The Emerging Roles of CIB1 in Cancer

Cellular Physiology and Biochemistry

Volumn 43, Issue 4, 2017, Pages 1413-1424

  Wang, Xianwang ^a,b   Peng, Xiaochun ^a   Zhang, Xueqing ^b   Xu, Hanyi ^a   Lu, Chengbiao ^b   Liu, Lian ^a   Song, Jiaxing ^c   Zhang, Yingjie ^d  

^a JINGZHOU CENTRAL HOSPITAL   (China)

^b YANGTZE UNIVERSITY   (China)

^c Shenzhen University School of Medicine   (China)

^d HUNAN UNIVERSITY   (China)

Author keywords

Calcium; Cancer; CIB1; Integrin; Tumor progression

Indexed keywords

CALCINEURIN; CALCIUM AND INTEGRIN BINDING PROTEIN 1; CALCIUM BINDING PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INTEGRIN; UNCLASSIFIED DRUG; CIB1 PROTEIN, HUMAN;

ACUTE MYELOID LEUKEMIA; ANGIOGENESIS; APOPTOSIS; BLADDER CANCER; CALCIUM SIGNALING; CARCINOGENESIS; CELL CYCLE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL CANCER; HUMAN; KAPOSI SARCOMA; LIVER CELL CARCINOMA; LUNG CANCER; MALIGNANT NEOPLASM; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; TUMOR GROWTH; UTERINE CERVIX CANCER; VIRUS INFECTION; ANIMAL; CELL MOTION; DISEASE EXACERBATION; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELL MOVEMENT; DISEASE PROGRESSION; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 85031429473     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000481873     Document Type: Review

References (80)

1. Naik UP, Patel PM, Parise LV: Identification of a novel calcium-binding protein that interacts with the integrin alphaIIb cytoplasmic domain. J Biol Chem 1997; 272: 4651-4654.
2. Yuan W, Leisner TM, McFadden AW, Wang Z, Larson MK, Clark S, Boudignon-Proudhon C, Lam SC, Parise LV: CIB1 is an endogenous inhibitor of agonist-induced integrin alphaIIbbeta3 activation. J Cell Biol 2006; 172: 169-175.
3. Freeman TC, Jr., Black JL, Bray HG, Dagliyan O, Wu YI, Tripathy A, Dokholyan NV, Leisner TM, Parise LV: Identification of novel integrin binding partners for calcium and integrin binding protein 1 (CIB1): structural and thermodynamic basis of CIB1 promiscuity. Biochemistry 2013; 52: 7082-7090.
4. Hennigs JK, Burhenne N, Stahler F, Winnig M, Walter B, Meyerhof W, Schmale H: Sweet taste receptor interacting protein CIB1 is a general inhibitor of InsP3-dependent Ca2+ release in vivo. J Neurochem 2008; 106: 2249-2262.
5. Rusnak F, Mertz P: Calcineurin: form and function. Physiol Rev 2000; 80: 1483-1521.
6. Gentry HR, Singer AU, Betts L, Yang C, Ferrara JD, Sondek J, Parise LV: Structural and biochemical characterization of CIB1 delineates a new family of EF-hand-containing proteins. J Biol Chem 2005; 280: 8407-8415.
7. Leisner TM, Freeman TC, Black JL, Parise LV: CIB1: a small protein with big ambitions. FASEB J 2016; 30: 2640-2650.
8. Huang H, Ishida H, Yamniuk AP, Vogel HJ: Solution structures of Ca2+-CIB1 and Mg2+-CIB1 and their interactions with the platelet integrin alphaIIb cytoplasmic domain. J Biol Chem 2011; 286: 17181-17192.
9. Gifford JL, Walsh MP, Vogel HJ: Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 2007; 405: 199-221.
10. Yamniuk AP, Anderson KL, Fraser ME, Vogel HJ: Auxiliary Ca2+ binding sites can influence the structure of CIB1. Protein Sci 2009; 18: 1128-1134.
11. Yamniuk AP, Nguyen LT, Hoang TT, Vogel HJ: Metal ion binding properties and conformational states of calcium-and integrin-binding protein. Biochemistry 2004; 43: 2558-2568.
12. Sobczak A, Blazejczyk M, Piszczek G, Zhao G, Kuznicki J, Wojda U: Calcium-binding calmyrin forms stable covalent dimers in vitro, but in vivo is found in monomeric form. Acta Biochim Pol 2005; 52: 469-476.
13. Stabler SM, Ostrowski LL, Janicki SM, Monteiro MJ: A myristoylated calcium-binding protein that preferentially interacts with the Alzheimer's disease presenilin 2 protein. J Cell Biol 1999; 145: 1277-1292.
14. Zhu J, Stabler SM, Ames JB, Baskakov I, Monteiro MJ: Calcium binding sequences in calmyrin regulates interaction with presenilin-2. Exp Cell Res 2004; 300: 440-454.
15. Jarman KE, Moretti PA, Zebol JR, Pitson SM: Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium-and integrin-binding protein 1. J Biol Chem 2010; 285: 483-492.
16. Heineke J, Auger-Messier M, Correll RN, Xu J, Benard MJ, Yuan W, Drexler H, Parise LV, Molkentin JD: CIB1 is a regulator of pathological cardiac hypertrophy. Nat Med 2010; 16: 872-879.
17. Zhu W, Gliddon BL, Jarman KE, Moretti PAB, Tin T, Parise LV, Woodcock JM, Powell JA, Ruszkiewicz A, Pitman MR, Pitson SM: CIB1 contributes to oncogenic signalling by Ras via modulating the subcellular localisation of sphingosine kinase 1. Oncogene 2017; 36: 2619-2627.
18. Tahara E, Jr., Tahara H, Kanno M, Naka K, Takeda Y, Matsuzaki T, Yamazaki R, Ishihara H, Yasui W, Barrett JC, Ide T, Tahara E: G1P3, an interferon inducible gene 6-16, is expressed in gastric cancers and inhibits mitochondrial-mediated apoptosis in gastric cancer cell line TMK-1 cell. Cancer Immunol Immunother 2005; 54: 729-740.
19. Yuan W, Leisner TM, McFadden AW, Clark S, Hiller S, Maeda N, O'Brien DA, Parise LV: CIB1 is essential for mouse spermatogenesis. Mol Cell Biol 2006; 26: 8507-8514.
20. Naik MU, Pham NT, Beebe K, Dai W, Naik UP: Calcium-dependent inhibition of polo-like kinase 3 activity by CIB1 in breast cancer cells. Int J Cancer 2011; 128: 587-596.
21. Nagayoshi Y, Nakamura M, Matsuoka K, Ohtsuka T, Mori Y, Kono H, Aso T, Ideno N, Takahata S, Ryo A, Takeda H, Ito T, Oda Y, Endo Y, Sawasaki T, Tanaka M: Profiling of autoantibodies in sera of pancreatic cancer patients. Ann Surg Oncol 2014; 21:S459-465.
22. Blazejczyk M, Wojda U, Sobczak A, Spilker C, Bernstein HG, Gundelfinger ED, Kreutz MR, Kuznicki J: Ca2+-independent binding and cellular expression profiles question a significant role of calmyrin in transduction of Ca2+-signals to Alzheimer's disease-related presenilin 2 in forebrain. Biochim Biophys Acta 2006; 1762: 66-72.
23. Bernstein HG, Blazejczyk M, Rudka T, Gundelfinger ED, Dobrowolny H, Bogerts B, Kreutz MR, Kuznicki J, Wojda U: The Alzheimer disease-related calcium-binding protein Calmyrin is present in human forebrain with an altered distribution in Alzheimer's as compared to normal ageing brains. Neuropathol Appl Neurobiol 2005; 31: 314-324.
24. Fang X, Chen C, Wang Q, Gu J, Chi C: The interaction of the calcium-and integrin-binding protein (CIBP) with the coagulation factor VIII. Thromb Res 2001; 102: 177-185.
25. Guse AH, Lee HC: NAADP: a universal Ca2+ trigger. Sci Signal 2008; 1:re10.
26. Zhang F, Jin S, Yi F, Li PL: TRP-ML1 functions as a lysosomal NAADP-sensitive Ca2+release channel in coronary arterial myocytes. J Cell Mol Med 2009; 13: 3174-3185.
27. Wang X, Song J, Wu Z, Fan B, Mode X: Dual Roles of CD38 in Autophagy. Yangtze Medicine 2017; 01: 8-19.
28. Gerasimenko JV, Charlesworth RM, Sherwood MW, Ferdek PE, Mikoshiba K, Parrington J, Petersen OH, Gerasimenko OV: Both RyRs and TPCs are required for NAADP-induced intracellular Ca(2)(+) release. Cell Calcium 2015; 58: 237-245.
29. Zhu S, Xu T, Luo Y, Zhang Y, Xuan H, Ma Y, Pan D, Li D, Zhu H: Luteolin Enhances Sarcoplasmic Reticulum Ca2+-ATPase Activity through p38 MAPK Signaling thus Improving Rat Cardiac Function after Ischemia/ Reperfusion. Cell Physiol Biochem 2017; 41: 999-1010.
30. Frost RJ, Olson EN: Separating the good and evil of cardiac growth by CIB1 and calcineurin. Cell Metab 2010; 12: 205-206.
31. Tandan S, Wang Y, Wang TT, Jiang N, Hall DD, Hell JW, Luo X, Rothermel BA, Hill JA: Physical and functional interaction between calcineurin and the cardiac L-type Ca2+ channel. Circ Res 2009; 105: 51-60.
32. White C, Yang J, Monteiro MJ, Foskett JK: CIB1, a ubiquitously expressed Ca2+-binding protein ligand of the InsP3 receptor Ca2+ release channel. J Biol Chem 2006; 281: 20825-20833.
33. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, Parkhouse RM, Walseth TF, Lee HC: Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 1993; 262: 1056-1059.
34. Aarhus R, Graeff RM, Dickey DM, Walseth TF, Lee HC: ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J Biol Chem 1995; 270: 30327-30333.
35. Cui C, Merritt R, Fu L, Pan Z: Targeting calcium signaling in cancer therapy. Acta Pharm Sin B 2017; 7: 3-17.
36. Zhang Y, Zhang T, Wu C, Xia Q, Xu D: ASIC1a mediates the drug resistance of human hepatocellular carcinoma via the Ca2+/PI3-kinase/AKT signaling pathway. Lab Invest 2017; 97: 53-69.
37. Davis FM, Azimi I, Faville RA, Peters AA, Jalink K, Putney JW, Jr., Goodhill GJ, Thompson EW, Roberts-Thomson SJ, Monteith GR: Induction of epithelial-mesenchymal transition (EMT) in breast cancer cells is calcium signal dependent. Oncogene 2014; 33: 2307-2316.
38. Azimi I, Roberts-Thomson SJ, Monteith GR: Calcium influx pathways in breast cancer: opportunities for pharmacological intervention. Br J Pharmacol 2014; 171: 945-960.
39. Kauselmann G, Weiler M, Wulff P, Jessberger S, Konietzko U, Scafidi J, Staubli U, Bereiter-Hahn J, Strebhardt K, Kuhl D: The polo-like protein kinases Fnk and Snk associate with a Ca(2+)-and integrin-binding protein and are regulated dynamically with synaptic plasticity. EMBO J 1999; 18: 5528-5539.
40. Armacki M, Joodi G, Nimmagadda SC, de Kimpe L, Pusapati GV, Vandoninck S, Van Lint J, Illing A, Seufferlein T: A novel splice variant of calcium and integrin-binding protein 1 mediates protein kinase D2-stimulated tumour growth by regulating angiogenesis. Oncogene 2014; 33: 1167-1180.
41. Black JL, Harrell JC, Leisner TM, Fellmeth MJ, George SD, Reinhold D, Baker NM, Jones CD, Der CJ, Perou CM, Parise LV: CIB1 depletion impairs cell survival and tumor growth in triple-negative breast cancer. Breast Cancer Res Treat 2015; 152: 337-346.
42. Tong JR, Zhou HC, He F, Gao Y, Yang XQ, Luo ZM, Zhang H, Zeng JY, Wang Y, Huang YH, Zhang JL, Sun LH, He GL: Proteomic identification of CIB1 as a potential diagnostic factor in hepatocellular carcinoma. J Biosciences 2011; 36: 659-668.
43. Leisner TM, Moran C, Holly SP, Parise LV: CIB1 prevents nuclear GAPDH accumulation and non-apoptotic tumor cell death via AKT and ERK signaling. Oncogene 2013; 32: 4017-4027.
44. Naik MU, Naik UP: Calcium-and integrin-binding protein 1 regulates microtubule organization and centrosome segregation through polo like kinase 3 during cell cycle progression. Int J Biochem Cell Biol 2011; 43: 120-129.
45. Ma S, Liu MA, Yuan YL, Erikson RL: The serum-inducible protein kinase Snk is a G1 phase polo-like kinase that is inhibited by the calcium-and integrin-binding protein CIB. Mol Cancer Res 2003; 1: 376-384.
46. Holtrich U, Wolf G, Yuan J, Bereiter-Hahn J, Karn T, Weiler M, Kauselmann G, Rehli M, Andreesen R, Kaufmann M, Kuhl D, Strebhardt K: Adhesion induced expression of the serine/threonine kinase Fnk in human macrophages. Oncogene 2000; 19: 4832-4839.
47. Hao Q, Wang L, Zhao ZJ, Tang H: Identification of protein kinase D2 as a pivotal regulator of endothelial cell proliferation, migration, and angiogenesis. J Biol Chem 2009; 284: 799-806.
48. Xia P, Gamble JR, Wang L, Pitson SM, Moretti PA, Wattenberg BW, D'Andrea RJ, Vadas MA: An oncogenic role of sphingosine kinase. Curr Biol 2000; 10: 1527-1530.
49. Pitson SM, Moretti PA, Zebol JR, Xia P, Gamble JR, Vadas MA, D'Andrea RJ, Wattenberg BW: Expression of a catalytically inactive sphingosine kinase mutant blocks agonist-induced sphingosine kinase activation. A dominant-negative sphingosine kinase. J Biol Chem 2000; 275: 33945-33950.
50. Gault CR, Eblen ST, Neumann CA, Hannun YA, Obeid LM: Oncogenic K-Ras regulates bioactive sphingolipids in a sphingosine kinase 1-dependent manner. J Biol Chem 2012; 287: 31794-31803.
51. Castaing-Berthou A, Malet N, Radojkovic C, Cabou C, Gayral S, Martinez LO, Laffargue M: PI3Kbeta Plays a Key Role in Apolipoprotein A-I-Induced Endothelial Cell Proliferation Through Activation of the Ecto-F1-ATPase/P2Y1 Receptors. Cell Physiol Biochem 2017; 42: 579-593.
52. Wang X, Chen WR, Xing D: A pathway from JNK through decreased ERK and Akt activities for FOXO3a nuclear translocation in response to UV irradiation. J Cell Physiol 2012; 227: 1168-1178.
53. Lee GE, Yu EY, Cho CH, Lee J, Muller MT, Chung IK: DNA-protein kinase catalytic subunit-interacting protein KIP binds telomerase by interacting with human telomerase reverse transcriptase. J Biol Chem 2004; 279: 34750-34755.
54. Khadka P, Lee JH, Baek SH, Oh SY, Chung IK: DNA-PKcs-interacting protein KIP binding to TRF2 is required for the maintenance of functional telomeres. Biochem J 2014; 463: 19-30.
55. Cen WJ, Pan Y, Li WX, Yang SQ: Comparison of DNA-dependent protein kinase catalytic subunit expression in two lung adenocarcinoma cell lines with different radiosensitivity. Nan Fang Yi Ke Da Xue Xue Bao 2009; 29: 2241-2243.
56. Henderson MJ, Russell AJ, Hird S, Munoz M, Clancy JL, Lehrbach GM, Calanni ST, Jans DA, Sutherland RL, Watts CK: EDD, the human hyperplastic discs protein, has a role in progesterone receptor coactivation and potential involvement in DNA damage response. J Biol Chem 2002; 277: 26468-26478.
57. Yoon KW, Cho JH, Lee JK, Kang YH, Chae JS, Kim YM, Kim J, Kim EK, Kim SE, Baik JH, Naik UP, Cho SG, Choi EJ: CIB1 functions as a Ca(2+)-sensitive modulator of stress-induced signaling by targeting ASK1. Proc Natl Acad Sci U S A 2009; 106: 17389-17394.
58. Wang X, Xing D, Liu L, Chen WR: BimL directly neutralizes Bcl-xL to promote Bax activation during UV-induced apoptosis. FEBS Lett 2009; 583: 1873-1879.
59. Wang X, He X, Hu S, Sun A, Lu C: Involvement of Bim in Photofrin-mediated photodynamically induced apoptosis. Cell Physiol Biochem 2015; 35: 1527-1536.
60. Hynes RO: Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110: 673-687.
61. Shock DD, Naik UP, Brittain JE, Alahari SK, Sondek J, Parise LV: Calcium-dependent properties of CIB binding to the integrin alphaIIb cytoplasmic domain and translocation to the platelet cytoskeleton. Biochem J 1999; 342 Pt 3: 729-735.
62. Litvinov RI, Farrell DH, Weisel JW, Bennett JS: The Platelet Integrin alphaIIbbeta3 Differentially Interacts with Fibrin Versus Fibrinogen. J Biol Chem 2016; 291: 7858-7867.
63. Duval C, Ariens RAS: Fibrinogen splice variation and cross-linking: Effects on fibrin structure/function and role of fibrinogen gamma' as thrombomobulin II. Matrix Biol 2017; 60-61: 8-15.
64. Naik MU, Naik TU, Summer R, Naik UP: Binding of CIB1 to the alphaIIb tail of alphaIIbbeta3 is required for FAK recruitment and activation in platelets. PLoS One 2017; 12:e0176602.
65. Tsuboi S, Nonoyama S, Ochs HD: Wiskott-Aldrich syndrome protein is involved in alphaIIb beta3-mediated cell adhesion. EMBO Rep 2006; 7: 506-511.
66. Haataja L, Kaartinen V, Groffen J, Heisterkamp N: The small GTPase Rac3 interacts with the integrin-binding protein CIB and promotes integrin alpha(IIb)beta(3)-mediated adhesion and spreading. J Biol Chem 2002; 277: 8321-8328.
67. Leisner TM, Liu M, Jaffer ZM, Chernoff J, Parise LV: Essential role of CIB1 in regulating PAK1 activation and cell migration. J Cell Biol 2005; 170: 465-476.
68. Zayed MA, Yuan W, Chalothorn D, Faber JE, Parise LV: Tumor growth and angiogenesis is impaired in CIB1 knockout mice. J Angiogenes Res 2010; 2: 17.
69. Naik MU, Naik UP: Contra-regulation of calcium-and integrin-binding protein 1-induced cell migration on fibronectin by PAK1 and MAP kinase signaling. J Cell Biochem 2011; 112: 3289-3299.
70. Naik MU, Naik UP: Calcium-and integrin-binding protein regulates focal adhesion kinase activity during platelet spreading on immobilized fibrinogen. Blood 2003; 102: 3629-3636.
71. Zayed MA, Yuan W, Leisner TM, Chalothorn D, McFadden AW, Schaller MD, Hartnett ME, Faber JE, Parise LV: CIB1 regulates endothelial cells and ischemia-induced pathological and adaptive angiogenesis. Circ Res 2007; 101: 1185-1193.
72. Sobczak A, Debowska K, Blazejczyk M, Kreutz MR, Kuznicki J, Wojda U: Calmyrin1 binds to SCG10 protein (stathmin2) to modulate neurite outgrowth. Biochim Biophys Acta 2011; 1813: 1025-1037.
73. Whitehouse C, Chambers J, Howe K, Cobourne M, Sharpe P, Solomon E: NBR1 interacts with fasciculation and elongation protein zeta-1 (FEZ1) and calcium and integrin binding protein (CIB) and shows developmentally restricted expression in the neural tube. Eur J Biochem 2002; 269: 538-545.
74. Wang S, Sun Z, Zhang X, Li Z, Wu M, Zhao W, Wang H, Chen T, Yan H, Zhu J: Wnt1 positively regulates CD36 expression via TCF4 and PPAR-gamma in macrophages. Cell Physiol Biochem 2015; 35: 1289-1302.
75. Hollenbach AD, McPherson CJ, Lagutina I, Grosveld G: The EF-hand calcium-binding protein calmyrin inhibits the transcriptional and DNA-binding activity of Pax3. Biochim Biophys Acta 2002; 1574: 321-328.
76. Sun W, Guan Q, Wen J, Zhang Q, Yang W, Zhang B, Cui W, Zou Z, Yu Y: Calcium-and integrin-binding protein-1 is down-regulated in the sperm of patients with oligoasthenozoospermia: CIB1 expression in patients with oligoasthenozoospermia. J Assist Reprod Genet 2014; 31: 541-547.
77. Godinho-Santos A, Hance AJ, Gonçalves J, Mammano F: CIB1 and CIB2 are HIV-1 helper factors involved in viral entry. Sci Rep 2016; 6: 30927.
78. Bandyopadhyay C, Valiya-Veettil M, Dutta D, Chakraborty S, Chandran B: CIB1 synergizes with EphrinA2 to regulate Kaposi's sarcoma-associated herpesvirus macropinocytic entry in human microvascular dermal endothelial cells. PLoS Pathog 2014; 10:e1003941.
79. Zhao F, Zhang S, Chen L, Wu Y, Qin J, Shao Y, Wang X, Chen Y: Calcium-and integrin-binding protein-1 and calcineurin are upregulated in the right atrial myocardium of patients with atrial fibrillation. Europace 2012; 14: 1726-1733.
80. Weljie AM, Yamniuk AP, Yoshino H, Izumi Y, Vogel HJ: Protein conformational changes studied by diffusion NMR spectroscopy: application to helix-loop-helix calcium binding proteins. Protein Sci 2003; 12: 228-236.