D, Baird B (2010) A basic sequence in STIM1 promotes Ca2+ influx by interacting with the C-terminal acidic coiled coil of Orai1. Biochemistry 49(6):1067–1071
Calloway N, Owens T, Corwith K, Rodgers W, Holowka D, Baird B (2011) Stimulated association of STIM1 and Orai1 is regulated by the balance of PtdIns(4,5)P(2) between distinct membrane pools. J Cell Sci 124(Pt 15):2602–2610
Cantero Mdel R, Velazquez IF, Streets AJ, Ong AC, Cantiello HF (2015) The cAMP signaling pathway and direct protein kinase A phosphorylation regulate Polycystin-2 (TRPP2) channel function. J Biol Chem 290(39):23888–23896
Cerny O, Anderson KE, Stephens LR, Hawkins PT, Sebo P (2017) cAMP signaling of adenylate cyclase toxin blocks the oxidative burst of neutrophils through Epac-mediated inhibition of phospholipase C activity. J Immunol 198(3):1285–1296
Chase A, Orchard CH (2011) Ca efflux via the sarcolemmal Ca ATPase occurs only in the t-tubules of rat ventricular myocytes. J Mol Cell Cardiol 50(1):187–193
Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289(5479):625–628
Chen YF, Chiu WT, Chen YT, Lin PY, Huang HJ, Chou CY, Chang HC, Tang MJ, Shen MR (2011) Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc Natl Acad Sci U S A 108(37):15225–15230
Chen J, Levin LR, Buck J (2012) Role of soluble adenylyl cyclase in the heart. Am J Physiol Heart Circ Physiol 302(3):H538–H543
Chen J, Wu F, Shi Y, Yang D, Xu M, Lai Y, Liu Y (2019) Identification of key candidate genes involved in melanoma metastasis. Mol Med Rep 20(2):903–914
Cheng KT, Liu X, Ong HL, Swaim W, Ambudkar IS (2011) Local Ca(2)+ entry via Orai1 regulates plasma membrane recruitment of TRPC1 and controls cytosolic Ca(2)+ signals required for specific cell functions. PLoS Biol 9(3):e1001025
Chen-Goodspeed M, Lukan AN, Dessauer CW (2005) Modeling of Galpha(s) and Galpha(i) regulation of human type V and VI adenylyl cyclase. J Biol Chem 280(3):1808–1816
Choi EJ, Xia Z, Storm DR (1992) Stimulation of the type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry 31(28):6492–6498. https://doi.org/10.1021/bi00143a019
Chow YW, Wang HL (1998) Functional modulation of P2X2 receptors by cyclic AMP-dependent protein kinase. J Neurochem 70(6):2606–2612
Cooper DM (2015) Store-operated Ca(2)(+)-entry and adenylyl cyclase. Cell Calcium 58(4):368–375
Cooper DM, Tabbasum VG (2014) Adenylate cyclase-centred microdomains. Biochem J 462(2):199–213
Cooper DM, Mons N, Karpen JW (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374(6521):421–424
Cosson MV, Hiis HG, Moltzau LR, Levy FO, Krobert KA (2019) Knockout of adenylyl cyclase isoform 5 or 6 differentially modifies the beta1-adrenoceptor-mediated inotropic response. J Mol Cell Cardiol 131:132–145
Crossthwaite AJ, Seebacher T, Masada N, Ciruela A, Dufraux K, Schultz JE, Cooper DM (2005) The cytosolic domains of Ca2+-sensitive adenylyl cyclases dictate their targeting to plasma membrane lipid rafts. J Biol Chem 280(8):6380–6391
Cuinas A, Garcia-Morales V, Vina D, Gil-Longo J, Campos-Toimil M (2016) Activation of PKA and Epac proteins by cyclic AMP depletes intracellular calcium stores and reduces calcium availability for vasoconstriction. Life Sci 155:102–109
Cumbay MG, Watts VJ (2004) Novel regulatory properties of human type 9 adenylate cyclase. J Pharmacol Exp Ther 310(1):108–115
Cumbay MG, Watts VJ (2005) Galphaq potentiation of adenylate cyclase type 9 activity through a Ca2+/calmodulin-dependent pathway. Biochem Pharmacol 69(8):1247–1256
Darbellay B, Arnaudeau S, Bader CR, Konig S, Bernheim L (2011) STIM1L is a new actin-binding splice variant involved in fast repetitive Ca2+ release. J Cell Biol 194(2):335–346
De Marinis YZ, Salehi A, Ward CE, Zhang Q, Abdulkader F, Bengtsson M, Braha O, Braun M, Ramracheya R, Amisten S, Habib AM, Moritoh Y, Zhang E, Reimann F, Rosengren A, Shibasaki T, Gribble F, Renstrom E, Seino S, Eliasson L, Rorsman P (2010) GLP-1 inhibits and adrenaline stimulates glucagon release by differential modulation of N- and L-type Ca2+ channel-dependent exocytosis. Cell Metab 11(6):543–553
Defer N, Best-Belpomme M, Hanoune J (2000) Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279(3):F400–F416
DeHaven WI, Smyth JT, Boyles RR, Putney JW Jr (2007) Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J Biol Chem 282(24):17548–17556
Desai PN, Zhang X, Wu S, Janoshazi A, Bolimuntha S, Putney JW, Trebak M (2015) Multiple types of calcium channels arising from alternative translation initiation of the Orai1 message. Sci Signal 8(387):ra74
Dessauer CW (2009) Adenylyl cyclase--A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol Pharmacol 76(5):935–941
Dessauer CW, Gilman AG (1997) The catalytic mechanism of mammalian adenylyl cyclase. Equilibrium binding and kinetic analysis of P-site inhibition. J Biol Chem 272(44):27787–27795
Dessauer CW, Tesmer JJ, Sprang SR, Gilman AG (1998) Identification of a Gialpha binding site on type V adenylyl cyclase. J Biol Chem 273(40):25831–25839
Dessauer CW, Watts VJ, Ostrom RS, Conti M, Dove S, Seifert R (2017) International union of basic and clinical pharmacology. CI. Structures and small molecule modulators of mammalian adenylyl cyclases. Pharmacol Rev 69(2):93–139
Diel S, Klass K, Wittig B, Kleuss C (2006) Gbetagamma activation site in adenylyl cyclase type II. Adenylyl cyclase type III is inhibited by Gbetagamma. J Biol Chem 281(1):288–294
Diez-Bello R, Jardin I, Salido GM, Rosado JA (2017) Orai1 and Orai2 mediate store-operated calcium entry that regulates HL60 cell migration and FAK phosphorylation. Biochim Biophys Acta 1864(6):1064–1070
Dionisio N, Galan C, Jardin I, Salido GM, Rosado JA (2011) Lipid rafts are essential for the regulation of SOCE by plasma membrane resident STIM1 in human platelets. Biochim Biophys Acta 1813(3):431–437
Dionisio N, Smani T, Woodard GE, Castellano A, Salido GM, Rosado JA (2015) Homer proteins mediate the interaction between STIM1 and Cav1.2 channels. Biochim Biophys Acta 1853(5):1145–1153
Doyle TB, Muntean BS, Ejendal KF, Hayes MP, Soto-Velasquez M, Martemyanov KA, Dessauer CW, Hu CD, Watts VJ (2019) Identification of novel adenylyl Cyclase 5 (AC5) signaling networks in D1 and D2 medium spiny neurons using bimolecular fluorescence complementation screening. Cell 8(11)
Duan B, Davis R, Sadat EL, Collins J, Sternweis PC, Yuan D, Jiang LI (2010) Distinct roles of adenylyl cyclase VII in regulating the immune responses in mice. J Immunol 185(1):335–344
Dubois C, Vanden Abeele F, Lehen'kyi V, Gkika D, Guarmit B, Lepage G, Slomianny C, Borowiec AS, Bidaux G, Benahmed M, Shuba Y, Prevarskaya N (2014) Remodeling of channel-forming ORAI proteins determines an oncogenic switch in prostate cancer. Cancer Cell 26(1):19–32
Duerr EM, Mizukami Y, Ng A, Xavier RJ, Kikuchi H, Deshpande V, Warshaw AL, Glickman J, Kulke MH, Chung DC (2008) Defining molecular classifications and targets in gastroenteropancreatic neuroendocrine tumors through DNA microarray analysis. Endocr Relat Cancer 15(1):243–256
Dunn TA, Storm DR, Feller MB (2009) Calcium-dependent increases in protein kinase-A activity in mouse retinal ganglion cells are mediated by multiple adenylate cyclases. PLoS One 4(11):e7877
Dutta K, Carmody MW, Cala SE, Davidoff AJ (2002) Depressed PKA activity contributes to impaired SERCA function and is linked to the pathogenesis of glucose-induced cardiomyopathy. J Mol Cell Cardiol 34(8):985–996
Efendiev R, Samelson BK, Nguyen BT, Phatarpekar PV, Baameur F, Scott JD, Dessauer CW (2010) AKAP79 interacts with multiple adenylyl cyclase (AC) isoforms and scaffolds AC5 and -6 to alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA) receptors. J Biol Chem 285(19):14450–14458
Eijkelkamp N, Linley JE, Torres JM, Bee L, Dickenson AH, Gringhuis M, Minett MS, Hong GS, Lee E, Oh U, Ishikawa Y, Zwartkuis FJ, Cox JJ, Wood JN (2013) A role for Piezo2 in EPAC1-dependent mechanical allodynia. Nat Commun 4:1682
Everett KL, Cooper DM (2013) An improved targeted cAMP sensor to study the regulation of adenylyl cyclase 8 by Ca2+ entry through voltage-gated channels. PLoS One 8(9):e75942
Fagan KA, Mahey R, Cooper DM (1996) Functional co-localization of transfected Ca(2+)-stimulable adenylyl cyclases with capacitative Ca2+ entry sites. J Biol Chem 271(21):12438–12444
Fagan KA, Graf RA, Tolman S, Schaack J, Cooper DM (2000) Regulation of a Ca2+-sensitive adenylyl cyclase in an excitable cell. Role of voltage-gated versus capacitative Ca2+ entry. J Biol Chem 275(51):40187–40194
Fan Y, Mu J, Huang M, Imani S, Wang Y, Lin S, Fan J, Wen Q (2019) Epigenetic identification of ADCY4 as a biomarker for breast cancer: an integrated analysis of adenylate cyclases. Epigenomics 11(14):1561–1579
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441(7090):179–185
Fierro L, Parekh AB (1999) Fast calcium-dependent inactivation of calcium release-activated calcium current (CRAC) in RBL-1 cells. J Membr Biol 168(1):9–17
Flacke JP, Flacke H, Appukuttan A, Palisaar RJ, Noldus J, Robinson BD, Reusch HP, Zippin JH, Ladilov Y (2013) Type 10 soluble adenylyl cyclase is overexpressed in prostate carcinoma and controls proliferation of prostate cancer cells. J Biol Chem 288(5):3126–3135
Foster LJ, De Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A 100(10):5813–5818
Fukushima M, Tomita T, Janoshazi A, Putney JW (2012) Alternative translation initiation gives rise to two isoforms of Orai1 with distinct plasma membrane mobilities. J Cell Sci 125(Pt 18):4354–4361
Gamper N, Rohacs T (2012) Phosphoinositide sensitivity of ion channels, a functional perspective. Subcell Biochem 59:289–333
Gao BN, Gilman AG (1991) Cloning and expression of a widely distributed (type IV) adenylyl cyclase. Proc Natl Acad Sci U S A 88(22):10178–10182
Geng J, Zhao Q, Zhang T, Xiao B (2017) In touch with the mechanosensitive piezo channels: structure, ion permeation, and mechanotransduction. Curr Top Membr 79:159–195
Gomes P, Soares-da-Silva P (2002) Role of cAMP-PKA-PLC signaling cascade on dopamine-induced PKC-mediated inhibition of renal Na(+)-K(+)-ATPase activity. Am J Physiol Renal Physiol 282(6):F1084–F1096
Gramajo-Buhler MC, Zelarayan L, Sanchez-Toranzo G (2016) Involvement of protein cAMP-dependent kinase, phospholipase A2 and phospholipase C in sperm acrosome reaction of Chinchilla lanigera. Reprod Domest Anim 51(1):150–157
Gu C, Cooper DM (1999) Calmodulin-binding sites on adenylyl cyclase type VIII. J Biol Chem 274(12):8012–8021
Gudlur A, Quintana A, Zhou Y, Hirve N, Mahapatra S, Hogan PG (2014) STIM1 triggers a gating rearrangement at the extracellular mouth of the ORAI1 channel. Nat Commun 5:5164
Gudlur A, Zeraik AE, Hirve N, Rajanikanth V, Bobkov AA, Ma G, Zheng S, Wang Y, Zhou Y, Komives EA, Hogan PG (2018) Calcium sensing by the STIM1 ER-luminal domain. Nat Commun 9(1):4536
Guillou JL, Nakata H, Cooper DM (1999) Inhibition by calcium of mammalian adenylyl cyclases. J Biol Chem 274(50):35539–35545
Hacker BM, Tomlinson JE, Wayman GA, Sultana R, Chan G, Villacres E, Disteche C, Storm DR (1998) Cloning, chromosomal mapping, and regulatory properties of the human type 9 adenylyl cyclase (ADCY9). Genomics 50(1):97–104
Halls ML, Cooper DM (2011) Regulation by Ca2+-signaling pathways of adenylyl cyclases. Cold Spring Harb Perspect Biol 3(1):a004143
Han JZ, Lin W, Chen YZ (2005) Inhibition of ATP-induced calcium influx in HT4 cells by glucocorticoids: involvement of protein kinase A. Acta Pharmacol Sin 26(2):199–204
Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145–174
Hasan R, Zhou GL (2019) The cytoskeletal protein cyclase-associated protein 1 (CAP1) in breast cancer: context-dependent roles in both the invasiveness and proliferation of cancer cells and underlying cell signals. Int J Mol Sci 20(11)
Haslauer M, Baltensperger K, Porzig H (1998) Thrombin and phorbol esters potentiate Gs-mediated cAMP formation in intact human erythroid progenitors via two synergistic signaling pathways converging on adenylyl cyclase type VII. Mol Pharmacol 53(5):837–845
He RQ, Li XJ, Liang L, Xie Y, Luo DZ, Ma J, Peng ZG, Hu XH, Chen G (2017) The suppressive role of miR-542-5p in NSCLC: the evidence from clinical data and in vivo validation using a chick chorioallantoic membrane model. BMC Cancer 17(1):655
Heemskerk JW, Feijge MA, Sage SO, Walter U (1994) Indirect regulation of Ca2+ entry by cAMP-dependent and cGMP-dependent protein kinases and phospholipase C in rat platelets. Eur J Biochem 223(2):543–551
Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397(6716):259–263
Hofmann F, Flockerzi V, Kahl S, Wegener JW (2014) L-type CaV1.2 calcium channels: from in vitro findings to in vivo function. Physiol Rev 94(1):303–326
Holz GG, Leech CA, Chepurny OG (2014) New insights concerning the molecular basis for defective glucoregulation in soluble adenylyl cyclase knockout mice. Biochim Biophys Acta 1842(12 Pt B):2593–2600
Holzmann C, Kilch T, Kappel S, Armbruster A, Jung V, Stockle M, Bogeski I, Schwarz EC, Peinelt C (2013) ICRAC controls the rapid androgen response in human primary prostate epithelial cells and is altered in prostate cancer. Oncotarget 4(11):2096–2107
Hong SH, Goh SH, Lee SJ, Hwang JA, Lee J, Choi IJ, Seo H, Park JH, Suzuki H, Yamamoto E, Kim IH, Jeong JS, Ju MH, Lee DH, Lee YS (2013) Upregulation of adenylate cyclase 3 (ADCY3) increases the tumorigenic potential of cells by activating the CREB pathway. Oncotarget 4(10):1791–1803
Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355(6358):353–356
Hou X, Pedi L, Diver MM, Long SB (2012) Crystal structure of the calcium release-activated calcium channel Orai. Science 338(6112):1308–1313
Hou X, Burstein SR, Long SB (2018) Structures reveal opening of the store-operated calcium channel Orai. Elife 7
Hua Y, Ma X, Liu X, Yuan X, Qin H, Zhang X (2017) Identification of the potential biomarkers for the metastasis of rectal adenocarcinoma. APMIS 125(2):93–100
Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8(9):1003–1010
Huang J, Zhou H, Mahavadi S, Sriwai W, Murthy KS (2007) Inhibition of Galphaq-dependent PLC-beta1 activity by PKG and PKA is mediated by phosphorylation of RGS4 and GRK2. Am J Physiol Cell Physiol 292(1):C200–C208
Inserte J, Hernando V, Ruiz-Meana M, Poncelas-Nozal M, Fernandez C, Agullo L, Sartorio C, Vilardosa U, Garcia-Dorado D (2014) Delayed phospholamban phosphorylation in post-conditioned heart favours Ca2+ normalization and contributes to protection. Cardiovasc Res 103(4):542–553
Islam MS, Leibiger I, Leibiger B, Rossi D, Sorrentino V, Ekstrom TJ, Westerblad H, Andrade FH, Berggren PO (1998) In situ activation of the type 2 ryanodine receptor in pancreatic beta cells requires cAMP-dependent phosphorylation. Proc Natl Acad Sci U S A 95(11):6145–6150
Jacobowitz O, Chen J, Premont RT, Iyengar R (1993) Stimulation of specific types of Gs-stimulated adenylyl cyclases by phorbol ester treatment. J Biol Chem 268(6):3829–3832
Jaiswal BS, Conti M (2003) Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc Natl Acad Sci U S A 100(19):10676–10681
Jardin I, Lopez JJ, Salido GM, Rosado JA (2008a) Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J Biol Chem 283(37):25296–25304
Jardin I, Redondo PC, Salido GM, Rosado JA (2008b) Phosphatidylinositol 4,5-bisphosphate enhances store-operated calcium entry through hTRPC6 channel in human platelets. Biochim Biophys Acta 1783(1):84–97
Jardin I, Albarran L, Salido GM, Lopez JJ, Sage SO, Rosado JA (2018a) Fine-tuning of store-operated calcium entry by fast and slow Ca(2+)-dependent inactivation: involvement of SARAF. Biochim Biophys Acta Mol Cell Res 1865(3):463–469
Jardin I, Diez-Bello R, Lopez JJ, Redondo PC, Salido GM, Smani T, Rosado JA (2018b) TRPC6 channels are required for proliferation, migration and invasion of breast cancer cell lines by modulation of Orai1 and Orai3 surface exposure. Cancers (Basel) 10(9):331
Jardin I, Lopez JJ, Salido GM, Rosado JA (2018c) Store-operated Ca(2+) entry in breast cancer cells: remodeling and functional role. Int J Mol Sci 19(12)
Kakurina GV, Kolegova ES, Kondakova IV (2018) Adenylyl cyclase-associated protein 1: structure, regulation, and participation in cellular processes. Biochemistry (Mosc) 83(1):45–53
Kapiloff MS, Piggott LA, Sadana R, Li J, Heredia LA, Henson E, Efendiev R, Dessauer CW (2009) An adenylyl cyclase-mAKAPbeta signaling complex regulates cAMP levels in cardiac myocytes. J Biol Chem 284(35):23540–23546
Kar P, Samanta K, Kramer H, Morris O, Bakowski D, Parekh AB (2014) Dynamic assembly of a membrane signaling complex enables selective activation of NFAT by Orai1. Curr Biol 24(12):1361–1368
Katsushika S, Chen L, Kawabe J, Nilakantan R, Halnon NJ, Homcy CJ, Ishikawa Y (1992) Cloning and characterization of a sixth adenylyl cyclase isoform: types V and VI constitute a subgroup within the mammalian adenylyl cyclase family. Proc Natl Acad Sci U S A 89(18):8774–8778
Kawabe J, Iwami G, Ebina T, Ohno S, Katada T, Ueda Y, Homcy CJ, Ishikawa Y (1994) Differential activation of adenylyl cyclase by protein kinase C isoenzymes. J Biol Chem 269(24):16554–16558
Kawabe J, Ebina T, Toya Y, Oka N, Schwencke C, Duzic E, Ishikawa Y (1996) Regulation of type V adenylyl cyclase by PMA-sensitive and -insensitive protein kinase C isoenzymes in intact cells. FEBS Lett 384(3):273–276
Kawasaki H, Kretsinger RH (2017) Conformational landscape mapping the difference between N-lobes and C-lobes of calmodulin. J Inorg Biochem 177:55–62
Kawasaki T, Lange I, Feske S (2009) A minimal regulatory domain in the C terminus of STIM1 binds to and activates ORAI1 CRAC channels. Biochem Biophys Res Commun 385(1):49–54
Kawasaki T, Ueyama T, Lange I, Feske S, Saito N (2010) Protein kinase C-induced phosphorylation of Orai1 regulates the intracellular Ca2+ level via the store-operated Ca2+ channel. J Biol Chem 285(33):25720–25730
Kheirbek MA, Britt JP, Beeler JA, Ishikawa Y, McGehee DS, Zhuang X (2009) Adenylyl cyclase type 5 contributes to corticostriatal plasticity and striatum-dependent learning. J Neurosci 29(39):12115–12124
Kim JA, Park JY, Kang HW, Huh SU, Jeong SW, Lee JH (2006) Augmentation of Cav3.2 T-type calcium channel activity by cAMP-dependent protein kinase A. J Pharmacol Exp Ther 318(1):230–237
Kim JH, Lkhagvadorj S, Lee MR, Hwang KH, Chung HC, Jung JH, Cha SK, Eom M (2014) Orai1 and STIM1 are critical for cell migration and proliferation of clear cell renal cell carcinoma. Biochem Biophys Res Commun 448(1):76–82
Kleinboelting S, Diaz A, Moniot S, van den Heuvel J, Weyand M, Levin LR, Buck J, Steegborn C (2014) Crystal structures of human soluble adenylyl cyclase reveal mechanisms of catalysis and of its activation through bicarbonate. Proc Natl Acad Sci U S A 111(10):3727–3732
Kolegova ES, Kakurina GV, Kondakova IV, Dobrodeev AY, Kostromitskii DN, Zhuikova LD (2019) Adenylate cyclase-associated protein 1 and Cofilin in progression of non-small cell lung cancer. Bull Exp Biol Med 167(3):393–395
Komal P, Estakhr J, Kamran M, Renda A, Nashmi R (2015) cAMP-dependent protein kinase inhibits alpha7 nicotinic receptor activity in layer 1 cortical interneurons through activation of D1/D5 dopamine receptors. J Physiol 593(16):3513–3532
Konieczny V, Tovey SC, Mataragka S, Prole DL, Taylor CW (2017) Cyclic AMP recruits a discrete intracellular Ca(2+) store by unmasking hypersensitive IP3 receptors. Cell Rep 18(3):711–722
Korzeniowski MK, Popovic MA, Szentpetery Z, Varnai P, Stojilkovic SS, Balla T (2009) Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem 284(31):21027–21035
Kostic M, Ludtmann MH, Bading H, Hershfinkel M, Steer E, Chu CT, Abramov AY, Sekler I (2015) PKA phosphorylation of NCLX reverses mitochondrial calcium overload and depolarization, promoting survival of PINK1-deficient dopaminergic neurons. Cell Rep 13(2):376–386
Krupinski J, Coussen F, Bakalyar HA, Tang WJ, Feinstein PG, Orth K, Slaughter C, Reed RR, Gilman AG (1989) Adenylyl cyclase amino acid sequence: possible channel- or transporter-like structure. Science 244(4912):1558–1564
Kumar S, Kostin S, Flacke JP, Reusch HP, Ladilov Y (2009) Soluble adenylyl cyclase controls mitochondria-dependent apoptosis in coronary endothelial cells. J Biol Chem 284(22):14760–14768
Kumar S, Appukuttan A, Maghnouj A, Hahn S, Peter Reusch H, Ladilov Y (2014) Suppression of soluble adenylyl cyclase protects smooth muscle cells against oxidative stress-induced apoptosis. Apoptosis 19(7):1069–1079
Kwan CY, Takemura H, Obie JF, Thastrup O, Putney JW Jr (1990) Effects of MeCh, thapsigargin, and La3+ on plasmalemmal and intracellular Ca2+ transport in lacrimal acinar cells. Am J Phys 258(6 Pt 1):C1006–C1015
Lai HL, Yang TH, Messing RO, Ching YH, Lin SC, Chern Y (1997) Protein kinase C inhibits adenylyl cyclase type VI activity during desensitization of the A2a-adenosine receptor-mediated cAMP response. J Biol Chem 272(8):4970–4977
Lefkimmiatis K, Srikanthan M, Maiellaro I, Moyer MP, Curci S, Hofer AM (2009) Store-operated cyclic AMP signalling mediated by STIM1. Nat Cell Biol 11(4):433–442
Li W, Zhang M, Xu L, Lin D, Cai S, Zou F (2013) The apoptosis of non-small cell lung cancer induced by cisplatin through modulation of STIM1. Exp Toxicol Pathol 65(7–8):1073–1081
Li C, Xie J, Lu Z, Chen C, Yin Y, Zhan R, Fang Y, Hu X, Zhang CC (2015) ADCY7 supports development of acute myeloid leukemia. Biochem Biophys Res Commun 465(1):47–52
Li Y, Baldwin TA, Wang Y, Subramaniam J, Carbajal AG, Brand CS, Cunha SR, Dessauer CW (2017) Loss of type 9 adenylyl cyclase triggers reduced phosphorylation of Hsp20 and diastolic dysfunction. Sci Rep 7(1):5522
Liauw J, Wu LJ, Zhuo M (2005) Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. J Neurophysiol 94(1):878–882
Lin FG, Cheng HF, Lee IF, Kao HJ, Loh SH, Lee WH (2001) Downregulation of phospholipase C delta3 by cAMP and calcium. Biochem Biophys Res Commun 286(2):274–280
Lin TH, Lai HL, Kao YY, Sun CN, Hwang MJ, Chern Y (2002) Protein kinase C inhibits type VI adenylyl cyclase by phosphorylating the regulatory N domain and two catalytic C1 and C2 domains. J Biol Chem 277(18):15721–15728
Linder JU, Schultz JE (2003) The class III adenylyl cyclases: multi-purpose signalling modules. Cell Signal 15(12):1081–1089
Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R (2007) CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr Biol 17(9):794–800
Litvin TN, Kamenetsky M, Zarifyan A, Buck J, Levin LR (2003) Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278(18):15922–15926
Liu L, Gritz D, Parent CA (2014) PKCbetaII acts downstream of chemoattractant receptors and mTORC2 to regulate cAMP production and myosin II activity in neutrophils. Mol Biol Cell 25(9):1446–1457
Liu B, Yu HH, Ye HL, Luo ZY, Xiao F (2015) Effects of stromal interacting molecule 1 gene silencing by short hairpin RNA on the biological behavior of human gastric cancer cells. Mol Med Rep 12(2):3047–3054
Liu X, Wu G, Yu Y, Chen X, Ji R, Lu J, Li X, Zhang X, Yang X, Shen Y (2019) Molecular understanding of calcium permeation through the open Orai channel. PLoS Biol 17(4):e3000096
Lopez JJ, Jardin I, Sanchez-Collado J, Salido GM, Smani T, Rosado JA (2020) TRPC channels in the SOCE scenario. Cell 9(1)
Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454(7203):538–542
Ma J, Hou X, Li M, Ren H, Fang S, Wang X, He C (2015) Genome-wide methylation profiling reveals new biomarkers for prognosis prediction of glioblastoma. J Cancer Res Ther 11(Suppl 2):C212–C215
Magro CM, Crowson AN, Desman G, Zippin JH (2012) Soluble adenylyl cyclase antibody profile as a diagnostic adjunct in the assessment of pigmented lesions. Arch Dermatol 148(3):335–344
Marsden AN, Dessauer CW (2019) Nanometric targeting of type 9 adenylyl cyclase in heart. Biochem Soc Trans 47(6):1749–1756
Martin AC, Cooper DM (2006) Capacitative and 1-oleyl-2-acetyl-sn-glycerol-activated Ca(2+) entry distinguished using adenylyl cyclase type 8. Mol Pharmacol 70(2):769–777
Martin AC, Willoughby D, Ciruela A, Ayling LJ, Pagano M, Wachten S, Tengholm A, Cooper DM (2009) Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol Pharmacol 75(4):830–842
Masada N, Ciruela A, Macdougall DA, Cooper DM (2009) Distinct mechanisms of regulation by Ca2+/calmodulin of type 1 and 8 adenylyl cyclases support their different physiological roles. J Biol Chem 284(7):4451–4463
Masada N, Schaks S, Jackson SE, Sinz A, Cooper DM (2012) Distinct mechanisms of calmodulin binding and regulation of adenylyl cyclases 1 and 8. Biochemistry 51(40):7917–7929
Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW Jr (2006) Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem 281(34):24979–24990
Michailidis IE, Zhang Y, Yang J (2007) The lipid connection-regulation of voltage-gated Ca(2+) channels by phosphoinositides. Pflugers Arch 455(1):147–155
Michel LYM, Verkaart S, Latta F, Hoenderop JGJ, Bindels RJM (2017) Differential regulation of the Na(+)-Ca(2+) exchanger 3 (NCX3) by protein kinase PKC and PKA. Cell Calcium 65:52–62
Miederer AM, Alansary D, Schwar G, Lee PH, Jung M, Helms V, Niemeyer BA (2015) A STIM2 splice variant negatively regulates store-operated calcium entry. Nat Commun 6:6899
Mignen O, Thompson JL, Shuttleworth TJ (2007) STIM1 regulates Ca2+ entry via arachidonate-regulated Ca2+-selective (ARC) channels without store depletion or translocation to the plasma membrane. J Physiol 579(Pt 3):703–715
Mignen O, Thompson JL, Shuttleworth TJ (2008) Both Orai1 and Orai3 are essential components of the arachidonate-regulated Ca2+-selective (ARC) channels. J Physiol 586(1):185–195
Motiani RK, Abdullaev IF, Trebak M (2010) A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells. J Biol Chem 285(25):19173–19183
Motiani RK, Tanwar J, Raja DA, Vashisht A, Khanna S, Sharma S, Srivastava S, Sivasubbu S, Natarajan VT, Gokhale RS (2018) STIM1 activation of adenylyl cyclase 6 connects Ca(2+) and cAMP signaling during melanogenesis. EMBO J 37(5)
Mou TC, Masada N, Cooper DM, Sprang SR (2009) Structural basis for inhibition of mammalian adenylyl cyclase by calcium. Biochemistry 48(15):3387–3397
Muik M, Fahrner M, Derler I, Schindl R, Bergsmann J, Frischauf I, Groschner K, Romanin C (2009) A cytosolic Homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels. J Biol Chem 284(13):8421–8426
Mullins FM, Lewis RS (2016) The inactivation domain of STIM1 is functionally coupled with the Orai1 pore to enable Ca2+-dependent inactivation. J Gen Physiol 147(2):153–164
Murphy JG, Sanderson JL, Gorski JA, Scott JD, Catterall WA, Sather WA, Dell'Acqua ML (2014) AKAP-anchored PKA maintains neuronal L-type calcium channel activity and NFAT transcriptional signaling. Cell Rep 7(5):1577–1588
Nalli AD, Kumar DP, Al-Shboul O, Mahavadi S, Kuemmerle JF, Grider JR, Murthy KS (2014) Regulation of Gbetagammai-dependent PLC-beta3 activity in smooth muscle: inhibitory phosphorylation of PLC-beta3 by PKA and PKG and stimulatory phosphorylation of Galphai-GTPase-activating protein RGS2 by PKG. Cell Biochem Biophys 70(2):867–880
Nelson EJ, Hellevuo K, Yoshimura M, Tabakoff B (2003) Ethanol-induced phosphorylation and potentiation of the activity of type 7 adenylyl cyclase. Involvement of protein kinase C delta. J Biol Chem 278(7):4552–4560
Oliveria SF, Dell'Acqua ML, Sather WA (2007) AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 55(2):261–275
Ong HL, de Souza LB, Ambudkar IS (2016) Role of TRPC channels in store-operated calcium entry. Adv Exp Med Biol 898:87–109
Onodera Y, Nam JM, Bissell MJ (2014) Increased sugar uptake promotes oncogenesis via EPAC/RAP1 and O-GlcNAc pathways. J Clin Invest 124(1):367–384
Ostrom RS, Naugle JE, Hase M, Gregorian C, Swaney JS, Insel PA, Brunton LL, Meszaros JG (2003) Angiotensin II enhances adenylyl cyclase signaling via Ca2+/calmodulin. Gq-Gs cross-talk regulates collagen production in cardiac fibroblasts. J Biol Chem 278(27):24461–24468
Pagano M, Clynes MA, Masada N, Ciruela A, Ayling LJ, Wachten S, Cooper DM (2009) Insights into the residence in lipid rafts of adenylyl cyclase AC8 and its regulation by capacitative calcium entry. Am J Physiol Cell Physiol 296(3):C607–C619
Palty R, Raveh A, Kaminsky I, Meller R, Reuveny E (2012) SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149(2):425–438
Palvolgyi A, Simpson J, Bodnar I, Biro J, Palkovits M, Radovits T, Skehel P, Antoni FA (2018) Auto-inhibition of adenylyl cyclase 9 (AC9) by an isoform-specific motif in the carboxyl-terminal region. Cell Signal 51:266–275
Parekh AB (1998) Slow feedback inhibition of calcium release-activated calcium current by calcium entry. J Biol Chem 273(24):14925–14932
Parekh AB (2017) Regulation of CRAC channels by Ca(2+)-dependent inactivation. Cell Calcium 63:20–23
Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136(5):876–890
Parker T, Wang KW, Manning D, Dart C (2019) Soluble adenylyl cyclase links Ca(2+) entry to Ca(2+)/cAMP-response element binding protein (CREB) activation in vascular smooth muscle. Sci Rep 9(1):7317
Patel TB, Du Z, Pierre S, Cartin L, Scholich K (2001) Molecular biological approaches to unravel adenylyl cyclase signaling and function. Gene 269(1–2):13–25
Piggott LA, Bauman AL, Scott JD, Dessauer CW (2008) The A-kinase anchoring protein Yotiao binds and regulates adenylyl cyclase in brain. Proc Natl Acad Sci U S A 105(37):13835–13840
Potenza DM, Janicek R, Fernandez-Tenorio M, Camors E, Ramos-Mondragon R, Valdivia HH, Niggli E (2019) Phosphorylation of the ryanodine receptor 2 at serine 2030 is required for a complete beta-adrenergic response. J Gen Physiol 151(2):131–145
Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443(7108):230–233
Price T, Brust TF (2019) Adenylyl cyclase 7 and neuropsychiatric disorders: a new target for depression? Pharmacol Res 143:106–112
Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7(1):1–12
Quinn SN, Graves SH, Dains-McGahee C, Friedman EM, Hassan H, Witkowski P, Sabbatini ME (2017) Adenylyl cyclase 3/adenylyl cyclase-associated protein 1 (CAP1) complex mediates the anti-migratory effect of forskolin in pancreatic cancer cells. Mol Carcinog 56(4):1344–1360
Ramos LS, Zippin JH, Kamenetsky M, Buck J, Levin LR (2008) Glucose and GLP-1 stimulate cAMP production via distinct adenylyl cyclases in INS-1E insulinoma cells. J Gen Physiol 132(3):329–338
Ramos-Espiritu L, Diaz A, Nardin C, Saviola AJ, Shaw F, Plitt T, Yang X, Wolchok J, Pirog EC, Desman G, Sboner A, Zhang T, Xiang J, Merghoub T, Levin LR, Buck J, Zippin JH (2016) The metabolic/pH sensor soluble adenylyl cyclase is a tumor suppressor protein. Oncotarget 7(29):45597–45607
Ramracheya R, Chapman C, Chibalina M, Dou H, Miranda C, Gonzalez A, Moritoh Y, Shigeto M, Zhang Q, Braun M, Clark A, Johnson PR, Rorsman P, Briant LJB (2018) GLP-1 suppresses glucagon secretion in human pancreatic alpha-cells by inhibition of P/Q-type Ca(2+) channels. Physiol Rep 6(17):e13852
Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, Nau C, Kress M (2002) PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22(11):4740–4745
Raymond LA, Blackstone CD, Huganir RL (1993) Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361(6413):637–641
Rieg T, Kohan DE (2014) Regulation of nephron water and electrolyte transport by adenylyl cyclases. Am J Physiol Renal Physiol 306(7):F701–F709
Roberts CD, Dvoryanchikov G, Roper SD, Chaudhari N (2009) Interaction between the second messengers cAMP and Ca2+ in mouse presynaptic taste cells. J Physiol 587(Pt 8):1657–1668
Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169(3):435–445
Rosado JA, Porras T, Conde M, Sage SO (2001) Cyclic nucleotides modulate store-mediated calcium entry through the activation of protein-tyrosine phosphatases and altered actin polymerization in human platelets. J Biol Chem 276(19):15666–15675
Ruiz-Hurtado G, Morel E, Dominguez-Rodriguez A, Llach A, Lezoualc'h F, Benitah JP, Gomez AM (2013) Epac in cardiac calcium signaling. J Mol Cell Cardiol 58:162–171
Sadana R, Dessauer CW (2009) Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 17(1):5–22
Sanchez-Collado J, Lopez JJ, Jardin I, Camello PJ, Falcon D, Regodon S, Salido GM, Smani T, Rosado JA (2019) Adenylyl cyclase type 8 overexpression impairs phosphorylation-dependent Orai1 inactivation and promotes migration in MDA-MB-231 breast cancer cells. Cancers (Basel) 11(11)
Schirmer I, Bualeong T, Budde H, Cimiotti D, Appukuttan A, Klein N, Steinwascher P, Reusch P, Mugge A, Meyer R, Ladilov Y, Jaquet K (2018) Soluble adenylyl cyclase: a novel player in cardiac hypertrophy induced by isoprenaline or pressure overload. PLoS One 13(2):e0192322
Schmidt M, Evellin S, Weernink PA, von Dorp F, Rehmann H, Lomasney JW, Jakobs KH (2001) A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a rap GTPase. Nat Cell Biol 3(11):1020–1024
Sculptoreanu A, Rotman E, Takahashi M, Scheuer T, Catterall WA (1993) Voltage-dependent potentiation of the activity of cardiac L-type calcium channel alpha 1 subunits due to phosphorylation by cAMP-dependent protein kinase. Proc Natl Acad Sci U S A 90(21):10135–10139
Shen JX, Wachten S, Halls ML, Everett KL, Cooper DM (2012) Muscarinic receptors stimulate AC2 by novel phosphorylation sites, whereas Gbetagamma subunits exert opposing effects depending on the G-protein source. Biochem J 447(3):393–405
Shuttleworth TJ, Thompson JL (1999) Discriminating between capacitative and arachidonate-activated Ca(2+) entry pathways in HEK293 cells. J Biol Chem 274(44):31174–31178
Simko V, Iuliano F, Sevcikova A, Labudova M, Barathova M, Radvak P, Pastorekova S, Pastorek J, Csaderova L (2017) Hypoxia induces cancer-associated cAMP/PKA signalling through HIF-mediated transcriptional control of adenylyl cyclases VI and VII. Sci Rep 7(1):10121
Simpson RE, Ciruela A, Cooper DM (2006) The role of calmodulin recruitment in Ca2+ stimulation of adenylyl cyclase type 8. J Biol Chem 281(25):17379–17389
Singhmar P, Huo X, Eijkelkamp N, Berciano SR, Baameur F, Mei FC, Zhu Y, Cheng X, Hawke D, Mayor F Jr, Murga C, Heijnen CJ, Kavelaars A (2016) Critical role for Epac1 in inflammatory pain controlled by GRK2-mediated phosphorylation of Epac1. Proc Natl Acad Sci U S A 113(11):3036–3041
Smit MJ, Iyengar R (1998) Mammalian adenylyl cyclases. Adv Second Messenger Phosphoprotein Res 32:1–21
Smith KE, Gu C, Fagan KA, Hu B, Cooper DM (2002) Residence of adenylyl cyclase type 8 in caveolae is necessary but not sufficient for regulation by capacitative Ca(2+) entry. J Biol Chem 277(8):6025–6031
Sobradillo D, Hernandez-Morales M, Ubierna D, Moyer MP, Nunez L, Villalobos C (2014) A reciprocal shift in transient receptor potential channel 1 (TRPC1) and stromal interaction molecule 2 (STIM2) contributes to Ca2+ remodeling and cancer hallmarks in colorectal carcinoma cells. J Biol Chem 289(42):28765–28782
Soulsby MD, Wojcikiewicz RJ (2007) Calcium mobilization via type III inositol 1,4,5-trisphosphate receptors is not altered by PKA-mediated phosphorylation of serines 916, 934, and 1832. Cell Calcium 42(3):261–270
Soulsby MD, Alzayady K, Xu Q, Wojcikiewicz RJ (2004) The contribution of serine residues 1588 and 1755 to phosphorylation of the type I inositol 1,4,5-trisphosphate receptor by PKA and PKG. FEBS Lett 557(1–3):181–184
Spirli C, Mariotti V, Villani A, Fabris L, Fiorotto R, Strazzabosco M (2017) Adenylyl cyclase 5 links changes in calcium homeostasis to cAMP-dependent cyst growth in polycystic liver disease. J Hepatol 66(3):571–580
Srikanth S, Jung HJ, Ribalet B, Gwack Y (2010) The intracellular loop of Orai1 plays a central role in fast inactivation of Ca2+ release-activated Ca2+ channels. J Biol Chem 285(7):5066–5075
Stathopulos PB, Schindl R, Fahrner M, Zheng L, Gasmi-Seabrook GM, Muik M, Romanin C, Ikura M (2013) STIM1/Orai1 coiled-coil interplay in the regulation of store-operated calcium entry. Nat Commun 4:2963
Steegborn C (2014) Structure, mechanism, and regulation of soluble adenylyl cyclases - similarities and differences to transmembrane adenylyl cyclases. Biochim Biophys Acta 1842(12 Pt B):2535–2547
Steegborn C, Litvin TN, Levin LR, Buck J, Wu H (2005) Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat Struct Mol Biol 12(1):32–37
Steiner D, Saya D, Schallmach E, Simonds WF, Vogel Z (2006) Adenylyl cyclase type-VIII activity is regulated by G(betagamma) subunits. Cell Signal 18(1):62–68
Stokes AJ, Shimoda LM, Koblan-Huberson M, Adra CN, Turner H (2004a) A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 200(2):137–147
Stokes L, Gordon J, Grafton G (2004b) Non-voltage-gated L-type Ca2+ channels in human T cells: pharmacology and molecular characterization of the major alpha pore-forming and auxiliary beta-subunits. J Biol Chem 279(19):19566–19573
Streb H, Irvine RF, Berridge MJ, Schulz I (1983) Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306(5938):67–69
Syed AU, Reddy GR, Ghosh D, Prada MP, Nystoriak MA, Morotti S, Grandi E, Sirish P, Chiamvimonvat N, Hell JW, Santana LF, Xiang YK, Nieves-Cintron M, Navedo MF (2019) Adenylyl cyclase 5-generated cAMP controls cerebral vascular reactivity during diabetic hyperglycemia. J Clin Invest 129(8):3140–3152
Takezawa R, Schmitz C, Demeuse P, Scharenberg AM, Penner R, Fleig A (2004) Receptor-mediated regulation of the TRPM7 channel through its endogenous protein kinase domain. Proc Natl Acad Sci U S A 101(16):6009–6014
Tang WJ, Gilman AG (1991) Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. Science 254(5037):1500–1503
Taussig R, Tang WJ, Hepler JR, Gilman AG (1994) Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases. J Biol Chem 269(8):6093–6100
Taylor CW (2017) Regulation of IP3 receptors by cyclic AMP. Cell Calcium 63:48–52
Taylor SS, Buechler JA, Yonemoto W (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59:971–1005
Tesmer JJ, Sunahara RK, Johnson RA, Gosselin G, Gilman AG, Sprang SR (1999) Two-metal-ion catalysis in adenylyl cyclase. Science 285(5428):756–760
Thangavel M, Liu X, Sun SQ, Kaminsky J, Ostrom RS (2009) The C1 and C2 domains target human type 6 adenylyl cyclase to lipid rafts and caveolae. Cell Signal 21(2):301–308
Thompson JL, Shuttleworth TJ (2015) Anchoring protein AKAP79-mediated PKA phosphorylation of STIM1 determines selective activation of the ARC channel, a store-independent Orai channel. J Physiol 593(3):559–572
Tian Y, Yang T, Yu S, Liu C, He M, Hu C (2018) Prostaglandin E2 increases migration and proliferation of human glioblastoma cells by activating transient receptor potential melastatin 7 channels. J Cell Mol Med 22(12):6327–6337
Tong T, Shen Y, Lee HW, Yu R, Park T (2016) Adenylyl cyclase 3 haploinsufficiency confers susceptibility to diet-induced obesity and insulin resistance in mice. Sci Rep 6:34179
Tovey SC, Dedos SG, Rahman T, Taylor EJ, Pantazaka E, Taylor CW (2010) Regulation of inositol 1,4,5-trisphosphate receptors by cAMP independent of cAMP-dependent protein kinase. J Biol Chem 285(17):12979–12989
Umemura M, Baljinnyam E, Feske S, De Lorenzo MS, Xie LH, Feng X, Oda K, Makino A, Fujita T, Yokoyama U, Iwatsubo M, Chen S, Goydos JS, Ishikawa Y, Iwatsubo K (2014) Store-operated Ca2+ entry (SOCE) regulates melanoma proliferation and cell migration. PLoS One 9(2):e89292
Vaeth M, Yang J, Yamashita M, Zee I, Eckstein M, Knosp C, Kaufmann U, Karoly Jani P, Lacruz RS, Flockerzi V, Kacskovics I, Prakriya M, Feske S (2017) ORAI2 modulates store-operated calcium entry and T cell-mediated immunity. Nat Commun 8:14714
Vatner SF, Park M, Yan L, Lee GJ, Lai L, Iwatsubo K, Ishikawa Y, Pessin J, Vatner DE (2013) Adenylyl cyclase type 5 in cardiac disease, metabolism, and aging. Am J Physiol Heart Circ Physiol 305(1):H1–H8
Venkatachalam K, Zheng F, Gill DL (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 278(31):29031–29040
Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312(5777):1220–1223
Vorherr T, Knopfel L, Hofmann F, Mollner S, Pfeuffer T, Carafoli E (1993) The calmodulin binding domain of nitric oxide synthase and adenylyl cyclase. Biochemistry 32(23):6081–6088
Wagner S, Storbeck CJ, Roovers K, Chaar ZY, Kolodziej P, McKay M, Sabourin LA (2008) FAK/src-family dependent activation of the Ste20-like kinase SLK is required for microtubule-dependent focal adhesion turnover and cell migration. PLoS One 3(4):e1868
Wang Z, Balet Sindreu C, Li V, Nudelman A, Chan GC, Storm DR (2006) Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J Neurosci 26(28):7375–7379
Wang C, Gu Y, Li GW, Huang LY (2007) A critical role of the cAMP sensor Epac in switching protein kinase signalling in prostaglandin E2-induced potentiation of P2X3 receptor currents in inflamed rats. J Physiol 584(Pt 1):191–203
Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD, Gill DL (2010) The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330(6000):105–109
Watson EL, Wu Z, Jacobson KL, Storm DR, Singh JC, Ott SM (1998) Capacitative Ca2+ entry is involved in cAMP synthesis in mouse parotid acini. Am J Phys 274(3):C557–C565
Wayman GA, Wei J, Wong S, Storm DR (1996) Regulation of type I adenylyl cyclase by calmodulin kinase IV in vivo. Mol Cell Biol 16(11):6075–6082
Webb BL, Hirst SJ, Giembycz MA (2000) Protein kinase C isoenzymes: a review of their structure, regulation and role in regulating airways smooth muscle tone and mitogenesis. Br J Pharmacol 130(7):1433–1452
Wecker L, Rogers CQ (2003) Phosphorylation sites within alpha4 subunits of alpha4beta2 neuronal nicotinic receptors: a comparison of substrate specificities for cAMP-dependent protein kinase (PKA) and protein kinase C (PKC). Neurochem Res 28(3–4):431–436
Wei J, Wayman G, Storm DR (1996) Phosphorylation and inhibition of type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo. J Biol Chem 271(39):24231–24235
Wei J, Zhao AZ, Chan GC, Baker LP, Impey S, Beavo JA, Storm DR (1998) Phosphorylation and inhibition of olfactory adenylyl cyclase by CaM kinase II in neurons: a mechanism for attenuation of olfactory signals. Neuron 21(3):495–504
Wieczorek L, Majumdar D, Wills TA, Hu L, Winder DG, Webb DJ, Muglia LJ (2012) Absence of Ca2+-stimulated adenylyl cyclases leads to reduced synaptic plasticity and impaired experience-dependent fear memory. Transl Psychiatry 2:e126
Willoughby D, Cooper DM (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87(3):965–1010
Willoughby D, Masada N, Wachten S, Pagano M, Halls ML, Everett KL, Ciruela A, Cooper DM (2010) AKAP79/150 interacts with AC8 and regulates Ca2+−dependent cAMP synthesis in pancreatic and neuronal systems. J Biol Chem 285(26):20328–20342
Willoughby D, Everett KL, Halls ML, Pacheco J, Skroblin P, Vaca L, Klussmann E, Cooper DM (2012) Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Sci Signal 5(219):ra29
Willoughby D, Ong HL, De Souza LB, Wachten S, Ambudkar IS, Cooper DM (2014) TRPC1 contributes to the Ca2+-dependent regulation of adenylate cyclases. Biochem J 464(1):73–84
Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27(3):487–497
Worley PF, Zeng W, Huang GN, Yuan JP, Kim JY, Lee MG, Muallem S (2007) TRPC channels as STIM1-regulated store-operated channels. Cell Calcium 42(2):205–211
Wu MM, Covington ED, Lewis RS (2014) Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at endoplasmic reticulum-plasma membrane junctions. Mol Biol Cell 25(22):3672–3685
Xiao R, Xu XZ (2010) Mechanosensitive channels: in touch with Piezo. Curr Biol 20(21):R936–R938
Xu J, Han Q, Shi H, Liu W, Chu T, Li H (2017) Role of PKA in the process of neonatal cardiomyocyte hypertrophy induced by urotensin II. Int J Mol Med 40(2):499–504
Yamashita M, Yeung PS, Ing CE, McNally BA, Pomes R, Prakriya M (2017) STIM1 activates CRAC channels through rotation of the pore helix to open a hydrophobic gate. Nat Commun 8:14512
Yang N, Tang Y, Wang F, Zhang H, Xu D, Shen Y, Sun S, Yang G (2013) Blockade of store-operated Ca(2+) entry inhibits hepatocarcinoma cell migration and invasion by regulating focal adhesion turnover. Cancer Lett 330(2):163–169
Yao X, Kwan HY, Huang Y (2005) Regulation of TRP channels by phosphorylation. Neurosignals 14(6):273–280
Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443(7108):226–229
Yi H, Wang K, Jin JF, Jin H, Yang L, Zou Y, Du B, Liu X (2018) Elevated adenylyl cyclase 9 expression is a potential prognostic biomarker for patients with colon cancer. Med Sci Monit 24:19–25
Yoast RE, Emrich SM, Zhang X, Xin P, Johnson MT, Fike AJ, Walter V, Hempel N, Yule DI, Sneyd J, Gill DL, Trebak M (2020) The native ORAI channel trio underlies the diversity of Ca(2+) signaling events. Nat Commun 11(1):2444
Yoshimaru T, Suzuki Y, Inoue T, Ra C (2009) L-type Ca2+ channels in mast cells: activation by membrane depolarization and distinct roles in regulating mediator release from store-operated Ca2+ channels. Mol Immunol 46(7):1267–1277
Yoshimura M, Cooper DM (1992) Cloning and expression of a Ca(2+)-inhibitable adenylyl cyclase from NCB-20 cells. Proc Natl Acad Sci U S A 89(15):6716–6720
Yu F, Sun L, Machaca K (2010) Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis. J Cell Biol 191(3):523–535
Yu T, Wang Y, Qian D, Sun X, Tang Y, Shen X, Lin L (2017) Advanced glycation end products impair Ca2+ mobilization and sensitization in colonic smooth muscle cells via the CAMP/PKA pathway. Cell Physiol Biochem 43(4):1571–1587
Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11(3):337–343
Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437(7060):902–905
Zhang M, Storm DR, Wang H (2011) Bidirectional synaptic plasticity and spatial memory flexibility require Ca2+−stimulated adenylyl cyclases. J Neurosci 31(28):10174–10183
Zhang H, Ghai P, Wu H, Wang C, Field J, Zhou GL (2013) Mammalian adenylyl cyclase-associated protein 1 (CAP1) regulates cofilin function, the actin cytoskeleton, and cell adhesion. J Biol Chem 288(29):20966–20977
Zhang X, Pathak T, Yoast R, Emrich S, Xin P, Nwokonko RM, Johnson M, Wu S, Delierneux C, Gueguinou M, Hempel N, Putney JW Jr, Gill DL, Trebak M (2019) A calcium/cAMP signaling loop at the ORAI1 mouth drives channel inactivation to shape NFAT induction. Nat Commun 10(1):1971
Zheng S, Zhou L, Ma G, Zhang T, Liu J, Li J, Nguyen NT, Zhang X, Li W, Nwokonko R, Zhou Y, Zhao F, Huang Y, Gill DL, Wang Y (2018) Calcium store refilling and STIM activation in STIM- and Orai-deficient cell lines. Pflugers Arch 470(10):1555–1567
Zhou Y, Mancarella S, Wang Y, Yue C, Ritchie M, Gill DL, Soboloff J (2009) The short N-terminal domains of STIM1 and STIM2 control the activation kinetics of Orai1 channels. J Biol Chem 284(29):19164–19168
Zimmermann G, Taussig R (1996) Protein kinase C alters the responsiveness of adenylyl cyclases to G protein alpha and betagamma subunits. J Biol Chem 271(43):27161–27166
Zippin JH, Chadwick PA, Levin LR, Buck J, Magro CM (2010) Soluble adenylyl cyclase defines a nuclear cAMP microdomain in keratinocyte hyperproliferative skin diseases. J Invest Dermatol 130(5):1279–1287
Zou T, Liu J, She L, Chen J, Zhu T, Yin J, Li X, Zhou H, Liu Z (2019) A perspective profile of ADCY1 in cAMP signaling with drug-resistance in lung cancer. J Cancer 10(27):6848–6857
Zweifach A, Lewis RS (1995a) Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105(2):209–226
Zweifach A, Lewis RS (1995b) Slow calcium-dependent inactivation of depletion-activated calcium current. Store-dependent and -independent mechanisms. J Biol Chem 270(24):14445–14451
Acknowledgements
This work was supported by MINECO (Grant BFU2016-74932-C2-1-P and PID2019-104084GB-C21) and Junta de Extremadura-Consejería de Economía e Infraestructura-FEDER (Fondo Europeo de Desarrollo Regional, Grants IB16046 and GR18061). We also thank Fundación Caja de Extremadura for its support. J.J.L. and I.J. are supported by a contract from Junta de Extremadura (TA18011 and TA18054, respectively). J.S.-C. is supported by a contract from Ministry of Science, Innovation, and Universities, Spain.
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Sanchez-Collado, J., Lopez, J.J., Jardin, I., Salido, G.M., Rosado, J.A. (2020). Cross-Talk Between the Adenylyl Cyclase/cAMP Pathway and Ca2+ Homeostasis. In: Pedersen, S.H.F. (eds) Reviews of Physiology, Biochemistry and Pharmacology. Reviews of Physiology, Biochemistry and Pharmacology, vol 179. Springer, Cham. https://doi.org/10.1007/112_2020_55
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