Stanniocalcin1 is a key mediator of amyloidogenic light chain induced cardiotoxicity

Basic Research in Cardiology

Volumn 108, Issue 5, 2013, Pages

  Guan, Jian ^a,b   Mishra, Shikha ^a   Shi, Jianru ^a   Plovie, Eva ^a   Qiu, Yiling ^a   Cao, Xin ^a   Gianni, Davide ^c   Jiang, Bingbing ^a   Del Monte, Federica ^a   Connors, Lawreen H ^b   Seldin, David C ^b   Lavatelli, Francesca ^d   Rognoni, Paola ^d   Palladini, Giovanni ^d   Merlini, Giampaolo ^d   Falk, Rodney H ^e   Semigran, Marc J ^a   Dec, G William ^a   MacRae, Calum A ^a   Liao, Ronglih ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF PAVIA   (Italy)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Amyloidosis; Cardiac toxicity; Cardiomyopathy

Indexed keywords

CALCIUM; HYPOCALCIN; IMMUNOGLOBULIN LIGHT CHAIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; STANNIOCALCIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CARDIOMYOPATHY; CARDIOTOXICITY; CONTROLLED STUDY; EMBRYO; HEART AMYLOIDOSIS; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAT; ZEBRA FISH;

EID: 84882528609     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-013-0378-5     Document Type: Article

References (45)

1. Block GJ, Ohkouchi S, Fung F, Frenkel J, Gregory C, Pochampally R, Dimattia G, Sullivan DE, Prockop DJ (2009) Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1. Stem Cells 27:670-681. doi: 10.1002/stem.20080742
2. Brenner DA, Jain M, Pimentel DR, Wang B, Connors LH, Skinner M, Apstein CS, Liao R (2004) Human amyloidogenic light chains directly impair cardiomyocyte function through an increase in cellular oxidant stress. Circ Res 94:1008-1010. doi: 10.1161/01.RES.0000126569.75419.74 (Pubitemid 38579694)
3. Chang AC, Cha J, Koentgen F, Reddel RR (2005) The murine stanniocalcin 1 gene is not essential for growth and development. Mol Cell Biol 25:10604-10610. doi: 10.1128/MCB.25.23.10604-10610.2005 (Pubitemid 41681980)
4. Chang AC, Jellinek DA, Reddel RR (2003) Mammalian stanniocalcins and cancer. Endocr Relat Cancer 10:359-373. doi: 10.1677/erc.0.0100359 (Pubitemid 37267555)
5. Connors LH, Jiang Y, Budnik M, Theberge R, Prokaeva T, Bodi KL, Seldin DC, Costello CE, Skinner M (2007) Heterogeneity in primary structure, post-translational modifications, and germline gene usage of nine full-length amyloidogenic kappa1 immunoglobulin light chains. Biochemistry 46:14259-14271. doi: 10.1021/bi7013773 (Pubitemid 350250319)
6. Du J, Wang Y, Hunter R, Wei Y, Blumenthal R, Falke C, Khairova R, Zhou R, Yuan P, Machado-Vieira R, McEwen BS, Manji HK (2009) Dynamic regulation of mitochondrial function by glucocorticoids. Proc Natl Acad Sci USA 106:3543-3548. doi: 10.1073/pnas.0812671106
7. Dubrey SW, Cha K, Anderson J, Chamarthi B, Reisinger J, Skinner M, Falk RH (1998) The clinical features of immunoglobulin light-chain (AL) amyloidosis with heart involvement. QJM 91:141-157. doi: 10.1093/qjmed/91.2.141 (Pubitemid 28102667)
8. Dubrey SW, Cha K, Skinner M, LaValley M, Falk RH (1997) Familial and primary (AL) cardiac amyloidosis: echocardiographically similar diseases with distinctly different clinical outcomes. Heart 78:74-82. doi: 10.1136/hrt.78.1.74 (Pubitemid 27346885)
9. Ellard JP, McCudden CR, Tanega C, James KA, Ratkovic S, Staples JF, Wagner GF (2007) The respiratory effects of stanniocalcin-1 (STC-1) on intact mitochondria and cells: STC-1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates. Mol Cell Endocrinol 264:90-101. doi: 10.1016/j.mce.2006.10.008 (Pubitemid 46097304)
10. Falk RH (2011) Cardiac amyloidosis: a treatable disease, often overlooked. Circulation 124:1079-1085. doi: 10.1161/CIRCULATIONAHA.110.010447
11. Falk RH (2005) Diagnosis and management of the cardiac amyloidoses. Circulation 112:2047-2060. doi: 10.1161/CIRCULATIONAHA.104.489187 (Pubitemid 41377426)
12. Filvaroff EH, Guillet S, Zlot C, Bao M, Ingle G, Steinmetz H, Hoeffel J, Bunting S, Ross J, Carano RA, Powell-Braxton L, Wagner GF, Eckert R, Gerritsen ME, French DM (2002) Stanniocalcin 1 alters muscle and bone structure and function in transgenic mice. Endocrinology 143:3681-3690. doi: 10.1210/en.2001-211424 (Pubitemid 34925745)
13. Fisch S, Gray S, Heymans S, Haldar SM, Wang B, Pfister O, Cui L, Kumar A, Lin Z, Sen-Banerjee S, Das H, Petersen CA, Mende U, Burleigh BA, Zhu Y, Pinto YM, Liao R, Jain MK (2007) Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 104:7074-7079. doi: 10.1073/pnas.0701981104 (Pubitemid 47186011)
14. Guan J, Mishra S, Falk RH, Liao R (2012) Current perspectives on cardiac amyloidosis. Am J Physiol Heart Circ Physiol 302:H544-H552. doi: 10.1152/ajpheart.00815.2011
15. Ishibashi K, Imai M (2002) Prospect of a stanniocalcin endocrine/paracrine system in mammals. Am J Physiol Renal Physiol 282:F367-F375. doi: 10.1152/ajprenal.00364.2000
16. Jain M, Brenner DA, Cui L, Lim CC, Wang B, Pimentel DR, Koh S, Sawyer DB, Leopold JA, Handy DE, Loscalzo J, Apstein CS, Liao R (2003) Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes. Circ Res 93:e9-e16. doi: 10.1161/01.RES.0000083489.83704. 76
17. Kanellis J, Bick R, Garcia G, Truong L, Tsao CC, Etemadmoghadam D, Poindexter B, Feng L, Johnson RJ, Sheikh-Hamad D (2004) Stanniocalcin-1, an inhibitor of macrophage chemotaxis and chemokinesis. Am J Physiol Renal Physiol 286:F356-F362. doi: 10.1152/ajprenal.00138.2003
18. 2+ overload and cell hypercontracture in cardiomyocytes. Circ J 71:796-801. doi: 10.1253/circj.71.796 (Pubitemid 46683375)
19. Koyama J, Falk RH (2010) Prognostic significance of strain Doppler imaging in light-chain amyloidosis. JACC Cardiovasc Imaging 3:333-342. doi: 10.1016/j.jcmg.2009.11.013
20. Lai KP, Law AY, Yeung HY, Lee LS, Wagner GF, Wong CK (2007) Induction of stanniocalcin-1 expression in apoptotic human nasopharyngeal cancer cells by p53. Biochem Biophys Res Commun 356:968-975. doi: 10.1016/j.bbrc.2007.03.074 (Pubitemid 46529385)
21. Law AY, Ching LY, Lai KP, Wong CK (2010) Identification and characterization of the hypoxia-responsive element in human stanniocalcin-1 gene. Mol Cell Endocrinol 314:118-127. doi: 10.1016/j.mce.2009.07.007
22. Law AY, Lai KP, Lui WC, Wan HT, Wong CK (2008) Histone deacetylase inhibitor-induced cellular apoptosis involves stanniocalcin-1 activation. Exp Cell Res 314:2975-2984. doi: 10.1016/j.yexcr.2008.07.002
23. Li K, Dong D, Yao L, Dai D, Gu X, Guo L (2008) Identification of STC1 as an beta-amyloid activated gene in human brain microvascular endothelial cells using cDNA microarray. Biochem Biophys Res Commun 376:399-403. doi: 10.1016/j.bbrc.2008.08.158
24. Liao R, Jain M, Teller P, Connors LH, Ngoy S, Skinner M, Falk RH, Apstein CS (2001) Infusion of light chains from patients with cardiac amyloidosis causes diastolic dysfunction in isolated mouse hearts. Circulation 104:1594-1597 (Pubitemid 32947519)
25. Merlini G, Bellotti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349:583-596. doi: 10.1056/NEJMra023144 (Pubitemid 36951371)
26. Merlini G, Seldin DC, Gertz MA (2011) Amyloidosis: pathogenesis and new therapeutic options. J Clin Oncol 29:1924-1933. doi: 10.1200/JCO.2010.32.2271
27. Migrino RQ, Hari P, Gutterman DD, Bright M, Truran S, Schlundt B, Phillips SA (2010) Systemic and microvascular oxidative stress induced by light chain amyloidosis. Int J Cardiol 145:67-68. doi: 10.1016/j.ijcard.2009.04.044
28. Migrino RQ, Truran S, Gutterman DD, Franco DA, Bright M, Schlundt B, Timmons M, Motta A, Phillips SA, Hari P (2011) Human microvascular dysfunction and apoptotic injury induced by AL amyloidosis light chain proteins. Am J Physiol Heart Circ Physiol 301:H2305-H2312. doi: 10.1152/ajpheart.00503.2011
29. Mishra S, Guan J, Plovie E, Seldin DC, Connors LH, Merlini G, Falk RH, Macrae CA, Liao R (2013) Human amyloidogenic light chain proteins result in cardiac dysfunction, cell death and early mortality in zebrafish. Am J Physiol Heart Circ Physiol 305:H95-H103. doi: 10.1152/ajpheart.00186.2013
30. Nguyen A, Chang AC, Reddel RR (2009) Stanniocalcin-1 acts in a negative feedback loop in the prosurvival ERK1/2 signaling pathway during oxidative stress. Oncogene 28:1982-1992. doi: 10.1038/onc.2009.65
31. Palladini G, Lavatelli F, Russo P, Perlini S, Perfetti V, Bosoni T, Obici L, Bradwell AR, D'Eril GM, Fogari R, Moratti R, Merlini G (2006) Circulating amyloidogenic free light chains and serum N-terminal natriuretic peptide type B decrease simultaneously in association with improvement of survival in AL. Blood 107:3854-3858. doi: 10.1182/blood-2005-11-4385 (Pubitemid 43726787)
32. Panakova D, Werdich AA, Macrae CA (2010) Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca(2+) channel. Nature 466:874-878. doi: 10.1038/nature09249
33. Sheikh-Hamad D, Bick R, Wu GY, Christensen BM, Razeghi P, Poindexter B, Taegtmeyer H, Wamsley A, Padda R, Entman M, Nielsen S, Youker K (2003) Stanniocalcin-1 is a naturally occurring L-channel inhibitor in cardiomyocytes: relevance to human heart failure. Am J Physiol Heart Circ Physiol 285:H442-H448. doi: 10.1152/ajpheart.01071.2002
34. Shi J, Guan J, Jiang B, Brenner DA, Del Monte F, Ward JE, Connors LH, Sawyer DB, Semigran MJ, Macgillivray TE, Seldin DC, Falk R, Liao R (2010) Amyloidogenic light chains induce cardiomyocyte contractile dysfunction and apoptosis via a non-canonical p38alpha MAPK pathway. Proc Natl Acad Sci USA 107:4188-4193. doi: 10.1073/pnas.0912263107
35. Shin JT, Pomerantsev EV, Mably JD, MacRae CA (2010) High-resolution cardiovascular function confirms functional orthology of myocardial contractility pathways in zebrafish. Physiol Genomics 42:300-309. doi: 10.1152/physiolgenomics.00206.2009
36. Sikkink LA, Ramirez-Alvarado M (2010) Cytotoxicity of amyloidogenic immunoglobulin light chains in cell culture. Cell Death Dis 1:e98. doi: 10.1038/cddis.2010.75
37. Varghese R, Gagliardi AD, Bialek PE, Yee SP, Wagner GF, Dimattia GE (2002) Overexpression of human stanniocalcin affects growth and reproduction in transgenic mice. Endocrinology 143:868-876. doi: 10.1210/en.143.3.868 (Pubitemid 34164035)
38. Wagner GF, Dimattia GE (2006) The stanniocalcin family of proteins. J Exp Zool A Comp Exp Biol 305:769-780. doi: 10.1002/jez.a.313 (Pubitemid 44358304)
39. Wang Y, Huang L, Abdelrahim M, Cai Q, Truong A, Bick R, Poindexter B, Sheikh-Hamad D (2009) Stanniocalcin-1 suppresses superoxide generation in macrophages through induction of mitochondrial UCP2. J Leukoc Biol 86:981-988. doi: 10.1189/jlb.0708454
40. Westberg JA, Serlachius M, Lankila P, Penkowa M, Hidalgo J, Andersson LC (2007) Hypoxic preconditioning induces neuroprotective stanniocalcin-1 in brain via IL-6 signaling. Stroke 38:1025-1030. doi: 10.1161/01.STR.0000258113.67252.fa (Pubitemid 46568469)
41. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene
42. Wu S, Yoshiko Y, De Luca F (2006) Stanniocalcin 1 acts as a paracrine regulator of growth plate chondrogenesis. J Biol Chem 281:5120-5127. doi: 10.1074/jbc.M506667200 (Pubitemid 43847777)
43. Yankner BA, Lu T (2009) Amyloid beta-protein toxicity and the pathogenesis of Alzheimer disease. J Biol Chem 284:4755-4759. doi: 10.1074/jbc.R800018200
44. Yeung HY, Lai KP, Chan HY, Mak NK, Wagner GF, Wong CK (2005) Hypoxia-inducible factor-1-mediated activation of stanniocalcin-1 in human cancer cells. Endocrinology 146:4951-4960. doi: 10.1210/en.2005-0365 (Pubitemid 41446634)
45. Zhang K, Lindsberg PJ, Tatlisumak T, Kaste M, Olsen HS, Andersson LC (2000) Stanniocalcin: a molecular guard of neurons during cerebral ischemia. Proc Natl Acad Sci USA 97:3637-3642. doi: 10.1073/pnas.070045897 (Pubitemid 30183355)